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The Glomerular Basement Membrane as a Model System to Study the Bioactivity of Heparan Sulfate Glycosaminoglycans

Published online by Cambridge University Press:  18 January 2012

Kevin J. McCarthy  and
Deborah J. Wassenhove-McCarthy
Kevin J. McCarthy*
Affiliation:
Department of Pathology, LSU Health Sciences Center-Shreveport, 1501 Kings Highway, Shreveport, LA 71130-3932, USA
Deborah J. Wassenhove-McCarthy
Affiliation:
Department of Pathology, LSU Health Sciences Center-Shreveport, 1501 Kings Highway, Shreveport, LA 71130-3932, USA
*
Corresponding author. E-mail: kmccar2@lsuhsc.edu
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Abstract

The glomerular basement membrane and its associated cells are critical elements in the renal ultrafiltration process. Traditionally the anionic charge associated with several carbohydrate moieties in the glomerular basement membrane are thought to form a charge selective barrier that restricts the transmembrane flux of anionic proteins across the glomerular basement membrane into the urinary space. The charge selective function, along with the size selective component of the basement membrane, serves to limit the efflux of plasma proteins from the capillary lumen. Heparan sulfate glycosaminoglycans are anionically charged carbohydrate structures attached to proteoglycan core proteins and have a role in establishing the charge selective function of the glomerular basement membrane. Although there are a large number of studies in the literature that support this concept, the results of several recent studies using molecular genetic approaches to minimize the anionic charge of the glomerular basement membrane would suggest that the role of heparan sulfate glycosaminoglycans in the glomerular capillary wall are still not yet entirely resolved, suggesting that this research area still requires new and novel exploration.

Keywords

heparan sulfateproteoglycanspodocyteglomerularbasement membraneultrafiltration
Type
Review Article
Information
Microscopy and Microanalysis , Volume 18 , Issue 1 , February 2012 , pp. 3 - 21
Copyright
Copyright © Microscopy Society of America 2012

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References

REFERENCES

Abrahamson, D.R. (1985). Origin of the glomerular basement membrane visualized after in vivo labeling of laminin in newborn rat kidneys. J Cell Biol 100, 1988–2000.Google Scholar
Abrahamson, D.R. & Perry, E.W. (1986). Evidence for splicing new basement membrane into old during glomerular development in newborn rat kidneys. J Cell Biol 103, 2489–2498.CrossRefGoogle ScholarPubMed
Abrahamson, D.R., St John, P.L., Isom, K., Robert, B. & Miner, J.H. (2007). Partial rescue of glomerular laminin alpha5 mutations by wild-type endothelia produce hybrid glomeruli. J Am Soc Nephrol 18(8), 2285–2293.Google Scholar
Acharya, A., Baek, S.T., Banfi, S., Eskiocak, B. & Tallquist, M.D. (2011). Efficient inducible Cre-mediated recombination in Tcf21 cell lineages in the heart and kidney. Genesis 49(11), 870–877.Google Scholar
Adhikari, N., Basi, D.L., Townsend, D., Rusch, M., Mariash, A., Mullegama, S., Watson, A., Larson, J., Tan, S., Lerman, B., Esko, J.D., Selleck, S.B. & Hall, J.L. (2010). Heparan sulfate Ndst1 regulates vascular smooth muscle cell proliferation, vessel size and vascular remodeling. J Mol Cell Cardiol 49(2), 287–293.CrossRefGoogle ScholarPubMed
Affolter, M., Zeller, R. & Caussinus, E. (2009). Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol 10(12), 831–842.CrossRefGoogle ScholarPubMed
Ala-Houhala, I. & Pasternack, A. (1987). Fractional dextran and protein clearances in glomerulonephritis and in diabetic nephropathy. Clin Sci (Lond) 72(3), 289–296.CrossRefGoogle ScholarPubMed
Anderson, S., Rennke, H.G. & Brenner, B.M. (1986). Therapeutic advantage of converting enzyme inhibitors in arresting progressive renal disease associated with systemic hypertension in the rat. J Clin Invest 77(6), 1993–2000.CrossRefGoogle ScholarPubMed
Andrews, P.M. (1978). Scanning electron microscopy of the kidney glomerular epithelium after treatment with polycations in situ and in vitro. Am J Anat 153(2), 291–303.CrossRefGoogle ScholarPubMed
Appel, D., Kershaw, D.B., Smeets, B., Yuan, G., Fuss, A., Frye, B., Elger, M., Kriz, W., Floege, J. & Moeller, M.J. (2009). Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol 20(2), 333–343.CrossRefGoogle ScholarPubMed
Asano, T., Niimura, F., Pastan, I., Fogo, A.B., Ichikawa, I. & Matsusaka, T. (2005). Permanent genetic tagging of podocytes: fate of injured podocytes in a mouse model of glomerular sclerosis. J Am Soc Nephrol 16(8), 2257–2262.Google Scholar
Banerjee, S.D., Cohn, R.H. & Bernfield, M.R. (1977). Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. J Cell Biol 73(2), 445–463.Google Scholar
Bass, M.D., Morgan, M.R. & Humphries, M.J. (2007). Integrins and syndecan-4 make distinct, but critical, contributions to adhesion contact formation. Soft Matter 3(3), 372–376.CrossRefGoogle ScholarPubMed
Belteki, G., Haigh, J., Kabacs, N., Haigh, K., Sison, K., Costantini, F., Whitsett, J., Quaggin, S.E. & Nagy, A. (2005). Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction. Nucleic Acids Res 33(5), 2765–2775.CrossRefGoogle ScholarPubMed
Bernfield, M. (1977). The basal lamina in epithelial-mesenchymal morphogenetic interactions. Ups J Med Sci 82(2), 111–112.CrossRefGoogle ScholarPubMed
Bernfield, M., Banerjee, S.D., Koda, J.E. & Rapraeger, A.C. (1984). Remodeling of the basement membrane as a mechanism of morphogenetic tissue interaction. In The Role of Extracellular Matrix in Development, Trelstad, R.L. (Ed.), pp. 545–572. New York: Alan R. Liss.Google Scholar
Bernfield, M., Gotte, M., Park, P.W., Reizes, O., Fitzgerald, M.L., Lincecum, J. & Zako, M. (1999). Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68, 729–777.CrossRefGoogle ScholarPubMed
Bishop, J.R., Schuksz, M. & Esko, J.D. (2007). Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446(7139), 1030–1037.Google Scholar
Bjornson Granqvist, A., Ebefors, K., Saleem, M.A., Mathieson, P.W., Haraldsson, B. & Nystrom, J.S. (2006). Podocyte proteoglycan synthesis is involved in the development of nephrotic syndrome. Am J Physiol Renal Physiol 291(4), F722–F730.CrossRefGoogle ScholarPubMed
Blantz, R.C., Konnen, K.S. & Tucker, B.J. (1975). Glomerular filtration response to elevated ureteral pressure in both the hydropenic and the plasma-expanded rat. Circ Res 37(6), 819–829.Google Scholar
Blantz, R.C., Konnen, K.S. & Tucker, B.J. (1976). Angiotensin II effects upon the glomerular microcirculation and ultrafiltration coefficient of the rat. J Clin Invest 57(2), 419–434.CrossRefGoogle ScholarPubMed
Blantz, R.C. & Wilson, C.B. (1976). Acute effects of antiglomerular basement membrane antibody on the process of glomerular filtration in the rat. J Clin Invest 58(4), 899–911.CrossRefGoogle ScholarPubMed
Bray, B.A. (1978). Cold-insoluble globulin (fibronectin) in connective tissues of adult human lung and in trophoblast basement membrane. J Clin Invest 62(4), 745–752.CrossRefGoogle ScholarPubMed
Brenner, B.M., Bohrer, M.P., Baylis, C. & Deen, W.M. (1977). Determinants of glomerular permselectivity: Insights derived from observations in vivo. Kidney Int 12(4), 229–237.CrossRefGoogle ScholarPubMed
Brenner, B.M., Hostetter, T.H. & Humes, H.D. (1978). Glomerular permselectivity: Barrier function based on discrimination of molecular size and charge. Am J Physiol 234(6), F455–F460.Google ScholarPubMed
Breyer, M.D., Bottinger, E., Brosius, F.C., Coffman, T.M., Fogo, A., Harris, R.C., Heilig, C.W. & Sharma, K. (2005). Diabetic nephropathy: Of mice and men. Adv Chronic Kidney Dis 12(2), 128–145.CrossRefGoogle ScholarPubMed
Brukamp, K., Jim, B., Moeller, M.J. & Haase, V.H. (2007). Hypoxia and podocyte-specific Vhlh deletion confer risk of glomerular disease. Am J Physiol Renal Physiol 293(4), F1397–1407.CrossRefGoogle ScholarPubMed
Bullock, S.L., Fletcher, J.M., Beddington, R.S. & Wilson, V.A. (1998). Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev 12(12), 1894–1906.CrossRefGoogle ScholarPubMed
Burgess, R.W., Skarnes, W.C. & Sanes, J.R. (2000). Agrin isoforms with distinct amino termini: Differential expression, localization, and function. J Cell Biol 151(1), 41–52.CrossRefGoogle ScholarPubMed
Camirand, G., Li, Q., Demetris, A.J., Watkins, S.C., Shlomchik, W.D., Rothstein, D.M. & Lakkis, F.G. (2011). Multiphoton intravital microscopy of the transplanted mouse kidney. Am J Transplant 11(10), 2067–2074.Google Scholar
Cevikbas, F., Schaefer, L., Uhlig, P., Robenek, H., Theilmeier, G., Echtermeyer, F. & Bruckner, P. (2008). Unilateral nephrectomy leads to up-regulation of syndecan-2- and TGF-beta-mediated glomerulosclerosis in syndecan-4 deficient male mice. Matrix Biol 27(1), 42–52.CrossRefGoogle ScholarPubMed
Chan, F.L. & Inoue, S. (1994). Lamina lucida of basement membrane: An artefact. Microsc Res Tech 28(1), 48–59.CrossRefGoogle ScholarPubMed
Chan, F.L., Inoue, S. & Leblond, C.P. (1993). The basement membranes of cryofixed or aldehyde-fixed, freeze-substituted tissues are composed of a lamina densa and do not contain a lamina lucida. Cell Tissue Res 273(1), 41–52.CrossRefGoogle Scholar
Chang, R.L., Deen, W.M., Robertson, C.R. & Brenner, B.M. (1975). Permselectivity of the glomerular capillary wall: III. Restricted transport of polyanions. Kidney Int 8(4), 212–218.Google Scholar
Chen, S., Wassenhove-McCarthy, D.J., Yamaguchi, Y., Holzman, L.B., van Kuppevelt, T.H., Jenniskens, G.J., Wijnhoven, T.J., Woods, A.C. & McCarthy, K.J. (2008). Loss of heparan sulfate glycosaminoglycan assembly in podocytes does not lead to proteinuria. Kidney Int 74(3), 289–299.Google Scholar
Chen, S., Wassenhove-McCarthy, D., Yamaguchi, Y., Holzman, L., van Kuppevelt, T.H., Orr, A.W., Funk, S., Woods, A. & McCarthy, K. (2010). Podocytes require the engagement of cell surface heparan sulfate proteoglycans for adhesion to extracellular matrices. Kidney Int 78(11), 1088–1099.CrossRefGoogle ScholarPubMed
Clark, C.C., Minor, R.R., Koszalka, T.R., Brent, R.L. & Kefalides, N.A. (1975). The embryonic rat parietal yolk sac. Changes in the morphology and composition of its basement membrane during development. Dev Biol 46, 243–261.CrossRefGoogle ScholarPubMed
Condac, E., Silasi-Mansat, R., Kosanke, S., Schoeb, T., Towner, R., Lupu, F., Cummings, R.D. & Hinsdale, M.E. (2007). Polycystic disease caused by deficiency in xylosyltransferase 2, an initiating enzyme of glycosaminoglycan biosynthesis. Proc Natl Acad Sci USA 104(22), 9416–9421.CrossRefGoogle ScholarPubMed
Costantini, F. & Kopan, R. (2010). Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18(5), 698–712.Google Scholar
Couchman, J.R., Chen, L. & Woods, A. (2001). Syndecans and cell adhesion. Int Rev Cytol 207, 113–150.Google Scholar
Couchman, J.R. & Woods, A. (1999). Syndecan-4 and integrins: Combinatorial signaling in cell adhesion. J Cell Sci 112(Pt 20), 3415–3420.Google Scholar
Couser, W.G. & Johnson, R.J. (1994). Mechanisms of progressive renal disease in glomerulonephritis. Am J Kidney Dis 23(2), 193–198.Google Scholar
Crawford, B.E., Garner, O.B., Bishop, J.R., Zhang, D.Y., Bush, K.T., Nigam, S.K. & Esko, J.D. (2010). Loss of the heparan sulfate sulfotransferase, Ndst1, in mammary epithelial cells selectively blocks lobuloalveolar development in mice. PLoS One 5(5), e10691.Google Scholar
Crawford, B.E., Olson, S.K., Esko, J.D. & Pinhal, M.A. (2001). Cloning, Golgi localization, and enzyme activity of the full-length heparin/heparan sulfate-glucuronic acid C5-epimerase. J Biol Chem 276(24), 21538–21543.Google Scholar
Cuellar, K., Chuong, H., Hubbell, S.M. & Hinsdale, M.E. (2007). Biosynthesis of chondroitin and heparan sulfate in chinese hamster ovary cells depends on xylosyltransferase II. J Biol Chem 282(8), 5195–5200.Google Scholar
Dai, C., Saleem, M.A., Holzman, L.B., Mathieson, P. & Liu, Y. (2010). Hepatocyte growth factor signaling ameliorates podocyte injury and proteinuria. Kidney Int 77(11), 962–973.CrossRefGoogle ScholarPubMed
David, G. & Bernfield, M.R. (1979). Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: Possible mechanism for basal lamina formation. Proc Natl Acad Sci USA 76(2), 786–790.Google Scholar
David, G. & Bernfield, M. (1981). Type I collagen reduces the degradation of basal lamina proteoglycan by mammary epithelial cells. J Cell Biol 91(1), 281–286.Google Scholar
David, G. & Bernfield, M. (1998). The emerging roles of cell surface heparan sulfate proteoglycans. Matrix Biol 17(7), 461–463.CrossRefGoogle ScholarPubMed
David, G. & Van den Berghe, H. (1985). Heparan sulfate-chondroitin sulfate hybrid proteoglycan of the cell surface and basement membrane of mouse mammary epithelial cells. J Biol Chem 260(20), 11067–11074.CrossRefGoogle ScholarPubMed
Deen, W.M., Bohrer, M.P., Robertson, C.R. & Brenner, B.M. (1977). Determinants of the transglomerular passage of macromolecules. Fed Proc 36(12), 2614–2618.Google ScholarPubMed
Dennissen, M.A., Jenniskens, G.J., Pieffers, M., Versteeg, E.M., Petitou, M., Veerkamp, J.H. & van Kuppevelt, T.H. (2002). Large, tissue-regulated domain diversity of heparan sulfates demonstrated by phage display antibodies. J Biol Chem 277(13), 10982–10986.Google Scholar
Dixon, J., Loftus, S.K., Gladwin, A.J., Scambler, P.J., Wasmuth, J.J. & Dixon, M.J. (1995). Cloning of the human heparan sulfate-N-deacetylase/N-sulfotransferase gene from the Treacher Collins syndrome candidate region at 5q32-q33.1. Genomics 26(2), 239–244.Google Scholar
Dunn, K.W., Sandoval, R.M. & Molitoris, B.A. (2003). Intravital imaging of the kidney using multiparameter multiphoton microscopy. Nephron Exp Nephrol 94(1), e7–11.Google Scholar
El-Aouni, C., Herbach, N., Blattner, S.M., Henger, A., Rastaldi, M.P., Jarad, G., Miner, J.H., Moeller, M.J., St-Arnaud, R., Dedhar, S., Holzman, L.B., Wanke, R. & Kretzler, M. (2006). Podocyte-specific deletion of integrin-linked kinase results in severe glomerular basement membrane alterations and progressive glomerulosclerosis. J Am Soc Nephrol 17(5), 1334–1344.CrossRefGoogle ScholarPubMed
Elger, M., Drenckhahn, D., Nobiling, R., Mundel, P. & Kriz, W. (1993). Cultured rat mesangial cells contain smooth muscle a-actin not found in vivo. Am J Path 142(2), 497–509.Google Scholar
Eremina, V., Cui, S., Gerber, H., Ferrara, N., Haigh, J., Nagy, A., Ema, M., Rossant, J., Jothy, S., Miner, J.H. & Quaggin, S.E. (2006). Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J Am Soc Nephrol 17(3), 724–735.CrossRefGoogle ScholarPubMed
Eremina, V., Wong, M.A., Cui, S., Schwartz, L. & Quaggin, S.E. (2002). Glomerular-specific gene excision in vivo. J Am Soc Nephrol 13(3), 788–793.Google Scholar
Eriksson, I., Sandback, D., Ek, B., Lindahl, U. & Kjellen, L. (1994). cDNA cloning and sequencing of mouse mastocytoma glucosaminyl N-deacetylase/N-sulfotransferase, an enzyme involved in the biosynthesis of heparin. J Biol Chem 269(14), 10438–10443.Google Scholar
Esko, J.D., Kimata, K. & Lindahl, U. (2009). Proteoglycans and sulfated glycosaminoglycans. In Essentials of Glycobiology, 2nd ed., Varki, A. (Ed.), pp. 229–249. New York: Cold Spring Harbor Press.Google Scholar
Esko, J.D. & Lindahl, U. (2001). Molecular diversity of heparan sulfate. J Clin Invest 108(2), 169–173.Google Scholar
Farquhar, M.G. (1991). The glomerular basement membrane: A selective macromolecular filter. In Cell Biology of Extracellular Matrix, Hay, E.D. (Ed.), pp. 365–418. New York: Plenum Press.Google Scholar
Filmus, J. & Selleck, S.B. (2001). Glypicans: Proteoglycans with a surprise. J Clin Invest 108(4), 497–501.Google Scholar
Fox, J.G., Quin, J.D., O'Reilly, D.S. & Boulton-Jones, J.M. (1994). Glomerular charge selectivity in primary glomerulopathies. Clin Sci (Lond) 87(4), 421–425.CrossRefGoogle ScholarPubMed
Friden, V., Oveland, E., Tenstad, O., Ebefors, K., Nystrom, J., Nilsson, U.A. & Haraldsson, B. (2011). The glomerular endothelial cell coat is essential for glomerular filtration. Kidney Int 79(12), 1322–1330.Google Scholar
Frommer, J.P., Laski, M.E., Wesson, D.E. & Kurtzman, N.A. (1984). Internephron heterogeneity for carbonic anhydrase-independent bicarbonate reabsorption in the rat. J Clin Invest 73(4), 1034–1045.Google Scholar
Frommer, J.P., Sheth, A.U., Senekjian, H.O., Babino, H. & Weinman, E.J. (1982). Free-flow micropuncture study of renal urate transport in the Munich-Wistar rat. Miner Electrolyte Metab 7(6), 324–330.Google Scholar
Fujigaki, Y., Morioka, T., Matsui, K., Kawachi, H., Orikasa, M., Oite, T., Shimizu, F., Batsford, S.R. & Vogt, A. (1996). Structural continuity of filtration slit (slit diaphragm) to plasma membrane of podocyte. Kidney Int 50(1), 54–62.Google Scholar
Funderburgh, J.L. (2000). Keratan sulfate: Structure, biosynthesis, and function. Glycobiology 10(10), 951–958.CrossRefGoogle ScholarPubMed
Fuster, M.M., Wang, L., Castagnola, J., Sikora, L., Reddi, K., Lee, P.H., Radek, K.A., Schuksz, M., Bishop, J.R., Gallo, R.L., Sriramarao, P. & Esko, J.D. (2007). Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis. J Cell Biol 177(3), 539–549.Google Scholar
Gambaro, G., Cavazzana, A.O., Luzi, P., Piccoli, A., Borsatti, A., Crepaldi, G., Marchi, E., Venturini, A.P. & Baggio, B. (1992). Glycosaminoglycans prevent morphological renal alterations and albuminuria in diabetic rats. Kidney Int 42(2), 285–291.CrossRefGoogle ScholarPubMed
Garg, P., Verma, R., Cook, L., Soofi, A., Venkatareddy, M., George, B., Mizuno, K., Gurniak, C., Witke, W. & Holzman, L.B. (2010). Actin-depolymerizing factor cofilin-1 is necessary in maintaining mature podocyte architecture. J Biol Chem 285(29), 22676–22688.Google Scholar
Garner, O.B., Bush, K.T., Nigam, K.B., Yamaguchi, Y., Xu, D., Esko, J.D. & Nigam, S.K. (2011). Stage-dependent regulation of mammary ductal branching by heparan sulfate and HGF-cMet signaling. Dev Biol 355, 394–403.CrossRefGoogle ScholarPubMed
Garner, O.B., Yamaguchi, Y., Esko, J.D. & Videm, V. (2008). Small changes in lymphocyte development and activation in mice through tissue-specific alteration of heparan sulphate. Immunology 125(3), 420–429.Google Scholar
Goldberg, S., Harvey, S.J., Cunningham, J., Tryggvason, K. & Miner, J.H. (2009). Glomerular filtration is normal in the absence of both agrin and perlecan-heparan sulfate from the glomerular basement membrane. Nephrol Dial Transplant 24(7), 2044–2051.Google Scholar
Goode, N.P., Shires, M., Crellin, D.M., Aparicio, S.R. & Davison, A.M. (1995). Alterations of glomerular basement membrane charge and structure in diabetic nephropathy. Diabetologia 38(12), 1455–1465.Google Scholar
Gopal, S., Bober, A., Whiteford, J.R., Multhaupt, H.A., Yoneda, A. & Couchman, J.R. (2010). Heparan sulfate chain valency controls syndecan-4 function in cell adhesion. J Biol Chem 285(19), 14247–14258.Google Scholar
Gorsi, B. & Stringer, S.E. (2007). Tinkering with heparan sulfate sulfation to steer development. Trends Cell Biol 17(4), 173–177.Google Scholar
Gotting, C., Kuhn, J., Zahn, R., Brinkmann, T. & Kleesiek, K. (2000). Molecular cloning and expression of human UDP-d-Xylose:proteoglycan core protein beta-d-xylosyltransferase and its first isoform XT-II. J Mol Biol 304(4), 517–528.Google Scholar
Greiling, H. (1994). Structure and biological functions of keratan sulfate proteoglycans. EXS 70, 101–122.Google ScholarPubMed
Grobe, K., Inatani, M., Pallerla, S.R., Castagnola, J., Yamaguchi, Y. & Esko, J.D. (2005). Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development 132(16), 3777–3786.Google Scholar
Grobstein, C. (1967). Mechanisms of organogenetic tissue interaction. Natl Cancer Inst Monogr 26, 279–299.Google Scholar
Groffen, A.J., Hop, F.W., Tryggvason, K., Dijkman, H., Assmann, K.J., Veerkamp, J.H., Monnens, L.A. & Van den Heuvel, L.P. (1997). Evidence for the existence of multiple heparan sulfate proteoglycans in the human glomerular basement membrane and mesangial matrix. Eur J Biochem 247(1), 175–182.Google Scholar
Groffen, A.J., Ruegg, M.A., Dijkman, H., van de Velden, T.J., Buskens, C.A., van den Born, J., Assman, K.J., Monnens, L., Veerkamp, J.H. & van den Heuvel, L.P. (1998). Agrin is a major heparan sulfate proteoglycan in the glomerular basement membrane. J Histochem Cytochem 46, 19–27.CrossRefGoogle Scholar
Groffen, A.J., Veerkamp, J.H., Monnens, L.A. & van den Heuvel, L.P. (1999). Recent insights into the structure and functions of heparan sulfate proteoglycans in the human glomerular basement membrane. Nephrol Dial Transplant 14(9), 2119–2129.Google Scholar
Habuchi, H., Nagai, N., Sugaya, N., Atsumi, F., Stevens, R.L. & Kimata, K. (2007). Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J Biol Chem 282(21), 15578–15588.Google Scholar
Habuchi, H., Tanaka, M., Habuchi, O., Yoshida, K., Suzuki, H., Ban, K. & Kimata, K. (2000). The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J Biol Chem 275(4), 2859–2868.Google Scholar
Halfter, W., Dong, S., Schurer, B. & Cole, G.J. (1998). Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 273(39), 25404–25412.Google Scholar
Harvey, S.J., Jarad, G., Cunningham, J., Goldberg, S., Schermer, B., Harfe, B.D., McManus, M.T., Benzing, T. & Miner, J.H. (2008). Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 19(11), 2150–2158.Google Scholar
Harvey, S.V., Jarad, G., Cunningham, J., Rops, A.L., Van Der Vlag, J., Berden, J.H., Moeller, M.J., Holzman, L.B., Burgess, R.W. & Miner, J.H. (2007). Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Path 171(1), 139–152.Google Scholar
Hassell, J.R., Robey, P.G., Barrach, H.J., Wilczek, J., Rennard, S.I. & Martin, G.R. (1980). Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci USA 77, 4504–4508.Google Scholar
Heikkila, E., Juhila, J., Lassila, M., Messing, M., Perala, N., Lehtonen, E., Lehtonen, S., Sjef Verbeek, J. & Holthofer, H. (2010). beta-Catenin mediates adriamycin-induced albuminuria and podocyte injury in adult mouse kidneys. Nephrol Dial Transplant 25(8), 2437–2446.Google Scholar
Hjalmarsson, C., Johansson, B.R. & Haraldsson, B. (2004). Electron microscopic evaluation of the endothelial surface layer of glomerular capillaries. Microvasc Res 67(1), 9–17.Google Scholar
Ho, J., Ng, K.H., Rosen, S., Dostal, A., Gregory, R.I. & Kreidberg, J.A. (2008). Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol 19(11), 2069–2075.Google Scholar
Holmborn, K., Ledin, J., Smeds, E., Eriksson, I., Kusche-Gullberg, M. & Kjellen, L. (2004). Heparan sulfate synthesized by mouse embryonic stem cells deficient in NDST1 and NDST2 is 6-O-sulfated but contains no N-sulfate groups. J Biol Chem 279(41), 42355–42358.Google Scholar
Holzman, L.B., St John, P.L., Kovari, I.A., Verma, R., Holthofer, H. & Abrahamson, D.R. (1999). Nephrin localizes to the slit pore of the glomerular epithelial cell. Kidney Int 56(4), 1481–1491.CrossRefGoogle Scholar
Horowitz, A. & Simons, M. (2008). Branching morphogenesis. Circ Res 103(8), 784–795.Google Scholar
Hsu, J.C. & Yamada, K.M. (2010). Salivary gland branching morphogenesis—Recent progress and future opportunities. Int J Oral Sci 2(3), 117–126.Google Scholar
Hudson, B.G., Wieslander, J., Wisdom, B.J. & Noelken, M.E. (1989). Biology of disease. Goodpasture syndrome: Molecular architecture and function of basement membrane antigen. Lab Invest 61, 256–269.Google Scholar
Humphries, M.J., Mostafavi-Pour, Z., Morgan, M.R., Deakin, N.O., Messent, A.J. & Bass, M.D. (2005). Integrin-syndecan cooperation governs the assembly of signalling complexes during cell spreading. Novartis Found Symp 269, 178–188; discussion 188–192, 223–130.Google Scholar
Hwang, H.Y., Olson, S.K., Brown, J.R., Esko, J.D. & Horvitz, H.R. (2003a). The Caenorhabditis elegans genes sqv-2 and sqv-6, which are required for vulval morphogenesis, encode glycosaminoglycan galactosyltransferase II and xylosyltransferase. J Biol Chem 278(14), 11735–11738.Google Scholar
Hwang, H.Y., Olson, S.K., Esko, J.D. & Horvitz, H.R. (2003b). Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature 423(6938), 439–443.Google Scholar
Inatani, M., Irie, F., Plump, A.S., Tessier-Lavigne, M. & Yamaguchi, Y. (2003). Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 302, 1044–1046.CrossRefGoogle ScholarPubMed
Inoue, S., LeBlond, C.P. & Laurie, G.W. (1983). Ultrastructure of Reichert's membrane, a multilayered basement membrane in the parietal wall of the rat yolk sac. J Cell Biol 97, 1524–1537.CrossRefGoogle ScholarPubMed
Iozzo, R.V. (1997). The family of the small leucine-rich proteoglycans: Key regulators of matrix assembly and cellular growth. CR Biochem Mol Biol 32, 141–174.Google Scholar
Iozzo, R.V. (1998). Matrix proteoglycans: From molecular design to cellular function. Annu Rev Biochem 67, 609–652.CrossRefGoogle ScholarPubMed
Iozzo, R.V. (2005). Basement membrane proteoglycans: From cellar to ceiling. Nat Rev Mol Cell Biol 6(8), 646–656.Google Scholar
Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Matsuo, S., Kusugami, K., Saito, H. & Muramatsu, T. (2001). Syndecan-4 deficiency increases susceptibility to kappa-carrageenan-induced renal damage. Lab Invest 81(4), 509–516.Google Scholar
Iwao, K., Inatani, M., Matsumoto, Y., Ogata-Iwao, M., Takihara, Y., Irie, F., Yamaguchi, Y., Okinami, S. & Tanihara, H. (2009). Heparan sulfate deficiency leads to Peters anomaly in mice by disturbing neural crest TGF-beta2 signaling. J Clin Invest 119(7), 1997–2008.Google ScholarPubMed
Iwao, K., Inatani, M., Ogata-Iwao, M., Yamaguchi, Y., Okinami, S. & Tanihara, H. (2010). Heparan sulfate deficiency in periocular mesenchyme causes microphthalmia and ciliary body dysgenesis. Exp Eye Res 90(1), 81–88.CrossRefGoogle ScholarPubMed
Jalkanen, M., Nguyen, H., Rapraeger, A., Kurn, N. & Bernfield, M. (1985). Heparan sulfate proteoglycans from mouse mammary epithelial cells: Localization on the cell surface with a monoclonal antibody. J Cell Biol 101(3), 976–984.Google Scholar
Jarad, G., Pippin, J.W., Shankland, S.J., Kreidberg, J.A. & Miner, J.H. (2011). Dystroglycan does not contribute significantly to kidney development or function, in health or after injury. Am J Physiol Renal Physiol 300(3), F811–F820.Google Scholar
Jenniskens, G.J., Oosterhof, A., Brandwijk, R., Veerkamp, J.H. & van Kuppevelt, T.H. (2000). Heparan sulfate heterogeneity in skeletal muscle basal lamina: Demonstration by phage display-derived antibodies. J Neurosci 20(11), 4099–4111.Google Scholar
Jia, Q., McDill, B.W., Sankarapandian, B., Wu, S., Liapis, H., Holzman, L.B., Capecchi, M.R., Miner, J.H. & Chen, F. (2008). Ablation of developing podocytes disrupts cellular interactions and nephrogenesis both inside and outside the glomerulus. Am J Physiol Renal Physiol 295(6), F1790–F1798.Google Scholar
Johnson, C.E., Crawford, B.E., Stavridis, M., Ten Dam, G., Wat, A.L., Rushton, G., Ward, C.M., Wilson, V., van Kuppevelt, T.H., Esko, J.D., Smith, A., Gallagher, J.T. & Merry, C.L. (2007). Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells 25(8), 1913–1923.Google Scholar
Jones, K.B., Piombo, V., Searby, C., Kurriger, G., Yang, B., Grabellus, F., Roughley, P.J., Morcuende, J.A., Buckwalter, J.A., Capecchi, M.R., Vortkamp, A. & Sheffield, V.C. (2010). A mouse model of osteochondromagenesis from clonal inactivation of Ext1 in chondrocytes. Proc Natl Acad Sci USA 107(5), 2054–2059.CrossRefGoogle ScholarPubMed
Juhila, J., Roozendaal, R., Lassila, M., Verbeek, S.J. & Holthofer, H. (2006). Podocyte cell-specific expression of doxycycline inducible Cre recombinase in mice. J Am Soc Nephrol 17(3), 648–654.Google Scholar
Kallunki, P. & Tryggvason, K. (1992). Human basement membrane heparan sulfate proteoglycan core protein: A 467-kD protein containing multiple domains resembling elements of the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J Cell Biol 116, 559–571.CrossRefGoogle ScholarPubMed
Kanwar, Y.S. & Farquhar, M.G. (1979). Anionic sites in the glomerular basement membrane. In vivo and in vitro localization to the lamina rarae by cationic probes. J Cell Biol 81, 137–153.Google Scholar
Kanwar, Y.S., Linker, A. & Farquhar, M.G. (1980). Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion. J Cell Biol 86, 688–693.Google Scholar
Kanwar, Y.S. & Rosenzweig, L.J. (1982). Clogging of the glomerular basement membrane. J Cell Biol 93, 489–494.Google Scholar
Kasinath, B.S., Grellier, P., Choudhury, G.G. & Abboud, S.L. (1996). Regulation of basement membrane heparan sulfate proteoglycan, perlecan, gene expression in glomerular epithelial cells by high glucose medium. J Cell Physiol 167(1), 131–136.Google Scholar
Katz, A., Fish, A.J., Kleppel, M.M., Hagen, S.G., Michael, A.F. & Butkowski, R.J. (1991). Renal entactin (nidogen): Isolation, characterization and tissue distribution. Kidney Int 40(4), 643–652.CrossRefGoogle ScholarPubMed
Kazama, I., Mahoney, Z., Miner, J.H., Graf, D., Economides, A.N. & Kreidberg, J.A. (2008). Podocyte-derived BMP7 is critical for nephron development. J Am Soc Nephrol 19(11), 2181–2191.CrossRefGoogle ScholarPubMed
Kefalides, N.A. (1971). Isolation of a collagen from basement membranes containing three identical—Chains. Biochem Biophys Res Commun 45(1), 226–234.Google Scholar
Khoshnoodi, J., Pedchenko, V. & Hudson, B.G. (2008). Mammalian collagen IV. Microsc Res Techn 71(5), 357–370.Google Scholar
Kim, B.T., Kitagawa, H., Tamura, J., Saito, T., Kusche-Gullberg, M., Lindahl, U. & Sugahara, K. (2001). Human tumor suppressor EXT gene family members EXTL1 and EXTL3 encode alpha 1,4-N-acetylglucosaminyltransferases that likely are involved in heparan sulfate/heparin biosynthesis. Proc Natl Acad Sci USA 98(13), 7176–7181.Google Scholar
Kitamura, M., Mitarai, T., Nagasawa, R. & Maruyama, N. (1996). Differentiated phenotype of glomerular mesangial cells in nodular culture. Am J Physiol 270(4 Pt 2), F614–F622.Google Scholar
Kleinman, H.K. & Martin, G.R. (2005). Matrigel: Basement membrane matrix with biological activity. Semin Cancer Biol 15(5), 378–386.Google Scholar
Kleinman, H.K., McGarvey, M.L., Liotta, L.A., Robey, P.G., Tryggvason, K. & Martin, G.R. (1982). Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21(24), 6188–6193.Google Scholar
Koda, J.E., Rapraeger, A. & Bernfield, M. (1985). Heparan sulfate proteoglycans from mouse mammary epithelial cells. Cell surface proteoglycan as a receptor for interstitial collagens. J Biol Chem 260(13), 8157–8162.Google Scholar
Kruegel, J. & Miosge, N. (2010). Basement membrane components are key players in specialized extracellular matrices. Cell Mol Life Sci 67(17), 2879–2895.Google Scholar
Lane, P.H., Steffes, M.W. & Mauer, S.M. (1990). Renal histologic changes in diabetes mellitus. Semin Nephrol 10, 254–259.Google Scholar
Li, J.P., Gong, F., Hagner-McWhirter, A., Forsberg, E., Abrink, M., Kisilevsky, R., Zhang, X. & Lindahl, U. (2003). Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J Biol Chem 278(31), 28363–28366.Google Scholar
Lin, X., Wei, G., Shi, Z., Dryer, L., Esko, J.D., Wells, D.E. & Matzuk, M.M. (2000). Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev Biol 224(2), 299–311.Google Scholar
Lind, T., Tufaro, F., McCormick, C., Lindahl, U. & Lidholt, K. (1998). The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate. J Biol Chem 273(41), 26265–26268.Google Scholar
Liu, J., Shriver, Z., Blaiklock, P., Yoshida, K., Sasisekharan, R. & Rosenberg, R.D. (1999). Heparan sulfate D-glucosaminyl 3-O-sulfotransferase-3A sulfates N-unsubstituted glucosamine residues. J Biol Chem 274(53), 38155–38162.Google Scholar
Lu, P., Sternlicht, M.D. & Werb, Z. (2006). Comparative mechanisms of branching morphogenesis in diverse systems. J Mammary Gland Biol Neoplasia 11(3-4), 213–228.Google Scholar
MacArthur, J.M., Bishop, J.R., Stanford, K.I., Wang, L., Bensadoun, A., Witztum, J.L. & Esko, J.D. (2007). Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest 117(1), 153–164.Google Scholar
Malmstrom, A., Roden, L., Feingold, D.S., Jacobsson, I., Backstrom, G. & Lindahl, U. (1980). Biosynthesis of heparin. Partial purification of the uronosyl C-5 epimerase. J Biol Chem 255(9), 3878–3883.Google Scholar
Martin, G.R., Kleinman, H.K., Terranova, V.P., Ledbetter, S. & Hassell, J.R. (1984). The regulation of basement membrane formation and cell-matrix interactions by defined supramolecular complexes. Ciba Found Symp 108, 197–212.Google Scholar
Matsumoto, Y., Irie, F., Inatani, M., Tessier-Lavigne, M. & Yamaguchi, Y. (2007). Netrin-1/DCC signaling in commissural axon guidance requires cell-autonomous expression of heparan sulfate. J Neurosci 27(16), 4342–4350.Google Scholar
Matsumoto, Y., Matsumoto, K., Irie, F., Fukushi, J., Stallcup, W.B. & Yamaguchi, Y. (2010). Conditional ablation of the heparan sulfate-synthesizing enzyme Ext1 leads to dysregulation of bone morphogenic protein signaling and severe skeletal defects. J Biol Chem 285(25), 19227–19234.Google Scholar
Mauer, S.M., Steffes, M.W., Ellis, E.N., Sutherland, D.E.R., Brown, D.M. & Goetz, F.C. (1984). Structural-functional relationships in diabetic nephropathy. J Clin Invest 74, 1143–1155.Google Scholar
McCarthy, K.J. (Ed.) (2008). Basement Membranes: From the Matrisome to Beyond. Microscopy Research and Technique. New York: Wiley Subscription Services, Inc.Google Scholar
McCarthy, K.J., Accavitti, M.A. & Couchman, J.R. (1989). Immunological characterization of a basement membrane-specific chondroitin sulfate proteoglycan. J Cell Biol 109, 3187–3198.Google Scholar
McCarthy, K.J. & Couchman, J.R. (1990). Basement membrane chondroitin sulfate proteoglycans: Localization in adult rat tissues. J Histochem Cytochem 38, 1479–1486.Google Scholar
McCormick, C., Duncan, G., Goutsos, K.T. & Tufaro, F. (2000). The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc Natl Acad Sci USA 97(2), 668–673.CrossRefGoogle Scholar
McCormick, C., Leduc, Y., Martindale, D., Mattison, K., Esford, L.E., Dyer, A.P. & Tufaro, F. (1998). The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat Genet 19(2), 158–161.Google Scholar
Metzger, R.J. & Krasnow, M.A. (1999). Genetic control of branching morphogenesis. Science 284(5420), 1635–1639.Google Scholar
Miettinen, A., Stow, J.L., Mentone, S. & Farquhar, M.G. (1986). Antibodies to basement membrane heparan sulfate proteoglycans bind to the lamina rarae of the glomerular basement membrane (GBM) and induce subepithelial basement membrane thickening. J Exp Med 163, 1064–1084.Google Scholar
Miner, J.H. (1999). Renal basement membrane components. Kidney Int 56(6), 2016–2024.Google Scholar
Miner, J.H. (2005). Building the glomerulus: A matricentric view. J Am Soc Nephrol 16(4), 857–861.Google Scholar
Miosge, N., Kother, F., Heinemann, S., Kohfeldt, E., Herken, R. & Timpl, R. (2000). Ultrastructural colocalization of nidogen-1 and nidogen-2 with laminin-1 in murine kidney basement membranes. Histochem Cell Biol 113(2), 115–124.Google Scholar
Moeller, M., Sanden, S., Soofi, A., Wiggins, R. & Holzman, L. (2003). Podocyte-specific expression of Cre recombinase in transgenic mice. Genesis 35, 39–42.Google Scholar
Molitoris, B.A. & Sandoval, R.M. (2006). Pharmacophotonics: Utilizing multi-photon microscopy to quantify drug delivery and intracellular trafficking in the kidney. Adv Drug Deliv Rev 58(7), 809–823.Google Scholar
Molitoris, B.A. & Sandoval, R.M. (2007). Quantifying dynamic kidney processes utilizing multi-photon microscopy. Contrib Nephrol 156, 227–235.Google Scholar
Mollet, G., Ratelade, J., Boyer, O., Muda, A.O., Morisset, L., Lavin, T.A., Kitzis, D., Dallman, M.J., Bugeon, L., Hubner, N., Gubler, M.C., Antignac, C. & Esquivel, E.L. (2009). Podocin inactivation in mature kidneys causes focal segmental glomerulosclerosis and nephrotic syndrome. J Am Soc Nephrol 20(10), 2181–2189.Google Scholar
Morano, S., D'Erme, M., Sensi, M., De Rossi, M.G., Medici, F., Galliccia, F., Andreani, D. & Di Mario, U. (1994). Characteristics of proteinuria in experimental diabetes mellitus. Biochem Med Metab Biol 53(2), 92–97.Google Scholar
Morano, S., Pietravalle, P., De Rossi, M.G., Mariani, G., Cristina, G., Medici, F., Sensi, M., Andreani, D. & Di Mario, U. (1993). A charge selectivity impairment in protein permselectivity is present in type 2 diabetes. Acta Diabetol 30(3), 138–142.Google Scholar
Morgan, M.R., Humphries, M.J. & Bass, M.D. (2007). Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 8(12), 957–969.Google Scholar
Morio, H., Honda, Y., Toyoda, H., Nakajima, M., Kurosawa, H. & Shirasawa, T. (2003). EXT gene family member rib-2 is essential for embryonic development and heparan sulfate biosynthesis in Caenorhabditis elegans. Biochem Biophys Res Commun 301(2), 317–323.Google Scholar
Morita, H., Yoshimura, A., Inui, K., Ideura, T., Watanabe, H., Wang, L., Soininen, R. & Tryggvason, K. (2005). Heparan sulfate of perlecan is involved in glomerular filtration. J Am Soc Nephrol 16, 1703–1710.Google Scholar
Mundy, C., Yasuda, T., Kinumatsu, T., Yamaguchi, Y., Iwamoto, M., Enomoto-Iwamoto, M., Koyama, E. & Pacifici, M. (2011). Synovial joint formation requires local Ext1 expression and heparan sulfate production in developing mouse embryo limbs and spine. Dev Biol 351(1), 70–81.Google Scholar
Murdoch, A.D., Dodge, G.R., Cohen, I., Tuan, R.S. & Iozzo, R.V. (1992). Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/Perlecan). J Biol Chem 267, 8544–8557.CrossRefGoogle ScholarPubMed
Nakagawa, T., Izumino, K., Ishii, Y., Oya, T., Hamashima, T., Jie, S., Ishizawa, S., Tomoda, F., Fujimori, T., Nabeshima, Y., Inoue, H. & Sasahara, M. (2011). Roles of PDGF receptor-beta in the structure and function of postnatal kidney glomerulus. Nephrol Dial Transplant 26(2), 458–468.Google Scholar
Nakato, H. & Kimata, K. (2002). Heparan sulfate fine structure and specificity of proteoglycan functions. Biochim Biophys Acta 1573(3), 312–318.Google Scholar
Noonan, D.M., Fulle, A., Valente, P., Cai, S., Horigan, E., Sasaki, M., Yamada, Y. & Hassell, J.R. (1991). The complete sequence of Perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J Biol Chem 266, 22939–22947.Google Scholar
Ogata-Iwao, M., Inatani, M., Iwao, K., Takihara, Y., Nakaishi-Fukuchi, Y., Irie, F., Sato, S., Furukawa, T., Yamaguchi, Y. & Tanihara, H. (2011). Heparan sulfate regulates intraretinal axon pathfinding by retinal ganglion cells. Invest Ophthalmol Vis Sci 52(9), 6671–6679.Google Scholar
Oh, E.S., Woods, A. & Couchman, J.R. (1997a). Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J Biol Chem 272(18), 11805–11811.Google Scholar
Oh, E.S., Woods, A. & Couchman, J.R. (1997b). Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem 272(13), 8133–8136.Google Scholar
Okada, K., Kawakami, K., Yano, I., Funai, M., Kagami, S., Kuroda, Y. & Oite, T. (1989). Ultrastructural alterations of glomerular anionic sites in IgA nephropathy. Clin Nephrol 31(2), 96–102.Google Scholar
Orellana, A., Hirschberg, C.B., Wei, Z., Swiedler, S.J. & Ishihara, M. (1994). Molecular cloning and expression of a glycosaminoglycan N-acetylglucosaminyl N-deacetylase/N-sulfotransferase from a heparin-producing cell line. J Biol Chem 269(3), 2270–2276.Google Scholar
Ori, A., Wilkinson, M.C. & Fernig, D.G. (2011). A systems biology approach for the investigation of the heparin/heparan sulfate interactome. J Biol Chem 286(22), 19892–198904.Google Scholar
Orkin, R.W., Gehron, P., McGoodwin, E.B., Martin, G.R., Valentine, T. & Swarm, R. (1977). A murine tumor producing a matrix of basement membrane. J Exp Med 145(1), 204–220.Google Scholar
Osterby, R. (1986). Structural changes in the diabetic kidney. Clin Endocrin Met 15, 733–751.Google Scholar
Pan, Y., Carbe, C., Powers, A., Zhang, E.E., Esko, J.D., Grobe, K., Feng, G.S. & Zhang, X. (2008). Bud specific N-sulfation of heparan sulfate regulates Shp2-dependent FGF signaling during lacrimal gland induction. Development 135(2), 301–310.Google Scholar
Park, P.W., Reizes, O. & Bernfield, M. (2000). Cell surface heparan sulfate proteoglycans: Selective regulators of ligand-receptor encounters. J Biol Chem 275(39), 29923–29926.Google Scholar
Patel, V.N., Rebustini, I.T. & Hoffman, M.P. (2006). Salivary gland branching morphogenesis. Differentiation 74(7), 349–364.Google Scholar
Peti-Peterdi, J. (2005). Multiphoton imaging of renal tissues in vitro. Am J Physiol Renal Physiol 288(6), F1079–F1083.Google Scholar
Peti-Peterdi, J. & Sipos, A. (2010). A high-powered view of the filtration barrier. J Am Soc Nephrol 21(11), 1835–1841.Google Scholar
Peti-Peterdi, J., Toma, I., Sipos, A. & Vargas, S.L. (2009). Multiphoton imaging of renal regulatory mechanisms. Physiol (Bethesda) 24, 88–96.Google Scholar
Ponighaus, C., Ambrosius, M., Casanova, J.C., Prante, C., Kuhn, J., Esko, J.D., Kleesiek, K. & Gotting, C. (2007). Human xylosyltransferase II is involved in the biosynthesis of the uniform tetrasaccharide linkage region in chondroitin sulfate and heparan sulfate proteoglycans. J Biol Chem 282(8), 5201–5206.Google Scholar
Pozzi, A., Jarad, G., Moeckel, G.W., Coffa, S., Zhang, X., Gewin, L., Eremina, V., Hudson, B.G., Borza, D.B., Harris, R.C., Holzman, L.B., Phillips, C.L., Fassler, R., Quaggin, S.E., Miner, J.H. & Zent, R. (2008). Beta1 integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol 316(2), 288–301.Google Scholar
Raats, C.J., Bakker, M.A., Hoch, W., Tamboer, W.P., Groffen, A.J., van den Heuvel, L.P., Berden, J.H. & van den Born, J. (1998). Differential expression of agrin in renal basement membranes as revealed by domain-specific antibodies. J Biol Chem 273(28), 17832–17838.Google Scholar
Raats, C.J., Van Den Born, J. & Berden, J.H. (2000). Glomerular heparan sulfate alterations: Mechanisms and relevance for proteinuria. Kidney Int 57(2), 385–400.Google Scholar
Rada, J.A. & Carlson, E.C. (1991). Anionic site and immunogold quantitation of heparan sulfate proteoglycans in glomerular basement membranes of puromycin aminonucleoside nephrotic rats. Anatomical Record 231, 35–47.Google Scholar
Rapraeger, A. & Bernfield, M. (1985). Cell surface proteoglycan of mammary epithelial cells. Protease releases a heparan sulfate-rich ectodomain from a putative membrane-anchored domain. J Biol Chem 260(7), 4103–4109.Google Scholar
Rapraeger, A., Jalkanen, M., Endo, E., Koda, J. & Bernfield, M. (1985). The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J Biol Chem 260(20), 11046–11052.Google Scholar
Rapraeger, A.C. (2001). Molecular interactions of syndecans during development. Semin Cell Dev Biol 12(2), 107–116.Google Scholar
Ray, M.C. & Gately, L.E. 3rd (1996). Basement membrane zone. Clin Dermatol 14(4), 321–330.Google Scholar
Reeves, W.H., Kanwar, Y.S. & Farquhar, M.G. (1980). Assembly of the glomerular filtration surface. Differentiation of anionic sites in glomerular capillaries of newborn rat kidney. J Cell Biol 85(3), 735–753.Google Scholar
Reijmers, R.M., Groen, R.W., Kuil, A., Weijer, K., Kimberley, F.C., Medema, J.P., van Kuppevelt, T.H., Li, J.P., Spaargaren, M. & Pals, S.T. (2011). Disruption of heparan sulfate proteoglycan conformation perturbs B-cell maturation and APRIL-mediated plasma cell survival. Blood 117(23), 6162–6171.Google Scholar
Rennke, H.G., Cotran, R.S. & Venkatachalam, M.A. (1975). Role of molecular charge in glomerular permeability. Tracer studies with cationized ferritins. J Cell Biol 67(3), 638–646.Google Scholar
Rennke, H.G. & Venkatachalam, M.A. (1977). Glomerular permeability: In vivo tracer studies with polyanionic and polycationic ferritins. Kidney Int 11(1), 44–53.Google Scholar
Rodewald, R. & Karnovsky, M. (1974). Porous substructure of the glomerular slit diaphragm in the rat and mouse. J Cell Biol 60, 423–433.CrossRefGoogle ScholarPubMed
Rong, J., Habuchi, H., Kimata, K., Lindahl, U. & Kusche-Gullberg, M. (2000). Expression of heparan sulphate L-iduronyl 2-O-sulphotransferase in human kidney 293 cells results in increased D-glucuronyl 2-O-sulphation. Biochem J 346, 463–468.Google Scholar
Rong, J., Habuchi, H., Kimata, K., Lindahl, U. & Kusche-Gullberg, M. (2001). Substrate specificity of the heparan sulfate hexuronic acid 2-O-sulfotransferase. Biochemistry 40(18), 5548–5555.Google Scholar
Rosenberg, R.D., Shworak, N.W., Liu, J., Schwartz, J.J. & Zhang, L. (1997). Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J Clin Invest 99(9), 2062–2070.Google Scholar
Rossi, M., Morita, H., Sormunen, R., Airenne, S., Kreivi, M., Wang, L., Fukai, N., Olsen, B.J., Tryggvason, K. & Soininen, R. (2003). Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J 22(2), 236–245.Google Scholar
Russo, L.M., Sandoval, R.M., Campos, S.B., Molitoris, B.A., Comper, W.D. & Brown, D. (2009). Impaired tubular uptake explains albuminuria in early diabetic nephropathy. J Am Soc Nephrol 20(3), 489–494.Google Scholar
Sakagami, Y., Nakajima, M., Takagawa, K., Ueda, T., Akazawa, H., Maruhashi, Y., Shimoyama, H., Kamitsuji, H. & Yoshioka, A. (2004). Analysis of glomerular anionic charge status in children with IgA nephropathy using confocal laser scanning microscopy. Nephron Clin Pract 96(3), c96–c104.Google Scholar
Saleem, M.A., Ni, L., Witherden, I., Tryggvason, K., Ruotsalainen, V., Mundel, P. & Mathieson, P.W. (2002). Co-localization of nephrin, podocin, and the actin cytoskeleton: Evidence for a role in podocyte foot process formation. Am J Pathol 161(4), 1459–1466.Google Scholar
Sanes, J.R. (2003). The basement membrane/basal lamina of skeletal muscle. J Biol Chem 278(15), 12601–12604.Google Scholar
Saoncella, S., Echtermeyer, F., Denhez, F., Nowlen, J.K., Mosher, D.F., Robinson, S.D., Hynes, R.O. & Goetinck, P.F. (1999). Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc Natl Acad Sci USA 96(6), 2805–2810.Google Scholar
Sasaki, T., Fassler, R. & Hohenester, E. (2004). Laminin: The crux of basement membrane assembly. J Cell Biol 164(7), 959–963.Google Scholar
Satchell, S.C. & Braet, F. (2009). Glomerular endothelial cell fenestrations: An integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol 296(5), F947–F956.Google Scholar
Schor, N., Ichikawa, I. & Brenner, B.M. (1981). Mechanisms of action of various hormones and vasoactive substances on glomerular ultrafiltration in the rat. Kidney Int 20(4), 442–451.CrossRefGoogle ScholarPubMed
Seiler, M.W., Rennke, H.G., Venkatachalam, M.A. & Cotran, R.S. (1977). Pathogenesis of polycation-induced alterations (fusion) of glomerular epithelium. Lab Invest 36(1), 48–61.Google Scholar
Seiler, M.W., Venkatachalam, M.A. & Cotran, R.S. (1975). Glomerular epithelium: Structural alterations induced by polycations. Science 189(4200), 390–393.Google Scholar
Shah, M.M., Sakurai, H., Gallegos, T.F., Sweeney, D.E., Bush, K.T., Esko, J.D. & Nigam, S.K. (2011). Growth factor-dependent branching of the ureteric bud is modulated by selective 6-O sulfation of heparan sulfate. Dev Biol 356(1), 19–27.Google Scholar
Shah, M.M., Sakurai, H., Sweeney, D.E., Gallegos, T.F., Bush, K.T., Esko, J.D. & Nigam, S.K. (2010). Hs2st mediated kidney mesenchyme induction regulates early ureteric bud branching. Dev Biol 339(2), 354–365.Google Scholar
Sheng, J., Liu, R., Xu, Y. & Liu, J. (2011). The dominating role of N-deacetylase/N-sulfotransferase 1 in forming domain structures in heparan sulfate. J Biol Chem 286(22), 19768–19776.Google Scholar
Shigehara, T., Zaragoza, C., Kitiyakara, C., Takahashi, H., Lu, H., Moeller, M., Holzman, L.B. & Kopp, J.B. (2003). Inducible podocyte-specific gene expression in transgenic mice. J Am Soc Nephrol 14(8), 1998–2003.Google Scholar
Shworak, N.W., Liu, J., Fritze, L.M., Schwartz, J.J., Zhang, L., Logeart, D. & Rosenberg, R.D. (1997). Molecular cloning and expression of mouse and human cDNAs encoding heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J Biol Chem 272(44), 28008–28019.Google Scholar
Shworak, N.W., Liu, J., Petros, L.M., Zhang, L., Kobayashi, M., Copeland, N.G., Jenkins, N.A. & Rosenberg, R.D. (1999). Multiple isoforms of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. Isolation, characterization, and expression of human cdnas and identification of distinct genomic loci. J Biol Chem 274(8), 5170–5184.Google Scholar
Simons, M. & Horowitz, A. (2001). Syndecan-4-mediated signalling. Cell Signal 13(12), 855–862.Google Scholar
Singh, A., Friden, V., Dasgupta, I., Foster, R.R., Welsh, G.I., Tooke, J.E., Haraldsson, B., Mathieson, P.W. & Satchell, S.C. (2011). High glucose causes dysfunction of the human glomerular endothelial glycocalyx. Am J Physiol Renal Physiol 300(1), F40–F48.Google Scholar
Singh, A., Satchell, S.C., Neal, C.R., McKenzie, E.A., Tooke, J.E. & Mathieson, P.W. (2007). Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 18(11), 2885–2893.Google Scholar
Smith, R.L. & Bernfield, M. (1982). Mesenchyme cells degrade epithelial basal lamina glycosaminoglycan. Dev Biol 94(2), 378–390.Google Scholar
Smits, N.C., Lensen, J.F., Wijnhoven, T.J., Ten Dam, G.B., Jenniskens, G.J. & van Kuppevelt, T.H. (2006). Phage display-derived human antibodies against specific glycosaminoglycan epitopes. Methods Enzymol 416, 61–87.Google Scholar
Spiro, R.G. (1978). Nature of the glycoprotein components of basement membranes. Ann NY Acad Sci 312, 106–121.Google Scholar
St John, P.L. & Abrahamson, D.R. (2001). Glomerular endothelial cells and podocytes jointly synthesize laminin-1 and -11 chains. Kidney Int 60(3), 1037–1046.Google Scholar
Stanford, K.I., Wang, L., Castagnola, J., Song, D., Bishop, J.R., Brown, J.R., Lawrence, R., Bai, X., Habuchi, H., Tanaka, M., Cardoso, W.V., Kimata, K. & Esko, J.D. (2010). Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem 285(1), 286–294.Google Scholar
Steenhard, B.M., Isom, K., Stroganova, L., St John, P.L., Zelenchuk, A., Freeburg, P.B., Holzman, L.B. & Abrahamson, D.R. (2010). Deletion of von Hippel-Lindau in glomerular podocytes results in glomerular basement membrane thickening, ectopic subepithelial deposition of collagen {alpha}1{alpha}2{alpha}1(IV), expression of neuroglobin, and proteinuria. Am J Pathol 177(1), 84–96.Google Scholar
Steer, D.L., Shah, M.M., Bush, K.T., Stuart, R.O., Sampogna, R.V., Meyer, T.N., Schwesinger, C., Bai, X., Esko, J.D. & Nigam, S.K. (2004). Regulation of ureteric bud branching morphogenesis by sulfated proteoglycans in the developing kidney. Dev Biol 272(2), 310–327.CrossRefGoogle ScholarPubMed
Steffes, M.W. & Mauer, S.M. (1984). Diabetic glomerulopathy in man and experimental animal models. Int Rev Exp Path 26, 147–175.Google Scholar
Steffes, M.W., Osterby, R., Chavers, B. & Mauer, S.M. (1989). Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients. Diabetes 38, 1077–1081.Google Scholar
Stenman, S. & Vaheri, A. (1978). Distribution of a major connective tissue protein, fibronectin, in normal human tissues. J Exp Med 147(4), 1054–1064.Google Scholar
Stephenson, L.A., Haney, L.B., Hussaini, I.M., Karns, L.R. & Glass, W.F. 2nd (1998). Reguation of smooth muscle a-actin expression and hypertrophy in cultured mesangial cells. Kidney Int 54, 1175–1187.Google Scholar
Stickens, D., Zak, B.M., Rougier, N., Esko, J.D. & Werb, Z. (2005). Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132(22), 5055–5068.Google Scholar
Takahashi, S., Watanabe, S., Wada, N., Murakami, H., Funaki, S., Yan, K., Kondo, Y., Harada, K. & Nagata, M. (2006). Charge selective function in childhood glomerular diseases. Pediatr Res 59(2), 336–340.Google Scholar
Tanner, G.A. (2009). Glomerular sieving coefficient of serum albumin in the rat: A two-photon microscopy study. Am J Physiol Renal Physiol 296(6), F1258–F1265.Google Scholar
Tapanadechopone, P., Hassell, J.R., Rigatti, B. & Couchman, J.R. (1999). Localization of glycosaminoglycan substitution sites on domain V of mouse perlecan. Biochem Biophys Res Commun 265(3), 680–690.Google Scholar
Ten Dam, G.B., Kurup, S., van de Westerlo, E.M., Versteeg, E.M., Lindahl, U., Spillmann, D. & van Kuppevelt, T.H. (2006). 3-O-sulfated oligosaccharide structures are recognized by anti-heparan sulfate antibody HS4C3. J Biol Chem 281(8), 4654–4662.Google Scholar
Thomas, G.J., Shewring, L., McCarthy, K.J., Couchman, J.R., Mason, R.M. & Davies, M. (1995). Rat mesangial cells in vitro synthesize a spectrum of proteoglycan species including those of the basement membrane and interstitium. Kidney Int 48(4), 1278–1289.Google Scholar
Thompson, S.M., Connell, M.G., Fernig, D.G., Ten Dam, G.B., van Kuppevelt, T.H., Turnbull, J.E., Jesudason, E.C. & Losty, P.D. (2007). Novel 'phage display antibodies identify distinct heparan sulfate domains in developing mammalian lung. Pediatr Surg Int 23, 411–417.Google Scholar
Timpl, R., Rohde, M., Robey, P.G., Rennard, S.I., Foidart, J.-M. & Martin, G.R. (1979). Laminin: A glycoprotein from basement membranes. J Biol Chem 254, 9933–9937.Google Scholar
Tkachenko, E., Rhodes, J.M. & Simons, M. (2005). Syndecans: New kids on the signaling block. Circ Res 96(5), 488–500.Google Scholar
Toyoda, H., Kinoshita-Toyoda, A. & Selleck, S.B. (2000). Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo. J Biol Chem 275(4), 2269–2275.Google Scholar
Uchimura, K., Fasakhany, F., Kadomatsu, K., Matsukawa, T., Yamakawa, T., Kurosawa, N. & Muramatsu, T. (2000). Diversity of N-acetylglucosamine-6-O-sulfotransferases: Molecular cloning of a novel enzyme with different distribution and specificities. Biochem Biophys Res Commun 274(2), 291–296.Google Scholar
Uchimura, K., Muramatsu, H., Kadomatsu, K., Fan, Q.W., Kurosawa, N., Mitsuoka, C., Kannagi, R., Habuchi, O. & Muramatsu, T. (1998). Molecular cloning and characterization of an N-acetylglucosamine-6-O-sulfotransferase. J Biol Chem 273(35), 22577–22583.Google Scholar
van den Born, J., Van Den Heuvel, L.P.W.J., Bakker, M.A.H., Veerkamp, J.H., Assmann, K.J.M. & Berden, J.H.M. (1992). A monoclonal antibody against GBM heparan sulfate induces an acute selective proteinuria in rats. Kidney Int 411, 115–123.Google Scholar
van den Born, J., van Kraats, A.A., Bakker, M.A., Assmann, K.J., Dijkman, H.B., van der Laak, J.A. & Berden, J.H. (1995). Reduction of heparan sulphate-associated anionic sites in the glomerular basement membrane of rats with streptozotocin-induced diabetic nephropathy. Diabetologia 38(10), 1169–1175.Google Scholar
van Kuppevelt, T.H., Dennissen, M.A., van Venrooij, W.J., Hoet, R.M. & Veerkamp, J.H. (1998). Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology. Further evidence for heparan sulfate heterogeneity in the kidney. J Biol Chem 273(21), 12960–12966.Google Scholar
van Kuppevelt, T.H., Jenniskens, G.J., Veerkamp, J.H., ten Dam, G.B. & Dennissen, M.A. (2001). Phage display technology to obtain antiheparan sulfate antibodies. Methods Mol Biol 171, 519–534.Google Scholar
Wada, N., Ueda, Y., Iidaka, K., Inage, Z., Kikkawa, Y. & Kitagawa, T. (1990). Portions of basement membrane with decreased negative charge in various glomerulonephritis. Clin Nephrol 34(1), 9–16.Google Scholar
Whiteside, C.I., Cameron, R., Munk, S. & Levy, J. (1993). Podocytic cytoskeletal disaggregation and basement-membrane detachment in puromycin aminonucleoside nephrosis. Am J Pathol 142(5), 1641–1653.Google Scholar
Wilcox-Adelman, S.A., Denhez, F., Iwabuchi, T., Saoncella, S., Calautti, E. & Goetinck, P.F. (2002). Syndecan-4: Dispensable or indispensable? Glycoconj J 19(4-5), 305–313.Google Scholar
Woods, A. (2001). Syndecans: Transmembrane modulators of adhesion and matrix assembly. J Clin Invest 107(8), 935–941.Google Scholar
Woods, A. & Couchman, J.R. (1998). Syndecans: Synergistic activators of cell adhesion. Trends Cell Biol 8(5), 189–192.Google Scholar
Woods, A. & Couchman, J.R. (2001). Syndecan-4 and focal adhesion function. Curr Opin Cell Biol 13(5), 578–583.Google Scholar
Woods, A., Couchman, J.R. & Hook, M. (1985). Heparan sulfate proteoglycans of rat embryo fibroblasts. A hydrophobic form may link cytoskeleton and matrix components. J Biol Chem 260(19), 10872–10879.Google Scholar
Woods, A., Hook, M., Kjellen, L., Smith, C.G. & Rees, D.A. (1984). Relationship of heparan sulfate proteoglycans to the cytoskeleton and extracellular matrix of cultured fibroblasts. J Cell Biol 99(5), 1743–1753.Google Scholar
Woods, A., Longley, R.L., Tumova, S. & Couchman, J.R. (2000). Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 374(1), 66–72.Google Scholar
Young, P.A., Clendenon, S.G., Byars, J.M., Decca, R.S. & Dunn, K.W. (2011a). The effects of spherical aberration on multiphoton fluorescence excitation microscopy. J Microsc 242(2), 157–165.Google Scholar
Young, P.A., Clendenon, S.G., Byars, J.M. & Dunn, K.W. (2011b). The effects of refractive index heterogeneity within kidney tissue on multiphoton fluorescence excitation microscopy. J Microsc 242(2), 148–156.Google Scholar
Yung, S., Woods, A., Chan, T.M., Davies, M., Williams, J.D. & Couchman, J.R. (2001). Syndecan-4 up-regulation in proliferative renal disease is related to microfilament organization. FASEB J 15(9), 1631–1633.Google Scholar
Yurchenco, P.D. & O'Rear, J. (1993). Supramolecular organization of basement membranes. In Molecular and Cellular Aspects of Basement Membranes, Rohrbach, D.H. & Timpl, R. (Eds.), pp. 19–47. San Diego, CA: Academic Press.Google Scholar
Zcharia, E., Metzger, S., Chajek-Shaul, T., Aingorn, H., Elkin, M., Friedmann, Y., Weinstein, T., Li, J.P., Lindahl, U. & Vlodavsky, I. (2004). Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. FASEB J 18(2), 252–263.Google Scholar
Zhang, L. & Esko, J.D. (1994). Amino acid determinants that drive heparan sulfate assembly in a proteoglycan. J Biol Chem 269(30), 19295–19299.Google Scholar
Zimmermann, P. & David, G. (1999). The syndecans, tuners of transmembrane signaling. FASEB J 13(Suppl), S91–S100.Google Scholar
Zuberi, R.I., Ge, X.N., Jiang, S., Bahaie, N.S., Kang, B.N., Hosseinkhani, R.M., Frenzel, E.M., Fuster, M.M., Esko, J.D., Rao, S.P. & Sriramarao, P. (2009). Deficiency of endothelial heparan sulfates attenuates allergic airway inflammation. J Immunol 183(6), 3971–3979.Google Scholar