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Laminin deficits induce alterations in the development of dopaminergic neurons in the mouse retina

Published online by Cambridge University Press:  22 August 2007

VIKTÓRIA DÉNES ,
PAUL WITKOVSKY ,
MANUEL KOCH ,
DALE D. HUNTER ,
GERMÁN PINZÓN-DUARTE  and
WILLIAM J. BRUNKEN
VIKTÓRIA DÉNES
Affiliation:
Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, Massachusetts Tufts Center for Vision Research, Boston, Massachusetts
PAUL WITKOVSKY
Affiliation:
Department of Ophthalmology, New York University School of Medicine, New York, New York
MANUEL KOCH
Affiliation:
Center for Biochemistry and Department of Dermatology, University of Köln, Köln, Germany
DALE D. HUNTER
Affiliation:
Tufts Center for Vision Research, Boston, Massachusetts
GERMÁN PINZÓN-DUARTE
Affiliation:
Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, Massachusetts Tufts Center for Vision Research, Boston, Massachusetts
WILLIAM J. BRUNKEN
Affiliation:
Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, Massachusetts Tufts Center for Vision Research, Boston, Massachusetts
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Abstract

Genetically modified mice lacking the β2 laminin chain (β2null), the γ3 laminin chain (γ3 null), or both β2/γ3 chains (compound null) were produced. The development of tyrosine hydroxylase (TH) immunoreactive neurons in these mouse lines was studied between birth and postnatal day (P) 20. Compared to wild type mice, no alterations were seen in γ3 null mice. In β2 null mice, however, the large, type I TH neurons appeared later in development, were at a lower density and had reduced TH immunoreactivity, although TH process number and size were not altered. In the compound null mouse, the same changes were observed together with reduced TH process outgrowth. Surprisingly, in the smaller, type II TH neurons, TH immunoreactivity was increased in laminin-deficient compared to wild type mice. Other retinal defects we observed were a patchy disruption of the inner limiting retinal basement membrane and a disoriented growth of Müller glial cells. Starburst and AII type amacrine cells were not apparently altered in laminin-deficient relative to wild type mice. We postulate that laminin-dependent developmental signals are conveyed to TH amacrine neurons through intermediate cell types, perhaps the Müller glial cell and/or the retinal ganglion cell.

Keywords

Extracellular matrixInner limitingMembraneAmacrine cellMuller cell
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 549 - 562
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Aisenbrey, S., Zhang, M., Bacher, D., Yee, J., Brunken, W.J. & Hunter, D.D. (2006). Retinal pigment epithelial cells synthesize laminins including laminin 5 and adhere to them using α3- and α6-containing integrins. Investigative Ophthalmology & Visual Science 47, 5537–5544.CrossRefGoogle Scholar
Barresi, R. & Campbell, K.P (2006). Dystroglycan: Form biosynthesis to pathogenesis of human disease. Journal of Cell Science 119, 199–207.CrossRefGoogle Scholar
Bates, R.C., Lincz, L.F. & Burns, G.F. (1995). Involvement of integrins in cell survival. Cancer Metastasis Review 14, 191–203.CrossRefGoogle Scholar
Beggs, H.E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K.A., Gorski, J., Jones, K.R., Sretavan, D. & Reichardt, L.F. (2003). FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501–514.CrossRefGoogle Scholar
Blackshaw, S., Harpavat, S., Trimarchi, J., Cai, L., Huang, H., Kuo, W.P., Weber, G., Lee, K., Fraioli, R.E., Cho, S.H., Yung, R., Asch, E., Ohno-Machado, L., Wong, W,H. & Cepko, C.L. (2004). Genomic analysis of mouse retinal development. Public Library of Science Biology 2, 1411–1431.CrossRefGoogle Scholar
Borba, J.C., Henze, I.P., Silvera, M.S., Kubrusly, R.C.C., Gardino, P.F., de Mello, M.C.F., Hokoc, J.N. & de Mello, F.G. (2005). Pituitary adenylate cyclase-activating polypeptide (PACAP) can act as determinant of the tyrosine hydroxylase phenotype of dopaminergic cells during retina development. Developmental Brain Research 156, 193–201.CrossRefGoogle Scholar
Cellerino, A. & Kohler, K. (1997). Brain-derived neurotrophic factor/neurotrophin-4 receptor TrkB is localized on ganglion cells and dopaminergic amacrine cells in the vertebrate retina. Journal of Comparative Neurology 386, 149–160.3.0.CO;2-F>CrossRefGoogle Scholar
Cellerino, A., Pinzón-Duarte, G., Carroll, P. & Kohler, K. (1998). Brain-derived neurotrophic factor modulates the development of the dopaminergic network in the rodent retina. Journal of Neuroscience 189, 3351–3362.Google Scholar
Chen, Z.L. & Strickland, S. (1997). Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91, 917–925.CrossRefGoogle Scholar
Claudepierre, T., Dalloz, C., Mornet, D., Matsumura, K., Sahel, J. & Rendon, A. (2000). Characterization of the intermolecular associations of the dystrophin-associated glycoprotein complex in retinal Muller glial cells. Journal of Cell Science 113, 3409–4317.Google Scholar
Claudepierre, T., Manglapus, M.K., Marengi, N., Radner, S., Champliaud, M.-F., Tasanen, K., Bruckner-Tuderman, L., Hunter, D.D. & Brunken, W.J. (2005). Collagen XVII and BPAG1 expression in the retina: Evidence for an anchoring complex in the central nervous system. Journal of Comparative Neurology 487, 190–203.CrossRefGoogle Scholar
Clegg, D.O., Mullick, L.H., Wingerd, K.L., Lin, H., Atienza, J.W., Bradshaw, A.D., Gervin, D.B. & Cann, G.M. (2000). Adhesive events in retinal development and function: The role of integrin receptors. Results and Problems in Cell Differentiation 31, 141–156.CrossRefGoogle Scholar
Colognato, H. & Yurchenco, P.D. (2000). Form and function: The laminin family of heterotrimers. Developmental Dynamics 218, 213–234.3.0.CO;2-R>CrossRefGoogle Scholar
Dacey, D.M. (1990). The dopaminergic amacrine cell. Journal of Comparative Neurology 301, 461–489.CrossRefGoogle Scholar
Daly, G., Pinzón-Duarte, G., Dénes, V., Koch, M., Hunter, D.D. & Brunken, W.J. (2006). Genetic deletion of laminin β2γ3 chains results in a retinal dysplasia. Investigative Ophthalmology & Visual Science 47, 2794.Google Scholar
DeCurtis, I. & Reichardt, L.F. (1993). Function and spatial distribution in developing chick retina of the laminin receptor α6β1 and its isoforms. Development 118, 377–388.Google Scholar
Ehinger, B. & Floren, I. (1978). Quantitation of the uptake of indolemaines and dopamine in the rabbit retina. Experimental Eye Research 26, 1–11.Google Scholar
Fisher, S.K., Lewis, G.P., Linberg, K.A. & Verardo, M.R. (2005). Cellular remodeling in mammalian retina: Results from studies of experimental retinal detachment. Progress in Retinal and Eye Research 24, 395–431.CrossRefGoogle Scholar
Ghee, M., Baker, H., Miller, J.C. & Ziff, E.B. (1998). AP-1, CREB and CBP transcription factors differentially regulate the tyrosine hydroxylase gene. Brain Research Molecular Brain Research 55, 101–114.CrossRefGoogle Scholar
Gustincich, S., Feigenspan, A., Wu, D.K., Koopman, L.J. & Raviola, E. (1997). Control of dopamine release in the retina: A transgenic approach to neural networks. Neuron 18, 723–736.CrossRefGoogle Scholar
Halfter, W. (1998). Disruption of the retinal basal lamina during early embryonic development leads to a retraction of vitreal end feet, an increased number of ganglion cells, and aberrant axonal outgrowth. Journal of Comparative Neurology 397, 89–1043.0.CO;2-E>CrossRefGoogle Scholar
Hunter, D.D., Murphy, M.D., Olsson, C.V. & Brunken, W.J. (1992). S-laminin expression in adult and developing retinae: A potential cue for photoreceptor morphogenesis. Neuron 8, 399–413.CrossRefGoogle Scholar
Hynes, R.O. (2002). Integrins: Bidirectional, allosteric signaling machines. Cell 110, 673–687.CrossRefGoogle Scholar
Ivins, J.K., Yurchenco, P.D. & Lander, A.D. (2000). Regulation of neurite outgrowth by integrin activation. Journal of Neuroscience 20, 6551–60.Google Scholar
Kay, J.N., Roeser, T., Mumm, J.S., Godinho, L., Mrejeru, A., Wong, R.O. & Baier, H. (2004). Transient requirement for ganglion cells during assembly of retinal synaptic layers. Development 131, 1331–1342.CrossRefGoogle Scholar
Lewis-Tuffin, L.J., Quinn, P.G. & Chikaraishi, D.M. (2004). Tyrosine hydroxylase transcription depends primarily on cAMP response element activity, regardless of the type of inducing stimulus. Molecular and Cellular Neuroscience 25, 536–547.CrossRefGoogle Scholar
Libby, R.T., Hunter, D.D. & Brunken, W.J. (1996). Developmental expression of laminin β2 in the rat retina. Investigative Ophthalmology and Visual Science 37, 1651–1661.Google Scholar
Libby, R.T., Xu, Y., Selfors, L.M., Brunken, W.J. & Hunter D.D. (1997). Identification of the cellular source of laminin β2 in adult and developing vertebrate retinae. Journal of Comparative Neurology 389, 655–667.3.0.CO;2-#>CrossRefGoogle Scholar
Libby, R.T., Lavallee, C.R., Balkema, G.W., Brunken, W.J. & Hunter, D.D. (1999). Disruption of laminin β2 chain production causes alterations in morphology and function in the CNS. Journal of Neuroscience 19, 9399–9411.Google Scholar
Libby, R.T., Champliaud, M-F., Claudepierre, T., Xu, Y., Gibbons, E.P., Koch, M., Burgeson, R.E., Hunter, D.D. & Brunken, W.J. (2000). Laminin expression in adult and developing retinae: Evidence of two novel CNS laminins. Journal of Neuroscience 20, 6517–6528.Google Scholar
Lin, B., Wang, S.W. & Masland, R.H. (2004). Retinal ganglion cell type, size and spacing can be specified independent of homotypic dendritic contacts. Neuron 43, 475–485.CrossRefGoogle Scholar
Linden, R., Rehen, S.K. & Chiarini, L.B. (1999). Apoptosis in developing retinal tissue. Progress in Retinal and Eye Research 18, 133–165.CrossRefGoogle Scholar
Linden, R., Martins, R.A.P. & Silveira, M.S. (2005). Control of programmed cell death by neurotransmitters and neuropeptides in the developing mammalian retina. Progress in Retinal and Eye Research 24, 457–491.CrossRefGoogle Scholar
Lunardi, A., Cremisi, F. & Dente, L. (2006). Dystroglycan is required for proper retinal layering. Developmental Biology 290, 411–420.CrossRefGoogle Scholar
MacNeil, M.A., Heussy, J.K., Dacheux, R., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photo-filled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. Journal of Comparative Neurology 423, 305–326.3.0.CO;2-E>CrossRefGoogle Scholar
Mariani, A.P. & Hokoc, J.N. (1988). Two types of tyrosine hydroxylase-immunoreactive amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 276, 81–91.CrossRefGoogle Scholar
Marrs, G.S., Honda, T., Fuller, L., Thangavel, R., Balsamo, J., Lilien, J., Dailey, M.E. & Arregui, C. (2006). Dendritic arbors of developing retinal ganglion cells are stabilized by β1-integrins. Molecular and Cellular Neuroscience 32, 230–41.CrossRefGoogle Scholar
McGillem, G.S., Guidry, C. & Dacheux, R.F. (1998). Antigenic changes of rabbit retinal Muller cells in culture. Investigative Ophthalmology & Visual Science 39, 1453–1461.Google Scholar
Méhes, E., Czirók, A., Hegedüs, B., Vicsek, T. & Jancsik, V. (2002). Laminin-1 increases motility, path-searching, and process dynamism of rat and mouse Muller glial cells in vitro: Implication of relationship between cell behavior and formation of retinal morphology. Cell Motility Cytoskeleton 53, 203–213.CrossRefGoogle Scholar
Meredith, J.E., Fazeli, B. & Schwartz, M.A. (1993). The extracellular matrix as a cell survival factor. Molecular Biology of the Cell 4, 953–961.CrossRefGoogle Scholar
Miner, J.H. & Yurchenco, P.D. (2004). Laminin functions in tissue morphogenesis. Annual Review of Cell Biology 20, 255–284.CrossRefGoogle Scholar
Moukhles, H., Roque, R. & Carbonetto, S. (2000). Alpha-dystroglycan isoforms are differentially distributed in adult rat retina. Journal of Comparative Neurology 420, 182–194.3.0.CO;2-2>CrossRefGoogle Scholar
Noakes, P.G., Gautam, M., Mudd, J., Sanes, J.R. & Merlie, J.P. (1995). Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2. Nature 374, 258–262.CrossRefGoogle Scholar
Noël, G., Belda, M., Guadagno, E., Micoud, J., Klöcker, N. & Moukhles, H. (2005). Dystroglycan and Kir4.1 coclustering in retinal Müller glia is regulated by laminin-1 and requires the PDZ-ligand domain of Kir4.1. Journal of Neurochemistry 94, 691–702.Google Scholar
Olson, E.C. & Walsh, C.A. (2002). Smooth, rough, and upside-down neorcortical development. Current Opinion in Genetics and Development 12, 320–327.CrossRefGoogle Scholar
Pinzón-Duarte, G., Dénes, V., Daly, G., Koch, M., Hunter, D.D. & Brunken, W.J. (2006). β2γ3 laminin deletion causes defective development of Müller cells and retinal vasculature. Investigative Ophthalmology & Visual Science 47, 2796.Google Scholar
Pinzón-Duarte, G., Daly, G., Hunter, D.D. & Brunken, W.J. (2007). Defective formation of the inner limiting membrane in the β2γ3 laminin null retina alters number and spatial organization of retinal ganglion cells. Investigative Ophthalmology & Visual Science 48, 5686.Google Scholar
Radner, S., Lefkowitz, J.J., Koch, M., Hunter, D.D. & Brunken, W.J. (2004). Aberrant CNS development in β2γ3 laminin knockout mice. Society for Neuroscience 609.4 Abstract Viewer on-line.Google Scholar
Rapoport, D.H., Wong, L.L., Wood, E.D., Yasumura, D. & LaVail, M.M. (2004). Timing and topography of cell genesis in the rat retina. Journal of Comparative Neurology 474, 304–324.CrossRefGoogle Scholar
Reh, T.A. & Levine, E.M. (1998). Multipotential stem cells and progenitors in the vertebrate retina. Journal of Neurobiology 36, 206–220.3.0.CO;2-5>CrossRefGoogle Scholar
Rice, D.S. & Curran, T. (2000). Disabled-1 is expressed in type AII amacrine cells in the mouse retina. Journal of Comparative Neurology 424, 327–338.3.0.CO;2-6>CrossRefGoogle Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P. & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. Journal of Neuroscience 22, 3831–3843.Google Scholar
Sherry, D.M. & Proske, P.A. (2001). Localization of alpha integrin subunits in the neural retina of the tiger salamander. Graefe's Arch. Clinical and Experimental Ophthalmology 239, 278–287CrossRefGoogle Scholar
Steinmetz, C.C., Buard, I., Claudepierre, T., Nagler, K. & Pfrieger, F.W. (2006). Regional variations in the glial influence on synapse development in the mouse CNS. Journal of Physiology 577, 249–261.CrossRefGoogle Scholar
Suzuki, N., Yokoyama, F. & Nomizu, M. (2005). Functional sites in the laminin alpha chains. Connective Tissue Research 46, 142–152.CrossRefGoogle Scholar
Vardimon, L., Fox, L.E. & Moscona, A.A. (1986). Developmental regulation of glutamine synthetase and carbonic anhydrase II in neural retina. Proceedings of the National Academy of Sciences of the United States of America 83, 9060–9064.CrossRefGoogle Scholar
Vecino, E., Garcia-Grespo, D., Garcia, M., Martinez-Millan, L. & Carrascal, E. (2002). Rat retinal ganglion cells co-express brain derived neurotrophic factor (BDNF) and its receptor TrkB. Vision Research 42, 151–157.CrossRefGoogle Scholar
Willbold, E. & Layer, P.G. (1998). Müller glia cells and their possible roles during retina differentiation in vivo and in vitro. Histology Histopathology 13, 531–552.Google Scholar
Witkovsky, P., Veisenberger, E., Haycock, J.W., Akopian, A., Garcia-Espana, A. & Meller, E. (2004). Activity-dependent phosphorylation of tyrosine hydroxylase in dopaminergic neurons of the rat retina. Journal of Neuroscience 24, 4242–4249.CrossRefGoogle Scholar
Witkovsky, P., Arango-Gonzalez, B., Haycock, J.W. & Kohler, K. (2005). Rat retinal dopaminergic neurons: Differential maturation of somatodendritic and axonal compartments. Journal of Comparative Neurology 481, 352–362.CrossRefGoogle Scholar
Wulle, I. & Schnitzer, J. (1989). Distribution and morphology of tyrosine hydroxylase-immunoreactive neurons in the developing mouse retina. Developmental Brian Research 48, 59–72.CrossRefGoogle Scholar
Yan, H.H.N. & Cheng, C.Y. (2006). Laminin α3 forms a complex with β3 and γ3 chains that serves as the ligand for α6β1-integrin at the apical ectoplasmic specialization in adult rat testes. Journal of Biological Chemistry 281, 17286–17309.CrossRefGoogle Scholar
Young, R.W. (1984). Cell death during differentiation of the retina in the mouse. Journal of Comparative Neurology 229, 362–373.CrossRefGoogle Scholar
Young, R.W. (1985). Cell differentiation in the retina of the mouse. Anatomical Record 212, 199–205.CrossRefGoogle Scholar
Yu, W.M., Feltri, M.L., Wrabetz, L., Strickland, S. & Chen, Z.L. (2005). Schwann cell-specific ablation of laminin gamma1 causes apoptosis and prevents proliferation. Journal of Neuroscience 25, 4463–72.Google Scholar
Yurchenco, P.D. & Wadsworth, W.G. (2004). Assembly and tissue functions of early embryonic laminins and netrins. Current Opinion in Cell Biology 16, 572–579.CrossRefGoogle Scholar
Zenker, M., Aigner, T., Wendler, O., Tralau, T., Müntefering, H., Fenski, R., Pitz, S., Schumacher, V., Royer-Pokora, B., Wühl, E., Cochat, P., Bouveier, R., Kraus, C., Mark, K., Madlon, H., Dötsch, J., Rascher, W., Maruniak-Chudek, I., Lennert, T., Neumann, L.M & Reis, A. (2004). Human laminin β2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Human Molecular Genetics 13, 2625–2632.CrossRefGoogle Scholar
Zenker, M., Pierson, M., Jonveaux, P. & Reis, A. (2005). Demonstration of two novel LAMB2 mutations in the original Pierson syndrome family reported 42 years ago. American Journal of Medical Genetics 138, 73–44.CrossRefGoogle Scholar
Zhang, J., Yang, Z. & Wu, S.M. (2005). Development of cholinergic amacrine cells is visual activity-dependent in the postnatal mouse retina. Journal of Comparative Neurology 484, 331–343.CrossRefGoogle Scholar
Zhang, D-Q. (2004). Type 2 catecholaminergic amacrine cells express calcium-binding proteins in the mouse retina. Investigative Ophthalmology & Visual Science 45, 4253.Google Scholar