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Distribution of tubulointerstitial nephritis antigen-like 1 and structural matrix proteins in mouse embryos during preimplantation development in vivo and in vitro

Published online by Cambridge University Press:  01 October 2012

Masahiro Sakurai ,
Yusuke Sato ,
Kuniaki Mukai ,
Makoto Suematsu ,
Emiko Fukui ,
Midori Yoshizawa ,
Kentaro Tanemura ,
Yumi Hoshino ,
Hiromichi Matsumoto  and
Eimei Sato
Masahiro Sakurai*
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai, 981-8555, Japan. Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, 981-8555, Japan.
Yusuke Sato
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, 981-8555, Japan.
Kuniaki Mukai
Affiliation:
Department of Biochemistry, School of Medicine, Keio University, 35 Shinano-machi, Shinjuku-ku, Tokyo, 160-8582, Japan.
Makoto Suematsu
Affiliation:
Department of Biochemistry, School of Medicine, Keio University, 35 Shinano-machi, Shinjuku-ku, Tokyo, 160-8582, Japan.
Emiko Fukui
Affiliation:
Laboratory of Animal Breeding and Reproduction, Faculty of Agriculture, Utsunomiya University, 350 Mine-machi, Utsunomiya, Tochigi, 321-8505, Japan.
Midori Yoshizawa
Affiliation:
Laboratory of Animal Breeding and Reproduction, Faculty of Agriculture, Utsunomiya University, 350 Mine-machi, Utsunomiya, Tochigi, 321-8505, Japan.
Kentaro Tanemura
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, 981-8555, Japan.
Yumi Hoshino
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, 981-8555, Japan.
Hiromichi Matsumoto
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, 981-8555, Japan. Laboratory of Animal Breeding and Reproduction, Faculty of Agriculture, Utsunomiya University, 350 Mine-machi, Utsunomiya, Tochigi, 321-8505, Japan.
Eimei Sato
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai, Miyagi, 981-8555, Japan.
*
All correspondence to: Masahiro Sakurai. Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai, 981-8555, Japan. Tel:/Fax: +81 22 717 8687. e-mail: msaku913@affrc.go.jp
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Summary

Tubulointerstitial nephritis antigen-like 1 (TINAGL1) is a novel matricellular protein that interacts with structural matrix proteins and promotes cell adhesion and spreading. We have previously reported unique localization of TINAGL1 to the trophectoderm (TE) of mouse blastocysts. TINAGL1 was found to be upregulated in implantation-competent blastocysts after estrogen treatment using progesterone-treated delayed-implantation models. Moreover, colocalization of TINAGL1 and extracellular matrix (ECM) protein laminin 1 was detected in the Reichert membrane on embryonic days 6.5 and 7.5. Although these data suggested a role for TINAGL1 in the embryo development at postimplantation, its relevance to other ECM proteins during preimplantation development is not clear. In this study, we examined the expression of TINAGL1 and its relevance to other ECM proteins fibronectin (FN) and collagen type IV (ColIV) during in vivo development of preimplantation embryos, particularly at blastocyst stage in detail. Localizations of TINAGL1, FN, and ColIV were similar. In 1-cell to 8-cell embryos, they were expressed in cytoplasm of blastomeres, and in morulae they were localized in the outer cells. FN and ColIV were expressed primarily on outer surface of the cells. In blastocysts, FN and ColIV were distributed in the cytoplasm of TE, but, just prior to implantation, they became localized uniquely to the blastocoelic surface of TE. In in vitro fertilized (IVF) blastocysts, expression levels of TINAGL1 and FN were lower than in in vivo blastocysts. These results suggest that, during preimplantation development, TINAGL1 may be involved in roles of structural matrix proteins, whose expression in blastocysts may be affected by in vitro culture.

Keywords

Collagen Type IVFibronectinPreimplantation developmentTINAGL1Trophectoderm
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 259 - 265
Copyright
Copyright © Cambridge University Press 2012 

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References

Armant, D.R., Kaplan, H.A. & Lennarz, W.J. (1986). Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts. Dev. Biol. 116, 519–23.Google Scholar
Aumailley, M. & Timpl, R. (1986). Attachment of cells to basement membrane collagen type IV. J. Cell Biol. 103, 1569–75.Google Scholar
Bartlett, S.E. & MeninoA.R., Jr A.R., Jr (1995). Evaluation of extracellular matrices and the plasminogen activator system in sheep inner cell mass and trophectodermal outgrowth in vitro. Biol. Reprod. 52, 1436–45.Google Scholar
Burrows, T.D., King, A. & Loke, Y.W. (1993). Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin. Hum. Reprod. (Oxford, England) 8, 475–84.Google Scholar
Carnegie, J.A. (1991). Immunolocalization of fibronectin and laminin within rat blastocysts cultured under serum-free conditions. J. Reprod. Fertil. 91, 423–34.CrossRefGoogle ScholarPubMed
Carnegie, J.A. & Cabaca, O. (1991). The influence of extracellular matrix components on the proliferation and migration of inner cell mass-derived parietal endodermal cells. Biol. Reprod. 45, 572–80.CrossRefGoogle ScholarPubMed
Carnegie, J.A. & Cabaca, O. (1993). Extracellular matrix composition and resilience: two parameters that influence the in vitro migration and morphology of rat inner cell mass-derived cells. Biol. Reprod. 48, 287–99.CrossRefGoogle ScholarPubMed
Damsky, C.H., Librach, C., Lim, K.H., Fitzgerald, M.L., McMaster, M.T., Janatpour, M., Zhou, Y., Logan, S.K. & Fisher, S.J. (1994). Integrin switching regulates normal trophoblast invasion. Development (Cambridge, England) 120, 3657–66.CrossRefGoogle ScholarPubMed
Dey, S.K., Lim, H., Das, S.K., Reese, J., Paria, B.C., Daikoku, T. & Wang, H. (2004). Molecular cues to implantation. Endocrine Rev. 25, 341–73.Google Scholar
Ecker, D.J., Stein, P., Xu, Z., Williams, C.J., Kopf, G.S., Bilker, W.B., Abel, T. & Schultz, R.M. (2004). Long-term effects of culture of preimplantation mouse embryos on behavior. Proc. Natl. Acad. Sci. USA 101, 1595–600.CrossRefGoogle ScholarPubMed
Fernandez-Gonzalez, R., Moreira, P., Bilbao, A., Jimenez, A., Perez-Crespo, M., Ramirez, M.A., Rodriguez De Fonseca, F., Pintado, B. & Gutierrez-Adan, A. (2004). Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc. Natl. Acad. Sci. USA 101, 5880–5.Google Scholar
Giritharan, G., Talbi, S., Donjacour, A., Di Sebastiano, F., Dobson, A.T. & Rinaudo, P.F. (2007). Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction (Cambridge, England), 134, 63–72.Google Scholar
Hierck, B.P., Thorsteinsdottir, S., Niessen, C.M., Freund, E., Iperen, L.V., Feyen, A., Hogervorst, F., Poelmann, R.E., Mummery, C.L. & Sonnenberg, A. (1993). Variants of the alpha 6 beta 1 laminin receptor in early murine development: distribution, molecular cloning and chromosomal localization of the mouse integrin alpha 6 subunit. Cell Adhes. Commun. 1, 33–53.Google Scholar
Hoshino, Y. & Sato, E. (2008). Protein kinase B (PKB/Akt) is required for the completion of meiosis in mouse oocytes. Dev. Biol. 314, 215–23.CrossRefGoogle ScholarPubMed
Hynes, R.O. (1990). Fibronectins, New York: Springer-Verlag.Google Scholar
Igarashi, T., Tajiri, Y., Sakurai, M., Sato, E., Li, D., Mukai, K., Suematsu, M., Fukui, E., Yoshizawa, M. & Matsumoto, H. (2009). Tubulointerstitial nephritis antigen-like 1 is expressed in extraembryonic tissues and interacts with laminin 1 in the Reichert membrane at postimplantation in the mouse. Biol. Reprod. 81, 948–55.CrossRefGoogle ScholarPubMed
Irving, J.A., Lysiak, J.J., Graham, C.H., Hearn, S., Han, V.K. & Lala, P.K. (1995). Characteristics of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture. Placenta 16, 413–33.CrossRefGoogle ScholarPubMed
Laurie, G.W., Bing, J.T., Kleinman, H.K., Hassell, J.R., Aumailley, M., Martin, G.R. & Feldmann, R.J. (1986). Localization of binding sites for laminin, heparan sulfate proteoglycan and fibronectin on basement membrane (type IV) collagen. J. Mol. Biol. 189, 205–216.CrossRefGoogle ScholarPubMed
Leivo, I., Vaheri, A., Timpl, R. & Wartiovaara, J. (1980). Appearance and distribution of collagens and laminin in the early mouse embryo. Dev. Biol. 76, 100–14.Google Scholar
Li, D., Mukai, K., Suzuki, T., Suzuki, R., Yamashita, S., Mitani, F. & Suematsu, M. (2007). Adrenocortical zonation factor 1 is a novel matricellular protein promoting integrin-mediated adhesion of adrenocortical and vascular smooth muscle cells. FEBS J. 274, 2506–22.Google Scholar
Matsumoto, H., Ma, W., Smalley, W., Trzaskos, J., Breyer, R.M. & Dey, S.K. (2001). Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol. Reprod. 64, 1557–65.Google Scholar
Matsumoto, H., Daikoku, T., Wang, H., Sato, E. & Dey, S.K. (2004). Differential expression of ezrin/radixin/moesin (ERM) and ERM-associated adhesion molecules in the blastocyst and uterus suggests their functions during implantation. Biol. Reprod. 70, 729–36.Google Scholar
McRae, A.C. & Church, R.B. (1990). Cytoplasmic projections of trophectoderm distinguish implanting from preimplanting and implantation-delayed mouse blastocytes. J. Reprod. Fertil. 88, 31–40.Google Scholar
Mohan, M., Hurst, A.G. & Malayer, J.R. (2004). Global gene expression analysis comparing bovine blastocysts flushed on day 7 or produced in vitro. Mol. Reprod. Dev. 68, 288–98.Google Scholar
Mukai, K., Mitani, F., Nagasawa, H., Suzuki, R., Suzuki, T., Suematsu, M. & Ishimura, Y. (2003). An inverse correlation between expression of a preprocathepsin B-related protein with cysteine-rich sequences and steroid 11beta-hydroxylase in adrenocortical cells. J. Biol. Chem. 278, 17084–92.Google Scholar
Murray, J.C., Stingl, G., Kleinman, H.K., Martin, G.R. & Katz, S.I. (1979). Epidermal cells adhere preferentially to type IV (basement membrane) collagen. J. Cell Biol. 80, 197–202.Google Scholar
Nilsson, O. (1966). Structural differentiation of luminal membrane in rat uterus during normal and experimental implantations. Zeitschrift fur Anatomie und Entwicklungsgeschichte 125, 152–9.Google Scholar
Paria, B.C., Huet-Hudson, Y.M. & Dey, S.K. (1993). Blastocyst's state of activity determines the “window” of implantation in the receptive mouse uterus. Proc. Natl. Acad. Sci. USA 90, 10159–62.CrossRefGoogle ScholarPubMed
Paria, B.C., Ma, W., Tan, J., Raja, S., Das, S.K., Dey, S.K. & Hogan, B.L. (2001). Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc. Natl. Acad. Sci. USA 98, 1047–52.Google Scholar
Psychoyos, A. (1973). Endocrine control of egg implantation. In: Handbook of Physiology (Greep, R.O., Astwood, E.B. & Geiger, S.R., eds) American Physiological Society, Washington, DC, pp. 187–215.Google Scholar
Rinaudo, P. & Schultz, R.M. (2004). Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction 128, 301–11.CrossRefGoogle ScholarPubMed
Rinaudo, P.F., Giritharan, G., Talbi, S., Dobson, A.T. & Schultz, R.M. (2006). Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil. Steril. 86, 1252–65, 1265.e1–36.Google Scholar
Rubin, K., Hook, M., Obrink, B. & Timpl, R. (1981). Substrate adhesion of rat hepatocytes: mechanism of attachment to collagen substrates. Cell 24, 463–70.Google Scholar
Salamat, M., Gotz, W., Werner, J. & Herken, R. (1993). Ultrastructural localization of lectin-binding sites in different basement membranes. Histochem. J. 25, 464–8.CrossRefGoogle Scholar
Schilperoort-Haun, K.R. & Menino, A.R. Jr. (2002a). Evaluation of extracellular matrix proteins and tissue inhibitor of matrix metalloproteinases-2 on bovine inner cell mass outgrowth in vitro. In Vitro Cell. Dev. Biol. 38, 41–7.Google Scholar
Schilperoort-Haun, K.R. & MeninoA.R., Jr A.R., Jr. (2002b). Factors affecting cellular outgrowth from porcine inner cell masses in vitro. J. Anim. Sci. 80, 2671–80.Google ScholarPubMed
Sherman, M.I., Gay, R., Gay, S. & Miller, E.J. (1980). Association of collagen with preimplantation and peri-implantation mouse embryos. Dev. Biol. 74, 470–8.Google Scholar
Stephens, L.E., Sutherland, A.E., Klimanskaya, I.V., Andrieux, A., Meneses, J., Pedersen, R.A. & Damsky, C.H. (1995). Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9, 1883–95.Google Scholar
Summers, M.C., McGinnis, L.K., Lawitts, J.A., Raffin, M. & Biggers, J.D. (2000). IVF of mouse ova in a simplex optimized medium supplemented with amino acids. Hum. Reprod. (Oxford, England), 15, 1791–801.Google Scholar
Sutherland, A.E., Calarco, P.G. & Damsky, C.H. (1988). Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth. J. Cell Biol. 106, 1331–48.CrossRefGoogle ScholarPubMed
Thorsteinsdottir, S. (1992). Basement membrane and fibronectin matrix are distinct entities in the developing mouse blastocyst. Anat. Rec. 232, 141–9.CrossRefGoogle ScholarPubMed
Wang, H. & Dey, S.K. (2006). Roadmap to embryo implantation: clues from mouse models. Nat. Rev. 7, 185–99.Google Scholar
Wartiovaara, J., Leivo, I. & Vaheri, A. (1979). Expression of the cell surface-associated glycoprotein, fibronectin, in the early mouse embryo. Dev. Biol. 69, 247–57.Google Scholar
Yelian, F.D., Yang, Y., Hirata, J.D., Schultz, J.F. & Armant, D.R. (1995). Molecular interactions between fibronectin and integrins during mouse blastocyst outgrowth. Mol. Reprod. Dev. 41, 435–48.Google Scholar
Yohkaichiya, T., Hoshiai, H., Uehara, S. & Yajima, A. (1988). Fibronectin localization in the mouse embryo from the two cell stage to the morula stage. Tohoku J. Exp. Med. 154, 95–100.Google Scholar
Yoshinaga, K. & Adams, C.E. (1966). Delayed implantation in the spayed, progesterone treated adult mouse. J. Reprod. Fertil. 12, 593–5.Google Scholar
Zetter, B.R. & Martin, G.R. (1978). Expression of a high molecular weight cell surface glycoprotein (LETS protein) by preimplantation mouse embryos and teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 75, 2324–8.Google Scholar