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The expression of platelet endothelial cell adhesion molecule-1 in mouse primordial germ cells during their migration and early gonadal formation

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Abstract

The platelet endothelial cell adhesion molecule-1 (PECAM-1), or CD31, a member of the immunoglobulin superfamily, is located on the plasma membrane of endothelial and hematopoietic cells and involved in vascular development and inflammation. In this study, by use of immunohistochemistry at light and electron microscopic levels in combination with enzyme histochemistry for alkaline phosphatase, we demonstrated that PECAM-1/CD31 is expressed in the mouse primordial germ cell (PGC). Up to 8 days postcoitum (dpc), PGCs with alkaline phosphatase activity showed no PECAM-1/CD31 immunoreactivity. At 9 dpc, PECAM-1/CD31 immunoreactivity was first detected with low intensity in some PGCs located in the hindgut. Between 10 and 11 dpc, intense immunoreactivity was shown on the entire surface of PGCs migrating along the dorsal wall. After arrival and settlement of PGCs in the genital ridges around 11.5 dpc, the intense immunoreactivity was maintained on the entire surface of PGCs. By electron microscopy, the immunoreactivity was localized exclusively on the plasma membrane of PGCs, being as strong at the portions adjacent to neighboring PGCs as those adjacent to somatic cells. As the male and female gonads began to differentiate, PECAM-1/CD31 immunoreactivity remained strong in germ cells until 13 dpc, after which it gradually decreased in intensity and disappeared by 16 dpc. These results suggested that cell-to-cell interaction through PECAM-1/CD31 plays roles in the development of PGCs during their migration on the dorsal wall and homing in the gonads.

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References

  • Albelda SM, Oliver PD, Romer LH, Buck CA (1990) EndoCAM: a novel endothelial cell-cell adhesion molecule. J Cell Biol 110:1227–1237

    CAS  PubMed  Google Scholar 

  • Albelda SM, Muller WA, Buck CA, Newman PJ (1991) Molecular and cellular properties of PECAM-1 (endoCAM/CD31): a novel vascular cell-cell adhesion molecule. J Cell Biol 114:1059–1068

    CAS  PubMed  Google Scholar 

  • Baldwin HS, Shen HM, Yan HC, DeLisser HM, Chung A, Mickanin C, Trask T, Kirschbaum NE, Newman PJ, Albelda SM (1994) Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120:2539–2553

    CAS  PubMed  Google Scholar 

  • Berman ME, Muller WA (1995) Ligation of platelet/endothelial cell adhesion molecule 1 (PECAM-1/CD31) on monocytes and neutrophils increases binding capacity of leukocyte CR3 (CD11b/CD18). J Immunol 154:299–307

    CAS  PubMed  Google Scholar 

  • Bird IN, Taylor V, Newton JP, Spragg JH, Simmons DL, Salmon M, Buckley CD (1999) Homophilic PECAM-1(CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci 112:1989–1997

    CAS  PubMed  Google Scholar 

  • Bogen S, Pak J, Garifallou M, Deng X, Muller WA (1994) Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J Exp Med 179:1059–1064

    CAS  PubMed  Google Scholar 

  • Buckley CD, Doyonnas R, Newton JP, Blystone SD, Brown EJ, Watt SM, Simmons DL (1996) Identification of alpha v beta 3 as a heterotypic ligand for CD31/PECAM-1. J Cell Sci 109:437–445

    PubMed  Google Scholar 

  • Buehr M, McLaren A, Bartley A, Darling S (1993) Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev Dyn 198:182–118

    CAS  PubMed  Google Scholar 

  • Deaglio S, Dianzani U, Horenstein AL, Fernandez JE, Kooten C van, Bragardo M, Funaro A, Garbarino G, Di Virgilio F, Banchereau J, Malavasi F (1998) Human CD38 ligand. A 120-kDa protein predominantly expressed on endothelial cells. J Immunol 156:727–734

    Google Scholar 

  • De Felici M (2000) Regulation of primordial germ cell development in the mouse. Int J Dev Biol 44:575–580

    PubMed  Google Scholar 

  • De Felici M, Dolci S (1989) In vitro adhesion of mouse fetal germ cells to extracellular matrix components. Cell Differ Dev 26:87–96

    Article  PubMed  Google Scholar 

  • DeLisser HM, Yan HC, Newman PJ, Muller WA, Buck CA, Albelda SM (1993) Platelet/endothelial cell adhesion molecule-1 (CD31)-mediated cellular aggregation involves cell surface glycosaminoglycans. J Biol Chem 268:16037–16046

    CAS  PubMed  Google Scholar 

  • DeLisser HM, Chilkotowsky J, Yan HC, Daise ML, Buck CA, Albelda SM (1994) Deletions in the cytoplasmic domain of platelet-endothelial cell adhesion molecule-1 (PECAM-1, CD31) result in changes in ligand binding properties. J Cell Biol 124:195–203

    CAS  PubMed  Google Scholar 

  • DeLisser HM, Christofidou-Solomidou M, Strieter RM, Burdick MD, Robinson CS, Wexler RS, Kerr JS, Garlanda C, Merwin JR, Madri JA, Albelda SM (1997) Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol 151:671–677

    CAS  PubMed  Google Scholar 

  • Di Carlo A, De Felici M (2000) A role for E-cadherin in mouse primordial germ cell development. Dev Biol 226:209–219

    Article  PubMed  Google Scholar 

  • Fujimoto T, Yoshinaga K, Kono I (1985) Distribution of fibronectin on the migratory pathway of primordial germ cells in mice. Anat Rec 211:271–278

    CAS  PubMed  Google Scholar 

  • Ginsburg M, Snow MH, McLaren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528

    CAS  PubMed  Google Scholar 

  • Gomperts M, Garcia-Castro M, Wylie C, Heasman J (1994) Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135–141

    CAS  PubMed  Google Scholar 

  • Horak ER, Leek R, Klenk N, LeJeune S, Smith K, Stuart N, Greenall M, Stepniewska K, Harris AL (1992) Angiogenesis, assessed by platelet/endothelial cell adhesion molecule antibodies, as indicator of node metastases and survival in breast cancer. Lancet 340:1120–1124

    CAS  PubMed  Google Scholar 

  • Ilan N, Cheung L, Pinter E, Madri JA (2000) Platelet-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different tyrosine and serine/threonine phosphorylation. J Biol Chem 275:21435–21443

    Article  CAS  PubMed  Google Scholar 

  • Jackson DE, Kupcho KR, Newman PJ (1997) Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2. J Biol Chem 272:24868–24875

    Article  CAS  PubMed  Google Scholar 

  • Kawase E, Yamamoto H, Hashimoto K, Nakatsuji N (1994) Tumor necrosis factor-alpha (TNF-alpha) stimulates proliferation of mouse primordial germ cells in culture. Dev Biol 161:91–95

    Article  PubMed  Google Scholar 

  • Lu TT, Yan LG, Madri JA (1996) Integrin engagement mediates tyrosine dephosphorylation on platelet-endothelial cell adhesion molecule 1. Proc Natl Acad Sci U S A 93:11808–11813

    Article  CAS  PubMed  Google Scholar 

  • Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B (1997) Male-specific cell migration into the developing gonad. Curr Biol 7:958–968

    CAS  PubMed  Google Scholar 

  • Matsui Y, Toksoz D, Nishikawa S, Nishikawa S, Williams D, Zsebo K, Hogan BL (1991) Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature 353:750–752

    CAS  PubMed  Google Scholar 

  • Muller WA (1995) The role of PECAM-1 (CD31) in leukocyte emigration: studies in vitro and in vivo. J Leukoc Biol 57:523–528

    CAS  PubMed  Google Scholar 

  • Muller WA, Berman ME, Newman PJ, DeLisser HM, Albelda SM (1992) A heterophilic adhesion mechanism for platelet/endothelial cell adhesion molecule 1 (CD31). J Exp Med 175:1401–1404

    CAS  PubMed  Google Scholar 

  • Newman PJ, Albelda SM (1992) Cellular and molecular aspects of PECAM-1. Nouv Rev Fr Hematol 34(suppl): S9–S13

    CAS  PubMed  Google Scholar 

  • Newman PJ, Berndt MC, Gorski J, White GC, Lyman S, Paddock C, Muller WA (1990) PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247:1219–1222

    CAS  PubMed  Google Scholar 

  • Paranko J, Pelliniemi LJ, Vaheri A, Foidart JM, Lakkala-Paranko T (1983) Morphogenesis and fibronectin in sexual differentiation of rat embryonic gonads. Differentiation 23(suppl):S72–S81

    PubMed  Google Scholar 

  • Piali L, Hammel P, Uherek C, Bachmann F, Gisler RH, Dunon D, Imhof BA (1995) CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. J Cell Biol 130:451–460

    CAS  PubMed  Google Scholar 

  • Pumphrey NJ, Taylor V, Freeman S, Douglas MR, Bradfield PF, Young SP, Lord JM, Wakelam MJ, Bird IN, Salmon M, Buckley CD (1999) Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31. FEBS Lett 450:77–83

    Article  CAS  PubMed  Google Scholar 

  • Robson P, Stein P, Zhou B, Schultz RM, Baldwin HS (2001) Inner cell mass-specific expression of a cell adhesion molecule (PECAM-1/CD31) in the mouse blastocyst. Dev Biol 234:317–329

    Article  CAS  PubMed  Google Scholar 

  • Saitou M, Barton SC, Surani MA (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418:293–300

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Williams J, Yan HC, Amin KM, Albelda SM, DeLisser HM (1996) Platelet endothelial cell adhesion molecule-1 (PECAM-1) homophilic adhesion is mediated by immunoglobulin-like domains 1 and 2 and depends on the cytoplasmic domain and the level of surface expression. J Biol Chem 271:18561–18570

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Wang X, Lasson A, Bojesson A, Annborn M, Andersson R (2001) Effects of inhibition of PAF, ICAM-1 and PECAM-1 on gut barrier failure caused by intestinal ischemia and reperfusion. Scand J Gastroenterol 36:55–65

    Article  CAS  PubMed  Google Scholar 

  • Tilmann C, Capel B (1999) Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126:2883–2890

    CAS  PubMed  Google Scholar 

  • Vecchi A, Garlanda C, Lampugnani MG, Resnati M, Matteucci C, Stoppacciaro A, Schnurch H, Risau W, Ruco L, Mantovani A (1994) Monoclonal antibodies specific for endothelial cells of mouse blood vessels. Their application in the identification of adult and embryonic endothelium. Eur J Cell Biol 63:247–254

    CAS  PubMed  Google Scholar 

  • Wakayama T, Koami H, Ariga H, Kobayashi D, Sai Y, Tsuji A, Yamamoto M, Iseki S (2003) Expression and functional characterization of the adhesion molecule spermatogenic immunoglobulin superfamily (SgIGSF) in the mouse testis. Biol Reprod 68:1755–1763

    CAS  PubMed  Google Scholar 

  • Wong CW, Wiedle G, Ballestrem C, Wehrle-Haller B, Etteldorf S, Bruckner M, Engelhardt B, Gisler RH, Imhof BA (2000) PECAM-1/CD31 trans-homophilic binding at the intercellular junctions is independent of its cytoplasmic domain; evidence for heterophilic interaction with integrin alphavbeta3 in Cis. Mol Biol Cell 11:3109–3121

    CAS  PubMed  Google Scholar 

  • Xie Y, Muller WA (1993) Molecular cloning and adhesive properties of murine platelet/endothelial cell adhesion molecule 1. Proc Natl Acad Sci U S A 90:5569–5573

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Mr. S. Yamazaki for his technical assistance. This work was supported by a research grant for young scientists from Kanazawa University.

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Authors and Affiliations

  1. Department of Histology and Embryology, Graduate School of Medical Science, Kanazawa University, 13-1 Takara-machi, 920-8640, Kanazawa, Japan

    Tomohiko Wakayama, Miyuki Yamamoto & Shoichi Iseki

  2. Department of Cell Differentiation, Institute of Molecular Embryology and Genetics, Kumamoto University School of Medicine, Kumamoto, Japan

    Koichi Hamada & Toshio Suda

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  1. Tomohiko Wakayama
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  2. Koichi Hamada
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  3. Miyuki Yamamoto
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  4. Toshio Suda
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  5. Shoichi Iseki
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Correspondence to Shoichi Iseki.

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Wakayama, T., Hamada, K., Yamamoto, M. et al. The expression of platelet endothelial cell adhesion molecule-1 in mouse primordial germ cells during their migration and early gonadal formation. Histochem Cell Biol 119, 355–362 (2003). https://doi.org/10.1007/s00418-003-0528-1

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  • DOI: https://doi.org/10.1007/s00418-003-0528-1

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