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JOURNAL ARTICLES
Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad
C. Tilmann, B. Capel
Development 1999 126: 2883-2890;

Summary

In mammals a single gene on the Y chromosome, Sry, controls testis formation. One of the earliest effects of Sry expression is the induction of somatic cell migration from the mesonephros into the XY gonad. Here we show that mesonephric cells are required for cord formation and male-specific gene expression in XY gonads in a stage-specific manner. Culturing XX gonads with an XY gonad at their surface, as a ‘sandwich’, resulted in cell migration into the XX tissue. Analysis of sandwich gonads revealed that in the presence of migrating cells, XX gonads organized cord structures and acquired male-specific gene expression patterns. From these results, we conclude that mesonephric cell migration plays a critical role in the formation of testis cords and the differentiation of XY versus XX cell types.

Reference

    1. Bostrom H.,
    2. Willetts K.,
    3. Pekny M.,
    4. Leveen P.,
    5. Lindahl P.,
    6. Hedstrand H.,
    7. Pekna M.,
    8. Hellstrom M.,
    9. Gebre-Medhin S.,
    10. Schalling M.,
    11. Nilsson M.,
    12. Kurland S.,
    13. Tornell J.,
    14. Heath J.,
    15. Betsholz C.
    (1996) PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863–873
    OpenUrlCrossRefPubMedWeb of Science
    1. Buehr M.,
    2. Gu S.,
    3. McLaren A.
    (1993) Mesonephric contribution to testis differentiation in the fetal mouse. Development 117, 273–281
    OpenUrlAbstract/FREE Full Text
    1. Burgoyne P. S.
    (1988) Role of mammalian Y chromosome in sex determination. Phil. Trans. R. Soc. Lond. B 322, 63–72
    OpenUrlAbstract/FREE Full Text
    1. Burgoyne P. S.,
    2. Buehr M.,
    3. Koopman P.,
    4. Rossant J.,
    5. McLaren A.
    (1988) Cell autonomous action of the testis-determining gene: Sertoli cells are exclusively XY in XXXY chimaeric mouse testes. Development 102, 443–450
    OpenUrlAbstract
    1. Capel B.,
    2. Rasberry C.,
    3. Dyson J.,
    4. Bishop C. E.,
    5. Simpson E.,
    6. Vivian N.,
    7. Lovell-Badge R.,
    8. Rastan S.,
    9. Cattanach B. M.
    (1993) Deletion of Y chromosome sequences located outside the testis determining region can cause XY female sex reversal. Nat. Genet 5, 301–307
    OpenUrlCrossRefPubMedWeb of Science
    1. da Silva S. M.,
    2. Hacker A.,
    3. Harley V.,
    4. Goodfellow P.,
    5. Swain A.,
    6. Lovell-Badge R.
    (1996) Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nature Genetics 14, 62–68
    OpenUrlCrossRefPubMedWeb of Science
    1. Dym M.,
    2. Lamsam-Casalotti S.,
    3. Jia M. C.,
    4. Kleinman H. K.,
    5. Papadopoulos V.
    (1991) Basement membrane increases G-protein levels and follicle-stimulating hormone responsiveness of Sertoli cell adenylyl cyclase activity. Endocrinology 128, 1167–1176
    OpenUrlCrossRefPubMedWeb of Science
    1. Eicher E. M.,
    2. Shown E. P.,
    3. Washburn L. L.
    (1995) Sex reversal in C57BL/6J-YPOSmice corrected by a Sry transgene. Phil. Trans. R. Soc. Lond. B 350, 263–269
    OpenUrlCrossRefPubMed
    1. Eicher E. M.,
    2. Washburn L. L.
    (1986) Genetic control of primary sex determination in mice. Ann. Rev. Genet 20, 327–360
    OpenUrlCrossRefPubMedWeb of Science
    1. Friedrich G.,
    2. Soriano P.
    (1991) Promoter trap in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev 5, 1513–1523
    OpenUrlAbstract/FREE Full Text
    1. Gubbay J.,
    2. Collignon J.,
    3. Koopman P.,
    4. Capel B.,
    5. Economou A.,
    6. Munsterberg A.,
    7. Vivian N.,
    8. Goodfellow P.,
    9. Lovell-Badge R.
    (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346, 245–250
    OpenUrlCrossRefPubMedWeb of Science
    1. Henrique D.,
    2. Adam J.,
    3. Myat A.,
    4. Chitnis A.,
    5. Lewis J.,
    6. Ish-Horowicz D.
    (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375, 787–790
    OpenUrlCrossRefPubMed
    1. Jager R. J.,
    2. Anvret M.,
    3. Hall K.,
    4. Scherer G.
    (1990) A human XY female with a frame shift mutation in the candidate testis-determining gene SRY. Nature 348, 452–454
    OpenUrlCrossRefPubMed
    1. Kent J.,
    2. Wheatley S. C.,
    3. Andrews J. E.,
    4. Sinclair A. H.,
    5. Koopman P.
    (1996) A male-specific role for SOX9 in vertebrate sex determination. Development 122, 2813–2822
    OpenUrlAbstract
    1. Koopman P.,
    2. Gubbay J.,
    3. Vivian N.,
    4. Goodfellow P.,
    5. Lovell-Badge R.
    (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351, 117–121
    OpenUrlCrossRefPubMedWeb of Science
    1. Lovell-Badge R.,
    2. Robertson E.
    (1990) XY female mice resulting from a heritable mutation in the murine primary testis determining gene, Tdy. Development 109, 635–646
    OpenUrlAbstract
    1. Martineau J.,
    2. Nordqvist K.,
    3. Tilmann C.,
    4. Lovell-Badge R.,
    5. Capel B.
    (1997) Male-specific cell migration into the developing gonad. Curr. Biol 7, 958–968
    OpenUrlCrossRefPubMedWeb of Science
    1. McLaren A.
    (1990) Of MIS and the mouse. Nature 345, 111–.
    OpenUrlCrossRefPubMed
    1. McLaren A.
    (1991) Development of the mammalian gonad: the fate of the supporting cell lineage. BioEssays 13, 151–156
    OpenUrlCrossRefPubMedWeb of Science
    1. Merchant-Larios H.,
    2. Moreno-Mendoza N.,
    3. Buehr M.
    (1993) The role of the mesonephros in cell differentiation and morphogenesis of the mouse fetal testis. Int. J. Dev. Biol 37, 407–415
    OpenUrlPubMedWeb of Science
    1. Moreno-Mendoza N.,
    2. Herrara-Munoz J.,
    3. Merchant-Larios H.
    (1995) Limb bud mesenchyme permits seminiferous cord formation in the mouse fetal testis but subsequent testosterone output is markedly affected by the sex of the donor stromal tissue. Dev. Biol 169, 51–56
    OpenUrlCrossRefPubMedWeb of Science
    1. Palmer S. J.,
    2. Burgoyne P. S.
    (1991) In situ analysis of fetal, prepuberal and adult XXXY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112, 265–268
    OpenUrlAbstract
    1. Palmer S. J.,
    2. Burgoyne P. S.
    (1991) The Mus musculus domesticus Tdy allele acts later than the Mus musculus musculus Tdy allele: A basis for XY sex reversal in C57Bl/6-YPOSmice. Development 113, 709–714
    OpenUrlAbstract
    1. Palmer S. J.,
    2. Burgoyne P. S.
    (1991) XY follicle cells in the ovaries of XO/XY and XO/XY/XYY mosaic mice. Development 111, 1017–1019
    OpenUrlAbstract/FREE Full Text
    1. Radice G.,
    2. Ferreira-Cornwell M.,
    3. Robinson S.,
    4. Rayburn H.,
    5. Chodosh L.,
    6. Takeichi M.,
    7. Hynes R.
    (1997) Precocious mammary gland development in P-cadherin deficient mice. J. Cell Biol 139, 1025–1032
    OpenUrlAbstract/FREE Full Text
    1. Shannon J. M.,
    2. Neilson L. D.,
    3. Gebb S. A.,
    4. Randell S. H.
    (1998) Mesenchyme specifies epithelial differentiation in reciprocal recombinant of embryonic lung and trachea. Dev. Dyn 212, 482–494
    OpenUrlCrossRefPubMedWeb of Science
    1. Sinclair A. H.,
    2. Berta P.,
    3. Palmer M. S.,
    4. Hawkins J. R.,
    5. Griffiths B. L.,
    6. Smith M. J.,
    7. Foster J. W.,
    8. Frischauf A. M.,
    9. Lovell-Badge R.,
    10. Goodfellow P. N.
    (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240–4
    OpenUrlCrossRefPubMedWeb of Science
    1. Skinner M. K.,
    2. Tung P. S.,
    3. Fritz I. B.
    (1985) Cooperativity between Sertoli cells and testicular peritubular myoid cells in the production and deposition of extracellular matrix components. J. Cell. Biol 100, 1941–1947
    OpenUrlAbstract/FREE Full Text
    1. Streuli C. H.,
    2. Bailey N.,
    3. Bissell M. J.
    (1991) Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological parity. J. Cell Biol 115, 1383–1395
    OpenUrlAbstract/FREE Full Text
    1. Swain A.,
    2. Narvaez V.,
    3. Burgoyne P.,
    4. Camerino G.,
    5. Lovell-Badge R.
    (1998) Daxl antagonizes Sry action in mammalian sex determination. Nature 391, 761–767
    OpenUrlCrossRefPubMed
    1. Taketo T.,
    2. Merchant L. H.,
    3. Koide S.
    (1984) Induction of testicular differentiation in the fetal mouse ovary by transplantation into adult male mice. Proc. Soc. Exp. Biol. Med 176, 148–153
    OpenUrlAbstract/FREE Full Text
    1. Tanabe Y.,
    2. Jessell T. M.
    (1996) Diversity and patterning in the developing spinal cord. Science 274, 1115–1123
    OpenUrlAbstract/FREE Full Text
    1. Thompson E. W.,
    2. Blackshaw A. W.,
    3. Raychoudhury S. S.
    (1995) Secreted products and extracellular matrix from testicular peritubular myoid cells influence androgen-binding protein secretion by Sertoli cells in culture. J. And 16, 28–35
    OpenUrlPubMed
    1. Tung P. S.,
    2. Fritz I. B.
    (1980) Interactions of Sertoli cells with myoid cells in vitro. Biol. Reprod 23, 207–217
    OpenUrlAbstract
    1. Vigier B.,
    2. Watrin F.,
    3. Magre S.,
    4. Tran D.,
    5. Josso N.
    (1987) Purified bovine AMH induces a characteristic freemartin effect in fetal rat prospective ovaries exposed to it in vitro. Development 100, 43–55
    OpenUrlAbstract
    1. Whitworth D. J.,
    2. Shaw G.,
    3. Renfree M. B.
    (1996) Gonadal sex reversal of the developing marsupial ovary in vivo and in vitro. Development 122, 4057–4063
    OpenUrlAbstract
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JOURNAL ARTICLES
Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad
C. Tilmann, B. Capel
Development 1999 126: 2883-2890;
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