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JOURNAL ARTICLES
Sry induces cell proliferation in the mouse gonad
J. Schmahl, E.M. Eicher, L.L. Washburn, B. Capel
Development 2000 127: 65-73;
J. Schmahl
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E.M. Eicher
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L.L. Washburn
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B. Capel
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Summary

Sry is the only gene on the Y chromosome that is required for testis formation in mammals. One of the earliest morphological changes that occurs as a result of Sry expression is a size increase of the rudimentary XY gonad relative to the XX gonad. Using 5′-bromo-2′-deoxyuridine (BrdU) incorporation to label dividing cells, we found that the size increase corresponds with a dramatic increase in somatic cell proliferation in XY gonads, which is not detected in XX gonads. This male-specific proliferation was observed initially in the cells of the coelomic epithelium and occurred in two distinct stages. During the first stage, proliferation in the XY gonad was observed largely in SF1-positive cells and contributed to the Sertoli cell population. During the second stage, proliferation was observed in SF1-negative cells at and below the coelomic epithelium and did not give rise to Sertoli cells. Both stages of proliferation were dependent on Sry and independent of any other genetic differences between male and female gonads, such as X chromosome dosage or other genes on the Y chromosome. The increase in cell proliferation began less than 24 hours after the onset of Sry expression, before the establishment of male-specific gene expression patterns, and before the appearance of any other known male-specific morphological changes in the XY gonad. Therefore, an increase in cell proliferation in the male coelomic epithelium is the earliest identified effect of Sry expression.

REFERENCES

    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. Buehr M.,
    2. Petzoldt U.
    (1974) Gonad size and sex differentiation in rabbit embryos. Verh. Anat. Ges 68, 163–167
    OpenUrlPubMed
    1. Capel B.,
    2. Albrecht K. H.,
    3. Washburn L. L.,
    4. Eicher E. M.
    (1999) Migration of mesonephric cells into the mammalian gonad depends on Sry. Mech. Dev 84, 127–131
    OpenUrlCrossRefPubMedWeb of Science
    1. Carayon P.,
    2. Boyd A.
    (1992) Identification of DNA-replicating lymphocyte subsets using a new method to label the bromo-deoxyuridine incorporated into the DNA. J. Immunol. Methods 147, 225–230
    OpenUrlPubMedWeb of Science
    1. Dolbeare F.
    (1995) Bromodeoxyuridine: a diagnostic tool in biology and medicine, Part I: Historical perspectives, histochemical methods and cell kinetics. Histochem. J 27, 339–369
    OpenUrlPubMedWeb of Science
    1. Eicher E. M.,
    2. Shown E. P.,
    3. Washburn L. L.
    (1995) Sex reversal inC57BL/6J-YPOSmice corrected by a Sry transgene. Phil. Trans. R. Soc. 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. Eicher E. M.,
    2. Washburn L. L.,
    3. Schork N.,
    4. Lee B.,
    5. Shown E.,
    6. Xu X.,
    7. Dredge R.,
    8. Pringle M.,
    9. Page D.
    (1996) Sex-determining genes on mouse autosomes identified by linkage analysis of C57BL/6J-YPOS. Nature Genetics, 14, 206–209
    OpenUrlCrossRefPubMedWeb of Science
    1. Eicher E. M.,
    2. Washburn L. L.,
    3. Whitney I. J.,
    4. Morrow K. E.
    (1982) Mus poschiavinus Y chromosome in the C57BL/6J murine genome causes sex reversal. Science 217, 535–537
    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
    OpenUrlCrossRefPubMed
    1. Haaf T.
    (1996) High-resolution analysis of DNA replication in released chromatin fibers containing 5-bromodeoxyuridine. Biotechniques 21, 1050–1054
    OpenUrlPubMed
    1. Hacker A.,
    2. Capel B.,
    3. Goodfellow P.,
    4. Lovell-Badge R.
    (1995) Expression of Sry, the mouse sex determining gene. Development 121, 1603–1614
    OpenUrlAbstract
    1. Harley V. R.,
    2. Jackson D. I.,
    3. Hextal P. J.,
    4. Hawkins J. R.,
    5. Berkovitz G. D.,
    6. Sockanathan S.,
    7. Lovell-Badge R.,
    8. Goodfellow P. N.
    (1992) DNA binding activity of recombinant SRY from normal males and XY females. Science 225, 453–456
    1. Hatano O.,
    2. Takayama K.,
    3. Imai T.,
    4. Waterman M. R.,
    5. Takakusu A.,
    6. Omura T.,
    7. Morohashi K.
    (1994) Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 120, 2787–2797
    OpenUrlAbstract
    1. Hawkins J. R.,
    2. Taylor A.,
    3. Berta P.,
    4. Levilliers J.,
    5. Van D. A. B.,
    6. Goodfellow P. N.
    (1992) Mutational analysis of SRY: Nonsense and missense mutations in XY sex reversal. Hum. Genet 88, 471–474
    OpenUrlCrossRefPubMedWeb of Science
    1. Horvitz R. H.,
    2. Herskowitz I.
    (1992) Mechanisms of asymmetric celldivision: Two Bs or not two Bs, that is the question. Cell 68, 237–255
    OpenUrlCrossRefPubMedWeb of Science
    1. Hunt S. E.,
    2. Mittwoch U.
    (1987) Y-chromosomal and other factors in the development of testis size in mice. Genet. Res 50, 205–211
    OpenUrlPubMedWeb of Science
    1. Karl J.,
    2. Capel B.
    (1998) Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol 203, 323–333
    OpenUrlCrossRefPubMedWeb of Science
    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
    OpenUrlCrossRefPubMed
    1. Lovell-Badge R.
    (1993) Sex determining gene expression during embryogenesis. Phil. Trans. R. Soc. London B 335, 159–164
    OpenUrl
    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. Luo X.,
    2. Ikeda Y.,
    3. Parker K. L.
    (1995) The cell-specific nuclear receptor steroidogenic factor 1 plays multiple roles in reproductive function. Phil. Trans. R. Soc. London 350, 279–283
    OpenUrlPubMed
    1. Magre S.,
    2. Jost A.
    (1991) Sertoli cells and testicular differentiation in the rat fetus. J. Electron Microsc. Tech 19, 172–188
    OpenUrlCrossRefPubMedWeb of Science
    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. Merchant-Larios H.
    (1979) Origin of the somatic cells in the rat gonad: an autoradiographic approach. Ann. Biol. Anim. Bioch. Biophys 19, 1219–1229
    OpenUrlCrossRef
    1. Merchant-Larios H.,
    2. Moreno-Mendoza N.
    (1998) Mesonephric stromal cells differentiate into Leydig cells in the mouse fetal testis. Exper. Cell Res 244, 230–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Mittwoch U.
    (1986) Males, females and hermaphrodites. Ann. Hum. Genet 50, 103–121
    OpenUrlPubMedWeb of Science
    1. Mittwoch U.,
    2. Delhanty J. D. A.,
    3. Beck F.
    (1969) Growth of differentiating testes and ovaries. Nature 224, 1323–1325
    OpenUrlCrossRefPubMed
    1. Mittwoch U.,
    2. Mahadevaiah S.
    (1980) Additional growth-a link between mammalian testes, avian ovaries, gonadal asymmetry in hermaphrodites and the expression of H-Y antigen. Growth 44, 287–300
    OpenUrlPubMedWeb of Science
    1. Ohsugi K.,
    2. Gardiner D. M.,
    3. Bryant S. V.
    (1997) Cell cycle length affects gene expression and pattern formation in limbs. Dev. Biol 189, 13–21
    OpenUrlCrossRefPubMed
    1. Page D. C.,
    2. Fisher E.,
    3. McGillivray B.,
    4. Brown L. G.
    (1990) Additional deletion in sex-determining region of human Y chromosome resolves paradox of X,t(Y,22) female. Nature 346, 279–281
    OpenUrlCrossRefPubMed
    1. Palmer S. J.,
    2. Burgoyne P. S.
    (1991) In situ analysis of fetal, prepuberal and adult XXXY chimaeric mouse testes: Sertoli cells are predominatly, 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. Pelliniemi L. J.
    (1976) Ultrastructure of the indifferent gonad in male and female pig embryos. Tissue Cell 8, 163–175
    OpenUrlCrossRefPubMed
    1. Pourquie O.
    (1998) Clocks regulating developmental processes. Curr. Opin. Neurobiol 8, 665–670
    OpenUrlCrossRefPubMed
    1. Rimini R.,
    2. Pontiggia A.,
    3. Spada F.,
    4. Ferrari S.,
    5. Harley V. R.,
    6. Goodfellow P. N.,
    7. Bianchi M. E.
    (1995) Interaction of normal and mutant SRY proteins with DNA. Phil. Trans. R. Soc. London 350, 215–220
    OpenUrlCrossRefPubMed
    1. Russell L. D.,
    2. de Franca L. R.,
    3. Hess R.,
    4. Cooke P.
    (1995) Characteristics of mitotic cells in developing and adult testes with observations on cell lineages. Tissue Cell 27, 105–128
    OpenUrlCrossRefPubMedWeb of Science
    1. Schutte B.,
    2. Reynders M. M. J.,
    3. Bosman F. T.,
    4. Blijham G. H.
    (1987) Effect of tissue fixation on anit-bromodeoxyuridine immunohistochemistry. J. Histochem. Cytochem., 35, 1343–1345
    OpenUrlAbstract/FREE Full Text
    1. Smith C. A.,
    2. Joss J. M. P.
    (1993) Gonadal sex differentiation in Alligator mississippiensis, a species with temperature-dependent determination. Cell Tiss. Res 273, 149–163
    OpenUrlCrossRef
    1. Swain A.,
    2. Narvaez S.,
    3. Burgoyne P.,
    4. Camerino G.,
    5. Lovell-Badge R.
    (1998) DAX1 antagonizes SRY action in mammalian sex determination. Nature 391, 761–767
    OpenUrlCrossRefPubMed
    1. Tabin C. J.
    (1998) A developmental model for thalidomide defects. Nature, 396, 322–323
    OpenUrlCrossRefPubMed
    1. Tam P.,
    2. Snow M.
    (1981) Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morph 64, 133–147
    OpenUrlPubMedWeb of Science
    1. Torrey T. W.
    (1945) Development of the urogenital system of albino rat gonads. Am. J. Anat., 76, 375–397
    OpenUrlCrossRef
    1. Vergouwen R. P. F. A.,
    2. Jacobs S. G. P. M.,
    3. Huiskamp R.,
    4. Davids J. A. G.,
    5. de Rooij D. G.
    (1991) Proliferative activity of gonocytes, Sertoli cells and intertitial cells during testicular development in mice. J. Reprod. Fert 93, 233–243
    OpenUrlAbstract/FREE Full Text
    1. Whitehead R. H.
    (1904) The embryonic development of the interstitial cells of Leydig. Am. J. Anat 3, 167–187
    OpenUrlCrossRef
    1. Witschi E.
    (1951) Embryogenesis of the adrenal and the reproductive glands. Recent Progr. Hormone Res 6, 1–27
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JOURNAL ARTICLES
Sry induces cell proliferation in the mouse gonad
J. Schmahl, E.M. Eicher, L.L. Washburn, B. Capel
Development 2000 127: 65-73;
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JOURNAL ARTICLES
Sry induces cell proliferation in the mouse gonad
J. Schmahl, E.M. Eicher, L.L. Washburn, B. Capel
Development 2000 127: 65-73;

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