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Molecular Regulation of Marsupial Reproduction and Development

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Marsupial Genetics and Genomics

Abstract

The three extant mammalian lineages are primarily defined by their differing strategies of reproduction. Monotremes lay eggs while eutherians generally have a long period of gestation and give birth to well developed young. Marsupials sit between the two strategies and have a relatively short gestation, giving birth to poorly developed young that complete the majority of their early development external to the mother while suckling. This unique reproductive strategy provides an ideal mammalian model system in which to study and manipulate early development. Here we summarise our current understanding of the molecular regulation of marsupial reproduction and development, and highlight how marsupial studies have informed our understanding of the function of genes in mammalian development.

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References

  • Alcorn GT, Robinson ES (1983) Germ cell development in female pouch young of the tammar wallaby (Macropus eugenii). J Reprod Fertil 67:319–325.

    Google Scholar 

  • Ambrosetti DC, Basilico C, Dailey L (1997) Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol Cell Biol 17:6321–6329.

    Google Scholar 

  • Anderson R, Copeland TK, Scholer H, Heasman J, Wylie C (2000) The onset of germ cell migration in the mouse embryo. Mech Dev 91:61–68.

    Google Scholar 

  • Arlt W, Walker EA, Draper N, et al. (2004) Congenital adrenal hyperplasia caused by mutant P450 oxidoreductase and human androgen synthesis: analytical study. Lancet 363: 2128–2135.

    Article  PubMed  CAS  Google Scholar 

  • Arnold AP (2009) The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav 55:570–578.

    Article  PubMed  CAS  Google Scholar 

  • Au PC, Whitley J, Vaux D, Selwood L, Familari M (2008) Identification of novel and known ovary-specific genes including ZP2, in a marsupial, the stripe-faced dunnart. Mol Reprod Dev 75:318–325.

    Article  PubMed  CAS  Google Scholar 

  • Bagheri-Fam S, Sinclair AH, Koopman P, Harley VR (2009) Conserved regulatory modules in the Sox9 testis-specific enhancer predict roles for SOX TCF/LEF Forkhead DMRT and GATA proteins in vertebrate sex determination. Int J Biochem Cell Biol 42:472–477.

    Google Scholar 

  • Bedford JM, Breed WG (1994) Regulated storage and subsequent transformation of spermatozoa in the fallopian tubes of an Australian marsupial Sminthopsis crassicaudata. Biol Reprod 50:845–854.

    Article  PubMed  CAS  Google Scholar 

  • Belov K, Harrison GA, Cooper DW (1998) Cloning of the red kangaroo (Macropus rufus) follicle stimulating hormone beta subunit. Reprod Fertil Dev 10:289–291.

    Article  PubMed  CAS  Google Scholar 

  • Bowles J, Knight D, Smith C, et al. (2006) Retinoid signaling determines germ cell fate in mice. Science 312:596–600.

    Article  PubMed  CAS  Google Scholar 

  • Braundmeier AG, Breed WG, Miller DJ (2008) Spermatozoa from a marsupial the brushtail possum contain beta14-galactosyltransferase. Reprod Fertil Dev 20:402–407.

    Article  PubMed  CAS  Google Scholar 

  • Britt KL, Stanton PG, Misso M, Simpson ER, Findlay JK (2004) The effects of estrogen on the expression of genes underlying the differentiation of somatic cells in the murine gonad. Endocrinology 145:3950–3960.

    Article  PubMed  CAS  Google Scholar 

  • Brown PR, Miki K, Harper DB, Eddy EM (2003) A-kinase anchoring protein 4 binding proteins in the fibrous sheath of the sperm flagellum. Biology Reprod 68:2241–2248.

    Article  CAS  Google Scholar 

  • Burgoyne PS, Thornhill AR, Boudrean SK, Darling SM, Bishop CE, Evans EP (1995) The genetic basis of XX–XY differences present before gonadal sex differentiation in the mouse Philos. Trans R Soc Lond B Biol Sci 350:253–260.

    Article  CAS  Google Scholar 

  • Burns RK (1955) Experimental reversal of sex in the gonads of the opossum Didelphis virginiana. PNAS 41:669–676.

    Article  PubMed  CAS  Google Scholar 

  • Burns RK (1961) Role of hormones in the differentiation of sex. In: Young WC (eds) Sex and Internal Secretions, Vol 1. Williams and Wilkins, Baltimore, pp. 76–158.

    Google Scholar 

  • Butler CM, Harry JL, Deakin JE, Cooper DW, Renfree MB (1998) Developmental expression of the androgen receptor during virilization of the urogenital system of a marsupial. Biol Reprod 59:725–732.

    Article  PubMed  CAS  Google Scholar 

  • Calatayud NE, Pask AJ, Shaw G, Renfree MB (2010) Oestrogen receptors ERα and ERb in the tammar wallaby. Reproduction 139:599–611.

    Google Scholar 

  • Carrera A, Gerton GL, Moss SB (1994) The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 165: 272–284.

    Article  PubMed  CAS  Google Scholar 

  • Carrera A, Moos J, Ning XP, et al. (1996) Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev Biol 180:284–296.

    Article  PubMed  CAS  Google Scholar 

  • Chambers I, Colby D, Robertson M, et al. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643–655.

    Article  PubMed  CAS  Google Scholar 

  • Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F (2004) Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 101:7641–7645.

    Article  PubMed  CAS  Google Scholar 

  • Cheung TC, Hearn JP (2002) Molecular cloning and tissue expression of the gonadotrophin-releasing hormone receptor in the tammar wallaby (Macropus eugenii). Reprod Fertil Dev 14:157–164.

    Article  PubMed  CAS  Google Scholar 

  • Cheung TC, Hearn JP (2003) Developmental expression and subcellular localization of wallaby gonadotropin-releasing hormone receptor and its splice variants. Gen Comp Endocrinol 133:88–99.

    Article  PubMed  CAS  Google Scholar 

  • Cheung TC, Hearn JP (2005) Dimerizations of the wallaby gonadotropin-releasing hormone receptor and its splice variants. Gen Comp Endocrinol 144:280–288.

    Article  PubMed  CAS  Google Scholar 

  • Colledge M, Scott JD (1999) AKAPs: from structure to function. Trends Cell Biol 9:216–221.

    Article  PubMed  CAS  Google Scholar 

  • Cooper DW (1993) The evolution of sex determination sex chromosome dimorphism and X-inactivation in Therian mammals: a comparison of metatherians (marsupials) and eutherians (‘placentals’). In: Reed KC Graves JAM (eds) Sex Chromosomes and Sex Determining Genes. Harwood Academic Publishers, GmbH Chur, Switzerland.

    Google Scholar 

  • Couse JF, Korach KS (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358–417.

    Article  PubMed  CAS  Google Scholar 

  • Coveney D, Shaw G, Renfree MB (2001) Estrogen-induced gonadal sex reversal in the tammar wallaby. Biol Reprod 65:613–621.

    Article  PubMed  CAS  Google Scholar 

  • Crawford JL, Heath DA, Haydon LJ, Thomson BP, Eckery DC (2009) Gene expression and secretion of LH and FSH in relation to gene expression of GnRH receptors in the brushtail possum (Trichosurus vulpecula) demonstrates highly conserved mechanisms. Reproduction 137:129–140.

    Article  PubMed  CAS  Google Scholar 

  • Cui S, Selwood L (2000) cDNA cloning characterization expression and recombinant protein production of leukemia inhibitory factor (LIF) from the marsupial the brushtail possum (Trichosurus vulpecula). Gene 243:167–178.

    Article  PubMed  CAS  Google Scholar 

  • Cui S, Selwood L (2003) Cloning and expression of a novel cDNA encoding shell coat protein cp4 from the brushtail possum (Trichosurus vulpecula). Mol Reprod Dev 65:141–147.

    Article  PubMed  CAS  Google Scholar 

  • Cui S, Nikolovski S, Nanayakkara K, Selwood L (2005) VAP1 with cystatin C motif an oocyte protein encoded by a novel ovarian-specific gene during oogenesis in the common brushtail possum (Trichosurus vulpecula). Mol Reprod Dev 71:19–28.

    Article  PubMed  CAS  Google Scholar 

  • Cummins JM (1980) Decondensation of sperm nuclei of Australian marsupials: effects of air drying and of calcium and magnesium. Gamete Res 3:351–367.

    Article  CAS  Google Scholar 

  • Curlewis JD, Saunders MC, Kuang J, Harrison GA, Cooper DW (1998) Cloning and sequence analysis of a pituitary prolactin cDNA from the brushtail possum (Trichosurus vulpecula). Gen Comp Endocrinol 111:61–67.

    Article  PubMed  CAS  Google Scholar 

  • de Santa Barbara P, Moniot B, Poulat F, Berta P (2000) Expression and subcellular localisation of SF1 SOX9 WT1 and AMH proteins during early human testicular development. Dev Dyn 217:293–298.

    Article  PubMed  Google Scholar 

  • Denker HW, Tyndale-Biscoe CH (1986) Embryo implantation and proteinase activities in a marsupial (Macropus eugenii). Histochemical patterns of proteinases in various gestational stages. Cell Tissue Res 246:279–291.

    Article  PubMed  Google Scholar 

  • Eckery DC, Lawrence SB, Juengel JL, Greenwood P, McNatty KP, Fidler AE (2002a) Gene expression of the tyrosine kinase receptor c-kit during ovarian development in the brushtail possum (Trichosurus vulpecula). Biol Reprod 66:346–353.

    Article  PubMed  CAS  Google Scholar 

  • Eckery DC, Lun S, Thomson BP, Chie WN, Moore LG, Juengel JL (2002b) Ovarian expression of messenger RNA encoding the receptors for luteinizing hormone and follicle-stimulating hormone in a marsupial the brushtail possum (Trichosurus vulpecula). Biol Reprod 66: 1310–1317.

    Article  PubMed  CAS  Google Scholar 

  • Eckery DC, Whale LJ, Lawrence SB, Wylde KA, McNatty KP, Juengel JL (2002c) Expression of mRNA encoding growth differentiation factor 9 and bone morphogenetic protein 15 during follicular formation and growth in a marsupial the brushtail possum (Trichosurus vulpecula). Mol Cell Endocrinol 192:115–126.

    Article  PubMed  CAS  Google Scholar 

  • Eddy EM, Toshimori K, O’Brien DA (2003) Fibrous sheath of mammalian spermatozoa. Microsc Res Tech 61:103–115.

    Article  PubMed  CAS  Google Scholar 

  • Edwards AS, Scott JD (2000) A-kinase anchoring proteins: protein kinase A and beyond. Curr Opin Cell Biol 12:217–221.

    Article  PubMed  CAS  Google Scholar 

  • Fidler AE, Lawrence SB, Vanmontfort DM, Tisdall DJ, McNatty KP (1998) The Australian brushtail possum (Trichosurus vulpecula) gonadotrophin alpha-subunit: analysis of cDNA sequence and pattern of expression. J Mol Endocrinol 20:345–353.

    Article  PubMed  CAS  Google Scholar 

  • Fletcher TP, Renfree MB (1988) Effects of corpus luteum removal on progesterone estradiol-17 beta and LH in early pregnancy of the tammar wallaby Macropus eugenii. J Reprod Fertil 83:185–191.

    Article  PubMed  CAS  Google Scholar 

  • Foster JW, Brennan FE, Hampikian GK, Goodfellow PN, Sinclair AH, Lovell-Badge R, Selwood L, Renfree MB, Cooper DW, Graves JA (1992) Evolution of sex determination and the Y chromosome: SRY-related sequences in marsupials. Nature 359:531–533.

    Article  PubMed  CAS  Google Scholar 

  • Foster JW, Graves JAM (1994) An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. Proc Natl Acad Sci USA 91:1927–1931.

    Article  PubMed  CAS  Google Scholar 

  • Frankenberg S, Tisdall D, Selwood L (2001) Identification of a homologue of POU5F1 (OCT3/4) in a marsupial the brushtail possum. Mol Reprod Dev 58:255–261.

    Article  PubMed  CAS  Google Scholar 

  • Frankenberg S, Pask AJ, Renfree MB (2010) The evolution of class V POU domain transcription factors in vertebrates and their characterisation in a marsupial Developmental Biology 337:162–170.

    Google Scholar 

  • Freyer C, Renfree MB (2009) The mammalian yolk sac placenta. J Exp Zool B Mol Dev Evol 312:545–554.

    Google Scholar 

  • Freyer C, Zeller U, Renfree MB (2003) The marsupial placenta: a phylogenetic analysis. J Exp Zool A Comp Exp Biol 299:59–77.

    Google Scholar 

  • Fulcher KD, Mori C, Welch JE, O’Brien DA, Klapper DG, Eddy EM (1995) Characterization of Fsc1 cDNA for a mouse sperm fibrous sheath component. Biol Reprod 52:41–49.

    Article  PubMed  CAS  Google Scholar 

  • Hamatani T, Daikoku T, Wang H, et al. (2004) Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci USA 101:10326–10331.

    Google Scholar 

  • Hanley NA, Hagan DM, Clement-Jones M, et al. (2000) SRY SOX9 and DAX1 expression patterns during human sex determination and gonadal development. Mech Dev 91: 403–407.

    Article  PubMed  CAS  Google Scholar 

  • Harris MS, Rodger JC (2005) Characterisation of an epitope shared by an acrosomal acrosin-like protein and the surface of tammar wallaby (Macropus eugenii) spermatozoa. J Exp Zool A Comp Exp Biol 303:713–721.

    PubMed  Google Scholar 

  • Harrison GA, Deane EM, Cooper DW (1998) cDNA cloning of luteinizing hormone subunits from brushtail possum and red kangaroo. Mamm Genome 9:638–642.

    Article  PubMed  CAS  Google Scholar 

  • Harry JL, Koopman P, Brennan FE, Graves JAM, Renfree MB (1995) Widespread expression of the testis determining gene SRY in a marsupial. Nat Genet 11:347–349.

    Article  PubMed  CAS  Google Scholar 

  • Haydon LJ, Juengel JL, Thomson BP, Eckery DC (2008) Expression of mRNAs encoding oestrogen receptor (ER) alpha and ERbeta, androgen receptor and progesterone receptor during gonadal and follicular development in the marsupial brushtail possum (Trichosurus vulpecula). Fertil Dev 20:335–349.

    Article  CAS  Google Scholar 

  • Heap RB, Renfree MB, Burton RD (1980) Steroid metabolism in the yolk sac placenta and endometrium of the tammar wallaby, Macropus eugenii. J Endocrinol 87:339–349.

    Article  PubMed  CAS  Google Scholar 

  • Homma K, Hasegawa T, Nagai T, et al. (2006) Urine steroid hormone profile analysis in cytochrome P450 oxidoreductase deficiency: implication for the backdoor pathway to dihydrotestosterone. J Clin Endocrinol Metab 91:2643–2649.

    Article  PubMed  CAS  Google Scholar 

  • Hondo E, Stewart CL (2005) Profiling gene expression in growth-arrested mouse embryos in diapause. Genome Biol 6:202.

    Article  PubMed  Google Scholar 

  • Hu Y, Yu H, Pask AJ, O’Brien DA, Shaw G, Renfree MB (2009) A-kinase anchoring protein 4 has a conserved role in mammalian spermatogenesis. Reproduction 137:645–653.

    Article  PubMed  CAS  Google Scholar 

  • Hughes RL, Hall LS (1988) Structural adaptations of the newborn marsupial. In: Tyndale-Biscoe CH Janssens PA (eds) The Developing Marsupial. Springer, Berlin, pp. 8–27.

    Chapter  Google Scholar 

  • Hutson JM, Shaw G, O WS, Short RV, Renfree MB (1988) The ontogeny of Mullerian inhibiting substance production and testicular differentiation migration and descent in the pouch young of a marsupial. Development 104:549–556.

    PubMed  CAS  Google Scholar 

  • Ingram JN, Shaw G, Renfree MB (1999) Cortisol in fetal fluids and the fetal adrenal at parturition in the tammar wallaby (Macropus eugenii). Biol Reprod 60:651–655.

    Article  PubMed  CAS  Google Scholar 

  • Jeays-Ward K, Hoyle C, Brennan J, et al. (2003) Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130:3663–3670.

    Article  PubMed  CAS  Google Scholar 

  • Jiang FX, Clark J, Renfree MB (1997) Ultrastructural characteristics of primordial germ cells and their amoeboid movement to the gonadal ridges in the tammar wallaby. Anat Embryol 195:473–481.

    Article  PubMed  CAS  Google Scholar 

  • Jordan BK, Shen JH, Olaso R, Ingraham HA, Vilain E (2003) Wnt4 over-expression disrupts normal testicular vasculature and inhibits testosterone synthesis by repressing steroidogenic factor 1/ beta-catenin synergy. Proc Natl Acad Sci USA 100:10866–10871.

    Article  PubMed  CAS  Google Scholar 

  • Jost A (1947) Recherches sur la differenciation sexuelle de l’embryon de lapin. J Arch Anat Microsc Morphol Exp 36:117–121.

    Google Scholar 

  • Jost A (1970) Hormonal factors in the sex differentiation of the mammalian foetus. Philos Trans R Soc Lond B Biol Sci 259:119–130.

    Article  PubMed  CAS  Google Scholar 

  • Juengel JL, Whale LJ, Wylde KA, Greenwood P, McNatty KP, Eckery DC (2002) Expression of anti-Müllerian hormone mRNA during gonadal and follicular development in the brushtail possum (Trichosurus vulpecula). Reprod Fertil Dev 14:345–353.

    Article  PubMed  CAS  Google Scholar 

  • Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD (2004) The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36:642–646.

    Article  PubMed  CAS  Google Scholar 

  • Koopman P, Münsterberg A, Capel B, Vivian N, Lovell-Badge R (1990) Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348:450–452.

    Article  PubMed  CAS  Google Scholar 

  • Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R (1991) Male development of chromosomal female mice transgenic for SRY. Nature 351:117–121.

    Article  PubMed  CAS  Google Scholar 

  • Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA 103:2474–2479.

    Article  PubMed  CAS  Google Scholar 

  • Kunath T, Strumpf D, Rossant J (2004) Early trophoblast determination and stem cell maintenance in the mouse–a review. Placenta 25:S32–S38.

    Article  PubMed  Google Scholar 

  • Kwek JHL, De Iongh R, Digby MR, Renfree MB, Nicholas KR, Familari M (2009) Cross-fostering of the tammar wallaby (Macropus eugenii) pouch young accelerates fore-stomach maturation. MOD 126:449–463.

    PubMed  CAS  Google Scholar 

  • Leatherland JF, Renfree MB (1983) Structure of the pars distalis in pouch-young tammar wallabies (Macropus eugenii). Cell Tissue Res 230:587–603.

    Article  PubMed  CAS  Google Scholar 

  • Lin M, Harman A, Rodger JC (1997) Spermiogenesis and spermiation in a marsupial the tammar wallaby (Macropus eugenii). J Anat 190:377–395.

    Article  PubMed  Google Scholar 

  • Lin M, Rodger JC (1999) Acrosome formation during sperm transit through the epididymis in two marsupials the tammar wallaby (Macropus eugenii) and the brushtail possum (Trichosurus vulpecula). J Anat 194:223–232.

    Article  PubMed  Google Scholar 

  • Liu L, Leaman D, Villalta M, Roberts RM (1997) Silencing of the gene for the alpha-subunit of human chorionic gonadotropin by the embryonic transcription factor Oct-3/4. Mol Endocrinol 11:1651–1658.

    Article  PubMed  CAS  Google Scholar 

  • Lumbers ER, Menzies RI, Gibson KJ, Tyndale-Biscoe CH (1994) Levels of active and inactive reninlike enzymes in plasma and reproductive tract of the pregnant wallaby. Am J Physiol 266:R1353–R1358.

    PubMed  CAS  Google Scholar 

  • Mahendroo M, Wilson JD, Richardson JA, Auchus RJ (2004) Steroid 5alpha-reductase 1 promotes 5alpha-androstane-3alpha17beta-diol synthesis in immature mouse testes by two pathways. Mol Cell Endocrinol 222:113–120.

    Article  PubMed  CAS  Google Scholar 

  • Mate KE, McCartney CA (1998) Sequence and analysis of zona pellucida 2 cDNA (ZP2) from a marsupial the brushtail possum Trichosurus vulpecula. Mol Reprod Dev 51:322–329.

    Article  PubMed  CAS  Google Scholar 

  • Mate KE, Rodger JC (1991) Stability of the acrosome of the brush-tailed possum (Trichosurus vulpecula) and tammar wallaby (Macropus eugenii) in vitro and after exposure to conditions and agents known to cause capacitation or acrosome reaction of eutherian spermatozoa. J Reprod Fertil 91:41–48.

    Article  PubMed  CAS  Google Scholar 

  • Mate KE, Buist JM, Duckworth JA (2003) Expression in Escherichia coli and immunological characterization of three zona pellucida proteins (ZP1 ZP2 and ZP3) from a marsupial the brushtail possum (Trichosurus vulpecula). Mol Reprod Dev 64:136–143.

    Article  PubMed  CAS  Google Scholar 

  • Matsuzawa-Watanabe Y, Inoue J, Semba K (2003) Transcriptional activity of testis-determining factor SRY is modulated by the Wilms’ tumor 1 gene product WT1. Oncogene 22:7900–7904.

    Article  PubMed  CAS  Google Scholar 

  • Mattiske D, Pask AJ, Shaw JM, Shaw G (2002) Structure and expression of the follicle-stimulating hormone receptor gene in a marsupial Macropus eugenii. Mol Reprod Dev 63:24–31.

    Article  PubMed  CAS  Google Scholar 

  • McCartney CA, Mate KE (1999) Cloning and characterisation of a zona pellucida 3 cDNA from a marsupial the brushtail possum Trichosurus vulpecular. Zygote 7:1–9.

    Article  PubMed  CAS  Google Scholar 

  • McLaren A (1981) The fate of germ cells in the testis of fetal Sex-reversed mice. J Reprod Fertil 61:461–467.

    Article  PubMed  CAS  Google Scholar 

  • McLaren A (2003) Primordial germ cells in mice. Dev Biol 262:1–15.

    Article  PubMed  CAS  Google Scholar 

  • Meeks JJ, Crawford SE, Russell TA, Morohashi K, Weiss J, Jameson JL (2003) Dax1 regulates testis cord organization during gonadal differentiation. Development 130:1029–1036.

    Article  PubMed  CAS  Google Scholar 

  • Menkhorst E, Selwood L, Cui S (2009) Uterine expression of cp4 gene homolog in the Stripe-faced Dunnart Sminthopsis macroura: relationship with conceptus development and progesterone profile. Mol Reprod Dev 76:863–872.

    Article  PubMed  CAS  Google Scholar 

  • Menzies BR, Shaw G, Fletcher TP, Renfree MB (2007) Perturbed growth and development in marsupial young after reciprocal cross-fostering between species. Reprod Fertil Dev 19: 976–983.

    Article  PubMed  Google Scholar 

  • Menzies BR, Shaw G, Fletcher TP, Pask AJ, Renfree MB (2008) Exon 3 of the growth hormone receptor (GH-R) is specific to eutherian mammals. Mol Cell Endocrinol 296:64–68.

    Article  PubMed  CAS  Google Scholar 

  • Menzies BR, Shaw G, Fletcher TP, Renfree MB (2009) Early onset of ghrelin production in a marsupial. Mol Cell Endocrinol 299:266–273.

    Article  PubMed  CAS  Google Scholar 

  • Miki K, Willis WD, Brown PR, Goulding EH, Fulcher KD, Eddy EM (2002) Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility. Dev Biol 248:331–342.

    Article  PubMed  CAS  Google Scholar 

  • Mitsui K, Tokuzawa Y, Itoh H, et al. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–642.

    Article  PubMed  CAS  Google Scholar 

  • Morais da Silva S, Hacker A, Harley V, et al. (1996) SOX9 expression during gonadal development implies a conserved role for the gene in Sertoli cell differentiation in mammals and birds. Nat Genet 14:62–68.

    Article  PubMed  CAS  Google Scholar 

  • Nation A, Cui S, Selwood L (2008) Vesicle-associated protein 1: a novel ovarian immunocontraceptive target in the common brushtail possum Trichosurus vulpecula. Reproduction 136:657–665.

    Article  PubMed  CAS  Google Scholar 

  • Natoli TA, Alberta JA, Bortvin A, et al. (2004) Wt1 functions in the development of germ cells in addition to somatic cell lineages of the testis. Dev Biol 268:429–440.

    Article  PubMed  CAS  Google Scholar 

  • O WS, Short RV, Renfree MB, Shaw G (1988) Primary genetic control of somatic sexual differentiation in a mammal. Nature 332:716–717.

    Article  Google Scholar 

  • Ohno S (1967) Sex Chromosomes and Sex Linked Genes. Springer, Berlin.

    Book  Google Scholar 

  • Oreal E, Pieau C, Mattei M, Picard J, Carre-eusebe D, Magre S (1998) MIS in chicken embryonic gonads precedes testicular SOX9 expression. Dev Dyn 21:522–532.

    Article  Google Scholar 

  • Parker KL (1998) The roles of steroidogenic factor 1 in endocrine development and function. Mol Cell Endocrinol 140:59–63.

    Article  PubMed  CAS  Google Scholar 

  • Pask A, Renfree MB, Graves JAM (2000a) The human sex reversing ATRX gene has a homologue on the marsupial Y chromosome ATRY: implications for the evolution of mammalian sex determination. Proc Natl Acad Sci USA 97:13198–13202.

    Article  PubMed  CAS  Google Scholar 

  • Pask A, Harry JL, Renfree MB, Graves JAM (2000b) Genesis 27:145–152.

    Article  PubMed  CAS  Google Scholar 

  • Pask A, Toder R, Wilcox SA, Camerino G, Graves JAM (1997) The candidate sex-reversing DAX1 gene is autosomal in marsupials: implications for the evolution of sex determination in mammals. Genomics 41:422–426.

    Article  PubMed  CAS  Google Scholar 

  • Pask AJ, Harry JL, Graves JAM, et al. (2002) SOX9 has both conserved and novel roles in marsupial sexual differentiation. Genesis 33:131–139.

    Article  PubMed  CAS  Google Scholar 

  • Pask AJ, Behringer RR, Renfree MB (2003) Expression of DMRT1 in the mammalian ovary and testis – from marsupials to mice. Cytogenet Genome Res 101:229–236.

    Article  PubMed  CAS  Google Scholar 

  • Pask AJ, Whitworth DJ, Mao C-A, et al. (2004) Marsupial anti-Müllerian hormone gene structure regulatory elements and expression. Biol Reprod 70:160–167.

    Article  PubMed  CAS  Google Scholar 

  • Pask AJ, Paplinska JZ, Shaw G, Graves JAM, Renfree MB (2007) Marsupial WT1 has a novel isoform and is expressed in both somatic and germ cells in the developing ovary and testis. Sex Dev 1:169–180.

    Article  PubMed  CAS  Google Scholar 

  • Ramsey M, Crews D (2009) Steroid signaling and temperature-dependent sex determination-Reviewing the evidence for early action of estrogen during ovarian determination in turtles. Semin Cell Dev Biol 20:283–292.

    Article  PubMed  CAS  Google Scholar 

  • Raymond CS, Shamu CE, Shen MM, et al. (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695.

    Article  PubMed  CAS  Google Scholar 

  • Raymond CS, Parker ED, Kettlewell JR (1999a) A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum molec Genet 8:989–996.

    Article  PubMed  CAS  Google Scholar 

  • Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D (1999b) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215:208–220.

    Article  PubMed  CAS  Google Scholar 

  • Renfree MB (1973) The composition of fetal fluids of the marsupial Macropus eugenii. Dev Biol 33:62–79.

    Article  PubMed  CAS  Google Scholar 

  • Renfree MB (1981) Marsupials: alternative mammals. Nature 293:100–101.

    Article  PubMed  CAS  Google Scholar 

  • Renfree MB (1983) Marsupial reproduction: the choice between placentation and lactation. In: Finn CA (ed) Oxford Reviews of Reproductive Biology, Vol 5. Oxford University Press, New York, pp. 1–29.

    Google Scholar 

  • Renfree MB (1992) The role of genes and hormones in marsupial sexual differentiation. J Zool Lond 226:165–173.

    Google Scholar 

  • Renfree MB (1993) Ontogeny genetic control and phylogeny of female reproduction in monotreme and therian mammals. In: Szalay FS Novacek JJ McKenna MC (eds) Mammal Phylogeny. Springer, New York, pp. 4–20.

    Chapter  Google Scholar 

  • Renfree MB, Lewis AM (1996) Cleavage in vivo and in vitro in the marsupial Macropus eugenii. Reprod Fertil Dev 8:725–742.

    Article  PubMed  CAS  Google Scholar 

  • Renfree MB, Short RV (1988) Sex determination in marsupials: evidence for a marsupial-eutherian dichotomy. Phil Trans R Soc Lond B 322:41–54.

    Article  CAS  Google Scholar 

  • Renfree MB, Tyndale-Biscoe CH (1973) Intrauterine development after diapause in the marsupial Macropus eugenii. Devl Biol 32:28–40.

    Article  CAS  Google Scholar 

  • Renfree MB, Tyndale-Biscoe CH (1978) Manipulation of marsupial embryos and pouch young. In: Daniel JC (ed) Methods of Mammalian Reproduction, Academic Press, pp. 307–331.

    Google Scholar 

  • Renfree MB, Flint AP, Green SW, Heap RB (1984) Ovarian steroid metabolism and oestrogens in the corpus luteum of the tammar wallaby. J Endocrinol 101:231–240.

    Article  PubMed  CAS  Google Scholar 

  • Renfree MB, Harry JL, Shaw G (1995) The marsupial male: a role model for sexual development. Phil Trans R Soc Lond B 350:243–251.

    Article  CAS  Google Scholar 

  • Renfree MB, O WS, Short RV, Shaw G (1996) Sexual differentiation of the urogenital system of the fetal and neonatal tammar wallaby Macropus eugenii. Anat Embryol 194: 111–134.

    Article  PubMed  CAS  Google Scholar 

  • Renfree MB, Coveney D, Shaw G (2001) The influence of estrogen on the developing male marsupial. Reprod Fertil Dev 13:231–240.

    Article  PubMed  CAS  Google Scholar 

  • Ricci M, Breed WG (2005) Morphogenesis of the fibrous sheath in the marsupial spermatozoon. J Anat 207:155–164.

    Article  PubMed  CAS  Google Scholar 

  • Russell AJ, Gilmore DP, Mackay S, Ullmann SL, Baker PJ, Payne AP (2003) The role of androgens in development of the scrotum of the grey short-tailed Brazilian opossum (Monodelphis domestica). Anat Embryol (Berl) 206:381–389.

    CAS  Google Scholar 

  • Schöler HR, Dressler GR, Balling R, Rohdewohld R, Gruss P (1990) Oct-4: a germline-specific transcription factor mapping to the mouse t-complex. EMBO J 9:2185–2195.

    PubMed  Google Scholar 

  • Sekido R, Lovell-Badge R (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930–9344.

    Article  PubMed  CAS  Google Scholar 

  • Selwood L (1986) Cleavage in vitro following destruction of some blastomeres in the marsupial Antechinus stuartii (Macleay). J Embryol Exp Morphol 92:71–84.

    PubMed  CAS  Google Scholar 

  • Selwood L (1992) Mechanisms underlying the development of pattern in marsupial embryos. Curr Top Dev Biol 27:175–233.

    Article  PubMed  CAS  Google Scholar 

  • Selwood L (2000) Mechanisms for pattern formation leading to axis formation and lineage allocation in mammals: a marsupial perspective. Reproduction 121:677–683.

    Article  Google Scholar 

  • Selwood L, Robinson ES, Pedersen RA, Vandeberg JL (1997) Development in vitro of Marsupials: a comparative review of species and a timetable of cleavage and early blastocyst stages of development in Monodelphis domestica. Int J Dev Biol 41:397–410.

    PubMed  CAS  Google Scholar 

  • Setchell BBP (1977) Reproduction in male marsupials. In: Stonehouse B Gilmorepp D (eds) The Biology of Marsupials. Macmillan, London, pp. 411–457.

    Google Scholar 

  • Sharman GB, Robinson ES, Walton SM, Berger RJ (1970) Sex chromosomes and reproductive anatomy of some intersexual marsupials. J Reprod Fertil 21:57–68.

    Article  PubMed  CAS  Google Scholar 

  • Sharman GB, Hughes RL, Cooper DW (1990) The chromosomal basis of sex differentiation in marsupials. Aust J Zool 37:443–450.

    Google Scholar 

  • Shaw G, Renfree MB, Short RV, O WS (1988) Experimental manipulation of sexual differentiation in wallaby pouch young treated with exogenous steroids. Development 104:689–701.

    PubMed  CAS  Google Scholar 

  • Shaw G, Renfree MB, Short RV (1990) Primary genetic control of sexual differentiation in marsupials. Aust J Zool 37:443–450.

    Google Scholar 

  • Shaw G, Gehring HM, Bell EC (1999) Production of prostaglandin f2alpha and its metabolite by endometrium and yolk sac placenta in late gestation in the tammar wallaby Macropus Eugenii. Biol Reprod 60:611–614.

    Article  PubMed  CAS  Google Scholar 

  • Shaw G, Renfree MB, Leihy MW, Shackleton CHL, Roitman E, Wilson JD (2000) Prostate formation in a marsupial is mediated by the testicular androgen 5α-androstane-3α, 17β-diol. Proc Natl Acad Sci USA 97:12256–12259.

    Article  PubMed  CAS  Google Scholar 

  • Short RV (2003) The magic and mystery of the oocyte: ex ovo omnia. In: Trounson AO Gosden RG (eds) The Biology and Pathology of the Oocyte. Cambridge University Press, New York.

    Google Scholar 

  • Sidhu KS, Mate KE, Molinia FC, Rodger JC (1999) Induction of thumbtack sperm during coculture with oviduct epithelial cell monolayers in a marsupial the brushtail possum (Trichosurus vulpecula). Biol Reprod 61:1356–1361.

    Article  PubMed  CAS  Google Scholar 

  • Sidhu KS, Mate KE, Gunasekera T, et al. (2004) A flow cytometric assay for global estimation of tyrosine phosphorylation associated with capacitation of spermatozoa from two marsupial species the tammar wallaby (Macropus eugenii) and the brushtail possum (Trichosurus vulpecula). Reproduction 127:95–103.

    Article  PubMed  CAS  Google Scholar 

  • Sinclair AH, Berta P, Palmer MS, et al. (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA binding motif. Nature 346:240–244.

    Article  PubMed  CAS  Google Scholar 

  • Sistina Y, Lin M, Mate KE, Robinson ES, Rodger JC (1993) The unique stability of the marsupial sperm acrosomal membranes examined by unprotected freeze-thawing and treatment with the detergent Triton X-100. Reprod Fertil Dev 5:1–14.

    Article  PubMed  CAS  Google Scholar 

  • Smith CA, Roeszler KN, Ohnesorg T, et al. (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267–271.

    Article  PubMed  CAS  Google Scholar 

  • Smith KK (2006) Craniofacial development in marsupial mammals: developmental origins of evolutionary change. Dev Dyn 235:1181–1193.

    Article  PubMed  Google Scholar 

  • Sonea IM, Iqbal J, Prins GS, Jacobson CD (1997) Ontogeny of androgen receptor-like immunoreactivity in the reproductive tract of male Monodelphis domestica. Biol Reprod 56:852–860.

    Article  PubMed  CAS  Google Scholar 

  • Spotila L, Spotila JR, Hall SE (1998) Sequence and expression analysis of WT-1 and SOX9 in the red-eared slider turtle Trachemys scripta. J Exp Zool 281:417–427.

    Article  PubMed  CAS  Google Scholar 

  • Takamatsu N, Kanda H, Ito M, Yamashita A, Yamashita S, Shiba T (1997) Rainbow trout SOX9: cDNA cloning gene structure and expression. Gene 202:167–170.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka SS, Yamaguchi YL, Tsoi B, Lickert H, Tam PP (2005) IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev Cell 9:745–756.

    Article  PubMed  CAS  Google Scholar 

  • Temple-Smith PD (1994) Comparative structure and function of marsupial spermatozoa. Reprod Fertil Dev 6:421–435.

    Article  PubMed  CAS  Google Scholar 

  • Temple-Smith PD, Bedford JM (1976) The features of sperm maturation in the epididymis of a marsupial the brushtailed possum Trichosurus vulpecula. Am J Anat 147:471–499.

    Article  PubMed  CAS  Google Scholar 

  • Trott JF, Simpson KJ, Moyle RL, et al. (2003) Maternal regulation of milk composition milk production and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biol Reprod 68:929–936.

    Article  PubMed  CAS  Google Scholar 

  • Turner RM, Johnson LR, Haig-Ladewig L, Gerton GL, Moss SB (1998) An X-linked gene encodes a major human sperm fibrous sheath protein hAKAP82 Genomic organization protein kinase A-RII binding and distribution of the precursor in the sperm tail. J Biol Chem 273: 32135–32141.

    Article  PubMed  CAS  Google Scholar 

  • Tyndale-Biscoe CH, Janssens PA (eds) (1988) The Developing Marsupial. Models for Biomedical Research. Springer, Berlin.

    Google Scholar 

  • Tyndale-Biscoe H, Renfree M (1987) Reproductive Physiology of Marsupials. Cambridge University Press, Cambridge, 476 pp.

    Book  Google Scholar 

  • Ullmann SL, Shaw G, Alcorn GT, Renfree MB (1997) Migration of primordial germ cells to the developing gonadal ridges in the tammar wallaby Macropus eugenii. J Reprod Fertil 110: 135–143.

    Article  PubMed  CAS  Google Scholar 

  • Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397:405–409.

    Article  PubMed  CAS  Google Scholar 

  • Vanmontfort D, Fidler AE, Heath DA, et al. (1998) cDNA sequence analysis gene expression and protein localisation of the inhibin alpha-subunit of Australian brushtail possum (Trichosurus vulpecula). J Mol Endocrinol 21:141–152.

    Article  PubMed  CAS  Google Scholar 

  • Vernet N, Dennefeld C, Rochette-Egly C, et al. (2006) Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147:96–110.

    Article  PubMed  CAS  Google Scholar 

  • Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, Jameson JL (2003) Sox3 is required for gonadal function but not sex determination in males and females. Mol Cell Biol 23:8084–8091.

    Article  PubMed  CAS  Google Scholar 

  • Western PS, Harry JL, Graves JAM, Sinclair AH (1999) Temperature dependent sex determination: upregulation of SOX9 expression after commitment to male development. Dev Dyn 214: 171–177.

    Article  PubMed  CAS  Google Scholar 

  • Whale LJ, Eckery DC, Juengel JL (2003) Determination of steroidogenic potential of ovarian cells of the brushtail possum (Trichosurus vulpecula). Biol Reprod 69:947–958.

    Article  PubMed  CAS  Google Scholar 

  • Whitworth DJ, Shaw G, Renfree MB (1996) Gonadal sex reversal of the developing marsupial ovary in vivo and in vitro. Development 122:4057–4063.

    PubMed  CAS  Google Scholar 

  • Whitworth DJ, Shaw G, Renfree MB (1997) Müllerian duct regression in a marsupial the tammar wallaby. Anat Embryol 196:39–46.

    Article  PubMed  CAS  Google Scholar 

  • Wilson JD, Leihy MW, Shaw G, Renfree MB (2003) Unsolved problems in male physiology: studies in a marsupial. Mol Cell Endocrinol 211:33–36.

    Article  PubMed  CAS  Google Scholar 

  • Whitworth DJ, Pask AJ, Shaw G, Marshall Graves JA, Behringer RR, Renfree MB (2001) Characterization of steroidogenic factor 1 during sexual differentiation in a marsupial. Gene 277:209–219.

    Article  PubMed  CAS  Google Scholar 

  • Wilson JD, Shaw G, Renfree MB, Auchus RJ, Leihy MW, Eckery DC (2005) Ontogeny and pathway of formation of 5alpha-androstane-3alpha, 17beta-diol in the testes of the immature brushtail possum Trichosurus vulpecula. Reprod Fertil Dev 17:603–609.

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Pask AJ, Shaw G, Renfree MB (2006) Differential expression of WNT4 in testicular and ovarian development in a marsupial. BMC Dev Biol 6:44.

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Pask AJ, Shaw G, Renfree MB (2009) Comparative analysis of the mammalian WNT4 promoter. BMC Genomics 10:416.

    Article  PubMed  CAS  Google Scholar 

  • Zanaria E, Muscatelli F, Bardoni B, et al. (1994) An unusual member of the nuclear hormone receptor super family responsible for X-linked adrenal hypoplasia congenita. Nature 372: 635–641.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, ARC Centre of Excellence for Kangaroo Genomics, The University of Melbourne, Melbourne, VIC, 3010, Australia

    Andrew J. Pask & Marilyn B. Renfree

  2. Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT, 06269, USA

    Andrew J. Pask

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  1. Andrew J. Pask
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  2. Marilyn B. Renfree
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Correspondence to Andrew J. Pask .

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Editors and Affiliations

  1. , Ecology, Evolution&Genetics, The Austral, ARC Centre for Excellence for Kangaroo G, Research School of Biology, building 46, Canberra ACT, 0200, Australia

    Janine E. Deakin

  2. , Ecology, Evolution&Genetics, The Austral, ARC Centre for Excellence for Kangaroo G, Research School of Biology, building 46, Canberra ACT, 0200, Australia

    Paul D. Waters

  3. , Ecology, Evolution and Genetics, ARC Centre of Excellence for Kangaroo Ge, Buidling 46, Canberra ACT, 0200, Australia

    Jennifer A. Marshall Graves

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Pask, A.J., Renfree, M.B. (2010). Molecular Regulation of Marsupial Reproduction and Development. In: Deakin, J., Waters, P., Marshall Graves, J. (eds) Marsupial Genetics and Genomics. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9023-2_14

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