Gonadal mRNA expression levels of TGFβ superfamily signaling factors correspond with post-hatching morphological development in American alligators

Sexual Development

Volumn 4, Issue 1-2, 2010, Pages 62-72

  Moore, B C ^a   Hamlin, H J ^a   Botteri, N L ^a   Guillette Jr , L J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Activin; Alligator; Development; Follistatin; FOXL2; GDF9; Inhibin; Ovary; Testis

Indexed keywords

ALLIGATOR; ALLIGATOR MISSISSIPPIENSIS; VERTEBRATA;

MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA;

ALLIGATOR; ANIMAL; ARTICLE; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GONAD; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MALE; METABOLISM; OVARY; SIGNAL TRANSDUCTION; TESTIS; WESTERN HEMISPHERE;

ALLIGATORS AND CROCODILES; AMERICAS; ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; MALE; OVARY; RNA, MESSENGER; SIGNAL TRANSDUCTION; TESTIS; TRANSFORMING GROWTH FACTOR BETA;

EID: 77949873863     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000277934     Document Type: Article

References (81)

1. Barakat B, O'Connor AE, Gold E, de Kretser DM, Loveland KL: Inhibin, activin, follistatin and FSH serum levels and testicular production are highly modulated during the first spermatogenic wave in mice. Reproduction 136: 345-359 (2008).
2. Belaid B, Richard-Mercier N, Pieau C, Dorizzi M: Sex reversal and aromatase in the European pond turtle: treatment with letrozole after the thermosensitive period for sex determination. J Exp Zool 290: 490-497 (2001).
3. Billiar RB, Zachos NC, Burch MG, Albrecht ED, Pepe GJ: Up-regulation of alpha-inhibin expression in the fetal ovary of estrogen-suppressed baboons is associated with impaired fetal ovarian folliculogenesis. Biol Reprod 68: 1989-1996 (2003).
4. Bozkurt HH, Aktas A, Ulkay MB, Firat UB: Sertoli cell proliferation during the post hatching period in domestic fowl. J Vet Sci 8: 219-222 (2007).
5. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, et al: Postnatal regulation of germ cells by activin: The establishment of the initial follicle pool. Dev Biol 298: 132-148 (2006).
6. Britt KL, Saunders PK, McPherson SJ, Misso ML, Simpson ER, Findlay JK: Estrogen actions on follicle formation and early follicle development. Biol Reprod 71: 1712-1723 (2004).
7. Buzzard JJ, Farnworth PG, de Kretser DM, O'Connor AE, Wreford NG, Morrison JR: Proliferative phase Sertoli cells display a developmentally regulated response to activin in vitro. Endocrinology 144: 474-483 (2003).
8. Buzzard JJ, Loveland KL, O'Bryan MK, O'Connor AE, Bakker M, et al: Changes in circulating and testicular levels of inhibin A and B and activin A during postnatal development in the rat. Endocrinology 145: 3532-3541 (2004).
9. Callebaut M: [3H]Uridine incorporation during previtellogenesis and early vitellogenesis in oocytes of chick ( Gallus gallus ). J Embryol Exp Morphol 20: 169-174 (1968a).
10. Callebaut M: Extracorporal development of quail oocytes. Experientia 24: 1242-1243 (1968b).
11. Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF: Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 204: 373-384 (1998).
12. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME: Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 148: 3580-3590 (2007).
13. Da Silva SJM, Bayne RAL, Cambray N, Hartley PS, McNeilly AS, Anderson RA: Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation. Dev Biol 266: 334-345 (2004).
14. De Kretser DM, Buzzard JJ, Okuma Y, O'Connor AE, Hayashi T, et al: The role of activin, follistatin and inhibin in testicular physiology. Mol Cell Endocrinol 225: 57-64 (2004).
15. Dong JW, Albertini DF, Nishimori K, Kumar TR, Lu NF, Matzuk MM: Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383: 531-535 (1996).
16. Drummond AE: TGF beta signalling in the development of ovarian function. Cell Tissue Res 322: 107-115 (2005).
17. Drummond AE, Findlay JK, Ireland JJ: Animal models of inhibin action. Seminars In Reproductive Medicine 22: 243-252 (2004).
18. Edwards TM, Gunderson MP, Milnes MR, Guillette LJ: Gonadotropin-induced testosterone response in peripubertal male alligators. Gen Comp Endocrinol 135: 372-380 (2004).
19. Ethier JF, Findlay JK: Roles of activin and its signal transduction mechanisms in reproductive tissues. Reproduction 121: 667-675 (2001).
20. Ferguson MWJ, Joanen T: Temperature-dependent sex determination in Alligator mississippiensis . J Zool Lond 200: 143-177 (1983).
21. Fitzpatrick SL, Sindoni DM, Shughrue PJ, Lane MV, Merchenthaler IJ, Frail DE: Expression of growth differentiation factor-9 messenger ribonucleic acid in ovarian and nonovarian rodent and human tissues. Endocrinology 139: 2571-2578 (1998).
22. Forbes TR: Studies on the reproductive system of the alligator I. The effects of prolonged injections of pituitary whole gland extract in the immature alligator. Anat Rec 70: 113-137 (1937).
23. Forbes TR: The development of the reproductive system of a lizard, Anolis carolinensis . Am J Anat 98: 139-157 (1956).
24. Gonzalez-Moran G, Gonzalez del Pliego M, Pedernera E: Morphological-changes in the ovary of newly hatched chickens treated with chorionic-gonadotropin during embryonicdevelopment. Gen Comp Endocrinol 59: 162-167 (1985).
25. Govoroun MS, Pannetier M, Pailhoux E, Cocquet J, Brillard JP, et al: Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev Dyn 231: 859-870 (2004).
26. Gribbins KM, Elsey RM, Gist DH: Cytological evaluation of the germ cell development strategy within the testis of the American alligator, Alligator mississippiensis . Acta Zoologica 87: 59-69 (2006).
27. Guillette LJ, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR: Developmental abnormalities of the gonad and abnormal sex-hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect 102: 680-688 (1994).
28. Gunderson MP, Kohno S, Blumberg B, Iguchi T, Guillette LJ: Up-regulation of the alligator CYP3A77 gene by toxaphene and dexamethasone and its short term effect on plasma testosterone concentrations. Aquat Toxicol 78: 272-283 (2006).
29. Guo QX, Kumar TR, Woodruff T, Hadsell LA, DeMayo FJ, Matzuk MM: Overexpression of mouse follistatin causes reproductive defects in transgenic mice. Mol Endocrinol 12: 96-106 (1998).
30. Hudson QJ, Smith CA, Sinclair AH: Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Dev Dyn 233: 1052-1055 (2005).
31. Joanen T, McNease L: Reproductive Biology of the American Alligator in Southwest Louisiana; in Murphy JB, Collins JT (eds): Reproductive Biology and Disease of Captive Reptiles, pp 153-159 (Lawrence, Kansas 1980).
32. Johnson PA, Dickens MJ, Kent TR, Giles JR: Expression and function of growth differentiation factor-9 in an oviparous species, Gallus domesticus . Biol Reprod 72: 1095-1100 (2005).
33. Katsu Y, Bermudez DS, Braun EL, Helbing C, Miyagawa S, et al: Molecular cloning of the estrogen and progesterone receptors of the American alligator. Gen Comp Endocrinol 136: 122-133 (2004).
34. Kezele PR, Ague JM, Nilsson E, Skinner MK: Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 72: 241-255 (2005).
35. Kipp JJL, Kilen SM, Woodruff TK, Mayo KE: Activin regulates estrogen receptor gene expression in the mouse ovary. J Biol Chem 282: 36755-36765 (2007a).
36. Kipp JL, Kilen SM, Bristol-Gould S, Woodruff TK, Mayo KE: Neonatal exposure to estrogens suppresses activin expression and signaling in the mouse ovary. Endocrinology 148: 1968-1976 (2007b).
37. Kohno S, Bermudez DS, Katsu Y, Iguchi T, Guillette LJ: Gene expression patterns in juvenile American alligators ( Alligator mississippiensis ) exposed to environmental contaminants. Aquat Toxicol 88: 95-101 (2008).
38. Krishna TSR, Kong XP, Gary S, Burgers PM, Kuriyan J: Crystal-structure of the eukaryotic DNA-polymerase processivity factor Pcna. Cell 79: 1233-1243 (1994).
39. Kumar TR, Varani S, Wreford NG, Telfer NM, de Kretser DM, Matzuk MM: Male reproductive phenotypes in double mutant mice lacking both FSH beta and activin receptor IIA. Endocrinology 142: 3512-3518 (2001).
40. Lance VA: Alligator physiology and life history: The importance of temperature. Exp Gerontol 38: 801-805 (2003).
41. Licht P, Pearson AK: Effects of mammalian gonadotropins (FSH and LH) on testes of lizard Anolis carolinensis . Gen Comp Endocrinol 13: 367-381 (1969).
42. Loffler KA, Zarkower D, Koopman P: Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development. Endocrinology 144: 3237-3243 (2003).
43. Loveland KL, Dias V, Meachem S, Meyts ERD: The transforming growth factor-beta superfamily in early spermatogenesis: Potential relevance to testicular dysgenesis. Int J Androl 30: 377-384 (2007).
44. Matova N, Cooley L: Comparative aspects of animal oogenesis. Dev Biol 231: 291-320 (2001).
45. Mayo K, Jameson L, Woodruff TK: Eggs in the nest. Endocrinology 148: 3577-3579 (2007).
46. Meachem SJ, Nieschlag E, Simoni M: Inhibin B in male reproduction: Pathophysiology and clinical relevance. Eur J Endocrinol 145: 561-571 (2001).
47. Menke DB, Page DC: Sexually dimorphic gene expression in the developing mouse gonad. Gene Expr Patterns 2: 359-367 (2002).
48. Milnes MR, Bryan TA, Katsu Y, Kohno S, Moore BC, Iguchi T, Guillette LJ: Increased posthatching mortality and loss of sexually dimorphic gene expression in alligators ( Alligator mississippiensis ) from a contaminated environment. Biol Reprod 78: 932-938 (2008).
49. Moore BC, Hamlin HJ, Botteri NL, Lawler AN, Mathavan KK, Guillette LJ: Post-hatching development of Alligator mississippiensis ovary and testis. J Morphol DOI:10.1002/ jmor.10818.
50. Moore BC, Uribe-Aranzabal MC, Boggs ASP, Guillette LJ: Developmental morphology of the neonatal alligator ( Alligator mississippiensis ) ovary. J Morphol 269: 302-312 (2008).
51. Narbaitz R, Adler R: Submicroscopical observations on differentiation of chick gonads. J Embryol Exp Morphol 16: 41-47 (1966).
52. Narbaitz R, DeRobertis EM: Postnatal evolution of steroidogenic cells in chick ovary. Histochemie 15: 187-193 (1968).
53. Nicholls PK, Harrison CA, Gilchrist RB, Farnworth PG, Stanton PG: Growth differentiation factor 9 (GDF9) is a germ-cell regulator of Sertoli cell function. Endocrinology 150: 2481-2490 (2009).
54. Nitta H, Osawa Y, Bahr JM: Immunolocalization of steroidogenic cells in small follicles of the chicken ovary - anatomical arrangement and location of steroidogenic cells change during follicular development. Domest Anim Endocrinol 8: 587-594 (1991a).
55. Nitta H, Osawa Y, Bahr JM: Multiple steroidogenic cell-populations in the thecal layer of preovulatory follicles of the chicken ovary. Endocrinology 129: 2033-2040 (1991b).
56. Oktay K, Schenken RS, Nelson JF: Proliferating cell nuclear antigen marks the initiation of follicular-growth in the rat. Biol Reprod 53: 295-301 (1995).
57. Onagbesan OM, Safi M, Decuypere E, Bruggeman V: Developmental changes in inhibin alpha and inhibin/activin beta A and beta B mRNA levels in the gonads during posthatch prepubertal development of male and female chickens. Mol Reprod Dev 68: 319-326 (2004).
58. Oshima Y, Uno Y, Matsuda Y, Kobayashi T, Nakamura M: Molecular cloning and gene expression of FOXL2 in the frog Rana rugosa . Gen Comp Endocrinol 159: 170-177 (2008).
59. Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, et al: Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet 14: 2053-2062 (2005).
60. Ottolenghi C, Uda M, Crisponi L, Omari S, Cao A, Forabosco A, Schlessinger D: Determination and stability of sex. Bioessays 29: 15-25 (2007).
61. Pangas SA, Jorgez CJ, Tran M, Agno J, Li XH, et al: Intraovarian activins are required for female fertility. Mol Endocrinol 21: 2458-2471 (2007).
62. Pannetier M, Fabre S, Batista F, Kocer A, Renault L, et al: FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 36: 399-413 (2006).
63. Pepling ME: From primordial germ cell to primordial follicle: Mammalian female germ cell development. Genesis 44: 622-632 (2006).
64. Pepling ME, De Cuevas M, Spradling AC: Germline cysts: A conserved phase of germ cell development? Trends Cell Biol 9: 257-262 (1999).
65. Pieau C, Dorizzi M: Oestrogens and temperature-dependent sex determination in reptiles: All is in the gonads. J Endocrinol 181: 367-377 (2004).
66. Raivio T, Dunkel L: Inhibins in childhood and puberty. Best Pract Res Clin Endocrinol Metab 16: 43-52 (2002).
67. Ramaswam LS, Jacob D: Effect of testosterone propionate on urogenital organs of immature crocodile Crocodylus palustris Lesson. Experientia 21: 206 (1965).
68. Rhen T, Metzger K, Schroeder A, Woodward R: Expression of putative sex-determining genes during the thermosensitive period of gonad development in the snapping turtle, Chelydra serpentina . Sex Dev 1: 255-270 (2007).
69. Rooney AA, Crain DA, Woodward AR, Guillette LJ: Seasonal variation in plasma sex steroid concentrations in juvenile American alligators. Gen Comp Endocrinol 135: 25-34 (2004).
70. Schlatt S, Weinbauer GF: Immunohistochemical localization of proliferating cell nuclear antigen as a tool to study cell-proliferation in rodent and primate testes. Int J Androl 17: 214-222 (1994).
71. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier AC, Treier M: The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131: 933-942 (2004).
72. Smith CA, Elf PK, Lang JW, Joss JMP: Aromatase enzyme-activity during gonadal sexdifferentiation in alligator embryos. Differentiation 58: 281-290 (1995).
73. Trombly DJ, Woodruff TK, Mayo KE: Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 150: 1014-1024 (2009).
74. Uda M, Ottolenghi C, Deiana M, Kimber W, Forabosco A, et al: Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 13: 1171-1181 (2004).
75. Uhlenhaut NH, Treier M: Foxl2 - function in ovarian development. Mol Genet Metab 88: 225-234 (2006).
76. Uribe MCA, Guillette LJ: Oogenesis and ovarian histology of the American alligator Alligator mississippiensis . J Morphol 245: 225-240 (2000).
77. van Tienhoven A: Reproductive Physiology of Vertebrates (Cornell University Press, Ithaca 1983).
78. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, et al: Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with Ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 21: 712-725 (2007).
79. Yao HHC: The Pathway to Femaleness: Current knowledge on embryonic development of the ovary. Mol Cell Endocrinol 230: 87-93 (2005).
80. Yao HHC, Aardema J, Holthusen K: Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol Reprod 74: 978-983 (2006).
81. Yao HHC, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A, Capel B: Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn 230: 210-215 (2004).