Structural changes in gonadal basement membranes during sex differentiation in the frog Rana rugosa

Journal of Experimental Zoology Part A: Ecological Genetics and Physiology

Volumn 313 A, Issue 6, 2010, Pages 369-380

  Saotome, Kazuhiro ^a   Isomura, Tomoko ^a   Seki, Tatsunori ^b   Nakamura, Yoriko ^c   Nakamura, Masahisa ^a  

^a WASEDA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; BASEMENT MEMBRANE; CELL PROLIFERATION; CYTOLOGY; FROG; GONAD; HISTOLOGY; SEX DIFFERENTIATION;

ANIMALS; BASEMENT MEMBRANE; CELL PROLIFERATION; GONADS; RANIDAE; SEX DIFFERENTIATION;

ANURA; RANA RUGOSA;

EID: 77953500015     PISSN: 19325223     EISSN: 19325231     Source Type: Journal    
DOI: 10.1002/jez.607     Document Type: Article

References (45)

1. Abrahamson LV. 1992. Immunoelectron microscopic localization of laminin in rat ovarian follicles. Anat Rec 233:41-52.
2. Capel B, Albrecht KH, Washburn LL, Eicher EM. 1999. Migration of mesonephric cells into the mammalian gonad depends on Sry. Mech Dev 84:127-131.
3. Chung AE, Jaffe R, Freeman IL, Vergnes J-P, Braginski JE, Carlin B. 1979. Properties of a basement membrane-related glycoprotein synthesized in culture by a mouse embryonal carcinoma-derived cell line. Cell 16:277-287.
4. Davis CM, Papadopoulos V, Sommers CL, Kleinman HK, Dym M. 1990. Differential expression of extracellular matrix components in rat Sertoli cells. Biol Reprod 43:860-869.
5. Dickson C, Webster DR, Johnson H, Cecilia Millena A, Khan SA. 2002. Transforming growth factor-beta effects on morphology of immature rat Leydig cells. Mol Cell Endocrinol 195:65-77.
6. Fridmacher V, Locquet O, Magre S. 1992. Differential expression of acidic cytokeratins 18 and 19 during sexual differentiation of the rat gonad. Development 115:503-517.
7. Fridmacher V, Le Bert M, Guillou F, Magre S. 1995. Switch in the expression of the K19/K18 keratin genes as a very early evidence of testicular differentiation in the rat. Mech Dev 52:199-207.
8. Frojdman K, Pelliniemi LJ, Virtanen I. 1998. Differential distribution of type IV collagen chains in the developing rat testis and ovary. Differentiation 63:125-130.
9. Frojdman K, Miner JH, Sanes JR, Pelliniemi LJ, Virtanen I. 1999. Sex- specific localization of laminin a5 chain in the differentiating rat testis and ovary. Differentiation 64:151-159.
10. Jamil A, Magre S, Mazabraud A, Penrad-Mobayed M. 2008. Early aspects of gonadal sex differentiation in Xenopus tropicalis with reference to an antero-posterior gradient. J Exp Zool Part A Ecol Genet Physiol 309:127-137.
11. Hayes TB. 1998. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J Exp Zool 281:373-399.
12. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. 2007. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78:333-341.
13. Iwade R, Maruo K, Okada G, Nakamura M. 2008. Elevated expression of P450c17 (CYP17) during testicular formation in the frog. Gen Comp Endocrinol 155:79-87.
14. Kobayashi T. 2010. In vitro germ cell differentiation during sex differentiation in a teleost fish. Int J Dev Biol 54:105-111.
15. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y. 2004. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231:518-526.
16. Kobayashi T, Nagahama Y. 2009. Molecular aspects of gonadal differentiation in a teleost fish, the Nile tilapia. Sex Dev 3:108-117.
17. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. 1991. Male development of chromosomally female mice transgenic for Sry. Nature 351:117-211.
18. Lovell-Badge R. 1993. Sex determining gene expression during embryogenesis. Phil Trans R Soc Lond B 335:159-164.
19. 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.
20. Miura I, Ohtani H, Nakamura M, Ichikawa Y, Saitoh K. 1998. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol Biol Evol 15:1612-1619.
21. Nakamura M. 2009. Sex determination in amphobians. Semin Cell Dev Biol 20:271-282.
22. Nishioka M, Miura I, Saitoh K. 1993. Sex chromosomes of Rana rugosa with special reference to local differences in sex-determining mechanism. Sci Rep Lab Amphib Biol Horoshima Univ 12:55-81.
23. Ohtani H, Miura I, Ichikawa Y. 2003. Role of aromatase and androgen receptor expression in gonadal sex differentiation of ZW/ZZ-type frogs, Rana rugosa. Comp Biochem Physiol C Toxicol Pharmacol 134:215-225.
24. Oshima Y, Naruse K, Nakamura Y, Nakamura M. 2009. Sox3: a transcription factor for Cyp19 expression in the frog Rana rugosa. Gene 445:38-48.
25. Paranko J. 1987. Expression of type I and III collagen during morphogenesis of fetal rat testis and ovary. Anat Rec 219:91-101.
26. Pelliniemi LJ, Frojdman K. 2001. Structural and regulatory macro- molecules in sex differentiation of gonads. J Exp Zool 290: 523-528.
27. Pelliniemi LJ, Frojdman K, Sundstrom J, Pollanen P, Kuopio T. 1998. Cellular and molecular changes during sex differentiation of ermbryonic mammalian gonads. J Exp Zool 281:482-493.
28. Ramsey M, Crews D. 2009. Analyzing the coordinated gene network underlying temperature-dependent sex determination in reptiles. Semin Cell Dev Biol 20:283-292.
29. Richardson LL, Kleinman HK, Dym M. 1995. Basement membrane gene expression by Sertoli and peritubular myoid cells in vitro in the rat. Biol Reprod 52:320-330.
30. Sawada H, Esaki M. 2003. Electron microscopic observation of 137Cs- irradiated rat testis: production of basal laminae for germ cells, despite their absence. J Electron Microsc (Tokyo) 52:391-397.
31. Schmahl J, Eicher EM, Washburn LL, Capel B. 2000. Sry induces cell proliferation in the mouse gonad. Development 127:65-73.
32. Shimada K. 1998. Gene expression of steroidogenic enzymes in chicken embryonic gonads. J Exp Zool 281:450-456.
33. Shoemaker CM, 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 20:293-303.
34. Shumway W. 1940. Stages in the normal development of Rana pipiens. I. External form. Anat Rec 78:139-147.
35. Taylor AC, Kollros JJ. 1946. Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7-23.
36. Tilmann C, Capel B. 1999. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126:2883-2890.
37. Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin GR. 1979. Laminin-a glycoprotein from basement membranes. J Biol Chem 254:9933-9937.
38. Turner ME, Martin C, Martins AS, Dunmire J, Farkas J, Ely DL, Milsted A. 2007. Genomic and expression analysis of multiple Sry loci from a single Rattus norvegicus Y chromosome. BMC Genet 8:1-11.
39. Tzu J, Marinkovich MP. 2008. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int J Biochem Cell Biol 40:199-214.
40. Uno Y, Nishida C, Oshima Y, Yokoyama S, Miura I, Matsuda Y, Nakamura M. 2008. Comparative chromosome mapping of sex- linked genes and identification of sex chromosomal rearrangements in the Japanese wrinkled frog (Rana rugosa, Ranidae) with ZW and XY sex chromosome systems. Chromosome Res 16:637-647.
41. Wibbels T, Bull JJ, Crews D. 1991. Chronology and morphology of temperature-dependent sex determination. J Exp Zool 260: 371-381.
42. Yao HH, DiNapoli, Capel B. 2004. Cellular mechanisms of sex determination in the red-eared slider turtle, Trachemys scripta. Mech Dev 121:1393-1401.
43. Yokoyama S, Oshima Y, Tokita J, Suda M, Shinozuka T, Nakamura M. 2009. Androgen receptor of the frog Rana rugosa: molecular cloning and its characterization. J Exp Zool A Ecol Genet Physiol 311A:796-812.
44. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M. 2008. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105:2469-2474.
45. Zhao Y, Luck MR. 1995. Gene expression and protein distribution of collagen, fibronectin and laminin in bovine follicles and corpora lutea. J Reprod Fertil 104:115-123.