Retinoic acid, meiosis and germ cell fate in mammals

Development

Volumn 134, Issue 19, 2007, Pages 3401-3411

  Bowles, Josephine ^a   Koopman, Peter ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; OCTAMER TRANSCRIPTION FACTOR 4; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RECEPTOR BETA; RETINOIC ACID RECEPTOR GAMMA; RETINOID X RECEPTOR ALPHA; RETINOID X RECEPTOR BETA; RETINOID X RECEPTOR GAMMA; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1;

CELL FATE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; COMPLEX FORMATION; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EYE DEVELOPMENT; GAMETOGENESIS; GENE EXPRESSION; GERM CELL; GONAD DEVELOPMENT; HUMAN; MEIOSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OOCYTE DEVELOPMENT; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PUBERTY; REVIEW; SEX DETERMINATION; SIGNAL TRANSDUCTION; SPERMATOCYTE; SPERMATOGENESIS; TESTIS DEVELOPMENT;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; GERM CELLS; HUMANS; MALE; MEIOSIS; MICE; MODELS, BIOLOGICAL; SEX DIFFERENTIATION; SEXUAL MATURATION; TESTIS; TRETINOIN; UROGENITAL SYSTEM;

MAMMALIA;

EID: 35648935410     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.001107     Document Type: Review

References (112)

1. Amleh, A., Smith, L., Chen, H. and Taketo, T. (2000). Both nuclear and cytoplasmic components are defective in oocytes of the B6.Y(TIR) sex-reversed female mouse. Dev. Biol. 219, 277-286.
2. Baltus, A. E., Menke, D. B., Hu, Y.-C., Goodheart, M. L., Carpenter, A. E., de Rooij, D. G. and Page, D. C. (2006). In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet. 38, 1430-1434.
3. Bouillet, P., Qulad-Abdelghani, M., Vicaire, S., Garnier, J. M., Schuhbaur, B., Dolle, P. and Chambon, P. (1995). Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel mouse gene, Stra1 (mouse LERK-2/Eplg2). Dev. Biol. 170, 420-433.
4. Boulogne, B., Levacher, C., Durand, P. and Habert, R. (1999). Retinoic acid receptors and retinoid X receptors in the rat testis during fetal and postnatal development: immunolocalization and implication in the control of the number of gonocytes. Biol. Reprod. 61, 1548-1557.
5. Bowles, J., Bullejos, M. and Koopman, P. (2000). A subtractive gene expression screen suggests a role for vanin-1 in testis development in mice. Genesis 27, 124-135.
6. Bowles, J., Knight D., Smith, C., Wilhelm, D., Richman, J. M., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M. J., Rossant, J. et al. (2006). Sex-specific regulation of retinoic acid levels in developing mouse gonads determines germ cell fate. Science 312, 596-600.
7. Bradbury, M. W. (1983). Functional capacity of sex-reversed (XX, Sxr/+) mouse germ cells as shown by progeny derived from XX, Sxr/+ oocytes of a female chimera. J. Exp. Zool. 226, 315-320.
8. Buehr, M., Gu, S. and McLaren, A. (1993). Mesonephric contribution to testis differentiation in the fetal mouse. Development 117, 273-281.
9. Bullejos, M. and Koopman, P. (2004). Germ cells enter meiosis in a rostrocaudal wave during development of the mouse ovary. Mol. Reprod. Dev. 68, 422-428.
10. Burgoyne, P. S. (1987). The role of the mammalian Y chromosome in spermatogeness. Dev. Suppl. 101, 133-141.
11. Byskov, A. G. (1974). Does the rete ovarii act as a trigger for the onset of meiosis? Nature 252, 396-397.
12. Byskov, A. G. (1975). The role of the rete ovarii in meiosis and follicle formation in the cat, mink and ferret. J. Reprod. Fertil. 45, 201-209.
13. Byskov, A. G. (1978a). Regulation of initiation of meiosis in fetal gonads. Int. J. Androl. Suppl. 2, 29-38.
14. Byskov, A. G. (1978b). The anatomy and ultrastructure of the rele system in the fetal mouse ovary. Biol. Reprod. 19, 720-735.
15. Byskov, A. G. (1978c), The meiosis-inducing interaction between germ cells and rete cells in the fetal mouse gonad. Ann. Biol. Anim. Biochim. Biophys. 18, 327-334.
16. Byskov, A. G. (1986). Differentiation of mammalian embryonic gonad. Physiol. Rev. 66, 71-117.
17. Byskov, A. G. and Saxen, L. (1976). Induction of meiosis in fetal mouse testis in vitro. Dev Biol. 52, 193-200.
18. Byskov, A. G., Fenger, M., Westergaard, L. and Anderson, C. Y. (1993). Forskolin and the meiosis inducing substance synergistically initiate meiosis in fetal male germ cells. Mol. Reprod. Dev. 34, 47-52.
19. Byskov, A. G., Andersen, C. Y., Nordholm, L., Thogersen, H., Guoliang, X., Wassmann, O., Andersen, J. V., Guddal, E. and Roed, T. (1995), Chemical structure of sterols that activate oocyte meiosis. Nature 374, 559-562.
20. Byskov, A. G., Baltsen, M. and Andersen, C. Y. (1998). Meioisis-activating sterols: background, discovery, and possible use. J. Mol. Med. 76, 818-823.
21. Chambon, P. (1996). A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954.
22. Chiba, H., Clifford, J., Metzger, D. and Chambon, P. (1997). Distinct retinoic X receptor-retinoic acid receptor heterodimers are differentially involved in the control of expression of retinoic target genes in F9 embryonal carcinoma cells. Mol. Cell. Biol. 17, 3013-3020.
23. Chuma, S. and Nakatsuji, N. (2001). Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev. Biol. 229, 468-479.
24. Deltour, L., Haselbeck, R. J., Ang, H. L. and Duester, G. (1997). Localization of class I and class IV alcohol dehydrogenases in mouse testis and epididymis: potential retinol dehydrogenases for endogenous retinoic acid synthesis. Biol. Reprod. 56, 102-109.
25. Di Carlo, A. D., Travia, G. and De Felici, M. (2000). The meiotic specific synaptonemal complex protein SCP3 is expressed by female and male primordial germ cells of the mouse embryo. Int. J. Dev. Biol. 44, 241-244.
26. Donovan, P. J., Stott, D., Cairns, L. A., Heasman, J. and Wylie, C. C. (1986). Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44, 831-838.
27. Evans, E. P., Ford, C. E. and Lyon, M. F. (1977). Direct evidence of the capacity of germ cell in the mouse to become an oocyte. Nature 267, 430-431.
28. Farini, D., La Sala, G., Tedesco, M. and De Felici, M. (2007). Chemoattractant action and molecular signaling pathways of Kit ligand on mouse primordial germ cells. Dev. Biol. 306, 572-583.
29. Francavilla, S. and Zamboni, L. (1985). Differentiation of mouse ectopic germinal cells in intra- and perigonadal locations. J. Exp. Zool. 233, 101-109.
30. Fuchs, E. and Green, H. (1981). Regulation of terminal differentiaiton of cultured human keratinocytes by vitamin A. Cell 25, 617-625.
31. Fuhrmann, G., Chung, A. C., Jackson, K. J., Hummelke, G., Baniahmad, A., Sutter, J., Sylvester, I., Scholer, H. R. and Cooney, A. J. (2001). Mouse germline restriction of Oct4 expression by germ cell nuclear factor. Dev. Cell 1, 377-387.
32. Ghyselinck, N. B., Vernet, N., Dennefeld, C., Giese, N., Nau, H., Chambon, P., Viville, S. and Mark, M. (2006). Retinoids and spermatogenesis: Lessons from mutant mice lacking the plasma retinol binding protein. Dev. Dyn. 235, 1608-1622.
33. Ginsburg, M., Snow, M. H. and McLaren, A. (1990). Primordial germ cells in the mouse embryo during gastrulation. Development 110, 521-528.
34. Grinsted, J. and Byskov, A. G. (1981). Meiosis-inducing and meiosis-preventing substances in human male reproductive organs. Fertil. Steril. 35, 199-204.
35. Grinsted, J., Byskov, A. G. and Andreasen, M. R. (1979). Induction of meiosis in fetal mouse testis in vitro by rete testis tissue from pubertal mice and bulls. J. Reprod. Fertil. 56, 653-656.
36. Gu, P., LeMenuet, D., Chung, A. C., Mancini, M., Wheeler, D. A. and Cooney, A. J. (2005). Orphan nuclear receptor GCNF is required for the repression of pluripotency genes during retinoic acid-induced embryonic stem cell differentiation. Mol. Cell. Biol. 25, 8507-8519.
37. Hernandez, R. E., Purzke, A. P., Myers, J. P., Margaretha, L. and Moens, C. B. (2007). Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 134, 177-187.
38. Hilscher, B., Hilscher, W., Bulthoff-Ohnolz, B., Kramer, U., Birke, A., Pelzer H. and Gauss, G. (1974). Kinetics of gemetogenesis. I. Comparative histological and autoradiographic studies of oocytes and transitional prospermatogonia during oogenesis and prespermatogenesis. Cell Tissue Res. 154, 443-470.
39. Horton, C. and Maden, M. (11995). Endogenous distribution of retinoids during normal development and teratogeness in the mouse embryo. Dev. Dyn. 202, 312-323.
40. Huang, H. F. S. and Hembree, W. C. (1979). Spermatogenic response to Vitamin A in Vitamin A deficient rats. Biol. Reprod. 21, 891-904.
41. Karl, J. and Capel, B. (1995). Three-dimensional structure of the developing mouse genital ridge. Philos. Trans. R. Soc. Lond. B Biol. Sci. 350, 235-242.
42. Kehler, J., Tolkunova, E., Koschorz, B., Pesce, M., Gentile, L., Boiani, M., Lomeli, H., Nagy, A., McLaughlin, K. J., Scholer, H. et al. (2004). Oct4 is required for primordial germ cell survival. EMBO Rep. 5, 1078-1083.
43. Koubova, J., Mencke, D. B., Zhou, Q., Capel, B., Griswold, M. D. and Page, D. C. (2006). Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl. Acad. Sci. USA 103, 2474-2479.
44. Lawson, K. A. and Hage, W. J. (1994). Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182, 84-91.
45. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright C. V., Korving, J. P. and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436.
46. Li, H. and Kim, K. H. (2004). Retinoic acid inhibits rat XY gonad development by blocking mesonephric cell migration and decreasing the number of gonocytes. Biol. Reprod. 70, 687-693.
47. Livera, G., Rouiller-Fabre, V., Valla, J. and Habert, R. (2000). Effects of retinoids on the meiosis in the fetal rat ovary in culture. Mol. Cell. Endocrinol. 165, 225-231.
48. MacLean, G., Abu-Abed, S., Dolle, P., Tahayato, A., Chambon, P. and Petkovich, M. (2001). Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 107, 195-201.
49. MacLean, G., Li, H., Metzger, D., Chambon, P. and Petkovich, M. (2007). Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology doi:10.1210/en.2007-0492.
50. Mark, M., Ghyselinck, N. B. and Chambon, P. (2006). Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 46, 451-480.
51. Matsui, Y. and Hayashi, K. (2007). Epigenetic regulation for the induction of meiosis. Cell. Mol. Life Sci. 64, 257-262.
52. McCaffery, P., Wagner, E., O'Neil, J., Petkovich, M. and Drager, U. C. (1999). Dorsal and ventral retinal territories defined by retinoic acid synthesis, breakdown and nuclear receptor expression. Mech. Dev. 82, 119-130.
53. McCarthy, P. T. and Cerecedo, L. R. (1952). Vitamin A deficiency in the mouse. J. Nutr. 46, 361-376.
54. McLaren, A. (1981). The fate of germ cells in the testis of fetal Sex-reversed mice. J. Reprod. Fertil. 61, 461-467.
55. McLaren, A. (1983). Studies on mouse germ cells inside and outside the gonad. J. Exp. Zool. 228, 167-171.
56. McLaren, A. (1984). Meiosis and differentiation of mouse germ cells. In Controlling Events in Meiosis, Thirty-eighth Symposium of the Society of Experimental Biology (ed. C. W. Evans and H. G. Dickinson), pp. 1-23. Cambridge: Company of Biologists.
57. McLaren, A. (1991). Development of the mammalian gonad: the fate of the supporting cell lineage. BioEssays 13, 151-156.
58. McLaren, A. (1995). Germ cells and germ cell sex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 350, 229-233.
59. McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1-15.
60. McLaren, A. and Buehr, M. (1990). Development of mouse germ cells in cultures of fetal gonads. Cell Differ. Dev. 31, 185-195.
61. McLaren, A. and Southee, D. (1997). Entry of mouse embryonic germ cells into meiosis. Dev. Biol. 187, 107-113.
62. Menke, D. B. and Page, D. C. (2002). Sexually dimorphic gene expression in the developing mouse gonad. Gene Expr. Patterns 2, 359-367.
63. Menke, D. B., Koubova, J. and Page, D. C. (2003). Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev. Biol. 262, 303-312.
64. Minucci, S., Botquin, V., Yeon, Y. I., Dey, A., Sylvester, I., Zand, D. J., Ohbo, K., Ozato, K. and Scholer, H. R. (1996). Retinoic acid-mediated down-regulation of Oct3/4 coincides with the loss of promoter occupancy in vivo. EMBO J. 15, 988-899.
65. Molyneaux, K. A., Stallock, J., Schaible, K. and Wylie, C. (2001). Time-lapse analysis of living mouse germ cell migration. Dev. Biol. 240, 488-498.
66. Molyneaux, K. A., Zinszner, H., Kunwar, P. S., Schaible, K., Stebler, J., Sunshine, M. J., O'Brien, W., Raz, E., Littman, D., Wylie, C. C. et al. (2003). The chemokine SDF1/CSCL12 and its receptor CXCR4 regulate mouse germ cellm igration and survival. Development 130, 4279-4286.
67. Morales, C. and Griswold, M. D. (1987). Retinol-incluced stage synchronization in seminiferous tubules of the rat. Endocrinology 121, 432-434.
68. Morita, Y. and Tilly, J. L. (1999). Aggregation of retinoic acid effects on fetal ovarian germ cell mitosis versus apoptosis by requirement for new macromolecular synthesis. Endocrinology 140, 2696-2703.
69. Nakatsuji, N. and Chuma, S. (2001). Differentiation of mouse primoridial germ cells into female or male germ cells. Int. J. Dev. Biol. 45, 541-548.
70. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Kiewe-Nebenius, D., Chambers, I., Scholer, H. and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391.
71. Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P. (1999). Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet. 21, 444-448.
72. Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S. C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A. et al. (2005). Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436, 207-213.
73. Ohkubo, Y., Shirayoshl, Y. and Nakatsuji, N. (1996). Autonomous regulation of proliferation and growth arrest in mouse primordial germ cells studied by mixed and clonal cultures. Exp. Cell Res. 222, 291-297.
74. Okamoto, K., Okazawa, H., Pkuda, A., Sakai, M., Muramatsu, M. and Hamada, H. (1990). A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 60, 461-472.
75. Oulad-Abdelghani, M., Bouillet, P., Decimo, D., Gansmuller, A., Heyberger, S., Dolle, P., Bronner, S., Lutz, Y. and Chambon, P. (1996). Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J. Cell Biol. 135, 469-477.
76. Palmer, S. J. and Burgoyne, P. S. (1991). In situ analysis of fetal, prepuberal and adult XXXXY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112, 265-268.
77. Park, E. H. and Taketo, T. (2003). Onset and progress of meiotic prophase in the oocytes in the B6. YTIR sex-reversed mouse ovary. Biol. Reprod. 69, 1879-1989.
78. Pesce, M., Wang, X., Wolgemuth, D. J. and Scholer, H. (1998). Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech. Dev. 71, 89-98.
79. Pikarsky, E., Sharir, H., Ben-Shushan, E. and Bergman, Y. (1994). Retinoic acid represses Oct-3/4 gene expression through several retinoic acid-responsive elements located in the promoter-enhancer region. Mol. Cell. Biol. 14, 1026-1038.
80. Pittman, D. L., Cobb, J., Schimenti, K. J., Wilson, L. A., Cooper, D. M., Brignull, E., Handel, M. A. and Schimenti, J. C. (1998). Meiotic prophase arrest with failure of chromsome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1, 697-705.
81. Romand, R., Dolle, P. and Hashino, E. (2006). Retinoid signaling in inner ear development. J. Neurobiol. 66, 687-704.
82. Rosner, M. H., Vigano, M. A., Ozato, K., Timmons, P. M., Poirier, F., Rigby, P. W. and Staudt L. M. (1990). A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345, 686-692.
83. Rossant, J., Zirngibl, R., Cado, D., Shago, M. and Giguere, V. (1991). Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5, 1333-1344.
84. Saitou, M., Barton, S. C. and Surani, M. A. (2002). A molecular programme for the specification of germ cell fate in mice. Nature 418, 293-300.
85. Sakai, Y., Luo, T., McCaffery, P., Hamada, H. and Drager, U. C. (2004). CYP26A1 and CYP26C1 cooperate in degrading retinoic acid within the equatorial retina during later eye development. Dev. Biol. 276, 143-157.
86. Scholer, H., Hatzopoulos, A., Balling, R., Suzuki, N. and Gruss, P. (1989). A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J. 8, 2543-2550.
87. Seki, Y., Hayashi, K., Itoh, K., Mizugaki, M., Saitou, M. and Matsui, Y. (2005). Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278, 440-458.
88. Speed, R. M. (1982). Meiosis in the foetal mouse ovary. I. An analysis at the light microscope level using surface-spreading. Chromosoma 85, 427-437.
89. DOM sex-reversed female mouse. Development 107, 95-105.
90. Tam, P. P. and Snow, M. H. (1981). Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morphol. 64, 133-147.
91. Tam, P. P. and Zhou, S. X. (1996). The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124-132.
92. Tanaka, S. S. and Matsui, Y. (2002). Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formaiton and differentiation of primordial germ cells. Mech. Dev. 119 Suppl. 1, S261-S267.
93. Thompson, J. N., Howell, J. M. and Pitt G. A. (1964). Vitamin A and reproduction in rats. Proc. R. Soc. Lond. B Biol. Sci. 159, 510-535.
94. Upadhyay, S. and Zamboni, L. (1982). Ectopic germ cells: natural model for the study of germ cell sexual differentiation. Proc Natl. Acad. Sci. USA 79, 6584-6588..
95. van Pelt, A. M. and de Rooij, D. G. (1990a). Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol. Reprod. 43, 363-367.
96. van Pelt A. M. and de Rooij, D. G. (1990b). The origin of the synchronization of the seminiferous epithelium in vitamin A-deficient rats after vitamin A replacement. Biol. Reprod. 42, 677-682.
97. van Pelt, A. M. and de Rooij, D. G. (1991). Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high replicate doses support the full development of spermatogenic cells. Endocrinology 128, 697-704.
98. Vermot, J., Garnier, J. M., Dierich, A., Niederreither, K., Harvey, R. P., Chambon, P. and Dolle, P. (2006). Conditional (loxP-flanked) allele for the gene encoding the retinoic acid-synthesizing enzyme retinaldehyde dehydrogenase 2 (RALDH2). Genesis 44, 155-158.
99. Vernet, N., Dennefeld, C., Rochette-Egly, C., Oulad-Abdelghani, M., Chambon, P., Ghyselinck, N. B. and Mark, M. (2006). Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147, 96-110.
100. Wang, J., Rao, S., Chu, J., Shen, X., Levasseur, D. N., Theunissen, T. W. and Orkin, S. H. (2006). A protein interaction network for pluripotency of embryonic stem cells. Nature 444, 364-368.
101. Westergaard, L., Byskov, A. G., Anderson, C. Y., Grinsted, J. and McNatty, K. P. (1984). Is resumption of meiosis in the human preovulatory oocyrte triggered by a meiosis-inducing substance (MIS) in the follicular fluid? Fertil. Steril. 41, 377-384.
102. Weston, A. D., Blumberg, B. and Underhill, T. M. (2003). Active repression by unliganded retinoid receptors in development: less is sometimes more. J. Cell Biol. 161, 223-228.
103. White, J. A., Ramshaw, H., Taimi, M., Stangle, W., Zhang, A., Everingham, S., Creighton, S., Tam, S. P., Jones, G. and Petkovich, M. (2000). Identification of the human cytochrome P450, P450RAI-2, which is predominantly expressed in the adult cerebellum and is responsible for all-transretinoic acid metabolism. Proc. Natl. Acad. Sci. USA 97, 6403-6408.
104. Yao, H. H., DiNapoli, L. and Capel, B. (2003). Meiotic germ cells antagonize mesonephric cell migration and testis cord formation in mouse gonads. Development 130, 5895-5902.
105. Yashiro, K., Zhao, X., Uehara, M., Yamashita, K., Nishijima, M., Nishino, J., Sakai, Y. and Hamada, H. (2004). Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell 6, 411-422.
106. Yeom, Y. I., Fuhrmann, G., Ovitt, C. E., Brehm, A., Ohbo, K., Gross, M., Hubner, K. and Scholer, H. R. (1996). Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122, 881-894.
107. Ying, Y. L., Liu, X. M., Marble, A., Lawson, K. A. and Zhao, G. Q. (2000). Requirement of Bmp8b for the generation of primoridal germ cells in the mouse. Mol. Endocrinol. 14, 1053-1063.
108. Yoshida, K., Kondoh, G., Matsuda, Y., Habu, T., Nishimune, Y. and Morita, T. (1998). The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell 1, 707-718.
109. Yuan, L., Liu, J., Zhao, J., Brundell, E., Daneholt, B. and Hoog, C. (2000). The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol. Cell 5, 73-83.
110. Yuan, L., Liu, J., Hoja, M., Wilbertz, J., Nordqvist, K. and Hoog, C. (2002). Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science 296, 1115-1118
111. Zamboni, L. and Upadhyay, S. (1983). Germ cell differentiation in mouse adrenal glands. J. Exp. Zool. 228, 173-193.
112. Zhai, Y., Higgins, D. and Napoli, J. L. (1997). Coexpression of the mRNAs encoding retinol dehydrogenase isozymes and cellular retinol-binding proteins. J. Cell. Physiol. 173, 36-43.