The mouse forkhead gene Foxc1 is required for primordial germ cell migration and antral follicle development

Developmental Biology

Volumn 290, Issue 2, 2006, Pages 447-458

  Mattiske, Deidre ^a   Kume, Tsutomu ^b   Hogan, Brigid L M ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Folliculogenesis; Forkhead; Gonad; Primordial germ cell; TGF

Indexed keywords

CELL MARKER; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL SPECIFICITY; EMBRYO; FEMALE; FOXC1 GENE; GENE EXPRESSION; GENE MUTATION; GONAD DEVELOPMENT; GRANULOSA CELL; KIDNEY CAPSULE; MESONEPHROS; MOUSE; MUTANT; NONHUMAN; OVARIECTOMY; OVARY; OVARY FOLLICLE DEVELOPMENT; OVIDUCT; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SOMATIC CELL; THECA CELL; TRANSPLANTATION;

ANIMALIA;

EID: 31544432542     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.12.007     Document Type: Article

References (80)

1. D. Accili, and K.C. Arden FoxOs at the crossroads of cellular metabolism, differentiation, and transformation Cell 117 2004 421 426
2. R. Anderson, R. Fassler, E. Georges-Labouesse, R.O. Hynes, B.L. Bader, J.A. Kreidberg, K. Schaible, J. Heasman, and C. Wylie Mouse primordial germ cells lacking beta1 integrins enter the germline but fail to migrate normally to the gonads Development 126 1999 1655 1664
3. M. Anttonen, I. Ketola, H. Parviainen, A.K. Pusa, and M. Heikinheimo FOG-2 and GATA-4 are coexpressed in the mouse ovary and can modulate mullerian-inhibiting substance expression Biol. Reprod. 68 2003 1333 1340
4. T. Ara, Y. Nakamura, T. Egawa, T. Sugiyama, K. Abe, T. Kishimoto, Y. Matsui, and T. Nagasawa Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1) Proc. Natl. Acad. Sci. U. S. A. 100 2003 5319 5323
5. R.R. Behringer The mullerian inhibitor and mammalian sexual development Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 350 1995 285 288 (discussion 289)
6. S. Bertuzzi, F.D. Porter, A. Pitts, M. Kumar, A. Agulnick, C. Wassif, and H. Westphal Characterization of Lhx9, a novel LIM/homeobox gene expressed by the pioneer neurons in the mouse cerebral cortex Mech. Dev. 81 1999 193 198
7. O.S. Birk, D.E. Casiano, C.A. Wassif, T. Cogliati, L. Zhao, Y. Zhao, A. Grinberg, S. Huang, J.A. Kreidberg, K.L. Parker, F.D. Porter, and H. Westphal The LIM homeobox gene Lhx9 is essential for mouse gonad formation Nature 403 2000 909 913
8. K. Block, A. Kardana, P. Igarashi, and H.S. Taylor In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing mullerian system FASEB J. 14 2000 1101 1108
9. C.W. Brown, D.E. Houston-Hawkins, T.K. Woodruff, and M.M. Matzuk Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions Nat. Genet. 25 2000 453 457
10. S.M. Chuva de Sousa Lopes, S. van den Driesche, R.L. Carvalho, J. Larsson, B. Eggen, M.A. Surani, and C.L. Mummery Altered primordial germ cell migration in the absence of transforming growth factor beta signaling via ALK5 Dev. Biol. 284 2005 194 203
11. P.J. Coffer, and B.M. Burgering Forkhead-box transcription factors and their role in the immune system Nat. Rev., Immunol. 4 2004 889 899
12. J.F. Couse, S.C. Hewitt, D.O. Bunch, M. Sar, V.R. Walker, B.J. Davis, and K.S. Korach Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta Science 286 1999 2328 2331
13. S.M. de Sousa Lopes, B.A. Roelen, R.M. Monteiro, R. Emmens, H.Y. Lin, E. Li, K.A. Lawson, and C.L. Mummery BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo Genes Dev. 18 2004 1838 1849
14. J. Dong, D.F. Albertini, K. Nishimori, T.R. Kumar, N. Lu, and M.M. Matzuk Growth differentiation factor-9 is required during early ovarian folliculogenesis Nature 383 1996 531 535
15. G.R. Dressler, U. Deutsch, K. Chowdhury, H.O. Nornes, and P. Gruss Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system Development 109 1990 787 795
16. A.E. Drummond TGFbeta signalling in the development of ovarian function Cell Tissue Res. 2005 (electronic publication ahead of print)
17. M.A. el-Fouly, B. Cook, M. Nekola, and A.V. Nalbandov Role of the ovum in follicular luteinization Endocrinology 87 1970 286 293
18. J.A. Elvin, C. Yan, P. Wang, K. Nishimori, and M.M. Matzuk Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary Mol. Endocrinol. 13 1999 1018 1034
19. J.K. Findlay, A.E. Drummond, M.L. Dyson, A.J. Baillie, D.M. Robertson, and J.F. Ethier Recruitment and development of the follicle; the roles of the transforming growth factor-beta superfamily Mol. Cell. Endocrinol. 191 2002 35 43
20. R.B. Gilchrist, L.J. Ritter, and D.T. Armstrong Oocyte-somatic cell interactions during follicle development in mammals Anim. Reprod. Sci. 82-82 2004 431 446
21. I. Godin, and C.C. Wylie TGF beta 1 inhibits proliferation and has a chemotropic effect on mouse primordial germ cells in culture Development 113 1991 1451 1457
22. M.C. Green The developmental effects of congenital hydrocephalus (ch) in the mouse Dev. Biol. 23 1970 585 608
23. X. Gueripel, M. Benahmed, and A. Gougeon Sequential gonadotropin treatment of immature mice leads to amplification of transforming growth factor beta action, via upregulation of receptor-type 1, Smad 2 and 4, and downregulation of Smad 6 Biol. Reprod. 70 2004 640 648
24. C.J. Guigon, N. Coudouel, S. Mazaud-Guittot, M.G. Forest, and S. Magre Follicular cells acquire sertoli cell characteristics after oocyte loss Endocrinology 146 2005 2992 3004
25. Q. Guo, T.R. Kumar, T. Woodruff, L.A. Hadsell, F.J. DeMayo, and M.M. Matzuk Overexpression of mouse follistatin causes reproductive defects in transgenic mice Mol. Endocrinol. 12 1998 96 106
26. A. Hacker, B. Capel, P. Goodfellow, and R. Lovell-Badge Expression of Sry, the mouse sex determining gene Development 121 1995 1603 1614
27. H. Hiemisch, G. Schutz, and K.H. Kaestner The mouse Fkh1/Mf1 gene: cDNA sequence, chromosomal localization and expression in adult tissues Gene 220 1998 77 82
28. B.L.M. Hogan, R. Beddinton, F. Constantini, and E. Lacy Manipulating the Mouse Embryo: A Laboratory Manual 1994 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
29. T. Hosaka, W.H. Biggs III, D. Tieu, A.D. Boyer, N.M. Varki, W.K. Cavenee, and K.C. Arden Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification Proc. Natl. Acad. Sci. U. S. A. 101 2004 2975 2980
30. J.L. Juengel, and K.P. McNatty The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development Hum. Reprod. Updat. 11 2005 143 160
31. M. Katoh, and M. Katoh Human FOX gene family Int. J. Oncol. 25 2004 1495 1500
32. G.M. Kidder, and A.A. Mhawi Gap junctions and ovarian folliculogenesis Reproduction 123 2002 613 620
33. A. Kobayashi, and R.R. Behringer Developmental genetics of the female reproductive tract in mammals Nat. Rev., Genet. 4 2003 969 980
34. T.R. Kumar, Y. Wang, and M.M. Matzuk Gonadotropins are essential modifier factors for gonadal tumor development in inhibin-deficient mice Endocrinology 137 1996 4210 4216
35. T.R. Kumar, G. Palapattu, P. Wang, T.K. Woodruff, I. Boime, M.C. Byrne, and M.M. Matzuk Transgenic models to study gonadotropin function: the role of follicle stimulating hormone in gonadal growth and tumorigenesis Mol. Endocrinol. 13 1999 851 865
36. T. Kume, K.Y. Deng, V. Winfrey, D.B. Gould, M.A. Walter, and B.L. Hogan The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus Cell 93 1998 985 996
37. T. Kume, K. Deng, and B.L. Hogan Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract Development 127 2000 1387 1395
38. K.A. Lantz, and K.H. Kaestner Winged helix transcription factors and pancreatic development Clin. Sci. (Lond.) 108 2005 195 204
39. K.A. Lawson, N.R. Dunn, B.A. Roelen, L.M. Zeinstra, A.M. Davis, C.V. Wright, J.P. Korving, and B.L. Hogan Bmp4 is required for the generation of primordial germ cells in the mouse embryo Genes Dev. 13 1999 424 436
40. O.J. Lehmann, J.C. Sowden, P. Carlsson, T. Jordan, and S.S. Bhattacharya Fox's in development and disease Trends Genet. 19 2003 339 344
41. X. Liu, K. Andoh, H. Yokota, J. Kobayashi, Y. Abe, K. Yamada, H. Mizunuma, and Y. Ibuki Effects of growth hormone, activin, and follistatin on the development of preantral follicle from immature female mice Endocrinology 139 1998 2342 2347
42. X. Liu, K. Andoh, Y. Abe, J. Kobayashi, K. Yamada, H. Mizunuma, and Y. Ibuki A comparative study on transforming growth factor beta and activin A for preantral follicles from adult, immature, and diethylstilbestrol primed immature mice Endocrinology 140 1999 2480 2485
43. K.A. Loffler, D. Zarkower, and P. Koopman Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development Endocrinology 144 2003 3237 3243
44. D. Mattiske, G. Shaw, and J.M. Shaw Influence of donor age on development of gonadal tissue from pouch young of the tammar wallaby, Macropus eugenii, after cryopreservation and xenografting into mice Reproduction 123 2002 143 153
45. M.M. Matzuk, M.J. Finegold, J.G. Su, A.J. Hsueh, and A. Bradley Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice Nature 360 1992 313 319
46. M.M. Matzuk, T.R. Kumar, and A. Bradley Different phenotypes for mice deficient in either activins or activin receptor type II Nature 374 1995 356 360
47. M.M. Matzuk, T.R. Kumar, A. Vassalli, J.R. Bickenbach, D.R. Roop, R. Jaenisch, and A. Bradley Functional analysis of activins during mammalian development Nature 374 1995 354 356
48. A. McLaren Primordial germ cells in the mouse Dev. Biol. 262 2003 1 15
49. H. Merchant Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study Dev. Biol. 44 1975 1 21
50. K. Molyneaux, and C. Wylie Primordial germ cell migration Int. J. Dev. Biol. 48 2004 537 544
51. K.A. Molyneaux, H. Zinszner, P.S. Kunwar, K. Schaible, J. Stebler, M.J. Sunshine, W. O'Brien, E. Raz, D. Littman, C. Wylie, and R. Lehmann The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival Development 130 2003 4279 4286
52. K.A. Molyneaux, Y. Wang, K. Schaible, and C. Wylie Transcriptional profiling identifies genes differentially expressed during and after migration in murine primordial germ cells Gene Expression Patterns 4 2004 167 181
53. A. Okada, Y. Ohta, S.L. Brody, H. Watanabe, A. Krust, P. Chambon, and T. Iguchi Role of foxj1 and estrogen receptor alpha in ciliated epithelial cell differentiation of the neonatal oviduct J. Mol. Endocrinol. 32 2004 615 625
54. C. Ottolenghi, S. Omari, J.E. Garcia-Ortiz, M. Uda, L. Crisponi, A. Forabosco, G. Pilia, and D. Schlessinger Foxl2 is required for commitment to ovary differentiation Hum. Mol. Genet. 14 2005 2053 2062
55. E. Pailhoux, B. Vigier, S. Chaffaux, N. Servel, S. Taourit, J.P. Furet, M. Fellous, F. Grosclaude, E.P. Cribiu, C. Cotinot, and D. Vaiman A 11.7-kb deletion triggers intersexuality and polledness in goats Nat. Genet. 29 2001 453 458
56. S.A. Pangas, and M.M. Matzuk Genetic models for transforming growth factor beta superfamily signaling in ovarian follicle development Mol. Cell. Endocrinol. 225 2004 83 91
57. M. Pannetier, L. Renault, G. Jolivet, C. Cotinot, and E. Pailhoux Ovarian-specific expression of a new gene regulated by the goat PIS region and transcribed by a FOXL2 bidirectional promoter Genomics 85 2005 715 726
58. D.J. Phillips Activins, inhibins and follistatins in the large domestic species Domest. Anim. Endocrinol. 28 2005 1 16
59. R.L. Prueitt, and A.R. Zinn A fork in the road to fertility Nat. Genet. 27 2001 132 134
60. R. Rice, D.P. Rice, B.R. Olsen, and I. Thesleff Progression of calvarial bone development requires Foxc1 regulation of Msx2 and Alx4 Dev. Biol. 262 2003 75 87
61. R. Rice, D.P. Rice, and I. Thesleff Foxc1 integrates Fgf and Bmp signalling independently of twist or noggin during calvarial bone development Dev. Dyn. 233 2005 847 852
62. A.J. Ross, and B. Capel Signaling at the crossroads of gonad development Trends Endocrinol. Metab. 16 2005 19 25
63. H. Sasaki, and B.L. Hogan Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo Development 118 1993 47 59
64. D. Schmidt, C.E. Ovitt, K. Anlag, S. Fehsenfeld, L. Gredsted, A.C. Treier, and M. Treier The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance Development 131 2004 933 942
65. J. Seoane, H.V. Le, L. Shen, S.A. Anderson, and J. Massague Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation Cell 117 2004 211 223
66. C. Smith, and S. Mackay Morphological development and fate of the mouse mesonephros J. Anat. 174 1991 171 184
67. N. Suzumori, C. Yan, M.M. Matzuk, and A. Rajkovic Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes Mech. Dev. 111 2002 137 141
68. H.S. Taylor, G.B. Vanden Heuvel, and P. Igarashi A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes Biol. Reprod. 57 1997 1338 1345
69. F. Tissir, C.E. Wang, and A.M. Goffinet Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development Brain Res. Dev. Brain Res. 149 2004 63 71
70. D.G. Wilkinson, and M.A. Nieto Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts Methods Enzymol. 225 1993 361 373
71. B. Wilm, R.G. James, T.M. Schultheiss, and B.L. Hogan The forkhead genes, Foxc1 and Foxc2, regulate paraxial versus intermediate mesoderm cell fate Dev. Biol. 271 2004 176 189
72. G.E. Winnier, L. Hargett, and B.L. Hogan The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo Genes Dev. 11 1997 926 940
73. G.E. Winnier, T. Kume, K. Deng, R. Rogers, J. Bundy, C. Raines, M.A. Walter, B.L. Hogan, and S.J. Conway Roles for the winged helix transcription factors MF1 and MFH1 in cardiovascular development revealed by nonallelic noncomplementation of null alleles Dev. Biol. 213 1999 418 431
74. H.H. Yao, M.M. Matzuk, C.J. Jorgez, D.B. Menke, D.C. Page, A. Swain, and B. Capel Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis Dev. Dyn. 230 2004 210 215
75. Y.I. Yeom, G. Fuhrmann, C.E. Ovitt, A. Brehm, K. Ohbo, M. Gross, K. Hubner, and H.R. Scholer Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells Development 122 1996 881 894
76. Y. Ying, X.M. Liu, A. Marble, K.A. Lawson, and G.Q. Zhao Requirement of Bmp8b for the generation of primordial germ cells in the mouse Mol. Endocrinol. 14 2000 1053 1063
77. H. Yokota, K. Yamada, X. Liu, J. Kobayashi, Y. Abe, H. Mizunuma, and Y. Ibuki Paradoxical action of activin A on folliculogenesis in immature and adult mice Endocrinology 138 1997 4572 4576
78. L. Zakin, B. Reversade, H. Kuroda, K.M. Lyons, and E.M. De Robertis Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm Development 132 2005 2489 2499
79. G.Q. Zhao, L. Liaw, and B.L. Hogan Bone morphogenetic protein 8A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis Development 125 1998 1103 1112
80. Y. Zhou, H. Kato, K. Asanoma, H. Kondo, T. Arima, K. Kato, T. Matsuda, and N. Wake Identification of FOXC1 as a TGF-beta1 responsive gene and its involvement in negative regulation of cell growth Genomics 80 2002 465 472