Foxl2 functions in sex determination and histogenesis throughout mouse ovary development

BMC Developmental Biology

Volumn 9, Issue 1, 2009, Pages

  Garcia Ortiz, José Elias ^a,b   Pelosi, Emanuele ^a   Omari, Shakib ^a   Nedorezov, Timur ^a   Piao, Yulan ^a   Karmazin, Jesse ^a   Uda, Manuela ^c   Cao, Antonio ^c   Cole, Steve W ^d   Forabosco, Antonino ^e   Schlessinger, David ^a   Ottolenghi, Chris ^a,f  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c CNR   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^f INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; WNT4 PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXL2 PROTEIN, MOUSE; WNT PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DHH GENE; EMBRYO; EMBRYO DEVELOPMENT; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE LOSS; HISTOGENESIS; INHBB GENE; MOUSE; NONHUMAN; OVARIAN RESERVE; OVARY DEVELOPMENT; PREMATURE OVARIAN FAILURE; PRINCIPAL COMPONENT ANALYSIS; SEX DETERMINATION; TESTIS DEVELOPMENT; TISSUE DIFFERENTIATION; TRANSGENE; ANIMAL; C57BL MOUSE; DNA MICROARRAY; FEMALE; GENDER AND SEX; GENETICS; MALE; METABOLISM; MOUSE MUTANT; OVARY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PRENATAL DEVELOPMENT; TESTIS; TRANSGENIC MOUSE;

ANIMALIA;

ANIMALS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARY; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; SEX DETERMINATION (GENETICS); TESTIS; WNT PROTEINS;

EID: 67650663277     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-9-36     Document Type: Article

References (61)

1. On regenerating the ovary and generating controversy. EE Telfer RG Gosden AG Byskov N Spears D Albertini CY Andersen R Anderson R Braw-Tal H Clarke A Gougeon E McLaughlin A McLaren K McNatty G Schatten S Silber A Tsafriri, Cell 2005 122 821 822 16179247 (Pubitemid 41345195)
2. The relation of age to numbers of oocytes. AM Mandl S Zuckerman, J Endocrinol 1951 7 190 193 14850606
3. Initial and cyclic recruitment of ovarian follicles. EA McGee AJ Hsueh, Endocr Rev 2000 21 200 214 10782364 (Pubitemid 32275595)
4. From primordial germ cell to primordial follicle: mammalian female germ cell development. ME Pepling, Genesis 2006 44 622 632 17146778 (Pubitemid 46047873)
5. Development of follicles in the mammalian ovary. AN Hirshfield, Int Rev Cytol 1991 124 43 101 2001918
6. Genetics of early mammalian folliculogenesis. Y Choi A Rajkovic, Cell Mol Life Sci 2006 63 579 590 16416028
7. Regulation of primordial follicle assembly and development. MK Skinner, Hum Reprod Update 2005 11 461 471 16006439 (Pubitemid 41418801)
8. Intercellular communication in the mammalian ovary: oocytes carry the conversation. MM Matzuk KH Burns MM Viveiros JJ Eppig, Science 2002 296 2178 2180 12077402 (Pubitemid 34680291)
9. Genetic control of early folliculogenesis in mice. O Epifano J Dean, Trends Endocrinol Metab 2002 13 169 173 11943561 (Pubitemid 36733991)
10. Role of mammalian Y chromosome in sex determination. PS Burgoyne, Philos Trans R Soc Lond B Biol Sci 1988 322 63 72 2907804
11. Studies on sex differentiation in mammals. A Jost B Vigier J Prepin JP Perchellet, Recent Prog Horm Res 1973 29 1 41 4584366
12. Differentiation of mammalian embryonic gonad. AG Byskov, Physiol Rev 1986 66 71 117 3511481
13. Testicular differentiation in mammals under normal and experimental conditions. H Merchant-Larios T Taketo, J Electron Microsc Tech 1991 19 158 171 1748900
14. Foxl2 is required for commitment to ovary differentiation. C Ottolenghi S Omari JE Garcia-Ortiz M Uda L Crisponi A Forabosco G Pilia D Schlessinger, Hum Mol Genet 2005 14 2053 2062 15944199 (Pubitemid 41418041)
15. Development of the mammalian gonad: the fate of the supporting cell lineage. A McLaren, Bioessays 1991 13 151 156 1859392 (Pubitemid 121000556)
16. Determination and stability of sex. C Ottolenghi M Uda L Crisponi S Omari A Cao A Forabosco D Schlessinger, Bioessays 2007 29 15 25 17187356 (Pubitemid 46181801)
17. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. C Ottolenghi E Pelosi J Tran M Colombino E Douglass T Nedorezov A Cao A Forabosco D Schlessinger, Hum Mol Genet 2007 16 2795 2804 17728319 (Pubitemid 350048379)
18. Sry and the hesitant beginnings of male development. JC Polanco P Koopman, Dev Biol 2007 302 13 24 16996051 (Pubitemid 46096923)
19. A regulatory cascade hypothesis for mammalian sex determination: SRY represses a negative regulator of male development. K McElreavey E Vilain N Abbas I Herskowitz M Fellous, Proc Natl Acad Sci USA 1993 90 3368 3372 8475082
20. Genetic control of primary sex determination in mice. EM Eicher LL Washburn, Annu Rev Genet 1986 20 327 60 3545061
21. Activation of beta-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. AA Chassot F Ranc EP Gregoire HL Roepers-Gajadien MM Taketo G Camerino DG de Rooij A Schedl MC Chaboissier, Hum Mol Genet 2008 17 1264 1277 18250098 (Pubitemid 351566963)
22. R-spondin1 and FOXL2 act into two distinct cellular types during goat ovarian differentiation. A Kocer I Pinheiro M Pannetier L Renault P Parma O Radi KA Kim G Camerino E Pailhoux, BMC Dev Biol 2008 8 36 18384673
23. Cloning and expression of R-Spondin1 in different vertebrates suggests a conserved role in ovarian development. CA Smith CM Shoemaker KN Roeszler J Queen DP Crews AH Sinclair, BMC Dev Biol 2008 8 72 18651984
24. Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. DM Maatouk L Dinapoli A Alvers KL Parker MM Taketo B Capel, Hum Mol Genet 2008 17 2949 2955 18617533
25. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. L Crisponi M Deiana A Loi F Chiappe M Uda P Amati L Bisceglia L Zelante R Nagaraja S Porcu MS Ristaldi R Marzella M Rocchi M Nicolino A Lienhardt-Roussie A Nivelon A Verloes D Schlessinger P Gasparini D Bonneau A Cao G Pilia, Nat Genet 2001 27 159 166 11175783 (Pubitemid 32157442)
26. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. M Uda C Ottolenghi L Crisponi JE Garcia M Deiana W Kimber A Forabosco A Cao D Schlessinger G Pilia, Hum Mol Genet 2004 13 1171 1181 15056605 (Pubitemid 38786999)
27. A 11.7-kb deletion triggers intersexuality and polledness in goats. E Pailhoux B Vigier S Chaffaux N Servel S Taourit JP Furet M Fellous F Grosclaude EP Cribiu C Cotinot D Vaiman, Nat Genet 2001 29 453 458 11726932 (Pubitemid 34326697)
28. R-spondin1 is essential in sex determination, skin differentiation and malignancy. P Parma O Radi V Vidal MC Chaboissier E Dellambra S Valentini L Guerra A Schedl G Camerino, Nat Genet 2006 38 1304 1309 17041600 (Pubitemid 44646293)
29. Diagnosis of multiple cancer types by shrunken centroids of gene expression. R Tibshirani T Hastie B Narasimhan G Chu, Proc Natl Acad Sci USA 2002 99 6567 6572 12011421 (Pubitemid 34526173)
30. Controlling false-negative errors in microarray differential expression analysis: a PRIM approach. SW Cole Z Galic JA Zack, Bioinformatics 2003 19 1808 1816 14512352 (Pubitemid 37220473)
31. Potential target genes of EMX2 include Odz/Ten-M and other gene families with implications for cortical patterning. H Li KM Bishop DD O'Leary, Mol Cell Neurosci 2006 33 136 149 16919471 (Pubitemid 44415488)
32. Plexin-B family members demonstrate non-redundant expression patterns in the developing mouse nervous system: an anatomical basis for morphogenetic effects of Sema4D during development. T Worzfeld AW Puschel S Offermanns R Kuner, Eur J Neurosci 2004 19 2622 2632 15147296 (Pubitemid 38746379)
33. The cortex-medulla oocyte growth pattern is organized during fetal life: an in-vitro study of the mouse ovary. AG Byskov X Guoliang CY Andersen, Mol Hum Reprod 1997 3 795 800 9358006 (Pubitemid 127509614)
34. Distinct roles of unliganded and liganded estrogen receptors in transcriptional repression. A Cvoro C Tzagarakis-Foster D Tatomer S Paruthiyil MS Fox DC Leitman, Mol Cell 2006 21 555 564 16483936 (Pubitemid 43228010)
35. Purification and characterization of NADP+dependent 3 alpha-hydroxysteroid dehydrogenase from mouse liver cytosol. A Hara Y Inoue M Nakagawa F Naganeo H Sawada, J Biochem 1988 103 1027 1034 3170514 (Pubitemid 18150725)
36. Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Y Morita GI Perez F Paris SR Miranda D Ehleiter A Haimovitz-Friedman Z Fuks Z Xie JC Reed EH Schuchman RN Kolesnick JL Tilly, Nat Med 2000 6 1109 1114 11017141 (Pubitemid 30792189)
37. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. H Pan MJ O'Brien K Wigglesworth JJ Eppig RM Schultz, Dev Biol 2005 286 493 506 16168984 (Pubitemid 41443288)
38. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. S Nef O Schaad NR Stallings CR Cederroth JL Pitetti G Schaer S Malki M Dubois-Dauphin B Boizet-Bonhoure P Descombes KL Parker JD Vassalli, Dev Biol 2005 287 361 377 16214126 (Pubitemid 41636770)
39. Mouse ovary developmental RNA and protein markers from gene expression profiling. L Herrera C Ottolenghi JE Garcia-Ortiz M Pellegrini F Manini MS Ko R Nagaraja A Forabosco D Schlessinger, Dev Biol 2005 279 271 290 15733658 (Pubitemid 40298738)
40. Emx2 developmental expression in the primordia of the reproductive and excretory systems. M Pellegrini S Pantano F Lucchini M Fumi A Forabosco, Anat Embryol (Berl) 1997 196 427 433 9453363 (Pubitemid 27510988)
41. Defects of urogenital development in mice lacking Emx2. N Miyamoto M Yoshida S Kuratani I Matsuo S Aizawa, Development 1997 124 1653 1664 9165114 (Pubitemid 27248333)
42. Lim Homeobox Gene, LHX8, Is Essential for Mouse Oocyte Differentiation and Survival. Y Choi DJ Ballow Y Xin A Rajkovic, Biol Reprod 2008 79 442 449 18509161
43. A microarray analysis of the XX Wnt4 mutant gonad targeted at the identification of genes involved in testis vascular differentiation. D Coveney AJ Ross JD Slone B Capel, Gene Expr Patterns 2007 7 82 92 16844427 (Pubitemid 44712730)
44. Genomewide discovery and classification of candidate ovarian fertility genes in the mouse. TD Gallardo GB John L Shirley CM Contreras EA Akbay JM Haynie SE Ward MJ Shidler DH Castrillon, Genetics 2007 177 179 94 17660561
45. Ovarian gene expression in the absence of FIGLA, an oocyte-specific transcription factor. S Joshi H Davies LP Sims SE Levy J Dean, BMC Dev Biol 2007 7 67 17567914
46. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. SM Soyal A Amleh J Dean, Development 2000 127 4645 4654 11023867 (Pubitemid 30952824)
47. Female development in mammals is regulated by Wnt-4 signalling. S Vainio M Heikkila A Kispert N Chin AP McMahon, Nature 1999 397 405 409 9989404
48. Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. MS Govoroun M Pannetier E Pailhoux J Cocquet JP Brillard I Couty F Batellier C Cotinot, Dev Dyn 2004 231 859 870 15517586 (Pubitemid 40022747)
49. 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. DS Wang T Kobayashi LY Zhou B Paul-Prasanth S Ijiri F Sakai K Okubo K Morohashi Y Nagahama, Mol Endocrinol 2007 21 712 725 17192407 (Pubitemid 46310192)
50. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. A Subramanian P Tamayo VK Mootha S Mukherjee BL Ebert MA Gillette A Paulovich SL Pomeroy TR Golub ES Lander JP Mesirov, Proc Natl Acad Sci USA 2005 102 15545 1550 16199517
51. FOXL2 and SOX9 as parameters of female and male gonadal differentiation in patients with various forms of disorders of sex development (DSD). R Hersmus N Kalfa B de Leeuw H Stoop JW Oosterhuis R de Krijger KP Wolffenbuttel SL Drop RA Veitia M Fellous F Jaubert LH Looijenga, J Pathol 2008 215 31 38 18348162 (Pubitemid 351619873)
52. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. F Batista D Vaiman J Dausset M Fellous RA Veitia, Proc Natl Acad Sci USA 2007 104 3330 3335 17360647 (Pubitemid 46364159)
53. Contribution of germ cells to the differentiation and maturation of the ovary: insights from models of germ cell depletion. CJ Guigon S Magre, Biol Reprod 2006 74 450 458 16339043 (Pubitemid 43273482)
54. Irx3 is differentially up-regulated in female gonads during sex determination. JS Jorgensen L Gao, Gene Expr Patterns 2005 5 756 762 15963769 (Pubitemid 40945860)
55. Profiling gene expression during the differentiation and development of the murine embryonic gonad. CL Small JE Shima M Uzumcu MK Skinner MD Griswold, Biol Reprod 2005 72 492 501 15496517 (Pubitemid 40129727)
56. Expression profiling of purified mouse gonadal somatic cells during the critical time window of sex determination reveals novel candidate genes for human sexual dysgenesis syndromes. A Beverdam P Koopman, Hum Mol Genet 2006 15 417 431 16399799 (Pubitemid 43159894)
57. Transcriptional profile of mouse pre-granulosa and Sertoli cells isolated from early-differentiated fetal gonads. GJ Bouma JP Affourtit CJ Bult EM Eicher, Gene Expr Patterns 2007 7 113 123 16839824 (Pubitemid 44712729)
58. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. SA Armstrong JE Staunton LB Silverman R Pieters ML den Boer MD Minden SE Sallan ES Lander TR Golub SJ Korsmeyer, Nat Genet 2002 30 41 47 11731795 (Pubitemid 34886688)
59. Semi-supervised methods to predict patient survival from gene expression data. E Bair R Tibshirani, PLoS Biol 2004 2 E108 15094809
60. Metagenes and molecular pattern discovery using matrix factorization. JP Brunet P Tamayo TR Golub JP Mesirov, Proc Natl Acad Sci USA 2004 101 4164 4169 15016911 (Pubitemid 38405900)
61. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. L Shi LH Reid WD Jones R Shippy JA Warrington SC Baker PJ Collins F de Longueville ES Kawasaki KY Lee Y Luo YA Sun JC Willey RA Setterquist GM Fischer W Tong YP Dragan DJ Dix FW Frueh FM Goodsaid D Herman RV Jensen CD Johnson EK Lobenhofer RK Puri U Schrf J Thierry-Mieg C Wang M Wilson PK Wolber L Zhang S Amur W Bao CC Barbacioru AB Lucas V Bertholet C Boysen B Bromley D Brown A Brunner R Canales XM Cao TA Cebula JJ Chen J Cheng TM Chu E Chudin J Corson JC Corton LJ Croner C Davies TS Davison G Delenstarr X Deng D Dorris AC Eklund XH Fan H Fang S Fulmer-Smentek JC Fuscoe K Gallagher W Ge L Guo X Guo J Hager PK Haje J Han T Han HC Harbottle SC Harris E Hatchwell CA Hauser S Hester H Hong P Hurban SA Jackson H Ji CR Knight WP Kuo JE LeClerc S Levy QZ Li C Liu Y Liu MJ Lombardi Y Ma SR Magnuson B Maqsodi T McDaniel N Mei O Myklebost B Ning N Novoradovskaya MS Orr TW Osborn A Papallo TA Patterson RG Perkins EH Peters R Peterson KL Philips PS Pine L Pusztai F Qian H Ren M Rosen BA Rosenzweig RR Samaha M Schena GP Schroth S Shchegrova DD Smith F Staedtler Z Su H Sun Z Szallasi Z Tezak D Thierry-Mieg KL Thompson I Tikhonova Y Turpaz B Vallanat C Van SJ Walker SJ Wang Y Wang R Wolfinger A Wong J Wu C Xiao Q Xie J Xu W Yang S Zhong Y Zong W Slikker Jr, Nat Biotechnol 2006 24 1151 1161 16964229 (Pubitemid 44359727)