FOXL2 Is regulated during the bovine estrous cycle and Its expression in the endometrium is independent of conceptus-derived interferon tau

Biology of Reproduction

Volumn 87, Issue 2, 2012, Pages

  Eozenou, Caroline ^a,b   Carvalho, Anaïs Vitorino ^a,b   Forde, Niamh ^c   Giraud Delville, Corinne ^a,b   Gall, Laurence ^a,b   Lonergan, Pat ^c   Auguste, Aurélie ^a,b   Charpigny, Gilles ^a,b   Richard, Christophe ^d   Pannetier, Maëlle ^a,b   Sandra, Olivier ^a,b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d INRA   (France)

Author keywords

Bovine; Endometrium; Estrous cycle; Foxl2; Pregnancy

Indexed keywords

PROGESTERONE; RECOMBINANT INTERFERON; RECOMBINANT TAU INTERFERON; TAU INTERFERON; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CATTLE; CELL CULTURE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONCEPTION; CONTROLLED STUDY; COW; ENDOMETRIAL STROMAL CELL; ENDOMETRIUM; ENDOMETRIUM CELL; ESTRUS CYCLE; FEMALE; GENE TARGETING; GLANDULAR CELL; IMMUNOHISTOCHEMISTRY; IMPLANTATION; IN VITRO STUDY; IN VIVO STUDY; LUTEAL PHASE; LUTEOLYSIS; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR DOWN REGULATION; STROMA CELL; TRANSCRIPTION REGULATION;

ANIMALS; CATTLE; EMBRYO IMPLANTATION; ENDOMETRIUM; ESTROUS CYCLE; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; INTERFERON TYPE I; PREGNANCY; PREGNANCY PROTEINS; PROGESTERONE;

BOS; BOVINAE;

EID: 84869440870     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.101584     Document Type: Article

References (68)

1. Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod 2010; 16:135-152.
2. Lee KY. Animal models of implantation. Reproduction 2004; 128: 679-695.
3. Bowen JA, Burghardt RC. Cellular mechanisms of implantation in domestic farm animals. Semin Cell Dev Biol 2000; 11:93-104.
4. Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G. Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways. Reprod Biol 2008; 8: 179-211.
5. Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP, O'Gaora P, Roche JF, Lonergan P, Crowe MA. Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biol Reprod 2010; 84:266-278.
6. Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O'Gaora P, Lonergan P, Roche JF. Progesteroneregulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod 2009; 81:784-794.
7. Gray CA. Identification of endometrial genes regulated by early pregnancy, progesterone, and interferon tau in the ovine uterus. Biol Reprod 2006; 74:383-394.
8. Okumu LA, Forde N, Fahey AG, Fitzpatrick E, Roche JF, Crowe MA, Lonergan P. The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus. Reproduction 2010; 140:143-153.
9. Satterfield MC, Song G, Kochan KJ, Riggs PK, Simmons RM, Elsik CG, Adelson DL, Bazer FW, Zhou H, Spencer TE. Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation. Physiol Genomics 2009; 39:85-99.
10. Roberts RM, Chen Y, Ezashi T, Walker AM. Interferons and the maternalconceptus dialog in mammals. Semin Cell Dev Biol 2008; 19:170-177.
11. Spencer TE. Implantation mechanisms: insights from the sheep. Reproduction 2004; 128:657-668.
12. Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O'Gaora P, Roche JF, et al. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod 2011; 85:144-156.
13. Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Taghouti G, Galio L, Everts RE, Degrelle S, Richard C, Hue I, Yang X, Tian XC, et al. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol Genomics 2009; 39:14-27.
14. Spencer TE, Sandra O, Wolf E. Genes involved in conceptus-endometrialinteractions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction 2008; 135:165-179.
15. Ott TL, Gifford CA. Effects of early conceptus signals on circulating immune cells: lessons from domestic ruminants. Am J Reprod Immunol 2010; 64:245-254.
16. Bott RC, Ashley RL, Henkes LE, Antoniazzi AQ, Bruemmer JE, Niswender GD, Bazer FW, Spencer TE, Smirnova NP, Anthony RV, Hansen TR. Uterine vein infusion of interferon tau (IFNT) extends luteal life span in ewes. Biol Reprod 2010; 82:725-735.
17. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X, Tian XC, Lewin HA, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Prod Natl Acad Sci U S A 2009; 106:5687-5692.
18. Walker CG, Meier S, Littlejohn MD, Lehnert K, Roche JR, Mitchell MD. Modulation of the maternal immune system by the pre-implantation embryo. BMC Genomics 2010; 11:474.
19. Hannenhalli S, Kaestner KH. The evolution of Fox genes and their role in development and disease. Nat Rev Genet 2009; 10:233-240.
20. Horn D, Kapeller J, Rivera-Brugues N, Moog U, Lorenz-Depiereux B, Eck S, Hempel M, Wagenstaller J, Gawthrope A, Monaco AP, Bonin M, Riess O, et al. Identification of FOXP1 deletions in three unrelated patients with mental retardation and significant speech and language deficits. Hum Mutat 2010; 31:E1851-1860.
21. Uhlenhaut NH, Treier M. Forkhead transcription factors in ovarian function. Reproduction 2011; 142:489-495.
22. Buzzio OL. FOXO1A differentially regulates genes of decidualization. Endocrinology 2006; 147:3870-3876.
23. Jeong JW, Kwak I, Lee KY, Kim TH, Large MJ, Stewart CL, Kaestner KH, Lydon JP, DeMayo FJ. Foxa2 is essential for mouse endometrial gland development and fertility. Biol Reprod 2010; 83:396-403.
24. Takano M, Lu Z, Goto T, Fusi L, Higham J, Francis J, Withey A, Hardt J, Cloke B, Stavropoulou AV, Ishihara O, Lam EWF, et al. Transcriptional cross talk between the forkhead transcription factor forkhead box O1A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells. Mol Endocrinol 2007; 21: 2334-2349.
25. Ellsworth BS, Egashira N, Haller JL, Butts DL, Cocquet J, Clay CM, Osamura RY, Camper SA. FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Mol Endocrinol 2006; 20:2796-2805.
26. Uda M. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 2004; 13:1171-1181.
27. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S, Ristaldi MS, Marzella R, et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ ptosis/epicanthus inversus syndrome. Nat Genet 2001; 27:159-166.
28. Naimi A, Martinez A-S, Specq M-L, Diss B, Mathieu M, Sourdaine P. Molecular cloning and gene expression of Cg-Foxl2 during the development and the adult gametogenetic cycle in the oyster Crassostrea gigas. Comp Biochem Physiol B Biochem Mol Biol 2009; 154:134-142.
29. Tu Q, Brown C, Davidson E, Oliveri P. Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev Biol 2006; 300:49-62.
30. Baron D. An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. JMol Endocrinol 2004; 33:705-715.
31. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, De Baere E, Messiaen L, Cotinot C, Fellous M, Veitia RA. Evolution and expression of FOXL2. J Med Genet 2002; 39:916-921.
32. Govoroun MS, Pannetier M, Pailhoux E, Cocquet J, Brillard JP, Couty I, Batellier F, Cotinot C. Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev Dyn 2004; 231:859-870.
33. Benayoun BA, Dipietromaria A, Bazin C, Veitia RA. FOXL2: at the crossroads of female sex determination and ovarian function. Adv Exp Med Biol 2009; 665:207-226.
34. Pailhoux E, Vigier B, Chaffaux S, Servel N, Taourit S, Furet JP, Fellous M, Grosclaude F, Cribiu EP, Cotinot C, Vaiman D. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat Genet 2001; 29: 453-458.
35. Schmidt D. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004; 131:933-942.
36. Uhlenhaut NH, Treier M. Foxl2 function in ovarian development. Mol Genet Metab 2006; 88:225-234.
37. Ellsworth BS, Burns AT, Escudero KW, Duval DL, Nelson SE, Clay CM. The gonadotropin releasing hormone (GnRH) receptor activating sequence (GRAS) is a composite regulatory element that interacts with multiple classes of transcription factors including Smads, AP-1 and a forkhead DNA binding protein. Mol Cell Endocrinol 2003; 206:93-111.
38. Moumné L, Batista F, Benayoun BA, Nallathambi J, Fellous M, Sundaresan P, Veitia RA. The mutations and potential targets of the forkhead transcription factor FOXL2. Mol Cell Endocrinol 2008; 282: 2-11.
39. Batista F, Vaiman D, Dausset J, Fellous M, Veitia RA. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Prod Natl Acad Sci U S A 2007; 104:3330-3335.
40. Pannetier M, Fabre S, Batista F, Kocer A, Renault L, Jolivet G, Mandon-Pepin B, Cotinot C, Veitia R, Pailhoux E. FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 2006; 36: 399-413.
41. Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue I. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev Biol 2005; 288: 448-460.
42. Constant F. Large offspring or large placenta syndrome? Morphometric analysis of late gestation bovine placentomes from somatic nuclear transfer pregnancies complicated by hydrallantois. Biol Reprod 2006; 75: 122-130.
43. Carter F, Forde N, Duffy P, Wade M, Fair T, Crowe MA, Evans AC, Kenny DA, Roche JF, Lonergan P. Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod Fertil Dev 2008; 20:368-375.
44. Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 2005; 6:62.
45. Marongiu M, Deiana M, Meloni A, Marcia L, Puddu A, Cao A, Schlessinger D, Crisponi L. The forkhead transcription factor Foxl2 is sumoylated in both human and mouse: sumoylation affects its stability, localization, and activity. PLoS ONE 2010; 5:e9477.
46. Baron D, Batista F, Chaffaux S, Cocquet J, Cotinot C, Cribiu E, De Baere E, Guiguen Y, Jaubert F, Pailhoux E, Pannetier M, Vaiman D, et al. Foxl2 gene and the development of the ovary: a story about goat, mouse, fish and woman. Reprod Nutr Dev 2005; 45:377-382.
47. Pannetier M, Pailhoux E. Sex differentiation: state of the art and future prospects [in French]. Med Sci (Paris) 2011; 27:859-865.
48. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier A-C, Klugmann C, Klasen C, Holter NI, Riethmacher D, Schütz G, et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009; 139:1130-1142.
49. Popovici RM, Betzler NK, Krause MS, Luo M, Jauckus J, Germeyer A, Bloethner S, Schlotterer A, Kumar R, Strowitzki T, von Wolff M. Gene expression profiling of human endometrial-trophoblast interaction in a coculture model. Endocrinology 2006; 147:5662-5675.
50. Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, Genbecev-Krtolica O, Mavrogianis P, Ferrer K, Kruessel J, Fazleabas AT, Fisher SJ, et al. Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod 2006; 76:102-117.
51. Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. Comparative aspects of implantation. Reproduction 2009; 138:195-209.
52. Mann GE, Fray MD, Lamming GE. Effects of time of progesterone supplementation on embryo development and interferon-s production in the cow. Vet J 2006; 171:500-503.
53. Talbi S. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normoovulatory women. Endocrinology 2005; 147:1097-1121.
54. Georges A, Benayoun BA, Marongiu M, Dipietromaria A, L'Hote D, Todeschini AL, Auer J, Crisponi L, Veitia RA. SUMOylation of the Forkhead transcription factor FOXL2 promotes its stabilization/activation through transient recruitment to PML bodies. PLoS ONE 2011; 6:e25463.
55. Pisarska MD, Barlow G, Kuo FT. Minireview: roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology. Endocrinology 2011; 152:1199-1208.
56. Kuo FT, Bentsi-Barnes IK, Barlow GM, Bae J, Pisarska MD. Sumoylation of forkhead L2 by Ubc9 is required for its activity as a transcriptional repressor of the Steroidogenic Acute Regulatory gene. Cell Signal 2009; 21:1935-1944.
57. Al-Sabbagh M, Lam EW, Brosens JJ. Mechanisms of endometrial progesterone resistance. Mol Cell Endocrinol 2012; 358(2):208-215.
58. Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, Nedorezov T, Cao A, Forabosco A, Schlessinger D. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 2007; 16:2795-2804.
59. Hamel M, Dufort I, Robert C, Leveille MC, Leader A, Sirard MA. Genomic assessment of follicular marker genes as pregnancy predictors for human IVF. Mol Hum Reprod 2010; 16:87-96.
60. Huang ZP, Ni H, Yang ZM, Wang J, Tso JK, Shen QX. Expression of regulator of G-protein signalling protein 2 (RGS2) in the mouse uterus at implantation sites. Reproduction 2003; 126:309-316.
61. Charpigny G, Reinaud P, Tamby JP, Creminon C, Martal J, Maclouf J, Guillomot M. Expression of cyclooxygenase-1 and -2 in ovine endometrium during the estrous cycle and early pregnancy. Endocrinology 1997; 138:2163-2171.
62. Dorniak P, Bazer FW, Spencer TE. Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol Reprod 2011; 84:1119-1127.
63. Al-Gubory KH, Bolifraud P, Garrel C. Regulation of key antioxidant enzymatic systems in the sheep endometrium by ovarian steroids. Endocrinology 2008; 149:4428-4434.
64. Sherwin JR, Sharkey AM, Cameo P, Mavrogianis PM, Catalano RD, Edassery S, Fazleabas AT. Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology 2007; 148:618-626.
65. Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol 2010; 42:1634-1650.
66. Sandra O, Mansouri-Attia N, Lea RG. Novel aspects of endometrial function: a biological sensor of embryo quality and driver of pregnancy success. Reprod Fertil Dev 2011; 24:68-79.
67. Kohan K, Carvajal R, Gabler F, Vantman D, Romero C, Vega M. Role of the transcriptional factors FOXO1 and PPARG on gene expression of SLC2A4 in endometrial tissue from women with polycystic ovary syndrome. Reproduction 2010; 140:123-131.
68. Shimizu T, Krebs S, Bauersachs S, Blum H, Wolf E, Miyamoto A. Actions and interactions of progesterone and estrogen on transcriptome profiles of the bovine endometrium. Physiol Genomics 2010; 42A:290-300.