FOXO1/3 depletion in granulosa cells alters follicle growth, death and regulation of pituitary FSH

Molecular Endocrinology

Volumn 27, Issue 2, 2013, Pages 238-252

  Liu, Zhilin ^a   Castrillon, Diego H ^c   Zhou, Wei ^b   Richards, JoAnne S ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN 2; FOLLITROPIN; LUTEINIZING HORMONE; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE EXPRESSION; GRANULOSA CELL; MALE; METABOLIC STRESS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OVARY FOLLICLE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; TRANSCRIPTION REGULATION;

ACTIVINS; ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 2; CELL PROLIFERATION; FEMALE; FOLLICLE STIMULATING HORMONE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENOTYPE; GRANULOSA CELLS; LUTEINIZING HORMONE; MICE; OVARIAN FOLLICLE; OVARY; PITUITARY GLAND;

EID: 84873045382     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1296     Document Type: Article

References (73)

1. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z, Miao L, Tothova Z, Horner JW, Carrasco DR, Jiang S, Gilliland DG, Chin L, Wong WH, Castrillon DH, DePinho RA 2007 FoxOs are lineagerestricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128:309-323
2. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA 2003 Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301:215-218
3. Liu L, Rajareddy S, Reddy P, Du C, Jagarlamudi K, Shen Y, Gunnarsson D, Selstam G, Boman K, Liu K 2007 Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 134:199-209
4. Liu Z, Rudd MD, Hernandez-Gonzalez I, Gonzalez-Robayna I, Fan HY, Zeleznik AJ, Richards JS 2009 FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells. Mol Endocrinol 23:649-661
5. Accili D, Arden KC 2004 FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117:421-426
6. McCormick M, Chen K, Ramaswamy P, Kenyon C 2012 New genes that extend Caenorhabditis elegans' lifespan in response to reproductive signals. Aging Cell 11:192-202
7. Kousteni S 2012 FoxO1, the transcriptional chief of staff of energy metabolism. Bone 50:437-443
8. Rached MT, Kode A, Silva BC, Jung DY, Gray S, Ong H, Paik JH, DePinho RA, Kim JK, Karsenty G, Kousteni S 2010 FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice. J Clin Invest 120:357-368
9. van der Vos KE, Coffer PJ 2008 FOXO-binding partners: it takes two to tango. Oncogene 27:2289-2299
10. Richards JS, Sharma SC, Falender AE, Lo YH 2002 Expression of FKHR, FKHRL1, and AFX genes in the rodent ovary: evidence for regulation by IGF-I, estrogen, and the gonadotropins. Mol Endocrinol 16:580-599
11. Shi F, LaPolt PS 2003 Relationship between FoxO1 protein levels and follicular development, atresia, and luteinization in the rat ovary. J Endocrinol 179:195-203
12. Burns KH, Owens GE, Ogbonna SC, Nilson JH, Matzuk MM 2003 Expression profiling analyses of gonadotropin responses and tumor development in the absence of inhibins. Endocrinology 144:4492-4507
13. Goertz MJ, Wu Z, Gallardo TD, Hamra FK, Castrillon DH 2011 Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J Clin Invest 121:3456-3466
14. John GB, Gallardo TD, Shirley LJ, Castrillon DH 2008 Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321:197-204
15. Gougeon A 1996 Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 17:121-155
16. Richards JS 2001 Perspective: the ovarian follicle-a perspective in 2001. Endocrinology 142:2184-2193
17. Zhou J, Kumar TR, Matzuk MM, Bondy C 1997 Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol Endocrinol 11:1924-1933
18. Pangas SA, Matzuk MM 2008 The TGF-B family in the reproductive tract. In: Derynck R, Miyazono K, eds. The TGF-b family. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
19. Richards JS 1994 Hormonal control of gene expression in the ovary. Endocr Rev 15:725-751
20. Shimasaki S, Moore RK, Otsuka F, Erickson GF 2004 The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25:72-101
21. Matzuk MM 1995 Functional analysis of mammalian members of the transforming growth factor-β superfamily. Trends Endocrinol Metab 6:120-127
22. Park Y, Maizels ET, Feiger ZJ, Alam H, Peters CA, Woodruff TK, Unterman TG, Lee EJ, Jameson JL, Hunzicker-Dunn M 2005 Induction of cyclin D2 in rat granulosa cells requires FSH-dependent relief from FOXO1 repression coupled with positive signals from Smad. J Biol Chem 280:9135-9148
23. Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellvé AR, Efstratiadis A 1996 Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 10:903-918
24. Robker RL, Richards JS 1998 Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol 12:924-940
25. Pisarska MD, Kuo FT, Tang D, Zarrini P, Khan S, Ketefian A 2009 Expression of forkhead transcription factors in human granulosa cells. Fertil Steril 91:1392-1394
26. Gross DN, van den Heuvel AP, Birnbaum MJ 2008 The role of FoxO in the regulation of metabolism. Oncogene 27:2320-2336
27. Hosaka T, Biggs 3rd WH, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC 2004 Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 101:2975-2980
28. Huang H, Tindall DJ 2007 Dynamic FoxO transcription factors. J Cell Sci 120:2479-2487
29. Erickson GF, Shimasaki S 2003 The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol 1:9
30. Furuyama T, Kitayama K, Shimoda Y, Ogawa M, Sone K, Yoshida-Araki K, Hisatsune H, Nishikawa S, Nakayama K, Nakayama K, Ikeda K, Motoyama N, Mori N 2004 Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice. J Biol Chem 279:34741-34749
31. Fan HY, Liu Z, Cahill N, Richards JS 2008 Targeted disruption of Pten in ovarian granulosa cells enhances ovulation and extends the life span of luteal cells. Mol Endocrinol 22:2128-2140
32. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR 2002 Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat Genet 32:408-410
33. Pangas SA, Jorgez CJ, Tran M, Agno J, Li X, Brown CW, Kumar TR, Matzuk MM 2007 Intraovarian activins are required for female fertility. Mol Endocrinol 21:2458-2471
34. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM 2008 Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 28:248-257
35. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM 2008 Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol Cell Biol 28:7001-7011
36. Lan ZJ, Xu X, Cooney AJ 2004 Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol Reprod 71:1469-1474
37. Hsieh M, Mulders SM, Friis RR, Dharmarajan A, Richards JS 2003 Expression and localization of secreted frizzled-related protein-4 in the rodent ovary: evidence for selective up-regulation in luteinized granulosa cells. Endocrinology 144:4597-4606
38. Liu Z, Fan HY, Wang Y, Richards JS 2010 Targeted disruption of Mapk14 (p38MAPKα) in granulosa cells and cumulus cells causes cell-specific changes in gene expression profiles that rescue cumulus cell-oocyte complex expansion and maintain fertility. Mol Endocrinol 24:1794-1804
39. Pierce A, Xu M, Bliesner B, Liu Z, Richards J, Tobet S, Wierman ME 2011 Hypothalamic but not pituitary or ovarian defects underlie the reproductive abnormalities in Axl/Tyro3 null mice. Mol Cell Endocrinol 339:151-158
40. Rozen S, Skaletsky H 2000 Primer3 on theWWWfor general users and for biologist programmers. Methods Mol Biol 132:365-386
41. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP 2003 Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264
42. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80
43. Bernard DJ, Fortin J, Wang Y, Lamba P 2010 Mechanisms of FSH synthesis: what we know, what we don't, and why you should care. Fertil Steril 93:2465-2485
44. Wang Y, Fortin J, Lamba P, Bonomi M, Persani L, Roberson MS, Bernard DJ 2008 Activator protein-1 and smad proteins synergistically regulate human follicle-stimulating hormone β-promoter activity. Endocrinology 149:5577-5591
45. Charles MA, Saunders TL, Wood WM, Owens K, Parlow AF, Camper SA, Ridgway EC, Gordon DF 2006 Pituitary-specific Gata2 knockout: effects on gonadotrope and thyrotrope function. Mol Endocrinol 20:1366-1377
46. Matzuk MM, Kumar TR, Shou W, Coerver KA, Lau AL, Behringer RR, Finegold MJ 1996 Transgenic models to study the roles of inhibins and activins in reproduction, oncogenesis, and development. Recent Prog Horm Res 51:123-154; discussion 155-127
47. Justice NJ, Blount AL, Pelosi E, Schlessinger D, Vale W, Bilezikjian LM 2011 Impaired FSHβ expression in the pituitaries of Foxl2 mutant animals. Mol Endocrinol 25:1404-1415
48. Arriola DJ, Mayo SL, Skarra DV, Benson CA, Thackray VG 2012 FOXO1 transcription factor inhibits luteinizing hormone β gene expression in pituitary gonadotrope cells. J Biol Chem 287:33424-33435
49. Parikh RV, Park CH, Thackray VG 2012 FOXO1 diminishes activin signaling in pituitary gonadotrope cells. Endocr Rev 33:SAT-678
50. Skarra D, Arriola DJ, Thackray VG 2012 FOXO1 Inhibition of follicle-stimulating hormone β gene transcription. Endocr Rev 33: SAT-683
51. Cho BN, McMullen ML, Pei L, Yates CJ, Mayo KE 2001 Reproductive deficiencies in transgenic mice expressing the rat inhibin α-subunit gene. Endocrinology 142:4994-5004
52. Gomis RR, Alarcón C, He W, Wang Q, Seoane J, Lash A, Massagué J 2006 A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci USA 103:12747-12752
53. Harlow CR, Davidson L, Burns KH, Yan C, Matzuk MM, Hillier SG 2002 FSH and TGF-β superfamily members regulate granulosa cell connective tissue growth factor gene expression in vitro and in vivo. Endocrinology 143:3316-3325
54. Nakajima Y, Akaogi K, Suzuki T, Osakabe A, Yamaguchi C, Sunahara N, Ishida J, Kako K, Ogawa S, Fujimura T, Homma Y, Fukamizu A, Murayama A, Kimura K, Inoue S, Yanagisawa J 2011 Estrogen regulates tumor growth through a nonclassical pathway that includes the transcription factors ERβ and KLF5. Sci Signal 4:ra22
55. Kuan CY, Whitmarsh AJ, Yang DD, Liao G, Schloemer AJ, Dong C, Bao J, Banasiak KJ, Haddad GG, Flavell RA, Davis RJ, Rakic P 2003 A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci USA 100:15184-15189
56. Gilley J, Coffer PJ, Ham J 2003 FOXOtranscription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 162:613-622
57. Kwon HS, Huang B, Unterman TG, Harris RA 2004 Protein kinase B-α inhibits human pyruvate dehydrogenase kinase-4 gene induction by dexamethasone through inactivation of FOXO transcription factors. Diabetes 53:899-910
58. Burns KH, Yan C, Kumar TR, Matzuk MM 2001 Analysis of ovarian gene expression in follicle-stimulating hormone β knockout mice. Endocrinology 142:2742-2751
59. Zhang X, Yalcin S, Lee DF, Yeh TY, Lee SM, Su J, Mungamuri SK, Rimmelé P, Kennedy M, Sellers R, Landthaler M, Tuschl T, Chi NW, Lemischka I, Keller G, Ghaffari S 2011 FOXO1 is an essential regulator of pluripotency in human embryonic stem cells. Nat Cell Biol 13:1092-1099
60. Downing JR 2011 A new FOXO pathway required for leukemogenesis. Cell 146:669-670
61. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hämäläinen T, Peng SL, Lan ZJ, Cooney AJ, Huhtaniemi I, Liu K 2008 Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319:611-613
62. Iyer AK, McCabe ER 2004 Molecular mechanisms of DAX1 action. Mol Genet Metab 83:60-73
63. Slee RB, Hillier SG, Largue P, Harlow CR, Miele G, Clinton M 2001 Differentiation-dependent expression of connective tissue growth factor and lysyl oxidase messenger ribonucleic acids in rat granulosa cells. Endocrinology 142:1082-1089
64. Arnott JA, Lambi AG, Mundy C, Hendesi H, Pixley RA, Owen TA, Safadi FF, Popoff SN 2011 The role of connective tissue growth factor (CTGF/CCN2) in skeletogenesis. Crit Rev Eukaryot Gene Expr 21:43-69
65. Rached MT, Kode A, Xu L, Yoshikawa Y, Paik JH, Depinho RA, Kousteni S 2010 FoxO1 is a positive regulator of bone formation by favoring protein synthesis and resistance to oxidative stress in osteoblasts. Cell Metab 11:147-160
66. Nagashima T, Kim J, Li Q, Lydon JP, DeMayo FJ, Lyons KM, Matzuk MM 2011 Connective tissue growth factor is required for normal follicle development and ovulation. Mol Endocrinol 25:1740-1759
67. Franks S, Stark J, Hardy K 2008 Follicle dynamics and anovulation in polycystic ovary syndrome. Hum Reprod Update 14:367-378
68. Pellatt L, Rice S, Mason HD 2010 Anti-Mullerian hormone and polycystic ovary syndrome: a mountain too high? Reproduction 139:825-833
69. Pellatt L, Hanna L, Brincat M, Galea R, Brain H, Whitehead S, Mason H 2007 Granulosa cell production of anti-Mullerian hormone is increased in polycystic ovaries. J Clin Endocrinol Metab 92:240-245
70. Nistala H, Lee-Arteaga S, Smaldone S, Siciliano G, Carta L, Ono RN, Sengle G, Arteaga-Solis E, Levasseur R, Ducy P, Sakai LY, Karsenty G, Ramirez F 2010 Fibrillin-1 and-2 differentially modulate endogenous TGF-β and BMP bioavailability during bone formation. J Cell Biol 190:1107-1121
71. Wan H, Luo F, Wert SE, Zhang L, Xu Y, Ikegami M, Maeda Y, Bell SM, Whitsett JA 2008 Kruppel-like factor 5 is required for perinatal lung morphogenesis and function. Development 135:2563-2572
72. Choi WS, Abel G, Klintworth H, Flavell RA, Xia Z 2010 JNK3 mediates paraquat-and rotenone-induced dopaminergic neuron death. J Neuropathol Exp Neurol 69:511-520
73. Wei D, Tao R, Zhang Y, White MF, Dong XC 2011 Feedback regulation of hepatic gluconeogenesis through modulation of SHP/ Nr0b2 gene expression by Sirt1 and FoxO1. Am J Physiol Endocrinol Metab 300:E312-E320