Gene expression profiling of preovulatory follicle in the buffalo cow: Effects of increased IGF-I concentration on periovulatory events

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Rao, Jyotsna U ^a   Shah, Kunal B ^a   Puttaiah, Jayaram ^a   Rudraiah, Medhamurthy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE; LUTEINIZING HORMONE; PROTEIN BCL 2; PROTEIN PAWR; SOMATOMEDIN C; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; FOLLITROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BUFFALO; CELL DIFFERENTIATION; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GRANULOSA CELL; IMMUNOCYTOCHEMISTRY; LUTEINIZING HORMONE RELEASE; MICROARRAY ANALYSIS; MOLECULAR BIOLOGY; NONHUMAN; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; REAL TIME POLYMERASE CHAIN REACTION; STEROIDOGENESIS; ANIMAL; BLOOD; CATTLE; DRUG EFFECT; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BOVINAE;

ANIMALS; CATTLE; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION PROFILING; GROWTH HORMONE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; LUTEINIZING HORMONE; OVARIAN FOLLICLE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79959318675     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020754     Document Type: Article

References (115)

1. Jainudeen M, Hafez E, (1993) Cattle and buffalo. Reproduction in Farm Animals Philadelphia Lea Febiger Press pp. 315-329.
2. Fayad T, Levesque V, Sirois J, Silversides DW, Lussier JG, (2004) Gene expression profiling of differentially expressed genes in granulosa cells of bovine dominant follicles using suppression subtractive hybridization. Biol Reprod 70: 523-533.
3. Mihm M, Baker PJ, Fleming LM, Monteiro AM, O'Shaughnessy PJ, (2008) Differentiation of the bovine dominant follicle from the cohort upregulates mRNA expression for new tissue development genes. Reproduction 135: 253-265.
4. Forde N, Mihm M, Canty MJ, Zielak AE, Baker PJ, et al. (2008) Differential expression of signal transduction factors in ovarian follicle development: a functional role for betaglycan and FIBP in granulosa cells in cattle. Physiol Genomics 33: 193-204.
5. Rhodes FM, Peterson AJ, Jolly PD, (2001) Gonadotrophin responsiveness, aromatase activity and insulin-like growth factor binding protein content of bovine ovarian follicles during the first follicular wave. Reproduction 122: 561-569.
6. Tajima K, Yoshii K, Fukuda S, Orisaka M, Miyamoto K, et al. (2005) Luteinizing hormone-induced extracellular-signal regulated kinase activation differently modulates progesterone and androstenedione production in bovine theca cells. Endocrinology 146: 2903-2910.
7. Beg MA, Meira C, Bergfelt DR, Ginther OJ, (2003) Role of oestradiol in growth of follicles and follicle deviation in heifers. Reproduction 125: 847-854.
8. Austin EJ, Mihm M, Evans AC, Knight PG, Ireland JL, et al. (2001) Alterations in intrafollicular regulatory factors and apoptosis during selection of follicles in the first follicular wave of the bovine estrous cycle. Biol Reprod 64: 839-848.
9. Beg MA, Bergfelt DR, Kot K, Wiltbank MC, Ginther OJ, (2001) Follicular-fluid factors and granulosa-cell gene expression associated with follicle deviation in cattle. Biol Reprod 64: 432-441.
10. Jo M, Komar CM, Fortune JE, (2002) Gonadotropin surge induces two separate increases in messenger RNA for progesterone receptor in bovine preovulatory follicles. Biol Reprod 67: 1981-1988.
11. Quirk SM, Cowan RG, Harman RM, Hu CL, Porter DA, (2004) Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J Anim Sci 82 E-Suppl: E40-52.
12. Bridges PJ, Fortune JE, (2007) Regulation, action and transport of prostaglandins during the periovulatory period in cattle. Mol Cell Endocrinol 263: 1-9.
13. Sirois J, (1994) Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology 135: 841-848.
14. Ndiaye K, Fayad T, Silversides DW, Sirois J, Lussier JG, (2005) Identification of downregulated messenger RNAs in bovine granulosa cells of dominant follicles following stimulation with human chorionic gonadotropin. Biol Reprod 73: 324-333.
15. Li Q, Jimenez-Krassel F, Ireland JJ, Smith GW, (2009) Gene expression profiling of bovine preovulatory follicles: gonadotropin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process. Reproduction 137: 297-307.
16. Evans AC, Ireland JL, Winn ME, Lonergan P, Smith GW, et al. (2004) Identification of genes involved in apoptosis and dominant follicle development during follicular waves in cattle. Biol Reprod 70: 1475-1484.
17. Yang MY, Rajamahendran R, (2000) Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biol Reprod 62: 1209-1217.
18. Porter DA, Harman RM, Cowan RG, Quirk SM, (2001) Relationship of Fas ligand expression and atresia during bovine follicle development. Reproduction 121: 561-566.
19. Hu CL, Cowan RG, Harman RM, Quirk SM, (2004) Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells. Mol Endocrinol 18: 326-338.
20. Quirk SM, Cowan RG, Harman RM, (2006) The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. J Endocrinol 189: 441-453.
21. Madan P, Bridges PJ, Komar CM, Beristain AG, Rajamahendran R, et al. (2003) Expression of messenger RNA for ADAMTS subtypes changes in the periovulatory follicle after the gonadotropin surge and during luteal development and regression in cattle. Biol Reprod 69: 1506-1514.
22. Bakke LJ, Dow MP, Cassar CA, Peters MW, Pursley JR, et al. (2002) Effect of the preovulatory gonadotropin surge on matrix metalloproteinase (MMP)-14, MMP-2, and tissue inhibitor of metalloproteinases-2 expression within bovine periovulatory follicular and luteal tissue. Biol Reprod 66: 1627-1634.
23. Dow MP, Bakke LJ, Cassar CA, Peters MW, Pursley JR, et al. (2002) Gonadotrophin surge-induced upregulation of mRNA for plasminogen activator inhibitors 1 and 2 within bovine periovulatory follicular and luteal tissue. Reproduction 123: 711-719.
24. Dow MP, Bakke LJ, Cassar CA, Peters MW, Pursley JR, et al. (2002) Gonadotropin surge-induced up-regulation of the plasminogen activators (tissue plasminogen activator and urokinase plasminogen activator) and the urokinase plasminogen activator receptor within bovine periovulatory follicular and luteal tissue. Biol Reprod 66: 1413-1421.
25. Bedard J, Brule S, Price CA, Silversides DW, Lussier JG, (2003) Serine protease inhibitor-E2 (SERPINE2) is differentially expressed in granulosa cells of dominant follicle in cattle. Mol Reprod Dev 64: 152-165.
26. Bakke LJ, Li Q, Cassar CA, Dow MP, Pursley JR, et al. (2004) Gonadotropin surge-induced differential upregulation of collagenase-1 (MMP-1) and collagenase-3 (MMP-13) mRNA and protein in bovine preovulatory follicles. Biol Reprod 71: 605-612.
27. Li Q, Bakke LJ, Pursley JR, Smith GW, (2004) Localization and temporal regulation of tissue inhibitors of metalloproteinases 3 and 4 in bovine preovulatory follicles. Reproduction 128: 555-564.
28. Klipper E, Tatz E, Kisliouk T, Vlodavsky I, Moallem U, et al. (2009) Induction of heparanase in bovine granulosa cells by luteinizing hormone: possible role during the ovulatory process. Endocrinology 150: 413-421.
29. Spicer LJ, Aad PY, (2007) Insulin-like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle-stimulating hormone and IGF2 receptor. Biol Reprod 77: 18-27.
30. Gong JG, McBride D, Bramley TA, Webb R, (1993) Effects of recombinant bovine somatotrophin, insulin-like growth factor-I and insulin on the proliferation of bovine granulosa cells in vitro. J Endocrinol 139: 67-75.
31. Armstrong DT, Xia P, de Gannes G, Tekpetey FR, Khamsi F, (1996) Differential effects of insulin-like growth factor-I and follicle-stimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells. Biol Reprod 54: 331-338.
32. Stewart RE, Spicer LJ, Hamilton TD, Keefer BE, (1995) Effects of insulin-like growth factor I and insulin on proliferation and on basal and luteinizing hormone-induced steroidogenesis of bovine thecal cells: involvement of glucose and receptors for insulin-like growth factor I and luteinizing hormone. J Anim Sci 73: 3719-3731.
33. Spicer LJ, Stewart RE, Alvarez P, Francisco CC, Keefer BE, (1997) Insulin-like growth factor-binding protein-2 and-3: their biological effects in bovine thecal cells. Biol Reprod 56: 1458-1465.
34. Mihm M, Good TE, Ireland JL, Ireland JJ, Knight PG, et al. (1997) Decline in serum follicle-stimulating hormone concentrations alters key intrafollicular growth factors involved in selection of the dominant follicle in heifers. Biol Reprod 57: 1328-1337.
35. Rivera GM, Fortune JE, (2001) Development of codominant follicles in cattle is associated with a follicle-stimulating hormone-dependent insulin-like growth factor binding protein-4 protease. Biol Reprod 65: 112-118.
36. Rivera GM, Fortune JE, (2003) Proteolysis of insulin-like growth factor binding proteins-4 and-5 in bovine follicular fluid: implications for ovarian follicular selection and dominance. Endocrinology 144: 2977-2987.
37. Rivera GM, Fortune JE, (2003) Selection of the dominant follicle and insulin-like growth factor (IGF)-binding proteins: evidence that pregnancy-associated plasma protein A contributes to proteolysis of IGF-binding protein 5 in bovine follicular fluid. Endocrinology 144: 437-446.
38. Jyotsna UR, Medhamurthy R, (2009) Standardization and validation of an induced ovulation model system in buffalo cows: Characterization of gene expression changes in the periovulatory follicle. Anim Reprod Sci 113: 71-81.
39. Oshlack A, Chabot AE, Smyth GK, Gilad Y, (2007) Using DNA microarrays to study gene expression in closely related species. Bioinformatics 23: 1235-1242.
40. Ji W, Zhou W, Gregg K, Yu N, Davis S, (2004) A method for cross-species gene expression analysis with high-density oligonucleotide arrays. Nucleic Acids Res 32: e93.
41. Nazar RN, Chen P, Dean D, Robb J, (2010) DNA chip analysis in diverse organisms with unsequenced genomes. Mol Biotechnol 44: 8-13.
42. Priyanka S, Jayaram P, Sridaran R, Medhamurthy R, (2009) Genome-wide gene expression analysis reveals a dynamic interplay between luteotropic and luteolytic factors in the regulation of corpus luteum function in the bonnet monkey (Macaca radiata). Endocrinology 150: 1473-1484.
43. Yadav VK, Sudhagar RR, Medhamurthy R, (2002) Apoptosis during spontaneous and prostaglandin F(2alpha)-induced luteal regression in the buffalo cow (Bubalus bubalis): involvement of mitogen-activated protein kinases. Biol Reprod 67: 752-759.
44. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
45. Reiner A, Yekutieli D, Benjamini Y, (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368-375.
46. Dai M, Wang P, Boyd AD, Kostov G, Athey B, et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33: e175.
47. Liu H, Zeeberg BR, Qu G, Koru AG, Ferrucci A, et al. (2007) AffyProbeMiner: a web resource for computing or retrieving accurately redefined Affymetrix probe sets. Bioinformatics 23: 2385-2390.
48. Komar CM, Berndtson AK, Evans AC, Fortune JE, (2001) Decline in circulating estradiol during the periovulatory period is correlated with decreases in estradiol and androgen, and in messenger RNA for p450 aromatase and p450 17alpha-hydroxylase, in bovine preovulatory follicles. Biol Reprod 64: 1797-1805.
49. Souza AH, Cunha AP, Silva EP, Gumen A, Ayres H, et al. (2009) Comparison of gonadorelin products in lactating dairy cows: efficacy based on induction of ovulation of an accessory follicle and circulating luteinizing hormone profiles. Theriogenology 72: 271-279.
50. Quirk SM, Cowan RG, Harman RM, (2004) Progesterone receptor and the cell cycle modulate apoptosis in granulosa cells. Endocrinology 145: 5033-5043.
51. Tilly JL, Tilly KI, Kenton ML, Johnson AL, (1995) Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology 136: 232-241.
52. Gonzalez IH, Santana P, Gonzalez-Robayna I, Ferrer M, Morales V, et al. (2007) Regulation of the expression of prostate apoptosis response protein 4 (Par-4) in rat granulosa cells. Apoptosis 12: 769-779.
53. 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.
54. Pru JK, Tilly JL, (2001) Programmed cell death in the ovary: insights and future prospects using genetic technologies. Mol Endocrinol 15: 845-853.
55. Schuur ER, Loktev AV, Sharma M, Sun Z, Roth RA, et al. (2001) Ligand-dependent interaction of estrogen receptor-alpha with members of the forkhead transcription factor family. J Biol Chem 276: 33554-33560.
56. Zhao HH, Herrera RE, Coronado-Heinsohn E, Yang MC, Ludes-Meyers JH, et al. (2001) Forkhead homologue in rhabdomyosarcoma functions as a bifunctional nuclear receptor-interacting protein with both coactivator and corepressor functions. J Biol Chem 276: 27907-27912.
57. Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG, et al. (2009) Angiogenesis and vascular function in the ovary. Reproduction 138: 869-881.
58. Mirza H, Yatsula V, Bahou WF, (1996) The proteinase activated receptor-2 (PAR-2) mediates mitogenic responses in human vascular endothelial cells. J Clin Invest 97: 1705-1714.
59. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, et al. (2000) Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6: 151-158.
60. McLean PG, Aston D, Sarkar D, Ahluwalia A, (2002) Protease-activated receptor-2 activation causes EDHF-like coronary vasodilation: selective preservation in ischemia/reperfusion injury: involvement of lipoxygenase products, VR1 receptors, and C-fibers. Circ Res 90: 465-472.
61. Shimo T, Nakanishi T, Nishida T, Asano M, Kanyama M, et al. (1999) Connective tissue growth factor induces the proliferation, migration, and tube formation of vascular endothelial cells in vitro, and angiogenesis in vivo. J Biochem 126: 137-145.
62. Brigstock DR, (1999) The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev 20: 189-206.
63. Babic AM, Chen CC, Lau LF, (1999) Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin alphavbeta3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 19: 2958-2966.
64. Harlow CR, Hillier SG, (2002) Connective tissue growth factor in the ovarian paracrine system. Mol Cell Endocrinol 187: 23-27.
65. Lorenzo P, Aspberg A, Onnerfjord P, Bayliss MT, Neame PJ, et al. (2001) Identification and characterization of asporin. a novel member of the leucine-rich repeat protein family closely related to decorin and biglycan. J Biol Chem 276: 12201-12211.
66. Henry SP, Takanosu M, Boyd TC, Mayne PM, Eberspaecher H, et al. (2001) Expression pattern and gene characterization of asporin. a newly discovered member of the leucine-rich repeat protein family. J Biol Chem 276: 12212-12221.
67. Nakajima M, Kizawa H, Saitoh M, Kou I, Miyazono K, et al. (2007) Mechanisms for asporin function and regulation in articular cartilage. J Biol Chem 282: 32185-32192.
68. Tomoeda M, Yamada S, Shirai H, Ozawa Y, Yanagita M, et al. (2008) PLAP-1/asporin inhibits activation of BMP receptor via its leucine-rich repeat motif. Biochem Biophys Res Commun 371: 191-196.
69. DeClerck YA, Laug WE, (1996) Cooperation between matrix metalloproteinases and the plasminogen activator-plasmin system in tumor progression. Enzyme Protein 49: 72-84.
70. Mazzieri R, Masiero L, Zanetta L, Monea S, Onisto M, et al. (1997) Control of type IV collagenase activity by components of the urokinase-plasmin system: a regulatory mechanism with cell-bound reactants. EMBO J 16: 2319-2332.
71. Lijnen HR, Van Hoef B, Lupu F, Moons L, Carmeliet P, et al. (1998) Function of the plasminogen/plasmin and matrix metalloproteinase systems after vascular injury in mice with targeted inactivation of fibrinolytic system genes. Arterioscler Thromb Vasc Biol 18: 1035-1045.
72. Makowski GS, Ramsby ML, (1998) Binding of latent matrix metalloproteinase 9 to fibrin: activation via a plasmin-dependent pathway. Inflammation 22: 287-305.
73. Cao M, Buratini J Jr, Lussier JG, Carriere PD, Price CA, (2006) Expression of protease nexin-1 and plasminogen activators during follicular growth and the periovulatory period in cattle. Reproduction 131: 125-137.
74. Zheng X, Boerboom D, Carriere PD, (2009) Transforming growth factor-beta1 inhibits luteinization and promotes apoptosis in bovine granulosa cells. Reproduction 137: 969-977.
75. Cadigan KM, Nusse R, (1997) Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-3305.
76. Miller JR, Hocking AM, Brown JD, Moon RT, (1999) Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene 18: 7860-7872.
77. Keel BA, Hildebrandt JM, May JV, Davis JS, (1995) Effects of epidermal growth factor on the tyrosine phosphorylation of mitogen-activated protein kinases in monolayer cultures of porcine granulosa cells. Endocrinology 136: 1197-1204.
78. Fan HY, O'Connor A, Shitanaka M, Shimada M, Liu Z, et al. (2010) Beta-Catenin (CTNNB1) Promotes Preovulatory Follicular Development but Represses LH-Mediated Ovulation and Luteinization. Mol Endocrinol 24: 1529-1542.
79. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP, (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397: 405-409.
80. Hsieh M, Johnson MA, Greenberg NM, Richards JS, (2002) Regulated expression of Wnts and Frizzleds at specific stages of follicular development in the rodent ovary. Endocrinology 143: 898-908.
81. Funston RN, Seidel GE Jr, Klindt J, Roberts AJ, (1996) Insulin-like growth factor I and insulin-like growth factor-binding proteins in bovine serum and follicular fluid before and after the preovulatory surge of luteinizing hormone. Biol Reprod 55: 1390-1396.
82. Holtorf AP, Furuya K, Ivell R, McArdle CA, (1989) Oxytocin production and oxytocin messenger ribonucleic acid levels in bovine granulosa cells are regulated by insulin and insulin-like growth factor-I: dependence on developmental status of the ovarian follicle. Endocrinology 125: 2612-2620.
83. Engelhardt H, Gore-Langton RE, Armstrong DT, (1991) Luteinization of porcine thecal cells in vitro. Mol Cell Endocrinol 75: 237-245.
84. Lorenzo PL, Illera MJ, Illera JC, Illera M, (1994) Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. J Reprod Fertil 101: 697-701.
85. Singh B, Armstrong DT, (1997) Insulin-like growth factor-1, a component of serum that enables porcine cumulus cells to expand in response to follicle-stimulating hormone in vitro. Biol Reprod 56: 1370-1375.
86. Rieger D, Luciano AM, Modina S, Pocar P, Lauria A, et al. (1998) The effects of epidermal growth factor and insulin-like growth factor I on the metabolic activity, nuclear maturation and subsequent development of cattle oocytes in vitro. J Reprod Fertil 112: 123-130.
87. Nemcova L, Nagyova E, Petlach M, Tomanek M, Prochazka R, (2007) Molecular mechanisms of insulin-like growth factor 1 promoted synthesis and retention of hyaluronic acid in porcine oocyte-cumulus complexes. Biol Reprod 76: 1016-1024.
88. Nagyova E, Prochazka R, Vanderhyden BC, (1999) Oocytectomy does not influence synthesis of hyaluronic acid by pig cumulus cells: retention of hyaluronic acid after insulin-like growth factor-I treatment in serum-free medium. Biol Reprod 61: 569-574.
89. Ginther OJ, Bergfelt DR, Beg MA, Meira C, Kot K, (2004) In vivo effects of an intrafollicular injection of insulin-like growth factor 1 on the mechanism of follicle deviation in heifers and mares. Biol Reprod 70: 99-105.
90. Kirby CJ, Thatcher WW, Collier RJ, Simmen FA, Lucy MC, (1996) Effects of growth hormone and pregnancy on expression of growth hormone receptor, insulin-like growth factor-I, and insulin-like growth factor binding protein-2 and-3 genes in bovine uterus, ovary, and oviduct. Biol Reprod 55: 996-1002.
91. Rhoads ML, Meyer JP, Kolath SJ, Lamberson WR, Lucy MC, (2008) Growth hormone receptor, insulin-like growth factor (IGF)-1, and IGF-binding protein-2 expression in the reproductive tissues of early postpartum dairy cows. J Dairy Sci 91: 1802-1813.
92. Kolle S, Sinowatz F, Boie G, Lincoln D, (1998) Developmental changes in the expression of the growth hormone receptor messenger ribonucleic acid and protein in the bovine ovary. Biol Reprod 59: 836-842.
93. de la Sota RL, Simmen FA, Diaz T, Thatcher WW, (1996) Insulin-like growth factor system in bovine first-wave dominant and subordinate follicles. Biol Reprod 55: 803-812.
94. Spicer LJ, Echternkamp SE, Canning SF, Hammond JM, (1988) Relationship between concentrations of immunoreactive insulin-like growth factor-I in follicular fluid and various biochemical markers of differentiation in bovine antral follicles. Biol Reprod 39: 573-580.
95. Sudo N, Shimizu T, Kawashima C, Kaneko E, Tetsuka M, et al. (2007) Insulin-like growth factor-I (IGF-I) system during follicle development in the bovine ovary: relationship among IGF-I, type 1 IGF receptor (IGFR-1) and pregnancy-associated plasma protein-A (PAPP-A). Mol Cell Endocrinol 264: 197-203.
96. Echternkamp SE, Howard HJ, Roberts AJ, Grizzle J, Wise T, (1994) Relationships among concentrations of steroids, insulin-like growth factor-I, and insulin-like growth factor binding proteins in ovarian follicular fluid of beef cattle. Biol Reprod 51: 971-981.
97. Rivera GM, Chandrasekher YA, Evans AC, Giudice LC, Fortune JE, (2001) A potential role for insulin-like growth factor binding protein-4 proteolysis in the establishment of ovarian follicular dominance in cattle. Biol Reprod 65: 102-111.
98. Claussen M, Kubler B, Wendland M, Neifer K, Schmidt B, et al. (1997) Proteolysis of insulin-like growth factors (IGF) and IGF binding proteins by cathepsin D. Endocrinology 138: 3797-3803.
99. Iwashita M, Kudo Y, Takeda Y, (1998) Effect of follicle stimulating hormone and insulin-like growth factors on proteolysis of insulin-like growth factor binding protein-4 in human granulosa cells. Mol Hum Reprod 4: 401-405.
100. Firth SM, Baxter RC, (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23: 824-854.
101. Manna PR, Chandrala SP, King SR, Jo Y, Counis R, et al. (2006) Molecular mechanisms of insulin-like growth factor-I mediated regulation of the steroidogenic acute regulatory protein in mouse leydig cells. Mol Endocrinol 20: 362-378.
102. Grado-Ahuir JA, Aad PY, Ranzenigo G, Caloni F, Cremonesi F, et al. (2009) Microarray analysis of insulin-like growth factor-I-induced changes in messenger ribonucleic acid expression in cultured porcine granulosa cells: possible role of insulin-like growth factor-I in angiogenesis. J Anim Sci 87: 1921-1933.
103. Sekar N, Lavoie HA, Veldhuis JD, (2000) Concerted regulation of steroidogenic acute regulatory gene expression by luteinizing hormone and insulin (or insulin-like growth factor I) in primary cultures of porcine granulosa-luteal cells. Endocrinology 141: 3983-3992.
104. Sekar N, Garmey JC, Veldhuis JD, (2000) Mechanisms underlying the steroidogenic synergy of insulin and luteinizing hormone in porcine granulosa cells: joint amplification of pivotal sterol-regulatory genes encoding the low-density lipoprotein (LDL) receptor, steroidogenic acute regulatory (stAR) protein and cytochrome P450 side-chain cleavage (P450scc) enzyme. Mol Cell Endocrinol 159: 25-35.
105. Natesampillai S, Kerkvliet J, Leung PC, Veldhuis JD, (2008) Regulation of Kruppel-like factor 4, 9, and 13 genes and the steroidogenic genes LDLR, StAR, and CYP11A in ovarian granulosa cells. Am J Physiol Endocrinol Metab 294: E385-391.
106. Schams D, Koll R, Li CH, (1988) Insulin-like growth factor-I stimulates oxytocin and progesterone production by bovine granulosa cells in culture. J Endocrinol 116: 97-100.
107. McArdle CA, Kohl C, Rieger K, Groner I, Wehrenberg U, (1991) Effects of gonadotropins, insulin and insulin-like growth factor I on ovarian oxytocin and progesterone production. Mol Cell Endocrinol 78: 211-220.
108. Meidan R, Altstein M, Girsh E, (1992) Biosynthesis and release of oxytocin by granulosa cells derived from preovulatory bovine follicles: effects of forskolin and insulin-like growth factor-I. Biol Reprod 46: 715-720.
109. Chrysis D, Calikoglu AS, Ye P, D'Ercole AJ, (2001) Insulin-like growth factor-I overexpression attenuates cerebellar apoptosis by altering the expression of Bcl family proteins in a developmentally specific manner. J Neurosci 21: 1481-1489.
110. Hilmi C, Larribere L, Giuliano S, Bille K, Ortonne JP, et al. (2008) IGF1 promotes resistance to apoptosis in melanoma cells through an increased expression of BCL2, BCL-X(L), and survivin. J Invest Dermatol 128: 1499-1505.
111. 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.
112. Park Y, Maizels ET, Feiger ZJ, Alam H, Peters CA, et al. (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.
113. Hsieh CL, Vogel US, Dixon RA, Francke U, (1989) Chromosome localization and cDNA sequence of murine and human genes for ras p21 GTPase activating protein (GAP). Somat Cell Mol Genet 15: 579-590.
114. Eerola I, Boon LM, Mulliken JB, Burrows PE, Dompmartin A, et al. (2003) Capillary malformation-arteriovenous malformation, a new clinical and genetic disorder caused by RASA1 mutations. Am J Hum Genet 73: 1240-1249.
115. Sharma SC, Richards JS, (2000) Regulation of AP1 (Jun/Fos) factor expression and activation in ovarian granulosa cells. Relation of JunD and Fra2 to terminal differentiation. J Biol Chem 275: 33718-33728.