Developmental programming: Effect of prenatal steroid excess on intraovarian components of insulin signaling pathway and related proteins in sheep

Biology of Reproduction

Volumn 82, Issue 6, 2010, Pages 1065-1075

  Ortega, Hugo H ^a   Rey, Florencia ^a,b   Velazquez, Melisa M L ^a   Padmanabhan, Vasantha ^c  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Developmental biology; Fetal programming; Follicular development; Insulin; Ovary; PCOS; Sheep

Indexed keywords

ADIPONECTIN; ANDROSTANOLONE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; MAMMALIAN TARGET OF RAPAMYCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3 KINASE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HYPERINSULINEMIA; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; NONHUMAN; OVARY FOLLICLE; PRENATAL DEVELOPMENT; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEEP; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADIPONECTIN; ANIMALS; DIHYDROTESTOSTERONE; FEMALE; FETUS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; OVARY; POLYCYSTIC OVARY SYNDROME; PPAR GAMMA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, INSULIN; SHEEP; SIGNAL TRANSDUCTION; TESTOSTERONE;

MAMMALIA; OVIS ARIES;

EID: 77953857781     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.082719     Document Type: Article

References (71)

1. Webb R, Campbell BK. Development of the dominant follicle: mechanisms of selection and maintenance of oocyte quality. Soc Reprod Fertil Suppl 2007; 64:141-163.
2. Padmanabhan V, Manikkam M, Recabarren S, Foster D. Prenatal testosterone excess programs reproductive and metabolic dysfunction in the female. Mol Cell Endocrinol 2006; 246:165-174.
3. Abbott DH, Padmanabhan V, Dumesic DA. Contributions of androgen and estrogen to fetal programming of ovarian dysfunction. Reprod Biol Endocrinol 2006; 4:17.
4. Dumesic DA, Abbott DH, Padmanabhan V. Polycystic ovary syndrome and its developmental origins. Rev Endocr Metab Disord 2007; 8:127-141.
5. Dunaif A. Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev 1997; 18:774-800.
6. Rosenfield RL. Current concepts of polycystic ovary syndrome. Baillieres Clin Obstet Gynaecol 1997; 11:307-333.
7. Franks S, McCarthy MI, Hardy K. Development of polycystic ovary syndrome: involvement of genetic and environmental factors. Int J Androl 2006; 29:278-285.
8. West C, Foster DL, Evans NP, Robinson J, Padmanabhan V. Intrafollicular activin availability is altered in prenatally-androgenized lambs. Mol Cell Endocrinol 2001; 185:51-59.
9. Smith P, Steckler TL, Veiga-Lopez A, Padmanabhan V. Developmental programming: differential effects of prenatal testosterone and dihydrotestosterone on follicular recruitment, depletion of follicular reserve, and ovarian morphology in sheep. Biol Reprod 2009; 80:726-736.
10. Manikkam M, Steckler TL, Welch KB, Inskeep EK, Padmanabhan V. Fetal programming: prenatal testosterone treatment leads to follicular persistence/luteal defects; partial restoration of ovarian function by cyclic progesterone treatment. Endocrinology 2006; 147:1997-2007.
11. Steckler T, Manikkam M, Inskeep EK, Padmanabhan V. Developmental programming: follicular persistence in prenatal testosterone-treated sheep is not programmed by androgenic actions of testosterone. Endocrinology 2007; 148:3532-3540.
12. Ortega HH, Salvetti NR, Padmanabhan V. Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance. Reproduction 2009; 137:865-877.
13. Recabarren SE, Padmanabhan V, Codner E, Lobos A, Durán C, Vidal M, Foster DL, Sirpetermann T. Postnatal developmental consequences of altered insulin sensitivity in female sheep treated prenatally with testosterone. Am J Physiol Endocrinol Metab 2005; 289:801-806.
14. Willis D, Mason H, Gilling-Smith C, Franks S. Modulation by insulin of follicle-stimulating hormone and luteinizing hormone actions in human granulosa cells of normal and polycystic ovaries. J Clin Endocrinol Metab 1996; 81:302-309.
15. Adashi EY, Resnick CE, Payne DW, Rosenfeld RG, Matsumoto T, Hunter MK, Gargosky SE, Zhou J, Bondy CA. The mouse intraovarian insulin-like growth factor I system: departures from the rat paradigm. Endocrinology 1997; 138:3881-3890.
16. Poretsky L, Cataldo NA, Rosenwaks Z, Giudice LC. The insulin-related ovarian regulatory system in health and disease. Endocr Rev 1999; 20: 535-582. (Pubitemid 30647079)
17. Neganova I, Al-Qassab H, Heffron H, Selman C, Choudhury AI, Lingard SJ, Diakonov I, Patterson M, Ghatei M, Bloom SR, Franks S, Huhtaniemi I, et al. Role of central nervous system and ovarian insulin receptor substrate 2 signaling in female reproductive function in the mouse. Biol Reprod 2007; 76:1045-1053.
18. Ledoux S, Campos DB, Lopes FL, Dobias-Goff M, Palin MF, Murphy BD. Adiponectin induces periovulatory changes in ovarian follicular cells. Endocrinology 2006; 147:5178-5186.
19. Seto-Young D, Avtanski D, Strizhevsky M, Parikh G, Patel P, Kaplun J, Holcomb K, Rosenwaks Z, Poretsky L. Interactions among peroxisome proliferator activated receptor-gamma, insulin signaling pathways, and steroidogenic acute regulatory protein in human ovarian cells. J Clin Endocrinol Metab 2007; 92:2232-2239.
20. Baba T, Endo T, Sata F, Honnma H, Kitajima Y, Hayashi T, Manase K, Kanaya M, Yamada H, Minakami H, Kishi R, Saito T. Polycystic ovary syndrome is associated with genetic polymorphism in the insulin signaling gene IRS-1 but not ENPP1 in a Japanese population. Life Sci 2007; 81: 850-854.
21. Kayampilly PP, Menon KM. Dihydrotestosterone inhibits insulin-stimulated cyclin D2 messenger ribonucleic acid expression in rat ovarian granulosa cells by reducing the phosphorylation of insulin receptor substrate-1. Endocrinology 2006; 147:464-471.
22. Yaba A, Bianchi V, Borini A, Johnson J. A putative mitotic checkpoint dependent on mTOR function controls cell proliferation and survival in ovarian granulosa cells. Reprod Sci 2008; 15:128-138.
23. Dunaif A, Thomas A. Current concepts in the polycystic ovary syndrome. Annu Rev Med 2001; 52:401-419.
24. Ardawi MS, Rouzi AA. Plasma adiponectin and insulin resistance in women with polycystic ovary syndrome. Fertil Steril 2005; 83:1708-1716.
25. Barber TM, McCarthy MI, Wass JA, Franks S. Obesity and polycystic ovary syndrome. Clin Endocrinol (Oxf) 2006; 65:137-145.
26. Qu J, Wang Y, Wu X, Gao L, Hou L, Erkkola R. Insulin resistance directly contributes to androgenic potential within ovarian theca cells. Fertil Steril 2009; 91:1990-1997.
27. Burks DJ, Font de MJ, Schubert M, Withers DJ, Myers MG, Towery HH, Altamuro SL, Flint CL, White MF. IRS-2 pathways integrate female reproduction and energy homeostasis. Nature 2000; 407:377-382.
28. Kim J, Sato M, Li Q, Lydon JP, Demayo FJ, Bagchi IC, Bagchi MK. Peroxisome proliferator-activated receptor gamma is a target of progesterone regulation in the preovulatory follicles and controls ovulation in mice. Mol Cell Biol 2008; 28:1770-1782.
29. Cui Y, Miyoshi K, Claudio E, Siebenlist UK, Gonzalez FJ, Flaws J, Wagner KU, Hennighausen L. Loss of the peroxisome proliferation-activated receptor gamma (PPARgamma) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J Biol Chem 2002; 277:17830-17835.
30. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001; 414:799-806.
31. Lizcano JM, Alessi DR. The insulin signalling pathway. Curr Biol 2002; 12:R236-R238.
32. Alam H, Weck J, Maizels E, Park Y, Lee EJ, Ashcroft M, Hunzicker-Dunn M. Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 2009; 150:915-928.
33. Carvalho CR, Carvalheira JB, Lima MH, Zimmerman SF, Caperuto LC, Amanso A, Gasparetti AL, Meneghetti V, Zimmerman LF, Velloso LA, Saad MJ. Novel signal transduction pathway for luteinizing hormone and its interaction with insulin: activation of Janus kinase/signal transducer and activator of transcription and phosphoinositol 3-kinase/Akt pathways. Endocrinology 2003; 144:638-647.
34. Lima MH, Souza LC, Caperuto LC, Bevilacqua E, Gasparetti AL, Zanuto R, Saad MJ, Carvalho CR. Up-regulation of the phosphatidylinositol 3-kinase/protein kinase B pathway in the ovary of rats by chronic treatment with hCG and insulin. J Endocrinol 2006; 190:451-459.
35. Yen HW, Jakimiuk AJ, Munir I, Magoffin DA. Selective alterations in insulin receptor substrates-1, -2 and -4 in theca but not granulosa cells from polycystic ovaries. Mol Hum Reprod 2004; 10:473-479.
36. Diamanti-Kandarakis E, Argyrakopoulou G, Economou F, Kandaraki E, Koutsilieris M. Defects in insulin signaling pathways in ovarian steroidogenesis and other tissues in polycystic ovary syndrome (PCOS). J Steroid Biochem Mol Biol 2008; 109:242-246.
37. Samoto T, Maruo T, Ladines-Llave CA, Matsuo H, Deguchi J, Barnea ER, Mochizuki M. Insulin receptor expression in follicular and stromal compartments of the human ovary over the course of follicular growth, regression and atresia. Endocr J 1993; 40:715-726. (Pubitemid 24085039)
38. Willis D, Franks S. Insulin action in human granulosa cells from normal and polycystic ovaries is mediated by the insulin receptor and not the type-I insulin-like growth factor receptor. J Clin Endocrinol Metab 1995; 80: 3788-3790.
39. Phy JL, Conover CA, Abbott DH, Zschunke MA, Walker DL, Session DR, Tummon IS, Thornhill AR, Lesnick TG, Dumesic DA. Insulin and messenger ribonucleic acid expression of insulin receptor isoforms in ovarian follicles from nonhirsute ovulatory women and polycystic ovary syndrome patients. J Clin Endocrinol Metab 2004; 89:3561-3566.
40. Seli E, Duleba AJ. Treatment of PCOS with metformin and other insulin-sensitizing agents. Curr Diab Rep 2004; 4:69-75. (Pubitemid 39359513)
41. Stout DL, Fugate SE. Thiazolidinediones for treatment of polycystic ovary syndrome. Pharmacotherapy 2005; 25:244-252.
42. Elkind-Hirsch KE. Thiazolidinediones for the therapeutic management of polycystic ovary syndrome: impact on metabolic and reproductive abnormalities. Treat Endocrinol 2006; 5:171-187.
43. Steckler TL, Herkimer C, Dumesic DA, Padmanabhan V. Developmental programming: excess weight gain amplifies the effects of prenatal testosterone excess on reproductive cyclicity - implication for polycystic ovary syndrome. Endocrinology 2009; 150:1456-1465.
44. Chabrolle C, Tosca L, Dupont J. Regulation of adiponectin and its receptors in rat ovary by human chorionic gonadotrophin treatment and potential involvement of adiponectin in granulosa cell steroidogenesis. Reproduction 2007; 133:719-731.
45. Sieminska L, Marek B, Kos-Kudla B, Niedziolka D, Kajdaniuk D, Nowak M, Glogowska-Szelag J. Serum adiponectin in women with polycystic ovarian syndrome and its relation to clinical, metabolic and endocrine parameters. J Endocrinol Invest 2004; 27:528-534.
46. Panidis D, Farmakiotis D, Rousso D, Koliakos G, Kaltsas T, Krassas G. Decrease in adiponectin levels in women with polycystic ovary syndrome after an oral glucose tolerance test. Fertil Steril 2005; 83:232-234.
47. Sepilian V, Nagamani M. Adiponectin levels in women with polycystic ovary syndrome and severe insulin resistance. J Soc Gynecol Investig 2005; 12:129-134. (Pubitemid 40202849)
48. Escobar-Morreale HF, Villuendas G, Botella-Carretero JI, Alvarez-Blasco F, Sanchon R, Luque-Ramirez M, San Millan JL. Adiponectin and resistin in PCOS: a clinical, biochemical and molecular genetic study. Hum Reprod 2006; 21:2257-2265.
49. Aroda V, Ciaraldi TP, Chang SA, Dahan MH, Chang RJ, Henry RR. Circulating and cellular adiponectin in polycystic ovary syndrome: relationship to glucose tolerance and insulin action. Fertil Steril 2008; 89:1200-1208.
50. Manikkam M, Crespi EJ, Doop DD, Herkimer C, Lee JS, Yu S, Brown MB, Foster DL, Padmanabhan V. Fetal programming: prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 2004; 145:790-798.
51. Steckler TL, Lee JS, Ye W, Inskeep EK, Padmanabhan V. Developmental programming: exogenous gondadotropin treatment rescues ovulatory function but does not completely normalize ovarian function in sheep treated prenatally with testosterone. Biol Reprod 2008; 79:686-695.
52. Zhu LJ, Hardy MP, Inigo IV, Huhtaniemi I, Bardin CW, Moo-Young AJ. Effects of androgen on androgen receptor expression in rat testicular and epididymal cells: a quantitative immunohistochemical study. Biol Reprod 2000; 63:368-376. (Pubitemid 30639921)
53. Lejeune M, Jaen J, Pons L, Lopez C, Salvado MT, Bosch R, Garcia M, Escriva P, Baucells J, Cugat X, Alvaro T. Quantification of diverse subcellular immunohistochemical markers with clinicobiological relevancies: validation of a new computer-assisted image analysis procedure. J Anat 2008; 212:868-878.
54. Pham NA, Morrison A, Schwock J, Aviel-Ronen S, Iakovlev V, Tsao MS, Ho J, Hedley DW. Quantitative image analysis of immunohistochemical stains using a CMYK color model. Diagn Pathol 2007; 2:8.
55. Theodosiou Z, Kasampalidis IN, Livanos G, Zervakis M, Pitas I, Lyroudia K. Automated analysis of FISH and immunohistochemistry images: a review. Cytometry A 2007; 71:439-450.
56. Peretti-Renucci R, Feuerstein C, Manier M, Lorimier P, Savasta M, Thibault J, Mons N, Geffard M. Quantitative image analysis with densitometry for immunohistochemistry and autoradiography of receptor binding sites - methodological considerations. J Neurosci Res 1991; 28:583-600.
57. Alam H, Maizels ET, Park Y, Ghaey S, Feiger ZJ, Chandel NS, Hunzicker-Dunn M. Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT/Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation. J Biol Chem 2004; 279:19431-19440.
58. Kowalewski MP, Dyson MT, Manna PR, Stocco DM. Involvement of peroxisome proliferator-activated receptor gamma in gonadal steroidogenesis and steroidogenic acute regulatory protein expression. Reprod Fertil Dev 2009; 21:909-922.
59. Lord E, Ledoux S, Murphy BD, Beaudry D, Palin MF. Expression of adiponectin and its receptors in swine. J Anim Sci 2005; 83:565-578. (Pubitemid 43324065)
60. Yamauchi T, Kamon J, Waki H, Murakami K, Motojima K, Komeda K, Ide T, Kubota N, Terauchi Y, Tobe K, Miki H, Tsuchida A, et al. The mechanisms by which both heterozygous peroxisome proliferator-activated receptor gamma (PPARgamma) deficiency and PPARgamma agonist improve insulin resistance. J Biol Chem 2001; 276:41245-41254.
61. Nawrocki AR, Rajala MW, Tomas E, Pajvani UB, Saha AK, Trumbauer ME, Pang Z, Chen AS, Ruderman NB, Chen H, Rossetti L, Scherer PE. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J Biol Chem 2006; 281:2654-2660.
62. Lagaly DV, Aad PY, Grado-Ahuir JA, Hulsey LB, Spicer LJ. Role of adiponectin in regulating ovarian theca and granulosa cell function. Mol Cell Endocrinol 2008; 284:38-45.
63. Ma K, Cabrero A, Saha PK, Kojima H, Li L, Chang BH, Paul A, Chan L. Increased beta-oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J Biol Chem 2002; 277:34658-34661.
64. Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, Ito Y, Kamon J, et al. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 2007; 13:332-339.
65. Schoppee PD, Garmey JC, Veldhuis JD. Putative activation of the peroxisome proliferator-activated receptor gamma impairs androgen and enhances progesterone biosynthesis in primary cultures of porcine theca cells. Biol Reprod 2002; 66:190-198.
66. Komar CM, Curry TE Jr. Localization and expression of messenger RNAs for the peroxisome proliferator-activated receptors in ovarian tissue from naturally cycling and pseudopregnant rats. Biol Reprod 2002; 66:1531-1539.
67. Panidis D, Kourtis A, Farmakiotis D, Mouslech T, Rousso D, Koliakos G. Serum adiponectin levels in women with polycystic ovary syndrome. Hum Reprod 2003; 18:1790-1796.
68. Escobar-Morreale HF, Luque-Ramirez M, San Millan JL. The molecular-genetic basis of functional hyperandrogenism and the polycystic ovary syndrome. Endocr Rev 2005; 26:251-282.
69. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, Tataranni PA. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab 2001; 86:1930-1935.
70. Ranheim T, Haugen F, Staff AC, Braekke K, Harsem NK, Drevon CA. Adiponectin is reduced in gestational diabetes mellitus in normal weight women. Acta Obstet Gynecol Scand 2004; 83:341-347.
71. Padmanabhan V, Veiga-Lopez A, Abbott D, Recabarren S, Herkimer C. Developmental programming: impact of prenatal testosterone excess and postnatal weight gain on insulin sensitivity index and transfer of traits to offspring of overweight females. Endocrinology 2009; 151:595-605.