Genetic factors modulate the impact of pubertal androgen excess on insulin sensitivity and fertility

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Dowling, Abigail R ^a   Nedorezov, Laura B ^a   Qiu, Xiaoliang ^a   Marino, Joseph S ^c   Hill, Jennifer W ^a,b  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF TOLEDO MEDICAL CENTER   (United States)

^c UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGENS; ANIMALS; BLOTTING, WESTERN; ESTROUS CYCLE; FEMALE; HUMANS; INSULIN RESISTANCE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OVARY; POLYCYSTIC OVARY SYNDROME;

EID: 84894286117     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079849     Document Type: Article

References (83)

1. Solano ME, Sander VA, Ho H, Motta AB, Arck PC (2011) Systemic inflammation, cellular influx and up-regulation of ovarian VCAM-1 expression in a mouse model of polycystic ovary syndrome (PCOS). J Reprod Immunol 92: 33-44.
2. Franks S, Gilling-Smith C, Watson H, Willis D (1999) Insulin action in the normal and polycystic ovary. Endocrinol Metab Clin North Am 28: 361-378. (Pubitemid 29242718)
3. Broekmans FJ, Knauff EA, Valkenburg O, Laven JS, Eijkemans MJ, et al. (2006) PCOS according to the Rotterdam consensus criteria: Change in prevalence among WHO-II anovulation and association with metabolic factors. BJOG 113: 1210-1217. (Pubitemid 44401217)
4. Liu N, Ma Y, Wang S, Zhang X, Zhang Q, et al. (2012) Association of the genetic variants of luteinizing hormone, luteinizing hormone receptor and polycystic ovary syndrome. Reprod Biol Endocrinol 10: 36.
5. Zhao H, Xu X, Xing X, Wang J, He L, et al. (2012) Family-based analysis of susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Hum Reprod 27: 294-298.
6. Calogero AE, Calabro V, Catanuso M, Condorelli RA, La Vignera S (2011) Understanding polycystic ovarian syndrome pathogenesis: an updated of its genetic aspects. J Endocrinol Invest 34: 630-644.
7. Kahsar-Miller MD, Nixon C, Boots LR, Go RC, Azziz R (2001) Prevalence of polycystic ovary syndrome (PCOS) in first-degree relatives of patients with PCOS. Fertil Steril 75: 53-58. (Pubitemid 32042114)
8. Mahesh VB, Greenblatt RB (1962) Isolation of dehydroepiandrosterone and 17alpha-hydroxy-delta5-pregenolone from the polycystic ovaries of the Stein-Leventhal syndrome. J Clin Endocrinol Metab 22: 441-448.
9. Bernal-Mizrachi C, Weng S, Feng C, Finck BN, Knutsen RH, et al. (2003) Dexamethasone induction of hypertension and diabetes is PPAR-alpha dependent in LDL receptor-null mice. Nat Med 9: 1069-1075. (Pubitemid 37021788)
10. Roy S, Mahesh VB, Greenblatt RB (1962) Effect of dehydroepiandrosterone and delta4-androstenedione on the reproductive organs of female rats: production of cystic changes in the ovary. Nature 196: 42-43.
11. Luchetti CG, Solano ME, Sander V, Arcos ML, Gonzalez C, et al. (2004) Effects of dehydroepiandrosterone on ovarian cystogenesis and immune function. J Reprod Immunol 64: 59-74. (Pubitemid 39642853)
12. Goren HJ, Kulkarni RN, Kahn CR (2004) Glucose homeostasis and tissue transcript content of insulin signaling intermediates in four inbred strains of mice: C57BL/6, C57BLKS/6, DBA/2, and 129X1. Endocrinology 145: 3307-3323. (Pubitemid 38830003)
13. Paigen B, Mitchell D, Holmes PA, Albee D (1987) Genetic analysis of strains C57BL/6J and BALB/cJ for Ath-1, a gene determining atherosclerosis susceptibility in mice. Biochem Genet 25: 881-892. (Pubitemid 18068340)
14. Alexander J, Chang GQ, Dourmashkin JT, Leibowitz SF (2006) Distinct phenotypes of obesity-prone AKR/J, DBA2J and C57BL/6J mice compared to control strains. Int J Obes (Lond) 30: 50-59. (Pubitemid 41790777)
15. Elia EM, Belgorosky D, Faut M, Vighi S, Pustovrh C, et al. (2009) The effects of metformin on uterine tissue of hyperandrogenized BALB/c mice. Mol Hum Reprod 15: 421-432.
16. Belgorosky D, Sander VA, Yorio MP, Faletti AG, Motta AB (2010) Hyperandrogenism alters intraovarian parameters during early folliculogenesis in mice. Reprod Biomed Online 20: 797-807.
17. Sander V, Solano ME, Elia E, Luchetti CG, Di Girolamo G, et al. (2005) The influence of dehydroepiandrosterone on early pregnancy in mice. Neuroimmunomodulation 12: 285-292. (Pubitemid 41318211)
18. Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE (1982) A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology. Biol Reprod 27: 327-339. (Pubitemid 13230807)
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
20. Mahesh VB, Greenblatt RB (1964) Steroid Secretions of the Normal and Polycystic Ovary. Recent Prog Horm Res 20: 341-394.
21. Motta AB (2010) Dehydroepiandrosterone to induce murine models for the study of polycystic ovary syndrome. J Steroid Biochem Mol Biol 119: 105-111.
22. Jansen E, Laven JS, Dommerholt HB, Polman J, van Rijt C, et al. (2004) Abnormal gene expression profiles in human ovaries from polycystic ovary syndrome patients. Mol Endocrinol 18: 3050-3063. (Pubitemid 39577925)
23. Biyasheva A, Legro RS, Dunaif A, Urbanek M (2009) Evidence for association between polycystic ovary syndrome (PCOS) and TCF7L2 and glucose intolerance in women with PCOS and TCF7L2. J Clin Endocrinol Metab 94: 2617-2625.
24. Ewens KG, Stewart DR, Ankener W, Urbanek M, McAllister JM, et al. (2010) Family-based analysis of candidate genes for polycystic ovary syndrome. J Clin Endocrinol Metab 95: 2306-2315.
25. Urbanek M (2007) The genetics of the polycystic ovary syndrome. Nat Clin Pract Endocrinol Metab 3: 103-111.
26. Cunliffe-Beamer TL, Feldman DB (1976) Vaginal septa in mice: incidence, inheritance, and effect on reproductive, performance. Lab Anim Sci 26: 895-898.
27. Gearhart S, Kalishman J, Melikyan H, Mason C, Kohn DF (2004) Increased incidence of vaginal septum in C57BL/6J mice since 1976. Comp Med 54: 418-421. (Pubitemid 39096029)
28. Kryshkina VP, Malashenko AM (1975) [Fecundity and embryonal mortality of four inbred strains of mice, BALB/c, B10.CW, A/Sn, CC57W and their hybrids]. Genetika 11: 68-73.
29. Botcherby M (2002) Harvesting the mouse genome. Comp Funct Genomics 3: 319-324.
30. Kaku K, Fiedorek FT, Jr., Province M, Permutt MA (1988) Genetic analysis of glucose tolerance in inbred mouse strains. Evidence for polygenic control. Diabetes 37: 707-713. (Pubitemid 19043176)
31. Kooptiwut S, Zraika S, Thorburn AW, Dunlop ME, Darwiche R, et al. (2002) Comparison of insulin secretory function in two mouse models with different susceptibility to beta-cell failure. Endocrinology 143: 2085-2092. (Pubitemid 34521556)
32. Toye AA, Lippiat JD, Proks P, Shimomura K, Bentley L, et al. (2005) A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia 48: 675-686. (Pubitemid 40591223)
33. Surwit RS, Feinglos MN, Rodin J, Sutherland A, Petro AE, et al. (1995) Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice. Metabolism 44: 645-651.
34. Petro AE, Cotter J, Cooper DA, Peters JC, Surwit SJ, et al. (2004) Fat, carbohydrate, and calories in the development of diabetes and obesity in the C57BL/6J mouse. Metabolism 53: 454-457. (Pubitemid 38419187)
35. Black BL, Croom J, Eisen EJ, Petro AE, Edwards CL, et al. (1998) Differential effects of fat and sucrose on body composition in A/J and C57BL/6 mice. Metabolism 47: 1354-1359. (Pubitemid 28523467)
36. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN (1988) Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37: 1163-1167. (Pubitemid 19035045)
37. Surwit RS, Seldin MF, Kuhn CM, Cochrane C, Feinglos MN (1991) Control of expression of insulin resistance and hyperglycemia by different genetic factors in diabetic C57BL/6J mice. Diabetes 40: 82-87.
38. Burcelin R, Crivelli V, Dacosta A, Roy-Tirelli A, Thorens B (2002) Heterogeneous metabolic adaptation of C57BL/6J mice to high-fat diet. Am J Physiol Endocrinol Metab 282: E834-842. (Pubitemid 34654745)
39. Fueger PT, Bracy DP, Malabanan CM, Pencek RR, Granner DK, et al. (2004) Hexokinase II overexpression improves exercise-stimulated but not insulin-stimulated muscle glucose uptake in high-fat-fed C57BL/6J mice. Diabetes 53: 306-314. (Pubitemid 38174544)
40. Paigen B, Ishida BY, Verstuyft J, Winters RB, Albee D (1990) Atherosclerosis susceptibility differences among progenitors of recombinant inbred strains of mice. Arteriosclerosis 10: 316-323. (Pubitemid 20103595)
41. Schreyer SA, Wilson DL, LeBoeuf RC (1998) C57BL/6 mice fed high fat diets as models for diabetes-accelerated atherosclerosis. Atherosclerosis 136: 17-24. (Pubitemid 28341437)
42. Shim J, Handberg A, Ostergren C, Falk E, Bentzon JF (2011) Genetic susceptibility of the arterial wall is an important determinant of atherosclerosis in C57BL/6 and FVB/N mouse strains. Arterioscler Thromb Vasc Biol 31: 1814-1820.
43. Hummel KP, Coleman DL, Lane PW (1972) The influence of genetic background on expression of mutations at the diabetes locus in the mouse. I. C57BL-KsJ and C57BL-6J strains. Biochem Genet 7: 1-13.
44. Coleman DL, Hummel KP (1973) The influence of genetic background on the expression of the obese (Ob) gene in the mouse. Diabetologia 9: 287-293.
45. Qiu J, Ogus S, Mounzih K, Ewart-Toland A, Chehab FF (2001) Leptin-deficient mice backcrossed to the BALB/cJ genetic background have reduced adiposity, enhanced fertility, normal body temperature, and severe diabetes. Endocrinology 142: 3421-3425. (Pubitemid 32681748)
46. Chua S, Jr., Liu SM, Li Q, Yang L, Thassanapaff VT, et al. (2002) Differential beta cell responses to hyperglycaemia and insulin resistance in two novel congenic strains of diabetes (FVB- Lepr (db)) and obese (DBA- Lep (ob)) mice. Diabetologia 45: 976-990. (Pubitemid 34762192)
47. Xita N, Lazaros L, Georgiou I, Tsatsoulis A (2010) CYP19 gene: a genetic modifier of polycystic ovary syndrome phenotype. Fertil Steril 94: 250-254.
48. Wang H, Li Q, Wang T, Yang G, Wang Y, et al. (2011) A common polymorphism in the human aromatase gene alters the risk for polycystic ovary syndrome and modifies aromatase activity in vitro. Mol Hum Reprod 17: 386-391.
49. Ito Y, Fisher CR, Conte FA, Grumbach MM, Simpson ER (1993) Molecular basis of aromatase deficiency in an adult female with sexual infantilism and polycystic ovaries. Proc Natl Acad Sci U S A 90: 11673-11677. (Pubitemid 24008701)
50. Stener-Victorin E (2013) Hypothetical physiological and molecular basis for the effect of acupuncture in the treatment of polycystic ovary syndrome. Mol Cell Endocrinol.
51. Clayton RN, Ogden V, Hodgkinson J, Worswick L, Rodin DA, et al. (1992) How Common Are Polycystic Ovaries in Normal Women and What Is Their Significance for the Fertility of the Population. Clinical Endocrinology 37: 127-134.
52. Polson DW, Adams J, Wadsworth J, Franks S (1988) Polycystic ovaries-a common finding in normal women. Lancet 1: 870-872. (Pubitemid 18092411)
53. Hughesdon PE (1982) Morphology and morphogenesis of the Stein-Leventhal ovary and of so-called "hyperthecosis". Obstet Gynecol Surv 37: 59-77.
54. Webber LJ, Stubbs S, Stark J, Trew GH, Margara R, et al. (2003) Formation and early development of follicles in the polycystic ovary. Lancet 362: 1017-1021. (Pubitemid 37186878)
55. Maciel GA, Baracat EC, Benda JA, Markham SM, Hensinger K, et al. (2004) Stockpiling of transitional and classic primary follicles in ovaries of women with polycystic ovary syndrome. J Clin Endocrinol Metab 89: 5321-5327. (Pubitemid 39518404)
56. Mason HD, Willis DS, Beard RW, Winston RM, Margara R, et al. (1994) Estradiol production by granulosa cells of normal and polycystic ovaries: relationship to menstrual cycle history and concentrations of gonadotropins and sex steroids in follicular fluid. J Clin Endocrinol Metab 79: 1355-1360. (Pubitemid 24369848)
57. Gilling-Smith C, Willis DS, Beard RW, Franks S (1994) Hypersecretion of androstenedione by isolated thecal cells from polycystic ovaries. J Clin Endocrinol Metab 79: 1158-1165. (Pubitemid 24342265)
58. Webber LJ, Stubbs SA, Stark J, Margara RA, Trew GH, et al. (2007) Prolonged survival in culture of preantral follicles from polycystic ovaries. J Clin Endocrinol Metab 92: 1975-1978. (Pubitemid 46997220)
59. Das M, Djahanbakhch O, Hacihanefioglu B, Saridogan E, Ikram M, et al. (2008) Granulosa cell survival and proliferation are altered in polycystic ovary syndrome. J Clin Endocrinol Metab 93: 881-887. (Pubitemid 351398567)
60. McNeilly AS, Duncan WC (2013) Rodent models of polycystic ovary syndrome. Mol Cell Endocrinol 373: 2-7.
61. van Houten EL, Kramer P, McLuskey A, Karels B, Themmen AP, et al. (2012) Reproductive and metabolic phenotype of a mouse model of PCOS. Endocrinology 153: 2861-2869.
62. Pan Z, Zhang J, Lin F, Ma X, Wang X, et al. (2012) Expression profiles of key candidate genes involved in steroidogenesis during follicular atresia in the pig ovary. Mol Biol Rep 39: 10823-10832.
63. Willis D, Franks S (1995) 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. Journal of Clinical Endocrinology & Metabolism 80: 3788-3790.
64. Nestler JE, Jakubowicz DJ, Falcon A, Brik VC, Quintero N, et al. (1998) Insulin stimulates testosterone biosynthesis by human thecal cells from women with polycystic ovary syndrome by activating its own receptor and using inositolglycan mediators as the signal transduction system. Journal of Clinical Endocrinology & Metabolism 83: 2001-2005. (Pubitemid 28496328)
65. Munir I, Yen HW, Geller DH, Torbati D, Bierden RM, et al. (2004) Insulin augmentation of 17 alpha-hydroxylase activity is mediated by phosphatidyl inositol 3-kinase but not extracellular signal-regulated kinase-1/2 in human ovarian theca cells. Endocrinology 145: 175-183. (Pubitemid 38094513)
66. Willis DS, Watson R, Mason HD, Galea R, Brincat M, et al. (1998) Premature response to luteinizing hormone of granulosa cells from anovulatory women with polycystic ovary syndrome: Relevance to mechanism of anovulation. Journal of Clinical Endocrinology & Metabolism 83: 3984-3991. (Pubitemid 28513584)
67. Rice S, Christoforidis N, Gadd C, Nikolaou D, Seyani L, et al. (2005) Impaired insulin-dependent glucose metabolism in granulosa-lutein cells from anovulatory women with polycystic ovaries. Human Reproduction 20: 373-381. (Pubitemid 40277604)
68. Willis D, Mason H, GillingSmith C, Franks S (1996) Modulation by insulin of follicle-stimulating hormone and luteinizing hormone actions in human granulosa cells of normal and polycystic ovaries. Journal of Clinical Endocrinology & Metabolism 81: 302-309. (Pubitemid 26035038)
69. Jakimiuk AJ, Weitsman SR, Navab A, Magoffin DA (2001) Luteinizing hormone receptor, steroidogenesis acute regulatory protein, and steroidogenic enzyme messenger ribonucleic acids are overexpressed in thecal and granulosa cells from polycystic ovaries. Journal of Clinical Endocrinology & Metabolism 86: 1318-1323. (Pubitemid 32323023)
70. Ewens KG, Stewart DR, Ankener W, Urbanek M, McAllister JM, et al. (2010) Family-Based Analysis of Candidate Genes for Polycystic Ovary Syndrome. Journal of Clinical Endocrinology & Metabolism 95: 2306-2315.
71. Goodarzi MO, Maher JF, Cui J, Guo X, Taylor KD, et al. (2008) FEM1A and FEM1B: novel candidate genes for polycystic ovary syndrome. Human Reproduction 23: 2842-2849.
72. O'Meara NM, Blackman JD, Ehrmann DA, Barnes RB, Jaspan JB, et al. (1993) Defects in beta-cell function in functional ovarian hyperandrogenism. J Clin Endocrinol Metab 76: 1241-1247. (Pubitemid 23155443)
73. Dunaif A (1997) Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev 18: 774-800.
74. Abdul-Ghani MA, Tripathy D, DeFronzo RA (2006) Contributions of beta-cell dysfunction and insulin resistance to the pathogenesis of impaired glucose tolerance and impaired fasting glucose. Diabetes Care 29: 1130-1139. (Pubitemid 44115261)
75. Nathan DM, Davidson MB, DeFronzo RA, Heine RJ, Henry RR, et al. (2007) Impaired fasting glucose and impaired glucose tolerance: implications for care. Diabetes Care 30: 753-759. (Pubitemid 46354366)
76. Karakas SE, Kim K, Duleba AJ (2010) Determinants of impaired fasting glucose versus glucose intolerance in polycystic ovary syndrome. Diabetes Care 33: 887-893.
77. Walters KA, Allan CM, Handelsman DJ (2012) Rodent Models for Human Polycystic Ovary Syndrome. Biology of Reproduction 86.
78. Keisler LW, Saal FSV, Keisler DH, Walker SE (1991) Hormonal Manipulation of the Prenatal Environment Alters Reproductive Morphology and Increases Longevity in Autoimmune Nzb/W Mice. Biology of Reproduction 44: 707-716.
79. Sullivan SD, Moenter SM (2004) Prenatal androgens alter GABAergic drive to gonadotropin-releasing hormone neurons: Implications for a common fertility disorder. Proceedings of the National Academy of Sciences of the United States of America 101: 7129-7134. (Pubitemid 38596454)
80. Roland AV, Nunemaker CS, Keller SR, Moenter SM (2010) Prenatal androgen exposure programs metabolic dysfunction in female mice. Journal of Endocrinology 207: 213-223.
81. Edwards DA (1971) Neonatal Administration of Androstenedione, Testosterone or Testosterone Propionate - Effects on Ovulation, Sexual Receptivity and Aggressive Behavior in Female Mice. Physiology & Behavior 6: 223-&.
82. Kamijo T, Mizunuma H, Yamada K, Ibuki Y (1994) In-Vitro Fertilization of Androgen Sterilized Mice. Life Sciences 55: 527-531. (Pubitemid 24230339)
83. Leonie E, van Houten AF, Kramer P, McLuskey A, Karels B, et al. (2012) Reproductive and Metabolic Phenotype of a Mouse Model of PCOS. Endocrinology 153: 2861-2869.