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Vol. 65 No. 3: Issue 3

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Molecular role of peptides/proteins in subfertility of polycystic ovarian syndrome

https://doi.org/10.14715/cmb/2019.65.3.5
Onder Celik
Private Clinic, Obstetrics and Gynecology, Usak, Turkey
Suleyman Aydin
Department of Medical Biochemistry, Firat University, School of Medicine, Elazig, Turkey
Nilufer Celik
Department of Biochemistry, Behcet Uz Children's Hospital, Izmir, Turkey
Kader Ugur
Department of Endocrine and Metabolism Diseases, Firat University, School of Medicine, Elazig, Turkey
Seyda Yavuzkir
Department of Obstetrics and Gynecology, Firat University, School of Medicine, Elazig, Turkey
Safak Hatirnaz
Department of Obstetrics and Gynecology, Bilge Hospital, ć°stanbul, Turkey
Meltem Yardim
Department of Medical Biochemistry, Firat University, School of Medicine, Elazig, Turkey
Sude Celik
Kent College, ć°zmir, Turkey

Corresponding Author(s) : Suleyman Aydin

saydin1@hotmail.com

Cellular and Molecular Biology, Vol. 65 No. 3: Issue 3

Abstract

Obesity and hyperandrogenemia are known to have adverse effects on both developing follicle and endometrium receptivity in polycystic ovarian syndrome (PCOS). Insulin resistance also contributes to this dilemma as a cause or a consequence and leads to worsening of the clinical picture. The difficulty in obtaining pregnancy despite the presence of a large number of oocyte has concentrated our attention on oocyte quality and development. However, the occurence of subfertility has also caused us to investigate the presence of different etiologic agents in non-obese PCOS women with normal androgen and insulin levels. In this context peptides have become the most accused and investigated molecules in cases of impaired fertility due to PCOS. Most of the studies investigating the relationship between PCOS and peptide did not support each other. The difficulties in measuring peptide levels as well as the individual variations in peptide synthesis and release are possible causes of this incongruity. For all these reasons, the incorporation of studies investigating the relationship between PCOS, peptide and subfertility in an article has become critical to pioneering future work. Understanding the association between peptides and subfertility will help us to understand the effects of peptides on failed fertility in PCOS. Moreover, updating our knowledge about peptides may allow us designing new drugs to to treat subfertility in PCOS. This review provides a general summary of the mechanisms of action of neuroendocrine peptides in regulating reproductive events. Since it is not usual to discuss all peptides in this context, only the effects of key central and peripheral peptides on fertility in PCOS have been extensively addressed.

Keywords

Peptides PCOS Subfertility.
Celik, O., Aydin, S., Celik, N., Ugur, K., Yavuzkir, S., Hatirnaz, S., Yardim, M., & Celik, S. (2019). Molecular role of peptides/proteins in subfertility of polycystic ovarian syndrome. Cellular and Molecular Biology, 65(3), 32–40. https://doi.org/10.14715/cmb/2019.65.3.5
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References
  1. De Leo V, Musacchio MC, Cappelli V, Massaro MG, Morgante G, Petraglia F. Genetic, hormonal and metabolic aspects of PCOS: an update. Reprod Biol Endocrinol 2016; 14:38.
  2. Azziz R, Woods KS, Reyna R, Key TJ, Knochenhauer ES, Yildiz BO. The prevalence and features of the polycystic ovary syndrome in an unselected population. J Clin Endocrinol Metab 2004; 89:2745-9.
  3. MarchWA, MooreVM, Willson KJ, Phillips DI, NormanRJ, Davies MJ. The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Hum Reprod 2010; 25:544-51.
  4. Carmina E, Lobo RA. Polycystic ovary syndrome (PCOS): arguably the most common endocrinopathy is associated with significant morbidity in women. J Clin Endocrinol Metab 1999; 84:1897-9.
  5. Lindholm A, Blomquist C, Bixo M, Dahlbom I, Hansson T, Sundström Poromaa I, et al. No difference in markers of adipose tissue inflammation between overweight women with polycystic ovary syndrome and weight-matched controls. Hum Reprod 2011; 26:1478-85.
  6. Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 2004; 89:2548-56.
  7. Kim SH, Chung JH, Song SW, Jung WS, Lee YA, Kim HN. Relationship between deep subcutaneous abdominal adipose tissue and metabolic syndrome: a case control study. Diabetol Metab Syndr 2016; 8:10.
  8. Sahin SB, Durakoglugil T, Ayaz T, Sahin OZ, Durakoglugil E, Sumer F, et al. Evaluation of para- and perirenal fat thickness and its association with metabolic disorders in polycystic ovary syndrome. Endocr Pract 2015; 21:878-86.
  9. Apparao KB, Lovely LP, Gui Y, Lininger RA, Lessey BA. Elevated endometrial androgen receptor expression in women with polycystic ovarian syndrome. Biol Reprod 2002; 66:297-304.
  10. Celik O, Aydin S, Celik N, Yilmaz M. Peptides: Basic determinants of reproductive functions. Peptides 2015; 72:34-43.
  11. Cermik D, Selam B, Taylor HS. Regulation of HOXA-10 expression by testosterone in vitro and in the endometrium of patients with polycystic ovary syndrome. J Clin Endocrinol Metab 2003; 88:238-43.
  12. Suikkari AM, Ruutiainen K, Erkkola R, Seppala M. Low levels of low molecular weight insulin-like growth factor-binding protein in patients with polycystic ovarian disease. Hum Reprod 1989; 4:136-9.
  13. Burcelin R, Thorens B, Glauser M, Gaillard RC, Pralong FP. Gonadotropin-releasing hormone secretion from hypothalamic neurons: stimulation by insulin and potentiation by leptin. Endocrinology 2003; 144:4484-91.
  14. Celik O, Celik N, Aydin S, Aygun BK, Haberal ET, Kuloglu T, et al. Ghrelin action on GnRH neurons and pituitary gonadotropes might be mediated by GnIH-GPR147 system. Horm Mol Biol Clin Investig 2016; 25:121-8.
  15. Gregoraszczuk EL, Rak-Mardyła A. Supraphysiological leptin levels shift the profile of steroidogenesis in porcine ovarian follicles toward progesterone and testosterone secretion through increased expressions of CYP11A1 and 17b-HSD: a tissue culture approach. Reproduction 2013; 145:311-7.
  16. Kawwass JF, Summer R, Kallen CB. Direct effects of leptin and adiponectin on peripheral reproductive tissues: a critical review. Mol Hum Reprod 2014; 21:617-32.
  17. Skorupskaite K, George JT, Anderson RA. The kisspeptin-GnRH pathway in human reproductive health and disease. Hum Reprod Update. 2014; 20:485-500.
  18. Okon MA, Laird SM, Tuckerman EM, Li TC. Serum androgen levels in women who have recurrent miscarriages and their correlation with markers of endometrial function. Fertil Steril 1998; 69:682-90.
  19. Thornton JW. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci USA 2001; 98:5671-6.
  20. Qiao J, Feng HL. Extra- and intra-ovarian factors in polycystic ovary syndrome: impact on oocyte maturation and embryo developmental competence. Hum Reprod Update 2010; 17:17-33.
  21. Palin MF, Bordignon VV, Murphy BD. Adiponectin and the control of female reproductive functions. Vitam Horm 2014; 90:239-87.
  22. Tabandeh MR, Golestani N, Kafi M, Hosseini A, Saeb M, Sarkoohi P. Gene expression pattern of adiponectin and adiponectin receptors in dominant and atretic follicles and oocytes screened based on brilliant cresyl blue staining. Anim Reprod Sci 2015; 131:30-40.
  23. Carmina E, Orio F, Palomba S, Cascella T, Longo RA, Colao AM, et al. Evidence for altered adipocyte function in polycystic ovary syndrome. Eur J Endocrinol 2005; 152:389-94.
  24. Mantzoros CS, Dunaif A, Flier JS. Leptin concentrations in the polycystic ovary syndrome. J Clin Endocrinol Metab 1997; 82:1687-91.
  25. Moran LJ, Noakes M, Clifton PM, Wittert GA, Tomlinson L, Galletly C, et al. Ghrelin and measures of satiety are altered in polycystic ovary syndrome but not differentially affected by diet composition. J Clin Endocrinol Metab 2004; 89:3337-44.
  26. Panidis D, Kourtis A, Farmakiotis D, Mouslech T, Rousso D, Koliakos G. Serum adiponectin levels in women with polycystic ovary syndrome. Human Reproduction 2003; 18:1790-6.
  27. Acet M, Celik N, Acet T, Ilhan S, Yardim M, Aktun HL, et al. Serum and follicular fluid irisin levels in poor and high responder women undergoing IVF/ICSI. Eur Rev Med Pharmacol Sci 2016; 20:1940-6.
  28. Adrian TE, Ferri GL, Bacarese-Hamilton AJ, Fuessl HS, Polak JM, Bloom SR. Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology 1985; 89:1070-7.
  29. Bertoldo MJ, Faure M, Dupont J, Froment P. AMPK: a master energy regulator for gonadal function. Front Neurosci 2014; 9:235.
  30. Dandona P, Aljada A, Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. TrendsImmunol 2004; 25:4-7.
  31. Mah PM, Wittert GA. Obesity and testicular function. Mol Cell Endocrinol 2015; 316:180-6.
  32. Suganami T, Nishida J, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler Thromb Vasc Biol 2005; 25:2062-8.
  33. Tengstrand B, Carlstrom K, Hafstrom I. Gonadal hormones in men with rheumatoid arthritis--from onset through 2 years. J Rheumatol 2009; 36: 887-92.
  34. Farooqi IS. Leptin and the onset of puberty: insights from rodent and human genetics. Semin Reprod Med 2002; 20:139-44.
  35. Psilopanagioti A, Papadaki H, Kranioti EF, Alexandrides TK, Varakis JN. Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology 2009; 89:38-47.
  36. Yan X, Yuan C, Zhao N, Cui Y, Liu J. Prenatal androgen excess enhances stimulation of the GNRH pulse in pubertal female rats. J Endocrinol 2014; 222:73-85.
  37. Brown RE, Imran SA, Ur E, Wilkinson M. KiSS-1 mRNA in adipose tissue is regulated by sex hormones and food intake. Mol Cell Endocrinol 2008; 281:64-72.
  38. Qi X, Salem M, Zhou W, Sato-Shimizu M, Ye G, Smitz J, et al. Neurokinin B Exerts Direct Effects on the Ovary to Stimulate Estradiol Production. Endocrinology 2016; 157:3355-65.
  39. Semple RK, Achermann JC, Ellery J, Farooqi IS, Karet FE, Stanhope RG, et al. Two novel missense mutations in g protein-coupled receptor 54 in a patient with hypogonadotropic hypogondism. J Clin Endocrinol Metab 2005; 90:1849-55.
  40. Chabrolle C, Tosca L, Crochet S, Tesseraud S, Dupont J. Expression of adiponectin and its receptors (AdipoR1 and AdipoR2) in chicken ovary: potential role in ovarian steroidogenesis. Domest Anim Endocrinol 2007; 33: 480-7.
  41. Chabrolle C, Tosca L, Ramé C, Lecomte P, Royère D, Dupont J. Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells. Fertil Steril 2009; 92:1988-96.
  42. Ersahin A, Acet M, Acet T, Yavuz Y. Disturbed endometrial NF-κB expression in women with recurrent implantation failure. Eur Rev Med Pharmacol Sci 2016; 20:5037-40.
  43. Wickham EP 3rd, Tao T, Nestler JE, McGee EA. Activation of the LH receptor up regulates the type 2 adiponectin receptor in human granulosa cells. J AssistReprodGenet 2014; 30:963-8.
  44. Wu L, Xu B, Fan W, Zhu X, Wang G, Zhang A. Adiponectin protects Leydig cells against proinflammatory cytokines by suppressing the nuclear factor-κB signaling pathway. Febs J 2015; 280:3920-7.
  45. Hameed W, Yousaf I, Latif R, Aslam M. Effect of visfatin on testicular steroidogenesis in purified Leydig cells. J Ayub Med Coll Abbottabad 2014; 24:62-4.
  46. Shen CJ, Tsai EM, Lee JN, Chen YL, Lee CH, Chan TF. The concentrations of visfatin in the follicular fluids of women undergoing controlled ovarian stimulation are correlated to the number of oocytes retrieved. Fertil Steril 2013; 93:1844-50.
  47. Ballinger AB, Savage MO, Sanderson IR. Delayed puberty associated with inflammatory bowel disease. Pediatr Res 2003; 53:205-10.
  48. Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 2007; 148:4687-94.
  49. Chu Y, Cui Q, Feng G, Song Z, Jiang X. The expression of resistin in adipose tissues of patients with polycystic ovary syndrome and insulin resistance. J Huazhong Univ Sci Technolog Med Sci 2009; 29:642-5.
  50. Ersahin A, Acet M, Ersahin SS, Acet T, Yardim M, Kenanoglu O, et al. Follicular Fluid Cerebellin and Betatrophin Regulate Metabolic Functions of Growing Follicles in PCOS. Clin Exp Reprod Med 2017; 44:33-9.
  51. Strowski MZ, Kaczmarek P, Mergler S, Wiedenmann B, Domin D, Szwajkowski P, et al. Insulinostaticactivity of cerebellin--evidencefrom in vivoand in vitrostudies in rats. Regul Pept 2009; 157:19-24.
  52. Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocrine Reviews 2000; 21:697-738.
  53. Coleman DL. Effects of parabiosis of obese with diabetes and normal mice. Diabetologia 1973; 9:294-8.
  54. Friedman JM, Leibel RL, Siegel DS, Walsh J, Bahary N. Molecular mapping of the mouse ob mutation. Genomics 1991; 11:1054-62.
  55. Moschos S, Chan JL, Mantzoros CS. Leptin and reproduction: a review. Fertil Steril 2002; 77:433-44.
  56. Chou K, Perry CM. Metreleptin: first global approval. Drugs 2013; 73:989-97.
  57. Abir R, Ao A, Jin S, Barnett M, Raanani H, Ben-Haroush A, et al. Leptin and its receptors in human fetal and adult ovaries. Fertil Steril 2005; 84:1779-82.
  58. Moro C, Galitzky J, Sengenes C, Crampes F, Lafontan M, Berlan M. Functional and pharmacological characterization of the natriuretic peptide-dependent lipolytic pathway in human fat cells. J Pharmacol Exp Ther 2004; 308:984-92.
  59. Ojeda SR, Lomniczi A, Mastronardi C, Heger S, Roth C, Parent AS, et al. Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology 2006; 147:1166-74.
  60. Mallinson RJ, Williams NI, Olmsted MP, Scheid JL, Riddle ES, De Souza MJ. A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration. J Int Soc Sports Nutr 2014; 10:34.
  61. von Schnurbein J, Moss A, Nagel SA, Muehleder H, Debatin KM, Farooqi IS, et al. Leptin substitution results in the induction of menstrual cycles in an adolescent with leptin deficiency and hypogonadotropic hypogonadism. Horm Res Paediatr 2014; 77:127-33.
  62. Zheng SH, Du DF, Li XL. Leptin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Reprod Sci 2016; 24:656-70.
  63. Lian Y, Zhao F, Wang W. Central leptin resistance and hypothalamic inflammation are involved in letrozole-induced polycystic ovary syndrome rats. Biochem Biophys Res Commun 2016; 476:306-12.
  64. Jacobs MB, Bazzano LA, Pridjian G, Harville EW. Childhood adiposity and fertility difficulties: the Bogalusa Heart Study. Pediatr Obes 2017; 12:477-84.
  65. Celik O, Hascalik S, Ozerol E, Hascalik M, Yologlu S. Cerebrospinal fluid leptin levels in preeclampsia: relation to maternal serum leptin levels. Acta Obstet Gynecol Scand 2004; 83:519-23.
  66. Garruti G, de Palo R, Rotelli MT, Nocera S, Totaro I, Nardelli C, et al. Association between follicular fluid leptin and serum insulin levels in nonoverweight women with polycystic ovary syndrome. Biomed Res Int 2014; 2014:980429.
  67. De Placido G, Alviggi C, Clarizia R, Mollo A, Alviggi E, Strina I, et al. Intra-follicular leptin concentration as a predictive factor for in vitro oocyte fertilization in assisted reproductive techniques. J Endocrinol Invest 2006; 29:719-26.
  68. Li MG, Ding GL, Chen XJ, Lu XP, Dong LJ, Dong MY, et al. Association of serum and follicular fluid leptin concentrations with granulosa cell phosphorylated signal transducer and activator of transcription 3 expression in fertile patients with polycystic ovarian syndrome. J Clin Endocrinol Metab 2007; 92:4771-6.
  69. Blüher S, Mantzoros CS. Leptin in reproduction. Curr Opin Endocrinol Diabetes Obes 2007; 14:458-64.
  70. Toulis KA, Goulis DG, Farmakiotis D, Georgopoulos NA, Katsikis I, Tarlatzis BC, et al. Adiponectin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Hum Reprod Update 2009; 15:297-307.
  71. Wickham EP, Cheang KI, Clore JN, Baillargeon JP, Nestler JE. Total and high-molecular weight adiponectin in women with the polycystic ovary syndrome. Metabolism 2011; 60:366-72.
  72. Mannerås-Holm L, Leonhardt H, Kullberg J, Jennische E, Odén A, Holm G, et al. Adipose tissue has aberrant morphology and function in PCOS: enlarged adipocytes and low serum adiponectin, but not circulating sex steroids, are strongly associated with insulin resistance. J Clin Endocrinol Metab 2011; 96:E304-11.
  73. Nambiar V, Vijesh VV, Lakshmanan P, Sukumaran S, Suganthi R. Association of adiponectin and resistin gene polymorphisms in South Indian women with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol 2016; 200:82-8.
  74. Artimani T, Saidijam M, Aflatoonian R, Ashrafi M, Amiri I, Yavangi M, et al. Downregulation of adiponectin system in granulosa cells and low levels of HMW adiponectin in PCOS. J Assist Reprod Genet 2016; 33:101-10.
  75. Garcí­a V, Oróstica L, Poblete C, Rosas C, Astorga I, Romero C, et al. Endometria from Obese PCOS Women with Hyperinsulinemia Exhibit Altered Adiponectin Signaling. Horm Metab Res 2015; 47:901-9.
  76. Gamundi-Segura S, Serna J, Oehninger S, Horcajadas JA, Arbones-Mainar JM. Effects of adipocytesecreted factors on decidualized endometrial cells: modulation of endometrial receptivity in vitro. J Physiol Biochem 2015; 71:537-46.
  77. Fernandez-Fernandez R, Tena-Sempere M, Navarro VM, Barreiro ML, Castel-lano JM, Aguilar E, et al. Effects of ghrelin upon gonadotropin-releasing hormone and gonadotropin secretion in adult female rats: in vivo and in vitro studies. Neuroendocrinology 2005; 82:245-55.
  78. Furuta M, Funabashi T, Kimura F. Intracerebroventricular administration of ghrelin rapidly suppresses pulsatile luteinizing hormone secretion in ovariectomized rats. Biochem Biophys Res Commun 2001; 288:780-5.
  79. Kluge M, Schussler P, Uhr M, Yassouridis A, Steiger A. Ghrelin suppresses secretion of luteinizing hormone in humans. J Clin Endocrinol Metab 2007; 92:3202-5.
  80. Bentley GE, Ubuka T, McGuire NL, Chowdhury VS, Morita Y, Yano T, et al. Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen Comp Endocrinol 2008; 156:34-43.
  81. Sirotkin A, Chrenek P, Darlak K, Valenzuela F, Kuklová Z. Some endocrine traits of transgenic rabbits. II. Changes in hormone secretion and response of isolated ovarian tissue to FSH and ghrelin. Physiol Res 2008; 57:745-51.
  82. Rak-Mardyia A, Durak M, Lucja Gregoraszczuk E. Effects of resistin on porcine ovarian follicle steroidogenesis in prepubertal animals: an in vitro study. Reprod Biol Endocrinol 2013; 11:45.
  83. Gul OO, Cander S, Gul B, Açıkgoz E, Sarandol E, Ersoy C. Evaluation of insulin resistance and plasma levels for visfatin and resistin in obese and non-obese patients with polycystic ovary syndrome. Eur Cytokine Netw 2015; 26:73-8.
  84. Seow KM, Juan CC, Wu LY, Hsu YP, Yang WM, Tsai YL, et al. Serum and adipocyte resistin in polycystic ovary syndrome with insulin resistance. Hum Reprod 2004; 19:48-53.
  85. Yang F. Amylin in vasodilation, energy expenditure and inflammation. Front Biosci (Landmark Ed) 2014; 19:936-44.
  86. James S, Moralez J, Nagamani M. Increased secretion of amylin in women with polycystic ovary syndrome. Fertil Steril 2010; 94:211-5.
  87. Cate RL, Mattaliano RJ, Hession C, Tizard R, Farber NM, Cheung A, et al. Isolation of the bovine and human genes for Müllerian inhibiting substance and expression of the human gene in animal cells. Cell 1986; 45:685-98.
  88. Rey R, Lukas-Croisier C, Lasala C, Bedecarrás P. AMH/MIS: what we know already about the gene, the protein and its regulation. Mol Cell Endocrinol 2003; 211:21-31.
  89. La Marca A, Volpe A. Anti-Müllerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool? Clin Endocrinol (Oxf) 2006; 64:603-10.
  90. Rajpert-De Meyts E, Jorgensen N, Graem N, Muller J, Cate RL, Skakkebaek NE. Expression of antiMüllerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab 1999; 84:3836-44.
  91. La Marca A, De Leo V, Giulini S, Orvieto R, Malmusi S, Giannella L, et al. Anti-Mullerian hormone in premenopausal women and after spontaneous or surgically induced menopause. J Soc Gynecol Investig 2005; 12:545-8.
  92. Vigier B, Picard JY, Tran D, Legeai L, Josso N. Production of anti-Müllerian hormone: another homology between Sertoli and granulosa cells. Endocrinology 1984; 114:1315-20.
  93. Andersen CY, Byskov AG. Estradiol and regulation of anti-Müllerian hormone, inhibin-A, and inhibin-B secretion: analysis of small antral and preovulatory human follicles' fluid. J Clin Endocrinol Metab 2006; 91:4064-9.
  94. Salmon NA, Handyside AH, Joyce IM. Oocyte regulation of anti-Müllerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev Biol 2004; 266:201-8.
  95. Themmen AP. Anti-Müllerian hormone: its role in follicular growth initiation and survival and as an ovarian reserve marker. J Natl Cancer Inst Monogr 2005; 34:18-21.
  96. Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, et al. Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 1999; 140:5789-96.
  97. Fleming R, Deshpande N, Traynor I, Yates RW. Dynamics of FSH-induced follicular growth in subfertile women: relationship with age, insulin resistance, oocyte yield and anti-Mullerian hormone. Hum Reprod 2006; 21:1436-41.
  98. Piltonen T, Morin-Papunen L, Koivunen R, Perheentupa A, Ruokonen A, Tapanainen JS. Serum antiMüllerian hormone levels remain high until late reproductive age and decrease during metformin therapy in women with polycystic ovary syndrome. Hum Reprod 2005; 20:1820-6.
  99. La Marca A, Orvieto R, Giulini S, Jasonni VM, Volpe A, De Leo V. Mullerian-inhibiting substance in women with polycystic ovary syndrome: relationship with hormonal and metabolic characteristics. Fertil Steril 2004; 82:970-2.
  100. Pellatt L, Hanna L, Brincat M, Galea R, Brain H, Whitehead S, et al. Granulosa cell production of antiMüllerian hormone is increased in polycystic ovaries. J Clin Endocrinol Metab 2007; 92:240-5.
  101. Joham AE, Palomba S, Hart R. Polycystic Ovary Syndrome, Obesity, and Pregnancy. Semin Reprod Med 2016; 34:93-101.
  102. Passeri E, Bugiardini E, Sansone VA, Pizzocaro A, Fulceri C, Valaperta R, et al. Gonadal failure is associated with visceral adiposity in myotonic dystrophies. Eur J Clin Invest 2015; 45:702-10.
  103. Renaud EJ, MacLaughlin DT, Oliva E, Rueda BR, Donahoe PK. Endometrial cancer is a receptormediated target for Mullerian Inhibiting Substance. Proc Natl Acad Sci U S A 2005; 102:111-6. Erratum in: Proc Natl Acad Sci U S A. 2005;102:6513.
  104. Wang J, Dicken C, Lustbader JW, Tortoriello DV. Evidence for a Müllerian-inhibiting substance autocrine/paracrine system in adult human endometrium. Fertil Steril 2009; 91:1195-203.
  105. Jayasena CN, Abbara A, Veldhuis JD, Comninos AN, Ratnasabapathy R, De Silva A, et al. Increasing LH pulsatility in women with hypothalamic amenorrhoea using intravenous infusion of Kisspeptin-54. J Clin Endocrinol Metab 2014; 99:E953-61.
  106. Chen X, Mo Y, Li L, Chen Y, Li Y, Yang D. Increased plasma metastin levels in adolescent women with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol 2010; 149:72-6.
  107. Panidis D, Rousso D, Koliakos G, Kourtis A, Katsikis I, Farmakiotis D, et al. Plasma metastin levels are negatively correlated with insulin resistance and free androgens in women with polycystic ovary syndrome. Fertil Steril 2006; 85:1778-83.
  108. Yilmaz SA, Kerimoglu OS, Pekin AT, Incesu F, Dogan NU, Celik C, et al. Metastin levels in relation with hormonal and metabolic profile in patients with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol 2014; 180:56-60.
  109. Emekci Ozay O, Ozay AC, Acar B, Cagliyan E, Seçil M, Küme T. Role of kisspeptin in polycystic ovary syndrome (PCOS). Gynecol Endocrinol 2016; 32:718-22.
  110. Jeon YE, Lee KE, Jung JA, Yim SY, Kim H, Seo SK, et al. Kisspeptin, leptin, and retinol-binding protein 4 in women with polycystic ovary syndrome. Gynecol Obstet Invest 2013; 75:268-74.
  111. Kondo M, Osuka S, Iwase A, Nakahara T, Saito A, Bayasula, et al. Increase of kisspeptin-positive cells in the hypothalamus of a rat model of polycystic ovary syndrome. Metab Brain Dis 2016; 31:673-81.
  112. Lehman MN, Coolen LM, Goodman RL. Mini review: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology. 2010; 151:3479-89.
  113. Osuka S, Iwase A, Nakahara T, Kondo M, Saito A, Bayasula, et al. Kisspeptin in the hypothalamus of two rat models of polycystic ovary syndrome. Endocrinology 2017; 158:367-77.
  114. Aydin S, Kuloglu T, Aydin S, Kalayci M, Yilmaz M, Cakmak T, et al. A comprehensive immunohistochemical examination of the distribution of the fat-burning protein irisin in biological tissues. Peptides 2014; 61:130-6.
  115. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo Jc, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012; 481:463-8.
  116. Pardo M, Crujeiras AB, Amil M, Aguera Z, Jiménez-Murcia S, Baños R, et al. Association of irisin with fat mass, resting energy expenditure, and daily activity in conditions of extreme body mass index. Int J Endocrinol 2014; 2014:857270.
  117. Kurdiova T, Balaz M, Vician M, Maderova D, Vlcek M, Valkovic L, et al. Effects of obesity, diabetes and exercise on Fndc5 gene expression and irisin release in human skeletal muscle and adipose tissue: in vivo and in vitro studies. J Physiol 2014; 592:1091-107.
  118. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998; 92:829-39.
  119. Chang CL, Huang SY, Soong YK, Cheng PJ, Wang CJ, Liang IT. Circulating irisin and glucosedependent insulinotropic peptide are associated with the development of polycystic ovary syndrome. J Clin Endocrinol Metab 2014; 99:E2539-48.
  120. Choi YK, Kim MK, Bae KH, Seo HA, Jeong JY, Lee WK, et al. Serum irisin levels in new-onset type 2 diabetes. Diabetes Res Clin Pract 2013; 100:96-101.
  121. Park KH, Zaichenko L, Brinkoetter M, Thakkar B, Sahin-Efe A, Joung KE, et al. Circulating irisin in relation to insulin resistance and the metabolic syndrome. J Clin Endocrinol Metab 2013; 98:4899-907.
  122. Fisher FM, Chui PC, Antonellis PJ, Bina HA, Kharitonenkov A, Flier JS, et al. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 2010; 59:2781-9.
  123. Garcés MF, Peralta JJ, Ruiz-Linares CE, Lozano AR, Poveda NE, Torres-Sierra AL, et al. Irisin levels during pregnancy and changes associated with the development of preeclampsia. J Clin Endocrinol Metab. 2014; 99:2113-9.
  124. Moro C, Berlan M. Cardiovascular and metabolic effects of natriuretic peptides. Fundam Clin Pharmacol 2006; 20:41-9.
  125. Sengenès C, Berlan M, De Glisezinski I, Lafontan M, Galitzky J. Natriuretic peptides: a new lipolytic pathway in human adipocytes. FASEB J 2000; 14:1345-51.
  126. Birkenfeld AL, Boschmann M, Engeli S, Moro C, Arafat AM, Luft FC, et al. Atrial natriuretic peptide and adiponectin interactions in man. PloSOne 2012; 7:e43238.
  127. Lauria PBM, Del Puerto HL, Reis AM, Candido AL, Reis FM. Low plasma atrial natriuretic peptide: a new piece in the puzzle of polycystic ovary syndrome. J Clin Endocrinol Metab 2013; 98:4882-9.
  128. Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shirakami G, et al. Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinology 1992; 130:229-39.
  129. Sawada Y, Suda M, Yokoyama H, Kanda T, Sakamaki T, Tanaka S, et al. Stretch-induced hypertrophic growth of cardiocytes and processing of brain-type natriuretic peptide are controlled by proproteinprocessing endoprotease furin. J Biol Chem 1997; 272:20545-54.
  130. Celik O, Sahin I, Celik N, Hascalik S, Keskin L, Ozcan H, et al. Diagnostic potential of serum N-terminal pro-B-type brain natriuretic peptide level in detection of cardiac wall stress in women with polycystic ovary syndrome: a cross-sectional comparison study. Hum Reprod 2007; 22:2992-8.
  131. Dineva J, Vangelov I, Nikolov G, Gulenova D, Ivanova M. Atrial natriuretic peptide is an antiapoptotic factor for human granulosa luteinized cells with impact on the results of COH/IVF in women undergoing IVF program. J Obstet Gynaecol Res 2011; 37:511-9.
  132. Johnson KM, Hughes FM Jr, Fong YY, Mathur RS, WilliamsonHO, Gorospe WC. Effects of atrial natriuretic peptide on rat ovarian granulosa cell steroidogenesis in vitro. Am J Reprod Immunol 1994; 31:163-8.
  133. Tornell J, Carlsson B, Billig H. Atrial natriuretic peptide inhibits spontaneous rat oocyte maturation. Endocrinology 1990; 126:1504-8.
  134. Zhang W, Yang Y, Liu W, Chen Q, Wang H, Wang X, et al. Brain natriuretic peptide and C-type natriuretic peptide maintain porcine oocyte meiotic arrest. J Cell Physiol 2015; 230:71-81.
  135. Celik O, Celik N, Gungor S, Haberal ET, Aydin S. Selective Regulation of Oocyte Meiotic Events Enhances Progress in Fertility Preservation Methods. Biochem Insights 2015; 8:11-21.
  136. Gerbes AL, Dagnino L, Nguyen T, Nemer M. Transcription of brain natriuretic peptide and atrial natriuretic peptide genes in human tissues. J Clin Endocrinol Metab 1994; 78:1307-11.
  137. Hirschberg AL, Naessen S, Stridsberg M, Bystrom B, Holtet J. Impaired cholecystokinin secretion and disturbed appetite regulation in women with polycystic ovary syndrome. Gynecol Endocrinol 2004; 19:7987.
  138. Le Roux CW, Batterham RL, Aylwin SJ, Patterson M, Borg CM, Wynne KJ, et al. Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology 2006; 147:3-8.
  139. Moran LJ, Noakes M, Clifton PM, Wittert GA, Le Roux CW, Ghatei MA, et al. Postprandial ghrelin, cholecystokinin, peptide YY, and appetite before and after weight loss in overweight women with and without polycystic ovary syndrome. Am J Clin Nutr 2007; 86:1603-10.
  140. Svendsen PF, Nilas L, Madsbad S, Holst JJ. Incretin hormone secretion in women with polycystic ovary syndrome: roles of obesity, insulin sensitivity, and treatment with metformin. Metabolism 2009; 58:58693.
  141. Vrbikova J, Hill M, Bendlova B, Grimmichova T, Dvorakova K, Vondra K, et al. Incretin levels in polycystic ovary syndrome. Eur J Endocrinol 2008; 159:121-7.
  142. Reverchon M, Cornuau M, Cloix L, Ramé C, Guerif F, Royère D, et al. Visfatin is expressed in human granulosa cells: regulation by metformin through AMPK/SIRT1 pathways and its role in steroidogenesis. Mol Hum Reprod 2013; 19:313-26.
  143. Celik O, Celik N, Hascalik S, Sahin I, Aydin S, Ozerol E. An appraisal of serum preptin levels in PCOS. Fertil Steril 2011; 95:314-6.
  144. Yildirim B, Celik O, Aydin S. Adropin: a key component and potential gatekeeper of metabolic disturbances in policystic ovarian syndrome. Clin Exp Obstet Gynecol 2014; 41:310-2.
  145. Yilmaz E, Celik O, Celik N, Simsek Y, Celik E, Yildirim E. Serum orexin-A (OXA) level decreases in polycystic ovarian syndrome. Gynecol Endocrinol 2013; 29:388-90.
  146. Celik í–, Yılmaz E, Celik N, Minareci Y, Turkcuoglu I, Simsek Y, et al. Salusins, newly identified regulators of hemodynamics and mitogenesis, increase in polycystic ovarian syndrome. Gynecol Endocrinol 2013; 29:83-6.
  147. Taylor AE. Insulin-lowering medications in polycystic ovary syndrome. Obstet Gynecol Clin North Am 2000; 27:583-95.
  148. Yuan X, Hu T, Zhao H, Huang Y, Ye R, Lin J, et al. Brown adipose tissue transplantation ameliorates polycystic ovary syndrome. Proc Natl Acad Sci U S A 2016; 113:2708-13.
  149. Clarke IJ, Arbabi L. New concepts of the central control of reproduction, integrating influence of stress, metabolic state, and season. Domest Anim Endocrinol 2016; 56 Suppl:S165-79.
  150. George JT, Seminara SB. Kisspeptin and the hypothalamic control of reproduction: lessons from the human. Endocrinology 2012; 153:5130-6.
  151. Irfan A, Mughal IA, Jalali S. Effect of metformin hydrochloride in correcting hyperinsulinemia and high leptin levels in treatment of infertile polycystic patients. J Ayub Med Coll Abbottabad 2013; 25:8-11.
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