Skip to main content

Advertisement

Log in

Adiponectin and Chemerin: Contrary Adipokines in Regulating Reproduction and Metabolic Disorders

  • Review
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Metabolic disorders such as obesity and type 2 diabetes are one of the most familiar risk factors in the present time among every age-group. It is associated with altered levels of adipokines such as adiponectin, chemerin, leptin, resistin, visfatin, and so on. Adiponectin is one of the adipocyte-specific protein with novel applications pertaining to metabolism by promoting insulin sensitivity and regulating glucose and fatty acid catabolism, while chemerin is considered as an inhibitor of insulin signaling and glucose catabolism. Other than these established functions, both the adipokines are intimately involved in coordinating reproductive activities, but they exhibit contrary functions. This review is an amalgamation of recent information related to adiponectin and chemerin in male and female reproduction and further its association with metabolism-related reproductive disorders. The direct effect of adiponectin and chemerin on various reproductive parameters has been investigated, but there was a rampant failure to account for in vivo data which gives a broad outlook on the regulatory mechanism of both adiponectin and chemerin related to male and female reproductive functions. Adiponectin is known to promote gonadal activities, while chemerin exerts antigonadal actions. Recent research suggests that high chemerin/low adiponectin ratio plays a vital role in causing dyslipidemia and metabolic syndrome in patients. The dysregulated ratio of adiponectin to chemerin during various metabolic disorders makes it really worthy in relation to an application for therapeutics. Still, a lot regarding both the adipokines has to be explored and brought forward in order to deal with therapeutics of metabolism-related reproductive disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Moges B, Amare B, Fantahun B, Kassu A. High prevalence of overweight, obesity, and hypertension with increased risk to cardiovascular disorders among adults in northwest Ethiopia: a cross sectional study. BMC Cardiovascu Disord. 2014;14:155.

    Article  Google Scholar 

  2. Coelho M, Oliveira T, Fernandes R. Biochemistry of adipose tissue: an endocrine organ. Arch Med Sci. 2013;9(2):191–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Reverchon M, Rameé C, Bertoldo M, Dupont J. Adipokines and the female reproductive tract. Int J Endocrinol. 2014;2014: 232454.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Rak A, Mellouk N, Froment P. Adiponectin and resistin: potential metabolic signals affecting hypothalamo-pituitary gonadal axis in females and males of different species. Reproduction. 2017; 153(6):R215–R226.

    Article  CAS  PubMed  Google Scholar 

  5. Yamauchi T, Kamon J, Waki H, et al. The fatderived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7(8):941–946.

    Article  CAS  PubMed  Google Scholar 

  6. Yamauchi T, Kamon J, Minokoshi Y, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med. 2002;8(11):1288–1295.

    Article  CAS  PubMed  Google Scholar 

  7. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med. 2001;7(8):947–953.

    Article  CAS  PubMed  Google Scholar 

  8. Stefan N, Stumvoll M. Adiponectin—its role in metabolism and beyond 24. Horm Metab Res. 2002;34(9):469–474.

    Article  CAS  PubMed  Google Scholar 

  9. Brochu-Gaudreau K, Rehfeldt C, Blouin R, Bordignon V, Murphy BD, Palin MF. Adiponectin action from head to toe. Endocrine. 2010;37(1):11–32.

    Article  CAS  PubMed  Google Scholar 

  10. Okamoto Y. Adiponectin provides cardiovascular protection in metabolic syndrome. Cardiol Res Pract. 2011;2011:313179.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Yamauchi T, Kadowaki T. Adiponectin receptor as a key player in healthy longevity and obesity-related diseases. Cell Metab. 2013; 17(2):185–196.

    Article  CAS  PubMed  Google Scholar 

  12. Comninos AN, Jayasena CN, Dhillo WS. The relationship between gut and adipose hormones, and reproduction. Hum Reprod Update. 2014;20(2):153–174.

    Article  CAS  PubMed  Google Scholar 

  13. Bondue B, Wittamer V, Parmentier M. Chemerin and its receptors in leukocyte trafficking, inflammation and metabolism. Cytokine Growth Factor Rev. 2011;22(5-6):331–338. doi:10.1016/j. cytogfr.2011.11.004

    Article  CAS  PubMed  Google Scholar 

  14. Weyer C, Funahashi T, Tanaka S, et al. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001; 86(5):1930–1935.

    Article  CAS  PubMed  Google Scholar 

  15. Hoffstedt J, Arvidsson E, Sjölin E, Wåhleén K, Arner P. Adipose tissue adiponectin production and adiponectin serum concentration in human obesity and insulin resistance. J Clin Endocrinol Metab. 2004;89(3):1391–1396.

    Article  CAS  PubMed  Google Scholar 

  16. Kim DH, Kim C, Ding EL, Townsend MK, Lipsitz LA. Adiponectin levels and the risk of hypertension: a systematic review and meta-analysis. Hypertension. 2013;62(1):27–32.

    Article  CAS  PubMed  Google Scholar 

  17. Kim HS, Jo J, Lim JE, et al. Adiponectin as predictor for diabetes among prediabetic groups. Endocrine. 2013;44(2):411–418.

    Article  CAS  PubMed  Google Scholar 

  18. Chu SH, Lee MK, Ahn KY, et al. Chemerin and adiponectin contribute reciprocally to metabolic syndrome. PLoS One. 2012;7(4):e34710.

    Article  CAS  Google Scholar 

  19. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem. 1995;270(45):26746–26750.

    Article  CAS  PubMed  Google Scholar 

  20. Hu E, Liang P, Spiegelman BM. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem. 1996; 271(18):10697–10703.

    Article  CAS  PubMed  Google Scholar 

  21. Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (adipose most abundant gene transcript 1). Biochem Biophys Res Commun. 1996; 221(2):286–289.

    Article  CAS  PubMed  Google Scholar 

  22. Nakano Y, Tobe T, Choi-Miura NH, Mazda T, Tomita M. Isolation and characterization of GBP28: a novel gelatin-binding protein purified from human, plasma. J Biochem. 1996; 120(4):803–812.

    Article  CAS  PubMed  Google Scholar 

  23. Yamauchi T, Kamon J, Ito Y, et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature. 2003; 423(6941):762–769.

    Article  CAS  PubMed  Google Scholar 

  24. Yamauchi T, Nio Y, Maki T, et al. Targeted disruption of Adi-poR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med. 2007;13(3):332–339.

    Article  CAS  PubMed  Google Scholar 

  25. Nagpal S, Patel S, Jacobe H, et al. Tazarotene-induced gene 2 (TIG2), a novel retinoid-responsive gene in skin. J Invest Dermatol. 1997;109(1):91–95.

    Article  CAS  PubMed  Google Scholar 

  26. Marchese A, Docherty JM, Nguyen T, et al. Cloning of human genes encoding novel G protein-coupled receptors. Genomics. 1994;23(3):609–618.

    Article  CAS  PubMed  Google Scholar 

  27. Barnea G, Strapps W, Herrada G, et al. The genetic design of signaling cascades to record receptor activation. Proc Natl Acad Sci U S A. 2008;105(1):64–69.

    Article  CAS  PubMed  Google Scholar 

  28. Gantz I, Konda Y, Yang YK, Miller DE, Dierick HA, Yamada T. Molecular cloning of a novel receptor (CMKLR1) with homology to the chemotactic factor receptors. Cytogenet Cell Genet. 1996; 74(4):286–290.

    Article  CAS  PubMed  Google Scholar 

  29. Fan P, Kyaw H, Su K, et al. Cloning and characterization of a novel human chemokine receptor. Biochem Biophys Res Commun. 1998;243(1):264–268.

    Article  CAS  PubMed  Google Scholar 

  30. Zabel BA, Nakae S, Zuniga L, et al. Mast cell-expressed orphan receptor CCRL2 binds chemerin and is required for optimal induction of IgE-mediated passive cutaneous anaphylaxis. J Exp Med. 2008;205(10):2207–2220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ruan H, Dong LQ. Adiponectin signaling and function in insulin target tissues. J Mol Cell Biol. 2016;8(2):101–109.doi:10.1093/ jmcb/mjw014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Arita Y, Kihara S, Ouchi N, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999;257(1):79–83.

    Article  CAS  PubMed  Google Scholar 

  33. Sieminska L, Marek B, Kos-Kudla B, et al. Serum adiponectin in women with polycystic ovarian syndrome and its relation to clinical, metabolic and endocrine parameters. J Endocrinol Invest. 2004;27(6):528–534.

    Article  CAS  PubMed  Google Scholar 

  34. Yang WS, Lee WJ, Funahashi T, et al. Weight reduction increases plasma levels of an adipose-derived anti-inflammatory protein, adiponectin. J Clin Endocrinol Metab. 2001;86(8):3815–3819.

    Article  CAS  PubMed  Google Scholar 

  35. Pajvani UB, Du X, Combs TP, et al. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin: implications for metabolic regulation and bioactivity. J Biol Chem. 2003;278(11):9073–9085.

    Article  CAS  PubMed  Google Scholar 

  36. Waki H, Yamauchi T, Kamon J, et al. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J Biol Chem. 2003;278(41):40352–40363.

    Article  CAS  PubMed  Google Scholar 

  37. Pajvani UB, Hawkins M, Combs TP, et al. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J Biol Chem. 2004;279(13):12152–12162.

    Article  CAS  PubMed  Google Scholar 

  38. Miyazaki T, Bub JD, Uzuki M, Iwamoto Y. Adiponectin activates c-Jun NH2-terminal kinase and inhibits signal transducer and activator of transcription 3. Biochem Biophys Res Commun. 2005;333(1):79–87.

    Article  CAS  PubMed  Google Scholar 

  39. Ceddia RB, Somwar R, Maida A, Fang X, Bikopoulos G, Sweeney G. Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia. 2005;48(1):132–139.

    Article  CAS  PubMed  Google Scholar 

  40. Fang X, Palanivel R, Zhou X, et al. Hyperglycemia- and hyperinsulinemia-induced alteration of adiponectin receptor expression and adiponectin effects in L6 myoblasts. J Mol Endocrinol. 2005;35(3):465–476.

    Article  CAS  PubMed  Google Scholar 

  41. Fruebis J, Tsao T, Javorschi S, et al. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci U S A. 2001;98(4):2005–2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mattern A, Zellmann T, Beck-Sickinger AG. Processing, signaling, and physiological function of chemerin. IUBMB Life. 2014; 66(1):19–26.

    Article  CAS  PubMed  Google Scholar 

  43. Zabel BA, Zuniga L, Ohyama T, et al. Chemoattractants, extra-cellular proteases, and the integrated host defense response. Exp Hematol. 2006;34(8):1021–1032.

    Article  CAS  PubMed  Google Scholar 

  44. Fatima SS, Rehman R, Baig M, Khan TA. New roles of the multidimensional adipokine: chemerin. Peptides. 2014;62:15–20.

    Article  CAS  PubMed  Google Scholar 

  45. Bozaoglu K, Bolton K, McMillan J, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology. 2007;148(10):4687–4694.

    Article  CAS  PubMed  Google Scholar 

  46. Coimbra S, Brandão Proença J, Santos-Silva A, Neuparth MJ. Adiponectin, leptin, and chemerin in elderly patients with type 2 diabetes mellitus: a close linkage with obesity and length of the disease. BioMed Res Int. 2014;2014:701915.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Tang YT, Hu T, Arterburn M, et al. PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol. 2005;61(3):372–380.

    Article  CAS  PubMed  Google Scholar 

  48. Tanabe H, Fujii Y, Okada-Iwabu M, et al. Crystal structures of the human adiponectin receptors. Nature. 2015;520(7547):312–316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Campos DB, Palin M-F, Bordignon V, Murphy BD. The “beneficial” adipokines in reproduction and fertility. Int J Obes (Lond). 2008;32(2):223–231.

    Article  CAS  Google Scholar 

  50. Matsunami T, Sato Y, Ariga S, et al. Regulation of oxidative stress and inflammation by hepatic adiponectin receptor 2 in an animal model of nonalcoholic steatohepatitis. Int J Clin Exp Pathol. 2010;3(5):472–481.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Yoshimura T, Oppenheim JJ. Chemokine-like receptor 1 (CMKLR1) and chemokine (C-C motif) receptor-like 2 (CCRL2): two multifunctional receptors with unusual properties. Exp Cell Res. 2011;317(5):674–684. doi:10.1016/j.yexcr.2010. 10.023

    Article  CAS  PubMed  Google Scholar 

  52. Monnier J, Lewen S, O’Hara E, Huang K, Tu H, Butcher EC. Expression, regulation, and function of atypical chemerin recep-torCCRL2 on endothelial cells. J Immunol. 2012;189(2):956–967. doi:10.4049/jimmunol.1102871

    Article  CAS  PubMed  Google Scholar 

  53. Helfer G, Ross AW, Thomson LM, et al. A neuroendocrine role for chemerin in hypothalamic remodelling and photoperiodic control of energy balance. Sci Rep. 2016;6:26830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Combs TP, Berg AH, Rajala MW, et al. Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes. 2003;52(2):268–276.

    Article  CAS  PubMed  Google Scholar 

  55. Nagasawa A, Fukui K, Funahashi T, et al. Effects of soy protein diet on the expression of adipose genes and plasma adiponectin. Horm Metab Res. 2002;34(11-12):635–639.

    Article  CAS  PubMed  Google Scholar 

  56. Flachs P, Mohamed-Ali V, Horakova O, et al. Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed a high-fat diet. Diabetologia. 2006;49(2):394–397.

    Article  CAS  PubMed  Google Scholar 

  57. Nagao K, Inoue N, Wang YM, Yanagita T. Conjugated linoleic acid enhances plasma adiponectin level and alleviates hyperinsu-linemia and hypertension in Zucker diabetic fatty (fa/fa) rats. Biochem Biophys Res Commun. 2003;310(2):562–566.

    Article  CAS  PubMed  Google Scholar 

  58. Mellouk N, Rame C, Marchand M, et al. Effect of different levels of feed restriction and fish oil fatty acid supplementation on fat deposition by using different techniques, plasma levels and mRNA expression of several adipokines in broiler breeder hens. PLoS One. 2018;13(1):e0191121.

    Article  CAS  Google Scholar 

  59. 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(4):480–487.

    Article  CAS  PubMed  Google Scholar 

  60. 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(4):719–731.

    Article  CAS  PubMed  Google Scholar 

  61. Comim F. V., Hardy K, Franks S. Adiponectin and its receptors in the ovary: further evidence for a link between obesity and hyperandrogenism in polycystic ovary syndrome. PLoS One. 2013; 8(11):e80416.

    Article  CAS  Google Scholar 

  62. Singh A, Bora P, Krishna A. Direct action of adiponectin ameliorates increased androgen synthesis and reduces insulin receptor expression in the polycystic ovary. Biochem Biophys Res Commun. 2017;488(3):509–515.

    Article  CAS  PubMed  Google Scholar 

  63. Ledoux S, Campos DB, Lopes FL, Dobiasgoff M, Palin M, Murphy BD. Adiponectin induces periovulatory changes in ovarian follicular cells. Endocrinology. 2006;147(11):5178–5186.

    Article  CAS  PubMed  Google Scholar 

  64. Lord E, Ledoux S, Murphy BD, Beaudry D, Palin MF. Expression of adiponectin and its receptors in swine. J Anim Sci. 2005; 83(3):565–578.

    Article  CAS  PubMed  Google Scholar 

  65. 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(1-2):38–45. doi:10. 1016/j.mce.2008.01.007

    Article  CAS  PubMed  Google Scholar 

  66. Maillard V, Uzbekova S, Guignot F, Perreau C, Rameé C, Coyralcastel S. Effect of adiponectin on bovine granulosa cell steroido-genesis, oocyte maturation and embryo development. Reprod Biol Endocrinol. 2010;8:23. doi:10.1186/1477-7827-8-23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Singh A, Krishna A. Localization of adiponectin and its receptor and its possible roles in the ovary of a vespertilionid bat, Scotophilus heathi. Gen Comp Endocrinol. 2012;176(2):240–251. doi: 10.1016/j.ygcen.2012.01.020

    Article  CAS  PubMed  Google Scholar 

  68. Oliveira BSP, Costa JAS, Gomes ET, et al. Expression of adiponectin and its receptors ( AdipoR1 and AdipoR2 ) in goat ovary and its effect on oocyte nuclear maturation in vitro. Theriogenology. 2017;104:127–133.

    Article  CAS  PubMed  Google Scholar 

  69. Chabrolle C, Tosca L, Rameé C, Lecomte P, Roye`re D, Dupont J. Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells. Fertil Steril. 2009;92(6):1988–1996.

    Article  CAS  PubMed  Google Scholar 

  70. Tabandeh MR, Hosseini A, Saeb M, Kafi M, Saeb S. Changes in the gene expression of adiponectin and adiponectin receptors (AdipoR1 and AdipoR2) in ovarian follicular cells of dairy cow at different stages of development. Theriogenology. 2010; 73(5):659–669.

    Article  CAS  PubMed  Google Scholar 

  71. Cheng L, Shi H, Jin Y, et al. Adiponectin deficiency leads to female subfertility and ovarian dysfunctions in mice. Endocrinology. 2016;157(12):4875–4887.

    Article  CAS  PubMed  Google Scholar 

  72. Gutman G, Barak V, Maslovitz S, Amit A, Lessing JB, Geva E. Recombinant luteinizing hormone induces increased production of ovarian follicular adiponectin in vivo: implications for enhanced insulin sensitivity. Fertil Steril. 2009;91(5):1837–1841.

    Article  CAS  PubMed  Google Scholar 

  73. Singh A, Krishna A. Effects of adiponectin on ovarian folliculo-genesis and steroidogenesis in the vespertilionid bat, Scotophilus heathi. Gen Comp Endocrinol. 2012;178(3):502–510. doi:10. 1016/j.ygcen.2012.06.027

    Article  CAS  PubMed  Google Scholar 

  74. Takemura Y, Osuga Y, Yamauchi T, et al. Expression of adiponectin receptors and its possible implication in the human endometrium. Endocrinology. 2006;147(7):3203–3210.

    Article  CAS  PubMed  Google Scholar 

  75. Caminos JE, Nogueiras R, Gallego R, et al. Expression and regulation of adiponectin and receptor in human and rat placenta. J Clin Endocrinol Metabolism. 2005;90(7):4276–4286.

    Article  CAS  Google Scholar 

  76. Chen J, Tan B, Karteris E, et al. Secretion of adiponectin by human placenta: differential modulation of adiponectin and its receptors by cytokines. Diabetologia. 2006;49(6):1292–1302.

    Article  CAS  PubMed  Google Scholar 

  77. Lappas M, Yee K, Permezel M, Rice GE. Release and regulation of leptin, resistin and adiponectin from human placenta, fetal membranes, and maternal adipose tissue and skeletal muscle from normal and gestational diabetes mellitus-complicated pregnancies. J Endocrinol. 2005;186(3):457–465.

    Article  CAS  PubMed  Google Scholar 

  78. McDonald EA, Wolfe MW. Adiponectin attenuation of endocrine function within human term trophoblast cells. Endocrinology. 2009;150(9):4358–4365.

    Article  CAS  PubMed  Google Scholar 

  79. Kim ST, Marquard K, Stephens S, Louden E, Allsworth J, Moley KH. Adiponectin and adiponectin receptors in the mouse preim-plantation embryo and uterus. Hum Reprod. 2011;26(1):82–95.

    Article  CAS  PubMed  Google Scholar 

  80. Pierre P, Froment P, Ngre D, et al. Role of adiponectin receptors, AdipoR1 and AdipoR2, in the steroidogenesis of the human granulosa tumor cell line, KGN. Hum Reprod. 2009; 24(11):2890–2901.

    Article  CAS  PubMed  Google Scholar 

  81. Kim JY, Xue K, Cao M, et al. Chemerin suppresses ovarian follicular development and its potential involvement in follicular arrest in rats treated chronically with dihydrotestosterone. Endocrinology. 2013;154(8):2912–2923.

    Article  CAS  PubMed  Google Scholar 

  82. Reverchon M, Cornuau M, Ram C., Guerif F, Royre D, Dupont J. Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells. Hum Reprod. 2012; 27(6):1790–1800.

    Article  CAS  PubMed  Google Scholar 

  83. Reverchon M, Bertoldo MJ, Rameé C, Froment P, Dupont J. CHE-MERIN (RARRES2) decreases in vitro granulosa cell steroidogenesis and blocks oocyte meiotic progression in bovine species. Biol Reprod. 2014;90(5):102. doi:10.1095/biolreprod. 113.117044

    Article  PubMed  CAS  Google Scholar 

  84. Yang YL, Ren LR, Sun LF, et al. The role of GPR1 signaling in mice corpus luteum. J Endocrinol. 2016;230(1):55–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Diot M, Reverchon M, Rame C, et al. Expression of adiponectin, chemerin and visfatin in plasma and different tissues during a laying season in turkeys. Reprod Biol Endocrinol. 2015;13:1–14.

    Article  CAS  Google Scholar 

  86. Garces MF, Sanchez E, Acosta BJ, et al. Expression and regulation of chemerin during rat pregnancy. Placenta. 2012;33(5)

    Google Scholar 

  87. Carlino C, Trotta E, Stabile H, et al. Chemerin regulates NK cell accumulation and endothelial cell morphogenesis in the decidua during early pregnancy. J Clin Endocrinol Metab. 2012; 97(10):3603–3612. doi:10.1210/jc.2012-1102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wang Q, Kim JY, Xue K, Liu JY, Leader A, Tsang BK. Chemerin, a novel regulator of follicular steroidogenesis and its potential involvement in polycystic ovarian syndrome. Endocrinology. 2012;153(11):5600–5611.

    Article  CAS  PubMed  Google Scholar 

  89. Ocoén-Grove OM, Krzysik-Walker SM, Maddineni SR, Hendricks GL, Ramachandran R. Adiponectin and its receptors are expressed in the chicken testis: influence of sexual maturation on testicular ADIPOR1 and ADIPOR2 mRNA abundance. Reproduction. 2008;136(5):627–638. doi:10.1530/REP-07-0446

    Article  CAS  Google Scholar 

  90. Caminos JE, Nogueiras R, Gayta F, Pineda R, Gonza CR. Novel expression and direct effects of adiponectin in the rat testis. Endocrinology. 2008;149(7):3390–3402.

    Article  CAS  PubMed  Google Scholar 

  91. Rahmanifara F, Tabandehb MR. Adiponectin and its receptors gene expression in the reproductive tract of Ram. Small Ruminant Res. 2012;105:263–267.

    Article  Google Scholar 

  92. Civitarese AE, Jenkinson CP, Richardson D, et al. Adiponectin receptors gene expression and insulin sensitivity in non-diabetic Mexican Americans with or without a family history of type 2 diabetes. Diabetologia. 2004;47(5):816–820.

    Article  CAS  PubMed  Google Scholar 

  93. Kasimanickam VR, Kasimanickam RK, Kastelic JP, Stevenson JS. Associations of adiponectin and fertility estimates in Holstein bulls. Theriogenology. 2013;79(5):766–777.

    Article  CAS  PubMed  Google Scholar 

  94. Bjursell M, Ahnmark A, Bohlooly YM, et al. Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes. 2007;56(3):583–593.

    Article  CAS  PubMed  Google Scholar 

  95. Maeda N, Shimomura I, Kishida K, et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med. 2002; 8(7):731–737.

    Article  CAS  PubMed  Google Scholar 

  96. Schäffler A, Schölmerich J, Salzberger B. Adipose tissue as an immunological organ: Toll-like receptors, C1q/TNFs and CTRPs. Trends in Immunology. 2007;28(9):393–399.

    Article  PubMed  CAS  Google Scholar 

  97. Wu L, Xu B, Fan W, Zhu X, Wang G, Zhang A. Adiponectin protects Leydig cells against proinflammatory cytokines by suppressing the nuclear factor-kB signaling pathway. FEBS J. 2013; 280(16):3920–3927.

    Article  CAS  PubMed  Google Scholar 

  98. Hong CY, Park JH, Ahn RS, et al. Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor alpha. Mol Cell Biol. 2004; 24(7):2593–2604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Pfaehler A, Nanjappa MK, Coleman ES, et al. Regulation of adiponectin secretion by soy isoflavones has implication for endocrine function of the testis. Toxicology Lett. 2012; 209(1):78–85.

    Article  CAS  Google Scholar 

  100. Landry D, Pareé A, Jean S, Martin LJ. Adiponectin influences progesterone production from MA-10 Leydig cells in a dose-dependent manner. Endocrine. 2015;48(3):957–967.

    Article  CAS  PubMed  Google Scholar 

  101. Jones R. Plasma membrane structure and remodelling during sperm maturation in the epididymis. J Reprod Fertil. 1998;53: 73–84.

    CAS  Google Scholar 

  102. Marengo SR.Maturing the sperm: unique mechanisms for modifying integral proteins in the sperm plasma membrane. Animal Reprod Sci. 2008;105(1-2):52–63.

    Article  CAS  Google Scholar 

  103. Wittamer V, Franssen JD, Vulcano M, et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J Exp Med. 2003; 198(7):977–985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Takahashi M, Okimura Y, Iguchi G, et al. Chemerin regulates β-cell function in mice. Sci Rep. 2011;1:123.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Li L, Ma P, Huang C, et al. Expression of chemerin and its receptors in rat testes and its action on testosterone secretion. J Endocrinol. 2014;220(2):155–163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Li L, Huang C, Zhang X, et al. Chemerin-derived peptide C-20 suppressed gonadal steroidogenesis. Am J Reprod Immunol. 2014;71(3):265–277. doi:10.1111/aji.12164

    Article  CAS  PubMed  Google Scholar 

  107. Escobar-Morreale HF, Villuendas G, Botella-Carretero JI, et al. Adiponectin and resistin in PCOS: a clinical, biochemical and molecular genetic study. Hum Reprod. 2006;21(9):2257–2265.

    Article  CAS  PubMed  Google Scholar 

  108. Orio F, Palomba S, Cascella T, et al. Adiponectin levels in women with polycystic ovary syndrome. J Clin Endocrinol Metabol. 2003;88:2619–2623.

    Article  CAS  Google Scholar 

  109. 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(9):1790–1796.

    Article  CAS  PubMed  Google Scholar 

  110. Carmina E, Orio F, Palomba S, et al. Evidence for altered adipocyte function in polycystic ovary syndrome. Eur J Endocrinol. 2005;152(3):389–394.

    Article  CAS  PubMed  Google Scholar 

  111. Benrick A, Chancloén B, Micallef P, Wu Y, Hadi L, Shelton JM. Adiponectin protects against development of metabolic disturbances in a PCOS mouse model. Proc Natl Acad Sci U S A. 2017;114(34):E7187–E7196. doi:10.1073/pnas.170885 4114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Singh A, Bora P, Krishna A. Systemic adiponectin treatment reverses polycystic ovary syndrome-like features in an animal model. Reprod Fertil Dev. 2017;30(4):571–584. doi:10.1071/ RD17255

    Article  CAS  Google Scholar 

  113. Krishna A. Modulation of ovarian steroidogenesis by adiponectin during delayed embryonic development of Cynopterus sphinx. J Steroid Biochem Mol Biol. 2014;143:291–305. doi: 10.1016/j.jsbmb.2014.04.009

    Article  PubMed  CAS  Google Scholar 

  114. Anuradha, Krishna A. Role of adiponectin in delayed embryonic development of the short-nosed fruit bat, Cynopterus sphinx. Mol Reprod Dev. 2014;81(12):1086–1102. doi:10.1002/mrd. 22425

    Article  CAS  PubMed  Google Scholar 

  115. Dal Maso L, Augustin LSA, Karalis A, et al. Circulating adiponectin and endometrial cancer risk. J Clin Endocrinol Metabol. 2004;89(3):1160–1163.

    Article  CAS  Google Scholar 

  116. Martin LJ. Implications of adiponectin in linking metabolism to testicular function. Endocrine. 2014;46(1):16–28. doi:10.1007/ s12020-013-0102-0

    Article  CAS  PubMed  Google Scholar 

  117. Bai J, Liu Y, Niu GF, et al. Relationship between adiponectin and testosterone in patients with type 2 diabetes. Biochem Med (Zagreb). 2011;21(1):65–70.

    Article  CAS  Google Scholar 

  118. Kashou AH, du Plessis SS, Agarwal A. The Role of Obesity in ROS Generation and Male Infertility. In: Agarwal A, Aitken R, Alvarez J, eds, Studies on Men’s Health and Fertility. Oxidative Stress in Applied Basic Research and Clinical Practice. New York, NY: Humana Press, c/o Springer Science+Business Media, LLC.; 2012;571–590.

    Google Scholar 

  119. Guo Z, Yan X, Wang L, Wu J, Jing X, Liu J. Effect of telmisartan or insulin on the expression of adiponectin and its receptors in the testis of streptozotocin-induced diabetic rats. Horm Metab Res. 2016;48(6):404–412. doi:10.1055/s-0042-101549

    Article  CAS  PubMed  Google Scholar 

  120. Rato MLG, Alves S, Socorro JE, et al. Metabolic regulation is important for spermatogenesis. Nat Rev Urol. 2012; 9(6):330–338.

    Article  CAS  PubMed  Google Scholar 

  121. Kawwass JF, Summer R, Kallen CB. Direct effects of leptin and adiponectin on peripheral reproductive tissues: a critical review. Mol Hum Reprod. 2015;21(8):617–632.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Fu S, Xu H, Gu M, et al. Adiponectin deficiency contributes to the development and progression of benign prostatic hyperplasia in obesity. Sci Rep. 2017;7:43771–143715. doi:10.1038/srep43771

    Article  PubMed  PubMed Central  Google Scholar 

  123. Wang Q, Leader A, Tsang BK. Inhibitory roles of prohibitin and chemerin in FSH-induced rat granulosa cell steroidogenesis. Endocrinology. 2013;154(2):956–967.

    Article  CAS  PubMed  Google Scholar 

  124. Kort DH, Kostolias A, Sullivan C, Lobo RA. Chemerin as a marker of body fat and insulin resistance in women with polycystic ovary syndrome. Gynecol Endocrinol. 2014;3590:1–4.

    Google Scholar 

  125. Tan BK, Chen J, Farhatullah S, et al. Insulin and metformin regulate circulating and adipose tissue chemerin. Diabetes. 2009;58(9):1971–1977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Tal S, Seifer DB, Arici A. The emerging role of angiogenic factor dysregulation in the pathogenesis of polycystic ovarian syndrome. Semin Reprod Med. 2015;33(3):195–207

    Article  CAS  PubMed  Google Scholar 

  127. Bozaoglu K, Curran JE, Stocker CJ, Zaibi MS, Segal D, Konstantopoulos N. Chemerin, a novel adipokine in the regulation of angiogenesis. J Clin Endocrinol Metab. 2010;95(5):2476–2485. doi:10.1210/jc.2010-0042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Kabiri N, Tabandeh M, Tabatabaie SR. Beneficial effects of pioglitazone and metformin in murine model of polycystic ovaries via improvement of chemerin gene up-regulation. DARU. 2014;22:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. Jialal I, Devaraj S, Kaur H, Adams-Huet B, Bremer AA. Increased chemerin and decreased omentin-1 in both adipose tissue and plasma in nascent metabolic syndrome. J Clin Endocrinol Metab. 2013;98(3):E514–E517.

    Article  CAS  PubMed  Google Scholar 

  130. Weigert J, Neumeier M, Wanninger J, et al. Systemic chemerin is related to inflammation rather than obesity in type 2 diabetes. Clin Endocrinol (Oxf). 2010;72(3):342–348.

    Article  CAS  Google Scholar 

  131. Fatima SS, Bozaoglu K, Rehman R, Alam F, Memon AS. Elevated chemerin levels in Pakistani men: an interrelation with metabolic syndrome phenotypes. PLoS One. 2013;8(2):e57113.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, A., Choubey, M., Bora, P. et al. Adiponectin and Chemerin: Contrary Adipokines in Regulating Reproduction and Metabolic Disorders. Reprod. Sci. 25, 1462–1473 (2018). https://doi.org/10.1177/1933719118770547

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719118770547

Keywords

Navigation