CHEMERIN (RARRES2) decreases in vitro granulosa cell steroidogenesis and blocks oocyte meiotic progression in bovine species

Biology of Reproduction

Volumn 90, Issue 5, 2014, Pages

  Reverchon, Maxime ^a   Bertoldo, Michael J ^a   Ramé, Christelle ^a   Froment, Pascal ^a   Dupont, Joëlle ^a  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

Adipokine; Cholesterol; Follicle; Granulosa; Hormone action; Oocyte maturation; Ovary; Reproduction; Signaling pathways

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; AROMATASE; CHEMERIN; CHEMOKINE RECEPTOR CCR2; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CMKLR1 PROTEIN; ESTRADIOL; G PROTEIN COUPLED RECEPTOR; INSULIN; LEPTIN; MESSENGER RNA; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROGESTERONE; PROTEIN; RESISTIN; ROSIGLITAZONE; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 2,4 THIAZOLIDINEDIONE DERIVATIVE; CHEMOKINE; CHEMOKINE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; RNA;

ANIMAL TISSUE; ARTICLE; CATTLE; CELL PROLIFERATION; CELL VIABILITY; CHOLESTEROL SYNTHESIS; CORPUS LUTEUM; CUMULUS CELL; ESTROGEN SYNTHESIS; GERMINAL VESICLE; GRANULOSA CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MEIOSIS; NONHUMAN; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; PROGESTERONE RELEASE; PROGESTERONE SYNTHESIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STEROID RELEASE; STEROIDOGENESIS; THECA CELL; ANIMAL; BOVINAE; CHEMISTRY; CYTOLOGY; FEMALE; GENETICS; METABOLISM; OVARY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; VETERINARY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CATTLE; CHEMOKINES; ESTRADIOL; FEMALE; GRANULOSA CELLS; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MEIOSIS; METFORMIN; MITOGEN-ACTIVATED PROTEIN KINASES; OOCYTES; OVARY; PROGESTERONE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CHEMOKINE; RNA; THIAZOLIDINEDIONES;

EID: 84903759280     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.117044     Document Type: Article

References (55)

1. Skrzeczynska-Moncznik J, Wawro K, Stefanska A, Oleszycka E, Kulig P, Zabel BA, Sulkowski M, Kapinska-Mrowiecka M, Czubak-Macugowska M, Butcher EC, Cichy J. Potential role of chemerin in recruitment of plasmacytoid dendritic cells to diseased skin. Biochem Biophys Res Commun 2009; 380:323-327.
2. Nagpal S, Patel S, Jacobe H, DiSepio D, Ghosn C, Malhotra M, Teng M, Duvic M, Chandraratna RA. Tazarotene-induced gene 2 (TIG2), a novel retinoid-responsive gene in skin. J Invest Dermatol 1997; 109:91-95.
3. Zabel BA, Allen SJ, Kulig P, Allen JA, Cichy J, Handel TM, Butcher EC. Chemerin activation by serine proteases of the coagulation, fibrinolytic, and inflammatory cascades. J Biol Chem 2005; 280:34661-34666.
4. Yoshimura T. Chemokine-like receptor 1 (CMKLR1) and chemokine (CC motif) receptor-like 2 (CCRL2); two multifunctional receptors with unusual properties. Exp Cell Res 2011; 317:674-684.
5. Barnea G, Strapps W, Herrada G, Berman Y, Ong J, Kloss B, Axel R, Lee KJ. The genetic design of signaling cascades to record receptor activation. Proc Natl Acad Sci U S A 2008; 105:64-69.
6. Bondue B, Wittamer V, Parmentier M. Chemerin and its receptors in leukocyte trafficking, inflammation and metabolism. Cytokine Growth Factor Rev 2011; 22:331-338.
7. Monnier J, Lewen S, O'Hara E, Huang K, Tu H, Butcher EC, Zabel BA. Expression, regulation, and function of atypical chemerin receptor CCRL2 on endothelial cells. J Immunol 2012; 189:956-967.
8. Wittamer V, Franssen JD, Vulcano M, Mirjolet JF, Le Poul E, Migeotte I, Brezillon S, Tyldesley R, Blanpain C, Detheux M, Mantovani A, Sozzani S, et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J Exp Med 2003; 198:977-985.
9. Goralski KB, McCarthy TC, Hanniman EA, Zabel BA, Butcher EC, Parlee SD, Muruganandan S, Sinal CJ. Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J Biol Chem 2007; 282: 28175-28188.
10. Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, Walder K, Segal D. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 2007; 148:4687-4694.
11. Tan BK, Chen J, Farhatullah S, Adya R, Kaur J, Heutling D, Lewandowski KC, O'Hare JP, Lehnert H, Randeva HS. Insulin and metformin regulate circulating and adipose tissue chemerin. Diabetes 2009; 58:1971-1977.
12. Suzuki Y, Song SH, Sato K, So KH, Ardiyanti A, Kitayama S, Hong YH, Lee SD, Choi KC, Hagino A, Katoh K, Roh SG. Chemerin analog regulates energy metabolism in sheep. Anim Sci J 2012; 83:263-267.
13. 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; 153:5600-5611.
14. Reverchon M, Cornuau M, Rame C, Guerif F, Royere D, Dupont J. Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells. Hum Reprod 2012; 27:1790-1800.
15. Li L, Ma P, Huang C, Liu Y, Zhang Y, Gao C, Xiao T, Ren PG, Zabel BA, Zhang JV. Expression of chemerin and its receptors in rat testes and its actions on testosterone secretion. J Endocrinol 2014; 220:155-163.
16. Mazaki-Tovi S, Kasher-Meron M, Hemi R, Haas J, Gat I, Lantsberg D, Hendler I, Kanety H. Chemerin is present in human cord blood and is positively correlated with birthweight. Am J Obstet Gynecol 2012; 207:412.
17. Kim JY, Xue K, Cao M, Wang Q, Liu JY, Leader A, Han JY, Tsang BK. Chemerin suppresses ovarian follicular development and its potential involvement in follicular arrest in rats treated chronically with dihydrotestosterone. Endocrinology 2013; 154:2912-2923.
18. Garces MF, Sanchez E, Acosta BJ, Angel E, Ruiz AI, Rubio-Romero JA, Dieguez C, Nogueiras R, Caminos JE. Expression and regulation of chemerin during rat pregnancy. Placenta 2012; 33:373-378.
19. Wang Q, Leader A, Tsang BK. Inhibitory roles of prohibitin and chemerin in FSH-induced rat granulosa cell steroidogenesis. Endocrinology 2013; 154:956-967.
20. Franks S. Polycystic ovary syndrome. N Engl J Med 1995; 333:853-861.
21. Gambineri A, Pelusi C, Vicennati V, Pagotto U, Pasquali R. Obesity and the polycystic ovary syndrome. Int J Obes Relat Metab Disord 2002; 26: 883-896.
22. Royal M, Mann GE, Flint AP. Strategies for reversing the trend towards subfertility in dairy cattle. Vet J 2000; 160:53-60.
23. Ohtani Y, Takahashi T, Sato K, Ardiyanti A, Song SH, Sato R, Onda K, Wada Y, Obara Y, Suzuki K, Hagino A, Roh SG, et al. Changes in circulating adiponectin and metabolic hormone concentrations during periparturient and lactation periods in Holstein dairy cows. Anim Sci J 2012; 83:788-795.
24. Mielenz M, Mielenz B, Singh SP, Kopp C, Heinz J, Haussler S, Sauerwein H. Development, validation, and pilot application of a semiquantitative Western blot analysis and an ELISA for bovine adiponectin. Domest Anim Endocrinol 2013; 44:121-130.
25. Laeger T, Sauerwein H, Tuchscherer A, Bellmann O, Metges CC, Kuhla B. Concentrations of hormones and metabolites in cerebrospinal fluid and plasma of dairy cows during the periparturient period. J Dairy Sci 2013; 96:2883-2893.
26. Elis S, Coyral-Castel S, Freret S, Cognie J, Desmarchais A, Fatet A, Rame C, Briant E, Maillard V, Dupont J. Expression of adipokine and lipid metabolism genes in adipose tissue of dairy cows differing in a female fertility quantitative trait locus. J Dairy Sci 2013; 96:7591-7602.
27. Tosca L, Chabrolle C, Uzbekova S, Dupont J. Effects of metformin on bovine granulosa cells steroidogenesis: possible involvement of adenosine 50 monophosphate-activated protein kinase (AMPK). Biol Reprod 2007; 76:368-378.
28. Tosca L, Uzbekova S, Chabrolle C, Dupont J. Possible role of 50AMPactivated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Biol Reprod 2007; 77:452-465.
29. Reverchon M, Cornuau M, Cloix L, Rame C, Guerif F, Royere D, Dupont J. Visfatin is expressed in human granulosa cells: regulation by metformin through AMPK/SIRT1 pathways and its role in steroidogenesis. Mol Hum Reprod 2013; 19:313-326.
30. Maillard V, Froment P, Rame C, Uzbekova S, Elis S, Dupont J. Expression and effect of resistin on bovine and rat granulosa cell steroidogenesis and proliferation. Reproduction 2011; 141:467-479.
31. Maillard V, Uzbekova S, Guignot F, Perreau C, Rame C, Coyral-Castel S, Dupont J. Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development. Reprod Biol Endocrinol 2010; 8:23.
32. Tabandeh MR, Hosseini A, Saeb M, KafiM, 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; 73:659-669.
33. Munoz-Gutierrez M, Findlay PA, Adam CL, Wax G, Campbell BK, Kendall NR, Khalid M, Forsberg M, Scaramuzzi RJ. The ovarian expression of mRNAs for aromatase, IGF-I receptor, IGF-binding protein-2,_4 and_5, leptin and leptin receptor in cycling ewes after three days of leptin infusion. Reproduction 2005; 130:869-881.
34. Sakumoto R, Shibaya M, Okuda K. Tumor necrosis factor-alpha (TNF alpha) inhibits progesterone and estradiol-17beta production from cultured granulosa cells: presence of TNFalpha receptors in bovine granulosa and theca cells. J Reprod Dev 2003; 49:441-449.
35. Tosca L, Froment P, Solnais P, Ferre P, Foufelle F, Dupont J. Adenosine 50-monophosphate-activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology 2005; 146:4500-4513.
36. Zhang X, Armstrong DT. Effects of follicle-stimulating hormone and ovarian steroids during in vitro meiotic maturation on fertilization of rat oocytes. Gamete Res 1989; 23:267-277.
37. Borman SM, Chaffin CL, Schwinof KM, Stouffer RL, Zelinski-Wooten MB. Progesterone promotes oocyte maturation, but not ovulation, in nonhuman primate follicles without a gonadotropin surge. Biol Reprod 2004; 71:366-373.
38. Jia Z, Zhang J, Wu Z, Tian J. Leptin enhances maturation and development of calf oocytes in vitro. Reprod Domest Anim 2011; 47: 718-723.
39. Zhao L, Yamaguchi Y, Sharif S, Du XY, Song JJ, Lee DM, Recht LD, Robinson WH, Morser J, Leung LL. Chemerin158K protein is the dominant chemerin isoform in synovial and cerebrospinal fluids but not in plasma. J Biol Chem 2011; 286:39520-39527.
40. Hu W, Feng P. Elevated serum chemerin concentrations are associated with renal dysfunction in type 2 diabetic patients. Diabetes Res Clin Pract 2011; 91:159-163.
41. Bozaoglu K, Curran JE, Stocker CJ, Zaibi MS, Segal D, Konstantopoulos N, Morrison S, Carless M, Dyer TD, Cole SA, Goring HH, Moses EK, et al. Chemerin, a novel adipokine in the regulation of angiogenesis. J Clin Endocrinol Metab 2010; 95:2476-2485.
42. Song SH, Fukui K, Nakajima K, Kozakai T, Sasaki S, Roh SG, Katoh K. Cloning, expression analysis, and regulatory mechanisms of bovine chemerin and chemerin receptor. Domest Anim Endocrinol 2010; 39: 97-105.
43. Bauer S, Bala M, Kopp A, Eisinger K, Schmid A, Schneider S, Neumeier M, Buechler C. Adipocyte chemerin release is induced by insulin without being translated to higher levels in vivo. Eur J Clin Invest 2012; 42: 1213-1220.
44. Pei L, Yang J, Du J, Liu H, Ao N, Zhang Y. Downregulation of chemerin and alleviation of endoplasmic reticulum stress by metformin in adipose tissue of rats. Diabetes Res Clin Pract 2012; 97:267-275.
45. Parlee SD, Ernst MC, Muruganandan S, Sinal CJ, Goralski KB. Serum chemerin levels vary with time of day and are modified by obesity and tumor necrosis factor-falphag. Endocrinology 2010; 151:2590-2602.
46. Spicer LJ. Tumor necrosis factor-alpha (TNF-alpha) inhibits steroidogenesis of bovine ovarian granulosa and thecal cells in vitro. Involvement of TNF-alpha receptors. Endocrine 1998; 8:109-115.
47. Wanninger J, Bauer S, Eisinger K, Weiss TS, Walter R, Hellerbrand C, Schaffler A, Higuchi A, Walsh K, Buechler C. Adiponectin upregulates hepatocyte CMKLR1 which is reduced in human fatty liver. Mol Cell Endocrinol 2012; 349:248-254.
48. Yang H, Li F, Kong X, Yuan X, Wang W, Huang R, Li T, Geng M, Wu G, Yin Y. Chemerin regulates proliferation and differentiation of myoblast cells via ERK1/2 and mTOR signaling pathways. Cytokine 2012; 60: 646-652.
49. Wang C, Wu WK, Liu X, To KF, Chen GG, Yu J, Ng EK. Increased serum chemerin level promotes cellular invasiveness in gastric cancer: a clinical and experimental study. Peptides 2014; 51C:131-138.
50. Becker M, Rabe K, Lebherz C, Zugwurst J, Goke B, Parhofer KG, Lehrke M, Broedl UC. Expression of human chemerin induces insulin resistance in the skeletal muscle but does not affect weight, lipid levels, and atherosclerosis in LDL receptor knockout mice on high-fat diet. Diabetes 2010; 59:2898-2903.
51. Seto-Young D, Zajac J, Liu HC, Rosenwaks Z, Poretsky L. The role of mitogen-activated protein kinase in insulin and insulin-like growth factor I (IGF-I) signaling cascades for progesterone and IGF-binding protein-1 production in human granulosa cells. J Clin Endocrinol Metab 2003; 88: 3385-3391.
52. Kraemer FB. Adrenal cholesterol utilization. Mol Cell Endocrinol 2007; 265-266:42-45.
53. Baranao JL, Hammond JM. FSH increases the synthesis and stores of cholesterol in porcine granulosa cells. Mol Cell Endocrinol 1986; 44: 227-236.
54. Spicer LJ, Hamilton TD, Keefer BE. Insulin-like growth factor I enhancement of steroidogenesis by bovine granulosa cells and thecal cells: dependence on de novo cholesterol synthesis. J Endocrinol 1996; 151:365-373.
55. Fissore RA, He CL, Vande Woude GF. Potential role of mitogen-activated protein kinase during meiosis resumption in bovine oocytes. Biol Reprod 1996; 55:1261-1270.