Sex steroid hormones induce acylation stimulating protein resistance in 3T3-L1 adipocytes

Journal of Cellular Biochemistry

Volumn 105, Issue 2, 2008, Pages 404-413

  Wen, Yu ^a   Wang, HongWei ^a   MacLaren, Robin ^b,c   Lu, HuiLing ^a   Hu, Xiu Fen ^a   Cianflone, Katherine ^a,b,c  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b LAVAL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

C3adesArg; C5L2; Estradiol and testosterone; Glucose transport; Intracellular signalling; Progesterone

Indexed keywords

ACYLATION STIMULATING PROTEIN; ESTRADIOL; GLUCOSE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; PROGESTERONE; PROTEIN KINASE C ALPHA; TESTOSTERONE;

ACYLATION; ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GLUCOSE TRANSPORT; HORMONE ACTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; COMPLEMENT C3; ESTRADIOL; GONADAL STEROID HORMONES; INSULIN RESISTANCE; MICE; PROGESTERONE; RECEPTORS, CHEMOKINE; TESTOSTERONE;

EID: 54849425545     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21838     Document Type: Article

References (45)

1. Baldo A, Sniderman AD, St-Luce S, Avramoglu RK, Maslowska M, Hoang B, Monge JC, Bell A, Mulay S, Cianflone K. 1993. The adipsin-acylation stimulating protein system and regulation of intracellular triglyceride synthesis. J Clin Invest 92:1543-1547.
2. Baldo A, Sniderman AD, St., Luce S, Zhang XJ, Cianflone K. 1995. Signal transduction pathway of acylation stimulating protein: Involvement of protein kinase C. J Lipid Res 36:1415-1426.
3. Bastard JP, Maachi M, Lagathu C, Kim MJ, XXX CM, Vidal H, Capeau J, Feve B. 2006. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17:4-12.
4. Boonyaratanakornkit V, Edwards DP. 2007. Receptor mechanisms mediating non-genomic actions of sex steroids. Semin Reprod Med 25(3):139-153.
5. Chen X, Li X, Huang HY, Li X, Lin JF. 2006. [Effects of testosterone on insulin receptor substrate-1 and glucose transporter 4 expression in cells sensitive to insulin]. Zhonghua Yi Xue Za Zhi 86(21):1474-1477.
6. Chen YH, Lee MJ, Chang HH, Hung PF, Kao YH. 2006. 17 beta-estradiol stimulates resistin gene expression in 3T3-L1 adipocytes via the estrogen receptor, extracellularly regulated kinase, and CCAAT/enhancer binding protein-alpha pathways. Endocrinology 147(9):4496-4504.
7. Cianflone K, Xia Z, Chen LY. 2003. Critical review of Acylation Stimulating Protein physiology in humans and rodents. Biochim Biophys Acta 1609:127-143.
8. Collison M, Campbell IW, Salt IP, Dominiczak AF, Connell JM, Lyall H, Gould GW. 2000. Sex hormones induce insulin resistance in 3T3-L1 adipocytes by reducing cellular content of IRS proteins. Diabetologia 43(11):1374-1380.
9. Combs TP, Berg AH, Rajala MW, Klebanov S, Iyengar P, Jimenez-Chillaron JC, Patti ME, Klein SL, Weinstein RS, Scherer PE. 2003. Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 52(2):268-276.
10. Corbould A. 2007. Chronic testosterone treatment induces selective insulin resistance in subcutaneous adipocytes of women. J Endocrinol 192(3):585-594.
11. Dyck DJ, Heigenhauser GJ, Bruce CR. 2006. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol (Oxf) 186:5-16.
12. Faraj M, Cianflone K. 2004. Differential regulation of fatty acid trapping in mice adipose tissue and muscle by ASP. Am J Physiol 287:E150-E159.
13. Faraj M, Sniderman AD, Cianflone K. 2004. ASP enhances in situ lipoprotein lipase activity by increasing fatty acid trapping in adipocytes. J Lipid Res 45:657-666.
14. Germinario R, Sniderman AD, Manuel S, Pratt S, Baldo A, Cianflone K. 1993. Coordinate regulation of triacylglycerol synthesis and glucose transport by acylation stimulating protein. Metabolism 42:574-580.
15. Hodgkinson CP, Mander A, Sale GJ. 2005. Identification of 80K-H as a protein involved in GLUT4 vesicle trafficking. Biochem J 388:785-793.
16. Kalant D, Cain SA, Maslowska M, Sniderman AD, Cianflone K, Monk PN. 2003. The chemoattractant receptor-like protein C5L2 binds the C3a des-Arg77/acylation-stimulating protein. J Biol Chem 278:11123-11129.
17. Kalant D, Maclaren R, Cui W, Samanta R, Monk PN, Laporte SA, Cianflone K. 2005. C5L2 is a functional receptor for acylation stimulating protein. J Biol Chem 280:23936-23944.
18. Kotani K, Ogawa W, Matsumoto M, Kitamura T, Sakaue H, Hino Y, Miyake K, Sano W, Akimoto K, Ohno S, Kasuga M. 1998. Requirement of atypical protein kinase clambda for insulin stimulation of glucose uptake but not for Akt activation in 3T3-L1 adipocytes. Mol Cell Biol 18:6971-6982.
19. Lappas M, Yee K, Permezel M, Rice GE. 2005. 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 186(3):457-465.
20. Li SH, Huang HL, Chen YH. 2002. Ovarian steroid-regulated synthesis and secretion of complement C3 and factor B in mouse endometrium during the natural estrous cycle and pregnancy period. Biol Reprod 66(2):322-332.
21. Liu LZ, He AB, Liu XJ, Li Y, Chang YS, Fang FD. 2006. Protein kinase Czeta and glucose uptake. Biochemistry (Mosc) 71:701-706.
22. MacLaren R, Kalant D, Cianflone K. 2007. C5L2, the ASP receptor, is regulated by metabolic hormones associated with insulin resistance. Biochem Cell Biol 85:11-21.
23. Maslowska M, Legakis H, Assadi F, Cianflone K. 2006. Targeting the signaling pathway of acylation stimulating protein. J Lipid Res 47:643-652.
24. Maslowska M, Sniderman AD, Germinario R, Cianflone K. 1997. ASP stimulates glucose transport in cultured human adipocytes. Int J Obes Relat Metab Disord 21:261-266.
25. Maslowska M, Wang HW, Cianflone K. 2005. Novel roles for acylation stimulating protein/C3adesArg: a review of recent in vitro and in vivo evidence. Vitam Horm 70:309-332.
26. Mayes JS, Watson GH. 2004. Direct effects of sex steroid hormones on adipose tissues and obesity. Obes Rev 5(4):197-216.
27. Monjo M, Pujol E, Roca P. 2005. alpha2- to beta3-Adrenoceptor switch in 3T3-L1 preadipocytes and adipocytes: modulation by testosterone, 17beta-estradiol, and progesterone. Am J Physiol Endocrinol Metab 289(1):E-145-E-150.
28. Munzberg H, Myers MG Jr. 2005. Molecular and anatomical determinants of central leptin resistance. Nat Neurosci 8:566-570.
29. Muraki K, Okuya S, Tanizawa Y. 2006. Estrogen receptor alpha regulates insulin sensitivity through IRS-1 tyrosine phosphorylation in mature 3T3-L1 adipocytes. Endocr J 53(6):841-851.
30. Murray I, Parker RA, Kirchgessner TG, Tran J, Zhang ZJ, Westerlund J, Cianflone K. 1997. Functional bioactive recombinant acylation stimulating protein is distinct from C3a anaphylatoxin. J Lipid Res 38:2492-2501.
31. Ohno M, Hirata T, Enomoto M, Araki T, Ishimaru H, Takahashi TA. 2000. A putative chemoattractant receptor, C5L2, is expressed in granulocyte and immature dendritic cells, but not in mature dendritic cells. Mol Immunol 37:407-412.
32. Ojeda, S. 1992. Female reproductive function. In: Griffin James E, Rojeda S, editors: Textbook of endocrine physiology. New York: Oxford University Press.
33. Okinaga S, Slattery D, Humbles A, Zsengeller Z, Morteau O, Kinrade MB, Brodbeck RM, Krause JE, Choe HR, Gerard NP, Gerard C. 2003. C5L2, a nonsignaling C5A binding protein. Biochemistry 42:9406-9415.
34. Oktenli C, Ozgurtas T, Dede M, Sanisoglu YS, Yenen MC, Yesilova Z, Kenar L, Kurt YG, Baser I, Smith J, Cianflone K. 2007. Metformin decreases circulating acylation-stimulating protein levels in polycystic ovary syndrome. Gynecol Endocrinol 23(12):710-717.
35. Oriente F, Andreozzi F, Romano C, Perruolo G, Perfetti A, Fiory F, Miele C, Beguinot F, Formisano P. 2005. Protein kinase C-alpha regulates insulin action and degradation by interacting with insulin receptor substrate-1 and 14-3-3 epsilon. J Biol Chem 280:40642-40649.
36. Ozata M, Ortenli C, Culec M, Ozgurtas T, Bulucu F, Caglar R, Bingol N, Vural A, Ozdemir C. 2002. Increased fasting plasma acylation-stimulating protein concentrations in nephrotic syndrome. J Clin Endocrinol Metab 87:853-858.
37. Polderman KH, Gooren LJ, Asscheman H, Bakker A, Heine RJ. 1994. Induction of insulin resistance by androgens and estrogens. J Clin Endocrinol Metab 79(1):265-271.
38. Rodriguez-Cuenca S, Monjo M, Proenza AM, Roca P. 2005. Depot differences in steroid receptor expression in adipose tissue: possible role of the local steroid milieu. Am J Physiol Endocrinol Metab 288(1):E-200-E-207.
39. Saleh J, Cianflone K, Chaudhary T, Al-Riyami H, Al-Abri AR, Bayoumi R. 2007. Increased plasma acylation-stimulating protein correlates with hyperlipidemia at late gestation. Obesity (Silver Spring) 15(3):646-652.
40. Tan BK, Chen J, Digby JE, Keay SD, Kennedy CR, Randeva HS. 2006. Upregulation of adiponectin receptor 1 and 2 mRNA and protein in adipose tissue and adipocytes in insulin-resistant women with polycystic ovary syndrome. Diabetologia 49(11):2723-2728.
41. Tao Y, Cianflone K, Sniderman AD, Colby-Germinario SP, Germinario RJ. 1997. Acylation-stimulating protein (ASP) regulates glucose transport in the rat L6 muscle cell line. Biochim Biophys Acta 1344:221-229.
42. Vague J, La différenciation sexuelle, facteur déterminant des formes de l'obésité. Presse Medicale 30:339.
43. Wen Y, Wang H, MacLaren R, Wu J, Lu H, Cianflone K. 2007. Palmitate and oleate induction of acylation stimulating protein resistance in 3T3-L1 adipocytes and preadipocytes. J Cell Biochem [Epub ahead of print].
44. Wu Y, Zhang J, Wen Y, Wang H, Zhang M, Cianflone K. 2008. Increased acylation-stimulating protein, C-reactive protein, and lipid levels in young women with polycystic ovary syndrome. Fertil Steril [Epub ahead of print].
45. Xia Z, Stanhope KL, Digitale E, Simion O-M, Chen LY, Havel PJ, Cianflone K. 2004. ASP deficiency results in increased energy expenditure in mice. J Biol Chem 279:4051-4057.