Extracellular conversion of adiponectin hexamers into trimers

Bioscience Reports

Volumn 32, Issue 6, 2012, Pages 641-652

  Kim, Jeong A ^a,b   Nuñez, Martha ^c   Briggs, David B ^c   Laskowski, Bethany L ^c   Chhun, Jimmy J ^c   Eleid, Joseph K ^c   Quon, Michael J ^d,e   Tsao, Tsu Shuen ^c  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Arizona   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e UNIVERSITY OF MARYLAND   (United States)

Author keywords

Adipocyte; Adiponectin; Oligomerization; Oxidation reduction; Redox; Thiol

Indexed keywords

ADIPONECTIN; AURANOFIN; GLUTATHIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ADIPOCYTE; ADIPOSE TISSUE CELL; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; DISULFIDE BOND; IMMUNOBLOTTING; NONHUMAN; OLIGOMERIZATION; OXIDATION REDUCTION REACTION; PROTEIN CLEAVAGE; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECRETION; RAT;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; ANIMALS; CELLS, CULTURED; GLUTATHIONE; MALE; MICE; NADP; OXIDATION-REDUCTION; PROTEIN MULTIMERIZATION; RATS; RATS, SPRAGUE-DAWLEY; SULFHYDRYL COMPOUNDS;

RATTUS;

EID: 84872403991     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20120067     Document Type: Article

References (52)

1. Matsuzawa, Y., Funahashi, T., Kihara, S. and Shimomura, I. (2004) Adiponectin and metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 24, 29-33
2. Trujillo, M. E. and Scherer, P. E. (2005) Adiponectin - journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J. Int. Med. 257, 167-175
3. Yamauchi, T. and Kadowaki, T. (2008) Physiological and pathophysiological roles of adiponectin and adiponectin receptors in the integrated regulation of metabolic and cardiovascular diseases. Int. J. Obes. 32 (Suppl 7), S13-S18
4. Berg, A. H., Combs, T. P., Du, X., Brownlee, M. and Scherer, P. E. (2001) The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat. Med. 7, 947-953
5. Pajvani, U. B. and Scherer, P. E. (2003) Adiponectin: systemic contributor to insulin sensitivity. Curr. Diab. Rep. 3, 207-213
6. Tsao, T.-S., Lodish, H. F. and Fruebis, J. (2002) ACRP30, a new hormone controlling fat and glucose metabolism. Eur. J. Pharmacol. 440, 213-221
7. Chen, H., Montagnani, M., Funahashi, T., Shimomura, I. and Quon, M. J. (2003) Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J. Biol. Chem. 278, 45021-45026
8. Ouchi, N., Shibata, R. and Walsh, K. (2006) Cardioprotection by adiponectin. Trends Cardiovasc. Med. 16, 141-146
9. Huang, H., Park, P.-H., McMullen, M. R. and Nagy, L. E. (2008) Mechanisms for the anti-inflammatory effects of adiponectin in macrophages. J. Gastroenterol. Hepatol. 23 (Suppl 1), S50-S53
10. Okamoto, Y., Kihara, S., Ouchi, N., Nishida, M., Arita, Y., Kumada, M., Ohashi, K., Sakai, N., Shimomura, I., Kobayashi, H. et al. (2002) Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation 106, 2767-2770
11. Lara-Castro, C., Fu, Y., Chung, B. H. and Garvey, W. T. (2007) Adiponectin and the metabolic syndrome: mechanisms mediating risk for metabolic and cardiovascular disease. Curr. Opin. Lipidol. 18, 263-270
12. Briggs, D. B., Jones, C. M., Mashalidis, E. H., Nuñez, M., Hausrath, A. C., Wysocki, V. H. and Tsao, T.-S. (2009) Disulfide-dependent self-assembly of adiponectin octadecamers from trimers and presence of stable octadecameric adiponectin lacking disulfide bonds in vitro. Biochemistry 48, 12345-12357
13. Waki, H., Yamauchi, T., Kamon, J., Ito, Y., Uchida, S., Kita, S., Hara, K., Hada, Y., Vasseur, F., Froguel, P. et al. (2003) Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J. Biol. Chem. 278, 40352-40363
14. Peake, P. W., Hughes, J. T., Shen, Y. and Charlesworth, J. A. (2007) Glycosylation of human adiponectin affects its conformation and stability. J. Mol. Endocrinol. 39, 45-52
15. Schraw, T., Wang, Z. V., Halberg, N., Hawkins, M. and Scherer, P. E. (2008) Plasma adiponectin complexes have distinct biochemical characteristics. Endocrinology 149, 2270-2282
16. Pajvani, U. B., Du, X., Combs, T. P., Berg, A. H., Rajala, M. W., Schulthess, T., Engel, J., Brownlee, M. and Scherer, P. E. (2003) Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity. J. Biol. Chem. 278, 9073-9085
17. Richards, A. A., Stephens, T., Charlton, H. K., Jones, A., Macdonald, G. A., Prins, J. B. and Whitehead, J. P. (2006) Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: evidence for regulation of multimerization by alterations in posttranslational modifications. Mol. Endocrinol. 20, 1673-1687
18. Suzuki, S., Wilson-Kubalek, E. M., Wert, D., Tsao, T.-S. and Lee, D. H. (2007) The oligomeric structure of high molecular weight adiponectin. FEBS Lett. 581, 809-814
19. Pajvani, U. B., Hawkins, M., Combs, T. P., Rajala, M. W., Doebber, T., Berger, J. P., Wagner, J. A., Wu, M., Knopps, A., Xiang, A. H. et al. (2004) Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J. Biol. Chem. 279, 12152-12162
20. Lara-Castro, C., Luo, N., Wallace, P., Klein, R. L. and Garvey, W. T. (2006) Adiponectin multimeric complexes and the metabolic syndrome trait cluster. Diabetes 55, 249-259
21. Basu, R., Pajvani, U. B., Rizza, R. A. and Scherer, P. E. (2007) Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 56, 2174-2177
22. O'Leary, V. B., Jorett, A. E., Marchetti, C. M., Gonzalez, F., Phillips, S. A., Ciaraldi, T. P. and Kirwan, J. P. (2007) Enhanced adiponectin multimer ratio and skeletal muscle adiponectin receptor expression following exercise training and diet in older insulin-resistant adults. Am. J. Physiol. Endocrinol. Metab. 293, E421-E427
23. Fisher, F. F. M., Trujillo, M. E., Hanif, W., Barnett, A. H., McTernan, P. G., Scherer, P. E. and Kumar, S. (2005) Serum high molecular weight complex of adiponectin correlates better with glucose tolerance than total serum adiponectin in Indo-Asian males. Diabetologia 48, 1084-1087
24. Tsao, T.-S., Tomas, E., Murrey, H. E., Hug, C., Lee, D. H., Ruderman, N. B., Heuser, J. E. and Lodish, H. F. (2003) Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J. Biol. Chem. 278, 50810-50817
25. Shibata, R., Ouchi, N., Ito, M., Kihara, S., Shiojima, I., Pimentel, D. R., Kumada, M., Sato, K., Schiekofer, S., Ohashi, S. et al. (2004) Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 10, 1384-1389
26. Wang, Y., Lam, K. S. L., Chan, L., Chan, K. W., Lam, J. B. B., Lam, M. C., Hoo, R. C. L., Mak, W. W. N., Cooper, G. J. S. and Xu, A. (2006) Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J. Biol. Chem. 281, 16391-16400
27. Combs, T. P., Pajvani, U. B., Berg, A. H., Lin, Y., Jelicks, L. A., Laplante, M., Nawrocki, A. R., Rajala, M. W., Parlow, A. F., Cheeseboro, L. et al. (2004) A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology 145, 367-383
28. Peake, P. W., Kriketos, A. D., Campbell, L. V., Shen, Y. and Charlesworth, J. A. (2005) The metabolism of isoforms of human adiponectin: studies in human subjects and in experimental animals. Eur. J. Endocrinol. 153, 409-417
29. Jones, D. P. (2006) Redefining oxidative stress. Antioxid. Redox. Signaling 8, 1865-1879
30. Samiec, P. S., Drews-Botsch, C., Flagg, E. W., Kurtz, J. C., Sternberg, P., Reed, R. L. and Jones, D. P. (1998) Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radical Biol. Med. 24, 699-704
31. Neal, J. W. and Clipstone, N. A. (2003) A constitutively active NFATc1 mutant induces a transformed phenotype in 3T3-L1 fibroblasts. J. Biol. Chem. 278, 17246-17254
32. Honnor, R. C., Dhillon, G. S. and Londos, C. (1985) cAMP-dependent protein kinase and lipolysis in rat adipocytes. I. Cell preparation, manipulation, and predictability in behavior. J. Biol. Chem. 260, 15122-15129
33. Kim, J.-A., Yeh, D. C., Ver, M., Li, Y., Carranza, A., Conrads, T. P., Veenstra, T. D., Harrington, M. A. and Quon, M. J. (2005) Phosphorylation of Ser24 in the pleckstrin homology domain of insulin receptor substrate-1 by mouse Pelle-like kinase/interleukin-1 receptor-associated kinase: cross-talk between inflammatory signaling and insulin signaling that may contribute to insulin resistance. J. Biol. Chem. 280, 23173-23183
34. Hug, C., Wang, J., Ahmad, N. S., Bogan, J. S., Tsao, T.-S. and Lodish, H. F. (2004) T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. U.S.A. 101, 10308-10313
35. Briggs, D. B., Giron, R. M., Malinowski, P. R., Nunez, M. and Tsao, T.-S. (2011) Role of redox environment on the oligomerization of higher molecular weight adiponectin. BMC Biochem. 12, 24
36. Briggs, D. B., Giron, R. M., Schnittker, K., Hart, M. V., Park, C. K., Hausrath, A. C. and Tsao, T.-S. (2012) Zinc enhances adiponectin oligomerization to octadecamers but decreases the rate of disulfide bond formation. Biometals 25, 469-486
37. Fruebis, J., Tsao, T. S., Javorschi, S., Ebbets-Reed, D., Erickson, M. R., Yen, F. T., Bihain, B. E. and Lodish, H. F. (2001) 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. 98, 2005-2010
38. Phillips, S. A., Kung, J., Ciaraldi, T. P., Choe, C., Christiansen, L., Mudaliar, S. and Henry, R. R. (2009) Selective regulation of cellular and secreted multimeric adiponectin by antidiabetic therapies in humans. Am. J. Physiol. Endocrinol. Metab. 297, E767-E773
39. Qian, S.-B., McDonough, H., Boellmann, F., Cyr, D. M. and Patterson, C. (2006) CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440, 551-555
40. Igarashi, Y., Heureux, E., Doctor, K. S., Talwar, P., Gramatikova, S., Gramatikoff, K., Zhang, Y., Blinov, M., Ibragimova, S. S., Boyd, S. et al. (2009) PMAP: databases for analyzing proteolytic events and pathways. Nucleic Acids Res. 37, D611-D618
41. Jones, D. P., Carlson, J. L., Mody, V. C., Cai, J., Lynn, M. J. and Sternberg, P. (2000) Redox state of glutathione in human plasma. Free Radical Biol. Med. 28, 625-635
42. Söderberg, A., Sahaf, B. and Rosén, A. (2000) Thioredoxin reductase, a redox-active selenoprotein, is secreted by normal and neoplastic cells: presence in human plasma. Cancer Res. 60, 2281-2289
43. Ottaviano, F. G., Handy, D. E. and Loscalzo, J. (2008) Redox regulation in the extracellular environment. Circ. J. 72, 1-16
44. Gromer, S., Arscott, L. D., Williams, C. H., Schirmer, R. H. and Becker, K. (1998) Human placenta thioredoxin reductase. Isolation of the selenoenzyme, steady state kinetics, and inhibition by therapeutic gold compounds. J. Biol. Chem. 273, 20096-20101
45. Wu, X., Motoshima, H., Mahadev, K., Stalker, T. J., Scalia, R. and Goldstein, B. J. (2003) Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 52, 1355-1363
46. Fu, Y., Luo, N., Klein, R. L. and Garvey, W. T. (2005) Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J. Lipid Res. 46, 1369-1379
47. Waki, H., Yamauchi, T., Kamon, J., Kita, S., Ito, Y., Hada, Y., Uchida, S., Tsuchida, A., Takekawa, S. and Kadowaki, T. (2005) Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1. Endocrinology 146, 790-796
48. Halberg, N., Schraw, T. D., Wang, Z. V., Kim, J.-Y., Yi, J., Hamilton, M. P., Luby-Phelps, K. and Scherer, P. E. (2009) Systemic fate of the adipocyte-derived factor adiponectin. Diabetes 58, 1961-1970
49. Georgiou, C. D., Grintzalis, K., Zervoudakis, G. and Papapostolou, I. (2008) Mechanism of Coomassie Brilliant Blue G-250 binding to proteins: a hydrophobic assay for nanogram quantities of proteins. Anal. Bioanal. Chem. 391, 391-403
50. Jones, D. P., Carlson, J. L., Samiec, P. S., Sternberg, P., Mody, V. C., Reed, R. L. and Brown, L. A. (1998) Glutathione measurement in human plasma. evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC. Clin. Chim. Acta. 275, 175-184
51. Jeevanandam, M., Begay, C. K., Shahbazian, L. M. and Petersen, S. R. (2000) Altered plasma cytokines and total glutathione levels in parenterally fed critically ill trauma patients with adjuvant recombinant human growth hormone (rhGH) therapy. Crit. Care. Med. 28, 324-329
52. Imhoff, B. R. and Hansen, J. M. (2010) Extracellular redox environments regulate adipocyte differentiation. Differentiation 80, 31-39