Essential roles of insulin, AMPK signaling and lysyl and prolyl hydroxylases in the biosynthesis and multimerization of adiponectin

Molecular and Cellular Endocrinology

Volumn 399, Issue , 2015, Pages 164-177

  Zhang, Lin ^a   Li, Ming Ming ^a   Corcoran, Marie ^a   Zhang, Shaoping ^a   Cooper, Garth J S ^a,b,c,d  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Adiponectin; Adipose tissue; Biosynthesis; Hormones; Molecular mechanisms; Post translational modification

Indexed keywords

ADENYLATE KINASE; ADIPONECTIN; ADIPONECTIN RECEPTOR; BIPYRIDINE; INSULIN; MINOXIDIL; POLYMER; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTOCATECHUIC ACID; ROSIGLITAZONE; ADIPOQ PROTEIN, MOUSE; ANTIDIABETIC AGENT; ANTIHYPERTENSIVE AGENT; ETHYL PROTOCATECHUATE; HYDROXYBENZOIC ACID DERIVATIVE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOPROTEIN; LYSYL HYDROXYLASE 3, MOUSE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; HYPERINSULINEMIA; IMPAIRED GLUCOSE TOLERANCE; INSULIN METABOLISM; INSULIN RESPONSE; MOUSE; MOUSE MODEL; NONHUMAN; OBESITY; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; UPREGULATION; WEIGHT GAIN; WHITE ADIPOSE TISSUE; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE MUTANT; PROTEIN MULTIMERIZATION;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIHYPERTENSIVE AGENTS; HYDROXYBENZOATES; HYPOGLYCEMIC AGENTS; INSULIN; MICE; MICE, OBESE; MINOXIDIL; PROCOLLAGEN-LYSINE, 2-OXOGLUTARATE 5-DIOXYGENASE; PROLYL HYDROXYLASES; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

EID: 84908566837     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.09.014     Document Type: Article

References (87)

1. Abi Khalil C., et al. Intensifying glycaemic control with insulin reduces adiponectin and its HMW isoform moderately in type 2, but not in type 1, diabetes. Diabetes Metab 2011, 37:259-261.
2. Andersen C.L., et al. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004, 64:5245-5250.
3. Antoniades C., et al. Adiponectin: from obesity to cardiovascular disease. Obes. Rev 2009, 10:269-279.
4. Arita Y., et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun 1999, 257:79-83.
5. Astapova O., LeffT. Adiponectin and PPARγ: cooperative and interdependent actions of two key regulators of metabolism. Vitam. Horm 2012, 90:143-162.
6. Bank R.A., et al. Defective collagen crosslinking in bone, but not in ligament or cartilage, in Bruck syndrome: indications for a bone-specific telopeptide lysyl hydroxylase on chromosome 17. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1054-1058.
7. Basu R., et al. Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 2007, 56:2174-2177.
8. Bauche I.B., et al. Adiponectin downregulates its own production and the expression of its AdipoR2 receptor in transgenic mice. Biochem. Biophys. Res. Commun 2006, 345:1414-1424.
9. Bluher M., et al. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev. Cell 2002, 3:25-38.
10. Bobbert T., et al. Changes of adiponectin oligomer composition by moderate weight reduction. Diabetes 2005, 54:2712-2719.
11. Chvapil M., et al. Mechanism of the action of chelating agents on proline hydroxylation and its incorporation into collagenous and non-collagenous proteins. Eur. J. Biochem 1967, 2:229-235.
12. Combs T.P., et al. Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 2003, 52:268-276.
13. Committee for the Update of the Guide for the Care and Use of Laboratory Animals Guide for the Care and Use of Laboratory Animals 2011, Institute for Laboratory Animal Research, Division on Earth and Life Studies, National Research Council of the National Academies, The National Academies Press, Washington, DC.
14. Cortini M., Sitia R. From antibodies to adiponectin: role of ERp44 in sizing and timing protein secretion. Diabetes Obes. Metab 2010, 12(Suppl. 2):39-47.
15. Eyre D., et al. The kyphoscoliotic type of Ehlers-Danlos syndrome (type VI): differential effects on the hydroxylation of lysine in collagens I and II revealed by analysis of cross-linked telopeptides from urine. Mol. Genet. Metab 2002, 76:211-216.
16. Fasshauer M., et al. Hormonal regulation of adiponectin gene expression in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun 2002, 290:1084-1089.
17. Gelse K., et al. Collagens - structure, function, and biosynthesis. Adv. Drug Deliv. Rev 2003, 55:1531-1546.
18. Gorres K.L., Raines R.T. Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol 2010, 45:106-124.
19. Ha-Vinh R., et al. Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am. J. Med. Genet. A 2004, 131:115-120.
20. Hajri T., et al. Regulation of adiponectin production by insulin: interactions with tumor necrosis factor-α and interleukin-6. Am. J. Physiol. Endocrinol. Metab 2011, 300:E350-E360.
21. Halberg N., et al. Systemic fate of the adipocyte-derived factor adiponectin. Diabetes 2009, 58:1961-1970.
22. Haluzik M., et al. Adiponectin and its role in the obesity-induced insulin resistance and related complications. Physiol. Res 2004, 53:123-129.
23. Hanauske-Abel H.M., Rohm K.H. The collagenous part of C1q is unaffected in the hydroxylysine-deficient collagen disease. FEBS Lett 1980, 110:73-76.
24. Heikkinen J., et al. Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J. Biol. Chem 2000, 275:36158-36163.
25. Hotta K., et al. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler. Thromb. Vasc. Biol 2000, 20:1595-1599.
26. Hu E., et al. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem 1996, 271:10697-10703.
27. 2+ and AMPK/SIRT1. Nature 2010, 464:1313-1319.
28. Iwaki M., et al. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 2003, 52:1655-1663.
29. Kadowaki T., et al. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest 2006, 116:1784-1792.
30. Kilkenny C., et al. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8(6):e1000412.
31. Kivirikko K.I., Myllyharju J. Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol 1998, 16:357-368.
32. Kivirikko K.I., Myllyla R. Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes. Methods Enzymol 1982, 82(Pt A):245-304.
33. Li W., et al. Insulin-sensitizing effects of thiazolidinediones are not linked to adiponectin receptor expression in human fat or muscle. Am. J. Physiol. Endocrinol. Metab 2007, 292:E1301-E1307.
34. Liu M., Liu F. Transcriptional and post-translational regulation of adiponectin. Biochem. J. 2010, 425:41-52.
35. Liu M., et al. A disulfide-bond A oxidoreductase-like protein (DsbA-L) regulates adiponectin multimerization. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18302-18307.
36. Liu M., et al. Fat-specific DsbA-L overexpression promotes adiponectin multimerization and protects mice from diet-induced obesity and insulin resistance. Diabetes 2012, 61:2776-2786.
37. Maeda N., et al. PPARγ ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 2001, 50:2094-2099.
38. Majamaa K., et al. Inhibition of prolyl hydroxylation during collagen biosynthesis in human skin fibroblast cultures by ethyl 3,4-dihydroxybenzoate. J. Invest. Dermatol 1987, 89:405-409.
39. Mercer D.K., et al. Identification, expression, and tissue distribution of the three rat lysyl hydroxylase isoforms. Biochem. Biophys. Res. Commun 2003, 307:803-809.
40. Murad S., Pinnell S.R. Suppression of fibroblast proliferation and lysyl hydroxylase activity by minoxidil. J. Biol. Chem 1987, 262:11973-11978.
41. Myllyharju J., Kivirikko K.I. Collagens and collagen-related diseases. Ann. Med 2001, 33:7-21.
42. Notbohm H., et al. Recombinant human type II collagens with low and high levels of hydroxylysine and its glycosylated forms show marked differences in fibrillogenesis in vitro. J. Biol. Chem 1999, 274:8988-8992.
43. Pajvani U.B., et al. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity. J. Biol. Chem 2003, 278:9073-9085.
44. Pajvani U.B., et al. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J. Biol. Chem 2004, 279:12152-12162.
45. Pasquali M., et al. Abnormal formation of collagen cross-links in skin fibroblasts cultured from patients with Ehlers-Danlos syndrome type VI. Proc. Assoc. Am. Physicians 1997, 109:33-41.
46. Passoja K., et al. Cloning and characterization of a third human lysyl hydroxylase isoform. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:10482-10486.
47. Phillips S.A., et al. Modulation of circulating and adipose tissue adiponectin levels by antidiabetic therapy. Diabetes 2003, 52:667-674.
48. Phillips S.A., et al. Selective regulation of cellular and secreted multimeric adiponectin by antidiabetic therapies in humans. Am. J. Physiol. Endocrinol. Metab 2009, 297:E767-E773.
49. Pornprasertsuk S., et al. Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J. Bone Miner. Res 2004, 19:1349-1355.
50. Purushotham A., et al. Maintenance of adiponectin attenuates insulin resistance induced by dietary conjugated linoleic acid in mice. J. Lipid Res 2007, 48:444-452.
51. Qiang L., et al. Adiponectin secretion is regulated by SIRT1 and the endoplasmic reticulum oxidoreductase Ero1-Lα. Mol. Cell. Biol 2007, 27:4698-4707.
52. Rasouli N., et al. Increased plasma adiponectin in response to pioglitazone does not result from increased gene expression. Am. J. Physiol. Endocrinol. Metab 2006, 290:E42-E46.
53. Rautavuoma K., et al. Premature aggregation of type IV collagen and early lethality in lysyl hydroxylase 3 null mice. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14120-14125.
54. Ruotsalainen H., et al. The activities of lysyl hydroxylase 3 (LH3) regulate the amount and oligomerization status of adiponectin. PLoS ONE 2012, 7:e50045.
55. Sasaki T., et al. Reduction of collagen production in keloid fibroblast cultures by ethyl-3,4-dihydroxybenzoate. Inhibition of prolyl hydroxylase activity as a mechanism of action. J. Biol. Chem 1987, 262:9397-9403.
56. Schegg B., et al. Core glycosylation of collagen is initiated by two β(1-O)galactosyltransferases. Mol. Cell. Biol 2009, 29:943-952.
57. Scherer P.E., et al. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem 1995, 270:26746-26749.
58. Semple R.K., et al. Elevated plasma adiponectin in humans with genetically defective insulin receptors. J. Clin. Endocrinol. Metab 2006, 91:3219-3223.
59. Semple R.K., et al. Paradoxical elevation of high-molecular weight adiponectin in acquired extreme insulin resistance due to insulin receptor antibodies. Diabetes 2007, 56:1712-1717.
60. Silha J.V., et al. Plasma resistin, adiponectin and leptin levels in lean and obese subjects: correlations with insulin resistance. Eur. J. Endocrinol 2003, 149:331-335.
61. Switzer B.R., Summer G.K. Inhibition of collagen synthesis by alpha, alpha1-dipyridyl in human skin fibroblasts in culture. In Vitro 1973, 9:160-166.
62. Tiikkainen M., et al. Effects of rosiglitazone and metformin on liver fat content, hepatic insulin resistance, insulin clearance, and gene expression in adipose tissue in patients with type 2 diabetes. Diabetes 2004, 53:2169-2176.
63. Trujillo M.E., Scherer P.E. Adiponectin - journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J. Intern. Med 2005, 257:167-175.
64. Tsao T.S., et al. Oligomerization state-dependent activation of NF-κ B signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J. Biol. Chem 2002, 277:29359-29362.
65. Ueno N., et al. Leptin modulates orexigenic effects of ghrelin and attenuates adiponectin and insulin levels and selectively the dark-phase feeding as revealed by central leptin gene therapy. Endocrinology 2004, 145:4176-4184.
66. van der Slot A.J., et al. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J. Biol. Chem 2003, 278:40967-40972.
67. Van Berendoncks A.M., et al. Adiponectin: key role and potential target to reverse energy wasting in chronic heart failure. Heart Fail. Rev 2012, 18:557-566.
68. Vandesompele J., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3. RESEARCH0034.
69. Viengchareun S., et al. Brown adipocytes are novel sites of expression and regulation of adiponectin and resistin. FEBS Lett 2002, 532:345-350.
70. Waki H., et al. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J. Biol. Chem 2003, 278:40352-40363.
71. Wang Y., et al. Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J. Biol. Chem 2002, 277:19521-19529.
72. Wang Y., et al. Proteomic and functional characterization of endogenous adiponectin purified from fetal bovine serum. Proteomics 2004, 4:3933-3942.
73. Wang Y., et al. 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 2006, 281:16391-16400.
74. Wang Y., et al. Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem. J. 2008, 409:623-633.
75. Wendel A.A., et al. Conjugated linoleic acid fails to worsen insulin resistance but induces hepatic steatosis in the presence of leptin in ob/ob mice. J. Lipid Res 2008, 49:98-106.
76. Wolf G. New insights into thiol-mediated regulation of adiponectin secretion. Nutr. Rev 2008, 66:642-645.
77. Wu X., et al. Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 2003, 52:1355-1363.
78. Yamauchi T., et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med 2002, 8:1288-1295.
79. Yamauchi T., et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003, 423:762-769.
80. Yamauchi T., et al. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med 2007, 13:332-339.
81. Yeowell H.N., Walker L.C. Mutations in the lysyl hydroxylase 1 gene that result in enzyme deficiency and the clinical phenotype of Ehlers-Danlos syndrome type VI. Mol. Genet. Metab 2000, 71:212-224.
82. Yokota T., et al. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 2000, 96:1723-1732.
83. Yokota T., et al. Adiponectin, a fat cell product, influences the earliest lymphocyte precursors in bone marrow cultures by activation of the cyclooxygenase-prostaglandin pathway in stromal cells. J. Immunol 2003, 171:5091-5099.
84. Zhang L., et al. Altered calcium homeostasis does not explain the contractile deficit of diabetic cardiomyopathy. Diabetes 2008, 57:2158-2166.
85. Zhang L., et al. Protection of the heart by treatment with a divalent-copper-selective chelator reveals a novel mechanism underlying cardiomyopathy in diabetic rats. Cardiovasc. Diabetol 2013, 12:123.
86. Zhou G., et al. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest 2001, 108:1167-1174.
87. Zuurmond A.M., et al. Minoxidil exerts different inhibitory effects on gene expression of lysyl hydroxylase 1, 2, and 3: implications for collagen cross-linking and treatment of fibrosis. Matrix Biol 2005, 24:261-270.