Metabolic function of the CTRP family of hormones

Reviews in Endocrine and Metabolic Disorders

Volumn 15, Issue 2, 2014, Pages 111-123

  Seldin, Marcus M ^a   Tan, Stefanie Y ^a   Wong, G William ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipokine; Fat oxidation; Gluconeognesis; Insulin resistance; Obesity; Type 2 diabetes

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; C1Q TNF RELATED PROTEIN; COMPLEMENT COMPONENT C1Q; CTRP1 PROTEIN; CTRP11 PROTEIN; CTRP12 PROTEIN; CTRP13 PROTEIN; CTRP15 PROTEIN; CTRP2 PROTEIN; CTRP3 PROTEIN; CTRP5 PROTEIN; CTRP6 PROTEIN; CTRP7 PROTEIN; CTRP9 PROTEIN; FIBROBLAST GROWTH FACTOR 21; GLUCAGON; INSULIN; LEPTIN; OLIGOMER; PEPTIDE; PROTEIN; T CADHERIN; UNCLASSIFIED DRUG; ADIPOCYTOKINE; GLUCOSE; TUMOR NECROSIS FACTOR;

BIOLOGICAL ACTIVITY; ENERGY BALANCE; ENERGY METABOLISM; HUMAN; LIPID METABOLISM; METABOLIC REGULATION; METABOLISM; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; ANALOGS AND DERIVATIVES; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADIPOKINES; ADIPONECTIN; ENERGY METABOLISM; GLUCOSE; HUMANS; LIPID METABOLISM; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTORS;

EID: 84901459654     PISSN: 13899155     EISSN: 15732606     Source Type: Journal    
DOI: 10.1007/s11154-013-9255-7     Document Type: Review

References (158)

1. Schwartz MW, Woods SC, Porte Jr D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000;404:661-71. (Pubitemid 30205071)
2. Spiegelman BM, Flier JS. Obesity and the regulation of energy balance. Cell. 2001;104:531-43. (Pubitemid 32201948)
3. Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 2006;444:847-53. (Pubitemid 46024991)
4. Trujillo ME, Scherer PE. Adipose tissue-derived factors: impact on health and disease. Endocr Rev. 2006;27:762-78. (Pubitemid 44936059)
5. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature. 1998;395:763-70. (Pubitemid 28485436)
6. Potthoff MJ, Kliewer SA, Mangelsdorf DJ. Endocrine fibroblast growth factors 15/19 and 21: from feast to famine. Genes Dev. 2012;26:312-24.
7. Deng Y, Scherer PE. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann N YAcad Sci. 2010;1212:E1-19.
8. Scherer PE. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes. 2006;55:1537-45. (Pubitemid 44324105)
9. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol. 2005;115:911-9.
10. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest. 2006;116:1784-92. (Pubitemid 44033298)
11. Turer AT, Scherer PE. Adiponectin: mechanistic insights and clinical implications. Diabetologia. 2012;55:2319-26.
12. Okamoto Y, Kihara S, Ouchi N, Nishida M, Arita Y, Kumada M, et al. Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2002;106:2767-70. (Pubitemid 35396973)
13. Ma K, Cabrero A, Saha PK, Kojima H, Li L, Chang BH, et al. Increased beta-oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J Biol Chem. 2002;277:34658-61.
14. Kubota N, Terauchi Y, Yamauchi T, Kubota T, Moroi M, Matsui J, et al. Disruption of adiponectin causes insulin resistance and neointimal formation. J Biol Chem. 2002;277:25863-6. (Pubitemid 34967064)
15. Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med. 2002;8:731-7. (Pubitemid 34778727)
16. Nawrocki AR, Rajala MW, Tomas E, Pajvani UB, Saha AK, Trumbauer ME, et al. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J Biol Chem. 2006;281:2654-60. (Pubitemid 43845727)
17. Nawrocki AR, Hofmann SM, Teupser D, Basford JE, Durand JL, Jelicks LA, et al. Lack of association between adiponectin levels and atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2010;30:1159-65.
18. Yano W, Kubota N, Itoh S, Kubota T, Awazawa M, Moroi M, et al. Molecular mechanism of moderate insulin resistance in adiponectin-knockout mice. Endocr J. 2008;55:515-22. (Pubitemid 351949746)
19. Iwabu M, Yamauchi T, Okada-Iwabu M, Sato K, Nakagawa T, Funata M, et al. Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature. 2010;464:1313-9.
20. Holland WL, Miller RA, Wang ZV, Sun K, Barth BM, Bui HH, et al. Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat Med. 2011;17:55-63.
21. Tullin S, Sams A, Brandt J, Dahl K, Gong W, Jeppesen CB, et al. Recombinant adiponectin does not lower plasma glucose in animal models of type 2 diabetes. PLoS One. 2012;7:e44270.
22. Qi Y, Takahashi N, Hileman SM, Patel HR, Berg AH, Pajvani UB, et al. Adiponectin acts in the brain to decrease body weight. Nat Med. 2004;10:524-9. (Pubitemid 38667912)
23. Kubota N, Yano W, Kubota T, Yamauchi T, Itoh S, Kumagai H, et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. CellMetab. 2007;6:55-68. (Pubitemid 47007437)
24. Ehling A, Schaffler A, Herfarth H, Tarner IH, Anders S, Distler O, et al. The potential of adiponectin in driving arthritis. J Immunol. 2006;176:4468-78. (Pubitemid 44264427)
25. Fayad R, Pini M, Sennello JA, Cabay RJ, Chan L, Xu A, et al. Adiponectin deficiency protects mice from chemically induced colonic inflammation. Gastroenterology. 2006;132:601-14. (Pubitemid 46274660)
26. Pini M, Sennello JA, Chan L, Fantuzzi G. Adiponectin deficiency does not affect the inflammatory response to endotoxin or concanavalin a in mice. Endocrinology. 2006;147:5019-22. (Pubitemid 44790552)
27. Brakenhielm E, Veitonmaki N, Cao R, Kihara S, Matsuzawa Y, Zhivotovsky B, et al. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proc Natl Acad Sci U S A. 2004;101:2476-81. (Pubitemid 38269336)
28. Landskroner-Eiger S, Qian B, Muise ES, Nawrocki AR, Berger JP, Fine EJ, et al. Proangiogenic contribution of adiponectin toward mammary tumor growth in vivo . Clin Cancer Res. 2009;15:3265-76.
29. Wong GW, Krawczyk SA, Kitidis-Mitrokostas C, Revett T, Gimeno R, Lodish HF. Molecular, biochemical and functional characterizations of C1q/TNF family members: adipose-tissue-selective expression patterns, regulation by PPAR-gamma agonist, cysteine-mediated oligomerizations, combinatorial associations and metabolic functions. Biochem J. 2008;416:161-77.
30. Davis KE, Scherer PE. Adiponectin: no longer the lone soul in the fight against insulin resistance? Biochem J. 2008;416:e7-9.
31. Kishore U, Gaboriaud C, Waters P, Shrive AK, Greenhough TJ, Reid KB, et al. C1q and tumor necrosis factor superfamily: modularity and versatility. Trends Immunol. 2004;25:551-61. (Pubitemid 39208354)
32. Tom Tang Y, Hu T, Arterburn M, Boyle B, Bright JM, Palencia S, et al. The complete complement of C1q-domain-containing proteins in Homo sapiens. Genomics. 2005;86:100-11. (Pubitemid 40805340)
33. Kishore U, Reid KB. C1q: structure, function, and receptors. Immunopharmacology. 2000;49:159-70. (Pubitemid 30445227)
34. Colombatti A, Spessotto P, Doliana R, Mongiat M, Bressan GM, Esposito G. The EMILIN/Multimerin family. Front Immunol. 2011;2:93.
35. Colombatti A, Doliana R, Bot S, Canton A, Mongiat M, Mungiguerra G, et al. The EMILIN protein family. Matrix Biol. 2000;19:289-301. (Pubitemid 30665652)
36. Wong GW, Wang J, Hug C, Tsao TS, Lodish HF. A family of Acrp30/adiponectin structural and functional paralogs. Proc Natl Acad Sci U S A. 2004;101:10302-7. (Pubitemid 38924920)
37. Yuzaki M. Cbln and C1q family proteins: new transneuronal cytokines. Cell Mol Life Sci. 2008;65:1698-705.
38. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. Anovel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem. 1995;270:26746-9.
39. Deans MR, Peterson JM, Wong GW. Mammalian Otolin: a multimeric glycoprotein specific to the inner ear that interacts with otoconial matrix protein Otoconin-90 and Cerebellin-1. PLoS One. 2010;5:e12765.
40. Berube NG, Swanson XH, Bertram MJ, Kittle JD, Didenko V, Baskin DS, et al. Cloning and characterization of CRF, a novel C1q-related factor, expressed in areas of the brain involved in motor function. Brain Res Mol Brain Res. 1999;63:233-40. (Pubitemid 29036973)
41. Aerbajinai W, Lee YT, Wojda U, Barr VA, Miller JL. Cloning and characterization of a gene expressed during terminal differentiation that encodes a novel inhibitor of growth. J Biol Chem. 2004;279:1916-21. (Pubitemid 38084462)
42. Yamaguchi N, Benya PD, van der Rest M, Ninomiya Y. The cloning and sequencing of alpha 1(VIII) collagen cDNAs demonstrate that type VIII collagen is a short chain collagen and contains triple-helical and carboxyl-terminal non-triple-helical domains similar to those of type X collagen. J Biol Chem. 1989;264:16022-9. (Pubitemid 19238361)
43. Muragaki Y, Jacenko O, Apte S, Mattei MG, Ninomiya Y, Olsen BR. The alpha 2(VIII) collagen gene. A novel member of the short chain collagen family located on the human chromosome 1. J Biol Chem. 1991;266:7721-7. (Pubitemid 21906424)
44. Thomas JT, Cresswell CJ, Rash B, Nicolai H, Jones T, Solomon E, et al. The human collagen X gene. Complete primary translated sequence and chromosomal localization. Biochem J. 1991;280(Pt 3):617-23.
45. Schaffler A, Buechler C. CTRP family: linking immunity to metabolism. Trends Endocrinol Metab. 2012;23:194-204.
46. Yuzaki M. Synapse formation and maintenance by C1q family proteins: a new class of secreted synapse organizers. Eur J Neurosci. 2010;32:191-7.
47. Wong GW, Krawczyk SA, Kitidis-Mitrokostas C, Ge G, Spooner E, Hug C, et al. Identification and characterization of CTRP9, a novel secreted glycoprotein, from adipose tissue that reduces serum glucose in mice and forms heterotrimers with adiponectin. FASEB J. 2009;23:241-58.
48. Peterson JM, Aja S, Wei Z, Wong GW. C1q/TNF-related protein-1 (CTRP1) enhances fatty acid oxidation via AMPK activation and ACC inhibition. J Biol Chem. 2012;287:1576-87.
49. Peterson JM, Wei Z, Wong GW. C1q/TNF-related protein-3 (CTRP3), a novel adipokine that regulates hepatic glucose output. J Biol Chem. 2010;285:39691-701.
50. Wei Z, Peterson JM, Lei X, Cebotaru L, Wolfgang MJ, Baldeviano GC, et al. C1q/TNF-related protein-12 (CTRP12), a novel adipokine that improves insulin sensitivity and glycemic control in mouse models of obesity and diabetes. J Biol Chem. 2012;287:10301-15.
51. Wei Z, Peterson JM, Wong GW. Metabolic regulation by C1q/TNF-related protein-13 (CTRP13): activation OFAMP-activated protein kinase and suppression of fatty acid-induced JNK signaling. J Biol Chem. 2011;286:15652-65.
52. Wei Z, Seldin MM, Natarajan N, Djemal DC, Peterson JM, Wong GW. C1q/tumor necrosis factor-related protein 11 (CTRP11), a novel adipose stroma-derived regulator of adipogenesis. J Biol Chem. 2013;288:10214-29.
53. Seldin MM, Peterson JM, Byerly MS, Wei Z, Wong GW. Myonectin (CTRP15), a novel myokine that links skeletal muscle to systemic lipid homeostasis. J Biol Chem. 2012;287:11968-80.
54. Enomoto T, Ohashi K, Shibata R, Higuchi A, Maruyama S, Izumiya Y, et al. Adipolin/C1qdc2/CTRP12 functions as an adipokine that improves glucose metabolism. J Biol Chem. 2011;286:34552-8.
55. Peterson JM, Wei Z, Wong GW. CTRP8 and CTRP9B are novel proteins that hetero-oligomerize with C1q/TNF family members. Biochem Biophys Res Commun. 2009;388:360-5.
56. Shapiro L, Scherer PE. The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr Biol. 1998;8:335-8. (Pubitemid 28159119)
57. Bogin O, Kvansakul M, Rom E, Singer J, Yayon A, Hohenester E. Insight into Schmid metaphyseal chondrodysplasia from the crystal structure of the collagen X NC1 domain trimer. Structure. 2002;10:165-73. (Pubitemid 34164595)
58. Gaboriaud C, Juanhuix J, Gruez A, Lacroix M, Darnault C, Pignol D, et al. The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J Biol Chem. 2003;278:46974-82. (Pubitemid 37452280)
59. Kvansakul M, Bogin O, Hohenester E, Yayon A. Crystal structure of the collagen alpha1(VIII) NC1 trimer.Matrix Biol. 2003;22:145-52. (Pubitemid 36627472)
60. Rety S, Salamitou S, Garcia-Verdugo I, Hulmes DJ, Le Hegarat F, Chaby R, et al. The crystal structure of the Bacillus anthracis spore surface protein BclA shows remarkable similarity to mammalian proteins. J Biol Chem. 2005;280:43073-8. (Pubitemid 43049273)
61. Tu X, Palczewski K. Crystal structure of the globular domain of C1QTNF5: implications for late-onset retinal macular degeneration. J Struct Biol. 2012;180:439-46.
62. Tsao TS, Tomas E, Murrey HE, Hug C, Lee DH, Ruderman NB, et al. Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J Biol Chem. 2003;278:50810-7. (Pubitemid 37548930)
63. Pajvani UB, Du X, Combs TP, Berg AH, Rajala MW, Schulthess T, et al. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity. J Biol Chem. 2003;278:9073-85. (Pubitemid 36800387)
64. Suzuki S, Wilson-Kubalek EM, Wert D, Tsao TS, Lee DH. The oligomeric structure of high molecular weight adiponectin. FEBS Lett. 2007;581:809-14. (Pubitemid 46282708)
65. Briggs DB, Jones CM, Mashalidis EH, Nunez M, Hausrath AC, Wysocki VH, et al. Disulfide-dependent self-assembly of adiponectin octadecamers from trimers and presence of stable octadecameric adiponectin lacking disulfide bonds in vitro . Biochemistry. 2009;48:12345-57.
66. Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S, Kita S, et al. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J Biol Chem. 2003;278:40352-63. (Pubitemid 37248604)
67. Radjainia M, Wang Y, Mitra AK. Structural polymorphism of oligomeric adiponectin visualized by electron microscopy. J Mol Biol. 2008;381:419-30.
68. Wang ZV, Schraw TD, Kim JY, Khan T, Rajala MW, Follenzi A, et al. Secretion of the adipocyte-specific secretory protein adiponectin critically depends on thiol-mediated protein retention. Mol Cell Biol. 2007;27:3716-31. (Pubitemid 46726179)
69. Liu M, Zhou L, Xu A, Lam KS, Wetzel MD, Xiang R, et al. A disulfide-bond A oxidoreductase-like protein (DsbA-L) regulates adiponectin multimerization. Proc Natl Acad Sci U S A. 2008;105:18302-7.
70. Tsao TS, Murrey HE, Hug C, Lee DH, Lodish HF. Oligomerization state-dependent activation of NF-kappa B signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J Biol Chem. 2002;277:29359-62. (Pubitemid 41079218)
71. Kobayashi H, Ouchi N, Kihara S, Walsh K, Kumada M, Abe Y, et al. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ Res. 2004;94:e27-31.
72. Pajvani UB, Hawkins M, Combs TP, Rajala MW, Doebber T, Berger JP, et al. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J Biol Chem. 2004;279:12152-62. (Pubitemid 38445780)
73. Aso Y, Yamamoto R, Wakabayashi S, Uchida T, Takayanagi K, Takebayashi K, et al. Comparison of serum high-molecular weight (HMW) adiponectin with total adiponectin concentrations in type 2 diabetic patients with coronary artery disease using a novel enzyme-linked immunosorbent assay to detect HMWadiponectin. Diabetes. 2006;55:1954-60. (Pubitemid 44509967)
74. Basu R, Pajvani UB, Rizza RA, Scherer PE. Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes. 2007;56:2174-7. (Pubitemid 47195840)
75. Wei Z, Lei X, Seldin MM, Wong GW. Endopeptidase cleavage generates a functionally distinct isoform of C1q/tumor necrosis factor-related protein-12 (CTRP12) with an altered oligomeric state and signaling specificity. J Biol Chem. 2012;287:35804-14.
76. Wang Y, Xu A, Knight C, Xu LY, Cooper GJ. 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;277:19521-9. (Pubitemid 34967464)
77. Wang Y, Lam KS, Chan L, Chan KW, Lam JB, Lam MC, 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;281:16391-400.
78. Richards AA, Stephens T, Charlton HK, Jones A, Macdonald GA, Prins JB, et al. Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: evidence for regulation of multimerization by alterations in posttranslational modifications. Mol Endocrinol. 2006;20:1673-87. (Pubitemid 43967574)
79. Sato C, Yasukawa Z, Honda N, Matsuda T, Kitajima K. Identification and adipocyte differentiation-dependent expression of the unique disialic acid residue in an adipose tissue-specific glycoprotein, adipo Q. J Biol Chem. 2001;276:28849-56.
80. Peake PW, Hughes JT, Shen Y, Charlesworth JA. Glycosylation of human adiponectin affects its conformation and stability. J Mol Endocrinol. 2007;39:45-52. (Pubitemid 47337865)
81. Choi KM, Hwang SY, Hong HC, Yang SJ, Choi HY, Yoo HJ, et al. C1q/TNF-related protein-3 (CTRP-3) and pigment epithelium-derived factor (PEDF) concentrations in patients with type 2 diabetes and metabolic syndrome. Diabetes. 2012;61:2932-6.
82. Yoo HJ, Hwang SY, Hong HC, Choi HY, Yang SJ, Choi DS, et al. Implication of progranulin and C1q/TNF-related protein-3 (CTRP3) on inflammation and atherosclerosis in subjects with or without metabolic syndrome. PLoS One. 2013;8:e55744.
83. Chalupova L, Zakovska A, Adamcova K. Development of a novel enzyme-linked immunosorbent assay (ELISA) for measurement of serum CTRP1: a pilot study: measurement of serum CTRP1 in healthy donors and patients with metabolic syndrome. Clin Biochem. 2013;46:73-8.
84. Schmid A, Kopp A, Aslanidis C, Wabitsch M, Muller M, Schaffler A. Regulation and function of C1Q/TNF-related protein-5 (CTRP-5) in the context of adipocyte biology. Exp Clin Endocrinol Diabetes. 2013;121:310-7.
85. Gale EA, Gillespie KM. Diabetes and gender. Diabetologia. 2001;44:3-15. (Pubitemid 32141879)
86. O'Rahilly S, Barroso I, Wareham NJ. Genetic factors in type 2 diabetes: the end of the beginning? Science. 2005;307:370-3. (Pubitemid 40139970)
87. West DB, Boozer CN, Moody DL, Atkinson RL. Dietary obesity in nine inbred mouse strains. Am J Physiol. 1992;262:R1025-32.
88. Haluzik M, Colombo C, Gavrilova O, Chua S, Wolf N, Chen M, et al. Genetic background (C57BL/6J versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice. Endocrinology. 2004;145:3258-64. (Pubitemid 38829998)
89. Nishizawa H, Shimomura I, Kishida K, Maeda N, Kuriyama H, Nagaretani H, et al. Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes. 2002;51:2734-41. (Pubitemid 34970926)
90. Xu A, Chan KW, Hoo RL, Wang Y, Tan KC, Zhang J, et al. Testosterone selectively reduces the high molecular weight form of adiponectin by inhibiting its secretion from adipocytes. J Biol Chem. 2005;280:18073-80. (Pubitemid 41389052)
91. Page ST, Herbst KL, Amory JK, Coviello AD, Anawalt BD, Matsumoto AM, et al. Testosterone administration suppresses adiponectin levels in men. J Androl. 2005;26:85-92. (Pubitemid 39665280)
92. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999;257:79-83. (Pubitemid 29299050)
93. Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, et al. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol. 2000;20:1595-9. (Pubitemid 30353893)
94. Hu E, Liang P, Spiegelman BM. Adipo Q is a novel adipose-specific gene dysregulated in obesity. J Biol Chem. 1996;271:10697-703. (Pubitemid 26145805)
95. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, et al. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001;86:1930-5. (Pubitemid 32472900)
96. Yang WS, Lee WJ, Funahashi T, Tanaka S, Matsuzawa Y, Chao CL, et al. Plasma adiponectin levels in overweight and obese Asians. Obes Res. 2002;10:1104-10. (Pubitemid 135686651)
97. Asayama K, Hayashibe H, Dobashi K, Uchida N, Nakane T, Kodera K, et al. Decrease in serum adiponectin level due to obesity and visceral fat accumulation in children. Obes Res. 2003;11:1072-9. (Pubitemid 41151584)
98. Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005;1:15-25. (Pubitemid 43960587)
99. Maeda T, Abe M, Kurisu K, Jikko A, Furukawa S. Molecular cloning and characterization of a novel gene, CORS26, encoding a putative secretory protein and its possible involvement in skeletal development. J Biol Chem. 2001;276:3628-34.
100. Schaffler A, Ehling A, Neumann E, Herfarth H, Paul G, Tarner I, et al. Genomic organization, promoter, amino acid sequence, chromosomal localization, and expression of the human gene for CORS-26 (collagenous repeat-containing sequence of 26-kDa protein). Biochim Biophys Acta. 2003;1630:123-9. (Pubitemid 37494883)
101. Schmid A, Kopp A, Hanses F, Bala M, Muller M, Schaffler A. The novel adipokine C1q/TNF-related protein-3 is expressed in human adipocytes and regulated by metabolic and infection-related parameters. Exp Clin Endocrinol Diabetes. 2012;120:611-7.
102. Schaffler A, Weigert J, Neumeier M, Scholmerich J, Buechler C. Regulation and function of collagenous repeat containing sequence of 26-kDa protein gene product "cartonectin ". Obesity (Silver Spring). 2007;15:303-13. (Pubitemid 46407310)
103. Schaffler A, Ehling A, Neumann E, Herfarth H, Tarner I, Gay S, et al. Genomic organization, chromosomal localization and adipocytic expression of the murine gene for CORS-26 (collagenous repeat-containing sequence of 26 kDa protein). Biochim Biophys Acta. 2003;1628:64-70. (Pubitemid 36794563)
104. Yokohama-Tamaki T, Maeda T, Tanaka TS, Shibata S. Functional analysis of CTRP3/cartducin in Meckel's cartilage and developing condylar cartilage in the fetal mouse mandible. J Anat. 2011;218:517-33.
105. Maeda T, Jikko A, Abe M, Yokohama-Tamaki T, Akiyama H, Furukawa S, et al. Cartducin, a paralog of Acrp30/adiponectin, is induced during chondrogenic differentiation and promotes proliferation of chondrogenic precursors and chondrocytes. J Cell Physiol. 2006;206:537-44. (Pubitemid 43062825)
106. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med. 2001;7:947-53. (Pubitemid 32756433)
107. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med. 2002;8:1288-95. (Pubitemid 35373562)
108. Miller RA, Chu Q, Le Lay J, Scherer PE, Ahima RS, Kaestner KH, et al. Adiponectin suppresses gluconeogenic gene expression in mouse hepatocytes independent of LKB1-AMPK signaling. J Clin Invest. 2011;121:2518-28.
109. Peterson JM, Seldin MM, Wei Z, Aja S, Wong GW. CTRP3 attenuates diet-induced hepatic steatosis by regulating triglyceride metabolism. Am J Physiol Gastrointest Liver Physiol. 2013;305:G214-224.
110. Xu A, Wang Y, Keshaw H, Xu LY, Lam KS, Cooper GJ. The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J Clin Invest. 2003;112:91-100. (Pubitemid 38056380)
111. Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444:860-7. (Pubitemid 46024993)
112. Weigert J, Neumeier M, Schaffler A, Fleck M, Scholmerich J, Schutz C, et al. The adiponectin paralog CORS-26 has anti-inflammatory properties and is produced by human monocytic cells. FEBS Lett. 2005;579:5565-70. (Pubitemid 41455631)
113. Kopp A, Bala M, Buechler C, Falk W, Gross P, Neumeier M, et al. C1q/TNF-related protein-3 represents a novel and endogenous lipopolysaccharide antagonist of the adipose tissue. Endocrinology. 2010;151:5267-78.
114. Hofmann C, Chen N, Obermeier F, Paul G, Buchler C, Kopp A, et al. C1q/TNF-related protein-3 (CTRP-3) is secreted by visceral adipose tissue and exerts antiinflammatory and antifibrotic effects in primary human colonic fibroblasts. Inflamm Bowel Dis. 2011;17:2462-71.
115. Akiyama H, Furukawa S, Wakisaka S, Maeda T. CTRP3/cartducin promotes proliferation and migration of endothelial cells. Mol Cell Biochem. 2007;304:243-8. (Pubitemid 47456872)
116. Yi W, Sun Y, Yuan Y, Lau WB, Zheng Q, Wang X, et al. C1q/tumor necrosis factor-related protein-3, a newly identified adipokine, is a novel antiapoptotic, proangiogenic, and cardioprotective molecule in the ischemic mouse heart. Circulation. 2012;125:3159-69.
117. Park SY, Choi JH, Ryu HS, Pak YK, Park KS, Lee HK, et al. C1q tumor necrosis factor alpha-related protein isoform 5 is increased in mitochondrial DNA-depleted myocytes and activates AMP-activated protein kinase. J Biol Chem. 2009;284:27780-9.
118. Hayward C, Shu X, Cideciyan AV, Lennon A, Barran P, Zareparsi S, et al. Mutation in a short-chain collagen gene, CTRP5, results in extracellular deposit formation in late-onset retinal degeneration: a genetic model for age-related macular degeneration. Hum Mol Genet. 2003;12:2657-67. (Pubitemid 37304688)
119. Ayyagari R, Mandal MN, Karoukis AJ, Chen L, McLaren NC, Lichter M, et al. Late-onset macular degeneration and long anterior lens zonules result from a CTRP5 gene mutation. Investig Ophthalmol Vis Sci. 2005;46:3363-71. (Pubitemid 44264327)
120. Shu X, Tulloch B, Lennon A, Vlachantoni D, Zhou X, Hayward C, et al. Diseasemechanisms in late-onset retinal macular degeneration associated with mutation in C1QTNF5. Hum Mol Genet. 2006;15:1680-9. (Pubitemid 43904834)
121. Mandal MN, Vasireddy V, Reddy GB, Wang X, Moroi SE, Pattnaik BR, et al. CTRP5 is a membrane-associated and secretory protein in the RPE and ciliary body and the S163R mutation of CTRP5 impairs its secretion. Investig Ophthalmol Vis Sci. 2006;47:5505-13. (Pubitemid 46723803)
122. Chavali VR, Khan NW, Cukras CA, Bartsch DU, Jablonski MM, Ayyagari R. A CTRP5 gene S163R mutation knock-in mouse model for late-onset retinal degeneration. Hum Mol Genet. 2011;20:2000-14.
123. Shu X, Luhmann UF, Aleman TS, Barker SE, Lennon A, Tulloch B, et al. Characterisation of a C1qtnf5 Ser163Arg knock-in mouse model of late-onset retinal macular degeneration. PLoS One. 2011;6:e27433.
124. Peterson JM, Wei Z, Seldin MM, Byerly MS, Aja S, Wong GW. CTRP9 transgenic mice are protected from diet-induced obesity and metabolic dysfunction. Am J Physiol Regul Integr Comp Physiol. 2013. doi:10.1152/ajpregu. 00110.2013.
125. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, 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;98:2005-10. (Pubitemid 32165613)
126. Tomas E, Tsao TS, Saha AK, Murrey HE, Zhang Cc C, Itani SI, et al. Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proc Natl Acad Sci U S A. 2002;99:16309-13. (Pubitemid 35462791)
127. Satoh H, Nguyen MT, Trujillo M, Imamura T, Usui I, Scherer PE, et al. Adenovirus-mediated adiponectin expression augments skeletal muscle insulin sensitivity in male Wistar rats. Diabetes. 2005;54:1304-13. (Pubitemid 40586658)
128. Combs TP, Berg AH, Obici S, Scherer PE, Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest. 2001;108:1875-81. (Pubitemid 34015133)
129. Karpe F. Insulin resistance by adiponectin deficiency: is the action in skeletal muscle? Diabetes. 2013;62:701-2.
130. Zheng Q, Yuan Y, Yi W, Lau WB, Wang Y, Wang X, et al. C1q/TNF-related proteins, a family of novel adipokines, induce vascular relaxation through the adiponectin receptor-1/AMPK/eNOS/nitric oxide signaling pathway. Arterioscler Thromb Vasc Biol. 2011;31:2616-23.
131. Kambara T, Ohashi K, Shibata R, Ogura Y, Maruyama S, Enomoto T, et al. CTRP9 protein protects against myocardial injury following ischemia-reperfusion through AMP-activated protein kinase (AMPK)-dependent mechanism. J Biol Chem. 2012;287:18965-73.
132. Su H, Yuan Y, Wang XM, Lau WB, Wang Y, Wang X, et al. Inhibition of CTRP9, a novel and cardiac-abundantly expressed cell survival molecule, by TNFalpha-initiated oxidative signaling contributes to exacerbated cardiac injury in diabetic mice. Basic Res Cardiol. 2013;108:315-26.
133. Uemura Y, Shibata R, Ohashi K, Enomoto T, Kambara T, Yamamoto T, et al. Adipose-derived factor CTRP9 attenuates vascular smooth muscle cell proliferation and neointimal formation. FASEB J. 2013;27:25-33.
134. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, et al. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation. 2006;113:898-918.
135. DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14:173-94.
136. Lamarche B, Lemieux S, Dagenais GR, Despres JP. Visceral obesity and the risk of ischaemic heart disease: insights from the Quebec Cardiovascular Study. Growth Horm IGF Res. 1998;8(Suppl B):1-8.
137. Tontonoz P, Hu E, Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell. 1994;79:1147-56.
138. Wu Z, Bucher NL, Farmer SR. Induction of peroxisome proliferator- activated receptor gamma during the conversion of 3T3 fibroblasts into adipocytes is mediated by C/EBPbeta, C/EBPdelta, and glucocorticoids. Mol Cell Biol. 1996;16:4128-36. (Pubitemid 26251212)
139. Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE, et al. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell. 1999;3:151-8. (Pubitemid 29292616)
140. Tang QQ, Otto TC, Lane MD. Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc Natl Acad Sci U S A. 2003;100:44-9. (Pubitemid 36078027)
141. Enomoto T, Shibata R, Ohashi K, Kambara T, Kataoka Y, Uemura Y, et al. Regulation of adipolin/CTRP12 cleavage by obesity. Biochem Biophys Res Commun. 2012;428:155-9.
142. Byerly MS, Swanson R, Wei Z, Seldin MM, McCulloh PS, Wong GW. A central role for C1q/TNF-related protein 13 (CTRP13) in modulating food intake and body weight. PLoS One. 2013;8:e62862.
143. Lim S, Choi SH, Koo BK, Kang SM, Yoon JW, Jang HC, et al. Effects of aerobic exercise training on C1q tumor necrosis factor alpha-related protein isoform 5 (Myonectin): association with insulin resistance and mitochondrial DNA density in women. J Clin Endocrinol Metab. 2012;97:E88-93.
144. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, et al. Cloning of adiponectin receptors thatmediate antidiabetic metabolic effects. Nature. 2003;423:762-9. (Pubitemid 36735700)
145. Hug C, Wang J, Ahmad NS, Bogan JS, Tsao TS, Lodish HF. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc Natl Acad Sci U S A. 2004;101:10308-13. (Pubitemid 38924921)
146. Awazawa M, Ueki K, Inabe K, Yamauchi T, Kubota N, Kaneko K, et al. Adiponectin enhances insulin sensitivity by increasing hepatic IRS-2 expression via a macrophage-derived IL-6-dependent pathway. Cell Metab. 2011;13:401-12.
147. Takemura Y, Ouchi N, Shibata R, Aprahamian T, Kirber MT, Summer RS, et al. Adiponectin modulates inflammatory reactions via calreticulin receptor-dependent clearance of early apoptotic bodies. J Clin Invest. 2007;117:375-86. (Pubitemid 46203966)
148. Ranscht B, Dours-Zimmermann MT. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron. 1991;7:391-402.
149. Denzel MS, Scimia MC, Zumstein PM, Walsh K, Ruiz-Lozano P, Ranscht B. T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J Clin Invest. 2010;120:4342-52.
150. Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, et al. APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol. 2006;8:516-23.
151. Zhou L, Deepa SS, Etzler JC, Ryu J, Mao X, Fang Q, et al. Adiponectin activates AMP-activated protein kinase in muscle cells via APPL1/LKB1-dependent and phospholipase C/Ca2+/Ca2+/cal-modulin-dependent protein kinase kinase-dependent pathways. J Biol Chem. 2009;284:22426-35.
152. Xin X, Zhou L, Reyes CM, Liu F, Dong LQ. APPL1 mediates adiponectin-stimulated p38 MAPK activation by scaffolding the TAK1-MKK3-p38 MAPK pathway. Am J Physiol Endocrinol Metab. 2011;300:E103-10.
153. Deepa SS, Zhou L, Ryu J, Wang C, Mao X, Li C, et al. APPL1 mediates adiponectin-induced LKB1 cytosolic localization through the PP2A-PKCzeta signaling pathway. Mol Endocrinol. 2011;25:1773-85.
154. Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, et al. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med. 2007;13:332-9. (Pubitemid 46376688)
155. Bjursell M, Ahnmark A, Bohlooly YM, William-Olsson L, Rhedin M, Peng XR, et al. Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes. 2007;56:583-93. (Pubitemid 46348449)
156. Liu Y, Michael MD, Kash S, Bensch WR, Monia BP, Murray SF, et al. Deficiency of adiponectin receptor 2 reduces diet-induced insulin resistance but promotes type 2 diabetes. Endocrinology. 2007;148:683-92. (Pubitemid 46143170)
157. Yamauchi T, Kadowaki T. Adiponectin receptor as a key player in healthy longevity and obesity-related diseases. Cell Metab. 2013;17:185-96.
158. Tang YT, Hu T, Arterburn M, Boyle B, Bright JM, Emtage PC, et al. PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol. 2005;61:372-80. (Pubitemid 41355862)