C1q/TNF-related proteins, a family of novel adipokines, induce vascular relaxation through the adiponectin receptor-1/AMPK/eNOS/nitric oxide signaling pathway

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 11, 2011, Pages 2616-2623

  Zheng, Qijun ^a,b   Yuan, Yuexing ^b   Yi, Wei ^a,b   Lau, Wayne Bond ^b   Wang, Yajing ^b   Wang, Xiaoliang ^b   Sun, Yang ^a,b   Lopez, Bernard L ^b   Christopher, Theodore A ^b   Peterson, Jonathan M ^c   Wong, G William ^c   Yu, Shiqiang ^a   Yi, Dinghua ^a   Ma, Xin Liang ^b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

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

Author keywords

diabetes mellitus; endothelial function; nitric oxide; signal transduction

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN RECEPTOR 1; COMPLEMENT COMPONENT C1Q; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR RING; VASODILATATION;

ADIPONECTIN; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AORTA; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; GLYCOPROTEINS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ADIPONECTIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASODILATION;

EID: 80054916958     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.231050     Document Type: Article

References (42)

1. Diamant M, Tushuizen ME. The metabolic syndrome and endothelial dysfunction: common highway to type 2 diabetes and CVD. Curr Diab Rep. 2006;6:279-286. (Pubitemid 44322700)
2. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation. 2006;113:1888-1904. (Pubitemid 43739401)
3. Quinones MJ, Nicholas SB, Lyon CJ. Insulin resistance and the endothelium. Curr Diab Rep. 2005;5:246-253. (Pubitemid 41269588)
4. Shimabukuro M, Higa N, Asahi T, Oshiro Y, Takasu N, Tagawa T, Ueda S, Shimomura I, Funahashi T, Matsuzawa Y. Hypoadiponectinemia is closely linked to endothelial dysfunction in man. J Clin Endocrinol Metab. 2003;88:3236-3240. (Pubitemid 36877499)
5. Ouchi N, Ohishi M, Kihara S, Funahashi T, Nakamura T, Nagaretani H, Kumada M, Ohashi K, Okamoto Y, Nishizawa H, Kishida K, Maeda N, Nagasawa A, Kobayashi H, Hiraoka H, Komai N, Kaibe M, Rakugi H, Ogihara T, Matsuzawa Y. Association of hypoadiponectinemia with impaired vasoreactivity. Hypertension. 2003;42:231-234. (Pubitemid 37093465)
6. Tan KC, Xu A, Chow WS, Lam MC, Ai VH, Tam SC, Lam KS. Hypoadiponectinemia is associated with impaired endotheliumdependent vasodilation. J Clin Endocrinol Metab. 2004;89:765-769. (Pubitemid 38269891)
7. Ma K, Cabrero A, Saha PK, Kojima H, Li L, Chang BH, Paul A, Chan L. Increased beta-oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J Biol Chem. 2002;277: 34658-34661.
8. Kubota N, Terauchi Y, Yamauchi T, Kubota T, Moroi M, Matsui J, Eto K, Yamashita T, Kamon J, Satoh H, Yano W, Froguel P, Nagai R, Kimura S, Kadowaki T, Noda T. Disruption of adiponectin causes insulin resistance and neointimal formation. J Biol Chem. 2002;277: 25863-25866. (Pubitemid 34967064)
9. Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, Furuyama N, Kondo H, Takahashi M, Arita Y, Komuro R, Ouchi N, Kihara S, Tochino Y, Okutomi K, Horie M, Takeda S, Aoyama T, Funahashi T, Matsuzawa Y. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med. 2002;8:731-737. (Pubitemid 34778727)
10. Ahima RS, Qi Y, Singhal NS, Jackson MB, Scherer PE. Brain adipocytokine action and metabolic regulation. Diabetes. 2006;55(Suppl 2):S145-S154. (Pubitemid 44927045)
11. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem. 1995;270:26746-26749.
12. Kopp A, Bala M, Weigert J, Buchler C, Neumeier M, Aslanidis C, Scholmerich J, Schaffler A. Effects of the new adiponectin paralogous protein CTRP-3 and of LPS on cytokine release from monocytes of patients with type 2 diabetes mellitus. Cytokine. 2010;49:51-57.
13. Peterson JM, Wei Z, Wong GW. C1q/TNF-related protein-3 (CTRP3), a novel adipokine that regulates hepatic glucose output. J Biol Chem. 2010;285:39691-39701.
14. Davis KE, Scherer PE. Adiponectin: no longer the lone soul in the fight against insulin resistance? Biochem J. 2008;416:e7-e9.
15. 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; 416:161-177.
16. Yamanoue T, Brum JM, Estafanous FG. Vasodilation and mechanism of action of propofol in porcine coronary artery. Anesthesiology. 1994;81: 443-451. (Pubitemid 24320636)
17. Colombo SL, Moncada S. AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochem J. 2009;421:163-169.
18. Chen H, Montagnani M, Funahashi T, Shimomura I, Quon MJ. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem. 2003;278:45021-45026. (Pubitemid 37377262)
19. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature. 2003;423:762-769. (Pubitemid 36735700)
20. Takeuchi T, Adachi Y, Ohtsuki Y, Furihata M. Adiponectin receptors, with special focus on the role of the third receptor, T-cadherin, in vascular disease. Med Mol Morphol. 2007;40:115-120. (Pubitemid 47415941)
21. Park SY, Choi JH, Ryu HS, Pak YK, Park KS, Lee HK, Lee W. 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;284:27780-27789.
22. Lasser G, Guchhait P, Ellsworth JL, Sheppard P, Lewis K, Bishop P, Cruz MA, Lopez JA, Fruebis J. C1qTNF-related protein-1 (CTRP-1): a vascular wall protein that inhibits collagen-induced platelet aggregation by blocking VWF binding to collagen. Blood. 2006;107:423-430. (Pubitemid 43076360)
23. Wong GW, Wang J, Hug C, Tsao TS, Lodish HF. A family of Acrp30/adiponectin structural and functional paralogs. Proc Natl Acad Sci USA. 2004;101:10302-10307. (Pubitemid 38924920)
24. Akiyama H, Furukawa S, Wakisaka S, Maeda T. Cartducin stimulates mesenchymal chondroprogenitor cell proliferation through both extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/Akt pathways. FEBS J. 2006;273:2257-2263.
25. Mandal MN, Vasireddy V, Reddy GB, Wang X, Moroi SE, Pattnaik BR, Hughes BA, Heckenlively JR, Hitchcock PF, Jablonski MM, Ayyagari R. CTRP5 is a membrane-associated and secretory protein in the RPE and ciliary body and the S163R mutation of CTRP5 impairs its secretion. Invest Ophthalmol Vis Sci. 2006;47:5505-5513. (Pubitemid 46723803)
26. Chang AC, Zsak L, Feng Y, Mosseri R, Lu Q, Kowalski P, Zsak A, Burrage TG, Neilan JG, Kutish GF, Lu Z, Laegreid W, Rock DL, Cohen SN. Phenotype-based identification of host genes required for replication of African swine fever virus. J Virol. 2006;80:8705-8717. (Pubitemid 44384880)
27. Wong GW, Krawczyk SA, Kitidis-Mitrokostas C, Ge G, Spooner E, Hug C, Gimeno R, Lodish HF. 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;23:241-258.
28. Scheiner-Bobis G, Eva A, Kirch U. Signalling pathways involving sodium pump stimulate endothelin-1 secretion and nitric oxide production in endothelial cells. Cell Mol Biol (Noisy-le-grand). 2006;52:58-63. (Pubitemid 46799706)
29. Yu J, Eto M, Akishita M, Kaneko A, Ouchi Y, Okabe T. Signaling pathway of nitric oxide production induced by ginsenoside Rb1 in human aortic endothelial cells: a possible involvement of androgen receptor. Biochem Biophys Res Commun. 2007;353:764-769. (Pubitemid 46048736)
30. Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL, Touyz RM. Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension. 2007;49:185-192. (Pubitemid 46360359)
31. Fisslthaler B, Fleming I. Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ Res. 2009;105:114-127.
32. Nagata D, Hirata Y. The role of AMP-activated protein kinase in the cardiovascular system. Hypertens Res.33:22-28.
33. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 1999;399: 597-601.
34. Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, Walsh K. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem. 2004;279:1304-1309. (Pubitemid 38082655)
35. Kadowaki T, Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev. 2005;26:439-451. (Pubitemid 40686653)
36. Heiker JT, Kosel D, Beck-Sickinger AG. Molecular mechanisms of signal transduction via adiponectin and adiponectin receptors. Biol Chem. 2010; 391:1005-1018.
37. Buechler C, Wanninger J, Neumeier M. Adiponectin receptor binding proteins-recent advances in elucidating adiponectin signalling pathways. FEBS Lett. 2010;584:4280-4286.
38. Motoshima H, Wu X, Mahadev K, Goldstein BJ. Adiponectin suppresses proliferation and superoxide generation and enhances eNOS activity in endothelial cells treated with oxidized LDL. Biochem Biophys Res Commun. 2004;315:264-271. (Pubitemid 38183103)
39. Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, Ito Y, Kamon J, Tsuchida A, Kumagai K, Kozono H, Hada Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Awazawa M, Takamoto I, Froguel P, Hara K, Tobe K, Nagai R, Ueki K, Kadowaki T. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med. 2007;13:332-339. (Pubitemid 46376688)
40. Kaplan JM, Hake PW, Denenberg A, Nowell M, Piraino G, Zingarelli B. Phosphorylation of extracellular signal-regulated kinase (ERK)-1/2 Is associated with the downregulation of peroxisome proliferator-activated receptor (PPAR)-gamma during polymicrobial sepsis. Mol Med. 2010; 16:491-497.
41. Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, Fang Q, Christ-Roberts CY, Hong JY, Kim RY, Liu F, Dong LQ. APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol. 2006;8:516-523.
42. Cheng KK, Lam KS, Wang Y, Huang Y, Carling D, Wu D, Wong C, Xu A. Adiponectin-induced endothelial nitric oxide synthase activation and nitric oxide production are mediated by APPL1 in endothelial cells. Diabetes. 2007;56:1387-1394. (Pubitemid 46715600)