CTRP3 promotes energy production by inducing mitochondrial ROS and up-expression of PGC-1α in vascular smooth muscle cells

Experimental Cell Research

Volumn 341, Issue 2, 2016, Pages 177-186

  Feng, Han ^a,b,c   Wang, Jin Yu ^a,b,c   Zheng, Ming ^a,b,c   Zhang, Cheng Lin ^a,b,c   An, Yuan Ming ^a,b,c   Li, Li ^a,b,c   Wu, Li Ling ^a,b,c  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c Beijing Key Laboratory of Cardiovascular Receptors Research Key Laboratory of Cardiovascular Molecular Biology and Regulatory Peptides   (China)

Author keywords

CTRP3; Energy metabolism; Mitochondrial reactive oxygen species; Oxidative phosphorylation; Peroxisome proliferator activated receptor co activator 1 ; Vascular smooth muscle cell

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ADIPOCYTOKINE; C1Q TUMOR NECROSIS FACTOR RELATED PROTEIN 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHENYLHYDRAZONE DERIVATIVE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SIRTUIN 3; SMALL INTERFERING RNA; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; C1Q TUMOR NECROSIS FACTOR-RELATED PROTEIN 3, RAT; HEAT SHOCK PROTEIN; PPARGC1A PROTEIN, RAT; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENERGY YIELD; GENE EXPRESSION REGULATION; GENE SILENCING; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNTHESIS; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CELL CULTURE; CELL LINE; DRUG EFFECTS; METABOLISM; MITOCHONDRION; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ACETYLCYSTEINE; ADIPOKINES; ANIMALS; CELL LINE; CELLS, CULTURED; HEAT-SHOCK PROTEINS; MITOCHONDRIA; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RATS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84958925458     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2016.02.001     Document Type: Article

References (60)

1. Wong G.W., Krawczyk S.A., Kitidis-Mitrokostas C., Revett T., Gimeno R., Lodish H.F. Molecular, biochemical and functional characterizations of C1q/TNF family members: adipose-tissue-selective expression patterns, regulation by PPARγ agonist, cysteine-mediated oligomerizations, combinatorial associations and metabolic functions. Biochem. J. 2008, 416:161-177.
2. 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 2007, 15:303-313.
3. Maeda T., Wakisaka S. CTRP3/cartducin is induced by transforming growth factor-beta1 and promotes vascular smooth muscle cell proliferation. Cell Biol. Int. 2010, 34:261-266.
4. Wu D., Lei H., Wang J.Y., Zhang C.L., Feng H., Fu F.Y., Li L., Wu L.L. CTRP3 attenuates post-infarct cardiac fibrosis by targeting Smad3 activation and inhibiting myofibroblast differentiation. J. Mol. Med. 2015, 93:1311-1325.
5. Li X., Jiang L., Yang M., Wu Y.W., Sun S.X., Sun J.Z. CTRP3 modulates the expression and secretion of adipokines in 3T3-L1 adipocytes. Endocr. J. 2014, 61:1153-1162.
6. Peterson J.M., Wei Z., Wong G.W. C1q/TNF-related protein-3 (CTRP3), a novel adipokine that regulates hepatic glucose output. J. Biol. Chem. 2010, 285:39691-39701.
7. Peterson J.M., Seldin M.M., Wei Z., Aja S., Wong G.W. CTRP3 attenuates diet-induced hepatic steatosis by regulating triglyceride metabolism. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 305:G214-G224.
8. Akiyama H., Furukawa S., Wakisaka S., Maeda T. CTRP3/cartducin promotes proliferation and migration of endothelial cells. Mol. Cell Biochem. 2007, 304:243-248.
9. Akiyama H., Furukawa S., Wakisaka S., Maeda T. Elevated expression of CTRP3/cartducin contributes to promotion of osteosarcoma cell proliferation. Oncol. Rep. 2009, 21:1477-1481.
10. Schmid A., Kopp A., Hanses F., Karrasch T., Schaffler A. C1q/TNF-related protein-3 (CTRP-3) attenuates lipopolysaccharide (LPS)-induced systemic inflammation and adipose tissue Erk-1/-2 phosphorylation in mice in vivo. Biochem. Biophys. Res. Commun. 2014, 452:8-13.
11. Hou M., Liu J., Liu F., Liu K., Yu B. C1q tumor necrosis factor-related protein-3 protects mesenchymal stem cells against hypoxia- and serum deprivation-induced apoptosis through the phosphoinositide 3-kinase/Akt pathway. Int. J. Mol. Med. 2014, 33:97-104.
12. Yi W., Sun Y., Yuan Y., Lau W.B., Zheng Q., Wang X., Wang Y., Shang X., Gao E., Koch W.J., Ma X.L. 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, 125:3159-3169.
13. Zheng Q., Yuan Y., Yi W., Lau W.B., Wang Y., Wang X., Sun Y., Lopez B.L., Christopher T.A., Peterson J.M., Wong G.W., Yu S., Yi D., Ma X.L. 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, 31:2616-2623.
14. Barron J.T., Kopp S.J., Tow J.P., Messer J.V. Effects of altering carbohydrate metabolism on energy status and contractile function of vascular smooth muscle. Biochem. Biophys. Acta 1989, 976:42-52.
15. Dromparis P., Michelakis E.D. Mitochondria in vascular health and disease. Annu. Rev. Physiol. 2013, 75:95-126.
16. Brayden J.E. Functional roles of KATP channels in vascular smooth muscle. Clin. Exp. Pharmacol. Physiol. 2002, 29:312-316.
17. 2+ influx by metabolic substrates in Saccharomyces cerevisiae: role of membrane potential and cellular ATP levels. J. Gen. Microbiol. 1990, 136:861-866.
18. Hardie D.G., Hawley S.A. AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 2001, 23:1112-1119.
19. Clifford P.S. Tripartite function of ATP in vascular signalling. J. Physiol. 2008, 586:4783-4784.
20. Li J.Y., Ueda H., Seiyama A., Seki J., Konaka K., Yanagida T., Sakoda S., Yanagihara T. Ischemic vasoconstriction and tissue energy metabolism during global cerebral ischemia in gerbils. J. Neurotrauma 2007, 24:547-558.
21. Postnov I. Energy-dependent pathogenesis in chronic hypertension. Arkh. Patol. 2009, 71:3-11.
22. Li W., Jeong J.H., Park H.G., Lee Y.R., Li M., Lee S.K. Endurance exercise training inhibits neointimal formation via enhancement of FOXOs expression in balloon-induced atherosclerosis rat model. J. Exerc. Nutr. Biochem. 2014, 18:105-110.
23. Beck D.T., Martin J.S., Casey D.P., Braith R.W. Exercise training reduces peripheral arterial stiffness and myocardial oxygen demand in young prehypertensive subjects. Am. J. Hypertens. 2013, 26:1093-1102.
24. Plant S., Shand B., Elder P., Scott R. Adiponectin attenuates endothelial dysfunction induced by oxidised low-density lipoproteins. Diabetes Vasc. Dis. Res. 2008, 5:102-108.
25. Matsuda M., Shimomura I., Sata M., Arita Y., Nishida M., Maeda N., Kumada M., Okamoto Y., Nagaretani H., Nishizawa H., Kishida K., Komuro R., Ouchi N., Kihara S., Nagai R., Funahashi T., Matsuzawa Y. Role of adiponectin in preventing vascular stenosis. The missing link of adipo-vascular axis. J. Biol. Chem. 2002, 277:37487-37491.
26. Zhou Y., Wang J.Y., Feng H., Wang C., Li L., Wu D., Lei H., Li H., Wu L.L. Overexpression of c1q/tumor necrosis factor-related protein-3 promotes phosphate-induced vascular smooth muscle cell calcification both in vivo and in vitro. Arterioscler. Thromb. Vasc. Biol. 2014, 34:1002-1010.
27. Jono S., Nishizawa Y., Shioi A., Morii H. Parathyroid hormone-related peptide as a local regulator of vascular calcification. Its inhibitory action on in vitro calcification by bovine vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 1997, 17:1135-1142.
28. Zhao M.M., Xu M.J., Cai Y., Zhao G., Guan Y., Kong W., Tang C., Wang X. Mitochondrial reactive oxygen species promote p65 nuclear translocation mediating high-phosphate-induced vascular calcification in vitro and in vivo. Kidney. Int. 2011, 79:1071-1079.
29. Chen J., Mathews C.E. Use of chemical probes to detect mitochondrial ROS by flow cytometry and spectrofluorometry. Methods Enzymol. 2014, 542:223-241.
30. Senior A.E. ATP synthesis by oxidative phosphorylation. Physiol. Rev. 1988, 68:177-231.
31. Cimen H., Han M.J., Yang Y., Tong Q., Koc H., Koc E.C. Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 2010, 49:304-311.
32. Liang H., Ward W.F. PGC-1α: a key regulator of energy metabolism. Adv. Physiol. Educ. 2006, 30:145-151.
33. Ruas J.L., White J.P., Rao R.R., Kleiner S., Brannan K.T., Harrison B.C., Greene N.P., Wu J., Estall J.L., Irving B.A., Lanza I.R., Rasbach K.A., Okutsu M., Nair K.S., Yan Z., Leinwand L.A., Spiegelman B.M. A. PGC-1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 2012, 151:1319-1331.
34. Kong X., Wang R., Xue Y., Liu X., Zhang H., Chen Y., Fang F., Chang Y. Sirtuin 3, a new target of PGC-1α, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS ONE 2010, 5:e11707.
35. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127:397-408.
36. Huss J.M., Kelly D.P. Mitochondrial energy metabolism in heart failure: a question of balance. J. Clin. Investig. 2005, 115:547-555.
37. Taha M., Lopaschuk G.D. Alterations in energy metabolism in cardiomyopathies. Ann. Med. 2007, 39:594-607.
38. Yu E., Mercer J., Bennett M. Mitochondria in vascular disease. Cardiovasc. Res. 2012, 95:173-182.
39. Ventura-Clapier R. Exercise training, energy metabolism, and heart failure. Appl. Physiol. Nutr. Metab. 2009, 34:336-339.
40. Van Berendoncks A.M., Garnier A., Ventura-Clapier R., Conraads V.M. Adiponectin: key role and potential target to reverse energy wasting in chronic heart failure. Heart Fail. Rev. 2013, 18:557-566.
41. Rhee J., Inoue Y., Yoon J.C., Puigserver P., Fan M., Gonzalez F.J., Spiegelman B.M. Regulation of hepatic fasting response by PPARγ coactivator-1α (PGC-1): requirement for hepatocyte nuclear factor 4α in gluconeogenesis. Proc. Natl. Acad. Sci. 2003, 100:4012-4017.
42. Summermatter S., Troxler H., Santos G., Handschin C. Coordinated balancing of muscle oxidative metabolism through PGC-1α increases metabolic flexibility and preserves insulin sensitivity. Biochem. Biophys. Res. Commun. 2011, 408:180-185.
43. Wenz T., Rossi S.G., Rotundo R.L., Spiegelman B.M., Moraes C.T. Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. 2009, 106:20405-20410.
44. Arany Z., He H., Lin J., Hoyer K., Handschin C., Toka O., Ahmad F., Matsui T., Chin S., Wu P.H., Rybkin I.I., Shelton J.M., Manieri M., Cinti S., Schoen F.J., Bassel-Duby R., Rosenzweig A., Ingwall J.S., Spiegelman B.M. Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005, 1:259-271.
45. Lehman J.J., Boudina S., Banke N.H., Sambandam N., Han X., Young D.M., Leone T.C., Gross R.W., Lewandowski E.D., Abel E.D., Kelly D.P. The transcriptional coactivator PGC-1α is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H185-H196.
46. Arany Z., Novikov M., Chin S., Ma Y., Rosenzweig A., Spiegelman B.M. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPARγ coactivator 1α. Proc. Natl. Acad. Sci. 2006, 103:10086-10091.
47. Arany Z., Foo S.Y., Ma Y., Ruas J.L., Bommi-Reddy A., Girnun G., Cooper M., Laznik D., Chinsomboon J., Rangwala S.M., Baek K.H., Rosenzweig A., Spiegelman B.M. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature 2008, 451:1008-1012.
48. Qu A., Jiang C., Xu M., Zhang Y., Zhu Y., Xu Q., Zhang C., Wang X. PGC-1α attenuates neointimal formation via inhibition of vascular smooth muscle cell migration in the injured rat carotid artery. Am. J. Physiol. Cell Physiol. 2009, 297:C645-C653.
49. Zhu L., Sun G., Zhang H., Zhang Y., Chen X., Jiang X., Jiang X., Krauss S., Zhang J., Xiang Y., Zhang C.Y. PGC-1α is a key regulator of glucose-induced proliferation and migration in vascular smooth muscle cells. PLoS ONE 2009, 4:e4182.
50. Xiong S., Salazar G., Patrushev N., Ma M., Forouzandeh F., Hilenski L., Alexander R.W. Peroxisome proliferator-activated receptor γ coactivator-1α is a central negative regulator of vascular senescence. Arterioscler. Thromb. Vasc. Biol. 2013, 33:988-998.
51. Kroller-Schon S., Jansen T., Schuler A., Oelze M., Wenzel P., Hausding M., Kerahrodi J.G., Beisele M., Lackner K.J., Daiber A., Munzel T., Schulz E. Peroxisome proliferator-activated receptor γ, coactivator 1α deletion induces angiotensin II-associated vascular dysfunction by increasing mitochondrial oxidative stress and vascular inflammation. Arterioscler. Thromb. Vasc. Biol. 2013, 33:1928-1935.
52. Bellizzi D., Rose G., Cavalcante P., Covello G., Dato S., De Rango F., Greco V., Maggiolini M., Feraco E., Mari V., Franceschi C., Passarino G., De Benedictis G. A novel VNTR enhancer within the SIRT3 gene, a human homologue of SIR2, is associated with survival at oldest ages. Genomics 2005, 85:258-263.
53. Winnik S., Auwerx J., Sinclair D.A., Matter C.M. Protective effects of sirtuins in cardiovascular diseases: from bench to bedside. Eur. Heart J. 2015, 36:3404-3412.
54. Ahn B.H., Kim H.S., Song S., Lee I.H., Liu J., Vassilopoulos A., Deng C.X., Finkel T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. 2008, 105:14447-14452.
55. Paulin R., Dromparis P., Sutendra G., Gurtu V., Zervopoulos S., Bowers L., Haromy A., Webster L., Provencher S., Bonnet S., Michelakis E.D. Sirtuin 3 deficiency is associated with inhibited mitochondrial function and pulmonary arterial hypertension in rodents and humans. Cell Metab. 2014, 20:827-839.
56. Ristow M., Schmeisser K. Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS). Dose Response 2014, 12:288-341.
57. 2 during myocardial ischemia/reperfusion. Cell Death Dis. 2014, 5:e1297.
58. Ristow M., Zarse K. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp. Gerontol. 2010, 45:410-418.
59. Fang X., Sweeney G. Mechanisms regulating energy metabolism by adiponectin in obesity and diabetes. Biochem. Soc. Trans. 2006, 34:798-801.
60. Bouitbir J., Charles A.L., Echaniz-Laguna A., Kindo M., Daussin F., Auwerx J., Piquard F., Geny B., Zoll J. Opposite effects of statins on mitochondria of cardiac and skeletal muscles: a''mitohormesis' mechanism involving reactive oxygen species and PGC-1. Eur. Heart J. 2012, 33:1397-1407.