Regulation of skeletal muscle oxidative phenotype by classical NF-κB signalling

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 8, 2013, Pages 1313-1325

  Remels, A H V ^a   Gosker, H R ^a   Bakker, J ^a   Guttridge, D C ^b   Schols, A M W J ^a   Langen, R C J ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Classical NF B; Inflammation; Mitochondria; Oxidative metabolism; Skeletal muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL LEVEL; CELL LINE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRION; MOUSE; MYOTUBE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; WILD TYPE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; EIF-2 KINASE; HUMANS; INFLAMMATION; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; NF-KAPPA B; OXIDATION-REDUCTION; PHENOTYPE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877351666     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.03.018     Document Type: Article

References (67)

1. Gosker H.R., van Mameren H., van Dijk P.J., Engelen M.P., van der Vusse G.J., Wouters E.F., Schols A.M. Skeletal muscle fibre-type shifting and metabolic profile in patients with chronic obstructive pulmonary disease. Eur. Respir. J. 2002, 19:617-625.
2. Gosker H.R., Lencer N.H., Franssen F.M., van der Vusse G.J., Wouters E.F., Schols A.M. Striking similarities in systemic factors contributing to decreased exercise capacity in patients with severe chronic heart failure or COPD. Chest 2003, 123:1416-1424.
3. Mettauer B., Zoll J., Garnier A., Ventura-Clapier R. Heart failure: a model of cardiac and skeletal muscle energetic failure. Pflugers Arch. 2006, 452:653-666.
4. Yndestad A., Damas J.K., Oie E., Ueland T., Gullestad L., Aukrust P. Systemic inflammation in heart failure-the whys and wherefores. Heart Fail. Rev. 2006, 11:83-92.
5. Tkacova R. Systemic inflammation in chronic obstructive pulmonary disease: may adipose tissue play a role? Review of the literature and future perspectives. Mediators Inflamm. 2010, 585989.
6. Kempf K., Rose B., Herder C., Kleophas U., Martin S., Kolb H. Inflammation in metabolic syndrome and type 2 diabetes: impact of dietary glucose. Ann. N. Y. Acad. Sci. 2006, 1084:30-48.
7. Hoeks J., Schrauwen P. Muscle mitochondria and insulin resistance: a human perspective. Trends Endocrinol. Metab. 2012, 23:444-450.
8. White J.P., Baltgalvis K.A., Puppa M.J., Sato S., Baynes J.W., Carson J.A. Muscle oxidative capacity during IL-6-dependent cancer cachexia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R201-R211.
9. Drexler H., Riede U., Munzel T., Konig H., Funke E., Just H. Alterations of skeletal muscle in chronic heart failure. Circulation 1992, 85:1751-1759.
10. Gosker H.R., Hesselink M.K., Duimel H., Ward K.A., Schols A.M. Reduced mitochondrial density in the vastus lateralis muscle of patients with COPD. Eur. Respir. J. 2007, 30:73-79.
11. Szendroedi J., Phielix E., Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat. Rev. Endocrinol. 2012, 8:92-103.
12. Mancini D.M., Walter G., Reichek N., Lenkinski R., McCully K.K., Mullen J.L., Wilson J.R. Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure. Circulation 1992, 85:1364-1373.
13. Sullivan M.J., Hawthorne M.H. Exercise intolerance in patients with chronic heart failure. Prog. Cardiovasc. Dis. 1995, 38:1-22.
14. Eisner M.D., Iribarren C., Blanc P.D., Yelin E.H., Ackerson L., Byl N., Omachi T.A., Sidney S., Katz P.P. Development of disability in chronic obstructive pulmonary disease: beyond lung function. Thorax 2011, 66:108-114.
15. Park S.W., Goodpaster B.H., Strotmeyer E.S., de Rekeneire N., Harris T.B., Schwartz A.V., Tylavsky F.A., Newman A.B. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes 2006, 55:1813-1818.
16. Remels A.H., Gosker H.R., Schrauwen P., Hommelberg P.P., Sliwinski P., Polkey M., Galdiz J., Wouters E.F., Langen R.C., Schols A.M. TNF-alpha impairs regulation of muscle oxidative phenotype: implications for cachexia?. FASEB J. 2010, 24:5052-5062.
17. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 2006, 116:615-622.
18. Shao D., Liu Y., Liu X., Zhu L., Cui Y., Cui A., Qiao A., Kong X., Liu Y., Chen Q., Gupta N., Fang F., Chang Y. PGC-1 beta-regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERR alpha. Mitochondrion 2010, 10:516-527.
19. Lin J., Handschin C., Spiegelman B.M. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005, 1:361-370.
20. Remels A.H., Schrauwen P., Broekhuizen R., Willems J., Kersten S., Gosker H.R., Schols A.M. Peroxisome proliferator-activated receptor expression is reduced in skeletal muscle in COPD. Eur. Respir. J. 2007, 30:245-252.
21. Mensink M., Hesselink M.K., Russell A.P., Schaart G., Sels J.P., Schrauwen P. Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1 alpha and PPAR beta/delta gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. Int. J. Obes. (Lond) 2007, 31:1302-1310.
22. Garnier A., Fortin D., Delomenie C., Momken I., Veksler V., Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J. Physiol. 2003, 551:491-501.
23. Calle M.C., Fernandez M.L. Inflammation and type 2 diabetes. Diabetes Metab. 2012, 38:183-191.
24. Garrod R., Marshall J., Barley E., Fredericks S., Hagan G. The relationship between inflammatory markers and disability in chronic obstructive pulmonary disease (COPD). Prim. Care Respir. J. 2007, 16:236-240.
25. Peterson J.M., Bakkar N., Guttridge D.C. NF-kappaB signaling in skeletal muscle health and disease. Curr. Top. Dev. Biol. 2011, 96:85-119.
26. Adams V., Spate U., Krankel N., Schulze P.C., Linke A., Schuler G., Hambrecht R. Nuclear factor-kappa B activation in skeletal muscle of patients with chronic heart failure: correlation with the expression of inducible nitric oxide synthase. Eur. J. Cardiovasc. Prev. Rehabil. 2003, 10:273-277.
27. Agusti A., Morla M., Sauleda J., Saus C., Busquets X. NF-kappaB activation and iNOS upregulation in skeletal muscle of patients with COPD and low body weight. Thorax 2004, 59:483-487.
28. Fermoselle C., Rabinovich R., Ausin P., Puig-Vilanova E., Coronell C., Sanchez F., Roca J., Gea J., Barreiro E. Does oxidative stress modulate limb muscle atrophy in severe copd patients?. Eur. Respir. J. 2012, 40:851-862.
29. Tantiwong P., Shanmugasundaram K., Monroy A., Ghosh S., Li M., DeFronzo R.A., Cersosimo E., Sriwijitkamol A., Mohan S., Musi N. NF-kappaB activity in muscle from obese and type 2 diabetic subjects under basal and exercise-stimulated conditions. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E794-E801.
30. Vogiatzis I., Simoes D.C., Stratakos G., Kourepini E., Terzis G., Manta P., Athanasopoulos D., Roussos C., Wagner P.D., Zakynthinos S. Effect of pulmonary rehabilitation on muscle remodelling in cachectic patients with COPD. Eur. Respir. J. 2010, 36:301-310.
31. Langen R.C., Schols A.M., Kelders M.C., Wouters E.F., Janssen-Heininger Y.M. Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-kappaB. FASEB J. 2001, 15:1169-1180.
32. Rando T.A., Blau H.M. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 1994, 125:1275-1287.
33. Remels A.H., Langen R.C., Schrauwen P., Schaart G., Schols A.M., Gosker H.R. Regulation of mitochondrial biogenesis during myogenesis. Mol. Cell. Endocrinol. 2010, 315:113-120.
34. Westergaard M., Henningsen J., Johansen C., Rasmussen S., Svendsen M.L., Jensen U.B., Schroder H.D., Staels B., Iversen L., Bolund L., Kragballe K., Kristiansen K. Expression and localization of peroxisome proliferator-activated receptors and nuclear factor kappaB in normal and lesional psoriatic skin. J. Invest. Dermatol. 2003, 121:1104-1117.
35. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
36. Gugneja S., Virbasius C.M., Scarpulla R.C. Nuclear respiratory factors 1 and 2 utilize similar glutamine-containing clusters of hydrophobic residues to activate transcription. Mol. Cell. Biol. 1996, 16:5708-5716.
37. Jornayvaz F.R., Shulman G.I. Regulation of mitochondrial biogenesis. Essays Biochem. 2010, 47:69-84.
38. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24:78-90.
39. Suematsu N., Tsutsui H., Wen J., Kang D., Ikeuchi M., Ide T., Hayashidani S., Shiomi T., Kubota T., Hamasaki N., Takeshita A. Oxidative stress mediates tumor necrosis factor-alpha-induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation 2003, 107:1418-1423.
40. Li Y.Y., Chen D., Watkins S.C., Feldman A.M. Mitochondrial abnormalities in tumor necrosis factor-alpha-induced heart failure are associated with impaired DNA repair activity. Circulation 2001, 104:2492-2497.
41. Mariappan N., Soorappan R.N., Haque M., Sriramula S., Francis J. TNF-alpha-induced mitochondrial oxidative stress and cardiac dysfunction: restoration by superoxide dismutase mimetic Tempol. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H2726-H2737.
42. Moe G.W., Marin-Garcia J., Konig A., Goldenthal M., Lu X., Feng Q. In vivo TNF-alpha inhibition ameliorates cardiac mitochondrial dysfunction, oxidative stress, and apoptosis in experimental heart failure. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H1813-H1820.
43. Chen X.H., Zhao Y.P., Xue M., Ji C.B., Gao C.L., Zhu J.G., Qin D.N., Kou C.Z., Qin X.H., Tong M.L., Guo X.R. TNF-alpha induces mitochondrial dysfunction in 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 2010, 328:63-69.
44. Cho S.Y., Park P.J., Shin E.S., Lee J.H., Chang H.K., Lee T.R. Proteomic analysis of mitochondrial proteins of basal and lipolytically (isoproterenol and TNF-alpha)-stimulated adipocytes. J. Cell. Biochem. 2009, 106:257-266.
45. Valerio A., Cardile A., Cozzi V., Bracale R., Tedesco L., Pisconti A., Palomba L., Cantoni O., Clementi E., Moncada S., Carruba M.O., Nisoli E. TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J. Clin. Invest. 2006, 116:2791-2798.
46. Cogswell P.C., Kashatus D.F., Keifer J.A., Guttridge D.C., Reuther J.Y., Bristow C., Roy S., Nicholson D.W., Baldwin A.S. NF-kappa B and I kappa B alpha are found in the mitochondria. Evidence for regulation of mitochondrial gene expression by NF-kappa B. J. Biol. Chem. 2003, 278:2963-2968.
47. Cao Z., Tanaka M., Regnier C., Rothe M., Yamit-hezi A., Woronicz J.D., Fuentes M.E., Durnin M.H., Dalrymple S.A., Goeddel D.V. NF-kappa B activation by tumor necrosis factor and interleukin-1. Cold Spring Harb. Symp. Quant. Biol. 1999, 64:473-483.
48. Jura J., Wegrzyn P., Zarebski A., Wladyka B., Koj A. Identification of changes in the transcriptome profile of human hepatoma HepG2 cells stimulated with interleukin-1 beta. Biochim. Biophys. Acta 2004, 1689:120-133.
49. Kitade H., Kanemaki T., Sakitani K., Inoue K., Matsui Y., Kamiya T., Nakagawa M., Hiramatsu Y., Kamiyama Y., Ito S., Okumura T. Regulation of energy metabolism by interleukin-1beta, but not by interleukin-6, is mediated by nitric oxide in primary cultured rat hepatocytes. Biochim. Biophys. Acta 1996, 1311:20-26.
50. Berthiaume F., MacDonald A.D., Kang Y.H., Yarmush M.L. Control analysis of mitochondrial metabolism in intact hepatocytes: effect of interleukin-1beta and interleukin-6. Metab. Eng. 2003, 5:108-123.
51. Chan D.C. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 2012, 46:265-287.
52. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., Michael L.F., Puigserver P., Isotani E., Olson E.N., Lowell B.B., Bassel-Duby R., Spiegelman B.M. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002, 418:797-801.
53. Zechner C., Lai L., Zechner J.F., Geng T., Yan Z., Rumsey J.W., Collia D., Chen Z., Wozniak D.F., Leone T.C., Kelly D.P. Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity. Cell Metab. 2010, 12:633-642.
54. Palomer X., Alvarez-Guardia D., Rodriguez-Calvo R., Coll T., Laguna J.C., Davidson M.M., Chan T.O., Feldman A.M., Vazquez-Carrera M. TNF-alpha reduces PGC-1alpha expression through NF-kappaB and p38 MAPK leading to increased glucose oxidation in a human cardiac cell model. Cardiovasc. Res. 2009, 81:703-712.
55. Handschin C., Chin S., Li P., Liu F., Maratos-Flier E., Lebrasseur N.K., Yan Z., Spiegelman B.M. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals. J. Biol. Chem. 2007, 282:30014-30021.
56. Lai L., Leone T.C., Zechner C., Schaeffer P.J., Kelly S.M., Flanagan D.P., Medeiros D.M., Kovacs A., Kelly D.P. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 2008, 22:1948-1961.
57. Eisele P.S., Salatino S., Sobek J., Hottiger M.O., Handschin C. The peroxisome proliferator-activated receptor gamma coactivator 1alpha/beta (PGC-1) coactivators repress the transcriptional activity of NF-kappaB in skeletal muscle cells. J. Biol. Chem. 2013, 288:2246-2260.
58. Safdar A., Little J.P., Stokl A.J., Hettinga B.P., Akhtar M., Tarnopolsky M.A. Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J. Biol. Chem. 2011, 286:10605-10617.
59. Alvarez-Guardia D., Palomer X., Coll T., Davidson M.M., Chan T.O., Feldman A.M., Laguna J.C., Vazquez-Carrera M. The p65 subunit of NF-kappaB binds to PGC-1alpha, linking inflammation and metabolic disturbances in cardiac cells. Cardiovasc. Res. 2010, 87:449-458.
60. Johnson R.F., Witzel I.I., Perkins N.D. p53-dependent regulation of mitochondrial energy production by the RelA subunit of NF-kappaB. Cancer Res. 2011, 71:5588-5597.
61. Guseva N.V., Taghiyev A.F., Sturm M.T., Rokhlin O.W., Cohen M.B. Tumor necrosis factor-related apoptosis-inducing ligand-mediated activation of mitochondria-associated nuclear factor-kappaB in prostatic carcinoma cell lines. Mol. Cancer Res. 2004, 2:574-584.
62. Aoi W., Naito Y., Mizushima K., Takanami Y., Kawai Y., Ichikawa H., Yoshikawa T. The microRNA miR-696 regulates PGC-1{alpha} in mouse skeletal muscle in response to physical activity. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E799-E806.
63. Safdar A., Abadi A., Akhtar M., Hettinga B.P., Tarnopolsky M.A. miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One 2009, 4:e5610.
64. Irrcher I., Ljubicic V., Kirwan A.F., Hood D.A. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS One 2008, 3:e3614.
65. Bakkar N., Ladner K., Canan B.D., Liyanarachchi S., Bal N.C., Pant M., Periasamy M., Li Q., Janssen P.M., Guttridge D.C. IKKalpha and alternative NF-kappaB regulate PGC-1beta to promote oxidative muscle metabolism. J. Cell Biol. 2012, 196:497-511.
66. Peterson J.M., Kline W., Canan B.D., Ricca D.J., Kaspar B., Delfin D.A., DiRienzo K., Clemens P.R., Robbins P.D., Baldwin A.S., Flood P., Kaumaya P., Freitas M., Kornegay J.N., Mendell J.R., Rafael-Fortney J.A., Guttridge D.C., Janssen P.M. Peptide-based inhibition of NF-kappaB rescues diaphragm muscle contractile dysfunction in a murine model of Duchenne muscular dystrophy. Mol. Med. 2011, 17:508-515.
67. Tang Y., Reay D.P., Salay M.N., Mi M.Y., Clemens P.R., Guttridge D.C., Robbins P.D., Huard J., Wang B. Inhibition of the IKK/NF-kappaB pathway by AAV gene transfer improves muscle regeneration in older mdx mice. Gene Ther. 2010, 17:1476-1483.