TNF-α impairs regulation of muscle oxidative phenotype: Implications for cachexia?

FASEB Journal

Volumn 24, Issue 12, 2010, Pages 5052-5062

  Remels, A H V ^a   Gosker, H R ^a   Schrauwen, P ^a   Hommelberg, P P H ^a   Sliwinski, P ^b   Polkey, M ^c   Galdiz, J ^d   Wouters, E F M ^a,e   Langen, R C J ^a   Schols, A M W J ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NATIONAL TUBERCULOSIS AND LUNG DISEASES RESEARCH INSTITUTE   (Poland)

^c ROYAL BROMPTON HOSPITAL   (United Kingdom)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^e Center for Integrated Rehabilitation of Organ Failure   (Netherlands)

Author keywords

Inflammation; Mitochondrial transcription factor A; Nuclear factor B; Peroxisome proliferator activated receptors

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CITRATE SYNTHASE; CYTOCHROME C OXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MYOSIN HEAVY CHAIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL CELL; ARTICLE; BIOGENESIS; BODY MASS; CACHEXIA; CELL CULTURE; CHRONIC DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; FEMALE; GENETIC TRANSCRIPTION; HEAVY CHAIN; HUMAN; HUMAN TISSUE; INFLAMMATION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE MASS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONTENT; REGULATORY MECHANISM; SKELETAL MUSCLE; SMOKING; STIMULATION; TISSUE LEVEL; TRANSCRIPTION INITIATION; VASTUS LATERALIS MUSCLE;

ANIMALS; BLOTTING, WESTERN; CACHEXIA; CELL LINE; CITRATE (SI)-SYNTHASE; DNA-BINDING PROTEINS; ELECTRON TRANSPORT COMPLEX IV; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEAT-SHOCK PROTEINS; HUMANS; HYDRO-LYASES; MICE; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; NF-KAPPA B; PPAR ALPHA; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78649743322     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-150714     Document Type: Article

References (56)

1. Tisdale, M. J. (2009) Mechanisms of cancer cachexia. Physiol. Rev. 89, 381-410
2. Pajak, B., Orzechowska, S., Pijet, B., Pijet, M., Pogorzelska, A., Gajkowska, B., and Orzechowski, A. (2008) Crossroads of cytokine signaling: the chase to stop muscle cachexia. J. Physiol. Pharmacol. 59(Suppl. 9), 251-264
3. Schols, A. M., Soeters, P. B., Dingemans, A. M., Mostert, R., Frantzen, P. J., and Wouters, E. F. (1993) Prevalence and characteristics of nutritional depletion in patients with stable COPD eligible for pulmonary rehabilitation. Am. Rev. Respir. Dis. 147, 1151-1156
4. Vermeeren, M. A., Creutzberg, E. C., Schols, A. M., Postma, D. S., Pieters, W. R., Roldaan, A. C., and Wouters, E. F. (2006) Prevalence of nutritional depletion in a large out-patient population of patients with COPD. Respir. Med. 100, 1349-1355
5. Schols, A. M., Broekhuizen, R., Weling-Scheepers, C. A., and Wouters, E. F. (2005) Body composition and mortality in chronic obstructive pulmonary disease. Am. J. Clin. Nutr. 82, 53-59
6. Sin, D. D., and Man, S. F. (2007) Systemic inflammation and mortality in chronic obstructive pulmonary disease. Can. J. Physiol. Pharmacol. 85, 141-147
7. Gan, W. Q., Man, S. F., Senthilselvan, A., and Sin, D. D. (2004) Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis. Thorax 59, 574-580
8. Gosker, H., Zeegers, M., Wouters, E., and Schols, A. M. (2007) Muscle fibre type shifting in the vastus lateralis of patients with COPD is associated with disease severity: a systematic review and meta-analysis. Thorax 62, 944-949
9. Gosker, H. R., Engelen, M. P., van Mameren, H., van Dijk, P. J., van der Vusse, G. J., Wouters, E. F., and Schols, A. M. (2002) Muscle fiber type IIX atrophy is involved in the loss of fat-free mass in chronic obstructive pulmonary disease. Am. J. Clin. Nutr. 76, 113-119
10. Cerami, A., Ikeda, Y., Le Trang, N., Hotez, P. J., and Beutler, B. (1985) Weight loss associated with an endotoxin-induced mediator from peritoneal macrophages: the role of cachectin (tumor necrosis factor). Immunol. Lett. 11, 173-177
11. Cai, D., Frantz, J. D., Tawa, N. E., Jr., Melendez, P. A., Oh, B. C., Lidov, H. G., Hasselgren, P. O., Frontera, W. R., Lee, J., Glass, D. J., and Shoelson, S. E. (2004) IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 119, 285-298
12. Tracey, K. J., Wei, H., Manogue, K. R., Fong, Y., Hesse, D. G., Nguyen, H. T., Kuo, G. C., Beutler, B., Cotran, R. S., Cerami, A., and Lowry, S. F. (1988) Cachectin/tumor necrosis factor induces cachexia, anemia, and inflammation. J. Exp. Med. 167, 1211-1227
13. Lee, M. D., Zentella, A., Vine, W., Pekala, P. H., and Cerami, A. (1987) Effect of endotoxin-induced monokines on glucose metabolism in the muscle cell line L6. Proc. Natl. Acad. Sci. U. S. A. 84, 2590-2594
14. Remels, A. H., Schrauwen, P., Broekhuizen, R., Willems, J., Kersten, S., Gosker, H. R., and Schols, A. M. (2007) Expression and content of PPARs is reduced in skeletal muscle of COPD patients. Eur. Respir. J. 30, 245-252
15. Fabbri, L., Pauwels, R. A., and Hurd, S. S. (2004) Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary updated 2003. COPD 1, 105-141; discussion 103-104
16. Gosker, H. R., Langen, R. C., Bracke, K. R., Joos, G. F., Brusselle, G. G., Steele, C., Ward, K. A., Wouters, E. F., and Schols, A. M. (2009) Extrapulmonary manifestations of chronic obstructive pulmonary disease in a mouse model of chronic cigarette smoke exposure. Am. J. Respir. Cell Mol. Biol. 40, 710-716
17. Van Wetering, C. R., Hoogendoorn, M., Broekhuizen, R., Geraerts-Keeris, G. J., De Munck, D. R., Rutten-van Molken, M. P., and Schols, A. M. (2010) Efficacy and costs of nutritional rehabilitation in muscle-wasted patients with chronic obstructive pulmonary disease in a community-based setting: a prespecified subgroup analysis of the INTERCOM trial. J. Am. Med. Dir. Assoc. 11, 179-187
18. Langen, R. C., Schols, A. M., Kelders, M. C., Wouters, E. F., and Janssen-Heininger, Y. M. (2001) Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-kappaB. FASEB J. 15, 1169-1180
19. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., and Spiegelman, B. M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124
20. Gugneja, S., Virbasius, C. M., and Scarpulla, R. C. (1996) Nuclear respiratory factors 1 and 2 utilize similar glutamine-containing clusters of hydrophobic residues to activate transcription. Mol. Cell. Biol. 16, 5708-5716
21. Gosker, H. R., Schrauwen, P., Broekhuizen, R., Hesselink, M. K., Moonen-Kornips, E., Ward, K. A., Franssen, F. F., Wouters, E. F., and Schols, A. M. (2005) Exercise training restores uncoupling protein-3 content in limb muscles of patients with chronic obstructive pulmonary disease. Am. J. Physiol. Endocrinol. Metab. 290, E976-E981
22. Van der Velden, J., Langen, R., Kelders, M., Willems, J., Wouters, E., Janssen-Heininger, Y., and Schols, A. (2006) Myogenic differentiation during regrowth of atrophied skeletal muscle is associated with inactivation of GSK-3β. Am. J. Physiol. Cell. Physiol. 292, C1636-C1644
23. Altman, D. G., Gore, S. M., Gardner, M. J., and Pocock, S. J. (1983) Statistical guidelines for contributors to medical journals. Br. Med. J. (Clin. Res. Ed.) 286, 1489-1493
24. Langen, R. C., Schols, A. M., Kelders, M. C., van der Velden, J. L., Wouters, E. F., and Janssen-Heininger, Y. M. (2006) Muscle wasting and impaired muscle regeneration in a murine model of chronic pulmonary inflammation. Am. J. Respir. Cell Mol. Biol. 35, 689-696
25. Puente-Maestu, L., Perez-Parra, J., Godoy, R., Moreno, N., Tejedor, A., Gonzalez-Aragoneses, F., Bravo, J. L., Alvarez, F. V., Camano, S., and Agusti, A. (2009) Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur. Respir. J. 33, 1045-1052
26. Lancaster, J. R., Jr., Laster, S. M., and Gooding, L. R. (1989) Inhibition of target cell mitochondrial electron transfer by tumor necrosis factor. FEBS Lett. 248, 169-174
27. Schulze-Osthoff, K., Bakker, A. C., Vanhaesebroeck, B., Beyaert, R., Jacob, W. A., and Fiers, W. (1992) Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions: evidence for the involvement of mitochondrial radical generation. J. Biol. Chem. 267, 5317-5323
28. Valerio, A., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Pisconti, A., Palomba, L., Cantoni, O., Clementi, E., Moncada, S., Carruba, M. O., and Nisoli, E. (2006) TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J. Clin. Invest. 116, 2791-2798
29. Jia, L., Kelsey, S. M., Grahn, M. F., Jiang, X. R., and Newland, A. C. (1996) Increased activity and sensitivity of mitochondrial respiratory enzymes to tumor necrosis factor alpha-mediated inhibition is associated with increased cytotoxicity in drug-resistant leukemic cell lines. Blood 87, 2401-2410
30. Marin-Garcia, J., Goldenthal, M. J., and Moe, G. W. (2001) Abnormal cardiac and skeletal muscle mitochondrial function in pacing-induced cardiac failure. Cardiovasc. Res. 52, 103-110
31. Lyons, C. N., Leary, S. C., and Moyes, C. D. (2004) Bioenergetic remodeling during cellular differentiation: changes in cytochrome c oxidase regulation do not affect the metabolic phenotype. Biochem. Cell Biol. 82, 391-399
32. Gosker, H. R., van Mameren, H., van Dijk, P. J., Engelen, M. P., van der Vusse, G. J., Wouters, E. F., and Schols, A. M. (2002) Skeletal muscle fibre-type shifting and metabolic profile in patients with chronic obstructive pulmonary disease. Eur. Respir. J. 19, 617-625
33. Jackman, R. W., and Kandarian, S. C. (2004) The molecular basis of skeletal muscle atrophy. Am. J. Physiol. Cell Physiol. 287, C834-C843
34. Attaix, D., Ventadour, S., Codran, A., Bechet, D., Taillandier, D., and Combaret, L. (2005) The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem. 41, 173-186
35. Luquet, S., Lopez-Soriano, J., Holst, D., Fredenrich, A., Melki, J., Rassoulzadegan, M., and Grimaldi, P. A. (2003) Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J. 17, 2299-2301
36. Acharyya, S., Ladner, K. J., Nelsen, L. L., Damrauer, J., Reiser, P. J., Swoap, S., and Guttridge, D. C. (2004) Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J. Clin. Invest. 114, 370-378
37. Petersen, A. M., Plomgaard, P., Fischer, C. P., Ibfelt, T., Pedersen, B. K., and van Hall, G. (2009) Acute moderate elevation of TNF-alpha does not affect systemic and skeletal muscle protein turnover in healthy humans. J. Clin. Endocrinol. Metab. 94, 294-299
38. Wust, R. C., and Degens, H. (2007) Factors contributing to muscle wasting and dysfunction in COPD patients. Int. J. Chron. Obstruct. Pulmon. Dis. 2, 289-300
39. Couillard, A., and Prefaut, C. (2005) From muscle disuse to myopathy in COPD: potential contribution of oxidative stress. Eur. Respir. J. 26, 703-719
40. Safdar, A., Hamadeh, M. J., Kaczor, J. J., Raha, S., Debeer, J., and Tarnopolsky, M. A. (2010) Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLoS ONE 5, e10778
41. Chabi, B., Adhihetty, P. J., O'Leary, M. F., Menzies, K. J., and Hood, D. A. (2009) Relationship between Sirt1 expression and mitochondrial proteins during conditions of chronic muscle use and disuse. J. Appl. Physiol. 107, 1730-1735
42. Lanza, I. R., and Sreekumaran Nair, K. (2010) Regulation of skeletal muscle mitochondrial function: genes to proteins. Acta Physiol. (Oxf.) 199, 529-547
43. Crul, T., Spruit, M. A., Gayan-Ramirez, G., Quarck, R., Gosselink, R., Troosters, T., Pitta, F., and Decramer, M. (2007) Markers of inflammation and disuse in vastus lateralis of chronic obstructive pulmonary disease patients. Eur. J. Clin. Invest. 37, 897-904
44. Montes de Oca, M., Torres, S. H., De Sanctis, J., Mata, A., Hernandez, N., and Talamo, C. (2005) Skeletal muscle inflammation and nitric oxide in patients with COPD. Eur. Respir. J. 26, 390-397
45. Barreiro, E., S.A., Polkey, M., Galdiz, J., Gosker, H., Swallow, E., Coronell, C., and Gea, J. (2007) Cytokine profile in quadriceps muscle of patients with severe chronic obstructive pulmonary disease. Thorax 63, 100-107
46. Barnes, P. J., and Celli, B. R. (2009) Systemic manifestations and comorbidities of COPD. Eur. Respir. J. 33, 1165-1185
47. Tang, K., Wagner, P. D., and Breen, E. C. (2010) TNF-alpha-mediated reduction in PGC-1alpha may impair skeletal muscle function after cigarette smoke exposure. J. Cell. Physiol. 222, 320-327
48. Rabinovich, R. A., Bastos, R., Ardite, E., Llinas, L., Orozco-Levi, M., Gea, J., Vilaro, J., Barbera, J. A., Rodriguez-Roisin, R., Fernandez-Checa, J. C., and Roca, J. (2007) Mitochondrial dysfunction in COPD patients with low body mass index. Eur. Respir. J. 29, 643-650
49. Pascual, G., Fong, A. L., Ogawa, S., Gamliel, A., Li, A. C., Perissi, V., Rose, D. W., Willson, T. M., Rosenfeld, M. G., and Glass, C. K. (2005) A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 437, 759-763
50. Remels, A. H., Langen, R. C., Gosker, H. R., Russell, A. P., Spaapen, F., Voncken, J. W., Schrauwen, P., and Schols, A. M. (2009) PPARgamma inhibits NF-kappaB-dependent transcriptional activation in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 297, E174-E183
51. Delerive, P., De Bosscher, K., Besnard, S., Vanden Berghe, W., Peters, J. M., Gonzalez, F. J., Fruchart, J. C., Tedgui, A., Haegeman, G., and Staels, B. (1999) Peroxisome proliferator-activated receptor alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappaB and AP-1. J. Biol. Chem. 274, 32048-32054
52. Zhao, C. Y., Wang, J. B., Deng, Z. J., Liu, J. W., Li, J. M., Li, L., and Jiang, L. L. (2005) Relationship between NF-kappa B binding activity and expression of PPAR gamma-mRNA in the livers of rats with fatty liver disease. [In Chinese] Zhonghua Gan Zang Bing Za Zhi 13, 96-100
53. Bakkar, N., Wang, J., Ladner, K. J., Wang, H., Dahlman, J. M., Carathers, M., Acharyya, S., Rudnicki, M. A., Hollenbach, A. D., and Guttridge, D. C. (2008) IKK/NF-kappaB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis. J. Cell Biol. 180, 787-802
54. Guttridge, D. C., Mayo, M. W., Madrid, L. V., Wang, C. Y., and Baldwin, A. S., Jr. (2000) NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289, 2363-2366
55. Broekhuizen, R., Wouters, E. F., Creutzberg, E. C., Weling-Scheepers, C. A., and Schols, A. M. (2005) Polyunsaturated fatty acids improve exercise capacity in chronic obstructive pulmonary disease. Thorax 60, 376-382
56. Mensink, M., Hesselink, M. K., Russell, A. P., Schaart, G., Sels, J. P., and Schrauwen, P. (2007) 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.) 31, 1302-1310