Classical NF-κB activation impairs skeletal muscle oxidative phenotype by reducing IKK-α expression

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 2, 2014, Pages 175-185

  Remels, A H V ^a   Gosker, H R ^a   Langen, R C ^a   Polkey, M ^b   Sliwinski, P ^c   Galdiz, J ^d   van den Borst, B ^a   Pansters, N A ^a   Schols, A M W J ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ROYAL BROMPTON AND HAREFIELD NHS FOUNDATION TRUST   (United Kingdom)

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

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

Author keywords

Classical NF B; IKK ; Oxidative metabolism; Skeletal muscle; TNF

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CYTOCHROME C OXIDASE; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SMALL INTERFERING RNA; SUCCINATE DEHYDROGENASE (UBIQUINONE); TUMOR NECROSIS FACTOR ALPHA; UBIQUINOL CYTOCHROME C REDUCTASE;

ADULT; AEROBIC METABOLISM; ANIMAL CELL; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; ENZYME ACTIVITY; FORCED EXPIRATORY VOLUME; FORCED VITAL CAPACITY; HUMAN; HUMAN CELL; LUNG FUNCTION; MOUSE; MUSCLE BIOPSY; MUSCLE CELL; MYOBLAST; MYOTUBE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONTENT; PROTEIN EXPRESSION; QUADRICEPS FEMORIS MUSCLE; SKELETAL MUSCLE;

3-MONOOXYGENASE/TRYPTOPHAN 5-MONOOXYGENASE ACTIVATION PROTEIN, ZETA POLYPEPTIDE; 50S RIBOSOMAL SUBUNIT PROTEIN L15; 60S RIBOSOMAL PROTEIN L13A; ACTB; AD; ADENOSINE TRIPHOSPHATE; ADENOVIRAL; ALAS1; ATP; B2M; BETA CYTOSKELETAL ACTIN; BMI; BODY MASS INDEX; CA; CHRONIC OBSTRUCTIVE PULMONARY DISEASE; CITRATE SYNTHASE; CLASSICAL NF-ΚB; CONSTITUTIVELY ACTIVE; COPD; COXIV; CS; CYTOCHROME C OXIDASE 4; DELTA-AMINOLEVULINATE SYNTHASE 1; DMEM; DULBECCO'S MODIFIED EAGLE MEDIUM; FEV1; FORCED EXPIRATORY VOLUME IN ONE SECOND; FORCED VITAL CAPACITY; FVC; GAPDH; GAPDH, GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GFP; GLUCURONIDASE, BÈTA; GREEN FLUORESCENT PROTEIN; GUSB; HAD; HANK'S BALANCED SALT SOLUTION; HBSS; HCBP; HMBS; HPRT; HPRT, HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE 1; HUMAN CARNITINE-PALMITOYL TRANSFERASE B; HYDROXYMETHYLBILANE SYNTHASE; ICAM-1; IKK-Α; IKK-Α, IΚB KINASE ALPHA; IKK-Β; IL-1Β; INTERLEUKIN 1Β; INTRA-CELLULAR ADHESION MOLECULE 1; IΚB KINASE BETA; IΚBΑ; MLC; MYHC; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; NF-ΚB; NOT SIGNIFICANT; NRF; NS; NUCLEAR FACTOR KAPPA B; NUCLEAR FACTOR OF KAPPA LIGHT POLYPEPTIDE GENE ENHANCER IN B-CELLS INHIBITOR ALPHA; NUCLEAR RESPIRATORY FACTOR; OXIDATIVE METABOLISM; OXIDATIVE PHENOTYPE; OXIDATIVE PHOSPHORYLATION; OXPHEN; OXPHOS; PBS; PEPTIDYLPROLYL ISOMERASE A (CYCLOPHILIN A); PGC-1; PGC-1, PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA CO-ACTIVATOR 1; PHOSPHATE-BUFFERED SALINE; PPAR; PPAR, PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PPIA; RPL13A; RPLO; SD; SEM; SKELETAL MUSCLE; SR; STANDARD DEVIATION; STANDARD EQUALITY OF THE MEAN; SUPER REPRESSOR; TFAM; TFAM, MITOCHONDRIAL TRANSCRIPTION FACTOR A; TNF-Α; TNF-Α, TUMOUR NECROSIS FACTOR ALPHA; UBC; UBIQUITIN C; WILD-TYPE; WT; YWHAZ; Β-HYDROXYACYL-COA DEHYDROGENASE; Β2M, BETA 2 MICROGLOBULIN;

AGED; ANIMALS; BLOTTING, WESTERN; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B KINASE; MALE; MICE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; NF-KAPPA B; OXIDATION-REDUCTION; PHENOTYPE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; QUADRICEPS MUSCLE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84890145435     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.11.001     Document Type: Article

References (44)

1. Skeletal muscle dysfunction in chronic obstructive pulmonary disease A statement of the American Thoracic Society and European Respiratory Society. Am. J. Respir. Crit. Care Med. 1999, 159:S1-S40.
2. Barnes P.J., Celli B.R. Systemic manifestations and comorbidities of COPD. Eur. Respir. J. 2009, 33:1165-1185.
3. Remels A.H., Gosker H.R., Langen R.C., Schols A.M. The mechanisms of cachexia underlying muscle dysfunction in COPD. J. Appl. Physiol. 2013, 114:1253-1263.
4. van den Borst B., Gosker H.R., Schols A.M. Central fat and peripheral muscle: partners in crime in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2013, 187:8-13.
5. Natanek S.A., Gosker H.R., Slot I.G., Marsh G.S., Hopkinson N.S., Man W.D., Tal-Singer R., Moxham J., Kemp P.R., Schols N.M., Polkey M.I. Heterogeneity of quadriceps muscle phenotype in chronic obstructive pulmonary disease (COPD); implications for stratified medicine?. Muscle Nerve 2013, 48:488-497.
6. 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.
7. 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.
8. Green H.J., Bombardier E., Burnett M., Iqbal S., D'Arsigny C.L., O'Donnell D.E., Ouyang J., Webb K.A. Organization of metabolic pathways in vastus lateralis of patients with chronic obstructive pulmonary disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R935-R941.
9. 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.
10. Luquet S., Lopez-Soriano J., Holst D., Fredenrich A., Melki J., Rassoulzadegan M., Grimaldi P.A. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J. 2003, 17:2299-2301.
11. Macnee W. Systemic inflammatory biomarkers and co-morbidities of chronic obstructive pulmonary disease. Ann. Med. 2013, 45:291-300.
12. 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.
13. Remels A.H., Gosker H.R., Bakker J., Guttridge D.C., Schols A.M., Langen R.C. Regulation of skeletal muscle oxidative phenotype by classical NF-kappaB signalling. Biochim. Biophys. Acta 2013, 1832:1313-1325.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. van den Borst B., Slot I.G., Hellwig V.A., Vosse B.A., Kelders M.C., Barreiro E., Schols A.M., Gosker H.R. Loss of quadriceps muscle oxidative phenotype and decreased endurance in patients with mild-to-moderate COPD. J. Appl. Physiol. 2013, 114:1319-1328.
21. Altman D.G., Gore S.M., Gardner M.J., Pocock S.J. Statistical guidelines for contributors to medical journals. Br. Med. J. (Clin. Res. Ed.) 1983, 286:1489-1493.
22. 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.
23. 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.
24. Rowe G.C., Patten I.S., Zsengeller Z.K., El-Khoury R., Okutsu M., Bampoh S., Koulisis N., Farrell C., Hirshman M.F., Yan Z., Goodyear L.J., Rustin P., Arany Z. Disconnecting mitochondrial content from respiratory chain capacity in PGC-1-deficient skeletal muscle. Cell Rep. 2013, 3:1449-1456.
25. Rao N.A., McCalman M.T., Moulos P., Francoijs K.J., Chatziioannou A., Kolisis F.N., Alexis M.N., Mitsiou D.J., Stunnenberg H.G. Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res. 2011, 21:1404-1416.
26. Schneider G., Kramer O.H. NFkappaB/p53 crosstalk-a promising new therapeutic target. Biochim. Biophys. Acta 2011, 1815:90-103.
27. Gu L., Zhu N., Findley H.W., Woods W.G., Zhou M. Identification and characterization of the IKKalpha promoter: positive and negative regulation by ETS-1 and p53, respectively. J. Biol. Chem. 2004, 279:52141-52149.
28. Marinari B., Ballaro C., Koster M.I., Giustizieri M.L., Moretti F., Crosti F., Papoutsaki M., Karin M., Alema S., Chimenti S., Roop D.R., Costanzo A. IKKalpha is a p63 transcriptional target involved in the pathogenesis of ectodermal dysplasias. J. Invest. Dermatol. 2009, 129:60-69.
29. Saleem A., Carter H.N., Iqbal S., Hood D.A. Role of p53 within the regulatory network controlling muscle mitochondrial biogenesis. Exerc. Sport Sci. Rev. 2011, 39:199-205.
30. Li T., Morgan M.J., Choksi S., Zhang Y., Kim Y.S., Liu Z.G. MicroRNAs modulate the noncanonical transcription factor NF-kappaB pathway by regulating expression of the kinase IKKalpha during macrophage differentiation. Nat. Immunol. 2010, 11:799-805.
31. Biggar K.K., Dubuc A., Storey K. MicroRNA regulation below zero: differential expression of miRNA-21 and miRNA-16 during freezing in wood frogs. Cryobiology 2009, 59:317-321.
32. Hamrick M.W., Herberg S., Arounleut P., He H.Z., Shiver A., Qi R.Q., Zhou L., Isales C.M., Mi Q.S. The adipokine leptin increases skeletal muscle mass and significantly alters skeletal muscle miRNA expression profile in aged mice. Biochem. Biophys. Res. Commun. 2010, 400:379-383.
33. Morin P., Dubuc A., Storey K.B. Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochim. Biophys. Acta 2008, 1779:628-633.
34. Pauley K.M., Satoh M., Chan A.L., Bubb M.R., Reeves W.H., Chan E.K. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res. Ther. 2008, 10:R101.
35. Pandis I., Ospelt C., Karagianni N., Denis M.C., Reczko M., Camps C., Hatzigeorgiou A.G., Ragoussis J., Gay S., Kollias G. Identification of microRNA-221/222 and microRNA-323-3p association with rheumatoid arthritis via predictions using the human tumour necrosis factor transgenic mouse model. Ann. Rheum. Dis. 2012, 71:1716-1723.
36. Shin V.Y., Jin H., Ng E.K., Cheng A.S., Chong W.W., Wong C.Y., Leung W.K., Sung J.J., Chu K.M. NF-kappaB targets miR-16 and miR-21 in gastric cancer: involvement of prostaglandin E receptors. Carcinogenesis 2011, 32:240-245.
37. Bakkar N., Guttridge D.C. NF-kappaB signaling: a tale of two pathways in skeletal myogenesis. Physiol. Rev. 2010, 90:495-511.
38. Bakkar N., Wang J., Ladner K.J., Wang H., Dahlman J.M., Carathers M., Acharyya S., Rudnicki M.A., Hollenbach A.D., Guttridge D.C. IKK/NF-kappaB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis. J. Cell Biol. 2008, 180:787-802.
39. Shembade N., Pujari R., Harhaj N.S., Abbott D.W., Harhaj E.W. The kinase IKKalpha inhibits activation of the transcription factor NF-kappaB by phosphorylating the regulatory molecule TAX1BP1. Nat. Immunol. 2011, 12:834-843.
40. Lin J., Handschin C., Spiegelman B.M. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005, 1:361-370.
41. 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.
42. Allaire J., Maltais F., Doyon J.F., Noel M., LeBlanc P., Carrier G., Simard C., Jobin J. Peripheral muscle endurance and the oxidative profile of the quadriceps in patients with COPD. Thorax 2004, 59:673-678.
43. Gosker H.R., Zeegers M.P., Wouters E.F., Schols A.M. Muscle fibre type shifting in the vastus lateralis of patients with COPD is associated with disease severity: a systematic review and meta-analysis. Thorax 2007, 62:944-949.
44. 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.