Skeletal Muscle Diseases, Inflammation, and NF-κB Signaling: Insights and Opportunities for Therapeutic Intervention

REFERENCES

• Perkins N. D. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 2007; 8: 49–62
   PubMed Web of Science ®Google Scholar
• Baldwin A. S., Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 1996; 14: 649–683
   PubMed Web of Science ®Google Scholar
• Hayden M. S., Ghosh S. Signaling to NF-kappaB. Genes Dev 2004; 18: 2195–2224
   PubMed Web of Science ®Google Scholar
• Hayden M. S., Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008; 132: 344–362
   PubMed Web of Science ®Google Scholar
• Blake D. J., Weir A., Newey S. E., Davies K. E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 2002; 82: 291–329
   PubMed Web of Science ®Google Scholar
• Durbeej M., Campbell K. P. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 2002; 12: 349–361
   PubMed Web of Science ®Google Scholar
• Lapidos K. A., Kakkar R., McNally E. M. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 2004; 94: 1023–1031
   PubMed Web of Science ®Google Scholar
• Acharyya S., Villalta S. A., Bakkar N., Bupha-Intr T., Janssen P. M., Carathers M., Li Z. W., Beg A. A., Ghosh S., Sahenk Z., Weinstein M., Gardner K. L., Rafael-Fortney J. A., Karin M., Tidball J. G., Baldwin A. S., Guttridge D. C. Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest 2007; 117: 889–901
   PubMed Web of Science ®Google Scholar
• Messina S., Altavilla D., Aguennouz M., Seminara P., Minutoli L., Monici M. C., Bitto A., Mazzeo A., Marini H., Squadrito F., Vita G. Lipid peroxidation inhibition blunts nuclear factor-kappaB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am J Pathol 2006; 168: 918–926
   Google Scholar
• Haslbeck K. M., Friess U., Schleicher E. D., Bierhaus A., Nawroth P. P., Kirchner A., Pauli E., Neundorfer B., Heuss D. The RAGE pathway in inflammatory myopathies and limb girdle muscular dystrophy. Acta Neuropathol 2005; 110: 247–254
   Google Scholar
• Monici M. C., Aguennouz M., Mazzeo A., Messina C., Vita G. Activation of nuclear factor-kappaB in inflammatory myopathies and Duchenne muscular dystrophy. Neurology 2003; 60: 993–997
   PubMed Web of Science ®Google Scholar
• Kumar A., Boriek A. M. Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J 2003; 17: 386–396
   PubMed Web of Science ®Google Scholar
• Guttridge D. C., Albanese C., Reuther J. Y., Pestell R. G., Baldwin A. S., Jr. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 1999; 19: 5785–5799
   PubMed Web of Science ®Google Scholar
• Lehtinen S. K., Rahkila P., Helenius M., Korhonen P., Salminen A. Down-regulation of transcription factors AP-1, Sp-1, and NF-kappa B precedes myocyte differentiation. Biochem Biophys Res Commun 1996; 229: 36–43
   PubMed Web of Science ®Google Scholar
• Cai D., Frantz J. D., Tawa N. E., Jr., Melendez P. A., Oh B.-C., Lidov W. R., Hasselgren P. O., Frontera W. R., Lee J., Glass D. J., Shoelson S. E. IKKbeta/NF-kB activation causes severe muscle wasting in mice. Cell 2004; 119: 285–298
   PubMed Web of Science ®Google Scholar
• Guttridge D. C., Mayo M. W., Madrid L. V., Wang C.-Y., Baldwin A. S., Jr. NF-kB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 2000; 289: 2363–2366
   PubMed Web of Science ®Google Scholar
• Ladner K. J., Caligiuri M. A., Guttridge D. C. Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products. J Biol Chem 2003; 278: 2294–2303
   PubMedGoogle Scholar
• Sitcheran R., Cogswell P. C., Baldwin A. S., Jr. NF-kappaB mediates inhibition of mesenchymal cell differentiation through a posttranscriptional gene silencing mechanism. Genes Dev 2003; 17: 2368–2373
   PubMedGoogle Scholar
• Wang H., Hertlein E., Bakkar N., Sun H., Acharyya S., Wang J., Carathers M., Davuluri R., Guttridge D. C. NF-kappaB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol 2007; 27: 4374–4387
   PubMed Web of Science ®Google Scholar
• Mourkioti F., Kratsios P., Luedde T., Song Y. H., Delafontaine P., Adami R., Parente V., Bottinelli R., Pasparakis M., Rosenthal N. Targeted ablation of IKK2 improves skeletal muscle strength, maintains mass, and promotes regeneration. J Clin Invest 2006; 116: 2945–2954
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Spencer M. J., Tidball J. G. Do immune cells promote the pathology of dystrophin-deficient myopathies?. Neuromuscul Disord 2001; 11: 556–564
   Google Scholar
• Fujiwara N., Kobayashi K. Macrophages in inflammation. Curr Drug Targets Inflamm Allergy 2005; 4: 281–286
   PubMedGoogle Scholar
• Disatnik M. H., Dhawan J., Yu Y., Beal M. F., Whirl M. M., Franco A. A., Rando T. A. Evidence of oxidative stress in mdx mouse muscle: studies of the pre-necrotic state. J Neurol Sci 1998; 161: 77–84
   PubMed Web of Science ®Google Scholar
• Ragusa R. J., Chow C. K., Porter J. D. Oxidative stress as a potential pathogenic mechanism in an animal model of Duchenne muscular dystrophy. Neuromuscul Disord 1997; 7: 379–386
   PubMedGoogle Scholar
• Rando T. A., Disatnik M. H., Yu Y., Franco A. Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord 1998; 8: 14–21
   PubMed Web of Science ®Google Scholar
• Wehling M., Spencer M. J., Tidball J. G. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 2001; 155: 123–131
   PubMed Web of Science ®Google Scholar
• Baghdiguian S., Martin M., Richard I., Pons F., Astier C., Bourg N., Hay R. T., Chemaly R., Halaby G., Loiselet J., Anderson L. V., Lopez de Munain A., Fardeau M., Mangeat P., Beckmann J. S., Lefranc G. Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A. Nat Med 1999; 5: 503–511
   PubMed Web of Science ®Google Scholar
• Baghdiguian S., Richard I., Martin M., Coopman P., Beckmann J. S., Mangeat P., Lefranc G. Pathophysiology of limb girdle muscular dystrophy type 2A: hypothesis and new insights into the IkappaBalpha/NF-kappaB survival pathway in skeletal muscle. J Mol Med 2001; 79: 254–261
   PubMed Web of Science ®Google Scholar
• Kramerova I., Beckmann J. S., Spencer M. J. Molecular and cellular basis of calpainopathy (limb girdle muscular dystrophy type 2A). Biochim Biophys Acta 2007; 1772: 128–144
   Google Scholar
• Benayoun B., Baghdiguian S., Lajmanovich A., Bartoli M., Daniele N., Gicquel E., Bourg N., Raynaud F., Pasquier M. A., Suel L., Lochmuller H., Lefranc G., Richard I. NF-kappaB-dependent expression of the antiapoptotic factor c-FLIP is regulated by calpain 3, the protein involved in limb-girdle muscular dystrophy type 2A. FASEB J 2008; 22: 1521–1529
   PubMedGoogle Scholar
• Richard I., Roudaut C., Marchand S., Baghdiguian S., Herasse M., Stockholm D., Ono Y., Suel L., Bourg N., Sorimachi H., Lefranc G., Fardeau M., Sebille A., Beckmann J. S. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IkappaBalpha/nuclear factor kappaB pathway perturbation in mice. J Cell Biol 2000; 151: 1583–1590
   PubMed Web of Science ®Google Scholar
• Nagaraju K., Casciola-Rosen L., Lundberg I., Rawat R., Cutting S., Thapliyal R., Chang J., Dwivedi S., Mitsak M., Chen Y. W., Plotz P., Rosen A., Hoffman E., Raben N. Activation of the endoplasmic reticulum stress response in autoimmune myositis: potential role in muscle fiber damage and dysfunction. Arthritis Rheum 2005; 52: 1824–1835
   PubMed Web of Science ®Google Scholar
• Han S. H., Yea S. S., Jeon Y. J., Yang K. H., Kaminski N. E. Transforming growth factor-beta 1 (TGF-beta1) promotes IL-2 mRNA expression through the up-regulation of NF-kappaB, AP-1 and NF-AT in EL4 cells. J Pharmacol Exp Ther 1998; 287: 1105–1112
   PubMedGoogle Scholar
• Vattemi G., Engel W. K., McFerrin J., Askanas V. Endoplasmic reticulum stress and unfolded protein response in inclusion body myositis muscle. Am J Pathol 2004; 164: 1–7
   PubMed Web of Science ®Google Scholar
• Pahl H. L., Baeuerle P. A. The ER-overload response: activation of NF-kappa B. Trends Biochem Sci 1997; 22: 63–67
   PubMed Web of Science ®Google Scholar
• Nogalska A., Wojcik S., Engel W. K., McFerrin J., Askanas V. Endoplasmic reticulum stress induces myostatin precursor protein and NF-kappaB in cultured human muscle fibers: relevance to inclusion body myositis. Exp Neurol 2007; 204: 610–618
   PubMed Web of Science ®Google Scholar
• Bakkar N., Wackerhage H., Guttridge D. C. Myostatin and NF-κ B regulate skeletal myogenesis through distinct signaling pathways. Signal Transduct 2005; 5: 202–210
   Google Scholar
• Bakay M., Wang Z., Melcon G., Schiltz L., Xuan J., Zhao P., Sartorelli V., Seo J., Pegoraro E., Angelini C., Shneiderman B., Escolar D., Chen Y. W., Winokur S. T., Pachman L. M., Fan C., Mandler R., Nevo Y., Gordon E., Zhu Y., Dong Y., Wang Y., Hoffman E. P. Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 2006; 129: 996–1013
   PubMed Web of Science ®Google Scholar
• Chakkalakal J. V., Thompson J., Parks R. J., Jasmin B. J. Molecular, cellular, and pharmacological therapies for Duchenne/Becker muscular dystrophies. FASEB J 2005; 19: 880–891
   PubMed Web of Science ®Google Scholar
• Mastaglia F. L., Garlepp M. J., Phillips B. A., Zilko P. J. Inflammatory myopathies: clinical, diagnostic and therapeutic aspects. Muscle Nerve 2003; 27: 407–425
   PubMed Web of Science ®Google Scholar
• Auphan N., DiDonato J. A., Rosette C., Helmberg A., Karin M. Immunosuppression by glucocorticoids: inhibition of NF-kappa B activity through induction of I kappa B synthesis. Science 1995; 270: 286–290
   PubMed Web of Science ®Google Scholar
• Scheinman R. I., Cogswell P. C., Lofquist A. K., Baldwin A. S., Jr. Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science 1995; 270: 283–286
   PubMed Web of Science ®Google Scholar
• De Bosscher K., Schmitz M. L., Vanden Berghe W., Plaisance S., Fiers W., Haegeman G. Glucocorticoid-mediated repression of nuclear factor-kappaB-dependent transcription involves direct interference with transactivation. Proc Natl Acad Sci USA 1997; 94: 13504–13509
   PubMed Web of Science ®Google Scholar
• De Bosscher K., Vanden Berghe W., Vermeulen L., Plaisance S., Boone E., Haegeman G. Glucocorticoids repress NF-kappaB-driven genes by disturbing the interaction of p65 with the basal transcription machinery, irrespective of coactivator levels in the cell. Proc Natl Acad Sci USA 2000; 97: 3919–3924
   PubMed Web of Science ®Google Scholar
• Gautam S. C., Gao X., Dulchavsky S. Immunomodulation by curcumin. Adv Exp Med Biol 2007; 595: 321–341
   PubMed Web of Science ®Google Scholar
• Jobin C., Bradham C. A., Russo M. P., Juma B., Narula A. S., Brenner D. A., Sartor R. B. Curcumin blocks cytokine-mediated NF-kappa B activation and proinflammatory gene expression by inhibiting inhibitory factor I-kappa B kinase activity. J Immunol 1999; 163: 3474–3483
   PubMed Web of Science ®Google Scholar
• Singh S., Aggarwal B. B. Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane) [corrected]. J Biol Chem 1995; 270: 24995–25000
   PubMed Web of Science ®Google Scholar
• Thaloor D., Miller K. J., Gephart J., Mitchell P. O., Pavlath G. K. Systemic administration of the NF-kappaB inhibitor curcumin stimulates muscle regeneration after traumatic injury. Am J Physiol 1999; 277: C320–329
   PubMed Web of Science ®Google Scholar
• Pan Y., Chen C., Shen Y., Zhu C. H., Wang G., Wang X. C., Chen H. Q., Zhu M. S. Curcumin alleviates dystrophic muscle pathology in mdx mice. Mol Cell 2008; 25: 531–537
   Google Scholar
• Durham W. J., Arbogast S., Gerken E., Li Y. P., Reid M. B. Progressive nuclear factor-kappaB activation resistant to inhibition by contraction and curcumin in mdx mice. Muscle Nerve 2006; 34: 298–303
   Google Scholar
• Goel A., Kunnumakkara A. B., Aggarwal B. B. Curcumin as “curecumin”: from kitchen to clinic. Biochem Pharmacol 2008; 75: 787–809
   PubMed Web of Science ®Google Scholar
• Archer J. D., Vargas C. C., Anderson J. E. Persistent and improved functional gain in mdx dystrophic mice after treatment with L-arginine and deflazacort. Faseb J 2006; 20: 738–740
   Google Scholar
• Barton E. R., Morris L., Kawana M., Bish L. T., Toursel T. Systemic administration of L-arginine benefits mdx skeletal muscle function. Muscle Nerve 2005; 32: 751–760
   PubMed Web of Science ®Google Scholar
• Hnia K., Gayraud J., Hugon G., Ramonatxo M., De La Porte S., Matecki S., Mornet D. L-arginine decreases inflammation and modulates the nuclear Factor-kappaB/matrix metalloproteinase cascade in mdx muscle fibers. Am J Pathol 2008; 172: 1509–1519
   PubMed Web of Science ®Google Scholar
• Carlson C. G., Samadi A., Siegel A. Chronic treatment with agents that stabilize cytosolic IkappaB-alpha enhances survival and improves resting membrane potential in MDX muscle fibers subjected to chronic passive stretch. Neurobiol Dis 2005; 20: 719–730
   PubMed Web of Science ®Google Scholar
• Messina S., Bitto A., Aguennouz M., Minutoli L., Monici M. C., Altavilla D., Squadrito F., Vita G. Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in Mdx mice. Exp Neurol 2006; 198: 234–241
   PubMed Web of Science ®Google Scholar
• Calviello G., Filippi G. M., Toesca A., Palozza P., Maggiano N., Nicuolo F. D., Serini S., Azzena G. B., Galeotti T. Repeated exposure to pyrrolidine-dithiocarbamate induces peripheral nerve alterations in rats. Toxicol Lett 2005; 158: 61–71
   Google Scholar
• Kim C. H., Kim J. H., Xu J., Hsu C. Y., Ahn Y. S. Pyrrolidine dithiocarbamate induces bovine cerebral endothelial cell death by increasing the intracellular zinc level. J Neurochem 1999; 72: 1586–1592
   PubMed Web of Science ®Google Scholar
• Dai S., Hirayama T., Abbas S., Abu-Amer Y. The IkappaB kinase (IKK) inhibitor, NEMO-binding domain peptide, blocks osteoclastogenesis and bone erosion in inflammatory arthritis. J Biol Chem 2004; 279: 37219–37222
   PubMedGoogle Scholar
• Jimi E., Aoki K., Saito H., D'Acquisto F., May M. J., Nakamura I., Sudo T., Kojima T., Okamoto F., Fukushima H., Okabe K., Ohya K., Ghosh S. Selective inhibition of NF-kappa B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat Med 2004; 10: 617–624
   PubMed Web of Science ®Google Scholar
• di Meglio P., Ianaro A., Ghosh S. Amelioration of acute inflammation by systemic administration of a cell-permeable peptide inhibitor of NF-kappaB activation. Arthritis Rheum 2005; 52: 951–958
   PubMed Web of Science ®Google Scholar
• Tas S. W., Vervoordeldonk M. J., Hajji N., May M. J., Ghosh S., Tak P. P. Local treatment with the selective IkappaB kinase beta inhibitor NEMO-binding domain peptide ameliorates synovial inflammation. Arthritis Res Ther 2006; 8: R86
   PubMed Web of Science ®Google Scholar
• Dave S. H., Tilstra J. S., Matsuoka K., Li F., Karrasch T., Uno J. K., Sepulveda A. R., Jobin C., Baldwin A. S., Robbins P. D., Plevy S. E. Amelioration of chronic murine colitis by peptide-mediated transduction of the IkappaB kinase inhibitor NEMO binding domain peptide. J Immunol 2007; 179: 7852–7859
   PubMed Web of Science ®Google Scholar
• Shibata W., Maeda S., Hikiba Y., Yanai A., Ohmae T., Sakamoto K., Nakagawa H., Ogura K., Omata M. Cutting edge: the IkappaB kinase (IKK) inhibitor, NEMO-binding domain peptide, blocks inflammatory injury in murine colitis. J Immunol 2007; 179: 2681–2685
   PubMedGoogle Scholar
• Dasgupta S., Jana M., Zhou Y., Fung Y. K., Ghosh S., Pahan K. Antineuroinflammatory effect of NF-kappaB essential modifier-binding domain peptides in the adoptive transfer model of experimental allergic encephalomyelitis. J Immunol 2004; 173: 1344–1354
   PubMed Web of Science ®Google Scholar
• Ghosh A., Roy A., Liu X., Kordower J. H., Mufson E. J., Hartley D. M., Ghosh S., Mosley R. L., Gendelman H. E., Pahan K. Selective inhibition of NF-kappaB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease. Proc Natl Acad Sci USA 2007; 104: 18754–18759
   PubMed Web of Science ®Google Scholar
• Chapoval S. P., Al-Garawi A., Lora J. M., Strickland I., Ma B., Lee P. J., Homer R. J., Ghosh S., Coyle A. J., Elias J. A. Inhibition of NF-kappaB activation reduces the tissue effects of transgenic IL-13. J Immunol 2007; 179: 7030–7041
   PubMed Web of Science ®Google Scholar
• May M. J., D'Acquisto F., Madge L. A., Glockner J., Pober J. S., Ghosh S. Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science 2000; 289: 1550–1554
   PubMed Web of Science ®Google Scholar