Interplay of IKK/NF-κB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy

Journal of Clinical Investigation

Volumn 117, Issue 4, 2007, Pages 889-901

  Acharyya, Swarnali ^a   Villalta, S Armando ^b   Bakkar, Nadine ^a   Bupha Intr, Tepmanas ^a   Janssen, Paul M L ^a   Carathers, Micheal ^a   Li, Zhi Wei ^c   Beg, Amer A ^c   Ghosh, Sankar ^d   Sahenk, Zarife ^e   Weinstein, Michael ^a   Gardner, Katherine L ^a   Rafael Fortney, Jill A ^a   Karin, Michael ^f   Tidball, James G ^b   Baldwin, Albert S ^g   Guttridge, Denis C ^a,h  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^d YALE UNIVERSITY   (United States)

^e THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF NORTH CAROLINA   (United States)

^h OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG TARGETING; DUCHENNE MUSCULAR DYSTROPHY; INFLAMMATION; MACROPHAGE; MOUSE; MUSCLE ATROPHY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TISSUE NECROSIS;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE DELETION; HUMANS; I-KAPPA B KINASE; MACROPHAGES; MICE; MICE, KNOCKOUT; MUSCLE FIBERS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; NF-KAPPA B; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA;

EID: 34147122660     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI30556     Document Type: Article

References (54)

1. Blake, D.J., Weir, A., Newey, S.E., and Davies, K.E. 2002. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82:291-329.
2. Emery, A.E. 2002. The muscular dystrophies. Lancet. 359:687-695.
3. Dalkilic, I., and Kunkel, L.M. 2003. Muscular dystrophies: genes to pathogenesis. Curr. Opin. Genet. Dev. 13:231-238.
4. Durbeej, M., and Campbell, K.P. 2002. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr. Opin. Genet. Dev. 12:349-361.
5. Gorospe, J.R., Tharp, M.D., Hinckley, J., Kornegay, J.N., and Hoffman, E.P. 1994. A role for mast cells in the progression of Duchenne muscular dystrophy? Correlations in dystrophin-deficient humans, dogs, and mice. J. Neurol. Sci. 122:44-56.
6. Tidball, J.G. 2005. Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:R345-R353.
7. Porreca, E., et al. 1999. Haemostatic abnormalities, cardiac involvement and serum tumor necrosis factor levels in X-linked dystrophic patients. Thromb. Haemost. 81:543-546.
8. Porter, J.D., et al. 2002. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 11:263-272.
9. Hayden, M.S., and Ghosh, S. 2004. Signaling to NF-kappaB. Genes Dev. 18:2195-2224.
10. Li, Q., Withoff, S., and Verma, I.M. 2005. Inflammation-associated cancer: NF-kappaB is the lynchpin. Trends Immunol. 26:318-325.
11. Karin, M., and Ben-Neriah, Y. 2000. Phosphorylation meets ubiquitination: the control of NF-kappaB activity. Annu. Rev. Immunol. 18:621-663.
12. Baldwin, A.S., Jr. 2001. Series introduction: the transcription factor NF-κB and human disease. J. Clin. Invest. 107:3-6.
13. Karin, M., Cao, Y., Greten, F.R., and Li, Z.W. 2002. NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer. 2:301-310.
14. Cai, D., et al. 2004. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell. 119:285-298.
15. Hunter, R.B., and Kandarian, S.C. 2004. Disruption of either the Nfkb1 or the Bcl3 gene inhibits skeletal muscle atrophy. J. Clin. Invest. 114:1504-1511. doi:10.1172/JCI200421696.
16. Baghdiguian, S., et al. 1999. 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. 5:503-511.
17. Monici, M.C., Aguennouz, M., Mazzeo, A., Messina, C., and Vita, G. 2003. Activation of nuclear factor-kappaB in inflammatory myopathies and Duchenne muscular dystrophy. Neurology. 60:993-997.
18. Kumar, A., and Boriek, A.M. 2003. Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J. 17:386-396.
19. Deconinck, A.E., et al. 1997. Utrophin-dystrophindeficient mice as a model for Duchenne muscular dystrophy. Cell. 90:717-727.
20. Sasaki, C.Y., Barberi, T.J., Ghosh, P., and Longo, D.L. 2005. Phosphorylation of RelA/p65 on serine 536 defines an IkappaBalpha-independent NFkappaB pathway. J. Biol. Chem. 280:34538-34547.
21. Carlsen, H., Moskaug, J.O., Fromm, S.H., and Blomhoff, R. 2002. In vivo imaging of NF-kappa B activity. J. Immunol. 168:1441-1446.
22. Beg, A.A., Sha, W.C., Bronson, R.T., Ghosh, S., and Baltimore, D. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature. 376:167-170.
23. Sha, W.C., Liou, H.C., Tuomanen, E.I., and Baltimore, D. 1995. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell. 80:321-330.
24. Doi, T.S., et al. 1999. Absence of tumor necrosis factor rescues RelA-deficient mice from embryonic lethality. Proc. Natl. Acad. Sci. U. S. A. 96:2994-2999.
25. Spencer, M.J., Marino, M.W., and Winckler, W.M. 2000. Altered pathological progression of diaphragm and quadriceps muscle in TNF-deficient, dystrophin-deficient mice. Neuromuscul. Disord. 10:612-619.
26. Khurana, T.S., and Davies, K.E. 2003. Pharmacological strategies for muscular dystrophy. Nat. Rev. Drug Discov. 2:379-390.
27. Charge, S.B., and Rudnicki, M.A. 2004. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84:209-238.
28. Guttridge, D.C., Albanese, C., Reuther, J.Y., Pestell, R.G., and Baldwin, A.S., Jr. 1999. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell. Biol. 19:5785-5799.
29. Li, Z.W., Omori, S.A., Labuda, T., Karin, M., and Rickert, R.C. 2003. IKK beta is required for peripheral B cell survival and proliferation. J. Immunol. 170:4630-4637.
30. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R., and Forster, I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265-277.
31. Sakurai, H., Chiba, H., Miyoshi, H., Sugita, T., and Toriumi, W. 1999. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 274:30353-30356.
32. Bothe, G.W., Haspel, J.A., Smith, C.L., Wiener, H.H., and Burden, S.J. 2000. Selective expression of Cre recombinase in skeletal muscle fibers. Genesis. 26:165-166.
33. Jiang, P., et al. 2002. Targeted deletion of the MLC1f/3f downstream enhancer results in precocious MLC expression and mesoderm ablation. Dev. Biol. 243:281-293.
34. 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.
35. Sherwood, R.I., et al. 2004. Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell. 119:543-554.
36. Montarras, D., et al. 2005. Direct isolation of satellite cells for skeletal muscle regeneration. Science. 309:2064-2067.
37. May, M.J., et al. 2000. Selective inhibition of NFkappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science. 289:1550-1554.
38. di Meglio, P., Ianaro, A., and Ghosh, S. 2005. Amelioration of acute inflammation by systemic administration of a cell-permeable peptide inhibitor of NF-kappaB activation. Arthritis Rheum. 52:951-958.
39. Lynch, G.S., et al. 1997. Contractile properties of diaphragm muscle segments from old mdx and old transgenic mdx mice. Am. J. Physiol. 272:C2063-C2068.
40. Mourkioti, F., et al. 2006. Targeted ablation of IKK2 improves skeletal muscle strength, maintains mass, and promotes regeneration. J. Clin. Invest. 116:2945-2954. doi:10.1172/JCI28721.
41. Thaloor, D., Miller, K.J., Gephart, J., Mitchell, P.O., and Pavlath, G.K. 1999. Systemic administration of the NF-kappaB inhibitor curcumin stimulates muscle regeneration after traumatic injury. Am. J. Physiol. 277:C320-C329.
42. Greten, F.R., et al. 2004. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 118:285-296.
43. Li, Q., et al. 2005. Enhanced NF-kappaB activation and cellular function in macrophages lacking IkappaB kinase 1 (IKK1). Proc. Natl. Acad. Sci. U. S. A. 102:12425-12430.
44. Bonuccelli, G., et al. 2003. Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and membrane localization of dystrophin and dystrophin-associated proteins. Am. J. Pathol. 163:1663-1675.
45. Messina, S., et al. 2006. Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in Mdx mice. Exp. Neurol. 198:234-241.
46. Sprong, R.C., et al. 1998. Low-dose N-acetylcysteine protects rats against endotoxin-mediated oxidative stress, but high-dose increases mortality. Am. J. Respir. Crit. Care Med. 157:1283-1293.
47. Jimi, E., et al. 2004. Selective inhibition of NFkappa B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat. Med. 10:617-624.
48. Lavon, I., et al. 2000. High susceptibility to bacterial infection, but no liver dysfunction, in mice compromised for hepatocyte NF-kappaB activation. Nat. Med. 6:573-577.
49. Acharyya, S., et al. 2005. Dystrophin glycoprotein complex dysfunction: a regulatory link between muscular dystrophy and cancer cachexia. Cancer Cell. 8:421-432.
50. Straub, V., Rafael, J.A., Chamberlain, J.S., and Campbell, K.P. 1997. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol. 139:375-385.
51. Jankowski, R.J., Haluszczak, C., Trucco, M., and Huard, J. 2001. Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells. Hum. Gene Ther. 12:619-628.
52. Acharyya, S., et al. 2004. Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J. Clin. Invest. 114:370-378. doi:10.1172/JCI200420174.
53. Rando, T.A., and Blau, H.M. 1994. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125:1275-1287.
54. Asakura, A., Komaki, M., and Rudnicki, M. 2001. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 68:245-253.