Inhibition of the IKK/NF-B pathway by AAV gene transfer improves muscle regeneration in older mdx mice

Gene Therapy

Volumn 17, Issue 12, 2010, Pages 1476-1483

  Tang, Y ^a   Reay, D P ^a   Salay, M N ^a   Mi, M Y ^a   Clemens, P R ^a,b   Guttridge, D C ^c   Robbins, P D ^a   Huard, J ^a   Wang, B ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

AAV; DMD; muscle regeneration; NF B

Indexed keywords

I KAPPA B KINASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PARVOVIRUS VECTOR; PHOSPHATE BUFFERED SALINE;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DUCHENNE MUSCULAR DYSTROPHY; ENZYME ACTIVATION; ENZYME INHIBITION; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; GENE SILENCING; GENE TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MUSCLE NECROSIS; MUSCLE REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIBIALIS ANTERIOR MUSCLE; TREATMENT DURATION; VIRAL GENE DELIVERY SYSTEM; WILD TYPE;

ANIMALS; CELL NUCLEUS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; I-KAPPA B KINASE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; NF-KAPPA B; REGENERATION; SIGNAL TRANSDUCTION;

MURINAE; MUS;

EID: 78650027468     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2010.110     Document Type: Article

References (39)

1. Hoffman EP, Monaco AP, Feener CC, Kunkel LM. Conservation of the Duchenne muscular dystrophy gene in mice and humans. Science 1987; 238: 347-350.
2. Lapidos KA, Kakkar R, McNally EM. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 2004; 94: 1023-1031.
3. Bonilla E, Samitt CE, Miranda AF, Hays AP, Salviati G, DiMauro S et al. Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface. Cell 1988; 54: 447-452.
4. Koenig M, Kunkel LM. Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem 1990; 265: 4560-4566.
5. Koenig M, Monaco AP, Kunkel LM. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 1988; 53: 219-228.
6. Miranda AF, Francke U, Bonilla E, Martucci G, Schmidt B, Salviati G et al. Dystrophin immunocytochemistry in muscle culture: detection of a carrier of Duchenne muscular dystrophy. Am J Med Genet 1989; 32: 268-273.
7. Senter L, Luise M, Presotto C, Betto R, Teresi A, Ceoldo S et al. Interaction of dystrophin with cytoskeletal proteins: binding to talin and actin. Biochem Biophys Res Commun 1993; 192: 899-904.
8. McLoon LK. Focusing on fibrosis: halofuginone-induced functional improvement in the mdx mouse model of Duchenne muscular dystrophy. Am J Physiol Heart Circ Physiol 2008; 294: H1505-H1507.
9. Gregorevic P, Allen JM, Minami E, Blankinship MJ, Haraguchi M, Meuse L et al. rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat Med 2006; 12: 787-789.
10. Yue Y, Liu M, Duan D. C-terminal-truncated microdystrophin recruits dystrobrevin and syntrophin to the dystrophin-asso-ciated glycoprotein complex and reduces muscular dystrophy in symptomatic utrophin/dystrophin double-knockout mice. Mol Ther 2006; 14: 79-87.
11. Wang B, Li J, Fu FH, Xiao X. Systemic human minidystrophin gene transfer improves functions and life span of dystrophin and dystrophin/utrophin-deficient mice. J Orthop Res 2009; 27: 421-426.
12. Roman-Blas JA, Jimenez SA. NF-kappaB as a potential therapeutic target in osteoarthritis and rheumatoid arthritis. Osteoarthr Cartil 2006; 14: 839-848.
13. Hayden MS, Ghosh S. Signaling to NF-κB. Genes Dev 2004; 18: 2195-2224.
14. Peters RT, Maniatis T. A new family of IKK-related kinases may function as I kappa B kinase kinases. Biochim Biophys Acta 2001; 1471: M57-M62.
15. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 2000; 18: 621-663.
16. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol 2002; 2: 725-734.
17. Messina S, Bitto A, Aguennouz M, Minutoli L, Monici MC, Altavilla D et al. Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in Mdx mice. Exp Neurol 2006; 198: 234-241.
18. Ladner KJ, Caligiuri MA, Guttridge DC. 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.
19. Kumar A, Boriek AM. 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.
20. Baghdiguian S, Richard I, Martin M, Coopman P, Beckmann JS, Mangeat P et al. 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.
21. Bakkar N, Wang J, Ladner KJ, Wang H, Dahlman JM, Carathers M et al. IKK/NF-kappaB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mito-chondrial biogenesis. J Cell Biol 2008; 180: 787-802.
22. Acharyya S, Villalta SA, Bakkar N, Bupha-Intr T, Janssen PM, Carathers M et al. Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest 2007; 117: 889-901.
23. Wang B, Li J, Xiao X. Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. Proc Natl Acad Sci USA 2000; 97: 13714-13719.
24. Watchko J, O'Day T, Wang B, Zhou L, Tang Y, Li J et al. Adeno-associated virus vector-mediated minidystrophin gene therapy improves dystrophic muscle contractile function in mdx mice. Hum Gene Ther 2002; 13: 1451-1460.
25. Wang Z, Kuhr CS, Allen JM, Blankinship M, Gregorevic P, Chamberlain JS et al. Sustained AAV-mediated dystrophin expression in a canine Model of Duchenne muscular dystrophy with a brief course of immunosuppression. Mol Ther 2007; 15: 1160-1166.
26. Heslop L, Morgan JE, Partridge TA. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 2000; 113 (Pt 12): 2299-2308.
27. Anderson JE. The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander. J Exp Biol 2006; 209: 2276-2292.
28. Carlson CG, 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.
29. Tas SW, Adriaansen J, Hajji N, Bakker AC, Firestein GS, Vervoordeldonk MJ et al. Amelioration of arthritis by intraarti-cular dominant negative Ikk beta gene therapy using adeno-associated virus type 5. Hum Gene Ther 2006; 17: 821-832.
30. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989; 244: 1578-1580.
31. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 1984; 81: 1189-1192.
32. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989; 244: 1578-1580.
33. Torres LF, Duchen LW. The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain 1987; 110 (Pt 2): 269-299.
34. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25: 280-288.
35. Demoule A, Divangahi M, Yahiaoui L, Danialou G, Gvozdic D, Labbe K et al. Endotoxin triggers nuclear factor-kappaB-dependent up-regulation of multiple proinflammatory genes in the diaphragm. Am J Respir Crit Care Med 2006; 174: 646-653.
36. Xiao X, Li J, Samulski RJ. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J Virol 1998; 72: 2224-2232.
37. Wang B, Li J, Qiao C, Chen C, Hu P, Zhu X et al. A canine minidystrophin is functional and therapeutic in mdx mice. Gene Ther 2008; 15: 1099-1106.
38. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin Jr AS. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 1999; 19: 5785-5799.
39. Straub V, Rafael JA, Chamberlain JS, Campbell KP. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J Cell Biol 1997; 139: 375-385.