Hsp72 preserves muscle function and slows progression of severe muscular dystrophy

Nature

Volumn 484, Issue 7394, 2012, Pages 394-398

  Gehrig, Stefan M ^a   Van Der Poel, Chris ^a,e   Sayer, Timothy A ^a   Schertzer, Jonathan D ^a,f   Henstridge, Darren C ^b   Church, Jarrod E ^a,e   Lamon, Severine ^c   Russell, Aaron P ^c   Davies, Kay E ^d   Febbraio, Mark A ^b   Lynch, Gordon S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e LA TROBE UNIVERSITY   (Australia)

^f MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 72; O (2 HYDROXY 3 PIPERIDINOPROPYL)NICOTINIC AMIDOXIME; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

CALCIUM; DEVELOPMENTAL BIOLOGY; DIABETES; DRUG; GENE EXPRESSION; ION; MUSCLE; MUTATION; PATHOLOGY; PROTEIN; RODENT;

ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DIAPHRAGM MUSCLE; DISEASE COURSE; DISEASE SEVERITY; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE STRENGTH; MUSCULAR DYSTROPHY; NONHUMAN; PATHOPHYSIOLOGY; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CALCIUM-TRANSPORTING ATPASES; DIAPHRAGM; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; HSP72 HEAT-SHOCK PROTEINS; KYPHOSIS; LONGEVITY; MALE; MICE; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; OXIMES; PIPERIDINES; RATS;

MUS;

EID: 84859910158     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10980     Document Type: Article

References (44)

1. Emery, A. E. The muscular dystrophies. Lancet 359, 687-695 (2002). (Pubitemid 34203773)
2. Ervasti, J. M. & Campbell, K. P. Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131 (1991). (Pubitemid 121001402)
3. Koenig, M., Monaco, A. P. & Kunkel, L. M. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53, 219-228 (1988).
4. Blake, D. J.,Weir, A.,Newey, S. E.&Davies, K. E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82, 291-329 (2002). (Pubitemid 34654455)
5. Straub, V., Rafael, J. A., Chamberlain, J. S. & Campbell, K. P. Animal models for muscular dystrophy showdifferent patterns of sarcolemmal disruption. J. Cell Biol. 139, 375-385 (1997). (Pubitemid 27459311)
6. Turner, P. R., Westwood, T., Regen, C. M. & Steinhardt, R. A. Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335, 735-738 (1988).
7. Grady, R. M. et al. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: amodel for Duchennemuscular dystrophy. Cell 90, 729-738 (1997). (Pubitemid 27357964)
8. Deconinck, A. E. et al. Utrophin-dystrophin-deficientmice as amodel forDuchenne muscular dystrophy. Cell 90, 717-727 (1997). (Pubitemid 27357963)
9. Gervasio, O. L., Whitehead, N. P., Yeung, E. W., Phillips, W. D. & Allen, D. G. TRPC1 binds to caveolin-3 and is regulated by Src kinase-role in Duchenne muscular dystrophy. J. Cell Sci. 121, 2246-2255 (2008).
10. Fong, P. Y., Turner, P. R., Denetclaw, W. F. & Steinhardt, R. A. Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250, 673-676 (1990). (Pubitemid 120034287)
11. Bellinger, A. M. et al. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nature Med. 15, 325-330 (2009).
12. Nicolas-Metral, V., Raddatz, E., Kucera, P. & Ruegg, U. T. Mdx myotubes have normal excitability but show reduced contraction-relaxation dynamics. J. Muscle Res. Cell Motil. 22, 69-75 (2001). (Pubitemid 32831639)
13. Tutdibi, O., Brinkmeier, H., Rudel, R. & Fohr, K. J. Increased calcium entry into dystrophin-deficient muscle fibres of MDX and ADR-MDX mice is reduced by ion channel blockers. J. Physiol. (Lond.) 515, 859-868 (1999). (Pubitemid 29140118)
14. Goonasekera, S. A. et al. Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. J. Clin. Invest. 121, 1044-1052 (2011).
15. Morine, K. J., Sleeper, M. M., Barton, E. R. & Sweeney, H. L. Overexpression of SERCA1a in the mdx diaphragm reduces susceptibility to contraction-induced damage. Hum. Gene Ther. 12, 1735-1739 (2010).
16. Porter, J. D. et al. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 11, 263-272 (2002). (Pubitemid 34173355)
17. Acharyya, S. et al. Interplay of IKK/NF-kB signaling inmacrophages andmyofibres promotes muscle degeneration in Duchenne muscular dystrophy. J. Clin. Invest. 117, 889-901 (2007). (Pubitemid 46556745)
18. Kolodziejczyk, S. M. et al. Activation of JNK1 contributes to dystrophic muscle pathogenesis. Curr. Biol. 11, 1278-1282 (2001). (Pubitemid 32774085)
19. Monici, M. C., Aguennouz, M.,Mazzeo, A.,Messina, C.&Vita, G. Activation of nuclear factor-kB in inflammatory myopathies and Duchenne muscular dystrophy. Neurology 60, 993-997 (2003). (Pubitemid 36348934)
20. Senf, S. M., Dodd, S. L., McClung, J. M.& Judge, A. R. Hsp70 overexpression inhibits NF-kB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J. 22, 3836-3845 (2008).
21. Park, H. S., Lee, J. S., Huh, S. H., Seo, J. S. & Choi, E. J. Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J. 20, 446-456 (2001).
22. Chung, J. et al. HSP72 protects against obesity-induced insulin resistance. Proc. Natl Acad. Sci. USA 105, 1739-1744 (2008). (Pubitemid 351346584)
23. Tupling, A. R. et al. HSP70 binds to the fast-twitch skeletal muscle sarco(endo)plasmic reticulum Ca21-ATPase (SERCA1a) and prevents thermal inactivation. J. Biol. Chem. 279, 52382-52389 (2004). (Pubitemid 39656615)
24. Bornman, L., Polla, B. S., Lotz, B. P.& Gericke, G. S. Expression of heat-shock/stress proteins in Duchenne muscular dystrophy. Muscle Nerve 18, 23-31 (1995).
25. Lou, J. S., Weiss, M. D. & Carter, G. T. Assessment and management of fatigue in neuromuscular disease. Am. J. Hosp. Palliat. Care 27, 145-157 (2010).
26. Finsterer, J. Cardiopulmonary support in Duchenne muscular dystrophy. Lung 184, 205-215 (2006). (Pubitemid 44477406)
27. Stedman, H. H. et al. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352, 536-539 (1991).
28. Briguet, A., Courdier-Fruh, I., Foster, M., Meier, T. & Magyar, J. P. Histological parameters for the quantitative assessment of muscular dystrophy in the mdxmouse. Neuromuscul. Disord. 14, 675-682 (2004). (Pubitemid 39194668)
29. Literati-Nagy, B. et al. Improvement of insulin sensitivity by a novel drug, BGP-15, in insulin-resistant patients: a proof of concept randomized double-blind clinical trial. Horm. Metab. Res. 41, 374-380 (2009).
30. Morimoto, R. I. Cells in stress: transcriptional activation of heat shock genes. Science 259, 1409-1410 (1993). (Pubitemid 23101373)
31. Marber, M. S. et al. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J. Clin. Invest. 95, 1446-1456 (1995).
32. Taleb, M. et al. Hsp70 inhibits aminoglycoside-induced hair cell death and is necessary for the protective effect of heat shock. J. Assoc. Res. Otolaryngol. 9, 277-289 (2008).
33. Literati-Nagy, B. et al. Beneficial effect of the insulin sensitizer (HSP inducer) BGP-15 on olanzapine-induced metabolic disorders. Brain Res. Bull. 20, 340-344 (2010).
34. Saegusa, Y. & Tabata, H. Usefulness of infrared thermometry in determining body temperature in mice. J. Vet. Med. Sci. 65, 1365-1367 (2003). (Pubitemid 41365440)
35. Gregorevic, P., Plant, D. R., Leeding, K. S., Bach, L. A. & Lynch, G. S. Improved contractile function of themdx dystrophicmouse diaphragmmuscle after insulinlike growth factor-I administration. Am. J. Pathol. 161, 2263-2272 (2002). (Pubitemid 35434870)
36. Schertzer, J. D., Ryall, J. G.&Lynch, G. S. Systemic administration of IGF-I enhances oxidative status andreduces contraction-induced injury in skeletalmuscles ofmdx dystrophic mice. Am. J. Physiol. 291, 499-505 (2006).
37. Schertzer, J. D., Gehrig, S. M., Ryall, J. G. & Lynch, G. S. Modulation of insulin-like growth factor (IGF)-I and IGF-binding protein interactions enhances skeletal muscle regeneration andameliorates the dystrophic pathology inmdx mice.Am. J. Pathol. 171, 1180-1188 (2007). (Pubitemid 47582892)
38. Gehrig, S. M., Koopman, R., Naim, T., Tjoakarfa, C.& Lynch, G. S. Making fast-twitch dystrophic muscles bigger protects them from contraction injury and attenuates the dystrophic pathology. Am. J. Pathol. 176, 29-33 (2010).
39. Briguet, A., Courdier-Fruh, I., Foster, M., Meier, T. & Magyar, J. P. Histological parameters for the quantitative assessment of muscular dystrophy in the mdxmouse. Neuromuscul. Disord. 14, 675-682 (2004). (Pubitemid 39194668)
40. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).
41. Schertzer, J. D. et al. b2-Agonist administration increases sarcoplasmic reticulum Ca21-ATPase activity in aged rat skeletal muscle. Am. J. Physiol. 288, 526-533 (2005).
42. Plant, D. R. & Lynch, G. S. Depolarization-induced contraction and SR function in mechanically skinnedmuscle fibres fromdystrophicmdx mice.Am. J. Physiol. 285, C522-C528 (2003). (Pubitemid 37022049)
43. Murphy, K. T. et al. Antibody-directed myostatin inhibition in 21-mo-old mice reveals novel roles for myostatin signaling in skeletal muscle structure and function. FASEB J. 24, 4433-4442 (2010).
44. Green, M. C. A rapid method for clearing and staining specimens for the demonstration of bone. Ohio J. Sci. 52, 31-33 (1952).