Muscle-specific calpastatin overexpression prevents diaphragm weakness in cecal ligation puncture-induced sepsis

Journal of Applied Physiology

Volumn 117, Issue 8, 2014, Pages 921-929

  Supinski, Gerald S ^a,b   Wang, Lin ^a,b   Song, Xiao Hong ^a,b   Moylan, Jennifer S ^a,b   Callahan, Leigh Ann ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Calpain; Cecal ligation puncture; Diaphragm; Proteolysis; Sepsis

Indexed keywords

CALCIUM BINDING PROTEIN; CALPAIN; CALPASTATIN; MUSCLE PROTEIN; MYOSIN HEAVY CHAIN; TALIN;

ANIMAL; CECUM; DIAPHRAGM; LIGATION; METABOLISM; MOUSE; MUSCLE; MUSCLE WEAKNESS; PATHOLOGY; PROCEDURES; SEPSIS;

ANIMALS; CALCIUM-BINDING PROTEINS; CALPAIN; CECUM; DIAPHRAGM; LIGATION; MICE; MUSCLE PROTEINS; MUSCLE WEAKNESS; MUSCLES; MYOSIN HEAVY CHAINS; SEPSIS; TALIN;

EID: 84908570833     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00975.2013     Document Type: Article

References (41)

1. Ahmad S, Choudhry MA, Sayeed MM. Ca2(+)-dependent and Ca2(+)-independent proteinase contents in the skeletal muscle in septic rats. Shock 5: 247-250, 1996.
2. Callahan LA, Supinski GS. Sepsis-induced myopathy. Crit Care Med 37: S354-S367, 2009.
3. Close RI. Dynamic properties of mammalian skeletal muscles. Physiol Rev 52: 129-197, 1972.
4. Conti FJ, Felder A, Monkley S, Schwander M, Wood MR, Lieber R, Critchley D, Muller U. Progressive myopathy and defects in the maintenance of myotendinous junctions in mice that lack talin 1 in skeletal muscle. Development 135: 2043-2053, 2008.
5. Dargelos E, Poussard S, Brule C, Daury L, Cottin P. Calcium-dependent proteolytic system and muscle dysfunctions: a possible role of calpains in sarcopenia. Biochimie 90: 359-368, 2008.
6. Demoule A, Jung B, Prodanovic H, Molinari N, Chanques G, Coirault C, Matecki S, Duguet A, Similowski T, Jaber S. Diaphragm dysfunction on admission to ICU: prevalence, risk factors and prognostic impact-a prospective study. Am J Respir Crit Care Med 188: 213-219, 2013.
7. Fareed MU, Evenson AR, Wei W, Menconi M, Poylin V, Petkova V, Pignol B, Hasselgren PO. Treatment of rats with calpain inhibitors prevents sepsis-induced muscle proteolysis independent of atrogin-1/ MAFbx and MuRF1 expression. Am J Physiol Regul Integr Comp Physiol 290: R1589-R1597, 2006.
8. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25: 386-401, 2001.
9. Goll DE, Neti G, Mares SW, Thompson VF. Myofibrillar protein turnover: the proteasome and the calpains. J Anim Sci 86: E19-E35, 2008.
10. Hermans G, Agten A, Testelmans D, Decramer M, Gayan-Ramirez G. Increased duration of mechanical ventilation is associated with decreased diaphragmatic force: a prospective observational study. Crit Care 14: R127, 2010.
11. Kanzaki K, Kuratani M, Mishima T, Matsunaga S, Yanaka N, Usui S, Wada M. The effects of eccentric contraction on myofibrillar proteins in rat skeletal muscle. Eur J Appl Physiol 110: 943-952, 2010.
12. Klaude M, Mori M, Tjader I, Gustafsson T, Wernerman J, Rooyackers O. Protein metabolism and gene expression in skeletal muscle of critically ill patients with sepsis. Clin Sci (Lond) 122: 133-142, 2012.
13. Laghi F, Cattapan SE, Jubran A, Parthasarathy S, Warshawsky P, Choi YS, Tobin MJ. Is weaning failure caused by low-frequency fatigue of the diaphragm? Am J Respir Crit Care Med 167: 120-127, 2003.
14. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, Zhu J, Sachdeva R, Sonnad S, Kaiser LR, Rubinstein NA, Powers SK, Shrager JB. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358: 1327-1335, 2008.
15. Li W, Moylan JS, Chambers MA, Smith J, Reid MB. Interleukin-1 stimulates catabolism in C2C12 myotubes. Am J Physiol Cell Physiol 297: C706-C714, 2009.
16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
17. McClung JM, Judge AR, Talbert EE, Powers SK. Calpain-1 is required for hydrogen peroxide-induced myotube atrophy. Am J Physiol Cell Physiol 296: C363-C371, 2009.
18. Moylan JS, Smith JD, Chambers MA, McLoughlin TJ, Reid MB. TNF induction of atrogin-1/MAFbx mRNA depends on Foxo4 expression but not AKT-Foxo1/3 signaling. Am J Physiol Cell Physiol 295: C986-C993, 2008.
19. Nelson WB, Smuder AJ, Hudson MB, Talbert EE, Powers SK. Crosstalk between the calpain and caspase-3 proteolytic systems in the diaphragm during prolonged mechanical ventilation. Crit Care Med 40: 1857-1863, 2012.
20. Pemrick SM, Grebenau RC. Qualitative analysis of skeletal myosin as substrate of Ca2+-activated neutral protease: comparison of filamentous and soluble, native, and L2-deficient myosin. J Cell Biol 99: 2297-2308, 1984.
21. Powers SK, Kavazis AN, DeRuisseau KC. Mechanisms of disuse muscle atrophy: role of oxidative stress. Am J Physiol Regul Integr Comp Physiol 288: R337-R344, 2005.
22. Powers SK, Kavazis AN, Levine S. Prolonged mechanical ventilation alters diaphragmatic structure and function. Crit Care Med 37: S347-S353, 2009.
23. Rabuel C, Samuel JL, Lortat-Jacob B, Marotte F, Lanone S, Keyser C, Lessana A, Payen D, Mebazaa A. Activation of the ubiquitin proteolytic pathway in human septic heart and diaphragm. Cardiovasc Pathol 19: 158-164, 2010.
24. Reid KF, Doros G, Clark DJ, Patten C, Carabello RJ, Cloutier GJ, Phillips EM, Krivickas LS, Frontera WR, Fielding RA. Muscle power failure in mobility-limited older adults: preserved single fiber function despite lower whole muscle size, quality and rate of neuromuscular activation. Eur J Appl Physiol 112: 2289-2301, 2012.
25. Rittirsch D, Huber-Lang MS, Flierl MA, Ward PA. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc 4: 31-36, 2009.
26. Salazar JJ, Michele DE, Brooks SV. Inhibition of calpain prevents muscle weakness and disruption of sarcomere structure during hindlimb suspension. J Appl Physiol 108: 120-127, 2010.
27. Showalter CJ, Engel AG. Acute quadriplegic myopathy: analysis of myosin isoforms and evidence for calpain-mediated proteolysis. Muscle Nerve 20: 316-322, 1997.
28. Smith IJ, Dodd SL. Calpain activation causes a proteasome-dependent increase in protein degradation and inhibits the Akt signalling pathway in rat diaphragm muscle. Exp Physiol 92: 561-573, 2007.
29. Smuder AJ, Kavazis AN, Hudson MB, Nelson WB, Powers SK. Oxidation enhances myofibrillar protein degradation via calpain and caspase-3. Free Radic Biol Med 49: 1152-1160, 2010.
30. Spencer MJ, Mellgren RL. Overexpression of a calpastatin transgene in mdx muscle reduces dystrophic pathology. Hum Mol Genet 11: 2645-2655, 2002.
31. Supinski GS, Callahan LA. Calpain activation contributes to endotoxininduced diaphragmatic dysfunction. Am J Respir Cell Mol Biol 42: 80-87, 2010.
32. Supinski GS, Callahan LA. Diaphragm weakness in mechanically ventilated critically ill patients. Crit Care 17: R120, 2013.
33. Supinski GS, Ji X, Callahan LA. The JNK MAP kinase pathway contributes to the development of endotoxin-induced diaphragm caspase activation. Am J Physiol Regul Integr Comp Physiol 297: R825-R834, 2009.
34. Supinski GS, Ji XY, Callahan LA. p38 Mitogen-activated protein kinase modulates endotoxin-induced diaphragm caspase activation. Am J Respir Cell Mol Biol 43: 121-127, 2010.
35. Supinski GS, Vanags J, Callahan LA. Effect of proteasome inhibitors on endotoxin-induced diaphragm dysfunction. Am J Physiol Lung Cell Mol Physiol 296: L994-L1001, 2009.
36. Supinski GS, Wang W, Callahan LA. Caspase and calpain activation both contribute to sepsis-induced diaphragmatic weakness. J Appl Physiol 107: 1389-1396, 2009.
37. Takamure M, Murata KY, Tamada Y, Azuma M, Ueno S. Calpaindependent alpha-fodrin cleavage at the sarcolemma in muscle diseases. Muscle Nerve 32: 303-309, 2005.
38. Talbert EE, Smuder AJ, Min K, Kwon OS, Szeto HH, Powers SK. Immobilization-induced activation of key proteolytic systems in skeletal muscles is prevented by a mitochondria-targeted antioxidant. J Appl Physiol 115: 529-538, 2013.
39. Tawa NE Jr, Odessey R, Goldberg AL. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J Clin Invest 100: 197-203, 1997.
40. Tidball JG, Spencer MJ. Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J Physiol 545: 819-828, 2002.
41. Watson AC, Hughes PD, Louise Harris M, Hart N, Ware RJ, Wendon J, Green M, Moxham J. Measurement of twitch transdiaphragmatic, esophageal, and endotracheal tube pressure with bilateral anterolateral magnetic phrenic nerve stimulation in patients in the intensive care unit. Crit Care Med 29: 1325-1331, 2001.