Leaky ryanodine receptors contribute to diaphragmatic weakness during mechanical ventilation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 32, 2016, Pages 9069-9074

  Matecki, Stefan ^a   Dridi, Haikel ^a   Jung, Boris ^a,b   Saint, Nathalie ^a   Reiken, Steven R ^c   Scheuermann, Valérie ^a   Mrozek, Ségolène ^a   Santulli, Gaetano ^c   Umanskaya, Alisa ^c   Petrof, Basil J ^d   Jaber, Samir ^a,b   Marks, Andrew R ^c   Lacampagne, Alain ^a  

^a UNIV MONTPELLIER   (France)

^b HÔPITAL SAINT ELOI   (France)

^c Columbia University ^*  (United States)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

Beta adrenergic signaling; Calcium; Excitation contraction coupling; Skeletal muscle; VIDD

Indexed keywords

RYANODINE RECEPTOR; BETA ADRENERGIC RECEPTOR; CALCIUM; FK 506 BINDING PROTEIN; FKBP1A PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTIFICIAL VENTILATION; CALCIUM TRANSPORT; CONFERENCE PAPER; CONTROLLED STUDY; DIAPHRAGM; DIAPHRAGM WEAKNESS; EXCITATION CONTRACTION COUPLING; HUMAN; MOUSE; MUSCLE WEAKNESS; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; VENTILATOR; VENTILATOR INDUCED DIAPHRAGMATIC DYSFUNCTION; ADVERSE DEVICE EFFECT; ANIMAL; MECHANICAL VENTILATOR; METABOLISM; MUSCLE CONTRACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CALCIUM; DIAPHRAGM; HUMANS; MICE; MUSCLE CONTRACTION; OXIDATIVE STRESS; RECEPTORS, ADRENERGIC, BETA; RESPIRATION, ARTIFICIAL; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SIGNAL TRANSDUCTION; TACROLIMUS BINDING PROTEINS; VENTILATORS, MECHANICAL;

EID: 84982953388     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1609707113     Document Type: Article

References (50)

1. Levine S, et al. (2008) Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358(13):1327-1335.
2. Jaber S, et al. (2011) Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 183(3):364-371.
3. Vassilakopoulos T, Petrof BJ (2004) Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 169(3):336-341.
4. Chang AT, Boots RJ, Brown MG, Paratz J, Hodges PW (2005) Reduced inspiratory muscle endurance following successful weaning from prolonged mechanical ventilation. Chest 128(2):553-559.
5. Tobin MJ, Laghi F, Brochard L (2009) Role of the respiratory muscles in acute respiratory failure of COPD: Lessons from weaning failure. J Appl Physiol (1985) 107(3): 962-970.
6. Esteban A, et al.; VENTILA Group (2008) Evolution of mechanical ventilation in response to clinical research. Am J Respir Crit Care Med 177(2):170-177.
7. Shanely RA, et al. (2002) Mechanical ventilation-induced diaphragmatic atrophy is associated with oxidative injury and increased proteolytic activity. Am J Respir Crit Care Med 166(10):1369-1374.
8. Betters JL, et al. (2004) Trolox attenuates mechanical ventilation-induced diaphragmatic dysfunction and proteolysis. Am J Respir Crit Care Med 170(11):1179-1184.
9. Powers SK, et al. (2011) Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med 39(7):1749-1759.
10. Picard M, et al. (2012) Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med 186(11): 1140-1149.
11. Chen M, Won DJ, Krajewski S, Gottlieb RA (2002) Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 277(32):29181-29186.
12. Belcastro AN, Shewchuk LD, Raj DA (1998) Exercise-induced muscle injury: A calpain hypothesis. Mol Cell Biochem 179(1-2):135-145.
13. Jackman RW, Kandarian SC (2004) The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287(4):C834-C843.
14. Maes K, Testelmans D, Powers S, Decramer M, Gayan-Ramirez G (2007) Leupeptin inhibits ventilator-induced diaphragm dysfunction in rats. Am J Respir Crit Care Med 175(11):1134-1138.
15. McClung JM, et al. (2007) Caspase-3 regulation of diaphragm myonuclear domain during mechanical ventilation-induced atrophy. AmJRespirCritCareMed175(2):150-159.
16. Jaber S, Jung B, Matecki S, Petrof BJ (2011) Clinical review: Ventilator-induced diaphragmatic dysfunction-human studies confirm animal model findings! Crit Care 15(2):206.
17. Dünser MW, Hasibeder WR (2009) Sympathetic overstimulation during critical illness: Adverse effects of adrenergic stress. J Intensive Care Med 24(5):293-316.
18. Boldt J, Menges T, Kuhn D, Diridis C, Hempelmann G (1995) Alterations in circulating vasoactive substances in the critically ill-a comparison between survivors and nonsurvivors. Intensive Care Med 21(3):218-225.
19. Ng Y, et al. (2002) Characterisation of isoprenaline myotoxicity on slow-twitch skeletal versus cardiac muscle. Int J Cardiol 86(2-3):299-309.
20. Mrozek S, et al. (2012) Rapid onset of specific diaphragm weakness in a healthy murine model of ventilator-induced diaphragmatic dysfunction. Anesthesiology 117(3):560-567.
21. Santulli G, Marks AR (2015) Essential roles of intracellular calcium release channels in muscle, brain, metabolism, and aging. Curr Mol Pharmacol 8(2):206-222.
22. Umanskaya A, et al. (2014) Genetically enhancing mitochondrial antioxidant activity improves muscle function in aging. Proc Natl Acad Sci USA 111(42):15250-15255.
23. Reiken S, et al. (2003) PKA phosphorylation activates the calcium release channel (ryanodine receptor) in skeletal muscle: Defective regulation in heart failure. J Cell Biol 160(6):919-928.
24. Ward CW, et al. (2003) Defects in ryanodine receptor calcium release in skeletal muscle from post-myocardial infarct rats. FASEB J 17(11):1517-1519.
25. Santulli G, Xie W, Reiken SR, Marks AR (2015) Mitochondrial calcium overload is a key determinant in heart failure. Proc Natl Acad Sci USA 112(36):11389-11394.
26. Bellinger AM, et al. (2008) Remodeling of ryanodine receptor complex causes "leaky" channels: A molecular mechanism for decreased exercise capacity. Proc Natl Acad Sci USA 105(6):2198-2202.
27. Andersson DC, et al. (2011) Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab 14(2):196-207.
28. Bellinger AM, et al. (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 15(3):325-330.
29. McClung JM, et al. (2008) Redox regulation of diaphragm proteolysis during mechanical ventilation. Am J Physiol Regul Integr Comp Physiol 294(5):R1608-R1617.
30. Whidden MA, et al. (2010) Oxidative stress is required for mechanical ventilation-induced protease activation in the diaphragm. J Appl Physiol (1985) 108(5):1376-1382.
31. Santulli G, et al. (2012) Age-related impairment in insulin release: The essential role of β(2)-adrenergic receptor. Diabetes 61(3):692-701.
32. Donoso P, Sanchez G, Bull R, Hidalgo C (2011) Modulation of cardiac ryanodine receptor activity by ROS and RNS. Front Biosci 16:553-567.
33. Fauconnier J, et al. (2010) Leaky RyR2 trigger ventricular arrhythmias in Duchenne muscular dystrophy. Proc Natl Acad Sci USA 107(4):1559-1564.
34. Santulli G, et al. (2015) Calcium release channel RyR2 regulates insulin release and glucose homeostasis. J Clin Invest 125(5):1968-1978.
35. Turan B, Vassort G (2011) Ryanodine receptor: A new therapeutic target to control diabetic cardiomyopathy. Antioxid Redox Signal 15(7):1847-1861.
36. Ward CW, Prosser BL, Lederer WJ (2014) Mechanical stretch-induced activation of ROS/RNS signaling in striated muscle. Antioxid Redox Signal 20(6):929-936.
37. McClung JM, et al. (2009) Apocynin attenuates diaphragm oxidative stress and protease activation during prolonged mechanical ventilation. Crit Care Med 37(4): 1373-1379.
38. Manders WT, Vatner SF (1976) Effects of sodium pentobarbital anesthesia on left ventricular function and distribution of cardiac output in dogs, with particular reference to the mechanism for tachycardia. Circ Res 39(4):512-517.
39. Barker SJ, Gamel DM, Tremper KK (1987) Cardiovascular effects of anesthesia and operation. Crit Care Clin 3(2):251-268.
40. Dellinger RP, et al.; International Surviving Sepsis Campaign Guidelines Committee; American Association of Critical-Care Nurses; American College of Chest Physicians; American College of Emergency Physicians; Canadian Critical Care Society; European Society of Clinical Microbiology and Infectious Diseases; European Society of Intensive Care Medicine; European Respiratory Society; International Sepsis Forum; Japanese Association for Acute Medicine; Japanese Society of Intensive Care Medicine; Society of Critical Care Medicine; Society of Hospital Medicine; Surgical Infection Society; World Federation of Societies of Intensive and Critical Care Medicine (2008) Surviving Sepsis Campaign: International guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med 36(1):296-327.
41. Kim WY, et al. (2016) Effect of theophylline on ventilator-induced diaphragmatic dysfunction. J Crit Care 33:145-150.
42. Petrof BJ, Jaber S, Matecki S (2010) Ventilator-induced diaphragmatic dysfunction. Curr Opin Crit Care 16(1):19-25.
43. Eu JP, Sun J, Xu L, Stamler JS, Meissner G (2000) The skeletal muscle calcium release channel: Coupled O2 sensor and NO signaling functions. Cell 102(4):499-509.
44. Jung B, et al. (2010) Adaptive support ventilation prevents ventilator-induced diaphragmatic dysfunction in piglet: An in vivo and in vitro study. Anesthesiology 112(6):1435-1443.
45. Heulitt MJ, Holt SJ, Wilson S, Hall RA (2003) Effects of continuous positive airway pressure/positive end-expiratory pressure and pressure-support ventilation on work of breathing, using an animal model. Respir Care 48(7):689-696.
46. Jung B, et al. (2016) Diaphragmatic dysfunction in patients with ICU-acquired weakness and its impact on extubation failure. Intensive Care Med 42(5):853-861.
47. Demoule A, et al. (2013) Diaphragm dysfunction on admission to the intensive care unit. Prevalence, risk factors, and prognostic impact-a prospective study. Am J Respir Crit Care Med 188(2):213-219.
48. Fauconnier J, et al. (2011) Ryanodine receptor leak mediated by caspase-8 activation leads to left ventricular injury after myocardial ischemia-reperfusion. Proc Natl Acad Sci USA 108(32):13258-13263.
49. Xie W, et al. (2015) Mitochondrial oxidative stress promotes atrial fibrillation. Sci Rep 5:11427.
50. Yuan Q, et al. (2016) Maintenance of normal blood pressure is dependent on IP3R1-mediated regulation of eNOS. Proc Natl Acad Sci USA 113(30):8532-8537.