Sphingomyelinase depresses force and calcium sensitivity of the contractile apparatus in mouse diaphragm muscle fibers

Journal of Applied Physiology

Volumn 112, Issue 9, 2012, Pages 1538-1545

  Ferreira, Leonardo F ^a,b   Moylan, Jennifer S ^a   Stasko, Shawn ^a   Smith, Jeffrey D ^a   Campbell, Kenneth S ^a   Reid, Michael B ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Mitochondria; Oxidative stress; Single fiber; Skeletal muscle; Sphingolipids

Indexed keywords

3 NITROTYROSINE; 3-NITROTYROSINE; ANTIOXIDANT; DRUG DERIVATIVE; REACTIVE OXYGEN METABOLITE; SPHINGOMYELIN PHOSPHODIESTERASE; TYROSINE;

ANIMAL; ARTICLE; C57BL MOUSE; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; CYTOLOGY; CYTOSOL; DIAPHRAGM; DRUG EFFECT; ELECTROSTIMULATION; ENZYMOLOGY; EXCITATION CONTRACTION COUPLING; METABOLISM; MOUSE; MUSCLE CONTRACTION; MUSCLE FIBRIL; MUSCLE MITOCHONDRION; MUSCLE STRENGTH; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN CARBONYLATION; PROTEIN PROCESSING; SKELETAL MUSCLE;

ANIMALS; ANTIOXIDANTS; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; CYTOSOL; DIAPHRAGM; ELECTRIC STIMULATION; EXCITATION CONTRACTION COUPLING; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE STRENGTH; MYOFIBRILS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN CARBONYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE OXYGEN SPECIES; SPHINGOMYELIN PHOSPHODIESTERASE; TYROSINE;

EID: 84862058399     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01269.2011     Document Type: Article

References (59)

1. Ackermann MA, Kontrogianni-Konstantopoulos A. Myosin binding protein-C slow is a novel substrate for protein kinase A (PKA) and C (PKC) in skeletal muscle. J Proteome Res 10: 4547-4555, 2011.
2. 2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119: 573-581, 2009.
3. Andrade FH, Reid MB, Allen DG, Westerblad H. Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol 509: 565-575, 1998. (Pubitemid 28287013)
4. 2 level, and muscle-derived nitric oxide. Am J Physiol Regul Integr Comp Physiol 287: R698-R705, 2004. (Pubitemid 39280453)
5. 2 alters rat cardiac sarcomere function and protein phosphorylation through redox signaling. Am J Physiol Heart Circ Physiol 299: H723-H730, 2010.
6. Barreiro E, Gea J, Di FM, Kriazhev L, James S, Hussain SN. Protein carbonyl formation in the diaphragm. Am J Respir Cell Mol Biol 32: 9-17, 2005. (Pubitemid 40053299)
7. Birbes H, El Bawab S, Obeid LM, Hannun YA. Mitochondria and ceramide: intertwined roles in regulation of apoptosis. Adv Enzyme Regul 42: 113-129, 2002. (Pubitemid 35033533)
8. Callahan LA, She ZW, Nosek TM. Superoxide, hydroxyl radical, and hydrogen peroxide effects on single-diaphragm fiber contractile apparatus. J Appl Physiol 90: 45-54, 2001. (Pubitemid 32038502)
9. Campbell KS, Moss RL. History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J 82: 929-943, 2002. (Pubitemid 34111233)
10. Campbell KS, Moss RL. SLControl: PC-based data acquisition and analysis for muscle mechanics. Am J Physiol Heart Circ Physiol 285: H2857-H2864, 2003. (Pubitemid 37443107)
11. Canton M, Menazza S, Sheeran FL, Polverino de Laureto P, Di Lisa F, Pepe S. Oxidation of myofibrillar proteins in human heart failure. J Am Coll Cardiol 57: 300-309, 2011.
12. Canton M, Neverova I, Menabo R, Van EJ, Di LF. Evidence of myofibrillar protein oxidation induced by postischemic reperfusion in isolated rat hearts. Am J Physiol Heart Circ Physiol 286: H870-H877, 2004. (Pubitemid 38248597)
13. Canton M, Skyschally A, Menabo R, Boengler K, Gres P, Schulz R, Haude M, Erbel R, Di Lisa F, Heusch G. Oxidative modification of tropomyosin and myocardial dysfunction following coronary microembolization. Eur Heart J 27: 875-881, 2006.
14. Close RI. Dynamic properties of mammalian skeletal muscles. Physiol Rev 52: 129-197, 1972.
15. Colson BA, Bekyarova T, Locher MR, Fitzsimons DP, Irving TC, Moss RL. Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circ Res 103: 244-251, 2008.
16. Cowart LA. A novel role for sphingolipid metabolism in oxidant-mediated skeletal muscle fatigue. Focus on "Sphingomyelinase stimulates oxidant signaling to weaken skeletal muscle and promote fatigue". Am J Physiol Cell Physiol 299: C549-C551, 2010.
17. Diaz PT, Brownstein E, Clanton TL. Effects of N-acetylcysteine on in vitro diaphragm function are temperature dependent. J Appl Physiol 77: 2434-2439, 1994. (Pubitemid 24346457)
18. Doehner W, Bunck AC, Rauchhaus M, von Haehling S, Brunkhorst FM, Cicoira M, Tschope C, Ponikowski P, Claus RA, Anker SD. Secretory sphingomyelinase is upregulated in chronic heart failure: a second messenger system of immune activation relates to body composition, muscular functional capacity, and peripheral blood flow. Eur Heart J 28: 821-828, 2007. (Pubitemid 47343591)
19. Dutka TL, Mollica JP, Lamb GD. Differential effects of peroxynitrite on contractile protein properties in fast- and slow-twitch skeletal muscle fibers of rat. J Appl Physiol 110: 705-716, 2011.
20. Ferreira LF, Moylan JS, Gilliam LA, Smith JD, Nikolova-Karakashian M, Reid MB. Sphingomyelinase stimulates oxidant signaling to weaken skeletal muscle and promote fatigue. Am J Physiol Cell Physiol 299: C552-C560, 2010.
21. Garcia-Ruiz C, Colell A, Mari M, Morales A, Fernandez-Checa JC. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species Role of mitochondrial glutathione. J Biol Chem 272: 11369-11377, 1997. (Pubitemid 27184141)
22. Geiger PC, Cody MJ, Sieck GC. Force-calcium relationship depends on myosin heavy chain and troponin isoforms in rat diaphragm muscle fibers. J Appl Physiol 87: 1894-1900, 1999.
23. Gordon AM, Homsher E, Regnier M. Regulation of contraction in striated muscle. Physiol Rev 80: 853-924, 2000. (Pubitemid 30164950)
24. Gregorevic P, Plant DR, Leeding KS, Bach LA, Lynch GS. Improved contractile function of the mdx dystrophic mouse diaphragm muscle after insulin-like growth factor-I administration. Am J Pathol 161: 2263-2272, 2002. (Pubitemid 35434870)
25. Gulbins E, Li PL. Physiological and pathophysiological aspects of ceramide. Am J Physiol Regul Integr Comp Physiol 290: R11-R26, 2006.
26. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150, 2008. (Pubitemid 351158911)
27. Hardin BJ, Campbell KS, Smith JD, Arbogast S, Smith J, Moylan JS, Reid MB. TNF- acts via TNFR1 and muscle-derived oxidants to depress myofibrillar force in murine skeletal muscle. J Appl Physiol 104: 694-699, 2008. (Pubitemid 351468797)
28. Heeley DH. Investigation of the effects of phosphorylation of rabbit striated muscle alpha alpha-tropomyosin and rabbit skeletal muscle troponin-T. Eur J Biochem 221: 129-137, 1994. (Pubitemid 24120554)
29. 2+ sensitivity in human cardiomyocytes. Antioxid Redox Signal 10: 1175-1184, 2008. (Pubitemid 351620310)
30. Heusch P, Canton M, Aker S, van de Sand A, Konietzka I, Rassaf T, Menazza S, Brodde OE, Di Lisa F, Heusch G, Schulz R. The contribution of reactive oxygen species and p38 mitogen-activated protein kinase to myofilament oxidation and progression of heart failure in rabbits. Br J Pharmacol 160: 1408-1416, 2010.
31. Kunst G, Kress KR, Gruen M, Uttenweiler D, Gautel M, Fink RH. Myosin binding protein C, a phosphorylation-dependent force regulator in muscle that controls the attachment of myosin heads by its interaction with myosin S2. Circ Res 86: 51-58, 2000. (Pubitemid 30044168)
32. Lamb GD, Posterino GS. Effects of oxidation and reduction on contractile function in skeletal muscle fibres of the rat. J Physiol 546: 149-163, 2003.
33. Marchesini N, Hannun YA. Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 82: 27-44, 2004. (Pubitemid 38580872)
34. Moss RL, Fitzsimons DP. Regulation of contraction in mammalian striated muscles-the plot thick-ens. J Gen Physiol 136: 21-27, 2010.
35. Murphy RM, Dutka TL, Lamb GD. Hydroxyl radical and glutathione interactions alter calcium sensitivity and maximum force of the contractile apparatus in rat skeletal muscle fibres. J Physiol 586: 2203-2216, 2008. (Pubitemid 351540511)
36. Murrant CL, Reid MB. Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55: 236-248, 2001. (Pubitemid 33136323)
37. Nethery D, DiMarco A, Stofan D, Supinski G. Sepsis increases contraction-related generation of reactive oxygen species in the diaphragm. J Appl Physiol 87: 1279-1286, 1999. (Pubitemid 29483109)
38. Nikolova-Karakashian MN, Reid MB. Sphingolipid metabolism, oxidant signaling, and contractile function of skeletal muscle. Antioxid Redox Signal 15: 2501-2517, 2011.
39. Nikolova-Karakashian MN, Rozenova KA. Ceramide in stress response. Adv Exp Med Biol 688: 86-108, 2010.
40. Noland TA Jr., Kuo JF. Protein kinase C phosphorylation of cardiac troponin I and troponin T inhibits Ca(2+)-stimulated MgATPase activity in reconstituted actomyosin and isolated myofibrils, and decreases actinmyosin interactions. J Mol Cell Cardiol 25: 53-65, 1993. (Pubitemid 23053315)
41. 2+-loading capacity and promotes apoptosis. J Biol Chem 286: 4644-4658, 2011.
42. Pinto JR, de Sousa VP, Sorenson MM. Redox state of troponin C cysteine in the D/E helix alters the C-domain affinity for the thin filament of vertebrate striated muscle. Biochim Biophys Acta 1810: 391-397, 2011.
43. Powell SR, Gurzenda EM, Wahezi SE. Actin is oxidized during myocardial ischemia. Free Radic Biol Med 30: 1171-1176, 2001. (Pubitemid 32441843)
44. Powers SK, Hudson MB, Nelson WB, Talbert EE, Min K, Szeto HH, Kavazis AN, Smuder AJ. Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med 39: 1749-1759, 2011.
45. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88: 1243-1276, 2008.
46. Prochniewicz E, Lowe DA, Spakowicz DJ, Higgins L, O'Conor K, Thompson LV, Ferrington DA, Thomas DD. Functional, structural, and chemical changes in myosin associated with hydrogen peroxide treatment of skeletal muscle fibers. Am J Physiol Cell Physiol 294: C613-C626, 2008. (Pubitemid 351264413)
47. Reid MB, Haack KE, Franchek KM, Valberg PA, Kobzik L, West MS. Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol 73: 1797-1804, 1992.
48. Reid MB, Lannergren J, Westerblad H. Respiratory and limb muscle weakness induced by tumor necrosis factor-alpha: involvement of muscle myofilaments. Am J Respir Crit Care Med 166: 479-484, 2002.
49. Sancho Solis R, Ge Y, Walker JW. A preferred AMPK phosphorylation site adjacent to the inhibitory loop of cardiac and skeletal troponin I. Protein Sci 20: 894-907, 2011.
50. 2+- stimulated sphingomyelinase is secreted by many cell types and is a product of the acid sphingomyelinase gene. J Biol Chem 271: 18431-18436, 1996. (Pubitemid 26322699)
51. Straczkowski M, Kowalska I, Baranowski M, Nikolajuk A, Otziomek E, Zabielski P, Adamska A, Blachnio A, Gorski J, Gorska M. Increased skeletal muscle ceramide level in men at risk of developing type 2 diabetes. Diabetologia 50: 2366-2373, 2007. (Pubitemid 47512392)
52. Sweeney HL, Bowman BF, Stull JT. Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. Am J Physiol Cell Physiol 264: C1085-C1095, 1993. (Pubitemid 23158813)
53. Szeto HH, Schiller PW. Novel therapies targeting inner mitochondrial membrane-from discovery to clinical development. Pharm Res 28: 2669-2679, 2011.
54. van der Poel C, Edwards JN, Macdonald WA, Stephenson DG. Effect of temperature-induced reactive oxygen species production on excitationcontraction coupling in mammalian skeletal muscle. Clin Exp Pharmacol Physiol 35: 1482-1487, 2008.
55. Winterbourn CC, Parsons-Mair HN, Gebicki S, Gebicki JM, Davies MJ. Requirements for superoxide-dependent tyrosine hydroperoxide formation in peptides. Biochem J 381: 241-248, 2004. (Pubitemid 38932230)
56. Won JS, Singh I. Sphingolipid signaling and redox regulation. Free Radic Biol Med 40: 1875-1888, 2006. (Pubitemid 43728861)
57. Wong ML, Xie B, Beatini N, Phu P, Marathe S, Johns A, Gold PW, Hirsch E, Williams KJ, Licinio J, Tabas I. Acute systemic inflammation up-regulates secretory sphingomyelinase in vivo: a possible link between inflammatory cytokines and atherogenesis. Proc Natl Acad Sci USA 97: 8681-8686, 2000. (Pubitemid 30639733)
58. Wright VP, Reiser PJ, Clanton TL. Redox modulation of global phosphatase activity and protein phosphorylation in intact skeletal muscle. J Physiol 587: 5767-5781, 2009.
59. Zhao K, Zhao GM, Wu D, Soong Y, Birk AV, Schiller PW, Szeto HH. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem 279: 34682-34690, 2004. (Pubitemid 39318098)