Oxidative capacity and fatigability in run-trained malignant hyperthermia-susceptible mice

Muscle and Nerve

Volumn 45, Issue 4, 2012, Pages 586-596

  Rouviere, Clement ^a   Corona, Benjamin T ^a   Ingalls, Christopher P ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Adaptation; Calcium; Injury; Mitochondria; Ryanodine receptor

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C OXIDASE; MYOSIN HEAVY CHAIN; RYANODINE RECEPTOR;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENDURANCE TRAINING; ENZYME ACTIVITY; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; IMMUNOBLOTTING; IN VITRO STUDY; LEG MUSCLE; MALE; MALIGNANT HYPERTHERMIA; MOUSE; MUSCLE CELL; MUSCLE FATIGUE; MUSCLE FUNCTION; MUSCLE INJURY; MUSCLE STRENGTH; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RUNNING; SEX DIFFERENCE; ANIMAL; C57BL MOUSE; DISEASE PREDISPOSITION; ENDURANCE; GENETICS; MALIGNANT HYPERTENSION; METABOLISM; MUSCLE ISOMETRIC CONTRACTION; MUSCLE MITOCHONDRION; ORGAN SIZE; OXIDATION REDUCTION REACTION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; WESTERN BLOTTING;

AEROBIOSIS; ANIMALS; BLOTTING, WESTERN; CITRATE (SI)-SYNTHASE; DISEASE SUSCEPTIBILITY; ELECTRON TRANSPORT COMPLEX IV; FEMALE; HYPERTENSION, MALIGNANT; ISOMETRIC CONTRACTION; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; MUSCLE STRENGTH; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; ORGAN SIZE; OXIDATION-REDUCTION; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; POLYMERASE CHAIN REACTION; RUNNING; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84860337422     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.22343     Document Type: Article

References (55)

1. Avila G. Intracellular Ca2+ dynamics in malignant hyperthermia and central core disease: established concepts, new cellular mechanisms involved. Cell Calcium 2005; 37: 121-127.
2. Dirksen RT, Avila G. Distinct effects on Ca2+ handling caused by malignant hyperthermia and central core disease mutations in RyR1. Biophys J 2004; 87: 3193-3204.
3. Rosenberg H, Davis M, James D, Pollock N, Stowell K. Malignant hyperthermia. Orphanet J Rare Dis 2007; 2: 21.
4. Magee KR, Shy GM. A new congenital non-progressive myopathy. Brain 1956; 79: 610-621.
5. Dulhunty AF. Excitation-contraction coupling from the 1950s into the new millennium. Clin Exp Pharmacol Physiol 2006; 33: 763-772.
6. Durham WJ, Aracena-Parks P, Long C, Rossi AE, Goonasekera SA, Boncompagni S, et al. RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1 knockin mice. Cell 2008; 133: 53-65.
7. Boncompagni S, Rossi AE, Micaroni M, Hamilton SL, Dirksen RT, Franzini-Armstrong C, et al. Characterization and temporal development of cores in a mouse model of malignant hyperthermia. Proc Natl Acad Sci USA 2009; 106: 21996-22001.
8. Quane KA, Keating KE, Healy JM, Manning BM, Krivosic-Horber R, Krivosic I, et al. Mutation screening of the RYR1 gene in malignant hyperthermia: detection of a novel Tyr to Ser mutation in a pedigree with associated central cores. Genomics 1994; 23: 236-239.
9. Capacchione JF, Muldoon SM. The relationship between exertional heat illness, exertional rhabdomyolysis, and malignant hyperthermia. Anesth Analg 2009; 109: 1065-1069.
10. Davis M, Brown R, Dickson A, Horton H, James D, Laing N, et al. Malignant hyperthermia associated with exercise-induced rhabdomyolysis or congenital abnormalities and a novel RYR1 mutation in New Zealand and Australian pedigrees. Br J Anaesth 2002; 88: 508-515.
11. Wappler F, Fiege M, Steinfath M, Agarwal K, Scholz J, Singh S, et al. Evidence for susceptibility to malignant hyperthermia in patients with exercise-induced rhabdomyolysis. Anesthesiology 2001; 94: 95-100.
12. Corona BT, Rouviere C, Hamilton SL, Ingalls CP. Eccentric contractions do not induce rhabdomyolysis in malignant hyperthermia susceptible mice. J Appl Physiol 2008; 105: 1542-1553.
13. Ben Abraham R, Cahana A, Krivosic-Horber RM, Perel A. Malignant hyperthermia susceptibility: anaesthetic implications and risk stratification. Q J Med 1997; 90: 13-18.
14. Ogletree JW, Antognini JF, Gronert GA. Postexercise muscle cramping associated with positive malignant hyperthermia contracture testing. Am J Sports Med 1996; 24: 49-51.
15. Wappler F, Fiege M, Antz M, Schulte am Esch J. Hemodynamic and metabolic alterations in response to graded exercise in a patient susceptible to malignant hyperthermia. Anesthesiology 2000; 92: 268-272.
16. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 1984; 56: 831-838.
17. Lerman I, Harrison BC, Freeman K, Hewett TE, Allen DL, Robbins J, et al. Genetic variability in forced and voluntary endurance exercise performance in seven inbred mouse strains. J Appl Physiol 2002; 92: 2245-2255.
18. Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP. Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol Cell Physiol 2010; 298: C365-376.
19. Corona BT, Rouviere C, Hamilton SL, Ingalls CP. FKBP12 deficiency reduces strength deficits after eccentric contraction-induced muscle injury. J Appl Physiol 2008; 105: 527-537.
20. Ingalls CP, Warren GL, Armstrong RB. Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions. J Muscle Res Cell Motil 1998; 19: 215-224.
21. Ingalls CP, Warren GL, Williams JH, Ward CW, Armstrong RB. E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 1998; 85: 58-67.
22. Ingalls CP, Warren GL, Zhang JZ, Hamilton SL, Armstrong RB. Dihydropyridine and ryanodine receptor binding after eccentric contractions in mouse skeletal muscle. J Appl Physiol 2004; 96: 1619-1625.
23. Delp MD, Duan C, Ray CA, Armstrong RB. Rat hindlimb muscle blood flow during level and downhill locomotion. J Appl Physiol 1999; 86: 564-568.
24. Allen DL, Harrison BC, Maass A, Bell ML, Byrnes WC, Leinwand LA. Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl Physiol 2001; 90: 1900-1908.
25. Corona BT, Hamilton SL, Ingalls CP. Effect of prior exercise on thermal sensitivity of malignant hyperthermia-susceptible muscle. Muscle Nerve 2010; 42: 270-272.
26. Lowe DA, Warren GL, Ingalls CP, Boorstein DB, Armstrong RB. Muscle function and protein metabolism after initiation of eccentric contraction-induced injury. J Appl Physiol 1995; 79: 1260-1270.
27. Srere P. Citrate synthase. In: Lowenstein JM, editor. Methods in enzymology. New York: Academic Press; 1969. p 3-11.
28. Bhattacharya SK, Thakar JH, Johnson PL, Shanklin DR. Isolation of skeletal muscle mitochondria from hamsters using an ionic medium containing ethylenediaminetetraacetic acid and nagarse. Anal Biochem 1991; 192: 344-349.
29. Warren GL, Hayes DA, Lowe DA, Williams JH, Armstrong RB. Eccentric contraction-induced injury in normal and hindlimb-suspended mouse soleus and EDL muscles. J Appl Physiol 1994; 77: 1421-1430.
30. Chelu MG, Goonasekera SA, Durham WJ, Tang W, Lueck JD, Riehl J, et al. Heat- and anesthesia-induced malignant hyperthermia in an RyR1 knock-in mouse. FASEB J 2006; 20: 329-330.
31. Itai Y, Kariya Y, Hoshino Y. Morphological changes in rat hindlimb muscle fibres during recovery from disuse atrophy. Acta Physiol Scand 2004; 181: 217-224.
32. Jungbluth H, Zhou H, Sewry CA, Robb S, Treves S, Bitoun M, et al. Centronuclear myopathy due to a de novo dominant mutation in the skeletal muscle ryanodine receptor (RYR1) gene. Neuromuscul Disord 2007; 17: 338-345.
33. Mezin P, Payen JF, Bosson JL, Brambilla E, Stieglitz P. Histological support for the difference between malignant hyperthermia susceptible (MHS), equivocal (MHE) and negative (MHN) muscle biopsies. Br J Anaesth 1997; 79: 327-331.
34. Sewry CA. Pathological defects in congenital myopathies. J Muscle Res Cell Motil 2008; 29: 231-238.
35. Iwata Y, Katanosaka Y, Arai Y, Shigekawa M, Wakabayashi S. Dominant-negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet 2009; 18: 824-834.
36. MacLennan DH. Ca2+ signalling and muscle disease. Eur J Biochem 2000; 267: 5291-5297.
37. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, Goodyear LJ. Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 2007; 56: 2062-2069.
38. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 2008; 88: 287-332.
39. Yan Z, Okutsu M, Akhtar YN, Lira VA. Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol 2011; 110: 264-274.
40. Fitts RH, Booth FW, Winder WW, Holloszy JO. Skeletal muscle respiratory capacity, endurance, and glycogen utilization. Am J Physiol 1975; 228: 1029-1033.
41. Takahashi M, Hood DA. Chronic stimulation-induced changes in mitochondria and performance in rat skeletal muscle. J Appl Physiol 1993; 74: 934-941.
42. Gollnick PD, Armstrong RB, Saubert CW, Piehl K, Saltin B. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol 1972; 33: 312-319.
43. Chen G, Carroll S, Racay P, Dick J, Pette D, Traub I, et al. Deficiency in parvalbumin increases fatigue resistance in fast-twitch muscle and upregulates mitochondria. Am J Physiol Cell Physiol 2001; 281: C114-122.
44. Chin ER, Grange RW, Viau F, Simard AR, Humphries C, Shelton J, et al. Alterations in slow-twitch muscle phenotype in transgenic mice overexpressing the Ca2+ buffering protein parvalbumin. J Physiol 2003; 547: 649-663.
45. Wredenberg A, Wibom R, Wilhelmsson H, Graff C, Wiener HH, Burden SJ, et al. Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci USA 2002; 99: 15066-15071.
46. Andronache Z, Hamilton SL, Dirksen RT, Melzer W. A retrograde signal from RyR1 alters DHP receptor inactivation and limits window Ca2+ release in muscle fibers of Y522S RyR1 knock-in mice. Proc Natl Acad Sci USA 2009; 106: 4531-4536.
47. Street SF. Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 1983; 114: 346-364.
48. Street SF, Ramsey RW. Sarcolemma: transmitter of active tension in frog skeletal muscle. Science 1965; 149: 1379-1380.
49. Bronikowski AM, Rhodes JS, Garland T Jr, Prolla TA, Awad TA, Gammie SC. The evolution of gene expression in mouse hippocampus in response to selective breeding for increased locomotor activity. Evolution 2004; 58: 2079-2086.
50. Bridge MW, Weller AS, Rayson M, Jones DA. Responses to exercise in the heat related to measures of hypothalamic serotonergic and dopaminergic function. Eur J Appl Physiol 2003; 89: 451-459.
51. Adeola O, Ball RO, House JD, O'Brien PJ. Regional brain neurotransmitter concentrations in stress-susceptible pigs. J Anim Sci 1993; 71: 968-974.
52. Weaver SA, Dixon WT, Schaefer AL. The effects of mutated skeletal ryanodine receptors on hypothalamic-pituitary-adrenal axis function in boars. J Anim Sci 2000; 78: 1319-1330.
53. Campbell IT, Ellis FR, Evans RT. Metabolic rate and blood hormone and metabolite levels of individuals susceptible to malignant hyperpyrexia at rest and in response to food and mild exercise. Anesthesiology 1981; 55: 46-52.
54. Green JH, Ellis FR, Halsall PJ, Campbell IT, Currie S, Caddy J. Thermoregulation, plasma catecholamine and metabolite levels during submaximal work in individuals susceptible to malignant hyperpyrexia. Acta Anaesthesiol Scand 1987; 31: 122-126.
55. Hunter SLR, Tuttle GH, DeWalt JL, Smodic R, Martin J. Malignant hyperthermia in a college football player. Phys Sportsmed 1987; 15: 77-81.