Carbonic anhydrase III and four-and-a-half LIM protein 1 are preferentially oxidized with muscle unloading

Journal of Applied Physiology

Volumn 105, Issue 5, 2008, Pages 1554-1561

  Chen, Chiao Nan ^a   Ferrington, Deborah A ^a   Thompson, LaDora V ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Hindlimb unloading; Muscle disuse

Indexed keywords

CARBONATE DEHYDRATASE III; LIM PROTEIN; SYNAPSIN I;

ANIMAL EXPERIMENT; ARTICLE; CONTROL GROUP; CONTROLLED STUDY; EXPERIMENTAL RAT; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; SLOT BLOT HYBRIDIZATION; SOLEUS MUSCLE; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

AGE FACTORS; AGING; ALDEHYDES; ANIMALS; CARBONIC ANHYDRASE III; HINDLIMB SUSPENSION; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PROTEOMICS; RATS; RATS, INBRED F344; TIME FACTORS; TYROSINE;

EID: 57349185571     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.90680.2008     Document Type: Article

References (58)

1. Bardag-Gorce F, Farout L, Veyrat-Durebex C, Briand Y, Briand M. Changes in 20S proteasome activity during ageing of the LOU rat. Mol Biol Rep 26: 89-93, 1999.
2. Bejma J, Ji LL. Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol 87: 465-470, 1999.
3. Cabiscol E, Levine RL. Carbonic anhydrase III. Oxidative modification in vivo and loss of phosphatase activity during aging. J Biol Chem 270: 14742-14747, 1995.
4. Cakatay U, Telci A, Kayali R, Tekeli F, Akcay T, Sivas A. Relation of aging with oxidative protein damage parameters in the rat skeletal muscle. Clin Biochem 36: 51-55, 2003.
5. Chakravarti B, Chakravarti DN. Oxidative modification of proteins: age-related changes. Gerontology 53: 128-139, 2007.
6. Chen C, Brown-Borg HM, Rakoczy SG, Thompson LV. Muscle disuse: adaptation of antioxidant systems is age dependent. J Gerontol A Biol Sci Med Sci 63: 461-466, 2008.
7. Chen J, Henderson GI, Freeman GL. Role of 4-hydroxynonenal in modification of cytochrome c oxidase in ischemia/reperfused rat heart. J Mol Cell Cardiol 33: 1919-1927, 2001.
8. Dupont-Versteegden EE, Fluckey JD, Knox M, Gaddy D, Peterson CA. Effect of flywheel-based resistance exercise on processes contributing to muscle atrophy during unloading in adult rats. J Appl Physiol 101: 202-212, 2006.
9. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128, 1991.
10. Ferrington DA, Husom AD, Thompson LV. Altered proteasome structure, function, and oxidation in aged muscle. FASEB J 19: 644-646, 2005.
11. Fugere NA, Ferrington DA, Thompson LV. Protein nitration with aging in the rat semimembranosus and soleus muscles. J Gerontol A Biol Sci Med Sci 61: 806-812, 2006.
12. Gianni P, Jan KJ, Douglas MJ, Stuart PM, Tarnopolsky MA. Oxidative stress and the mitochondrial theory of aging in human skeletal muscle. Exp Gerontol 39: 1391-1400, 2004.
13. Gunduz F, Senturk UK, Kuru O, Aktekin B, Aktekin MR. The effect of one year's swimming exercise on oxidant stress and antioxidant capacity in aged rats. Physiol Res 53: 171-176, 2004.
14. Hollander J, Bejma J, Ookawara T, Ohno H, Ji LL. Superoxide dismutase gene expression in skeletal muscle: fiber-specific effect of age. Mech Ageing Dev 116: 33-45, 2000.
15. Husom AD, Ferrington DA, Thompson LV. Age-related differences in the adaptive potential of type I skeletal muscle fibers. Exp Gerontol 40: 227-235, 2005.
16. Husom AD, Peters EA, Kolling EA, Fugere NA, Thompson LV, Ferrington DA. Altered proteasome function and subunit composition in aged muscle. Arch Biochem Biophys 421: 67-76, 2004.
17. Hussain SN, Matar G, Barreiro E, Florian M, Divangahi M, Vassilakopoulos T. Modifications of proteins by 4-hydroxy-2-nonenal in the ventilatory muscles of rats. Am J Physiol Lung Cell Mol Physiol 290: L996-L1003, 2006.
18. Ikemoto M, Nikawa T, Takeda S, Watanabe C, Kitano T, Baldwin KM, Izumi R, Nonaka I, Towatari T, Teshima S, Rokutan K, Kishi K. Space shuttle flight (STS-90) enhances degradation of rat myosin heavy chain in association with activation of ubiquitin-proteasome pathway. FASEB J 15: 1279-1281, 2001.
19. Ikemoto M, Okamura Y, Kano M, Hirasaka K, Tanaka R, Yamamoto T, Sasa T, Ogawa T, Sairyo K, Kishi K, Nikawa T. A relative high dose of vitamin E does not attenuate unweighting-induced oxidative stress and ubiquitination in rat skeletal muscle. J Physiol Anthropol Appl Human Sci 21: 257-263, 2002.
20. Kandarian SC, Stevenson EJ. Molecular events in skeletal muscle during disuse atrophy. Exerc Sport Sci Rev 30: 111-116, 2002.
21. Koesterer TJ, Dodd SL, Powers S. Increased antioxidant capacity does not attenuate muscle atrophy caused by unweighting. J Appl Physiol 93: 1959-1965, 2002.
22. Kondo H, Kodama J, Kishibe T, Itokawa Y. Oxidative stress during recovery from muscle atrophy. FEBS Lett 326: 189-191, 1993.
23. Lambertucci RH, Levada-Pires AC, Rossoni LV, Curi R, Pithon-Curi TC. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech Ageing Dev 128: 267-275, 2007.
24. Lee SM, Tsui SK, Chan KK, Garcia-Barcelo M, Waye MM, Fung KP, Liew CC, Lee CY. Chromosomal mapping, tissue distribution and cDNA sequence of four-and-a-half LIM domain protein 1 (FHL1). Gene 216: 163-170, 1998.
25. Leeuwenburgh C, Fiebig R, Chandwaney R, Ji LL. Aging and exercise training in skeletal muscle: responses of glutathione and antioxidant enzyme systems. Am J Physiol Regul Integr Comp Physiol 267: R439-R445, 1994.
26. Levine RL, Stadtman ER. Oxidative modification of proteins during aging. Exp Gerontol 36: 1495-1502, 2001.
27. Lipman RD, Chrisp CE, Hazzard DG, Bronson RT. Pathologic characterization of Brown Norway, Brown Norway x Fischer 344, and Fischer 344 x Brown Norway rats with relation to age. J Gerontol A Biol Sci Med Sci 51: B54-B59, 1996.
28. Liu MJ, Li JX, Lee KM, Qin L, Chan KM. Oxidative stress after muscle damage from immobilization and remobilization occurs locally and systemically. Clin Orthop Relat Res 434: 246-250, 2005.
29. Loughna PT, Mason P, Bayol S, Brownson C. The LIM-domain protein FHL1 (SLIM 1) exhibits functional regulation in skeletal muscle. Mol Cell Biol Res Commun 3: 136-140, 2000.
30. Luhtala TA, Roecker EB, Pugh T, Feuers RJ, Weindruch R. Dietary restriction attenuates age-related increases in rat skeletal muscle antioxidant enzyme activities. J Gerontol B Psychol Sci Soc Sci 49: B231-B238, 1994.
31. MacMillan-Crow LA, Crow JP, Kerby JD, Beckman JS, Thompson JA. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci USA 93: 11853-11858, 1996.
32. McDonough JL, Neverova I, Van Eyk JE. Proteomic analysis of human biopsy samples by single two-dimensional electrophoresis: Coomassie, silver, mass spectrometry, and Western blotting. Proteomics 2: 978-987, 2002.
33. McGrath MJ, Cottle DL, Nguyen MA, Dyson JM, Coghill ID, Robinson PA, Holdsworth M, Cowling BS, Hardeman EC, Mitchell CA, Brown S. Four and a half LIM protein 1 binds myosin-binding protein C and regulates myosin filament formation and sarcomere assembly. J Biol Chem 281: 7666-7683, 2006.
34. 1-integrin-dependent myocyte elongation. Am J Physiol Cell Physiol 285: C1513-C15126, 2003.
35. Morgan MJ, Madgwick AJ. The LIM proteins FHL1 and FHL3 are expressed differently in skeletal muscle. Biochem Biophys Res Commun 255: 245-250, 1999.
36. Muller FL, Song W, Liu Y, Chaudhuri A, Pieke-Dahl S, Strong R, Huang TT, Epstein CJ, Roberts LJ 2nd, Csete M, Faulkner JA, Van Remmen H. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic Biol Med 40: 1993-2004, 2006.
37. Pansarasa O, Castagna L, Colombi B, Vecchiet J, Felzani G, Marzatico F. Age and sex differences in human skeletal muscle: role of reactive oxygen species. Free Radic Res 33: 287-293, 2000.
38. 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.
39. Powers SK, Kavazis AN, McClung JM. Oxidative stress and disuse muscle atrophy. J Appl Physiol 102: 2389-2397, 2007.
40. Quinzii CM, Vu TH, Min KC, Tanji K, Barral S, Grewal RP, Kattah A, Camano P, Otaegui D, Kunimatsu T, Blake DM, Wilhelmsen KC, Rowland LP, Hays AP, Bonilla E, Hirano M. X-linked dominant scapuloperoneal myopathy is due to a mutation in the gene encoding four-and-a-half-LIM protein 1. Am J Hum Genet 82: 208-213, 2008.
41. Raisanen SR, Lehenkari P, Tasanen M, Rahkila P, Harkonen PL, Vaananen HK. Carbonic anhydrase III protects cells from hydrogen peroxide-induced apoptosis. FASEB J 13: 513-522, 1999.
42. Robinson PA, Brown S, McGrath MJ, Coghill ID, Gurung R, Mitchell CA. Skeletal muscle LIM protein 1 regulates integrin-mediated myoblast adhesion, spreading, and migration. Am J Physiol Cell Physiol 284: C681-C695, 2003.
43. Selsby JT, Dodd SL. Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am J Physiol Regul Integr Comp Physiol 289: R134-R139, 2005.
44. Selsby JT, Rother S, Tsuda S, Pracash O, Quindry J, Dodd SL. Intermittent hyperthermia enhances skeletal muscle regrowth and attenuates oxidative damage following reloading. J Appl Physiol 102: 1702-1707, 2007.
45. Shanely RA, Zergeroglu MA, Lennon SL, Sugiura T, Yimlamai T, Enns D, Belcastro A, Powers SK. Mechanical ventilation-induced diaphragmatic atrophy is associated with oxidative injury and increased proteolytic activity. Am J Respir Crit Care Med 166: 1369-1374, 2002.
46. Stadtman ER, Berlett BS. Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10: 485-494, 1997.
47. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol 551: 33-48, 2003.
48. Thomason DB, Booth FW. Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68: 1-12, 1990.
49. Thompson LV, Durand D, Fugere NA, Ferrington DA. Myosin and actin expression and oxidation in aging muscle. J Appl Physiol 101: 1581-1587, 2006.
50. Uchida K, Hasui Y, Osawa T. Covalent attachment of 4-hydroxy-2-nonenal to erythrocyte proteins. J Biochem 122: 1246-1251, 1997.
51. Vermaelen M, Marini JF, Chopard A, Benyamin Y, Mercier J, Astier C. Ubiquitin targeting of rat muscle proteins during short periods of unloading. Acta Physiol Scand 185: 33-40, 2005.
52. 2+-ATPase in skeletal muscle. Biochem J 340: 657-669, 1999.
53. Windpassinger C, Schoser B, Straub V, Hochmeister S, Noor A, Lohberger B, Farra N, Petek E, Schwarzbraun T, Ofner L, Loscher WN, Wagner K, Lochmuller H, Vincent JB, Quasthoff S. An X-linked myopathy with postural muscle atrophy and generalized hypertrophy, termed XMPMA, is caused by mutations in FHL1. Am J Hum Genet 82: 88-99, 2008.
54. Yimlamai T, Dodd SL, Borst SE, Park S. Clenbuterol induces muscle-specific attenuation of atrophy through effects on the ubiquitin-proteasome pathway. J Appl Physiol 99: 71-80, 2005.
55. Zainal TA, Oberley TD, Allison DB, Szweda LI, Weindruch R. Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB J 14: 1825-1836, 2000.
56. Zergeroglu MA, McKenzie MJ, Shanely RA, Van Gammeren D, DeRuisseau KC, Powers SK. Mechanical ventilation-induced oxidative stress in the diaphragm. J Appl Physiol 95: 1116-1124, 2003.
57. Zhong S, Lowe DA, Thompson LV. Effects of hindlimb unweighting and aging on rat semimembranosus muscle and myosin. J Appl Physiol 101: 873-880, 2006.
58. Zimmerman UJ, Wang P, Zhang X, Bogdanovich S, Forster R. Anti-oxidative response of carbonic anhydrase III in skeletal muscle. IUBMB Life 56: 343-347, 2004.