Redox remodeling is pivotal in murine diaphragm muscle adaptation to chronic sustained hypoxia

American Journal of Respiratory Cell and Molecular Biology

Volumn 55, Issue 1, 2016, Pages 12-23

  Lewis, Philip ^a   Sheehan, David ^b   Soares, Renata ^c   Coelho, Ana Varela ^c   O'Halloran, Ken D ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Antioxidants; Cell signaling; Diaphragm; Function; Hypoxia

Indexed keywords

ANTIOXIDANT; CATALASE; CHYMOTRYPSIN; GLYCOLYTIC ENZYME; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEASOME; TRANSCRIPTION FACTOR FKHRL1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; THIOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHRONIC SUSTAINED HYPOXIA; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DIAPHRAGM; DISEASE DURATION; ENZYME ACTIVITY; HOMEOSTASIS; HYPOXIA; MOUSE; NONHUMAN; PROTEIN CARBONYLATION; PROTEIN CONTENT; PROTEOMICS; REDOX STRESS; SIGNAL TRANSDUCTION; ADAPTATION; ANIMAL; C57BL MOUSE; CHRONIC DISEASE; DISEASE MODEL; METABOLISM; MUSCLE CONTRACTION; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PHOSPHORYLATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIOXIDANTS; CHRONIC DISEASE; DIAPHRAGM; DISEASE MODELS, ANIMAL; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE CONTRACTION; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CARBONYLATION; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS;

EID: 84988958177     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2015-0272OC     Document Type: Article

References (57)

1. Puig-Vilanova E, Rodriguez DA, Lloreta J, Ausin P, Pascual-Guardia S, Broquetas J, Roca J, Gea J, Barreiro E. Oxidative stress, redox signaling pathways, and autophagy in cachectic muscles of male patients with advanced COPD and lung cancer. Free Radic Biol Med 2015;79:91-108.
2. Marquis K, DebigaréR, Lacasse Y, LeBlanc P, Jobin J, Carrier G, Maltais F. Midthigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002;166:809-813.
3. Mostert R, Goris A, Weling-Scheepers C, Wouters EF, Schols AM. Tissue depletion and health related quality of life in patients with chronic obstructive pulmonary disease. Respir Med 2000;94:859-867.
4. Gray-Donald K, Gibbons L, Shapiro SH, Macklem PT, Martin JG. Nutritional status and mortality in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996;153:961-966.
5. Zielinski J, MacNee W, Wedzicha J, Ambrosino N, Braghiroli A, Dolensky J, Howard P, Gorzelak K, Lahdensuo A, Strom K, et al. Causes of death in patients with COPD and chronic respiratory failure. Monaldi Arch Chest Dis 1997;52:43-47.
6. Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas JM, Gea J. Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;164: 1734-1739.
7. Saglam M, Vardar-Yagli N, Savci S, Inal-Ince D, Calik-Kutukcu E, Arikan H, Coplu L. Functional capacity, physical activity, and quality of life in hypoxemic patients with chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2015;10: 423-428.
8. DebigaréR, Marquis K, CôtéCH, Tremblay RR, Michaud A, LeBlanc P, Maltais F. Catabolic/anabolic balance and muscle wasting in patients with COPD. Chest 2003;124:83-89.
9. Koechlin C, Maltais F, Saey D, Michaud A, LeBlanc P, Hayot M, Préfaut C. Hypoxaemia enhances peripheral muscle oxidative stress in chronic obstructive pulmonary disease. Thorax 2005;60: 834-841.
10. Kent BD, Mitchell PD, McNicholas WT. Hypoxemia in patients with COPD: cause, effects, and disease progression. Int J Chron Obstruct Pulmon Dis 2011;6:199-208.
11. McMorrow C, Fredsted A, Carberry J, O?Connell RA, Bradford A, Jones JFX, O?Halloran KD. Chronic hypoxia increases rat diaphragm muscle endurance and sodium-potassium ATPase pump content. Eur Respir J 2011;37:1474-1481.
12. Gamboa JL, Andrade FH. Muscle endurance and mitochondrial function after chronic normobaric hypoxia: contrast of respiratory and limb muscles. Pflugers Arch 2012;463:327-338.
13. Mador MJ, Kufel TJ, Pineda LA, Sharma GK. Diaphragmatic fatigue and high-intensity exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000;161:118-123.
14. Degens H, Bosutti A, Gilliver SF, Slevin M, van Heijst A, Wüst RCI. Changes in contractile properties of skinned single rat soleus and diaphragm fibres after chronic hypoxia. Pflugers Arch 2010;460: 863-873.
15. Ottenheijm CA, Heunks LM, Sieck GC, Zhan WZ, Jansen SM, Degens H, de Boo T, Dekhuijzen PNR. Diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2005; 172:200-205.
16. Wijnhoven JH, Janssen AJ, van Kuppevelt TH, Rodenburg RJT, Dekhuijzen PNR. Metabolic capacity of the diaphragm in patients with COPD. Respir Med 2006;100:1064-1071.
17. Marin-Corral J, Minguella J, Ramírez-Sarmiento AL, Hussain SNA, Gea J, Barreiro E. Oxidised proteins and superoxide anion production in the diaphragm of severe COPD patients. Eur Respir J 2009;33: 1309-1319.
18. Levine S, Gregory C, Nguyen T, Shrager J, Kaiser L, Rubinstein N, Dudley G. Bioenergetic adaptation of individual human diaphragmatic myofibers to severe COPD. J Appl Physiol (1985) 2002;92:1205-1213.
19. Doucet M, DubéA, Joanisse DR, DebigaréR, Michaud A, Paré MÈ, Vaillancourt R, Fréchette E, Maltais F. Atrophy and hypertrophy signalling of the quadriceps and diaphragm in COPD. Thorax 2010; 65:963-970.
20. Gamboa JL, Andrade FH. Mitochondrial content and distribution changes specific to mouse diaphragm after chronic normobaric hypoxia. Am J Physiol Regul Integr Comp Physiol 2010;298: R575-R583.
21. Lewis P, Sheehan D, Soares R, Varela Coelho A, O?Halloran KD. Chronic sustained hypoxia-induced redox remodeling causes contractile dysfunction in mouse sternohyoid muscle. Front Physiol 2015;6:122.
22. 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 1998;509:565-575.
23. Cano I, Selivanov V, Gomez-Cabrero D, Tegnér J, Roca J, Wagner PD, Cascante M. Oxygen pathway modeling estimates high reactive oxygen species production above the highest permanent human habitation. PLoS One 2014;9:e111068.
24. Chaudhary P, Suryakumar G, Prasad R, Singh SN, Ali S, Ilavazhagan G. Chronic hypobaric hypoxia mediated skeletal muscle atrophy: role of ubiquitin-proteasome pathway and calpains. Mol Cell Biochem 2012;364:101-113.
25. Williams R, Lemaire P, Lewis P, McDonald FB, Lucking E, Hogan S, Sheehan D, Healy V, O?Halloran KD. Chronic intermittent hypoxia increases rat sternohyoid muscle NADPH oxidase expression with attendant modest oxidative stress. Front Physiol 2015;6:15.
26. Chaudhary P, Suryakumar G, Sharma YK, Ilavazhagan G. Differential response of the gastrocnemius and soleus muscles of rats to chronic hypobaric hypoxia. Aviat Space Environ Med 2012;83:1037-1043.
27. Thomas S, Fell DA. The role of multiple enzyme activation in metabolic flux control. Adv Enzyme Regul 1998;38:65-85.
28. Barreiro E, Gea J, Di Falco M, Kriazhev L, James S, Hussain SNA. Protein carbonyl formation in the diaphragm. Am J Respir Cell Mol Biol 2005;32:9-17.
29. Lustgarten MS, Jang YC, Liu Y, Muller FL, Qi W, Steinhelper M, Brooks SV, Larkin L, Shimizu T, Shirasawa T, et al. Conditional knockout of Mn-SOD targeted to type IIB skeletal muscle fibers increases oxidative stress and is sufficient to alter aerobic exercise capacity. Am J Physiol Cell Physiol 2009;297:C1520-C1532.
30. Boutilier RG. Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 2001;204:3171-3181.
31. Hochachka PW, Gunga HC, Kirsch K. Our ancestral physiological phenotype: an adaptation for hypoxia tolerance and for endurance performance? Proc Natl Acad Sci USA 1998;95:1915-1920.
32. Ramirez JM, Folkow LP, Blix AS. Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol 2007;69: 113-143.
33. Scholander PF, Irving L, Grinnell SW. On the temperature and metabolism of the seal during diving. J Cell Comp Physiol 1942;19:67-78.
34. Storey KB, Storey JM. Metabolic rate depression: the biochemistry of mammalian hibernation. Adv Clin Chem 2010;52:77-108.
35. Sheafor BA. Metabolic enzyme activities across an altitudinal gradient: an examination of pikas (genus Ochotona). J Exp Biol 2003;206: 1241-1249.
36. Emerling BM, Platanias LC, Black E, Nebreda AR, Davis RJ, Chandel NS. Mitochondrial reactive oxygen species activation of p38 mitogen-activated protein kinase is required for hypoxia signaling. Mol Cell Biol 2005;25:4853-4862.
37. Bonello S, Zähringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C, Kietzmann T, Görlach A. Reactive oxygen species activate the HIF-1a promoter via a functional NFkB site. Arter Thromb Vasc Biol 2007; 27:755-761.
38. Jung SN, Yang WK, Kim J, Kim HS, Kim EJ, Yun H, Park H, Kim SS, Choe W, Kang I, et al. Reactive oxygen species stabilize hypoxiainducible factor-1 a protein and stimulate transcriptional activity via AMP-activated protein kinase in DU145 human prostate cancer cells. Carcinogenesis 2008;29:713-721.
39. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 1996;271:32529-32537.
40. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005;2005:re12.
41. Yuan G, Peng YJ, Reddy VD, Makarenko VV, Nanduri J, Khan SA, Garcia JA, Kumar GK, Semenza GL, Prabhakar NR. Mutual antagonism between hypoxia-inducible factors 1a and 2a regulates oxygen sensing and cardio-respiratory homeostasis. Proc Natl Acad Sci USA 2013;110:E1788-E1796.
42. Testelmans D, Crul T, Maes K, Agten A, Crombach M, Decramer M, Gayan-Ramirez G. Atrophy and hypertrophy signalling in the diaphragm of patients with COPD. Eur Respir J 2010;35: 549-556.
43. Grant CM. Metabolic reconfiguration is a regulated response to oxidative stress. J Biol 2008;7:1.
44. Holm L, Haslund ML, Robach P, van Hall G, Calbet JA, Saltin B, Lundby C. Skeletal muscle myofibrillar and sarcoplasmic protein synthesis rates are affected differently by altitude-induced hypoxia in native lowlanders. PLoS One 2010;5:e15606.
45. Imoberdorf R, Garlick PJ, McNurlan MA, Casella GA, Marini JC, Turgay M, Bärtsch P, Ballmer PE. Skeletal muscle protein synthesis after active or passive ascent to high altitude. Med Sci Sports Exerc 2006; 38:1082-1087.
46. Derbre F, Ferrando B, Gomez-Cabrera MC, Sanchis-Gomar F, Martinez-Bello VE, Olaso-Gonzalez G, Diaz A, Gratas-Delamarche A, Cerda M, Viña J. Inhibition of xanthine oxidase by allopurinol prevents skeletal muscle atrophy: role of p38 MAPKinase and E3 ubiquitin ligases. PLoS One 2012;7:e46668.
47. Lemire BB, DebigaréR, DubéA, Thériault ME, CôtéCH, Maltais F. MAPK signaling in the quadriceps of patients with chronic obstructive pulmonary disease. J Appl Physiol (1985) 2012;113:159-166.
48. Jia YT, Wei W, Ma B, Xu Y, Liu WJ, Wang Y, Lv KY, Tang HT, Wei D, Xia ZF. Activation of p38 MAPK by reactive oxygen species is essential in a rat model of stress-induced gastric mucosal injury. J Immunol 2007;179:7808-7819.
49. Hsieh CC, Papaconstantinou J. Thioredoxin-ASK1 complex levels regulate ROS-mediated p38 MAPK pathway activity in livers of aged and long-lived Snell dwarf mice. FASEB J 2006;20:259-268.
50. Shiota S, Okada T, Naitoh H, Ochi R, Fukuchi Y. Hypoxia and hypercapnia affect contractile and histological properties of rat diaphragm and hind limb muscles. Pathophysiology 2004;11:23-30.
51. El-Khoury R, O?Halloran KD, Bradford A. Effects of chronic hypobaric hypoxia on contractile properties of rat sternohyoid and diaphragm muscles. Clin Exp Pharmacol Physiol 2003;30:551-554.
52. Nguyen T, Rubinstein NA, Vijayasarathy C, Rome LC, Kaiser LR, Shrager JB, Levine S. Effect of chronic obstructive pulmonary disease on calcium pump ATPase expression in human diaphragm. J Appl Physiol (1985) 2005;98:2004-2010.
53. van Hees H, Ottenheijm C, Ennen L, Linkels M, Dekhuijzen R, Heunks L. Proteasome inhibition improves diaphragm function in an animal model for COPD. Am J Physiol Lung Cell Mol Physiol 2011;301: L110-L116.
54. Roussos C, Grassino A, Macklem PT. Inspiratory muscle fatigue and acute respiratory failure. Can Med Assoc J 1980;122:1375-1377.
55. Levine S, Nguyen T, Kaiser LR, Rubinstein NA, Maislin G, Gregory C, Rome LC, Dudley GA, Sieck GC, Shrager JB. Human diaphragm remodeling associated with chronic obstructive pulmonary disease: clinical implications. Am J Respir Crit Care Med 2003;168: 706-713.
56. Shortt CM, Fredsted A, Chow HB, Williams R, Skelly JR, Edge D, Bradford A, O?Halloran KD. Reactive oxygen species mediated diaphragm fatigue in a rat model of chronic intermittent hypoxia. Exp Physiol 2014;99:688-700.
57. van Lunteren E, Pollarine J, Moyer M. Isotonic contractile impairment due to genetic CLC-1 chloride channel deficiency in myotonic mouse diaphragm muscle. Exp Physiol 2007;92:717-729.