The immune response to resistive breathing

European Respiratory Journal

Volumn 24, Issue 6, 2004, Pages 1033-1043

  Vassilakopoulos, T ^a   Roussos, C ^a   Zakynthinos, S ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Control of breathing; Exercise immunology; Interleukin 6; Oxidants antioxidants; Respiratory immunology; Respiratory muscle

Indexed keywords

ACUTE PHASE PROTEIN; BETA ENDORPHIN; CORTICOTROPIN; CYTOKINE; FATTY ACID; GLUCOCORTICOID; GLUCOSE;

ADIPOSE TISSUE; ARTICLE; BREATHING DISORDER; BREATHING MUSCLE; BREATHING PATTERN; CACHEXIA; CELL DAMAGE; CYTOKINE PRODUCTION; DIAPHRAGM; GLUCOSE METABOLISM; HORMONAL REGULATION; HORMONE RESPONSE; HORMONE SYNTHESIS; HUMAN; HYPOPHYSIS ADRENAL SYSTEM; IMMUNE RESPONSE; LIVER; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; LYMPHOCYTE SUBPOPULATION; MONOCYTE; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE CONTRACTION; NONHUMAN; OXIDATIVE STRESS; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN INDUCTION; TACHYPNEA; TISSUE REPAIR;

AIRWAY RESISTANCE; ASTHMA; CYTOKINES; EXERCISE; HUMANS; OXIDATIVE STRESS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE;

EID: 10444257256     PISSN: 09031936     EISSN: None     Source Type: Journal    
DOI: 10.1183/09031936.04.00067904     Document Type: Article

References (83)

1. Roussos CS, Macklem PT. Diaphragmatic fatigue in man. J Appl Physiol 1977; 43: 189-197.
2. Reid WD, Belcastro AN. Time course of diaphragm injury and calpain activity during resistive loading. Am J Respir Crit Care Med 2000; 162: 1801-1806.
3. 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.
4. Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000; 80: 1055-1081.
5. Vassilakopoulos T, Zakynthinos S, Roussos C. Strenuous resistive breathing induces proinflammatory cytokines and stimulates the HPA axis in humans. Am J Physiol 1999; 277: R1013-R1019.
6. Vassilakopoulos T, Katsaounou P, Karatza MH, Kollintza A, Zakynthinos S, Roussos C. Strenuous resistive breathing induces plasma cytokines: role of antioxidants and monocytes. Am J Respir Crit Care Med 2002; 166: 1572-1578.
7. Katsaounou P, Karatza MH, Kollintza A, et al. The immune response to strenuous resistive breathing (abstract). Am J Respir Crit Care Med 2001; 163: A621.
8. van Furth R. Human monocytes and cytokines. Res Immunol 1998; 149: 719-720.
9. Bosenberg AT, Brock-Utne JG, Gaffin SL, Wells MT, Blake GT. Strenuous exercise causes systemic endotoxemia. J Appl Physiol 1988; 65: 106-108.
10. Steppich B, Dayyani F, Gruber R, Lorenz R, Mack M, Ziegler-Heitbrock HW. Selective mobilization of CD14(+)CD16(+) monocytes by exercise. Am J Physiol Cell Physiol 2000; 279: C578-C586.
11. Prussin C. Cytokine flow cytometry: understanding cytokine biology at the single-cell level. J Clin Immunol 1997; 17: 195-204.
12. Saghizadeh M, Ong JM, Garvey WT, Henry RR, Kern PA. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest 1996; 97: 1111-1116.
13. Belec L, Authier FJ, Chazaud B, Piedouillet C, Barlovatz-Meimon G, Gherardi RK. Interleukin (IL)-1 beta and IL-1 beta mRNA expression in normal and diseased skeletal muscle assessed by immunocytochemistry, immunoblotting and reverse transcriptase-nested polymerase chain reaction. J Neuropathol Exp Neurol 1997; 56: 651-663.
14. Keller C, Steensberg A, Pilegaard H, et al. Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J 2001; 15: 2748-2750.
15. Vassilakopoulos T, Divangahi M, Rallis G, et al. Differential cytokine gene expression in the diaphragm in response to strenuous resistive breathing. Am J Respir Crit Care Med 2004; 170: 154-161.
16. Oh-ishi S, Kizaki T, Ookawara T, et al. Endurance training improves the resistance of rat diaphragm to exercise-induced oxidative stress. Am J Respir Crit Care Med 1997; 156: 1579-1585.
17. Wang T, Brown MJ. mRNA quantification by real time TaqMan polymerase chain reaction: validation and comparison with RNase protection. Anal Biochem 1999; 269: 198-201.
18. Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund PB. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 2000; 529: 237-242.
19. von Bethmann AN, Brasch F, Nusing R, et al. Hyperventilation induces release of cytokines from perfused mouse lung. Am J Respir Crit Care Med 1998; 157: 263-272.
20. Zakynthinos SG, Vassilakopoulos T, Roussos C. The load of inspiratory muscles in patients needing mechanical ventilation. Am J Respir Crit Care Med 1995; 152: 1248-1255.
21. Ronsen O, Lea T, Bahr R, Pedersen BK. Enhanced plasma IL-6 and IL-1ra responses to repeated versus single bouts of prolonged cycling in elite athletes. J Appl Physiol 2002; 92: 2547-2553.
22. Rabinovich RA, Figueras M, Ardite E, et al. Increased tumour necrosis factor-alpha plasma levels during moderate-intensity exercise in COPD patients. Eur Respir J 2003; 21: 789-794.
23. Reid MB. Invited review: redox modulation of skeletal muscle contraction: what we know and what we don't. J Appl Physiol 2001; 90: 724-731.
24. Kosmidou I, Vassilakopoulos T, Xagorari A, Zakynthinos S, Papapetropoulos A, Roussos C. Production of interleukin-6 by skeletal myotubes: role of reactive oxygen species. Am J Respir Cell Mol Biol 2002; 26: 587-593.
25. Pedersen BK, Steensberg A, Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol 2001; 536: 329-337.
26. Ciufo R, Dimarco A, Stofan D, Nethery D, Supinski G. Dichloroacetate reduces diaphragmatic lactate formation but impairs respiratory performance. Am J Respir Crit Care Med 2001; 164: 1669-1674.
27. Jiang TX, Darlene RW, Road JD. Free radical scavengers and diaphragm injury following inspiratory resistive loading. Am J Respir Crit Care Med 2001; 164: 1288-1294.
28. Cannon JG, St Pierre BA. Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem 1998; 179: 159-167.
29. Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG. Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol 1993; 265: R166-R172.
30. Reid MB, Li YP. Cytokines and oxidative signalling in skeletal muscle. Acta Physiol Scand 2001; 171: 225-232.
31. Warren GL, Hulderman T, Jensen N, et al. Physiological role of tumour necrosis factor alpha in traumatic muscle injury. FASEB J 2002; 16: 1630-1632.
32. De Letter MA, van Doorn PA, Savelkoul HF, et al. Critical illness polyneuropathy and myopathy (CIPNM): evidence for local immune activation by cytokine-expression in the muscle tissue. J Neuroimmunol 2000; 106: 206-213.
33. Xing Z, Gauldie J, Cox G, et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest 1998; 101: 311-320.
34. Kami K, Senba E. Localization of leukemia inhibitory factor and interleukin-6 messenger ribonucleic acids in regenerating rat skeletal muscle. Muscle Nerve 1998; 21: 819-822.
35. Kurek JB, Nouri S, Kannourakis G, Murphy M, Austin L. Leukemia inhibitory factor and interleukin-6 are produced by diseased and regenerating skeletal muscle. Muscle Nerve 1996; 19: 1291-1301.
36. Cannon JG, Fielding RA, Fiatarone MA, Orencole SF, Dinarello CA, Evans WJ. Increased interleukin 1 beta in human skeletal muscle after exercise. Am J Physiol 1989; 257: R451-R455.
37. Kami K, Morikawa Y, Sekimoto M, Senba E. Gene expression of receptors for IL-6, LIF, and CNTF in regenerating skeletal muscles. J Histochem Cytochem 2000; 48: 1203-1213.
38. Llovera M, Carbo N, Lopez-Soriano J, et al. Different cytokines modulate ubiquitin gene expression in rat skeletal muscle. Cancer Lett 1998; 133: 83-87.
39. Tsujinaka T, Kishibuchi M, Yano M, et al. Involvement of interleukin-6 in activation of lysosomal cathepsin and atrophy of muscle fibers induced by intramuscular injection of turpentine oil in mice. J Biochem (Tokyo) 1997; 122: 595-600.
40. Li YP. TNF-alpha is a mitogen in skeletal muscle. Am J Physiol Cell Physiol 2003; 285: C370-C376.
41. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001; 91: 534-551.
42. Wilcox P, Milliken C, Bressler B. High-dose tumour necrosis factor alpha produces an impairment of hamster diaphragm contractility. Attenuation with a prostaglandin inhibitor. Am J Respir Crit Care Med 1996; 153: 1611-1615.
43. Reid MB, Lannergren J, Westerblad H. Respiratory and limb muscle weakness induced by tumour necrosis factor-alpha: involvement of muscle myofilaments. Am J Respir Crit Care Med 2002; 166: 479-484.
44. Li X, Moody MR, Engel D, et al. Cardiac-specific overexpression of tumour necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation 2000; 102: 1690-1696.
45. Wilcox PG, Wakai Y, Walley KR, Cooper DJ, Road J. Tumour necrosis factor alpha decreases in vivo diaphragm contractility in dogs. Am J Respir Crit Care Med 1994; 150: 1368-1373.
46. Jiang TX, Reid WD, Road JD. Delayed diaphragm injury and diaphragm force production. Am J Respir Crit Care Med 1998; 157: 736-742.
47. Vernooy JH, Kucukaycan M, Jacobs JA, et al. Local and systemic inflammation in patients with chronic obstructive pulmonary disease: soluble tumour necrosis factor receptors are increased in sputum. Am J Respir Crit Care Med 2002; 166: 1218-1224.
48. Eid AA, Ionescu AA, Nixon LS, et al. Inflammatory response and body composition in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001; 164: 1414-1418.
49. Godoy I, Campana AO, Geraldo RR, Padovani CR, Paiva SA. Cytokines and dietary energy restriction in stable chronic obstructive pulmonary disease patients. Eur Respir J 2003; 22: 920-925.
50. Koechlin C, Couillard A, Cristol JP, et al. Does systemic inflammation trigger local exercise-induced oxidative stress in COPD? Eur Respir J 2004; 23: 538-544.
51. Wedzicha JA, Seemungal TA, MacCallum PK, et al. Acute exacerbations of chronic obstructive pulmonary disease are accompanied by elevations of plasma fibrinogen and serum IL-6 levels. Thromb Haemost 2000; 84: 210-215.
52. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Sleep apnoea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Clin Endocrinol Metab 2000; 85: 1151-1158.
53. Roytblat L, Rachinsky M, Fisher A, et al. Raised interleukin-6 levels in obese patients. Obes Res 2000; 8: 673-675.
54. Yokoe T, Minoguchi K, Matsuo H, et al. Elevated levels of C-reactive protein and interleukin-6 in patients with obstructive sleep apnoea syndrome are decreased by nasal continuous positive airway pressure. Circulation 2003; 107: 1129-1134.
55. Alberti A, Sarchielli P, Gallinella E, et al. Plasma cytokine levels in patients with obstructive sleep apnoea syndrome: a preliminary study. J Sleep Res 2003; 12: 305-311.
56. Klausen T, Olsen NV, Poulsen TD, Richalet JP, Pedersen BK. Hypoxemia increases serum interleukin-6 in humans. Eur J Appl Physiol Occup Physiol 1997; 76: 480-482.
57. Entzian P, Linnemann K, Schlaak M, Zabel P. Obstructive sleep apnoea syndrome and circadian rhythms of hormones and cytokines. Am J Respir Crit Care Med 1996; 153: 1080-1086.
58. Drenth JP, Van Uum SH, Van Deuren M, Pesman GJ, Van der Ven-Jongekrijg J, van der Meer JW. Endurance run increases circulating IL-6 and IL-1ra but downregulates ex vivo TNF-alpha and IL-1 beta production. J Appl Physiol 1995; 79: 1497-1503.
59. Steensberg A, Febbraio MA, Osada T, et al. Interleukin-6 production in contracting human skeletal muscle is influenced by pre-exercise muscle glycogen content. J Physiol 2001; 537: 633-639.
60. van Hall G, Steensberg A, Sacchetti M, et al. Interleukin-6 stimulates lipolysis and fat oxidation in humans. J Clin Endocrinol Metab 2003; 88: 3005-3010.
61. Faldt J, Wernstedt I, Fitzgerald SM, Wallenius K, Bergstrom G, Jansson JO. Reduced exercise endurance in interleukin-6 deficient mice. Endocrinology 2004; 145: 2680-2686.
62. Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J 2003; 17: 884-886.
63. Reid MB, Li YP. Tumour necrosis factor-alpha and muscle wasting: a cellular perspective. Respir Res 2001; 2: 269-272.
64. Debigare R, Cote CH, Maltais F. Peripheral muscle wasting in chronic obstructive pulmonary disease. Clinical relevance and mechanisms. Am J Respir Crit Care Med 2001; 164: 1712-1717.
65. Wouters EF, Creutzberg EC, Schols AM. Systemic effects in COPD. Chest 2002; 121: 127S-130S.
66. Krueger JM, Obal FJ, Fang J, Kubota T, Taishi P. The role of cytokines in physiological sleep regulation. Ann N Y Acad Sci 2001; 933: 211-221.
67. Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 1995; 332: 1351-1362.
68. Watanabe T, Morimoto A, Tan N, et al. ACTH response induced in capsaicin-desensitized rats by intravenous injection of interleukin-1 or prostaglandin E. J Physiol 1994; 475: 139-145.
69. Mastorakos G, Chrousos GP, Weber JS. Recombinant interleukin-6 activates the hypothalamic-pituitary-adrenal axis in humans. J Clin Endocrinol Metab 1993; 77: 1690-1694.
70. Turnbull AV, Rivier CL. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 1999; 79: 1-71.
71. Perlstein RS, Whitnall MH, Abrams JS, Mougey EH, Neta R. Synergistic roles of interleukin-6, interleukin-1, and tumour necrosis factor in the adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology 1993; 132: 946-952.
72. Hussain SN, Magder S, Chatillon A, Roussos C. Chemical activation of thin-fiber phrenic afferents: respiratory responses. J Appl Physiol 1990; 69: 1002-1011.
73. Graff GR, Gozal D. Cardiorespiratory responses to interleukin-1beta in adult rats: role of nitric oxide, eicosanoids and glucocorticoids. Arch Physiol Biochem 1999; 107: 97-112.
74. Preas HL, Jubran A, Vandivier RW, et al. Effect of endotoxin on ventilation and breath variability: role of cyclooxygenase pathway. Am J Respir Crit Care Med 2001; 164: 620-626.
75. Gosselin LE, Barkley JE, Spencer MJ, McCormick KM, Farkas GA. Ventilatory dysfunction in mdx mice: impact of tumour necrosis factor-alpha deletion. Muscle Nerve 2003; 28: 336-343.
76. Scardella AT, Edelman NH. Central fatigue in respiratory control. In: Charis Roussos, ed. The thorax. New York, Marcel Dekker Inc., 1995; pp. 1007-1025.
77. Petrozzino JJ, Scardella AT, Santiago TV, Edelman NH. Dichloroacetate blocks endogenous opioid effects during inspiratory flow-resistive loading. J Appl Physiol 1992; 72: 590-596.
78. Petrozzino JJ, Scardella AT, Edelman NH, Santiago TV. Respiratory muscle acidosis stimulates endogenous opioids during inspiratory loading. Am Rev Respir Dis 1993; 147: 607-615.
79. Scardella AT, Santiago TV, Edelman NH. Naloxone alters the early response to an inspiratory flow-resistive load. J Appl Physiol 1989; 67: 1747-1753.
80. Scardella AT, Parisi RA, Phair DK, Santiago TV, Edelman NH. The role of endogenous opioids in the ventilatory response to acute flow-resistive loads. Am Rev Respir Dis 1986; 133: 26-31.
81. Wanke T, Lahrmann H, Auinger M, et al. Endogenous opioid system during inspiratory loading in patients with type I diabetes. Am Rev Respir Dis 1993; 148: 1335-1340.
82. Santiago TV, Remolina C, Scoles V III, Edelman NH. Endorphins and the control of breathing. Ability of naloxone to restore flow-resistive load compensation in chronic obstructive pulmonary disease. N Engl J Med 1981; 304: 1190-1195.
83. Bellofiore S, Di Maria GU, Privitera S, Sapienza S, Milic-Emili J, Mistretta A. Endogenous opioids modulate the increase in ventilatory output and dyspnoea during severe acute bronchoconstriction. Am Rev Respir Dis 1990; 142: 812-816.