Strenuous resistive breathing induces proinflammatory cytokines and stimulates the HPA axis in humans

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 277, Issue 4 46-4, 1999, Pages

  Vassilakopoulos, Theodoros ^a,b   Zakynthinos, Spyros ^a   Roussos, Charis ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b EVANGELISMOS HOSPITAL   (Greece)

Author keywords

Adrenocorticotropic hormone; Interleukin 1; Interleukin 6; Respiratory muscles; endorphin

Indexed keywords

BETA ENDORPHIN; CORTICOTROPIN; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ARTICLE; BLOOD LEVEL; BREATHING EXERCISE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MUSCLE FATIGUE; NORMAL HUMAN; PRIORITY JOURNAL;

EID: 0032719635     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.1999.277.4.r1013     Document Type: Article

References (47)

1. Ala, Y., O. Palluy, J. Favero, C. Bonne, G. Modat, and J. Dornand. Hypoxia/reoxygenation stimulates endothelial cells to promote interleukin-1 and interleukin-6 production. Effects of free radical scavengers. Agents Actions 37: 134-139, 1992.
2. Anzueto, A., F. H. Andrate, L. C. Maxwell, S. M. Levine, R. A. Lawrence, W. J. Gibbons, and S. G. Jenkinson. Resistive breathing activates the glutathione redox cycle and impairs performance of the rat diaphragm. J. Appl. Physiol. 72: 529-534, 1992.
3. Anzueto, A., G. S. Supinski, S. M. Levine, and S. G. Jenkinson. Methods of disease: are oxygen derived free radicals involved in diaphragmatic dysfunction? Am. J. Respir. Crit. Care Med. 149: 1048-1052, 1994.
4. Baeuerle, P. A., and T. Henkel. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12: 141-179, 1994.
5. Bury, T. B., R. Louis, M. F. Radermemecker, and F. Pirnay. Blood mononuclear cell mobilization and cytokines secretion during prolonged exercises. Int. J. Sports Med. 17: 156-160, 1996.
6. Cannon, J. G., S. N. Meydani, R. A. Fielding, M. A. Fiatarone, M. Meydani, M. Farhangmehr, S. F. Orencole, J. B. Blumberg, and W. J. Evans. Acute phase response in exercise. II. Associations between vitamin E, cytokines, and muscle proteolysis. Am. J. Physiol. 260 (Regulatory Integrative Comp. Physiol. 29): R1235-R1240, 1991.
7. Cannon, J. G., J. L. Nerad, D. D. Poutsiaka, and C. A. Dinarello. Measuring circulating cytokines. J. Appl. Physiol. 75: 1897-1902, 1993.
8. Chrousos, G. P. The hypothalamic-pituitary-adrenal' axis and immune-mediated inflammation. N. Engl. J. Med. 332: 1351-1361, 1995.
9. Drenth, J. P., S. H. M. Van Uum, M. Van Deuren, G. J. Pesman, J. Van Der VenJongekrijg, and J. W. M. Van Der Meer. Endurance run increases circulating IL-6 and IL-1ra but downregulates ex vivo TNF-a and IL-1β production. J. Appl. Physiol. 79: 1497-1503, 1995.
10. Friden, J., and R. L. Lieber. Structural and mechanical basis of exercise-induced muscle injury. Med. Sci. Sports Exerc. 24: 521-530, 1992.
11. Gallagher, C. G., V. I. Hof, and M. Younes. Effect of inspiratory muscle fatigue on breathing pattern. J. Appl. Physiol. 59: 1152-1158, 1985.
12. Guillemin, R., T. Vargo, and J. Rossier. β-Endorphin and adrenocorticotropin are secreted concomitantly by the pituitary gland. Science 197: 1367-1369, 1977.
13. Hale, A. C., and L. H. Rees. ACTH and related peptides In: Endocrinology (2nd ed.), edited by L. J. DeGroot. Philadelphia: Saunders, 1989, p. 363-374.
14. Hussain, S. N. A., A. Chatillon, A. Comtois, C. Roussos, and S. Magder. Chemical activation of thin-fiber phrenic afferents. II. Cardiovascular responses. J. Appl. Physiol. 70: 77-86, 1991.
15. Hussain, S. N. A., S. Magder, A. Chatillon, and C. Roussos. Chemical activation of thin-fiber phrenic afferents: respiratory responses. J. Appl. Physiol. 69: 1002-1011, 1990.
16. Hussain, S. N. A., and C. Roussos. The role of small-fiber phrenic afferents in the control of breathing. In: The Thorax (2nd ed.), edited by C. Roussos. New York: Dekker, 1995, p. 869-901.
17. Jammes, Y., and E. Balzamo. Changes in afferent and efferent phrenic activities with electrically induced diaphragmatic fatigue. J. Appl. Physiol. 73: 894-902, 1992.
18. Jiang, T.-X., D. W. Reid, and D. J. Road. Delayed diaphragm injury and diaphragm force production. Am. J. Respir. Crit. Care Med. 157: 736-742, 1998.
19. Jirik, F. R., T. J. Podor, T. Hirano, T. Kishimoto, D. J. Loskutoff, D. A. Carson, and M. Lotz. Bacterial lipopolysaccharide and inflammatory mediators augment IL-6 secretion by human endothelial cells. J. Immunol. 142: 144-147, 1989.
20. Kjoer, A., U. Knigge, F. W. Bach, and J. Warberg. Stress induced secretion of pro-opiomelanocortin-derived peptides in rats: relative importance of the anterior and intermediate pituitary lobes. Neuroendocrinology 61: 167-172, 1995.
21. Liebermann, T. A., and D. Baltimore. Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 10: 2327-2334, 1990.
22. 2. J. Physiol. (Lond.) 455: 17-32, 1992.
23. Mastorakos, G., G. P. Chrousos, and J. S. Weber. Recombinant interleukin-6 activates the hypothalamic-pituitary-adrenal axis in humans. J. Clin. Endocrinol. Metab. 77: 1690-1694, 1993.
24. Mastorakos, G., J. S. Weber, M. A. Magiakou, H. Gunn, and G. P. Chrousos. Hypothalamic-pituitary-adrenal axis activation and stimulation of systemic vasopressin secretion by recombinant interleukin-6 in humans: potential implications for the syndrome of inappropriate vasopressin secretion. J. Clin. Endocrinol. Metab. 79: 934-939, 1994.
25. Matuschak, G. M. Oxidative stress and oxygen-dependent cytokine production. In: Yearbook of Intensive Care and Emergency Medicine, edited by J.-L. Vincent. Berlin: Springer Verlag, 1995, p. 413-421.
26. Neta, R., S. N. Vogel, J. D. Sipe, G. G. Wong, and R. P. Nordan. Comparison of in vivo effects of human recombinant IL-1β and human recombinant IL-6 in mice. Lymphokine Res 7: 403-412, 1988.
27. Nieman, D. C. Immune response to heavy exertion. J. Appl. Physiol. 82: 1385-1394, 1997.
28. Ostrowski, K., T. Rohde, M. Zacho, S. Asp, and B. K. Pedersen. Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J. Physiol. (Lond.) 508: 949-953, 1998.
29. Papanicolaou, D. A., J. S. Petrides, C. Tsigos, S. Bina, K. T. Kalogeras, R. Wilder, P. W. Gold, P. A. Deuster, and G. P. Chroussos. Exercise stimulates interleukin-6 secretion: inhibition by glucorticoids and correlation with catecholamines. Am. J. Physiol. 271 (Endocrinol. Metab. 34): E601-E605, 1996.
30. Perlstein, R. S., M. H. Whitall, J. S. Abrams, E. H. Mougey, and R. Neta. Synergistic roles of interleukin-6, interleukin-1, and tumor necrosis factor in the adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology 132: 946-952, 1993.
31. Petrozzino, J. J., A. T. Scardella, N. H. Edelman, and T. V. Santiago. Respiratory muscle acidosis stimulates endogenous opioids during inspiratory loading. Am. Rev. Respir. Dis. 144: 607-615, 1993.
32. Petrozzino, J. J., A. T. Scardella, T. V. Santiago, and N. H. Edelman. Dichloroacetate blocks endogeous opiod effects during inspiratory flow resistive loading. J. Appl. Physiol. 72: 590-596, 1992.
33. Roussos, C., and N. Campbell. Respiratory muscle energetics. In: Handbook of Physiology. The Respiratory System. Mechanics of Breathing. Bethesda, MD: Am. Physiol. Soc., 1983, sect. 3, vol. III, pt. 2, chapt. 28, p. 481-509.
34. Roussos, C., M. Fixley, D. Gross, and P. T. Macklem. Fatigue of inspiratory muscles and their synergic behavior. J. Appl. Physiol. 46: 897-904, 1979.
35. Roussos, C., and P. T. Macklem. Diaphragmatic fatigue in man. J. Appl. Physiol. 43: 189-197, 1977.
36. Santiago, T. V., and N. H. Edelman. Opioids and breathing. J. Appl. Physiol. 59: 1675-1685, 1985.
37. Scardella, A. T., R. A. Parisi, D. K. Phair, T. V. Santiago, and N. H. Edelman. The role of endogenous opioids in the ventilatory response to acute flow-resistive loads. Am. Rev. Respir. Dis. 133: 26-31, 1986.
38. Sehgal, P. B., G. Grieninger, and G. Tosato. Regulation of the acute phase and immune responses: interleukin-6. Ann. NY Acad. Sci. 1: 557-583, 1989.
39. Sen, C. K. Oxidants and antioxidants in exercise. J. Appl. Physiol. 79: 675-686, 1995.
40. Shindoh, C., W. Hida, Y. Ohkawawara, K. Yamacuhi, I. Ohno, T. Takishima, and K. Shirato. TNF-α mRNA expression in diaphragm muscle after endotoxin administration. Am. J. Respir. Crit. Care Med. 152: 1690-1696, 1995.
41. Smith, J. A., R. D. Telford, M. S. Baker, A. J. Hapel, and M. J. Weidemann. Cytokine immunoreactivity in plasma does not change after moderate endurance exercise. J. Appl. Physiol. 73: 1396-1401, 1992.
42. Turnbull, A. V., and C. L. Rivier. Regulation of hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol. Rev. 79: 1-71, 1999.
43. Ullum, H., P. M. Haahr, M. Diamant, J. Palmo, J. Halkjaer-Kristensen, and B. K. Pedersen. Bicycle exercise enhances plasma IL-6 but does not change IL-1α, IL-1β, IL-6 or TNF-α pre-mRNA in BMNC. J. Appl. Physiol. 77: 93-97, 1994.
44. Vassilakopoulos, T., S. Zakynthinos, and C. Roussos. Weaning failure and the respiratory muscles. Eur. Respir. J. 9: 2383-2400, 1996.
45. Wanke, T., H. Lahrmann, M. Auinger, M. Merkle, D. Formanek, E. Ogris, K. Irsigler, and H. Zwick. Endogenous opioid system during inspiratory loading in patients with type I diabetes. Am. Rev. Respir. Dis. 148: 1335-40, 1993.
46. Watanabe, T. A., A. Morimoto A., N. Tan, T. Makisumi S. Shimada, T. Nakamori, and N. Murakami. ACTH response induced in capsaicin-desensitized rats by interleukin-1 or prostaglandin E. J. Physiol. (Lond.) 475: 139-145, 1994.
47. Zhe, E., B. J. Petrof, J. Gea, N. Comtois, and A. Grassino. Diaphragm muscle fiber injury after inspiratory resistive breathing. Am. J. Respir. Crit. Care Med. 155: 1110-1116, 1997.