N-acetyl-1-cysteine protects intestinal lymphocytes from apoptotic death after acute exercise in adrenalectomized mice

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 288, Issue 6 57-6, 2005, Pages

  Quadrilatero, Joe ^a   Hoffman Goetz, Laurie ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Antioxidant; Apoptosis; Exercise; Glucocorticoids; Intestinal lymphocytes

Indexed keywords

ACETYLCYSTEINE; CASPASE 3; CYTOCHROME C; GLUCOCORTICOID; GLUTATHIONE; HYDROGEN PEROXIDE; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; CASP3 PROTEIN, MOUSE; CASPASE; CORTICOSTERONE; MEMBRANE ANTIGEN; PHOSPHATIDYLSERINE; PROPIDIUM IODIDE; SCAVENGER;

ADRENALECTOMY; ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BLOOD ANALYSIS; CELL ISOLATION; CELL LOSS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CYTOSOL; DRUG EFFECT; DRUG MECHANISM; EXERCISE; INTESTINE CELL; LYMPHOCYTE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIOIMMUNOASSAY; TREADMILL; ANIMAL; C57BL MOUSE; CYTOLOGY; FEMALE; FLOW CYTOMETRY; INTESTINE; MEMBRANE; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

ACETYLCYSTEINE; ADRENALECTOMY; ANIMALS; ANTIGENS, SURFACE; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CASPASES; CORTICOSTERONE; CYTOCHROMES C; EXERTION; FEMALE; FLOW CYTOMETRY; FREE RADICAL SCAVENGERS; GLUCOCORTICOIDS; GLUTATHIONE; HYDROGEN PEROXIDE; INTESTINES; LYMPHOCYTES; MEMBRANES; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PHOSPHATIDYLSERINES; PROPIDIUM; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 19344363495     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00843.2004     Document Type: Article

References (63)

1. Abreu-Martin MT and Targan SR. Regulation of immune responses of the intestinal mucosa. Crit Rev Immunol 16: 277-309, 1996.
2. Ashton T, Young IS, Davison GW, Rowlands CC, McEneny J, Van Blerk C, Jones E, Peters JR, and Jackson SK. Exercise-induced endotoxemia: the effect of ascorbic acid supplementation. Free Radic Biol Med 35: 284-291.
3. Atalay M, Marnila P, Lilius EM, Hanninen O, and Sen CK. Glutathione-dependent modulation of exhausting exercise-induced changes in neutrophil function of rats. Eur J Appl Physiol Occup Physiol 74: 342-347, 1996.
4. Azenabor AA and Hoffman-Goetz L. Effect of exhaustive exercise on membrane estradiol concentration, intracellular calcium, and oxidative damage in mouse thymic lymphocytes. Free Radic Biol Med 28: 84-90, 2000.
5. Baker AF, Briehl MM, Dorr R, and Powis G. Decreased antioxidant defence and increased oxidant stress during dexamethasone-induced apoptosis: bcl-2 prevents the loss of antioxidant enzyme activity. Cell Death Differ 3: 207-213, 1996.
6. Briehl MM, Cotgreave IA, and Powis G. Downregulation of the antioxidant defence during glucocorticoid-mediated apoptosis. Cell Death Differ 2: 41-46, 1995.
7. Brunner T, Arnold D, Wasem C, Herren S, and Frutschi C. Regulation of cell death and survival in intestinal intraepithelial lymphocytes. Cell Death Differ 8: 706-714, 2001.
8. Bustamante J, Tovar-B A, Montero G, and Boveris A. Early redox changes during rat thymocyte apoptosis. Arch Biochem Biophys 337: 121-128, 1997.
9. Campbell JD, Cole M, Bunditrutavorn B, and Vella AT. Ascorbic acid is a potent inhibitor of various forms of T cell apoptosis. Cell Immunol 194: 1-5, 1999.
10. Camus G, Poortmans J, Nys M, Deby-Dupont G, Duchateau J, Deby C, and Lamy M. Mild endotoxaemia and the inflammatory response induced by a marathon race. Clin Sci (Lond) 92: 415-422, 1997.
11. Cheroutre H. Starting at the beginning: new perspectives on the biology of mucosal T cells. Annu Rev Immunol 22: 217-246, 2004.
12. Chiba T, Takahashi S, Sato N, Ishii S, and Kikuchi K. Fas-mediated apoptosis is modulated by intracellular glutathione in human T cells. Eur J Immunol 26: 1164-1169, 1996.
13. Concordet JP and Ferry A. Physiological programmed cell death in thymocytes is induced by physical stress (exercise). Am J Physiol Cell Physiol 265: C626-C629, 1993.
14. Distelhorst CW. Recent insights into the mechanism of glucocorticosteroid-induced apoptosis. Cell Death Differ 9: 6-19, 2002.
15. Eray M, Matto M, Kaartinen M, Andersson L, and Pelkonen J. Flow cytometric analysis of apoptotic subpopulations with a combination of annexin V-FITC, propidium iodide, and SYTO 17. Cytometry 43: 134-142, 2001.
16. Fernandez A, Kiefer J, Fosdick L, and McConkey DJ. Oxygen radical production and thiol depletion are required for Ca(2+)-mediated endogenous endonuclease activation in apoptotic thymocytes. J Immunol 155: 5133-5139, 1995.
17. Fukuzuka K, Edwards 3rd CK, Clare-Salzler M, Copeland 3rd EM, Moldawer LL, and Mozingo DW. Glucocorticoid and Fas ligand induced mucosal lymphocyte apoptosis after burn injury. J Trauma 49: 710-716, 2000.
18. Fukuzuka K, Edwards 3rd CK, Clare-Salzler M, Copeland 3rd EM, Moldawer LL, and Mozingo DW. Glucocorticoid-induced, caspase-dependent organ apoptosis early after burn injury. Am J Physiol Regul Integr Comp Physiol 278: R1005-R1018, 2000.
19. Gardai SJ, Hoontrakoon R, Goddard CD, Day BJ, Chang LY, Henson PM, and Bratton DL. Oxidant-mediated mitochondrial injury in eosinophil apoptosis: enhancement by glucocorticoids and inhibition by granulocyte-macrophage colony-stimulating factor. J Immunol 170: 556-566, 2003.
20. Hall AG. The role of glutathione in the regulation of apoptosis. Eur J Clin Invest 29: 238-245, 1999.
21. Hartmann A, Niess AM, Grunert-Fuchs M, Poch B, and Speit G. Vitamin E prevents exercise-induced DNA damage. Mutat Res 346: 195-202, 1995.
22. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, and Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251, 1993.
23. Hoffman-Goetz L and Quadrilatero J. Treadmill exercise in mice increases intestinal lymphocyte loss via apoptosis. Acta Physiol Scand 179: 289-297, 2003.
24. Hoffman-Goetz L, Quadrilatero J, Boudreau J, and Guan J. Adrenalectomy in mice does not prevent loss of intestinal lymphocytes after exercise. J Appl Physiol 96: 2073-2081, 2004.
25. Hoffman-Goetz L and Zajchowski S. In vitro apoptosis of lymphocytes after exposure to levels of corticosterone observed following submaximal exercise. J Sports Med Phys Fitness 39: 269-274, 1999.
26. Hotchkiss RS, Schmieg RE Jr, Swanson PE, Freeman BD, Tinsley KW, Cobb JP, Karl IE, and Buchman TG. Rapid onset of intestinal epithelial and lymphocyte apoptotic cell death in patients with trauma and shock. Crit Care Med 28: 3207-3217, 2000.
27. Hsu TG, Hsu KM, Kong CW, Lu FJ, Cheng H, and Tsai K. Leukocyte mitochondria alterations after aerobic exercise in trained human subjects. Med Sci Sports Exerc 34: 438-442, 2002.
28. Ina K, Itoh J, Fukushima K, Kusugami K, Yamaguchi T, Kyokane K, Imada A, Binion DG, Musso A, West GA, Dobrea GM, McCormick TS, Lapetina EG, Levine AD, Ottaway CA, and Fiocchi C. Resistance of Crohn's disease T cells to multiple apoptotic signals is associated with a Bcl-2/Bax mucosal imbalance. J Immunol 163: 1081-1090, 1999.
29. Jeukendrup AE, Vet-Joop K, Sturk Stegen JH A, Senden J, Saris WH, Wagenmakers AJ. Relationship between gastrointestinal complaints and endotoxemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci (Lond) 98: 47-55, 2000.
30. Kohen R and Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30: 620-650, 2002.
31. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, and van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84: 1415-1420, 1994.
32. Lagranha CJ, Senna SM, de Lima TM, Silva EP, Doi SQ, Curi R, and Pithon-Curi TC. Beneficial effect of glutamine on exercise-induced apoptosis of rat neutrophils. Med Sci Sports Exerc 36: 210-217, 2004.
33. Lecoeur H, Prevost MC, and Gougeon ML. Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry 44: 65-72, 2001.
34. Lefrançois L. Isolation of mouse small intestine intraepithelial lymphocytes. In: Current Protocols in Immunology. New York: Wiley, 1993, p. 3.19.1-3.19.7.
35. Lin YS, Kuo HL, Kuo CF, Wang ST, Yang BC, and Chen HI. Antioxidant administration inhibits exercise-induced thymocyte apoptosis in rats. Med Sci Sports Exerc 31: 1594-1598, 1999.
36. Luo J, Borgens R, and Shi R. Polyethylene glycol immediately repairs neuronal membranes and inhibits free radical production after acute spinal cord injury. J Neurochem 83: 471-480, 2002.
37. Macho A, Hirsch T, Marzo I, Marchetti P, Dallaporta B, Susin SA, Zamzami N, and Kroemer G. Glutathione depletion is an early and calcium elevation is a late event of thymocyte apoptosis. J Immunol 158: 4612-4619, 1997.
38. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, and Kroemer G. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184: 1155-1160, 1996.
39. Mars M, Govendor S, Weston A, Naicker V, and Chuturgoon A. High-intensity exercise: a cause of lymphocyte apoptosis? Biochem Biophys Res Commun 249: 366-370, 1998.
40. McLaughlin KA, Osborne BA, and Goldsby RA. The role of oxygen in thymocyte apoptosis. Eur J Immunol 26: 1170-1174, 1996.
41. Mooren FC, Bloming D, Lechtermann A, Lerch MM, and Volker K. Lymphocyte apoptosis after exhaustive and moderate exercise. J Appl Physiol 93: 147-153, 2002.
42. Mooren FC, Lechtermann A, Fromme A, Thorwesten L, and Volker K. Alterations in intracellular calcium signaling of lymphocytes after exhaustive exercise. Med Sci Sports Exerc 33: 242-248, 2001.
43. Mooren FC, Lechtermann A, and Volker K. Exercise-induced apoptosis of lymphocytes depends on training status. Med Sci Sports Exerc 36: 1476-1483, 2004.
44. Murosaki S, Inagaki-Ohara K, Kusaka H, Ikeda H, and Yoshikai Y. Apoptosis of intestinal intraepithelial lymphocytes induced by exogenous and endogenous glucocorticoids. Microbiol Immunol 41: 139-148, 1997.
45. Patel H and Hoffman-Goetz L. Effects of oestrogen and exercise on caspase-3 activity in primary and secondary lymphoid compartments in ovariectomized mice. Acta Physiol Scand 176: 177-184, 2002.
46. Phaneuf S and Leeuwenburgh C. Apoptosis and exercise. Med Sci Sports Exerc 33: 393-396, 2001.
47. Quadrilatero J and Hoffman-Goetz L. N-Acetyl-1-cysteine prevents exercise-induced intestinal lymphocyte apoptosis by maintaining intracellular glutathione levels and reducing mitochondrial membrane depolarization. Biochem Biophys Res Commun 319: 894-901, 2004.
48. Quadrilatero J, Guan J, Boudreau J, Marra S, and Hoffman-Goetz L. Polyethylene glycol but not mifepristone prevents intestinal lymphocyte loss following treadmill exercise in mice. Acta Physiol Scand 183: 201-209, 2005.
49. Rice GC, Bump EA, Shrieve DC, Lee W, and Kovacs M. Quantitative analysis of cellular glutathione by flow cytometry utilizing monochlorobimane: some applications to radiation and drug resistance in vitro and in vivo. Cancer Res 46: 6105-6110, 1986.
50. Rosati E, Sabatini R, Ayroldi E, Tabilio A, Bartoli A, Bruscoli S, Simoncelli C, Rossi R, and Marconi P. Apoptosis of human primary B lymphocytes is inhibited by N-acetyl-1-cysteine. J Leukoc Biol 76: 152-161, 2004.
51. 2 in cultured endothelial cells. Arch Biochem Biophys 302: 348-355, 1993.
52. Sen CK. Glutathione homeostasis in response to exercise training and nutritional supplements. Mol Cell Biochem 196: 31-42, 1999.
53. Sen CK, Atalay M, and Hanninen O. Exercise-induced oxidative stress: glutathione supplementation and deficiency. J Appl Physiol 77: 2177-2187, 1994.
54. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD Jr, and Chen LB. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88: 3671-3675, 1991.
55. Steensberg A, Morrow J, Toft AD, Bruunsgaard H, and Pedersen BK. Prolonged exercise, lymphocyte apoptosis and F2-isoprostanes. Eur J Appl Physiol 87: 38-42, 2002.
56. Stefanelli C, Stanic I, and Bonavita F. Oxygen tension influences DNA fragmentation and cell death in glucocorticoid-treated thymocytes. Biochem Biophys Res Commun 212: 300-306, 1995.
57. Tonomura N, McLaughlin K, Grimm L, Goldsby RA, and Osborne BA. Glucocorticoid-induced apoptosis of thymocytes: requirement of proteasome-dependent mitochondrial activity. J Immunol 170: 2469-2478, 2003.
58. Torres-Roca JF, Lecoeur H, Amatore C, and Gougeon ML. The early intracellular production of reactive oxygen intermediates mediates apoptosis in dexamethasone-treated thymocytes. Cell Death Differ 2: 309-319, 1995.
59. Tsai K, Hsu TG, Hsu KM, Cheng H, Liu TY, Hsu CF, and Kong CW. Oxidative DNA damage in human peripheral leukocytes induced by massive aerobic exercise. Free Radic Biol Med 31: 1465-1472, 2001.
60. Van Houten N, Blake SF, Li EJ, Hallam TA, Chilton DG, Gourley WK, Boise LH, Thompson CB, and Thompson EB. Elevated expression of Bcl-2 and Bcl-x by intestinal intraepithelial lymphocytes: resistance to apoptosis by glucocorticoids and irradiation. Int Immunol 9: 945-953, 1997.
61. Van Houten N and Gasic G. Intestinal intraepithelial lymphocyte responses to glucocorticoid signaling. Ann NY Acad Sci 778: 431-433, 1996.
62. Verities I, Haanen C, Steffens-Nakken H, and Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein-labeled Annexin V. J Immunol Methods 184: 39-51, 1995.
63. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, and Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182: 367-377, 1995.