Severe exercise and exercise training exert opposite effects on human neutrophil apoptosis via altering the redox status

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Syu, Guan Da ^a   Chen, Hsiun Ing ^a   Jen, Chauying J ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; HYDROGEN PEROXIDE; LIPOCORTIN 5; REACTIVE OXYGEN METABOLITE;

ADULT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOSOL; EXERCISE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NEUTROPHIL; NORMAL HUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; SEDENTARY LIFESTYLE; UPREGULATION; CLINICAL TRIAL; CYTOLOGY; DRUG EFFECT; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; REST;

APOPTOSIS; EXERCISE; HUMANS; HYDROGEN PEROXIDE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEUTROPHILS; OXIDATION-REDUCTION; REST; YOUNG ADULT;

EID: 80052607643     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024385     Document Type: Article

References (59)

1. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
2. Donowitz GR, Maki DG, Crnich CJ, Pappas PG, Rolston KV, (2001) Infections in the neutropenic patient-new views of an old problem. Hematology Am Soc Hematol Educ Program 2001: 113-139.
3. Dibbert B, Weber M, Nikolaizik WH, Vogt P, Schoni MH, et al. (1999) Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc Natl Acad Sci U S A 96: 13330-13335.
4. Geering B, Simon HU, (2011) Peculiarities of cell death mechanisms in neutrophils. Cell Death Differ In press.
5. Rollet-Labelle E, Grange MJ, Elbim C, Marquetty C, Gougerot-Pocidalo MA, et al. (1998) Hydroxyl radical as a potential intracellular mediator of polymorphonuclear neutrophil apoptosis. Free Radic Biol Med 24: 563-572.
6. Oishi K, Machida K, (1997) Inhibition of neutrophil apoptosis by antioxidants in culture medium. Scand J Immunol 45: 21-27.
7. Aoshiba K, Yasui S, Hayashi M, Tamaoki J, Nagai A, (1999) Role of p38-mitogen-activated protein kinase in spontaneous apoptosis of human neutrophils. J Immunol 162: 1692-1700.
8. Kasahara Y, Iwai K, Yachie A, Ohta K, Konno A, et al. (1997) Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood 89: 1748-1753.
9. Fadeel B, Ahlin A, Henter JI, Orrenius S, Hampton MB, (1998) Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92: 4808-4818.
10. Scheel-Toellner D, Wang K, Craddock R, Webb PR, McGettrick HM, et al. (2004) Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 104: 2557-2564.
11. Maianski NA, Geissler J, Srinivasula SM, Alnemri ES, Roos D, et al. (2004) Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ 11: 143-153.
12. Whyte MK, Meagher LC, MacDermot J, Haslett C, (1993) Impairment of function in aging neutrophils is associated with apoptosis. J Immunol 150: 5124-5134.
13. Niess AM, Dickhuth HH, Northoff H, Fehrenbach E, (1999) Free radicals and oxidative stress in exercise-immunological aspects. Exerc Immunol Rev 5: 22-56.
14. Niess AM, Simon P, (2007) Response and adaptation of skeletal muscle to exercise-the role of reactive oxygen species. Front Biosci 12: 4826-4838.
15. Pedersen BK, Toft AD, (2000) Effects of exercise on lymphocytes and cytokines. Br J Sports Med 34: 246-251.
16. Peake J, Nosaka K, Suzuki K, (2005) Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev 11: 64-85.
17. Gleeson M, (2007) Immune function in sport and exercise. J Appl Physiol 103: 693-699.
18. Nieman DC, (2000) Is infection risk linked to exercise workload? Med Sci Sports Exerc 32: S406-S411.
19. Woods JA, Vieira VJ, Keylock KT, (2006) Exercise, inflammation, and innate immunity. Neurol Clin 24: 585-599.
20. Hessel E, Haberland A, Muller M, Lerche D, Schimke I, (2000) Oxygen radical generation of neutrophils: a reason for oxidative stress during marathon running? Clin Chim Acta 298: 145-156.
21. Quindry JC, Stone WL, King J, Broeder CE, (2003) The effects of acute exercise on neutrophils and plasma oxidative stress. Med Sci Sports Exerc 35: 1139-1145.
22. Sureda A, Ferrer MD, Tauler P, Maestre I, Aguilo A, et al. (2007) Intense physical activity enhances neutrophil antioxidant enzyme gene expression. Immunocytochemistry evidence for catalase secretion. Free Radic Res 41: 874-883.
23. Chinda D, Nakaji S, Umeda T, Shimoyama T, Kurakake S, et al. (2003) A competitive marathon race decreases neutrophil functions in athletes. Luminescence 18: 324-329.
24. Peake J, Wilson G, Hordern M, Suzuki K, Yamaya K, et al. (2004) Changes in neutrophil surface receptor expression, degranulation, and respiratory burst activity after moderate- and high-intensity exercise. J Appl Physiol 97: 612-618.
25. Pyne DB, Smith JA, Baker MS, Telford RD, Weidemann MJ, (2000) Neutrophil oxidative activity is differentially affected by exercise intensity and type. J Sci Med Sport 3: 44-54.
26. Lagranha CJ, Levada-Pires AC, Sellitti DF, Procopio J, Curi R, et al. (2008) The effect of glutamine supplementation and physical exercise on neutrophil function. Amino Acids 34: 337-346.
27. Suzuki K, Sato H, Kikuchi T, Abe T, Nakaji S, et al. (1996) Capacity of circulating neutrophils to produce reactive oxygen species after exhaustive exercise. J Appl Physiol 81: 1213-1222.
28. Hsu TG, Hsu KM, Kong CW, Lu FJ, Cheng H, et al. (2002) Leukocyte mitochondria alterations after aerobic exercise in trained human subjects. Med Sci Sports Exerc 34: 438-442.
29. Tuan TC, Hsu TG, Fong MC, Hsu CF, Tsai KK, et al. (2008) Deleterious effects of short-term, high-intensity exercise on immune function: evidence from leucocyte mitochondrial alterations and apoptosis. Br J Sports Med 42: 11-15.
30. Su SH, Jen CJ, Chen HI, (2011) NO signaling in exercise training-induced anti-apoptotic effects in human neutrophils. Biochem Biophys Res Commun 405: 58-63.
31. Petersen AM, Pedersen BK, (2005) The anti-inflammatory effect of exercise. J Appl Physiol 98: 1154-1162.
32. Sim YJ, Yu S, Yoon KJ, Loiacono CM, Kohut ML, (2009) Chronic exercise reduces illness severity, decreases viral load, and results in greater anti-inflammatory effects than acute exercise during influenza infection. J Infect Dis 200: 1434-1442.
33. Wang JS, Jen CJ, Chen HI, (1995) Effects of exercise training and deconditioning on platelet function in men. Arterioscler Thromb Vasc Biol 15: 1668-1674.
34. Wang JS, Jen CJ, Kung HC, Lin LJ, Hsiue TR, et al. (1994) Different effects of strenuous exercise and moderate exercise on platelet function in men. Circulation 90: 2877-2885.
35. Bass DA, Parce JW, Dechatelet LR, Szejda P, Seeds MC, et al. (1983) Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J Immunol 130: 1910-1917.
36. Rahman I, Kode A, Biswas SK, (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1: 3159-3165.
37. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, et al. (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci U S A 88: 3671-3675.
38. Mukhopadhyay P, Rajesh M, Hasko G, Hawkins BJ, Madesh M, et al. (2007) Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2: 2295-2301.
39. Fossati G, Moulding DA, Spiller DG, Moots RJ, White MR, et al. (2003) The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J Immunol 170: 1964-1972.
40. Tauler P, Aguilo A, Cases N, Sureda A, Gimenez F, et al. (2002) Acute phase immune response to exercise coexists with decreased neutrophil antioxidant enzyme defences. Free Radic Res 36: 1101-1107.
41. Tauler P, Aguilo A, Gimeno I, Guix P, Tur JA, et al. (2004) Different effects of exercise tests on the antioxidant enzyme activities in lymphocytes and neutrophils. J Nutr Biochem 15: 479-484.
42. Lorne E, Zmijewski JW, Zhao X, Liu G, Tsuruta Y, et al. (2008) Role of extracellular superoxide in neutrophil activation: interactions between xanthine oxidase and TLR4 induce proinflammatory cytokine production. Am J Physiol Cell Physiol 294: C985-C993.
43. Mitra S, Abraham E, (2006) Participation of superoxide in neutrophil activation and cytokine production. Biochim Biophys Acta 1762: 732-741.
44. van Raam BJ, Sluiter W, de WE, Roos D, Verhoeven AJ, et al. (2008) Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organisation. PLoS One 3: e2013.
45. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E, (2004) Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J Immunol 172: 2522-2529.
46. Sastre J, Asensi M, Gasco E, Pallardo FV, Ferrero JA, et al. (1992) Exhaustive physical exercise causes oxidation of glutathione status in blood: prevention by antioxidant administration. Am J Physiol 263: R992-R995.
47. Elokda AS, Shields RK, Nielsen DH, (2005) Effects of a maximal graded exercise test on glutathione as a marker of acute oxidative stress. J Cardiopulm Rehabil 25: 215-219.
48. Conus S, Perozzo R, Reinheckel T, Peters C, Scapozza L, et al. (2008) Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J Exp Med 205: 685-698.
49. Moulding DA, Quayle JA, Hart CA, Edwards SW, (1998) Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. Blood 92: 2495-2502.
50. Witko-Sarsat V, Mocek J, Bouayad D, Tamassia N, Ribeil JA, et al. (2010) Proliferating cell nuclear antigen acts as a cytoplasmic platform controlling human neutrophil survival. J Exp Med 207: 2631-2645.
51. Witko-Sarsat V, Pederzoli-Ribeil M, Hirsch E, Sozzani S, Cassatella MA, (2011) Regulating neutrophil apoptosis: new players enter the game. Trends Immunol 32: 117-124.
52. Vina J, Gimeno A, Sastre J, Desco C, Asensi M, et al. (2000) Mechanism of free radical production in exhaustive exercise in humans and rats; role of xanthine oxidase and protection by allopurinol. IUBMB Life 49: 539-544.
53. Ji LL, Gomez-Cabrera MC, Steinhafel N, Vina J, (2004) Acute exercise activates nuclear factor (NF)-kappaB signaling pathway in rat skeletal muscle. FASEB J 18: 1499-1506.
54. Gomez-Cabrera MC, Borras C, Pallardo FV, Sastre J, Ji LL, et al. (2005) Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol 567: 113-120.
55. Gomez-Cabrera MC, Domenech E, Vina J, (2008) Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44: 126-131.
56. Glasser L, Fiederlein RL, (1987) Functional differentiation of normal human neutrophils. Blood 69: 937-944.
57. Chukhlovin A, (2000) Enhanced ex vivo apoptosis of peripheral granulocytes is a sufficient factor of neutropenia following myeloablative chemotherapy. Leuk Res 24: 507-509.
58. Kimhi O, Drucker L, Neumann A, Shapiro H, Shapira J, et al. (2004) Fluorouracil induces apoptosis and surface molecule modulation of peripheral blood leukocytes. Clin Lab Haematol 26: 327-333.
59. Pitrak DL, Tsai HC, Mullane KM, Sutton SH, Stevens P, (1996) Accelerated neutrophil apoptosis in the acquired immunodeficiency syndrome. J Clin Invest 98: 2714-2719.