Reduced oxygen tension results in reduced human T cell proliferation and increased intracellular oxidative damage and susceptibility to apoptosis upon activation

Free Radical Biology and Medicine

Volumn 48, Issue 1, 2010, Pages 26-34

  Larbi, Anis ^a   Cabreiro, Filipe ^b   Zelba, Henning ^a   Marthandan, Shiva ^c   Combet, Emilie ^d   Friguet, Bertrand ^b   Petropoulos, Isabelle ^b   Barnett, Yvonne ^c   Pawelec, Graham ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Apoptosis; Free radicals; Methionine sulfoxide reductase; Oxidative damage; Oxygen tension; Proteasome; T cells

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; METHIONINE SULFOXIDE REDUCTASE; PROTEASOME;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LYMPHOCYTE CULTURE; LYMPHOCYTE PROLIFERATION; OXIDATIVE STRESS; OXYGEN TENSION; OXYGENATION; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANTIOXIDANTS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; LYMPHOCYTE ACTIVATION; METHIONINE SULFOXIDE REDUCTASES; MIDDLE AGED; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN; PROTEASOME ENDOPEPTIDASE COMPLEX; REFERENCE VALUES; STILBENES; T-LYMPHOCYTES;

EID: 74149086692     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.09.025     Document Type: Article

References (44)

1. Ostler T., and Ehl S. A cautionary note on experimental artefacts induced by fetal calf serum in a viral model of pulmonary eosinophilia. J. Immunol. Methods 268 (2002) 211-218
2. Coolen N.A., Verkerk M., Reijnen L., Vlig M., van den Bogaerdt A.J., Breetveld M., Gibbs S., Middelkoop E., and Ulrich M.M. Culture of keratinocytes for transplantation without the need of feeder layer cells. Cell Transplant 16 (2007) 649-661
3. de Souza N. Too much of a good thing. Nat. Methods 4 (2007) 386
4. Bodeker B.G., Lehmann J., and Muhlradt P.F. Lymphokine (interleukin-2) production by mitogen-stimulated human lymphocytes in small reactors. Dev. Biol. Stand. 50 (1981) 193-200
5. Caldwell C.C., Kojima H., Lukashev D., Armstrong J., Farber M., Apasov S.G., and Sitkovsky M.V. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J. Immunol. 167 (2001) 6140-6149
6. Atkuri K.R., Herzenberg L.A., Niemi A.K., Cowan T., and Herzenberg L.A. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc. Natl. Acad. Sci. USA 104 (2007) 4547-4552
7. Westermann J., and Bode U. Distribution of activated T cells migrating through the body: a matter of life and death. Immunol. Today 20 (1999) 302-306
8. Vaupel P., Kallinowski F., and Okunieff P. Blood flow, oxygen consumption and tissue oxygenation of human tumors. Adv. Exp. Med. Biol. 277 (1990) 895-905
9. MacDonald H.R., and Koch C.J. Energy metabolism and T-cell-mediated cytolysis. I. Synergism between inhibitors of respiration and glycolysis. J. Exp. Med. 146 (1977) 698-709
10. Zuckerberg A.L., Goldberg L.I., and Lederman H.M. Effects of hypoxia on interleukin-2 mRNA expression by T lymphocytes. Crit. Care Med. 22 (1994) 197-203
11. Naldini A., Carraro F., Silvestri S., and Bocci V. Hypoxia affects cytokine production and proliferative responses by human peripheral mononuclear cells. J. Cell. Physiol. 173 (1997) 335-342
12. Atkuri K.R., Herzenberg L.A., and Herzenberg L.A. Culturing at atmospheric oxygen levels impacts lymphocyte function. Proc. Natl. Acad. Sci. USA 102 (2005) 3756-3759
13. Griffith O.W. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic. Biol. Med. 27 (1999) 922-935
14. Yermolaieva O., Xu R., Schinstock C., Brot N., Weissbach H., Heinemann S.H., and Hoshi T. Methionine sulfoxide reductase A protects neuronal cells against brief hypoxia/reoxygenation. Proc. Natl. Acad. Sci. USA 101 (2004) 1159-1164
15. Cabreiro F., Picot C.R., Perichon M., Castel J., Friguet B., and Petropoulos I. Overexpression of mitochondrial methionine sulfoxide reductase B2 protects leukemia cells from oxidative stress-induced cell death and protein damage. J. Biol. Chem. 283 (2008) 16673-16681
16. Levine R.L., Mosoni L., Berlett B.S., and Stadtman E.R. Methionine residues as endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. USA 93 (1996) 15036-15040
17. Poppek D., and Grune T. Proteasomal defense of oxidative protein modifications. Antioxid. Redox Signaling 8 (2006) 173-184
18. Orlowski M., and Wilk S. Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch. Biochem. Biophys. 383 (2000) 1-16
19. Newby D., Marks L., and Lyall F. Dissolved oxygen concentration in culture medium: assumptions and pitfalls. Placenta 26 (2005) 353-357
20. Herzenberg L.A., Tung J., Moore W.A., Herzenberg L.A., and Parks D.R. Interpreting flow cytometry data: a guide for the perplexed. Nat. Immunol. 7 (2006) 681-685
21. Collins A.R., Duthie S.J., and Dobson V.L. Direct enzymic detection of endogenous oxidative base damage in human lymphocyte DNA. Carcinogenesis 14 (1993) 1733-1735
22. Benzie I.F., and Strain J.J. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal. Biochem. 239 (1996) 70-76
23. Lukashev D., Klebanov B., Kojima H., Grinberg A., Ohta A., Berenfeld L., Wenger R.H., Ohta A., and Sitkovsky M. Cutting edge: hypoxia-inducible factor 1alpha and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J. Immunol. 177 (2006) 4962-4965
24. Esteban M.A., and Maxwell P.H. Manipulation of oxygen tensions for in vitro cell culture using a hypoxic workstation. Expert Rev. Proteomics 2 (2005) 307-314
25. Zhdanov A.V., Ward M.W., Prehn J.H., and Papkovsky D.B. Dynamics of intracellular oxygen in PC12 cells upon stimulation of neurotransmission. J. Biol. Chem. 283 (2008) 5650-5661
26. Fiorucci S., Mencarelli A., Distrutti E., Baldoni M., del Soldato P., and Morelli A. Nitric oxide regulates immune cell bioenergetic: a mechanism to understand immunomodulatory functions of nitric oxide-releasing anti-inflammatory drugs. J. Immunol. 173 (2004) 874-882
27. Magalhaes J., Ascensao A., Soares J.M., Ferreira R., Neuparth M.J., Marques F., and Duarte J.A. Acute and severe hypobaric hypoxia increases oxidative stress and impairs mitochondrial function in mouse skeletal muscle. J. Appl. Physiol. 99 (2005) 1247-1253
28. Petropoulos I., and Friguet B. Protein maintenance in aging and replicative senescence: a role for the peptide methionine sulfoxide reductases. Biochim. Biophys. Acta 1703 (2005) 261-266
29. Hultqvist M., Backlund J., Bauer K., Gelderman K.A., and Holmdahl R. Lack of reactive oxygen species breaks T cell tolerance to collagen type II and allows development of arthritis in mice. J. Immunol. 179 (2007) 1431-1437
30. D'Autreaux B., and Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8 (2007) 813-824
31. Williams M.S., and Kwon J. T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic. Biol. Med. 37 (2004) 1144-1151
32. Reyes B.M., Danese S., Sans M., Fiocchi C., and Levine A.D. Redox equilibrium in mucosal T cells tunes the intestinal TCR signaling threshold. J. Immunol. 175 (2005) 2158-2166
33. Kim H., Peng G., Hicks J.M., Weiss H.L., Van Meir E.G., Brenner M.K., and Yotnda P. Engineering human tumor-specific cytotoxic T cells to function in a hypoxic environment. Mol. Ther. 16 (2008) 599-606
34. Botto L., Beretta E., Daffara R., Miserocchi G., and Palestini P. Biochemical and morphological changes in endothelial cells in response to hypoxic interstitial edema. Respir. Res. 7 (2006) 7
35. Bhatnagar A. Surviving hypoxia: the importance of rafts, anchors, and fluidity. Circ. Res. 92 (2003) 821-823
36. Block E.R., Patel J.M., and Edwards D. Mechanism of hypoxic injury to pulmonary artery endothelial cell plasma membranes. Am. J. Physiol. 257 (1989) C223-C231
37. Chen Z.H., Saito Y., Yoshida Y., and Niki E. Effect of oxygen concentration on free radical-induced cytotoxicity. Biosci. Biotechnol. Biochem. 72 (2008) 1491-1497
38. Weinmann M., Jendrossek V., Handrick R., Guner D., Goecke B., and Belka C. Molecular ordering of hypoxia-induced apoptosis: critical involvement of the mitochondrial death pathway in a FADD/caspase-8 independent manner. Oncogene 23 (2004) 3757-3769
39. Carraro F., Pucci A., Pellegrini M., Pelicci P.G., Baldari C.T., and Naldini A. p66Shc is involved in promoting HIF-1alpha accumulation and cell death in hypoxic T cells. J. Cell. Physiol. 211 (2007) 439-447
40. Chandel N.S., and Budinger G.R. The cellular basis for diverse responses to oxygen. Free Radic. Biol. Med. 42 (2007) 165-174
41. Lukashev D., and Sitkovsky M. Preferential expression of the novel alternative isoform I.3 of hypoxia-inducible factor 1alpha in activated human T lymphocytes. Hum. Immunol. 69 (2008) 421-425
42. Haddad J.J., and Land S.C. A non-hypoxic, ROS-sensitive pathway mediates TNF-alpha-dependent regulation of HIF-1alpha. FEBS Lett. 505 (2001) 269-274
43. Scharte M., Jurk K., Kehrel B., Zarbock A., Aken H., and Singbaertl K. IL-4 enhances hypoxia induced HIF-1α protein levels in human transformed intestinal cells. FEBS Lett. 27 (2006) 6399-6404
44. Lukashev D., Caldwell C., Ohta A., Chen P., and Sitkovsky M. Differential regulation of two alternatively spliced isoforms of hypoxia-inducible factor-1 alpha in activated T lymphocytes. J. Biol. Chem. 276 (2001) 48754-48763