In vivo T cell activation in lymphoid tissues is inhibited in the oxygen-poor microenvironment

Frontiers in Immunology

Volumn 2, Issue JUL, 2011, Pages

  Ohta, Akio ^a   Diwanji, Rohan ^a   Kini, Radhika ^a   Subramanian, Meenakshi ^a   Ohta, Akiko ^a   Sitkovsky, Michail ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Cytometry; Hyperoxia; Hypoxia; Hypoxyprobe 1; Oxygen; T cell; Tumor

Indexed keywords

EID: 84874036703     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.00027     Document Type: Article

References (69)

1. Andersen, V., Hellung-Larsen, P., and Sorensen, S. F. (1968). Optimal oxygen tension for human lymphocytes in culture. J. Cell. Physiol. 72, 149-152.
2. Arteel, G. E., Thurman, R. G., and Raleigh, J. A. (1998). Reductive metabolism of the hypoxia marker pimonidazole is regulated by oxygen tension independent of the pyri-dine nucleotide redox state. Eur. J. Biochem. 253, 743-750.
3. Arteel, G. E., Thurman, R. G., Yates, J. M., and Raleigh, J. A. (1995). Evidence that hypoxia markers detect oxygen gradients in liver: pimonidazole and retrograde perfu-sion of rat liver. Br. J. Cancer 72, 889-895.
4. Atkuri, K. R., Herzenberg, L. A., and Herzenberg, L. A. (2005). Cultur-ing at atmospheric oxygen levels impacts lymphocyte function. Proc. Natl. Acad. Sci. U.S.A. 102, 3756-3759.
5. Atkuri, K. R., Herzenberg, L. A., Niemi, A. K., Cowan, T., and Herzenberg, L. A. (2007). Importance of culturing primary lymphocytes at physiological oxygen levels. Proc. Natl. Acad. Sci. U.S.A. 104, 4547-4552.
6. Bai, A., Higham, E., Eisen, H. N., Wit-trup, K. D., and Chen, J. (2008). Rapid tolerization of virus-activated tumor-specific CD8+ T cells in prostate tumors of TRAMP mice. Proc. Natl. Acad. Sci. U.S.A. 105, 13003-13008.
7. Bergeron, M., Evans, S. M., Sharp, F. R., Koch, C. J., Lord, E. M., and Ferriero, D. M. (1999). Detection of hypoxic cells with the 2-nitroimidazole, EF5, correlates with early redox changes in rat brain after perinatal hypoxia-ischemia. Neuroscience 89, 1357-1366.
8. Biselli, R., Le Moli, S., Matricardi, P. M., Farrace, S., Fattorossi, A., Nisini, R., and D'Amelio, R. (1991). The effects of hypobaric hypoxia on specific B cell responses following immunization in mice and humans. Aviat. Space Environ. Med. 62, 870-874.
9. Blay, J., White, T. D., and Hoskin, D. W. (1997). The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res. 57, 2602-2605.
10. Braun, R. D., Lanzen, J. L., Sny-der, S. A., and Dewhirst, M. W. (2001). Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents. Am. J. Physiol. Heart Circ. Physiol. 280, H2533-H2544.
11. Caldwell, C. C., Kojima, H., Lukashev, D., Armstrong, J., Farber, M., Apasov, S. G., and Sitkovsky, M. V. (2001). Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J. Immunol. 167, 6140-6149.
12. Carotenuto, P., Pontesilli, O., Cam-bier, J. C., and Hayward, A. R. (1986). Desferoxamine blocks IL 2 receptor expression on human T lymphocytes. J. Immunol. 136, 2342-2347.
13. Carswell, K. S., Weiss, J. W., and Papout-sakis, E. T. (2000). Low oxygen tension enhances the stimulation and proliferation of human T lymphocytes in the presence of IL-2. Cytotherapy 2, 25-37.
14. Chaudhri, G., Clark, I. A., Hunt, N. H., Cowden, W. B., and Ceredig, R. (1986). Effect of antioxidants on primary alloantigen-induced T cell activation and proliferation. J. Immunol. 137, 2646-2652.
15. Choukèr, A., Thiel, M., Lukashev, D., Ward, J. M., Kaufmann, I., Apasov, S., Sitkovsky, M. V., and Ohta, A. (2008). Critical role of hypoxia and A2A adenosine receptors in liver tissue-protecting physiological anti-inflammatory pathway. Mol. Med. 14, 116-123.
16. Conforti, L., Petrovic, M., Mohammad, D., Lee, S., Ma, Q., Barone, S., and Filipovich, A. H. (2003). Hypoxia regulates expression and activity of Kv1.3 channels in T lymphocytes: a possible role in T cell proliferation. J. Immunol. 170, 695-702.
17. Cramer, T., Yamanishi, Y., Clausen, B. E., Förster, I., Pawlinski, R., Mack-man, N., Haase, V. H., Jaenisch, R., Corr, M., Nizet, V., Firestein, G. S., Gerber, H. P., Ferrara, N., and Johnson, R. S. (2003). HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112, 645-657.
18. Evans, S. M., Hahn, S., Pook, D. R., Jenkins, W. T., Chalian, A. A., Zhang, P., Stevens, C., Weber, R., Weinstein, G., Benjamin, I., Mirza, N., Morgan, M., Rubin, S., McKenna, W. G., Lord, E. M., and Koch, C. J. (2000). Detection of hypoxia in human squamous cell carcinoma by EF5 binding. Cancer Res. 60, 2018-2024.
19. Fang, H. Y., Hughes, R., Murdoch, C., Coffelt, S. B., Biswas, S. K., Harris, A. L., Johnson, R. S., Imityaz, H. Z., Simon, M. C., Fredlund, E., Greten, F. R., Rius, J., and Lewis, C. E. (2009). Hypoxia-inducible factors 1 and 2 are important transcriptional effec tors in primary macrophages experi encing hypoxia. Blood 114, 844-859.
20. Fink, T., Ebbesen, P., Koppelhus, U., and Zachar, V. (2003). Natural killer cell-mediated basal and interferon-enhanced cytotoxicity against liver cancer cells is significantly impaired under in vivo oxygen conditions. Scand. J. Immunol. 58, 607-612.
21. Gajewski, T. F., Meng, Y., and Har-lin, H. (2006). Immune suppression in the tumor microenvironment. J. Immunother. 29, 233-240.
22. Guo, J., Lu, W., Shimoda, L. A., Semenza, G. L., and Georas, S. N. (2009). Enhanced interferon-gamma gene expression in T Cells and reduced ovalbumin-dependent lung eosinophilia in hypoxia-inducible factor-1-alpha-deficient mice. Int. Arch. Allergy Immunol. 149, 98-102.
23. Hale, L. P., Braun, R. D., Gwinn, W. M., Greer, P. K., and Dewhirst, M. W. (2002). Hypoxia in the thymus: role of oxygen tension in thymocyte survival. Am. J. Physiol. Heart Circ. Physiol. 282, H1467-H1477.
24. Harris, A. L. (2002). Hypoxia - a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47.
25. Hoek, K. L., Gordy, L. E., Collins, P. L., Parekh, V. V., Aune, T. M., Joyce, S., Thomas, J. W., Van Kaer, L., and Sebzda, E. (2010). Follic-ular B cell trafficking within the spleen actively restricts humoral immune responses. Immunity 33, 254-265.
26. Karhausen, J., Haase, V. H., and Colgan, S. P. (2005). Inflammatory hypoxia: role of hypoxia-inducible factor. Cell Cycle 4, 256-258.
27. Kim, H., Peng, G., Hicks, J. M., Weiss, H. L., Van Meir, E. G., Brenner, M. K., and Yotnda, P. (2008). Engineering human tumor-specific cytotoxic T cells to function in a hypoxic environment. Mol. Ther. 16, 599-606.
28. Koch, C. J. (2002). Measurement of absolute oxygen levels in cells and tissues using oxygen sensors and 2-nitroimidazole EF5. Meth. Enzymol. 352, 3-31.
29. Kojima, H., Gu, H., Nomura, S., Cald-well, C. C., Kobata, T., Carmeliet, P., Semenza, G. L., and Sitkovsky, M. V (2002). Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1alpha -deficient chimeric mice. Proc. Natl. Acad. Sci U.S.A. 99, 2170-2174.
30. Kojima, H., Kobayashi, A., Sakurai, D., Kanno, Y., Hase, H., Taka-hashi, R., Totsuka, Y., Semenza, G. L., Sitkovsky, M. V., and Kobata, T. (2010). Differentiation stage-specific requirement in hypoxia-inducible factor-1alpha-regulated glycolytic pathway during murine B cell development in bone marrow.J. Immunol. 184, 154-163.
31. Krieger, J. A., Landsiedel, J. C., and Lawrence, D. A. (1996). Differential in vitro effects of physiological and atmospheric oxygen tension on normal human peripheral blood mononuclear cell proliferation, cytokine and immunoglobulin production. Int. J. Immunopharmacol. 18, 545-552.
32. Larbi, A., Zelba, H., Goldeck, D., and Pawelec, G. (2010). Induction of HIF-1alpha and the glycolytic pathway alters apoptotic and differentiation profiles of activated human T cells. J. Leukoc. Biol. 87, 265-273.
33. Lederman, H. M., Cohen, A., Lee, J. W., Freedman, M. H., and Gelfand, E. W. (1984). Deferoxamine: a reversible S-phase inhibitor of human lymphocyte proliferation. Blood 64, 748-753.
34. Loeffler, D. A., Juneau, P. L., and Masserant, S. (1992). Influence of tumour physico-chemical conditions on interleukin-2-stimulated lymphocyte proliferation. Br. J. Cancer 66, 619-622.
35. Lord, E. M., Harwell, L., and Koch, C. J. (1993). Detection of hypoxic cells by monoclonal antibody recognizing 2-nitroimidazole adducts. Cancer Res. 53, 5721-5726.
36. + T lymphocytes. J. Immunol. 177, 4962-4965.
37. Majmundar, A. J., Wong, W J., and Simon, M. C. (2010). Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40, 294-309.
38. McLaughlin, K. A., Osborne, B. A., and Goldsby, R. A. (1996). The role of oxygen in thymocyte apoptosis. Eur. J. Immunol. 26, 1170-1174.
39. Meehan, R., Duncan, U., Neale, L., Taylor, G., Muchmore, H., Scott, N., Ramsey, K., Smith, E., Rock, P., Goldblum, R., and Houston, C. (1988). Operation Everest II: alterations in the immune system at high altitudes. J. Clin. Immunol. 8, 397-406.
40. Meehan, R.T. (1987). Immune suppression at high altitude. Ann. Emerg. Med. 16, 974-979.
41. Mellor, A. L., and Munn, D. H. (2008). Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat. Rev. Immunol. 8, 74-80.
42. Michiels, C. (2004). Physiological and pathological responses to hypoxia. Am. J. Pathol. 164, 187 5-1882.
43. Naldini, A., Carraro, F., Silvestri, S., andBocci, V. (1997). Hypoxia affects cytokine production and prolifera-tive responses by human peripheral mononuclear cells. J. Cell. Physiol. 173, 335-342.
44. Neumann, A. K., Yang, J., Biju, M. P., Joseph, S. K., Johnson, R. S., Haase, V. H., Freedman, B. D., and Turka, L. A. (2005). Hypoxia inducible factor 1 alpha regulates T cell receptor signal transduction. Proc. Natl. Acad. Sci. U.S.A. 102, 17071-17076.
45. Niinikoski, J., Hunt, T. K., and Dun-phy, J. E. (1972). Oxygen supply in healing tissue. Am. J. Surg. 123, 247-252.
46. Nizet, V., and Johnson, R. S. (2009). Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 9, 609-617.
47. Ohta, A., Gorelik, E., Prasad, S. J., Ronchese, F., Lukashev, D., Wong, M. K., Huang, X., Caldwell, S., Liu, K., Smith, P., Chen, J. F., Jackson, E. K., Apasov, S., Abrams, S., and Sitkovsky, M. (2006). A2A adenosine receptor protects tumors from antitumor T cells. Proc. Natl. Acad. Sci. U.S.A. 103, 13132-13137.
48. Ohta, A., Ohta, A., Madasu, M., Kini, R., Subramanian, M., Goel, N., and Sitkovsky, M. (2009). A2A adenosine receptor may allow expansion of T cells lacking effector functions in extracellular adenosine-rich microenvironments. J. Immunol. 183, 5487-5493.
49. Ohta, A., and Sitkovsky, M. (2001). Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 414, 916-920.
50. Pae, H. O., Choi, B. M., Oh, G. S., Lee, M. S., Ryu, D. G., Rhew, H. Y., Kim, Y M., and Chung, H. T. (2004). Roles of heme oxygenase-1 in the antiproliferative and anti-apoptotic effects of nitric oxide on Jurkat T cells. Mol. Pharmacol. 66, 122-128.
51. Parliament, M. B., Wiebe, L. I., and Franko, A. J. (1992). Nitroim-idazole adducts as markers for tissue hypoxia: mechanistic studies in aerobic normal tissues and tumour cells. Br. J. Cancer 66, 1103-1108.
52. Peters, C. L., Morris, C. J., Mapp, P. I., Blake, D. R., Lewis, C. E., and Winrow, V R. (2004). The transcription factors hypoxia-inducible factor 1alpha and Ets-1 colocal-ize in the hypoxic synovium of inflamed joints in adjuvant-induced arthritis. Arthritis Rheum. 50, 291-296.
53. Peyssonnaux, C., Cejudo-Martin, P., Doedens, A., Zinkernagel, A. S., Johnson, R. S., and Nizet, V (2007). Cutting edge: essential role of hypoxia inducible factor-1alpha in development of lipopolysaccharide-induced sepsis. J. Immunol. 178, 7516-7519.
54. Robbins, J. R., Lee, S. M., Filipovich, A. H., Szigligeti, P., Neumeier, L., Petrovic, M., and Conforti, L. (2005). Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels. J. Physiol. 564, 131-143.
55. Roman, J., Rangasamy, T., Guo, J., Sug-unan, S., Meednu, N., Packirisamy, G., Shimoda, L. A., Golding, A., Semenza, G., and Georas, S. N. (2010). T-cell activation under hypoxic conditions enhances IFN-gamma secretion. Am. J. Respir. Cell Mol. Biol. 42, 123-128.
56. Semenza, G. L. (2003). Angiogenesis in ischemic and neoplastic disorders. Annu. Rev. Med. 54, 17-28.
57. Shabsigh, A., Ghafar, M. A., de la Taille, A., Burchardt, M., Kaplan, S. A., Anastasiadis, A. G., and Buttyan, R. (2001). Biomarker analysis demonstrates a hypoxic environment in the castrated rat ventral prostate gland. J. Cell. Biochem. 81, 437-444.
58. Sitkovsky, M. V., Lukashev, D., Apasov, S., Kojima, H., Koshiba, M., Caldwell, C., Ohta, A., and Thiel, M. (2004). Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu. Rev. Immunol. 22, 657-682.
59. Sitkovsky, M. V., and Ohta, A. (2005). The 'danger' sensors that STOP the immune response: the A2 adeno-sine receptors? Trends Immunol. 26, 299-304.
60. Thiel, M., Caldwell, C. C., Kreth, S., Kuboki, S., Chen, P., Smith, P., Ohta, A., Lentsch, A. B., Lukashev, D., and Sitkovsky, M. V. (2007). Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS ONE 2, e853. doi:10.1371/journal.pone. 0000853.
61. Thiel, M., Chouker, A., Ohta, A., Jackson, E., Caldwell, C., Smith, P., Lukashev, D., Bittmann, I., and Sitkovsky, M. V. (2005). Oxygenation inhibits the physiological tissue-protecting mechanism and thereby exacerbates acute inflammatory lung injury. PLoS Biol. 3, e174. doi: 10.1371/journal.pbio.0030174.
62. Vaupel, P., and Mayer, A. (2007). Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 26, 225-239.
63. Vukovic, V., Haugland, H. K., Nick-lee, T., Morrison, A. J., and Hedley, D. W. (2001). Hypoxia-inducible factor-1alpha is an intrinsic marker for hypoxia in cervical cancer xenografts. Cancer Res. 61, 7394-7398.
64. Walmsley, S. R., Print, C., Farahi, N., Peyssonnaux, C., Johnson, R. S., Cramer, T., Sobolewski, A., Condliffe, A. M., Cowburn, A. S., Johnson, N., and Chilvers, E. R. (2005). Hypoxia-induced neu-trophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 201, 105-115.
65. Wang, J. Y., Tsukayama, D. T., Wicklund, B. H., and Gustilo, R. B. (1996). Inhibition of T and B cell proliferation by titanium, cobalt, and chromium: role of IL-2 and IL-6. J. Biomed. Mater. Res. 32, 655-661.
66. Wang, Q., Liu, C., Zhu, F., Liu, F., Zhang, P., Guo, C., Wang, X., Li, H., Ma, C., Sun, W., Zhang, Y., Chen, W., and Zhang, L. (2010). Reoxygena-tion of hypoxia-differentiated den-tritic cells induces Th1 and Th17 cell differentiation. Mol. Immunol. 47, 922-931.
67. Yang, M., Ma, C., Liu, S., Sun, J., Shao, Q., Gao, W., Zhang, Y., Li, Z., Xie, Q., Dong, Z., and Qu, X. (2009). Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopon-tin. Immunology 128, e237-e249.
68. Zandvoort, A., and Timens, W. (2002). The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin. Exp. Immunol. 130, 4-11.
69. Zuckerberg, A. L., Goldberg, L. I., and Lederman, H. M. (1994). Effects of hypoxia on interleukin-2 mRNA expression by T lymphocytes. Crit. Care Med. 22, 197-203.