Distinctive immunoregulatory effects of adenosine on T cells of older humans

FASEB Journal

Volumn 26, Issue 3, 2012, Pages 1301-1310

  Hesdorffer, Charles S ^a   Malchinkhuu, Enkhzol ^a   Biragyn, Arya ^a   Mabrouk, Omar S ^b   Kennedy, Robert T ^b   Madara, Karen ^a   Taub, Dennis D ^a   Longo, Dan L ^a   Schwartz, Janice B ^c,d   Ferrucci, Luigi ^a   Goetzl, Edward J ^a,c,d  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Geriatric Research Laboratories   (United States)

Author keywords

Cellular antigens; Chemotaxis; Cytokines; Immunodeficiency; Immunosenescence

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; CD28 ANTIGEN; CD39 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHEMOTAXIS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; IMMUNOREGULATION; LYMPHOCYTE CULTURE; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADENINE; ADENOSINE; ADENOSINE A2 RECEPTOR AGONISTS; ADENOSINE A2 RECEPTOR ANTAGONISTS; ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; ANTIGENS, CD; ANTIGENS, CD28; APYRASE; CELLS, CULTURED; CHEMOTAXIS; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MIDDLE AGED; PHENETHYLAMINES; PYRIMIDINES; T-LYMPHOCYTES; TRIAZOLES; YOUNG ADULT;

EID: 84857752694     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-197046     Document Type: Article

References (26)

1. Resta, R., Yamashita, Y., and Thompson, L. F. (1998) Ectoenzyme and signaling functions of lymphocyte CD73. Immunol. Rev. 161, 95-109
2. Borsellino, G., Kleinewietfeld, M., Di Mitri, D., Sternjak, A., Diamantini, A., Giometto, R., Hopner, S., Centonze, D., Bernardi, G., Dell'Acqua, M. L., Rossini, P. M., Battistini, L., Rotzschke, O., and Falk, K. (2007) Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 110, 1225-1232 (Pubitemid 47281420)
3. Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J. F., Enjyoji, K., Linden, J., Oukka, M., Kuchroo, V. K., Strom, T. B., and Robson, S. C. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204, 1257-1265 (Pubitemid 46919862)
4. Zhou, Q., Yan, J., Putheti, P., Wu, Y., Sun, X., Toxavidis, V., Tigges, J., Kassam, N., Enjyoji, K., Robson, S. C., Strom, T. B., and Gao, W. (2009) Isolated CD39 expression on CD4+ T cells denotes both regulatory and memory populations. Am. J. Transplant. 9, 2303-2311
5. Airas, L., Niemela, J., Salmi, M., Puurunen, T., Smith, D. J., and Jalkanen, S. (1997) Differential regulation and function of CD73, a glycosyl-phosphatidylinositol-linked 70-kD adhesion molecule, on lymphocytes and endothelial cells. J. Cell Biol. 136, 421-431 (Pubitemid 27063091)
6. Takedachi, M., Qu, D., Ebisuno, Y., Oohara, H., Joachims, M. L., McGee, S. T., Maeda, E., McEver, R. P., Tanaka, T., Miyasaka, M., Murakami, S., Krahn, T., Blackburn, M. R., and Thompson, L. F. (2008) CD73-generated adenosine restricts lymphocyte migration into draining lymph nodes. J. Immunol. 180, 6288-6296
7. Algars, A., Karikoski, M., Yegutkin, G. G., Stoitzner, P., Niemela, J., Salmi, M., and Jalkanen, S. (2011) Different role of CD73 in leukocyte trafficking via blood and lymph vessels. Blood 117, 4387-4393
8. 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 (Pubitemid 27283766)
9. DosReis, G. A., Nobrega, A. F., and de Carvalho, R. P. (1986) Purinergic modulation of T-lymphocyte activation: differential susceptibility of distinct activation steps and correlation with intracellular 3′,5′-cyclic adenosine monophosphate accumulation. Cell. Immunol. 101, 213-231
10. Butler, J. J., Mader, J. S., Watson, C. L., Zhang, H., Blay, J., and Hoskin, D. W. (2003) Adenosine inhibits activation-induced T cell expression of CD2 and CD28 co-stimulatory molecules: role of interleukin-2 and cyclic AMP signaling pathways. J. Cell. Biochem. 89, 975-991 (Pubitemid 36927729)
11. Gessi, S., Varani, K., Merighi, S., Fogli, E., Sacchetto, V., Benini, A., Leung, E., Mac-Lennan, S., and Borea, P. A. (2007) Adenosine and lymphocyte regulation. Purinergic Signal. 3, 109-116
12. Parish, S. T., Kim, S., Sekhon, R. K., Wu, J. E., Kawakatsu, Y., and Effros, R. B. (2010) Adenosine deaminase modulation of telomerase activity and replicative senescence in human CD8 T lymphocytes. J. Immunol. 184, 2847-2854
13. Hoskin, D. W., Mader, J. S., Furlong, S. J., Conrad, D. M., and Blay, J. (2008) Inhibition of T cell and natural killer cell function by adenosine and its contribution to immune evasion by tumor cells [Review]. Intl. J. Oncol. 32, 527-535 (Pubitemid 351330458)
14. Ernst, P. B., Garrison, J. C., and Thompson, L. F. (2010) Much ado about adenosine: adenosine synthesis and function in regulatory T cell biology. J. Immunol. 185, 1993-1998
15. Himer, L., Csoka, B., Selmeczy, Z., Koscso, B., Pocza, T., Pacher, P., Nemeth, Z. H., Deitch, E. A., Vizi, E. S., Cronstein, B. N., and Hasko, G. (2010) Adenosine A2A receptor activation protects CD4+ T lymphocytes against activation-induced cell death. FASEB J. 24, 2631-2640
16. Zheng, Y., Voice, J. K., Kong, Y., and Goetzl, E. J. (2000) Altered expression and functional profile of lysophosphatidic acid receptors in mitogen-activated human blood T lymphocytes. FASEB J. 14, 2387-2389
17. Huang, M. C., Greig, N. H., Luo, W., Tweedie, D., Schwartz, J. B., Longo, D. L., Ferrucci, L., Ershler, W. B., and Goetzl, E. J. (2011) Preferential enhancement of older human T cell cytokine generation, chemotaxis, proliferation and survival by lenalidomide. Clin. Immunol. 138, 201-211
18. Olkhanud, P. B., Damdinsuren, B., Bodogai, M., Gress, R. E., Sen, R., Wejksza, K., Malchinkhuu, E., Wersto, R. P., and Biragyn, A. (2011) Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4 T cells to T-regulatory cells. Cancer Res. 71, 3505-3515
19. Graler, M. H., Huang, M. C., Watson, S., and Goetzl, E. J. (2005) Immunological effects of transgenic constitutive expression of the type 1 sphingosine 1-phosphate receptor by mouse lymphocytes. J. Immunol. 174, 1997-2003 (Pubitemid 40223941)
20. Gillis, S., Kozak, R., Durante, M., and Weksler, M. E. (1981) Immunological studies of aging. Decreased production of and response to T cell growth factor by lymphocytes from aged humans. J. Clin. Invest. 67, 937-942 (Pubitemid 11090530)
21. Rea, I. M., Stewart, M., Campbell, P., Alexander, H. D., Crockard, A. D., and Morris, T. C. (1996) Changes in lymphocyte subsets, interleukin 2, and soluble interleukin 2 receptor in old and very old age. Gerontology 42, 69-78 (Pubitemid 26110374)
22. Caruso, C., Candore, G., Cigna, D., DiLorenzo, G., Sireci, G., Dieli, F., and Salerno, A. (1996) Cytokine production pathway in the elderly. Immunol. Res. 15, 84-90 (Pubitemid 26142224)
23. Weng, N. P., Akbar, A. N., and Goronzy, J. (2009) CD28 T cells: their role in the age-associated decline of immune function. Trends Immunol. 30, 306-312
24. Kase, H., Richardson, P., and Jenner, P., eds (1999) Adenosine Receptors and Parkinson's Disease, Academic Press, New York
25. El Yacoubi, M., Ledent, C., Parmentier, M., Bertorelli, R., Ongini, E., Costentin, J., and Vaugeois, J. M. (2001) Adenosine A2A receptor antagonists are potential antidepressants: evidence based on pharmacology and A2A receptor knockout mice. Brit. J. Pharmacol. 134, 68-77 (Pubitemid 32835469)
26. Shook, B. C., Rassnick, S., Osborne, M. C., Davis, S., Westover, L., Boulet, J., Hall, D., Rupert, K. C., Heintzelman, G. R., Hansen, K., Chakravarty, D., Bullington, J. L., Russell, R., Branum, S., Wells, K. M., Damon, S., Youells, S., Li, X., Beauchamp, D. A., Palmer, D., Reyes, M., Demarest, K., Tang, Y., Rhodes, K., and Jackson, P. F. (2010) In vivo characterization of a dual adenosine A2A/A1 receptor antagonist in animal models of Parkinson's disease. J. Med. Chem. 53, 8104-8115