Expression of CD39 on Activated T Cells Impairs their Survival in Older Individuals

Cell Reports

Volumn 14, Issue 5, 2016, Pages 1218-1231

  Fang, Fengqin ^a,b   Yu, Mingcan ^a,b   Cavanagh, Mary M ^a,b   Hutter Saunders, Jessica ^a,b   Qi, Qian ^a,b   Ye, Zhongde ^a,b   Le Saux, Sabine ^a,b   Sultan, William ^a,b   Turgano, Emerson ^a,b   Dekker, Cornelia L ^a   Tian, Lu ^a   Weyand, Cornelia M ^a,b   Goronzy, Jörg J ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CD39 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; PROTEIN BAX; APYRASE; ECTOATPASE; LEUKOCYTE ANTIGEN;

AMINO TERMINAL SEQUENCE; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL FATE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTPD1 GENE; ENZYME ACTIVITY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION; ADULT; AGED; AGING; CELL CLONE; CELL PROLIFERATION; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; PHYSIOLOGICAL STRESS; VERY ELDERLY; YOUNG ADULT;

ADENOSINE TRIPHOSPHATASES; ADULT; AGED; AGED, 80 AND OVER; AGING; ANTIGENS, CD; APOPTOSIS; APYRASE; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELL SURVIVAL; CLONE CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MIDDLE AGED; STRESS, PHYSIOLOGICAL; YOUNG ADULT;

EID: 84957990383     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.002     Document Type: Article

References (49)

1. Araki K., Turner A.P., Shaffer V.O., Gangappa S., Keller S.A., Bachmann M.F., Larsen C.P., Ahmed R. mTOR regulates memory CD8 T-cell differentiation. Nature 2009, 460:108-112.
2. Aymerich I., Foufelle F., Ferré P., Casado F.J., Pastor-Anglada M. Extracellular adenosine activates AMP-dependent protein kinase (AMPK). J. Cell Sci. 2006, 119:1612-1621.
3. Bensaad K., Tsuruta A., Selak M.A., Vidal M.N., Nakano K., Bartrons R., Gottlieb E., Vousden K.H. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006, 126:107-120.
4. Boeynaems J.M., Communi D., Gonzalez N.S., Robaye B. Overview of the P2 receptors. Semin. Thromb. Hemost. 2005, 31:139-149.
5. Bungard D., Fuerth B.J., Zeng P.Y., Faubert B., Maas N.L., Viollet B., Carling D., Thompson C.B., Jones R.G., Berger S.L. Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science 2010, 329:1201-1205.
6. Chipuk J.E., Kuwana T., Bouchier-Hayes L., Droin N.M., Newmeyer D.D., Schuler M., Green D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014.
7. Clayton A., Al-Taei S., Webber J., Mason M.D., Tabi Z. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J. Immunol. 2011, 187:676-683.
8. Deaglio S., Dwyer K.M., Gao W., Friedman D., Usheva A., Erat A., Chen J.F., Enjyoji K., Linden J., Oukka M., et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 2007, 204:1257-1265.
9. Dong R.P., Tachibana K., Hegen M., Munakata Y., Cho D., Schlossman S.F., Morimoto C. Determination of adenosine deaminase binding domain on CD26 and its immunoregulatory effect on T cell activation. J. Immunol. 1997, 159:6070-6076.
10. Dormitzer P.R., Galli G., Castellino F., Golding H., Khurana S., Del Giudice G., Rappuoli R. Influenza vaccine immunology. Immunol. Rev. 2011, 239:167-177.
11. Dwyer K.M., Hanidziar D., Putheti P., Hill P.A., Pommey S., McRae J.L., Winterhalter A., Doherty G., Deaglio S., Koulmanda M., et al. Expression of CD39 by human peripheral blood CD4+ CD25+ T cells denotes a regulatory memory phenotype. Am. J. Transplant. 2010, 10:2410-2420.
12. Ferraro A., D'Alise A.M., Raj T., Asinovski N., Phillips R., Ergun A., Replogle J.M., Bernier A., Laffel L., Stranger B.E., et al. Interindividual variation in human T regulatory cells. Proc. Natl. Acad. Sci. USA 2014, 111:E1111-E1120.
13. Friedman D.J., Kunzli B.M., A-Rahim Y.I., Sevigny J., Berberat P.O., Enjyoji K., Csizmadia E., Friess H., Robson S.C. CD39 deletion exacerbates experimental murine colitis and human polymorphisms increase susceptibility to inflammatory bowel disease. Proc. Natl. Acad. Sci. USA 2009, 106:16788-16793.
14. Goronzy J.J., Weyand C.M. Understanding immunosenescence to improve responses to vaccines. Nat. Immunol. 2013, 14:428-436.
15. Haynes L., Swain S.L. Aged-related shifts in T cell homeostasis lead to intrinsic T cell defects. Semin. Immunol. 2012, 24:350-355.
16. Intlekofer A.M., Takemoto N., Kao C., Banerjee A., Schambach F., Northrop J.K., Shen H., Wherry E.J., Reiner S.L. Requirement for T-bet in the aberrant differentiation of unhelped memory CD8+ T cells. J. Exp. Med. 2007, 204:2015-2021.
17. Jones R.G., Plas D.R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M.J., Thompson C.B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 2005, 18:283-293.
18. Kaech S.M., Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells. Nat. Immunol. 2001, 2:415-422.
19. Kaech S.M., Wherry E.J. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 2007, 27:393-405.
20. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 2003, 4:1191-1198.
21. Levin M.J. Immune senescence and vaccines to prevent herpes zoster in older persons. Curr. Opin. Immunol. 2012, 24:494-500.
22. Li G., Yu M., Lee W.W., Tsang M., Krishnan E., Weyand C.M., Goronzy J.J. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat. Med. 2012, 18:1518-1524.
23. Mandapathil M., Hilldorfer B., Szczepanski M.J., Czystowska M., Szajnik M., Ren J., Lang S., Jackson E.K., Gorelik E., Whiteside T.L. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J. Biol. Chem. 2010, 285:7176-7186.
24. Marshall H.D., Chandele A., Jung Y.W., Meng H., Poholek A.C., Parish I.A., Rutishauser R., Cui W., Kleinstein S.H., Craft J., Kaech S.M. Differential expression of Ly6C and T-bet distinguish effector and memory Th1 CD4(+) cell properties during viral infection. Immunity 2011, 35:633-646.
25. Miyashita T., Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995, 80:293-299.
26. Moncrieffe H., Nistala K., Kamhieh Y., Evans J., Eddaoudi A., Eaton S., Wedderburn L.R. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J. Immunol. 2010, 185:134-143.
27. Montecino-Rodriguez E., Berent-Maoz B., Dorshkind K. Causes, consequences, and reversal of immune system aging. J. Clin. Invest. 2013, 123:958-965.
28. Nieminen A.I., Eskelinen V.M., Haikala H.M., Tervonen T.A., Yan Y., Partanen J.I., Klefström J. Myc-induced AMPK-phospho p53 pathway activates Bak to sensitize mitochondrial apoptosis. Proc. Natl. Acad. Sci. USA 2013, 110:E1839-E1848.
29. Ohta A., Sitkovsky M. Extracellular adenosine-mediated modulation of regulatory T cells. Front. Immunol. 2014, 5:304.
30. Pepper M., Pagán A.J., Igyártó B.Z., Taylor J.J., Jenkins M.K. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 2011, 35:583-595.
31. Petersen L.R., Brault A.C., Nasci R.S. West Nile virus: review of the literature. JAMA 2013, 310:308-315.
32. Powell J.D., Delgoffe G.M. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 2010, 33:301-311.
33. Qi Q., Liu Y., Cheng Y., Glanville J., Zhang D., Lee J.Y., Olshen R.A., Weyand C.M., Boyd S.D., Goronzy J.J. Diversity and clonal selection in the human T-cell repertoire. Proc. Natl. Acad. Sci. USA 2014, 111:13139-13144.
34. Rolf J., Zarrouk M., Finlay D.K., Foretz M., Viollet B., Cantrell D.A. AMPKα1: a glucose sensor that controls CD8 T-cell memory. Eur. J. Immunol. 2013, 43:889-896.
35. Salgado F.J., Perez-Diaz A., Villanueva N.M., Lamas O., Arias P., Nogueira M. CD26: a negative selection marker for human Treg cells. Cytometry A 2012, 81:843-855.
36. Sarkar S., Kalia V., Haining W.N., Konieczny B.T., Subramaniam S., Ahmed R. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 2008, 205:625-640.
37. Schenk U., Westendorf A.M., Radaelli E., Casati A., Ferro M., Fumagalli M., Verderio C., Buer J., Scanziani E., Grassi F. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 2008, 1:ra6.
38. Thompson W.W., Shay D.K., Weintraub E., Brammer L., Cox N., Anderson L.J., Fukuda K. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003, 289:179-186.
39. Tresini M., Lorenzini A., Torres C., Cristofalo V.J. Modulation of replicative senescence of diploid human cells by nuclear ERK signaling. J. Biol. Chem. 2007, 282:4136-4151.
40. van Leeuwen E.M., Sprent J., Surh C.D. Generation and maintenance of memory CD4(+) T Cells. Curr. Opin. Immunol. 2009, 21:167-172.
41. Weng N.P. Aging of the immune system: how much can the adaptive immune system adapt?. Immunity 2006, 24:495-499.
42. Wertheimer A.M., Bennett M.S., Park B., Uhrlaub J.L., Martinez C., Pulko V., Currier N.L., Nikolich-Žugich D., Kaye J., Nikolich-Žugich J. Aging and cytomegalovirus infection differentially and jointly affect distinct circulating T cell subsets in humans. J. Immunol. 2014, 192:2143-2155.
43. Williams M.A., Bevan M.J. Effector and memory CTL differentiation. Annu. Rev. Immunol. 2007, 25:171-192.
44. Williams M.A., Ravkov E.V., Bevan M.J. Rapid culling of the CD4+ T cell repertoire in the transition from effector to memory. Immunity 2008, 28:533-545.
45. Xie D.L., Wu J., Lou Y.L., Zhong X.P. Tumor suppressor TSC1 is critical for T-cell anergy. Proc. Natl. Acad. Sci. USA 2012, 109:14152-14157.
46. Yip L., Woehrle T., Corriden R., Hirsh M., Chen Y., Inoue Y., Ferrari V., Insel P.A., Junger W.G. Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J. 2009, 23:1685-1693.
47. Yu M., Li G., Lee W.W., Yuan M., Cui D., Weyand C.M., Goronzy J.J. Signal inhibition by the dual-specific phosphatase 4 impairs T cell-dependent B-cell responses with age. Proc. Natl. Acad. Sci. USA 2012, 109:E879-E888.
48. Zhang W., Brahmakshatriya V., Swain S.L. CD4 T cell defects in the aged: causes, consequences and strategies to circumvent. Exp. Gerontol. 2014, 54:67-70.
49. Zhao J., Cao Y., Lei Z., Yang Z., Zhang B., Huang B. Selective depletion of CD4+CD25+Foxp3+ regulatory T cells by low-dose cyclophosphamide is explained by reduced intracellular ATP levels. Cancer Res. 2010, 70:4850-4858.