Predicting cytotoxic T-cell age from multivariate analysis of static and dynamic biomarkers

Molecular and Cellular Proteomics

Volumn 10, Issue 3, 2011, Pages

  Rivet, Catherine A ^a   Hill, Abby S ^b   Lu, Hang ^a,c   Kemp, Melissa L ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b Emory University   (United States)

^c Georgia Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CD27 ANTIGEN; CD28 ANTIGEN; LYMPHOCYTE SURFACE MARKER; T LYMPHOCYTE RECEPTOR; CD3 ANTIGEN; INTERLEUKIN 2; LYMPHOCYTE ANTIGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL AGING; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LYMPHOCYTE CULTURE; LYMPHOCYTE SUBPOPULATION; MICROFLUIDIC ANALYSIS; MULTIVARIATE ANALYSIS; NORMAL HUMAN; PREDICTIVE VALIDITY; PRIORITY JOURNAL; CELL CULTURE; CELL MEMBRANE; CELL PROLIFERATION; CELL SHAPE; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; FLOW CYTOMETRY; LYMPHOCYTE ACTIVATION; METABOLISM; MICROFLUIDICS; PHOSPHORYLATION; PROTEIN DATABASE; SIGNAL TRANSDUCTION; TIME;

ADULT; ANTIGENS, CD28; ANTIGENS, CD3; BIOLOGICAL MARKERS; CELL AGING; CELL MEMBRANE; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; DATABASES, PROTEIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MICROFLUIDICS; MULTIVARIATE ANALYSIS; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC; TIME FACTORS; YOUNG ADULT;

EID: 79953175640     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.003921     Document Type: Article

References (81)

1. Gattinoni, L., Powell, D. J., Jr., Rosenberg, S. A., and Restifo, N. P. (2006) Adoptive immunotherapy for cancer: building on success. Nat. Rev. Immunol. 6, 383-393
2. Rosenberg, S. A., Restifo, N. P., Yang, J. C., Morgan, R. A., and Dudley, M. E. (2008) Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer 8, 299-308
3. Mackensen, A., Meidenbauer, N., Vogl, S., Laumer, M., Berger, J., and Andreesen, R. (2006) Phase I study of adoptive T-cell therapy using antigen-specific CD8(+) T cells for the treatment of patients with metastatic melanoma. J. Clin. Oncol. 24, 5060-5069
4. Porter, D. L., Levine, B. L., Bunin, N., Stadtmauer, E. A., Luger, S. M., Goldstein, S., Loren, A., Phillips, J., Nasta, S., Perl, A., Schuster, S., Tsai, D., Sohal, A., Veloso, E., Emerson, S., and June, C. H. (2006) A phase 1 trial of donor lymphocyte infusions expanded and activated ex vivo via CD3/CD28 costimulation. Blood 107, 1325-1331
5. Park, J. R., DiGiusto, D. L., Slovak, M., Wright, C., Naranjo, A., Wagner, J., Meechoovet, H. B., Bautista, C., Chang, W. C., Ostberg, J. R., and Jensen, M. C. (2007) Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol. Ther. 15, 825-833
6. Effros, R. B. (2007) Role of T lymphocyte replicative senescence in vaccine efficacy. Vaccine 25, 599-604
7. Effros, R. B., Dagarag, M., Spaulding, C., and Man, J. (2005) The role of CD8(+) T-cell replicative senescence in human aging. Immunol. Rev. 205, 147-157
8. Larbi, A., Franceschi, C., Mazzatti, D., Solana, R., Wikby, A., and Pawelec, G. (2008) Aging of the immune system as a prognostic factor for human longevity. Physiology 23, 64-74
9. Perillo, N. L., Walford, R. L., Newman, M. A., and Effros, R. B. (1989) Human T-lymphocytes possess a limited in vitro life-span. Exp. Gerontol. 24, 177-187
10. Yee, C., Thompson, J. A., Byrd, D., Riddell, S. R., Roche, P., Celis, E., and Greenberg, P. D. (2002) Adoptive T cell therapy using antigen-specific CD8(+) T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells. Proc. Natl. Acad. Sci. U.S.A. 99, 16168-16173
11. Shen, X., Zhou, J., Hathcock, K. S., Robbins, P., Powell, D. J., Jr., Rosenberg, S. A., and Hodes, R. J. (2007) Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J. Immunother. 30, 123-129 (Pubitemid 46052211)
12. Gattinoni, L., Klebanoff, C. A., Palmer, D. C., Wrzesinski, C., Kerstann, K., Yu, Z., Finkelstein, S. E., Theoret, M. R., Rosenberg, S. A., and Restifo, N. P. (2005) Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8(+) T cells. J. Clin. Invest. 115, 1616-1626
13. Pawelec, G., Akbar, A., Caruso, C., Solana, R., Grubeck-Loebenstein, B., and Wikby, A. (2005) Human immunosenescence: is it infectious?. Immunol. Rev. 205, 257-268
14. Hamann, D., Kostense, S., Wolthers, K. C., Otto, S. A., Baars, P. A., Miedema, F., and van Lier, R. A. W. (1999) Evidence that human CD8(+)CD45RA()CD27(-) cells are induced by antigen and evolve through extensive rounds of division. Int. Immunol. 11, 1027-1033
15. Effros, R. B., Boucher, N., Porter, V., Zhu, X., Spaulding, C., Walford, R. L., Kronenberg, M., Cohen, D., and Schächter, F. (1994) Decline in CD28(+) T-cells in centenarians and in long-term T-cell cultures - a possible cause for both in-vivo and in-vitro immunosenescence. Exp. Gerontol. 29, 601-609
16. Wilson, S., and Mazzatti, D. J. (2008) Current status and future prospects in the search for protein biomarkers of immunosenescence. Expert Rev. Proteomics 5, 561-569
17. Mazzatti, D. J., White, A., Forsey, R. J., Powell, J. R., and Pawelec, G. (2007) Gene expression changes in long-term culture of T-cell clones: genomic effects of chronic antigenic stress in aging and immunosenescence. Aging Cell 6, 155-163 (Pubitemid 46455060)
18. Cao, J. N., Gollapudi, S., Sharman, E. H., Jia, Z., and Gupta, S. (2010) Age-related alterations of gene expression patterns in human CD8+T cells. Aging Cell 9, 19-31
19. Mazzatti, D. J., Pawelec, G., Longdin, R., Powell, J. R., and Forsey, R. J. (2007) SELDI-TOF-MS ProteinChip array profiling of T-cell clones propagated in long-term culture identifies human profilin-1 as a potential bio-marker of immunosenescence. Proteome Sci 5, 7-
20. Hirsch, A. M., Rivet, C. A., Zhang, B., Kemp, M. L., and Lu, H. (2009) Parallel multi-time point cell stimulation and lysis on-chip for studying early signaling events in T cell activation. Lab. Chip 9, 536-544
21. Salieb-Beugelaar, G. B., Simone, G., Arora, A., Philippi, A., and Manz, A. (2010) Latest developments in microfluidic cell biology and analysis systems. Analyt. Chem. 82, 4848-4864
22. Cheong, R., Wang, C. J., and Levchenko, A. (2009) High content cell screening in a microfluidic device. Mol. Cell Proteomics 8, 433-442
23. Thompson, J. A., Figlin, R. A., Sifri-Steele, C., Berenson, R. J., and Frohlich, M. W. (2003) A Phase I Trial of CD3/CD28-activated T Cells (Xcellerated T Cells) and Interleukin-2 in Patients with Metastatic Renal Cell Carcinoma. Clin. Cancer Res. 9, 3562-3570
24. Newrzela, S., Gunda, B., and Laer, D. V. (2008) T cell culture for gamma retroviral transfer. Genetic Modifications of Hematopoietic Stem Cells. Methods and Protocols 506, 71-82
25. McDonald, J. C., Duffy, D. C., Anderson, J. R., Chiu, D. T., Wu, H., Schueller, O. J., and Whitesides, G. M. (2000) Fabrication of microfluidic systems in poly(dimethylsiloxane). Electrophoresis 21, 27-40
26. Krutzik, P. O., and Nolan, G. P. (2003) Intracellular phospho-protein staining techniques for flow cytometry: Monitoring single cell signaling events. Cytom. Part A 55A, 61-70
27. Gaudet, S., Janes, K. A., Albeck, J. G., Pace, E. A., Lauffenburger, D. A., and Sorger, P. K. (2005) A compendium of signals and responses triggered by prodeath and prosurvival cytokines. Mol. Cell Proteomics 4, 1569-1590
28. Wold, S., Sjostrom, M., and Eriksson, L. (2001) PLS-regression: a basic tool of chemometrics. Chemometr. Intell. Lab. 58, 109-130
29. Stroock, A. D., Dertinger, S. K., Ajdari, A., Mezic, I., Stone, H. A., and Whitesides, G. M. (2002) Chaotic mixer for microchannels. Science 295, 647-651
30. Partanen, S. (2001) Alkaline fixation-resistant acid phosphatases in human tissues: Histochemical evidence for a new type of acid phosphatase in endothefial, endometrial and neuronal sites. Histochem. J. 33, 387-395
31. Röth, A., Schneider, L., Himmelreich, H., Baerlocher, G. M., and Dührsen, U. (2007) Impact of culture conditions on the proliferative lifespan of human T cells in vitro. Cytotherapy 9, 91-98
32. Laux, I., Khoshnan, A., Tindell, C., Bae, D., Zhu, X., June, C. H., Effros, R. B., and Nel, A. (2000) Response differences between human CD4+ and CD8+ T-cells during CD28 costimulation: Implications for immune cell-based therapies and studies related to the expansion of doublepositive T-cells during aging. Clin. Immunol. 96, 187-197
33. Perillo, N. L., Naeim, F., Walford, R. L., and Effros, R. B. (1993) The in vitro senescence of human T lymphocytes: Failure to divide is not associated with a loss of cytolytic activity or memory T cell phenotype. Mechanisms Ageing Develop. 67, 173-185
34. Jaruga, E., Skierski, J., Radziszewska, E., and Sikora, E. (2000) Proliferation and apoptosis of human T cells during replicative senescence - a critical approach. Acta Biochim. Pol. 47, 293-300
35. Erickson, S., Sangfelt, O., Heyman, M., Castro, J., Einhorn, S., and Grandér, D. (1998) Involvement of the Ink4 proteins p16 and p15 in T-lymphocyte senescence. Oncogene 17, 595-602 (Pubitemid 28401028)
36. Vallejo, A. N., Weyand, C. M., and Goronzy, J. J. (2004) T-cell senescence: a culprit of immune abnormalities in chronic inflammation and persistent infection. Trends Mol. Med. 10, 119-124
37. Brenchley, J. M., Karandikar, N. J., Betts, M. R., Ambrozak, D. R., Hill, B. J., Crotty, L. E., Casazza, J. P., Kuruppu, J., Migueles, S. A., Connors, M., Roederer, M., Douek, D. C., and Koup, R. A. (2003) Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood 101, 2711-2720
38. Koch, S., Larbi, A., Derhovanessian, E., Ozcelik, D., Naumova, E., and Pawelec, G. (2008) Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun. Ageing 5, 6
39. Effros, R. B. "Loss of CD28 expression on T lymphocyes: A marker of replicative senescence." Developmental & Comparative Immunology 21(6): 471-478
40. Fülöp, T., Jr., Larbi, A., Dupuis, G., and Pawelec, G. (2003) Ageing, autoimmunity and arthritis - Perturbations of TCR signal transduction pathways with ageing a biochemical paradigm for the ageing immune system. Arthritis Res. Ther. 5, 290-302
41. Berg, N. N., Puente, L. G., Dawicki, W., and Ostergaard, H. L. (1998) Sustained TCR signaling is required for mitogen-activated protein kinase activation and degranulation by cytotoxic T lymphocytes. J. Immunol. 161, 2919-2924
42. Fauce, S. R., Jamieson, B. D., Chin, A. C., Mitsuyasy, R. T., Parish, S. T., Ng, H. L., Kitchen, C. M., Yang, O. O., Harley, C. B., and Effros, R. B. (2008) Telomerase-Based Pharmacologic Enhancement of Antiviral Function of Human CD8(+) T Lymphocytes. J. Immunol. 181, 7400-7406
43. Altan-Bonnet, G., and Germain, R. N. (2005) Modeling T cell antigen discrimination based on feedback control of digital ERK responses. Plos Biol. 3, 1925-1938
44. Singh, K., Deshpande, P., Pryshchep, S., Colmegna, I., Liarski, V., Weyand, C. M., and Goronzy, J. J. (2009) ERK-dependent T cell receptor threshold calibration in rheumatoid arthritis. J. Immunol. 183, 8258-8267
45. Lin, J., Harding, A., Giurisato, E., and Shaw, A. S. (2009) KSR1 modulates the sensitivity of mitogen-activated protein kinase pathway activation in T cells without altering fundamental system outputs. Mol. Cell. Biol. 29, 2082-2091
46. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95, 14863-14868
47. Miller-Jensen, K., Janes, K. A., Brugge, J. S., and Lauffenburger, D. A. (2007) Common effector processing mediates cell-specific responses to stimuli. Nature 448, 604-608
48. Kemp, M. L., Wille, L., Lewis, C. L., Nicholson, L. B., and Lauffenburger, D. A. (2007) Quantitative network signal combinations downstream of TCR activation can predict IL-2 production response. J. Immunol. 178, 4984-4992
49. Carr, J. M., Carrasco, M. J., Thaventhiran, J. E., Bambrough, P. J., Kraman, M., Edwards, A. D., Al-Shamkhani, A., and Fearon, D. T. (2006) CD27 mediates interieukin-2-independent clonal expansion of the CD8(+) T cell without effector differentiation. Proc. Natl. Acad .Sci. U.S.A. 103, 19454-19459
50. Frauwirth, K. A., Riley, J. L., Harris, M. H., Parry, R. V., Rathmell, J. C., Plas, D. R., Elstrom, R. L., June, C. H., and Thompson, C. B. (2002) The CD28 signaling pathway regulates glucose metabolism. Immunity 16, 769-777
51. Miller, J., Baker, C., Cook, K., Graf, B., Sanchez-Lockhart, M., Sharp, K., Wang, X., Yang, B., and Yoshida, T. (2009) Two pathways of costimulation through CD28. Immunol. Res. 45, 159-172
52. Carey, K. D., Dillon, T. J., Schmitt, J. M., Baird, A. M., Holdorf, A. D., Straus, D. B., Shaw, A. S., and Stork, P. J. S. (2000) CD28 and the tyrosine kinase Lck stimulate mitogen-activated protein kinase activity in T cells via inhibition of the small G protein Rap1. Mol. Cell. Biol. 20, 8409-8419
53. Melenhorst, J. J. (2009) Optimizing T-cell expansion: have we reached the limit?. Cytotherapy 11, 813-814
54. Rasmussen, A. M., Borelli, G., Hoel, H. J., Lislerud, K., Gaudernack, G., Kvalheim, G., and Aarvak, T. (2010) Ex vivo expansion protocol for human tumor specific T cells for adoptive T cell therapy. J. Immunol. Methods 355, 52-60
55. Zhang, H., Snyder, K. M., Suhoski, M. M., Maus, M. V., Kapoor, V., June, C. H., and Mackall, C. L. (2007) 4-1BB is superior to CD28 costimulation for generating CD8(+) cytotoxic lymphocytes for adoptive immunotherapy. J. Immunol. 179, 4910-4918
56. Jeras, M., Bricl, I., Zorec, R., and Svajger, U. (2010) Induction/engineering, detection, selection, and expansion of clinical-grade human antigen-specific CD8(+) cytotoxic T cell clones for adoptive immunotherapy. J. Biomed. Biotechnol. 2010, 1-15
57. Germenis, A. E., and Karanikas, V. (2010) Cord blood as a source of non-senescent lymphocytes for tumor immunotherapy. J. Reprod. Immunol. 85, 47-50
58. Dagarag, M., Ng, H., Lubong, R., Effros, R. B., and Yang, O. O. (2003) Differential impairment of lytic and cytokine functions in senescent human immunodeficiency virus type 1-specific cytotoxic T lymphocytes. J. Virol. 77, 3077-3083
59. Parish, S. T., Wu, J. E., and Effros, R. B. (2009) Modulation of T lymphocyte replicative senescence via TNF-alpha inhibition: role of caspase-3. J. Immunol. 182, 4237-4243
60. Bryl, E., Vallejo, A. N., Weyand, C. M., and Goronzy, J. J. (2001) Downregulation of CD28 expression by TNF-alpha. J. Immunol. 167, 3231-3238
61. Warrington, K. J., Vallejo, A. N., Weyand, C. M., and Goronzy, J. J. (2003) CD28 loss in senescent CD4+ T cells: reversal by interleukin-12 stimulation. Blood 101, 3543-3549 (Pubitemid 36857940)
62. Brzezińska, A., Magalska, A., Szybińska, A., and Sikora, E. (2004) Proliferation and apoptosis of human CD8(+)CD28(+) and CD8(+)CD28(-) lymphocytes during aging. Exp. Gerontol. 39, 539-544
63. Larbi, A., Dupuis, G., Khalil, A., Douziech, N., Fortin, C., and Fülöp, T., Jr. (2006) Differential role of lipid rafts in the functions of CD4(+) and CD8(+) human T lymphocytes with aging. Cell Signal 18, 1017-1030
64. Suni, M. A., Maino, V. C., and Maecker, H. T. (2005) Ex vivo analysis of T-cell function. Curr. Opin. Immunol. 17, 434-440
65. Barber, D. L., Wherry, E. J., and Ahmed, R. (2003) Cutting edge: Rapid in vivo killing by memory CD8 T cells. J. Immunol. 171, 27-31 (Pubitemid 36745269)
66. Djeu, J. Y., Jiang, K., and Wei, S. (2002) A view to a kill. Clin. Cancer Res. 8, 636-640
67. Lawless, C., Wang, C., Jurk, D., Merz, A., Zglinicki, T. V., and Passos, J. F. (2010) Quantitative assessment of markers for cell senescence. Exp. Gerontol. 45, 772-778
68. Tsygankov, D., Liu, Y., Sanoff, H. K., Sharpless, N. E., and Elston, T. C. (2009) A quantitative model for age-dependent expression of the p16INK4a tumor suppressor. Proc. Natl. Acad. Sci.U. S. A. 106, 16562-16567
69. Huse, M., Klein, L. O., Girvin, A. T., Faraj, J. M., Li, Q. J., Kuhns, M. S., and Davis, M. M. (2007) Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. Immunity 27, 76-88
70. Janes, K. A., Albeck, J. G., Gaudet, S., Sorger, P. K., Lauffenburger, D. A., and Yaffe, M. B. (2005) A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310, 1646-1653
71. Janes, K. A., Kelly, J. R., Gaudet, S., Albeck, J. G., Sorger, P. K., and Lauffenburger, D. A. (2004) Cue-signal-response analysis of TNF-induced apoptosis by partial least squares regression of dynamic multivariate data. J. Comput. Biol. 11, 544-561
72. Borthwick, N. J., Lowdell, M., Salmon, M., and Akbar, A. N. (2000) Loss of CD28 expression on CD8(+) T cells is induced by IL-2 receptor gamma chain signalling cytokines and type IIFN, and increases susceptibility to activation-induced apoptosis. Int. Immunol. 12, 1005-1013
73. Miller, R. A., Garcia, G., Kirk, C. J., and Witkowski, J. M. (1997) Early activation defects in T lymphocytes from aged mice. Immunol. Rev. 160, 79-90
74. Larbi, A., Douziech, N., Dupuis, G., Khalil, A., Pelletier, H., Guerard, K. P., and Fülöp, T., Jr. (2004) Age-associated alterations in the recruitment of signal-transduction proteins to lipid rafts in human T lymphocytes. J. Leukocyte Biol. 75, 373-381 (Pubitemid 38174595)
75. Larbi, A., Kempf, J., and Pawelec, G. (2007) Oxidative stress modulation and T cell activation. Exp. Gerontol. 42, 852-858
76. Weber, G. F. (2002) Altered lymphocyte calcium signaling and age-related diseases. In Calcium Homeostasis and Signaling in Aging. Advances in Cell Aging and Gerontology, 10 (Mattson, M. P., ed.), 127-145, Elsevier, Amsterdam
77. Tomoiu, A., Larbi, A., Fortin, C., Dupuis, G., and Fülöp, T., Jr. (2007) Do membrane rafts contribute to human immunosenescence?. Ann. NY Acad. Sci. 1100, 98-110
78. Passos, J. F., Saretzki, G., Ahmed, S., Nelson, G., Richter, T., Peters, H., Wappler, I., Birket, M. J., Harold, G., Schaeuble, K., Birch-Machin, M. A., Kirkwood, T. B., and von, Zglinicki, T. (2007) Mitochondrial Dysfunction Accounts for the Stochastic Heterogeneity in Telomere-Dependent Senescence. Plos Biol. 5, e110
79. Bahar, R., Hartmann, C. H., Rodriguez, K. A., Denny, A. D., Busuttil, R. A., Dollé, M. E., Calder, R. B., Chisholm, G. B., Pollock, B. H., Klein, C. A., and Vijg, J. (2006) Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 441, 1011-1014 (Pubitemid 43980358)
80. Feinerman, O., Veiga, J., Dorfman, J. R., Germain, R. N., and Altan-Bonnet, G. (2008) Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 321, 1081-1084
81. Pritchard, J. R., Cosgrove, B. D., Hemann, M. T., Griffith, L. G., Wands, J. R., and Lauffenburger, D. A. (2009) Three-kinase inhibitor combination recreates multipathway effects of a geldanamycin analogue on hepatocellular carcinoma cell death. Mol. Cancer Ther. 8, 2183-2192