CD8 T cell priming in the presence of IFN-α renders CTLs with improved responsiveness to homeostatic cytokines and recall antigens: important traits for adoptive T cell therapy

Journal of Immunology

Volumn 189, Issue 7, 2012, Pages 3299-3310

  Hervas Stubbs, Sandra ^a   Mancheño, Uxua ^b   Riezu Boj, Jose Ignacio ^a   Larraga, Ana ^a   Ochoa, Maria C ^a   Alignani, Diego ^a   Alfaro, Carlos ^a   Morales Kastresana, Aizea ^a   Gonzalez, Iranzu ^b   Larrea, Esther ^a   Pircher, Hanspeter ^c   Le Bon, Agnes ^d   Lopez Picazo, Jose M ^e   Martín Algarra, Salvador ^e   Prieto, Jesus ^e   Melero, Ignacio ^a,e  

^a UNIVERSITY OF NAVARRA   (Spain)

^b Digna Biotech   (Spain)

^c UNIVERSITY OF FREIBURG   (Germany)

^d INSTITUT COCHIN   (France)

^e UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CYTOKINE; GAMMA INTERFERON; HLA A2 ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 7; MART1[26-35] PEPTIDE; MELAN A; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EFFECTOR CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; HOMEOSTASIS; HUMANS; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; INTERFERON-ALPHA; INTERLEUKIN-15; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84866541815     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102495     Document Type: Article

References (55)

1. Joshi, N. S., and S. M. Kaech. 2008. Effector CD8 T cell development: a balancing act between memory cell potential and terminal differentiation. J. Immunol. 180: 1309-1315.
2. Williams, M. A., and M. J. Bevan. 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25: 171-192. (Pubitemid 46697906)
3. Sprent, J., and C. D. Surh. 2011. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat. Immunol. 12: 478-484.
4. Harty, J. T., and V. P. Badovinac. 2008. Shaping and reshaping CD8+ T-cell memory. Nat. Rev. Immunol. 8: 107-119. (Pubitemid 351161304)
5. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393: 480-483.
6. Butler, M. O., O. Imataki, Y. Yamashita, M. Tanaka, S. Ansén, A. Berezovskaya, G. Metzler, M. I. Milstein, M. M. Mooney, A. P. Murray, et al. 2012. Ex vivo expansion of human CD8+ T cells using autologous CD4+ T cell help. PLoS ONE 7: e30229.
7. Bourgeois, C., B. Rocha, and C. Tanchot. 2002. A role for CD40 expression on CD8+ T cells in the generation of CD8+ T cell memory. Science 297: 2060-2063.
8. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393: 478-480.
9. Bennett, S. R., F. R. Carbone, F. Karamalis, J. F. Miller, and W. R. Heath. 1997. Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help. J. Exp. Med. 186: 65-70. (Pubitemid 27304848)
10. Jennings, S. R., R. H. Bonneau, P. M. Smith, R. M. Wolcott, and R. Chervenak. 1991. CD4-positive T lymphocytes are required for the generation of the primary but not the secondary CD8-positive cytolytic T lymphocyte response to herpes simplex virus in C57BL/6 mice. Cell. Immunol. 133: 234-252.
11. Janssen, E. M., E. E. Lemmens, T. Wolfe, U. Christen, M. G. von Herrath, and S. P. Schoenberger. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856. (Pubitemid 36254145)
12. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339. (Pubitemid 36433726)
13. Assudani, D., H. I. Cho, N. DeVito, N. Bradley, and E. Celis. 2008. In vivo expansion, persistence, and function of peptide vaccine-induced CD8 T cells occur independently of CD4 T cells. Cancer Res. 68: 9892-9899.
14. Bachmann, M. F., R. M. Zinkernagel, and A. Oxenius. 1998. Immune responses in the absence of costimulation: viruses know the trick. J. Immunol. 161: 5791-5794. (Pubitemid 28535939)
15. Buller, R. M., K. L. Holmes, A. Hügin, T. N. Frederickson, and H. C. Morse, III. 1987. Induction of cytotoxic T-cell responses in vivo in the absence of CD4 helper cells. Nature 328: 77-79. (Pubitemid 17103585)
16. Di Rosa, F., and P. Matzinger. 1996. Long-lasting CD8 T cell memory in the absence of CD4 T cells or B cells. J. Exp. Med. 183: 2153-2163. (Pubitemid 26158907)
17. Marzo, A. L., V. Vezys, K. D. Klonowski, S. J. Lee, G. Muralimohan, M. Moore, D. F. Tough, and L. Lefrançois. 2004. Fully functional memory CD8 T cells in the absence of CD4 T cells. J. Immunol. 173: 969-975. (Pubitemid 38924270)
18. Rahemtulla, A., W. P. Fung-Leung, M.W. Schilham, T.M. Kündig, S. R. Sambhara, A. Narendran, A. Arabian, A.Wakeham, C. J. Paige, R. M. Zinkernagel, et al. 1991. Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353: 180-184. (Pubitemid 21912486)
19. Derré, L., J. P. Rivals, C. Jandus, S. Pastor, D. Rimoldi, P. Romero, O. Michielin, D. Olive, and D. E. Speiser. 2010. BTLA mediates inhibition of human tumor-specific CD8+ T cells that can be partially reversed by vaccination. J. Clin. Invest. 120: 157-167.
20. Hervas-Stubbs, S., A. Olivier, F. Boisgerault, N. Thieblemont, and C. Leclerc. 2007. TLR3 ligand stimulates fully functional memory CD8+ T cells in the absence of CD4+ T-cell help. Blood 109: 5318-5326. (Pubitemid 46890553)
21. Wiesel, M., W. Kratky, and A. Oxenius. 2011. Type I IFN substitutes for T cell help during viral infections. J. Immunol. 186: 754-763.
22. Kolumam, G. A., S. Thomas, L. J. Thompson, J. Sprent, and K. Murali-Krishna. 2005. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202: 637-650. (Pubitemid 41248415)
23. Xiao, Z., K. A. Casey, S. C. Jameson, J. M. Curtsinger, and M. F. Mescher. 2009. Programming for CD8 T cell memory development requires IL-12 or type I IFN. J. Immunol. 182: 2786-2794.
24. Curtsinger, J. M., J. O. Valenzuela, P. Agarwal, D. Lins, and M. F. Mescher. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174: 4465-4469.
25. Ramos, H. J., A. M. Davis, A. G. Cole, J. D. Schatzle, J. Forman, and J. D. Farrar. 2009. Reciprocal responsiveness to interleukin-12 and interferon-alpha specifies human CD8+ effector versus central memory T-cell fates. Blood 113: 5516-5525.
26. Hervas-Stubbs, S., J. I. Riezu-Boj, I. Gonzalez, U. Mancheño, J. Dubrot, A. Azpilicueta, I. Gabari, A. Palazon, A. Aranguren, J. Ruiz, et al. 2010. Effects of IFN-α as a signal-3 cytokine on human naïve and antigen-experienced CD8 (+) T cells. Eur. J. Immunol. 40: 3389-3402.
27. Badovinac, V. P., and J. T. Harty. 2006. Programming, demarcating, and manipulating CD8+ T-cell memory. Immunol. Rev. 211: 67-80. (Pubitemid 43882962)
28. Ho, W. Y., H. N. Nguyen, M. Wolfl, J. Kuball, and P. D. Greenberg. 2006. In vitro methods for generating CD8+ T-cell clones for immunotherapy from the naïve repertoire. J. Immunol. Methods 310: 40-52. (Pubitemid 43375974)
29. Voehringer, D., M. Koschella, and H. Pircher. 2002. Lack of proliferative capacity of human effector and memory T cells expressing killer cell lectinlike receptor G1 (KLRG1). Blood 100: 3698-3702. (Pubitemid 35303941)
30. Bevan, M. J. 2004. Helping the CD8(+) T-cell response. Nat. Rev. Immunol. 4: 595-602.
31. Santini, S. M., T. Di Pucchio, C. Lapenta, S. Parlato, M. Logozzi, and F. Belardelli. 2002. The natural alliance between type I interferon and dendritic cells and its role in linking innate and adaptive immunity. J. Interferon Cytokine Res. 22: 1071-1080. (Pubitemid 36051179)
32. Gattinoni, L., S. E. Finkelstein, C. A. Klebanoff, P. A. Antony, D. C. Palmer, P. J. Spiess, L. N. Hwang, Z. Yu, C. Wrzesinski, D. M. Heimann, et al. 2005. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J. Exp. Med. 202: 907-912. (Pubitemid 41396891)
33. Klebanoff, C. A., L. Gattinoni, P. Torabi-Parizi, K. Kerstann, A. R. Cardones, S. E. Finkelstein, D. C. Palmer, P. A. Antony, S. T. Hwang, S. A. Rosenberg, et al. 2005. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc. Natl. Acad. Sci. USA 102: 9571-9576. (Pubitemid 40981722)
34. Hinrichs, C. S., Z. A. Borman, L. Gattinoni, Z. Yu, W. R. Burns, J. Huang, C. A. Klebanoff, L. A. Johnson, S. P. Kerkar, S. Yang, et al. 2011. Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood 117: 808-814.
35. Ibegbu, C. C., Y. X. Xu, W. Harris, D. Maggio, J. D. Miller, and A. P. Kourtis. 2005. Expression of killer cell lectin-like receptor G1 on antigen-specific human CD8+ T lymphocytes during active, latent, and resolved infection and its relation with CD57. J. Immunol. 174: 6088-6094. (Pubitemid 40663797)
36. Intlekofer, A. M., N. Takemoto, E. J. Wherry, S. A. Longworth, J. T. Northrup, V. R. Palanivel, A. C. Mullen, C. R. Gasink, S. M. Kaech, J. D. Miller, et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6: 1236-1244. (Pubitemid 43045635)
37. Wojciechowski, S., P. Tripathi, T. Bourdeau, L. Acero, H. L. Grimes, J. D. Katz, F. D. Finkelman, and D. A. Hildeman. 2007. Bim/Bcl-2 balance is critical for maintaining naive and memory T cell homeostasis. J. Exp. Med. 204: 1665-1675. (Pubitemid 47048032)
38. Wallace, D. L., M. Bérard, M. V. Soares, J. Oldham, J. E. Cook, A. N. Akbar, D. F. Tough, and P. C. Beverley. 2006. Prolonged exposure of naïve CD8+ T cells to interleukin-7 or interleukin-15 stimulates proliferation without differentiation or loss of telomere length. Immunology 119: 243-253. (Pubitemid 44401643)
39. Gattinoni, L., E. Lugli, Y. Ji, Z. Pos, C. M. Paulos, M. F. Quigley, J. R. Almeida, E. Gostick, Z. Yu, C. Carpenito, et al. 2011. A human memory T cell subset with stem cell-like properties. Nat. Med. 17: 1290-1297.
40. Huang, J., H. T. Khong, M. E. Dudley, M. El-Gamil, Y. F. Li, S. A. Rosenberg, and P. F. Robbins. 2005. Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J. Immunother. 28: 258-267. (Pubitemid 40593992)
41. Huang, J., K. W. Kerstann, M. Ahmadzadeh, Y. F. Li, M. El-Gamil, S. A. Rosenberg, and P. F. Robbins. 2006. Modulation by IL-2 of CD70 and CD27 expression on CD8+ T cells: importance for the therapeutic effectiveness of cell transfer immunotherapy. J. Immunol. 176: 7726-7735. (Pubitemid 43849073)
42. Zhou, J., X. Shen, J. Huang, R. J. Hodes, S. A. Rosenberg, and P. F. Robbins. 2005. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J. Immunol. 175: 7046-7052. (Pubitemid 41598952)
43. Hinrichs, C. S., Z. A. Borman, L. Cassard, L. Gattinoni, R. Spolski, Z. Yu, L. Sanchez-Perez, P. Muranski, S. J. Kern, C. Logun, et al. 2009. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc. Natl. Acad. Sci. USA 106: 17469-17474.
44. Gattinoni, L., C. A. Klebanoff, D. C. Palmer, C. Wrzesinski, K. Kerstann, Z. Yu, S. E. Finkelstein, M. R. Theoret, S. A. Rosenberg, and N. P. Restifo. 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. (Pubitemid 40814670)
45. Gattinoni, L., X. S. Zhong, D. C. Palmer, Y. Ji, C. S. Hinrichs, Z. Yu, C. Wrzesinski, A. Boni, L. Cassard, L. M. Garvin, et al. 2009. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 15: 808-813.
46. Hinrichs, C. S., R. Spolski, C. M. Paulos, L. Gattinoni, K. W. Kerstann, D. C. Palmer, C. A. Klebanoff, S. A. Rosenberg, W. J. Leonard, and N. P. Restifo. 2008. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 111: 5326-5333.
47. Zhou, W., S. Chang, and T. M. Aune. 2004. Long-range histone acetylation of the Ifng gene is an essential feature of T cell differentiation. Proc. Natl. Acad. Sci. USA 101: 2440-2445. (Pubitemid 38269330)
48. Lu, Q., A. Wu, D. Ray, C. Deng, J. Attwood, S. Hanash, M. Pipkin, M. Lichtenheld, and B. Richardson. 2003. DNA methylation and chromatin structure regulate T cell perforin gene expression. J. Immunol. 170: 5124-5132. (Pubitemid 36554744)
49. Agarwal, P., A. Raghavan, S. L. Nandiwada, J. M. Curtsinger, P. R. Bohjanen, D. L. Mueller, and M. F. Mescher. 2009. Gene regulation and chromatin remodeling by IL-12 and type I IFN in programming for CD8 T cell effector function and memory. J. Immunol. 183: 1695-1704.
50. Fann, M., J. M. Godlove, M. Catalfamo, W. H. Wood, III, F. J. Chrest, N. Chun, L. Granger, R. Wersto, K. Madara, K. Becker, et al. 2006. Histone acetylation is associated with differential gene expression in the rapid and robust memory CD8 (+) T-cell response. Blood 108: 3363-3370.
51. Northrop, J. K., R. M. Thomas, A. D. Wells, and H. Shen. 2006. Epigenetic remodeling of the IL-2 and IFN-gamma loci in memory CD8 T cells is influenced by CD4 T cells. J. Immunol. 177: 1062-1069. (Pubitemid 44036608)
52. Northrop, J. K., A. D. Wells, and H. Shen. 2008. Cutting edge: chromatin remodeling as a molecular basis for the enhanced functionality of memory CD8 T cells. J. Immunol. 181: 865-868.
53. Araki, Y., M. Fann, R. Wersto, and N. P. Weng. 2008. Histone acetylation facilitates rapid and robust memory CD8 T cell response through differential expression of effector molecules (eomesodermin and its targets: perforin and granzyme B). J. Immunol. 180: 8102-8108.
54. Overwijk, W. W., M. R. Theoret, S. E. Finkelstein, D. R. Surman, L. A. de Jong, F. A. Vyth-Dreese, T. A. Dellemijn, P. A. Antony, P. J. Spiess, D. C. Palmer, et al. 2003. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med. 198: 569-580. (Pubitemid 37040391)
55. Zeng, R., R. Spolski, S. E. Finkelstein, S. Oh, P. E. Kovanen, C. S. Hinrichs, C. A. Pise-Masison, M. F. Radonovich, J. N. Brady, N. P. Restifo, et al. 2005. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J. Exp. Med. 201: 139-148. (Pubitemid 40130091)