Dysfunction of PSA-specific CD8+ T cells in prostate cancer patients correlates with CD38 and Tim-3 expression

Cancer Immunology, Immunotherapy

Volumn 64, Issue 11, 2015, Pages 1487-1494

  Japp, Alberto Sada ^a   Kursunel, M Alper ^a   Meier, Sarah ^a   Mälzer, Julia N ^a   Li, Xiangdong ^b   Rahman, Nafis A ^c   Jekabsons, Waltraut ^a   Krause, Hans ^a   Magheli, Ahmed ^a   Klopf, Christian ^a   Thiel, Andreas ^a   Frentsch, Marco ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

Antigen specific T cells; Exhaustion; Prostate cancer; PSA

Indexed keywords

CD38 ANTIGEN; CD40 LIGAND; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PROSTATE SPECIFIC ANTIGEN; PROTEIN; TIM 3 PROTEIN; UNCLASSIFIED DRUG; CD38 PROTEIN, HUMAN; HAVCR2 PROTEIN, HUMAN; MEMBRANE PROTEIN;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DEGRANULATION; HAPLOTYPE; HLA SYSTEM; HUMAN; HUMAN CELL; MALE; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; TREATMENT RESPONSE; CHEMISTRY; IMMUNOLOGY; MIDDLE AGED; PROSTATIC NEOPLASMS;

AGED; ANTIGENS, CD38; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MIDDLE AGED; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS;

EID: 84945449684     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1752-y     Document Type: Article

References (44)

1. Cameron BJ, Gerry AB, Dukes J, Harper JV, Kannan V, Bianchi FC, Grand F, Brewer JE, Gupta M, Plesa G, Bossi G, Vuidepot A, Powlesland AS, Legg A, Adams KJ, Bennett AD, Pumphrey NJ, Williams DD, Binder-Scholl G, Kulikovskaya I, Levine BL, Riley JL, Varela-Rohena A, Stadtmauer EA, Rapoport AP, Linette GP, June CH, Hassan NJ, Kalos M, Jakobsen BK (2013) Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med 5(197):197ra103. doi:10.1126/scitranslmed.3006034
2. Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, Litzky L, Bagg A, Carreno BM, Cimino PJ, Binder-Scholl GK, Smethurst DP, Gerry AB, Pumphrey NJ, Bennett AD, Brewer JE, Dukes J, Harper J, Tayton-Martin HK, Jakobsen BK, Hassan NJ, Kalos M, June CH (2013) Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122(6):863–871. doi:10.1182/blood-2013-03-490565
3. Elkord E, Williams PE, Kynaston H, Rowbottom AW (2005) Differential CTLs specific for prostate-specific antigen in healthy donors and patients with prostate cancer. Int Immunol 17(10):1315–1325. doi:10.1093/intimm/dxh309
4. Hadaschik B, Su Y, Huter E, Ge Y, Hohenfellner M, Beckhove P (2012) Antigen specific T-cell responses against tumor antigens are controlled by regulatory T cells in patients with prostate cancer. J Urol 187(4):1458–1465. doi:10.1016/j.juro.2011.11.083
5. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, Xu Y, Frohlich MW, Schellhammer PF, Investigators IS (2010) Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363(5):411–422. doi:10.1056/NEJMoa1001294
6. Kantoff PW, Schuetz TJ, Blumenstein BA, Glode LM, Bilhartz DL, Wyand M, Manson K, Panicali DL, Laus R, Schlom J, Dahut WL, Arlen PM, Gulley JL, Godfrey WR (2010) Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSA-targeted immunotherapy in metastatic castration-resistant prostate cancer. J Clin Oncol 28(7):1099–1105. doi:10.1200/JCO.2009.25.0597
7. Sanda MG, Smith DC, Charles LG, Hwang C, Pienta KJ, Schlom J, Milenic D, Panicali D, Montie JE (1999) Recombinant vaccinia-PSA (PROSTVAC) can induce a prostate-specific immune response in androgen-modulated human prostate cancer. Urology 53(2):260–266
8. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, Rubin SC, Coukos G (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348(3):203–213. doi:10.1056/NEJMoa020177
9. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pages F (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313(5795):1960–1964. doi:10.1126/science.1129139
10. + T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci USA 104(9):3360–3365. doi:10.1073/pnas.0611533104
11. Ulloa-Montoya F, Louahed J, Dizier B, Gruselle O, Spiessens B, Lehmann FF, Suciu S, Kruit WH, Eggermont AM, Vansteenkiste J, Brichard VG (2013) Predictive gene signature in MAGE-A3 antigen-specific cancer immunotherapy. J Clin Oncol 31(19):2388–2395. doi:10.1200/JCO.2012.44.3762
12. Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, Alaparthy S, Berman D, Jure-Kunkel M, Siemers NO, Jackson JR, Shahabi V (2012) An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 61(7):1019–1031. doi:10.1007/s00262-011-1172-6
13. Galon J, Pages F, Marincola FM, Thurin M, Trinchieri G, Fox BA, Gajewski TF, Ascierto PA (2012) The immune score as a new possible approach for the classification of cancer. J Transl Med 10:1. doi:10.1186/1479-5876-10-1
14. Angell H, Galon J (2013) From the immune contexture to the immunoscore: the role of prognostic and predictive immune markers in cancer. Curr Opin Immunol 25(2):261–267. doi:10.1016/j.coi.2013.03.004
15. Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12(4):298–306. doi:10.1038/nrc3245
16. Chang S, Kohrt H, Maecker HT (2014) Monitoring the immune competence of cancer patients to predict outcome. Cancer Immunol Immunother 63(7):713–719. doi:10.1007/s00262-014-1521-3
17. + T cell dysfunction in melanoma patients. J Exp Med 207(10):2175–2186. doi:10.1084/jem.20100637
18. Frentsch M, Arbach O, Kirchhoff D, Moewes B, Worm M, Rothe M, Scheffold A, Thiel A (2005) Direct access to CD4 + T cells specific for defined antigens according to CD154 expression. Nat Med 11(10):1118–1124
19. Kennedy-Smith AG, McKenzie JL, Owen MC, Davidson PJ, Vuckovic S, Hart DN (2002) Prostate specific antigen inhibits immune responses in vitro: a potential role in prostate cancer. J Urol 168(2):741–747
20. Van Parijs L, Abbas AK (1998) Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 280(5361):243–248
21. Terhorst C, van Agthoven A, LeClair K, Snow P, Reinherz E, Schlossman S (1981) Biochemical studies of the human thymocyte cell-surface antigens T6, T9 and T10. Cell 23(3):771–780
22. Baitsch L, Baumgaertner P, Devevre E, Raghav SK, Legat A, Barba L, Wieckowski S, Bouzourene H, Deplancke B, Romero P, Rufer N, Speiser DE (2011) Exhaustion of tumor-specific CD8(+) T cells in metastases from melanoma patients. J Clin Invest 121(6):2350–2360. doi:10.1172/JCI46102
23. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, Zheng XX, Strom TB, Kuchroo VK (2005) The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6(12):1245–1252. doi:10.1038/ni1271
24. Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC (2010) Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 207(10):2187–2194. doi:10.1084/jem.20100643
25. Jones RB, Ndhlovu LC, Barbour JD, Sheth PM, Jha AR, Long BR, Wong JC, Satkunarajah M, Schweneker M, Chapman JM, Gyenes G, Vali B, Hyrcza MD, Yue FY, Kovacs C, Sassi A, Loutfy M, Halpenny R, Persad D, Spotts G, Hecht FM, Chun TW, McCune JM, Kaul R, Rini JM, Nixon DF, Ostrowski MA (2008) Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 205(12):2763–2779. doi:10.1084/jem.20081398
26. McMahan RH, Golden-Mason L, Nishimura MI, McMahon BJ, Kemper M, Allen TM, Gretch DR, Rosen HR (2010) Tim-3 expression on PD-1 + HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J Clin Invest 120(12):4546–4557. doi:10.1172/JCI43127
27. Yang ZZ, Grote DM, Ziesmer SC, Niki T, Hirashima M, Novak AJ, Witzig TE, Ansell SM (2012) IL-12 upregulates TIM-3 expression and induces T cell exhaustion in patients with follicular B cell non-Hodgkin lymphoma. J Clin Invest 122(4):1271–1282. doi:10.1172/JCI59806
28. Afanasiev OK, Yelistratova L, Miller N, Nagase K, Paulson K, Iyer JG, Ibrani D, Koelle DM, Nghiem P (2013) Merkel polyomavirus-specific T cells fluctuate with merkel cell carcinoma burden and express therapeutically targetable PD-1 and Tim-3 exhaustion markers. Clin Cancer Res 19(19):5351–5360. doi:10.1158/1078-0432.CCR-13-0035
29. Jin HT, Anderson AC, Tan WG, West EE, Ha SJ, Araki K, Freeman GJ, Kuchroo VK, Ahmed R (2010) Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci USA 107(33):14733–14738. doi:10.1073/pnas.1009731107
30. Ngiow SF, von Scheidt B, Akiba H, Yagita H, Teng MW, Smyth MJ (2011) Anti-TIM3 antibody promotes T cell IFN-gamma-mediated antitumor immunity and suppresses established tumors. Cancer Res 71(10):3540–3551. doi:10.1158/0008-5472.CAN-11-0096
31. Fourcade J, Sun Z, Pagliano O, Chauvin JM, Sander C, Janjic B, Tarhini AA, Tawbi HA, Kirkwood JM, Moschos S, Wang H, Guillaume P, Luescher IF, Krieg A, Anderson AC, Kuchroo VK, Zarour HM (2014) PD-1 and Tim-3 regulate the expansion of tumor antigen-specific CD8(+) T cells induced by melanoma vaccines. Cancer Res 74(4):1045–1055. doi:10.1158/0008-5472.CAN-13-2908
32. Fourcade J, Sun Z, Pagliano O, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Olive D, Kuchroo V, Zarour HM (2012) CD8(+) T cells specific for tumor antigens can be rendered dysfunctional by the tumor microenvironment through upregulation of the inhibitory receptors BTLA and PD-1. Cancer Res 72(4):887–896. doi:10.1158/0008-5472.CAN-11-2637
33. + T lymphocytes are oligoclonal and PD-1+. Prostate 69(15):1694–1703. doi:10.1002/pros.21020
34. Ebelt K, Babaryka G, Frankenberger B, Stief CG, Eisenmenger W, Kirchner T, Schendel DJ, Noessner E (2009) Prostate cancer lesions are surrounded by FOXP3+, PD-1+ and B7-H1+ lymphocyte clusters. Eur J Cancer 45(9):1664–1672. doi:10.1016/j.ejca.2009.02.015
35. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M (2012) Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366(26):2443–2454. doi:10.1056/NEJMoa1200690
36. Kwek SS, Cha E, Fong L (2012) Unmasking the immune recognition of prostate cancer with CTLA4 blockade. Nat Rev Cancer 12(4):289–297. doi:10.1038/nrc3223
37. Vanneman M, Dranoff G (2012) Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer 12(4):237–251. doi:10.1038/nrc3237
38. Xue BH, Zhang Y, Sosman JA, Peace DJ (1997) Induction of human cytotoxic T lymphocytes specific for prostate-specific antigen. Prostate 30(2):73–78
39. Perambakam SM, Srivastava R, Peace DJ (2005) Distinct cytokine patterns exist in peripheral blood mononuclear cell cultures of patients with prostate cancer. Clin Immunol 117(1):94–99. doi:10.1016/j.clim.2005.06.011
40. Corman JM, Sercarz EE, Nanda NK (1998) Recognition of prostate-specific antigenic peptide determinants by human CD4 and CD8 T cells. Clin Exp Immunol 114(2):166–172
41. Martins PN, Tullius SG, Markmann JF (2014) Immunosenescence and immune response in organ transplantation. Int Rev Immunol 33(3):162–173. doi:10.3109/08830185.2013.829469
42. do Canto FB, Lima Junior C, Teixeira IA, Bellio M, Nobrega A, Fucs R (2008) Susceptibility of neonatal T cells and adult thymocytes to peripheral tolerance to allogeneic stimuli. Immunology 125(3):387–396. doi:10.1111/j.1365-2567.2008.02855.x
43. Prelog M (2006) Aging of the immune system: a risk factor for autoimmunity? Autoimmun Rev 5(2):136–139. doi:10.1016/j.autrev.2005.09.008
44. Yu W, Jiang N, Ebert PJ, Kidd BA, Muller S, Lund PJ, Juang J, Adachi K, Tse T, Birnbaum ME, Newell EW, Wilson DM, Grotenbreg GM, Valitutti S, Quake SR, Davis MM (2015) Clonal deletion prunes but does not eliminate self-specific alphabeta CD8(+) T lymphocytes. Immunity 42(5):929–941. doi:10.1016/j.immuni.2015.05.001