Very late antigen-1 marks functional tumor-resident CD8 T cells and correlates with survival of melanoma patients

Frontiers in Immunology

Volumn 7, Issue DEC, 2016, Pages

  Murray, Timothy ^a   Marraco, Silvia A Fuertes ^a   Baumgaertner, Petra ^a   Bordry, Natacha ^a   Cagnon, Laurène ^a   Donda, Alena ^a   Romero, Pedro ^a   Verdeil, Grégory ^a   Speiser, Daniel E ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

CD103; Melanoma; Tissue resident memory T cells,cancer vaccines; VLA 1

Indexed keywords

CD103 ANTIGEN; HOMING RECEPTOR; MONOCLONAL ANTIBODY; VACCINE; VERY LATE ACTIVATION ANTIGEN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CLINICAL ARTICLE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNIZATION; MELANOMA; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR VOLUME;

EID: 85009428646     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00573     Document Type: Article

References (46)

1. Schadendorf D, Hodi FS, Robert C, Weber JS, Margolin K, Hamid O, et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma. J Clin Oncol (2015) 33:1889-94. doi:10.1200/JCO.2014.56.2736
2. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res (2011) 17:4550-7. doi:10.1158/1078-0432.CCR-11-0116
3. June CH, Riddell SR, Schumacher TN. Adoptive cellular therapy: a race to the finish line. Sci Transl Med (2015) 7:280s7. doi:10.1126/scitranslmed.aaa3643
4. Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol (2015) 33:1974-82. doi:10.1200/JCO.2014.59.4358
5. Dudley ME, Gross CA, Somerville RP, Hong Y, Schaub NP, Rosati SF, et al. Randomized selection design trial evaluating CD8+-enriched versus unselected tumor-infiltrating lymphocytes for adoptive cell therapy for patients with melanoma. J Clin Oncol (2013) 31:2152-9. doi:10.1200/JCO.2012.46.6441
6. Gajewski TF, Schumacher T. Cancer immunotherapy. Curr Opin Immunol (2013) 25:259-60. doi:10.1016/j.coi.2013.03.008
7. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer (2012) 12:298-306. doi:10.1038/nrc3245
8. Sapoznik S, Ortenberg R, Galore-Haskel G, Kozlovski S, Levy D, Avivi C, et al. CXCR1 as a novel target for directing reactive T cells toward melanoma: implications for adoptive cell transfer immunotherapy. Cancer Immunol Immunother (2012) 61:1833-47. doi:10.1007/s00262-012-1245-1
9. Asai H, Fujiwara H, An J, Ochi T, Miyazaki Y, Nagai K, et al. Co-introduced functional CCR2 potentiates in vivo anti-lung cancer functionality mediated by T cells double gene-modified to express WT1-specific T-cell receptor. PLoS One (2013) 8:e56820. doi:10.1371/journal.pone.0056820
10. Hong M, Puaux AL, Huang C, Loumagne L, Tow C, Mackay C, et al. Chemotherapy induces intratumoral expression of chemokines in cutaneous melanoma, favoring T-cell infiltration and tumor control. Cancer Res (2011) 71:6997-7009. doi:10.1158/0008-5472.CAN-11-1466
11. Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, Slingluff C, et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res (2009) 69:3077-85. doi:10.1158/0008-5472.CAN-08-2281
12. Moon EK, Carpenito C, Sun J, Wang LC, Kapoor V, Predina J, et al. Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T cells expressing a mesothelin-specific chimeric antibody receptor. Clin Cancer Res (2011) 17:4719-30. doi:10.1158/1078-0432.CCR-11-0351
13. Peng W, Ye Y, Rabinovich BA, Liu C, Lou Y, Zhang M, et al. Transduction of tumor-specific T cells with CXCR2 chemokine receptor improves migration to tumor and antitumor immune responses. Clin Cancer Res (2010) 16:5458-68. doi:10.1158/1078-0432.CCR-10-0712
14. Okada N, Sasaki A, Niwa M, Okada Y, Hatanaka Y, Tani Y, et al. Tumor suppressive efficacy through augmentation of tumor-infiltrating immune cells by intratumoral injection of chemokine-expressing adenoviral vector. Cancer Gene Ther (2006) 13:393-405. doi:10.1038/sj.cgt.7700903
15. Mullins IM, Slingluff CL, Lee JK, Garbee CF, Shu J, Anderson SG, et al. CXC chemokine receptor 3 expression by activated CD8+ T cells is associated with survival in melanoma patients with stage III disease. Cancer Res (2004) 64:7697-701. doi:10.1158/0008-5472.CAN-04-2059
16. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol (2009) 10:524-30. doi:10.1038/ni.1718
17. Mackay LK, Rahimpour A, Ma JZ, Collins N, Stock AT, Hafon ML, et al. The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat Immunol (2013) 14:1294-301. doi:10.1038/ni.2744
18. Zhang N, Bevan MJ. Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity (2013) 39:687-96. doi:10.1016/j.immuni.2013.08.019
19. Ariotti S, Hogenbirk MA, Dijkgraaf FE, Visser LL, Hoekstra ME, Song JY, et al. T cell memory. Skin-resident memory CD8+ T cells trigger a state of tissue-wide pathogen alert. Science (2014) 346:101-5. doi:10.1126/science.1254803
20. Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res (2014) 20:434-44. doi:10.1158/1078-0432.CCR-13-1877
21. Djenidi F, Adam J, Goubar A, Durgeau A, Meurice G, de Montpréville V, et al. CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J Immunol (2015) 194:3475-86. doi:10.4049/jimmunol.1402711
22. Wang B, Wu S, Zeng H, Liu Z, Dong W, He W, et al. CD103+ tumor infiltrating lymphocytes predict a favorable prognosis in urothelial cell carcinoma of the bladder. J Urol (2015) 194:556-62. doi:10.1016/j.juro.2015.02.2941
23. Schuler P, Contassot E, Irla M, Hugues S, Preynat-Seauve O, Beermann F, et al. Direct presentation of a melanocyte-associated antigen in peripheral lymph nodes induces cytotoxic CD8+ T cells. Cancer Res (2008) 68:8410-8. doi:10.1158/0008-5472.CAN-08-0809
24. Baumgaertner P, Jandus C, Rivals JP, Derré L, Lövgren T, Baitsch L, et al. Vaccination-induced functional competence of circulating human tumor-specific CD8 T-cells. Int J Cancer (2012) 130:2607-17. doi:10.1002/ijc.26297
25. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol (2005) 5:546-59. doi:10.1038/nri1646
26. Mokrani M, Klibi J, Bluteau D, Bismuth G, Mami-Chouaib F. Smad and NFAT pathways cooperate to induce CD103 expression in human CD8 T lymphocytes. J Immunol (2014) 192:2471-9. doi:10.4049/jimmunol.1302192
27. Chan BM, Wong JG, Rao A, Hemler ME. T cell receptor-dependent, antigen-specific stimulation of a murine T cell clone induces a transient, VLA protein-mediated binding to extracellular matrix. J Immunol (1991) 147:398-404.
28. Wakim LM, Woodward-Davis A, Liu R, Hu Y, Villadangos J, Smyth G, et al. The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J Immunol (2012) 189:3267-8. doi:10.4049/jimmunol.1290055
29. Legat A, Speiser DE, Pircher H, Zehn D, Fuertes Marraco SA. Inhibitory receptor expression depends more dominantly on differentiation and activation than 'exhaustion' of human CD8 T cells. Front Immunol (2013) 4:455. doi:10.3389/fimmu.2013.00455
30. Salerno EP, Olson WC, McSkimming C, Shea S, Slingluff CL. T cells in the human metastatic melanoma microenvironment express site-specific homing receptors and retention integrins. Int J Cancer (2014) 134:563-74. doi:10.1002/ijc.28391
31. Sandoval F, Terme M, Nizard M, Badoual C, Bureau MF, Freyburger L, et al. Mucosal imprinting of vaccine-induced CD8+ T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med (2013) 5:172ra20. doi:10.1126/scitranslmed.3004888
32. Hemler ME. VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annu Rev Immunol (1990) 8:365-400. doi:10.1146/annurev.iy.08.040190.002053
33. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the [alpha]E[beta]7 integrin. Nature (1994) 372:190-3. doi:10.1038/372190a0
34. Ray SJ, Franki SN, Pierce RH, Dimitrova S, Koteliansky V, Sprague AG, et al. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity (2004) 20:167-79. doi:10.1016/S1074-7613(04)00021-4
35. Franciszkiewicz K, Le Floc'h A, Jalil A, Vigant F, Robert T, Vergnon I, et al. Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention. Cancer Res (2009) 69:6249-55. doi:10.1158/0008-5472.CAN-08-3571
36. Franciszkiewicz K, Le Floc'h A, Boutet M, Vergnon I, Schmitt A, Mami-Chouaib F. CD103 or LFA-1 engagement at the immune synapse between cytotoxic T cells and tumor cells promotes maturation and regulates T-cell effector functions. Cancer Res (2013) 73:617-28. doi:10.1158/0008-5472.CAN-12-2569
37. Mackay LK, Wynne-Jones E, Freestone D, Pellicci DG, Mielke LA, Newman DM, et al. T-box transcription factors combine with the cytokines TGF-β and IL-15 to control tissue-resident memory T cell fate. Immunity (2015) 43:1101-11. doi:10.1016/j.immuni.2015.11.008
38. Wakim LM, Woodward-Davis A, Bevan MJ. Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci U S A (2010) 107:17872-9. doi:10.1073/pnas.1010201107
39. Kim SK, Reed DS, Heath WR, Carbone F, Lefrançois L. Activation and migration of CD8 T cells in the intestinal mucosa. J Immunol (1997) 159:4295-306.
40. Schenkel JM, Fraser KA, Vezys V, Masopust D. Sensing and alarm function of resident memory CD8 T cells. Nat Immunol (2013) 14:509-13. doi:10.1038/ni.2568
41. Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, et al. Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol (2012) 188:4866-75. doi:10.4049/jimmunol.1200402
42. Massagué J. TGFβ signalling in context. Nat Rev Mol Cell Biol (2012) 13:616-30. doi:10.1038/nrm3434
43. Sanjabi S, Mosaheb MM, Flavell RA. Opposing effects of TGF-beta and IL-15 cytokines control the number of short-lived effector CD8+ T cells. Immunity (2009) 31:131-44. doi:10.1016/j.immuni.2009.04.020
44. Ma C, Zhang N. Transforming growth factor-β signaling is constantly shaping memory T-cell population. Proc Natl Acad Sci U S A (2015) 112:11013-7. doi:10.1073/pnas.1510119112
45. Ishigame H, Mosaheb MM, Sanjabi S, Flavell RA. Truncated form of TGF-βRII, but not its absence, induces memory CD8+ T cell expansion and lymphoproliferative disorder in mice. J Immunol (2013) 190:6340-50. doi:10.4049/jimmunol.1300397
46. Webb JR, Milne K, Nelson BH. PD-1 and CD103 are widely coexpressed on prognostically favorable intraepithelial CD8 T cells in human ovarian cancer. Cancer Immunol Res (2015) 3:926-35. doi:10.1158/2326-6066.CIR-14-0239