Long-term survival and clinical benefit from adoptive T-cell transfer in stage IV melanoma patients is determined by a four-parameter tumor immune signature

Cancer Immunology Research

Volumn 5, Issue 2, 2017, Pages 170-179

  Melief, Sara M ^a   Visconti, Valeria V ^a   Visser, Marten ^a   Van Diepen, Merel ^a   Kapiteijn, Ellen H W ^a   Van Den Berg, Joost H ^b   Haanen, John B A G ^b   Smit, Vincent T H B M ^a   Oosting, Jan ^a   Van Der Burg, Sjoerd H ^a   Verdegaal, Els M E ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ECALECTIN; GALECTIN 1; GALECTIN 3; BIOLOGICAL MARKER; GALECTIN;

ADOPTIVE TRANSFER; ADULT; AGED; ARTICLE; BONE MARROW CELL; CANCER PATIENT; CANCER STAGING; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HUMAN; HUMAN TISSUE; LONG TERM SURVIVAL; LYMPHOCYTE COUNT; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; METASTATIC MELANOMA; PROTEIN EXPRESSION; T LYMPHOCYTE; TREATMENT RESPONSE; TUMOR CELL; ADOPTIVE IMMUNOTHERAPY; IMMUNITY; IMMUNOLOGY; MELANOMA; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS; T LYMPHOCYTE SUBPOPULATION; TREATMENT OUTCOME;

ADULT; AGED; BIOMARKERS; FEMALE; GALECTINS; HUMANS; IMMUNITY; IMMUNOTHERAPY, ADOPTIVE; MACROPHAGES; MALE; MELANOMA; MIDDLE AGED; NEOPLASM STAGING; PROGNOSIS; SURVIVAL ANALYSIS; T-LYMPHOCYTE SUBSETS; TREATMENT OUTCOME;

EID: 85016131548     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-16-0288     Document Type: Article

References (40)

1. Rosenberg SA, Yannelli JR, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS, et al. Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J Natl Cancer Inst 1994;86:1159-66.
2. 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.
3. Kalialis LV, Drzewiecki KT, Klyver H. Spontaneous regression ofmetastases from melanoma: review of the literature. Melanoma Res 2009;19:275-82.
4. Erdag G, Schaefer JT, Smolkin ME, Deacon DH, Shea SM, Dengel LT, et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res 2012;72:1070-80.
5. Akbani R, Akdemir Kadir C, Aksoy BA, Albert M, Ally A, Amin Samirkumar B, et al. Genomic classification of cutaneous melanoma. Cell 2015; 161:1681-96.
6. Ladanyi A. Prognostic and predictive significance of immune cells infiltrating cutaneous melanoma. Pigment Cell Melanoma Res 2015;28: 490-500.
7. Kluger HM, Zito CR, Barr ML, Baine MK, Chiang VLS, Sznol M, et al. Characterization of PD-L1 expression and associated T-cell infiltrates in metastatic melanoma samples from variable anatomic sites. Clin Cancer Res 2015;21:3052-60.
8. Emri E, Egervari K, Varvolgyi T, Rozsa D, Miko E, Dezso B, et al. Correlation among metallothionein expression, intratumoural macrophage infiltration and the risk of metastasis in human cutaneous malignant melanoma. J Eur Acad Dermatol Venereol 2013;27:e320-7.
9. Jensen TO, Schmidt H, Moller HJ, Hoyer M, Maniecki MB, Sjoegren P, et al. Macrophage markers in serum and tumor have prognostic impact in American Joint Committee on Cancer stage I/II melanoma. J Clin Oncol 2009;27:3330-7.
10. Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, et al. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 2012;61:1019-31.
11. Tjin EP, Krebbers G, Meijlink KJ, van de Kasteele W, Rosenberg EH, Sanders J, et al. Immune-escapemarkers in relation to clinical outcome of advanced melanoma patients following immunotherapy. Cancer Immunol Res 2014;2:538-46.
12. Brown ER, Doig T, Anderson N, Brenn T, Doherty V, Xu Y, et al. Association of galectin-3 expression with melanoma progression and prognosis. Eur J Cancer 2012;48:865-74.
13. 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.
14. Gajewski T, Zha Y, Thurner B, Schuler G. Association of gene expression profile in metastatic melanoma and survival to a dendritic cell-based vaccine. J Clin Oncol 2009;27.
15. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014;515:568-71.
16. Romano E, Kusio-Kobialka M, Foukas PG, Baumgaertner P, Meyer C, Ballabeni P, et al. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc Natl Acad Sci 2015;112:6140-5.
17. Zikich D, Schachter J, Besser MJ. Predictors of tumor-infiltrating lymphocyte efficacy in melanoma. Immunotherapy 2016;8:35-43.
18. Balch CM, Gershenwald JE, Soong S-j, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199-206.
19. van Esch EM, van Poelgeest MI, Kouwenberg S, Osse EM, Trimbos JB, Fleuren GJ, et al. Expression of coinhibitory receptors on T cells in the microenvironment of usual vulvar intraepithelial neoplasia is related to proinflammatory effector T cells and an increased recurrence-free survival. Int J Cancer 2015;136:E95-106.
20. van Esch EM, van Poelgeest MI, Trimbos JB, Fleuren GJ, Jordanova ES, van der Burg SH. Intraepithelial macrophage infiltration is related to a high number of regulatory T cells and promotes a progressive course of HPVinduced vulvar neoplasia. Int J Cancer 2015;136:E85-94.
21. Specht E, Kaemmerer D, Sanger J, Wirtz RM, Schulz S, Lupp A. Comparison of immunoreactive score, HER2/neu score and H score for the immunohistochemical evaluation of somatostatin receptors in bronchopulmonary neuroendocrine neoplasms. Histopathology 2015;67:368-77.
22. Verdegaal EM, Visser M, Ramwadhdoebe TH, van der Minne CE, van Steijn JA, Kapiteijn E, et al. Successful treatment of metastatic melanoma by adoptive transfer of blood-derived polyclonal tumor-specific CD4+ and CD8+ T cells in combination with low-dose interferon-alpha. Cancer Immunol Immunother 2011;60:953-63.
23. Donia M, Larsen SM, Met O, Svane IM. Simplified protocol for clinicalgrade tumor-infiltrating lymphocyte manufacturing with use of the Wave bioreactor. Cytotherapy 2014;16:1117-20.
24. Sullivan BM, Juedes A, Szabo SJ, von Herrath M, Glimcher LH. Antigendriven effector CD8 T cell function regulated by T-bet. Proc Natl Acad Sci U S A 2003;100:15818-23.
25. Gieseke F, Kruchen A, Tzaribachev N, Bentzien F, Dominici M, Muller I. Proinflammatory stimuli induce galectin-9 in human mesenchymal stromal cells to suppress T-cell proliferation. Eur J Immunol 2013;43:2741-9.
26. Korn EL, Liu PY, Lee SJ, Chapman JA, Niedzwiecki D, Suman VJ, et al. Metaanalysis of phase II cooperative group trials in metastatic stage IV melanoma to determine progression-free and overall survival benchmarks for future phase II trials. J Clin Oncol 2008;26:527-34.
27. Imaizumi T, Kumagai M, Sasaki N, Kurotaki H, Mori F, Seki M, et al. Interferon-gamma stimulates the expression of galectin-9 in cultured human endothelial cells. J Leukoc Biol 2002;72:486-91.
28. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013;38:729-41.
29. Nobumoto A, Oomizu S, Arikawa T, Katoh S, Nagahara K, Miyake M, et al. Galectin-9 expands unique macrophages exhibiting plasmacytoid dendritic cell-like phenotypes that activate NK cells in tumor-bearing mice. Clin Immunol 2009;130:322-30.
30. Nagahara K, Arikawa T, Oomizu S, Kontani K, Nobumoto A, Tateno H, et al. Galectin-9 increases Tim-3+ dendritic cells and CD8+ T cells and enhances antitumor immunity via galectin-9-Tim-3 interactions. J Immunol 2008;181:7660-9.
31. Ali TH, Pisanti S, Ciaglia E, Mortarini R, Anichini A, Garofalo C, et al. Enrichment of CD56(dim)KIR + CD57 + highly cytotoxic NK cells in tumour-infiltrated lymph nodes of melanoma patients. Nat Commun 2014;5:5639.
32. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012;4:127ra37.
33. de Vos van Steenwijk PJ, Ramwadhdoebe TH, Goedemans R, Doorduijn EM, van Ham JJ, Gorter A, et al. Tumor-infiltrating CD14-positive myeloid cells and CD8-positive T-cells prolong survival in patients with cervical carcinoma. Int J Cancer 2013;133:2884-94.
34. Ohri CM, Shikotra A, Green RH, Waller DA, Bradding P. Macrophages within NSCLC tumour islets are predominantly of a cytotoxic M1 phenotype associated with extended survival. Eur Respir J 2009;33:118-26.
35. Braeuer RR, Shoshan E, Kamiya T, Bar-Eli M. The sweet and bitter sides of galectins in melanoma progression. Pigment Cell Melanoma Res 2012;25: 592-601.
36. Demotte N, Wieers G, Van Der Smissen P, Moser M, Schmidt C, Thielemans K, et al. A galectin-3 ligand corrects the impaired function of human CD4 and CD8 tumor-infiltrating lymphocytes and favors tumor rejection in mice. Cancer Res 2010;70:7476-88.
37. Kouo T, Huang L, Pucsek AB, Cao M, Solt S, Armstrong T, et al. Galectin-3 shapes antitumor immune responses by suppressing CD8+T cells via LAG- 3 and inhibiting expansion of plasmacytoid dendritic cells. Cancer Immunol Res 2015;3:412-23.
38. Zubieta MR, Furman D, Barrio M, Bravo AI, Domenichini E, Mordoh J. Galectin-3 expression correlates with apoptosis of tumor-associated lymphocytes in human melanoma biopsies. Am J Pathol 2006;168:1666-75.
39. Chen HY, Fermin A, Vardhana S, Weng IC, Lo KF, Chang EY, et al. Galectin- 3 negatively regulates TCR-mediated CD4+ T-cell activation at the immunological synapse. Proc Natl Acad Sci U S A 2009;106:14496-501.
40. Borges BE, Teixeira VR, Appel MH, Steclan CA, Rigo F, Filipak Neto F, et al. De novo galectin-3 expression influences the response of melanoma cells to isatin-Schiff base copper (II) complex-induced oxidative stimulus. Chem Biol Interact 2013;206:37-46.