Blocking tumor necrosis factor α enhances CD8 T-cell-dependent immunity in experimental melanoma

Cancer Research

Volumn 75, Issue 13, 2015, Pages 2619-2628

  Bertrand, Florie ^a,b   Rochotte, Julia ^a,b,c   Colacios, Céline ^a,b,c   Montfort, Anne ^a,b,e   Tilkin Mariamé, Anne Francoise ^a   Touriol, Christian ^a   Rochaix, Philippe ^d   Lajoie Mazenc, Isabelle ^a,c   Andrieu Abadie, Nathalie ^a,b   Levade, Thierry ^a,b,c   Benoist, Hervé ^a,b,c   Ségui, Bruno ^a,b,c  

^a CANCER RESEARCH CENTER OF TOULOUSE   (France)

^b Equipe 'Labellisée LA LIGUE CONTRE LE CANCER 2013'   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d INSTITUT CLAUDIUS REGAUD   (France)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ETANERCEPT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CD8+ T LYMPHOCYTE; CELL DEATH; CELL DENSITY; CELL GROWTH; CELL INFILTRATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; EXPERIMENTAL MELANOMA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR ESCAPE; VENULE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DEFICIENCY; IMMUNOLOGY; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; TUMOR ESCAPE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84942693817     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2524     Document Type: Article

References (50)

1. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci U S A 1975;72:3666-70.
2. Balkwill F. Tumour necrosis factor and cancer. Nat Rev Cancer 2009;9:361-71.
3. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
4. Moore RJ, Owens DM, Stamp G, Arnott C, Burke F, East N, et al. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med 1999;5:828-31.
5. Suganuma M, Okabe S, Marino MW, Sakai A, Sueoka E, Fujiki H. Essential role of tumor necrosis factor alpha (TNF-alpha) in tumor promotion as revealed by TNF-alpha-deficient mice. Cancer Res 1999;59:4516-8.
6. Arnott CH, Scott KA, Moore RJ, Robinson SC, Thompson RG, Balkwill FR. Expression of both TNF-alpha receptor subtypes is essential for optimal skin tumour development. Oncogene 2004;23:1902-10.
7. Hong DS, Vence L, Falchook G, Radvanyi LG, Liu C, Goodman V, et al. BRAF(V600) inhibitor GSK2118436 targeted inhibition of mutant BRAF in cancer patients does not impair overall immune competency. Clin Cancer Res 2012;18:2326-35.
8. Wilmott JS, Haydu LE, Menzies AM, Lum T, Hyman J, Thompson JF, et al. Dynamics of chemokine, cytokine, and growth factor serum levels in BRAF-mutant melanoma patients during BRAF inhibitor treatment. J Immunol 2014;192:2505-13.
9. Menon DR, Wels C, Bonyadi Rad E, Joshi S, Knausz H, Lade-Keller J, et al. TGF-beta1 and TNF-alpha differentially regulate Twist1 mediated resistance towards BRAF/MEK inhibition in melanoma. Pigment Cell Melanoma Res 2013;26:912-6.
10. Li B, Vincent A, Cates J, Brantley-Sieders DM, Polk DB, Young PP. Low levels of tumor necrosis factor alpha increase tumor growth by inducing an endothelial phenotype of monocytes recruited to the tumor site. Cancer Res 2009;69:338-48.
11. Ardestani S, Li B, Deskins DL, Wu H, Massion PP, Young PP. Membrane versus soluble isoforms of TNF-alpha exert opposing effects on tumor growth and survival of tumor-associated myeloid cells. Cancer Res 2013;73:3938-50.
12. Sasi SP, Yan X, Enderling H, Park D, Gilbert HY, Curry C, et al. Breaking the 'harmony' of TNF-alpha signaling for cancer treatment. Oncogene 2012;31:4117-27.
13. Chopra M, Riedel SS, Biehl M, Krieger S, von Krosigk V, Bauerlein CA, et al. Tumor necrosis factor receptor 2-dependent homeostasis of regulatory T cells as a player in TNF-induced experimental metastasis. Carcinogenesis 2013;34:1296-303.
14. Waterston AM, Salway F, Andreakos E, Butler DM, Feldmann M, Coombes RC. TNF autovaccination induces self anti-TNF antibodies and inhibits metastasis in a murine melanoma model. Br J Cancer 2004;90:1279-84.
15. Cubillos S, Scallon B, Feldmann M, Taylor P. Effect of blocking TNF on IL-6 levels and metastasis in a B16-BL6 melanoma/mouse model. Anticancer Res 1997;17:2207-11.
16. Smith MP, Sanchez-Laorden B, O'Brien K, Brunton H, Ferguson J, Young H, et al. The immune microenvironment confers resistance to MAPK pathway inhibitors through macrophage-derived TNFalpha. Cancer Discov 2014; 4:1214-29.
17. Moulis G, Sommet A, Bene J, Montastruc F, Sailler L, Montastruc JL, et al. Cancer risk of anti-TNF-alpha at recommended doses in adult rheumatoid arthritis: a meta-analysis with intention to treat and per protocol analyses. PLoS One 2012;7:e48991.
18. Mercer LK, Lunt M, Low AL, Dixon WG, Watson KD, Symmons DP, et al. Risk of solid cancer in patients exposed to anti-tumour necrosis factor therapy: results from the British Society for Rheumatology Biologics Register for Rheumatoid Arthritis. Ann Rheum Dis 2015; 74:1087-93.
19. Askling J, Fahrbach K, Nordstrom B, Ross S, Schmid CH, Symmons D. Cancer risk with tumor necrosis factor alpha (TNF) inhibitors: meta-analysis of randomized controlled trials of adalimumab, etanercept, and infliximab using patient level data. Pharmacoepidemiol Drug Saf 2011;20:119-30.
20. Leombruno JP, Einarson TR, Keystone EC. The safety of anti-tumour necrosis factor treatments in rheumatoid arthritis: meta and exposure-adjusted pooled analyses of serious adverse events. Ann Rheum Dis 2009;68: 1136-45.
21. Ratner A, Clark WR. Role of TNF-alpha in CD8+ cytotoxic T lymphocyte-mediated lysis. J Immunol 1993;150:4303-14.
22. Kim EY, Teh HS. TNF type 2 receptor (p75) lowers the threshold of T cell activation. J Immunol 2001;167:6812-20.
23. Chatzidakis I, Fousteri G, Tsoukatou D, Kollias G, Mamalaki C. Anessential role for TNF in modulating thresholds for survival, activation, and tolerance of CD8+ T cells. J Immunol 2007;178:6735-45.
24. Braumuller H, Wieder T, Brenner E, Assmann S, Hahn M, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013; 494:361-5.
25. Ding X, Yang W, Shi X, Du P, Su L, Qin Z, et al. TNF receptor 1 mediates dendritic cell maturation and CD8 T cell response through two distinct mechanisms. J Immunol 2011;187:1184-91.
26. Calzascia T, Pellegrini M, Hall H, Sabbagh L, Ono N, Elford AR, et al. TNF-alpha is critical for antitumor but not antiviral T cell immunity in mice. J Clin Invest 2007;117:3833-45.
27. Zheng L, Fisher G, Miller RE, Peschon J, Lynch DH, Lenardo MJ. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 1995;377:348-51.
28. Okubo Y, Mera T, Wang L, Faustman DL. Homogeneous expansion of human T-regulatory cells via tumor necrosis factor receptor 2. Sci Rep 2013;3:3153.
29. Schioppa T, Moore R, Thompson RG, Rosser EC, Kulbe H, Nedospasov S, et al. B regulatory cells and the tumor-promoting actions of TNF-alpha during squamous carcinogenesis. Proc Natl Acad Sci U S A 2011;108: 10662-7.
30. Zhao X, Rong L, Li X, Liu X, Deng J, Wu H, et al. TNF signaling drives myeloid-derived suppressor cell accumulation. J Clin Invest 2012; 122:4094-104.
31. Sade-Feldman M, Kanterman J, Ish-Shalom E, Elnekave M, Horwitz E, Baniyash M. Tumor necrosis factor-alpha blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 2013;38:541-54.
32. Landsberg J, Kohlmeyer J, Renn M, Bald T, Rogava M, Cron M, et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 2012;490:412-6.
33. Porgador A, Feldman M, Eisenbach L. H-2Kb transfection of B16 melanoma cells results inreducedtumourigenicity and metastatic competence. J Immunogenet 1989;16:291-303.
34. Pequeux C, Raymond-Letron I, Blacher S, Boudou F, Adlanmerini M, Fouque MJ, et al. Stromal estrogen receptor-alpha promotes tumor growth by normalizing an increased angiogenesis. Cancer Res 2012;72:3010-9.
35. Pencheva N, Buss CG, Posada J, Merghoub T, Tavazoie SF. Broad-spectrum therapeutic suppression of metastatic melanoma through nuclear hormone receptor activation. Cell 2014;156:986-1001.
36. Martinet L, Le Guellec S, Filleron T, Lamant L, Meyer N, Rochaix P, et al. High endothelial venules (HEVs) in human melanoma lesions: major gateways for tumor-infiltrating lymphocytes. Oncoimmunology 2012;1: 829-39.
37. Avram G, Sanchez-Sendra B, Martin JM, Terradez L, Ramos D, Monteagudo C. The density and type of MECA-79-positive high endothelial venules correlate with lymphocytic infiltration and tumour regression in primary cutaneous melanoma. Histopathology 2013;63:852-61.
38. Cipponi A, Mercier M, Seremet T, Baurain JF, Theate I, van den Oord J, et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res 2012;72:3997-4007.
39. Schrama D, Voigt H, Eggert AO, Xiang R, Zhou H, Schumacher TN, et al. Immunological tumor destruction in a murine melanoma model by targeted LTalpha independent of secondary lymphoid tissue. Cancer Immunol Immunother 2008;57:85-95.
40. Popivanova BK, Kitamura K, Wu Y, Kondo T, Kagaya T, Kaneko S, et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008;118:560-70.
41. Chen X, Baumel M, Mannel DN, Howard OM, Oppenheim JJ. Interaction of TNF with TNF receptor type 2 promotes expansion and function of mouse CD4+CD25+ T regulatory cells. J Immunol 2007;179:154-61.
42. Youn JI, Collazo M, Shalova IN, Biswas SK, Gabrilovich DI. Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J Leukoc Biol 2012;91:167-81.
43. Hu X, Li B, Li X, Zhao X, Wan L, Lin G, et al. Transmembrane TNF-alpha promotes suppressive activities of myeloid-derived suppressor cells via TNFR2. J Immunol 2014;192:1320-31.
44. Meyer C, Sevko A, Ramacher M, Bazhin AV, Falk CS, Osen W, et al. Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model. Proc Natl Acad Sci U S A 2011;108:17111-6.
45. Moussion C, Girard JP. Dendritic cells control lymphocyte entry to lymph nodes through high endothelial venules. Nature 2011;479:542-6.
46. Hohmann HP, Remy R, Poschl B, van Loon AP. Tumor necrosis factors-alpha and -beta bind to the same two types of tumor necrosis factor receptors and maximally activate the transcription factor NF-kappa Bat low receptor occupancy and within minutes after receptor binding. J Biol Chem 1990;265:15183-8.
47. Sevko A, Michels T, Vrohlings M, Umansky L, Beckhove P, Kato M, et al. Antitumor effect of paclitaxel is mediated by inhibition of myeloid-derived suppressor cells and chronic inflammation in the spontaneous melanoma model. J Immunol 2013;190:2464-71.
48. Brown ER, Charles KA, Hoare SA, Rye RL, Jodrell DI, Aird RE, et al. A clinical study assessing the tolerability and biological effects of infliximab, a TNF-alpha inhibitor, in patients with advanced cancer. Ann Oncol 2008;19: 1340-6.
49. Turcotte S, Gros A, Hogan K, Tran E, Hinrichs CS, Wunderlich JR, et al. Phenotype and function of T cells infiltrating visceral metastases from gastrointestinal cancers and melanoma: implications for adoptive cell transfer therapy. J Immunol 2013;191:2217-25.
50. Yuan J, Gnjatic S, Li H, Powel S, Gallardo HF, Ritter E, et al. CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit. Proc Natl Acad Sci U S A 2008;105:20410-5.