Maximal T cell-mediated antitumor responses rely upon CCR5 expression in both CD4+ and CD8+ T cells

Cancer Research

Volumn 71, Issue 16, 2011, Pages 5455-5466

  González Martín, Alicia ^a   Gómez, Lucio ^a   Lustgarten, Joseph ^b   Mira, Emilia ^a   Mañes, Santos ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR5; GAMMA INTERFERON; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; RANTES; TOLL LIKE RECEPTOR 9; TUMOR ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CPG ISLAND; CYTOTOXIC T LYMPHOCYTE; FIBROSARCOMA; HELPER CELL; IMMUNE RESPONSE; IMMUNOCOMPETENCE; LEWIS CARCINOMA; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; THYMOMA; TUMOR IMMUNITY; TUMOR REJECTION; UPREGULATION;

EID: 80051703591     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1687     Document Type: Article

References (50)

1. Dougan M, Dranoff G. Immune therapy for cancer. Annu Rev Immunol 2009;27:83-117.
2. Murphy A, Westwood JA, Teng MW, Moeller M, Darcy PK, Kershaw MH. Gene modification strategies to induce tumor immunity. Immunity 2005;22:403-14. (Pubitemid 40545107)
3. Rosenberg SA, Dudley ME, Restifo NP. Cancer immunotherapy. N Engl J Med 2008;359:1072.
4. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
5. Viola A, Luster AD. Chemokines and their receptors: drug targets in immunity and inflammation. Annu Rev Pharmacol Toxicol 2008;48:171-97. (Pubitemid 351756361)
6. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 2006;440:890-5.
7. Nesbeth YC, Martinez DG, Toraya S, Scarlett UK, Cubillos-Ruiz JR, Rutkowski MR, et al. CD4+ T cells elicit host immune responses to MHC class II- ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells. J Immunol 2010;184:5654-62.
8. Contento RL, Molon B, Boularan C, Pozzan T, Manes S, Marullo S, et al. CXCR4-CCR5: a couple modulating T cell functions. Proc Natl Acad Sci U S A 2008;105:10101-6.
9. Molon B, Gri G, Bettella M, Gomez-Mouton C, Lanzavecchia A, Martinez-A C, et al. T cell costimulation by chemokine receptors. Nat Immunol 2005;6:465-71. (Pubitemid 41716759)
10. Camargo JF, Quinones MP, Mummidi S, Srinivas S, Gaitan AA, Begum K, et al. CCR5 expression levels influence NFAT translocation, IL-2 production, and subsequent signaling events during T lymphocyte activation. J Immunol 2009;182:171-82.
11. Dolan MJ, Kulkarni H, Camargo JF, He W, Smith A, Anaya JM, et al. CCL3L1 and CCR5 influence cell-mediated immunity and affect HIV-AIDS pathogenesis via viral entry-independent mechanisms. Nat Immunol 2007;8:1324-36. (Pubitemid 350131170)
12. Lim JK, McDermott DH, Lisco A, Foster GA, Krysztof D, Follmann D, et al. CCR5 deficiency is a risk factor for early clinical manifestations of West Nile virus infection but not for viral transmission. J Infect Dis 2010;201:178-85.
13. Luboshits G, Shina S, Kaplan O, Engelberg S, Nass D, Lifshitz-Mercer B, et al. Elevated expression of the CC chemokine regulated on activation, normal T cell expressed and secreted (RANTES) in advanced breast carcinoma. Cancer Res 1999;59:4681-7. (Pubitemid 29428976)
14. Mira E, Lacalle RA, Gonzalez MA, Gomez-Mouton C, Abad JL, Bernad A, et al. A role for chemokine receptor transactivation in growth factor signaling. EMBO Rep 2001;2:151-6. (Pubitemid 32229743)
15. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007;449:557-63. (Pubitemid 47525152)
16. Kallikourdis M, Andersen KG, Welch KA, Betz AG. Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc Natl Acad Sci U S A 2007;104:594-9. (Pubitemid 46123070)
17. Mellado M, de Ana AM, Moreno MC, Martinez-A. C, Rodriguez-Frade JM. A potential immune escape mechanism by melanoma cells through the activation of chemokine-induced T cell death. Curr Biol 2001;11:691-6. (Pubitemid 32418165)
18. Wu Y, Li YY, Matsushima K, Baba T, Mukaida N. CCL3-CCR5 axis regulates intratumoral accumulation of leukocytes and fibroblasts and promotes angiogenesis in murine lung metastasis process. J Immunol 2008;181:6384-93.
19. Robinson SC, Scott KA, Wilson JL, Thompson RG, Proudfoot AE, Balkwill FR. A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res 2003;63:8360-5. (Pubitemid 37549490)
20. Uekusa Y, Yu WG, Mukai T, Gao P, Yamaguchi N, Murai M, et al. A pivotal role for CC chemokine receptor 5 in T-cell migration to tumor sites induced by interleukin 12 treatment in tumor-bearing mice. Cancer Res 2002;62:3751-8. (Pubitemid 34728857)
21. Gough M, Crittenden M, Thanarajasingam U, Sanchez-Perez L, Thompson J, Jevremovic D, et al. Gene therapy to manipulate effector T cell trafficking to tumors for immunotherapy. J Immunol 2005;174:5766-73. (Pubitemid 40593220)
22. Iida N, Nakamoto Y, Baba T, Nakagawa H, Mizukoshi E, Naito M, et al. Antitumor effect after radiofrequency ablation of murine hepatoma is augmented by an active variant of CC Chemokine ligand 3/macrophage inflammatory protein-1alpha. Cancer Res 2010;70:6556-65.
23. Liu C, Lou Y, Lizee G, Qin H, Liu S, Rabinovich B, et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J Clin Invest 2008;118:1165-75. (Pubitemid 351364623)
24. Weiss JM, Back TC, Scarzello AJ, Subleski JJ, Hall VL, Stauffer JK, et al. Successful immunotherapy with IL-2/anti-CD40 induces the chemokine-mediated mitigation of an immunosuppressive tumor microenvironment. Proc Natl Acad Sci U S A 2009;106:19455-60.
25. Nakazaki Y, Hase H, Inoue H, Beppu Y, Meng XK, Sakaguchi G, et al. Serial analysis of gene expression in progressing and regressing mouse tumors implicates the involvement of RANTES and TARC in antitumor immune responses. Mol Ther 2006;14:599-606. (Pubitemid 44296094)
26. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13. (Pubitemid 36077915)
27. Zimmermann T, Moehler M, Gockel I, Sgourakis GG, Biesterfeld S, Muller M, et al. Low expression of chemokine receptor CCR5 in human colorectal cancer correlates with lymphatic dissemination and reduced CD8+ T-cell infiltration. Int J Colorectal Dis 2010;25:417-24.
28. Mañes S, Mira E, Colomer R, Montero S, Real LM, Gómez-Moutón C, et al. CCR5 expression influences the progression of human breast cancer in a p53-dependent manner. J Exp Med 2003;198:1381-9. (Pubitemid 37392483)
29. Ugurel S, Schrama D, Keller G, Schadendorf D, Brocker EB, Houben R, et al. Impact of the CCR5 gene polymorphism on the survival of metastatic melanoma patients receiving immunotherapy. Cancer Immunol Immunother 2008;57:685-91. (Pubitemid 351641030)
30. Nanni P, Pupa SM, Nicoletti G, De Giovanni C, Landuzzi L, Rossi I, et al. p185(neu) protein is required for tumor and anchorage-independent growth, not for cell proliferation of transgenic mammary carcinoma. Int J Cancer 2000;87:186-94. (Pubitemid 30434343)
31. Hugues S, Scholer A, Boissonnas A, Nussbaum A, Combadiere C, Amigorena S, et al. Dynamic imaging of chemokine-dependent CD8+ T cell help for CD8+ T cell responses. Nat Immunol 2007;8:921-30. (Pubitemid 47300006)
32. Marzo AL, Lake RA, Robinson BW, Scott B. T-cell receptor transgenic analysis of tumor-specific CD8 and CD4 responses in the eradication of solid tumors. Cancer Res 1999;59:1071-9. (Pubitemid 29135968)
33. Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med 2007;204:345-56. (Pubitemid 46294550)
34. Melief CJ. Cancer immunotherapy by dendritic cells. Immunity 2008;29:372-83.
35. Dal Secco V, Soldani C, Debrat C, Asperti-Boursin F, Donnadieu E, Viola A, et al. Tunable chemokine production by antigen presenting dendritic cells in response to changes in regulatory T cell frequency in mouse reactive lymph nodes. PLoS One 2009;4:e7696.
36. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011;29:235-71.
37. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci U S A 1992;89:10578-82.
38. Houghton AN, Guevara-Patiño JA. Immune recognition of self in immunity against cancer. J Clin Invest 2004;114:468-71. (Pubitemid 39572095)
39. Feuerer M, Beckhove P, Bai L, Solomayer EF, Bastert G, Diel IJ, et al. Therapy of human tumors in NOD/SCID mice with patient-derived reactivated memory T cells from bone marrow. Nat Med 2001;7:452-8. (Pubitemid 32298548)
40. Lustgarten J, Dominguez AL, Cuadros C. The CD8+ T cell repertoire against Her-2/neu antigens in neu transgenic mice is of low avidity with antitumor activity. Eur J Immunol 2004;34:752-61. (Pubitemid 39255923)
41. Sharma S, Dominguez AL, Hoelzinger DB, Lustgarten J. CpG-ODN but not other TLR-ligands restore the antitumor responses in old mice: the implications for vaccinations in the aged. Cancer Immunol Immunother 2008;57:549-61. (Pubitemid 351170538)
42. Lapteva N, Huang XF. CCL5 as an adjuvant for cancer immunotherapy. Expert Opin Biol Ther 2010;10:725-33.
43. Braunersreuther V, Zernecke A, Arnaud C, Liehn EA, Steffens S, Shagdarsuren E, et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2007;27:373-9. (Pubitemid 46143054)
44. Eis V, Luckow B, Vielhauer V, Siveke JT, Linde Y, Segerer S, et al. Chemokine receptor CCR1 but not CCR5 mediates leukocyte recruitment and subsequent renal fibrosis after unilateral ureteral obstruction. J Am Soc Nephrol 2004;15:337-47. (Pubitemid 38140774)
45. Weber C, Weber KS, Klier C, Gu S, Wank R, Horuk R, et al. Specialized roles of the chemokine receptors CCR1 and CCR5 in the recruitment of monocytes and T(H)1-like/CD45RO(+) T cells. Blood 2001;97:1144-6. (Pubitemid 32154307)
46. Beuneu H, Garcia Z, Bousso P. Cutting edge: cognate CD4 help promotes recruitment of antigen-specific CD8 T cells around dendritic cells. J Immunol 2006;177:1406-10. (Pubitemid 44092471)
47. Schubert LA, King G, Cron RQ, Lewis DB, Aruffo A, Hollenbaugh D. The human gp39 promoter. Two distinct nuclear factors of activated T cell protein-binding elements contribute independently to transcriptional activation. J Biol Chem 1995;270:29624-7. (Pubitemid 26002152)
48. Conforti R, Ma Y, Morel Y, Paturel C, Terme M, Viaud S, et al. Opposing effects of toll-like receptor (TLR3) signaling in tumors can be therapeutically uncoupled to optimize the anticancer efficacy of TLR3 ligands. Cancer Res 2010;70:490-500.
49. Ogawa S, Lozach J, Benner C, Pascual G, Tangirala RK, Westin S, et al. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 2005;122:707-21. (Pubitemid 41242636)
50. Ruiperez V, Astudillo AM, Balboa MA, Balsinde J. Coordinate regulation of TLR-mediated arachidonic acid mobilization in macrophages by group IVA and group V phospholipase A2s. J Immunol 2009;182:3877-83.