CCR5 as a potential target in cancer therapy: Inhibition or stimulation?

Anti-Cancer Agents in Medicinal Chemistry

Volumn 12, Issue 9, 2012, Pages 1045-1057

  González Martín, Alicia ^a   Mira, Emilia ^b   Mañes, Santos ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

CCR5; Chemokines; Crosspriming; Immune Response; Immunotherapy; Inflammation; Maraviroc; Tumor microenvironment

Indexed keywords

4 [(4 BROMOPHENYL) (ETHOXYIMINO) METHYL] 1' [(2, 4 DIMETHYL 3 PYRIDINYL) CARBONYL] 4' METHYL 1, 4' BIPIPERIDINE; 4 [(4 BROMOPHENYL)(ETHOXYIMINO)METHYL] 1' [(2,4 DIMETHYL 3 PYRIDINYL)CARBONYL] 4' METHYL 1,4' BIPIPERIDINE; APLAVIROC; B7 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; CENICRIVIROC; CHEMOKINE; CHEMOKINE RECEPTOR CCR5; G PROTEIN COUPLED RECEPTOR; GLYCOSAMINOGLYCAN; GSK873140; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MARAVIROC; MONOCYTE CHEMOTACTIC PROTEIN 2; N [4 [[[6, 7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL] CARBONYL] AMINO] BENZYL] N, N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; RANTES; UNCLASSIFIED DRUG; VICRIVIROC;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER THERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; DRUG TARGETING; EFFECTOR CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSURVEILLANCE; LIVER TOXICITY; LYMPHOCYTE ACTIVATION; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PROTEIN STRUCTURE; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; ANTINEOPLASTIC AGENTS; CHEMOKINES; HUMANS; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; NEOPLASMS; RECEPTORS, CCR5;

EID: 84872246692     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/187152012803529637     Document Type: Article

References (145)

1. Dougan, M.; Dranoff, G. Immune therapy for cancer. Annu. Rev. Immunol., 2009, 27, 83-117.
2. Murphy, A.; Westwood, J.A.; Teng, M.W.; Moeller, M.; Darcy, P.K.; Kershaw, M.H. Gene modification strategies to induce tumor immunity. Immunity, 2005, 22(4), 403-414.
3. Morgan, R.A.; Dudley, M.E.; Rosenberg, S.A. Adoptive cell therapy: genetic modification to redirect effector cell specificity. Cancer J., 2010, 16(4), 336-341.
4. Apetoh, L.; Ghiringhelli, F.; Tesniere, A.; Obeid, M.; Ortiz, C.; Criollo, A.; Mignot, G.; Maiuri, M.C.; Ullrich, E.; Saulnier, P.; Yang, H.; Amigorena, S.; Ryffel, B.; Barrat, F.J.; Saftig, P.; Levi, F.; Lidereau, R.; Nogues, C.; Mira, J.P.; Chompret, A.; Joulin, V.; Clavel-Chapelon, F.; Bourhis, J.; Andre, F.; Delaloge, S.; Tursz, T.; Kroemer, G.; Zitvogel, L. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med., 2007, 13(9), 1050-1059.
5. Iida, N.; Nakamoto, Y.; Baba, T.; Kakinoki, K.; Li, Y.Y.; Wu, Y.; Matsushima, K.; Kaneko, S.; Mukaida, N. Tumor cell apoptosis induces tumor-specific immunity in a CC chemokine receptor 1-and 5-dependent manner in mice. J. Leukoc. Biol., 2008, 84(4), 1001-1010.
6. Zitvogel, L.; Kroemer, G. Anticancer effects of imatinib via immunostimulation. Nat. Med., 2011, 17(9), 1050-1051.
7. Luster, A.D. Chemokines--chemotactic cytokines that mediate inflammation. N. Engl. J. Med., 1998, 338(7), 436-445.
8. Viola, A.; Contento, R.L.; Molon, B. T cells and their partners: The chemokine dating agency. Trends Immunol., 2006, 27(9), 421-427.
9. Mañes, S.; Gómez-Moutón, C.; Lacalle, R.A.; Jiménez-Baranda, S.; Mira, E.; Martinez A.C. Mastering time and space: immune cell polarization and chemotaxis. Semin. Immunol., 2005, 17(1), 77-86.
10. Molon, B.; Gri, G.; Bettella, M.; Gómez-Moutón, C.; Lanzavecchia, A.; Martinez A.C.; Mañes, S.; Viola, A. T cell costimulation by chemokine receptors. Nat. Immunol., 2005, 6(5), 465-471.
11. Contento, R.L.; Molon, B.; Boularan, C.; Pozzan, T.; Mañes, S.; Marullo, S.; Viola, A. CXCR4-CCR5: a couple modulating T cell functions. Proc. Natl. Acad. Sci. U.S.A., 2008, 105(29), 10101-10106.
12. Nesbeth, Y.C.; Martinez, D.G.; Toraya, S.; Scarlett, U.K.; Cubillos-Ruiz, J.R.; Rutkowski, M.R.; Conejo-Garcia, J.R. CD4+ T cells elicit host immune responses to MHC class II-negative ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells. J. Immunol., 2010, 184(10), 5654-5662.
13. González-Martín, A.; Gómez, L.; Lustgarten, J.; Mira, E.; Mañes, S. Maximal T cell-mediated antitumor responses rely upon CCR5 expression in both CD4(+) and CD8(+) T cells. Cancer Res., 2011, 71(16), 5455-5466.
14. Mira, E.; Lacalle, R.A.; Gonzalez, M.A.; Gomez-Mouton, C.; Abad, J.L.; Bernad, A.; Martinez A.C.; Mañes, S. A role for chemokine receptor transactivation in growth factor signaling. EMBO Rep., 2001, 2(2), 151-156.
15. Karnoub, A.E.; Dash, A.B.; Vo, A.P.; Sullivan, A.; Brooks, M.W.; Bell, G.W.; Richardson, A.L.; Polyak, K.; Tubo, R.; Weinberg, R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature, 2007, 449(7162), 557-563.
16. Wu, Y.; Li, Y.Y.; 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(9), 6384-6393.
17. Kast, R.E. Glioblastoma: synergy of growth promotion between CCL5 and NK-1R can be thwarted by blocking CCL5 with miraviroc, an FDA approved anti-HIV drug and blocking NK-1R with aprepitant, an FDA approved anti-nausea drug. J. Clin. Pharm. Ther., 2010, 35(6), 657-663.
18. Rossi, D.; Zlotnik, A. The biology of chemokines and their receptors. Annu. Rev. Immunol., 2000, 18, 217-242.
19. Bromley, S.K.; Mempel, T.R.; Luster, A.D. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat. Immunol., 2008, 9(9), 970-980.
20. Ransohoff, R.M. Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity, 2009, 31(5), 711-721.
21. Arya, M.; Patel, H.R.; Williamson, M. Chemokines: key players in cancer. Curr. Med. Res. Opin., 2003, 19(6), 557-564.
22. Balkwill, F. Chemokine biology in cancer. Semin. Immunol., 2003, 15(1), 49-55.
23. Mantovani, A. Chemokines in neoplastic progression. Semin. Cancer Biol., 2004, 14(3), 147-148.
24. Choi, W.T.; An, J. Biology and clinical relevance of chemokines and chemokine receptors CXCR4 and CCR5 in human diseases. Exp. Biol. Med. (Maywood), 2011, 236(6), 637-647.
25. Deng, H.; Liu, R.; Ellmeier, W.; Choe, S.; Unutmaz, D.; Burkhart, M.; Di Marzio, P.; Marmon, S.; Sutton, R.E.; Hill, C.M.; Davis, C.B.; Peiper, S.C.; Schall, T.J.; Littman, D.R.; Landau, N.R. Identification of a major co-receptor for primary isolates of HIV-1. Nature, 1996, 381(6584), 661-666.
26. Dragic, T.; Litwin, V.; Allaway, G.P.; Martin, S.R.; Huang, Y.; Nagashima, K.A.; Cayanan, C.; Maddon, P.J.; Koup, R.A.; Moore, J.P.; Paxton, W.A. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature, 1996, 381(6584), 667-673.
27. Alkhatib, G.; Combadiere, C.; Broder, C.C.; Feng, Y.; Kennedy, P.E.; Murphy, P.M.; Berger, E.A. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophagetropic HIV-1. Science, 1996, 272(5270), 1955-1958.
28. Choe, H.; Farzan, M.; Sun, Y.; Sullivan, N.; Rollins, B.; Ponath, P.D.; Wu, L.; Mackay, C.R.; LaRosa, G.; Newman, W.; Gerard, N.; Gerard, C.; Sodroski, J. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell, 1996, 85(7), 1135-1148.
29. Doranz, B.J.; Rucker, J.; Yi, Y.; Smyth, R.J.; Samson, M.; Peiper, S.C.; Parmentier, M.; Collman, R.G.; Doms, R.W. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell, 1996, 85(7), 1149-1158.
30. van Deventer, H.W.; O'Connor, W., Jr.; Brickey, W.J.; Aris, R.M.; Ting, J.P.; Serody, J.S. C-C chemokine receptor 5 on stromal cells promotes pulmonary metastasis. Cancer Res., 2005, 65(8), 3374-3379.
31. Lapteva, N.; Huang, X.F. CCL5 as an adjuvant for cancer immunotherapy. Expert Opin. Biol. Ther., 2010, 10(5), 725-733.
32. Samson, M.; Libert, F.; Doranz, B.J.; Rucker, J.; Liesnard, C.; Farber, C.M.; Saragosti, S.; Lapoumeroulie, C.; Cognaux, J.; Forceille, C.; Muyldermans, G.; Verhofstede, C.; Burtonboy, G.; Georges, M.; Imai, T.; Rana, S.; Yi, Y.; Smyth, R.J.; Collman, R.G.; Doms, R.W.; Vassart, G.; Parmentier, M. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature, 1996, 382(6593), 722-725.
33. Liu, H.; Chao, D.; Nakayama, E.E.; Taguchi, H.; Goto, M.; Xin, X.; Takamatsu, J.K.; Saito, H.; Ishikawa, Y.; Akaza, T.; Juji, T.; Takebe, Y.; Ohishi, T.; Fukutake, K.; Maruyama, Y.; Yashiki, S.; Sonoda, S.; Nakamura, T.; Nagai, Y.; Iwamoto, A.; Shioda, T. Polymorphism in RANTES chemokine promoter affects HIV-1 disease progression. Proc. Natl. Acad. Sci. U.S.A., 1999, 96(8), 4581-4585.
34. An, P.; Nelson, G.W.; Wang, L.; Donfield, S.; Goedert, J.J.; Phair, J.; Vlahov, D.; Buchbinder, S.; Farrar, W.L.; Modi, W.; O'Brien, S.J.; Winkler, C.A. Modulating influence on HIV/AIDS by interacting RANTES gene variants. Proc. Natl. Acad. Sci. U.S.A., 2002, 99(15), 10002-10007.
35. Gonzalez, E.; Kulkarni, H.; Bolivar, H.; Mangano, A.; Sanchez, R.; Catano, G.; Nibbs, R.J.; Freedman, B.I.; Quinones, M.P.; Bamshad, M.J.; Murthy, K.K.; Rovin, B.H.; Bradley, W.; Clark, R.A.; Anderson, S.A.; O'Connell R, J.; Agan, B.K.; Ahuja, S.S.; Bologna, R.; Sen, L.; Dolan, M.J.; Ahuja, S.K. The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science, 2005, 307(5714), 1434-1440.
36. Gilliam, B.L.; Riedel, D.J.; Redfield, R.R. Clinical use of CCR5 inhibitors in HIV and beyond. J. Transl. Med., 2011, 9 Suppl. 1, S9.
37. Glass, W.G.; McDermott, D.H.; Lim, J.K.; Lekhong, S.; Yu, S.F.; Frank, W.A.; Pape, J.; Cheshier, R.C.; Murphy, P.M. CCR5 deficiency increases risk of symptomatic West Nile virus infection. J. Exp. Med., 2006, 203(1), 35-40.
38. Rasmussen, H.B.; Timm, S.; Wang, A.G.; Soeby, K.; Lublin, H.; Fenger, M.; Hemmingsen, R.; Werge, T. Association between the CCR5 32-bp deletion allele and late onset of schizophrenia. Am. J. Psychiatry, 2006, 163(3), 507-511.
39. Wells, T.N.; Power, C.A.; Shaw, J.P.; Proudfoot, A.E. Chemokine blockers--therapeutics in the making? Trends Pharmacol. Sci., 2006, 27(1), 41-47.
40. Wilkin, T.J.; Gulick, R.M. CCR5 antagonism in HIV infection: Current concepts and future opportunities. Annu. Rev. Med., 2012, 63, 81-93.
41. Dorr, P.; Westby, M.; Dobbs, S.; Griffin, P.; Irvine, B.; Macartney, M.; Mori, J.; Rickett, G.; Smith-Burchnell, C.; Napier, C.; Webster, R.; Armour, D.; Price, D.; Stammen, B.; Wood, A.; Perros, M. Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob. Agents Chemother., 2005, 49(11), 4721-4732.
42. Rossi, R.; Lichtner, M.; De Rosa, A.; Sauzullo, I.; Mengoni, F.; Massetti, A.P.; Mastroianni, C.M.; Vullo, V. In vitro effect of antihuman immunodeficiency virus CCR5 antagonist maraviroc on chemotactic activity of monocytes, macrophages and dendritic cells. Clin. Exp. Immunol., 2011, 166(2), 184-190.
43. Strizki, J.M.; Xu, S.; Wagner, N.E.; Wojcik, L.; Liu, J.; Hou, Y.; Endres, M.; Palani, A.; Shapiro, S.; Clader, J.W.; Greenlee, W.J.; Tagat, J.R.; McCombie, S.; Cox, K.; Fawzi, A.B.; Chou, C.C.; Pugliese-Sivo, C.; Davies, L.; Moreno, M.E.; Ho, D.D.; Trkola, A.; Stoddart, C.A.; Moore, J.P.; Reyes, G.R.; Baroudy, B.M. SCH-C (SCH 351125), an orally bioavailable, small molecule antagonist of the chemokine receptor CCR5, is a potent inhibitor of HIV-1 infection in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A., 2001, 98(22), 12718-12723.
44. Sanguinetti, M.C.; Tristani-Firouzi, M. hERG potassium channels and cardiac arrhythmia. Nature, 2006, 440(7083), 463-469.
45. Strizki, J.M.; Tremblay, C.; Xu, S.; Wojcik, L.; Wagner, N.; Gonsiorek, W.; Hipkin, R.W.; Chou, C.C.; Pugliese-Sivo, C.; Xiao, Y.; Tagat, J.R.; Cox, K.; Priestley, T.; Sorota, S.; Huang, W.; Hirsch, M.; Reyes, G.R.; Baroudy, B.M. Discovery and characterization of vicriviroc (SCH 417690), a CCR5 antagonist with potent activity against human immunodeficiency virus type 1. Antimicrob. Agents Chemother., 2005, 49(12), 4911-4919.
46. Baba, M.; Takashima, K.; Miyake, H.; Kanzaki, N.; Teshima, K.; Wang, X.; Shiraishi, M.; Iizawa, Y. TAK-652 inhibits CCR5-mediated human immunodeficiency virus type 1 infection in vitro and has favorable pharmacokinetics in humans. Antimicrob. Agents Chemother., 2005, 49(11), 4584-4591.
47. Gao, P.; Zhou, X.Y.; Yashiro-Ohtani, Y.; Yang, Y.F.; Sugimoto, N.; Ono, S.; Nakanishi, T.; Obika, S.; Imanishi, T.; Egawa, T.; Nagasawa, T.; Fujiwara, H.; Hamaoka, T. The unique target specificity of a nonpeptide chemokine receptor antagonist: selective blockade of two Th1 chemokine receptors CCR5 and CXCR3. J. Leukoc. Biol., 2003, 73(2), 273-280.
48. Tokuyama, H.; Ueha, S.; Kurachi, M.; Matsushima, K.; Moriyasu, F.; Blumberg, R.S.; Kakimi, K. The simultaneous blockade of chemokine receptors CCR2, CCR5 and CXCR3 by a non-peptide chemokine receptor antagonist protects mice from dextran sodium sulfate-mediated colitis. Int. Immunol., 2005, 17(8), 1023-1034.
49. Gong, J.H.; Uguccioni, M.; Dewald, B.; Baggiolini, M.; Clark-Lewis, I. RANTES and MCP-3 antagonists bind multiple chemokine receptors. J. Biol. Chem., 1996, 271(18), 10521-10527.
50. Proudfoot, A.E.; Power, C.A.; Hoogewerf, A.J.; Montjovent, M.O.; Borlat, F.; Offord, R.E.; Wells, T.N. Extension of recombinant human RANTES by the retention of the initiating methionine produces a potent antagonist. J. Biol. Chem., 1996, 271(5), 2599-2603.
51. Teixeira, M.M.; Wells, T.N.; Lukacs, N.W.; Proudfoot, A.E.; Kunkel, S.L.; Williams, T.J.; Hellewell, P.G. Chemokine-induced eosinophil recruitment. Evidence of a role for endogenous eotaxin in an in vivo allergy model in mouse skin. J. Clin. Invest., 1997, 100(7), 1657-1666.
52. Lloyd, C.M.; Dorf, M.E.; Proudfoot, A.; Salant, D.J.; Gutierrez-Ramos, J.C. Role of MCP-1 and RANTES in inflammation and progression to fibrosis during murine crescentic nephritis. J. Leukoc. Biol., 1997, 62(5), 676-680.
53. Mack, M.; Luckow, B.; Nelson, P.J.; Cihak, J.; Simmons, G.; Clapham, P.R.; Signoret, N.; Marsh, M.; Stangassinger, M.; Borlat, F.; Wells, T.N.; Schlondorff, D.; Proudfoot, A.E. Aminooxypentane-RANTES induces CCR5 internalization but inhibits recycling: a novel inhibitory mechanism of HIV infectivity. J. Exp. Med., 1998, 187(8), 1215-1224.
54. Kiss, D.L.; Longden, J.; Fechner, G.A.; Avery, V.M. The functional antagonist Met-RANTES: a modified agonist that induces differential CCR5 trafficking. Cell. Mol. Biol. Lett., 2009, 14(4), 537-547.
55. Longden, J.; Cooke, E.L.; Hill, S.J. Effect of CCR5 receptor antagonists on endocytosis of the human CCR5 receptor in CHOK1 cells. Br. J. Pharmacol., 2008, 153(7), 1513-1527.
56. Simmons, G.; Clapham, P.R.; Picard, L.; Offord, R.E.; Rosenkilde, M.M.; Schwartz, T.W.; Buser, R.; Wells, T.N.; Proudfoot, A.E. Potent inhibition of HIV-1 infectivity in macrophages and lymphocytes by a novel CCR5 antagonist. Science, 1997, 276(5310), 276-279.
57. Lederman, M.M.; Veazey, R.S.; Offord, R.; Mosier, D.E.; Dufour, J.; Mefford, M.; Piatak, M., Jr.; Lifson, J.D.; Salkowitz, J.R.; Rodriguez, B.; Blauvelt, A.; Hartley, O. Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science, 2004, 306(5695), 485-487.
58. Rodriguez-Frade, J.M.; Vila-Coro, A.J.; Martin, A.; Nieto, M.; Sanchez-Madrid, F.; Proudfoot, A.E.; Wells, T.N.; Martinez A.C.; Mellado, M. Similarities and differences in RANTES-and (AOP)-RANTES-triggered signals: implications for chemotaxis. J. Cell. Biol., 1999, 144(4), 755-765.
59. Gaertner, H.; Cerini, F.; Escola, J.M.; Kuenzi, G.; Melotti, A.; Offord, R.; Rossitto-Borlat, I.; Nedellec, R.; Salkowitz, J.; Gorochov, G.; Mosier, D.; Hartley, O. Highly potent, fully recombinant anti-HIV chemokines: reengineering a low-cost microbicide. Proc. Natl. Acad. Sci. U.S.A., 2008, 105(46), 17706-17711.
60. Rot, A. Chemokine patterning by glycosaminoglycans and interceptors. Front. Biosci., 2010, 15, 645-660.
61. Kuschert, G.S.; Coulin, F.; Power, C.A.; Proudfoot, A.E.; Hubbard, R.E.; Hoogewerf, A.J.; Wells, T.N. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry, 1999, 38(39), 12959-12968.
62. Burns, J.M.; Gallo, R.C.; DeVico, A.L.; Lewis, G.K. A new monoclonal antibody, mAb 4A12, identifies a role for the glycosaminoglycan (GAG) binding domain of RANTES in the antiviral effect against HIV-1 and intracellular Ca2+ signaling. J. Exp. Med., 1998, 188(10), 1917-1927.
63. Webb, L.M.; Ehrengruber, M.U.; Clark-Lewis, I.; Baggiolini, M.; Rot, A. Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc. Natl. Acad. Sci. U.S.A., 1993, 90(15), 7158-7162.
64. Wagner, L.; Yang, O.O.; Garcia-Zepeda, E.A.; Ge, Y.; Kalams, S.A.; Walker, B.D.; Pasternack, M.S.; Luster, A.D. Betachemokines are released from HIV-1-specific cytolytic T-cell granules complexed to proteoglycans. Nature, 1998, 391(6670), 908-911.
65. Kuschert, G.S.; Coulin, F.; Power, C.A.; Proudfoot, A.E.; Hubbard, R.E.; Hoogewerf, A.J.; Wells, T.N. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry, 1999, 38(39), 12959-12968.
66. Proudfoot, A.E.; Fritchley, S.; Borlat, F.; Shaw, J.P.; Vilbois, F.; Zwahlen, C.; Trkola, A.; Marchant, D.; Clapham, P.R.; Wells, T.N. The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity. J. Biol. Chem., 2001, 276(14), 10620-10626.
67. Canavese, M.; Altruda, F.; Silengo, L. Therapeutic efficacy and immunological response of CCL5 antagonists in models of contact skin reaction. PLoS One, 2010, 5(1), e8725.
68. Jacobson, J.M.; Saag, M.S.; Thompson, M.A.; Fischl, M.A.; Liporace, R.; Reichman, R.C.; Redfield, R.R.; Fichtenbaum, C.J.; Zingman, B.S.; Patel, M.C.; Murga, J.D.; Pemrick, S.M.; D'Ambrosio, P.; Michael, M.; Kroger, H.; Ly, H.; Rotshteyn, Y.; Buice, R.; Morris, S.A.; Stavola, J.J.; Maddon, P.J.; Kremer, A.B.; Olson, W.C. Antiviral activity of single-dose PRO 140, a CCR5 monoclonal antibody, in HIV-infected adults. J. Infect. Dis., 2008, 198(9), 1345-1352.
69. Lalezari, J.; Yadavalli, G.K.; Para, M.; Richmond, G.; Dejesus, E.; Brown, S.J.; Cai, W.; Chen, C.; Zhong, J.; Novello, L.A.; Lederman, M.M.; Subramanian, G.M. Safety, pharmacokinetics, and antiviral activity of HGS004, a novel fully human IgG4 monoclonal antibody against CCR5, in HIV-1-infected patients. J. Infect. Dis., 2008, 197(5), 721-727.
70. Luboshits, G.; Shina, S.; Kaplan, O.; Engelberg, S.; Nass, D.; Lifshitz-Mercer, B.; Chaitchik, S.; Keydar, I.; Ben-Baruch, A. Elevated expression of the CC chemokine regulated on activation, normal T cell expressed and secreted (RANTES) in advanced breast carcinoma. Cancer Res., 1999, 59(18), 4681-4687.
71. Niwa, Y.; Akamatsu, H.; Niwa, H.; Sumi, H.; Ozaki, Y.; Abe, A. Correlation of tissue and plasma RANTES levels with disease course in patients with breast or cervical cancer. Clin. Cancer Res., 2001, 7(2), 285-289.
72. Soria, G.; Ben-Baruch, A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett., 2008, 267(2), 271-285.
73. Yaal-Hahoshen, N.; Shina, S.; Leider-Trejo, L.; Barnea, I.; Shabtai, E.L.; Azenshtein, E.; Greenberg, I.; Keydar, I.; Ben-Baruch, A. The chemokine CCL5 as a potential prognostic factor predicting disease progression in stage II breast cancer patients. Clin. Cancer Res., 2006, 12(15), 4474-4480.
74. Hartmann, M.C.; Dwyer, R.M.; Costello, M.; Potter, S.M.; Curran, C.; Hennessy, E.; Newell, J.; Griffin, D.G.; Kerin, M.J. Relationship between CCL5 and transforming growth factor-beta1 (TGFbeta1) in breast cancer. Eur. J. Cancer, 2011, 47(11), 1669-1675.
75. Zlotnik, A.; Morales, J.; Hedrick, J.A. Recent advances in chemokines and chemokine receptors. Crit. Rev. Immunol., 1999, 19(1), 1-47.
76. Mrowietz, U.; Schwenk, U.; Maune, S.; Bartels, J.; Kupper, M.; Fichtner, I.; Schroder, J.M.; Schadendorf, D. The chemokine RANTES is secreted by human melanoma cells and is associated with enhanced tumour formation in nude mice. Br. J. Cancer, 1999, 79(7-8), 1025-1031.
77. Vaday, G.G.; Peehl, D.M.; Kadam, P.A.; Lawrence, D.M. Expression of CCL5 (RANTES) and CCR5 in prostate cancer. Prostate, 2006, 66(2), 124-134.
78. Schimanski, C.C.; Moehler, M.; Gockel, I.; Zimmermann, T.; Lang, H.; Galle, P.R.; Berger, M.R. Expression of chemokine receptor CCR5 correlates with the presence of hepatic molecular metastases in K-ras positive human colorectal cancer. J. Cancer Res. Clin. Oncol., 2011, 137(7), 1139-1145.
79. Stormes, K.A.; Lemken, C.A.; Lepre, J.V.; Marinucci, M.N.; Kurt, R.A. Inhibition of metastasis by inhibition of tumor-derived CCL5. Breast Cancer. Res. Treat., 2005, 89(2), 209-212.
80. Mañes, S.; Mira, E.; Gómez-Moutón, C.; Lacalle, R.A.; Martinez A.C. Cells on the move: a dialogue between polarization and motility. IUBMB Life, 2000, 49(2), 89-96.
81. Karnoub, A.E.; Dash, A.B.; Vo, A.P.; Sullivan, A.; Brooks, M.W.; Bell, G.W.; Richardson, A.L.; Polyak, K.; Tubo, R.; Weinberg, R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature, 2007, 449(7162), 557-563.
82. van Deventer, H.W.; Wu, Q.P.; Bergstralh, D.T.; Davis, B.K.; O'Connor, B.P.; Ting, J.P.; Serody, J.S. C-C chemokine receptor 5 on pulmonary fibrocytes facilitates migration and promotes metastasis via matrix metalloproteinase 9. Am. J. Pathol., 2008, 173(1), 253-264.
83. Yang, X.; Lu, P.; Fujii, C.; Nakamoto, Y.; Gao, J.-L.; Kaneko, S.; Murphy, P.M.; Mukaida, N. Essential contribution of a chemokine, CCL3, and its receptor, CCR1, to hepatocellular carcinoma progression. Int. J. Cancer, 2006, 118, 1869-1876.
84. Azenshtein, E.; Luboshits, G.; Shina, S.; Neumark, E.; Shahbazian, D.; Weil, M.; Wigler, N.; Keydar, I.; Ben-Baruch, A. The CC chemokine RANTES in breast carcinoma progression: regulation of expression and potential mechanisms of promalignant activity. Cancer Res., 2002, 62(4), 1093-1102.
85. Arnold, S.; Mira, E.; Muneer, S.; Korpanty, G.; Beck, A.W.; Holloway, S.E.; Mañes, S.; Brekken, R.A. Forced expression of MMP9 rescues the loss of angiogenesis and abrogates metastasis of pancreatic tumors triggered by the absence of host SPARC. Exp. Biol. Med. (Maywood), 2008, 233(7), 860-873.
86. Mira, E.; Lacalle, R.A.; Buesa, J.M.; de Buitrago, G.G.; Jiménez-Baranda, S.; Gómez-Moutón, C.; Martinez A.C.; Mañes, S. Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J. Cell Sci., 2004, 117(Pt 9), 1847-1857.
87. Adler, E.P.; Lemken, C.A.; Katchen, N.S.; Kurt, R.A. A dual role for tumor-derived chemokine RANTES (CCL5). Immunol. Lett., 2003, 90(2-3), 187-194.
88. Robinson, S.C.; Scott, K.A.; Wilson, J.L.; Thompson, R.G.; Proudfoot, A.E.; Balkwill, F.R. A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res., 2003, 63(23), 8360-8365.
89. Tan, M.C.; Goedegebuure, P.S.; Belt, B.A.; Flaherty, B.; Sankpal, N.; Gillanders, W.E.; Eberlein, T.J.; Hsieh, C.S.; Linehan, D.C. Disruption of CCR5-dependent homing of regulatory T cells inhibits tumor growth in a murine model of pancreatic cancer. J. Immunol., 2009, 182(3), 1746-1755.
90. Ng-Cashin, J.; Kuhns, J.J.; Burkett, S.E.; Powderly, J.D.; Craven, R.R.; van Deventer, H.W.; Kirby, S.L.; Serody, J.S. Host absence of CCR5 potentiates dendritic cell vaccination. J. Immunol., 2003, 170(8), 4201-4208.
91. Mellado, M.; de Ana, A.M.; Moreno, M.C.; Martinez, C.; Rodriguez-Frade, J.M. A potential immune escape mechanism by melanoma cells through the activation of chemokine-induced T cell death. Curr. Biol., 2001, 11(9), 691-696.
92. Murooka, T.T.; Wong, M.M.; Rahbar, R.; Majchrzak-Kita, B.; Proudfoot, A.E.; Fish, E.N. CCL5-CCR5-mediated apoptosis in T cells: Requirement for glycosaminoglycan binding and CCL5 aggregation. J. Biol. Chem., 2006, 281(35), 25184-25194.
93. Jayasinghe, M.M.; Golden, J.M.; Nair, P.; O'Donnell, C.M.; Werner, M.T.; Kurt, R.A. Tumor-derived CCL5 does not contribute to breast cancer progression. Breast Cancer Res. Treat., 2008, 111(3), 511-521.
94. Kondo, T.; Ito, F.; Nakazawa, H.; Horita, S.; Osaka, Y.; Toma, H. High expression of chemokine gene as a favorable prognostic factor in renal cell carcinoma. J. Urol., 2004, 171(6 Pt 1), 2171-2175.
95. Liou, J.M.; Lin, J.T.; Huang, S.P.; Wu, C.Y.; Wang, H.P.; Lee, Y.C.; Chiu, H.M.; Shun, C.T.; Lin, M.T.; Wu, M.S. RANTES-403 polymorphism is associated with reduced risk of gastric cancer in women. J. Gastroenterol., 2008, 43(2), 115-123.
96. Mañes, S.; Mira, E.; Colomer, R.; Montero, S.; Real, L.M.; Gómez-Moutón, C.; Jiménez-Baranda, S.; Garzón, A.; Lacalle, R.A.; Harshman, K.; Ruiz, A.; Martinez A.C. CCR5 expression influences the progression of human breast cancer in a p53-dependent manner. J. Exp. Med., 2003, 198(9), 1381-1389.
97. Aoki, M.N.; da Silva do Amaral Herrera, A.C.; Amarante, M.K.; do Val Carneiro, J.L.; Fungaro, M.H.; Watanabe, M.A. CCR5 and p53 codon 72 gene polymorphisms: implications in breast cancer development. Int. J. Mol. Med., 2009, 23(3), 429-435.
98. Cartier, L.; Dubois-Dauphin, M.; Hartley, O.; Irminger-Finger, I.; Krause, K.H. Chemokine-induced cell death in CCR5-expressing neuroblastoma cells. J. Neuroimmunol., 2003, 145(1-2), 27-39.
99. Lim, J.K.; Glass, W.G.; McDermott, D.H.; Murphy, P.M. CCR5: no longer a "good for nothing" gene--chemokine control of West Nile virus infection. Trends Immunol., 2006, 27(7), 308-312.
100. Kohlmeier, J.E.; Miller, S.C.; Smith, J.; Lu, B.; Gerard, C.; Cookenham, T.; Roberts, A.D.; Woodland, D.L. The chemokine receptor CCR5 plays a key role in the early memory CD8+ T cell response to respiratory virus infections. Immunity, 2008, 29(1), 101-113.
101. Crawford, A.; Angelosanto, J.M.; Nadwodny, K.L.; Blackburn, S.D.; Wherry, E.J. A role for the chemokine RANTES in regulating CD8 T cell responses during chronic viral infection. PLoS Pathog., 2011, 7(7), e1002098.
102. Mañes, S.; Viola, A. Lipid rafts in lymphocyte activation and migration. Mol. Membr. Biol., 2006, 23(1), 59-69.
103. Melief, C.J. Cancer immunotherapy by dendritic cells. Immunity, 2008, 29(3), 372-383.
104. Bennett, S.R.; Carbone, F.R.; Karamalis, F.; Flavell, R.A.; Miller, J.F.; Heath, W.R. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature, 1998, 393(6684), 478-480.
105. Schoenberger, S.P.; Toes, R.E.; van der Voort, E.I.; Offringa, R.; Melief, C.J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature, 1998, 393(6684), 480-483.
106. 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(3), 1406-1410.
107. Castellino, F.; Huang, A.Y. Altan-Bonnet, G.; Stoll, S.; Scheinecker, C.; Germain, R.N. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature, 2006, 440(7086), 890-895.
108. Hugues, S.; Scholer, A.; Boissonnas, A.; Nussbaum, A.; Combadiere, C.; Amigorena, S.; Fetler, L. Dynamic imaging of chemokine-dependent CD8+ T cell help for CD8+ T cell responses. Nat. Immunol., 2007, 8(9), 921-930.
109. Boissonnas, A.; Fetler, L.; Zeelenberg, I.S.; Hugues, S.; Amigorena, S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med., 2007, 204(2), 345-356.
110. Marrogi, A.J.; Munshi, A.; Merogi, A.J.; Ohadike, Y.; El-Habashi, A.; Marrogi, O.L.; Freeman, S.M. Study of tumor infiltrating lymphocytes and transforming growth factor-beta as prognostic factors in breast carcinoma. Int. J. Cancer, 1997, 74(5), 492-501.
111. Zhang, L.; Conejo-Garcia, J.R.; Katsaros, D.; Gimotty, P.A.; Massobrio, M.; Regnani, G.; Makrigiannakis, A.; Gray, H.; Schlienger, K.; Liebman, M.N.; Rubin, S.C.; Coukos, G. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med., 2003, 348(3), 203-213.
112. Naito, Y.; Saito, K.; Shiiba, K.; Ohuchi, A.; Saigenji, K.; Nagura, H.; Ohtani, H. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res., 1998, 58(16), 3491-3494.
113. Nakano, O.; Sato, M.; Naito, Y.; Suzuki, K.; Orikasa, S.; Aizawa, M.; Suzuki, Y.; Shintaku, I.; Nagura, H.; Ohtani, H. Proliferative activity of intratumoral CD8(+) T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res., 2001, 61(13), 5132-5136.
114. Schumacher, K.; Haensch, W.; Roefzaad, C.; Schlag, P.M. Prognostic significance of activated CD8(+) T cell infiltrations within esophageal carcinomas. Cancer Res., 2001, 61(10), 3932-3936.
115. Zimmermann, T.; Moehler, M.; Gockel, I.; Sgourakis, G.G.; Biesterfeld, S.; Muller, M.; Berger, M.R.; Lang, H.; Galle, P.R.; Schimanski, C.C. 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(4), 417-424.
116. Uekusa, Y.; Yu, W.G.; Mukai, T.; Gao, P.; Yamaguchi, N.; Murai, M.; Matsushima, K.; Obika, S.; Imanishi, T.; Higashibata, Y.; Nomura, S.; Kitamura, Y.; Fujiwara, H.; Hamaoka, T. 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(13), 3751-3758.
117. Mule, J.J.; Custer, M.; Averbook, B.; Yang, J.C.; Weber, J.S.; Goeddel, D.V.; Rosenberg, S.A.; Schall, T.J. RANTES secretion by gene-modified tumor cells results in loss of tumorigenicity in vivo: role of immune cell subpopulations. Hum. Gene Ther., 1996, 7(13), 1545-1553.
118. Lavergne, E.; Combadiere, C.; Iga, M.; Boissonnas, A.; Bonduelle, O.; Maho, M.; Debre, P.; Combadiere, B. Intratumoral CC chemokine ligand 5 overexpression delays tumor growth and increases tumor cell infiltration. J. Immunol., 2004, 173(6), 3755-3762.
119. Chabot, V.; Reverdiau, P.; Iochmann, S.; Rico, A.; Senecal, D.; Goupille, C.; Sizaret, P.Y.; Sensebe, L. CCL5-enhanced human immature dendritic cell migration through the basement membrane in vitro depends on matrix metalloproteinase-9. J. Leukoc. Biol., 2006, 79(4), 767-778.
120. Hu, Y.; Ivashkiv, L.B. Costimulation of chemokine receptor signaling by matrix metalloproteinase-9 mediates enhanced migration of IFN-alpha dendritic cells. J. Immunol., 2006, 176(10), 6022-6033.
121. Franciszkiewicz, K.; Le Floc'h, A.; Jalil, A.; Vigant, F.; Robert, T.; Vergnon, I.; Mackiewicz, A.; Benihoud, K.; Validire, P.; Chouaib, S.; Combadiere, C.; Mami-Chouaib, F. Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention. Cancer Res., 2009, 69(15), 6249-6255.
122. Burnet, F.M. The concept of immunological surveillance. Prog. Exp. Tumor Res., 1970, 13, 1-27.
123. Schreiber, T.H.; Podack, E.R. A critical analysis of the tumour immunosurveillance controversy for 3-MCA-induced sarcomas. Br. J. Cancer., 2009, 101(3), 381-386.
124. Sanchez, E.Q.; Marubashi, S.; Jung, G.; Levy, M.F.; Goldstein, R.M.; Molmenti, E.P.; Fasola, C.G.; Gonwa, T.A.; Jennings, L.W.; Brooks, B.K.; Klintmalm, G.B. De novo tumors after liver transplantation: a single-institution experience. Liver Transpl., 2002, 8(3), 285-291.
125. Tenderich, G.; Deyerling, W.; Schulz, U.; Heller, R.; Hornik, L.; Schulze, B.; Jahanyar, J.; Koerfer, R. Malignant neoplastic disorders following long-term immunosuppression after orthotopic heart transplantation. Transplant. Proc., 2001, 33(7-8), 3653-3655.
126. Dunn, G.P.; Old, L.J.; Schreiber, R.D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity, 2004, 21(2), 137-148.
127. Pardoll, D. T cells and tumours. Nature, 2001, 411(6841), 1010-1012.
128. Srivastava, A.; Pandey, S.N.; Choudhuri, G.; Mittal, B. CCR5 Delta32 polymorphism: associated with gallbladder cancer susceptibility. Scand. J. Immunol., 2008, 67(5), 516-522.
129. Zheng, B.; Wiklund, F.; Gharizadeh, B.; Sadat, M.; Gambelunghe, G.; Hallmans, G.; Dillner, J.; Wallin, K.L.; Ghaderi, M. Genetic polymorphism of chemokine receptors CCR2 and CCR5 in Swedish cervical cancer patients. Anticancer Res., 2006, 26(5B), 3669-3674.
130. Singh, H.; Sachan, R.; Jain, M.; Mittal, B. CCR5-Delta32 polymorphism and susceptibility to cervical cancer: association with early stage of cervical cancer. Oncol. Res., 2008, 17(2), 87-91.
131. Duell, E.J.; Casella, D.P.; Burk, R.D.; Kelsey, K.T.; Holly, E.A. Inflammation, genetic polymorphisms in proinflammatory genes TNF-A, RANTES, and CCR5, and risk of pancreatic adenocarcinoma. Cancer. Epidemiol. Biomarkers Prev., 2006, 15(4), 726-731.
132. Lustgarten, J.; Dominguez, A.L.; 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(3), 752-761.
133. Vesely, M.D.; Kershaw, M.H.; Schreiber, R.D.; Smyth, M.J. Natural innate and adaptive immunity to cancer. Annu. Rev. Immunol., 2011, 29, 235-271.
134. Ugurel, S.; Schrama, D.; Keller, G.; Schadendorf, D.; Brocker, E.B.; Houben, R.; Zapatka, M.; Fink, W.; Kaufman, H.L.; Becker, J.C. Impact of the CCR5 gene polymorphism on the survival of metastatic melanoma patients receiving immunotherapy. Cancer Immunol. Immunother., 2008, 57(5), 685-691.
135. Magnani, M.; Castro-Gomez, R.H.; Aoki, M.N.; Gregorio, E.P.; Libos, F.; Morimoto, H.K.; Reiche, E.M.; Watanabe, M.A. Analysis of peripheral T cells and the CC chemokine receptor (CCR5) delta32 polymorphism in prostate cancer patients treated with carboxymethyl-glucan (CM-G). Nat. Prod. Res., 2012. In press. doi: 10.1080/14786419.2010.535159
136. Dorgham, K.; Abadie, V.; Iga, M.; Hartley, O.; Gorochov, G.; Combadiere, B. Engineered CCR5 superagonist chemokine as adjuvant in anti-tumor DNA vaccination. Vaccine, 2008, 26(26), 3252-3260.
137. Gough, M.; Crittenden, M.; Thanarajasingam, U.; Sanchez-Perez, L.; Thompson, J.; Jevremovic, D.; Vile, R. Gene therapy to manipulate effector T cell trafficking to tumors for immunotherapy. J. Immunol., 2005, 174(9), 5766-5773.
138. Aravindaram, K.; Yu, H.H.; Lan, C.W.; Wang, P.H.; Chen, Y.H.; Chen, H.M.; Yagita, H.; Yang, N.S. Transgenic expression of human gp100 and RANTES at specific time points for suppression of melanoma. Gene Ther., 2009, 16(11), 1329-1339.
139. Sharma, S.; Dominguez, A.L.; Hoelzinger, D.B.; 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(4), 549-561.
140. Conforti, R.; Ma, Y.; Morel, Y.; Paturel, C.; Terme, M.; Viaud, S.; Ryffel, B.; Ferrantini, M.; Uppaluri, R.; Schreiber, R.; Combadiere, C.; Chaput, N.; Andre, F.; Kroemer, G.; Zitvogel, L. 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(2), 490-500.
141. Zitvogel, L.; Kepp, O.; Kroemer, G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat. Rev. Clin. Oncol., 2011, 8(3), 151-160.
142. Nesbeth, Y.; Scarlett, U.; Cubillos-Ruiz, J.; Martinez, D.; Engle, X.; Turk, M.J.; Conejo-Garcia, J.R. CCL5-mediated endogenous antitumor immunity elicited by adoptively transferred lymphocytes and dendritic cell depletion. Cancer Res., 2009, 69(15), 6331-6338.
143. Mellado, M.; Rodriguez-Frade, J.M.; Mañes, S.; Martinez A.C. Chemokine signaling and functional responses: the role of receptor dimerization and TK pathway activation. Annu. Rev. Immunol., 2001, 19, 397-421.
144. Iida, N.; Nakamoto, Y.; Baba, T.; Nakagawa, H.; Mizukoshi, E.; Naito, M.; Mukaida, N.; Kaneko, S. 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(16), 6556-6565.
145. Liu, C.; Lou, Y.; Lizee, G.; Qin, H.; Liu, S.; Rabinovich, B.; Kim, G.J.; Wang, Y.H.; Ye, Y.; Sikora, A.G.; Overwijk, W.W.; Liu, Y.J.; Wang, G.; Hwu, P. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J. Clin. Invest., 2008, 118(3), 1165-1175.