CCR5+ myeloid-derived suppressor cells are enriched and activated in melanoma lesions

Cancer Research

Volumn 78, Issue 1, 2018, Pages 157-167

  Blattner, Carolin ^a   Fleming, Viktor ^a   Weber, Rebekka ^a   Himmelhan, Bianca ^a   Altevogt, Peter ^a   Gebhardt, Christoffer ^a   Schulze, Torsten J ^b   Razon, Hila ^c   Hawila, Elias ^c   Wildbaum, Gizi ^c   Utikal, Jochen ^a   Karin, Nathan ^c   Umansky, Viktor ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CCR5 IMMUNOGLOBULIN FUSION PROTEIN; CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR5; HYBRID PROTEIN; UNCLASSIFIED DRUG; CCR5 PROTEIN, HUMAN; PROTEIN RET; RET PROTEIN, HUMAN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CANCER GROWTH; CANCER INHIBITION; CELL ACTIVATION; CELL INFILTRATION; CELL MIGRATION; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MELANOMA; MOUSE; MYELOID-DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SURVIVAL; TRANSGENIC MOUSE; TUMOR MICROENVIRONMENT; UPREGULATION; VERY ELDERLY; ANIMAL; C57BL MOUSE; CELL MOTION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CELL MOVEMENT; FEMALE; HUMANS; MALE; MELANOMA; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; MYELOID-DERIVED SUPPRESSOR CELLS; PROTO-ONCOGENE PROTEINS C-RET; RECEPTORS, CCR5; TUMOR MICROENVIRONMENT;

EID: 85040123083     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-17-0348     Document Type: Article

References (49)

1. Kumar V, Patel S, Tcyganov E, Gabrilovich DI. The nature of myeloidderived suppressor cells in the tumor microenvironment. Trends Immunol 2016;37:208-20.
2. Parker KH, Beury DW, Ostrand-Rosenberg S. Myeloid-derived suppressor cells: critical cells driving immune suppression in the tumor microenvironment. Adv Cancer Res 2015;128:95-139.
3. De Sanctis F, Solito S, Ugel S, Molon B, Bronte V, Marigo I.MDSCsin cancer: Conceiving new prognostic and therapeutic targets. Biochim Biophys Acta 2016;1865:35-48.
4. Umansky V, Sevko A. Melanoma-induced immunosuppression and its neutralization. Semin Cancer Biol 2012;22:319-26.
5. Bronte V, Brandau S, Chen SH, Colombo MP, Frey AB, Greten TF, et al. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun 2016;7:12150.
6. Filipazzi P, Huber V, Rivoltini L. Phenotype, function and clinical implications ofmyeloid-derived suppressor cells in cancer patients. Cancer Immunol Immunother 2012;61:255-63.
7. Solito S, Marigo I, Pinton L, Damuzzo V, Mandruzzato S, Bronte V. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann NY Acad Sci 2014;1319:47-65.
8. Poschke I, Kiessling R. On the armament and appearances of human myeloid-derived suppressor cells. Clin Immunol 2012;144: 250-68.
9. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
10. Kanterman J, Sade-Feldman M, Baniyash M. New insights into chronic inflammation-induced immunosuppression. Semin Cancer Biol 2012;22: 307-18.
11. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009;182:4499-506.
12. Homey B, Muller A, Zlotnik A. Chemokines: agents for theimmunotherapy of cancer? Nature Rev Immunol 2002;2:175-84.
13. Combadiere C, Ahuja SK, Tiffany HL, Murphy PM. Cloning and functional expression of CC CKR5, a human monocyte CC chemokine receptor selective forMIP-1(alpha), MIP-1(beta), and RANTES. J Leukoc Biol 1996; 60:147-52.
14. Balistreri CR, Carruba G, Calabro M, Campisi I, Di Carlo D, Lio D, et al. CCR5 proinflammatory allele in prostate cancer risk: a pilot study in patients and centenarians from Sicily. Ann N Y Acad Sci 2009;1155: 289-92.
15. 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;59:4681-87.
16. Mrowietz U, Schwenk U, Maune S, Bartels J, Küpper M, Fichtner I, et al. The chemokine RANTES is secreted byhuman melanomacells and is associated with enhanced tumour formation in nude mice. Br J Cancer 1999;79: 1025-31.
17. Robinson SC, Scott KA, Wilson JL, Thompson RG, Proudfoot AE, Balkwill FR. A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res 2003;63:8360-65.
18. Tan MC, Goedegebuure PS, Belt BA, Flaherty B, Sankpal N, Gillanders WE, et al. Disruption of CCR5-dependent homing of regulatory T cells inhibits tumor growth in a murine model of pancreatic cancer. J Immunol 2009;182:1746-55.
19. Zhang X, Haney KM, Richardson AC, Wilson E, Gewirtz DA, Ware JL, et al. Anibamine, a natural product CCR5 antagonist, as a novel lead for the development of anti-prostate cancer agents. Bioorg Med Chem Lett 2010; 20:4627-30.
20. Velasco-Velazquez M, Jiao X, De La Fuente M, Pestell TG, Ertel A, Lisanti MP, et al. CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res 2012;72:3839-50.
21. Halama N, Zoernig I, Berthel A, Kahlert C, Klupp F, Suarez-Carmona M, et al. Tumoral immune cell exploitation in colorectal cancer metastases can be targeted effectively by anti-CCR5 therapy in cancer patients. Cancer Cell 2016;29:587-601.
22. Lesokhin AM, Hohl TM, Kitano S, Cortez C, Hirschhorn-Cymerman D, Avogadri F, et al. Monocytic CCR2(+) myeloid-derived suppressor cells promote immune escape by limiting activated CD8 T-cell infiltration into the tumor microenvironment. Cancer Res 2012;72:876-86.
23. Izhak L, Wildbaum G, Zohar Y, Anunu R, Klapper L, Elkeles A, et al. A novel recombinant fusion protein encoding a 20-amino acid residue of the third extracellular (E3) domain of CCR2 neutralizes the biological activity of CCL2. J Immunol 2009;183:732-9.
24. Izhak L, Wildbaum G, Jung S, Stein A, Shaked Y, Karin N. Dissecting the autocrine and paracrine roles of the CCR2-CCL2 axis in tumor survival and angiogenesis. PLoS ONE 2012;7:e28305.
25. Kato M, Takahashi M, Akhand AA, Liu W, Dai Y, Shimizu S, et al. Transgenic mouse model for skin malignant melanoma. Oncogene 1998;17:1885-8.
26. Umansky V, Abschuetz O, Osen W, Ramacher M, Zhao F, Kato M, et al. Melanoma-specificmemory T cells are functionally active in Ret transgenic mice without macroscopic tumors. Cancer Res 2008;68:9451-8.
27. Sapir Y, Vitenshtein A, Barsheshet Y, Zohar Y, Wildbaum G, Karin N. A fusion protein encoding the second extracellular domain of CCR5 arrests chemokine-induced cosignaling and effectively suppresses ongoing experimental autoimmune encephalomyelitis. J Immunol 2010;185: 2589-99.
28. Zohar Y, Wildbaum G, Novak R, Salzman AL, Thelen M, Alon R, et al. CXCL11-dependent induction of FOXP3-negative regulatory T cells suppresses autoimmune encephalomyelitis. J Clin Invest 2014;124:2009-22.
29. Schlecker E, Stojanovic A, Eisen C, Quack C, Falk CS, Umansky V, et al. Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth. J Immunol 2012;189:5602-11.
30. Appay V, Rowland-Jones SL. RANTES: a versatile and controversial chemokine. Trends Immunol 2001;22:83-7.
31. Velasco-Velazquez M, Jiao X, De La Fuente M, Pestell TG, Ertel A, Lisanti MP, et al. CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res 2012;72:3839-50.
32. Zhu Z, Aref AR, Cohoon TJ, Barbie TU, Imamura Y, Yang S, et al. Barbie, Inhibition of KRAS-driven tumorigenicity by interruption of an autocrine cytokine circuit. Cancer Discov 2014;4:452-65.
33. Aldinucci D, Colombatti A. The inflammatory chemokine CCL5 and cancer progression. Mediators Inflamm 2014;2014:292376.
34. Richmond A, Yang J, Su Y. The good and the bad of chemokines/chemokine receptors in melanoma. Pigment Cell Melanoma Res 2009;22: 175-86.
35. Gao D, Rahbar R, Fish EN. CCL5 activation of CCR5 regulates cell metabolism to enhance proliferation of breast cancer cells. Open Biol 2016;6:160122.
36. Meyer C, Sevko A, Ramacher M, Bazhin AV, Falk CS, Osen W, et al. Chronic inflammation promotesmyeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mousemelanoma model. Proc Natl Acad Sci U S A 2011;108:17111-6.
37. Sevko A, Michels T, Vrohlings M, Umansky L, Beckhove P, Kato M, et al. Antitumor effect of paclitaxel is mediated by inhibition ofmyeloid-derived suppressor cells and chronic inflammation in the spontaneous melanoma model. J Immunol 2013;190:2464-71.
38. Lin S, Wan S, Sun L, Hu J, Fang D, Zhao R, et al. Chemokine C-C motif receptor 5 and C-C motif ligand 5 promote cancer cell migration under hypoxia. Cancer Sci 2012;103:904-12.
39. Zhang Y, Lv D, Kim HJ, Kurt RA, Bu W, Li Y, et al. A novel role of hematopoietic CCL5 in promoting triple-negative mammary tumor progression by regulating generation of myeloid-derived suppressor cells. Cell Res 2013;23:394-408.
40. Ward ST, Li KK, Hepburn E, Weston CJ, Curbishley SM, Reynolds GM, et al. The effects of CCR5 inhibition on regulatory T-cell recruitment to colorectal cancer. Br J Cancer 2015;112:319-28.
41. Chang LY, Lin YC, Kang CW, Hsu CY, Chu YY, Huang CT, et al. The indispensable role of CCR5 for in vivo suppressor function of tumorderived CD103+ effector/memory regulatory T cells. J Immunol 2012; 189:567-74.
42. Pervaiz A, Ansari S, Berger MR, Adwan H. CCR5 blockage by maraviroc induces cytotoxic and apoptotic effects in colorectal cancer cells. Med Oncol 2015;32:158.
43. Mencarelli A, Graziosi L, Renga B, Cipriani S, D'Amore C, Francisci D, et al. CCR5 antagonism by maraviroc reduces the potential for gastric cancer cell dissemination. Transl Oncol 2013;6:784-93.
44. Sicoli D, Jiao X, Ju X, Velasco-Velazquez M, Ertel A, Addya S, et al. CCR5 receptor antagonists block metastasis to bone of v-Src oncogene-transformed metastatic prostate cancer cell lines. Cancer Res 2014;74:7103-14.
45. Tang Q, Jiang J, Liu J. CCR5 blockade suppresses melanoma development through inhibition of IL-6-Stat3 pathway via upregulation of SOCS3. Inflammation 2015;38:2049-56.
46. Jiang H, Gebhardt C, Umansky L, Beckhove P, Schulze TJ, Utikal J, et al. Elevated chronic inflammatory factors and myeloid-derived suppressor cells indicate poor prognosis in advanced melanoma patients. Int J Cancer 2015;136:2352-60.
47. Weide B, Martens A, Zelba H, Stutz C, Derhovanessian E, Di Giacomo AM, et al. Myeloid-derived suppressor cells predict survival of advanced melanoma patients: comparison with regulatory T cells and NY-ESO-1- or Melan-A-specific T cells. Clin Cancer Res 2014;20:1601-9.
48. Jordan KR, Amaria RN, Ramirez O, Callihan EB, Gao D, Borakove M, et al. Myeloid-derived suppressor cells are associated with disease progression and decreased overall survival in advanced-stage melanoma patients. Cancer Immunol Immunother 2013;62:1711-22.
49. Schilling B, Sucker A, Griewank K, Zhao F, Weide B, Görgens A, et al. Vemurafenib reverses immunosuppression bymyeloid-derived suppressor cells. Int J Cancer 2013;133:1653-63.