Ex vivo generation of myeloid-derived suppressor cells that model the tumor immunosuppressive environment in colorectal cancer

Oncotarget

Volumn 6, Issue 14, 2015, Pages 12369-12382

  Dufait, Inès ^a,b   Schwarze, Julia Katharina ^a   Liechtenstein, Therese ^c,d   Leonard, Wim ^a   Jiang, Heng ^a   Escors, David ^c,d   De Ridder, Mark ^a   Breckpot, Karine ^b  

^a UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c Atención Primaria Y Promoción de La Salud   (Spain)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Arginase 1; CRC; GM CSF; Inducible nitric oxide synthase; MDSC

Indexed keywords

ARGINASE 1; CD11B ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; N(G) NITROARGININE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL CULTURE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; COLORECTAL CANCER; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE RELEASE; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; DNA MODIFICATION; DRUG CYTOTOXICITY; ENZYME INHIBITION; EX VIVO STUDY; FEMALE; IMMUNE DEFICIENCY; IN VITRO STUDY; IN VIVO STUDY; MONOCYTE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; MYELOPOIESIS; NONHUMAN; PROTEIN SECRETION; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; TUMOR VOLUME; ANIMAL; BAGG ALBINO MOUSE; COLORECTAL TUMOR; DISEASE MODEL; FLOW CYTOMETRY; GENETIC TRANSDUCTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PATHOLOGY; T LYMPHOCYTE; TUMOR ESCAPE;

ANIMALS; CELL DIFFERENTIATION; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MYELOID CELLS; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TUMOR ESCAPE;

EID: 84931351248     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3682     Document Type: Article

References (68)

1. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes Anne, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc P et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med. 2005; 353: 2654-66.
2. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc P et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006; 313: 1960-64.
3. Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman W, Pagès F and Galon J. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, Th2, Treg, Th17) in Patients with colorectal Cancer. Cancer Res. 2011; 71: 1263-71.
4. Zhang B, Wang Z, Wu L, Zhang M, Li W, Ding J, Zhu J, Wei H and Zhao K. Circulating and tumor-infiltrating myeloid-derived suppressor cells in patients with colorectal carcinoma. PLoS ONE. 2013; 8: e57114.
5. Sermeus A, Leonard W, Engels B and De Ridder M. Advances in radiotherapy and targeted therapies for rectal cancer. World J Gastroenterol. 2014; 20: 1-5.
6. Lechner MG, Karimi SS, Barry-Holson K, Angell TE, Murphy KA, Church CH, Ohlfest JR, Hu P and Epstein AL. Immunogenicity of murine solid tumor models as a defining feature of in vivo behavior and response to immunotherapy. J Immunother. 2013; 36: 477-89.
7. Gabrilovich DI and Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009; 9: 162-74.
8. Lechner MG, Liebertz DJ and Epstein AL. Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol. 2010; 185: 2273-84.
9. Talmadge JE. Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy. Clin Cancer Res. 2007; 13: 5243-48.
10. Gabrilovich DI, Ostrand-Rosenberg S and Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 2012; 12: 253-68.
11. Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A, Martin F, Apetoh L, Rébé C and Ghiringhelli F. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 2010; 70: 3052-61.
12. Suzuki E, Kapoor V, Jassar AS, Kaiser LR and Albelda SM. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res. 2005; 11: 6713-21.
13. Le HK, Graham L, Cha E, Morales JK and Bear HD. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunopharmacol. 2009; 9: 900-09.
14. Kodumudi KN, Woan K, Gilvary DL, Sahakian E, Wei S and Djeu JY. A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin Cancer Res. 2010; 16: 4583-94.
15. Maenhout SK, Van Lint S, Emeagi PU, Thielemans K and Aerts JL. Enhanced suppressive capacity of tumorinfiltrating myeloid-derived suppressor cells compared with their peripheral counterparts. Int J Cancer. 2014; 134: 1077-90.
16. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn J, Cheng P, Cho H, Celis E, Quiceno DG, Padhya T, McCaffery TV, McCaffrey JC and Gabrilovich D. HIF-1 regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med. 2010; 207: 2439-53.
17. Thaci B, Ahmed AU, Ulasov IV, Wainwright DA, Nigam P, Auffinger B, Tobias AL, Han Y, Zhang L, Moon KS and Lesniak MS. Depletion of myeloid-derived suppressor cells during interleukin-12 immunogene therapy does not confer a survival advantage in experimental malignant glioma. Cancer Gene Ther. 2014; 21: 38-44.
18. Apolloni E, Bronte V, Mazzoni A, Serafini P, Cabrelle A, Segal DM, Young A and Zanovello P. Immortalized myeloid suppressor cells trigger apoptosis in antigenactivated T lymphocytes. J Immunol. 2000; 165: 6723-30.
19. Lutz M, Kukutsch N, Menges M, Rössner S and Schuler G. Culture of bone marrow cells in GM-CSF plus high doses of lipopolysaccharide generates exclusively immature dendritic cells which induce alloantigen-specific CD4 T cell anergy in vitro. Eur J Immunol. 2000; 30: 1048-52.
20. Morales JK, Kmieciak M, Knutson KL, Bear HD and Manjili MH. GM-CSF is one of the main breast tumorderived soluble factors involved in the differentiation of CD11b-Gr1-bone marrow progenitor cells into myeloidderived suppressor cells. Breast Cancer Res Treat. 2009; 123: 39-49.
21. Youn J-I, Nagaraj S, Collazo M and Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumorbearing mice. J Immunol. 2008; 181: 5791-802.
22. Marigo I, Bosio E, Solito S, Mesa C, Fernandez A, Dolcetti L, Ugel S, Sonda N, Bicciato S, Falisi E, Calabrese F, Basso G, Zanovello P et al. Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription Factor. Immunity. 2010; 32: 790-802.
23. Zhou Z, French DL, Ma G, Eisenstein S, Cheng Y, Divino CM, Keller G, Chen S and Pan P. Development and function of myeloid-derived suppressor cells generated from mouse embryonic and hematopoietic stem cells. Stem Cells. 2010; 28: 620-32.
24. Obermajer N and Kalinski P. Generation of myeloidderived suppressor cells using prostaglandin E2. Transplant Res. 2012; 1: 15.
25. Xiang X, Poliakov A, Liu C, Liu Y, Deng Z, Wang J, Cheng Z, Shah SV, Wang G, Zhang L, Grizzle WE, Mobley J and Zhang H. Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer. 2008; 124: 2621-33.
26. Highfill SL, Rodriguez PC, Zhou Q, Goetz CA, Koehn BH, Veenstra R, Taylor PA, Panoskaltsis-Mortari A, Serody JS, Munn DV, Tolar J, Ochoa AC and Blazer BR. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graftversus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood. 2010; 116: 5738-47.
27. Escors D, Liechtenstein T, Perez-Janices N, Schwarze J, Dufait I, Goyvaerts C, Lanna A, Arce F, Blanco-Luquin I, Kochan G, Guerrero-Setas D and Breckpot K. Assessing T-cell responses in anticancer immunotherapy: Dendritic cells or myeloid-derived suppressor cells?. Oncoimmunology. 2013; 2: e26148.
28. Liechtenstein T, Perez-Janices N, Gato M Caliendo F, Kochan G, Blanco-Luquin A, Van Der Jeught K, Arce F, Guerrero-Setas D, Fernandez-Irigoyen J, Santamari E, Breckpot K and Escors D. A highly efficient tumorinfiltrating MDSC differentiation system for discovery of anti-neoplastic targets, which circumvents the need for tumor establishment in mice. Oncotarget. 2014; 5: 7843-57.
29. Solito S, Falisi E, Diaz-Montero CM, Doni A, Pinton L, Rosata A, Francescato S, Basso G, Zanovello P, Onicescu G, Garrett-Mayer E, Montero AJ, Bronte V et al. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood. 2011; 118: 2254-65.
30. Sun HL, Zhou X, Xue YF, Wang K, Shen Y, Mao J, Guo H and Miao Z. Increased frequency and clinical significance of myeloid-derived suppressor cells in human colorectal carcinoma. World J Gastroenterol. 2012; 18: 3303-09.
31. Choi J, Suh B, Ahn YO, Kim TM, Lee JO, Lee SH and Heo DS. CD15+/CD16low human granulocytes from terminal cancer patients: granulocytic myeloid-derived suppressor cells that have suppressive function. Tumor Biol. 2011; 33: 121-29.
32. Kusmartsev S, Nagaraj S and Gabrilovich DI. Tumorassociated CD8+ T cell tolerance induced by bone marrowderived immature myeloid cells. J Immunol. 2005; 175: 4583-92.
33. Bronte V, Chappell DB, Apolloni E, Cabrelle A, Wang M, Hwu P and Restifo NP. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J Immunol. 1999; 162: 5728-37.
34. Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S and Schreiber H. The terminology issue for myeloid-derived suppressor cells. Cancer Res. 2007; 67: 425.
35. Ostrand-Rosenberg S and Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol. 2009; 182: 4499-506.
36. Serafini P, Borrello I and Bronte V. Myeloid suppressor cells in cancer: Recruitment, phenotype, properties, and mechanisms of immune suppression. Seminars in Cancer Biology. 2006; 16: 53-65.
37. Ribechini E, Greifenberg V, Sandwick S and Lutz MB. Subsets, expansion and activation of myeloid-derived suppressor cells. Med Microbiol Immunol. 2010; 199: 273-81.
38. Zheng Y, Xu M, Li X, Jia J, Fan K and Lai G. Cimetidine suppresses lung tumor growth in mice through proapoptosis of myeloid-derived suppressor cells. Mol Immunol. 2013; 54: 74-83.
39. Mao Y, Sarhan D, Steven A, Seliger B, Kiessling R and Lundqvist A. Inhibition of tumor-derived prostaglandin-E2 blocks the induction of myeloid-derived suppressor cells and recovers natural killer cell activity. Clin Cancer Res. 2014; 20: 4096-106.
40. Mikysková R, Indrová M, Vlková V, Bieblová J, Simová J, Paracková Z, Pajtasz-Piasecka E, Rossowskai J and Reinis M. DNA demethylating agent 5-azacytidine inhibits myeloid-derived suppressor cells induced by tumor growth and cyclophosphamide treatment. J Leukoc Biol. 2014; 95: 743-53.
41. Alizadeh D, Trad M, Hanke NT, Larmonier CB, Janikashvill N, Bonnotte B, Katsanis E and Larmonier N. Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer. Cancer Res. 2014; 74: 104-18.
42. Chakraborty P, Das S, Banerjee K, Sinha A, Roy S, Chatterjee M and Choudhuri SK. A copper chelate selectively triggers apoptosis in myeloid-derived suppressor cells in a drug-resistant tumor model and enhances antitumor immune response. Immunopharmacol Immunotoxicol. 2014; 36: 165-75.
43. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, Mandruzzato S and Bronte V. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol. 2010; 22: 238-44.
44. Van der Jeught K, Tjok Joe P, Bialkowski L, Heirman C, Daszkiewicz L, Liechtenstein T, Escors D, Thielemans K and Breckpot K. Intratumoral administration of mRNA encoding a fusokine consisting of IFN-β and the ectodomain of the TGF-β receptor II potentiates antitumor immunity. Oncotarget. 2014; 5: 10100-13.
45. Burke B, Pridmore A, Harraghy N, Collick A, Brown J and Mitchell T. Transgenic mice showing inflammationinducible overexpression of granulocyte macrophage colony-stimulating factor. Clin Diagn Lab Immunol. 2004; 11: 588-98.
46. Lang RA, Metcalf D, Cuthbertson RA, Lyons I, Stanley E, Kelso A, Kannourakis G, Williamson DJ, Klinthworth GK and Gonda TJ. Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage. Cell. 1987; 51: 675-86.
47. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, Jackson V, Hamada H, Pardoll D and Mulligan RC. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting antitumor immunity. Proc Natl Acad Sci USA. 1993; 90: 3539-43.
48. Lesokhin AM, Hohl TM, Kitano S, Cortez C, Hirschhorn-Cymerman D, Avogadri F, Rizzuto GA, Lazarus JJ, Pamer EG, Houghton AN, Merghoub T and Wolchok JD. 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.
49. Ruff MR, Farrar WL and Pert CB. Interferon gamma and granulocyte/macrophage colony-stimulating factor inhibit growth and induce antigens characteristic of myeloid differentiation in small-cell lung cancer cell lines. Proc Natl Acad Sci USA. 1986; 83: 6613-17.
50. Yamashita Y, Nara N and Aoki N. Antiproliferative and differentiative effect of granulocyte-macrophage colonystimulating factor on a variant human small cell lung cancer cell line. Cancer Res. 1989; 49: 5334-8.
51. Berdel WE, Danhauser-Riedl S, Steinhauser G and Winton EF. Various human hematopoietic growth factors (interleukin-3, GM-CSF, G-CSF) stimulate clonal growth of nonhematopoietic tumor cells. Blood. 1989; 73: 80-83.
52. Dedhar S, Gaboury L, Galloway P and Eaves C. Human granulocyte-macrophage colony-stimulating factor is a growth factor active on a variety of cell types of nonhemopoietic origin. Proc Natl Acad Sci USA. 1988; 85: 9253-57.
53. Berdel WE, Zafferani M, Senekowitsch R, Kreuser ED and Thiel E. Effect of interleukin-3 and granulocytemacrophage colony-stimulating factor on growth of xenotransplanted human tumour cell lines in nude mice. Eur J Cancer. 1992; 28-377-80.
54. Foulke RS, Marshall MH, Trotta PP and Von Hoff DD. In vitro assessment of the effects of granulocyte-macrophage colony-stimulating factor on primary human tumors and derived lines. Cancer Res. 1990; 50: 6264-67.
55. Obermueller E, Vosseler S, Fusenig NE and Mueller MM. Cooperative autocrine and paracrine functions of granulocyte colony-stimulating factor and granulocytemacrophage colony-stimulating factor in the progression of skin carcinoma cells. Cancer Res. 2001; 64: 7801-12.
56. Gutschalk CM, Herold-Mende CC, Fusening NE and Mueller MM. Granulocyte Colony-Stimulating Factor and Granulocyte-Macrophage Colony-Stimulating Factor Promote Malignant Growth of Cells from Head and Neck Squamous Cell Carcinomas In vivo. Cancer Res. 2006; 66: 8026-36.
57. Gutschalk CM, Yanamandra AK, Linde N, Meides A, Depner S and Mueller MM. GM-CSF enhances tumor invasion by elevated MMP-2,-9, and-26 expression. Cancer Med. 2012; 2: 117-29.
58. Nebiker C, Han J, Eppenberger-Castori S, Iezzi G, Amicarella F, Cremonesi E, Huber X, Padovan E, Angrisani B, Droeser RA, Rosso R, Bolli M, Oertli D et al. GM-CSF production by tumor cells is associated with improved survival in colorectal cancer. Clin Cancer Res. 2014; 20: 3094-106.
59. Le DT, Pardoll DM and Jaffee EM. Cellular vaccine approaches. Cancer Journal. 2010; 16: 304-10.
60. Faries MB, Hsueh EC, Ye X, Hoban M and Morton DL. Effect of granulocyte/macrophage colony-stimulating factor on vaccination with an allogeneic whole-cell melanoma vaccine. Clin Cancer Res. 2009; 15: 7029-35.
61. Slingluff CL, Petroni GR, Olson WC, Smolkin ME, Ross MI, Haas NB, Grosh WW, Boisvert ME, Kirkwood JM and Chianese-Bullock KA. Effect of granulocyte/macrophage colony-stimulating factor on circulating CD8+ and CD4+ T-cell responses to a multipeptide melanoma vaccine: outcome of a multicenter randomized trial. Clin Cancer Res. 2009; 15: 7036-44.
62. Jayaraman P, Alfarano MG, Svider PF, Parikh F, Lu G, Xiong H and Sikora AG. iNOS expression in CD4+ T cells limits T-reg induction by repressing TGFb-1: combined iNOS inhibition and T-reg depletion unmask endogenous anti-tumor immunity. Clin Cancer Res. 2014; 20(23).
63. Rigamonti N, Capuano G, Ricupito A, Jachetti E, Grioni M, Generoso L, Freschi M and Bellone M. Modulators of arginine metabolism do not impact on peripheral T-cell tolerance and disease progression in a model of spontaneous prostate cancer. Clin Cancer Res. 2011; 17: 1012-23.
64. Rodriguez PC, Ernstoff MS, Hernandez C Atkins M, Zabaleta J, Sierra R and Ochoa AC. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 2009; 69: 1553-60.
65. Goyvaerts C, De Groeve K, Dingemans J, Van Lint S, Robays L, Heirman C, Reiser J, Zhang XY, De Baestelier P, Raes G and Breckpot K. Development of the Nanobody display technology to target lentiviral vectors to antigenpresenting cells. Gene Therapy. 2012; 19: 1133-40.
66. Emeagi PU, Thielemans K and Breckpot K. The role of SMAC mimetics in regulation of tumor cell death and immunity. Oncoimmunology. 2012; 1: 965-67.
67. Breckpot K, Dullaers M, Bonehill A, Meirvenne SV, Heirman C, Greef CD, Van der Bruggen P and Thielemans K. Lentivirally transduced dendritic cells as a tool for cancer immunotherapy. J Gene Med. 2003; 5: 654-67.
68. Van Lint S, Goyvaerts C, Maenhout S, Goethals L, Disy A, Benteyn D, Pen J, Bonehill A, Heirman C, Breckpot K and Thielemans K. Preclinical evaluation of triMix and antigen mRNA-based antitumor therapy. Cancer Res. 2012; 72: 1661-71.