Anti-tumor immunity: Myeloid leukocytes control the immune landscape

Cellular Immunology

Volumn 278, Issue 1-2, 2012, Pages 21-26

  Rutkowski, Melanie R ^a   Stephen, Tom L ^a   Conejo Garcia, Jose R ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

Dendritic cell; Immune surveillance; Immunoediting; Immunosuppression; Immunotherapy; Tumor immunology; Tumor microenvironment

Indexed keywords

3 METHYLCHOLANTHRENE; CXCL1 CHEMOKINE; DIMETHYLBENZ[A]ANTHRACENE; GAMMA INTERFERON; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; PHORBOL 13 ACETATE 12 MYRISTATE; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN A;

ADAPTIVE IMMUNITY; ANGIOGENESIS; ANTIGENICITY; BONE MARROW CELL; CANCER GROWTH; CARCINOGENESIS; DENDRITIC CELL; ENERGY METABOLISM; EOSINOPHIL; GAMMA DELTA T LYMPHOCYTE; HUMAN; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; LEUKOCYTE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

ADAPTIVE IMMUNITY; ANTIGENS, NEOPLASM; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; DENDRITIC CELLS; DISEASE PROGRESSION; HUMANS; IMMUNE TOLERANCE; IMMUNITY, INNATE; IMMUNOLOGIC SURVEILLANCE; MYELOID CELLS; NEOPLASMS; T-LYMPHOCYTES; TUMOR ESCAPE;

EID: 84868288550     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2012.06.014     Document Type: Review

References (80)

1. Burnet M. Cancer; a biological approach. I. The processes of control. Br. Med. J. 1957, 1:779-786.
2. Thomas L. Cellular and Humoral Aspects of the Hypersensitive States 1959, Hoeber-Harper, New York.
3. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., Schreiber R.D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 2002, 3:991-998.
4. Matsushita H., Vesely M.D., Koboldt D.C., Rickert C.G., Uppaluri R., Magrini V.J., Arthur C.D., White J.M., Chen Y.S., Shea L.K., Hundal J., Wendl M.C., Demeter R., Wylie T., Allison J.P., Smyth M.J., Old L.J., Mardis E.R., Schreiber R.D. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012, 482:400-404.
5. Yoshimoto M., Sakamoto G., Ohashi Y. Time dependency of the influence of prognostic factors on relapse in breast cancer. Cancer 1993, 72:2993-3001.
6. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pages C., Tosolini M., Camus M., Berger A., Wind P., Zinzindohoue F., Bruneval P., Cugnenc P.H., Trajanoski Z., Fridman W.H., Pages F. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960-1964.
7. Clemente C.G., Mihm M.C., Bufalino R., Zurrida S., Collini P., Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 1996, 77:1303-1310.
8. 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, 348:203-213.
9. Kalos M., Levine B.L., Porter D.L., Katz S., Grupp S.A., Bagg A., June C.H. T cells with chimeric antigen receptors have potent antitumor effects can establish memory in patients with advanced leukemia. Sci. Transl. Med. 2011, 3:95ra73.
10. Porter D.L., Levine B.L., Kalos M., Bagg A., June C.H. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 2011, 365:725-733.
11. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., Topalian S.L., Sherry R., Restifo N.P., Hubicki A.M., Robinson M.R., Raffeld M., Duray P., Seipp C.A., Rogers-Freezer L., Morton K.E., Mavroukakis S.A., White D.E., Rosenberg S.A. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002, 298:850-854.
12. Pardoll D., Drake C. Immunotherapy earns its spot in the ranks of cancer therapy. J. Exp. Med. 2012, 209:201-209.
13. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., Leming P.D., Spigel D.R., Antonia S.J., Horn L., Drake C.G., Pardoll D.M., Chen L., Sharfman W.H., Anders R.A., Taube J.M., McMiller T.L., Xu H., Korman A.J., Jure-Kunkel M., Agrawal S., McDonald D., Kollia G.D., Gupta A., Wigginton J.M., Sznol M. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 2012.
14. Scarlett U.K., Rutkowski M.R., Rauwerdink A.M., Fields J., Escovar-Fadul X., Baird J., Cubillos-Ruiz J.R., Jacobs A.C., Gonzalez J.L., Weaver J., Fiering S., Conejo-Garcia J.R. Ovarian cancer progression is controlled by phenotypic changes in dendritic cells. J. Exp. Med. 2012, 209:495-506.
15. 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.
16. Prestwich R.J., Errington F., Hatfield P., Merrick A.E., Ilett E.J., Selby P.J., Melcher A.A. The immune system-is it relevant to cancer development, progression and treatment?. Clin. Oncol. (R. Coll. Radiol.) 2008, 20:101-112.
17. Fridlender Z.G., Albelda S.M. Tumor-associated neutrophils: friend or foe?. Carcinogenesis 2012, 33:949-955.
18. Granot Z., Henke E., Comen E.A., King T.A., Norton L., Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 2011, 20:300-314.
19. Fridlender Z.G., Sun J., Kim S., Kapoor V., Cheng G., Ling L., Worthen G.S., Albelda S.M. Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 2009, 16:183-194.
20. Koebel C.M., Vermi W., Swann J.B., Zerafa N., Rodig S.J., Old L.J., Smyth M.J., Schreiber R.D. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007, 450:903-907.
21. Curiel T.J., Coukos G., Zou L., Alvarez X., Cheng P., Mottram P., Evdemon-Hogan M., Conejo-Garcia J.R., Zhang L., Burow M., Zhu Y., Wei S., Kryczek I., Daniel B., Gordon A., Myers L., Lackner A., Disis M.L., Knutson K.L., Chen L., Zou W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 2004, 10:942-949.
22. Peng G., Wang H.Y., Peng W., Kiniwa Y., Seo K.H., Wang R.F. Tumor-infiltrating gammadelta T cells suppress T and dendritic cell function via mechanisms controlled by a unique toll-like receptor signaling pathway. Immunity 2007, 27:334-348.
23. Sato E., Olson S.H., Ahn J., Bundy B., Nishikawa H., Qian F., Jungbluth A.A., Frosina D., Gnjatic S., Ambrosone C., Kepner J., Odunsi T., Ritter G., Lele S., Chen Y.T., Ohtani H., Old L.J., Odunsi K. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci. USA 2005, 102:18538-18543.
24. Quezada S.A., Simpson T.R., Peggs K.S., Merghoub T., Vider J., Fan X., Blasberg R., Yagita H., Muranski P., Antony P.A., Restifo N.P., Allison J.P. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J. Exp. Med. 2010, 207:637-650.
25. Xie Y., Akpinarli A., Maris C., Hipkiss E.L., Lane M., Kwon E.K., Muranski P., Restifo N.P., Antony P.A. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 2010, 207:651-667.
26. Ma Y., Aymeric L., Locher C., Mattarollo S.R., Delahaye N.F., Pereira P., Boucontet L., Apetoh L., Ghiringhelli F., Casares N., Lasarte J.J., Matsuzaki G., Ikuta K., Ryffel B., Benlagha K., Tesniere A., Ibrahim N., Dechanet-Merville J., Chaput N., Smyth M.J., Kroemer G., Zitvogel L. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J. Exp. Med. 2011, 208:491-503.
27. Nesbeth Y., Conejo-Garcia J.R. Harnessing the effect of adoptively transferred tumor-reactive T cells on endogenous (host-derived) antitumor immunity. Clin. Dev. Immunol. 2010, 2010:139304.
28. 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, 69:6331-6338.
29. 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- ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells. J. Immunol. 2010, 184:5654-5662.
30. Hildner K., Edelson B.T., Purtha W.E., Diamond M., Matsushita H., Kohyama M., Calderon B., Schraml B.U., Unanue E.R., Diamond M.S., Schreiber R.D., Murphy T.L., Murphy K.M. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008, 322:1097-1100.
31. Zitvogel L., Tesniere A., Kroemer G. Cancer despite immunosurveillance. immunoselection and immunosubversion. Nat. Rev. Immunol. 2006, 6:715-727.
32. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., Schreiber R.D. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001, 410:1107-1111.
33. Dunn G.P., Old L.J., Schreiber R.D. The three Es of cancer immunoediting. Annu. Rev. Immunol. 2004, 22:329-360.
34. Dunn G.P., Old L.J., Schreiber R.D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004, 21:137-148.
35. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565-1570.
36. DuPage M., Mazumdar C., Schmidt L.M., Cheung A.F., Jacks T. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 2012, 482:405-409.
37. Blankenstein T., Coulie P.G., Gilboa E., Jaffee E.M. The determinants of tumour immunogenicity. Nat Rev Cancer 2012, 12:307-313.
38. D. Hanahan, R.A. Weinberg, Hallmarks of cancer: the next generation, Cell 144 646-674.
39. Wherry E.J. T cell exhaustion. Nat. Immunol. 2011, 12:492-499.
40. Baitsch L., Fuertes-Marraco S.A., Legat A., Meyer C., Speiser D.E. The three main stumbling blocks for anticancer T cells. Trends Immunol. 2012.
41. Zheng Y., Zha Y., Gajewski T.F. Molecular regulation of T-cell anergy. EMBO Rep. 2008, 9:50-55.
42. Han S., Asoyan A., Rabenstein H., Nakano N., Obst R. Role of antigen persistence and dose for CD4+ T-cell exhaustion and recovery. Proc. Natl. Acad. Sci. USA 2010, 107:20453-20458.
43. Baitsch L., Baumgaertner P., Devevre E., Raghav S.K., Legat A., Barba L., Wieckowski S., Bouzourene H., Deplancke B., Romero P., Rufer N., Speiser D.E. Exhaustion of tumor-specific CD8(+) T cells in metastases from melanoma patients. J. Clin. Invest. 2011, 121:2350-2360.
44. Wang S.F., Fouquet S., Chapon M., Salmon H., Regnier F., Labroquere K., Badoual C., Damotte D., Validire P., Maubec E., Delongchamps N.B., Cazes A., Gibault L., Garcette M., Dieu-Nosjean M.C., Zerbib M., Avril M.F., Prevost-Blondel A., Randriamampita C., Trautmann A., Bercovici N. Early T cell signalling is reversibly altered in PD-1+ T lymphocytes infiltrating human tumors. PLoS One 2011, 6:e17621.
45. Beatty G.L., Smith J.S., Reshef R., Patel K.P., Colligon T.A., Vance B.A., Frey N.V., Johnson F.B., Porter D.L., Vonderheide R.H. Functional unresponsiveness and replicative senescence of myeloid leukemia antigen-specific CD8+ T cells after allogeneic stem cell transplantation. Clin. Cancer Res. 2009, 15:4944-4953.
46. Shay J.W., Roninson I.B. Hallmarks of senescence in carcinogenesis and cancer therapy. Oncogene 2004, 23:2919-2933.
47. Lechner M.G., Liebertz D.J., Epstein A.L. Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J. Immunol. 2010, 185:2273-2284.
48. Norian L.A., Rodriguez P.C., O'Mara L.A., Zabaleta J., Ochoa A.C., Cella M., Allen P.M. Tumor-infiltrating regulatory dendritic cells inhibit CD8+ T cell function via l-arginine metabolism. Cancer Res. 2009, 69:3086-3094.
49. Prendergast G.C., Metz R., Muller A.J. Towards a genetic definition of cancer-associated inflammation: role of the IDO pathway. Am. J. Pathol. 2010, 176:2082-2087.
50. Stone T.W., Darlington L.G. Endogenous kynurenines as targets for drug discovery and development. Nat. Rev. Drug Discov. 2002, 1:609-620.
51. Ahmadzadeh M., Rosenberg S.A. TGF-beta 1 attenuates the acquisition and expression of effector function by tumor antigen-specific human memory CD8 T cells. J. Immunol. 2005, 174:5215-5223.
52. Torre-Amione G., Beauchamp R.D., Koeppen H., Park B.H., Schreiber H., Moses H.L., Rowley D.A. A highly immunogenic tumor transfected with a murine transforming growth factor type beta 1 cDNA escapes immune surveillance. Proc. Natl. Acad. Sci. USA 1990, 87:1486-1490.
53. Sinha P., Okoro C., Foell D., Freeze H.H., Ostrand-Rosenberg S., Srikrishna G. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J. Immunol. 2008, 181:4666-4675.
54. Meyer C., Sevko A., Ramacher M., Bazhin A.V., Falk C.S., Osen W., Borrello I., Kato M., Schadendorf D., Baniyash M., Umansky V. Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model. Proc. Natl. Acad. Sci. USA 2011, 108:17111-17116.
55. Lu T., Ramakrishnan R., Altiok S., Youn J.I., Cheng P., Celis E., Pisarev V., Sherman S., Sporn M.B., Gabrilovich D. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J. Clin. Invest. 2011, 121:4015-4029.
56. Serafini P., Meckel K., Kelso M., Noonan K., Califano J., Koch W., Dolcetti L., Bronte V., Borrello I. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J. Exp. Med. 2006, 203:2691-2702.
57. Gabrilovich D.I., Ostrand-Rosenberg S., Bronte V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012, 12:253-268.
58. Nagaraj S., Gupta K., Pisarev V., Kinarsky L., Sherman S., Kang L., Herber D.L., Schneck J., Gabrilovich D.I. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 2007, 13:828-835.
59. Corzo C.A., Condamine T., Lu L., Cotter M.J., Youn J.I., Cheng P., Cho H.I., Celis E., Quiceno D.G., Padhya T., McCaffrey T.V., McCaffrey J.C., Gabrilovich D.I. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 2010, 207:2439-2453.
60. Conejo-Garcia J.R., Benencia F., Courreges M.C., Kang E., Mohamed-Hadley A., Buckanovich R.J., Holtz D.O., Jenkins A., Na H., Zhang L., Wagner D.S., Katsaros D., Caroll R., Coukos G. Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat. Med. 2004, 10:950-958.
61. Conejo-Garcia J.R., Buckanovich R.J., Benencia F., Courreges M.C., Rubin S.C., Carroll R.G., Coukos G. Vascular leukocytes contribute to tumor vascularization. Blood 2005, 105:679-681.
62. Cubillos-Ruiz J.R., Engle X., Scarlett U.K., Martinez D., Barber A., Elgueta R., Wang L., Nesbeth Y., Durant Y., Gewirtz A.T., Sentman C.L., Kedl R., Conejo-Garcia J.R. Polyethylenimine-based siRNA nanocomplexes reprogram tumor-associated dendritic cells via TLR5 to elicit therapeutic antitumor immunity. J. Clin. Invest. 2009, 119:2231-2244.
63. Cubillos-Ruiz J.R., Fiering S., Conejo-Garcia J.R. Nanomolecular targeting of dendritic cells for ovarian cancer therapy. Future Oncol. 2009, 5:1189-1192.
64. J.R. Cubillos-Ruiz, M. Rutkowski, J.R. Conejo-Garcia, Blocking ovarian cancer progression by targeting tumor microenvironmental leukocytes, Cell Cycle, 9 260-268.
65. Huarte E., Cubillos-Ruiz J.R., Nesbeth Y.C., Scarlett U.K., Martinez D.G., Buckanovich R.J., Benencia F., Stan R.V., Keler T., Sarobe P., Sentman C.L., Conejo-Garcia J.R. Depletion of dendritic cells delays ovarian cancer progression by boosting antitumor immunity. Cancer Res. 2008, 68:7684-7691.
66. Scarlett U.K., Cubillos-Ruiz J.R., Nesbeth Y.C., Martinez D.G., Engle X., Gewirtz A.T., Ahonen C.L., Conejo-Garcia J.R. In situ stimulation of CD40 and toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res. 2009, 69:7329-7337.
67. Curiel T.J., Wei S., Dong H., Alvarez X., Cheng P., Mottram P., Krzysiek R., Knutson K.L., Daniel B., Zimmermann M.C., David O., Burow M., Gordon A., Dhurandhar N., Myers L., Berggren R., Hemminki A., Alvarez R.D., Emilie D., Curiel D.T., Chen L., Zou W. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat. Med. 2003, 9:562-567.
68. Watkins S.K., Zhu Z., Riboldi E., Shafer-Weaver K.A., Stagliano K.E., Sklavos M.M., Ambs S., Yagita H., Hurwitz A.A. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer. J Clin Invest 2011, 121:1361-1372.
69. Cheong C., Matos I., Choi J.H., Dandamudi D.B., Shrestha E., Longhi M.P., Jeffrey K.L., Anthony R.M., Kluger C., Nchinda G., Koh H., Rodriguez A., Idoyaga J., Pack M., Velinzon K., Park C.G., Steinman R.M. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 2010, 143:416-429.
70. A. Rivollier, J. He, A. Kole, V. Valatas, B.L. Kelsall, Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon, J Exp Med 209 139-155.
71. Diao J., Mikhailova A., Tang M., Gu H., Zhao J., Cattral M.S. Immunostimulatory conventional dendritic cells evolve into regulatory macrophage-like cells. Blood. 2012, 119:4919-4927.
72. Elia A.R., Cappello P., Puppo M., Fraone T., Vanni C., Eva A., Musso T., Novelli F., Varesio L., Giovarelli M. Human dendritic cells differentiated in hypoxia down-modulate antigen uptake and change their chemokine expression profile. J. Leukoc. Biol. 2008, 84:1472-1482.
73. Sica A., Larghi P., Mancino A., Rubino L., Porta C., Totaro M.G., Rimoldi M., Biswas S.K., Allavena P., Mantovani A. Macrophage polarization in tumour progression. Semin. Cancer Biol. 2008, 18:349-355.
74. Palucka K., Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012, 12:265-277.
75. Herber D.L., Cao W., Nefedova Y., Novitskiy S.V., Nagaraj S., Tyurin V.A., Corzo A., Cho H.I., Celis E., Lennox B., Knight S.C., Padhya T., McCaffrey T.V., McCaffrey J.C., Antonia S., Fishman M., Ferris R.L., Kagan V.E., Gabrilovich D.I. Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med 2010, 16:880-886.
76. Zhang Z., Liu Q., Che Y., Yuan X., Dai L., Zeng B., Jiao G., Zhang Y., Wu X., Yu Y., Yang R. Antigen presentation by dendritic cells in tumors is disrupted by altered metabolism that involves pyruvate kinase M2 and its interaction with SOCS3. Cancer Res 2010, 70:89-98.
77. Christofk H.R., Vander Heiden M.G., Harris M.H., Ramanathan A., Gerszten R.E., Wei R., Fleming M.D., Schreiber S.L., Cantley L.C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233.
78. S. Grebhardt, C. Veltkamp, P. Strobel, D. Mayer, Hypoxia and HIF-1 increase S100A8 and S100A9 expression in prostate cancer, Int J Cancer (2012). http://dx.doi.org/10.1002/ijc.27591.
79. Ricciardi A., Elia A.R., Cappello P., Puppo M., Vanni C., Fardin P., Eva A., Munroe D., Wu X., Giovarelli M., Varesio L. Transcriptome of hypoxic immature dendritic cells: modulation of chemokine/receptor expression. Mol. Cancer Res. 2008, 6:175-185.
80. Cubillos-Ruiz J.R., Baird J.R., Tesone A.J., Rutkowski M.R., Scarlett U.K., Camposeco-Jacobs A.L., Anadon-Arnillas J., Harwood N.M., Korc M., Fiering S.N., Sempere L.F., Conejo-Garcia J.R. Reprogramming tumor-associated dendritic cells in vivo using microRNA mimetics triggers protective immunity against ovarian cancer. Cancer Res. 2012, 72:1683-1693.