Molecular Profiling Reveals a Tumor-Promoting Phenotype of Monocytes and Macrophages in Human Cancer Progression

Immunity

Volumn 41, Issue 5, 2014, Pages 815-829

  Chittezhath, Manesh ^a   Dhillon, Manprit Kaur ^a   Lim, Jyue Yuan ^a   Laoui, Damya ^b,c   Shalova, Irina N ^a   Teo, Yi Ling ^a   Chen, Jinmiao ^a   Kamaraj, Revathy ^d   Raman, Lata ^d   Lum, Josephine ^a   Thamboo, Thomas Paulraj ^d   Chiong, Edmund ^d   Zolezzi, Francesca ^a   Yang, Henry ^a   VanGinderachter, Jo A ^b,c   Poidinger, Michael ^a   Wong, Alvin S C ^d   Biswas, Subhra K ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN DELTA; I KAPPA B; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; RANTES; TUMOR NECROSIS FACTOR; CYTOKINE; IL1B PROTEIN, HUMAN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MYD88 PROTEIN, HUMAN; MYELOID DIFFERENTIATION FACTOR 88; RELA PROTEIN, HUMAN; TRANSCRIPTION FACTOR RELA;

ARTICLE; CANCER GROWTH; CANCER STAGING; CELL DISRUPTION; CLINICAL ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE ONTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CARCINOMA; MACROPHAGE; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CANCER TRANSPLANTATION; CELL PROLIFERATION; GENETICS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); SCID MOUSE; TUMOR CELL CULTURE; XENOGRAFT;

ANIMALS; CARCINOMA, RENAL CELL; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION PROFILING; HUMANS; INFLAMMATION; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, KNOCKOUT; MICE, SCID; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, INTERLEUKIN-1; TRANSCRIPTION FACTOR RELA; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84912096268     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.09.014     Document Type: Article

References (53)

1. Andreu P., Johansson M., Affara N.I., Pucci F., Tan T., Junankar S., Korets L., Lam J., Tawfik D., DeNardo D.G., et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010, 17:121-134.
2. Balkwill F. Tumour necrosis factor and cancer. Nat. Rev. Cancer 2009, 9:361-371.
3. Bingle L., Brown N.J., Lewis C.E. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 2002, 196:254-265.
4. Biswas S.K., Lewis C.E. NF-κB as a central regulator of macrophage function in tumors. J.Leukoc. Biol. 2010, 88:877-884.
5. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
6. Biswas S.K., Sica A., Lewis C.E. Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms. J.Immunol. 2008, 180:2011-2017.
7. Burt B.M., Rodig S.J., Tilleman T.R., Elbardissi A.W., Bueno R., Sugarbaker D.J. Circulating and tumor-infiltrating myeloid cells predict survival in human pleural mesothelioma. Cancer 2011, 117:5234-5244.
8. Carmi Y., Voronov E., Dotan S., Lahat N., Rahat M.A., Fogel M., Huszar M., White M.R., Dinarello C.A., Apte R.N. The role of macrophage-derived IL-1 in induction and maintenance of angiogenesis. J.Immunol. 2009, 183:4705-4714.
9. Caso R., Silvera R., Carrio R., Iragavarapu-Charyulu V., Gonzalez-Perez R.R., Torroella-Kouri M. Blood monocytes from mammary tumor-bearing mice: early targets of tumor-induced immune suppression?. Int. J. Oncol. 2010, 37:891-900.
10. Cataisson C., Salcedo R., Hakim S., Moffitt B.A., Wright L., Yi M., Stephens R., Dai R.M., Lyakh L., Schenten D., et al. IL-1R-MyD88 signaling in keratinocyte transformation and carcinogenesis. J.Exp. Med. 2012, 209:1689-1702.
11. Cavnar M.J., Zeng S., Kim T.S., Sorenson E.C., Ocuin L.M., Balachandran V.P., Seifert A.M., Greer J.B., Popow R., Crawley M.H., et al. KIT oncogene inhibition drives intratumoral macrophage M2 polarization. J.Exp. Med. 2013, 210:2873-2886.
12. Chow W.H., Dong L.M., Devesa S.S. Epidemiology and risk factors for kidney cancer. Nat. Rev. Urol. 2010, 7:245-257.
13. Chuang M.J., Sun K.H., Tang S.J., Deng M.W., Wu Y.H., Sung J.S., Cha T.L., Sun G.H. Tumor-derived tumor necrosis factor-alpha promotes progression and epithelial-mesenchymal transition in renal cell carcinoma cells. Cancer Sci. 2008, 99:905-913.
14. Coussens L.M., Tinkle C.L., Hanahan D., Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000, 103:481-490.
15. Coussens L.M., Zitvogel L., Palucka A.K. Neutralizing tumor-promoting chronic inflammation: a magic bullet?. Science 2013, 339:286-291.
16. DeNardo D.G., Brennan D.J., Rexhepaj E., Ruffell B., Shiao S.L., Madden S.F., Gallagher W.M., Wadhwani N., Keil S.D., Junaid S.A., et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 2011, 1:54-67.
17. Dosquet C., Schaetz A., Faucher C., Lepage E., Wautier J.L., Richard F., Cabane J. Tumour necrosis factor-alpha, interleukin-1 beta and interleukin-6 in patients with renal cell carcinoma. Eur. J. Cancer 1994, 30A:162-167.
18. Erez N., Truitt M., Olson P., Arron S.T., Hanahan D. Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-kappaB-Dependent Manner. Cancer Cell 2010, 17:135-147.
19. Franklin R.A., Liao W., Sarkar A., Kim M.V., Bivona M.R., Liu K., Pamer E.G., Li M.O. The cellular and molecular origin of tumor-associated macrophages. Science 2014, 344:921-925.
20. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
21. Gautier E.L., Shay T., Miller J., Greter M., Jakubzick C., Ivanov S., Helft J., Chow A., Elpek K.G., Gordonov S., et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 2012, 13:1118-1128. Immunological Genome Consortium.
22. Granowitz E.V., Clark B.D., Vannier E., Callahan M.V., Dinarello C.A. Effect of interleukin-1 (IL-1) blockade on cytokine synthesis: I. IL-1 receptor antagonist inhibits IL-1-induced cytokine synthesis and blocks the binding of IL-1 to its type II receptor on human monocytes. Blood 1992, 79:2356-2363.
23. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
24. Hagemann T., Lawrence T., McNeish I., Charles K.A., Kulbe H., Thompson R.G., Robinson S.C., Balkwill F.R. "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J.Exp. Med. 2008, 205:1261-1268.
25. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
26. Howlader N., Noone A.M., Krapcho M., Neyman N., Aminou R., Waldron W., Altekruse S.F., Kosary C.L., Ruhl J., Tatalovich Z., et al. SEER Cancer Statistics Review, 1975-2008 2000, National Cancer Institute, Bethesda, MD.
27. Karin M., Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 2005, 5:749-759.
28. Komohara Y., Hasita H., Ohnishi K., Fujiwara Y., Suzu S., Eto M., Takeya M. Macrophage infiltration and its prognostic relevance in clear cell renal cell carcinoma. Cancer Sci. 2011, 102:1424-1431.
29. Koo A.S., Armstrong C., Bochner B., Shimabukuro T., Tso C.L., deKernion J.B., Belldegrum A. Interleukin-6 and renal cell cancer: production, regulation, and growth effects. Cancer Immunol. Immunother. 1992, 35:97-105.
30. Koul H., Huh J.S., Rove K.O., Crompton L., Koul S., Meacham R.B., Kim F.J. Molecular aspects of renal cell carcinoma: a review. Am. J. Cancer Res. 2011, 1:240-254.
31. Krelin Y., Voronov E., Dotan S., Elkabets M., Reich E., Fogel M., Huszar M., Iwakura Y., Segal S., Dinarello C.A., Apte R.N. Interleukin-1beta-driven inflammation promotes the development and invasiveness of chemical carcinogen-induced tumors. Cancer Res. 2007, 67:1062-1071.
32. Kuang D.M., Zhao Q., Peng C., Xu J., Zhang J.P., Wu C., Zheng L. Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J.Exp. Med. 2009, 206:1327-1337.
33. Lewis C.E., Pollard J.W. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006, 66:605-612.
34. Lin E.Y., Pollard J.W. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res. 2007, 67:5064-5066.
35. Lin E.Y., Li J.F., Gnatovskiy L., Deng Y., Zhu L., Grzesik D.A., Qian H., Xue X.N., Pollard J.W. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006, 66:11238-11246.
36. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
37. Martinez F.O., Gordon S., Locati M., Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J.Immunol. 2006, 177:7303-7311.
38. Martinez F.O., Helming L., Milde R., Varin A., Melgert B.N., Draijer C., Thomas B., Fabbri M., Crawshaw A., Ho L.P., et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood 2013, 121:e57-e69.
39. Motzer R.J., Hudes G.R., Curti B.D., McDermott D.F., Escudier B.J., Negrier S., Duclos B., Moore L., O'Toole T., Boni J.P., Dutcher J.P. Phase I/II trial of temsirolimus combined with interferon alfa for advanced renal cell carcinoma. J.Clin. Oncol. 2007, 25:3958-3964.
40. Motzer R.J., Michaelson M.D., Rosenberg J., Bukowski R.M., Curti B.D., George D.J., Hudes G.R., Redman B.G., Margolin K.A., Wilding G. Sunitinib efficacy against advanced renal cell carcinoma. J.Urol. 2007, 178:1883-1887.
41. Movahedi K., Laoui D., Gysemans C., Baeten M., Stangé G., Van den Bossche J., Mack M., Pipeleers D., In't Veld P., De Baetselier P., Van Ginderachter J.A. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010, 70:5728-5739.
42. Murdoch C., Muthana M., Coffelt S.B., Lewis C.E. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 2008, 8:618-631.
43. Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., Gordon S., Hamilton J.A., Ivashkiv L.B., Lawrence T., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014, 41:14-20.
44. Noy R., Pollard J.W. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014, 41:49-61.
45. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
46. Rakoff-Nahoum S., Medzhitov R. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 2007, 317:124-127.
47. Rhodes D.R., Yu J., Shanker K., Deshpande N., Varambally R., Ghosh D., Barrette T., Pandey A., Chinnaiyan A.M. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004, 6:1-6.
48. Steidl C., Lee T., Shah S.P., Farinha P., Han G., Nayar T., Delaney A., Jones S.J., Iqbal J., Weisenburger D.D., et al. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N.Engl. J. Med. 2010, 362:875-885.
49. Tu S., Bhagat G., Cui G., Takaishi S., Kurt-Jones E.A., Rickman B., Betz K.S., Penz-Oesterreicher M., Bjorkdahl O., Fox J.G., Wang T.C. Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 2008, 14:408-419.
50. van Rossum A.P., Vlasveld L.T., Vlasveld I.N., Jansen P.M., Dik W.A., Hooijkaas H., Castel A. Granulocytosis and thrombocytosis in renal cell carcinoma: a pro-inflammatory cytokine response originating in the tumour. Neth. J. Med. 2009, 67:191-194.
51. Yang X.J., Tan M.H., Kim H.L., Ditlev J.A., Betten M.W., Png C.E., Kort E.J., Futami K., Furge K.A., Takahashi M., et al. A molecular classification of papillary renal cell carcinoma. Cancer Res. 2005, 65:5628-5637.
52. Yoshida N., Ikemoto S., Narita K., Sugimura K., Wada S., Yasumoto R., Kishimoto T., Nakatani T. Interleukin-6, tumour necrosis factor alpha and interleukin-1beta in patients with renal cell carcinoma. Br. J. Cancer 2002, 86:1396-1400.
53. Zhang Q.W., Liu L., Gong C.Y., Shi H.S., Zeng Y.H., Wang X.Z., Zhao Y.W., Wei Y.Q. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS ONE 2012, 7:e50946.