Polarization of macrophages in the tumor microenvironment is influenced by EGFR signaling within colon cancer cells

Oncotarget

Volumn 7, Issue 46, 2016, Pages 75366-75378

  Zhang, Weina ^a   Chen, Lechuang ^a   Ma, Kai ^a   Zhao, Yahui ^a   Liu, Xianghe ^a   Wang, Yu ^a   Liu, Mei ^a   Liang, Shufang ^b   Zhu, Hongxia ^a   Xu, Ningzhi ^a,b  

^a CANCER HOSPITAL   (China)

^b SICHUAN UNIVERSITY   (China)

Author keywords

Colon cancer; EGFR; IGF 1; TAM; Tumor microenvironment

Indexed keywords

ARGINASE 1; CHEMOKINE RECEPTOR CCR7; EPIDERMAL GROWTH FACTOR RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; MACROPHAGE DERIVED CHEMOKINE; SOMATOMEDIN C; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TUMOR NECROSIS FACTOR; CETUXIMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL POLARITY; COLON CANCER; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; ANIMAL; COLON TUMOR; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; GENE KNOCKOUT; GENETICS; IMMUNOLOGY; MACROPHAGE ACTIVATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CETUXIMAB; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; GENE KNOCKOUT TECHNIQUES; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84996843174     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12207     Document Type: Article

References (63)

1. Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ and He J. Cancer statistics in China, 2015. CA: a cancer journal for clinicians. 2016.
2. Rustgi AK. The genetics of hereditary colon cancer. Genes & development. 2007; 21:2525-2538.
3. Cannon J. Colorectal Neoplasia and Inflammatory Bowel Disease. The Surgical clinics of North America. 2015; 95:1261-1269.
4. Markowitz SD, Dawson DM, Willis J and Willson JK. Focus on colon cancer. Cancer cell. 2002; 1:233-236.
5. Klemm F and Joyce JA. Microenvironmental regulation of therapeutic response in cancer. Trends in cell biology. 2015; 25:198-213.
6. Johansson A, Hamzah J and Ganss R. License for destruction: tumor-specific cytokine targeting. Trends in molecular medicine. 2014; 20:16-24.
7. De Palma M and Lewis CE. Macrophage regulation of tumor responses to anticancer therapies. Cancer cell. 2013; 23:277-286.
8. Mantovani A, Bottazzi B, Colotta F, Sozzani S and Ruco L. The origin and function of tumor-associated macrophages. Immunology today. 1992; 13:265-270.
9. Qian BZ and Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010; 141:39-51.
10. Mantovani A and Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Current opinion in immunology. 2010; 22:231-237.
11. Geissmann F, Gordon S, Hume DA, Mowat AM and Randolph GJ. Unravelling mononuclear phagocyte heterogeneity. Nature reviews Immunology. 2010; 10:453-460.
12. Gordon S and Taylor PR. Monocyte and macrophage heterogeneity. Nature Reviews Immunology. 2005; 5:953-964.
13. Mantovani A, Sozzani S, Locati M, Allavena P and Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends in immunology. 2002; 23:549-555.
14. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA and Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of immunology. 1986; 136:2348-2357.
15. Martinez FO, Helming L and Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annual review of immunology. 2009; 27:451-483.
16. Murray PJ and Wynn TA. Protective and pathogenic functions of macrophage subsets. Nature reviews Immunology. 2011; 11:723-737.
17. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A and Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends in immunology. 2004; 25:677-686.
18. Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG, Rimoldi M, Biswas SK, Allavena P and Mantovani A. Macrophage polarization in tumour progression. Seminars in cancer biology. 2008; 18:349-355.
19. Radinsky R, Risin S, Fan D, Dong Z, Bielenberg D, Bucana CD and Fidler IJ. Level and function of epidermal growth factor receptor predict the metastatic potential of human colon carcinoma cells. Clinical cancer research. 1995; 1:1931.
20. Roberts RB, Min L, Washington MK, Olsen SJ, Settle SH, Coffey RJ and Threadgill DW. Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis. Proceedings of the National Academy of Sciences. 2002; 99:1521-1526.
21. Tong WM, Ellinger A, Sheinin Y and Cross HS. Epidermal growth factor receptor expression in primary cultured human colorectal carcinoma cells. British journal of cancer. 1998; 77:1792-1798.
22. Cohen RB. Epidermal Growth Factor Receptor as a Therapeutic Target in Colorectal Cancer. Clinical Colorectal Cancer. 2003; 2:246-251.
23. Elbaz M, Nasser MW, Ravi J, Wani NA, Ahirwar DK, Zhao H, Oghumu S, Satoskar AR, Shilo K, Carson WE, 3rd and Ganju RK. Modulation of the tumor microenvironment and inhibition of EGF/EGFR pathway: novel anti-tumor mechanisms of Cannabidiol in breast cancer. Molecular oncology. 2015; 9:906-919.
24. Ciardiello F, Caputo R, Bianco R, Damiano V, Fontanini G, Cuccato S, De Placido S, Bianco AR and Tortora G. Inhibition of growth factor production and angiogenesis in human cancer cells by ZD1839 (Iressa), a selective epidermal growth factor receptor tyrosine kinase inhibitor. Clinical cancer research. 2001; 7:1459-1465.
25. Hotz B, Keilholz U, Fusi A, Buhr HJ and Hotz HG. In vitro and in vivo antitumor activity of cetuximab in human gastric cancer cell lines in relation to epidermal growth factor receptor (EGFR) expression and mutational phenotype. Gastric cancer. 2012; 15:252-264.
26. Lu N, Wang L, Cao H, Liu L, Van Kaer L, Washington MK, Rosen MJ, Dube PE, Wilson KT, Ren X, Hao X, Polk DB and Yan F. Activation of the epidermal growth factor receptor in macrophages regulates cytokine production and experimental colitis. Journal of immunology. 2014; 192:1013-1023.
27. Wu Y, Brodt P, Sun H, Mejia W, Novosyadlyy R, Nunez N, Chen X, Mendoza A, Hong SH, Khanna C and Yakar S. Insulin-like growth factor-I regulates the liver microenvironment in obese mice and promotes liver metastasis. Cancer research. 2010; 70:57-67.
28. Salomon DS, Brandt R, Ciardiello F and Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Critical reviews in oncology/hematology. 1995; 19:183-232.
29. Gibson TB, Ranganathan A and Grothey A. Randomized phase III trial results of panitumumab, a fully human anti-epidermal growth factor receptor monoclonal antibody, in metastatic colorectal cancer. Clin Colorectal Cancer. 2006; 6:29-31.
30. Jonker DJ, O'Callaghan CJ, Karapetis CS, Zalcberg JR, Tu D, Au HJ, Berry SR, Krahn M, Price T, Simes RJ, Tebbutt NC, van Hazel G, Wierzbicki R, Langer C and Moore MJ. Cetuximab for the treatment of colorectal cancer. The New England journal of medicine. 2007; 357:2040-2048.
31. Ma X, Wu D, Zhou S, Wan F, Liu H, Xu X, Xu X, Zhao Y and Tang M. The pancreatic cancer secreted REG4 promotes macrophage polarization to M2 through EGFR/AKT/CREB pathway. Oncology reports. 2016; 35:189-196.
32. Mulligan JK, Lathers DM and Young MR. Tumors skew endothelial cells to disrupt NK cell, T-cell and macrophage functions. Cancer immunology, immunotherapy: CII. 2008; 57:951-961.
33. Wang T, Ge Y, Xiao M, Lopez-Coral A, Azuma R, Somasundaram R, Zhang G, Wei Z, Xu X, Rauscher FJ, 3rd, Herlyn M and Kaufman RE. Melanoma-derived conditioned media efficiently induce the differentiation of monocytes to macrophages that display a highly invasive gene signature. Pigment cell & melanoma research. 2012; 25:493-505.
34. Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, Squadrito ML, Segura I, Li X, Knevels E, Costa S, Vinckier S, Dresselaer T, Akerud P, De Mol M, Salomaki H, et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer cell. 2011; 19:31-44.
35. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM, Cline GW, Phillips AJ and Medzhitov R. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 2014; 513:559-563.
36. Chen PC, Cheng HC, Wang J, Wang SW, Tai HC, Lin CW and Tang CH. Prostate cancer-derived CCN3 induces M2 macrophage infiltration and contributes to angiogenesis in prostate cancer microenvironment. Oncotarget. 2014; 5:1595-1608. doi: 10.18632/oncotarget.1570.
37. Pyonteck SM, Gadea BB, Wang HW, Gocheva V, Hunter KE, Tang LH and Joyce JA. Deficiency of the macrophage growth factor CSF-1 disrupts pancreatic neuroendocrine tumor development. Oncogene. 2012; 31:1459-1467.
38. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA and Pollard JW. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011; 475:222-225.
39. Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, Rich JN and Bao S. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nature cell biology. 2015; 17:170-182.
40. Huang CT, Chang MC, Chen YL, Chen TC, Chen CA and Cheng WF. Insulin-like growth factors inhibit dendritic cell-mediated anti-tumor immunity through regulating ERK1/2 phosphorylation and p38 dephosphorylation. Cancer letters. 2015; 359:117-126.
41. Samani AA, Yakar S, LeRoith D and Brodt P. The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocrine reviews. 2007; 28:20-47.
42. Fenton JI, Hord NG, Lavigne JA, Perkins SN and Hursting SD. Leptin, insulin-like growth factor-1, and insulin-like growth factor-2 are mitogens in ApcMin/+ but not Apc+/+ colonic epithelial cell lines. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2005; 14:1646-1652.
43. Singh P, Dai B, Yallampalli U, Lu X and Schroy PC. Proliferation and differentiation of a human colon cancer cell line (CaCo2) is associated with significant changes in the expression and secretion of insulin-like growth factor (IGF) IGF-II and IGF binding protein-4: role of IGF-II. Endocrinology. 1996; 137:1764-1774.
44. Zhang XH, Jin X, Malladi S, Zou Y, Wen YH, Brogi E, Smid M, Foekens JA and Massague J. Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma. Cell. 2013; 154:1060-1073.
45. Sprinzl MF, Puschnik A, Schlitter AM, Schad A, Ackermann K, Esposito I, Lang H, Galle PR, Weinmann A, Heikenwalder M and Protzer U. Sorafenib inhibits macrophage-induced growth of hepatoma cells by interference with insulin-like growth factor-1 secretion. Journal of hepatology. 2015; 62:863-870.
46. Kaburagi Y, Yamauchi T, Yamamoto-Honda R, Ueki K, Tobe K, Akanuma Y, Yazaki Y and Kadowaki T. The mechanism of insulin-induced signal transduction mediated by the insulin receptor substrate family. Endocrine journal. 1999; 46:S25-34.
47. Richards RG, Walker MP, Sebastian J and DiAugustine RP. Insulin-like growth factor-1 (IGF-1) receptor-insulin receptor substrate complexes in the uterus. Altered signaling response to estradiol in the IGF-1(m/m) mouse. The Journal of biological chemistry. 1998; 273:11962-11969.
48. Sun XJ, Miralpeix M, Myers MG, Jr., Glasheen EM, Backer JM, Kahn CR and White MF. Expression and function of IRS-1 in insulin signal transmission. The Journal of biological chemistry. 1992; 267:22662-22672.
49. Shabo I, Olsson H, Sun XF and Svanvik J. Expression of the macrophage antigen CD163 in rectal cancer cells is associated with early local recurrence and reduced survival time. International journal of cancer Journal international du cancer. 2009; 125:1826-1831.
50. Kang JC, Chen JS, Lee CH, Chang JJ and Shieh YS. Intratumoral macrophage counts correlate with tumor progression in colorectal cancer. Journal of surgical oncology. 2010; 102:242-248.
51. Forssell J, Oberg A, Henriksson ML, Stenling R, Jung A and Palmqvist R. High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clinical cancer research. 2007; 13:1472-1479.
52. Lundholm M, Hagglof C, Wikberg ML, Stattin P, Egevad L, Bergh A, Wikstrom P, Palmqvist R and Edin S. Secreted Factors from Colorectal and Prostate Cancer Cells Skew the Immune Response in Opposite Directions. Scientific reports. 2015; 5:15651.
53. Erreni M, Mantovani A and Allavena P. Tumor-associated Macrophages (TAM) and Inflammation in Colorectal Cancer. Cancer microenvironment. 2011; 4:141-154.
54. Hsu SC and Hung MC. Characterization of a novel tripartite nuclear localization sequence in the EGFR family. The Journal of biological chemistry. 2007; 282:10432-10440.
55. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, KagnoffMF and Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004; 118:285-296.
56. Bain CC, Bravo-Blas A, Scott CL, Gomez Perdiguero E, Geissmann F, Henri S, Malissen B, Osborne LC, Artis D and Mowat AM. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nature immunology. 2014; 15:929-937.
57. Zhou C, Liu S, Zhou X, Xue L, Quan L, Lu N, Zhang G, Bai J, Wang Y, Liu Z, Zhan Q, Zhu H and Xu N. Overexpression of human pituitary tumor transforming gene (hPTTG), is regulated by beta-catenin/TCF pathway in human esophageal squamous cell carcinoma. International journal of cancer Journal international du cancer. 2005; 113:891-898.
58. Fujimoto H, Sangai T, Ishii G, Ikehara A, Nagashima T, Miyazaki M and Ochiai A. Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression. International journal of cancer Journal international du cancer. 2009; 125:1276-1284.
59. Kang FB, Wang L, Li D, Zhang YG and Sun DX. Hepatocellular carcinomas promote tumor-associated macrophage M2-polarization via increased B7-H3 expression. Oncology reports. 2015; 33:274-282.
60. Nakanishi Y, Nakatsuji M, Seno H, Ishizu S, Akitake-Kawano R, Kanda K, Ueo T, Komekado H, Kawada M, Minami M and Chiba T. COX-2 inhibition alters the phenotype of tumor-associated macrophages from M2 to M1 in ApcMin/+ mouse polyps. Carcinogenesis. 2011; 32:1333-1339.
61. Wu TH, Li YY, Wu TL, Chang JW, Chou WC, Hsieh LL, Chen JR and Yeh KY. Culture supernatants of different colon cancer cell lines induce specific phenotype switching and functional alteration of THP-1 cells. Cellular immunology. 2014; 290:107-115.
62. Hefetz-Sela S, Stein I, Klieger Y, Porat R, Sade-Feldman M, Zreik F, Nagler A, Pappo O, Quagliata L, Dazert E, Eferl R, Terracciano L, Wagner EF, Ben-Neriah Y, Baniyash M and Pikarsky E. Acquisition of an immunosuppressive protumorigenic macrophage phenotype depending on c-Jun phosphorylation. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111:17582-17587.
63. Ma K, Xu Q, Wang S, Zhang W, Liu M, Liang S, Zhu H and Xu N. Nuclear accumulation of yes-associated protein (YAP) maintains the survival of doxorubicin-induced senescent cells by promoting survivin expression. Cancer letters. 2016.