CCL2/CCR2 regulates the tumor microenvironment in HER-2/neu-driven mammary carcinomas in mice

PLoS ONE

Volumn 11, Issue 11, 2016, Pages

  Chen, Xuguang ^a,b   Wang, Yunyue ^a,b   Nelson, David ^a   Tian, Sara ^a   Mulvey, Erin ^a   Patel, Bhumi ^a   Conti, Ilaria ^a,d   Jaen, Juan ^c,e   Rollins, Barrett J ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c ChemoCentryx Inc   (United States)

^d ELI LILLY AND COMPANY   (United States)

^e Arcus Biosciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR2 ANTAGONIST; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MONOCYTE CHEMOTACTIC PROTEIN 1; CCL2 PROTEIN, MOUSE; ERBB2 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; FEMALE; GENE DISRUPTION; GENE EXPRESSION; GROWTH RATE; HUMAN; HUMAN CELL; MONOCYTE; MOUSE; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION; STEM CELL MOBILIZATION; SURVIVAL RATE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; DEFICIENCY; EXPERIMENTAL MAMMARY NEOPLASM; GENE DELETION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CHEMOKINE CCL2; ENDOTHELIAL PROGENITOR CELLS; FEMALE; GENE DELETION; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; RECEPTOR, ERBB-2; RECEPTORS, CCR2; TUMOR MICROENVIRONMENT;

EID: 84994613953     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0165595     Document Type: Article

References (50)

1. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010; 140(6):883-99. doi: 10.1016/j.cell.2010.01.025 PMID: 20303878
2. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008; 454 (7203):436-44. doi: 10.1038/nature07205 PMID: 18650914
3. Balkwill FR, Capasso M, Hagemann T. The tumor microenvironment at a glance. J Cell Sci. 2012; 125 (Pt 23):5591-6. doi: 10.1242/jcs.116392 PMID: 23420197
4. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010; 11(10):889-96. doi: 10.1038/ni.1937 PMID: 20856220
5. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010; 141(1):39-51. doi: 10.1016/j.cell.2010.03.014 PMID: 20371344
6. Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, et al. The cellular and molecular origin of tumor-associated macrophages. Science. 2014; 344(6186):921-5. doi: 10.1126/science.1252510 PMID: 24812208
7. Allavena P, Germano G, Marchesi F, Mantovani A. Chemokines in cancer related inflammation. Exp Cell Res. 2011; 317(5):664-73. doi: 10.1016/j.yexcr.2010.11.013 PMID: 21134366
8. Balkwill FR. The chemokine system and cancer. J Pathol. 2012; 226(2):148-57. doi: 10.1002/path. 3029 PMID: 21989643
9. Lazennec G, Richmond A. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med. 2010; 16(3):133-44. doi: 10.1016/j.molmed.2010.01.003 PMID: 20163989
10. Matsushima K, Larsen CG, DuBois GC, Oppenheim JJ. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J Exp Med. 1989; 169:1485-90. PMID: 2926331
11. Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med. 1989; 169(4):1449-59. PMID: 2926329
12. Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, et al. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood. 2000; 96(1):34-40. PMID: 10891427
13. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell. 1998; 2(2):275-81. PMID: 9734366
14. Haringman JJ, Gerlag DM, Smeets TJ, Baeten D, van den Bosch F, Bresnihan B, et al. A randomized controlled trial with an anti-CCL2 (anti-monocyte chemotactic protein 1) monoclonal antibody in patients with rheumatoid arthritis. Arthritis Rheum. 2006; 54(8):2387-92. doi: 10.1002/art.21975 PMID: 16869001
15. Negus RP, Stamp GW, Relf MG, Burke F, Malik ST, Bernasconi S, et al. The detection and localization of monocyte chemoattractant protein-1 (MCP-1) in human ovarian cancer. J Clin Invest. 1995; 95 (5):2391-6. doi: 10.1172/JCI117933 PMID: 7738202
16. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011; 475(7355):222-5. doi: 10.1038/nature10138 PMID: 21654748
17. Saji H, Koike M, Yamori T, Saji S, Seiki M, Matsushima K, et al. Significant correlation of monocyte chemoattractant protein-1 expression with neovascularization and progression of breast carcinoma. Cancer. 2001; 92(5):1085-91. PMID: 11571719
18. Ueno T, Toi M, Saji H, Muta M, Bando H, Kuroi K, et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res. 2000; 6(8):3282-9. PMID: 10955814
19. Zhang J, Lu Y, Pienta KJ. Multiple roles of chemokine (C-C motif) ligand 2 in promoting prostate cancer growth. J Natl Cancer Inst. 2010; 102(8):522-8. doi: 10.1093/jnci/djq044 PMID: 20233997
20. Svensson S, Abrahamsson A, Vazquez Rodriguez G, Olsson AK, Jensen L, Cao Y, et al. CCL2 and CCL5 are novel therapeutic targets for estrogen-dependent breast cancer. Clin Cancer Res. 2015.
21. Goede V, Brogelli L, Ziche M, Augustin HG. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int J Cancer. 1999; 82(5):765-70. PMID: 10417778
22. Hong KH, Ryu J, Han KH. Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood. 2005; 105(4):1405-7. doi: 10.1182/blood-2004-08-3178 PMID: 15498848
23. Dwyer RM, Potter-Beirne SM, Harrington KA, Lowery AJ, Hennessy E, Murphy JM, et al. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res. 2007; 13(17):5020-7. doi: 10.1158/1078-0432.CCR-07-0731 PMID: 17785552
24. Kitamura T, Qian BZ, Soong D, Cassetta L, Noy R, Sugano G, et al. CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J Exp Med. 2015; 212(7):1043-59. doi: 10.1084/jem.20141836 PMID: 26056232
25. Huang S, Singh RK, Xie K, Gutman M, Berry KK, Bucana CD, et al. Expression of the JE/MCP-1 gene suppresses metastatic potential in murine colon carcinoma cells. Cancer Immunol Immunother. 1994; 39:231-8. PMID: 7954525
26. Charo IF, Myers SJ, Herman A, Franci C, Connolly AJ, Coughlin SR. Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails. Proc Natl Acad Sci USA. 1994; 91:2752-6. PMID: 8146186
27. Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV Jr., Broxmeyer HE, et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest. 1997; 100(10):2552-61. doi: 10.1172/JCI119798 PMID: 9366570
28. Gosling J, Slaymaker S, Gu L, Tseng S, Zlot CH, Young SG, et al. MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J Clin Invest. 1999; 103 (6):773-8. doi: 10.1172/JCI5624 PMID: 10079097
29. Lu B, Rutledge BJ, Gu L, Fiorillo J, Lukacs NW, Kunkel SL, et al. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med. 1998; 187(4):601-8. PMID: 9463410
30. Gu L, Tseng S, Horner RM, Tam C, Loda M, Rollins BJ. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature. 2000; 404(6776):407-11. doi: 10.1038/35006097 PMID: 10746730
31. Muller WJ, Sinn E, Pattengale E, Wallace R, Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell. 1988; 54:105-15. PMID: 2898299
32. Mack M, Cihak J, Simonis C, Luckow B, Proudfoot AE, Plachy J, et al. Expression and characterization of the chemokine receptors CCR2 and CCR5 in mice. J Immunol. 2001; 166(7):4697-704. PMID: 11254730
33. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005; 5(12):953-64. doi: 10.1038/nri1733 PMID: 16322748
34. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009; 325 (5940):612-6. doi: 10.1126/science.1175202 PMID: 19644120
35. Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol. 2006; 7(3):311-7. doi: 10.1038/ni1309 PMID: 16462739
36. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science. 2008; 319(5860):195-8. doi: 10.1126/science.1150224 PMID: 18187653
37. Spring H, Schuler T, Arnold B, Hammerling GJ, Ganss R. Chemokines direct endothelial progenitors into tumor neovessels. Proc Natl Acad Sci U S A. 2005; 102(50):18111-6. doi: 10.1073/pnas. 0507158102 PMID: 16326806
38. Owens MA, Horten BC, Da Silva MM. HER2 amplification ratios by fluorescence in situ hybridization and correlation with immunohistochemistry in a cohort of 6556 breast cancer tissues. Clin Breast Cancer. 2004; 5(1):63-9. PMID: 15140287
39. Fang WB, Jokar I, Zou A, Lambert D, Dendukuri P, Cheng N. CCL2/CCR2 chemokine signaling coordinates survival and motility of breast cancer cells through Smad3 protein- and p42/44 mitogen-activated protein kinase (MAPK)-dependent mechanisms. J Biol Chem. 2012; 287(43):36593-608. doi: 10.1074/jbc.M112.365999 PMID: 22927430
40. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol. 2003; 163(5):2113-26. doi: 10.1016/S0002-9440(10)63568-7 PMID: 14578209
41. Takahashi M, Miyazaki H, Furihata M, Sakai H, Konakahara T, Watanabe M, et al. Chemokine CCL2/MCP-1 negatively regulates metastasis in a highly bone marrow-metastatic mouse breast cancer model. Clin Exp Metastasis. 2009; 26(7):817-28. doi: 10.1007/s10585-009-9281-8 PMID: 19629725
42. Gazzaniga S, Bravo AI, Guglielmotti A, van Rooijen N, Maschi F, Vecchi A, et al. Targeting tumorassociated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft. J Invest Dermatol. 2007; 127(8):2031-41. doi: 10.1038/sj.jid.5700827 PMID: 17460736
43. Roca H, Varsos ZS, Sud S, Craig MJ, Ying C, Pienta KJ. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem. 2009; 284(49):34342-54. doi: 10.1074/jbc.M109.042671 PMID: 19833726
44. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med. 2001; 193(6):713-26. PMID: 11257138
45. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ. CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med. 2000; 192(6):899-905. PMID: 10993920
46. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med. 2000; 192(7):1075-80. PMID: 11015448
47. Takahashi M, Galligan C, Tessarollo L, Yoshimura T. Monocyte chemoattractant protein-1 (MCP-1), not MCP-3, is the primary chemokine required for monocyte recruitment in mouse peritonitis induced with thioglycollate or zymosan A. J Immunol. 2009; 183(5):3463-71. doi: 10.4049/jimmunol.0802812 PMID: 19641140
48. Li M, Knight DA, L AS, Smyth MJ, Stewart TJ. A role for CCL2 in both tumor progression and immunosurveillance. Oncoimmunology. 2013; 2(7):e25474. doi: 10.4161/onci.25474 PMID: 24073384
49. Jia T, Serbina NV, Brandl K, Zhong MX, Leiner IM, Charo IF, et al. Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J Immunol. 2008; 180(10):6846-53. PMID: 18453605
50. Bose R, Kavuri SM, Searleman AC, Shen W, Shen D, Koboldt DC, et al. Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov. 2013; 3(2):224-37. doi: 10.1158/2159-8290.CD-12-0349 PMID: 23220880