Loss of monocyte chemoattractant protein-1 expression delays mammary tumorigenesis and reduces localized inflammation in the C3(1)/SV40Tag triple negative breast cancer model

References

• Group, U.S Cancer Statistics Working. United States Cancer Statistics: 1999–2012 Incidence and Mortality Web-based Report 2015, Department of Health and Human Services, Centers for Disease Control and Prevention, and National Cancer Institute; http://dx.doi.org/10.1517/14656566.2015.1102226
   Google Scholar
• Society, American Cancer. Learn about cancer: Breast Cancer. What are the key statistics about breast cancer? 2016 05/04/2016 [cited 2016 06/30]; Available from: http://www.cancer.org/cancer/breastcancer/detailedguide/breast-cancer-key-statistics
   Google Scholar
• Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 2003; 100(14):8418-23; PMID:12829800; http://dx.doi.org/10.1200/JCO.2014.58.022510.1073/pnas.0932692100
   PubMed Web of Science ®Google Scholar
• Haffty BG, Yang Q, Reiss M, Kearney T, Higgins SA, Weidhaas J, Harris L, Hait W, Toppmeyer D. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol 2006; 24(36):5652-7; PMID:17116942; http://dx.doi.org/10.1158/0008-5472.CAN-11-277810.1200/JCO.2006.06.5664
   PubMed Web of Science ®Google Scholar
• Dolle JM, Daling JR, White E, Brinton LA, Doody DR, PorterL, Malone KE. Risk factors for triple-negative breast cancer in women under the age of 45 years. Cancer Epidemiol Biomarkers Prev 2009; 18(4):1157-66; PMID:19336554; http://dx.doi.org/10.18632/oncotarget.250510.1158/1055-9965.EPI-08-1005
   PubMed Web of Science ®Google Scholar
• Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007; 13(15 Pt 1):4429-34; PMID:17671126; http://dx.doi.org/10.1158/2326-6066.CIR-13-022410.1158/1078-0432.CCR-06-3045
   PubMed Web of Science ®Google Scholar
• Harris LN, Broadwater G, Lin NU, Miron A, Schnitt SJ, Cowan D, Lara J, Bleiweiss I, Berry D, Ellis M, et al. Molecular subtypes of breast cancer in relation to paclitaxel response and outcomes in women with metastatic disease: results from CALGB 9342. Breast Cancer Res 2006; 8(6):R66; PMID:17129383; http://dx.doi.org/10.1186/bcr1622
   PubMed Web of Science ®Google Scholar
• Badve S, Dabbs DJ, Schnitt SJ, Baehner FL, Decker T, Eusebi V, Fox SB, Ichihara S, Jacquemier J, Lakhani SR, et al. Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod Pathol 2011; 24(2):157-67; PMID:21076464; http://dx.doi.org/10.1186/s40425-015-0067-z10.1038/modpathol.2010.200
   PubMed Web of Science ®Google Scholar
• Tischkowitz M, Brunet JS, Begin LR, Huntsman DG, Cheang MC, Akslen LA, Nielsen TO, Foulkes WD. Use of immunohistochemical markers can refine prognosis i triple negative breast cancer. BMC Cancer 2007; 7:134; PMID:17650314; http://dx.doi.org/10.1016/S1471-4906(03)00132-710.1186/1471-2407-7-134
   PubMed Web of Science ®Google Scholar
• Rodler E, Korde L, Gralow J. Current treatment options in triple negative breast cancer. Breast Dis 2010; 32(1-2):99-122; PMID:21778572; http://dx.doi.org/10.1084/jem.2004202810.3233/BD-2010-0304
   PubMedGoogle Scholar
• Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 2009; 29(6):313-26; PMID:19441883; http://dx.doi.org/10.1038/onc.2016.3710.1089/jir.2008.0027
   PubMed Web of Science ®Google Scholar
• Ohta M, Kitadai Y, Tanaka S, Yoshihara M, Yasui W, Mukaida N, Haruma K, Chayama K. Monocyte chemoattractant protein-1 expression correlates with macrophage infiltration and tumor vascularity in human gastric carcinomas. Int J Oncol 2003; 22(4):773-8; PMID:12632067; http://dx.doi.org/10.1016/j.cell.2015.08.016
   PubMed Web of Science ®Google Scholar
• Ueno T, Toi M, Saji H, Muta M, Bando H, Kuroi K, Koike M, Inadera H, Matsushima K. 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; http://dx.doi.org/10.1182/blood-2006-06-031856
   PubMed Web of Science ®Google Scholar
• 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; PMID:22927430; http://dx.doi.org/10.1074/jbc.M11067520010.1074/jbc.M112.365999
   PubMed Web of Science ®Google Scholar
• Fang WB, Yao M, Brummer G, Acevedo D, Alhakamy N, Berkland C, Cheng N. Targeted gene silencing of CCL2 inhibits triple negative breast cancer progression by blocking cancer stem cell renewal and M2 macrophage recruitment. Oncotarget 2016; 7(31): 49349-67; PMID:27283985; http://dx.doi.org/10.18632/oncotarget.9885
   Web of Science ®Google Scholar
• Bennett CN, Green JE. Genomic analyses as a guide to target identification and preclinical testing of mouse models of breast cancer. Toxicol Pathol 2010; 38(1):88-95; PMID:20080934; http://dx.doi.org/10.1016/j.intimp.2016.03.00210.1177/0192623309357074
   PubMed Web of Science ®Google Scholar
• Maroulakou IG, Anver M, Garrett L, Green JE. Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene. Proc Natl Acad Sci U S A 1994; 91(23):11236-40; PMID:7972041; http://dx.doi.org/10.1038/nrclinonc.2016.3610.1073/pnas.91.23.11236
   PubMed Web of Science ®Google Scholar
• Cranford TL, Enos RT, Velazquez KT, McClellan JL, Davis JM, Singh UP, Nagarkatti M, NagarkattiS, Robinson CM, Murphy EA. Role of MCP-1 on inflammatory processes and metabolic dysfunction following high-fat feedings in the FVB/N strain. Int J Obes (Lond) 2016; 40(5):844-51; PMID:26620890; http://dx.doi.org/10.1158/1078-0432.CCR-14-270810.1038/ijo.2015.244
   PubMed Web of Science ®Google Scholar
• Green JE, Shibata MA, Yoshidome K, Liu ML, Jorcyk C, Anver MR, Wigginton J, Wiltrout R, Shibata E, Kaczmarczyk S, et al. The C3(1)/SV40 T-antigen transgenic mouse model of mammary cancer: ductal epithelial cell targeting with multistage progression to carcinoma. Oncogene 2000; 19(8):1020-7; PMID:10713685; http://dx.doi.org/10.2217/imt-2016-004810.1038/sj.onc.1203280
   PubMed Web of Science ®Google Scholar
• Steiner J, Davis J, McClellan J, Enos R, Carson J, Fayad R, Nagarkatti M, Nagarkatti P, Altomare D, Creek K, et al. Dose-dependent benefits of quercetin on tumorigenesis in the C3(1)/SV40Tag transgenic mouse model of breast cancer. Cancer Biol Ther 2014; 15(11):1456-67; PMID:25482952; http://dx.doi.org/10.1016/j.cell.2015.08.01210.4161/15384047.2014.955444
   PubMed Web of Science ®Google Scholar
• Enos RT, Davis JM, Velazquez KT, McClellan JL, Day SD, Carnevale KA, Murphy EA. Influence of dietary saturated fat content on adiposity, macrophage behavior, inflammation, and metabolism: composition matters. J Lipid Res 2013; 54(1):152-63; PMID:23103474; http://dx.doi.org/10.18632/oncotarget.368210.1194/jlr.M030700
   PubMed Web of Science ®Google Scholar
• Warden CH, Fisler JS. Comparisons of diets used in animal models of high-fat feeding. Cell Metab 2008; 7(4):277; PMID:18396128; http://dx.doi.org/10.1126/scitranslmed.aad711810.1016/j.cmet.2008.03.014
   PubMed Web of Science ®Google Scholar
• Velazquez KT, Enos RT, McClellan JL, Cranford TL, Chatzistamou I, Singh UP, Nagarkatti M, NagarkattiS, Fan D, Murphy EA. MicroRNA-155 deletion promotes tumorigenesis in the azoxymethane-dextran sulfate sodium model of colon cancer. Am J Physiol Gastrointest Liver Physiol 2016; 310(6):G347-58; PMID:26744471; http://dx.doi.org/10.1172/JCI8001110.1152/ajpgi.00326.2015
   PubMedGoogle Scholar
• Enos RT, Velazquez KT, McClellan JL, Cranford TL, Walla MD, Murphy EA. Lowering the dietary omega-6: omega-3 does not hinder nonalcoholic fatty-liver disease development in a murine model. Nutr Res 2015; 35(5):449-59; PMID:25934114; http://dx.doi.org/10.1016/j.nutres.2015.04.003
   PubMed Web of Science ®Google Scholar
• Hoenerhoff MJ, Shibata MA, Bode A, Green JE. Pathologic progression of mammary carcinomas in a C3(1)/SV40 T/t-antigen transgenic rat model of human triple-negative and Her2-positive breast cancer. Transgenic Res 2011; 20(2):247-59; PMID:20549348; http://dx.doi.org/10.1007/s11248-010-9406-5
   PubMed Web of Science ®Google Scholar
• Balkwill FR, Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 2012; 22(1):33-40; PMID:22210179; http://dx.doi.org/10.1016/j.semcancer.2011.12.005
   PubMed Web of Science ®Google Scholar
• Rose DP, GracheckJ, Vona-Davis L. The Interactions of Obesity, Inflammation and Insulin Resistance in Breast Cancer. Cancers (Basel) 2015; 7(4):2147-68; PMID:26516917; http://dx.doi.org/10.3390/cancers7040883
   PubMedGoogle Scholar
• Allavena P, Sica A, Solinas G, Porta C, Mantovani A. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev Oncol Hematol 2008; 66(1):1-9; PMID:17913510; http://dx.doi.org/10.1016/j.critrevonc.2007.07.004
   PubMed Web of Science ®Google Scholar
• Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004; 4(7):540-50; PMID:15229479; http://dx.doi.org/10.1038/nrc1388
   PubMed Web of Science ®Google Scholar
• Bailey C, Negus R, Morris A, Ziprin P, Goldin R, Allavena P, Peck D, Darzi A. Chemokine expression is associated with the accumulation of tumour associated macrophages (TAMs) and progression in human colorectal cancer. Clin Exp Metastasis 2007; 24(2):121-30; PMID:17390111; http://dx.doi.org/10.1007/s10585-007-9060-3
   PubMed Web of Science ®Google Scholar
• McClellan JL, Davis JM, Steiner JL, Enos RT, Jung SH, Carson JA, Pena MM, Carnevale KA, Berger FG, Murphy EA. Linking tumor-associated macrophages, inflammation, and intestinal tumorigenesis: role of MCP-1. Am J Physiol Gastrointest Liver Physiol 2012; 303(10):G1087-95; PMID:23019193; http://dx.doi.org/10.1152/ajpgi.00252.2012
   PubMedGoogle Scholar
• Fridlender ZG, Buchlis G, Kapoor V, Cheng G, Sun J, Singhal S, Crisanti MC, Wang LC, Heitjan D, Snyder LA, et al. CCL2 blockade augments cancer immunotherapy. Cancer Res 2010; 70(1):109-18; PMID:20028856; http://dx.doi.org/10.1158/0008-5472.CAN-09-2326
   PubMed Web of Science ®Google Scholar
• Valkovic T, Lucin K, Krstulja M, Dobi-Babic R, Jonjic N. Expression of monocyte chemotactic protein-1 in human invasive ductal breast cancer. Pathol Res Pract 1998; 194(5):335-40; PMID:9651946; http://dx.doi.org/10.1016/S0344-0338(98)80057-5
   PubMed Web of Science ®Google Scholar
• Soria G, Yaal-Hahoshen N, Azenshtein E, Shina S, Leider-Trejo L, Ryvo L, Cohen-Hillel E, Shtabsky A, Ehrlich M, Meshel T, et al. Concomitant expression of the chemokines RANTES and MCP-1 in human breast cancer: a basis for tumor-promoting interactions. Cytokine 2008; 44(1):191-200; PMID:18790652; http://dx.doi.org/10.1016/j.cyto.2008.08.002
   PubMed Web of Science ®Google Scholar
• Yao M, Yu E, Staggs V, Fan F, Cheng N. Elevated expression of chemokine C-C ligand 2 in stroma is associated with recurrent basal-like breast cancers. Mod Pathol 2016; 29(8):810-23; PMID:27125354; http://dx.doi.org/10.1038/modpathol.2016.78
   PubMed Web of Science ®Google Scholar
• Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA, Pollard JW. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011; 475(7355):222-5; PMID:21654748; http://dx.doi.org/10.1038/nature10138
   PubMed Web of Science ®Google Scholar
• Hollmen M, Roudnicky F, Karaman S, Detmar M. Characterization of macrophage–cancer cell crosstalk in estrogen receptor positive and triple-negative breast cancer. Sci Rep 2015; 5:9188; PMID:25776849; http://dx.doi.org/10.1038/srep09188
   PubMed Web of Science ®Google Scholar
• Su S, Liu Q, Chen J, Chen J, Chen F, He C, Huang D, Wu W, Lin L, Huang W, et al. A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell 2014; 25(5):605-20; PMID:24823638; http://dx.doi.org/10.1016/j.ccr.2014.03.021
   PubMed Web of Science ®Google Scholar
• Patsialou A, Wyckoff J, Wang Y, Goswami S, Stanley ER, Condeelis JS. Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor. Cancer Res 2009; 69(24):9498-506; PMID:19934330; http://dx.doi.org/10.1158/0008-5472.CAN-09-1868
   PubMed Web of Science ®Google Scholar
• Soria G, Ben-Baruch A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett 2008; 267(2):271-85; PMID:18439751; http://dx.doi.org/10.1016/j.canlet.2008.03.018
   PubMed Web of Science ®Google Scholar
• Steiner JL, Davis JM, McClellan JL, Guglielmotti A, Murphy EA. Effects of the MCP-1 synthesis inhibitor bindarit on tumorigenesis and inflammatory markers in the C3(1)/SV40Tag mouse model of breast cancer. Cytokine 2014; 66(1):60-8; PMID:24548426; http://dx.doi.org/10.1016/j.cyto.2013.12.011
   PubMed Web of Science ®Google Scholar
• Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454(7203):436-44; PMID:18650914; http://dx.doi.org/10.1038/nature07205
   PubMed Web of Science ®Google Scholar
• Solinas G, Germano G, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 2009; 86(5):1065-73; PMID:19741157; http://dx.doi.org/10.1189/jlb.0609385
   PubMed Web of Science ®Google Scholar
• Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG, 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(11):1118-28; PMID:23023392; http://dx.doi.org/10.1038/ni.2419
   PubMed Web of Science ®Google Scholar
• Nguyen KQ, Tsou WI, Calarese DA, Kimani SG, Singh S, Hsieh S, Liu Y, Lu B, Wu Y, Garforth SJ, et al. Overexpression of MERTK receptor tyrosine kinase in epithelial cancer cells drives efferocytosis in a gain-of-function capacity. J Biol Chem 2014; 289(37):25737-49; PMID:25074939; http://dx.doi.org/10.1074/jbc.M114.570838
   PubMed Web of Science ®Google Scholar
• Knupfer H, Preiss R. Significance of interleukin-6 (IL-6) in breast cancer (review). Breast Cancer Res Treat 2007; 102(2):129-35; PMID:16927176; http://dx.doi.org/10.1007/s10549-006-9328-3
   PubMed Web of Science ®Google Scholar
• Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, Huget P, Dirix LY. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer 2003; 103(5):642-6; PMID:12494472; http://dx.doi.org/10.1002/ijc.10833
   PubMed Web of Science ®Google Scholar