Perivascular M2 macrophages stimulate tumor relapse after chemotherapy

Cancer Research

Volumn 75, Issue 17, 2015, Pages 3479-3491

  Hughes, Russell ^a   Qian, Bin Zhi ^b   Rowan, Charlotte ^a   Muthana, Munitta ^a   Keklikoglou, Ioanna ^c   Olson, Oakley C ^d   Tazzyman, Simon ^a   Danson, Sarah ^a   Addison, Christina ^e   Clemons, Mark ^e   Gonzalez Angulo, Ana Maria ^f   Joyce, Johanna A ^d   De Palma, Michele ^c   Pollard, Jeffrey W ^b,g   Lewis, Claire E ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c EPFL   (Switzerland)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^g ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; CHEMOKINE RECEPTOR CXCR4; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; FLUOROURACIL; HEME OXYGENASE 1; LECTIN; MANNOSE RECEPTOR C TYPE LECTIN; PACLITAXEL; PAMIDRONIC ACID; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1; TAMOXIFEN; UNCLASSIFIED DRUG; VASCULOTROPIN A; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE METASTASIS; BREAST ADENOCARCINOMA; BREAST CANCER; BREAST CARCINOMA; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RECURRENCE; CASE REPORT; CONTROLLED STUDY; DRUG EFFICACY; DRUG TARGETING; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOREACTIVITY; LEWIS CARCINOMA; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; SINGLE DRUG DOSE; TREATMENT DURATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR HYPOXIA; TUMOR VASCULARIZATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BREAST NEOPLASMS; CARCINOMA, LEWIS LUNG; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MACROPHAGE; METABOLISM; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR RECURRENCE;

ANIMALS; BREAST NEOPLASMS; CARCINOMA, LEWIS LUNG; CHEMOKINE CXCL12; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MACROPHAGES; MICE; NEOPLASM RECURRENCE, LOCAL; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; TAMOXIFEN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84941779973     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3587     Document Type: Article

References (50)

1. Savir G, Huber KE, Saif MW. Locally advanced pancreatic cancer. Looking beyond traditional chemotherapy and radiation. JOP 2013;14: 337-9.
2. Strom HH, Bremnes RM, Sundstrom SH, Helbekkmo N, Aasebo U. Poor prognosis patients with inoperable locally advanced NSCLC and large tumors benefit from palliative chemoradiotherapy: A subset analysis from a randomized clinical phase III trial. J Thorac Oncol 2014;9: 825-33.
3. Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 2010;176: 1564-76.
4. Noy R, Pollard JW. Tumor-Associated Macrophages: From Mechanisms to Therapy. Immunity 2014;41: 49-61.
5. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141: 39-51.
6. Movahedi K, Laoui D, Gysemans C, Baeten M, Stange G, Van den Bossche J, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 2010;70: 5728-39.
7. Coffelt SB, Hughes R, Lewis CE. Tumor-associated macrophages: Effectors of angiogenesis and tumor progression. Biochimica et biophysica acta 2009;1796: 11-8.
8. Biswas SK, Sica A, Lewis CE. Plasticity of macrophage function during tumor progression: Regulation by distinctmolecular mechanisms. J Immunol 2008;180: 2011-7.
9. Pucci F, Venneri MA, Biziato D, Nonis A, Moi D, Sica A, et al. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 2009;114: 901-14.
10. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005;8: 211-26.
11. Daenen LG, Houthuijzen JM, Cirkel GA, Roodhart JM, Shaked Y, Voest EE. Treatment-induced host-mediated mechanisms reducing the efficacy of antitumor therapies. Oncogene 2014;33: 1341-7.
12. De Palma M, Lewis CE. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 2013;23: 277-86.
13. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011;1: 54-67.
14. Nakasone ES, Askautrud HA, Kees T, Park JH, Plaks V, Ewald AJ, et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 2012;21: 488-503.
15. Shree T, Olson OC, Elie BT, Kester JC, Garfall AL, Simpson K, et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 2011;25: 2465-79.
16. Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci U S A 2010;107: 8363-8.
17. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest 2010; 120: 694-705.
18. Kozin SV, Kamoun WS, Huang Y, Dawson MR, Jain RK, Duda DG. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res 2010;70: 5679-85.
19. Welford AF, Biziato D, Coffelt SB, Nucera S, Fisher M, Pucci F, et al. TIE2-expressing macrophages limit the therapeutic efficacy of the vasculardisrupting agent combretastatin A4 phosphate in mice. J Clin Invest 2011; 121: 1969-73.
20. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013;229: 176-85.
21. Browder T, Butterfield CE, Kraling BM, Shi B, Marshall B, O'Reilly MS, et al. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 2000;60: 1878-86.
22. Affara NI, Ruffell B, Medler TR, Gunderson AJ, Johansson M, Bornstein S, et al. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell 2014;25: 809-21.
23. 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: 222-5.
24. Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, et al. Direct visualization ofmacrophage-assisted tumor cell intravasation inmammary tumors. Cancer Res 2007;67: 2649-56.
25. Hilton JF, Amir E, Hopkins S, Nabavi M, DiPrimio G, Sheikh A, et al. Acquisition of metastatic tissue from patients with bone metastases from breast cancer. Breast Cancer Res Treat 2011;129: 761-5.
26. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, et al. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 2011;19: 512-26.
27. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, Greenberg JI, et al. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 2008;456: 814-8.
28. Kodumudi KN, Woan K, Gilvary DL, Sahakian E, Wei S, Djeu JY. A novel chemoimmunomodulating property of docetaxel: Suppression of myeloid-derived suppressor cells in tumor bearers. Clin Cancer Res 2010; 16: 4583-94.
29. Murdoch C, Giannoudis A, Lewis CE. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 2004;104: 2224-34.
30. Fang HY, Hughes R, Murdoch C, Coffelt SB, Biswas SK, Harris AL, et al. Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood 2009;114: 844-59.
31. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006;66: 11238-46.
32. Miao Z, Luker KE, Summers BC, Berahovich R, BhojaniMS, Rehemtulla A, et al. CXCR7(RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc Natl Acad Sci U S A 2007;104: 15735-40.
33. Weiss ID, Jacobson O, Kiesewetter DO, Jacobus JP, Szajek LP, Chen X, et al. Positron emission tomography imaging of tumors expressing the human chemokine receptor CXCR4 in mice with the use of 64Cu-AMD3100. Mol Imaging Biol 2012;14: 106-14.
34. Feig C, Jones JO, Kraman M, Wells RJ, Deonarine A, Chan DS, et al. Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proc Natl Acad Sci U S A 2013;110: 20212-7.
35. Hitchon C, Wong K, Ma G, Reed J, Lyttle D, El-Gabalawy H. Hypoxiainduced production of stromal cell-derived factor 1 (CXCL12) and vascular endothelial growth factor by synovial fibroblasts. Arthritis Rheum 2002; 46: 2587-97.
36. Li L, Jiang L, Geng C, Cao J, Zhong L. The role of oxidative stress in acrolein-induced DNA damage in HepG2 cells. Free Radic Res 2008; 42: 354-61.
37. Lin HH, Chen YH, Chang PF, Lee YT, Yet SF, Chau LY. Heme oxygenase-1 promotes neovascularization in ischemic heart by coinduction of VEGF and SDF-1. J Mol Cell Cardiol 2008;45: 44-55.
38. Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T, et al. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature 2014;515: 130-3.
39. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicincyclophosphamide chemotherapy. Cancer Immunol Immunother 2009; 58: 49-59.
40. Shaked Y, Henke E, Roodhart JM, Mancuso P, Langenberg MH, Colleoni M, et al. Rapid chemotherapy-induced acute endothelial progenitor cell mobilization: Implications for antiangiogenic drugs as chemosensitizing agents. Cancer Cell 2008;14: 263-73.
41. Chen Y, Jungsuwadee P, Vore M, Butterfield DA, StClair DK. Collateral damage in cancer chemotherapy: Oxidative stress in nontargeted tissues. Mol Interv 2007;7: 147-56.
42. Tu TH, Joe Y, Choi HS, Chung HT, Yu R. Induction of heme oxygenase-1 with hemin reduces obesity-induced adipose tissue inflammation via adipose macrophage phenotype switching. Mediators Inflamm 2014; 2014: 290708.
43. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, et al. VEGFinduced adult neovascularization: Recruitment, retention, and role of accessory cells. Cell 2006;124: 175-89.
44. Stratmann A, Risau W, Plate KH. Cell type-specific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am J Pathol 1998;153: 1459-66.
45. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005;8: 299-309.
46. Rigamonti N, Kadioglu E, Keklikoglou I, Rmili CW, Leow CC, De Palma M. Role of angiopoietin-2 in adaptive tumor resistance to VEGF signalling blockade. Cell Rep 2014;8: 696-706
47. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, et al. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumorswithout affecting healthy vessels. Cell 2007;131: 463-75.
48. + myeloid cells. Nat Biotechnol 2007;25: 911-20.
49. Roussos ET, Goswami S, Balsamo M, Wang Y, Stobezki R, Adler E, et al. Mena invasive (Mena(INV)) and Mena11a isoforms play distinct roles in breast cancer cell cohesion and association with TMEM. Clin Exp Metastasis 2011;28: 515-27.
50. GalskyMD, Vogelzang NJ, Conkling P, Raddad E, Polzer J, Roberson S, et al. A Phase I Trial of LY2510924, a CXCR4 peptide antagonist, in patients with advanced cancer. Clin Cancer Res 2014;20: 3581-8.