Colony-stimulating factor 1 receptor blockade inhibits tumor growth by altering the polarization of tumor-associated macrophages in hepatocellular carcinoma

Molecular Cancer Therapeutics

Volumn 16, Issue 8, 2017, Pages 1544-1554

  Ao, Jian Yang ^a,b,c   Zhu, Xiao Dong ^a,b   Chai, Zong Tao ^a,b   Cai, Hao ^a,b   Zhang, Yuan Yuan ^a,b   Zhang, Ke Zhi ^d   Kong, Ling Qun ^e   Zhang, Ning ^a,b   Ye, Bo Gen ^a,b   Ma, De Ning ^a,b   Sun, Hui Chuan ^a,b  

^a FUDAN UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c WENZHOU MEDICAL UNIVERSITY   (China)

^d Taizhou People's Hospital   (China)

^e BINZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; B7 ANTIGEN; COLONY STIMULATING FACTOR 1; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 23P19; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 6; PLX 3397; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG; 5-((5-CHLORO-1H-PYRROLO(2,3-B)PYRIDIN-3-YL)METHYL)-N-((6-(TRIFLUOROMETHYL)PYRIDIN-3-YL)METHYL)PYRIDIN-2-AMINE; AMINOPYRIDINE DERIVATIVE; COLONY STIMULATING FACTOR RECEPTOR; PYRROLE DERIVATIVE; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL PROLIFERATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; THERAPY EFFECT; TUMOR ASSOCIATED LEUKOCYTE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; BONE MARROW CELL; C57BL MOUSE; CELL POLARITY; CHEMISTRY; DRUG EFFECT; LIVER TUMOR; MACROPHAGE; METABOLISM; MONOCYTE; PATHOLOGY; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

AMINOPYRIDINES; ANIMALS; BIOMARKERS, TUMOR; BONE MARROW CELLS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL POLARITY; CELL PROLIFERATION; HUMANS; LIVER NEOPLASMS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MONOCYTES; PHENOTYPE; PYRROLES; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; TUMOR MICROENVIRONMENT;

EID: 85027172512     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-16-0866     Document Type: Article

References (53)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87–108.
2. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860–7.
3. Wan S, Kuo N, Kryczek I, Zou W, Welling TH. Myeloid cells in hepatocellular carcinoma. Hepatology 2015;62:1304–12.
4. Wang L, Fu H, Nanayakkara G, Li Y, Shao Y, Johnson C, et al. Novel extracellular and nuclear caspase-1 and inflammasomes propagate inflammation and regulate gene expression: a comprehensive database mining study. J Hematol Oncol 2016;9:122.
5. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005;7:211–7.
6. Capece D, Fischietti M, Verzella D, Gaggiano A, Cicciarelli G, Tessitore A, et al. The inflammatory microenvironment in hepatocellular carcinoma: a pivotal role for tumor-associated macrophages. BioMed Res Int 2013; 2013:187204.
7. Mantovani A, Germano G, Marchesi F, Locatelli M, Biswas SK. Cancer-promoting tumor-associated macrophages: new vistas and open questions. Eur J Immunol 2011;41:2522–5.
8. Allavena P, Mantovani A. Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 2012; 167:195–205.
9. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39–51.
10. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014;41:49–61.
11. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002;23:549–55.
12. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003;3:23–35.
13. Zhu XD, Zhang JB, Zhuang PY, Zhu HG, Zhang W, Xiong YQ, et al. High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J Clin Oncol 2008; 26:2707–16.
14. Jia JB, Wang WQ, Sun HC, Zhu XD, Liu L, Zhuang PY, et al. High expression of macrophage colony-stimulating factor-1 receptor in peritumoral liver tissue is associated with poor outcome in hepatocellular carcinoma after curative resection. Oncologist 2010;15:732–43.
15. Kong LQ, Zhu XD, Xu HX, Zhang JB, Lu L, Wang WQ, et al. The clinical significance of the CD163+ and CD68+ macrophages in patients with hepatocellular carcinoma. PLoS One 2013;8:e59771.
16. Chai ZT, Zhu XD, Ao JY, Wang WQ, Gao DM, Kong J, et al. microRNA-26a suppresses recruitment of macrophages by down-regulating macrophage colony-stimulating factor expression through the PI3K/Akt pathway in hepatocellular carcinoma. J Hematol Oncol 2015;8:56.
17. Laoui D, Van Overmeire E, De Baetselier P, Van Ginderachter JA, Raes G. Functional relationship between tumor-associated macrophages and macrophage colony-stimulating factor as contributors to cancer progression. Front Immunol 2014;5:489.
18. Galdiero MR, Bonavita E, Barajon I, Garlanda C, Mantovani A, Jaillon S. Tumor associated macrophages and neutrophils in cancer. Immunobiology 2013;218:1402–10.
19. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014;41:14–20.
20. Verreck FA, de Boer T, Langenberg DM, Hoeve MA, Kramer M, Vaisberg E, et al. Human IL-23-producing type 1 macrophages promote but IL-10producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci U S A 2004;101:4560–5.
21. Joshi S, Singh AR, Zulcic M, Bao L, Messer K, Ideker T, et al. Rac2 controls tumor growth, metastasis and M1-M2 macrophage differentiation in vivo. PLoS One 2014;9:e95893.
22. Zhang W, Zhu XD, Sun HC, Xiong YQ, Zhuang PY, Xu HX, et al. Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects. Clin Cancer Res 2010;16:3420–30.
23. Zhu XD, Sun HC, Xu HX, Kong LQ, Chai ZT, Lu L, et al. Antiangiogenic therapy promoted metastasis of hepatocellular carcinoma by suppressing host-derived interleukin-12b in mouse models. Angiogenesis 2013; 16:809–20.
24. Cassier PA, Gelderblom H, Stacchiotti S, Thomas D, Maki RG, Kroep JR, et al. Efficacy of imatinib mesylate for the treatment of locally advanced and/or metastatic tenosynovial giant cell tumor/pigmented villonodular synovitis. Cancer 2012;118:1649–55.
25. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 2013;19:1264–72.
26. Coniglio SJ, Eugenin E, Dobrenis K, Stanley ER, West BL, Symons MH, et al. Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling. Mol Med (Cambridge, Mass) 2012; 18:519–27.
27. De I, Nikodemova M, Steffen MD, Sokn E, Maklakova VI, Watters JJ, et al. CSF1 overexpression has pleiotropic effects on microglia in vivo. Glia 2014;62:1955–67.
28. He Y, Rhodes SD, Chen S, Wu X, Yuan J, Yang X, et al. c-Fms signaling mediates neurofibromatosis Type-1 osteoclast gain-in-functions. PLoS One 2012;7:e46900.
29. Mok S, Koya RC, Tsui C, Xu J, Robert L, Wu L, et al. Inhibition of CSF-1 receptor improves the antitumor efficacy of adoptive cell transfer immunotherapy. Cancer Res 2014;74:153–61.
30. Patwardhan PP, Surriga O, Beckman MJ, de Stanchina E, Dematteo RP, Tap WD, et al. Sustained inhibition of receptor tyrosine kinases and macrophage depletion by PLX3397 and rapamycin as a potential new approach for the treatment of MPNSTs. Clin Cancer Res 2014;20:3146–58.
31. Prada CE, Jousma E, Rizvi TA, Wu J, Dunn RS, Mayes DA, et al. Neurofibroma-associated macrophages play roles in tumor growth and response to pharmacological inhibition. Acta Neuropathol 2013;125:159–68.
32. Sluijter M, van der Sluis TC, van der Velden PA, Versluis M, West BL, van der Burg SH, et al. Inhibition of CSF-1R supports T-cell mediated melanoma therapy. PLoS One 2014;9:e104230.
33. Tap WD, Wainberg ZA, Anthony SP, Ibrahim PN, Zhang C, Healey JH, et al. Structure-guided blockade of CSF1R kinase in tenosynovial giant-cell tumor. N Engl J Med 2015;373:428–37.
34. Li Y, Tang Y, Ye L, Liu B, Liu K, Chen J, et al. Establishment of a hepatocellular carcinoma cell line with unique metastatic characteristics through in vivo selection and screening for metastasis-related genes through cDNA microarray. J Cancer Res Clin Oncol 2003; 129:43–51.
35. Li Y, Tian B, Yang J, Zhao L, Wu X, Ye SL, et al. Stepwise metastatic human hepatocellular carcinoma cell model system with multiple metastatic potentials established through consecutive in vivo selection and studies on metastatic characteristics. J Cancer Res Clin Oncol 2004;130:460–8.
36. Genin M, Clement F, Fattaccioli A, Raes M, Michiels C. M1 and M2 macrophages derived from THP-1 cells differentially modulate the response of cancer cells to etoposide. BMC Cancer 2015;15:577.
37. Bain CC, Bravo-Blas A, Scott CL, Gomez Perdiguero E, Geissmann F, Henri S, et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol 2014; 15:929–37.
38. Ying W, Cheruku PS, Bazer FW, Safe SH, Zhou B. Investigation of macrophage polarization using bone marrow derived macrophages. J Vis Exp 2013;76:e50323.
39. Chai ZT, Kong J, Zhu XD, Zhang YY, Lu L, Zhou JM, et al. MicroRNA-26a inhibits angiogenesis by down-regulating VEGFA through the PIK3C2alpha/Akt/HIF-1alpha pathway in hepatocellular carcinoma. PLoS One 2013;8:e77957.
40. Martinez FO, 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; 177:7303–11.
41. Martinez FO, Helming L, Milde R, Varin A, Melgert BN, Draijer C, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood 2013;121:e57–69.
42. Vogel DY, Vereyken EJ, Glim JE, Heijnen PD, Moeton M, van der Valk P, et al. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status. J Neuroinflammation 2013;10:35.
43. 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.
44. Fleetwood AJ, Dinh H, Cook AD, Hertzog PJ, Hamilton JA. GM-CSF- and M-CSF-dependent macrophage phenotypes display differential dependence on type I interferon signaling. J Leukoc Biol 2009;86: 411–21.
45. Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, Pixley FJ, et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res 2005;65:5278–83.
46. Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 2004;64:7022–9.
47. Swierczak A, Cook AD, Lenzo JC, Restall CM, Doherty JP, Anderson RL, et al. The promotion of breast cancer metastasis caused by inhibition of CSF-1R/CSF-1 signaling is blocked by targeting the G-CSF receptor. Cancer Immunol Res 2014;2:765–76.
48. Mueller MM, Peter W, Mappes M, Huelsen A, Steinbauer H, Boukamp P, et al. Tumor progression of skin carcinoma cells in vivo promoted by clonal selection, mutagenesis, and autocrine growth regulation by granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor. Am J Pathol 2001;159:1567–79.
49. Su S, Liu Q, Chen J, Chen J, Chen F, He C, et al. A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell 2014;25:605–20.
50. Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 2014;25:846–59.
51. Hashimoto O, Yoshida M, Koma Y, Yanai T, Hasegawa D, Kosaka Y, et al. Collaboration of cancer-associated fibroblasts and tumour-associated macrophages for neuroblastoma development. J Pathol 2016; 240:211–23.
52. Lou G, Song X, Yang F, Wu S, Wang J, Chen Z, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J Hematol Oncol 2015; 8:122.
53. Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res 2013;73:1128–41.