Tumor‑associated macrophages in lung cancer: Friend or foe? (Review)
- Authors:
- Fei Xu
- Ying Wei
- Zhao Tang
- Baojun Liu
- Jingcheng Dong
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Affiliations: Department of Geriatric Medicine, Affiliated Hospital of Shandong University of Traditional Chinese Medicine, Jinan, Shandong 250014, P.R. China, Department of Integrative Medicine, Huashan Hospital of Fudan University, Shanghai 200032, P.R. China - Published online on: September 17, 2020 https://doi.org/10.3892/mmr.2020.11518
- Pages: 4107-4115
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Copyright: © Xu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Brenman JE and Temple BR: Opinion: Alternative views of AMP-activated protein kinase. Cell Biochem Biophys. 47:321–331. 2007. View Article : Google Scholar : PubMed/NCBI | |
Gridelli C, Perrone F and Monfardini S: Lung cancer in the elderly. Eur J Cancer. 33:2313–2314. 1997. View Article : Google Scholar : PubMed/NCBI | |
Goswami KK, Ghosh T, Ghosh S, Sarkar M, Bose A and Baral R: Tumor promoting role of anti-tumor macrophages in tumor microenvironment. Cell Immunol. 316:1–10. 2017. View Article : Google Scholar : PubMed/NCBI | |
Mosser DM and Edwards JP: Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 8:958–969. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sumitomo R, Hirai T, Fujita M, Murakami H, Otake Y and Huang CL: PD-L1 expression on tumor-infiltrating immune cells is highly associated with M2 TAM and aggressive malignant potential in patients with resected non-small cell lung cancer. Lung Cancer. 136:136–144. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ruffell B and Coussens LM: Macrophages and therapeutic resistance in cancer. Cancer Cell. 27:462–472. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cao L, Che X, Qiu X, Li Z, Yang B, Wang S, Hou K, Fan Y, Qu X and Liu Y: M2 macrophage infiltration into tumor islets leads to poor prognosis in non-small-cell lung cancer. Cancer Manag Res. 11:6125–6138. 2019. View Article : Google Scholar : PubMed/NCBI | |
Sumitomo R, Hirai T, Fujita M, Murakami H, Otake Y and Huang CL: M2 tumor-associated macrophages promote tumor progression in non-small-cell lung cancer. Exp Ther Med. 18:4490–4498. 2019.PubMed/NCBI | |
Zhou Z, Peng Y, Wu X, Meng S, Yu W, Zhao J, Zhang H, Wang J and Li W: CCL18 secreted from M2 macrophages promotes migration and invasion via the PI3K/Akt pathway in gallbladder cancer. Cell Oncol (Dordr). 42:81–92. 2019. View Article : Google Scholar : PubMed/NCBI | |
Yeung OW, Lo CM, Ling CC, Qi X, Geng W, Li CX, Ng KT, Forbes SJ, Guan XY, Poon RT, et al: Alternatively activated (M2) macrophages promote tumour growth and invasiveness in hepatocellular carcinoma. J Hepatol. 62:607–616. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sarode P, Zheng X, Giotopoulou GA, Weigert A, Kuenne C, Günther S, Friedrich A, Gattenlöhner S, Stiewe T, Brüne B, et al: Reprogramming of tumor-associated macrophages by targeting β-catenin/FOSL2/ARID5A signaling: A potential treatment of lung cancer. SCI ADV. 6:eaaz61052020. View Article : Google Scholar : PubMed/NCBI | |
Kimura Y, Sumiyoshi M and Baba K: Antitumor and antimetastatic activity of synthetic hydroxystilbenes through inhibition of lymphangiogenesis and M2 macrophage differentiation of tumor-associated macrophages. Anticancer Res. 36:137–148. 2016.PubMed/NCBI | |
Hughes R, Qian BZ, Rowan C, Muthana M, Keklikoglou I, Olson OC, Tazzyman S, Danson S, Addison C, Clemons M, et al: Perivascular M2 macrophages stimulate tumor relapse after chemotherapy. Cancer Res. 75:3479–3491. 2015. View Article : Google Scholar : PubMed/NCBI | |
Flaherty DM, Monick MM and Hinde SL: Human alveolar macrophages are deficient in PTEN. The role of endogenous oxidants. J Biol Chem. 281:5058–5064. 2006. View Article : Google Scholar : PubMed/NCBI | |
Biswas SK and Mantovani A: Macrophage plasticity and interaction with lymphocyte subsets: Cancer as a paradigm. Nat Immunol. 11:889–896. 2010. View Article : Google Scholar : PubMed/NCBI | |
Biswas SK, Gangi L, Paul S, Schioppa T, Saccani A, Sironi M, Bottazzi B, Doni A, Vincenzo B, Pasqualini F, et al: A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood. 107:2112–2122. 2006. View Article : Google Scholar : PubMed/NCBI | |
Klimp AH, Hollema H, Kempinga C, van der Zee AG, de Vries EG and Daemen T: Expression of cyclooxygenase-2 and inducible nitric oxide synthase in human ovarian tumors and tumor-associated macrophages. Cancer Res. 61:7305–7309. 2001.PubMed/NCBI | |
Nam S and Lim J: Essential role of interferon regulatory factor 4 (IRF4) in immune cell development. Arch Pharm Res. 39:1548–1555. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gong M, Zhuo X and Ma A: STAT6 Upregulation promotes M2 macrophage polarization to suppress atherosclerosis. Med Sci Monit Basic Res. 23:240–249. 2017. View Article : Google Scholar : PubMed/NCBI | |
Vergadi E, Ieronymaki E, Lyroni K, Vaporidi K and Tsatsanis C: Akt signaling pathway in macrophage activation and M1/M2 polarization. J Immunol. 198:1006–1014. 2017. View Article : Google Scholar : PubMed/NCBI | |
Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, De Nardo D, Gohel TD, Emde M, Schmidleithner L, et al: Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity. 40:274–288. 2014. View Article : Google Scholar : PubMed/NCBI | |
Nelson MP, Christmann BS, Dunaway CW, Morris A and Steele C: Experimental Pneumocystis lung infection promotes M2a alveolar macrophage-derived MMP12 production. Am J Physiol Lung Cell Mol Physiol. 303:L469–L475. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhang W, Xu W and Xiong S: Blockade of Notch1 signaling alleviates murine lupus via blunting macrophage activation and M2b polarization. J Immunol. 184:6465–6478. 2010. View Article : Google Scholar : PubMed/NCBI | |
Koscsó B, Csóka B, Kókai E, Németh ZH, Pacher P, Virág L, Leibovich SJ and Haskó G: Adenosine augments IL-10-induced STAT3 signaling in M2c macrophages. J Leukoc Biol. 94:1309–1315. 2013. View Article : Google Scholar : PubMed/NCBI | |
Olmes G, Büttner-Herold M, Ferrazzi F, Distel L, Amann K and Daniel C: CD163+ M2c-like macrophages predominate in renal biopsies from patients with lupus nephritis. Arthritis Res Ther. 18:902016. View Article : Google Scholar : PubMed/NCBI | |
Wang Q, Ni H, Lan L, Wei X, Xiang R and Wang Y: Fra-1 protooncogene regulates IL-6 expression in macrophages and promotes the generation of M2d macrophages. Cell Res. 20:701–712. 2010. View Article : Google Scholar : PubMed/NCBI | |
Watkins SK, Egilmez NK, Suttles J and Stout RD: IL-12 rapidly alters the functional profile of tumor-associated and tumor-infiltrating macrophages in vitro and in vivo. J Immunol. 178:1357–1362. 2007. View Article : Google Scholar : PubMed/NCBI | |
Schoppmann SF, Birner P, Stöckl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K and Kerjaschki D: Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol. 161:947–956. 2002. View Article : Google Scholar : PubMed/NCBI | |
Hotchkiss KA, Ashton AW, Klein RS, Lenzi ML, Zhu GH and Schwartz EL: Mechanisms by which tumor cells and monocytes expressing the angiogenic factor thymidine phosphorylase mediate human endothelial cell migration. Cancer Res. 63:527–533. 2003.PubMed/NCBI | |
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 Immunol. 23:549–555. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ohri CM, Shikotra A, Green RH, Waller DA and Bradding P: Macrophages within NSCLC tumour islets are predominantly of a cytotoxic M1 phenotype associated with extended survival. Eur Respir J. 33:118–126. 2009. View Article : Google Scholar : PubMed/NCBI | |
Helm O, Held-Feindt J, Grage-Griebenow E, Reiling N, Ungefroren H, Vogel I, Krüger U, Becker T, Ebsen M, Röcken C, et al: Tumor-associated macrophages exhibit pro- and anti-inflammatory properties by which they impact on pancreatic tumorigenesis. Int J Cancer. 135:843–861. 2014. View Article : Google Scholar : PubMed/NCBI | |
Che D, Zhang S, Jing Z, Shang L, Jin S, Liu F, Shen J, Li Y, Hu J, Meng Q and Yu Y: Macrophages induce EMT to promote invasion of lung cancer cells through the IL-6-mediated COX-2/PGE(2)/β-catenin signalling pathway. Mol Immunol. 90:197–210. 2017. View Article : Google Scholar : PubMed/NCBI | |
Dehai C, Bo P, Qiang T, Lihua S, Fang L, Shi J, Jingyan C, Yan Y, Guangbin W and Zhenjun Y: Enhanced invasion of lung adenocarcinoma cells after co-culture with THP-1-derived macrophages via the induction of EMT by IL-6. Immunol Lett. 160:1–10. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yang L, Dong Y, Li Y, Wang D, Liu S, Wang D, Gao Q, Ji S, Chen X, Lei Q, et al: IL-10 derived from M2 macrophage promotes cancer stemness via JAK1/STAT1/NF-κB/Notch1 pathway in non-small cell lung cancer. Int J Cancer. 145:1099–1110. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Cao J, Ma S, Dong R, Meng W, Ying M, Weng Q, Chen Z, Ma J, Fang Q, et al: Tumor hypoxia enhances Non-Small Cell Lung Cancer metastasis by selectively promoting macrophage M2 polarization through the activation of ERK signaling. Oncotarget. 5:9664–9677. 2014. View Article : Google Scholar : PubMed/NCBI | |
Laoui D, Van Overmeire E, Di Conza G, Aldeni C, Keirsse J, Morias Y, Movahedi K, Houbracken I, Schouppe E, Elkrim Y, et al: Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population. Cancer Res. 74:24–30. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang R, Lu M, Zhang J, Chen S, Luo X, Qin Y and Chen H: Increased IL-10 mRNA expression in tumor-associated macrophage correlated with late stage of lung cancer. J Exp Clin Cancer Res. 30:622011. View Article : Google Scholar : PubMed/NCBI | |
Fu XL, Duan W, Su CY, Mao FY, Lv YP, Teng YS, Yu PW, Zhuang Y and Zhao YL: Interleukin 6 induces M2 macrophage differentiation by STAT3 activation that correlates with gastric cancer progression. Cancer Immunol Immunother. 66:1597–1608. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Yang X, Tsai Y, Yang L, Chuang KH, Keng PC, Lee SO and Chen Y: IL-6 mediates macrophage infiltration after irradiation via up-regulation of CCL2/CCL5 in non-small cell lung cancer. Radiat Res. 187:50–59. 2017. View Article : Google Scholar : PubMed/NCBI | |
de Cortie K, Russell NS, Coppes RP, Stewart FA and Scharpfenecker M: Bone marrow-derived macrophages incorporate into the endothelium and influence vascular and renal function after irradiation. Int J Radiat Biol. 90:769–777. 2014. View Article : Google Scholar : PubMed/NCBI | |
Russell NS, Floot B, van Werkhoven E, Schriemer M, de Jong-Korlaar R, Woerdeman LA, Stewart FA and Scharpfenecker M: Blood and lymphatic microvessel damage in irradiated human skin: The role of TGF-β, endoglin and macrophages. Radiother Oncol. 116:455–461. 2015. View Article : Google Scholar : PubMed/NCBI | |
Maeda H, Kuwahara H, Ichimura Y, Ohtsuki M, Kurakata S and Shiraishi A: TGF-beta enhances macrophage ability to produce IL-10 in normal and tumor-bearing mice. J immunol. 155:4926–4932. 1995.PubMed/NCBI | |
Zhang S, Che D, Yang F, Chi C, Meng H, Shen J, Qi L, Liu F, Lv L, Li Y, et al: Tumor-associated macrophages promote tumor metastasis via the TGF-β/SOX9 axis in non-small cell lung cancer. Oncotarget. 8:99801–99815. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lee HJ, Park MK, Lee EJ and Lee CH: Resolvin D1 inhibits TGF-β1-induced epithelial mesenchymal transition of A549 lung cancer cells via lipoxin A4 receptor/formyl peptide receptor 2 and GPR32. Int J Biochem Cell Biol. 45:2801–2807. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang R, Zhang J, Chen S, Lu M, Luo X, Yao S, Liu S, Qin Y and Chen H: Tumor-associated macrophages provide a suitable microenvironment for non-small lung cancer invasion and progression. Lung Cancer. 74:188–196. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cardoso AP, Pinto ML, Pinto AT, Pinto MT, Monteiro C, Oliveira MI, Santos SG, Relvas JB, Seruca R, Mantovani A, et al: Matrix metalloproteases as maestros for the dual role of LPS- and IL-10-stimulated macrophages in cancer cell behaviour. BMC Cancer. 15:4562015. View Article : Google Scholar : PubMed/NCBI | |
Kim YH, Kwon HJ and Kim DS: Matrix metalloproteinase 9 (MMP-9)-dependent processing of βig-h3 protein regulates cell migration, invasion, and adhesion. J Biol Chem. 287:38957–38969. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wang B, Shi L, Sun X, Wang L, Wang X and Chen C: Production of CCL20 from lung cancer cells induces the cell migration and proliferation through PI3K pathway. J Cell Mol Med. 20:920–929. 2016. View Article : Google Scholar : PubMed/NCBI | |
Shi L, Zhang B, Sun X, Zhang X, Lv S, Li H, Wang X, Zhao C, Zhang H, Xie X, et al: CC chemokine ligand 18(CCL18) promotes migration and invasion of lung cancer cells by binding to Nir1 through Nir1-ELMO1/DOC180 signaling pathway. Mol Carcinog. 55:2051–2062. 2016. View Article : Google Scholar : PubMed/NCBI | |
Huang R, Wang S, Wang N, Zheng Y, Zhou J, Yang B, Wang X, Zhang J, Guo L, Wang S, et al: CCL5 derived from tumor-associated macrophages promotes prostate cancer stem cells and metastasis via activating β-catenin/STAT3 signaling. Cell Death Dis. 11:2342020. View Article : Google Scholar : PubMed/NCBI | |
Nakanishi T, Imaizumi K, Hasegawa Y, Kawabe T, Hashimoto N, Okamoto M and Shimokata K: Expression of macrophage-derived chemokine (MDC)/CCL22 in human lung cancer. Cancer Immunol Immunother. 55:1320–1329. 2006. View Article : Google Scholar : PubMed/NCBI | |
Nakamura ES, Koizumi K, Kobayashi M, Saitoh Y, Arita Y, Nakayama T, Sakurai H, Yoshie O and Saiki I: RANKL-induced CCL22/macrophage-derived chemokine produced from osteoclasts potentially promotes the bone metastasis of lung cancer expressing its receptor CCR4. Clin Exp Metastasis. 23:9–18. 2006. View Article : Google Scholar : PubMed/NCBI | |
Li W, Zhang X, Wu F, Zhou Y, Bao Z, Li H, Zheng P and Zhao S: Gastric cancer-derived mesenchymal stromal cells trigger M2 macrophage polarization that promotes metastasis and EMT in gastric cancer. Cell Death Dis. 10:9182019. View Article : Google Scholar : PubMed/NCBI | |
Cao H, Huang Y, Wang L, Wang H, Pang X, Li K, Dang W, Tang H, Wei L, Su M, et al: Leptin promotes migration and invasion of breast cancer cells by stimulating IL-8 production in M2 macrophages. Oncotarget. 7:65441–65453. 2016. View Article : Google Scholar : PubMed/NCBI | |
Liu Q, Li A, Yu S, Qin S, Han N, Pestell RG, Han X and Wu K: DACH1 antagonizes CXCL8 to repress tumorigenesis of lung adenocarcinoma and improve prognosis. J Hematol Oncol. 11:532018. View Article : Google Scholar : PubMed/NCBI | |
Tataroğlu C, Kargi A, Ozkal S, Eşrefoğlu N and Akkoçlu A: Association of macrophages, mast cells and eosinophil leukocytes with angiogenesis and tumor stage in non-small cell lung carcinomas (NSCLC). Lung Cancer. 43:47–54. 2004. View Article : Google Scholar : PubMed/NCBI | |
Chen JJ, Yao PL, Yuan A, Hong TM, Shun CT, Kuo ML, Lee YC and Yang PC: Up-regulation of tumor interleukin-8 expression by infiltrating macrophages: Its correlation with tumor angiogenesis and patient survival in non-small cell lung cancer. Clin Cancer Res. 9:729–737. 2003.PubMed/NCBI | |
Lewis JS, Landers RJ, Underwood JC, Harris AL and Lewis CE: Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J Pathol. 192:150–158. 2000. View Article : Google Scholar : PubMed/NCBI | |
Leek RD and Harris AL: Tumor-associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia. 7:177–189. 2002. View Article : Google Scholar : PubMed/NCBI | |
Giatromanolaki A, Koukourakis MI, Sivridis E, Turley H, Talks K, Pezzella F, Gatter KC and Harris AL: Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer. 85:881–890. 2001. View Article : Google Scholar : PubMed/NCBI | |
Gordon SR, Maute RL, Dulken BW, Hutter G, George BM, McCracken MN, Gupta R, Tsai JM, Sinha R, Corey D, et al: PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature. 545:495–499. 2017. View Article : Google Scholar : PubMed/NCBI | |
Peranzoni E, Lemoine J, Vimeux L, Feuillet V, Barrin S, Kantari-Mimoun C, Bercovici N, Guerin M, Biton J, Ouakrim H, et al: Macrophages impede CD8 T cells from reaching tumor cells and limit the efficacy of anti-PD-1 treatment. Proc Natl Acad Sci USA. 115:E4041–E4050. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sharma SK, Chintala NK, Vadrevu SK, Patel J, Karbowniczek M and Markiewski MM: Pulmonary alveolar macrophages contribute to the premetastatic niche by suppressing antitumor T cell responses in the lungs. J Immunol. 194:5529–5538. 2015. View Article : Google Scholar : PubMed/NCBI | |
Allavena P, Sica A, Vecchi A, Locati M, Sozzani S and Mantovani A: The chemokine receptor switch paradigm and dendritic cell migration: Its significance in tumor tissues. Immunol Rev. 177:141–149. 2000. View Article : Google Scholar : PubMed/NCBI | |
Qiao J, Liu Z, Dong C, Luan Y, Zhang A, Moore C, Fu K, Peng J, Wang Y, Ren Z, et al: Targeting tumors with IL-10 prevents dendritic cell-mediated CD8+ T cell apoptosis. Cancer Cell. 35:901–915.e4. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wang D, Yang L, Yue D, Cao L, Li L, Wang D, Ping Y, Shen Z, Zheng Y, Wang L and Zhang Y: Macrophage-derived CCL22 promotes an immunosuppressive tumor microenvironment via IL-8 in malignant pleural effusion. Cancer Lett. 452:244–253. 2019. View Article : Google Scholar : PubMed/NCBI | |
Young MR, Endicott RA, Duffie GP and Wepsic HT: Suppressor alveolar macrophages in mice bearing metastatic Lewis lung carcinoma tumors. J Leukoc Biol. 42:682–688. 1987. View Article : Google Scholar : PubMed/NCBI | |
De Palma M and Lewis CE: Cancer: Macrophages limit chemotherapy. Nature. 472:303–304. 2011. View Article : Google Scholar : PubMed/NCBI | |
Dijkgraaf EM, Heusinkveld M, Tummers B, Vogelpoel LT, Goedemans R, Jha V, Nortier JW, Welters MJ, Kroep JR and van der Burg SH: Chemotherapy alters monocyte differentiation to favor generation of cancer-supporting M2 macrophages in the tumor microenvironment. Cancer Res. 73:2480–2492. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, Belaygorod L, Carpenter D, Collins L, Piwnica-Worms D, et al: Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res. 73:1128–1141. 2013. View Article : Google Scholar : PubMed/NCBI | |
DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA, et al: Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 1:54–67. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zhang C, Yu X, Gao L, Zhao Y, Lai J, Lu D, Bao R, Jia B, Zhong L, Wang F and Liu Z: Noninvasive imaging of CD206-positive M2 macrophages as an early biomarker for post-chemotherapy tumor relapse and lymph node metastasis. Theranostics. 7:4276–4288. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sugimura K, Miyata H, Tanaka K, Takahashi T, Kurokawa Y, Yamasaki M, Nakajima K, Takiguchi S, Mori M and Doki Y: High infiltration of tumor-associated macrophages is associated with a poor response to chemotherapy and poor prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer. J Surg Oncol. 111:752–759. 2015. View Article : Google Scholar : PubMed/NCBI | |
Paulus P, Stanley ER, Schäfer R, Abraham D and Aharinejad S: Colony-stimulating factor-1 antibody reverses chemoresistance in human MCF-7 breast cancer xenografts. Cancer Res. 66:4349–4356. 2006. View Article : Google Scholar : PubMed/NCBI | |
Salvagno C, Ciampricotti M, Tuit S, Hau CS, van Weverwijk A, Coffelt SB, Kersten K, Vrijland K, Kos K, Ulas T, et al: Therapeutic targeting of macrophages enhances chemotherapy efficacy by unleashing type I interferon response. Nat Cell Biol. 21:511–521. 2019. View Article : Google Scholar : PubMed/NCBI | |
Dai F, Liu L, Che G, Yu N, Pu Q, Zhang S, Ma J, Ma L and You Z: The number and microlocalization of tumor-associated immune cells are associated with patient's survival time in non-small cell lung cancer. BMC Cancer. 10:2202010. View Article : Google Scholar : PubMed/NCBI | |
Welsh TJ, Green RH, Richardson D, Waller DA, O'Byrne KJ and Bradding P: Macrophage and mast-cell invasion of tumor cell islets confers a marked survival advantage in non-small-cell lung cancer. J Clin Oncol. 23:8959–8967. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pei BX, Sun BS, Zhang ZF, Wang AL and Ren P: Interstitial tumor-associated macrophages combined with tumor-derived colony-stimulating factor-1 and interleukin-6, a novel prognostic biomarker in non-small cell lung cancer. J Thorac Cardiovasc Surg. 148:1208–1216.e2. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ma J, Liu L, Che G, Yu N, Dai F and You Z: The M1 form of tumor-associated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer. 10:1122010. View Article : Google Scholar : PubMed/NCBI | |
Zhang B, Yao G, Zhang Y and Gao J, Yang B, Rao Z and Gao J: M2-polarized tumor-associated macrophages are associated with poor prognoses resulting from accelerated lymphangiogenesis in lung adenocarcinoma. Clinics (Sao Paulo). 66:1879–1886. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jung KY, Cho SW, Kim YA, Kim D, Oh BC, Park DJ and Park YJ: Cancers with higher density of tumor-associated macrophages were associated with poor survival rates. J Pathol Transl Med. 49:318–324. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hirayama S, Ishii G, Nagai K, Ono S, Kojima M, Yamauchi C, Aokage K, Hishida T, Yoshida J, Suzuki K and Ochiai A: Prognostic impact of CD204-positive macrophages in lung squamous cell carcinoma: Possible contribution of Cd204-positive macrophages to the tumor-promoting microenvironment. J Thorac Oncol. 7:1790–1797. 2012. View Article : Google Scholar : PubMed/NCBI | |
Li X, Yao W, Yuan Y, Chen P, Li B, Li J, Chu R, Song H, Xie D, Jiang X and Wang H: Targeting of tumour-infiltrating macrophages via CCL2/CCR2 signalling as a therapeutic strategy against hepatocellular carcinoma. Gut. 66:157–167. 2017. View Article : Google Scholar : PubMed/NCBI | |
Keklikoglou I and De Palma M: Cancer: Metastasis risk after anti-macrophage therapy. Nature. 515:46–47. 2014. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Cao F, Li M, Li P, Yu Y, Xiang L, Xu T, Lei J, Tai YY, Zhu J, et al: Hydroxychloroquine induced lung cancer suppression by enhancing chemo-sensitization and promoting the transition of M2-TAMs to M1-like macrophages. J Exp Clin Cancer Res. 37:2592018. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Sun Z, Pei J, Luo Q, Zeng X, Li Q, Yang Z and Quan J: Identification of α-mangostin as an agonist of human STING. Chemmedchem. 13:2057–2064. 2018. View Article : Google Scholar : PubMed/NCBI | |
Brandão RD, Veeck J, Van de Vijver KK, Lindsey P, de Vries B, van Elssen CH, Blok MJ, Keymeulen K, Ayoubi T, Smeets HJ, et al: A randomised controlled phase II trial of pre-operative celecoxib treatment reveals anti-tumour transcriptional response in primary breast cancer. Breast Cancer Res. 15:R292013. View Article : Google Scholar : PubMed/NCBI | |
Zhu B, Zou L, Cheng X, Lin Z, Duan Y, Wu Y, Zhou F and Chen Z: Administration of MIP-3alpha gene to the tumor following radiation therapy boosts anti-tumor immunity in a murine model of lung carcinoma. Immunol Lett. 103:101–107. 2006. View Article : Google Scholar : PubMed/NCBI | |
Shiri S, Alizadeh AM, Baradaran B, Farhanghi B, Shanehbandi D, Khodayari S, Khodayari H and Tavassoli A: Dendrosomal curcumin suppresses metastatic breast cancer in mice by changing m1/m2 macrophage balance in the tumor microenvironment. Asian Pac J Cancer Prev. 16:3917–3922. 2015. View Article : Google Scholar : PubMed/NCBI | |
Han S, Wang W, Wang S, Wang S, Ju R, Pan Z, Yang T, Zhang G, Wang H and Wang L: Multifunctional biomimetic nanoparticles loading baicalin for polarizing tumor-associated macrophages. Nanoscale. 11:20206–20220. 2019. View Article : Google Scholar : PubMed/NCBI | |
Cao M, Yan H, Han X, Weng L, Wei Q, Sun X, Lu W, Wei Q, Ye J, Cai X, et al: Ginseng-derived nanoparticles alter macrophage polarization to inhibit melanoma growth. J Immunother Cancer. 7:3262019. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Song W, Guo J, Zhang J, Sun Z, Li L, Ding F and Gao M: Cytotoxicity of different sized TiO2 nanoparticles in mouse macrophages. Toxicol Ind Health. 29:523–533. 2013. View Article : Google Scholar : PubMed/NCBI | |
Park J, Lim DH, Lim HJ, Kwon T, Choi JS, Jeong S, Choi IH and Cheon J: Size dependent macrophage responses and toxicological effects of Ag nanoparticles. Chem Commun (Camb). 47:4382–4384. 2011. View Article : Google Scholar : PubMed/NCBI |