Research progress on the role of tumor‑associated macrophages in tumor development and their use as molecular targets (Review)
- Authors:
- Chenglin Lu
- Ying Liu
- Linxuan Miao
- Xiangle Kong
- Huili Li
- Haoran Chen
- Xu Zhao
- Bin Zhang
- Xiaonan Cui
-
Affiliations: Department of Oncology, The First Affiliated Hospital of Dalian Medical University, Dalian, Liaoning 860411, P.R. China, Department of Oncology, The First Affiliated Hospital of Dalian Medical University, Dalian, Liaoning 860411, P.R. China - Published online on: December 7, 2023 https://doi.org/10.3892/ijo.2023.5599
- Article Number: 11
-
Copyright: © Lu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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 |
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|
Yan S and Wan G: Tumor-associated macrophages in immunotherapy. FEBS J. 288:6174–6186. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, et al: Macrophage activation and polarization: Nomenclature and experimental guidelines. Immunity. 41:14–20. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Y, Song Y, Du W, Gong L, Chang H and Zou Z: Tumor-associated macrophages: An accomplice in solid tumor progression. J Biomed Sci. 26:782019. View Article : Google Scholar : PubMed/NCBI | |
|
Pathria P, Louis TL and Varner JA: Targeting tumor-associated macrophages in cancer. Trends Immunol. 40:310–327. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Li F, Okreglicka KM, Pohlmeier LM, Schneider C and Kopf M: Fetal monocytes possess increased metabolic capacity and replace primitive macrophages in tissue macrophage development. EMBO J. 39:e1032052020. View Article : Google Scholar : PubMed/NCBI | |
|
Locati M, Curtale G and Mantovani A: Diversity, mechanisms, and significance of macrophage plasticity. Annu Rev Pathol. 15:123–147. 2020. View Article : Google Scholar | |
|
Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T and Bentires-Alj M: Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature. 515:130–133. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang WJ, Wang XH, Gao ST, Chen C, Xu XY, Sun Q, Zhou ZH, Wu GZ, Yu Q, Xu G, et al: Tumor-associated macrophages correlate with phenomenon of epithelial-mesenchymal transition and contribute to poor prognosis in triple-negative breast cancer patients. J Surg Res. 222:93–101. 2018. View Article : Google Scholar | |
|
Xu Y, Zeng H, Jin K, Liu Z, Zhu Y, Xu L, Wang Z, Chang Y and Xu J: Immunosuppressive tumor-associated macrophages expressing interlukin-10 conferred poor prognosis and therapeutic vulnerability in patients with muscle-invasive bladder cancer. J Immunother Cancer. 10:e0034162022. View Article : Google Scholar : PubMed/NCBI | |
|
Kumar AT, Knops A, Swendseid B, Martinez-Outschoom U, Harshyne L, Philp N, Rodeck U, Luginbuhl A, Cognetti D, Johnson J and Curry J: Prognostic significance of tumor-associated macrophage content in head and neck squamous cell carcinoma: A meta-analysis. Front Oncol. 9:6562019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang H, Luo YB, Wu W, Zhang L, Wang Z, Dai Z, Feng S, Cao H, Cheng Q and Liu Z: The molecular feature of macrophages in tumor immune microenvironment of glioma patients. Comput Struct Biotechnol J. 19:4603–4618. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Wu Z, Lei K, Li H, He J and Shi E: Transcriptome-based network analysis related to M2-like tumor-associated macrophage infiltration identified VARS1 as a potential target for improving melanoma immunotherapy efficacy. J Transl Med. 20:4892022. View Article : Google Scholar : PubMed/NCBI | |
|
Yuri P, Shigemura K, Kitagawa K, Hadibrata E, Risan M, Zulfiqqar A, Soeroharjo I, Hendri AZ, Danarto R, Ishii A, et al: Increased tumor-associated macrophages in the prostate cancer microenvironment predicted patients' survival and responses to androgen deprivation therapies in Indonesian patients cohort. Prostate Int. 8:62–69. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Cortese N, Carriero R, Laghi L, Mantovani A and Marchesi F: Prognostic significance of tumor-associated macrophages: Past, present and future. Semin Immunol. 48:1014082020. View Article : Google Scholar : PubMed/NCBI | |
|
Qian BZ and Pollard JW: Macrophage diversity enhances tumor progression and metastasis. Cell. 141:39–51. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Movahedi K, Laoui D, Gysemans C, Baeten M, Stangé G, Van den Bossche J, Mack M, Pipeleers D, In't Veld P, De Baetselier P and Van Ginderachter JA: Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 70:5728–5739. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Shapouri-Moghaddam A, Mohammadian S, Vazini H, Taghadosi M, Esmaeili SA, Mardani F, Seifi B, Mohammadi A, Afshari JT and Sahebkar A: Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol. 233:6425–6440. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Martinez FO, Sica A, Mantovani A and Locati M: Macrophage activation and polarization. Front Biosci. 13:453–461. 2008. View Article : Google Scholar | |
|
Zizzo G, Hilliard BA, Monestier M and Cohen PL: Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK Induction. J Immunol. 189:3508–3520. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ferrante AW Jr: Macrophages, fat, and the emergence of immunometabolism. J Clin Invest. 123:4992–4993. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Haskó G, Pacher P, Deitch EA and Vizi ES: Shaping of monocyte and macrophage function by adenosine receptors. Pharmacol Ther. 113:264–275. 2007. View Article : Google Scholar | |
|
Pinhal-Enfield G, Ramanathan M, Hasko G, Vogel SN, Salzman AL, Boons GJ and Leibovich SJ: An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A(2A) receptors. Am J Pathol. 163:711–721. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A and Locati M: The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677–686. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Huang YH, Cai K, Xu PP, Wang L, Huang CX, Fang Y, Cheng S, Sun XJ, Liu F, Huang JY, et al: CREBBP/EP300 mutations promoted tumor progression in diffuse large B-cell lymphoma through altering tumor-associated macrophage polarization via FBXW7-NOTCH-CCL2/CSF1 axis. Signal Transduct Target Ther. 6:102021. View Article : Google Scholar : PubMed/NCBI | |
|
Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA and Pollard JW: CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 475:222–225. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Sierra-Filardi E, Nieto C, Domínguez-Soto Á, Barroso R, Sánchez-Mateos P, Puig-Kroger A, López-Bravo M, Joven J, Ardavín C, Rodríguez-Fernández JL, et al CCL2 Shapes Macrophage Polarization by GM-CSF and M-CSF: Identification of CCL2/CCR2-dependent gene expression profile. J Immunol. 192:3858–3867. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Archer M, Bernhardt SM, Hodson LJ, Woolford L, Van der Hoek M, Dasari P, Evdokiou A and Ingman WV: CCL2-Mediated stromal interactions drive macrophage polarization to increase breast tumorigenesis. Int J Mol Sci. 24:73852023. View Article : Google Scholar : PubMed/NCBI | |
|
Valero JG, Matas-Céspedes A, Arenas F, Rodriguez V, Carreras J, Serrat N, Guerrero-Hernández M, Yahiaoui A, Balagué O, Martin S, et al: The receptor of the colony-stimulating factor-1 (CSF-1R) is a novel prognostic factor and therapeutic target in follicular lymphoma. Leukemia. 35:2635–2649. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Mu G, Zhu Y, Dong Z, Shi L, Deng Y and Li H: Calmodulin 2 facilitates angiogenesis and metastasis of gastric cancer via STAT3/HIF-1A/VEGF-A mediated macrophage polarization. Front Oncol. 11:7273062021. View Article : Google Scholar : PubMed/NCBI | |
|
Lian G, Chen S, Ouyang M, Li F, Chen L and Yang J: Colon cancer cell secretes EGF to Promote M2 Polarization of TAM Through EGFR/PI3K/AKT/mTOR pathway. Technol Cancer Res Treat. 18:15330338198490682019. View Article : Google Scholar : PubMed/NCBI | |
|
Mazzoni M, Mauro G, Erreni M, Romeo P, Minna E, Vizioli MG, Belgiovine C, Rizzetti MG, Pagliardini S, Avigni R, et al: Senescent thyrocytes and thyroid tumor cells induce M2-like macrophage polarization of human monocytes via a PGE2-dependent mechanism. J Exp Clin Cancer Res. 38:2082019. View Article : Google Scholar : PubMed/NCBI | |
|
Vaupel P and Harrison L: Tumor hypoxia: Causative factors, compensatory mechanisms, and cellular response. Oncologist. 9(Suppl 5): S4–S9. 2004. View Article : Google Scholar | |
|
Zhou HC, Xin-Yan Yan, Yu WW, Liang XQ, Du XY, Liu ZC, Long JP, Zhao GH and Liu HB: Lactic acid in macrophage polarization: The significant role in inflammation and cancer. Inter Rev Immunol. 41:4–18. 2021. View Article : Google Scholar | |
|
Zhang L and Li S: Lactic acid promotes macrophage polarization through MCT-HIF1α signaling in gastric cancer. Exp Cell Res. 388:1118462020. View Article : Google Scholar | |
|
Park JE, Dutta B, Tse SW, Gupta N, Tan CF, Low JK, Yeoh KW, Kon OL, Tam JP and Sze SK: Hypoxia-induced tumor exosomes promote M2-like macrophage polarization of infiltrating myeloid cells and microRNA-mediated metabolic shift. Oncogene. 38:5158–5173. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Hynes RO: The extracellular matrix: Not just pretty fibrils. Science. 326:1216–1219. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Colombatti A, Spessotto P, Doliana R, Mongiat M, Bressan GM and Esposito G: The EMILIN/Multimerin family. Front Immunol. 2:932012. View Article : Google Scholar : | |
|
Mongiat M, Marastoni S, Ligresti G, Lorenzon E, Schiappacassi M, Perris R, Frustaci S and Colombatti A: The extracellular matrix glycoprotein elastin microfibril interface located protein 2: A dual role in the tumor microenvironment. Neoplasia. 12:294–304. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Andreuzzi E, Fejza A, Polano M, Poletto E, Camicia L, Carobolante G, Tarticchio G, Todaro F, Di Carlo E, Scarpa M, et al: Colorectal cancer development is affected by the ECM molecule EMILIN-2 hinging on macrophage polarization via the TLR-4/MyD88 pathway. J Exp Clin Cancer Res. 41:602022. View Article : Google Scholar : PubMed/NCBI | |
|
Bernsmeier C, van der Merwe S and Périanin A: Innate immune cells in cirrhosis. J Hepatol. 73:186–201. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Bruns H, Büttner M, Fabri M, Mougiakakos D, Bittenbring JT, Hoffmann MH, Beier F, Pasemann S, Jitschin R, Hofmann AD, et al: Vitamin D-dependent induction of cathelicidin in human macrophages results in cytotoxicity against high-grade B cell lymphoma. Sci Transl Med. 7:282ra472015. View Article : Google Scholar : PubMed/NCBI | |
|
Pan Y, Yu Y, Wang X and Zhang T: Tumor-Associated macrophages in tumor immunity. Front Immunol. 11:5830842020. View Article : Google Scholar : PubMed/NCBI | |
|
Haque ASMR, Moriyama M, Kubota K, Ishiguro N, Sakamoto M, Chinju A, Mochizuki K, Sakamoto T, Kaneko N, Munemura R, et al: CD206+tumor-associated macrophages promote proliferation and invasion in oral squamous cell carcinoma via EGF production. Sci Rep. 9:146112019. View Article : Google Scholar | |
|
Xu W, Wu Y, Liu W, Anwaier A, Tian X, Su J, Huang H, Wei G, Qu Y, Zhang H and Ye D: Tumor-associated macrophage-derived chemokine CCL5 facilitates the progression and immunosuppressive tumor microenvironment of clear cell renal cell carcinoma. Int J Biol Sci. 18:4884–4900. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Radharani NNV, Yadav AS, Nimma R, Kumar TVS, Bulbule A, Chanukuppa V, Kumar D, Patnaik S, Rapole S and Kundu GC: Tumor-associated macrophage derived IL-6 enriches cancer stem cell population and promotes breast tumor progression via Stat-3 pathway. Cancer Cell Int. 22:1222022. View Article : Google Scholar : PubMed/NCBI | |
|
Valković T, Dobrila F, Melato M, Sasso F, Rizzardi C and Jonjić N: Correlation between vascular endothelial growth factor, angiogenesis, and tumor-associated macrophages in invasive ductal breast carcinoma. Virchows Arch. 440:583–588. 2002. View Article : Google Scholar | |
|
Fu LQ, Du WL, Cai MH, Yao JY, Zhao YY and Mou XZ: The roles of tumor-associated macrophages in tumor angiogenesis and metastasis. Cell Immunol. 353:1041192020. View Article : Google Scholar : PubMed/NCBI | |
|
Wu H, Zhang X, Han D, Cao J and Tian J: Tumour-associated macrophages mediate the invasion and metastasis of bladder cancer cells through CXCL8. PeerJ. 8:e87212020. View Article : Google Scholar : PubMed/NCBI | |
|
Riabov V, Gudima A, Wang N, Mickley A, Orekhov A and Kzhyshkowska J: Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front Physiol. 5:752014. View Article : Google Scholar : PubMed/NCBI | |
|
Kawahara A, Hattori S, Akiba J, Nakashima K, Taira T, Watari K, Hosoi F, Uba M, Basaki Y, Koufuji K, et al: Infiltration of thymidine phosphorylase-positive macrophages is closely associated with tumor angiogenesis and survival in intestinal type gastric cancer. Oncol Rep. 24:405–415. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Hori T, Sasayama T, Tanaka K, Koma YI, Nishihara M, Tanaka H, Nakamizo S, Nagashima H, Maeyama M, Fujita Y, et al: Tumor-associated macrophage related interleukin-6 in cerebrospinal fluid as a prognostic marker for glioblastoma. J Clin Neurosci. 68:281–289. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou M, Na R, Lai S, Guo Y, Shi J, Nie J, Zhang S, Wang Y and Zheng T: The present roles and future perspectives of Interleukin-6 in biliary tract cancer. Cytokine. 169:1562712023. View Article : Google Scholar : PubMed/NCBI | |
|
Sceneay J, Smyth MJ and Möller A: The pre-metastatic niche: Finding common ground. Cancer Metastasis Rev. 32:449–464. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Lu X and Kang Y: Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia. 12:153–162. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, et al: Involvement of chemokine receptors in breast cancer metastasis. Nature. 410:50–56. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, Berman T and Joyce JA: IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 24:241–255. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Q, Zhang XH and Massagué J: Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell. 20:538–549. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Qian B, Deng Y, Im JH, Muschel RJ, Zou Y, Li J, Lang RA and Pollard JW: A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One. 4:e65622009. View Article : Google Scholar : PubMed/NCBI | |
|
Genna A, Duran CL, Entenberg D, Condeelis JS and Cox D: Macrophages Promote tumor cell extravasation across an endothelial barrier through thin membranous connections. Cancers (Basel). 15:20922023. View Article : Google Scholar : PubMed/NCBI | |
|
Chen X, Yang M, Yin J, Li P, Zeng S, Zheng G, He Z, Liu H, Wang Q, Zhang F and Chen D: Tumor-associated macrophages promote epithelial-mesenchymal transition and the cancer stem cell properties in triple-negative breast cancer through CCL2/AKT/β-catenin signaling. Cell Commun Signal. 20:922022. View Article : Google Scholar | |
|
Li X, Shao C, Shi Y and Han W: Lessons learned from the blockade of immune checkpoints in cancer immunotherapy. J Hematol Oncol. 11:312018. View Article : Google Scholar : PubMed/NCBI | |
|
DeNardo DG and Ruffell B: Macrophages as regulators of tumour immunity and immunotherapy. Nat Rev Immunol. 19:369–382. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, et al: Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 10:942–949. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Liu J, Zhang N, Li Q, Zhang W, Ke F, Leng Q and Wang H, Chen J and Wang H: Tumor-associated macrophages recruit CCR6+ regulatory T cells and promote the development of colorectal cancer via enhancing CCL20 production in mice. PLoS One. 6:e194952011. View Article : Google Scholar : PubMed/NCBI | |
|
Arlauckas SP, Garren SB, Garris CS, Kohler RH, Oh J, Pittet MJ and Weissleder R: Arg1 expression defines immunosuppressive subsets of tumor-associated macrophages. Theranostics. 8:5842–5854. 2018. View Article : Google Scholar | |
|
Menjivar RE, Nwosu ZC, Du W, Donahue KL, Hong HS, Espinoza C, Brown K, Velez-Delgado A, Yan W, Lima F, et al: Arginase 1 is a key driver of immune suppression in pancreatic cancer. Elife. 12:e807212023. View Article : Google Scholar : PubMed/NCBI | |
|
Mantovani A, Marchesi F, Malesci A, Laghi L and Allavena P: Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 14:399–416. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Cassetta L and Pollard JW: Targeting macrophages: Therapeutic approaches in cancer. Nat Rev Drug Discov. 17:887–904. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
van der Heide D, Weiskirchen R and Bansal R: Therapeutic targeting of hepatic macrophages for the treatment of liver diseases. Front Immunol. 10:28522019. View Article : Google Scholar : PubMed/NCBI | |
|
Roelofs AJ, Thompson K, Gordon S and Rogers MJ: Molecular mechanisms of action of bisphosphonates: Current status. Clin Cancer Res. 12(20 Pt 2): 6222s–6230s. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Van Acker HH, Anguille S, Willemen Y, Smits EL and Van Tendeloo VF: Bisphosphonates for cancer treatment: Mechanisms of action and lessons from clinical trials. Pharmacol Ther. 158:24–40. 2016. View Article : Google Scholar | |
|
Rogers TL and Holen I: Tumour macrophages as potential targets of bisphosphonates. J Transl Med. 9:1772011. View Article : Google Scholar : PubMed/NCBI | |
|
Van Rooijen N, Kors N, vd Ende M and Dijkstra CD: Depletion and repopulation of macrophages in spleen and liver of rat after intravenous treatment with liposome-encapsulated dichloromethylene diphosphonate. Cell Tissue Res. 260:215–222. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Giraudo E, Inoue M and Hanahan D: An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest. 114:623–633. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Zang X, Zhou J, Zhang X, Chen D, Han Y and Chen X: Dual-targeting tumor cells and tumor associated macrophages with lipid coated calcium zoledronate for enhanced lung cancer chemoimmunotherapy. Int J Pharm. 594:1201742021. View Article : Google Scholar | |
|
Lv J, Chen FK, Liu C, Liu PJ, Feng ZP, Jia L, Yang ZX, Hou F and Deng ZY: Zoledronic acid inhibits thyroid cancer stemness and metastasis by repressing M2-like tumor-associated macrophages induced Wnt/β-catenin pathway. Life Sci. 256:1179252020. View Article : Google Scholar | |
|
Choi J, Lee EJ, Yang SH, Im YR and Seong J: A prospective phase II study for the efficacy of radiotherapy in combination with zoledronic acid in treating painful bone metastases from gastrointestinal cancers. J Radiat Res. 60:242–248. 2019. View Article : Google Scholar : | |
|
D'Incalci M and Galmarini CM: A review of trabectedin (ET-743): A unique mechanism of action. Mol Cancer Ther. 9:2157–2163. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Germano G, Frapolli R, Belgiovine C, Anselmo A, Pesce S, Liguori M, Erba E, Uboldi S, Zucchetti M, Pasqualini F, et al: Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell. 23:249–262. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Belgiovine C, Frapolli R, Liguori M, Digifico E, Colombo FS, Meroni M, Allavena P and D'Incalci M: Inhibition of tumor-associated macrophages by trabectedin improves the antitumor adaptive immunity in response to anti-PD-1 therapy. Eur J Immunol. 51:2677–2686. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
de Sande González LM, Martin-Broto J, Kasper B, Blay JY and Le Cesne A: Real-world evidence of the efficacy and tolerability of trabectedin in patients with advanced soft-tissue sarcoma. Expert Rev Anticancer Ther. 20:957–963. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Romero I, López-Guerrero JA and Pignata S: Real-world experience with trabectedin for the treatment of recurrent ovarian cancer. Expert Rev Anticancer Ther. 21:1089–1095. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Cortinovis D, Grosso F, Carlucci L, Zucali PA, Pasello G, Tiseo M, Sperandi F, Hollander L, Galli F, Torri V, et al: Trabectedin in malignant pleural mesothelioma: Results from the multicentre, single arm, phase II ATREUS study. Clin Lung Cancer. 22:361–370.e3. 2021. View Article : Google Scholar | |
|
Belli C, Piemonti L, D'Incalci M, Zucchetti M, Porcu L, Cappio S, Doglioni C, Allavena P, Ceraulo D, Maggiora P, et al: Phase II trial of salvage therapy with trabectedin in metastatic pancreatic adenocarcinoma. Cancer Chemother Pharmacol. 77:477–484. 2016. View Article : Google Scholar | |
|
Cao Y, Qiao B, Chen Q, Xie Z, Dou X, Xu L, Ran H, Zhang L and Wang Z: Tumor microenvironment remodeling via targeted depletion of M2-like tumor-associated macrophages for cancer immunotherapy. Acta Biomater. 160:239–251. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Kalbasi A, Komar C, Tooker GM, Liu M, Lee JW, Gladney WL, Ben-Josef E and Beatty GL: Tumor-Derived CCL2 mediates resistance to radiotherapy in pancreatic ductal adenocarcinoma. Clin Cancer Res. 23:137–148. 2017. View Article : Google Scholar | |
|
Yang H, Zhang Q, Xu M, Wang L, Chen X, Feng Y, Li Y, Zhang X, Cui W and Jia X: CCL2-CCR2 axis recruits tumor associated macrophages to induce immune evasion through PD-1 signaling in esophageal carcinogenesis. Mol Cancer. 19:412020. View Article : Google Scholar : PubMed/NCBI | |
|
Noel M, O'Reilly EM, Wolpin BM, Ryan DP, Bullock AJ, Britten CD, Linehan DC, Belt BA, Gamelin EC, Ganguly B, et al: Phase 1b study of a small molecule antagonist of human chemokine (C-C motif) receptor 2 (PF-04136309) in combination with nab-paclitaxel/gemcitabine in first-line treatment of metastatic pancreatic ductal adenocarcinoma. Invest New Drugs. 38:800–811. 2020. View Article : Google Scholar : | |
|
Brana I, Calles A, LoRusso PM, Yee LK, Puchalski TA, Seetharam S, Zhong B, de Boer CJ, Tabernero J and Calvo E: Carlumab, an anti-C-C chemokine ligand 2 monoclonal antibody, in combination with four chemotherapy regimens for the treatment of patients with solid tumors: An open-label, multicenter phase 1b study. Target Onco. 10:111–123. 2015. View Article : Google Scholar | |
|
Cherney RJ, Anjanappa P, Selvakumar K, Batt DG, Brown GD, Rose AV, Vuppugalla R, Chen J, Pang J, Xu S, et al: BMS-813160: A Potent CCR2 and CCR5 dual antagonist selected as a clinical candidate. ACS Med Chem Lett. 12:1753–1758. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Lelios I, Cansever D, Utz SG, Mildenberger W, Stifter SA and Greter M: Emerging roles of IL-34 in health and disease. J Exp Med. 217:e201902902020. View Article : Google Scholar : PubMed/NCBI | |
|
Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, Rey-Giraud F, Pradel LP, Feuerhake F, Klaman I, et al: Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell. 25:846–859. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Gomez-Roca CA, Italiano A, Le Tourneau C, Cassier PA, Toulmonde M, D'Angelo SP, Campone M, Weber KL, Loirat D, Cannarile MA, et al: Phase I study of emactuzumab single agent or in combination with paclitaxel in patients with advanced/metastatic solid tumors reveals depletion of immunosuppressive M2-like macrophages. Ann Oncol. 30:1381–1392. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Hua F, Tian Y, Gao Y, Li C and Liu X: Colony-stimulating factor 1 receptor inhibition blocks macrophage infiltration and endometrial cancer cell proliferation. Mol Med Rep. 19:3139–3147. 2019.PubMed/NCBI | |
|
Lee JH, Chen TW, Hsu CH, Yen YH, Yang JC, Cheng AL, Sasaki SI, Chiu LL, Sugihara M, Ishizuka T, et al: A phase I study of pexidartinib, a colony-stimulating factor 1 receptor inhibitor, in Asian patients with advanced solid tumors. Invest New Drugs. 38:99–110. 2020. View Article : Google Scholar : | |
|
Smith BD, Kaufman MD, Wise SC, Ahn YM, Caldwell TM, Leary CB, Lu WP, Tan G, Vogeti L, Vogeti S, et al: Vimseltinib: A Precision CSF1R therapy for tenosynovial giant cell tumors and diseases promoted by macrophages. Mol Cancer Ther. 20:2098–2109. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Nie Y, Huang H, Guo M, Chen J, Wu W, Li W, Xu X, Lin X, Fu W, Yao Y, et al: Breast Phyllodes Tumors Recruit and Repolarize Tumor-Associated Macrophages via Secreting CCL5 to promote malignant progression, which can be inhibited by CCR5 inhibition therapy. Clin Cancer Res. 25:3873–3886. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Altevogt P, Sammar M, Hüser L and Kristiansen G: Novel insights into the function of CD24: A driving force in cancer. Int J Cancer. 148:546–559. 2021. View Article : Google Scholar | |
|
Tarhriz V, Bandehpour M, Dastmalchi S, Ouladsahebmadarek E, Zarredar H and Eyvazi S: Overview of CD24 as a new molecular marker in ovarian cancer. J Cell Physiol. 234:2134–2142. 2019. View Article : Google Scholar | |
|
Barkal AA, Brewer RE, Markovic M, Kowarsky M, Barkal SA, Zaro BW, Krishnan V, Hatakeyama J, Dorigo O, Barkal LJ and Weissman IL: CD24 signalling through macrophage Siglec-10 is a target for cancer immunotherapy. Nature. 572:392–396. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Freile JÁ, Ustyanovska Avtenyuk N, Corrales MG, Lourens HJ, Huls G, van Meerten T, Cendrowicz E and Bremer E: CD24 Is a Potential Immunotherapeutic Target for Mantle Cell Lymphoma. Biomedicines. 10:11752022. View Article : Google Scholar : PubMed/NCBI | |
|
Maute R, Xu J and Weissman IL: CD47-SIRPα-targeted therapeutics: Status and prospects. Immunooncol Technol. 13:1000702022. View Article : Google Scholar | |
|
Schürch CM, Roelli MA, Forster S, Wasmer MH, Brühl F, Maire RS, Di Pancrazio S, Ruepp MD, Giger R, Perren A, et al: Targeting CD47 in anaplastic thyroid carcinoma enhances tumor phagocytosis by macrophages and is a promising therapeutic strategy. Thyroid. 29:979–992. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Nishiga Y, Drainas AP, Baron M, Bhattacharya D, Barkal AA, Ahrari Y, Mancusi R, Ross JB, Takahashi N, Thomas A, et al: Radiotherapy in combination with CD47 blockade elicits a macrophage-mediated abscopal effect. Nat Cancer. 3:1351–1366. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang M, Hutter G, Kahn SA, Azad TD, Gholamin S, Xu CY, Liu J, Achrol AS, Richard C, Sommerkamp P, et al: Anti-CD47 treatment stimulates phagocytosis of glioblastoma by M1 and M2 polarized macrophages and promotes M1 polarized macrophages in vivo. PLoS One. 11:e01535502016. View Article : Google Scholar : PubMed/NCBI | |
|
Advani R, Flinn I, Popplewell L, Forero A, Bartlett NL, Ghosh N, Kline J, Roschewski M, LaCasce A, Collins GP, et al: CD47 Blockade by Hu5F9-G4 and Rituximab in Non-Hodgkin's Lymphoma. N Engl J Med. 379:1711–1721. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zeidan AM, DeAngelo DJ, Palmer J, Seet CS, Tallman MS, Wei X, Raymon H, Sriraman P, Kopytek S, Bewersdorf JP, et al: Phase 1 study of anti-CD47 monoclonal antibody CC-90002 in patients with relapsed/refractory acute myeloid leukemia and high-risk myelodysplastic syndromes. Ann Hematol. 101:557–569. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Solinas G and Becattini B: The role of PI3Kγ in metabolism and macrophage activation. Oncotarget. 8:106145–106146. 2017. View Article : Google Scholar : | |
|
Qiu X, Tian Y, Liang Z, Sun Y, Li Z and Bian J: Recent discovery of phosphoinositide 3-kinase γ inhibitors for the treatment of immune diseases and cancers. Future Med Chem. 11:2151–2169. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Qin H, Yu H, Sheng J, Zhang D, Shen N, Liu L, Tang Z and Chen X: PI3Kgamma inhibitor attenuates immunosuppressive effect of Poly(l-Glutamic Acid)-Combretastatin A4 conjugate in metastatic breast cancer. Adv Sci (Weinh). 6:19003272019. View Article : Google Scholar : PubMed/NCBI | |
|
Carnevalli LS, Taylor MA, King M, Coenen-Stass AML, Hughes AM, Bell S, Proia TA, Wang Y, Ramos-Montoya A, Wali N, et al: Macrophage activation status rather than repolarization is associated with enhanced checkpoint activity in combination with PI3Kγ Inhibition. Mol Cancer Ther. 20:1080–1091. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Hong DS, Postow M, Chmielowski B, Sullivan R, Patnaik A, Cohen EEW, Shapiro G, Steuer C, Gutierrez M, Yeckes-Rodin H, et al: Eganelisib a first-in-class PI3Kγ inhibitor, in patients with advanced solid tumors: Results of the phase 1/1b MARIO-1 trial. Clin Cancer Res. 29:2210–2219. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Brennan JJ and Gilmore TD: Evolutionary Origins of Toll-like Receptor Signaling. Mol Biol Evol. 35:1576–1587. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kim SY, Kim S, Kim JE, Lee SN, Shin IW, Shin HS, Jin SM, Noh YW, Kang YJ, Kim YS, et al: Lyophilizable and multifaceted toll-like receptor 7/8 agonist-loaded nanoemulsion for the reprogramming of tumor microenvironments and enhanced cancer immunotherapy. ACS Nano. 13:12671–12686. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Liu Z, Xie Y, Xiong Y, Liu S, Qiu C, Zhu Z, Mao H, Yu M and Wang X: TLR 7/8 agonist reverses oxaliplatin resistance in colorectal cancer via directing the myeloid-derived suppressor cells to tumoricidal M1-macrophages. Cancer Lett. 469:173–185. 2020. View Article : Google Scholar | |
|
Vidyarthi A, Khan N, Agnihotri T, Negi S, Das DK, Aqdas M, Chatterjee D, Colegio OR, Tewari MK and Agrewala JN: TLR-3 Stimulation Skews M2 Macrophages to M1 Through IFN-αβ signaling and restricts tumor progression. Front Immunol. 9:16502018. View Article : Google Scholar | |
|
Sun L, Kees T, Almeida AS, Liu B, He XY, Ng D, Han X, Spector DL, McNeish IA, Gimotty P, et al: Activating a collaborative innate-adaptive immune response to control metastasis. Cancer Cell. 39:1361–1374.e9. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Chow LQM, Morishima C, Eaton KD, Baik CS, Goulart BH, Anderson LN, Manjarrez KL, Dietsch GN, Bryan JK, Hershberg RM, et al: Phase Ib trial of the toll-like receptor 8 agonist, motolimod (VTX-2337), combined with cetuximab in patients with recurrent or metastatic SCCHN. Clin Cancer Res. 23:2442–2450. 2017. View Article : Google Scholar | |
|
Shayan G, Kansy BA, Gibson SP, Srivastava RM, Bryan JK, Bauman JE, Ohr J, Kim S, Duvvuri U, Clump DA, et al: Phase Ib study of immune biomarker modulation with neoadjuvant cetuximab and TLR8 stimulation in head and neck cancer to overcome suppressive myeloid signals. Clin Cancer Res. 24:62–72. 2018. View Article : Google Scholar : | |
|
Trutnovsky G, Reich O, Joura EA, Holter M, Ciresa-König A, Widschwendter A, Schauer C, Bogner G, Jan Z, Boandl A, et al: Topical imiquimod versus surgery for vulvar intraepithelial neoplasia: A multicentre, randomised, phase 3, non-inferiority trial. Lancet. 399:1790–1798. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y and Noelle RJ: Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev. 229:152–172. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Valencia JC, Erwin-Cohen RA, Clavijo PE, Allen C, Sanford ME, Day CP, Hess MM, Johnson M, Yin J, Fenimore JM, et al: Myeloid-Derived suppressive cell expansion promotes melanoma growth and autoimmunity by inhibiting CD40/IL27 regulation in macrophages. Cancer Res. 81:5977–5990. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Lim CY, Chang JH, Lee WS, Kim J and Park IY: CD40 agonists alter the pancreatic cancer microenvironment by shifting the macrophage phenotype toward M1 and suppress human pancreatic cancer in organotypic slice cultures. Gut Liver. 16:645–659. 2022. View Article : Google Scholar : | |
|
Frankish J, Mukherjee D, Romano E, Billian-Frey K, Schröder M, Heinonen K, Merz C, Redondo Müller M, Gieffers C, Hill O, et al: The CD40 agonist HERA-CD40L results in enhanced activation of antigen presenting cells, promoting an anti-tumor effect alone and in combination with radiotherapy. Front Immunol. 14:11601162023. View Article : Google Scholar : PubMed/NCBI | |
|
Byrne KT, Betts CB, Mick R, Sivagnanam S, Bajor DL, Laheru DA, Chiorean EG, O'Hara MH, Liudahl SM, Newcomb C, et al: Neoadjuvant selicrelumab, an agonist CD40 antibody, induces changes in the tumor microenvironment in patients with resectable pancreatic cancer. Clin Cancer Res. 27:4574–4586. 2021. View Article : Google Scholar : PubMed/NCBI |
