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Oncology

The regulatory network of the chemokine CCL5 in colorectal cancer

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Article: 2205168 | Received 06 Nov 2022, Accepted 15 Apr 2023, Published online: 04 May 2023

References

  • Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):1–11.
  • Zhong Z, Sanchez-Lopez E, Karin M. Autophagy, inflammation, and immunity: a troika governing cancer and its treatment. Cell. 2016;166(2):288–298.
  • Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366(26):2443–2454.
  • Fridman WH, Pages F, Sautes-Fridman C, et al. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12(4):298–306.
  • Ogino S, Galon J, Fuchs CS, et al. Cancer immunology–analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol. 2011;8(12):711–719.
  • Zhang S, Zhong M, Wang C, et al. CCL5-deficiency enhances intratumoral infiltration of CD8(+) T cells in colorectal cancer. Cell Death Dis. 2018;9(7):766.
  • Dangaj D, Bruand M, Grimm AJ, et al. Cooperation between constitutive and inducible chemokines enables T cell engraftment and immune attack in solid tumors. Cancer Cell. 2019;35(6):885.e810–900.e810.
  • Lv D, Zhang Y, Kim HJ, et al. CCL5 as a potential immunotherapeutic target in triple-negative breast cancer. Cell Mol Immunol. 2013;10(4):303–310.
  • Palomino DC, Marti LC. Chemokines and immunity. Einstein. 2015;13(3):469–473.
  • Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004;4(7):540–550.
  • Viola A, Sarukhan A, Bronte V, et al. The pros and cons of chemokines in tumor immunology. Trends Immunol. 2012;33(10):496–504.
  • Romero JM, Grunwald B, Jang GH, et al. A four-chemokine signature is associated with a T-cell-Inflamed phenotype in primary and metastatic pancreatic cancer. Clin Cancer Res. 2020;26(8):1997–2010.
  • Broekman ML, Maas SLN, Abels ER, et al. Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol. 2018;14(8):482–495.
  • Schall TJ, Jongstra J, Dyer BJ, et al. A human T cell-specific molecule is a member of a new gene family. J Immunol. 1988;141(3):1018–1025.
  • Soria G, Ben-Baruch A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett. 2008;267(2):271–285.
  • Hinrichs AC, Blokland SLM, Lopes AP, et al. Transcriptome analysis of CCR9+ T helper cells from primary Sjogren’s syndrome patients identifies CCL5 as a novel effector molecule. Front Immunol. 2021;12:702733.
  • Hinrichs AC, Blokland SLM, Kruize AA, et al. CCL5 release by CCR9+ CD8 T cells: a potential contributor to immunopathology of primary Sjogren’s syndrome. Front Immunol. 2022;13:887972.
  • Mladinich MC, Conde JN, Schutt WR, et al. Blockade of autocrine CCL5 responses inhibits Zika virus persistence and spread in human brain microvascular endothelial cells. mBio. 2021;12(4):e0196221.
  • Liu J, Guan X, Ma X. Interferon regulatory factor 1 is an essential and direct transcriptional activator for interferon {gamma}-induced RANTES/CCl5 expression in macrophages. J Biol Chem. 2005;280(26):24347–24355.
  • Ma J, Shayiti F, Ma J, et al. Tumor-associated macrophage-derived CCL5 promotes chemotherapy resistance and metastasis in prostatic cancer. Cell Biol Int. 2021;45(10):2054–2062.
  • Nagarsheth N, Wicha MS, Zou W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat Rev Immunol. 2017;17(9):559–572.
  • Seki E, De Minicis S, Gwak GY, et al. CCR1 and CCR5 promote hepatic fibrosis in mice. J Clin Invest. 2009;119(7):1858–1870.
  • Roscic-Mrkic B, Fischer M, Leemann C, et al. RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood. 2003;102(4):1169–1177.
  • Bronte V, Bria E. Interfering with CCL5/CCR5 at the tumor-stroma interface. Cancer Cell. 2016;29(4):437–439.
  • Halama N, Zoernig I, Berthel A, et al. Tumoral immune cell exploitation in colorectal cancer metastases can be targeted effectively by anti-CCR5 therapy in cancer patients. Cancer Cell. 2016;29(4):587–601.
  • Suenaga M, Stintzing S, Cao S, et al. Role of CCL5 and CCR5 gene polymorphisms in epidermal growth factor receptor signalling blockade in metastatic colorectal cancer: analysis of the FIRE-3 trial. Eur J Cancer. 2019;107:100–114.
  • Gerard C, Rollins BJ. Chemokines and disease. Nat Immunol. 2001;2(2):108–115.
  • Berger EA, Murphy PM, Farber JM. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol. 1999;17:657–700.
  • Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol. 2014;32:659–702.
  • Rosenbaum DM, Rasmussen SG, Kobilka BK. The structure and function of G-protein-coupled receptors. Nature. 2009;459(7245):356–363.
  • Zazo S, Gonzalez-Alonso P, Martin-Aparicio E, et al. Autocrine CCL5 effect mediates trastuzumab resistance by ERK pathway activation in HER2-positive breast cancer. Mol Cancer Ther. 2020;19(8):1696–1707.
  • Velasco-Velazquez M, Jiao X, De La Fuente M, et al. CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res. 2012;72(15):3839–3850.
  • Weber C, Weber KS, Klier C, et al. Specialized roles of the chemokine receptors CCR1 and CCR5 in the recruitment of monocytes and T(H)1-like/CD45RO(+) T cells. Blood. 2001;97(4):1144–1146.
  • Zernecke A, Shagdarsuren E, Weber C. Chemokines in atherosclerosis: an update. Arterioscler Thromb Vasc Biol. 2008;28(11):1897–1908.
  • Furuichi K, Gao JL, Horuk R, et al. Chemokine receptor CCR1 regulates inflammatory cell infiltration after renal ischemia-reperfusion injury. J Immunol. 2008;181(12):8670–8676.
  • Bertrand CP, Ponath PD. CCR3 blockade as a new therapy for asthma. Expert Opin Investig Drugs. 2000;9(1):43–52.
  • Pease JE. Targeting chemokine receptors in allergic disease. Biochem J. 2011;434(1):11–24.
  • Willems LI, Ijzerman AP. Small molecule antagonists for chemokine CCR3 receptors. Med Res Rev. 2010;30(5):778–817.
  • Pease JE, Horuk R. Recent progress in the development of antagonists to the chemokine receptors CCR3 and CCR4. Expert Opin Drug Discov. 2014;9(5):467–483.
  • Yamaguchi M, Takagi K, Narita K, et al. Stromal CCL5 promotes breast cancer progression by interacting with CCR3 in tumor cells. Int J Mol Sci. 2021;22:1981.
  • Iellem A, Mariani M, Lang R, et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med. 2001;194(6):847–853.
  • Purandare AV, Somerville JE. Antagonists of CCR4 as immunomodulatory agents. Curr Top Med Chem. 2006;6(13):1335–1344.
  • Ishida T, Ueda R. CCR4 as a novel molecular target for immunotherapy of cancer. Cancer Sci. 2006;97(11):1139–1146.
  • Scheu S, Ali S, Ruland C, et al. The C-C chemokines CCL17 and CCL22 and their receptor CCR4 in CNS autoimmunity. Int J Mol Sci. 2017;18:2306.
  • Matsuo K, Nagakubo D, Komori Y, et al. CCR4 is critically involved in skin allergic inflammation of BALB/c mice. J Invest Dermatol. 2018;138(8):1764–1773.
  • Jiao X, Velasco-Velazquez MA, Wang M, et al. CCR5 governs DNA damage repair and breast cancer stem cell expansion. Cancer Res. 2018;78(7):1657–1671.
  • Do HTT, Lee CH, Cho J. Chemokines and their receptors: multifaceted roles in cancer progression and potential value as cancer prognostic markers. Cancers. 2020;12(2):287.
  • Novak M, Koprivnikar Krajnc M, Hrastar B, et al. CCR5-Mediated signaling is involved in invasion of glioblastoma cells in its microenvironment. Int J Mol Sci. 2020;21:4199.
  • Aldinucci D, Borghese C, Casagrande N. Formation of the immunosuppressive microenvironment of classic hodgkin lymphoma and therapeutic approaches to counter it. Int J Mol Sci. 2019;20:2416.
  • Chang LY, Lin YC, Mahalingam J, et al. Tumor-derived chemokine CCL5 enhances TGF-beta-mediated killing of CD8(+) T cells in Colon cancer by T-regulatory cells. Cancer Res. 2012;72(5):1092–1102.
  • Ban Y, Mai J, Li X, et al. Targeting autocrine CCL5-CCR5 axis reprograms immunosuppressive myeloid cells and reinvigorates antitumor immunity. Cancer Res. 2017;77(11):2857–2868.
  • Wang SW, Liu SC, Sun HL, et al. CCL5/CCR5 axis induces vascular endothelial growth factor-mediated tumor angiogenesis in human osteosarcoma microenvironment. Carcinogenesis. 2015;36(1):104–114.
  • Yang X, Hou J, Han Z, et al. One cell, multiple roles: contribution of mesenchymal stem cells to tumor development in tumor microenvironment. Cell Biosci. 2013;3(1):5.
  • Wang X, Lang M, Zhao T, et al. Cancer-FOXP3 directly activated CCL5 to recruit FOXP3(+) treg cells in pancreatic ductal adenocarcinoma. Oncogene. 2017;36(21):3048–3058.
  • Wang B, Qin Y, Wu Q, et al. mTOR signaling pathway regulates the release of proinflammatory molecule CCL5 implicated in the pathogenesis of autism spectrum disorder. Front Immunol. 2022;13:818518.
  • Yang T, Deng Z, Xu L, et al. Macrophages-aPKCi-CCL5 feedback loop modulates the progression and chemoresistance in cholangiocarcinoma. J Exp Clin Cancer Res. 2022;41(1):23.
  • Liu C, Yao Z, Wang J, et al. Correction: macrophage-derived CCL5 facilitates immune escape of colorectal cancer cells via the p65/STAT3-CSN5-PD-L1 pathway. Cell Death Differ. 2020;27(7):2293.
  • Chen D, Bao X, Zhang R, et al. Depiction of the genomic and genetic landscape identifies CCL5 as a protective factor in colorectal neuroendocrine carcinoma. Br J Cancer. 2021;125(7):994–1002.
  • Liu T, Xia Q, Zhang H, et al. CCL5-dependent mast cell infiltration into the tumor microenvironment in clear cell renal cell carcinoma patients. Aging. 2020;12(21):21809–21836.
  • Marin Oyarzun CP, Glembotsky AC, Goette NP, et al. Platelet Toll-Like receptors mediate thromboinflammatory responses in patients with essential thrombocythemia. Front Immunol. 2020;11:705.
  • Chen K, Liu Q, Tsang LL, et al. Human MSCs promotes colorectal cancer epithelial-mesenchymal transition and progression via CCL5/beta-catenin/slug pathway. Cell Death Dis. 2017;8(5):e2819.
  • Keophiphath M, Rouault C, Divoux A, et al. CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler Thromb Vasc Biol. 2010;30(1):39–45.
  • Eriksson EE. Mechanisms of leukocyte recruitment to atherosclerotic lesions: future prospects. Curr Opin Lipidol. 2004;15(5):553–558.
  • Long H, Xie R, Xiang T, et al. Autocrine CCL5 signaling promotes invasion and migration of CD133+ ovarian cancer stem-like cells via NF-kappaB-mediated MMP-9 upregulation. Stem Cells. 2012;30(10):2309–2319.
  • Moriyama M, Hayashida JN, Toyoshima T, et al. Cytokine/chemokine profiles contribute to understanding the pathogenesis and diagnosis of primary Sjogren’s syndrome. Clin Exp Immunol. 2012;169(1):17–26.
  • Manfroi B, De Grandis M, Moreaux J, et al. The microenvironment of DLBCL is characterized by noncanonical macrophages recruited by tumor-derived CCL5. Blood Adv. 2021;5(21):4338–4351.
  • Pham K, Huynh D, Le L, et al. E-cigarette promotes breast carcinoma progression and lung metastasis: macrophage-tumor cells crosstalk and the role of CCL5 and VCAM-1. Cancer Lett. 2020;491:132–145.
  • Wang X, Li X, Wei X, et al. PD-L1 is a direct target of cancer-FOXP3 in pancreatic ductal adenocarcinoma (PDAC), and combined immunotherapy with antibodies against PD-L1 and CCL5 is effective in the treatment of PDAC. Signal Transduct Target Ther. 2020;5:38.
  • Jia J, Zhang H, He L, et al. Cutaneous neurofibroma cells with active Yap promotes proliferation of macrophages resulting in increased accumulation of macrophages by modulating CCL5 and TGFbeta1. Oncol Rep. 2020;43(4):1319–1330.
  • Huang R, Wang S, Wang N, et al. CCL5 derived from tumor-associated macrophages promotes prostate cancer stem cells and metastasis via activating beta-catenin/STAT3 signaling. Cell Death Dis. 2020;11(4):234.
  • Aldinucci D, Casagrande N. Inhibition of the CCL5/CCR5 axis against the progression of gastric cancer. Int J Mol Sci. 2018;19:1477.
  • Marcuzzi E, Angioni R, Molon B, et al. Chemokines and chemokine receptors: orchestrating tumor metastasization. Int J Mol Sci. 2018;20:96.
  • Marech I, Ammendola M, Gadaleta C, et al. Possible biological and translational significance of mast cells density in colorectal cancer. World J Gastroenterol. 2014;20:8910–8920.
  • Coussens LM, Raymond WW, Bergers G, et al. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 1999;13(11):1382–1397.
  • Tanaka T, Ishikawa H. Mast cells and inflammation-associated colorectal carcinogenesis. Semin Immunopathol. 2013;35(2):245–254.
  • Chen Y, Li C, Xie H, et al. Infiltrating mast cells promote renal cell carcinoma angiogenesis by modulating PI3K–>AKT–>GSK3beta–>AM signaling. Oncogene. 2017;36(20):2879–2888.
  • Rigoni A, Colombo MP, Pucillo C. The role of mast cells in molding the tumor microenvironment. Cancer Microenviron. 2015;8(3):167–176.
  • Krstic J, Santibanez JF. Transforming growth factor-beta and matrix metalloproteinases: functional interactions in tumor stroma-infiltrating myeloid cells. ScientificWorldJournal. 2014;2014:521754.
  • Cao P, Ma B, Sun D, et al. Hsa_circ_0003410 promotes hepatocellular carcinoma progression by increasing the ratio of M2/M1 macrophages through the miR-139-3p/CCL5 axis. Cancer Sci. 2022;113(2):634–647.
  • Robinson SC, Scott KA, Balkwill FR. Chemokine stimulation of monocyte matrix metalloproteinase-9 requires endogenous TNF-alpha. Eur J Immunol. 2002;32(2):404–412.
  • Derlindati E, Dei Cas A, Montanini B, et al. Transcriptomic analysis of human polarized macrophages: more than one role of alternative activation? PLOS One. 2015;10(3):e0119751.
  • Rolny C, Mazzone M, Tugues S, et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell. 2011;19(1):31–44.
  • DeNardo DG, Ruffell B. Macrophages as regulators of tumour immunity and immunotherapy. Nat Rev Immunol. 2019;19(6):369–382.
  • Wang D, Li X, Li J, et al. APOBEC3B interaction with PRC2 modulates microenvironment to promote HCC progression. Gut. 2019;68(10):1846–1857.
  • Sheppard KA, Fitz LJ, Lee JM, et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett. 2004;574(1-3):37–41.
  • Gordon SR, Maute RL, Dulken BW, et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature. 2017;545(7655):495–499.
  • Etzerodt A, Tsalkitzi K, Maniecki M, et al. Specific targeting of CD163(+) TAMs mobilizes inflammatory monocytes and promotes T cell-mediated tumor regression. J Exp Med. 2019;216(10):2394–2411.
  • Bottcher JP, Bonavita E, Chakravarty P, et al. NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell. 2018;172(5):1022.e14–1037.e14.
  • Cueto FJ, Del Fresno C, Brandi P, et al. DNGR-1 limits Flt3L-mediated antitumor immunity by restraining tumor-infiltrating type I conventional dendritic cells. J Immunother Cancer. 2021;9(5):e002054.
  • Salmon H, Idoyaga J, Rahman A, et al. Expansion and activation of CD103(+) dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity. 2016;44(4):924–938.
  • Broz ML, Binnewies M, Boldajipour B, et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell. 2014;26(5):638–652.
  • Mittal D, Vijayan D, Putz EM, et al. Interleukin-12 from CD103(+) Batf3-Dependent dendritic cells required for NK-Cell suppression of metastasis. Cancer Immunol Res. 2017;5(12):1098–1108.
  • Zumwalt TJ, Arnold M, Goel A, et al. Active secretion of CXCL10 and CCL5 from colorectal cancer microenvironments associates with GranzymeB + CD8+ T-cell infiltration. Oncotarget. 2015;6(5):2981–2991.
  • Lapteva N, Aldrich M, Weksberg D, et al. Targeting the intratumoral dendritic cells by the oncolytic adenoviral vaccine expressing RANTES elicits potent antitumor immunity. J Immunother. 2009;32(2):145–156.
  • Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239–252.
  • Mueller MM, Fusenig NE. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer. 2004;4(11):839–849.
  • Nishikawa G, Kawada K, Nakagawa J, et al. Bone marrow-derived mesenchymal stem cells promote colorectal cancer progression via CCR5. Cell Death Dis. 2019;10(4):264.
  • Tlsty TD, Coussens LM. Tumor stroma and regulation of cancer development. Annu Rev Pathol. 2006;1:119–150.
  • Seo W, Shimizu K, Kojo S, et al. Runx-mediated regulation of CCL5 via antagonizing two enhancers influences immune cell function and anti-tumor immunity. Nat Commun. 2020;11(1):1562.
  • Cambien B, Richard-Fiardo P, Karimdjee BF, et al. CCL5 neutralization restricts cancer growth and potentiates the targeting of PDGFRbeta in colorectal carcinoma. PLOS One. 2011;6(12):e28842.
  • Sugasawa H, Ichikura T, Kinoshita M, et al. Gastric cancer cells exploit CD4+ cell-derived CCL5 for their growth and prevention of CD8+ cell-involved tumor elimination. Int J Cancer. 2008;122(11):2535–2541.
  • Raghavakaimal A, Cristofanilli M, Tang CM, et al. CCR5 activation and endocytosis in circulating tumor-derived cells isolated from the blood of breast cancer patients provide information about clinical outcome. Breast Cancer Res. 2022;24(1):35.
  • Xu H, Zhao J, Li J, et al. Cancer associated fibroblast-derived CCL5 promotes hepatocellular carcinoma metastasis through activating HIF1alpha/ZEB1 axis. Cell Death Dis. 2022;13(5):478.
  • Yang T, Chen M, Yang X, et al. Down-regulation of KLF5 in cancer-associated fibroblasts inhibit gastric cancer cells progression by CCL5/CCR5 axis. Cancer Biol Ther. 2017;18(10):806–815.
  • Melese ES, Franks E, Cederberg RA, et al. CCL5 production in lung cancer cells leads to an altered immune microenvironment and promotes tumor development. Oncoimmunology. 2022;11(1):2010905.
  • Suenaga M, Cao S, Zhang W, et al. Genetic variants in CCL5 and CCR5 genes and serum VEGF-A levels predict efficacy of bevacizumab in metastatic colorectal cancer patients. Int J Cancer. 2019;144(10):2567–2577.
  • Ucuncu M, Serilmez M, Sari M, et al. The diagnostic significance of PDGF, EphA7, CCR5, and CCL5 levels in colorectal cancer. Biomolecules. 2019;9(9):464.
  • Suenaga M, Schirripa M, Cao S, et al. Gene polymorphisms in the CCL5/CCR5 pathway as a genetic biomarker for outcome and Hand-Foot skin reaction in metastatic colorectal cancer patients treated with regorafenib. Clin Colorectal Cancer. 2018;17(2):e395–e414.
  • Kan JY, Wu DC, Yu FJ, et al. Chemokine (C-C motif) ligand 5 is involved in Tumor-Associated dendritic Cell-Mediated Colon cancer progression through Non-Coding RNA MALAT-1. J Cell Physiol. 2015;230(8):1883–1894.
  • Gao LF, Zhong Y, Long T, et al. Tumor bud-derived CCL5 recruits fibroblasts and promotes colorectal cancer progression via CCR5-SLC25A24 signaling. J Exp Clin Cancer Res. 2022;41(1):81.
  • Zhang Y, Lv D, Kim HJ, et al. A novel role of hematopoietic CCL5 in promoting triple-negative mammary tumor progression by regulating generation of myeloid-derived suppressor cells. Cell Res. 2013;23(3):394–408.
  • Zhao H, Chen D, Cao R, et al. Alcohol consumption promotes colorectal carcinoma metastasis via a CCL5-induced and AMPK-pathway-mediated activation of autophagy. Sci Rep. 2018;8(1):8640.
  • Chen M, Yang X, Yang M, et al. Identification of a novel biomarker-CCL5 using antibody microarray for colorectal cancer. Pathol Res Pract. 2019;215(5):1033–1037.
  • Hu B, Elinav E, Huber S, et al. Microbiota-induced activation of epithelial IL-6 signaling links inflammasome-driven inflammation with transmissible cancer. Proc Natl Acad Sci U S A. 2013;110(24):9862–9867.
  • Sax MJ, Gasch C, Athota VR, et al. Cancer cell CCL5 mediates bone marrow independent angiogenesis in breast cancer. Oncotarget. 2016;7(51):85437–85449.
  • Dwyer RM, Kerin MJ. Mesenchymal stem cells and cancer: tumor-specific delivery vehicles or therapeutic targets? Hum Gene Ther. 2010;21(11):1506–1512.
  • Knoop K, Schwenk N, Schmohl K, et al. Mesenchymal stem cell-mediated, tumor stroma-targeted radioiodine therapy of metastatic Colon cancer using the sodium iodide symporter as theranostic gene. J Nucl Med. 2015;56(4):600–606.
  • Ovais M, Guo M, Chen C. Tailoring nanomaterials for targeting Tumor-Associated macrophages. Adv Mater. 2019;31(19):e1808303.