Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-04-30T23:52:15.843Z Has data issue: false hasContentIssue false
  • English
  • Français

Roles of CCR10/CCL27–CCL28 axis in tumour development: mechanisms, diagnostic and therapeutic approaches, and perspectives

Published online by Cambridge University Press:  26 September 2022

Ermias Mergia Terefe ,
Maria Jade Catalan Opulencia ,
Amir Rakhshani ,
Mohammad Javed Ansari ,
Sergushina Elena Sergeevna ,
Sura A. Awadh ,
Djamila Sh. Polatova ,
Adnan Hashim Abdulkadhim ,
Yasser Fakri Mustafa  and
Hamzah H. Kzar
...Show all authors
Ermias Mergia Terefe
Affiliation:
School of Pharmacy and Health Science, United States International University, Nairobi, Kenya
Maria Jade Catalan Opulencia
Affiliation:
College of Business Administration, Ajman University, Ajman, United Arab Emirates
Amir Rakhshani
Affiliation:
Department of Pharmaceutical Nanotechnology, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
Mohammad Javed Ansari
Affiliation:
Department of Pharmaceutics, College of Pharmacy, Prince Sattam Bin Abdulaziz University, Al-Kharj, Saudi Arabia
Sergushina Elena Sergeevna
Affiliation:
National Research Ogarev Mordovia State University, 68, Bolshevitskaya str., 430005 Saransk, Republic of Mordovia, Russia
Sura A. Awadh
Affiliation:
Department of Anesthesia Techniques, Al-Mustaqbal University College, Hillah, Iraq
Djamila Sh. Polatova
Affiliation:
Department of Oncology and Medical Radiology, Tashkent State Dental Institute, Tashkent, Uzbekistan
Adnan Hashim Abdulkadhim
Affiliation:
Department of Computer Engineering, Technical Engineering College, Al-Ayen University, Thi-Qar, Iraq
Yasser Fakri Mustafa
Affiliation:
Department of Pharmaceutical Chemistry, College of Pharmacy, University of Mosul, Mosul 41001, Iraq
Hamzah H. Kzar
Affiliation:
Veterinary Medicine College, Al-Qasim Green University, Al-Qasim, Iraq
Moaed E. Al-Gazally
Affiliation:
College of Medicine, University of Al-Ameed, Karbala, Iraq
Mustafa M. Kadhim
Affiliation:
Department of Dentistry, Kut University College, Kut, Wasit 52001, Iraq College of Technical Engineering, The Islamic University, Najaf, Iraq Department of Pharmacy, Osol Aldeen University College, Baghdad, Iraq
Gholamali Taherian*
Affiliation:
Halal Research Center of IRI, FDA, Tehran, Iran
*
Author for correspondence: Gholamali Taherian, E-mail: rzalitaheri@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Cancer is now one of the major causes of death across the globe. The imbalance of cytokine and chemokine secretion has been reported to be involved in cancer development. Meanwhile, CC chemokines have received considerable interest in cancer research. CCR10, as the latest identified CC chemokine receptor (CCR), has been implicated in the recruitment and infiltration of immune cells, especially lymphocytes, into epithelia such as skin via ligation to two ligands, CCL27 and CCL28. Other than homoeostatic function, several mechanisms have been shown to dysregulate CCR10/CCL27–CCL28 expression in the tumour microenvironment. As such, these receptors and ligands mediate T-cell trafficking in the tumour microenvironment. Depending on the types of lymphocytes recruited, CCR10/CCL27–CCL28 interaction has been shown to play conflicting roles in cancer development. If they were T helper and cytotoxic T cells and natural killer cells, the role of this axis would be tumour-suppressive. In contrast, if CCR10/CCL27–CCL28 recruited regulatory T cells, cancer-associated fibroblasts or myeloid-derived suppressor cells, it would lead to tumour progression. In addition to the trafficking of lymphocytes and immune cells, CCR10 also leads to the migration of tumour cells or endothelial cells (called angiogenesis and lymphangiogenesis) to promote tumour metastasis. Furthermore, CCR10 signalling triggers tumour-promoting signalling such as PI3K/AKT and mitogen-activated protein kinase/extracellular signal-regulated kinase, resulting in tumour cell growth. Since CCR10/CCL27–CCL28 is dysregulated in the tumour tissues, it is suggested that analysis and measurement of them might predict tumour development. Finally, it is hoped using therapeutic approaches based on this axis might increase our knowledge to overcome tumour progression.

Keywords

CancerCCL27CCL28CCR10chemokine
Type
Review
Information
Expert Reviews in Molecular Medicine , Volume 24 , 2022 , e37
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bray, F et al. (2021) The ever-increasing importance of cancer as a leading cause of premature death worldwide. Cancer 127, 3029–3030.CrossRefGoogle ScholarPubMed
Smith, RA and Oeffinger, KC (2020) The importance of cancer screening. The Medical Clinics of North America 104, 919–938.CrossRefGoogle ScholarPubMed
Hanahan, D and Weinberg, RA (2011) Hallmarks of cancer: the next generation. Cell 144, 646–674.CrossRefGoogle ScholarPubMed
Mollica Poeta, V. et al. (2019) Chemokines and chemokine receptors: new targets for cancer immunotherapy. Frontiers in Immunology 10, 379.CrossRefGoogle ScholarPubMed
Bhat, AA et al. (2021) Cytokine-chemokine network driven metastasis in esophageal cancer; promising avenue for targeted therapy. Molecular Cancer 20, 2.CrossRefGoogle ScholarPubMed
Nagarsheth, N, Wicha, MS and Zou, W (2017) Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nature Reviews. Immunology 17, 559–572.CrossRefGoogle ScholarPubMed
Hughes, CE and Nibbs, RJB (2018) A guide to chemokines and their receptors. FEBS Journal 285, 2944–2971.CrossRefGoogle ScholarPubMed
Shabgah, AG et al. (2021) Chemokine CXCL14; a double-edged sword in cancer development. International Immunopharmacology 97, 107681.CrossRefGoogle Scholar
Navashenaq, JG et al. (2020) Doxil chemotherapy plus liposomal P5 immunotherapy decreased myeloid-derived suppressor cells in murine model of breast cancer. Nanomedicine: Nanotechnology, Biology, and Medicine 24, 102150.CrossRefGoogle ScholarPubMed
Zamani, P et al. (2020) Combination therapy with liposomal doxorubicin and liposomal vaccine containing E75, an HER-2/neu-derived peptide, reduces myeloid-derived suppressor cells and improved tumor therapy. Life Sciences, 252.CrossRefGoogle ScholarPubMed
Marchese, A et al. (1994) Cloning of human genes encoding novel G protein-coupled receptors. Genomics 23, 609–618.CrossRefGoogle ScholarPubMed
Jarmin, DI et al. (2000) Cutting edge: identification of the orphan receptor G-protein-coupled receptor 2 as CCR10, a specific receptor for the chemokine ESkine. Journal of Immunology 164, 3460–3464.CrossRefGoogle ScholarPubMed
Morales, J et al. (1999) CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proceedings of the National Academy of Sciences of the USA 96, 14470–5.CrossRefGoogle ScholarPubMed
Pan, J et al. (2000) A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. Journal of Immunology 165, 2943–2949.CrossRefGoogle ScholarPubMed
Wang, W et al. (2000) Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). Journal of Biological Chemistry 275, 22313–22323.CrossRefGoogle Scholar
Bonini, JA et al. (1997) Cloning, expression, and chromosomal mapping of a novel human CC-chemokine receptor (CCR10) that displays high-affinity binding for MCP-1 and MCP-3. DNA and Cell Biology 16, 1249–1256.CrossRefGoogle ScholarPubMed
Allen, SJ, Crown, SE and Handel, TM (2007) Chemokine:receptor structure, interactions, and antagonism. Annual Review of Immunology 25, 787–820.CrossRefGoogle ScholarPubMed
Lazarus, NH et al. (2003) A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. Journal of Immunology 170, 3799–3805.CrossRefGoogle ScholarPubMed
Mickanin, CS, Bhatia, U and Labow, M (2001) Identification of a novel beta-chemokine, MEC, down-regulated in primary breast tumors. International Journal of Oncology 18, 939–944.Google ScholarPubMed
Homey, B et al. (2002) CCL27–CCR10 interactions regulate T cell-mediated skin inflammation. Nature Medicine 8, 157–165.CrossRefGoogle ScholarPubMed
Jansma, AL et al. (2010) NMR analysis of the structure, dynamics, and unique oligomerization properties of the chemokine CCL27. The Journal of Biological Chemistry 285, 14424–14437.CrossRefGoogle ScholarPubMed
Nibbs, RJ and Graham, GJ (2003) CCL27/PESKY: a novel paradigm for chemokine function. Expert Opinion on Biological Therapy 3, 15–22.CrossRefGoogle ScholarPubMed
Gortz, A et al. (2002) The chemokine ESkine/CCL27 displays novel modes of intracrine and paracrine function. Journal of Immunology 169, 1387–1394.CrossRefGoogle ScholarPubMed
John, AE et al. (2005) Temporal production of CCL28 corresponds to eosinophil accumulation and airway hyperreactivity in allergic airway inflammation. American Journal of Pathology 166, 345–353.CrossRefGoogle ScholarPubMed
Dimberg, J, Hugander, A and Wågsäter, D (2006) Protein expression of the chemokine, CCL28, in human colorectal cancer. International Journal of Oncology 28, 315–319.Google ScholarPubMed
Maghazachi, AA, Sand, KL and Al-Jaderi, Z (2016) Glatiramer acetate, dimethyl fumarate, and monomethyl fumarate upregulate the expression of CCR10 on the surface of natural killer cells and enhance their chemotaxis and cytotoxicity. Frontiers in Immunology 7, 291–299.CrossRefGoogle ScholarPubMed
Pivarcsi, A et al. (2007) Tumor immune escape by the loss of homeostatic chemokine expression. Proceedings of the National Academy of Sciences of the United States of America 104, 19055–19060.CrossRefGoogle ScholarPubMed
Lin, HY et al. (2017) CCR10 activation stimulates the invasion and migration of breast cancer cells through the ERK1/2/MMP-7 signaling pathway. International Immunopharmacology 51, 124–130.CrossRefGoogle ScholarPubMed
Yang, XL et al. (2017) CCL28 promotes breast cancer growth and metastasis through MAPK-mediated cellular anti-apoptosis and pro-metastasis. Oncology Reports 38, 1393–1401.CrossRefGoogle ScholarPubMed
Gao, JQ et al. (2009) NK cells are migrated and indispensable in the anti-tumor activity induced by CCL27 gene therapy. Cancer Immunology Immunotherapy 58, 291–299.CrossRefGoogle ScholarPubMed
Degos, C et al. (2019) Endometrial tumor microenvironment alters human NK cell recruitment, and resident NK cell phenotype and function. Frontiers in Immunology 10, 877.CrossRefGoogle ScholarPubMed
Gao, JQ et al. (2007) Cotransduction of CCL27 gene can improve the efficacy and safety of IL-12 gene therapy for cancer. Gene Therapy 14, 491–502.CrossRefGoogle ScholarPubMed
Harasawa, H et al. (2006) Survey of chemokine receptor expression reveals frequent co-expression of skin-homing CCR4 and CCR10 in adult T-cell leukemia/lymphoma. Leukemia & Lymphoma 47, 2163–2173.CrossRefGoogle ScholarPubMed
Fujita, Y et al. (2006) Presence of circulating CCR10 + T cells and elevated serum CTACK/CCL27 in the early stage of mycosis fungoides. Clinical Cancer Research 12, 2670–2675.CrossRefGoogle ScholarPubMed
Notohamiprodjo, M et al. (2005) CCR10 is expressed in cutaneous T-cell lymphoma. International Journal of Cancer 115, 641–647.CrossRefGoogle ScholarPubMed
Hanamoto, H et al. (2004) Expression of CCL28 by Reed-Sternberg cells defines a major subtype of classical Hodgkin's disease with frequent infiltration of eosinophils and/or plasma cells. The American Journal of Pathology 164, 997–1006.CrossRefGoogle ScholarPubMed
Goteri, G et al. (2012) Serum and tissue CTACK/CCL27 chemokine levels in early mycosis fungoides may be correlated with disease-free survival following treatment with interferon alfa and psoralen plus ultraviolet A therapy. British Journal of Dermatology 166, 948–952.CrossRefGoogle ScholarPubMed
Hoeller, C et al. (2009) In vivo imaging of cutaneous T-cell lymphoma migration to the skin. Cancer Research 69, 2704–2708.CrossRefGoogle ScholarPubMed
Masui, Y et al. (2007) Sézary syndrome treated with narrowband ultraviolet B: time-course measurement of serum levels of CCL17/CCL27. Clinical and Experimental Dermatology 32, 57–59.CrossRefGoogle ScholarPubMed
Zhong, W et al. (2020) Serum CCL27 predicts the response to Bacillus Calmette–Guerin immunotherapy in non-muscle-invasive bladder cancer. Oncoimmunology 9, 1776060–60.CrossRefGoogle ScholarPubMed
Wu, Q et al. (2018) The chemokine receptor CCR10 promotes inflammation-driven hepatocarcinogenesis via PI3K/Akt pathway activation. Cell Death & Disease 9, 232.CrossRefGoogle ScholarPubMed
Ren, L et al. (2016) Hypoxia-induced CCL28 promotes recruitment of regulatory T cells and tumor growth in liver cancer. Oncotarget 7, 75763–75773.CrossRefGoogle ScholarPubMed
Thangavadivel, S et al. (2016) CCR10/CCL27 crosstalk contributes to failure of proteasome-inhibitors in multiple myeloma. Oncotarget 7, 78605–78618.CrossRefGoogle ScholarPubMed
Murakami, T et al. (2003) Immune evasion by murine melanoma mediated through CC chemokine receptor-10. The Journal of Experimental Medicine 198, 1337–1347.CrossRefGoogle ScholarPubMed
Simonetti, O et al. (2006) Potential role of CCL27 and CCR10 expression in melanoma progression and immune escape. European Journal of Cancer 42, 1181–1187.CrossRefGoogle ScholarPubMed
Martinez-Rodriguez, M, Thompson, AK and Monteagudo, C (2017) High CCL27 immunoreactivity in ‘supratumoral’ epidermis correlates with better prognosis in patients with cutaneous malignant melanoma. Journal of Clinical Pathology 70, 15–19.CrossRefGoogle ScholarPubMed
Kühnelt-Leddihn, L et al. (2012) Overexpression of the chemokine receptors CXCR4, CCR7, CCR9, and CCR10 in human primary cutaneous melanoma: a potential prognostic value for CCR7 and CCR10? Archives of Dermatological Research 304, 185–193.CrossRefGoogle ScholarPubMed
Monteagudo, C et al. (2012) CCL27–CCR10 and CXCL12-CXCR4 chemokine ligand-receptor mRNA expression ratio: new predictive factors of tumor progression in cutaneous malignant melanoma. Clinical & Experimental Metastasis 29, 625–637.CrossRefGoogle ScholarPubMed
Park, J et al. (2019) CCL28-induced RARβ expression inhibits oral squamous cell carcinoma bone invasion. The Journal of Clinical Investigation 129, 5381–5399.CrossRefGoogle ScholarPubMed
Facciabene, A et al. (2011) Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 475, 226–230.CrossRefGoogle Scholar
Chen, L et al. (2014) Upregulation of chemokine receptor CCR10 is essential for glioma proliferation, invasion and patient survival. Oncotarget 5, 6576–6583.CrossRefGoogle ScholarPubMed
Liu, B and Wei, C (2021) Hypoxia induces overexpression of CCL28 to recruit Treg cells to enhance angiogenesis in lung adenocarcinoma. Journal of Environmental Pathology Toxicology and Oncology 40, 65–74.CrossRefGoogle ScholarPubMed
Huang, G et al. (2016) Hypoxia induced CCL28 promotes angiogenesis in lung adenocarcinoma by targeting CCR3 on endothelial cells. Scientific Reports 6, 27152.CrossRefGoogle ScholarPubMed
Lin, D et al. (2020) Dispensable role of CCL28 in Kras-mutated non-small cell lung cancer mouse models. Acta Biochimica et Biophysica Sinica 52, 691–694.CrossRefGoogle ScholarPubMed
Ji, L et al. (2020) Blockade of β-catenin-induced CCL28 suppresses gastric cancer progression via inhibition of Treg cell infiltration. Cancer Research 80, 2004–2016.CrossRefGoogle ScholarPubMed
Zou, HY et al. (2016) A truncated splice variant of human lysyl oxidase-like 2 promotes migration and invasion in esophageal squamous cell carcinoma. International Journal of Biochemistry & Cell Biology 75, 85–98.CrossRefGoogle ScholarPubMed
Ribatti, D (2017) The concept of immune surveillance against tumors. The first theories. Oncotarget 8, 7175–7180.CrossRefGoogle ScholarPubMed
Gao, JQ et al. (2003) Antitumor effect by interleukin-11 receptor alpha-locus chemokine/CCL27, introduced into tumor cells through a recombinant adenovirus vector. Cancer Research 63, 4420–4425.Google ScholarPubMed
Guo, YJ et al. (2020) ERK/MAPK signalling pathway and tumorigenesis. Experimental and Therapeutic Medicine 19, 1997–2007.Google ScholarPubMed
Pinto, A. et al. (1997) The role of eosinophils in the pathobiology of Hodgkin's disease. Annals of Oncology 8 (suppl. 2), 89–96.CrossRefGoogle ScholarPubMed
Pinto, A et al. (1996) Human eosinophils express functional CD30 ligand and stimulate proliferation of a Hodgkin's disease cell line. Blood 88, 3299–3305.CrossRefGoogle ScholarPubMed
Alitalo, A and Detmar, M (2012) Interaction of tumor cells and lymphatic vessels in cancer progression. Oncogene 31, 4499–4508.CrossRefGoogle ScholarPubMed
Karnezis, T et al. (2019) CCL27/CCL28-CCR10 chemokine signaling mediates migration of lymphatic endothelial cells. Cancer Research 79, 1558–1572.CrossRefGoogle ScholarPubMed
Arezoo, GS et al. (2021) The role of non-coding genome in cancer-associated fibroblasts; state-of- the-art and perspectives in cancer targeted therapy. Current Drug Targets 22, 1524–1535.Google Scholar
Roy, I et al. (2017) Cancer cell chemokines direct chemotaxis of activated stellate cells in pancreatic ductal adenocarcinoma. Laboratory Investigation; A Journal of Technical Methods and Pathology 97, 302–317.CrossRefGoogle ScholarPubMed
Taghizadeh, E et al. (2019) Macrophage: a key therapeutic target in atherosclerosis? Current Pharmaceutical Design 25, 3165–3174.CrossRefGoogle ScholarPubMed
Kai, H et al. (2011) CCR10 and CCL27 are overexpressed in cutaneous squamous cell carcinoma. Pathology Research and Practice 207, 43–48.CrossRefGoogle ScholarPubMed
Mao, MJ et al. (2018) Chemokine CCL27 is a novel plasma biomarker for identification the nasopharyngeal carcinoma patients from the Epstein–Barr virus capsid antigen-specific IgA seropositive population. BMC Cancer 18, 9.CrossRefGoogle ScholarPubMed
Kagami, S et al. (2006) Elevated serum CTACK/CCL27 levels in CTCL. Journal of Investigative Dermatology 126, 1189–1191.CrossRefGoogle ScholarPubMed
Sokolowska-Wojdylo, M et al. (2005) Circulating clonal CLA(+) and CD4(+) T cells in Sezary syndrome express the skin-homing chemokine receptors CCR4 and CCR10 as well as the lymph node-homing chemokine receptor CCR7. British Journal of Dermatology 152, 258–264.CrossRefGoogle ScholarPubMed
Grant, SW, Collins, GS and Nashef, SAM (2018) Statistical primer: developing and validating a risk prediction model. European Journal of Cardio-Thoracic Surgery 54, 203–208.CrossRefGoogle ScholarPubMed
Wang, J et al. (2020) A novel prognostic signature of immune-related genes for patients with colorectal cancer. Journal of Cellular and Molecular Medicine 24, 8491–8504.CrossRefGoogle ScholarPubMed
Titeca, K et al. (2019) Discovering cellular protein–protein interactions: technological strategies and opportunities. Mass Spectrometry Reviews 38, 79–111.CrossRefGoogle ScholarPubMed
Wang, F et al. (2020) Prognostic value of TP53 co-mutation status combined with EGFR mutation in patients with lung adenocarcinoma. Journal of Cancer Research and Clinical Oncology 146, 2851–2859.CrossRefGoogle ScholarPubMed
Chen, L et al. (2019) Identification of biomarkers associated with diagnosis and prognosis of colorectal cancer patients based on integrated bioinformatics analysis. Gene 692, 119–125.CrossRefGoogle ScholarPubMed
McLaren, PJ et al. (2017) Specific gene expression profiles are associated with a pathologic complete response to neoadjuvant therapy in esophageal adenocarcinoma. American Journal of Surgery 213, 915–920.CrossRefGoogle ScholarPubMed
Krech, T et al. (2012) ABCB1/MDR1 contributes to the anticancer drug-resistant phenotype of IPH-926 human lobular breast cancer cells. Cancer Letters 315, 153–160.CrossRefGoogle Scholar
Tsao, DA et al. (2010) Gene expression profiles for predicting the efficacy of the anticancer drug 5-fluorouracil in breast cancer. DNA and Cell Biology 29, 285–293.CrossRefGoogle ScholarPubMed
Supiot, S et al. (2013) Early dynamic transcriptomic changes during preoperative radiotherapy in patients with rectal cancer: a feasibility study. World Journal of Gastroenterology 19, 3249–3254.CrossRefGoogle ScholarPubMed
Conlon, KC, Miljkovic, MD and Waldmann, TA (2019) Cytokines in the treatment of cancer. Journal of Interferon and Cytokine Research 39, 6–21.CrossRefGoogle ScholarPubMed
Lu, R-M et al. (2020) Development of therapeutic antibodies for the treatment of diseases. Journal of Biomedical Science 27, 1.CrossRefGoogle ScholarPubMed