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Published in: Virology Journal 1/2021

Open Access 01-12-2021 | Review

CC and CXC chemokines play key roles in the development of polyomaviruses related pathological conditions

Authors: Mohammad Hassan Mohammadi, Ashraf Kariminik

Published in: Virology Journal | Issue 1/2021

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Abstract

It has been reported that polyomaviruses are the microbes which can be a cause of several human pathological conditions including cancers, nephropathy, progressive multifocal leukoencephalopathy and gynaecological disease. Although investigators proposed some mechanisms used by the viruses to induce the disorders, the roles played by chemokines in the pathogenesis of polyomaviruses infections are yet to be clarified. This review article investigated recent studies regarding the roles played by chemokines in the pathogenesis of the polyomaviruses infections. The research in the literature revealed that CXC chemokines, including CXCL1, CXCL5, CXCL8, CXCL9, CXCL10, CXCL11, CXCL12 and CXCL16, significantly participate in the pathogenesis of polyomaviruses. CC chemokines, such as CCL2, CCL5 and CCL20 also participate in the induction of the pathological conditions. Therefore, it appears that CXC chemokines may be considered as the strategic factors involved in the pathogenesis of polyomaviruses.
Literature
1.
Van Ghelue M, Khan MT, Ehlers B, Moens U. Genome analysis of the new human polyomaviruses. Rev Med Virol. 2012;22(6):354–77.PubMedCrossRef
2.
Kariminik A. IL-2 and polyoma BK virus infection; a systematic review article. Cytokine. 2016;88:276–80.PubMedCrossRef
3.
4.
White MK, Gordon J, Reiss K, Del Valle L, Croul S, Giordano A, et al. Human polyomaviruses and brain tumors. Brain Res Brain Res Rev. 2005;50(1):69–85.PubMedCrossRef
5.
Kariminik A, Yaghobi R, Dabiri S. Innate immunity and BK virus: prospective strategies. Viral Immunol. 2016;29(2):74–82.PubMedCrossRef
6.
Bodnar RJ. Chemokine regulation of angiogenesis during wound healing. Adv Wound Care (New Rochelle). 2015;4(11):641–50.CrossRef
7.
Myhre MR, Olsen G-H, Gosert R, Hirsch HH, Rinaldo CH. Clinical polyomavirus BK variants with agnogene deletion are non-functional but rescued by trans-complementation. Virology. 2010;398(1):12–20.PubMedCrossRef
8.
Kariminik A, Kheirkhah B. Tumor growth factor-beta is an important factor for immunosuppression and tumorgenesis in Polyoma BK virus infection; a systematic review article. Cytokine. 2017;95:64–9.PubMedCrossRef
9.
Darbinyan A, Siddiqui KM, Slonina D, Darbinian N, Amini S, White MK, et al. Role of JC virus agnoprotein in DNA repair. J Virol. 2004;78(16):8593–600.PubMedPubMedCentralCrossRef
10.
Panou MM, Prescott EL, Hurdiss DL, Swinscoe G, Hollinshead M, Caller LG, et al. Agnoprotein is an essential egress factor during BK polyomavirus infection. Int J Mol Sci. 2018;19(3):902.PubMedCentralCrossRef
11.
Trofe-Clark J, Sawinski D. BK and other polyomaviruses in kidney transplantation. Semin Nephrol. 2016;36(5):372–85.PubMedCrossRef
12.
Padilla-Fernandez B, Bastida-Bermejo J, Virseda-Rodriguez A, Labrador-Gomez J, Caballero-Barrigon D, Silva-Abuin J, et al. Hemorrhagic cytitis after bone marrow transplantation. Arch Esp Urol. 2014;67(2):167–74.PubMed
13.
Sharma SG, Nickeleit V, Herlitz LC, de Gonzalez AK, Stokes MB, Singh HK, et al. BK polyoma virus nephropathy in the native kidney. Nephrol Dial Transplant. 2013;28(3):620–31.PubMedCrossRef
14.
Shakiba E, Yaghobi R, Ramzi M. Prevalence of viral infections and hemorrhagic cystitis in hematopoietic stem cell transplant recipients. Exp Clin Transplant. 2011;9(6):405–12.PubMed
15.
Knowles WA. Discovery and epidemiology of the human polyomaviruses BK virus (BKV) and JC virus (JCV). Adv Exp Med Biol. 2006;577:19–45.PubMedCrossRef
16.
Van Aalderen M, Heutinck K, Huisman C, Ten Berge I. BK virus infection in transplant recipients: clinical manifestations, treatment options and the immune response. Neth J Med. 2012;70(4):172–83.PubMed
17.
Kwun HJ, Chang Y, Moore PS. Protein-mediated viral latency is a novel mechanism for Merkel cell polyomavirus persistence. Proc Natl Acad Sci U S A. 2017;114(20):E4040–7.PubMedPubMedCentralCrossRef
18.
Olsen GH, Hirsch HH, Rinaldo CH. Functional analysis of polyomavirus BK non-coding control region quasispecies from kidney transplant recipients. J Med Virol. 2009;81(11):1959–67.PubMedCrossRef
19.
Olsen GH, Andresen PA, Hilmarsen HT, Bjørang O, Scott H, Midtvedt K, et al. Genetic variability in BK Virus regulatory regions in urine and kidney biopsies from renal-transplant patients. J Med Virol. 2006;78(3):384–93.PubMedCrossRef
20.
Broekema NM, Imperiale MJ. Efficient propagation of archetype BK and JC polyomaviruses. Virology. 2012;422(2):235–41.PubMedCrossRef
21.
Geramizadeh B, Roozbeh J, Malek-Hosseini S-A, Azarpira N, Ayatollahi M, Salahi H, et al. Urine cytology as a useful screening method for polyoma virus nephropathy in renal transplant patients: a single-center experience. Transplant Proc. 2006;38(9):2923–5.PubMedCrossRef
22.
Kaydani GA, Makvandi M, Samarbafzadeh A, Shahbazian H, Fard MH. Prevalence and distribution of BK virus subtypes in renal transplant recipients referred to golestan hospital in Ahvaz, Iran. Jundishapur J Microbiol. 2015;8(3):e16738.PubMedPubMedCentralCrossRef
23.
Baksh FK, Finkelstein SD, Swalsky PA, Stoner GL, Ryschkewitsch CF, Randhawa P. Molecular genotyping of BK and JC viruses in human polyomavirus [ndash] associated interstitial nephritis after renal transplantation. Am J Kidney Dis. 2001;38(2):354–65.PubMedCrossRef
24.
Yogo Y, Sugimoto C, Zheng HY, Ikegaya H, Takasaka T, Kitamura T. JC virus genotyping offers a new paradigm in the study of human populations. Rev Med Virol. 2004;14(3):179–91.PubMedCrossRef
25.
Hirsch HH, Kardas P, Kranz D, Leboeuf C. The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS. 2013;121(8):685–727.PubMedCrossRef
26.
Yogo Y, Sugimoto C, Zhong S, Homma Y. Evolution of the BK polyomavirus: epidemiological, anthropological and clinical implications. Rev Med Virol. 2009;19(4):185–99.PubMedCrossRef
27.
Boldorini R, Allegrini S, Miglio U, Paganotti A, Cocca N, Zaffaroni M, et al. Serological evidence of vertical transmission of JC and BK polyomaviruses in humans. J Gen Virol. 2011;92(5):1044–50.PubMedCrossRef
28.
Dharnidharka VR, Abdulnour HA, Araya CE. The BK virus in renal transplant recipients—review of pathogenesis, diagnosis, and treatment. Pediatr Nephrol. 2011;26(10):1763–74.PubMedCrossRef
29.
Portolani M, Piani M, Gazzanelli G, Borgatti M, Bartoletti A, Grossi M, et al. Restricted replication of BK virus in human lymphocytes. Microbiologica. 1985;8(1):59–66.PubMed
30.
Hirsch HH. Virology, epidemiology, and pathogenesis of JC polyomavirus, BK polyomavirus, and other human polyomaviruses. UpToDate. 2019.
31.
32.
Legler DF, Thelen M. Chemokines: chemistry, biochemistry and biological function. Chimia (Aarau). 2016;70(12):856–9.CrossRef
33.
34.
35.
Bizzarri C, Beccari AR, Bertini R, Cavicchia MR, Giorgini S, Allegretti M. ELR+ CXC chemokines and their receptors (CXC chemokine receptor 1 and CXC chemokine receptor 2) as new therapeutic targets. Pharmacol Ther. 2006;112(1):139–49.PubMedCrossRef
36.
37.
Liu W, Jiang L, Bian C, Liang Y, Xing R, Yishakea M, et al. Role of CX3CL1 in diseases. Arch Immunol Ther Exp (Warsz). 2016;64(5):371–83.CrossRef
38.
Marzocchetti A, Cingolani A, Giambenedetto SD, Ammassari A, Giancola ML, Cauda R, et al. Macrophage chemoattractant protein-1 levels in cerebrospinal fluid correlate with containment of JC virus and prognosis of acquired immunodeficiency syndrome–associated progressive multifocal leukoencephalopathy. J Neurovirol. 2005;11(2):219–24.PubMedCrossRef
39.
De-Simone FI, Sariyer R, Otalora YL, Yarandi S, Craigie M, Gordon J, et al. IFN-Gamma inhibits JC virus replication in glial cells by suppressing T-antigen expression. PLoS ONE. 2015;10(6):e0129694.PubMedPubMedCentralCrossRef
40.
Cason C, Campisciano G, Zanotta N, Valencic E, Delbue S, Bella R, et al. SV40 infection of mesenchymal stromal cells from Wharton’s jelly drives the production of inflammatory and tumoral mediators. J Cell Physiol. 2017;232(11):3060–6.PubMedCrossRef
41.
42.
Kariminik A, Yaghobi R, Dabiri S. CXCL9 expression and polyomavirus BK infectivity in renal transplant patients with nephropathy. Cell Mol Biol (Noisy-le-grand). 2016;62(1):104–8.
43.
Kariminik A, Dabiri S, Yaghobi R. Polyomavirus BK induces inflammation via up-regulation of CXCL10 at translation levels in renal transplant patients with nephropathy. Inflammation. 2016;39(4):1514–9.PubMedCrossRef
44.
Kariminik A, Yaghobi R, Dabiri S. Association of BK virus infection with CXCL11 gene expression and protein levels in kidney transplant patients. Exp Clin Transplant. 2018;16(1):50–4.PubMed
45.
An P, Sáenz Robles MT, Duray AM, Cantalupo PG, Pipas JM. Human polyomavirus BKV infection of endothelial cells results in interferon pathway induction and persistence. PLoS Pathog. 2019;15(1):e1007505.PubMedPubMedCentralCrossRef
46.
Schachtner T, Stein M, Sefrin A, Babel N, Reinke P. Inflammatory activation and recovering BKV-specific immunity correlate with self-limited BKV replication after renal transplantation. Transpl Int. 2014;27(3):290–301.PubMedCrossRef
47.
Jackson JA, Kim EJ, Begley B, Cheeseman J, Harden T, Perez SD, et al. Urinary chemokines CXCL9 and CXCL10 are noninvasive markers of renal allograft rejection and BK viral infection. Am J Transplant. 2011;11(10):2228–34.PubMedPubMedCentralCrossRef
48.
Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol. 2002;168(7):3195–204.PubMedCrossRef
49.
Angiolillo AL, Sgadari C, Taub DD, Liao F, Farber JM, Maheshwari S, et al. Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J Exp Med. 1995;182(1):155–62.PubMedCrossRef
50.
Ribeiro A, Wornle M, Motamedi N, Anders HJ, Grone EF, Nitschko H, et al. Activation of innate immune defense mechanisms contributes to polyomavirus BK-associated nephropathy. Kidney Int. 2012;81(1):100–11.PubMedCrossRef
51.
52.
Yoshio S, Mano Y, Doi H, Shoji H, Shimagaki T, Sakamoto Y, et al. Cytokine and chemokine signatures associated with hepatitis B surface antigen loss in hepatitis B patients. JCI Insight. 2018;3(20):122268.PubMedCrossRef
53.
Chi Y, Zhu Y, Wen T, Cui L, Ge Y, Jiao Y, et al. Cytokine and chemokine levels in patients infected with the novel avian influenza A (H7N9) virus in China. J Infect Dis. 2013;208(12):1962–7.PubMedCrossRef
54.
Comar M, Zanotta N, Bonotti A, Tognon M, Negro C, Cristaudo A, et al. Increased levels of C-C chemokine RANTES in asbestos exposed workers and in malignant mesothelioma patients from an hyperendemic area. PLoS ONE. 2014;9(8):e104848.PubMedPubMedCentralCrossRef
55.
Steiner JL, Davis JM, McClellan JL, Guglielmotti A, Murphy EA. Effects of the MCP-1 synthesis inhibitor bindarit on tumorigenesis and inflammatory markers in the C3(1)/SV40Tag mouse model of breast cancer. Cytokine. 2014;66(1):60–8.PubMedPubMedCentralCrossRef
56.
Wheat R, Roberts C, Waterboer T, Steele J, Marsden J, Steven NM, et al. Inflammatory cell distribution in primary merkel cell carcinoma. Cancers (Basel). 2014;6(2):1047–64.CrossRef
57.
Tran K, Risingsong R, Royce D, Williams CR, Sporn MB, Liby K. The synthetic triterpenoid CDDO-methyl ester delays estrogen receptor-negative mammary carcinogenesis in polyoma middle T mice. Cancer Prev Res (Phila). 2012;5(5):726–34.CrossRef
58.
Ngambenjawong C, Gustafson HH, Pun SH. Progress in tumor-associated macrophage (TAM)-targeted therapeutics. Adv Drug Deliv Rev. 2017;15(114):206–21.CrossRef
59.
Boyle ST, Faulkner JW, McColl SR, Kochetkova M. The chemokine receptor CCR6 facilitates the onset of mammary neoplasia in the MMTV-PyMT mouse model via recruitment of tumor-promoting macrophages. Mol Cancer. 2015;14(115):115.PubMedPubMedCentralCrossRef
60.
Richards KF, Guastafierro A, Shuda M, Toptan T, Moore PS, Chang Y. Merkel cell polyomavirus T antigens promote cell proliferation and inflammatory cytokine gene expression. J Gen Virol. 2015;96(12):3532–44.PubMedPubMedCentralCrossRef
61.
Ribeiro A, Merkle M, Motamedi N, Nitschko H, Koppel S, Wornle M. BK virus infection activates the TNFalpha/TNF receptor system in Polyomavirus-associated nephropathy. Mol Cell Biochem. 2016;411(1–2):191–9.PubMedCrossRef
62.
Boratynska M, Dubinski B, Rybka K, Jezior D, Szyber P, Klinger M. Immunocytological urinalysis and monocyte chemotactic peptide-1 in renal transplant recipients with polyomavirus replication. Transplant Proc. 2006;38(1):151–4.PubMedCrossRef
63.
Hornsby E, Pfeffer PE, Laranjo N, Cruikshank W, Tuzova M, Litonjua AA, et al. Vitamin D supplementation during pregnancy: effect on the neonatal immune system in a randomized controlled trial. J Allergy Clin Immunol. 2018;141(1):269-278.e1.PubMedCrossRef
64.
Darbinyan A, Kaminski R, White MK, Darbinian-Sarkissian N, Khalili K. Polyomavirus JC infection inhibits differentiation of oligodendrocyte progenitor cells. J Neurosci Res. 2013;91(1):116–27.PubMed
65.
Merabova N, Kaminski R, Krynska B, Amini S, Khalili K, Darbinyan A. JCV agnoprotein-induced reduction in CXCL5/LIX secretion by oligodendrocytes is associated with activation of apoptotic signaling in neurons. J Cell Physiol. 2012;227(8):3119–27.PubMedPubMedCentralCrossRef
66.
Zhang XY, Guckian M, Nasiri N, Lovell PA, Dalgleish AG, Barton DP. Normal and SV40 transfected human peritoneal mesothelial cells produce IL-6 and IL-8: implication for gynaecological disease. Clin Exp Immunol. 2002;129(2):288–96.PubMedPubMedCentralCrossRef
67.
Asamitsu K, Sakurada S, Mashiba K, Nakagawa K, Torikai K, Onozaki K, et al. Alteration of the cellular response to interleukin-1 beta by SV40 large T antigen in rheumatoid synovial fibroblasts. Arch Virol. 1999;144(2):317–27.PubMedCrossRef
68.
Qidwai T. Chemokine genetic polymorphism in human health and disease. Immunol Lett. 2016;176:128–38.PubMedCrossRef
69.
Guerini FR, Delbue S, Zanzottera M, Agliardi C, Saresella M, Mancuso R, et al. Analysis of CCR5, CCR2, SDF1 and RANTES gene polymorphisms in subjects with HIV-related PML and not determined leukoencephalopathy. Biomed Pharmacother. 2008;62(1):26–30.PubMedCrossRef
Metadata
Title
CC and CXC chemokines play key roles in the development of polyomaviruses related pathological conditions
Authors
Mohammad Hassan Mohammadi
Ashraf Kariminik
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2021
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-021-01582-4

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