nach oben

Journal of NeuroVirology

Erschienen in:

02.09.2023 | Review

Revisiting JC virus and progressive multifocal leukoencephalopathy

verfasst von: Angela Rocchi, Ilker K. Sariyer, Joseph R. Berger

Erschienen in: Journal of NeuroVirology | Ausgabe 5/2023

Einloggen, um Zugang zu erhalten

Abstract

Since its definition 65 years ago, progressive multifocal leukoencephalopathy (PML) has continued to devastate a growing population of immunosuppressed patients despite major advances in our understanding of the causative JC virus (JCV). Unless contained by the immune system, JCV lyses host oligodendrocytes collateral to its life cycle, leading to demyelination, neurodegeneration, and death. Novel treatments have stagnated in the absence of an animal model while current antiviral agents fail to address the now ubiquitous polyomavirus. In this review, we highlight the established pathogenesis by which JCV infection progresses to PML, highlighting major challenges that must be overcome to eliminate the underlying virus and, therefore, the debilitating disease.

Abbott TR, Dhamdhere G, Liu Y et al (2020) Development of CRISPR as an antiviral strategy to combat SARS-CoV-2 and influenza. Cell 181:865-876.e12. https://doi.org/10.1016/j.cell.2020.04.020CrossRefPubMedPubMedCentral

Agostini HT, Ryschkewitsch CF, Singer EJ, Stoner GL (1997) JC virus regulatory region rearrangements and genotypes in progressive multifocal leukoencephalopathy: two independent aspects of virus variation. J Gen Virol 78:659–664. https://doi.org/10.1099/0022-1317-78-3-659CrossRefPubMed

Akan I, Sariyer IK, Biffi R et al (2006) Human polyomavirus JCV late leader peptide region contains important regulatory elements. Virology 349:66–78. https://doi.org/10.1016/j.virol.2006.01.025CrossRefPubMed

Anand P, Hotan GC, Vogel A et al (2019) Progressive multifocal leukoencephalopathy: a 25-year retrospective cohort study. Neurol Neuroimmunol Neuroinflamm 6:e618. https://doi.org/10.1212/NXI.0000000000000618

Astrom KE, Mancall EL, Richardson EP (1958) Progressive multifocal leuko-encephalopathy; a hitherto unrecognized complication of chronic lymphatic leukaemia and Hodgkin’s disease. Brain 81:93–111. https://doi.org/10.1093/brain/81.1.93CrossRefPubMed

Ault GS (1997) Activity of JC virus archetype and PML-type regulatory regions in glial cells. J Gen Virol 78(Pt 1):163–169. https://doi.org/10.1099/0022-1317-78-1-163CrossRefPubMed

Ault GS, Stoner GL (1993) Human polyomavirus JC promoter/enhancer rearrangement patterns from progressive multifocal leukoencephalopathy brain are unique derivatives of a single archetypal structure. J Gen Virol 74(Pt 8):1499–1507. https://doi.org/10.1099/0022-1317-74-8-1499CrossRefPubMed

Bakal JA, Charlton CL, Hlavay B et al (2021) Progressive multifocal leukoencephalopathy and Creutzfeldt-Jakob disease: population-wide incidences, comorbidities, costs of care, and outcomes. J Neurovirol 27:476–481. https://doi.org/10.1007/s13365-021-00983-zCrossRefPubMed

Bao Z, Fang K, Miao Z et al (2021) Human cerebral organoid implantation alleviated the neurological deficits of traumatic brain injury in mice. Oxid Med Cell Longev 2021:6338722. https://doi.org/10.1155/2021/6338722CrossRefPubMedPubMedCentral

Barreras P, Pamies D, Monaco MC et al (2022) A human-derived 3D brain organoid model to study JC virus infection. J Neurovirol 28:17–26. https://doi.org/10.1007/s13365-022-01062-7CrossRefPubMedPubMedCentral

Berger JR (2014) Chapter 17 - Progressive multifocal leukoencephalopathy. In: Tselis AC, Booss J (eds) Handbook of Clinical Neurology. Elsevier, pp 357–376

Berger JR, Aksamit AJ, Clifford DB et al (2013a) PML diagnostic criteria: consensus statement from the AAN Neuroinfectious Disease Section. Neurology 80:1430–1438. https://doi.org/10.1212/WNL.0b013e31828c2fa1CrossRefPubMedPubMedCentral

Berger JR, Hartung H-P (2023) Commentary: progressive multifocal leukoencephalopathy genetic risk variants for pharmacovigilance of immunosuppressant therapies. Front Neurol 14:1146027. https://doi.org/10.3389/fneur.2023.1146027CrossRefPubMedPubMedCentral

Berger JR, Houff SA, Gurwell J et al (2013b) JC virus antibody status underestimates infection rates. Ann Neurol 74:84–90. https://doi.org/10.1002/ana.23893CrossRefPubMedPubMedCentral

Berger JR, Koralnik IJ (2005) Progressive multifocal leukoencephalopathy and natalizumab–unforeseen consequences. N Engl J Med 353:414–416. https://doi.org/10.1056/NEJMe058122CrossRefPubMed

Bofill-Mas S, Clemente-Casares P, Major EO et al (2003) Analysis of the excreted JC virus strains and their potential oral transmission. J Neurovirol 9:498–507. https://doi.org/10.1080/13550280390218887CrossRefPubMed

Bofill-Mas S, Formiga-Cruz M, Clemente-Casares P et al (2001) Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J Virol 75:10290–10299. https://doi.org/10.1128/JVI.75.21.10290-10299.2001CrossRefPubMedPubMedCentral

Bofill-Mas S, Girones R (2003) Role of the environment in the transmission of JC virus. J Neurovirol 9:54–58. https://doi.org/10.1080/13550280390195306CrossRefPubMed

Bollag B, Hofstetter CA, Reviriego-Mendoza MM, Frisque RJ (2010) JC virus small T antigen binds phosphatase PP2A and Rb family proteins and is required for efficient viral DNA replication activity. PLoS One 5:e10606. https://doi.org/10.1371/journal.pone.0010606

Brambilla AM, Castagna A, Novati R et al (1999) Remission of AIDS-associated progressive multifocal leukoencephalopathy after cidofovir therapy. J Neurol 246:723–725. https://doi.org/10.1007/s004150050440CrossRefPubMed

Brickelmaier M, Lugovskoy A, Kartikeyan R et al (2009) Identification and characterization of mefloquine efficacy against JC virus in vitro. Antimicrob Agents Chemother 53:1840–1849. https://doi.org/10.1128/AAC.01614-08CrossRefPubMedPubMedCentral

Chapagain ML, Sumibcay L, Gurjav U et al (2008) Serotonin receptor 2A blocker (risperidone) has no effect on human polyomavirus JC infection of primary human fetal glial cells. J Neurovirol 14:448–454. https://doi.org/10.1080/13550280802235916CrossRefPubMedPubMedCentral

Chen NN, Kerr D, Chang CF et al (1997) Evidence for regulation of transcription and replication of the human neurotropic virus JCV genome by the human S(mu)bp-2 protein in glial cells. Gene 185:55–62. https://doi.org/10.1016/s0378-1119(96)00630-0CrossRefPubMed

Cheng Y, Ma N, Witt C et al (2021) Face masks effectively limit the probability of SARS-CoV-2 transmission. Science 372:1439–1443. https://doi.org/10.1126/science.abg6296CrossRefPubMedPubMedCentral

Chiang C, Dvorkin S, Chiang JJ et al (2021) The small t antigen of JC virus antagonizes RIG-I-mediated innate immunity by inhibiting TRIM25’s RNA binding ability. mBio 12:e00620–21. https://doi.org/10.1128/mBio.00620-21

Christensen KLY, Holman RC, Hammett TA et al (2010) Progressive multifocal leukoencephalopathy deaths in the USA, 1979–2005. Neuroepidemiology 35:178–184. https://doi.org/10.1159/000311014CrossRefPubMed

Cortese I, Muranski P, Enose-Akahata Y et al (2019) Pembrolizumab treatment for progressive multifocal leukoencephalopathy. N Engl J Med 380:1597–1605. https://doi.org/10.1056/NEJMoa1815039CrossRefPubMed

Cortese I, Reich DS, Nath A (2021) Progressive multifocal leukoencephalopathy and the spectrum of JC virus-related disease. Nat Rev Neurol 17:37–51. https://doi.org/10.1038/s41582-020-00427-yCrossRefPubMed

Dang X, Axthelm MK, Letvin NL, Koralnik IJ (2005) Rearrangement of simian virus 40 regulatory region is not required for induction of progressive multifocal leukoencephalopathy in immunosuppressed rhesus monkeys. J Virol 79:1361–1366. https://doi.org/10.1128/JVI.79.3.1361-1366.2005CrossRefPubMedPubMedCentral

Daniel AM, Swenson JJ, Mayreddy RP et al (1996) Sequences within the early and late promoters of archetype JC virus restrict viral DNA replication and infectivity. Virology 216:90–101. https://doi.org/10.1006/viro.1996.0037CrossRefPubMed

Daniel DC, Wortman MJ, Schiller RJ et al (2001) Coordinate effects of human immunodeficiency virus type 1 protein Tat and cellular protein Puralpha on DNA replication initiated at the JC virus origin. J Gen Virol 82:1543–1553. https://doi.org/10.1099/0022-1317-82-7-1543CrossRefPubMed

Daniels R, Rusan NM, Wadsworth P, Hebert DN (2006) SV40 VP2 and VP3 insertion into ER membranes is controlled by the capsid protein VP1: implications for DNA translocation out of the ER. Mol Cell 24:955–966. https://doi.org/10.1016/j.molcel.2006.11.001CrossRefPubMed

d’Arminio Monforte A, Cinque P, Vago L et al (1997) A comparison of brain biopsy and CSF-PCR in the diagnosis of CNS lesions in AIDS patients. J Neurol 244:35–39. https://doi.org/10.1007/pl00007727CrossRefPubMed

Dash PK, Kaminski R, Bella R et al (2019) Sequential LASER ART and CRISPR treatments eliminate HIV-1 in a subset of infected humanized mice. Nat Commun 10:2753. https://doi.org/10.1038/s41467-019-10366-yCrossRefPubMedPubMedCentral

Datta PK, Kaminski R, Hu W et al (2016) HIV-1 latency and eradication: past, present and future. Curr HIV Res 14:431–441. https://doi.org/10.2174/1570162x14666160324125536CrossRefPubMedPubMedCentral

De Luca A, Ammassari A, Pezzotti P et al (2008) Cidofovir in addition to antiretroviral treatment is not effective for AIDS-associated progressive multifocal leukoencephalopathy: a multicohort analysis. AIDS 22:1759–1767. https://doi.org/10.1097/QAD.0b013e32830a5043CrossRefPubMed

De Luca A, Fantoni M, Tartaglione T, Antinori A (1999) Response to cidofovir after failure of antiretroviral therapy alone in AIDS-associated progressive multifocal leukoencephalopathy. Neurology 52:891–892. https://doi.org/10.1212/wnl.52.4.891CrossRefPubMed

Deckhut AM, Tevethia MJ, Haggerty S et al (1991) Localization of common cytotoxic T lymphocyte recognition epitopes on simian papovavirus SV40 and human papovavirus JC virus T antigens. Virology 183:122–132. https://doi.org/10.1016/0042-6822(91)90125-uCrossRefPubMed

Del Valle L, Khalili K (2021) Induction of brain tumors by the archetype strain of human neurotropic JCPyV in a transgenic mouse model. Viruses 13:162. https://doi.org/10.3390/v13020162CrossRefPubMedPubMedCentral

Del Valle L, White MK, Enam S et al (2005) Detection of JC virus DNA sequences and expression of viral T antigen and agnoprotein in esophageal carcinoma. Cancer 103:516–527. https://doi.org/10.1002/cncr.20806CrossRefPubMed

Devireddy LR, Kumar KU, Pater MM, Pater A (2000) BAG-1, a novel Bcl-2-interacting protein, activates expression of human JC virus. J Gen Virol 81:351–357. https://doi.org/10.1099/0022-1317-81-2-351CrossRefPubMed

Dolci M, Favero C, Bollati V et al (2018) Particulate matter exposure increases JC polyomavirus replication in the human host. Environ Pollut 241:234–239. https://doi.org/10.1016/j.envpol.2018.05.044CrossRefPubMed

Dong X, Xu S-B, Chen X et al (2021) Human cerebral organoids establish subcortical projections in the mouse brain after transplantation. Mol Psychiatry 26:2964–2976. https://doi.org/10.1038/s41380-020-00910-4CrossRefPubMed

Dsilva L, McCarthy K, Lyons J et al (2023) Progressive multifocal leukoencephalopathy with natalizumab extended or standard interval dosing in the United States and the rest of the world. Expert Opinion on Drug Safety 0:1–8. https://doi.org/10.1080/14740338.2023.2221027

Du Pasquier RA, Clark KW, Smith PS et al (2001) JCV-specific cellular immune response correlates with a favorable clinical outcome in HIV-infected individuals with progressive multifocal leukoencephalopathy. J Neurovirol 7:318–322. https://doi.org/10.1080/13550280152537175CrossRefPubMed

Du Pasquier RA, Kuroda MJ, Zheng Y et al (2004) A prospective study demonstrates an association between JC virus-specific cytotoxic T lymphocytes and the early control of progressive multifocal leukoencephalopathy. Brain 127:1970–1978. https://doi.org/10.1093/brain/awh215CrossRefPubMed

Egli A, Infanti L, Dumoulin A et al (2009) Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis 199:837–846. https://doi.org/10.1086/597126CrossRefPubMed

Elsner C, Dörries K (1998) Human polyomavirus JC control region variants in persistently infected CNS and kidney tissue. J Gen Virol 79(Pt 4):789–799. https://doi.org/10.1099/0022-1317-79-4-789CrossRefPubMed

Enam S, Del Valle L, Lara C et al (2002) Association of human polyomavirus JCV with colon cancer: evidence for interaction of viral T-antigen and beta-catenin. Cancer Res 62:7093–7101PubMed

Epperla N, Medina-Flores R, Mazza JJ, Yale SH (2014) Mirtazapine and mefloquine therapy for non-AIDS-related progressive multifocal leukoencephalopathy. WMJ 113:242–245PubMed

Fang C-Y, Chen S-Y, Hsiao B-X et al (2022) Unusually high incidence of polyomavirus JC infection in the higher grade of colorectal cancer tissues in Taiwan. Eur J Med Res 27:127. https://doi.org/10.1186/s40001-022-00756-2CrossRefPubMedPubMedCentral

Fedele CG, Ciardi MR, Delia S et al (2003) Identical rearranged forms of JC polyomavirus transcriptional control region in plasma and cerebrospinal fluid of acquired immunodeficiency syndrome patients with progressive multifocal leukoencephalopathy. J Neurovirol 9:551–558. https://doi.org/10.1080/13550280390241188CrossRefPubMed

Ferretti F, Bestetti A, Yiannoutsos CT et al (2018) Diagnostic and prognostic value of JC Virus DNA in plasma in progressive multifocal leukoencephalopathy. Clin Infect Dis 67:65–72. https://doi.org/10.1093/cid/ciy030CrossRefPubMed

Flaegstad T, Sundsfjord A, Arthur RR et al (1991) Amplification and sequencing of the control regions of BK and JC virus from human urine by polymerase chain reaction. Virology 180:553–560. https://doi.org/10.1016/0042-6822(91)90069-nCrossRefPubMed

Frisque RJ, Bream GL, Cannella MT (1984) Human polyomavirus JC virus genome. J Virol 51:458–469. https://doi.org/10.1128/JVI.51.2.458-469.1984CrossRefPubMedPubMedCentral

Frohman EM, Monaco MC, Remington G et al (2014) JC virus in CD34+ and CD19+ cells in patients with multiple sclerosis treated with natalizumab. JAMA Neurol 71:596–602. https://doi.org/10.1001/jamaneurol.2014.63CrossRefPubMed

Gan D-D, Reiss K, Carrill T et al (2001) Involvement of Wnt signaling pathway in murine medulloblastoma induced by human neurotropic JC virus. Oncogene 20:4864–4870. https://doi.org/10.1038/sj.onc.1204670CrossRefPubMed

Gasnault J, Kousignian P, Kahraman M et al (2001) Cidofovir in AIDS-associated progressive multifocal leukoencephalopathy: a monocenter observational study with clinical and JC virus load monitoring. J Neurovirol 7:375–381. https://doi.org/10.1080/13550280152537274CrossRefPubMed

Gasparovic ML, Gee GV, Atwood WJ (2006) JC virus minor capsid proteins Vp2 and Vp3 are essential for virus propagation. J Virol 80:10858–10861. https://doi.org/10.1128/JVI.01298-06CrossRefPubMedPubMedCentral

Ghosh S, Goldin E, Gordon FH et al (2003) Natalizumab for active Crohn’s disease. N Engl J Med 348:24–32. https://doi.org/10.1056/NEJMoa020732CrossRefPubMed

Gordon J, Del Valle L, Otte J, Khalili K (2000) Pituitary neoplasia induced by expression of human neurotropic polyomavirus, JCV, early genome in transgenic mice. Oncogene 19:4840–4846. https://doi.org/10.1038/sj.onc.1203849CrossRefPubMed

Gorelik L, Reid C, Testa M et al (2011) Progressive multifocal leukoencephalopathy (PML) development is associated with mutations in JC virus capsid protein VP1 that change its receptor specificity. J Infect Dis 204:103–114. https://doi.org/10.1093/infdis/jir198CrossRefPubMedPubMedCentral

Grinnell BW, Martin JD, Padgett BL, Walker DL (1983) Naturally occurring and passage-induced variation in the genome of JC virus. Prog Clin Biol Res 105:61–77PubMed

Ho P-R, Koendgen H, Campbell N et al (2017) Risk of natalizumab-associated progressive multifocal leukoencephalopathy in patients with multiple sclerosis: a retrospective analysis of data from four clinical studies. Lancet Neurol 16:925–933. https://doi.org/10.1016/S1474-4422(17)30282-XCrossRefPubMed

Hogan TF, Padgett BL, Walker DL et al (1980) Rapid detection and identification of JC virus and BK virus in human urine by using immunofluorescence microscopy. J Clin Microbiol 11:178–183. https://doi.org/10.1128/jcm.11.2.178-183.1980CrossRefPubMedPubMedCentral

Holman RC, Janssen RS, Buehler JW et al (1991) Epidemiology of progressive multifocal leukoencephalopathy in the United States: analysis of national mortality and AIDS surveillance data. Neurology 41:1733–1736. https://doi.org/10.1212/wnl.41.11.1733CrossRefPubMed

Huang WE, Lim B, Hsu C-C et al (2020) RT-LAMP for rapid diagnosis of coronavirus SARS-CoV-2. Microb Biotechnol 13:950–961. https://doi.org/10.1111/1751-7915.13586CrossRefPubMedPubMedCentral

Huang Y-L, Wang M, Ou W-C et al (2003) Analysis of DNA-binding activity of the JC virus minor capsid protein VP2. J Neurovirol 9(Suppl 1):21–24. https://doi.org/10.1080/13550280390195289CrossRefPubMed

Iannetta M, Zingaropoli MA, Bellizzi A et al (2016) Natalizumab affects T-cell phenotype in multiple sclerosis: implications for JCV reactivation. PLoS One 11:e0160277. https://doi.org/10.1371/journal.pone.0160277

Iannetta M, Zingaropoli MA, Latronico T et al (2019) Dynamic changes of MMP-9 plasma levels correlate with JCV reactivation and immune activation in natalizumab-treated multiple sclerosis patients. Sci Rep 9:311. https://doi.org/10.1038/s41598-018-36535-5CrossRefPubMedPubMedCentral

Iida T, Kitamura T, Guo J et al (1993) Origin of JC polyomavirus variants associated with progressive multifocal leukoencephalopathy. Proc Natl Acad Sci USA 90:5062–5065. https://doi.org/10.1073/pnas.90.11.5062CrossRefPubMedPubMedCentral

Ikeda J, Matsushima A, Ishii W et al (2017) Brain biopsy is more reliable than the DNA test for JC virus in cerebrospinal fluid for the diagnosis of progressive multifocal leukoencephalopathy. Intern Med 56:1231–1234. https://doi.org/10.2169/internalmedicine.56.7689CrossRefPubMedPubMedCentral

Jamilloux Y, Kerever S, Ferry T et al (2016) Treatment of progressive multifocal leukoencephalopathy with mirtazapine. Clin Drug Investig 36:783–789. https://doi.org/10.1007/s40261-016-0433-8CrossRefPubMed

Jiang Z-G, Cohen J, Marshall LJ, Major EO (2010) Hexadecyloxypropyl-cidofovir (CMX001) suppresses JC virus replication in human fetal brain SVG cell cultures. Antimicrob Agents Chemother 54:4723–4732. https://doi.org/10.1128/AAC.00837-10CrossRefPubMedPubMedCentral

Kaminski R, Chen Y, Fischer T et al (2016) Elimination of HIV-1 genomes from human T-lymphoid cells by CRISPR/Cas9 gene editing. Sci Rep 6:22555. https://doi.org/10.1038/srep22555CrossRefPubMedPubMedCentral

Kato K, Guo J, Taguchi F et al (1994) Phylogenetic comparison between archetypal and disease-associated JC virus isolates in Japan. Jpn J Med Sci Biol 47:167–178. https://doi.org/10.7883/yoken1952.47.167CrossRefPubMed

Kitamura T, Aso Y, Kuniyoshi N et al (1990) High incidence of urinary JC virus excretion in nonimmunosuppressed older patients. J Infect Dis 161:1128–1133. https://doi.org/10.1093/infdis/161.6.1128CrossRefPubMed

Kitamura T, Sugimoto C, Kato A et al (1997) Persistent JC virus (JCV) infection is demonstrated by continuous shedding of the same JCV strains. J Clin Microbiol 35:1255–1257CrossRefPubMedPubMedCentral

Kleinschmidt-DeMasters BK, Tyler KL (2005) Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N Engl J Med 353:369–374. https://doi.org/10.1056/NEJMoa051782CrossRefPubMed

Kobayashi S, Suzuki T, Igarashi M et al (2013) Cysteine residues in the major capsid protein, Vp1, of the JC virus are important for protein stability and oligomer formation. PLoS One 8:e76668. https://doi.org/10.1371/journal.pone.0076668

Kondo Y, Windrem MS, Zou L et al (2014) Human glial chimeric mice reveal astrocytic dependence of JC virus infection. J Clin Invest 124:5323–5336. https://doi.org/10.1172/JCI76629CrossRefPubMedPubMedCentral

Koralnik IJ (2002) Overview of the cellular immunity against JC virus in progressive multifocal leukoencephalopathy. J Neurovirol 8(Suppl 2):59–65. https://doi.org/10.1080/13550280290167894CrossRefPubMed

Krauzewicz N, Streuli CH, Stuart-Smith N et al (1990) Myristylated polyomavirus VP2: role in the life cycle of the virus. J Virol 64:4414–4420. https://doi.org/10.1128/JVI.64.9.4414-4420.1990

Krynska B, Gordon J, Otte J et al (1997) Role of cell cycle regulators in tumor formation in transgenic mice expressing the human neurotropic virus, JCV, early protein. J Cell Biochem 67:223–230. https://doi.org/10.1002/(SICI)1097-4644(19971101)67:2%3c223::AID-JCB7%3e3.0.CO;2-ZCrossRefPubMed

Kurmann R, Weisstanner C, Kardas P et al (2015) Progressive multifocal leukoencephalopathy in common variable immunodeficiency: mitigated course under mirtazapine and mefloquine. J Neurovirol 21:694–701. https://doi.org/10.1007/s13365-015-0340-4CrossRefPubMed

Langer-Gould A, Atlas SW, Green AJ et al (2005) Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N Engl J Med 353:375–381. https://doi.org/10.1056/NEJMoa051847CrossRefPubMed

Leech G, Rogers-Smith C, Monrad JT et al (2022) Mask wearing in community settings reduces SARS-CoV-2 transmission. Proc Natl Acad Sci USA 119:e2119266119. https://doi.org/10.1073/pnas.2119266119

London WT, Houff SA, Madden DL et al (1978) Brain tumors in owl monkeys inoculated with a human polyomavirus (JC virus). Science 201:1246–1249. https://doi.org/10.1126/science.211583CrossRefPubMed

London WT, Houff SA, McKeever PE et al (1983) Viral-induced astrocytomas in squirrel monkeys. Prog Clin Biol Res 105:227–237PubMed

Maas RPPWM, Muller-Hansma AHG, Esselink RAJ et al (2016) Drug-associated progressive multifocal leukoencephalopathy: a clinical, radiological, and cerebrospinal fluid analysis of 326 cases. J Neurol 263:2004–2021. https://doi.org/10.1007/s00415-016-8217-xCrossRefPubMedPubMedCentral

Mancuso P, Chen C, Kaminski R et al (2020) CRISPR based editing of SIV proviral DNA in ART treated non-human primates. Nat Commun 11:6065. https://doi.org/10.1038/s41467-020-19821-7CrossRefPubMedPubMedCentral

Marra CM, Rajicic N, Barker DE et al (2002) A pilot study of cidofovir for progressive multifocal leukoencephalopathy in AIDS. AIDS 16:1791–1797. https://doi.org/10.1097/00002030-200209060-00012CrossRefPubMed

Marshall LJ, Dunham L, Major EO (2010) Transcription factor Spi-B binds unique sequences present in the tandem repeat promoter/enhancer of JC virus and supports viral activity. J Gen Virol 91:3042–3052. https://doi.org/10.1099/vir.0.023184-0CrossRefPubMedPubMedCentral

Martin JD, King DM, Slauch JM, Frisque RJ (1985) Differences in regulatory sequences of naturally occurring JC virus variants. J Virol 53:306–311. https://doi.org/10.1128/JVI.53.1.306-311.1985CrossRefPubMedPubMedCentral

Martins F, Sofiya L, Sykiotis GP et al (2019) Adverse effects of immune-checkpoint inhibitors: epidemiology, management and surveillance. Nat Rev Clin Oncol 16:563–580. https://doi.org/10.1038/s41571-019-0218-0CrossRefPubMed

Matoba T, Orba Y, Suzuki T et al (2008) An siRNA against JC virus (JCV) agnoprotein inhibits JCV infection in JCV-producing cells inoculated in nude mice. Neuropathology 28:286–294. https://doi.org/10.1111/j.1440-1789.2007.00878.xCrossRefPubMed

Mayberry CL, Soucy AN, Lajoie CR et al (2019) JC polyomavirus entry by clathrin-mediated endocytosis is driven by β-arrestin. J Virol 93:e01948-e2018. https://doi.org/10.1128/JVI.01948-18CrossRefPubMedPubMedCentral

Merabova N, Kaniowska D, Kaminski R et al (2008) JC virus agnoprotein inhibits in vitro differentiation of oligodendrocytes and promotes apoptosis. J Virol 82:1558–1569. https://doi.org/10.1128/JVI.01680-07CrossRefPubMed

Miller DH, Khan OA, Sheremata WA et al (2003) A controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 348:15–23. https://doi.org/10.1056/NEJMoa020696CrossRefPubMed

Morioka K, Fukai K, Sakamoto K et al (2014) Evaluation of monoclonal antibody-based sandwich direct ELISA (MSD-ELISA) for antigen detection of foot-and-mouth disease virus using clinical samples. PLoS One 9:e94143. https://doi.org/10.1371/journal.pone.0094143

Muftuoglu M, Olson A, Marin D et al (2018) Allogeneic BK virus–specific t cells for progressive multifocal leukoencephalopathy. N Engl J Med 379:1443–1451. https://doi.org/10.1056/NEJMoa1801540CrossRefPubMedPubMedCentral

Nakanishi A, Nakamura A, Liddington R, Kasamatsu H (2006) Identification of amino acid residues within simian virus 40 capsid proteins Vp1, Vp2, and Vp3 that are required for their interaction and for viral infection. J Virol 80:8891–8898. https://doi.org/10.1128/JVI.00781-06CrossRefPubMedPubMedCentral

Nambirajan A, Suri V, Kataria V et al (2017) Progressive multifocal leukoencephalopathy in a 44-year old male with idiopathic CD4+ T-lymphocytopenia treated with mirtazapine and mefloquine. Neurol India 65:1061–1064. https://doi.org/10.4103/neuroindia.NI_535_16CrossRefPubMed

Oh D-Y, Buda S, Biere B et al (2021) Trends in respiratory virus circulation following COVID-19-targeted nonpharmaceutical interventions in Germany, January - September 2020: Analysis of national surveillance data. Lancet Reg Health Eur 6:100112. https://doi.org/10.1016/j.lanepe.2021.100112

Okada Y, Endo S, Takahashi H et al (2001) Distribution and function of JCV agnoprotein. J Neurovirol 7:302–306. https://doi.org/10.1080/13550280152537148CrossRefPubMed

Okada Y, Sawa H, Tanaka S et al (2000) Transcriptional activation of JC virus by human T-lymphotropic virus type I Tax protein in human neuronal cell lines. J Biol Chem 275:17016–17023. https://doi.org/10.1074/jbc.275.22.17016CrossRefPubMed

O’Neill FJ, Greenlee JE, Dörries K et al (2003) Propagation of archetype and nonarchetype JC virus variants in human fetal brain cultures: demonstration of interference activity by archetype JC virus. J Neurovirol 9:567–576. https://doi.org/10.1080/13550280390241223CrossRefPubMed

Otlu O, De Simone FI, Otalora Y-L et al (2014) The agnoprotein of polyomavirus JC is released by infected cells: evidence for its cellular uptake by uninfected neighboring cells. Virology 0:88–95. https://doi.org/10.1016/j.virol.2014.07.054

Ou W-C, Chen L-H, Wang M et al (2001) Analysis of minimal sequences on JC virus VP1 required for capsid assembly. J Neurovirol 7:298–301. https://doi.org/10.1080/13550280152537139CrossRefPubMed

Padgett BL, Zurhein GM, Walker DL et al (1971) Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. The Lancet 297:1257–1260. https://doi.org/10.1016/S0140-6736(71)91777-6CrossRef

Padgett BL, Walker DL (1973) Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. J Infect Dis 127:467–470. https://doi.org/10.1093/infdis/127.4.467CrossRefPubMed

Padgett BL, Walker DL, ZuRhein GM et al (1976) JC Papovavirus in progressive multifocal leukoencephalopathy. J Infect Dis 133:686–690. https://doi.org/10.1093/infdis/133.6.686CrossRefPubMed

Paz SPC, Branco L, Pereira MA, de C et al (2018) Systematic review of the published data on the worldwide prevalence of John Cunningham virus in patients with multiple sclerosis and neuromyelitis optica. Epidemiol Health 40:e2018001. https://doi.org/10.4178/epih.e2018001

Peretti A, Scorpio DG, Kong W-P et al (2023) A multivalent polyomavirus vaccine elicits durable neutralizing antibody responses in macaques. Vaccine 41:1735–1742. https://doi.org/10.1016/j.vaccine.2023.02.002CrossRefPubMed

Pfister LA, Letvin NL, Koralnik IJ (2001) JC virus regulatory region tandem repeats in plasma and central nervous system isolates correlate with poor clinical outcome in patients with progressive multifocal leukoencephalopathy. J Virol 75:5672–5676. https://doi.org/10.1128/JVI.75.12.5672-5676.2001CrossRefPubMedPubMedCentral

Pietropaolo V, Videtta M, Fioriti D et al (2003) Rearrangement patterns of JC virus noncoding control region from different biological samples. J Neurovirol 9:603–611. https://doi.org/10.1080/13550280390246507CrossRefPubMed

Piu C, Ibba G, Bertoli D et al (2020) Early reduction of the splicing factor2/alternative splicing factor: a cellular inhibitor of the JC polyomavirus in natalizumab-treated MS patients long before developing progressive multifocal leukoencephalopathy. J Neurovirol 26:133–137. https://doi.org/10.1007/s13365-019-00793-4CrossRefPubMed

Querbes W, Benmerah A, Tosoni D et al (2004) A JC virus-induced signal is required for infection of glial cells by a clathrin- and eps15-dependent pathway. J Virol 78:250–256. https://doi.org/10.1128/JVI.78.1.250-256.2004CrossRefPubMedPubMedCentral

Querido S, Fernandes I, Weigert A et al (2020) High-grade urothelial carcinoma in a kidney transplant recipient after JC virus nephropathy: the first evidence of JC virus as a potential oncovirus in bladder cancer. Am J Transplant 20:1188–1191. https://doi.org/10.1111/ajt.15663CrossRefPubMed

Ravichandran V, Sabath BF, Jensen PN et al (2006) Interactions between c-Jun, nuclear factor 1, and JC virus promoter sequences: implications for viral tropism. J Virol 80:10506–10513. https://doi.org/10.1128/JVI.01355-06CrossRefPubMedPubMedCentral

Ray U, Cinque P, Gerevini S et al (2015) JC polyomavirus mutants escape antibody-mediated neutralization. Sci Transl Med 7:306ra151. https://doi.org/10.1126/scitranslmed.aab1720

Richardson EP (1961) Progressive multifocal leukoencephalopathy. N Engl J Med 265:815–823. https://doi.org/10.1056/NEJM196110262651701CrossRefPubMed

Richardson EP Jr (1974) Our evolving understanding of progressive multifocal leukoencephalopathy*. Ann N Y Acad Sci 230:358–364. https://doi.org/10.1111/j.1749-6632.1974.tb14469.xCrossRefPubMed

Safak M, Barrucco R, Darbinyan A et al (2001) Interaction of JC virus agno protein with T antigen modulates transcription and replication of the viral genome in glial cells. J Virol 75:1476–1486. https://doi.org/10.1128/JVI.75.3.1476-1486.2001CrossRefPubMedPubMedCentral

Saribas AS, Mun S, Johnson J et al (2014) Human polyoma JC virus minor capsid proteins, VP2 and VP3, enhance large T antigen binding to the origin of viral DNA replication: evidence for their involvement in regulation of the viral DNA replication. Virology 449:1–16. https://doi.org/10.1016/j.virol.2013.10.031CrossRefPubMed

Saribas AS, White MK, Safak M (2018) Structure-based release analysis of the JC virus agnoprotein regions: A role for the hydrophilic surface of the major alpha helix domain in release. J Cell Physiol 233:2343–2359. https://doi.org/10.1002/jcp.26106CrossRefPubMed

Saribas S, Safak M (2020) A comprehensive proteomics analysis of the JC virus (JCV) large and small tumor antigen interacting proteins: large T primarily targets the host protein complexes with V-ATPase and ubiquitin ligase activities while small t mostly associates with those having phosphatase and chromatin-remodeling functions. Viruses 12:1192. https://doi.org/10.3390/v12101192CrossRefPubMedPubMedCentral

Sariyer IK, Khalili K (2011) Regulation of human neurotropic JC virus replication by alternative splicing factor SF2/ASF in glial cells. PLoS One 6:e14630. https://doi.org/10.1371/journal.pone.0014630

Saxena R, Saribas S, Jadiya P et al (2021) Human neurotropic polyomavirus, JC virus, agnoprotein targets mitochondrion and modulates its functions. Virology 553:135–153. https://doi.org/10.1016/j.virol.2020.11.004CrossRefPubMed

Shavaleh R, Kamandi M, Feiz Disfani H et al (2020) Association between JC virus and colorectal cancer: systematic review and meta-analysis. Infect Dis (lond) 52:152–160. https://doi.org/10.1080/23744235.2019.1692145CrossRefPubMed

Sheridan C (2006) Tysabri back on market. Nat Biotechnol 24:874–874. https://doi.org/10.1038/nbt0806-874CrossRefPubMed

Shin SK, Li M-S, Fuerst F et al (2006) Oncogenic T-antigen of JC virus is present frequently in human gastric cancers. Cancer 107:481–488. https://doi.org/10.1002/cncr.22028CrossRefPubMed

Shishido-Hara Y, Hara Y, Larson T et al (2000) Analysis of capsid formation of human polyomavirus JC (Tokyo-1 strain) by a eukaryotic expression system: splicing of late RNAs, translation and nuclear transport of major capsid protein VP1, and capsid assembly. J Virol 74:1840–1853. https://doi.org/10.1128/jvi.74.4.1840-1853.2000CrossRefPubMedPubMedCentral

Shishido-Hara Y, Ichinose S, Higuchi K et al (2004) Major and minor capsid proteins of human polyomavirus JC cooperatively accumulate to nuclear domain 10 for assembly into virions. J Virol 78:9890–9903. https://doi.org/10.1128/JVI.78.18.9890-9903.2004CrossRefPubMedPubMedCentral

Simon MA, Ilyinskii PO, Baskin GB et al (1999) Association of simian virus 40 with a central nervous system lesion distinct from progressive multifocal leukoencephalopathy in macaques with AIDS. Am J Pathol 154:437–446. https://doi.org/10.1016/S0002-9440(10)65290-XCrossRefPubMedPubMedCentral

Sock E, Renner K, Feist D et al (1996) Functional comparison of PML-type and archetype strains of JC virus. J Virol 70:1512–1520. https://doi.org/10.1128/jvi.70.3.1512-1520.1996CrossRefPubMedPubMedCentral

Stoner GL, Ryschkewitsch CF (1995) Capsid protein VP1 deletions in JC virus from two AIDS patients with progressive multifocal leukoencephalopathy. J Neurovirol 1:189–194. https://doi.org/10.3109/13550289509113965CrossRefPubMed

Summers NA, Kelley CF, Armstrong W et al (2019) Not a disease of the past: a case series of progressive multifocal leukoencephalopathy in the established antiretroviral era. AIDS Res Hum Retroviruses 35:544–552. https://doi.org/10.1089/AID.2018.0232CrossRefPubMedPubMedCentral

Suzuki T, Orba Y, Okada Y et al (2010) The Human polyoma JC virus agnoprotein acts as a viroporin. PLOS Pathogens 6:e1000801. https://doi.org/10.1371/journal.ppat.1000801

Swinnen B, Saegeman V, Beuselinck K et al (2019) Predictive value of JC virus PCR in cerebrospinal fluid in the diagnosis of PML. Diagnostic Microbiology and Infectious Disease 95:114859. https://doi.org/10.1016/j.diagmicrobio.2019.06.011

Tan CS, Ellis LC, Wüthrich C et al (2010) JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J Virol 84:9200–9209. https://doi.org/10.1128/JVI.00609-10CrossRefPubMedPubMedCentral

Tanimoto Y, Mori A, Miyamoto S et al (2022) Comparison of RT-PCR, RT-LAMP, and antigen quantification assays for the detection of SARS-CoV-2. Jpn J Infect Dis 75:249–253. https://doi.org/10.7883/yoken.JJID.2021.476CrossRefPubMed

Tornatore C, Berger JR, Houff SA et al (1992) Detection of JC virus DNA in peripheral lymphocytes from patients with and without progressive multifocal leukoencephalopathy. Ann Neurol 31:454–462. https://doi.org/10.1002/ana.410310426CrossRefPubMed

Uleri E, Regan P, Dolei A, Sariyer IK (2013) SF2/ASF binding region within JC virus NCCR limits early gene transcription in glial cells. Virol J 10:147. https://doi.org/10.1186/1743-422X-10-147CrossRefPubMedPubMedCentral

Van Assche G, Van Ranst M, Sciot R et al (2005) Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn’s disease. N Engl J Med 353:362–368. https://doi.org/10.1056/NEJMoa051586CrossRefPubMed

van Diemen FR, Kruse EM, Hooykaas MJG et al (2016) CRISPR/Cas9-mediated genome editing of herpesviruses limits productive and latent infections. PLoS Pathog 12:e1005701. https://doi.org/10.1371/journal.ppat.1005701

Van Loy T, Thys K, Ryschkewitsch C et al (2015) JC virus quasispecies analysis reveals a complex viral population underlying progressive multifocal leukoencephalopathy and supports viral dissemination via the hematogenous route. J Virol 89:1340–1347. https://doi.org/10.1128/JVI.02565-14CrossRefPubMed

Vigiser I, Piura Y, Kolb H et al (2022) JCV seroconversion rate during the SARS COVID-19 pandemic. Multiple Sclerosis and Related Disorders 68:104244. https://doi.org/10.1016/j.msard.2022.104244

Walker DL, Padgett BL, ZuRhein GM et al (1973) Human papovavirus (JC): induction of brain tumors in hamsters. Science 181:674–676. https://doi.org/10.1126/science.181.4100.674CrossRefPubMed

White FA, Ishaq M, Stoner GL, Frisque RJ (1992) JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy. J Virol 66:5726–5734CrossRefPubMedPubMedCentral

White MK, Gordon J, Berger JR, Khalili K (2015) Animal models for progressive multifocal leukoencephalopathy. J Cell Physiol 230:2869–2874. https://doi.org/10.1002/jcp.25047CrossRefPubMedPubMedCentral

Wilczek MP, Pike AMC, Craig SE et al (2022) Rearrangement in the hypervariable region of JC polyomavirus genomes isolated from patient samples and impact on transcription factor-binding sites and disease outcomes. Int J Mol Sci 23:5699. https://doi.org/10.3390/ijms23105699CrossRefPubMedPubMedCentral

Winklhofer KF, Albrecht I, Wegner M, Heilbronn R (2000) Human cytomegalovirus immediate-early gene 2 expression leads to JCV replication in nonpermissive cells via transcriptional activation of JCV T antigen. Virology 275:323–334. https://doi.org/10.1006/viro.2000.0503CrossRefPubMed

Wollebo HS, White MK, Gordon J et al (2015) Persistence and pathogenesis of the neurotropic polyomavirus JC. Ann Neurol 77:560–570. https://doi.org/10.1002/ana.24371CrossRefPubMedPubMedCentral

Wortman MJ, Krachmarov CP, Kim JH et al (2000) Interaction of HIV-1 Tat with Puralpha in nuclei of human glial cells: characterization of RNA-mediated protein-protein binding. J Cell Biochem 77:65–74. https://doi.org/10.1002/(sici)1097-4644(20000401)77:1%3c65::aid-jcb7%3e3.0.co;2-uCrossRefPubMed

Yogo Y, Guo J, Iida T et al (1994) Occurrence of multiple JC virus variants with distinctive regulatory sequences in the brain of a single patient with progressive multifocal leukoencephalopathy. Virus Genes 8:99–105. https://doi.org/10.1007/BF01703608CrossRefPubMed

Yogo Y, Iida T, Taguchi F et al (1991) Typing of human polyomavirus JC virus on the basis of restriction fragment length polymorphisms. J Clin Microbiol 29:2130–2138. https://doi.org/10.1128/jcm.29.10.2130-2138.1991CrossRefPubMedPubMedCentral

Yogo Y, Kitamura T, Sugimoto C et al (1990) Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals. J Virol 64:3139–3143. https://doi.org/10.1128/JVI.64.6.3139-3143.1990CrossRefPubMedPubMedCentral

Yousry TA, Major EO, Ryschkewitsch C et al (2006) Evaluation of patients treated with natalizumab for progressive multifocal leukoencephalopathy. N Engl J Med 354:924–933. https://doi.org/10.1056/NEJMoa054693CrossRefPubMedPubMedCentral

Yuen K-S, Chan C-P, Wong N-HM et al (2015) CRISPR/Cas9-mediated genome editing of Epstein-Barr virus in human cells. J Gen Virol 96:626–636. https://doi.org/10.1099/jgv.0.000012CrossRefPubMed

Zai J, Yi K, Xie L et al (2018) Dual monoclonal antibody-based sandwich ELISA for detection of in vitro packaged Ebola virus. Diagn Pathol 13:96. https://doi.org/10.1186/s13000-018-0773-1CrossRefPubMedPubMedCentral

Zingaropoli MA, Iannetta M, Pontecorvo S et al (2018) JC virus-DNA detection is associated with CD8 effector accumulation in peripheral blood of patients with multiple sclerosis under natalizumab treatment, independently from JC virus serostatus. Biomed Res Int 2018:5297980. https://doi.org/10.1155/2018/5297980CrossRefPubMedPubMedCentral

Zurhein G, Chou SM (1965) Particles resembling papova viruses in human cerebral demyelinating disease. Science 148:1477–1479. https://doi.org/10.1126/science.148.3676.1477CrossRefPubMed

Titel: Revisiting JC virus and progressive multifocal leukoencephalopathy
verfasst von: Angela Rocchi
Ilker K. Sariyer
Joseph R. Berger
Publikationsdatum: 02.09.2023
Verlag: Springer International Publishing
Erschienen in: Journal of NeuroVirology / Ausgabe 5/2023
Print ISSN: 1355-0284
Elektronische ISSN: 1538-2443
DOI: https://doi.org/10.1007/s13365-023-01164-w

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Nicht Creutzfeldt Jakob, sondern Abführtee-Vergiftung

29.05.2024 Hyponatriämie Nachrichten

Eine ältere Frau trinkt regelmäßig Sennesblättertee gegen ihre Verstopfung. Der scheint plötzlich gut zu wirken. Auf Durchfall und Erbrechen folgt allerdings eine Hyponatriämie. Nach deren Korrektur kommt es plötzlich zu progredienten Kognitions- und Verhaltensstörungen.

Schutz der Synapsen bei Alzheimer

29.05.2024 Morbus Alzheimer Nachrichten

Mit einem Neurotrophin-Rezeptor-Modulator lässt sich möglicherweise eine bestehende Alzheimerdemenz etwas abschwächen: Erste Phase-2-Daten deuten auf einen verbesserten Synapsenschutz.

Sozialer Aufstieg verringert Demenzgefahr

24.05.2024 Demenz Nachrichten

Ein hohes soziales Niveau ist mit die beste Versicherung gegen eine Demenz. Noch geringer ist das Demenzrisiko für Menschen, die sozial aufsteigen: Sie gewinnen fast zwei demenzfreie Lebensjahre. Umgekehrt steigt die Demenzgefahr beim sozialen Abstieg.

Hirnblutung unter DOAK und VKA ähnlich bedrohlich

17.05.2024 Direkte orale Antikoagulanzien Nachrichten

Kommt es zu einer nichttraumatischen Hirnblutung, spielt es keine große Rolle, ob die Betroffenen zuvor direkt wirksame orale Antikoagulanzien oder Marcumar bekommen haben: Die Prognose ist ähnlich schlecht.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 5/2023

Correction: Tat expression led to increased histone 3 tri-methylation at lysine 27 and contributed to HIV latency in astrocytes through regulation of MeCP2 and Ezh2 expression

Guillain-Barré syndrome as clinical presentation of a recently acquired hepatitis C

Metagenomic search of viral coinfections in herpes simplex encephalitis patients

Sex differences in cognitive function among people with HIV-1 clade C infection in Northern India

Serum of COVID-19 patients changes neuroinflammation and mitochondrial homeostasis markers in hippocampus of aged rats