Viral miRNAs in plasma and urine divulge JC polyomavirus infection

Virology Journal

Volumn 11, Issue 1, 2014, Pages

  Lagatie, Ole ^a   Van Loy, Tom ^a   Tritsmans, Luc ^b   Stuyver, Lieven J ^a  

^a JANSSEN RESEARCH FOUNDATION   (Belgium)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

Biomarker; Circulating microRNA; JC Polyomavirus; Progressive Multifocal Leukoencephalopathy; Viral activity; Viral microRNA

Indexed keywords

MICRORNA; VIRUS RNA;

ADULT; ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; JC VIRUS; MALE; NONHUMAN; NORMAL HUMAN; POLYOMAVIRUS INFECTION; PROTEIN BLOOD LEVEL; PROTEIN URINE LEVEL; QUANTITATIVE ANALYSIS; RNA ANALYSIS; SEROLOGY; VIRUS SHEDDING; BLOOD; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MIDDLE AGED; POLYOMAVIRUS INFECTIONS; SENSITIVITY AND SPECIFICITY; TUMOR VIRUS INFECTIONS; URINE; VIRUS LOAD; YOUNG ADULT;

JC POLYOMAVIRUS;

ADULT; FEMALE; HUMANS; JC VIRUS; MALE; MICRORNAS; MIDDLE AGED; POLYOMAVIRUS INFECTIONS; RNA, VIRAL; SENSITIVITY AND SPECIFICITY; TUMOR VIRUS INFECTIONS; VIRAL LOAD; VIRUS SHEDDING; YOUNG ADULT;

EID: 84907432363     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-11-158     Document Type: Article

References (49)

1. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Ferenczy MW, Marshall LJ, Nelson CD, Atwood WJ, Nath A, Khalili K, Major EO, Clin Microbiol Rev 2012 25 3 471 506 10.1128/CMR.05031-11 22763635
2. Human polyomavirus JC reactivation and pathogenetic mechanisms of progressive multifocal leukoencephalopathy and cancer in the era of monoclonal antibody therapies. Bellizzi A, Nardis C, Anzivino E, Rodio D, Fioriti D, Mischitelli M, Chiarini F, Pietropaolo V, J Neurovirol 2012 18 1 1 11 10.1007/s13365-012-0080-7 22290500
3. JC Virus in CD34+ and CD19+ Cells in Patients With Multiple Sclerosis Treated With Natalizumab. Frohman EM, Monaco MC, Remington G, Ryschkewitsch C, Jensen PN, Johnson K, Perkins M, Liebner J, Greenberg B, Monson N, Frohman TC, Douek D, Major EO, JAMA Neurol 2014 71 5 596 602 10.1001/jamaneurol.2014.63 24664166
4. Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects. Markowitz RB, Thompson HC, Mueller JF, Cohen JA, Dynan WS, J Infect Dis 1993 167 1 13 20 10.1093/infdis/167.1.13 8380288
5. Detection of JC virus DNA and proteins in the bone marrow of HIV-positive and HIV-negative patients: implications for viral latency and neurotropic transformation. Tan CS, Dezube BJ, Bhargava P, Autissier P, Wuthrich C, Miller J, Koralnik IJ, J Infect Dis 2009 199 6 881 888 10.1086/597117 19434914
6. Human polyomavirus JC (JCV) infection of human B lymphocytes: a possible mechanism for JCV transmigration across the blood-brain barrier. Chapagain ML, Nerurkar VR, J Infect Dis 2010 202 2 184 191 10.1086/653823 20550458
7. Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. Knowles WA, Pipkin P, Andrews N, Vyse A, Minor P, Brown DW, Miller E, J Med Virol 2003 71 1 115 123 10.1002/jmv.10450 12858417
8. A second-generation ELISA (STRATIFY JCV DxSelect) for detection of JC virus antibodies in human serum and plasma to support progressive multifocal leukoencephalopathy risk stratification. Lee P, Plavina T, Castro A, Berman M, Jaiswal D, Rivas S, Schlain B, Subramanyam M, J Clin Virol 2013 57 2 141 146 10.1016/j.jcv.2013.02.002 23465394
9. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Major EO, Annu Rev Med 2010 61 35 47 10.1146/annurev.med.080708.082655 19719397
10. Quasispecies analysis of JC virus DNA present in urine of healthy subjects. Van Loy T, Thys K, Tritsmans L, Stuyver LJ, PLoS One 2013 8 8 70950 10.1371/journal.pone.0070950 23967139
11. Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. Padgett BL, Walker DL, J Infect Dis 1973 127 4 467 470 10.1093/infdis/127.4.467 4571704
12. Prevalence rate and age of acquisition of antibodies against JC virus and BK virus in human sera. Taguchi F, Kajioka J, Miyamura T, Microbiol Immunol 1982 26 11 1057 1064 10.1111/j.1348-0421.1982.tb00254.x 6300615
13. The epidemiology of human polyomaviruses. Walker DL, Padgett BL, Prog Clin Biol Res 1983 105 99 106 6304775
14. Assessment of JC virus DNA in blood and urine from natalizumab-treated patients. Rudick RA, O'Connor PW, Polman CH, Goodman AD, Ray SS, Griffith NM, Jurgensen SA, Gorelik L, Forrestal F, Sandrock AW SEG, Ann Neurol 2010 68 3 304 310 10.1002/ana.22107 20737514
15. JC virus antibody and viremia as predictors of progressive multifocal leukoencephalopathy in human immunodeficiency virus-1-infected individuals. Viscidi RP, Khanna N, Tan CS, Li X, Jacobson L, Clifford DB, Nath A, Margolick JB, Shah KV, Hirsch HH, Koralnik IJ, Clin Infect Dis: Offic Publ Infect Dis Soc Am 2011 53 7 711 715 10.1093/cid/cir507
16. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J, Stebler C, Gosert R, Hirsch HH, J Infect Dis 2009 199 6 837 846 10.1086/597126 19434930
17. Natalizumab discontinuation in the increasing complexity of multiple sclerosis therapy. Sormani MP, De Stefano N, Neurology 2014 82 17 1484 1485 10.1212/WNL.0000000000000369 24682968
18. Risk of natalizumab-associated progressive multifocal leukoencephalopathy. Bloomgren G, Richman S, Hotermans C, Subramanyam M, Goelz S, Natarajan A, Lee S, Plavina T, Scanlon JV, Sandrock A, Bozic C, N Engl J Med 2012 366 20 1870 1880 10.1056/NEJMoa1107829 22591293
19. Does risk stratification decrease the risk of natalizumab-associated PML? Where is the evidence? Cutter GR, Stuve O, Mult Scler 2014 20 10 1304 1305 10.1177/1352458514531843 24812045
20. MicroRNAs: small RNAs with a big role in gene regulation. He L, Hannon GJ, Nat Rev Genet 2004 5 7 522 531 10.1038/nrg1379 15211354
21. Viral miRNAs: tools for immune evasion. Boss IW, Renne R, Curr Opin Microbiol 2010 13 4 540 545 10.1016/j.mib.2010.05.017 20580307
22. Virus-encoded microRNAs: an overview and a look to the future. Kincaid RP, Sullivan CS, PLoS Pathog 2012 8 12 1003018 10.1371/journal.ppat.1003018 23308061
23. A blood based 12-miRNA signature of Alzheimer disease patients. Leidinger P, Backes C, Deutscher S, Schmitt K, Mueller SC, Frese K, Haas J, Ruprecht K, Paul F, Stahler C, Lang CJ, Meder B, Bartfai T, Meese E, Keller A, Genome Biol 2013 14 7 78 10.1186/gb-2013-14-7-r78 23895045
24. Circulating microRNAs as novel biomarkers for diabetes mellitus. Guay C, Regazzi R, Nat Rev Endocrinol 2013 9 9 513 521 10.1038/nrendo.2013.86 23629540
25. Cancer diagnosis and prognosis decoded by blood-based circulating microRNA signatures. Madhavan D, Cuk K, Burwinkel B, Yang R, Front Genet 2013 4 116 23802013
26. Circulating human microRNAs are not linked to JC polyomavirus serology or urinary viral load in healthy subjects. Lagatie O, Van Loy T, Tritsmans L, Stuyver LJ, Virol J 2014 11 1 41 10.1186/1743-422X-11-41 24588811
27. The miRNA world of polyomaviruses. Lagatie O, Tritsmans L, Stuyver LJ, Virol J 2013 10 268 10.1186/1743-422X-10-268 23984639
28. Evolutionarily conserved function of a viral microRNA. Seo GJ, Fink LH, O'Hara B, Atwood WJ, Sullivan CS, J Virol 2008 82 20 9823 9828 10.1128/JVI.01144-08 18684810
29. An identical miRNA of the human JC and BK polyoma viruses targets the stress-induced ligand ULBP3 to escape immune elimination. Bauman Y, Nachmani D, Vitenshtein A, Tsukerman P, Drayman N, Stern-Ginossar N, Lankry D, Gruda R, Mandelboim O, Cell Host Microbe 2011 9 2 93 102 10.1016/j.chom.2011.01.008 21320692
30. Plasma viral microRNA profiles reveal potential biomarkers for chronic active Epstein-Barr virus infection. Kawano Y, Iwata S, Kawada J, Gotoh K, Suzuki M, Torii Y, Kojima S, Kimura H, Ito Y, J Infect Dis 2013 208 5 771 779 10.1093/infdis/jit222 23687223
31. Systemically circulating viral and tumor-derived microRNAs in KSHV-associated malignancies. Chugh PE, Sin SH, Ozgur S, Henry DH, Menezes P, Griffith J, Eron JJ, Damania B, Dittmer DP, PLoS Pathog 2013 9 7 1003484 10.1371/journal.ppat.1003484 23874201
32. MicroRNA miR-J1-5p as a potential biomarker for JC virus infection in the gastrointestinal tract. Link A, Balaguer F, Nagasaka T, Boland CR, Goel A, PLoS One 2014 9 6 100036 10.1371/journal.pone.0100036 24932487
33. Real-time quantification of microRNAs by stem-loop RT-PCR. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ, Nucleic Acids Res 2005 33 20 179 10.1093/nar/gni178 16314309
34. JC viremia in natalizumab-treated patients with multiple sclerosis. Major EO, Frohman E, Douek D, N Engl J Med 2013 368 23 2240 2241 10.1056/NEJMc1214233 23738566
35. More on JC viremia in natalizumab-treated patients with multiple sclerosis. Major EO, Frohman E, Douek D, N Engl J Med 2013 369 13 1280 10.1056/NEJMc1213681
36. JC virus antibody status underestimates infection rates. Berger JR, Houff SA, Gurwell J, Vega N, Miller CS, Danaher RJ, Ann Neurol 2013 74 1 84 90 10.1002/ana.23893 23526716
37. Progressive multifocal leukoencephalopathy (PML) development is associated with mutations in JC virus capsid protein VP1 that change its receptor specificity. Gorelik L, Reid C, Testa M, Brickelmaier M, Bossolasco S, Pazzi A, Bestetti A, Carmillo P, Wilson E, McAuliffe M, Tonkin C, Carulli JP, Lugovskoy A, Lazzarin A, Sunyaev S, Simon K, Cinque P, J Infect Dis 2011 204 1 103 114 10.1093/infdis/jir198 21628664
38. Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. Reid CE, Li H, Sur G, Carmillo P, Bushnell S, Tizard R, McAuliffe M, Tonkin C, Simon K, Goelz S, Cinque P, Gorelik L, Carulli JP, J Infect Dis 2011 204 2 237 244 10.1093/infdis/jir256 21673034
39. Identical rearranged forms of JC polyomavirus transcriptional control region in plasma and cerebrospinal fluid of acquired immunodeficiency syndrome patients with progressive multifocal leukoencephalopathy. Fedele CG, Ciardi MR, Delia S, Contreras G, Perez JL, De Ona M, Vidal E, Tenorio A, J Neurovirol 2003 9 5 551 558 10.1080/13550280390241188 13129769
40. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Sullivan CS, Grundhoff AT, Tevethia S, Pipas JM, Ganem D, Nature 2005 435 7042 682 686 10.1038/nature03576 15931223
41. miRNA regulation of BK polyomavirus replication during early infection. Broekema NM, Imperiale MJ, Proc Natl Acad Sci U S A 2013 110 20 8200 8205 10.1073/pnas.1301907110 23630296
42. Polyomavirus BK-encoded microRNA suppresses autoregulation of viral replication. Tian YC, Li YJ, Chen HC, Wu HH, Weng CH, Chen YC, Lee CC, Chang MY, Hsu HH, Yen TH, Hung CC, Yang CW, Biochem Biophys Res Commun 2014 447 3 543 549 10.1016/j.bbrc.2014.04.030 24735545
43. Murine polyomavirus encodes a microRNA that cleaves early RNA transcripts but is not essential for experimental infection. Sullivan CS, Sung CK, Pack CD, Grundhoff A, Lukacher AE, Benjamin TL, Ganem D, Virology 2009 387 1 157 167 10.1016/j.virol.2009.02.017 19272626
44. Extracellular circulating viral microRNAs: current knowledge and perspectives. Lagana A, Russo F, Veneziano D, Bella SD, Giugno R, Pulvirenti A, Croce CM, Ferro A, Front Genet 2013 4 120 23805153
45. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Umbach JL, Kramer MF, Jurak I, Karnowski HW, Coen DM, Cullen BR, Nature 2008 454 7205 780 783 18596690
46. Comprehensive profiling of Epstein-Barr virus-encoded miRNA species associated with specific latency types in tumor cells. Yang HJ, Huang TJ, Yang CF, Peng LX, Liu RY, Yang GD, Chu QQ, Huang JL, Liu N, Huang HB, Zhu ZY, Qian CN, Huang BJ, Virol J 2013 10 314 10.1186/1743-422X-10-314 24161012
47. BK virus encoded microRNAs are present in blood of renal transplant recipients with BK viral nephropathy. Li JY, McNicholas K, Yong TY, Rao N, Coates PT, Higgins GD, Carroll RP, Woodman RJ, Michael MZ, Gleadle JM, Am J Transplant: Offic J Am Soc Transplant Am Soc Transplant Surgeons 2014 14 5 1183 1190 10.1111/ajt.12694
48. The microRNA registry. Griffiths-Jones S, Nucleic Acids Res 2004 32 Database issue 109 D111 14681370
49. An antibody response to human polyomavirus 15-mer peptides is highly abundant in healthy human subjects. Stuyver LJ, Verbeke T, Van Loy T, Van Gulck E, Tritsmans L, Virol J 2013 10 192 10.1186/1743-422X-10-192 23758776