Molecular characterization of BK and JC viruses circulating among potential kidney donors in Kuwait

Wassim Chehadeh 1, Susan Silpi Kurien, Mangalathillam Raman Nampoory

Affiliations

01 January 2013

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doi: 10.1155/2013/683464

Abstract

BK and JC polyomaviruses can be associated with nephropathy following renal transplantation. The aim of this study was to determine the prevalence, load, and genotypes of BK and JC viruses circulated in potential kidney donors in Kuwait. The detection of polyomavirus DNA was carried out in serum and urine samples of 165 potential kidney donors. Seventy (42%) individuals were tested positive for polyomavirus DNA, of whom 20 (12%) had detectable polyomavirus DNA in their serum samples, 40 (24%) in their urine samples, and 10 (6%) in both serum and urine samples. In the group of polyomavirus-positive patients, JC DNA could be detected in 78% of urine samples and 11% of serum samples, whereas BK DNA could be detected in 7% of urine samples and 3% of serum samples. The median polyomaviral load was low. The detected BK sequences in Kuwaiti adults formed new clusters sharing common ancestor with subgroups Ib1 and IVc, which are prevalent in Asia and Europe. Additionally, around half of the detected JCV sequences in Kuwaiti adults formed new clusters within the African subtype 3. Our results suggest high rate of polyomavirus shedding among healthy adults in Kuwait that can jeopardize their suitability for kidney donation.

Figures

Figure 1 Bayesian phylogenetic analysis of a 432-bp fragment of the BKV VP1 gene. The values of posterior probability greater than 0.5 are depicted at the nodes of the trees. Each reference BKV sequence is labeled with its corresponding subtype followed by its GenBank accession number. Scale is in substitutions/site.

Figure 1 Bayesian phylogenetic analysis of a 432-bp fragment of the BKV VP1 gene. The values of posterior probability greater than 0.5 are depicted at the nodes of the trees. Each reference BKV sequence is labeled with its corresponding subtype followed by its GenBank accession number. Scale is in substitutions/site.

Figure 2 Bayesian phylogenetic analysis of a 432-bp fragment of the JCV VP1 gene. The values of posterior probability greater than 0.5 are depicted at the nodes of the trees. Each reference JCV sequence is labeled with its corresponding genotype followed by its GenBank accession number. Scale is in substitutions/site.

Figure 2 Bayesian phylogenetic analysis of a 432-bp fragment of the JCV VP1 gene. The values of posterior probability greater than 0.5 are depicted at the nodes of the trees. Each reference JCV sequence is labeled with its corresponding genotype followed by its GenBank accession number. Scale is in substitutions/site.

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References

  1.  
    1. Hirsch HH, Randhawa P. BK virus in solid organ transplant recipients. American Journal of Transplantation. 2009;9(supplement 4):S136–S146. - PubMed
  2.  
    1. O’Donnell PH, Swanson K, Josephson MA, et al. BK virus infection is associated with hematuria and renal impairment in recipients of allogeneic hematopoetic stem cell transplants. Biology of Blood and Marrow Transplantation. 2009;15(9):1038–1048. - PMC - PubMed
  3.  
    1. Brinkert F, Briem-Richter A, Ilchmann C, Kemper MJ, Ganschow R. Prevalence of polyomavirus viruria (JC virus/BK virus) in children following liver transplantation. Pediatric Transplantation. 2010;14(1):105–108. - PubMed
  4.  
    1. Vats A, Shapiro R, Randhawa PS, et al. Quantitative viral load monitoring and cidofovir therapy for the management of BK virus-associated nephropathy in children and adults. Transplantation. 2003;75(1):105–112. - PubMed
  5.  
    1. Williams JW, Javaid B, Kadambi PV, et al. Leflunomide for polyomavirus type BK nephropathy. New England Journal of Medicine. 2005;352(11):1157–1158. - PubMed
  6.  
    1. Halim MA, Al-Otaibi T, El-Kholy O, et al. Active management of post-renal transplantation BK virus nephropathy: preliminary report. Transplantation Proceedings. 2009;41(7):2850–2852. - PubMed
  7.  
    1. Wen M-C, Wang C-L, Wang M, et al. Association of JC virus with tubulointerstitial nephritis in a renal allograft recipient. Journal of Medical Virology. 2004;72(4):675–678. - PubMed
  8.  
    1. Kantarci G, Eren Z, Demirağ A, Dogan I, Çakalagaoglu F, Yilmaz G. JC virus-associated nephropathy in a renal transplant recipient and comparative analysis of previous cases. Transplant Infectious Disease. 2011;13(1):89–92. - PubMed
  9.  
    1. Hammarin A-L, Bogdanovic G, Svedhem V, Pirskanen R, Morfeldt L, Grandien M. Analysis of PCR as a tool for detection of JC virus DNA in cerebrospinal fluid for diagnosis of progressive multifocal leukoencephalopathy. Journal of Clinical Microbiology. 1996;34(12):2929–2932. - PMC - PubMed
  10.  
    1. Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. The Lancet. 1971;1(7712):1257–1260. - PubMed
  11.  
    1. Sharma PM, Gupta G, Vats A, Shapiro R, Randhawa PS. Polyomavirus BK non-coding control region rearrangements in health and disease. Journal of Medical Virology. 2007;79(8):1199–1207. - PubMed
  12.  
    1. Bolen JB, Anders DG, Trempy J, Consigli RA. Differences in the subpopulations of the structural proteins of polyoma virions and capsids: biological functions of the multiple VP1 species. Journal of Virology. 1981;37(1):80–91. - PMC - PubMed
  13.  
    1. Jin L, Gibson PE. Genomic function and variation of human polyomavirus BK (BKV) Reviews in Medical Virology. 1996;6(4):201–214. - PubMed
  14.  
    1. Randhawa PS, Khaleel-Ur-Rehman K, Swalsky PA, et al. DNA sequencing of viral capsid protein VP-1 region in patients with BK virus interstitial nephritis. Transplantation. 2002;73(7):1090–1094. - PubMed
  15.  
    1. Boldorini R, Allegrini S, Miglio U, et al. Genomic mutations of viral protein 1 and BK virus nephropathy in kidney transplant recipients. Journal of Medical Virology. 2009;81(8):1385–1393. - PubMed
  16.  
    1. Jin L, Pietropaolo V, Booth JC, Ward KH, Brown DW. Prevalence and distribution of BK virus subtypes in healthy people and immunocompromised patients detected by PCR-restriction enzyme analysis. Clinical and Diagnostic Virology. 1995;3(3):285–295. - PubMed
  17.  
    1. Yogo Y, Sugimoto C, Zhong S, Homma Y. Evolution of the BK polyomavirus: epidemiological, anthropological and clinical implications. Reviews in Medical Virology. 2009;19(4):185–199. - PubMed
  18.  
    1. Agostini HT, Deckhut A, Jobes DV, et al. Genotypes of JC virus in east, central and southwest Europe. Journal of General Virology. 2001;82(5):1221–1331. - PubMed
  19.  
    1. Yanagihara R, Nerurkar VR, Scheirich I, et al. JC virus genotypes in the western Pacific suggest Asian mainland relationships and virus association with early population movements. Human Biology. 2002;74(3):473–488. - PubMed
  20.  
    1. Rafique A, Jiang SC. Genetic diversity of human polyomavirus JCPyV in Southern California wastewater. Journal of Water and Health. 2008;6(4):533–538. - PubMed
  21.  
    1. Sugimoto C, Hasegawa M, Kato A, et al. Evolution of human polyomavirus JC: implications for the population history of humans. Journal of Molecular Evolution. 2002;54(3):285–297. - PubMed
  22.  
    1. Pavesi A. African origin of polyomavirus JC and implications for prehistoric human migrations. Journal of Molecular Evolution. 2003;56(5):564–572. - PubMed
  23.  
    1. Nampoory MRN, Johny KV, Pacsa A, et al. BK virus nephropathy in renal transplant recipients in Kuwait: a preliminary report. Transplantation Proceedings. 2005;37(7):3048–3050. - PubMed
  24.  
    1. Kapila K, Nampoory MRN, Johny KV, et al. Role of urinary cytology in detecting human polyoma BK virus in kidney transplant recipients: a preliminary report. Medical Principles and Practice. 2007;16(3):237–239. - PubMed
  25.  
    1. Bohl DL, Storch GA, Ryschkewitsch C, et al. Donor origin of BK virus in renal transplantation and role of HLA C7 in susceptibility to sustained BK viremia. American Journal of Transplantation. 2005;5(9):2213–2221. - PubMed
  26.  
    1. Vera-Sempere FJ, Rubio L, Felipe-Ponce V, et al. Renal donor implication in the origin of BK infection: analysis of genomic viral subtypes. Transplantation Proceedings. 2006;38(8):2378–2381. - PubMed
  27.  
    1. Saundh K, Baker R, Harris M, et al. Early BK polyomavirus (BKV) reactivation in donor kidney is a risk factor for development of BKV-associated nephropathy. Journal of Infectious Diseases. 2013;207(1):137–141. - PubMed
  28.  
    1. Nickeleit V, Klimkait T, Binet IF, et al. Testing for polyomavirus type BK DNA in plasma to identify renal-allograft recipients with viral nephropathy. New England Journal of Medicine. 2000;342(18):1309–1315. - PubMed
  29.  
    1. Arthur RR, Dagostin S, Shah KV. Detection of BK virus and JC virus in urine and brain tissue by the polymerase chain reaction. Journal of Clinical Microbiology. 1989;27(6):1174–1179. - PMC - PubMed
  30.  
    1. Fink MCD, de Oliveira ACP, Romano CM, et al. Molecular characterization of human polyomavirus JC in Brazilian AIDS patients with and without progressive multifocal leukoencephalopathy. Journal of Clinical Virology. 2010;48(1):6–10. - PubMed
  31.  
    1. Whiley DM, Mackay IM, Sloots TP. Detection and differentiation of human polyomaviruses JC and BK by LightCycler PCR. Journal of Clinical Microbiology. 2001;39(12):4357–4361. - PMC - PubMed
  32.  
    1. Takasaka T, Kitamura T, Sugimoto C, Guo J, Zheng H-Y, Yogo Y. Phylogenetic analysis of major African genotype (Af2) of JC virus: implications for origin and dispersals of modern Africans. American Journal of Physical Anthropology. 2006;129(3):465–472. - PubMed
  33.  
    1. Zheng H-Y, Nishimoto Y, Chen Q, et al. Relationships between BK virus lineages and human populations. Microbes and Infection. 2007;9(2):204–213. - PubMed
  34.  
    1. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution. 2007;24(8):1596–1599. - PubMed
  35.  
    1. Drummond AJ, Rambaut A. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. 2007;7(1, article 214) - PMC - PubMed
  36.  
    1. Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. - PubMed
  37.  
    1. Andrews CA, Shah KV, Daniel RW, Hirsch MS, Rubin RH. A serological investigation of BK virus and JC virus infections in recipients of renal allografts. Journal of Infectious Diseases. 1988;158(1):176–181. - PubMed
  38.  
    1. Markowitz R-B, Thompson HC, Mueller JF, Cohen JA, Dynan WS. Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects. Journal of Infectious Diseases. 1993;167(1):13–20. - PubMed
  39.  
    1. Kazory A, Ducloux D, Chalopin J-M, Angonin R, Fontanière B, Moret H. The first case of JC virus allograft nephropathy. Transplantation. 2003;76(11):1653–1655. - PubMed
  40.  
    1. Drachenberg CB, Hirsch HH, Papadimitriou JC, et al. Polyomavirus BK versus JC replication and nephropathy in renal transplant recipients: a prospective evaluation. Transplantation. 2007;84(3):323–330. - PubMed
  41.  
    1. Padgett BL, Walker DL. Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. Journal of Infectious Diseases. 1973;127(4):467–470. - PubMed
  42.  
    1. Reploeg MD, Storch GA, Clifford DB. BK virus: a clinical review. Clinical Infectious Diseases. 2001;33(2):191–202. - PubMed
  43.  
    1. Egli A, Infanti L, Dumoulin A, et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. Journal of Infectious Diseases. 2009;199(6):837–846. - PubMed
  44.  
    1. Arthur RR, Shah KV, Baust SJ, Santos GW, Saral R. Association of BK viruria with hemorrhagic cystitis in recipients of bone marrow transplants. New England Journal of Medicine. 1986;315(4):230–234. - PubMed
  45.  
    1. Heritage J, Chesters PM, McCance DJ. The persistence of papovavirus BK DNA sequences in normal human renal tissue. Journal of Medical Virology. 1981;8(2):143–150. - PubMed
  46.  
    1. Dorries K. Latent and persistent polyomavirus infection. In: Khalili K, Stoner GL, editors. Human Polyomaviruses: Molecular and Clinical Perspectives. New York, NY, USA: Wiley-Liss; 2001. pp. 197–236.
  47.  
    1. Randhawa P, Vats A, Shapiro R, Weck K, Scantlebury V. BK virus: discovery, epidemiology, and biology. Graft. 2002;5(supplement):S19–S27.
  48.  
    1. Elsner C, Dorries K. Evidence of human polyomavirus BK and JC infection in normal brain tissue. Virology. 1992;191(1):72–80. - PubMed
  49.  
    1. De Mattei M, Martini F, Tognon M, Serra M, Baldini N, Barbanti-Brodano G. Polyomavirus latency and human tumors. Journal of Infectious Diseases. 1994;169(5):1175–1176. - PubMed
  50.  
    1. Knepper JE, diMayorca G. Cloning and characterization of BK virus-related DNA sequences from normal and neoplastic human tissues. Journal of Medical Virology. 1987;21(3):289–299. - PubMed
  51.  
    1. Gallia GL, Houff SA, Major EO, Khalili K. JC virus infection of lymphocytes-revisited. Journal of Infectious Diseases. 1997;176(6):1603–1609. - PubMed
  52.  
    1. Imperiale MJ. Oncogenic transformation by the human polyomaviruses. Oncogene. 2001;20(54):7917–7923. - PubMed
  53.  
    1. Nishimoto Y, Zheng H-Y, Zhong S, et al. An Asian origin for subtype IV BK virus based on phylogenetic analysis. Journal of Molecular Evolution. 2007;65(1):103–111. - PubMed

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