1932

Abstract

In 1971, the first human polyomavirus was isolated from the brain of a patient who died from a rapidly progressing demyelinating disease known as progressive multifocal leukoencephalopathy. The virus was named JC virus after the initials of the patient. In that same year a second human polyomavirus was discovered in the urine of a kidney transplant patient and named BK virus. In the intervening years it became clear that both viruses were widespread in the human population but only rarely caused disease. The past decade has witnessed the discovery of eleven new human polyomaviruses, two of which cause unusual and rare cancers. We present an overview of the history of these viruses and the evolution of JC polyomavirus–induced progressive multifocal leukoencephalopathy over three different epochs. We review what is currently known about JC polyomavirus, what is suspected, and what remains to be done to understand the biology of how this mostly harmless endemic virus gives rise to lethal disease.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-101416-041439
2017-09-29
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/virology/4/1/annurev-virology-101416-041439.html?itemId=/content/journals/10.1146/annurev-virology-101416-041439&mimeType=html&fmt=ahah

Literature Cited

  1. Calvignac-Spencer S, Feltkamp MC, Daugherty MD, Moens U. Polyomaviridae Study Group of the International Committee on Taxonomy of Viruses et al. 2016. A taxonomy update for the family Polyomaviridae. Arch. Virol. 161:1739–50 [Google Scholar]
  2. Imperiale MJ, Jiang M. 2.  2016. Polyomavirus persistence. Annu. Rev. Virol. 3:517–32 [Google Scholar]
  3. Gardner SD, Field AM, Coleman DV, Hulme B. 3.  1971. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1:1253–57 [Google Scholar]
  4. Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH. 4.  1971. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1:1257–60 [Google Scholar]
  5. Allander T, Andreasson K, Gupta S, Bjerkner A, Bogdanovic G. 5.  et al. 2007. Identification of a third human polyomavirus. J. Virol. 81:4130–36 [Google Scholar]
  6. Gaynor AM, Nissen MD, Whiley DM, Mackay IM, Lambert SB. 6.  et al. 2007. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLOS Pathog 3:e64 [Google Scholar]
  7. Feng H, Shuda M, Chang Y, Moore PS. 7.  2008. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319:1096–100 [Google Scholar]
  8. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB. 8.  2010. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7:509–15 [Google Scholar]
  9. van der Meijden E, Janssens RW, Lauber C, Bouwes Bavinck JN, Gorbalenya AE, Feltkamp MC. 9.  2010. Discovery of a new human polyomavirus associated with trichodysplasia spinulosa in an immunocompromized patient. PLOS Pathog 6:e1001024 [Google Scholar]
  10. Scuda N, Hofmann J, Calvignac-Spencer S, Ruprecht K, Liman P. 10.  et al. 2011. A novel human polyomavirus closely related to the African green monkey–derived lymphotropic polyomavirus. J. Virol. 85:4586–90 [Google Scholar]
  11. Buck CB, Phan GQ, Raiji MT, Murphy PM, McDermott DH, McBride AA. 11.  2012. Complete genome sequence of a tenth human polyomavirus. J. Virol. 86:10887 [Google Scholar]
  12. Lim ES, Reyes A, Antonio M, Saha D, Ikumapayi UN. 12.  et al. 2013. Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology 436:295–303 [Google Scholar]
  13. Korup S, Rietscher J, Calvignac-Spencer S, Trusch F, Hofmann J. 13.  et al. 2013. Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLOS ONE 8:e58021 [Google Scholar]
  14. Mishra N, Pereira M, Rhodes RH, An P, Pipas JM. 14.  et al. 2014. Identification of a novel polyomavirus in a pancreatic transplant recipient with retinal blindness and vasculitic myopathy. J. Infect. Dis. 210:1595–99 [Google Scholar]
  15. Chang Y, Moore PS. 15.  2012. Merkel cell carcinoma: a virus-induced human cancer. Annu. Rev. Pathol. 7:123–44 [Google Scholar]
  16. Dalianis T, Hirsch HH. 16.  2013. Human polyomaviruses in disease and cancer. Virology 437:63–72 [Google Scholar]
  17. Hirsch HH, Steiger J. 17.  2003. Polyomavirus BK. Lancet Infect. Dis. 3:611–23 [Google Scholar]
  18. Berger JR, Major EO. 18.  1999. Progressive multifocal leukoencephalopathy. Semin. Neurol. 19:193–200 [Google Scholar]
  19. Ferenczy MW, Marshall LJ, Nelson CD, Atwood WJ, Nath A. 19.  et al. 2012. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus–induced demyelinating disease of the human brain. Clin. Microbiol. Rev. 25:471–506 [Google Scholar]
  20. Ambrose C, Lowman H, Rajadhyaksha A, Blasquez V, Bina M. 20.  1990. Location of nucleosomes in simian virus 40 chromatin. J. Mol. Biol. 214:875–84 [Google Scholar]
  21. Wollebo HS, Bellizzi A, Cossari DH, Safak M, Khalili K, White MK. 21.  2015. Epigenetic regulation of polyomavirus JC involves acetylation of specific lysine residues in NF-κB p65. J. Neurovirol. 21:679–87 [Google Scholar]
  22. Wollebo HS, Woldemichaele B, Khalili K, Safak M, White MK. 22.  2013. Epigenetic regulation of polyomavirus JC. Virol. J. 10:264 [Google Scholar]
  23. Milavetz B, Kallestad L, Gefroh A, Adams N, Woods E, Balakrishnan L. 23.  2012. Virion-mediated transfer of SV40 epigenetic information. Epigenetics 7:528–34 [Google Scholar]
  24. White MK, Khalili K. 24.  2011. Pathogenesis of progressive multifocal leukoencephalopathy—revisited. J. Infect. Dis. 203:578–86 [Google Scholar]
  25. Jensen PN, Major EO. 25.  2001. A classification scheme for human polyomavirus JCV variants based on the nucleotide sequence of the noncoding regulatory region. J. Neurovirol. 7:280–87 [Google Scholar]
  26. Cubitt CL, Cui X, Agostini HT, Nerurkar VR, Scheirich I. 26.  et al. 2001. Predicted amino acid sequences for 100 JCV strains. J. Neurovirol. 7:339–44 [Google Scholar]
  27. Newman JT, Frisque RJ. 27.  1997. Detection of archetype and rearranged variants of JC virus in multiple tissues from a pediatric PML patient. J. Med. Virol 52243–52 [Google Scholar]
  28. Ranganathan PN, Khalili K. 28.  1993. The transcriptional enhancer element, κB, regulates promoter activity of the human neurotropic virus, JCV, in cells derived from the CNS. Nucleic Acids Res 21:1959–64 [Google Scholar]
  29. Marshall LJ, Dunham L, Major EO. 29.  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:Pt. 123042–52 [Google Scholar]
  30. Marshall LJ, Moore LD, Mirsky MM, Major EO. 30.  2012. JC virus promoter/enhancers contain TATA box–associated Spi-B-binding sites that support early viral gene expression in primary astrocytes. J. Gen. Virol. 93:Pt. 3651–61 [Google Scholar]
  31. Sumner C, Shinohara T, Durham L, Traub R, Major E, Amemiya K. 31.  1996. Expression of multiple classes of the nuclear factor-1 family in the developing human brain: differential expression of two classes of NF-1 genes. J. Neurovirol. 2:87–100 [Google Scholar]
  32. Major EO, Amemiya K, Elder G, Houff SA. 32.  1990. Glial cells of the human developing brain and B cells of the immune system share a common DNA binding factor for recognition of the regulatory sequences of the human polyomavirus, JCV. J. Neurosci. Res. 27:461–71 [Google Scholar]
  33. Marshall LJ, Ferenczy MW, Daley EL, Jensen PN, Ryschkewitsch CF, Major EO. 33.  2014. Lymphocyte gene expression and JC virus noncoding control region sequences are linked with the risk of progressive multifocal leukoencephalopathy. J. Virol. 88:5177–83 [Google Scholar]
  34. Imperiale MJ, Jiang M. 34.  2015. What DNA viral genomic rearrangements tell us about persistence. J. Virol. 89:1948–50 [Google Scholar]
  35. White FA III, Ishaq M, Stoner GL, Frisque RJ. 35.  1992. JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy. J. Virol. 66:5726–34 [Google Scholar]
  36. Shah KV. 36.  1996. Polyomaviruses. Fields Virology BN Fields, DM Knipe, PM Howley 2027–43 Philadelphia: Lippincott-Raven [Google Scholar]
  37. Trowbridge PW, Frisque RJ. 37.  1995. Identification of three new JC virus proteins generated by alternative splicing of the early viral mRNA. J. Neurovirol. 1:195–206 [Google Scholar]
  38. Frisque RJ. 38.  2001. Structure and function of JC virus T′ proteins. J. Neurovirol. 7:293–97 [Google Scholar]
  39. Swenson JJ, Frisque RJ. 39.  1995. Biochemical characterization and localization of JC virus large T antigen phosphorylation domains. Virology 212:295–308 [Google Scholar]
  40. Meinke G, Phelan PJ, Kalekar R, Shin J, Archambault J. 40.  et al. 2014. Insights into the initiation of JC virus DNA replication derived from the crystal structure of the T-antigen origin binding domain. PLOS Pathog 10:e1003966 [Google Scholar]
  41. Lynch K, Frisque R. 41.  1991. Factors contributing to the restricted DNA replicating activity of JC virus. Virology 180:306–17 [Google Scholar]
  42. Neu U, Stehle T, Atwood WJ. 42.  2009. The Polyomaviridae: contributions of virus structure to our understanding of virus receptors and infectious entry. Virology 384:389–99 [Google Scholar]
  43. Neu U, Maginnis MS, Palma AS, Stroh LJ, Nelson CD. 43.  et al. 2010. Structure-function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif. Cell Host Microbe 8:309–19 [Google Scholar]
  44. Salunke DM, Caspar DL, Garcea RL. 44.  1986. Self-assembly of purified polyomavirus capsid protein VP1. Cell 46:895–904 [Google Scholar]
  45. Nelson CD, Stroh LJ, Gee GV, O'Hara BA, Stehle T, Atwood WJ. 45.  2015. Modulation of a pore in the capsid of JC polyomavirus reduces infectivity and prevents exposure of the minor capsid proteins. J. Virol. 89:3910–21 [Google Scholar]
  46. Gasparovic ML, Gee GV, Atwood WJ. 46.  2006. JC virus minor capsid proteins Vp2 and Vp3 are essential for virus propagation. J. Virol. 80:10858–61 [Google Scholar]
  47. Saribas AS, Coric P, Hamazaspyan A, Davis W, Axman R. 47.  et al. 2016. Emerging from the unknown: structural and functional features of agnoprotein of polyomaviruses. J. Cell. Physiol. 231:2115–27 [Google Scholar]
  48. Imperiale MJ. 48.  2014. Polyomavirus miRNAs: the beginning. Curr. Opin. Virol. 7:29–32 [Google Scholar]
  49. Sullivan CS, Grundhoff AT, Tevethia S, Pipas JM, Ganem D. 49.  2005. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435:682–86 [Google Scholar]
  50. Seo GJ, Fink LH, O'Hara B, Atwood WJ, Sullivan CS. 50.  2008. Evolutionarily conserved function of a viral microRNA. J. Virol. 82:9823–28 [Google Scholar]
  51. Bauman Y, Nachmani D, Vitenshtein A, Tsukerman P, Drayman N. 51.  et al. 2011. An identical miRNA of the human JC and BK polyoma viruses targets the stress-induced ligand ULBP3 to escape immune elimination. Cell Host Microbe 9:93–102 [Google Scholar]
  52. Rocca A, Martelli F, Delbue S, Ferrante P, Bartolozzi D. 52.  et al. 2015. The JCPYV DNA load inversely correlates with the viral microRNA expression in blood and cerebrospinal fluid of patients at risk of PML. J. Clin. Virol. 70:1–6 [Google Scholar]
  53. Broekema NM, Imperiale MJ. 53.  2013. miRNA regulation of BK polyomavirus replication during early infection. PNAS 110:8200–5 [Google Scholar]
  54. O'Hara SD, Stehle T, Garcea R. 54.  2014. Glycan receptors of the Polyomaviridae: structure, function, and pathogenesis. Curr. Opin. Virol. 7:73–78 [Google Scholar]
  55. Stroh LJ, Maginnis MS, Blaum BS, Nelson CD, Neu U. 55.  et al. 2015. The greater affinity of JC polyomavirus capsid for α2,6-linked lactoseries tetrasaccharide c than for other sialylated glycans is a major determinant of infectivity. J. Virol. 89:6364–75 [Google Scholar]
  56. Elphick GF, Querbes W, Jordan JA, Gee GV, Eash S. 56.  et al. 2004. The human polyomavirus, JCV, uses serotonin receptors to infect cells. Science 306:1380–83 [Google Scholar]
  57. Assetta B, Maginnis MS, Gracia Ahufinger I, Haley SA, Gee GV. 57.  et al. 2013. 5-HT2 receptors facilitate JC polyomavirus entry. J. Virol. 87:13490–98 [Google Scholar]
  58. Maginnis MS, Stroh LJ, Gee GV, O'Hara BA, Derdowski A. 58.  et al. 2013. Progressive multifocal leukoencephalopathy–associated mutations in the JC polyomavirus capsid disrupt lactoseries tetrasaccharide c binding. mBio 4:e00247–13 [Google Scholar]
  59. Chapagain ML, Verma S, Mercier F, Yanagihara R, Nerurkar VR. 59.  2007. Polyomavirus JC infects human brain microvascular endothelial cells independent of serotonin receptor 2A. Virology 364:55–63 [Google Scholar]
  60. Kurmann R, Weisstanner C, Kardas P, Hirsch HH, Wiest R. 60.  et al. 2015. Progressive multifocal leukoencephalopathy in common variable immunodeficiency: mitigated course under mirtazapine and mefloquine. J. Neurovirol. 21:694–701 [Google Scholar]
  61. Park JH, Ryoo S, Noh HJ, Seo JM, Kang HH. 61.  et al. 2011. Dual therapy with cidofovir and mirtazapine for progressive multifocal leukoencephalopathy in a sarcoidosis patient. Case Rep. Neurol. 3:258–62 [Google Scholar]
  62. Vulliemoz S, Lurati-Ruiz F, Borruat FX, Delavelle J, Koralnik IJ. 62.  et al. 2006. Favourable outcome of progressive multifocal leucoencephalopathy in two patients with dermatomyositis. J. Neurol. Neurosurg. Psychiatry 77:1079–82 [Google Scholar]
  63. Jamilloux Y, Kerever S, Ferry T, Broussolle C, Honnorat J, Seve P. 63.  2016. Treatment of progressive multifocal leukoencephalopathy with mirtazapine. Clin. Drug Investig. 36:783–89 [Google Scholar]
  64. Clifford DB, Nath A, Cinque P, Brew BJ, Zivadinov R. 64.  et al. 2013. A study of mefloquine treatment for progressive multifocal leukoencephalopathy: results and exploration of predictors of PML outcomes. J. Neurovirol. 19:351–58 [Google Scholar]
  65. Haley SA, O'Hara BA, Nelson CD, Brittingham FL, Henriksen KJ. 65.  et al. 2015. Human polyomavirus receptor distribution in brain parenchyma contrasts with receptor distribution in kidney and choroid plexus. Am. J. Pathol. 185:2246–58 [Google Scholar]
  66. Agnihotri SP, Wuthrich C, Dang X, Nauen D, Karimi R. 66.  et al. 2014. A fatal case of JC virus meningitis presenting with hydrocephalus in a human immunodeficiency virus–seronegative patient. Ann. Neurol. 76:140–47 [Google Scholar]
  67. Sunyaev SR, Lugovskoy A, Simon K, Gorelik L. 67.  2009. Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML). PLOS Genet 5:e1000368 [Google Scholar]
  68. Gorelik L, Reid C, Testa M, Brickelmaier M, Bossolasco S. 68.  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. 204:103–14 [Google Scholar]
  69. Reid CE, Li H, Sur G, Carmillo P, Bushnell S. 69.  et al. 2011. Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. J. Infect. Dis. 204:237–44 [Google Scholar]
  70. Wharton KA Jr., Quigley C, Themeles M, Dunstan RW, Doyle K. 70.  et al. 2016. JC polyomavirus abundance and distribution in progressive multifocal leukoencephalopathy (PML) brain tissue implicates myelin sheath in intracerebral dissemination of infection. PLOS ONE 11:e0155897 [Google Scholar]
  71. Ray U, Cinque P, Gerevini S, Longo V, Lazzarin A. 71.  et al. 2015. JC polyomavirus mutants escape antibody-mediated neutralization. Sci. Transl. Med. 7:306ra151 [Google Scholar]
  72. Jelcic I, Combaluzier B, Jelcic I, Faigle W, Senn L. 72.  et al. 2015. Broadly neutralizing human monoclonal JC polyomavirus VP1-specific antibodies as candidate therapeutics for progressive multifocal leukoencephalopathy. Sci. Transl. Med. 7:306ra150 [Google Scholar]
  73. Querbes W, Benmerah A, Tosoni D, Di Fiore PP, Atwood WJ. 73.  2004. A JC virus–induced signal is required for infection of glial cells by a clathrin- and eps15-dependent pathway. J. Virol. 78:250–56 [Google Scholar]
  74. Pho MT, Ashok A, Atwood WJ. 74.  2000. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J. Virol. 74:2288–92 [Google Scholar]
  75. Eash S, Querbes W, Atwood WJ. 75.  2004. Infection of Vero cells by BK virus is dependent on caveolae. J. Virol. 78:11583–90 [Google Scholar]
  76. Maginnis MS, Nelson CD, Atwood WJ. 76.  2015. JC polyomavirus attachment, entry, and trafficking: unlocking the keys to a fatal infection. J. Neurovirol. 21:601–13 [Google Scholar]
  77. Sapp M, Day PM. 77.  2009. Structure, attachment and entry of polyoma- and papillomaviruses. Virology 384:400–9 [Google Scholar]
  78. Chen Y, Norkin LC. 78.  1999. Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae. Exp. Cell Res. 246:83–90 [Google Scholar]
  79. Anderson HA, Chen Y, Norkin LC. 79.  1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 7:1825–34 [Google Scholar]
  80. Dupzyk A, Tsai B. 80.  2016. How polyomaviruses exploit the ERAD machinery to cause infection. Viruses 8:242 [Google Scholar]
  81. Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L. 81.  et al. 2007. Simian virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131:516–29 [Google Scholar]
  82. Gilbert J, Ou W, Silver J, Benjamin T. 82.  2006. Downregulation of protein disulfide isomerase inhibits infection by the mouse polyomavirus. J. Virol. 80:10868–70 [Google Scholar]
  83. Walczak CP, Tsai B. 83.  2011. A PDI family network acts distinctly and coordinately with ERp29 to facilitate polyomavirus infection. J. Virol. 85:2386–96 [Google Scholar]
  84. Nelson C, Carney D, Derdowski A, Lipovsky A, Gee G. 84.  et al. 2013. A retrograde trafficking inhibitor of ricin and Shiga-like toxins inhibits infection of cells by human and monkey polyomaviruses. mBio 4:13 [Google Scholar]
  85. Nelson C, Derdowski A, Maginnis M, O'Hara B, Atwood W. 85.  2012. The VP1 subunit of JC polyomavirus recapitulates early events in viral trafficking and is a novel tool to study polyomavirus entry. Virology 428:30–40 [Google Scholar]
  86. Goodwin EC, Lipovsky A, Inoue T, Magaldi TG, Edwards AP. 86.  et al. 2011. BiP and multiple DNAJ molecular chaperones in the endoplasmic reticulum are required for efficient simian virus 40 infection. mBio 2:e00101–11 [Google Scholar]
  87. Querbes W, O'Hara B, Williams G, Atwood W. 87.  2006. Invasion of host cells by JC virus identifies a novel role for caveolae in endosomal sorting of noncaveolar ligands. J. Virol. 80:9402–13 [Google Scholar]
  88. Stechmann B, Bai SK, Gobbo E, Lopez R, Merer G. 88.  et al. 2010. Inhibition of retrograde transport protects mice from lethal ricin challenge. Cell 141:231–42 [Google Scholar]
  89. Astrom KE, Mancall EL, Richardson EP Jr. 89.  1958. Progressive multifocal leuko-encephalopathy; a hitherto unrecognized complication of chronic lymphatic leukaemia and Hodgkin's disease. Brain 81:93–111 [Google Scholar]
  90. Richardson EP Jr. 90.  1961. Progressive multifocal leukoencephalopathy. N. Engl. J. Med. 265:815–23 [Google Scholar]
  91. Zurhein G, Chou SM. 91.  1965. Particles resembling papova viruses in human cerebral demyelinating disease. Science 148:1477–79 [Google Scholar]
  92. Silverman L, Rubinstein LJ. 92.  1965. Electron microscopic observations on a case of progressive multifocal leukoencephalopathy. Acta Neuropathol 5:215–24 [Google Scholar]
  93. Padgett BL, Walker DL, ZuRhein GM, Hodach AE, Chou SM. 93.  1976. JC papovavirus in progressive multifocal leukoencephalopathy. J. Infect. Dis. 133:686–90 [Google Scholar]
  94. Shein HM. 94.  1965. Propagation of human fetal spongioblasts and astrocytes in dispersed cell cultures. Exp. Cell Res. 40:554–69 [Google Scholar]
  95. Major EO, Vacante DA. 95.  1989. Human fetal astrocytes in culture support the growth of the neurotropic human polyomavirus, JCV. J. Neuropathol. Exp. Neurol. 48:425–36 [Google Scholar]
  96. Major EO, Miller AE, Mourrain P, Traub RG, de Widt E, Sever J. 96.  1985. Establishment of a line of human fetal glial cells that supports JC virus multiplication. PNAS 82:1257–61 [Google Scholar]
  97. Wroblewska Z, Wellish M, Gilden D. 97.  1980. Growth of JC virus in adult human brain cell cultures. Arch. Virol. 65:141–48 [Google Scholar]
  98. Mandl C, Walker DL, Frisque RJ. 98.  1987. Derivation and characterization of POJ cells, transformed human fetal glial cells that retain their permissivity for JC virus. J. Virol. 61:755–63 [Google Scholar]
  99. Adelman B, Sandrock A, Panzara MA. 99.  2005. Natalizumab and progressive multifocal leukoencephalopathy. N. Engl. J. Med. 353:432–33 [Google Scholar]
  100. Major EO. 100.  2010. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu. Rev. Med. 61:35–47 [Google Scholar]
  101. Friedman-Kien AE. 101.  1981. Disseminated Kaposi's sarcoma syndrome in young homosexual men. J. Am. Acad. Dermatol. 5:468–71 [Google Scholar]
  102. Gottlieb MS, Shanker HM, Fan PT. 102.  1981. Pneumocystis pneumonia—Los Angeles. Morb. Mortal. Wkly. Rep. 30:250–52 [Google Scholar]
  103. Friedman-Kien AE, Laubenstein L, Marmor M. 103.  1981. Kaposi's sarcoma and pneumocystis pneumonia among homosexual men—New York City and California. Morb. Mortal. Wkly. Rep. 30:305–8 [Google Scholar]
  104. Miller JR, Barrett RE, Britton CB, Tapper ML, Bahr GS. 104.  et al. 1982. Progressive multifocal leukoencephalopathy in a male homosexual with T-cell immune deficiency. N. Engl. J. Med. 307:1436–38 [Google Scholar]
  105. Bernick C, Gregorios JB. 105.  1984. Progressive multifocal leukoencephalopathy in a patient with acquired immune deficiency syndrome. Arch. Neurol. 41:780–82 [Google Scholar]
  106. Brooks BR, Walker DL. 106.  1984. Progressive multifocal leukoencephalopathy. Neurol. Clin. 2:299–313 [Google Scholar]
  107. Holman RC, Torok TJ, Belay ED, Janssen RS, Schonberger LB. 107.  1998. Progressive multifocal leukoencephalopathy in the United States, 1979–1994: increased mortality associated with HIV infection. Neuroepidemiology 17:303–9 [Google Scholar]
  108. Holman RC, Janssen RS, Buehler JW, Zelasky MT, Hooper WC. 108.  1991. Epidemiology of progressive multifocal leukoencephalopathy in the United States: analysis of national mortality and AIDS surveillance data. Neurology 41:1733–36 [Google Scholar]
  109. Berger JR, Pall L, Lanska D, Whiteman M. 109.  1998. Progressive multifocal leukoencephalopathy in patients with HIV infection. J. Neurovirol. 4:59–68 [Google Scholar]
  110. Berger JR, Levy RM, Flomenhoft D, Dobbs M. 110.  1998. Predictive factors for prolonged survival in acquired immunodeficiency syndrome–associated progressive multifocal leukoencephalopathy. Ann. Neurol. 44:341–49 [Google Scholar]
  111. Selik RM, Karon JM, Ward JW. 111.  1997. Effect of the human immunodeficiency virus epidemic on mortality from opportunistic infections in the United States in 1993. J. Infect. Dis. 176:632–36 [Google Scholar]
  112. Molloy ES, Calabrese LH. 112.  2009. Progressive multifocal leukoencephalopathy: a national estimate of frequency in systemic lupus erythematosus and other rheumatic diseases. Arthritis Rheum 60:3761–65 [Google Scholar]
  113. Koralnik IJ. 113.  2004. New insights into progressive multifocal leukoencephalopathy. Curr. Opin. Neurol. 17:365–70 [Google Scholar]
  114. Christensen KL, Holman RC, Hammett TA, Belay ED, Schonberger LB. 114.  2010. Progressive multifocal leukoencephalopathy deaths in the USA, 1979–2005. Neuroepidemiology 35:178–84 [Google Scholar]
  115. Antinori A, Cingolani A, Lorenzini P, Giancola ML, Uccella I. 115.  et al. 2003. Clinical epidemiology and survival of progressive multifocal leukoencephalopathy in the era of highly active antiretroviral therapy: data from the Italian Registry Investigative Neuro AIDS (IRINA). J. Neurovirol. 9:Suppl. 147–53 [Google Scholar]
  116. Cinque P, Koralnik IJ, Gerevini S, Miro JM, Price RW. 116.  2009. Progressive multifocal leukoencephalopathy in HIV-1 infection. Lancet Infect. Dis. 9:625–36 [Google Scholar]
  117. Sacktor N. 117.  2002. The epidemiology of human immunodeficiency virus–associated neurological disease in the era of highly active antiretroviral therapy. J. Neurovirol. 8:Suppl. 2115–21 [Google Scholar]
  118. Arkema EV, van Vollenhoven RF, Askling J, Group AS. 118.  2012. Incidence of progressive multifocal leukoencephalopathy in patients with rheumatoid arthritis: a national population-based study. Ann. Rheum. Dis. 71:1865–67 [Google Scholar]
  119. Patera AC, Butler SL, Cinque P, Clifford DB, Elston R. 119.  et al. 2015. 2nd International Conference on Progressive Multifocal Leukoencephalopathy (PML) 2015: JCV virology, progressive multifocal leukoencephalopathy pathogenesis, diagnosis and risk stratification, and new approaches to prevention and treatment. J. Neurovirol. 21:702–5 [Google Scholar]
  120. Williamson EM, Berger JR. 120.  2015. Infection risk in patients on multiple sclerosis therapeutics. CNS Drugs 29:229–44 [Google Scholar]
  121. Williamson EM, Berger JR. 121.  2015. Central nervous system infections with immunomodulatory therapies. Continuum 21:1577–98 [Google Scholar]
  122. Major EO, Nath A. 122.  2016. A link between long-term natalizumab dosing in MS and PML: putting the puzzle together. Neurol. Neuroimmunol. Neuroinflamm. 3:e235 [Google Scholar]
  123. Berger JR, Fox RJ. 123.  2016. Reassessing the risk of natalizumab-associated PML. J. Neurovirol 22:533–35 Erratum; 2016. J. Neurovirol. 22:536–37 [Google Scholar]
  124. Houff SA, Major EO, Katz DA, Kufta CV, Sever JL. 124.  et al. 1988. Involvement of JC virus–infected mononuclear cells from the bone marrow and spleen in the pathogenesis of progressive multifocal leukoencephalopathy. N. Engl. J. Med. 318:301–5 [Google Scholar]
  125. Tornatore C, Berger JR, Houff SA, Curfman B, Meyers K. 125.  et al. 1992. Detection of JC virus DNA in peripheral lymphocytes from patients with and without progressive multifocal leukoencephalopathy. Ann. Neurol. 31:454–62 [Google Scholar]
  126. Frohman EM, Monaco MC, Remington G, Ryschkewitsch C, Jensen PN. 126.  et al. 2014. JC virus in CD34+ and CD19+ cells in patients with multiple sclerosis treated with natalizumab. JAMA Neurol 71:596–602 [Google Scholar]
  127. Lindberg RL, Achtnichts L, Hoffmann F, Kuhle J, Kappos L. 127.  2008. Natalizumab alters transcriptional expression profiles of blood cell subpopulations of multiple sclerosis patients. J. Neuroimmunol. 194:153–64 [Google Scholar]
  128. Bonig H, Wundes A, Chang KH, Lucas S, Papayannopoulou T. 128.  2008. Increased numbers of circulating hematopoietic stem/progenitor cells are chronically maintained in patients treated with the CD49d blocking antibody natalizumab. Blood 111:3439–41 [Google Scholar]
  129. Zohren F, Toutzaris D, Klarner V, Hartung HP, Kieseier B, Haas R. 129.  2008. The monoclonal anti–VLA-4 antibody natalizumab mobilizes CD34+ hematopoietic progenitor cells in humans. Blood 111:3893–95 [Google Scholar]
  130. Tan CS, Ellis LC, Wuthrich C, Ngo L, Broge TA Jr. 130.  et al. 2010. JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J. Virol. 84:9200–9 [Google Scholar]
  131. Lam WY, Leung BW, Chu IM, Chan AC, Ng HK, Chan PK. 131.  2010. Survey for the presence of BK, JC, KI, WU and Merkel cell polyomaviruses in human brain tissues. J. Clin. Virol. 48:11–4 [Google Scholar]
  132. Bayliss J, Karasoulos T, Bowden S, Glogowski I, McLean CA. 132.  2011. Immunosuppression increases latent infection of brain by JC polyomavirus. Pathology 43:362–67 [Google Scholar]
  133. Perez-Liz G, Del Valle L, Gentilella A, Croul S, Khalili K. 133.  2008. Detection of JC virus DNA fragments but not proteins in normal brain tissue. Ann. Neurol. 64:379–87 [Google Scholar]
  134. Delbue S, Branchetti E, Boldorini R, Vago L, Zerbi P. 134.  et al. 2008. Presence and expression of JCV early gene large T antigen in the brains of immunocompromised and immunocompetent individuals. J. Med. Virol 802147–52 [Google Scholar]
  135. Haley SA, Atwood WJ. 135.  2014. An animal model for progressive multifocal leukoencephalopathy. J. Clin. Investig. 124:5103–6 [Google Scholar]
  136. Kondo Y, Windrem MS, Zou L, Chandler-Militello D, Schanz SJ. 136.  et al. 2014. Human glial chimeric mice reveal astrocytic dependence of JC virus infection. J. Clin. Investig. 124:5323–36 [Google Scholar]
  137. White MK, Gordon J, Berger JR, Khalili K. 137.  2015. Animal models for progressive multifocal leukoencephalopathy. J. Cell. Physiol. 230:2869–74 [Google Scholar]
  138. Fanning E, Zhao K. 138.  2009. SV40 DNA replication: from the A gene to a nanomachine. Virology 384:352–59 [Google Scholar]
  139. Eichman BF, Fanning E. 139.  2004. The power of pumping together; deconstructing the engine of a DNA replication machine. Cell 119:3–4 [Google Scholar]
  140. Sowd GA, Fanning E. 140.  2012. A wolf in sheep's clothing: SV40 co-opts host genome maintenance proteins to replicate viral DNA. PLOS Pathog 8:e1002994 [Google Scholar]
/content/journals/10.1146/annurev-virology-101416-041439
Loading
/content/journals/10.1146/annurev-virology-101416-041439
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error