Human Polyomavirus Receptor Distribution in Brain Parenchyma Contrasts with Receptor Distribution in Kidney and Choroid Plexus

American Journal of Pathology

Volumn 185, Issue 8, 2015, Pages 2246-2258

  Haley, Sheila A ^a   O'Hara, Bethany A ^a   Nelson, Christian D S ^a   Brittingham, Frances L P ^a   Henriksen, Kammi J ^a   Stopa, Edward G ^a   Atwood, Walter J ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN POLYOMAVIRUS RECEPTOR; PENTASACCHARIDE; SEROTONIN RECEPTOR; TETRASACCHARIDE; UNCLASSIFIED DRUG; VIRUS RECEPTOR; GLYCAN SIALYLNEOLACTO-N-TETRAOSE C; POLYSACCHARIDE; SEROTONIN 2 RECEPTOR; SIALIC ACID DERIVATIVE;

ANTIGEN RETRIEVAL; ARTICLE; ASTROCYTE; BRAIN; BRAIN PARENCHYMA; CENTRAL NERVOUS SYSTEM; CHOROID PLEXUS; CONTROLLED STUDY; DEMYELINATING DISEASE; DISEASE COURSE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY; OLIGODENDROGLIA; PARENCHYMA; POLYOMAVIRUS; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; TISSUE PREPARATION; VASCULAR ENDOTHELIUM; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INFECTION; ADULT; AGED; FEMALE; JC VIRUS; MALE; METABOLISM; MIDDLE AGED; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ASTROCYTES; BRAIN; CHOROID PLEXUS; FEMALE; HUMANS; JC VIRUS; KIDNEY; MALE; MIDDLE AGED; OLIGODENDROGLIA; POLYSACCHARIDES; RECEPTORS, SEROTONIN, 5-HT2; RECEPTORS, VIRUS; SIALIC ACIDS;

EID: 84937853690     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.04.003     Document Type: Article

References (95)

1. J.M. Kean, S. Rao, M. Wang, and R.L. Garcea Seroepidemiology of human polyomaviruses PLoS Pathog 5 2009 e1000363
2. W.A. Knowles, P. Pipkin, N. Andrews, A. Vyse, P. Minor, D.W. Brown, and E. Miller Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40 J Med Virol 71 2003 115 123
3. K. Dorries Molecular biology and pathogenesis of human polyomavirus infections Dev Biol Stand 94 1998 71 79
4. A. Egli, L. Infanti, A. Dumoulin, A. Buser, J. Samaridis, C. Stebler, R. Gosert, and H.H. Hirsch Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors J Infect Dis 199 2009 837 846
5. M.C. Monaco, P.N. Jensen, J. Hou, L.C. Durham, and E.O. Major Detection of JC virus DNA in human tonsil tissue: evidence for site of initial viral infection J Virol 72 1998 9918 9923
6. M.C. Monaco, W.J. Atwood, M. Gravell, C.S. Tornatore, and E.O. Major JC virus infection of hematopoietic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: implications for viral latency J Virol 70 1996 7004 7012
7. B. Grinnell, B. Padgett, and D. Walker Distribution of nonintegrated DNA from JC papovavirus in organs of patients with progressive multifocal leukoencephalopathy J Infect Dis 147 1983 669 675
8. J.T. Newman, and R.J. Frisque Detection of archetype and rearranged variants of JC virus in multiple tissues from a pediatric PML patient J Med Virol 52 1997 243 252
9. W.J. Atwood, K. Amemiya, R. Traub, J. Harms, and E.O. Major Interaction of the human polyomavirus, JCV, with human B-lymphocytes Virology 190 1992 716 723
10. E.O. Major, K. Amemiya, G. Elder, and S.A. Houff 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 1990 461 471
11. R. Caldarelli-Stefano, L. Vago, E. Omodeo-Zorini, M. Mediati, L. Losciale, M. Nebuloni, G. Costanzi, and P. Ferrante Detection and typing of JC virus in autopsy brains and extraneural organs of AIDS patients and non-immunocompromised individuals J Neurovirol 5 1999 125 133
12. J. Bayliss, T. Karasoulos, and C.A. McLean Immunosuppression increases JC polyomavirus large T antigen DNA load in the brains of patients without progressive multifocal leukoencephalopathy J Infect Dis 207 2013 133 136
13. C.S. Tan, L.C. Ellis, C. Wuthrich, L. Ngo, T.A. Broge Jr., J. Saint-Aubyn, J.S. Miller, and I.J. Koralnik JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy J Virol 84 2010 9200 9209
14. S. Gheuens, C. Wuthrich, and I.J. Koralnik Progressive multifocal leukoencephalopathy: why gray and white matter Annu Rev Pathol 8 2013 189 215
15. J.R. Berger, A.J. Aksamit, D.B. Clifford, L. Davis, I.J. Koralnik, J.J. Sejvar, R. Bartt, E.O. Major, and A. Nath PML diagnostic criteria: consensus statement from the AAN Neuroinfectious Disease Section Neurology 80 2013 1430 1438
16. K. Astrom, E. Mancall, and E.P. Richardson Jr. Progressive multifocal leukoencephalopathy Brain 81 1958 93 127
17. B. Brooks, and D. Walker Progressive multifocal leukoencephalopathy Neurol Clin 2 1984 299 313
18. P. Cinque, I.J. Koralnik, S. Gerevini, J.M. Miro, and R.W. Price Progressive multifocal leukoencephalopathy in HIV-1 infection Lancet Infect Dis 9 2009 625 636
19. M.W. Ferenczy, L.J. Marshall, C.D. Nelson, W.J. Atwood, A. Nath, K. Khalili, and E.O. Major Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain Clin Microbiol Rev 25 2012 471 506
20. S. Grabar, E. Lanoy, C. Allavena, M. Mary-Krause, M. Bentata, P. Fischer, A. Mahamat, C. Rabaud, D. Costagliola Clinical Epidemiology Group of the French Hospital Database on HIV Causes of the first AIDS-defining illness and subsequent survival before and after the advent of combined antiretroviral therapy HIV Med 9 2008 246 256
21. K.R. Carson, D. Focosi, E.O. Major, M. Petrini, E.A. Richey, D.P. West, and C.L. Bennett Monoclonal antibody-associated progressive multifocal leucoencephalopathy in patients treated with rituximab, natalizumab, and efalizumab: a Review from the Research on Adverse Drug Events and Reports (RADAR) Project Lancet Oncol 10 2009 816 824
22. E.O. Major Reemergence of PML in natalizumab-treated patients-new cases, same concerns N Engl J Med 361 2009 1041 1043
23. G. Van Assche, M. Van Ranst, R. Sciot, B. Dubois, S. Vermeire, M. Noman, J. Verbeeck, K. Geboes, W. Robberecht, and P. Rutgeerts Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease N Engl J Med 353 2005 362 368
24. B.K. Kleinschmidt-DeMasters, and K.L. Tyler Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis N Engl J Med 353 2005 369 374
25. A. Langer-Gould, S.W. Atlas, A.J. Green, A.W. Bollen, and D. Pelletier Progressive multifocal leukoencephalopathy in a patient treated with natalizumab N Engl J Med 353 2005 375 381
26. F. Zaheer, and J.R. Berger Treatment-related progressive multifocal leukoencephalopathy: current understanding and future steps Ther Adv Drug Saf 3 2012 227 239
27. I.J. Koralnik, C. Wuthrich, X. Dang, M. Rottnek, A. Gurtman, D. Simpson, and S. Morgello JC virus granule cell neuronopathy: a novel clinical syndrome distinct from progressive multifocal leukoencephalopathy Ann Neurol 57 2005 576 580
28. C. Wuthrich, X. Dang, S. Westmoreland, J. McKay, A. Maheshwari, M.P. Anderson, A.H. Ropper, R.P. Viscidi, and I.J. Koralnik Fulminant JC virus encephalopathy with productive infection of cortical pyramidal neurons Ann Neurol 65 2009 742 748
29. P. Randhawa, F. Baksh, N. Aoki, D. Tschirhart, and S. Finkelstein JC virus infection in allograft kidneys: analysis by polymerase chain reaction and immunohistochemistry Transplantation 71 2001 1300 1303
30. I. Lautenschlager, T. Jahnukainen, P. Kardas, J. Lohi, E. Auvinen, L. Mannonen, A. Dumoulin, H.H. Hirsch, and H. Jalanko A Case of Primary JC Polyomavirus Infection-Associated Nephropathy Am J Transplant 14 2014 2887 2892
31. C.B. Drachenberg, H.H. Hirsch, J.C. Papadimitriou, R. Gosert, R.K. Wali, R. Munivenkatappa, J. Nogueira, C.B. Cangro, A. Haririan, S. Mendley, and E. Ramos Polyomavirus BK versus JC replication and nephropathy in renal transplant recipients: a prospective evaluation Transplantation 84 2007 323 330
32. A. Kazory, D. Ducloux, J.M. Chalopin, R. Angonin, B. Fontaniere, and H. Moret The first case of JC virus allograft nephropathy Transplantation 76 2003 1653 1655
33. Shah KV: Polyomaviruses. Fields Virology, 3rd Edition. Edited by Fields BN, Knipe DM, Howley PM. Philadelphia, PA, Lippincott-Raven, 1996. pp. 2027-2043
34. A.S. Dugan, M.L. Gasparovic, and W.J. Atwood Direct correlation between sialic acid binding and infection of cells by two human polyomaviruses (JC virus and BK virus) J Virol 82 2008 2560 2564
35. R. Komagome, H. Sawa, T. Suzuki, Y. Suzuki, S. Tanaka, W.J. Atwood, and K. Nagashima Oligosaccharides as receptors for JC virus J Virol 76 2002 12992 13000
36. C.K. Liu, G. Wei, and W.J. Atwood Infection of glial cells by the human polyomavirus JC is mediated by an N-linked glycoprotein containing terminal alpha 2-6 linked sialic acids J Virol 72 1998 4643 4649
37. U. Neu, M.S. Maginnis, A.S. Palma, L.J. Stroh, C.D. Nelson, T. Feizi, W.J. Atwood, and T. Stehle Structure-function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif Cell Host Microbe 8 2010 309 319
38. G.F. Elphick, W. Querbes, J.A. Jordan, G.V. Gee, S. Eash, K. Manley, A. Dugan, M. Stanifer, A. Bhatnagar, W.K. Kroeze, B.L. Roth, and W.J. Atwood The human polyomavirus, JCV, uses serotonin receptors to infect cells Science 306 2004 1380 1383
39. B. Assetta, M.S. Maginnis, I. Gracia Ahufinger, S.A. Haley, G.V. Gee, C.D. Nelson, B.A. O'Hara, S.A. Allen Ramdial, and W.J. Atwood 5-HT2 receptors facilitate JC polyomavirus entry J Virol 87 2013 13490 13498
40. C.K. Liu, and W.J. Atwood Propagation and assay of the JC virus Methods Mol Biol 165 2001 9 17
41. C.D. Nelson, D.W. Carney, A. Derdowski, A. Lipovsky, G.V. Gee, B. O'Hara, P. Williard, D. DiMaio, J.K. Sello, and W.J. Atwood A retrograde trafficking inhibitor of ricin and Shiga-like toxins inhibits infection of cells by human and monkey polyomaviruses MBio 4 2013 e00729-13
42. S. Morgello, B.B. Gelman, P.B. Kozlowski, H.V. Vinters, E. Masliah, M. Cornford, W. Cavert, C. Marra, I. Grant, and E.J. Singer The National NeuroAIDS Tissue Consortium: a new paradigm in brain banking with an emphasis on infectious disease Neuropathol Appl Neurobiol 27 2001 326 335
43. W.J. Atwood, L. Wang, L.C. Durham, K. Amemiya, R.G. Traub, and E.O. Major Evaluation of the role of cytokine activation in the multiplication of JC virus (JCV) in human fetal glial cells J Neurovirol 1 1995 40 49
44. C. Henmi, H. Sawa, H. Iwata, Y. Orba, S. Tanaka, and K. Nagashima Establishment of an immunoscreening system using recombinant VP1 protein for the isolation of a monoclonal antibody that blocks JC virus infection Biochem Biophys Res Commun 327 2005 242 251
45. A.J. Howie Epithelial membrane antigen in normal and proteinuric glomeruli and in damaged proximal tubules J Pathol 148 1986 55 60
46. S.M. Meehan, M.D. Kraus, P.V. Kadambi, and A. Chang Nephron segment localization of polyoma virus large T antigen in renal allografts Hum Pathol 37 2006 1400 1406
47. H. Mo, H.C. Winter, and I.J. Goldstein Purification and characterization of a Neu5Acalpha2-6Galbeta1-4Glc/GlcNAc-specific lectin from the fruiting body of the polypore mushroom Polyporus squamosus J Biol Chem 275 2000 10623 10629
48. B. Zhang, M.M. Palcic, H. Mo, I.J. Goldstein, and O. Hindsgaul Rapid determination of the binding affinity and specificity of the mushroom Polyporus squamosus lectin using frontal affinity chromatography coupled to electrospray mass spectrometry Glycobiology 11 2001 141 147
49. V. Toma, C. Zuber, H.C. Winter, I.J. Goldstein, and J. Roth Application of a lectin from the mushroom Polysporus squamosus for the histochemical detection of the NeuAcalpha2,6Galbeta1,4Glc/GlcNAc sequence of N-linked oligosaccharides: a comparison with the Sambucus nigra lectin Histochem Cell Biol 116 2001 183 193
50. M.S. Maginnis, S.A. Haley, G.V. Gee, and W.J. Atwood Role of N-linked glycosylation of the 5-HT2A receptor in JC virus infection J Virol 84 2010 9677 9684
51. K. Dorries, and V. ter Meulen Progressive multifocal leucoencephalopathy: detection of papovavirus JC in kidney tissue J Med Virol 11 1983 307 317
52. R. Boldorini, E. Omodeo-Zorini, M. Nebuloni, E. Benigni, L. Vago, A. Ferri, and G. Monga Lytic JC virus infection in the kidneys of AIDS subjects Mod Pathol 16 2003 35 42
53. M.C. Wen, C.L. Wang, M. Wang, C.H. Cheng, M.J. Wu, C.H. Chen, K.H. Shu, and D. Chang Association of JC virus with tubulointerstitial nephritis in a renal allograft recipient J Med Virol 72 2004 675 678
54. G. Kantarci, Z. Eren, A. Demirag, I. Dogan, F. Cakalagaoglu, and G. Yilmaz JC virus-associated nephropathy in a renal transplant recipient and comparative analysis of previous cases Transpl Infect Dis 13 2011 89 92
55. S. Delbue, M. Ferraresso, L. Ghio, C. Carloni, S. Carluccio, M. Belingheri, A. Edefonti, and P. Ferrante A review on JC virus infection in kidney transplant recipients Clin Dev Immunol 2013 2013 926391
56. N. Aoki, T. Kitamura, T. Tominaga, N. Fukumori, Y. Sakamoto, K. Kato, and M. Mori Immunohistochemical detection of JC virus in nontumorous renal tissue of a patient with renal cancer but without progressive multifocal leukoencephalopathy J Clin Microbiol 37 1999 1165 1167
57. H.H. Hirsch, P. Kardas, D. Kranz, and C. Leboeuf The human JC polyomavirus (JCPyV): virological background and clinical implications APMIS 121 2013 685 727
58. V. Nickeleit, and M.J. Mihatsch Polyomavirus nephropathy in native kidneys and renal allografts: an update on an escalating threat Transpl Int 19 2006 960 973
59. K. Dorries, R.T. Johnson, and V. ter Meulen Detection of polyoma virus DNA in PML-brain tissue by (in situ) hybridization J Gen Virol 42 1979 49 57
60. R.W. von Einsiedel, I.W. Samorei, M. Pawlita, B. Zwissler, M. Deubel, and H.V. Vinters New JC virus infection patterns by in situ polymerase chain reaction in brains of acquired immunodeficiency syndrome patients with progressive multifocal leukoencephalopathy J Neurovirol 10 2004 1 11
61. M.L. Chapagain, S. Verma, F. Mercier, R. Yanagihara, and V.R. Nerurkar Polyomavirus JC infects human brain microvascular endothelial cells independent of serotonin receptor 2A Virology 364 2007 55 63
62. B. Engelhardt, and R.M. Ransohoff Capture, crawl, cross: the T cell code to breach the blood-brain barriers Trends Immunol 33 2012 579 589
63. W.F. Hickey Leukocyte traffic in the central nervous system: the participants and their roles Semin Immunol 11 1999 125 137
64. N.S. Ivey, A.G. MacLean, and A.A. Lackner Acquired immunodeficiency syndrome and the blood-brain barrier J Neurovirol 15 2009 111 122
65. P. Annunziata Blood-brain barrier changes during invasion of the central nervous system by HIV-1. Old and new insights into the mechanism J Neurol 250 2003 901 906
66. Y. Persidsky, A. Ghorpade, J. Rasmussen, J. Limoges, X.J. Liu, M. Stins, M. Fiala, D. Way, K.S. Kim, M.H. Witte, M. Weinand, L. Carhart, and H.E. Gendelman Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis Am J Pathol 155 1999 1599 1611
67. C.K. Petito, B. Adkins, M. McCarthy, B. Roberts, and I. Khamis CD4+ and CD8+ cells accumulate in the brains of acquired immunodeficiency syndrome patients with human immunodeficiency virus encephalitis J Neurovirol 9 2003 36 44
68. H.E. Gendelman, S. Ding, N. Gong, J. Liu, S.H. Ramirez, Y. Persidsky, R.L. Mosley, T. Wang, D.J. Volsky, and H. Xiong Monocyte chemotactic protein-1 regulates voltage-gated K+ channels and macrophage transmigration J Neuroimmune Pharmacol 4 2009 47 59
69. N. Didier, I.A. Romero, C. Creminon, A. Wijkhuisen, J. Grassi, and A. Mabondzo Secretion of interleukin-1beta by astrocytes mediates endothelin-1 and tumour necrosis factor-alpha effects on human brain microvascular endothelial cell permeability J Neurochem 86 2003 246 254
70. A.G. Maclean, G.E. Belenchia, D.N. Bieniemy, T.A. Moroney-Rasmussen, and A.A. Lackner Simian immunodeficiency virus disrupts extended lengths of the blood-brain barrier J Med Primatol 34 2005 237 242
71. J.P. Louboutin, B.A. Reyes, L. Agrawal, E.J. Van Bockstaele, and D.S. Strayer HIV-1 gp120 upregulates matrix metalloproteinases and their inhibitors in a rat model of HIV encephalopathy Eur J Neurosci 34 2011 2015 2023
72. B. Wispelwey, A.J. Lesse, E.J. Hansen, and W.M. Scheld Haemophilus influenzae lipopolysaccharide-induced blood brain barrier permeability during experimental meningitis in the rat J Clin Invest 82 1988 1339 1346
73. W.A. Banks, and M.A. Erickson The blood-brain barrier and immune function and dysfunction Neurobiol Dis 37 2010 26 32
74. W.A. Banks, A.J. Kastin, J.M. Brennan, and K.L. Vallance Adsorptive endocytosis of HIV-1gp120 by blood-brain barrier is enhanced by lipopolysaccharide Exp Neurol 156 1999 165 171
75. C. Johanson, E. Stopa, P. McMillan, D. Roth, J. Funk, and G. Krinke The distributional nexus of choroid plexus to cerebrospinal fluid, ependyma and brain: toxicologic/pathologic phenomena, periventricular destabilization, and lesion spread Toxicol Pathol 39 2011 186 212
76. J. Szmydynger-Chodobska, N. Strazielle, J.R. Gandy, T.H. Keefe, B.J. Zink, J.F. Ghersi-Egea, and A. Chodobski Posttraumatic invasion of monocytes across the blood-cerebrospinal fluid barrier J Cereb Blood Flow Metab 32 2012 93 104
77. R. Shechter, A. London, and M. Schwartz Orchestrated leukocyte recruitment to immune-privileged sites: absolute barriers versus educational gates Nat Rev Immunol 13 2013 206 218
78. G. Kunis, K. Baruch, N. Rosenzweig, A. Kertser, O. Miller, T. Berkutzki, and M. Schwartz IFN-gamma-dependent activation of the brain's choroid plexus for CNS immune surveillance and repair Brain 136 2013 3427 3440
79. M. Pasqualetti, M. Ori, M. Castagna, D. Marazziti, G.B. Cassano, and I. Nardi Distribution and cellular localization of the serotonin type 2C receptor messenger RNA in human brain Neuroscience 92 1999 601 611
80. D.E. Nichols, and C.D. Nichols Serotonin receptors Chem Rev 108 2008 1614 1641
81. J.R. Backstrom, R.S. Westphal, H. Canton, and E. Sanders-Bush Identification of rat serotonin 5-HT2C receptors as glycoproteins containing N-linked oligosaccharides Brain Res Mol Brain Res 33 1995 311 318
82. M. Sathyanesan, M.J. Girgenti, M. Banasr, K. Stone, C. Bruce, E. Guilchicek, K. Wilczak-Havill, A. Nairn, K. Williams, S. Sass, J.G. Duman, and S.S. Newton A molecular characterization of the choroid plexus and stress-induced gene regulation Transl Psychiatry 2 2012 e139
83. S.P. Agnihotri, C. Wuthrich, X. Dang, D. Nauen, R. Karimi, R. Viscidi, E. Bord, S. Batson, J. Troncoso, and I.J. Koralnik A fatal case of JC virus meningitis presenting with hydrocephalus in a human immunodeficiency virus-seronegative patient Ann Neurol 76 2014 140 147
84. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo Science 308 2005 1314 1318
85. R.M. Ransohoff, and A.E. Cardona The myeloid cells of the central nervous system parenchyma Nature 468 2010 253 262
86. R. Grossmann, N. Stence, J. Carr, L. Fuller, M. Waite, and M.E. Dailey Juxtavascular microglia migrate along brain microvessels following activation during early postnatal development Glia 37 2002 229 240
87. D. Davalos, J. Grutzendler, G. Yang, J.V. Kim, Y. Zuo, S. Jung, D.R. Littman, M.L. Dustin, and W.B. Gan ATP mediates rapid microglial response to local brain injury in vivo Nat Neurosci 8 2005 752 758
88. N. Stence, M. Waite, and M.E. Dailey Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices Glia 33 2001 256 266
89. S.E. Haynes, G. Hollopeter, G. Yang, D. Kurpius, M.E. Dailey, W.B. Gan, and D. Julius The P2Y12 receptor regulates microglial activation by extracellular nucleotides Nat Neurosci 9 2006 1512 1519
90. M. Prinz, and J. Priller Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease Nat Rev Neurosci 15 2014 300 312
91. E.A. Siebrasse, N.L. Nguyen, C. Smith, P. Simmonds, and D. Wang Immunohistochemical detection of KI polyomavirus in lung and spleen Virology 468-470 2014 178 184
92. J. Simon-Santamaria, C.H. Rinaldo, P. Kardas, R. Li, I. Malovic, K. Elvevold, P. McCourt, B. Smedsrod, H.H. Hirsch, and K.K. Sorensen Efficient Uptake of Blood-Borne BK and JC Polyomavirus-Like Particles in Endothelial Cells of Liver Sinusoids and Renal Vasa Recta PLoS One 9 2014 e111762
93. C.E. Reid, H. Li, G. Sur, P. Carmillo, S. Bushnell, R. Tizard, M. McAuliffe, C. Tonkin, K. Simon, S. Goelz, P. Cinque, L. Gorelik, and J.P. Carulli Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients J Infect Dis 204 2011 237 244
94. L. Gorelik, C. Reid, M. Testa, M. Brickelmaier, S. Bossolasco, A. Pazzi, A. Bestetti, P. Carmillo, E. Wilson, M. McAuliffe, C. Tonkin, J.P. Carulli, A. Lugovskoy, A. Lazzarin, S. Sunyaev, K. Simon, and P. Cinque Progressive multifocal leukoencephalopathy (PML) development is associated with mutations in JC virus capsid protein VP1 that change its receptor specificity J Infect Dis 204 2011 103 114
95. M.S. Maginnis, L.J. Stroh, G.V. Gee, B.A. O'Hara, A. Derdowski, T. Stehle, and W.J. Atwood Progressive multifocal leukoencephalopathy-associated mutations in the JC polyomavirus capsid disrupt lactoseries tetrasaccharide c binding MBio 4 2013 e00247-13