Infectious Entry and Neutralization of Pathogenic JC Polyomaviruses

Cell Reports

Volumn 21, Issue 5, 2017, Pages 1169-1179

  Geoghegan, Eileen M ^a   Pastrana, Diana V ^a   Schowalter, Rachel M ^a   Ray, Upasana ^a   Gao, Wei ^a   Ho, Mitchell ^a   Pauly, Gary T ^b   Sigano, Dina M ^b   Kaynor, Campbell ^c   Cahir McFarland, Ellen ^c   Combaluzier, Benoit ^d   Grimm, Jan ^d   Buck, Christopher B ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c BIOGEN   (United States)

^d Neurimmune Holding AG   (Switzerland)

Author keywords

BK; JC; mAb; monoclonal antibody; PML; polyomavirus; progressive multifocal leukoencephalopathy; receptor; SV40; virus entry

Indexed keywords

CAPSID PROTEIN; GLYCOSAMINOGLYCAN; NEUTRALIZING ANTIBODY; GANGLIOSIDE; MONOCLONAL ANTIBODY; NUCLEOTIDE TRANSPORTER; P-3F(AX)-NEU5AC; PROTEIN BINDING; SIALIC ACID DERIVATIVE; SIALIDASE; SLC35A1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; JC VIRUS; NONHUMAN; PRIORITY JOURNAL; SIALYLATION; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS MUTANT; VIRUS NEUTRALIZATION; VIRUS STRAIN; VIRUS VIRULENCE; ANTAGONISTS AND INHIBITORS; DRUG EFFECT; GENETICS; GENOTYPE; HEMAGGLUTINATION; HUMAN; IMMUNOLOGY; METABOLISM; MUTATION; PATHOLOGY; PHYSIOLOGY; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; RNA INTERFERENCE; TUMOR CELL LINE; VIROLOGY;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; CAPSID PROTEINS; CELL LINE, TUMOR; GANGLIOSIDES; GENOTYPE; GLYCOSAMINOGLYCANS; HEMAGGLUTINATION; HUMANS; JC VIRUS; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; MUTATION; NEURAMINIDASE; NUCLEOTIDE TRANSPORT PROTEINS; PROTEIN BINDING; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIALIC ACIDS; VIRUS INTERNALIZATION;

EID: 85034854854     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.10.027     Document Type: Article

References (78)

1. Al-Zahrani, A.A., Gajewski, J.B., Long-term efficacy and tolerability of pentosan polysulphate sodium in the treatment of bladder pain syndrome. Can. Urol. Assoc. J. 5 (2011), 113–118.
2. Arthur, R.R., Shah, K.V., Baust, S.J., Santos, G.W., Saral, R., Association of BK viruria with hemorrhagic cystitis in recipients of bone marrow transplants. N. Engl. J. Med. 315 (1986), 230–234.
3. Bauer, P.H., Cui, C., Liu, W.R., Stehle, T., Harrison, S.C., DeCaprio, J.A., Benjamin, T.L., Discrimination between sialic acid-containing receptors and pseudoreceptors regulates polyomavirus spread in the mouse. J. Virol. 73 (1999), 5826–5832.
4. Bauer, J., Gold, R., Adams, O., Lassmann, H., Progressive multifocal leukoencephalopathy and immune reconstitution inflammatory syndrome (IRIS). Acta Neuropathol. 130 (2015), 751–764.
5. Berger, J.R., Fox, R.J., Reassessing the risk of natalizumab-associated PML. J. Neurovirol. 22, 533–535, 2016.
6. Buck, C.B., Pastrana, D.V., Lowy, D.R., Schiller, J.T., Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78 (2004), 751–757.
7. Carroll, J., Dey, D., Kreisman, L., Velupillai, P., Dahl, J., Telford, S., Bronson, R., Benjamin, T., Receptor-binding and oncogenic properties of polyoma viruses isolated from feral mice. PLoS Pathog., 3, 2007, e179.
8. Carson, K.R., Focosi, D., Major, E.O., Petrini, M., Richey, E.A., West, D.P., Bennett, C.L., 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.
9. Casado, J.L., Corral, I., García, J., Martinez-San Millán, J., Navas, E., Moreno, A., Moreno, S., Continued declining incidence and improved survival of progressive multifocal leukoencephalopathy in HIV/AIDS patients in the current era. Eur. J. Clin. Microbiol. Infect. Dis. 33 (2014), 179–187.
10. Cervigni, M., Interstitial cystitis/bladder pain syndrome and glycosaminoglycans replacement therapy. Transl. Androl. Urol. 4 (2015), 638–642.
11. Collazos, J., Opportunistic infections of the CNS in patients with AIDS: diagnosis and management. CNS Drugs 17 (2003), 869–887.
12. Dasgupta, S., Hogan, E.L., Molecular characterization of gangliotetraosylceramide (GA1) in normal human brain and its developmental change. Indian J. Biochem. Biophys. 30 (1993), 341–345.
13. Dasgupta, S., van Halbeek, H., Hogan, E.L., Ganglio-N-tetraosylceramide (GA1) of bovine and human brain. Molecular characterization and presence in myelin. FEBS Lett. 301 (1992), 141–144.
14. Dasgupta, S., van Halbeek, H., Spicer, S., Hogan, E.L., Molecular characterization and immunohistochemical localization of IV(4)GalNAcGgOse(4)Cer: a naturally occurring novel neutral glycosphingolipid in bovine brain. Glycobiology 10 (2000), 1–9.
15. Dasgupta, S., Bhat, N.R., Spicer, S.S., Hogan, E.L., Furuya, S., Hirabayashi, Y., Cell-specific expression of neutral glycosphingolipids in vertebrate brain: immunochemical localization of 3-O-acetyl-sphingosine-series glycolipid(s) in myelin and oligodendrocytes. J. Neurosci. Res. 85 (2007), 2856–2862.
16. DeCaprio, J.A., Garcea, R.L., A cornucopia of human polyomaviruses. Nat. Rev. Microbiol. 11 (2013), 264–276.
17. Diotti, R.A., Nakanishi, A., Clementi, N., Mancini, N., Criscuolo, E., Solforosi, L., Clementi, M., JC polyomavirus (JCV) and monoclonal antibodies: friends or potential foes?. Clin. Dev. Immunol., 2013, 2013, 967581.
18. Diotti, R.A., Mancini, N., Clementi, N., Sautto, G., Moreno, G.J., Criscuolo, E., Cappelletti, F., Man, P., Forest, E., Remy, L., et al. Cloning of the first human anti-JCPyV/VP1 neutralizing monoclonal antibody: epitope definition and implications in risk stratification of patients under natalizumab therapy. Antiviral Res. 108 (2014), 94–103.
19. Dowd, K.A., Pierson, T.C., Antibody-mediated neutralization of flaviviruses: a reductionist view. Virology 411 (2011), 306–315.
20. Dugan, A.S., Gasparovic, M.L., Atwood, W.J., 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.
21. Esko, J.D., Stewart, T.E., Taylor, W.H., Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA 82 (1985), 3197–3201.
22. Ewers, H., Romer, W., Smith, A.E., Bacia, K., Dmitrieff, S., Chai, W., Mancini, R., Kartenbeck, J., Chambon, V., Berland, L., et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat. Cell. Biol. 12 (2010), 11–18.
23. Farhy Tselnicker, I., Boisvert, M.M., Allen, N.J., The role of neuronal versus astrocyte-derived heparan sulfate proteoglycans in brain development and injury. Biochem. Soc. Trans. 42 (2014), 1263–1269.
24. Gao, W., Kim, H., Feng, M., Phung, Y., Xavier, C.P., Rubin, J.S., Ho, M., Inactivation of Wnt signaling by a human antibody that recognizes the heparan sulfate chains of glypican-3 for liver cancer therapy. Hepatology 60 (2014), 576–587.
25. Gorelik, L., Reid, C., Testa, M., Brickelmaier, M., Bossolasco, S., Pazzi, A., Bestetti, A., Carmillo, P., Wilson, E., McAuliffe, M., et al. 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.
26. Gossai, A., Waterboer, T., Nelson, H.H., Michel, A., Willhauck-Fleckenstein, M., Farzan, S.F., Hoen, A.G., Christensen, B.C., Kelsey, K.T., Marsit, C.J., et al. Seroepidemiology of human polyomaviruses in a US population. Am. J. Epidemiol. 183 (2016), 61–69.
27. Haley, S.A., O'Hara, B.A., Nelson, C.D.S., Brittingham, F.L.P., Henriksen, K.J., Stopa, E.G., Atwood, W.J., Human polyomavirus receptor distribution in brain parenchyma contrasts with receptor distribution in kidney and choroid plexus. Am. J. Pathol. 185 (2015), 2246–2258.
28. Hensley, S.E., Das, S.R., Bailey, A.L., Schmidt, L.M., Hickman, H.D., Jayaraman, A., Viswanathan, K., Raman, R., Sasisekharan, R., Bennink, J.R., Yewdell, J.W., Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326 (2009), 734–736.
29. Huang, L.Y., Halder, S., Agbandje-McKenna, M., Parvovirus glycan interactions. Curr. Opin. Virol. 7 (2014), 108–118.
30. Iavazzo, C., Athanasiou, S., Pitsouni, E., Falagas, M.E., Hyaluronic acid: an effective alternative treatment of interstitial cystitis, recurrent urinary tract infections, and hemorrhagic cystitis?. Eur. Urol. 51 (2007), 1534–1541.
31. Isik, P., Özbek, N., Azik, F., Arman Bilir, Ö., Baylan, B., Tunç, B., Successful treatment of hemorrhagic cystitis after hematopoietic stem cell transplantation with intravesical hyaluronic acid. Pediatr. Transplant. 18 (2014), 780–781.
32. Jelcic, I., Combaluzier, B., Jelcic, I., Faigle, W., Senn, L., Reinhart, B.J., Ströh, L., Nitsch, R.M., Stehle, T., Sospedra, M., et al. Broadly neutralizing human monoclonal JC polyomavirus VP1-specific antibodies as candidate therapeutics for progressive multifocal leukoencephalopathy. Sci. Transl. Med., 7, 2015, 306ra150.
33. Kamhi, E., Joo, E.J., Dordick, J.S., Linhardt, R.J., Glycosaminoglycans in infectious disease. Biol. Rev. Camb. Philos. Soc. 88 (2013), 928–943.
34. Kanda, T., Sullivan, K.F., Wahl, G.M., Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8 (1998), 377–385.
35. Kean, J.M., Rao, S., Wang, M., Garcea, R.L., Seroepidemiology of human polyomaviruses. PLoS Pathog., 5, 2009, e1000363.
36. Kleinschmidt-DeMasters, B.K., Tyler, K.L., Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N. Engl. J. Med. 353 (2005), 369–374.
37. Knowles, W.A., Pipkin, P., Andrews, N., Vyse, A., Minor, P., Brown, D.W., Miller, E., Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. J. Med. Virol. 71 (2003), 115–123.
38. Komagome, R., Sawa, H., Suzuki, T., Suzuki, Y., Tanaka, S., Atwood, W.J., Nagashima, K., Oligosaccharides as receptors for JC virus. J. Virol. 76 (2002), 12992–13000.
39. Kondo, Y., Windrem, M.S., Zou, L., Chandler-Militello, D., Schanz, S.J., Auvergne, R.M., Betstadt, S.J., Harrington, A.R., Johnson, M., Kazarov, A., et al. Human glial chimeric mice reveal astrocytic dependence of JC virus infection. J. Clin. Invest. 124 (2014), 5323–5336.
40. Kusunoki, S., Tsuji, S., Nagai, Y., Ganglio-N-tetraosylceramide (asialo GM1), an antigen common to the brain and immune system: its localization in myelin. Brain Res. 334 (1985), 117–124.
41. Langer-Gould, A., Atlas, S.W., Green, A.J., Bollen, A.W., Pelletier, D., Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N. Engl. J. Med. 353 (2005), 375–381.
42. Liu, C.K., Wei, G., Atwood, W.J., 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.
43. Lopes da Silva, R., Polyoma BK virus: an emerging opportunistic infectious agent of the human central nervous system. Braz. J. Infect. Dis. 15 (2011), 276–284.
44. Luo, Y., Motamedi, N., Magaldi, T.G., Gee, G.V., Atwood, W.J., DiMaio, D., Interaction between Simian virus 40 major capsid protein VP1 and cell surface ganglioside GM1 triggers vacuole formation. MBio, 7, 2016, e00297.
45. Madersbacher, H., van Ophoven, A., van Kerrebroeck, P.E.V.A., GAG layer replenishment therapy for chronic forms of cystitis with intravesical glycosaminoglycans–a review. Neurourol. Urodyn. 32 (2013), 9–18.
46. Maeda, N., Proteoglycans and neuronal migration in the cerebral cortex during development and disease. Front. Neurosci., 9, 2015, 98.
47. Magaldi, T.G., Buch, M.H.C., Murata, H., Erickson, K.D., Neu, U., Garcea, R.L., Peden, K., Stehle, T., DiMaio, D., Mutations in the GM1 binding site of simian virus 40 VP1 alter receptor usage and cell tropism. J. Virol. 86 (2012), 7028–7042.
48. Maginnis, M.S., Ströh, L.J., Gee, G.V., O'Hara, B.A., Derdowski, A., Stehle, T., Atwood, W.J., Progressive multifocal leukoencephalopathy-associated mutations in the JC polyomavirus capsid disrupt lactoseries tetrasaccharide c binding. MBio, 4, 2013, e00247-13.
49. Major, E.O., Amemiya, K., Tornatore, C.S., Houff, S.A., Berger, J.R., Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin. Microbiol. Rev. 5 (1992), 49–73.
50. Miodosky, M., Abdul-Hai, A., Tsirigotis, P., Or, R., Bitan, M., Resnick, I.B., Gesundheit, B., Zilberman, I., Ioffe, L., Leubovic, A., et al. Treatment of post-hematopoietic stem cell transplantation hemorrhagic cystitis with intravesicular sodium hyaluronate. Bone Marrow Transplant. 38 (2006), 507–511.
51. Neu, U., Woellner, K., Gauglitz, G., Stehle, T., Structural basis of GM1 ganglioside recognition by simian virus 40. Proc. Natl. Acad. Sci. USA 105 (2008), 5219–5224.
52. Neu, U., Maginnis, M.S., Palma, A.S., Ströh, L.J., Nelson, C.D.S., Feizi, T., Atwood, W.J., Stehle, T., Structure-function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif. Cell Host Microbe 8 (2010), 309–319.
53. Neu, U., Allen, S.-A., Blaum, B.S., Liu, Y., Frank, M., Palma, A.S., Ströh, L.J., Feizi, T., Peters, T., Atwood, W.J., Stehle, T., A structure-guided mutation in the major capsid protein retargets BK polyomavirus. PLoS Pathog., 9, 2013, e1003688.
54. O'Donnell, C.D., Vogel, L., Wright, A., Das, S.R., Wrammert, J., Li, G.M., McCausland, M., Zheng, N.Y., Yewdell, J.W., Ahmed, R., et al. Antibody pressure by a human monoclonal antibody targeting the 2009 pandemic H1N1 virus hemagglutinin drives the emergence of a virus with increased virulence in mice. MBio, 3, 2012, e00120-12.
55. Parsons, C.L., Mulholland, S.G., Successful therapy of interstitial cystitis with pentosanpolysulfate. J. Urol. 138 (1987), 513–516.
56. Pastrana, D.V., Tolstov, Y.L., Becker, J.C., Moore, P.S., Chang, Y., Buck, C.B., Quantitation of human seroresponsiveness to Merkel cell polyomavirus. PLoS Pathog., 5, 2009, e1000578.
57. Pastrana, D.V., Pumphrey, K.A., Cuburu, N., Schowalter, R.M., Buck, C.B., Characterization of monoclonal antibodies specific for the Merkel cell polyomavirus capsid. Virology 405 (2010), 20–25.
58. Pastrana, D.V., Ray, U., Magaldi, T.G., Schowalter, R.M., Çuburu, N., Buck, C.B., BK polyomavirus genotypes represent distinct serotypes with distinct entry tropism. J. Virol. 87 (2013), 10105–10113.
59. Ray, U., Cinque, P., Gerevini, S., Longo, V., Lazzarin, A., Schippling, S., Martin, R., Buck, C.B., Pastrana, D.V., JC polyomavirus mutants escape antibody-mediated neutralization. Sci. Transl. Med., 7, 2015, 306ra151.
60. Reid, C.E., Li, H., Sur, G., Carmillo, P., Bushnell, S., Tizard, R., McAuliffe, M., Tonkin, C., Simon, K., Goelz, S., et al. Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. J. Infect. Dis. 204 (2011), 237–244.
61. Reploeg, M.D., Storch, G.A., Clifford, D.B., Bk virus: a clinical review. Clin. Infect. Dis. 33 (2001), 191–202.
62. Rillahan, C.D., Antonopoulos, A., Lefort, C.T., Sonon, R., Azadi, P., Ley, K., Dell, A., Haslam, S.M., Paulson, J.C., Global metabolic inhibitors of sialyl- and fucosyltransferases remodel the glycome. Nat. Chem. Biol. 8 (2012), 661–668.
63. Schowalter, R.M., Pastrana, D.V., Buck, C.B., Glycosaminoglycans and sialylated glycans sequentially facilitate Merkel cell polyomavirus infectious entry. PLoS Pathog., 7, 2011, e1002161.
64. Shao, Y., Lu, G.L., Shen, Z.J., Comparison of intravesical hyaluronic acid instillation and hyperbaric oxygen in the treatment of radiation-induced hemorrhagic cystitis. BJU Int. 109 (2012), 691–694.
65. Steiner, I., Berger, J.R., Update on progressive multifocal leukoencephalopathy. Curr. Neurol. Neurosci. Rep. 12 (2012), 680–686.
66. Ströh, L.J., Stehle, T., Glycan engagement by viruses: receptor switches and specificity. Annu. Rev. Virol. 1 (2014), 285–306.
67. Ströh, L.J., Maginnis, M.S., Blaum, B.S., Nelson, C.D.S., Neu, U., Gee, G.V., O'Hara, B.A., Motamedi, N., DiMaio, D., Atwood, W.J., et al. Increased affinity of JC polyomavirus capsid for LSTc over other sialylated glycans is a major determinant of infectivity. J. Virol. 89 (2015), 6364–6375.
68. Sunyaev, S.R., Lugovskoy, A., Simon, K., Gorelik, L., Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML). PLoS Genet., 5, 2009, e1000368.
69. Tolstov, Y.L., Pastrana, D.V., Feng, H., Becker, J.C., Jenkins, F.J., Moschos, S., Chang, Y., Buck, C.B., Moore, P.S., Human Merkel cell polyomavirus infection II. MCV is a common human infection that can be detected by conformational capsid epitope immunoassays. Int. J. Cancer 125 (2009), 1250–1256.
70. Tsai, B., Gilbert, J.M., Stehle, T., Lencer, W., Benjamin, T.L., Rapoport, T.A., Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 22 (2003), 4346–4355.
71. Tur, C., Montalban, X., Natalizumab: risk stratification of individual patients with multiple sclerosis. CNS Drugs 28 (2014), 641–648.
72. Tutolo, M., Ammirati, E., Castagna, G., Klockaerts, K., Plancke, H., Ost, D., Van der Aa, F., De Ridder, D., A prospective randomized controlled multicentre trial comparing intravesical DMSO and chondroitin sulphate 2% for painful bladder syndrome/interstitial cystitis. Int. Braz. J. Urol. 43 (2017), 134–141.
73. Van Assche, G., Van Ranst, M., Sciot, R., Dubois, B., Vermeire, S., Noman, M., Verbeeck, J., Geboes, K., Robberecht, W., Rutgeerts, P., Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N. Engl. J. Med. 353 (2005), 362–368.
74. Van der Aa, F., Beckley, I., de Ridder, D., Polyomavirus BK–a potential new therapeutic target for painful bladder syndrome/interstitial cystitis?. Med. Hypotheses 83 (2014), 317–320.
75. Varki, A., Cummings, R.D., Aebi, M., Packer, N.H., Seeberger, P.H., Esko, J.D., Stanley, P., Hart, G., Darvill, A., Kinoshita, T., et al. Symbol nomenclature for graphical representations of glycans. Glycobiology 25 (2015), 1323–1324.
76. Varki, A., Cummings, R.D., Esko, J.D., Stanley, P., Hart, G., Aebi, M., Darvill, A., Kinoshita, T., Packer, N.H., Prestegard, J.J., et al. Essentials of Glycobiology. 2015, Cold Spring Harbor.
77. Winter, B.J., O'Connell, H.E., Bowden, S., Carey, M., Eisen, D.P., A case control study reveals that polyomaviruria is significantly associated with interstitial cystitis and vesical ulceration. PLoS ONE, 10, 2015, e0137310.
78. Yim, S.H., Sherin, J.E., Szuchet, S., Oligodendrocyte proteoglycans: modulation by cell-substratum adhesion. J. Neurosci. Res. 34 (1993), 401–413.