JC polyomavirus mutants escape antibody-mediated neutralization

Science Translational Medicine

Volumn 7, Issue 306, 2015, Pages

  Ray, Upasana ^a   Cinque, Paola ^b   Gerevini, Simonetta ^b   Longo, Valeria ^b   Lazzarin, Adriano ^b,c   Schippling, Sven ^d   Martin, Roland ^d   Buck, Christopher B ^a   Pastrana, Diana V ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

IMIQUIMOD; VIRUS LIKE PARTICLE VACCINE; VIRUS VACCINE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CASE REPORT; CONTROLLED STUDY; DRUG TOLERABILITY; FEMALE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNE EVASION; IMMUNIZATION; JC VIRUS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; SINGLE DRUG DOSE; VIRUS LIKE AGENT; VIRUS MUTANT; VIRUS NEUTRALIZATION; VIRUS STRAIN; WILD TYPE; GENETICS; IMMUNOLOGY; MUTATION; PATHOGENICITY; SERODIAGNOSIS;

HUMANS; IMMUNE EVASION; JC VIRUS; MUTATION; NEUTRALIZATION TESTS; VIRAL VACCINES;

EID: 84942543721     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aab1720     Document Type: Article

References (48)

1. P. Cinque, I. J. Koralnik, S. Gerevini, J. M. Miro, R. W. Price, Progressive multifocal leukoencephalopathy in HIV-1 infection. Lancet Infect. Dis. 9, 625-636 (2009).
2. H. H. Hirsch, P. Kardas, D. Kranz, C. Leboeuf, The human JC polyomavirus (JCPyV): Virological background and clinical implications. APMIS 121, 685-727 (2013).
3. M. D. Carrithers, Update on disease-modifying treatments for multiple sclerosis. Clin. Ther. 36, 1938-1945 (2014).
4. C. Bozic, S. Richman, T. Plavina, A. Natarajan, J. V. Scanlon, M. Subramanyam, A. Sandrock, G. Bloomgren, Anti-John Cunnigham virus antibody prevalence in multiple sclerosis patients: Baseline results of STRATIFY-1. Ann. Neurol. 70, 742-750 (2011).
5. P. Lee, T. Plavina, A. Castro, M. Berman, D. Jaiswal, S. Rivas, B. Schlain, M. Subramanyam, A second-generation ELISA (STRATIFY JCVTM DxSelectTM) for detection of JC virus antibodies in human serum and plasma to support progressive multifocal leukoencephalopathy risk stratification. J. Clin. Virol. 57, 141-146 (2013).
6. G. Bloomgren, S. Richman, C. Hotermans, M. Subramanyam, S. Goelz, A. Natarajan, S. Lee, T. Plavina, J. V. Scanlon, A. Sandrock, C. Bozic, Risk of natalizumab-associated progressive multifocal leukoencephalopathy. N. Engl. J. Med. 366, 1870-1880 (2012).
7. D. M. Keller, JCV test stratifies PML risk in antibody-positive MS; http://www.medscape. com/viewarticle/806294.
8. R. A. Diotti, N. Mancini, N. Clementi, G. Sautto, G. J. Moreno, E. Criscuolo, F. Cappelletti, P. Man, E. Forest, L. Remy, S. Giannecchini, M. Clementi, R. Burioni, 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, 94-103 (2014).
9. X. Dang, I. J. Koralnik, A granule cell neuron-associated JC virus variant has a unique deletion in the VP1 gene. J. Gen. Virol. 87, 2533-2537 (2006).
10. S. R. Sunyaev, A. Lugovskoy, K. Simon, L. Gorelik, Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML). PLOS Genet. 5, e1000368 (2009).
11. 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, 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, 103-114 (2011).
12. 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, J. P. Carulli, Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. J. Infect. Dis. 204, 237-244 (2011).
13. X. Dang, J. E. Vidal, A. C. Oliveira,D.M. Simpson, S. Morgello, J. H. Hecht, L. H. Ngo, I. J. Koralnik, JC virus granule cell neuronopathy is associated with VP1 C terminus mutants. J. Gen. Virol. 93, 175-183 (2012).
14. M. S. Maginnis, L. J. Ströh, G. V. Gee, B. A. O'Hara, A. Derdowski, T. Stehle, W. J. Atwood, Progressive multifocal leukoencephalopathy-associated mutations in the JC polyomavirus capsid disrupt lactoseries tetrasaccharide c binding. MBio 4, e00247-e13 (2013).
15. Y.Kondo, M. S.Windrem, L. Zou, D. Chandler-Militello, S. J. Schanz,R.M.Auvergne, S. J.Betstadt, A. R. Harrington, M. Johnson, A. Kazarov, L. Gorelik, S. A. Goldman, Human glial chimeric mice reveal astrocytic dependence of JC virus infection. J. Clin. Invest. 124, 5323-5336 (2014).
16. S. A. Haley, W. J. Atwood, An animal model for progressive multifocal leukoencephalopathy. J. Clin. Invest. 124, 5103-5106 (2014).
17. S. D. O'Hara, T. Stehle, R. Garcea, Glycan receptors of the Polyomaviridae: Structure, function, and pathogenesis. Curr. Opin. Virol. 7, 73-78 (2014).
18. T. J. Kemp, M. Safaeian, A. Hildesheim, Y. Pan, K. J. Penrose, C. Porras, J. T. Schiller, D. R. Lowy, R. Herrero, L. A. Pinto, Kinetic and HPV infection effects on cross-type neutralizing antibody and avidity responses induced by Cervarix. Vaccine 31, 165-170 (2012).
19. E. Draper, S. L. Bissett, R. Howell-Jones, P. Waight, K. Soldan, M. Jit, N. Andrews, E. Miller, S. Beddows, A randomized, observer-blinded immunogenicity trial of Cervarix and Gardasil human papillomavirus vaccines in 12-15 year old girls. PLOS One 8, e61825 (2013).
20. J. T. Schiller, D. R. Lowy, Raising expectations for subunit vaccine. J. Infect. Dis. 211, 1373-1375 (2015).
21. D. V. Pastrana, Y. L. Tolstov, J. C. Becker, P. S. Moore, Y. Chang, C. B. Buck, Quantitation of human seroresponsiveness to Merkel cell polyomavirus. PLOS Pathog. 5, e1000578 (2009).
22. G. Tibbling, H. Link, S. hman, Principles of albumin and IgG analyses in neurological disorders. I. Establishment of reference values. Scand. J. Clin. Lab. Invest. 37, 385-390 (1977).
23. C. Ahlgren, A. Odén, S. Haghighi, O. Andersen, T. Bergström, J. Lycke, The effect of live, attenuated measles vaccine and measles infection on measles antibody levels in serum and CSF of patients with multiple sclerosis or clinically isolated syndrome. J. Neuroimmunol. 235, 98-103 (2011).
24. Y. J. Yu, R. J. Watts, Developing therapeutic antibodies for neurodegenerative disease. Neurotherapeutics 10, 459-472 (2013).
25. L. Gorelik, A. Lugovskoy, Methods for the detection of JC polyoma virus. Patent WO/2010/090757 (2010).
26. M. Sospedra, S. Schippling, S. Yousef, I. Jelcic, S. Bofill-Mas, R. Planas, J.-P. Stellmann, V. Demina, P. Cinque, R. Garcea, T. Croughs, R. Girones, R. Martin, Treating progressive multifocal leukoencephalopathy with interleukin 7 and vaccination with JC virus capsid protein VP1. Clin. Infect. Dis. 59, 1588-1592 (2014).
27. K. B. Alstadhaug, T. Croughs, S. Henriksen, C. Leboeuf, I. Sereti, H. H. Hirsch, C. H. Rinaldo, Treatment of progressive multifocal leukoencephalopathy with interleukin 7. JAMA Neurol. 71, 1030-1035 (2014).
28. W. E. Purtha, T. F. Tedder, S. Johnson, D. Bhattacharya, M. S. Diamond, Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J. Exp. Med. 208, 2599-2606 (2011).
29. D. V. Pastrana, U. Ray, T. G. Magaldi, R. M. Schowalter, N. uburu, C. B. Buck, BK polyomavirus genotypes represent distinct serotypes with distinct entry tropism. J. Virol. 87, 10105-10113 (2013).
30. R. Fox, Advances in the management of PML: Focus on natalizumab. Cleve. Clin. J. Med. 78 (Suppl. 2), S33-S37 (2011).
31. Q. Zhao, S. Li, H. Yu, N. Xia, Y. Modis, Virus-like particle-based human vaccines: Quality assessment based on structural and functional properties. Trends Biotechnol. 31, 654-663 (2013).
32. A. R. Kreimer, M. E. Sherman, V. V. Sahasrabuddhe, M. Safaeian, The case for conducting a randomized clinical trial to assess the efficacy of a single dose of prophylactic HPV vaccines among adolescents. J. Natl. Cancer Inst. 107, dju436 (2015).
33. M. Kaufman, G. Pardo, H. Rossman, M. T. Sweetser, F. Forrestal, P. Duda, Natalizumab treatment shows no clinically meaningful effects on immunization responses in patients with relapsing-remitting multiple sclerosis. J. Neurol. Sci. 341, 22-27 (2014).
34. A. Patel, J. Patel, J. Ikwuagwu, A case of progressive multifocal leukoencephalopathy and idiopathic CD4+ lymphocytopenia. J. Antimicrob. Chemother. 65, 2697-2698 (2010).
35. C. B. Buck, D. V. Pastrana, D. R. Lowy, J. T. Schiller, Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78, 751-757 (2004).
36. D. V. Pastrana, D. C. Brennan, N. uburu, G. A. Storch, R. P. Viscidi, P. S. Randhawa, C. B. Buck, Neutralization serotyping of BK polyomavirus infection in kidney transplant recipients. PLOS Pathog. 8, e1002650 (2012).
37. A. V. Roschke, G. Tonon, K. S. Gehlhaus, N. McTyre, K. J. Bussey, S. Lababidi, D. A. Scudiero, J. N. Weinstein, I. R. Kirsch, Karyotypic complexity of the NCI-60 drug-screening panel. Cancer Res. 63, 8634-8647 (2003).
38. L. A. Garraway, H. R. Widlund, M. A. Rubin, G. Getz, A. J. Berger, S. Ramaswamy, R. Beroukhim, D. A.Milner, S. R. Granter, J. Du, C. Lee, S.N. Wagner, C. Li, T. R. Golub, D. L. Rimm, M. L.Meyerson, D. E. Fisher, W. R. Sellers, Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436, 117-122 (2005).
39. J. T. Rutka, J. R. Giblin, H. K. Hifdt, D. V. Dougherty, C. W. Bell, J. R. McCulloch, R. L. Davis, C. B. Wilson, M. L. Rosenblum, Establishment and characterization of a cell line from a human gliosarcoma. Cancer Res. 46, 5893-5902 (1986).
40. H. T. Agostini, A. Deckhut, D. V. Jobes, R. Girones, G. Schlunck, M. G. Prost, C. Frias, E. Pérez-Trallero, C. F. Ryschkewitsch, G. L. Stoner, Genotypes of JC virus in east, central and southwest Europe. J. Gen. Virol. 82, 1221-1331 (2001).
41. D. V. Pastrana, C. B. Buck, Y.-Y. S. Pang, C. D. Thompson, P. E. Castle, P. C. FitzGerald, S. Krger Kjaer, D. R. Lowy, J. T. Schiller, Reactivity of human sera in a sensitive, high-throughput pseudovirusbased papillomavirus neutralization assay for HPV16 and HPV18. Virology 321, 205-216 (2004).
42. R. M. Schowalter, W. C. Reinhold, C. B. Buck, Entry tropism of BK and Merkel cell polyomaviruses in cell culture. PLOS One 7, e42181 (2012).
43. G. Shaw, S. Morse, M. Ararat, F. L. Graham, Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 16, 869-871 (2002).
44. S. Henriksen, G. D. Tylden, A. Dumoulin, B. N. Sharma, H. H. Hirsch, C. H. Rinaldo, The human fetal glial cell line SVG p12 contains infectious BK polyomavirus. J. Virol. 88, 7556-7568 (2014).
45. H. C. Lehmann, W. Chen, R. Mi, S. Wang, Y. Liu, M. Rao, A. Höke, Human Schwann cells retain essential phenotype characteristics after immortalization. Stem Cells Dev. 21, 423-431 (2012).
46. J. L. Gross, D. L. Behrens, D. E. Mullins, P. L. Kornblith, D. L. Dexter, Plasminogen activator and inhibitor activity in human glioma cells and modulation by sodium butyrate. Cancer Res. 48, 291-296 (1988).
47. T. C. Pierson, M. D. Sánchez, B. A. Puffer, A. A. Ahmed, B. J. Geiss, L. E. Valentine, L. A. Altamura, M. S. Diamond, R. W. Doms, A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Virology 346, 53-65 (2006).
48. S. Bossolasco, G. Calori, F. Moretti, A. Boschini, D. Bertelli, M. Mena, S. Gerevini, A. Bestetti, R. Pedale, S. Sala, S. Sala, A. Lazzarin, P. Cinque, Prognostic significance of JC virus DNA levels in cerebrospinal fluid of patients with HIV-associated progressive multifocal leukoencephalopathy. Clin. Infect. Dis. 40, 738-744 (2005).