Mechanisms of immune escape in central nervous system infection with neurotropic JC virus variant

Annals of Neurology

Volumn 79, Issue 3, 2016, Pages 404-418

  Jelcic, Ivan ^a   Jelcic, Ilijas ^a   Kempf, Christian ^a   Largey, Fabienne ^a   Planas, Raquel ^a   Schippling, Sven ^a   Budka, Herbert ^b   Sospedra, Mireia ^a   Martin, Roland ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CORTICOSTEROID; NATALIZUMAB; PROTEIN VP1; VIRUS LARGE T ANTIGEN;

ADULT; AMNESIA; ARTICLE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM INFECTION; CEREBELLUM ATROPHY; CLINICAL ARTICLE; CORTICOSTEROID THERAPY; EXPANDED DISABILITY STATUS SCALE; FATIGUE; FEMALE; GENE MUTATION; HEMIPARESIS; HUMAN; HUMAN TISSUE; HYPESTHESIA; IMMUNE RESPONSE; JC VIRUS; LYMPHOCYTIC INFILTRATION; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; T LYMPHOCYTE SUBPOPULATION; VIRAL CLEARANCE; BRAIN; CASE REPORT; CLASSIFICATION; GENETICS; IMMUNE EVASION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNOLOGY; PHYSIOLOGY; VIROLOGY;

ADULT; BRAIN; FEMALE; HUMANS; IMMUNE EVASION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; JC VIRUS; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS;

EID: 84960384607     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24574     Document Type: Article

References (39)

1. Major EO,. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu Rev Med 2010; 61: 35-47.
2. Kleinschmidt-DeMasters BK, Tyler KL,. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N Engl J Med 2005; 353: 369-374.
3. Gheuens S, Wuthrich C, Koralnik IJ,. Progressive multifocal leukoencephalopathy: why gray and white matter. Annu Rev Pathol 2013; 8: 189-215.
4. Koralnik IJ, Wuthrich C, Dang X, et al., JC virus granule cell neuronopathy: a novel clinical syndrome distinct from progressive multifocal leukoencephalopathy. Ann Neurol 2005; 57: 576-580.
5. Du Pasquier RA, Corey S, Margolin DH, et al., Productive infection of cerebellar granule cell neurons by JC virus in an HIV + individual. Neurology 2003; 61: 775-782.
6. Dang X, Vidal JE, Oliveira AC, et al., JC virus granule cell neuronopathy is associated with VP1 C terminus mutants. J Gen Virol 2012; 93 (pt 1): 175-183.
7. Gorelik L, Reid C, Testa 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 2011; 204: 103-114.
8. Tan IL, McArthur JC, Clifford DB, et al., Immune reconstitution inflammatory syndrome in natalizumab-associated PML. Neurology 2011; 77: 1061-1067.
9. Dahlhaus S, Hoepner R, Chan A, et al., Disease course and outcome of 15 monocentrically treated natalizumab-associated progressive multifocal leukoencephalopathy patients. J Neurol Neurosurg Psychiatry 2013; 84: 1068-1074.
10. Ryschkewitsch CF, Jensen PN, Monaco MC, Major EO,. JC virus persistence following progressive multifocal leukoencephalopathy in multiple sclerosis patients treated with natalizumab. Ann Neurol 2010; 68: 384-391.
11. Jelcic I, Jelcic I, Faigle W, et al., Immunology of progressive multifocal leukoencephalopathy. J Neurovirol 2015; 21: 614-622.
12. Du Pasquier RA, Kuroda MJ, Zheng Y, et al., A prospective study demonstrates an association between JC virus-specific cytotoxic T lymphocytes and the early control of progressive multifocal leukoencephalopathy. Brain 2004; 127 (pt 9): 1970-1978.
13. Gheuens S, Bord E, Kesari S, et al., Role of CD4 + and CD8 + T-cell responses against JC virus in the outcome of patients with progressive multifocal leukoencephalopathy (PML) and PML with immune reconstitution inflammatory syndrome. J Virol 2011; 85: 7256-7263.
14. Wuthrich C, Kesari S, Kim WK, et al., Characterization of lymphocytic infiltrates in progressive multifocal leukoencephalopathy: co-localization of CD8(+) T cells with JCV-infected glial cells. J Neurovirol 2006; 12: 116-128.
15. Martin-Blondel G, Bauer J, Cuvinciuc V, et al., In situ evidence of JC virus control by CD8 + T cells in PML-IRIS during HIV infection. Neurology 2013; 81: 964-970.
16. Aly L, Yousef S, Schippling S, et al., Central role of JC virus-specific CD4 + lymphocytes in progressive multi-focal leucoencephalopathy-immune reconstitution inflammatory syndrome. Brain 2011; 134 (pt 9): 2687-2702.
17. Yousef S, Planas R, Chakroun K, et al., TCR bias and HLA cross-restriction are strategies of human brain-infiltrating JC virus-specific CD4 + T cells during viral infection. J Immunol 2012; 189: 3618-3630.
18. Zonios DI, Falloon J, Bennett JE, et al., Idiopathic CD4 + lymphocytopenia: natural history and prognostic factors. Blood 2008; 112: 287-294.
19. Gillespie SM, Chang Y, Lemp G, et al., Progressive multifocal leukoencephalopathy in persons infected with human immunodeficiency virus, San Francisco, 1981-1989. Ann Neurol 1991; 30: 597-604.
20. Jelcic I, Aly L, Binder TM, et al., T cell epitope mapping of JC polyoma virus-encoded proteome reveals reduced T cell responses in HLA-DRB1∗04:01 + donors. J Virol 2013; 87: 3393-3408.
21. Sundqvist E, Buck D, Warnke C, et al., JC polyomavirus infection is strongly controlled by human leucocyte antigen class II variants. PLoS Pathog 2014; 10: e1004084.
22. Schippling S, Kempf C, Buchele F, et al., JCV granule cell neuronopathy and GCN-IRIS under natalizumab treatment. Ann Neurol 2013; 74: 622-626.
23. Nakanishi A, Chapellier B, Maekawa N, et al., SV40 vectors carrying minimal sequence of viral origin with exchangeable capsids. Virology 2008; 379: 110-117.
24. Kitchen SG, LaForge S, Patel VP, et al., Activation of CD8 T cells induces expression of CD4, which functions as a chemotactic receptor. Blood 2002; 99: 207-212.
25. Zloza A, Schenkel JM, Tenorio AR, et al., Potent HIV-specific responses are enriched in a unique subset of CD8 + T cells that coexpresses CD4 on its surface. Blood 2009; 114: 3841-3853.
26. Kitchen SG, Whitmire JK, Jones NR, et al., The CD4 molecule on CD8 + T lymphocytes directly enhances the immune response to viral and cellular antigens. Proc Natl Acad Sci U S A 2005; 102: 3794-3799.
27. Nascimbeni M, Shin EC, Chiriboga L, et al., Peripheral CD4(+)CD8(+) T cells are differentiated effector memory cells with antiviral functions. Blood 2004; 104: 478-486.
28. Kitchen SG, Korin YD, Roth MD, et al., Costimulation of naive CD8(+) lymphocytes induces CD4 expression and allows human immunodeficiency virus type 1 infection. J Virol 1998; 72: 9054-9060.
29. Dang X, Koralnik IJ,. Gone over to the dark side: natalizumab-associated JC virus infection of neurons in cerebellar gray matter. Ann Neurol 2013; 74: 503-505.
30. Agnihotri SP, Dang X, Carter JL, et al., JCV GCN in a natalizumab-treated MS patient is associated with mutations of the VP1 capsid gene. Neurology 2014; 83: 727-732.
31. Metz I, Radue EW, Oterino A, et al., Pathology of immune reconstitution inflammatory syndrome in multiple sclerosis with natalizumab-associated progressive multifocal leukoencephalopathy. Acta Neuropathol 2012; 123: 235-245.
32. Dang L, Dang X, Koralnik IJ, Todd PK,. JC polyomavirus granule cell neuronopathy in a patient treated with rituximab. JAMA Neurol 2014; 71: 487-489.
33. Wuthrich C, Cheng YM, Joseph JT, et al., Frequent infection of cerebellar granule cell neurons by polyomavirus JC in progressive multifocal leukoencephalopathy. J Neuropathol Exp Neurol 2009; 68: 15-25.
34. Kurschner C, Yuzaki M,. Neuronal interleukin-16 (NIL-16): a dual function PDZ domain protein. J Neurosci 1999; 19: 7770-7780.
35. Liblau RS, Gonzalez-Dunia D, Wiendl H, Zipp F,. Neurons as targets for T cells in the nervous system. Trends Neurosci 2013; 36: 315-324.
36. Sloan-Lancaster J, Allen PM,. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu Rev Immunol 1996; 14: 1-27.
37. Walton S, Mandaric S, Oxenius A,. CD4 T cell responses in latent and chronic viral infections. Front Immunol 2013; 4: 105.
38. Sant AJ, McMichael A,. Revealing the role of CD4(+) T cells in viral immunity. J Exp Med 2012; 209: 1391-1395.
39. Jelcic I, Combaluzier B, Jelcic I, et al., Broadly neutralizing human monoclonal JC polyomavirus VP1-specific antibodies as candidate therapeutics for progressive multifocal leukoencephalopathy. Sci Transl Med 2015; 7: 306ra150.