Illuminating viral infections in the nervous system

Nature Reviews Immunology

Volumn 11, Issue 5, 2011, Pages 318-329

  McGavern, Dorian B ^a   Kang, Silvia S ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; CENTRAL NERVOUS SYSTEM INFECTION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE SYSTEM; IMMUNITY; IMMUNOSURVEILLANCE; MICROGLIA; NONHUMAN; PERIPHERAL NERVE; PERSISTENT INFECTION; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS; VASCULAR ENDOTHELIUM; VIRUS ENTRY; VIRUS INFECTION; VIRUS MENINGITIS;

ANIMALS; BLOOD-BRAIN BARRIER; BLOOD-NERVE BARRIER; CAPILLARY PERMEABILITY; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; ENDOTHELIUM, VASCULAR; HUMANS; PERIPHERAL NERVOUS SYSTEM; VIRUS INTERNALIZATION; VIRUS LATENCY; VIRUSES;

EID: 79955458125     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2971     Document Type: Review

References (120)

1. Ginhoux, F. et-al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845 (2010).
2. Nimmerjahn, A., Kirchhoff, F. & Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in-vivo. Science 308, 1314-1318 (2005). (Pubitemid 40746128)
3. Bulloch, K. et-al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J.-Compar. Neurol. 508, 687-710 (2008). (Pubitemid 351693557)
4. Chinnery, H.-R., Ruitenberg, M.-J. & McMenamin, P.-G. Novel characterization of monocyte-derived cell populations in the meninges and choroid plexus and their rates of replenishment in bone marrow chimeric mice. J.-Neuropathol. Exp. Neurol. 69, 896-909 (2010).
5. Tyler, K.-L. Emerging viral infections of the central nervous system: part 2. Arch. Neurol. 66, 1065-1074 (2009).
6. Tyler, K.-L. Emerging viral infections of the central nervous system: part 1. Arch. Neurol. 66, 939-948 (2009).
7. Bechmann, I., Galea, I. & Perry, V.-H. What is the blood-brain barrier (not)? Trends Immunol. 28, 5-11 (2007). (Pubitemid 46001619)
8. Kutcher, M.-E. & Herman, I.-M. The pericyte: cellular regulator of microvascular blood flow. Microvasc. Res. 77, 235-246 (2009).
9. Armulik, A. et-al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561 (2010).
10. Daneman, R., Zhou, L., Kebede, A.-A. & Barres, B.-A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468, 562-566 (2010).
11. Grossmann, R. et-al. Juxtavascular microglia migrate along brain microvessels following activation during early postnatal development. Glia 37, 229-240 (2002).
12. Hickey, W.-F. & Kimura, H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in-vivo. Science 239, 290-292 (1988). (Pubitemid 18061496)
13. Prodinger, C. et-al. CD11c-expressing cells reside in the juxtavascular parenchyma and extend processes into the glia limitans of the mouse nervous system. Acta Neuropathol. 121, 445-458 (2011).
14. Bartholomaus, I. et-al. Effector T-cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462, 94-98 (2009).
15. Mathiisen, T.-M., Lehre, K.-P., Danbolt, N.-C. & Ottersen, O.-P. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58, 1094-1103 (2010).
16. Chapagain, M.-L., Verma, S., Mercier, F., Yanagihara, R. & Nerurkar, V.-R. Polyomavirus JC infects human brain microvascular endothelial cells independent of serotonin receptor 2A. Virology 364, 55-63 (2007). (Pubitemid 46829276)
17. Coyne, C.-B., Kim, K.-S. & Bergelson, J.-M. Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. EMBO J. 26, 4016-4028 (2007).
18. Casiraghi, C., Dorovini-Zis, K. & Horwitz, M.-S. Epstein-Barr virus infection of human brain microvessel endothelial cells: a novel role in multiple sclerosis. J.-Neuroimmunol. 230, 173-177 (2010).
19. Gralinski, L.-E., Ashley, S.-L., Dixon, S.-D. & Spindler, K.-R. Mouse adenovirus type-1-induced breakdown of the blood-brain barrier. J.-Virol. 83, 9398-9410 (2009).
20. Afonso, P.-V. et-al. Alteration of blood-brain barrier integrity by retroviral infection. PLoS Pathog. 4, e1000205 (2008).
21. Verma, S., Kumar, M., Gurjav, U., Lum, S. & Nerurkar, V.-R. Reversal of West Nile virus-induced blood-brain barrier disruption and tight junction proteins degradation by matrix metalloproteinases inhibitor. Virology 397, 130-138 (2010).
22. Antar, A.-A. et-al. Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe 5, 59-71 (2009).
23. Alexaki, A. & Wigdahl, B. HIV-1 infection of bone marrow hematopoietic progenitor cells and their role in trafficking and viral dissemination. PLoS Pathog. 4, e1000215 (2008).
24. Clay, C.-C. et-al. Neuroinvasion of fluorescein-positive monocytes in acute simian immunodeficiency virus infection. J.-Virol. 81, 12040-12048 (2007).
25. Ancuta, P., Wang, J. & Gabuzda, D. CD16+ monocytes produce IL-6, CCL2, and matrix metalloproteinase-9 upon interaction with CX3CL1-expressing endothelial cells. J.-Leukoc. Biol. 80, 1156-1164 (2006). (Pubitemid 44646321)
26. Roberts, T.-K., Buckner, C.-M. & Berman, J.-W. Leukocyte transmigration across the blood-brain barrier: perspectives on neuroAIDS. Front. Biosci. 15, 478-536 (2010).
27. Monaco, M.-C., Atwood, W.-J., Gravell, M., Tornatore, C.-S. & Major, E.-O. JC virus infection of hematopoietic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: implications for viral latency. J.-Virol. 70, 7004-7012 (1996). (Pubitemid 26307415)
28. Chapagain, M.-L. & Nerurkar, V.-R. Human polyomavirus JC (JCV) infection of human B lymphocytes: a possible mechanism for JCV transmigration across the blood-brain barrier. J.-Infect. Dis. 202, 184-191 (2010).
29. Salinas, S., Schiavo, G. & Kremer, E.-J. A hitchhiker's guide to the nervous system: the complex journey of viruses and toxins. Nature Rev. Microbiol. 8, 645-655 (2010).
30. Diefenbach, R.-J., Miranda-Saksena, M., Douglas, M.-W. & Cunningham, A.-L. Transport and egress of herpes simplex virus in neurons. Rev. Med. Virol. 18, 35-51 (2008). (Pubitemid 351155901)
31. Mata, M., Zhang, M., Hu, X. & Fink, D.-J. HveC (nectin-1) is expressed at high levels in sensory neurons, but not in motor neurons, of the rat peripheral nervous system. J.-Neurovirol. 7, 476-480 (2001). (Pubitemid 33040436)
32. Curanovic, D. & Enquist, L. Directional transneuronal spread of α-herpesvirus infection. Future Virol. 4, 591-603 (2009).
33. Mori, I., Nishiyama, Y., Yokochi, T. & Kimura, Y. Olfactory transmission of neurotropic viruses. J.-Neurovirol. 11, 129-137 (2005). (Pubitemid 40852420)
34. Samuel, M.-A., Wang, H., Siddharthan, V., Morrey, J.-D. & Diamond, M.-S. Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc. Natl Acad. Sci. USA 104, 17140-17145 (2007). (Pubitemid 350210990)
35. Roussarie, J.-P., Ruffie, C., Edgar, J.-M., Griffiths, I. & Brahic, M. Axon myelin transfer of a non-enveloped virus. PLoS ONE 2, e1331 (2007).
36. Dietzschold, B., Li, J., Faber, M. & Schnell, M. Concepts in the pathogenesis of rabies. Future Virol. 3, 481-490 (2008).
37. Young, V.-A. & Rall, G.-F. Making it to the synapse: measles virus spread in and among neurons. Curr. Top. Microbiol. Immunol. 330, 3-30 (2009).
38. Bajramovic, J.-J. et-al. Borna disease virus glycoprotein is required for viral dissemination in neurons. J.-Virol. 77, 12222-12231 (2003).
39. de la Torre, J.-C. Bornavirus and the brain. J.-Infect. Dis. 186, S241-S247 (2002).
40. Hsieh, M.-J., White, P.-J. & Pouton, C.-W. Interaction of viruses with host cell molecular motors. Curr. Opin. Biotechnol. 21, 633-639 (2010).
41. Iannacone, M. et-al. Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 465, 1079-1083 (2010).
42. De Regge, N. et-al. α-herpesvirus glycoprotein D interaction with sensory neurons triggers formation of varicosities that serve as virus exit sites. J.-Cell Biol. 174, 267-275 (2006). (Pubitemid 44079861)
43. Knipe, D.-M. & Cliffe, A. Chromatin control of herpes simplex virus lytic and latent infection. Nature Rev. Microbiol. 6, 211-221 (2008). (Pubitemid 351256316)
44. Conrady, C.-D., Drevets, D.-A. & Carr, D.-J. Herpes simplex type-I (HSV-1) infection of the nervous system: is an immune response a good thing? J.-Neuroimmunol. 220, 1-9 (2010).
45. Perez de Diego, R. et-al. Human TRAF3 adaptor molecule deficiency leads to impaired Toll-like receptor-3 response and susceptibility to herpes simplex encephalitis. Immunity 33, 400-411 (2010).
46. Zhou, Y. et-al. Activation of Toll-like receptors inhibits herpes simplex virus-1 infection of human neuronal cells. J.-Neurosci. Res. 87, 2916-2925 (2009).
47. Samuel, C.-E. Antiviral actions of interferons. Clin. Microbiol. Rev. 14, 778-809 (2001).
48. De Regge, N., Van Opdenbosch, N., Nauwynck, H.-J., Efstathiou, S. & Favoreel, H.-W. Interferon alpha induces establishment of alphaherpesvirus latency in sensory neurons in-vitro. PLoS ONE 5, e13076 (2010).
49. Sobol, P.-T. & Mossman, K.-L. ICP0 prevents RNase-L- independent rRNA cleavage in herpes simplex virus type-1-infected cells. J.-Virol. 80, 218-225 (2006).
50. Harle, P., Sainz, B. Jr, Carr, D.-J. & Halford, W.-P. The immediate-early protein, ICP0, is essential for the resistance of herpes simplex virus to interferon-α/β. Virology 293, 295-304 (2002).
51. Khanna, K.-M., Lepisto, A.-J., Decman, V. & Hendricks, R.-L. Immune control of herpes simplex virus during latency. Curr. Opin. Immunol. 16, 463-469 (2004). (Pubitemid 38881674)
52. Simmons, A. & Tscharke, D.-C. Anti-CD8 impairs clearance of herpes simplex virus from the nervous system: implications for the fate of virally infected neurons. J.-Exp. Med. 175, 1337-1344 (1992).
53. Khanna, K.-M., Bonneau, R.-H., Kinchington, P.-R. & Hendricks, R.-L. Herpes simplex virus-specific memory CD8+ T-cells are selectively activated and retained in latently infected sensory ganglia. Immunity 18, 593-603 (2003).
54. Orr, M.-T., Mathis, M.-A., Lagunoff, M., Sacks, J.-A. & Wilson, C.-B. CD8 T-cell control of HSV reactivation from latency is abrogated by viral inhibition of MHC class I. Cell Host Microbe 2, 172-180 (2007). (Pubitemid 47355202)
55. Sheridan, B.-S., Cherpes, T.-L., Urban, J., Kalinski, P. & Hendricks, R.-L. Reevaluating the CD8 T-cell response to herpes simplex virus type-1: involvement of CD8 T-cells reactive to subdominant epitopes. J.-Virol. 83, 2237-2245 (2009).
56. Wakim, L.-M., Gebhardt, T., Heath, W.-R. & Carbone, F.-R. Cutting edge: local recall responses by memory T-cells newly recruited to peripheral nonlymphoid tissues. J.-Immunol. 181, 5837-5841 (2008).
57. Gebhardt, T. et-al. Memory T-cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nature Immunol. 10, 524-530 (2009).
58. Theil, D. et-al. Latent herpesvirus infection in human trigeminal ganglia causes chronic immune response. Am. J.-Pathol. 163, 2179-2184 (2003). (Pubitemid 37466462)
59. Hufner, K. et-al. Latency of α-herpes viruses is accompanied by a chronic inflammation in human trigeminal ganglia but not in dorsal root ganglia. J.-Neuropathol. Exp. Neurol. 65, 1022-1030 (2006). (Pubitemid 44521803)
60. Verjans, G.-M. et-al. Selective retention of herpes simplex virus-specific T-cells in latently infected human trigeminal ganglia. Proc. Natl Acad. Sci. USA 104, 3496-3501 (2007).
61. Liu, T., Khanna, K.-M., Chen, X., Fink, D.-J. & Hendricks, R.-L. CD8+ T-cells can block herpes simplex virus type-1 (HSV-1) reactivation from latency in sensory neurons. J.-Exp. Med. 191, 1459-1466 (2000). (Pubitemid 30257343)
62. Decman, V., Freeman, M.-L., Kinchington, P.-R. & Hendricks, R.-L. Immune control of HSV-1 latency. Viral Immunol. 18, 466-473 (2005).
63. Frank, G.-M. et-al. Early CD4+ T-cell help prevents partial CD8+ T-cell exhaustion and promotes maintenance of herpes simplex virus 1 latency. J.-Immunol. 184, 277-286 (2010).
64. Wakim, L.-M., Waithman, J., van Rooijen, N., Heath, W.-R. & Carbone, F.-R. Dendritic cell-induced memory T-cell activation in nonlymphoid tissues. Science 319, 198-202 (2008).
65. Divito, S., Cherpes, T.-L. & Hendricks, R.-L. A triple entente: virus, neurons, and CD8+ T-cells maintain HSV-1 latency. Immunol. Res. 36, 119-126 (2006). (Pubitemid 46398586)
66. Derfuss, T. et-al. Presence of HSV-1 immediate early genes and clonally expanded T-cells with a memory effector phenotype in human trigeminal ganglia. Brain Pathol. 17, 389-398 (2007). (Pubitemid 47537596)
67. Mandal, M., Bandyopadhyay, D., Goepfert, T.-M. & Kumar, R. Interferon-induces expression of cyclin-dependent kinase-inhibitors p21WAF1 and p27Kip1 that prevent activation of cyclin-dependent kinase by CDK-activating kinase (CAK). Oncogene 16, 217-225 (1998). (Pubitemid 28045108)
68. Liu, T., Khanna, K.-M., Carriere, B.-N. & Hendricks, R.-L. Gamma interferon can prevent herpes simplex virus type-1 reactivation from latency in sensory neurons. J.-Virol. 75, 11178-11184 (2001). (Pubitemid 33031584)
69. Knickelbein, J.-E. et-al. Noncytotoxic lytic granule-mediated CD8+ T-cell inhibition of HSV-1 reactivation from neuronal latency. Science 322, 268-271 (2008).
70. Jiang, X. et-al. The herpes simplex virus type-1 latency-associated transcript can protect neuron-derived C1300 and Neuro2A cells from granzyme B-induced apoptosis and CD8 T-cell killing. J.-Virol. 85, 2325-2332 (2011).
71. Alexaki, A., Liu, Y. & Wigdahl, B. Cellular reservoirs of HIV-1 and their role in viral persistence. Curr. HIV Res. 6, 388-400 (2008).
72. Yadav, A. & Collman, R.-G. CNS inflammation and macrophage/microglial biology associated with HIV-1 infection. J.-Neuroimmune Pharmacol. 4, 430-447 (2009).
73. Brenchley, J.-M. et-al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nature Med. 12, 1365-1371 (2006).
74. Witwer, K.-W. et-al. Coordinated regulation of SIV replication and immune responses in the CNS. PLoS ONE 4, e8129 (2009).
75. Barber, S.-A. et-al. Mechanism for the establishment of transcriptional HIV latency in the brain in a simian immunodeficiency virus-macaque model. J.-Infect. Dis. 193, 963-970 (2006).
76. Barber, S.-A., Herbst, D.-S., Bullock, B.-T., Gama, L. & Clements, J.-E. Innate immune responses and control of acute simian immunodeficiency virus replication in the central nervous system. J.-Neurovirol. 10 (Suppl. 1), 15-20 (2004). (Pubitemid 38325088)
77. Ravimohan, S., Gama, L., Barber, S.-A. & Clements, J.-E. Regulation of SIVmac239 basal long terminal repeat activity and viral replication in macrophages: functional roles of two CCAAT/enhancer-binding protein β sites in activation and interferon β-mediated suppression. J.-Biol. Chem. 285, 2258-2273 (2010).
78. Witwer, K.-W., Sisk, J.-M., Gama, L. & Clements, J.-E. MicroRNA regulation of IFN-β protein expression: rapid and sensitive modulation of the innate immune response. J.-Immunol. 184, 2369-2376 (2010).
79. Akhtar, L.-N. et-al. Suppressor of cytokine signaling 3 inhibits antiviral IFN-β signaling to enhance HIV-1 replication in macrophages. J.-Immunol. 185, 2393-2404 (2010).
80. Mankowski, J.-L., Clements, J.-E. & Zink, M.-C. Searching for clues: tracking the pathogenesis of human immunodeficiency virus central nervous system disease by use of an accelerated, consistent simian immunodeficiency virus macaque model. J.-Infect. Dis. 186, S199-S208 (2002).
81. Schmitz, J.-E. et-al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283, 857-860 (1999).
82. Jin, X. et-al. Dramatic rise in plasma viremia after CD8+ T-cell depletion in simian immunodeficiency virus-infected macaques. J.-Exp. Med. 189, 991-998 (1999). (Pubitemid 29149355)
83. Fox, H.-S. Virus-host interaction in the simian immunodeficiency virus-infected brain. J.-Neurovirol. 14, 286-291 (2008).
84. Kim, W.-K. et-al. Identification of T lymphocytes in simian immunodeficiency virus encephalitis: distribution of CD8+ T-cells in association with central nervous system vessels and virus. J.-Neurovirol. 10, 315-325 (2004). (Pubitemid 39429942)
85. Roberts, E.-S. et-al. Host response and dysfunction in the CNS during chronic simian immunodeficiency virus infection. J.-Neurosci. 26, 4577-4585 (2006).
86. Sadagopal, S. et-al. Enhancement of human immunodeficiency virus (HIV)-specific CD8+ T-cells in cerebrospinal fluid compared to those in blood among antiretroviral therapy-naive HIV-positive subjects. J.-Virol. 82, 10418-10428 (2008). (Pubitemid 352691154)
87. McCrossan, M. et-al. An immune control model for viral replication in the CNS during presymptomatic HIV infection. Brain 129, 503-516 (2006). (Pubitemid 43164372)
88. Cosenza, M.-A., Zhao, M.-L., Si, Q. & Lee, S.-C. Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol. 12, 442-455 (2002). (Pubitemid 35154931)
89. Denk, W., Strickler, J.-H. & Webb, W.-W. Two-photon laser scanning fluorescence microscopy. Science 248, 73-76 (1990).
90. Germain, R.-N., Miller, M.-J., Dustin, M.-L. & Nussenzweig, M.-C. Dynamic imaging of the immune system: progress, pitfalls and promise. Nature Rev. Immunol. 6, 497-507 (2006).
91. Zinselmeyer, B.-H. et-al. Chapter 16. Two-photon microscopy and multidimensional analysis of cell dynamics. Methods Enzymol. 461, 349-378 (2009).
92. Kang, S.-S. & McGavern, D.-B. Inflammation on the mind: visualizing immunity in the central nervous system. Curr. Top. Microbiol. Immunol. 334, 227-263 (2009).
93. Yang, G., Pan, F., Parkhurst, C.-N., Grutzendler, J. & Gan, W.-B. Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nature Protoc. 5, 201-208 (2010).
94. Xu, H.-T., Pan, F., Yang, G. & Gan, W.-B. Choice of cranial window type for in-vivo imaging affects dendritic spine turnover in the cortex. Nature Neurosci. 10, 549-551 (2007). (Pubitemid 46652440)
95. Mainen, Z.-F. et-al. Two-photon imaging in living brain slices. Methods 18, 231-239 (1999).
96. Wilson, E.-H. et-al. Behavior of parasite-specific effector CD8+ T-cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 30, 300-311 (2009).
97. Schaeffer, M. et-al. Dynamic imaging of T-cell-parasite interactions in the brains of mice chronically infected with Toxoplasma gondii. J.-Immunol. 182, 6379-6393 (2009).
98. Bajenoff, M. et-al. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25, 989-1001 (2006). (Pubitemid 44914055)
99. Brockhaus, J., Moller, T. & Kettenmann, H. Phagocytozing ameboid microglial cells studied in a mouse corpus callosum slice preparation. Glia 16, 81-90 (1996). (Pubitemid 26350514)
100. Davalos, D. et-al. ATP mediates rapid microglial response to local brain injury in-vivo. Nature Neurosci. 8, 752-758 (2005). (Pubitemid 43085841)
101. Haynes, S.-E. et-al. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nature Neurosci. 9, 1512-1519 (2006).
102. Kim, J.-V. & Dustin, M.-L. Innate response to focal necrotic injury inside the blood-brain barrier. J.-Immunol. 177, 5269-5277 (2006).
103. Vilela, M.-C. et-al. Traffic of leukocytes in the central nervous system is associated with chemokine up-regulation in a severe model of herpes simplex encephalitis: an intravital microscopy study. Neurosci. Lett. 445, 18-22 (2008).
104. Kim, J.-V., Kang, S.-S., Dustin, M.-L. & McGavern, D.-B. Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 457, 191-195 (2009).
105. Kang, S.-S. & McGavern, D.-B. Lymphocytic choriomeningitis infection of the central nervous system. Front. Biosci. 13, 4529-4543 (2008).
106. McGavern, D.-B., Christen, U. & Oldstone, M.-B. Molecular anatomy of antigen-specific CD8+ T-cell engagement and synapse formation in-vivo. Nature Immunol. 3, 918-925 (2002). (Pubitemid 35154004)
107. Fung-Leung, W.-P., Kundig, T.-M., Zinkernagel, R.-M. & Mak, T.-W. Immune response against lymphocytic choriomeningitis virus infection in mice without CD8 expression. J.-Exp. Med. 174, 1425-1429 (1991).
108. Kang, S.-S. & McGavern, D.-B. Microbial induction of vascular pathology in the CNS. J.-Neuroimmune Pharmacol. 5, 370-386 (2010).
109. Major, E.-O. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu. Rev. Med. 61, 35-47 (2010).
110. 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, 375-381 (2005). (Pubitemid 41132342)
111. Carrat, F. & Flahault, A. Influenza vaccine: the challenge of antigenic drift. Vaccine 25, 6852-6862 (2007). (Pubitemid 47398929)
112. Wong, K.-T. Emerging epidemic viral encephalitides with a special focus on henipaviruses. Acta Neuropathol. 120, 317-325 (2010).
113. Astrom, K.-E., Mancall, E.-L. & Richardson, E.-P. Jr. Progressive multifocal leuko-encephalopathy: a hitherto unrecognized complication of chronic lymphatic leukaemia and Hodgkin's disease. Brain 81, 93-111 (1958).
114. Cinque, P., Koralnik, I.-J., Gerevini, S., Miro, J.-M. & Price, R.-W. Progressive multifocal leukoencephalopathy in HIV-1 infection. Lancet Infect. Dis. 9, 625-636 (2009).
115. Focosi, D. et-al. Progressive multifocal leukoencephalopathy: what's new? Neuroscientist 16, 308-323 (2010).
116. 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, e1000368 (2009).
117. Tan, C.-S. et-al. JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J.-Virol. 84, 9200-9209 (2010).
118. Tan, C.-S. & Koralnik, I.-J. Progressive multifocal leukoencephalopathy and other disorders caused by JC virus: clinical features and pathogenesis. Lancet Neurol. 9, 425-437 (2010).
119. Aksamit, A.-J., Mourrain, P., Sever, J.-L. & Major, E.-O. Progressive multifocal leukoencephalopathy: investigation of three cases using in-situ hybridization with JC virus biotinylated DNA probe. Ann. Neurol. 18, 490-496 (1985). (Pubitemid 16138022)
120. Pho, M.-T., Ashok, A. & Atwood, W.-J. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J.-Virol. 74, 2288-2292 (2000). (Pubitemid 30091483)