Microbes' roadmap to neurons

Nature Reviews Neuroscience

Volumn 12, Issue 6, 2011, Pages 345-357

  Kristensson, Krister ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD BRAIN BARRIER; BRAIN MAPPING; CHIKUNGUNYA ALPHAVIRUS; HERPES SIMPLEX VIRUS; HOST; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN T CELL LEUKEMIA VIRUS 1; IMMUNE RESPONSE; INFECTION; JAPANESE ENCEPHALITIS VIRUS; LISTERIA MONOCYTOGENES; MICROORGANISM; NAEGLERIA FOWLERI; NEISSERIA MENINGITIDIS; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; RABIES VIRUS; REVIEW; TAENIA SOLIUM; TICK BORNE ENCEPHALITIS FLAVIVIRUS; TOXOPLASMA GONDII; TRYPANOSOMA BRUCEI; TRYPANOSOMA GAMBIENSE; TRYPANOSOMA RHODESIENSE; WEST NILE FLAVIVIRUS;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; NEURONS;

EID: 79957526749     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3029     Document Type: Review

References (104)

1. Griffin, D. E. Emergence and re-emergence of viral diseases of the nervous system. Prog. Neurobiol. 91, 95-101 (2010).
2. Niederkorn, J. Y. See no evil, hear no evil, do no evil: The lessons of immune privilege. Nature Immunol. 7, 354-359 (2006).
3. Charles, P. C., Guida, J. D., Brosnan, C. F. & Horwitz, M. S. Mouse adenovirus type-1 replication is restricted to vascular endothelum in the CNS of susceptible strains of mice. Virology 245, 216-228 (1998). (Pubitemid 28394184)
4. Maisner, A. Neufeld, J. & Weingart, H. Organ-and endotheliotropism of Nipah virus infections in vivo and in vitro. Thromb. Haemost. 102, 1014-1023 (2009).
5. Ebrahimi, C. M. et al. Penetration of the blood-brain barrier by Bacillus anthracis requires the pXO1-encoded BslA protein. J. Bacteriol. 191, 7165-7173 (2009).
6. Warfel, J. M. & D'Agnillo, F. Anthrax lethal toxin enhances I?B kinase activation and differentially regulates pro-inflammatory genes in human endothelium. J. Biol. Chem. 284, 2571-2577 (2009).
7. Mankowski, J. L. et al. Neurovirulent simian immunodeficiency virus replicates productively in endothelial cells of the central nervous system in vivo and in vitro. J. Virol. 68, 8202-8208 (1994). (Pubitemid 24362711)
8. Bobardt, M. D. et al. Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J. Virol. 78, 6567-6584 (2004). (Pubitemid 38715954)
9. Alfonso, P. V. et al. Alteration of blood-brain barrier integrity by retroviral infection. PLoS Pathog. 4, e1000205 (2008).
10. Liou, M. L. & Hsu, C. Y. Japanese encephalitis virus is transported across the cerebral blood vessels by endocytosis in mouse brain. Cell Tissue Res. 293, 389-394 (1998).
11. Armulik, A. et al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561 (2010).
12. Ludlow, M., Allen, I. & Schneider-Schaulis, J. Systemic spread of measles virus: Overcoming the eipthelial and endothelial barriers. Thromb. Haemost. 102, 1050-1056 (2009).
13. Owens, T., Bechmann, I. & Engelhardt, B. Perivascular spaces and the two steps to neuroinflammation. J. Neuropathol. Exp. Neurol. 67, 1113-1121 (2008).
14. Sorokin, L. The impact of the extracellular matrix on inflammation. Nature Rev. Immunol. 10, 712-723 (2010). This study provides a detailed biochemical explanation of how various laminins in basement membranes can form networks with differences in resistance to cell penetration. It includes extensive references to the nervous system.
15. Gonzalez-Scarano, F. & Martin-Garcia, J. The neuropathogenesis of AIDS. Nature Rev. Immunol. 5, 69-81 (2005). (Pubitemid 40070332)
16. Muratori, C., Mangino, G., Affabris, E. & Federico, M. Astrocytes contacting HIV-1-infected macrophages increase the release of CCL2 in response to the HIV-1-dependent enhancement of membrane-associated TNFa in macrophages. Glia 58, 1893-1904 (2010).
17. Clay, C. C. et al. Neuroinvasion of fluorescein-positive monocytes in acute simian immunodeficiency virus infection. J. Virol. 81, 12040-12048 (2007). (Pubitemid 47623834)
18. Drevets, D. A. & Bronze, M. S. Listeria monocytogenes: Epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol. Med. Microbiol. 53, 151-165 (2008). This paper provides a good overview of mechanisms through which L. monocytogenes can spread to the nervous system of an infected individual. (Pubitemid 351832182)
19. Huang, S. H. & Jong, A. Y. Cellular mechanisms of microbial proteins contributing to invasion of the blood-brain barrier. Cell. Microbiol. 3, 277-287 (2001). (Pubitemid 32377565)
20. Lambert, H. & Barragan, A. Modelling parasite dissemination: Host cell subversion and immune evasion by Toxoplasma gondii. Cell. Microbiol. 12, 292-300 (2010).
21. Kristensson, K., Nygerd, M., Bertini, G. & Bentivoglio, M. African trypanosome infections of the nervous system: Parasite entry and effects on neuronal functions. Prog. Neurobiol. 91, 152-171 (2010).
22. Amin, D. N. et al. Expression and role of CXCL10 during the encephalitic stage of experimental and clinical African trypanosomiasis. J. Infect. Dis. 200, 1556-1565 (2009).
23. Wang, T. et al. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nature Med. 10, 1366-1373 (2004). (Pubitemid 40022719)
24. Wang, P. et al. Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J. Virol. 82, 8978-8985 (2008).
25. Davis, L. E. et al. West Nile virus neuroinvasive disease. Ann. Neurol. 60, 286-300 (2006). (Pubitemid 44520233)
26. Combes, V., El-Assaad, F., Faille, D., Jambou, R., Hunt, N. H. & Grau, G. E. R. Microvesiculation and cell interactions at the brain-endothelial interface in cerebral malaria pathogenesis. Prog. Neurobiol. 91, 140-151 (2010). The original report of the release of microparticles in cerebral malaria; microparticles could potentially provide a new target for adjunctive therapy.
27. Vogt, A. M. et al. Release of sequestered malaria parasites upon injection of a glycosaminoglycan. PLoS Pathog. 2, 853-863 (2006).
28. Luuginbühl, A., Nikolic, M., Beck, H. P., Wahlgren, M. & Lutz, H. U. Complement factor D, albumin, and immunoglobulin G anti-band 3 protein antibodies mimic serum in promoting resetting of malaria-infected red blood cells. Infect. Immun. 75, 1771-1777 (2007). (Pubitemid 46559444)
29. Couper, K. N. et al. Parasite-derived plasma microparticles contribute significantly to malaria infection-induced inflammation through potent macrophage stimulation. PloS Pathog. 6, e1000744 (2010).
30. Mahnty, S. & Garcia, H. H. Cysticercosis and neurocysticercosis as pathogens affecting the nervous system. Prog. Neurobiol. 91, 172-184 (2010).
31. Wang, I.-C., Fan, P.-C., Lu, S.-C, Fan, C. K. & Su, K.-E. Suppresion of host Th1-type granulomatous inflammation by Taenia solium metacestodes is related to down-regulation of osteopontin gene expression. Int. J. Parasitol. 38, 239-248 (2008). (Pubitemid 350266648)
32. Alvarez, J. I. & Teale, J. M. Multiple expression of matrix metalloproteinases in murine neurocysticercosis: Implications for leukocyte migration through multiple central nervous system barriers. Brain Res. 1214, 145-158 (2008).
33. Broadwell, R. D. & Sofroniew, M. V. Serum proteins bypass the blood-brain fluid barriers for extracellular entry to the central nervous system. Exp. Neurol. 120, 245-263 (1993). (Pubitemid 23165019)
34. Vu, K., Weksler, B., Romero, I., Couraud, P.-O. & Gelli. A. Immortalized human brain endothelial cell line HCMEC/D3 as a model of the blood-brain barrier facilitates in vitro studies of central nervous system infection by Cryptococcus neoformans. Eukaryotic Cell 8, 1803-1807 (2009).
35. Ring, A., Weiser, J. N. & Tuomanen, E. I. Pneumococcal trafficking across the blood-brain barrier molecular analysis of a novel bidirectional pathway. J. Clin. Invest. 102, 347-360 (1998). (Pubitemid 28335194)
36. Thornton, J. A., Durick-Eder, K. & Tuomanen, E. I. Pneumococcal pathogenesis: "innate invasion" yet organ-specific damage. J. Mol. Med. 88, 103-107 (2010).
37. Coureuil, M. et al. Meningococcus hijacks a β2-adrenoceptor/β- arrestin pathway to cross brain microvasculature endothelium. Cell 143, 1149-1160 (2010). A recent paper on the mechanisms used by meningococcus bacteria to cross the BBB.
38. van Ginkel, F. W. et al. Pneumococcal carriage results in ganglioside-mediated olfactory tissue infection. Proc. Natl Acad. Sci. USA 100, 14363-14367 (2003). (Pubitemid 37499242)
39. Tenenbaum, T. et al. Polar bacterial invasion and translocation of Streptococcus suis across the blood-cerebrospinal fluid barrier in vitro. Cell. Microbiol. 11, 323-336 (2009).
40. Domínguez-Punaro, M. C. et al. Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J. Immunol. 179, 1842-1854 (2007).
41. Rudd, P. A., Cattaneo, R. & von Messling, V. Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J. Virol. 80, 9361-9370 (2006). (Pubitemid 44435615)
42. Christensen, J. E., de Lemos, C., Moos, T., Christensen, J. P. & Thomsen, A. R. CXCL10 is the key ligand for CXCR3 on CD8+ effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J. Immunol. 176, 4235-4243 (2006). (Pubitemid 44264402)
43. Thomsen, A. R. Lymphocytic choriomeningitis virus-induced central nervous system disease: A model for studying the role of chemokines in regulating the acute antiviral CD8+ T-cell response in an immune-privileged organ. J. Virol. 83, 20-28 (2009). A detailed review of the role of chemokines for the attraction or retention of T cells in the brain during a viral infection.
44. Kappes, D. J. et al. Protection of CD3 d knockout mice from lymphocytic choriomeningitis virus-induced immunopathology: Implications for viral neuroinvasion. Virology 269, 248-256 (2000). (Pubitemid 30210897)
45. Chen, H., Wood, C. & Petito, C. K. Comparisons of HIV-1 viral sequences in brain, choroid plexus and spleen: Potential role of choroid plexus in the pathogenesis of HIV encephalitis. J. Neurovirol. 6, 498-506 (2000). (Pubitemid 32098064)
46. Kristensson, K. & Olsson, Y. Diffusion pathways and retrograde axonal transport of protein tracers in peripheral nerves. Prog. Neurobiol. 1, 87-109 (1973).
47. Mercer, J., Schelhaas, M. & Helenius, A. Virus entry by endocytosis. Annu. Rev. Biochem. 79, 803-820 (2011).
48. Radtke, K., Döhner, K. & Sodeik, B. Viral interactions with the cytoskeleton: A hitchhiker's guide to the cell. Cell. Microbiol. 8, 367-400 (2006).
49. Dollery, S. J., Delboy, M. G. & Nicola, A. V. Low pH-induced conformational change in herpes simplex virus glycoprotein B. J. Virol. 84, 3759-3766 (2010).
50. Salinas, S., Schiavo, G. & Kremer, E. J. A hitchhikers's guide to the nervous system: The complex journey of viruses and toxins. Nature Rev. Microbiol. 8, 645-655 (2010).
51. Lakadamyali, M., Rust, M. J. & Zhuang, X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124, 997-1009 (2006). (Pubitemid 43344239)
52. Klingen, Y., Conzelmann, K.-K. & Finke, S. Double-labeled rabies virus: Live tracking of enveloped virus transport. J. Virol. 82, 237-245 (2008). (Pubitemid 350309140)
53. Lafon, M. Subversive neuroinvasive strategy of rabies virus. Arch. Virol. Suppl. 18, 149-159 (2004).
54. Salinas, S. et al. CAR-associated vesicular transport of an adenovirus in motor neuron axons. PloS Pathog. 5, e1000442 (2009).
55. Ohka, S. et al. Receptor-dependent and-independent axonal retrograde transport of poliovirus in motor neurons. J. Virol. 83, 4995-5004 (2009).
56. McGraw, H. M. & Friedman, H. M. Herpes simplex virus type 1 glycoprotein E mediates retrograde spread from epithelial cells to neurites. J. Virol. 83, 4791-4799 (2009).
57. Lee, J. I. et al. A herpesvirus encoded deubiquitinase is a novel neuroinvasive determinant. PloS Pathog. 5, e1000387 (2009).
58. Desai, P., DeLuca, N. A. & Person, S. Herpes simplex virus type 1 VP26 is not essential for replication in cell culture but influences production of infectious virus in the nervous system of infected mice. Virology 247, 115-124 (1998). (Pubitemid 28384031)
59. LaVail, J. H., Tauscher, A. N., Sucher, A., Harrabi, O. & Brandimarti, R. Viral regulation of the long distance axonal transport of herpes simplex virus nucleocapsid. Neuroscience 146, 974-985 (2007). (Pubitemid 46694131)
60. Miranda-Saksena, M. et al. Herpes simplex virus utilizes the large secretory vesicle pathway for anterograde transport of tegument and envelope proteins and for viral exocytosis from growth cones and human fetal axons. J. Virol. 83, 3187-3199 (2009).
61. Coller, K. E. & Smith G. A. Two viral kinases are required for sustained long distance axon transport of a neuroinvasive herpesvirus. Traffic 9, 1458-1470 (2008).
62. Curanovicí, D. & Enquist L. W. Directional transneuronal spread of a-herpesvirus infection. Future Virol. 4, 591-610 (2009). A comprehensive article on molecular mechanisms for the spread of various strains of herpesviruses in retrograde and anterograde directions in axons.
63. Dons, L., Jin, Y., Kristensson, K. & Rottenberg, M. Axonal transport of Listeria monocytogenes and nerve-cell-induced bacterial killing. J. Neurosci. Rev. 85, 2529-2537 (2007). (Pubitemid 47344555)
64. Mohammed, A., Norrby, E. & Kristensson, K. Viruses and behavioural changes: A review of clinical and experimental findings. Rev. Neurosci. 4, 267-286 (1993). (Pubitemid 23331465)
65. 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)
66. Morrey, J. D. et al. Increased blood brain barrier permeability is not a primary determinant for lethality of West Nile virus infection in rodents. J. Gen. Virol. 89, 467-473 (2008). (Pubitemid 351622443)
67. Yamada, M., Nakamura, K., Yoshii, M., Kaku, Y. & Narita, M. Brain lesions induced by experimental intranasal infection of Japanese encephalitis virus in piglets. J. Comp. Path. 141, 156-162 (2009).
68. Das, T. et al. Chikungunya fever: CNS infection and pathologies of a re-emerging arbovirus. Prog. Neurobiol. 91, 121-129 (2009).
69. Kiderlen, A. F. & Laube, U. Balamuthia mandrillaris, an opportunistic agent of granulomatous amebic encephalitis, infects the brain via the olfactory nerve pathway. Parasitol. Res. 94, 49-52 (2004). (Pubitemid 39243636)
70. Jung, S. Y. et al. Gene silencing of nfa1 affects the in vitro cytotoxicity of Naegleria fowleri in murine macrophages. Mol. Biochem. Parasitol. 165, 87-93 (2009).
71. Serrano-Luna, J., Cervantes-Sandoval, I., Tsutsumi, V. & Shibayama, M. A biochemical comparison of proteases from pathogenic Naegleria fowleri and non-pathogenic Naegleria gruberi. J. Eukaryot. Microbiol. 54, 411-417 (2007). (Pubitemid 47512288)
72. Backstrfm, E., Ljunggren, H.-G. & Kristensson K. NK cell-mediated destruction of influenza A virus-infected peripheral but not central neurones. Scand. J. Immunol. 65, 353-361 (2007). (Pubitemid 46481105)
73. Decman, V., Kinchington, P. R., Harvey, S. A. K. & Hendricks, R. L. Gamma interferon can block herpes simplex virus type 1 reactivation from latency, even in the presence of late gene expression. J. Virol. 79, 10339-10347 (2005). (Pubitemid 41098574)
74. Neumann, H., Medana, I. M., Bauer, J. & Lassmann, H. Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases. Trends Neurosci. 25, 313-319 (2002). (Pubitemid 34667013)
75. Binder, G. K. & Griffin, D. E. Immune-mediated clearance of virus from the central nervous system. Microb. Infect. 5, 439-448 (2003). (Pubitemid 36549186)
76. Kristensson, K. & Norrby, E. Persistence of RNA viruses in the central nervous system. Ann. Rev. Microbiol. 40, 159-184 (1986).
77. Drögemüller, K. et al. Astrocyte gp130 expression is critical for the control of Toxoplasma encephalitis. J. Immunol. 181, 2683-2693 (2008).
78. Lafon, M. et al. Modulation of HLA-G expression in human neural cells after neurotropic viral infections. J. Virol. 79, 15226-15237 (2005). (Pubitemid 43032305)
79. Bock, M. & Stoye, J. P. Endogenous retroviruses and the human germline. Curr. Opin. Genet. Dev. 10, 651-655 (2000).
80. Mi, S. et al. Syncytin is a captive retroviral envelope protein ionvolved in human placental morphogenesis. Nature 403, 785-789 (2000).
81. Buckley, P. T. et al. Cytoplasmic intron sequence-retaining transcripts can be dendritically targeted via ID element retrotransposons. Neuron 69, 877-884 (2011). This paper may open up a new field of research on how retroviral elements could play a fundamental part in neuronal functions.
82. Prat, C. M. et al. Mutation of the protein kinase C site in Borna disease virus phosphoprotein abrogates viral interference with neuronal signaling and restores normal synaptic activity. PLoS Pathog. 5, 1-10 (2009).
83. Viviani, B., Gardoni, F. & Marinovich, M. Cytokines and neuronal ion channels in health and disease. Int. Rev. Neurobiol. 82, 247-263 (2007).
84. Lamberton, P. H., Donnelly, C. A. & Webster, J. P. Specificity of the Toxoplasma gondii-altered behaviour to definitive versus non-definitive host predation risk. Parasitology 135, 1143-1150 (2008).
85. Gulinello, M. et al. Acquired infection with Toxoplasma gondii in adult mice results in sensorimotor deficits but normal cognitive behavior despite widespread brain pathology. Microbes Infect. 12, 528-537 (2010).
86. Bingham, J. & van der Merwe, M. Distribution of rabies antigen in brain material: Determining the reliability of different regions of the brain for the fluorescent antibody test. J. Virol. Meth. 101, 85-94 (2002). (Pubitemid 34159111)
87. Dellacasa-Lindberg, I., Hitziger, N. & Barragan, A. Localized recrudescence of Toxoplasma infections in the central nervous system of immunocompromised mice assessed by in vivo bioluminescence imaging. Microbes Infect. 9, 1291-1298 (2007). (Pubitemid 47539205)
88. Mansfield, K. L. et al. Tick-borne encephalitis virus-a review of an emerging zoonosis. J. Gen. Virol. 90, 1781-1794 (2009).
89. Murthy, J. M. K. & Prabhakar, S. Bacterial meningitis and epilepsy. Epilepsia 49, 8-12 (2008).
90. Misra, U. K., Tan, T. C. & Kalita, J. Viral encephalitis and epilepsy. Epilepsia 49, 13-18 (2008).
91. Idro, R., Ndiritu, M., Ogutu, B. & Mithwani, S. Burden, features, and outcome of neurological involvement in acute falciparum malaria in Kenyan children. JAMA 297, 2232-2240 (2007). (Pubitemid 47010881)
92. Palmer, B. S. Meta-analyses of three case controlled studies and an ecological study into the link between cryptogenic epilepsy and chronic toxoplasmosis infection. Seizure 16, 657-663 (2007). (Pubitemid 350018662)
93. Quet, F. et al. Meta-analysis of the association between cysticercosis and epilepsy in Africa. Epilepsia 51, 830-837 (2010).
94. Vezzani, A., French, J., Bartfai, T. & Baram, T. Z. The role of inflammation in epilepsy. Nature Rev. Neurol. 7, 31-40 (2011).
95. Stewart, K. A., Wilcox, K. S., Fujinami, R. S. & White, H. S. Theiler's virus infection chronically alters seizure susceptibility. Epilepsia 51, 1418-1428 (2010).
96. Vikman, K. S., Duggan, A. W. & Siddall, P. J. Interferon-γ induced disruption of GABAergic inhibition in the spinal dorsal horn in vivo. Pain 133, 18-28 (2007). (Pubitemid 350138308)
97. Pitkänen, A., Kharatishvili, I., Karhunen, H. & Lukasiuk, K. Epileptogenesis in experimental models. Epilepsia 48, 13-20 (2007). (Pubitemid 46849999)
98. Houweling, A. R., Bazhenov, M., Timofeev, I., Steriade, M. & Sejnowsski, T. J. Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb. Cortex 15, 834-845 (2005). (Pubitemid 40696122)
99. Takeuchi, O. & Akira, S. Pattern recognition receptors and inflammation. Cell 140, 805-820 (2010).
100. Dfring, A., Wild, M., Vestweber, D., Deutsch, U. & Engelhardt, B. E-and P-selectin are not required for the development of experimental autoimmune encephalomyelitis in C57BL/6 and SJL mice. J. Immunol. 179, 8470-8479 (2007).
101. Poteryaev, D., Datta, S., Ackema, K., Zerial, M. & Spang, A. Identification of the switch in early-to-late endosome transition. Cell 141, 497-508 (2010).
102. Deinhardt, K. et al. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52, 293-305 (2006). (Pubitemid 44548343)
103. Hirokawa, N., Niwa, S. & Tanaka, S. Molecular motors in neurons: Transport mechanisms and roles in brain function, development, and disease. Neuron 68, 610-638 (2010). A comprehensive review on the molecular mechanisms for axonal transport. It also describes how disturbances to the transport machinery can cause distinct diseases.
104. Urbanska, E., Chambers, B. J., Ljunggren, H.-G., Norrby, E. & Kristensson. K. Spread of measles virus through axonal pathways into limbic structures in the brain of TAP1-/-mice. J. Med. Virol. 52, 362-369 (1997). (Pubitemid 27356180)