Proteomic profiling reveals that rabies virus infection results in differential expression of host proteins involved in ion homeostasis and synaptic physiology in the central nervous system

Journal of NeuroVirology

Volumn 13, Issue 2, 2007, Pages 107-117

  Dhingra, Vikas ^a   Li, Xiaqing ^a   Liu, Yuru ^a   Fu, Zhen F ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Neuronal dysfunction; Neurotransmission; Pathogenesis; Proteomics; Rabies virus

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM ION; MEMBRANE PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SNARE PROTEIN; SODIUM ION; SULFAPERIN; SYNAPTOSOMAL ASSOCIATED PROTEIN; SYNTAXIN; TRIPARTITE MOTIF PROTEIN 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; MOUSE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RABIES; RABIES VIRUS; SODIUM CELL LEVEL; SYNAPSE VESICLE; UPREGULATION; VIRUS IMMUNITY; VIRUS PATHOGENESIS; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALCIUM; CELL MEMBRANE; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; IONS; MICE; MICE, INBRED ICR; POTASSIUM; PROTEINS; PROTEOMICS; RABIES; RABIES VIRUS; SNARE PROTEINS; SODIUM; SYNAPTIC VESICLES; VIRULENCE;

ANIMALIA; MUS; RABIES VIRUS;

EID: 34249035067     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.1080/13550280601178226     Document Type: Article

References (60)

1. Couto, L Araujo, Narciso, M Sampaio, Hokoc, J. N. and Martinez, A M Blanco (2004) Calpain inhibitor 2 prevents axonal degeneration of opossum optic nerve fibers. J Neurosci Res, 77, pp. 410-419.
2. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 72, pp. 248-254.
3. 1, receptor subtypes in rat brain. Eur J Pharmacol, 245, pp. 129-138.
4. Cecconi, F. (1999) Apaf1 and the apoptotic machinery. Cell Death Differ, 6, pp. 1087-1098.
5. + transport in skeletal muscle. Physiol Rev, 66, pp. 542-580.
6. DeFilippis, V., Raggo, C., Moses, A. and Fruh, K. (2003) Functional genomics in virology and antiviral drug discovery. Trends Biotechnol, 21, pp. 452-457.
7. Despres, P., Griffin, J. W. and Griffin, D. E. (1995) Antiviral activity of alpha interferon in Sindbis virus-infected cells is restored by anti-E2 monoclonal antibody treatment. J Virol, 69, pp. 7345-7348.
8. Dhingra, V., Allison, A. B., Stallknecht, D. E. and Fu, Z. F. (2005) Proteomic profiling and neurodegeneration in west-nile-virus-infected neurons. J. Biomed Biotech, 3, pp. 271-279.
9. Dietzschold, B., Rupprecht, C. E., Fu, Z. F. and Koprowski, H. (1996) Rhabdoviruses. Fields virology, pp. 1137-1159. Raven Press, New York
10. Duffy, S. and MacVicar, B. A. (1996) In vitro ischemia promotes calcium influx and intracellular calcium release in hippocampal astrocytes. J Neurosci, 16, pp. 71-81.
11. Etessami, R., Conzelmann, K. K., Fadai-Ghotbi, B., Natelson, B., Tsiang, H. and Ceccaldi, P. E. (2000) Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: An in vitro and in vivo study. J Gen Virol, 81, pp. 2147-2153.
12. +. J Neurosci, 13, pp. 63-72.
13. Fu, Z. F. and Jackson, A. C. (2005) Neuronal dysfunction and death in rabies virus infection. J NeuroVirol, 11, pp. 101-106.
14. Gottlieb, R. A., Giesing, H. A., Zhu, J. Y., Engler, R. L. and Babior, B. M. (1995) Cell acidification in apoptosis: Granulocyte colony-stimulating factor delays programmed cell death in neutrophils by up-regulating the vacuolar H(+)-ATPase. Proc Natl Acad Sci USA, 92, pp. 5965-5968.
15. Gourmelon, P., Briet, D., Clarencon, D., Court, L. and Tsiang, H. (1991) Sleep alterations in experimental street rabies virus infection occur in the absence of major EEG abnormalities. Brain Res, 554, pp. 159-165.
16. Gourmelon, P., Briet, D., Court, L. and Tsiang, H. (1986) Electrophysiological and sleep alterations in experimental mouse rabies. Brain Res, 398, pp. 128-140.
17. Hanson, P. I., Heuser, J. E. and Jahn, R. (1997) Neurotransmitter release-4 years of SNARE complexes. Curr. Opin. Neurobiol., 9, pp. 310-315.
18. Hemachudha, T. (1994) Human rabies: Clinical aspects, pathogenesis, and potential therapy. Curr Top Microbiol Immunol., 187, pp. 121-143.
19. Henzel, W. J., Billeci, T. M., Stults, J. T., Wong, S. C., Grimley, C. and Watanabe, C. (1993) Identifying proteins from two dimensional gels by molecular mass searching of peptide fragments in protein sequence databases. Proc Natl Acad Sci USA., 90, pp. 5011-5015.
20. Hong, W. (2005) SNAREs and traffic. Biochim Biophys Acta, 1744, pp. 493-517.
21. Iwasaki, Y. and Tobita, M. (2002) Pathology. Rabies, pp. 283-306. Academic Press, San Diego
22. Jackson, A. C. (2003) Rabies virus infection: An update. J NeuroVirol, 9, pp. 253-258.
23. Juntrakul, S., Ruangvejvorachai, P., Shuangshoti, S., Wacharapluesadee, S. and Hemachudha, T. (2005) Mechanisms of escape phenomenon of spinal cord and brainstem in human rabies. BMC Infect Dis, 5, p. 104.
24. Kellam, P. (2001) Post-genomic virology: The impact of bioinformatics, microarrays and proteomics on investigating host and pathogen interactions. Rev Med Virol, 11, pp. 313-329.
25. Ladogana, A., Bouzamondo, E., Pocchiari, M. and Tsiang, H. (1994) Modification of tritiated gamma-amino-n-butyric acid transport in rabies virus-infected primary cortical cultures. J Gen Virol, 75, pp. 623-627.
26. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, pp. 680-685.
27. Lalli, G., Bohnert, S., Deinhardt, K., Verastegui, C. and Schiavo, G. (2003) The journey of tetanus and botulinum neurotoxins in neurons. Trends Microbiol, 11, pp. 431-437.
28. Lentz, T. L., Burrage, T. G., Smith, A. L., Crick, J. and Tignor, G. H. (1982) Is the acetylcholine receptor a rabies virus receptor?. Science, 215, pp. 182-184.
29. Samento, L. and Fu, Z. F. (2005) Degenerative changes of mouse neuronal processes after rabies infection. J Virol, 79, pp. 10063-10068.
30. Lynch, J. J., Yu, S. P., Canzoniero, L. M., Sensi, S. L. and Choi, D. W. (1995) Sodium channel blockers reduce oxygen-glucose deprivation-induced cortical neuronal injury when combined with glutamate receptor antagonists. J Pharmacol Exp Ther, 273, pp. 554-560.
31. McGinnis, K. M., Wang, K. K. and Gnegy, M. E. (1999) Alterations of extracellular calcium elicit selective modes of cell death and protease activation in SH-SY5Y human neuroblastoma cells. J Neurochem, 72, pp. 1853-1863.
32. Mitrabhakdi, E., Shuangshoti, S., Wannakrairot, P., Lewis, R. A., Susuki, K., Laothamatas, J. and Hemachudha, T. (2005) Difference in neuropathogenetic mechanisms in human furious and paralytic rabies. J Neurol Sci, 238, pp. 3-10.
33. +-ATPase isozyme diversity; comparative biochemistry and physiological implications of novel functional interactions. Biosci Rep, 20, pp. 51-91.
34. Morimoto, K., Hooper, D. C., Carbaugh, H., Fu, Z. F., Koprowski, H. and Dietzschold, B. (1998) Rabies virus quasispecies: Implications for pathogenesis. Proc Natl Acad Sci USA, 95, pp. 3152-3156.
35. Morimoto, K., Hooper, D. C., Spitsin, S., Koprowski, H. and Dietzschold, B. (1999) Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J Virol., 73, pp. 510-518.
36. Morimoto, K., Patel, M., Corisdeo, S., Hooper, D. C., Fu, Z. F., Rupprecht, C. E., Koprowski, H. and Dietzschold, B. (1996) Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America. Proc Natl Acad Sci USA, 93, pp. 5653-5658.
37. Muller, E. E. and Nistico, G. (1988) Brain messengers and the pituitary, Academic Press, New York
38. Murphy, F. A. and Bauer, S. P. (1974) Early street rabies virus infection in striated muscle and later progression to the central nervous system. Intervirology, 3, pp. 256-268.
39. Murphy, F. A. (1977) Rabies pathogenesis. Arch Virol, 54, pp. 279-297.
40. Odland, R. M. and Sutton, R. L. (1999) Hyperosmosis of cerebral injury. Neurol Res, 21, pp. 500-508.
41. Ohta, T., Arakawa, H., Futagami, F., Fushida, S., Kitagawa, H., Kayahara, M., Nagakawa, T., Miyazaki, I., Numata, M. and Ohkuma, S. (1996) A new strategy for the therapy of pancreatic cancer by proton pump inhibitor. Gan To Kagaku Ryoho, 23, pp. 1660-1664.
42. Pozzo-Miller, L. D., Gottschalk, W., Zhang, L., McDermott, K., Gopalakrishnan, R., Oho, C. and Sheng, Z. H. (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J Neurosci, 19, pp. 4972-4983.
43. Romero, M. F. (2004) In the beginning, there was the cell: Cellular homeostasis. Adv Physiol Educ, 28, pp. 135-138.
44. Shankar, V., Dietzschold, B. and Koprowski, H. (1991) Direct entry of rabies virus into the central nervous system without prior local replication. J Virol, 65, pp. 2736-2738.
45. Sarmento, L., Li, X. Q., Howerth, E., Jackson, A. C. and Fu, Z. F. (2005) Glycoprotein-mediated induction of apoptosis limits the spread of attenuated rabies viruses in the central nervous system of mice. J NeuroVirol, 11, pp. 571-581.
46. Sarmento, L., Tseggai, T., Dhingra, V. and Fu, Z. F. (2006) Rabies virus-induced apoptosis involves caspase-dependent and caspase-independent pathways. Virus Res, 121, pp. 144-151.
47. Schiavo, G. and Stenbeck, G. (1998) Molecular analysis of neurotransmitter release. Essays Biochem, 33, pp. 29-41.
48. Somjen, G. G. (2002) Ion regulation in the brain: Implications for pathophysiology. Neuroscientist, 8, pp. 254-267.
49. Stys, P. K. (1998) Anoxic and ischemic injury of myelinated axons in CNS white matter: From mechanistic concepts to therapeutics. J Cereb Blood Flow Metab, 18, pp. 2-25.
50. 2+ exchanger. J Neurosci, 12, pp. 430-439.
51. Szule, J. A. and Coorssen, J. R. (2003) Revisiting the role of SNAREs in exocytosis and membrane fusion. Biochim Biophys Acta, 1641, pp. 121-135.
52. Thoulouze, M. I., Lafage, M., Schachner, M., Hartmann, U., Cremer, H. and Lafon, M. (1998) The neural cell adhesion molecule is a receptor for rabies virus. J Virol, 72, pp. 7181-7190.
53. Tirawatnpong, S., Hemachudha, T., Manutsathit, S., Shuangshoti, S., Phanthumchinda, K. and Phanuphak, P. (1989) Regional distribution of rabies viral antigen in central nervous system of human encephalitic and paralytic rabies. J Neurol Sci, 92, pp. 91-99.
54. Tuffereau, C., Benejean, J., Blondel, D., Kieffer, B. and Flamand, A. (1998) Low-affinity nerve-growth factor receptor (P75NTR) can serve as a receptor for rabies virus. EMBO J, 17, pp. 7250-7259.
55. Tsiang, H. (1982) Neuronal function impairment in rabies-infected rat brain. J Gen Virol, 61, pp. 277-281.
56. + ATPase activity in membranes of Sindbis virus-infected chick cells. Virology, 216, pp. 299-308.
57. + channels: A rational and effective strategy against ischemic brain damage. Pharmacol Rev, 48, pp. 21-67.
58. Wait, R., Gianazza, E. and Eberini, I. (2001) Proteins of rat serum, urine, and cerebrospinal fluid. VI. Further protein identifications and interstrain comparison. Electrophoresis, 22, pp. 3043-3052.
59. Wang, Z. W., Sarmento, L., Wang, Y., Li, X. Q., Dhingra, V., Tseggai, T., Jiang, B. and Fu, Z. F. (2005) Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol, 79, pp. 12554-12565.
60. Yan, X., Prosniak, M., Curtis, M. T., Weiss, M. L., Faber, M., Dietzschold, B. and Fu, Z. F. (2001) Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J NeuroVirol, 7, pp. 518-527.