Mutation of the protein kinase C site in Borna disease virus phosphoprotein abrogates viral interference with neuronal signaling and restores normal synaptic activity

PLoS Pathogens

Volumn 5, Issue 5, 2009, Pages

  Prat, Christine M A ^a   Schmid, Sonja ^b   Farrugia, Fanny ^c   Cenac, Nicolas ^d   Le Masson, Gwendal ^c   Schwemmle, Martin ^b   Gonzalez Dunia, Daniel ^a  

^a INSERM   (France)

^b UNIVERSITY OF FREIBURG   (Germany)

^c INSTITUT FRANÇOIS MAGENDIE   (France)

^d France   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; MARCKS PROTEIN; PROTEIN KINASE C; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; VIRUS PHOSPHOPROTEIN; VIRUS PROTEIN; PHOSPHOPROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BORNA DISEASE VIRUS; BRAIN NERVE CELL; CONTROLLED STUDY; DEPOLARIZATION; DYNAMICS; ELECTRIC ACTIVITY; ENZYME PHOSPHORYLATION; GENE MUTATION; KINETICS; MICROELECTRODE; MODULATION; MUTANT; NERVE CELL NETWORK; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROTEIN EXPRESSION; RAT; STIMULATION; SYNAPSE; VIRUS INFECTION; VIRUS INTERFERENCE; VIRUS RECOMBINANT; ACTION POTENTIAL; ANIMAL; BORNA DISEASE; CELL CULTURE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; MUTATION; NERVE CELL; NERVE CELL PLASTICITY; PATCH CLAMP; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION; VIROLOGY; WESTERN BLOTTING;

BORNA DISEASE VIRUS;

ACTION POTENTIALS; ANIMALS; BLOTTING, WESTERN; BORNA DISEASE; BORNA DISEASE VIRUS; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; MUTATION; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION; VIRAL PROTEINS;

EID: 67249121408     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000425     Document Type: Article

References (59)

1. Oldstone MB, Sinha YN, Blount P, Tishon A, Rodriguez M, et al. (1982) Virus-induced alterations in homeostasis: alteration in differentiated functions of infected cells in vivo. Science 218: 1125-1127. (Pubitemid 13223314)
2. Ahmed R, Morrison LA, Knipe DM (1996) Persistence of Viruses. In: Fields BN, Knipe DM, Howley PM, Chanock RM, Melnick JL, et al . Fields Virology. 3rd ed. Philadelphia: Lippincott-Raven. pp 219-249.
3. Lipkin WI, Hornig M (2004) Psychotropic viruses. Curr Opin Microbiol 7: 420-425. (Pubitemid 39091129)
4. Tomonaga K (2004) Virus-induced neurobehavioral disorders: mechanisms and implications. Trends Mol Med 10: 71-77. (Pubitemid 38210027)
5. Kristensson K, Norrby E (1986) Persistence of RNA viruses in the central nervous system. Annu Rev Microbiol 40: 159-184.
6. de la Torre JC, Oldstone MBA (1996) The anatomy of viral persistence: mechanisms of persistence and associated disease. Adv Virus Res 46: 311-343. (Pubitemid 3027547)
7. de la Torre JC (1994) Molecular biology of Borna disease virus: prototype of a new group of animal viruses. J Virol 68: 7669-7675. (Pubitemid 24362651)
8. Schneemann A, Schneider PA, Lamb RA, Lipkin WI (1995) The remarkable coding strategy of Borna disease virus: a new member of the nonsegmented negative strand RNA viruses. Virology 210: 1-8.
9. Briese T, Schneemann A, Lewis AJ, Park YS, Kim S, et al. (1994) Genomic organization of Borna disease virus. Proc Natl Acad Sci USA 91: 4362-4366. (Pubitemid 24143433)
10. Cubitt B, Oldstone C, Valcarcel J, de la Torre JC (1994) RNA splicing contributes to the generation of mature mRNAs of Borna disease virus, a nonsegmented negative strand RNA virus. Virus Res 34: 69-79. (Pubitemid 24293254)
11. Schneider PA, Schneemann A, Lipkin WI (1994) RNA splicing in Borna disease virus, a nonsegmented, negative-strand RNA virus. J Virol 68: 5007-5012. (Pubitemid 2114592)
12. Ludwig H, Bode L (2000) Borna disease virus: new aspects on infection, disease, diagnosis and epidemiology. Rev Sci Tech 19: 259-288.
13. Staeheli P, Sauder C, Hausmann J, Ehrensperger F, Schwemmle M (2000) Epidemiology of Borna disease virus. J Gen Virol 81: 2123-2135. (Pubitemid 30705983)
14. Pletnikov M, Gonzalez-Dunia D, Stitz L (2002) Experimental infection: pathogenesis of neurobehavioral disease. In: Carbone K, ed. Borna disease virus and its role in neurobehavioral disease. Washington D.C.: ASM press. pp 125-178.
15. Gonzalez-Dunia D, Volmer R, Mayer D, Schwemmle M (2005) Borna disease virus interference with neuronal plasticity. Virus Res 111: 224-234. (Pubitemid 40909738)
16. Hornig M, Solbrig M, Horscroft N, Weissenbock H, Lipkin WI (2001) Borna disease virus infection of adult and neonatal rats: models for neuropsychiatric disease. Curr Top Microbiol Immunol 253: 157-177. (Pubitemid 32416664)
17. Bode L, Ludwig H (2003) Borna disease virus infection, a human mental-health risk. Clin Microbiol Rev 16: 534-545. (Pubitemid 36871320)
18. Ikuta K, Ibrahim MS, Kobayashi T, Tomonaga K (2002) Borna disease virus and infection in humans. Front Biosci 7: 470-495.
19. Chalmers RM, Thomas DR, Salmon RL (2005) Borna disease virus and the evidence for human pathogenicity: a systematic review. QJM 98: 255-274. (Pubitemid 40500686)
20. Gosztonyi G, Ludwig H (1984) Neurotransmitter receptors and viral neurotropism. Neuropsychiatria Clinica 3: 107-114.
21. Gonzalez-Dunia D, Sauder C, de la Torre JC (1997) Borna disease virus and the brain. Brain Res Bull 44: 647-664. (Pubitemid 27527862)
22. Brady S, Colman DR, Brophy P (1999) Subcellular organization of the nervous system. In: Zigmond MJ, Bloom FE, Landis SC, Roberts JL, Squire LR, eds. Fundamental neuroscience. San Diego: Academic Press. pp 71-106.
23. Volmer R, Prat CM, Le Masson G, Garenne A, Gonzalez-Dunia D (2007) Borna disease virus infection impairs synaptic plasticity. J Virol 81: 8833-8837. (Pubitemid 47242857)
24. Volmer R, Monnet C, Gonzalez-Dunia D (2006) Borna disease virus blocks potentiation of synaptic activity through inhibition of protein kinase C signaling. Plos Pathog 2(3): e19. doi:10.1371/journal.ppat.0020019.
25. Abeliovich A, Chen C, Goda Y, Silva AJ, Stevens CF, et al. (1993) Modified hippocampal long-term potentiation in PKC gamma-mutant mice. Cell 75: 1253-1262. (Pubitemid 24021901)
26. De BP, Banerjee AK (1997) Role of host proteins in gene expression of nonsegmented negative strand RNA viruses. Adv Virus Res 48: 169-204.
27. Schwemmle M, De B, Shi LC, Banerjee A, Lipkin WI (1997) Borna disease virus P-protein is phosphorylated by protein kinase c-epsilon and casein kinase II. J Biol Chem 272: 21818-21823. (Pubitemid 27382797)
28. Schneider U, Schwemmle M, Staeheli P (2005) Genome trimming: a unique strategy for replication control employed by Borna disease virus. Proc Natl Acad Sci U S A 102: 3441-3446. (Pubitemid 40328064)
29. Schmid S, Mayer D, Schneider U, Schwemmle M (2007) Functional characterization of the major and minor phosphorylation sites of the P protein of Borna disease virus. J Virol 81: 5497-5507. (Pubitemid 46846990)
30. Pleschka S, Staeheli P, Kolodziejek J, Richt JA, Nowotny N, et al. (2001) Conservation of coding potential and terminal sequences in four different isolates of Borna disease virus. J Gen Virol 82: 2681-2690. (Pubitemid 32998646)
31. Bajramovic JJ, Münter S, Syan S, Nerhbass U, Brahic M, et al. (2003) Borna disease virus glycoprotein is required for viral dissemination in neurons. J Virol 77: 12222-12231. (Pubitemid 37339875)
32. McNamara RK, Lenox RH (2004) The myristoylated alanine-rich C kinase substrate: a lithium-regulated protein linking cellular signaling and cytoskeletal plasticity. Clin Neurosci Res 4: 155-159. (Pubitemid 40197839)
33. Shimazaki Y, Nishiki T, Omori A, Sekiguchi M, Kamata Y, et al. (1996) Phosphorylation of 25-kDa synaptosome-associated protein. Possible involvement in protein kinase C-mediated regulation of neurotransmitter release. J Biol Chem 271: 14548-14553. (Pubitemid 26190359)
34. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547. (Pubitemid 39050412)
35. Pozzi D, Condliffe S, Bozzi Y, Chikhladze M, Grumelli C, et al. (2008) Activity-dependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels. Proc Natl Acad Sci U S A 105: 323-328.
36. Microelectrode Arrays. http://www.multichannelsystems.com/.
37. Berdondini L, Chiappalone M, van der Wal PD, Imfeld K, de Rooij NF, et al. (2006) A microelectrode array (MEA) integrated with clustering structures for investigating in vitro neurodynamics in confined interconnected sub-populations of neurons. Sensors Actuat B: Chem 114: 530-541. (Pubitemid 43276224)
38. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84: 87-136. (Pubitemid 38049877)
39. Mozhayeva MG, Sara Y, Liu X, Kavalali ET (2002) Development of vesicle pools during maturation of hippocampal synapses. J Neurosci 22: 654-665. (Pubitemid 34141746)
40. Arnold FJ, Hofmann F, Bengtson CP, Wittmann M, Vanhoutte P, et al. (2005) Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependent plasticity. J Physiol 564: 3-19. (Pubitemid 40542185)
41. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44: 5-21. (Pubitemid 39348827)
42. Saito N, Itouji A, Totani Y, Osawa I, Koide H, et al. (1993) Cellular and intracellular localization of epsilon-subspecies of protein kinase C in the rat brain; presynaptic localization of the epsilon-subspecies. Brain Res 607: 241-248. (Pubitemid 23104971)
43. Asenjo A, Gonzalez-Armas JC, Villanueva N (2008) Phosphorylation of human respiratory syncytial virus P protein at serine 54 regulates viral uncoating. Virology 380: 26-33.
44. Calabrese B, Halpain S (2005) Essential Role for the PKC Target MARCKS in Maintaining Dendritic Spine Morphology. Neuron 48: 77-90. (Pubitemid 41384167)
45. Ramakers GM, McNamara RK, Lenox RH, De Graan PN (1999) Differential changes in the phosphorylation of the protein kinase C substrates myristoylated alanine-rich C kinase substrate and growth-associated protein-43/B-50 following Schaffer collateral long-term potentiation and long-term depression. J Neurochem 73: 2175-2183. (Pubitemid 29491833)
46. Solbrig MV, Fallon JH, Lipkin WI (1995) Behavioral disturbances and pharmacology of Borna disease. In: Koprowski H, Lipkin I, eds. Borna Disease. Berlin: Springer-Verlag KG. pp 93-101.
47. Faraone SV, Perlis RH, Doyle AE, Smoller JW, Goralnick JJ, et al. (2005) Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry 57: 1313-1323. (Pubitemid 40798551)
48. Gosso MF, de Geus EJ, Polderman TJ, Boomsma DI, Heutink P, et al. (2008) Common variants underlying cognitive ability: further evidence for association between the SNAP-25 gene and cognition using a family-based study in two independent Dutch cohorts. Genes Brain Behav 7: 355-364.
49. Suberbielle E, Stella A, Pont F, Monnet C, Mouton E, et al. (2008) Proteomic Analysis Reveals Selective Impediment of Neuronal Remodeling upon Borna Disease Virus Infection. J Virol 82: 12265-12279.
50. Gupta AK, Blondel D, Choudhary S, Banerjee AK (2000) The phosphoprotein of rabies virus is phosphorylated by a unique cellular protein kinase and specific isomers of protein kinase C. J Virol 74: 91-98. (Pubitemid 30002887)
51. Kamitani W, Shoya Y, Kobayashi T, Watanabe M, Lee BJ, et al. (2001) Borna disease virus phosphoprotein binds a neurite outgrowth factor, amphoterin/HMG-1. J Virol 75: 8742-8751. (Pubitemid 32768978)
52. Unterstab G, Ludwig S, Anton A, Planz O, Dauber B, et al. (2005) Viral targeting of the interferon-{beta}-inducing Traf family member-associated NF- {kappa}B activator (TANK)-binding kinase-1. Proc Natl Acad Sci U S A 102: 13640-13645. (Pubitemid 41420901)
53. Peng G, Yan Y, Zhu C, Wang S, Yan X, et al. (2008) Borna disease virus p protein affects neural transmission through interactions with gamma-aminobutyric acid receptor-associated protein. J Virol 82: 12487-12497.
54. Kamitani W, Ono E, Yoshino S, Kobayashi T, Taharaguchi S, et al. (2003) Glial expression of Borna disease virus phosphoprotein induces behavioral and neurological abnormalities in transgenic mice. Proc Natl Acad Sci U S A 100: 8969-8974. (Pubitemid 36899207)
55. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2: 185-193. (Pubitemid 33673371)
56. Vitkovic L, Aloyo VJ, Maeda S, Benzil DL, Bressler JP, et al. (2005) Identification of myristoylated alanine-rich C kinase substrate (MARCKS) in astrocytes. Front Biosci 10: 160-165. (Pubitemid 40543026)
57. Hans A, Bajramovic JJ, Syan S, Perret E, Dunia I, et al. (2004) Persistent, noncytolytic infection of neurons by Borna disease virus interferes with ERK 1/2 signaling and abrogates BDNF-induced synaptogenesis. Faseb J 18: 863-865.
58. Nakanishi K, Kukita F (1998) Functional synapses in synchronized bursting of neocortical neurons in culture. Brain Res 795: 137-146. (Pubitemid 28337825)
59. Li X, Zhou W, Zeng S, Liu M, Luo Q (2007) Long-term recording on multielectrode array reveals degraded inhibitory connection in neuronal network development. Biosens Bioelectron 22: 1538-1543. (Pubitemid 46135982)