Alpha-synuclein expression restricts RNA viral infections in the brain

Journal of Virology

Volumn 90, Issue 6, 2016, Pages 2767-2782

  Beatman, Erica L ^a   Massey, Aaron ^a   Shives, Katherine D ^a   Burrack, Kristina S ^a,b   Chamanian, Mastooreh ^a   Morrison, Thomas E ^a   Beckham, David J ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; RAB PROTEIN; VIRUS ENVELOPE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN INFECTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMAN; HUMAN TISSUE; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VENEZUELAN EQUINE ENCEPHALITIS; VIRUS INFECTION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TITRATION; WEST NILE FEVER; WILD TYPE; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION; IMMUNOLOGY; INNATE IMMUNITY; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; NERVE CELL; RNA VIRUS INFECTIONS; SURVIVAL ANALYSIS; VENEZUELAN EQUINE ENCEPHALITIS VIRUS; VIROLOGY; WEST NILE VIRUS;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; CELLS, CULTURED; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; FEMALE; GENE EXPRESSION; IMMUNITY, INNATE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; RNA VIRUS INFECTIONS; SURVIVAL ANALYSIS; WEST NILE VIRUS;

EID: 84961126184     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02949-15     Document Type: Article

References (46)

1. Beckham JD, Tyler KL. 2012. Neuro-intensive care of patients with acute CNS infections. Neurotherapeutics 9:124-138. http://dx.doi.org/10.1007/s13311-011-0086-5.
2. Carrera JP, Forrester N, Wang E, Vittor AY, Haddow AD, Lopez-Verges S, Abadia I, Castano E, Sosa N, Baez C, Estripeaut D, Diaz Y, Beltran D, Cisneros J, Cedeno HG, Travassos da Rosa AP, Hernandez H, Martinez-Torres AO, Tesh RB, Weaver SC. 2013. Eastern equine encephalitis in Latin America. N Engl J Med 369:732-744. http://dx.doi.org/10.1056/NEJMoa1212628.
3. Solomon T. 2004. Flavivirus encephalitis. N Engl J Med 351:370-378. http://dx.doi.org/10.1056/NEJMra030476.
4. Ali M, Safriel Y, Sohi J, Llave A, Weathers S. 2005. West Nile virus infection: MR imaging findings in the nervous system. AJNR Am J Neuroradiol 26:289-297.
5. Armah HB, Wang G, Omalu BI, Tesh RB, Gyure KA, Chute DJ, Smith RD, Dulai P, Vinters HV, Kleinschmidt-DeMasters BK, Wiley CA. 2007. Systemic distribution of West Nile virus infection: postmortem immunohistochemical study of six cases. Brain Pathol 17:354-362. http://dx.doi.org/10.1111/j.1750-3639.2007.00080.x.
6. Tyler KL, Pape J, Goody RJ, Corkill M, Kleinschmidt-DeMasters BK. 2006. CSF findings in 250 patients with serologically confirmed West Nile virus meningitis and encephalitis. Neurology 66:361-365. http://dx.doi.org/10.1212/01.wnl.0000195890.70898.1f.
7. Sejvar JJ, Haddad MB, Tierney BC, Campbell GL, Marfin AA, Van Gerpen JA, Fleischauer A, Leis AA, Stokic DS, Petersen LR. 2003. Neurologic manifestations and outcome of West Nile virus infection. JAMA 290:511-515. http://dx.doi.org/10.1001/jama.290.4.511.
8. Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ. 2009. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A 106:14063-14068. http://dx.doi.org/10.1073/pnas.0900096106.
9. Jang H, Boltz DA, Webster RG, Smeyne RJ. 2009. Viral parkinsonism. Biochim Biophys Acta 1792:714-721. http://dx.doi.org/10.1016/j.bbadis.2008.08.001.
10. Cho H, Proll SC, Szretter KJ, Katze MG, Gale M, Jr, Diamond MS. 2013. Differential innate immune response programs in neuronal subtypes determine susceptibility to infection in the brain by positivestranded RNA viruses. Nat Med 19:458-464. http://dx.doi.org/10.1038/nm.3108.
11. Forman MS, Trojanowski JQ, Lee VM. 2004. Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat Med 10:1055-1063. http://dx.doi.org/10.1038/nm1113.
12. Vila M, Przedborski S. 2004. Genetic clues to the pathogenesis of Parkinson's disease. Nat Med 10(Suppl):S58-S62.
13. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M. 1998. Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci U S A 95:6469-6473. http://dx.doi.org/10.1073/pnas.95.11.6469.
14. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, Lincoln S, Levecque C, Larvor L, Andrieux J, Hulihan M, Waucquier N, Defebvre L, Amouyel P, Farrer M, Destee A. 2004. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364: 1167-1169. http://dx.doi.org/10.1016/S0140-6736(04)17103-1.
15. Ibanez P, Bonnet AM, Debarges B, Lohmann E, Tison F, Pollak P, Agid Y, Durr A, Brice A. 2004. Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet 364:1169-1171. http://dx.doi.org/10.1016/S0140-6736(04)17104-3.
16. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O. 1998. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18:106-108. http://dx.doi.org/10.1038/ng0298-106.
17. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL. 1997. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276:2045-2047. http://dx.doi.org/10.1126/science.276.5321.2045.
18. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K. 2003. Alphasynuclein locus triplication causes Parkinson's disease. Science 302:841. http://dx.doi.org/10.1126/science.1090278.
19. Tan EK, Chai A, Teo YY, Zhao Y, Tan C, Shen H, Chandran VR, Teoh ML, Yih Y, Pavanni R, Wong MC, Puvan K, Lo YL, Yap E. 2004. Alpha-synuclein haplotypes implicated in risk of Parkinson's disease. Neurology 62:128-131. http://dx.doi.org/10.1212/01.WNL.0000101721.25345.DC.
20. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Atares B, Llorens V, Gomez Tortosa E, del Ser T, Munoz DG, de Yebenes JG. 2004. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55:164-173. http://dx.doi.org/10.1002/ana.10795.
21. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, Sagara Y, Sisk A, Mucke L. 2000. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287:1265-1269. http://dx.doi.org/10.1126/science.287.5456.1265.
22. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, Shinsky N, Verdugo JM, Armanini M, Ryan A, Hynes M, Phillips H, Sulzer D, Rosenthal A. 2000. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25:239-252. http://dx.doi.org/10.1016/S0896-6273(00)80886-7.
23. Dauer W, Kholodilov N, Vila M, Trillat AC, Goodchild R, Larsen KE, Staal R, Tieu K, Schmitz Y, Yuan CA, Rocha M, Jackson-Lewis V, Hersch S, Sulzer D, Przedborski S, Burke R, Hen R. 2002. Resistance of alpha-synuclein null mice to the Parkinsonian neurotoxin MPTP. Proc Natl Acad Sci U S A 99:14524-14529. http://dx.doi.org/10.1073/pnas.172514599.
24. Burre J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Sudhof TC. 2010. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329:1663-1667. http://dx.doi.org/10.1126/science.1195227.
25. Burre J, Sharma M, Sudhof TC. 2014. Alpha-synuclein assembles into higher-order multimers upon membrane binding to promote SNARE complex formation. Proc Natl Acad SciUSA111:E4274-E4283. http://dx.doi.org/10.1073/pnas.1416598111.
26. Auluck PK, Caraveo G, Lindquist S. 2010. Alpha-synuclein: membrane interactions and toxicity in Parkinson's disease. Annu Rev Cell Dev Biol 26:211-233. http://dx.doi.org/10.1146/annurev.cellbio.042308.113313.
27. Cooper AA, Gitler AD, Cashikar A, Haynes CM, Hill KJ, Bhullar B, Liu K, Xu K, Strathearn KE, Liu F, Cao S, Caldwell KA, Caldwell GA, Marsischky G, Kolodner RD, Labaer J, Rochet JC, Bonini NM, Lindquist S. 2006. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313:324-328. http://dx.doi.org/10.1126/science.1129462.
28. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
29. Beatman E, Oyer R, Shives KD, Hedman K, Brault AC, Tyler KL, Beckham JD. 2012. West Nile virus growth is independent of autophagy activation. Virology 433:262-272. http://dx.doi.org/10.1016/j.virol.2012.08.016.
30. Shives KD, Beatman EL, Chamanian M, O'Brien C, Hobson-Peters J, Beckham JD. 2014. West Nile virus-induced activation of mammalian target of rapamycin complex 1 supports viral growth and viral protein expression. J Virol 88:9458-9471. http://dx.doi.org/10.1128/JVI.01323-14.
31. Beckham JD, Tuttle KD, Tyler KL. 2010. Caspase-3 activation is required for reovirus-induced encephalitis in vivo. J Neurovirol 16:306-317. http://dx.doi.org/10.3109/13550284.2010.499890.
32. Clarke P, Leser JS, Quick ED, Dionne KR, Beckham JD, Tyler KL. 2014. Death receptor-mediated apoptotic signaling is activated in the brain following infection with West Nile virus in the absence of a peripheral immune response. J Virol 88:1080-1089. http://dx.doi.org/10.1128/JVI.02944-13.
33. Hyde JL, Gardner CL, Kimura T, White JP, Liu G, Trobaugh DW, Huang C, Tonelli M, Paessler S, Takeda K, Klimstra WB, Amarasinghe GK, Diamond MS. 2014. A viral RNA structural element alters host recognition of nonself RNA. Science 343:783-787. http://dx.doi.org/10.1126/science.1248465.
34. Ambrose RL, Mackenzie JM. 2011. West Nile virus differentially modulates the unfolded protein response to facilitate replication and immune evasion. J Virol 85:2723-2732. http://dx.doi.org/10.1128/JVI.02050-10.
35. Pena J, Harris E. 2011. Dengue virus modulates the unfolded protein response in a time-dependent manner. J Biol Chem 286:14226-14236. http://dx.doi.org/10.1074/jbc.M111.222703.
36. Colla E, Coune P, Liu Y, Pletnikova O, Troncoso JC, Iwatsubo T, Schneider BL, Lee MK. 2012. Endoplasmic reticulum stress is important for the manifestations of alpha-synucleinopathy in vivo. J Neurosci 32: 3306-3320. http://dx.doi.org/10.1523/JNEUROSCI.5367-11.2012.
37. Ambrose RL, Mackenzie JM. 2013. ATF6 signaling is required for efficient West Nile virus replication by promoting cell survival and inhibition of innate immune responses. J Virol 87:2206-2214. http://dx.doi.org/10.1128/JVI.02097-12.
38. Schuck S, Prinz WA, Thorn KS, Voss C, Walter P. 2009. Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 187:525-536. http://dx.doi.org/10.1083/jcb.200907074.
39. Samuel MA, Morrey JD, Diamond MS. 2007. Caspase 3-dependent cell death of neurons contributes to the pathogenesis of West Nile virus encephalitis. J Virol 81:2614-2623. http://dx.doi.org/10.1128/JVI.02311-06.
40. Bendor JT, Logan TP, Edwards RH. 2013. The function of alphasynuclein. Neuron 79:1044-1066. http://dx.doi.org/10.1016/j.neuron.20 13.09.004.
41. Boassa D, Berlanga ML, Yang MA, Terada M, Hu J, Bushong EA, Hwang M, Masliah E, George JM, Ellisman MH. 2013. Mapping the subcellular distribution of alpha-synuclein in neurons using genetically encoded probes for correlated light and electron microscopy: implications for Parkinson's disease pathogenesis. J Neurosci 33:2605-2615. http://dx.doi.org/10.1523/JNEUROSCI.2898-12.2013.
42. Sharma M, Burre J, Sudhof TC. 2011. CSPalpha promotes SNAREcomplex assembly by chaperoning SNAP-25 during synaptic activity. Nat Cell Biol 13:30-39. http://dx.doi.org/10.1038/ncb2131.
43. Thayanidhi N, Helm JR, Nycz DC, Bentley M, Liang Y, Hay JC. 2010. Alpha-synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs. Mol Biol Cell 21:1850-1863. http://dx.doi.org/10.1091/mbc.E09-09-0801.
44. Enyedi B, Varnai P, Geiszt M. 2010. Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid Redox Signal 13:721-729. http://dx.doi.org/10.1089/ars.2009.2880.
45. Zhao G, Lu H, Li C. 2015. Proapoptotic activities of protein disulfide isomerase (PDI) and PDIA3 protein, a role of the Bcl-2 protein Bak. J Biol Chem 290:8949-8963. http://dx.doi.org/10.1074/jbc.M114.619353.
46. 4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J Virol 80:12060-12069. http://dx.doi.org/10.1128/JVI.01650-06.