The genetics of alphaviruses

Future Virology

Volumn 6, Issue 12, 2011, Pages 1407-1422

  Foo, Suan Sin ^a,b   Chen, Weiqiang ^a,b   Herrero, Lara ^b   Bettadapura, Jayaram ^b   Narayan, Jayasuryan ^c   Dar, Lalit ^d   Broor, Shobha ^d   Mahalingam, Suresh ^b  

^a AGENCY FOR SCIENCE   (Singapore)

^b GRIFFITH UNIVERSITY   (Australia)

^c Microtest Innovations Pvt Ltd   (India)

^d ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

adaptation; alphavirus; arthropod vector; clinical feature; evolution; genetic determinant; IFN; therapeutic aspect

Indexed keywords

ALPHAVIRUS PROTEIN; INTERFERON; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA VIRUS; ALPHAVIRUS INFECTION; CLINICAL FEATURE; DNA VECTOR; GENE EXPRESSION; GENE THERAPY; GENETIC ANALYSIS; HUMAN; IMMUNE RESPONSE; MOSQUITO; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA VECTOR; VIRUS CLASSIFICATION; VIRUS GENE; VIRUS LIKE AGENT; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS TRANSMISSION;

EID: 82455206363     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.11.123     Document Type: Review

References (131)

1. Strauss JH, Strauss EG. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58(3), 491-562 (1994).
2. Powers AM, Brault AC, Shirako Y et al. Evolutionary relationships and systematics of the alphaviruses. J. Virol. 75(21), 10118-10131 (2001).
3. The positive sense single stranded RNA viruses. In: Virus Taxonomy. Academic Press, CA, USA, 739-1128 (2005).
4. Kononchik J, Hernandez R, Brown D. An alternative pathway for alphavirus entry. Virol. J. 15(8), 304 (2011).
5. Jose J, Snyder JE, Kuhn RJ. A structural and functional perspective of alphavirus replication and assembly. Future Microbiol. 4(7), 837-856 (2009).
6. Gould EA, Coutard B, Malet H et al. Understanding the alphaviruses: recent research on important emerging pathogens and progress towards their control. Antiviral Res. 87(2), 111-124 (2010).
7. Paredes A, Weaver S, Watowich S, Chiu W. Structural biology of old world and new world alphaviruses. Arch. Virol. Suppl. (19), 179-185 (2005).
8. Das T, Jaffar-Bandjee MC, Hoarau JJ et al. Chikungunya fever: CNS infection and pathologies of a re-emerging arbovirus. Prog. Neurobiol. 91(2), 121-129 (2010).
9. Rulli NE, Melton J, Wilmes A, Ewart G, Mahalingam S. The molecular and cellular aspects of arthritis due to alphavirus infections. Ann. NY Acad. Sci. 1102(1), 96-108 (2007).
10. Leung JY-S, Ng MM-L, Chu JJH. Replication of alphaviruses: a review on the entry process of alphaviruses into cells. Adv. Virol. doi:10.1155/2011/ 249640 (2011) (Epub ahead of print).
11. Lewthwaite P, Vasanthapuram R, Osborne JC et al. Chikungunya virus and central nervous system infections in children, India. Emerg. Infect. Dis. 15(2), 329-331 (2009).
12. Deardorff ER, Weaver SC. Vector competence of Culex (Melanoconion) taeniopus for equine-virulent subtype IE strains of Venezuelan equine encephalitis virus. Am. J. Trop. Med. Hyg. 82(6), 1047-1052 (2010).
13. Weinstein P, Judge D, Carver S. Biological and cultural coevolution and emerging infectious disease: Ross River virus in Australia. Med. Hypotheses 76(6), 893-896 (2011).
14. Gibney KB, Fischer M, Prince HE et al. Chikungunya fever in the United States: a fifteen year review of cases. Clin. Infect. Dis. 52(5), E121-E126 (2011).
15. Pongsiri P, Auksornkitti V, Theamboonlers A, Luplertlop N, Rianthavorn P, Poovorawan Y. Entire genome characterization of Chikungunya virus from the 2008-2009 outbreaks in Thailand. Trop. Biomed. 27(2), 167-176 (2010).
16. Sam IC, Kamarulzaman A, Ong GS et al. Chikungunya virus-associated death in Malaysia. Trop. Biomed. 27(2), 343-347 (2010).
17. Rivas F, Diaz LA, Cardenas VM et al. Epidemic Venezuelan equine encephalitis in La Guajira, Colombia, 1995. J. Infect. Dis. 175(4), 828-832 (1997).
18. Her Z, Kam Y-W, Lin RTP, Ng LFP. Chikungunya: a bending reality. Microbes Infect. 11(14-15), 1165-1176 (2009).
19. Outbreak and spread of chikungunya. Wkly Epidemiol. Rec. 82(47), 409-415 (2007).
20. Paessler S, Weaver SC. Vaccines for Venezuelan equine encephalitis. Vaccine 27(Suppl. 4), D80-D85 (2009).
21. Griffin DE. Alphaviruses. In: Fields Virology. Knipe DM (Ed.).Lippincott Williams and Wilkins, PA, USA, 1023-1059 (2007).
22. Queyriaux B, Simon F, Grandadam M, Michel R, Tolou H, Boutin JP. Clinical burden of Chikungunya virus infection. Lancet Infect. Dis. 8(1), 2-3 (2008).
23. Sissoko D, Moendandze A, Malvy D et al. Seroprevalence and risk factors of chikungunya virus infection in Mayotte, Indian Ocean, 2005-2006: a population-based survey. PLoS One 3(8), E3066 (2008).
24. Jacups SP, Whelan PI, Currie BJ. Ross River virus and Barmah Forest virus infections: a review of history, ecology, and predictive models, with implications for tropical northern Australia. Vector Borne Zoonotic Dis. 8(2), 283-297 (2008).
25. Couderc T, Lecuit M. Focus on Chikungunya pathophysiology in human and animal models. Microbes Infect. 11(14-15), 1197-1205 (2009).
26. Fraser JR. Epidemic polyarthritis and Ross River virus disease. Clin. Rheum. Dis. 12(2), 369-388 (1986).
27. Harley D, Bossingham D, Purdie DM, Pandeya N, Sleigh AC. Ross River virus disease in tropical Queensland: evolution of rheumatic manifestations in an inception cohort followed for six months. Med. J. Aust. 177(7), 352-355 (2002).
28. Harley D, Sleigh A, Ritchie S. Ross River virus transmission, infection, and disease: a cross-disciplinary review. Clin. Microbiol. Rev. 14(4), 909-932, table of contents (2001).
29. Jaffar-Bandjee MC, Das T, Hoarau JJ et al. Chikungunya virus takes centre stage in virally induced arthritis: possible cellular and molecular mechanisms to pathogenesis. Microbes Infect. 11(14-15), 1206-1218 (2009).
30. Laine M, Luukkainen R, Toivanen A. Sindbis viruses and other alphaviruses as cause of human arthritic disease. J. Intern. Med. 256(6), 457-471 (2004).
31. Simon F, Parola P, Grandadam M et al. Chikungunya infection: an emerging rheumatism among travelers returned from Indian Ocean islands. Report of 47 cases. Medicine (Baltimore) 86(3), 123-137 (2007).
32. Parola P, Simon F, Oliver M. Tenosynovitis and vascular disorders associated with Chikungunya virus-related rheumatism. Clin. Infect. Dis. 45(6), 801-802 (2007).
33. Mylonas AD, Brown AM, Carthew TL et al. Natural history of Ross River virus-induced epidemic polyarthritis. Med. J. Aust. 177(7), 356-360 (2002).
34. Laine M, Luukkainen R, Jalava J, Ilonen J, Kuusisto P, Toivanen A. Prolonged arthritis associated with sindbis-related (Pogosta) virus infection. Rheumatology (Oxford) 39(11), 1272-1274 (2000).
35. Earnest MP, Goolishian HA, Calverley JR, Hayes RO, Hill HR. Neurologic, intellectual, and psychologic sequelae following western encephalitis. A follow-up study of 35 cases. Neurology 21(9), 969-974 (1971).
36. Deresiewicz RL, Thaler SJ, Hsu L, Zamani AA. Clinical and neuroradiographic manifestations of eastern equine encephalitis. N. Engl. J. Med. 336(26), 1867-1874 (1997).
37. Johnson KM, Martin DH. Venezuelan equine encephalitis. Adv. Vet. Sci. Comp. Med. 18(0), 79-116 (1974).
38. Reed DS, Larsen T, Sullivan LJ et al. Aerosol exposure to western equine encephalitis virus causes fever and encephalitis in cynomolgus macaques. J. Infect. Dis. 192(7), 1173-1182 (2005).
39. Paredes AM, Simon MN, Brown DT. The mass of the Sindbis virus nucleocapsid suggests it has T = 4 icosahedral symmetry. Virology 187(1), 329-332 (1992).
40. Migliaccio G, Castagnola P, Leone A, Cerasuolo A, Bonatti S. mRNA activity of a Sindbis virus defective-interfering RNA. J. Virol. 55(3), 877-880 (1985).
41. Katz D, Straussman Y. Evaluation of immunoadsorbent electron microscopic techniques for detection of Sindbis virus. J. Virol. Methods 8(3), 243-254 (1984).
42. Firth AE, Chung BY, Fleeton MN, Atkins JF. Discovery of frameshifting in Alphavirus 6K resolves a 20 year enigma. Virol. J. 5, 108 (2008).
43. Ou JH, Rice CM, Dalgarno L, Strauss EG, Strauss JH. Sequence studies of several alphavirus genomic RNAs in the region containing the start of the subgenomic RNA. Proc. Natl Acad. Sci. USA 79(17), 5235-5239 (1982).
44. Holland J, Domingo E. Origin and evolution of viruses. Virus Genes 16(1), 13-21 (1998).
45. Steinhauer DA, Domingo E, Holland JJ. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122(2), 281-288 (1992).
46. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 422(6927), 37-44 (2003).
47. Li G, Rice CM. The signal for translational readthrough of a UGA codon in Sindbis virus RNA involves a single cytidine residue immediately downstream of the termination codon. J. Virol. 67(8), 5062-5067 (1993).
48. Myles KM, Kelly CL, Ledermann JP, Powers AM. Effects of an opal termination codon preceding the nsP4 gene sequence in the O'Nyong-Nyong virus genome on Anopheles gambiae infectivity. J. Virol. 80(10), 4992-4997 (2006).
49. De Groot RJ, Hardy WR, Shirako Y, Strauss JH. Cleavage-site preferences of Sindbis virus polyproteins containing the non-structural proteinase. Evidence for temporal regulation of polyprotein processing in vivo. EMBO J. 9(8), 2631-2638 (1990).
50. Shirako Y, Strauss JH. Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis. J. Virol. 68(3), 1874-1885 (1994).
51. Ahola T, Laakkonen P, Vihinen H, Kaariainen L. Critical residues of Semliki Forest virus RNA capping enzyme involved in methyltransferase and guanylyltransferase-like activities. J. Virol. 71(1), 392-397 (1997).
52. Ahola T, Kaariainen L. Reaction in alphavirus mRNA capping: formation of a covalent complex of nonstructural protein nsP1 with 7-methyl-GMP. Proc. Natl Acad. Sci. USA 92(2), 507-511 (1995).
53. Sawicki DL, Perri S, Polo JM, Sawicki SG. Role for nsP2 proteins in the cessation of alphavirus minus-strand synthesis by host cells. J. Virol. 80(1), 360-371 (2006).
54. Varjak M, Zusinaite E, Merits A. Novel functions of the alphavirus nonstructural protein nsP3 C-terminal region. J. Virol. 84(5), 2352-2364 (2010).
55. Lastarza MW, Lemm JA, Rice CM. Genetic analysis of the nsP3 region of Sindbis virus: evidence for roles in minus-strand and subgenomic RNA synthesis. J. Virol. 68(9), 5781-5791 (1994).
56. Wang YF, Sawicki SG, Sawicki DL. Alphavirus nsP3 functions to form replication complexes transcribing negative-strand RNA. J. Virol. 68(10), 6466-6475 (1994).
57. Rupp JC, Jundt N, Hardy RW. Requirement for the amino-terminal domain of sindbis virus nsP4 during virus infection. J. Virol. 85(7), 3449-3460 (2011).
58. Aliperti G, Schlesinger MJ. Evidence for an autoprotease activity of sindbis virus capsid protein. Virology 90(2), 366-369 (1978).
59. Frolova E, Frolov I, Schlesinger S. Packaging signals in alphaviruses. J. Virol. 71(1), 248-258 (1997).
60. Kim DY, Firth AE, Atasheva S, Frolova EI, Frolov I. Conservation of a packaging signal and the viral genome RNA packaging mechanism in alphavirus evolution. J. Virol. 85(16), 8022-8036 (2011).
61. Garoff H, Huylebroeck D, Robinson A, Tillman U, Liljestrom P. The signal sequence of the p62 protein of Semliki Forest virus is involved in initiation but not in completing chain translocation. J. Cell Biol. 111(3), 867-876 (1990).
62. Sariola M, Saraste J, Kuismanen E. Communication of post-Golgi elements with early endocytic pathway: regulation of endoproteolytic cleavage of Semliki Forest virus p62 precursor. J. Cell Sci. 108(Pt 6), 2465-2475 (1995).
63. De Curtis I, Simons K. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl Acad. Sci. USA 85(21), 8052-8056 (1988).
64. Ziemiecki A, Garoff H, Simons K. Formation of the Semliki Forest virus membrane glycoprotein complexes in the infected cell. J. Gen. Virol. 50(1), 111-123 (1980).
65. Weaver SC, Hagenbaugh A, Bellew LA et al. A comparison of the nucleotide sequences of eastern and western Equine encephalomyelitis viruses with those of other alphaviruses and related RNA viruses. Virology 197(1), 375-390 (1993).
66. Luers AJ, Adams SD, Smalley JV, Campanella JJ. A phylogenomic study of the genus Alphavirus employing whole genome comparison. Comp. Funct. Genomics 6(4), 217-227 (2005).
67. Cilnis MJ, Kang W, Weaver SC. Genetic conservation of Highlands J viruses. Virology 218(2), 343-351 (1996).
68. Parrott MM, Sitarski SA, Arnold RJ, Picton LK, Hill RB, Mukhopadhyay S. Role of conserved cysteines in the alphavirus E3 protein. J. Virol. 83(6), 2584-2591 (2009).
69. George J, Raju R. Alphavirus RNA genome repair and evolution: molecular characterization of infectious sindbis virus isolates lacking a known conserved motif at the 3′ end of the genome. J. Virol. 74(20), 9776-9785 (2000).
70. Rausalu K, Iofik A, Ulper L, Karo-Astover L, Lulla V, Merits A. Properties and use of novel replication-competent vectors based on Semliki Forest virus. Virol. J. 6, 33 (2009).
71. Jones A, Lowry K, Aaskov J, Holmes EC, Kitchen A. Molecular evolutionary dynamics of Ross River virus and implications for vaccine efficacy. J. Gen. Virol. 91(1), 182-188 (2010).
72. Arrigo NC, Adams AP, Weaver SC. Evolutionary patterns of eastern equine encephalitis virus in North versus South America suggest ecological differences and taxonomic revision. J. Virol. 84(2), 1014-1025 (2010).
73. Sherman MB, Weaver SC. Structure of the recombinant alphavirus western equine encephalitis virus revealed by cryoelectron microscopy. J. Virol. 84(19), 9775-9782 (2010).
74. Sammels LM, Lindsay MD, Poidinger M, Coelen RJ, Mackenzie JS. Geographic distribution and evolution of Sindbis virus in Australia. J. Gen. Virol. 80(3), 739-748 (1999).
75. Mackenzie JS, Smith DW. Mosquito-borne viruses and epidemic polyarthritis. Med. J. Aust. 164(2), 90-93 (1996).
76. Schilte C, Couderc T, Chretien F et al. Type I IFN controls chikungunya virus via its action on nonhematopoietic cells. J. Exp. Med. 207(2), 429-442 (2010).
77. Mccartney SA, Colonna M. Viral sensors: diversity in pathogen recognition. Immunol. Rev. 227(1), 87-94 (2009).
78. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8(8), 594-606 (2008).
79. O'Neill LA, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7(5), 353-364 (2007).
80. Haller O, Frese M, Kochs G. Mx proteins: mediators of innate resistance to RNA viruses. Rev. Sci. Tech. 17(1), 220-230 (1998).
81. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 147(927), 258-267 (1957).
82. He Y, Katze MG. To interfere and to anti-interfere: the interplay between hepatitis C virus and interferon. Viral Immunol. 15(1), 95-119 (2002).
83. Tan SL, Katze MG. How hepatitis C virus counteracts the interferon response: the jury is still out on NS5A. Virology 284(1), 1-12 (2001).
84. Taylor DR. Hepatitis C virus and interferon resistance: it's more than just PKR. Hepatology 33(6), 1547-1549 (2001).
85. Ankel H, Westra DF, Welling-Wester S, Lebon P. Induction of interferon-alpha by glycoprotein D of herpes simplex virus: a possible role of chemokine receptors. Virology 251(2), 317-326 (1998).
86. Ryman KD, Klimstra WB. Host responses to alphavirus infection. Immunol. Rev. 225, 27-45 (2008).
87. Breakwell L, Dosenovic P, Karlsson Hedestam GB et al. Semliki Forest virus nonstructural protein 2 is involved in suppression of the type I interferon response. J. Virol. 81(16), 8677-8684 (2007).
88. Simmons JD, Wollish AC, Heise MT. A determinant of Sindbis virus neurovirulence enables efficient disruption of Jak/STAT signaling. J. Virol. 84(21), 11429-11439 (2010).
89. Fros JJ, Liu WJ, Prow NA et al. Chikungunya virus nonstructural protein 2 inhibits type I/II interferon-stimulated JAK-STAT signaling. J. Virol. 84(20), 10877-10887 (2010).
90. Aguilar PV, Weaver SC, Basler CF. Capsid protein of eastern equine encephalitis virus inhibits host cell gene expression. J. Virol. 81(8), 3866-3876 (2007).
91. Garmashova N, Atasheva S, Kang W, Weaver SC, Frolova E, Frolov I. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 81(24), 13552-13565 (2007).
92. Shabman RS, Morrison TE, Moore C et al. Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alphaviruses. J. Virol. 81(1), 237-247 (2007).
93. Lidbury BA, Rulli NE, Musso CM et al. Identification and characterization of a ross river virus variant that grows persistently in macrophages, shows altered disease kinetics in a mouse model, and exhibits resistance to type I interferon. J. Virol. 85(11), 5651-5663 (2011).
94. Jupille HJ, Oko L, Stoermer KA et al. Mutations in nsP1 and PE2 are critical determinants of Ross River virus-induced musculoskeletal inflammatory disease in a mouse model. Virology 410(1), 216-227 (2011).
95. Weaver SC. Host range, amplification and arboviral disease emergence. Arch. Virol. Suppl. (19), 33-44 (2005).
96. Fragkoudis R, Attarzadeh-Yazdi G, Nash AA, Fazakerley JK, Kohl A. Advances in dissecting mosquito innate immune responses to arbovirus infection. J. Gen. Virol. 90(Pt 9), 2061-2072 (2009).
97. Siu RW, Fragkoudis R, Simmonds P et al. Antiviral RNA interference responses induced by Semliki Forest virus infection of mosquito cells: characterization, origin, and frequency-dependent functions of virus-derived small interfering RNAs. J. Virol. 85(6), 2907-2917 (2011).
98. Renault P, Solet JL, Sissoko D et al. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005-2006. Am. J. Trop. Med. Hyg. 77(4), 727-731 (2007).
99. Win MK, Chow A, Dimatatac F, Go CJ, Leo YS. Chikungunya fever in Singapore: acute clinical and laboratory features, and factors associated with persistent arthralgia. J. Clin. Virol. 49(2), 111-114 (2010).
100. Simon F, Savini H, Parola P. Chikungunya: a paradigm of emergence and globalization of vector-borne diseases. Med. Clin. North Am. 92(6), 1323-1343, IX (2008).
101. Ng LC, Hapuarachchi HC. Tracing the path of Chikungunya virus - evolution and adaptation. Infect. Genet. Evol. 10(7), 876-885 (2010).
102. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 3(12), E201 (2007).
103. Rico-Hesse R, Roehrig JT, Trent DW, Dickerman RW. Genetic variation of Venezuelan equine encephalitis virus strains of the ID variety in Colombia. Am. J. Trop. Med. Hyg. 38(1), 195-204 (1988).
104. Brault AC, Powers AM, Holmes EC, Woelk CH, Weaver SC. Positively charged amino acid substitutions in the E2 envelope glycoprotein are associated with the emergence of venezuelan equine encephalitis virus. J. Virol. 76(4), 1718-1730 (2002).
105. Greene IP, Paessler S, Austgen L et al. Envelope glycoprotein mutations mediate equine amplification and virulence of epizootic venezuelan equine encephalitis virus. J. Virol. 79(14), 9128-9133 (2005).
106. Byrnes AP, Griffin DE. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72(9), 7349-7356 (1998).
107. Chen Y, Maguire T, Hileman RE et al. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3(8), 866-871 (1997).
108. Zhu W, Wang L, Yang Y et al. Interaction of E2 glycoprotein with heparan sulfate is crucial for cellular infection of Sindbis virus. PLoS One 5(3), E9656 (2010).
109. Gardner CL, Ebel GD, Ryman KD, Klimstra WB. Heparan sulfate binding by natural eastern equine encephalitis viruses promotes neurovirulence. Proc. Natl Acad. Sci. USA 108(38), 16026-16031 (2011).
110. Atkins GJ, Fleeton MN, Sheahan BJ. Therapeutic and prophylactic applications of alphavirus vectors. Expert Rev. Mol. Med. 10, 1-18 (2008).
111. Quetglas JI, Ruiz-Guillen M, Aranda A, Casales E, Bezunartea J, Smerdou C. Alphavirus vectors for cancer therapy. Virus Res. 153(2), 179-196 (2010).
112. Viru L, Heller G, Lehto T et al. Novel viral vectors utilizing intron splice-switching to activate genome rescue, expression and replication in targeted cells. Virol. J. 8, 243 (2011).
113. Lundstrom K. Expression of mammalian membrane proteins in mammalian cells using Semliki Forest virus vectors. In: Heterologous Expression of Membrane Proteins. Mus-Veteau I (Ed.).Humana Press, NY, USA, 149-163 (2010).
114. Spuul P, Balistreri G, Hellstrom K, Golubtsov AV, Jokitalo E, Ahola T. Assembly of alphavirus replication complexes from RNA and protein components in a novel trans-replication system in mammalian cells. J. Virol. 85(10), 4739-4751 (2011).
115. Casales E, Aranda A, Quetglas JI et al. A novel system for the production of high levels of functional human therapeutic proteins in stable cells with a Semliki Forest virus noncytopathic vector. New Biotechnol. 27(2), 138-148 (2010).
116. Roche FP, Sheahan BJ, O'Mara SM, Atkins GJ. Semliki Forest virus-mediated gene therapy of the RG2 rat glioma. Neuropathol. Appl. Neurobiol. 36(7), 648-660 (2010).
117. Yamaguchi Y, Shirako Y. Engineering of a Sagiyama alphavirus RNA-based transient expression vector. Microbiol. Immunol. 46(2), 119-129 (2002).
118. Vanlandingham DL, Tsetsarkin K, Hong C et al. Development and characterization of a double subgenomic chikungunya virus infectious clone to express heterologous genes in Aedes aegypti mosqutioes. Insect Biochem. Mol. Biol. 35(10), 1162-1170 (2005).
119. Smerdou C, Liljestrom P. Two-helper RNA system for production of recombinant Semliki Forest virus particles. J. Virol. 73(2), 1092-1098 (1999).
120. Quetglas JI, Fioravanti J, Ardaiz N et al. A Semliki Forest virus vector engineered to express IFN[alpha] induces efficient elimination of established tumors. Gene Ther. doi:10.1038/gt.2011.99 (2011) (Epub ahead of print).
121. Zhang J, Asselin-Paturel C, Bex F et al. Cloning of human IL-12 p40 and p35 DNA into the Semliki Forest virus vector: expression of IL-12 in human tumor cells. Gene Ther. 4(4), 367-374 (1997).
122. Chikkanna-Gowda CP, Mcnally S, Sheahan BJ, Fleeton MN, Atkins GJ. Inhibition of murine K-BALB and CT26 tumour growth using a Semliki Forest virus vector with enhanced expression of IL-18. Oncol. Rep. 16(4), 713-719 (2006).
123. Forsell MNE, Mcinerney GM, Dosenovic P et al. Increased human immunodeficiency virus type 1 Env expression and antibody induction using an enhanced alphavirus vector. J. Gen. Virol. 88(10), 2774-2779 (2007).
124. Tsetsarkin K, Higgs S, Mcgee CE, Lamballerie XD, Charrel RN, Vanlandingham DL. Infectious clones of Chikungunya virus (La Réunion isolate) for vector competence studies. Vector Borne Zoonotic Dis. 6(4), 325-337 (2006).
125. Barry G, Fragkoudis R, Ferguson MC et al. Semliki Forest virus-induced endoplasmic reticulum stress accelerates apoptotic death of mammalian cells. J. Virol. 84(14), 7369-7377 (2010).
126. Dubensky T Jr, Driver D, Polo J et al. Sindbis virus DNA-based expression vectors: utility for in vitro and in vivo gene transfer. J. Virol. 70(1), 508-519 (1996).
127. Boorsma M, Saudan P, Pfruender H et al. Alphavirus cDNA-based expression vectors: Effects of RNA transcription and nuclear export. Biotechnol. Bioeng. 81(5), 553-562 (2003).
128. Griffith IP, Crook NE, White DO. Protection of mice against cancer by immunization with membranes but not purified virions from virus infected cancer cells. Br. J. Cancer 31(6), 603-613 (1975).
129. Ying H, Zaks TZ, Wang R-F et al. Cancer therapy using a self-replicating RNA vaccine. Nat. Med. 5(7), 823-827 (1999).
130. Tseng J-C, Levin B, Hurtado A et al. Systemic tumor targeting and killing by Sindbis viral vectors. Nat. Biotech. 22(1), 70-77 (2004).
131. Riezebos-Brilman A, Walczak M, Regts J et al. A comparative study on the immunotherapeutic efficacy of recombinant Semliki Forest virus and adenovirus vector systems in a murine model for cervical cancer. Gene Ther. 14(24), 1695-1704 (2007).