Genetic variation in vitro and in vivo of an attenuated lassa vaccine candidate

Journal of Virology

Volumn 88, Issue 6, 2014, Pages 3058-3066

  Zapata, Juan C ^a   Goicochea, Marco ^a   Nadai, Yuka ^a   Eyzaguirre, Lindsay M ^a   Carr, Jean K ^a   Tallon, Luke J ^a   Sadzewicz, Lisa ^a   Myers, Garry ^a   Fraser, Claire M ^a   Su, Qi ^a   Djavani, Mahmoud ^a   Lukashevich, Igor S ^a,b   Salvato, Maria S ^a  

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

^b UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIVE VACCINE; MOPEIA LASSA CLONE 29 VACCINE; UNCLASSIFIED DRUG; VIRUS VACCINE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARENAVIRUS; ARTICLE; CALLITRICHINAE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; GENE LOCUS; GENE MUTATION; GENETIC VARIABILITY; GENOTYPE; HOST RANGE; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; IN VITRO STUDY; IN VIVO STUDY; LASSA VIRUS; MOPEIA VIRUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; PYROSEQUENCING; RHESUS MONKEY; SEQUENCE ANALYSIS; SIMIAN IMMUNODEFICIENCY VIRUS; SINGLE NUCLEOTIDE POLYMORPHISM; VACCINATION; VACCINE PRODUCTION; VERO CELL; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS ISOLATION; VIRUS MORPHOLOGY;

ANIMALS; CALLITHRIX; CERCOPITHECUS AETHIOPS; GENETIC VARIATION; HUMANS; IMMUNITY, CELLULAR; LASSA FEVER; LASSA VIRUS; MACACA MULATTA; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; VACCINES, ATTENUATED; VERO CELLS; VIRAL VACCINES;

EID: 84894541092     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03035-13     Document Type: Article

References (49)

1. Barton LL, Hyndman NJ. 2000. Lymphocytic choriomeningitis virus: reemerging central nervous system pathogen. Pediatrics 105:E35. http://dx.doi.org/10.1542/peds.105.3.e35.
2. Salvato MS, Clegg JCS, Buchmeier MJ, Charrel RN, Gonzalez JP, Lukashevich IS, Peters CJ, Romanowski V. 2012. Arenaviridae, p 715-723. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed). Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, CA.
3. McCormick JB. 1988. Lassa fever: epidemiology, therapy and vaccine development. Kansenshogaku Zasshi 62(Suppl):353-366.
4. McCormick JB, Fisher-Hoch SP. 2002. Lassa fever. Curr. Top. Microbiol. Immunol. 262:75-109. http://dx.doi.org/10.1007/978-3-642-56029-3_4.
5. Ogbu O, Ajuluchukwu E, Uneke CJ. 2007. Lassa fever in West African sub-region: an overview. J. Vector Borne Dis. 44:1-11.
6. Kerneis S, Koivogui L, Magassouba N, Koulemou K, Lewis R, Aplogan A, Grais RF, Guerin PJ, Fichet-Calvet E. 2009. Prevalence and risk factors of Lassa seropositivity in inhabitants of the forest region of Guinea: a cross-sectional study. PLoS Negl. Trop. Dis. 3:e548. http://dx.doi.org/10.1371/journal.pntd.0000548.
7. Fisher-Hoch SP, Tomori O, Nasidi A, Perez-Oronoz GI, Fakile Y, Hutwagner L, McCormick JB. 1995. Review of cases of nosocomial Lassa fever in Nigeria: the high price of poor medical practice. BMJ 311:857-859. http://dx.doi.org/10.1136/bmj.311.7009.857.
8. McCormick JB. 1987. Epidemiology and control of Lassa fever. Curr. Top. Microbiol. Immunol. 134:69-78.
9. Lukashevich IS. 1992. Generation of reassortants between African arenaviruses. Virology 188:600-605. http://dx.doi.org/10.1016/0042-6822(92)90514-P.
10. Lukashevich IS, Patterson J, Carrion R, Moshkoff D, Ticer A, Zapata J, Brasky K, Geiger R, Hubbard GB, Bryant J, Salvato MS. 2005. A live attenuated vaccine for Lassa fever made by reassortment of Lassa and Mopeia viruses. J. Virol. 79:13934-13942. http://dx.doi.org/10.1128/JVI.79.22.13934-13942.2005.
11. Carrion R, Jr, Bredenbeek PJ, Jiang X, Tretyakova I, Pushko P, ISL. 2012. Vaccine platforms to control arenaviral hemorrhagic fevers. J. Vaccines Vaccin. 3:1000160. http://dx.doi.org/10.4172/2157-7560.1000160.
12. Carrion R, Jr, Brasky K, Mansfield K, Johnson C, Gonzales M, Ticer A, Lukashevich I, Tardif S, Patterson J. 2007. Lassa virus infection in experimentally infected marmosets: liver pathology and immunophenotypic alterations in target tissues. J. Virol. 81:6482-6490. http://dx.doi.org/10.1128/JVI.02876-06.
13. Lukashevich IS, Carrion R, Jr, Salvato MS, Mansfield K, Brasky K, Zapata J, Cairo C, Goicochea M, Hoosien GE, Ticer A, Bryant J, Davis H, Hammamieh R, Mayda M, Jett M, Patterson J. 2008. Safety, immunogenicity, and efficacy of the ML29 reassortant vaccine for Lassa fever in small non-human primates. Vaccine 26:5246-5254. http://dx.doi.org/10.1016/j.vaccine.2008.07.057.
14. Poonia B, Salvato MS, Yagita H, Maeda T, Okumura K, Pauza CD. 2009. Treatment with anti-FasL antibody preserves memory lymphocytes and virus-specific cellular immunity in macaques challenged with simian immunodeficiency virus. Blood 114:1196-1204. http://dx.doi.org/10.1182/blood-2009-02-202655.
15. Zapata JC, Poonia B, Bryant J, Davis H, Ateh E, George L, Crasta O, Zhang Y, Slezak T, Jaing C, Pauza CD, Goicochea M, Moshkoff D, Lukashevich IS, Salvato MS. 2013. An attenuated Lassa vaccine in SIVinfected rhesus macaques does not persist or cause arenavirus disease but does elicit Lassa virus-specific immunity. Virol. J. 10:52. http://dx.doi.org/10.1186/1743-422X-10-52.
16. Moshkoff DA, Salvato MS, Lukashevich IS. 2007. Molecular characterization of a reassortant virus derived from Lassa and Mopeia viruses. Virus Genes 34:169-176. http://dx.doi.org/10.1007/s11262-006-0050-3.
17. Salvato M, Shimomaye E, Oldstone MB. 1989. The primary structure of the lymphocytic choriomeningitis virus L gene encodes a putative RNA polymerase. Virology 169:377-384. http://dx.doi.org/10.1016/0042-6822(89)90163-3.
18. Zapata JC, Salvato MS. 2013. Arenavirus variations due to host-specific adaptation. Viruses 5:241-278. http://dx.doi.org/10.3390/v5010241.
19. FDA. 2010. Guidance for industry. Characterization and qualification of cell substrates and other biological materials used in the production of viral vaccines for infectious disease indications. http://www.fda.gov/downloads/BiologicsBloodVaccines/GuidanceComplianceRegulatory Information/Guidances/Vaccines/UCM202439.pdf.
20. Cheng-Mayer C, Weiss C, Seto D, Levy JA. 1989. Isolates of human immunodeficiency virus type 1 from the brain may constitute a special group of the AIDS virus. Proc. Natl. Acad. Sci. U.S.A. 86:8575-8579. http://dx.doi.org/10.1073/pnas.86.21.8575.
21. Ahmed R, Oldstone MB. 1988. Organ-specific selection of viral variants during chronic infection. J. Exp. Med. 167:1719-1724. http://dx.doi.org/10.1084/jem.167.5.1719.
22. Trivedi P, Meyer KK, Streblow DN, Preuninger BL, Schultz KT, Pauza CD. 1994. Selective amplification of simian immunodeficiency virus genotypes after intrarectal inoculation of rhesus monkeys. J. Virol. 68:7649-7653.
23. Hall JS, French R, Hein GL, Morris TJ, Stenger DC. 2001. Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages. Virology 282:230-236. http://dx.doi.org/10.1006/viro.2001.0841.
24. Cabot B, Martell M, Esteban JI, Sauleda S, Otero T, Esteban R, Guardia J, Gomez J. 2000. Nucleotide and amino acid complexity of hepatitis C virus quasispecies in serum and liver. J. Virol. 74:805-811. http://dx.doi.org/10.1128/JVI.74.2.805-811.2000.
25. Sanjuan R, Codoner FM, Moya A, Elena SF. 2004. Natural selection and the organ-specific differentiation of HIV-1 V3 hypervariable region. Evolution 58:1185-1194. http://dx.doi.org/10.1111/j.0014-3820.2004.tb01699.x.
26. Deforges S, Evlashev A, Perret M, Sodoyer M, Pouzol S, Scoazec JY, Bonnaud B, Diaz O, Paranhos-Baccala G, Lotteau V, Andre P. 2004. Expression of hepatitis C virus proteins in epithelial intestinal cells in vivo. J. Gen. Virol. 85:2515-2523. http://dx.doi.org/10.1099/vir.0.80071-0.
27. Jelcic I, Hotz-Wagenblatt A, Hunziker A, Zur Hausen H, de Villiers EM. 2004. Isolation of multiple TT virus genotypes from spleen biopsy tissue from a Hodgkin's disease patient: genome reorganization and diversity in the hypervariable region. J. Virol. 78:7498-7507. http://dx.doi.org/10.1128/JVI.78.14.7498-7507.2004.
28. Jridi C, Martin JF, Marie-Jeanne V, Labonne G, Blanc S. 2006. Distinct viral populations differentiate and evolve independently in a single perennial host plant. J. Virol. 80:2349-2357. http://dx.doi.org/10.1128/JVI.80.5.2349-2357.2006.
29. Brown RJ, Peters PJ, Caron C, Gonzalez-Perez MP, Stones L, Ankghuambom C, Pondei K, McClure CP, Alemnji G, Taylor S, Sharp PM, Clapham PR, Ball JK. 2011. Intercompartmental recombination of HIV-1 contributes to env intrahost diversity and modulates viral tropism and sensitivity to entry inhibitors. J. Virol. 85:6024-6037. http://dx.doi.org/10.1128/JVI.00131-11.
30. Wright CF, Morelli MJ, Thebaud G, Knowles NJ, Herzyk P, Paton DJ, Haydon DT, King DP. 2011. Beyond the consensus: dissecting withinhost viral population diversity of foot-and-mouth disease virus by using next-generation genome sequencing. J. Virol. 85:2266-2275. http://dx.doi.org/10.1128/JVI.01396-10.
31. Pinschewer DD, Perez M, de la Torre JC. 2003. Role of the virus nucleoprotein in the regulation of lymphocytic choriomeningitis virus transcription and RNA replication. J. Virol. 77:3882-3887. http://dx.doi.org/10.1128/JVI.77.6.3882-3887.2003.
32. Eichler R, Strecker T, Kolesnikova L, ter Meulen J, Weissenhorn W, Becker S, Klenk HD, Garten W, Lenz O. 2004. Characterization of the Lassa virus matrix protein Z: electron microscopic study of virus-like particles and interaction with the nucleoprotein (NP). Virus Res. 100:249-255. http://dx.doi.org/10.1016/j.virusres.2003.11.017.
33. Casabona JC, Levingston Macleod JM, Loureiro ME, Gomez GA, Lopez N. 2009. The RING domain and the L79 residue of Z protein are involved in both the rescue of nucleocapsids and the incorporation of glycoproteins into infectious chimeric arenavirus-like particles. J. Virol. 83:7029-7039. http://dx.doi.org/10.1128/JVI.00329-09.
34. Shtanko O, Imai M, Goto H, Lukashevich IS, Neumann G, Watanabe T, Kawaoka Y. 2010. A role for the C terminus of Mopeia virus nucleoprotein in its incorporation into Z protein-induced virus-like particles. J. Virol. 84:5415-5422. http://dx.doi.org/10.1128/JVI.02417-09.
35. Martinez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre JC. 2006. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 80:9192-9199. http://dx.doi.org/10.1128/JVI.00555-06.
36. Martinez-Sobrido L, Emonet S, Giannakas P, Cubitt B, Garcia-Sastre A, de la Torre JC. 2009. Identification of amino acid residues critical for the anti-interferon activity of the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 83:11330-11340. http://dx.doi.org/10.1128/JVI.00763-09.
37. Hastie KM, Kimberlin CR, Zandonatti MA, MacRae IJ, Saphire EO. 2011. Structure of the Lassa virus nucleoprotein reveals a dsRNAspecific 3' to 5' exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U.S.A. 108:2396-2401. http://dx.doi.org/10.1073/pnas.1016404108.
38. Qi X, Lan S, Wang W, Schelde LM, Dong H, Wallat GD, Ly H, Liang Y, Dong C. 2010. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468:779-783. http://dx.doi.org/10.1038/nature09605.
39. Grande-Perez A, Sierra S, Castro MG, Domingo E, Lowenstein PR. 2002. Molecular indetermination in the transition to error catastrophe: systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity. Proc. Natl. Acad. Sci. U.S.A. 99:12938-12943. http://dx.doi.org/10.1073/pnas.182426999.
40. Holmes EC. 2003. Patterns of intra-and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J. Virol. 77:11296-11298. http://dx.doi.org/10.1128/JVI.77.20.11296-11298.2003.
41. Graci JD, Cameron CE. 2008. Therapeutically targeting RNA viruses via lethal mutagenesis. Future Virol. 3:553-566. http://dx.doi.org/10.2217/17460794.3.6.553.
42. Plotkin JB, Robins H, Levine AJ. 2004. Tissue-specific codon usage and the expression of human genes. Proc. Natl. Acad. Sci. U.S.A. 101:12588-12591. http://dx.doi.org/10.1073/pnas.0404957101.
43. Zhi N, Wan Z, Liu X, Wong S, Kim DJ, Young NS, Kajigaya S. 2010. Codon optimization of human parvovirus B19 capsid genes greatly increases their expression in nonpermissive cells. J. Virol. 84:13059-13062. http://dx.doi.org/10.1128/JVI.00912-10.
44. Wong EH, Smith DK, Rabadan R, Peiris M, Poon LL. 2010. Codon usage bias and the evolution of influenza A viruses. Codon usage biases of influenza virus. BMC Evol. Biol. 10:253. http://dx.doi.org/10.1186/1471-2148-10-253.
45. Pandit A, Sinha S. 2011. Differential trends in the codon usage patterns in HIV-1 genes. PLoS One 6:e28889. http://dx.doi.org/10.1371/journal.pone.0028889.
46. Pfeiffer JK, Kirkegaard K. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog. 1:e11. http://dx.doi.org/10.1371/journal.ppat.0010011.
47. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344-348. http://dx.doi.org/10.1038/nature04388.
48. Pariente N, Sierra S, Lowenstein PR, Domingo E. 2001. Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J. Virol. 75:9723-9730. http://dx.doi.org/10.1128/JVI.75.20.9723-9730.2001.
49. Crotty S, Cameron CE, Andino R. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. U.S.A. 98:6895-6900. http://dx.doi.org/10.1073/pnas.111085598.