VaxCelerate II: Rapid development of a self-assembling vaccine for Lassa fever

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 10, 2014, Pages 3022-3038

  Leblanc, Pierre ^a   Moise, Leonard ^b   Luza, Cybelle ^a   Chantaralawan, Kanawat ^a   Lezeau, Lynchy ^a   Yuan, Jianping ^a   Field, Mary ^a   Richer, Daniel ^a   Boyle, Christine ^b   Martin, William D ^b   Fishman, Jordan B ^c   Berg, Eric A ^c   Baker, David ^d   Zeigler, Brandon ^e   Mais, Dale E ^e   Taylor, William ^f   Coleman, Russell ^f   Warren, H Shaw ^a   Gelfand, Jeffrey A ^a   De Groot, Anne S ^b   Brauns, Timothy ^a   Poznansky, Mark C ^a   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b EpiVax Inc   (United States)

^c 21st Century Biochemicals   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e MPI RESEARCH   (United States)

^f Pfenex Inc   (United States)

Author keywords

Arenavirus; Emerging infectious diseases; Flu vaccine; Lassa fever virus; Mycobacterium tuberculosis heat shock protein 70; Peptide design; Self assembled vaccine; Vaccine; VaxCelerate

Indexed keywords

AVIDIN; GAMMA INTERFERON; HEAT SHOCK PROTEIN 70; HLA DR3 ANTIGEN; HYBRID PROTEIN; INFLUENZA VACCINE; OVALBUMIN; SELF ASSEMBLING VACCINE; UNCLASSIFIED DRUG; VIRUS VACCINE; BACTERIAL PROTEIN; HSP70 PROTEIN, MYCOBACTERIUM TUBERCULOSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; BIOINFORMATICS; BIOTINYLATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG DESIGN; DRUG EFFICACY; DRUG SAFETY; DRUG SYNTHESIS; GOOD LABORATORY PRACTICE; GOOD MANUFACTURING PRACTICE; IMMUNOGENICITY; IMMUNOSTIMULATION; LASSA FEVER; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN ENGINEERING; PROTEIN SYNTHESIS; RELIABILITY; REPRODUCIBILITY; REVIEW; ANIMAL; C57BL MOUSE; COMMUNICABLE DISEASES, EMERGING; FEMALE; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); LASSA VIRUS; TRANSGENIC MOUSE;

ANIMALS; AVIDIN; BACTERIAL PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; COMMUNICABLE DISEASES, EMERGING; FEMALE; HLA-DR3 ANTIGEN; HSP70 HEAT-SHOCK PROTEINS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERFERON-GAMMA; LASSA FEVER; LASSA VIRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYCOBACTERIUM TUBERCULOSIS; OVALBUMIN; PROTEIN ENGINEERING; RECOMBINANT FUSION PROTEINS; VIRAL VACCINES;

EID: 84921297531     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.34413     Document Type: Review

References (81)

1. Biological Advanced Research and Development Authority. BARDA Strategic Plan 2011-2016. 2011:1-20
2. Hayden EC. The price of protection. Nature 2011; 477:150-2; PMID:21900990; http://dx.doi.org/10.1038/477150a
3. Roux D, Pier GB, Skurnik D. Magic bullets for the 21st century: the reemergence of immunotherapy for multi- and pan-resistant microbes. J Antimicrob Chemother 2012; 67:2785-7; PMID:22899807; http://dx.doi.org/10.1093/jac/dks335
4. Gronvall GK, Rambhia KJ, Adalja A, Cicero A, Inglesby T, Kadlec R. Next-generation monoclonal antibodies: Challenges and opportunities. 2013; Available from: http://www.upmc-biosecurity.org/website/resources/publications/2013/2013-02-04-next-gen-monoclonal-antibodies.html.
5. Leblanc PR, Yuan J, Brauns T, Gelfand JA, Poznansky MC. Accelerated vaccine development against emerging infectious diseases. Hum Vaccin Immunother 2012; 8:1010-2; PMID:22777091; http://dx.doi.org/10.4161/hv.20805
6. Wang Y, Kelly CG, Karttunen JT, Whittall T, Lehner PJ, Duncan L, MacAry P, Younson JS, Singh M, Oehlmann W, et al. CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 2001; 15:971-83; http://dx.doi.org/10.1016/S1074-7613(01)00242-4
7. Floto RA, MacAry PA, Boname JM, Mien TS, Kampmann B, Hair JR, Huey OS, Houben ENG, Pieters J, Day C, et al. Dendritic cell stimulation by mycobacterial Hsp70 is mediated through CCR5. Science [Internet] 2006; 314:454-8. Available from: https://phsexchweb.partners.org/exchange/PLEBLANC/Inbox/FW:%20needed%20PDFs.EML/science2006.pdf/C58EA28C-18C0-4a97-9AF2-036E93DDAFB3/science2006.pdf?attach=1; PMID:17053144; http://dx.doi.org/10.1126/science.1133515
8. Vorobiev DS, Kiselevskii MV, Chikileva IO, Semenova IB. Effect of recombinant heat shock protein 70 of mycobacterial origin on cytotoxic activity and immunophenotype of human peripheral blood mononuclear leukocytes. Bull Exp Biol Med 2009; 148:64-7; Bull Exp Biol Med 2009; 148:64-7; PMID:19902099
9. Mizukami S, Kajiwara C, Tanaka M, Kaisho T, Udono H. Differential MyD88/IRAK4 requirements for cross-priming and tumor rejection induced by heat shock protein 70-model antigen fusion protein. Cancer Sci 2012; 103:851-9; PMID:22320267; http://dx.doi.org/10.1111/j.1349-7006.2012.02233.x
10. Richmond JK, Baglole DJ. Lassa fever: epidemiology, clinical features, and social consequences. BMJ 2003; 327:1271-5; PMID:14644972; http://dx.doi.org/10.1136/bmj.327.7426.1271
11. Ölschläger S, Flatz L. Vaccination Strategies against Highly Pathogenic Arenaviruses: The Next Steps toward Clinical Trials. PLoS Pathog 2013; 9: e1003212; http://dx.doi.org/10.1371/journal.ppat.1003212
12. Hensley LE, Smith MA, Geisbert JB, Fritz EA, Daddario-DiCaprio KM, Larsen T, Geisbert TW. Pathogenesis of Lassa fever in cynomolgus macaques. Virol J 2011; 8:205; PMID:21548931; http://dx.doi.org/10.1186/1743-422X-8-205
13. Jahrling PB. Protection of Lassa virus-infected guinea pigs with Lassa-immune plasma of guinea pig, primate, and human origin. J Med Virol 1983; 12:93-102; http://dx.doi.org/10.1002/jmv.1890120203
14. Morrison HG, Bauer SP, Lange JV, Esposito JJ, McCormick JB, Auperin DD. Protection of guinea pigs from Lassa fever by vaccinia virus recombinants expressing the nucleoprotein or the envelope glycoproteins of Lassa virus. Virology 1989; 171:179-88; http://dx.doi.org/10.1016/0042-6822(89)90525-4
15. Fisher-Hoch SP, Hutwagner L, Brown B, McCormick JB. Effective vaccine for lassa fever. J Virol 2000; 74:6777-83; http://dx.doi.org/10.1128/JVI.74.15.6777-6783.2000
16. Botten J, Alexander J, Pasquetto V, Sidney J, Barrowman P, Ting J, Peters B, Southwood S, Stewart B, Rodriguez-Carreno MP, et al. Identification of protective lassa virus epitopes that are restricted by HLA-A2. J Virol 2006; 80:8351-61; PMID:16912286; http://dx.doi.org/10.1128/JVI.00896-06
17. Clegg JC, Lloyd G. Structural and cell-associated proteins of Lassa virus. J Gen Virol 1983; 64:1127-36; http://dx.doi.org/10.1099/0022-1317-64-5-1127
18. Bishop DH, Auperin DD. Arenavirus gene structure and organization. Curr Top Microbiol Immunol 1987; 133:5-17; PMID:2435460
19. Botten J, Whitton JL, Barrowman P, Sidney J, Whitmire JK, Alexander J, Kotturi MF, Sette A, Buchmeier MJ. A multivalent vaccination strategy for the prevention of Old World arenavirus infection in humans. J Virol 2010; 84:9947-56; PMID:20668086; http://dx.doi.org/10.1128/JVI.00672-10
20. Badger CV, Guttieri MC, Sardesai NY, Schmaljohn CS. Enhanced efficacy of a codon-optimized DNA vaccine encoding the glycoprotein precursor gene of Lassa virus in a guinea pig disease model when delivered by . . .. Vaccines 2013
21. Rötzschke O, Falk K, Stevanović S, Jung G, Walden P, Rammensee HG. Exact prediction of a natural T cell epitope. Eur J Immunol 1991; 21:2891-4; PMID:1718764; http://dx.doi.org/10.1002/eji.1830211136
22. Lipford GB, Hoffman M, Wagner H, Heeg K. Primary in vivo responses to ovalbumin. Probing the predictive value of the Kb binding motif. J Immunol 1993; 150:1212-22; PMID:7679422
23. Moise L, Tassone R, Latimer H, Terry F, Levitz L, Haran JP, Ross TM, Boyle CM, Martin WD, De Groot AS. Immunization with cross-conserved H1N1 influenza CD4+ T-cell epitopes lowers viral burden in HLA DR3 transgenic mice. Hum Vaccin Immunother 2013; 9:2060-8; PMID:24045788; http://dx.doi.org/10.4161/hv.26511
24. Moise L, McMurry JA, Buus S, Frey S, Martin WD, De Groot AS. In silico-accelerated identification of conserved and immunogenic variola/vaccinia T-cell epitopes. Vaccine 2009; 27:6471-9; PMID:19559119; http://dx.doi.org/10.1016/j.vaccine.2009.06.018
25. Spiering R, van der Zee R, Wagenaar J, Van Eden W, Broere F. Mycobacterial and mouse HSP70 have immuno-modulatory effects on dendritic cells. Cell Stress Chaperones 2013; 18:439-46; PMID:23269491; http://dx.doi.org/10.1007/s12192-012-0397-4
26. Borges TJ, Wieten L, van Herwijnen MJC, Broere F, van der Zee R, Bonorino C, van Eden W. The anti-inflammatory mechanisms of Hsp70. Front Immunol 2012; 3:95; PMID:22566973; http://dx.doi.org/10.3389/fimmu.2012.00095
27. Arribillaga L, Durantez M, Lozano T, Rudilla F, Rehberger F, Casares N, Villanueva L, Martinez M, Gorraiz M, Borrás-Cuesta F, et al. A fusion protein between streptavidin and the endogenous TLR4 Ligand EDA targets biotinylated antigens to dendritic cells and induces T cell responses in vivo. Biomed Res Int 2013; 2013:864720; PMID:24093105; http://dx.doi.org/10.1155/2013/864720
28. Carbone FR, Bevan MJ. Induction of ovalbumin-specific cytotoxic T cells by in vivo peptide immunization. J Exp Med 1989; 169:603-12; http://dx.doi.org/10.1084/jem.169.3.603
29. Huang Q, Richmond JFL, Suzue K, Eisen H, Young R. In vivo cytotoxic T lymphocyte elicitation by mycobacterial heat shock protein 70 fusion proteins maps to a discrete domain and is CD4+ T cell independent. J Exp Med 2000; 191:403-8; http://dx.doi.org/10.1084/jem.191.2.403
30. Suzue K, Zhou X, Eisen HN, Young RA. Heat shock fusion proteins as vehicles for antigen delivery into the major histocompatibility complex class I presentation pathway. Proc Natl Acad Sci USA 1997; 94:13146-51; http://dx.doi.org/10.1073/pnas.94.24.13146
31. Del Val M, Iborra S, Ramos M, Lázaro S. Generation of MHC class I ligands in the secretory and vesicular pathways. Cell Mol Life Sci 2011; 68:1543-52; PMID:21387141; http://dx.doi.org/10.1007/s00018-011-0661-2
32. Gil-Torregrosa BC, Raúl Castaño A, Del Val M. Major histocompatibility complex class I viral antigen processing in the secretory pathway defined by the trans-Golgi network protease furin. J Exp Med 1998; 188:1105-16; http://dx.doi.org/10.1084/jem.188.6.1105
33. Gil-Torregrosa BC, Castaño AR, López D, Del Val M. Generation of MHC class I peptide antigens by protein processing in the secretory route by furin. Traffic 2000; 1:641-51; http://dx.doi.org/10.1034/j.1600-0854.2000.010808.x
34. Medina F, Ramos M, Iborra S, de León P, Rodríguez-Castro M, Del Val M. Furin-processed antigens targeted to the secretory route elicit functional TAP1-/- CD8+ T lymphocytes in vivo. J Immunol 2009; 183:4639-47; http://dx.doi.org/10.4049/jimmunol.0901356
35. Lu J, Higashimoto Y, Appella E, Celis E. Multiepitope Trojan antigen peptide vaccines for the induction of antitumor CTL and Th immune responses. J Immunol 2004; 172:4575-82; http://dx.doi.org/10.4049/jimmunol.172.7.4575
36. Haug M, Dannecker L, Schepp CP, Kwok WW, Wernet D, Buckner JH, Kalbacher H, Dannecker GE, Holzer U. The heat shock protein Hsp70 enhances antigen-specific proliferation of human CD4+ memory T cells. Eur J Immunol 2005; 35:3163-72; PMID:16245362; http://dx.doi.org/10.1002/eji.2005-35050
37. Haug M, Schepp CP, Kalbacher H, Dannecker GE, Holzer U. 70-kDa heat shock proteins: specific interactions with HLA-DR molecules and their peptide fragments. Eur J Immunol 2007; 37:1053-63; PMID:17357109; http://dx.doi.org/10.1002/eji.200-636811
38. Fischer N, Haug M, Kwok WW, Kalbacher H, Wernet D, Dannecker GE, Holzer U. Involvement of CD91 and scavenger receptors in Hsp70-facilitated activation of human antigen-specific CD4+ memory T cells. Eur J Immunol 2010; 40:986-97; PMID:20101615; http://dx.doi.org/10.1002/eji.200939738
39. Soloway P, Fish S, Passmore H, Gefter M, Coffee R, Manser T. Regulation of the immune response to peptide antigens: differential induction of immediate-type hypersensitivity and T cell proliferation due to changes in either peptide structure or major histocompatibility complex haplotype. J Exp Med 1991; 174:847-58; http://dx.doi.org/10.1084/jem.174.4.847
40. La Rosa C, Wang Z, Brewer JC, Lacey SF, Villacres MC, Sharan R, Krishnan R, Crooks M, Markel S, Maas R, et al. Preclinical development of an adjuvant-free peptide vaccine with activity against CMV pp65 in HLA transgenic mice. Blood 2002; 100:3681-9; PMID:12393676; http://dx.doi.org/10.1182/blood-2002-03-0926
41. La Rosa C, Longmate J, Lacey SF, Kaltcheva T, Sharan R, Marsano D, Kwon P, Drake J, Williams B, Denison S, et al. Clinical evaluation of safety and immunogenicity of PADRE-cytomegalovirus (CMV) and tetanus-CMV fusion peptide vaccines with or without PF03512676 adjuvant. J Infect Dis 2012; 205:1294-304; PMID:22402037; http://dx.doi.org/10.1093/infdis/jis107
42. Clegg JC, Lloyd G. Vaccinia recombinant expressing Lassa-virus internal nucleocapsid protein protects guineapigs against Lassa fever. Lancet 1987; 2:186-8; http://dx.doi.org/10.1016/S0140-6736(87)90767-7
43. Auperin DD, Esposito JJ, Lange JV, Bauer SP, Knight J, Sasso DR, McCormick JB. Construction of a recombinant vaccinia virus expressing the Lassa virus glycoprotein gene and protection of guinea pigs from a lethal Lassa virus infection. Virus Res 1988; 9:233-48; http://dx.doi.org/10.1016/0168-1702(88)90033-0
44. Morrison HG, Goldsmith CS, Regnery HL, Auperin DD. Simultaneous expression of the Lassa virus N and GPC genes from a single recombinant vaccinia virus. Virus Res 1991; 18:231-41; http://dx.doi.org/10.1016/0168-1702(91)90021-M
45. Pushko P, Geisbert J, Parker M, Jahrling P, Smith J. Individual and bivalent vaccines based on alphavirus replicons protect guinea pigs against infection with Lassa and Ebola viruses. J Virol 2001; 75:11677-85; PMID:11689649; http://dx.doi.org/10.1128/JVI.75.23.11677-11685.2001
46. Geisbert TW, Jones S, Fritz EA, Shurtleff AC, Geisbert JB, Liebscher R, Grolla A, Ströher U, Fernando L, Daddario KM, et al. Development of a new vaccine for the prevention of Lassa fever. PLoS Med 2005; 2:e183; PMID:15971954
47. Lukashevich IS, Patterson J, Carrion R, Moshkoff D, Ticer A, Zapata J, Brasky K, Geiger R, Hubbard GB, Bryant J, et al. A live attenuated vaccine for Lassa fever made by reassortment of Lassa and Mopeia viruses. J Virol 2005; 79:13934-42; PMID:16254329; http://dx.doi.org/10.1128/JVI.79.22.13934-13942.2005
48. Rodriguez-Carreno MP, Nelson MS, Botten J, Smith-Nixon K, Buchmeier MJ, Whitton JL. Evaluating the immunogenicity and protective efficacy of a DNA vaccine encoding Lassa virus nucleoprotein. Virology 2005; 335:87-98; PMID:15823608; http://dx.doi.org/10.1016/j.virol.2005.01.019
49. Bredenbeek PJ, Molenkamp R, Spaan WJM, Deubel V, Marianneau P, Salvato MS, Moshkoff D, Zapata J, Tikhonov I, Patterson J, et al. A recombinant yellow fever 17D vaccine expressing Lassa virus glycoproteins. Virology 2006; 345:299-304; PMID:16412488; http://dx.doi.org/10.1016/j.virol.2005.12.001
50. Carrion R, Patterson JL, Johnson C, Gonzales M, Moreira CR, Ticer A, Brasky K, Hubbard GB, Moshkoff D, Zapata J, et al. A ML29 reassortant virus protects guinea pigs against a distantly related Nigerian strain of Lassa virus and can provide sterilizing immunity. Vaccine 2007; 25:4093-102; PMID:17360080; http://dx.doi.org/10.1016/j.vaccine.2007.02.038
51. Lukashevich IS, Carrion R, Salvato MS, Mansfield K, Brasky K, Zapata J, Cairo C, Goicochea M, Hoosien GE, Ticer A, et al. Safety, immunogenicity, and efficacy of the ML29 reassortant vaccine for Lassa fever in small non-human primates. Vaccine 2008; 26:5246-54; PMID:18692539; http://dx.doi.org/10.1016/j.vaccine.2008.07.057
52. Branco LM, Grove JN, Geske FJ, Boisen ML, Muncy IJ, Magliato SA, Henderson LA, Schoepp RJ, Cashman KA, Hensley LE, et al. Lassa virus-like particles displaying all major immunological determinants as a vaccine candidate for Lassa hemorrhagic fever. Virol J 2010; 7:279; PMID:20961433; http://dx.doi.org/10.1186/1743-422X-7-279
53. Jiang X, Dalebout TJ, Bredenbeek PJ, Carrion R, Brasky K, Patterson J, Goicochea M, Bryant J, Salvato MS, Lukashevich IS. Yellow fever 17D-vectored vaccines expressing Lassa virus GP1 and GP2 glycoproteins provide protection against fatal disease in guinea pigs. Vaccine 2011; 29:1248-57; PMID:21145373; http://dx.doi.org/10.1016/j.vaccine.2010.11.079
54. Grant-Klein RJ, Altamura LA, Schmaljohn CS. Progress in recombinant DNA-derived vaccines for Lassa virus and filoviruses. Virus Res 2011; 162:148-61; PMID:21925552; http://dx.doi.org/10.1016/j.virusres.2011.09.005
55. Goicochea MA, Zapata JC, Bryant J, Davis H, Salvato MS, Lukashevich IS. Evaluation of Lassa virus vaccine immunogenicity in a CBA/J-ML29 mouse model. Vaccine 2012; 30:1445-52; PMID:22234266; http://dx.doi.org/10.1016/j.vaccine.2011.12.134
56. Zapata JC, Poonia B, Bryant J, Davis H, Ateh E, George L, Crasta O, Zhang Y, Slezak T, Jaing C, et al. An attenuated Lassa vaccine in SIV-infected rhesus macaques does not persist or cause arenavirus disease but does elicit Lassa virus-specific immunity. Virol J 2013; 10:52; PMID:23402317; http://dx.doi.org/10.1186/1743-422X-10-52
57. Meulen ter J. Lassa fever: implications of T-cell immunity for vaccine development. J Biotechnol 1999; 73:207-12; http://dx.doi.org/10.1016/S0168-1656(99)00122-4
58. Meulen ter J, Badusche M, Kuhnt K, Doetze A, Satoguina J, Marti T, Loeliger C, Koulemou K, Koivogui L, Schmitz H, et al. Characterization of human CD4 (+) T-cell clones recognizing conserved and variable epitopes of the Lassa virus nucleoprotein. J Virol 2000; 74:2186-92; http://dx.doi.org/10.1128/JVI.74.5.2186-2192.2000
59. Oldstone MB, Lewicki H, Homann D, Nguyen C, Julien S, Gairin JE. Common antiviral cytotoxic t-lymphocyte epitope for diverse arenaviruses. J Virol 2001; 75:6273-8; PMID:11413293; http://dx.doi.org/10.1128/JVI.75.14.6273-6278.2001
60. Meulen ter J, Sakho M, Koulemou K, Magassouba N, Bah A, Preiser W, Daffis S, Klewitz C, Bae H-G, Niedrig M, et al. Activation of the cytokine network and unfavorable outcome in patients with yellow fever. J Infect Dis 2004; 190:1821-7; PMID:15499539; http://dx.doi.org/10.1086/425016
61. Boesen A, Sundar K, Coico R. Lassa fever virus peptides predicted by computational analysis induce epitope-specific cytotoxic-T-lymphocyte responses in HLA-A2.1 transgenic mice. Clin Diagn Lab Immunol 2005; 12:1223-30
62. Kotturi MF, Botten J, Sidney J, Bui H-H, Giancola L, Maybeno M, Babin J, Oseroff C, Pasquetto V, Greenbaum JA, et al. A multivalent and cross-protective vaccine strategy against arenaviruses associated with human disease. PLoS Pathog 2009; 5:e1000695
63. Kotturi MF, Botten J, Maybeno M, Sidney J, Glenn J, Bui H-H, Oseroff C, Crotty S, Peters B, Grey H, et al. Polyfunctional CD4+ T cell responses to a set of pathogenic arenaviruses provide broad population coverage. Immunome Res 2010; 6:4; PMID:20478058; http://dx.doi.org/10.1186/1745-7580-6-4
64. Kotturi MF, Peters B, Buendia-Laysa F, Sidney J, Oseroff C, Botten J, Grey H, Buchmeier MJ, Sette A. The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: uncovering new tricks for an old virus. J Virol 2007; 81:4928-40; PMID:17329346; http://dx.doi.org/10.1128/JVI.02632-06
65. Riviere Y, Oldstone MB. Genetic reassortants of lymphocytic choriomeningitis virus: unexpected disease and mechanism of pathogenesis. J Virol 1986; 59:363-8
66. Djavani M, Lukashevich IS, Salvato MS. Sequence comparison of the large genomic RNA segments of two strains of lymphocytic choriomeningitis virus differing in pathogenic potential for guinea pigs. Virus Genes 1998; 17:151-5; http://dx.doi.org/10.1023/A:1008016724243
67. Riviere Y, Ahmed R, Southern PJ, Buchmeier MJ, Oldstone MB. Genetic mapping of lymphocytic choriomeningitis virus pathogenicity: virulence in guinea pigs is associated with the L RNA segment. J Virol 1985; 55:704-9
68. Lukashevich IS, Djavani M, Shapiro K, Sanchez A, Ravkov E, Nichol ST, Salvato MS. The Lassa fever virus L gene: nucleotide sequence, comparison, and precipitation of a predicted 250 kDa protein with monospecific antiserum. J Gen Virol 1997; 78(Pt 3):547-51
69. Lelke M, Brunotte L, Busch C, Günther S. An N-terminal region of Lassa virus L protein plays a critical role in transcription but not replication of the virus genome. J Virol 2010; 84:1934-44; PMID:20007273; http://dx.doi.org/10.1128/JVI.01657-09
70. Albariño CG, Bird BH, Chakrabarti AK, Dodd KA, Erickson BR, Nichol ST. Efficient rescue of recombinant Lassa virus reveals the influence of S segment noncoding regions on virus replication and virulence. J Virol 2011; 85:4020-4; PMID:21307206; http://dx.doi.org/10.1128/JVI.02556-10
71. De Groot AS, Martin W. Reducing risk, improving outcomes: bioengineering less immunogenic protein therapeutics. Clin Immunol 2009; 131:189-201; PMID:19269256; http://dx.doi.org/10.1016/j.clim.2009.01.009
72. Southwood S, Sidney J, Kondo A, del Guercio MF, Appella E, Hoffman S, Kubo RT, Chesnut RW, Grey HM, Sette A. Several common HLA-DR types share largely overlapping peptide binding repertoires. J Immunol 1998; 160:3363-73
73. Sette A, Sidney J. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 1999; 50:201-12; http://dx.doi.org/10.1007/s002510050594
74. De Groot AS. Immunomics: discovering new targets for vaccines and therapeutics. Drug Discov Today 2006; 11:203-9; http://dx.doi.org/10.1016/S1359-6446(05)03720-7
75. Moise L, Gutierrez AH, Bailey-Kellogg C, Terry F, Leng Q, Hady KMA, VerBerkmoes NC, Sztein MB, Losikoff PT, Martin WD, et al. The two-faced T cell epitope: examining the host-microbe interface with JanusMatrix. Hum Vaccin Immunother 2013; 9:1577-86; PMID:23584251; http://dx.doi.org/10.4161/hv.24615
76. Frey A, Di Canzio J, Zurakowski D. A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods 1998; 221:35-41; http://dx.doi.org/10.1016/S0022-1759(98)00170-7
77. Lindow JC, Borochoff-Porte N, Durbin AP, Whitehead SS, Fimlaid KA, Bunn JY, Kirkpatrick BD. Primary vaccination with low dose live dengue 1 virus generates a proinflammatory, multifunctional T cell response in humans. PLoS Negl Trop Dis 2012; 6: e1742; PMID:22816004; http://dx.doi.org/10.1371/journal.pntd.0001742
78. Sugauchi F, Wang RYH, Qiu Q, Jin B, Alter HJ, Shih JWK. Vigorous hepatitis C virus-specific CD4+ and CD8+ T cell responses induced by protein immunization in the presence of Montanide ISA720 plus synthetic oligodeoxynucleotides containing immunostimulatory cytosine-guanine dinucleotide motifs. J Infect Dis 2006; 193:563-72; PMID:16425136; http://dx.doi.org/10.1086/499823
79. Chege GK, Burgers WA, Stutz H, Meyers AE, Chapman R, Kiravu A, Bunjun R, Shephard EG, Jacobs WR, Rybicki EP, et al. Robust immunity to an auxotrophic Mycobacterium bovis BCG-VLP prime-boost HIV vaccine candidate in a nonhuman primate model. J Virol 2013; 87:5151-60; PMID:23449790; http://dx.doi.org/10.1128/JVI.03178-12
80. Meseda CA, Mayer AE, Kumar A, Garcia AD, Campbell J, Listrani P, Manischewitz J, King LR, Golding H, Merchlinsky M, et al. Comparative evaluation of the immune responses and protection engendered by LC16m8 and Dryvax smallpox vaccines in a mouse model. Clin Vaccine Immunol 2009; 16:1261-71; PMID:19605597; http://dx.doi.org/10.1128/CVI.00040-09
81. James EA, LaFond RE, Gates TJ, Mai DT, Malhotra U, Kwok WW. Yellow fever vaccination elicits broad functional CD4+ T cell responses that recognize structural and nonstructural proteins. J Virol 2013; 87:12794-804; PMID:24049183; http://dx.doi.org/10.1128/JVI.01160-13