What are the most powerful immunogen design vaccine strategies?: Reverse vaccinology 2.0 shows great promise

Cold Spring Harbor Perspectives in Biology

Volumn 9, Issue 11, 2017, Pages

  Burton, Dennis R ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT VACCINE; VACCINE;

ANIMAL; DRUG DESIGN; HUMAN; IMMUNOLOGY;

ANIMALS; DRUG DESIGN; HUMANS; VACCINES; VACCINES, SYNTHETIC;

EID: 85030671126     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a030262     Document Type: Article

References (30)

1. Briney B, Sok D, Jardine JG, Kulp DW, Skog P, Menis S, Jacak R, Kalyuzhniy O, de Val N, Sesterhenn F, et al. 2016. Tailored immunogens direct affinity maturation toward HIV neutralizing antibodies. Cell 166: 1459–1470.e11.
2. Burton DR. 2002. Antibodies, viruses and vaccines. Nat Rev Immunol 2: 706–713.
3. Burton DR, Hangartner L. 2016. Broadly neutralizing antibodies to HIVand their role in vaccine design. Annu Rev Immunol 34: 635–659.
4. Burton DR, Poignard P, Stanfield RL, Wilson IA. 2012. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337: 183–186.
5. Correia BE, Bates JT, Loomis RJ, Baneyx G, Carrico C, Jardine JG, Rupert P, Correnti C, Kalyuzhniy O, Vittal V, et al. 2014. Proof of principle for epitope-focused vaccine design. Nature 507: 201–206.
6. Corti D, Bianchi S, Vanzetta F, Minola A, Perez L, Agatic G, Guarino B, Silacci C, Marcandalli J, Marsland BJ, et al. 2013. Cross-neutralization of four paramyxoviruses by a human monoclonal antibody. Nature 501: 439–443.
7. Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, DeKosky BJ, Ernandes MJ, Georgiev IS, Kim HJ, Pancera M, et al. 2014. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509: 55–62.
8. Escolano A, Steichen JM, Dosenovic P, Kulp DW, Golijanin J, Sok D, Freund NT, Gitlin AD, Oliveira T, Araki T, et al. 2016. Sequential immunization elicits broadly neutralizing anti-HIV-1 antibodies in Ig knockin mice. Cell 166: 1445–1458.e1412.
9. Haynes BF. 2015. New approaches to HIV vaccine development. Curr Opin Immunol 35: 39–47.
10. Hofmann I, Wen Y, Ciferri C, Schulze A, Fuhner V, Leong M, Gerber A, Gerrein R, Nandi A, Lilja AE, et al. 2015. Expression of the human cytomegalovirus pentamer complex for vaccine use in a CHO system. Biotechnol Bioeng 112: 2505–2515.
11. Jardine JG, Ota T, Sok D, Pauthner M, Kulp DW, Kalyuzhniy O, Skog PD, Thinnes TC, Bhullar D, Briney B, et al. 2015. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science 349: 156–161.
12. Kabanova A, Perez L, Lilleri D, Marcandalli J, Agatic G, Becattini S, Preite S, Fuschillo D, Percivalle E, Sallusto F, et al. 2014. Antibody-driven design of a human cytomegalovirus gHgLpUL128L subunit vaccine that selectively elicits potent neutralizing antibodies. Proc Natl Acad Sci 111: 17965–17970.
13. Krammer F, Palese P. 2015. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 14: 167–182.
14. Lanzavecchia A, Fruhwirth A, Perez L, Corti D. 2016. Antibody- guided vaccine design: Identification of protective epitopes. Curr Opin Immunol 41: 62–67.
15. Liao HX, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, et al. 2013. Coevolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469–476.
16. Macagno A, Bernasconi NL, Vanzetta F, Dander E, Sarasini A, Revello MG, Gerna G, Sallusto F, Lanzavecchia A. 2010. Isolation of human monoclonal antibodies that potently neutralize human cytomegalovirus infection by targeting different epitopes on the gH/gL/UL128-131A complex. J Virol 84: 1005–1013.
17. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Chen L, Srivatsan S, Zheng A, et al. 2013a. Structure-βased design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342: 592–598.
18. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, et al. 2013b. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340: 1113–1117.
19. Mouquet H, Scharf L, Euler Z, Liu Y, Eden C, Scheid JF, Halper-Stromberg A, Gnanapragasam PN, Spencer DI, Seaman MS, et al. 2012. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc Natl Acad Sci 109: E3268–E3277.
20. Rappuoli R, Bottomley MJ, D’Oro U, Finco O, De Gregorio E. 2016. Reverse vaccinology 2.0: Human immunology instructs vaccine antigen design. J Exp Med 213: 469–481.
21. Sok D, Doores KJ, Briney B, Le KM, Saye-Francisco KL, Ramos A, Kulp DW, Julien JP, Menis S, Wickramasinghe L, et al. 2014. Promiscuous glycan site recognition by antibodies to the high-mannose patch of gp120 broadens neutralization of HIV. Sci Transl Med 6: 236ra263.
22. Sok D, Briney B, Jardine JG, Kulp DW, Menis S, Pauthner M, Wood A, Lee EC, Le KM, Jones M, et al. 2016a. Priming HIV-1 broadly neutralizing antibody precursors in human Ig loci transgenic mice. Science 353: 1557–1560.
23. Sok D, Pauthner M, Briney B, Lee JH, Saye-Francisco KL, Hsueh J, Ramos A, Le KM, Jones M, Jardine JG, et al. 2016b. A prominent site of antibody vulnerability on HIV envelope incorporates a motif associated with CCR5 binding and its camouflaging glycans. Immunity 45: 31–45.
24. Steichen JM, Kulp DW, Tokatlian T, Escolano A, Dosenovic P, Stanfield RL, McCoy LE, Ozorowski G, Hu X, Kalyuzhniy O, et al. 2016. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 45: 483–496.
25. Sundling C, Martinez P, Soldemo M, Spangberg M, Bengtsson KL, Stertman L, Forsell MN, Karlsson Hedestam GB. 2013. Immunization of macaques with soluble HIV type 1 and influenza virus envelope glycoproteins results in a similarly rapid contraction of peripheral Β-cell responses after boosting. J Infect Dis 207: 426–431.
26. Tian M, Cheng C, Chen X, Duan H, Cheng HL, Dao M, Sheng Z, Kimble M, Wang L, Lin S, et al. 2016. Induction of HIV neutralizing antibody lineages in mice with diverse precursor repertoires. Cell 166: 1471–1484.e18.
27. Wang S, Mata-Fink J, Kriegsman B, Hanson M, Irvine DJ, Eisen HN, Burton DR, Wittrup KD, Kardar M, Chakraborty AK. 2015. Manipulating the selection forces during affinity maturation to generate cross-reactive HIV antibodies. Cell 160: 785–797.
28. Ward AB, Wilson IA. 2015. Insights into the trimeric HIV-1 envelope glycoprotein structure. Trends Biochem Sci 40: 101–107.
29. Xiao X, Chen W, Feng Y, Zhu Z, Prabakaran P, Wang Y, Zhang MY, Longo NS, Dimitrov DS. 2009. Germlinelike predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem Biophys Res Commun 390: 404–409.
30. Zhou T, Zhu J, Wu X, Moquin S, Zhang B, Acharya P, Georgiev IS, Altae-Tran HR, Chuang GY, Joyce MG, et al. 2013. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39: 245–258.