An approach for a synthetic CTL vaccine design against Zika flavivirus using class I and class II epitopes identified by computer modeling

Frontiers in Immunology

Volumn 8, Issue JUN, 2017, Pages

  Cunha Neto, Edecio ^a,b   Rosa, Daniela S ^b,c   Harris, Paul E ^d   Olson, Tim ^e   Morrow, Alex ^e   Ciotlos, Serban ^e   Herst, Charles V ^e   Rubsamen, Reid Martin ^e,f  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Institute for Investigation in Immunology INCT   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

^e HeartFlow Inc   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Computer model; CTL vaccine; Dengue; Epitope; Flavivirus; Protein folding; Zika vaccine

Indexed keywords

ZIKA VIRUS VACCINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; CLINICAL TRIAL (TOPIC); COMPUTER MODEL; CYTOTOXIC T LYMPHOCYTE; DRUG DESIGN; ENTROPY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX; MATHEMATICAL MODEL; NONHUMAN; ZIKA FEVER;

EID: 85020391707     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00640     Document Type: Article

References (87)

1. CDC. Zika Virus Case Counts in the US. (2016). Available from: http://www.cdc.gov/zika/geo/unitedstates.html
2. Zhang Q, Sun K, Chinazzi M, Pastore-Pinotti A, Dean NE, Rojas DP, et al. Projected spread of Zika virus in the Americas. bioRxiv (2016). doi: 10.1101/066456
3. Brasil P, Pereira JP, Gabaglia J, Damasceno CR, Wakimoto LM, Nogueira R, et al. Zika virus infection in pregnant women in Rio de Janeiro-preliminary report. N Engl J Med (2016). doi:10.1056/NEJMoa1602412
4. Ye Q, Liu Z, Han J, Jiang T, Li X, Qin C. Genomic characterization and phylogenetic analysis of Zika virus circulating in the Americas. Infect Genet Evol (2016) 43:43-9. doi:10.1016/j.meegid.2016.05.004
5. Sant A, McMichael A. Revealing the role of CD4(+) T cells in viral immunity. J Exp Med (2012) 209(8):1391-5. doi:10.1084/jem.20121517
6. Swain S, McKinstry K, Strutt. Expanding roles for CD4+ T cells in immunity to viruses. Nat Rev Immunol (2012) 12(2):136-48. doi:10.1038/nri3152
7. Yauch L, Zellweger M, Kotturi M, Qutubuddin A, Sidney J, Peters B, et al. A protective role for dengue virus-specific CD8+ T cells. J Immunol (2009) 182(8):4865-73. doi:10.4049/jimmunol.0801974
8. Weiskopf D, Bangs D, Sidney J, Kolla R, Silva AD, de Silva A, et al. Dengue virus infection elicits highly polarized CX3CR1+ cytotoxic CD4+ T cells associated with protective immunity. Proc Natl Acad Sci U S A (2015) 112(31):E4256-63. doi:10.1073/pnas.1505956112
9. Netland J, Bevan M. CD8 and CD4 T cells in West Nile virus immunity and pathogenesis. Viruses (2013) 5(10):2573-84. doi:10.3390/v5102573
10. Weiskopf D, Angelo M, Bangs D, Sidney J, Paul S, Peters B, et al. The human CD8+ T cell responses induced by a live attenuated tetravalent dengue vaccine are directed against highly conserved epitopes. J Virol (2015) 89(1):120-8. doi:10.1128/JVI.02129-14
11. Akondy R, Johnson L, Nakaya H, Edupuganti S, Mulligan M, Lawson B, et al. Initial viral load determines the magnitude of the human CD8 T cell response to yellow fever vaccination. Proc Natl Acad Sci U S A (2015) 112(10):3050-5. doi:10.1073/pnas.1500475112
12. Bassi M, Kongsgaard M, Steffensen M, Fenger C, Rasmussen M, Skødt K, et al. CD8+ T cells complement antibodies in protecting against yellow fever virus. J Immunol (2015) 194(3):1141-53. doi:10.4049/jimmunol.1402605
13. Marraco SF, Soneson C, Po G, Allard M, Maillard SA, Montandon N, et al. Long-lasting stem cell-like memory CD8+ T cells with a naïve-like profile upon yellow fever vaccination. Sci Transl Med (2015) 7(282):4111-6. doi:10.1126/scitranslmed.aaa3700
14. Watson A, Lam L, Klimstra W, Ryman K. The 17D-204 vaccine strain-induced protection against virulent yellow fever virus is mediated by humoral immunity and CD4+ but not CD8+ T cells. PLoS Pathog (2016) 12(7):e1005786. doi:10.1371/journal.ppat.1005786
15. Chen H-W, Hu H-M, Wu S-H, Chiang C-Y, Hsiao Y-J, Wu C-K, et al. The immunodominance change and protection of CD4+ T-cell responses elicited by an envelope protein domain III-based tetravalent dengue vaccine in mice. PLoS One (2015) 10(12):e0145717. doi:10.1371/journal.pone.0145717
16. Brien J, Uhrlaub J, Nikolich-Zugich J. West Nile virus-specific Cd4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are sufficient for antiviral protection. J Immunol (2008) 181(12):8568-75. doi:10.4049/jimmunol.181.12.8568
17. Ngono E, Vizcarra E, Tang W, Sheets N, Kim K, Gorman M, et al. Mapping and role of the CD8+ T cell response during primary Zika virus infection in mice. Cell Host Microbe (2017) 21(1):35-46. doi:10.1016/j.chom.2016.12.010
18. Cao-Lormeau V, Blake A, Mons S, Lastere S, Roche C, Vanhomwegen J, et al. Guillain-Barre syndrome outbreak associated with Zika virus infection in French polynesia: a case-control study. Lancet (2016) 387(10027):1531-9. doi:10.1016/S0140-6736(16)00562-6
19. Parra B, Lizarazo J, Jimenez-Arango JA, Zea-Vera AF, Gonzalez-Manrique G, Vargas J, et al. Guillain-Barre syndrome associated with Zika virus infection in colombia. N Engl J Med (2016) 375(16):1513-23. doi:10.1056/NEJMoa1605564
20. Guzman MG, Alvarez M, Halstead SB. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol (2013) 158(7):1445-59. doi:10.1007/s00705-013-1645-3
21. Guzman MG, Alvarez M, Rodriguez-Roche R, Bernardo L, Montes T, Vazquez S, et al. Neutralizing antibodies after infection with dengue 1 virus. Emerg Infect Dis (2007) 13(2):282-6. doi:10.3201/eid1302.060539
22. Schmid M, Diamond MS, Harris E. Dendritic cells in dengue virus infection: targets of virus replication and mediators of immunity. Front Immunol (2014) 5:647. doi:10.3389/fimmu.2014.00647
23. Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G, Duangchinda T, et al. Dengue virus serocross-reactivity drives antibody-dependent enhancement of infection with Zika virus. Nat Immunol (2016) 17:1102-8. doi:10.1038/ni.3515
24. Paul LM, Carlin ER, Jenkins MM, Tan AL, Barcellona CM, Nicholson CO, et al. Dengue virus antibodies enhance Zika virus infection. bioRxiv (2016). doi:10.1101/050112
25. Kawiecki A, Christofferson R. Zika virus-induced antibody response enhances dengue virus serotype 2 replication in vitro. J Infect Dis (2016) 214(9):1357-60. doi:10.1093/infdis/jiw377
26. Russell P, Halstead S. Challenges to the design of clinical trials for live-attenuated tetravalent dengue vaccines. PLoS Negl Trop Dis (2016) 10:8. doi:10.1371/journal.pntd.0004854
27. Zellweger RM, Prestwood TR, Shresta S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe (2010) 7(2):128-39. doi:10.1016/j.chom.2010.01.004
28. Dudley DW, Aliota MT, Mohr EL, Weiler AM, Lehrer-Brey G, Weisgrau KL, et al. A rhesus macaque model of Asian-lineage Zika virus infection. Nat Commun (2016) 7:12204. doi:10.1038/ncomms12204
29. Yauch LE, Prestwood TR, May MM, Morar MM, Zellweger RM, Peters B, et al. CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J Immunol (2010) 185(9):5405-16. doi:10.4049/jimmunol.1001709
30. Zellweger RM, Tang WW, Eddy WE, King K, Sanchez MC, Shresta S. CD8+ T cells can mediate short-term protection against heterotypic dengue virus reinfection in mice. J Virol (2015) 89(12):6494-505. doi:10.1128/JVI.00036-15
31. Zellweger R, Eddy WE, Tang WW, Miller R, Shresta S. CD8+ T cells prevent antigen-induced antibody-dependent enhancement of dengue disease in mice. J Immunol (2014) 193(8):4117-24. doi:10.4049/jimmunol.1401597
32. Vaccine Pipeline Tracker. (2016). Available from: http://www.who.int/immunization/research/vaccine_pipeline_tracker_spreadsheet/en/
33. Abbink P, Larocca R, de La Barrera R, Bricault C, Moseley E, Boyd M, et al. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science (2016) 353(6304):1129-32. doi:10.1126/science.aah6157
34. Dowd K, Ko S, Morabito K, Yang E, Pelc R, DeMaso C, et al. Rapid development of a DNA vaccine for Zika virus. Science (2016) 354(6309):237-40. doi:10.1126/science.aai3197
35. Alam A, Ali S, Ahamad S, Malik M, Ishrat R. From ZikV genome to vaccine: in silico approach for the epitope-based peptide vaccine against Zika virus envelope glycoprotein. Immunology (2016) 149(4):386-99. doi:10.1111/imm.12656
36. Khan A, Miotto O, Heiny A, Salmon J, Srinivasan K, Nascimento E, et al. A systematic bioinformatics approach for selection of epitope-based vaccine targets. Cell Immunol (2006) 244(2):141-7. doi:10.1016/j.cellimm.2007.02.005
37. Sánchez-Burgos G, Ramos-Castañeda J, Cedillo-Rivera R, Dumonteil E. Immunogenicity of novel dengue virus epitopes identified by bioinformatic analysis. Virus Res (2006) 153(1):113-20. doi:10.1016/j.virusres.2010.07.014
38. Shi J, Sun J, Wu M, Hu N, Li J, Li Y, et al. Inferring protective CD8+ T-cell epitopes for NS5 protein of four serotypes of dengue virus Chinese isolates based on HLA-a,-b and-c allelic distribution: implications for epitope-based universal vaccine design. PLoS One (2015) 10(9):e0138729. doi:10.1371/journal.pone.0138729
39. Gilbert S. T-cell-inducing vaccines-what's the future? Immunology (2012) 135(1):19-26. doi:10.1111/j.1365-2567.2011.03517.x
40. Borthwick N, Ahmed T, Ondondo B, Hayes P, Rose A, Ebrahimsa U, et al. Vaccine-elicited human T cells recognizing conserved protein regions inhibit HIV-1. Mol Ther (2014) 22(2):464-75. doi:10.1038/mt.2013.248
41. Rosa D, Iwai L, Tzelepis F, Bargieri D, Medeiros M, Soares I, et al. Immunogenicity of a recombinant protein containing the Plasmodium vivax vaccine candidate msp1(19) and two human CD4+ T-cell epitopes administered to non-human primates (Callithrix jacchus jacchus). Microbes Infect (2006) 8(8):2130-7. doi:10.1016/j.micinf.2006.03.012
42. Soria-Guerra R, Nieto-Gomez R, Govea-Alonso D, Rosales-Mendoza S. An overview of bioinformatics tools for epitope prediction: implications on vaccine development. J Biomed Inform (2014) 53:405-14. doi:10.1016/j.jbi.2014.11.003
43. Sridhar S. Heterosubtypic T-cell immunity to influenza in humans: challenges for universal T-cell influenza vaccines. Front Immunol (2016) 7:195. doi:10.3389/fimmu.2016.00195
44. Kimata JT, Rice AP, Wang J. Challenges and strategies for the eradication of the HIV reservoir. Curr Opin Immunol (2016) 42:65-70. doi:10.1016/j.coi.2016.05.015
45. Abbas W, Tariq M, Iqbal M, Kumar A, Herbein G. Eradication of HIV-1 from the macrophage reservoir: an uncertain goal? Viruses (2015) 7:1578-98. doi:10.3390/v7041578
46. Govero J, Esakky P, Scheaffer S, Fernandez E, Drury A, Platt D, et al. Zika virus infection damages the testes in mice. Nature (2016) 540:438-42. doi:10.1038/nature20556
47. Connick E, Folkvord JM, Lind KT, Rakasz EG, Miles B, Wilson NA, et al. Compartmentalization of simian immunodeficiency virus replication within secondary lymphoid tissues of rhesus macaques is linked to disease stage and inversely related to localization of virus-specific CTL. J Immunol (2014) 193(11):5613-25. doi:10.4049/jimmunol.1401161
48. Douek DC. Disrupting T-cell homeostasis: how HIV-1 infection causes disease. AIDS Rev (2003) 5(3):172-7
49. Streeck H, Jolin JS, Qi Y, Yassine-Diab B, Johnson RC, Kwon DS, et al. Human immunodeficiency virus type 1-specific CD8+ T-cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J Virol (2009) 83(15):7641-8. doi:10.1128/JVI.00182-09
50. Rademeyer C, Korber B, Seaman MS, Giorgi EE, Thebus R, Robles A, et al. Features of recently transmitted HIV-1 clade c viruses that impact antibody recognition: implications for active and passive immunization. PLoS Pathog (2016) 12(7):e1005742. doi:10.1371/journal.ppat.1005742
51. Pereyra F, Heckerman D, Carlson JM, Soghoian CK, Karel D, Goldenthal A, et al. HIV control is mediated in part by CD8+ T-cell targeting of specific epitopes. J Virol (2014) 88(22):12937-48. doi:10.1128/JVI.01004-14
52. Schein C, Zhou B, Braun W. Stereophysicochemical variability plots highlight conserved antigenic areas in flaviviruses. Virol J (2005) 2:40. doi:10.1186/1743-422X-2-40
53. Faria NR, Rdo SA, Kraemer MU, Souza R, Cunha MS, Hill SC, et al. Zika virus in the Americas: early epidemiological and genetic findings. Science (2016) 352(6283):345-9. doi:10.1126/science.aaf5036
54. Wang L, Valderramos SG, Wu A, Ouyang S, Li C, Brasil P, et al. From mosquitos to humans: genetic evolution of Zika virus. Cell Host Microbe (2016) 19(5):561-5. doi:10.1016/j.chom.2016.04.006
55. Logan I. Zika-how fast does this virus mutate? Dongwuxue Yanjiu (2016) 37(2):110-5. doi:10.13918/j.issn.2095-8137.2016.2.110
56. Ashfaq U, Ahmed B. De novo structural modeling and conserved epitopes prediction of Zika virus envelop protein for vaccine development. Viral Immunol (2016) 29(7):1-8. doi:10.1089/vim.2016.0033
57. Shawan M, Mahmud H, Hasan M, Parvin M, Rahman N, Rahman SMB. In silico modeling and immunoinformatics probing disclose the epitope based peptidevaccine against Zika virus envelope glycoprotein. Indian J Pharm Biol Res (2014) 2(4):44-57
58. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A, Bianchi S, et al. Specificity, cross-reactivity and function of antibodies elicited by Zika virus infection. Science (2016) 353(6301):823-6. doi:10.1126/science.aaf8505
59. Zika-Strain. Complete Coding Sequence of Zika Virus from a French Polynesia Outbreak in 2013. (2014). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4047448/
60. IEDB. IEDB MHC-I Binding Predictions Tool. (2013). Available from: http://tools.iedb.org/mhci/reference/
61. UniProtKB/Swiss-Prot. (2016). Available from: https://www.ebi.ac.uk/uniprot
62. Katoh K, Misawa K, Kuma K, Miyata T. Mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res (2002) 30(14):3059-66. doi:10.1093/nar/gkf436
63. Löytynoja A, Goldman N. webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics (2010) 11:579. doi:10.1186/1471-2105-11-579
64. RCSB PDB Policies and References. (2013). Available from: http://www.rcsb.org/pdb/static.do?p=general_information/about_pdb/policies_references.html
65. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L. The foldx web server: an online force field. Nucleic Acids Res (2005) 33:W382-8. doi:10.1093/nar/gki387
66. Sirohi D, Chen Z, Sun L, Klose T, Pierson TC, Rossman MG, et al. The 3.8Å resolution cryo-EM structure of Zika virus. Science (2016) 22:467-70. doi:10.1126/science.aaf5316
67. Aslan N, Yurdaydin C, Wiegand J, Greten T, Ciner A, Meyer M, et al. Cytotoxic CD4 T cells in viral hepatitis. J Viral Hepat (2006) 13(8):505-14. doi:10.1111/j.1365-2893.2006.00723.x
68. Marshall N, Swain S. Cytotoxic CD4 T cells in antiviral immunity. J Biomed Biotechnol (2011) 2011:954602. doi:10.1155/2011/954602
69. Sáez-Borderías A, Gumá M, Angulo A, Bellosillo B, Pende D, Lípez-Botet M. Expression and function of nkg2d in CD4+ T cells specific for human cytomegalovirus. Eur J Immunol (2006) 36(12):3198-206. doi:10.1002/eji.200636682
70. Soghoian D, Jessen H, Flanders M, Sierra-Davidson K, Cutler S, Pertel T, et al. HIV-specific cytolytic CD4 T cell responses during acute HIV infection predict disease outcome. Sci Transl Med (2012) 29(4):123-5. doi:10.1126/scitranslmed.3003165
71. Rosa D, Ribeiro S, Cunha-Neto E. CD4+ T cell epitope discovery and rational vaccine design. Arch Immunol Ther Exp (Warsz) (2010) 32(2):121-30. doi:10.1007/s00005-010-0067-0
72. Sturniolo T, Bono E, Ding J, Raddrizzani L, Tuereci O, Sahin U, et al. Generation of tissue-specific and promiscuous HLA ligand databases using DNA microarrays and virtual HLA class II matrices. Nat Biotechnol (1999) 17(6):555-61. doi:10.1038/9858
73. Singh H, Raghava G. Propred: prediction of HLA-DR binding sites. Bioinformatics (2001) 17(12):1236-7. doi:10.1093/bioinformatics/17.12.1236
74. Hammer J, Belunis C, Bolin D, Papadopoulos J, Walsky R, Higelin J. High-affinity binding of short peptides to major histocompatibility complex class II molecules by anchor combinations. Proc Natl Acad Sci U S A (1994) 91:4456-60. doi:10.1073/pnas.91.10.4456
75. LK LI, Yoshida M, Sidney J, Shikanai-Yasuda M, Goldberg A, Juliano M, et al. In silico prediction of peptides binding to multiple HLA-DR molecules accurately identifies immunodominant epitopes from gp43 of Paracoccidioides brasiliensis frequently recognized in primary peripheral blood mononuclear cell responses from sensitized individuals. Mol Med (2003) 9:209-19
76. Ribeiro S, Rosa D, Fonseca S, Mairena E, Postól E, Oliveira S, et al. A vaccine encoding conserved promiscuous HIV CD4 epitopes induces broad T cell responses in mice transgenic to multiple common HLA class II molecules. PLoS One (2010) 5(6):e11072. doi:10.1371/journal.pone.0011072
77. Garcia T, Fonseca C, Pacifico L, Fdo VD, Marinho F, Penido M, et al. Peptides containing T cell epitopes, derived from Sm14, but not from paramyosin, induce a Th1 type of immune response, reduction in liver pathology and partial protection against Schistosoma mansoni infection in mice. Acta Trop (2008) 106(3):162-7. doi:10.1016/j.actatropica.2008.03.003
78. Whitton JL, Sheng N, Oldstone MBA, McKee TA. A "string-of-beads" vaccine, comprising linked mini genes, confers protection from lethal-dose virus challenge. J Virol (1993) 67(1):348-52
79. Mothe B. DNA-MVA Prime-Boost Vaccine Eliciting T-Cell Specificities Associated with HIV-1 Control is Highly Immunogenic in Mice and Breaks CTL Immuno-Dominance. Barcelona, Spain (2013)
80. Kopycinski J, Cheeseman H, Ashraf A, Gill D, Hayes P, Hannaman D. A DNA-based candidate HIV vaccine delivered via in vivo electroporation induces CD4 responses toward the 4-7-binding v2 loop of HIV gp120 in healthy volunteers. Clin Vaccine Immunol (2012) 19(9):1557-9. doi:10.1128/CVI.00327-12
81. Mullins J. Refocusing CTL and Antibody Responses with p24 gag Conserved Elements Vaccines. Barcelona, Spain (2013)
82. Groot AD, Marcon L, Bishop E, Rivera D, Kutzler M, Weiner D, et al. HIV vaccine development by computer assisted design: the GAIA vaccine. Vaccine (2005) 23(17-18):2136-48. doi:10.1016/j.vaccine.2005.01.097
83. Rubsamen RM, Herst CV, Lloyd PM, Heckerman DE. Eliciting cytotoxic t-lymphocyte responses from synthetic vectors containing one or two epitopes in a c57bl/6 mouse model using peptide-containing biodegradable microspheres and adjuvants. Vaccine (2014) 32:4111-6. doi:10.1016/j.vaccine.2014.05.071
84. Jain S, O'Hagan D, Singh M. The long-term potential of biodegradable poly (lactide co-glycolide) micro particles as the next-generation vaccine adjuvant. Expert Rev Vaccines (2007) 28:13. doi:10.1586/erv.11.126
85. Martin-Banderas LF, Flores-Mosquera M, Riesco-Chueca P, Rodriguez-Gil A, Cebolla A, Chávez S. Flow focusing: a versitile technology to produce size-controlled and specific-morphology microparticles. Small (2005) 1(7):688-92. doi:10.1002/smll.200500087
86. Waeckerle-Men Y, Allmen E, Gander B, Scandella E, Schlosser E, Schmidtke G. Encapsulation of proteins and peptides into biodegradable poly(d,l-lactide-co-glycolide) microspheres prolongs and enhances antigen presentation by human dendritic cells. Vaccine (2006) 24(11):1847-57. doi:10.1016/j.vaccine.2005.10.032
87. Salvadori L, Santana F, Marcos E. Frequency of alleles and haplotypes of the human leukocyte antigen system in Bauru, São Paulo, Brazil. Rev Bras Hematol Hemoter (2014) 36(2):108-14. doi:10.5581/1516-8484.20140026