Immune profile and responses of a novel dengue DNA vaccine encoding an EDIII-NS1 consensus design based on Indo-African sequences

Molecular Therapy - Tập 30 - Trang 2058-2077 - 2022
Arun Sankaradoss1, Suraj Jagtap2, Junaid Nazir1, Shefta E. Moula1, Ayan Modak3, Joshuah Fialho, Meenakshi Iyer1, Jayanthi S. Shastri4, Mary Dias5, Ravisekhar Gadepalli6, Alisha Aggarwal6, Manoj Vedpathak4, Sachee Agrawal4, Awadhesh Pandit1, Amul Nisheetha1, Anuj Kumar1, Mahasweta Bordoloi1, Mohamed Shafi1, Bhagyashree Shelar1, Swathi S. Balachandra
1National Centre for Biological Sciences (Tata Institute of Fundamental Research), Bangalore 560065, India
2Department of Chemical Engineering, Indian Institute of Science, Bangalore 560012, India
3Molecular Virology Laboratory, Rajiv Gandhi Centre for Biotechnology (RGCB), Thiruvananthapuram, Kerala 695014, India
4Department of Microbiology, T.N.Medical College & B.y.L.Nair Hospital, Mumbai 400008, India
5Division of Infectious Disease, St. John's Medical College and Hospital, Bangalore 560034, India
6Department of Microbiology, All India Institute of Medical Sciences, Jodhpur 342005, India

Tài liệu tham khảo

Polack, 2020, Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine, N. Engl. J. Med., 383, 2603, 10.1056/NEJMoa2034577 Silveira, 2021, DNA vaccines against COVID-19: perspectives and challenges, Life Sci., 267, 118919, 10.1016/j.lfs.2020.118919 Barros-Martins, 2021, Humoral and cellular immune response against SARS-CoV-2 variants following heterologous and homologous ChAdOx1 nCoV-19/BNT162b2 vaccination, medRxiv Schmidt, 2021, Immunogenicity and reactogenicity of heterologous ChAdOx1 nCoV-19/mRNA vaccination, Nat. Med., 2021, 1 Restifo, 2000, The promise of nucleic acid vaccines, Gene Ther., 7, 89, 10.1038/sj.gt.3301117 Flingai, 2013, Synthetic DNA vaccines: improved vaccine potency by electroporation and co-delivered genetic adjuvants, Front. Immunol., 4, 354, 10.3389/fimmu.2013.00354 Momin, 2021, Safety and immunogenicity of a DNA SARS-CoV-2 vaccine (ZyCoV-D): results of an open-label, non-randomized phase I part of phase I/II clinical study by intradermal route in healthy subjects in India, EClinicalMedicine, 38, 101020, 10.1016/j.eclinm.2021.101020 Ramanathan, 2009, Development of a novel DNA SynCon™ tetravalent dengue vaccine that elicits immune responses against four serotypes, Vaccine, 27, 6444, 10.1016/j.vaccine.2009.06.061 Pinto, 2019, T cell responses induced by DNA vaccines based on the DENV2 e and NS1 proteins in mice: importance in protection and immunodominant epitope identification, Front. Immunol., 10, 1522, 10.3389/fimmu.2019.01522 Bhatt, 2013, The global distribution and burden of dengue, Nature, 496, 504, 10.1038/nature12060 Drumond, 2013, Circulation of different lineages of Dengue virus 2, genotype American/Asian in Brazil: dynamics and molecular and phylogenetic characterization, PLoS ONE, 8, e59422, 10.1371/journal.pone.0059422 Manakkadan, 2013, Lineage shift in Indian strains of Dengue virus serotype-3 (Genotype III), evidenced by detection of lineage IV strains in clinical cases from Kerala, Virol. J., 10, 1, 10.1186/1743-422X-10-37 Ahamed, 2019, Emergence of new genotypes and lineages of dengue viruses during the 2012–15 epidemics in southern India, Int. J. Infect. Dis., 84, S34, 10.1016/j.ijid.2019.01.014 Dias, 2018, Complete assembly of a dengue virus type 3 genome from a recent genotype III clade by metagenomic sequencing of serum, Wellcome Open Res., 3, 44, 10.12688/wellcomeopenres.14438.1 Kar, 2019, Isolation and molecular characterization of dengue virus clinical isolates from pediatric patients in New Delhi, Int. J. Infect. Dis., 84, S25, 10.1016/j.ijid.2018.12.003 Alagarasu, 2021, Serotype and genotype diversity of dengue viruses circulating in India: a multi-centre retrospective study involving the Virus Research Diagnostic Laboratory Network in 2018, Int. J. Infect. Dis., 111, 242, 10.1016/j.ijid.2021.08.045 Shrivastava, 2018, Co-circulation of all the four dengue virus serotypes and detection of a novel clade of DENV-4 (genotype I) virus in Pune, India during 2016 season, PLoS ONE, 13, e0192672, 10.1371/journal.pone.0192672 2019, Dengue vaccine: WHO position paper, September 2018-Recommendations, Vaccine, 37, 4848, 10.1016/j.vaccine.2018.09.063 Fahimi, 2018, Dengue viruses and promising envelope protein domain III-based vaccines, Appl. Microbiol. Biotechnol., 1027, 2977, 10.1007/s00253-018-8822-y Ramasamy, 2018, A tetravalent virus-like particle vaccine designed to display domain III of dengue envelope proteins induces multi-serotype neutralizing antibodies in mice and macaques which confer protection against antibody dependent enhancement in AG129 mice, Plos Negl. Trop. Dis., 12, e0006191, 10.1371/journal.pntd.0006191 Chen, 2015, 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, 10, e0145717, 10.1371/journal.pone.0145717 Gallichotte, 2019, Role of zika virus envelope protein domain III as a target of human neutralizing antibodies, MBio, 10, e01485, 10.1128/mBio.01485-19 Lin, 2003, A functional epitope determinant on domain III of the Japanese encephalitis virus envelope protein interacted with neutralizing-antibody combining sites, J. Virol., 77, 2600, 10.1128/JVI.77.4.2600-2606.2003 Gromowski, 2010, Mutations of an antibody binding energy hot spot on domain III of the dengue 2 envelope glycoprotein exploited for neutralization escape, Virology, 407, 237, 10.1016/j.virol.2010.06.044 Chen, 2018, Dengue virus non-structural protein 1: a pathogenic factor, therapeutic target, and vaccine candidate, J. Biomed. Sci., 25, 1, 10.1186/s12929-018-0462-0 Wan, 2014, Protection against dengue virus infection in mice by administration of antibodies against modified nonstructural protein 1, PLoS ONE, 9, e92495, 10.1371/journal.pone.0092495 Grubor-Bauk, 2019, NS1 DNA vaccination protects against Zika infection through T cell–mediated immunity in immunocompetent mice, Sci. Adv., 5, eaax2388, 10.1126/sciadv.aax2388 Beatty, 2015, Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination, Sci. Transl. Med., 7, 304ra141, 10.1126/scitranslmed.aaa3787 Lai, 2017, Antibodies against modified NS1 wing domain peptide protect against dengue virus infection, Sci. Rep., 7, 1, 10.1038/s41598-017-07308-3 Weaver, 2011, Protection against divergent influenza H1N1 virus by a centralized influenza hemagglutinin, PLoS ONE, 6, e18314, 10.1371/journal.pone.0018314 Meyerhoff, 2017, HIV-1 consensus envelope-induced broadly binding antibodies, AIDS Res. Hum. Retroviruses, 33, 859, 10.1089/aid.2016.0294 Wang, 2019, Vaccination with a single consensus envelope protein ectodomain sequence administered in a heterologous regimen induces tetravalent immune responses and protection against dengue viruses in mice, Front. Microbiol., 0, 1113, 10.3389/fmicb.2019.01113 Moutaftsi, 2006, A consensus epitope prediction approach identifies the breadth of murine T CD8+-cell responses to vaccinia virus, Nat. Biotechnol., 24, 817, 10.1038/nbt1215 Singla, 2016, Immune response to dengue virus infection in pediatric patients in New Delhi, India—association of viremia, inflammatory mediators and monocytes with disease severity, Plos Negl. Trop. Dis., 10, e0004497, 10.1371/journal.pntd.0004497 Shastri, 2017, Nine year trends of dengue virus infection in Mumbai, Western India, J. Lab. Physicians, 9, 296, 10.4103/JLP.JLP_169_16 Masika, 2020, Detection of dengue virus type 2 of Indian origin in acute febrile patients in rural Kenya, Plos Negl. Trop. Dis., 14, e0008099, 10.1371/journal.pntd.0008099 Renner, 2018, Characterization of a potent and highly unusual minimally-enhancing antibody directed against dengue virus, Nat. Immunol., 19, 1248, 10.1038/s41590-018-0227-7 Wahala, 2010, Natural strain variation and antibody neutralization of dengue serotype 3 viruses, PLOS Pathog., 6, e1000821, 10.1371/journal.ppat.1000821 Zhou, 2013, The mechanism of differential neutralization of dengue serotype 3 strains by monoclonal antibody 8A1, Virology, 439, 57, 10.1016/j.virol.2013.01.022 Sukupolvi-Petty, 2013, Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection, J. Virol., 87, 8826, 10.1128/JVI.01314-13 Chao, 2005, Strategically examining the full-genome of dengue virus type 3 in clinical isolates reveals its mutation spectra, Virol. J., 2, 1, 10.1186/1743-422X-2-72 Roehrig, 2008, Guidelines for plaque-reduction neutralization testing of human antibodies to dengue viruses, Viral Immunol., 21, 123, 10.1089/vim.2008.0007 Querec, 2009, Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans, Nat. Immunol., 10, 116, 10.1038/ni.1688 Diamond, 2000, Modulation of dengue virus infection in human cells by alpha, beta, and gamma interferons, J. Virol., 74, 4957, 10.1128/JVI.74.11.4957-4966.2000 Sharma, 1996, Interleukin-4 mediates down regulation of antiviral cytokine expression and cytotoxic T-lymphocyte responses and exacerbates vaccinia virus infection in vivo, J. Virol., 70, 7103, 10.1128/jvi.70.10.7103-7107.1996 Rosenthal, 2006, Vaccines: all things considered, Clin. Vaccin. Immunol., 13, 821, 10.1128/CVI.00152-06 de Alwis, 2021, A single dose of self-transcribing and replicating RNA-based SARS-CoV-2 vaccine produces protective adaptive immunity in mice, Mol. Ther., 29, 1970, 10.1016/j.ymthe.2021.04.001 Krathwohl, 2006, Chemokine CXCL10 (IP-10) is sufficient to trigger an immune response to injected antigens in a mouse model, Vaccine, 24, 2987, 10.1016/j.vaccine.2005.11.032 Inoue, 2004, SOCS proteins in T helper cell differentiation: implications for allergic disorders?, Expert Rev. Mol. Med., 6, 1, 10.1017/S1462399404008348 Ford, 2019, CCL7 is a negative regulator of cutaneous inflammation following Leishmania major infection, Front. Immunol., 10, 3063, 10.3389/fimmu.2018.03063 Mahmood, 2018, Multifaceted role of the urokinase-type plasminogen activator (uPA) and its receptor (uPAR): diagnostic, prognostic, and therapeutic applications, Front. Oncol., 8, 24, 10.3389/fonc.2018.00024 Andresen, 2011, Increased expression of beta-defensin 1 (DEFB1) in chronic obstructive pulmonary disease, PLoS ONE, 6, e21898, 10.1371/journal.pone.0021898 Loyet, 2005, Proteomic profiling of surface proteins on Th1 and Th2 Cells, J. Proteome Res., 4, 400, 10.1021/pr049810q Urata, 2018, BST-2 controls T cell proliferation and exhaustion by shaping the early distribution of a persistent viral infection, Plos Pathog., 14, e1007172, 10.1371/journal.ppat.1007172 Salem, 2011, Interferon regulatory factor-7 modulates experimental autoimmune encephalomyelitis in mice, J. Neuroinflammation, 8, 1, 10.1186/1742-2094-8-181 Vander Ark, 2018, TGF-β receptors: in and beyond TGF-β signaling, Cell Signal., 52, 112, 10.1016/j.cellsig.2018.09.002 Kong, 2018, Emerging roles of vascular cell adhesion molecule-1 (VCAM-1) in immunological disorders and cancer, Int. J. Mol. Sci., 19, 1057, 10.3390/ijms19041057 Peters, 2009, October. CD40 and autoimmunity: the dark side of a great activator, Semin. Immunol., 21, 293, 10.1016/j.smim.2009.05.012 Waggoner, 2016, Homotypic dengue virus reinfections in nicaraguan children, J. Infect. Dis., 214, 986, 10.1093/infdis/jiw099 Forshey, 2016, Incomplete protection against dengue virus type 2 re-infection in Peru, Plos Negl. Trop. Dis., 10, e0004398, 10.1371/journal.pntd.0004398 Martinez, 2020, Antigenic variation of the dengue virus 2 genotypes impacts the neutralization activity of human antibodies in vaccinees, Cell Rep, 33, 108226, 10.1016/j.celrep.2020.108226 Sukupolvi-Petty, 2010, Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2, J. Virol., 84, 9227, 10.1128/JVI.01087-10 Shrestha, 2010, The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1, PLoS Pathog., 6, e1000823, 10.1371/journal.ppat.1000823 Brien, 2010, Genotype-specific neutralization and protection by antibodies against dengue virus type 3, J. Virol., 84, 10630, 10.1128/JVI.01190-10 Juraska, 2018, Viral genetic diversity and protective efficacy of a tetravalent dengue vaccine in two phase 3 trials, Proc. Natl. Acad. Sci. U S A, 115, E8378, 10.1073/pnas.1714250115 Frei, 2018, Engineered dengue virus domain III proteins elicit cross-neutralizing antibody responses in mice, J. Virol., 92, 10.1128/JVI.01023-18 Zhou, 2013, The mechanism of differential neutralization of dengue serotype 3 strains by monoclonal antibody 8A1, Virology, 439, 57, 10.1016/j.virol.2013.01.022 Wahala, 2010, Natural strain variation and antibody neutralization of dengue serotype 3 viruses, Plos Pathog., 6, 1000821, 10.1371/journal.ppat.1000821 Chan, 2019, A T164S mutation in the dengue virus NS1 protein is associated with greater disease severity in mice, Sci. Transl. Med., 11, 10.1126/scitranslmed.aat7726 Hobernik, 2018, DNA vaccines—how far from clinical use?, Int. J. Mol. Sci., 19, 3605, 10.3390/ijms19113605 Muthumani, 2008, Immunogenicity of novel consensus-based DNA vaccines against Chikungunya virus, Vaccine, 26, 5128, 10.1016/j.vaccine.2008.03.060 Tebas, 2017, Safety and immunogenicity of an anti–zika virus DNA vaccine — preliminary report, N. Engl. J. Med. Modjarrad, 2019, Safety and immunogenicity of an anti-Middle East respiratory syndrome coronavirus DNA vaccine: a phase 1, open-label, single-arm, dose-escalation trial, Lancet Infect. Dis., 19, 1013, 10.1016/S1473-3099(19)30266-X Smith, 2020, Immunogenicity of a DNA vaccine candidate for COVID-19, Nat. Commun., 11, 1, 10.1038/s41467-020-16505-0 Dey, 2021, Immunogenic potential of DNA vaccine candidate, ZyCoV-D against SARS-CoV-2 in animal models, Vaccine, 39, 4108, 10.1016/j.vaccine.2021.05.098 Osorio, 2011, Efficacy of a tetravalent chimeric dengue vaccine (DENVax) in cynomolgus macaques, Am. J. Trop. Med. Hyg., 84, 978, 10.4269/ajtmh.2011.10-0592 Guirakhoo, 2004, Safety and efficacy of chimeric yellow fever-dengue virus tetravalent vaccine formulations in nonhuman primates, J. Virol., 78, 4761, 10.1128/JVI.78.9.4761-4775.2004 Hellerstein, 2020, What are the roles of antibodies versus a durable, high quality T-cell response in protective immunity against SARS-CoV-2?, Vaccin. X, 6, 100076, 10.1016/j.jvacx.2020.100076 Huber, 2011, Regulation of effector and memory T-cell functions by type I interferon, Immunology, 132, 466, 10.1111/j.1365-2567.2011.03412.x Costa, 2013, Inflammatory and innate immune responses in dengue infection: protection versus disease induction, Am. J. Pathol., 182, 1950, 10.1016/j.ajpath.2013.02.027 Foulds, 2006, Th1 memory: implications for vaccine development, Immunol. Rev., 211, 58, 10.1111/j.0105-2896.2006.00400.x Wieten, 2016, A single 17D yellow fever vaccination provides lifelong immunity; characterization of yellow-fever-specific neutralizing antibody and T-cell responses after vaccination, PLoS ONE, 11, e0149871, 10.1371/journal.pone.0149871 Maciejewski, 2020, Distinct neutralizing antibody correlates of protection among related Zika virus vaccines identify a role for antibody quality, Sci. Transl. Med., 12, 9066, 10.1126/scitranslmed.aaw9066 Nguyen, 2015, IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol., 32, 268, 10.1093/molbev/msu300 Trifinopoulos, 2016, W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis, Nucleic Acids Res., 44, W232, 10.1093/nar/gkw256 Rambaut, 2010 Malavige, 2012, Identification of serotype-specific T cell responses to highly conserved regions of the dengue viruses, Clin. Exp. Immunol., 168, 215, 10.1111/j.1365-2249.2012.04566.x Kringelum, 2012, Reliable B cell epitope predictions: impacts of method development and improved benchmarking, PLoS Comput. Biol., 8, e1002829, 10.1371/journal.pcbi.1002829 Bagarazzi, 2012, Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses, Sci. Translational Med., 4, 155ra138, 10.1126/scitranslmed.3004414 Singh, 2017, Comparative whole genome analysis of dengue virus serotype-2 strains differing in trans-endothelial cell leakage induction in vitro, Infect. Genet. Evol., 52, 34, 10.1016/j.meegid.2017.04.022