Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study
Summary: Background: A recombinant vesicular stomatitis virus vector expressing the Zaire Ebola virus glycoprotein (rVSVΔG-ZEBOV-GP) vaccine has been reported as safe, immunogenic, and highly protective in a ring vaccination trial. We aimed to identify transcriptomic immune response biomarker signa...
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-02-01
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| Series: | The Lancet Microbe |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666524721002354 |
| _version_ | 1818869984048185344 |
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| author | Eleonora Vianello, PhD Patricia Gonzalez-Dias, MSc Suzanne van Veen, BSc Carmen G Engele, BSc Edwin Quinten, BSc Thomas P Monath, MD Donata Medaglini, ProfPhD Francesco Santoro, PhD Angela Huttner, MD Sheri Dubey, PhD Michael Eichberg, PhD Francis M Ndungu, PhD Peter G Kremsner, ProfMD Paulin N Essone, PhD Selidji Todagbe Agnandji, MD Claire-Anne Siegrist, ProfMD Helder I Nakaya, PhD Tom H M Ottenhoff, ProfMD Mariëlle C Haks, PhD Selidij T Agnandij Rafi Ahmed Jenna Anderson Floriane Auderset Philip Bejon Luisa Borgianni Jessica Brosnahan Annalisa Ciabattini Olivier Engler Mariëlle C Haks Ali M Harandi Donald G Heppner Alice Gerlini Angela Huttner Peter G Kremsner Donata Medaglini Thomas P Monath Francis M Ndungu Patricia Njuguna Tom H M Ottenhoff David Pejoski Mark Page Gianni Pozzi Francesco Santoro Claire-Anne Siegrist Selidij T Agnandij Luisa Borgianni Annalisa Ciabattini Sheri Dubey Michael Eichberg Olivier Engler Essone P Ndong Ali M Harandi Alice Gerlini Angela Huttner Peter G Kremsner Kabwende Lumeka Donata Medaglini Helder I Nakaya Patricia Gonzales Dias Carvalho Tom H M Ottenhoff Gianni Pozzi Sylvia Rothenberger Francesco Santoro Claire-Anne Siegrist Eleonora Vianello Sravya S Nakka Mariëlle C Haks Suzanne van Veen |
| author_facet | Eleonora Vianello, PhD Patricia Gonzalez-Dias, MSc Suzanne van Veen, BSc Carmen G Engele, BSc Edwin Quinten, BSc Thomas P Monath, MD Donata Medaglini, ProfPhD Francesco Santoro, PhD Angela Huttner, MD Sheri Dubey, PhD Michael Eichberg, PhD Francis M Ndungu, PhD Peter G Kremsner, ProfMD Paulin N Essone, PhD Selidji Todagbe Agnandji, MD Claire-Anne Siegrist, ProfMD Helder I Nakaya, PhD Tom H M Ottenhoff, ProfMD Mariëlle C Haks, PhD Selidij T Agnandij Rafi Ahmed Jenna Anderson Floriane Auderset Philip Bejon Luisa Borgianni Jessica Brosnahan Annalisa Ciabattini Olivier Engler Mariëlle C Haks Ali M Harandi Donald G Heppner Alice Gerlini Angela Huttner Peter G Kremsner Donata Medaglini Thomas P Monath Francis M Ndungu Patricia Njuguna Tom H M Ottenhoff David Pejoski Mark Page Gianni Pozzi Francesco Santoro Claire-Anne Siegrist Selidij T Agnandij Luisa Borgianni Annalisa Ciabattini Sheri Dubey Michael Eichberg Olivier Engler Essone P Ndong Ali M Harandi Alice Gerlini Angela Huttner Peter G Kremsner Kabwende Lumeka Donata Medaglini Helder I Nakaya Patricia Gonzales Dias Carvalho Tom H M Ottenhoff Gianni Pozzi Sylvia Rothenberger Francesco Santoro Claire-Anne Siegrist Eleonora Vianello Sravya S Nakka Mariëlle C Haks Suzanne van Veen |
| author_sort | Eleonora Vianello, PhD |
| collection | DOAJ |
| description | Summary: Background: A recombinant vesicular stomatitis virus vector expressing the Zaire Ebola virus glycoprotein (rVSVΔG-ZEBOV-GP) vaccine has been reported as safe, immunogenic, and highly protective in a ring vaccination trial. We aimed to identify transcriptomic immune response biomarker signatures induced by vaccination and associated signatures with its immunogenicity and reactogenicity to better understand the potential mechanisms of action of the vaccine. Methods: 354 healthy adult volunteers were vaccinated in randomised, double-blind, placebo-controlled trials in Europe (Geneva, Switzerland [November, 2014, to January, 2015]) and North America (USA [Dec 5, 2014, to June 23, 2015]), and dose-escalation trials in Africa (Lambaréné, Gabon [November, 2014, to January, 2015], and Kilifi, Kenya [December, 2014, to January, 2015]) using different doses of the recombinant vesicular stomatitis virus vector expressing the Zaire Ebola virus glycoprotein (rVSVΔG-ZEBOV-GP; 3 × 105 to 1 × 108 plaque-forming units [pfu]). Longitudinal transcriptomic responses (days 0, 1, 2, 3, 7, 14, and 28) were measured in whole blood using a targeted gene expression profiling platform (dual-colour reverse-transcriptase multiplex ligation-dependent probe amplification) focusing on 144 immune-related genes. The effect of time and dose on transcriptomic response was also assessed. Logistic regression with lasso regularisation was applied to identify host signatures with optimal discriminatory capability of vaccination at day 1 or day 7 versus baseline, whereas random-effects models and recursive feature elimination combined with regularised logistic regression were used to associate signatures with immunogenicity and reactogenicity. Findings: Our results indicated that perturbation of gene expression peaked on day 1 and returned to baseline levels between day 7 and day 28. The magnitude of the response was dose-dependent, with vaccinees receiving a high dose (≥9 × 106 pfu) of rVSVΔG-ZEBOV-GP exhibiting the largest amplitude. The most differentially expressed genes that were significantly upregulated following vaccination consisted of type I and II interferon-related genes and myeloid cell-associated markers, whereas T cell, natural killer cell, and cytotoxicity-associated genes were downregulated. A gene signature associated with immunogenicity (common to all four cohorts) was identified correlating gene expression profiles with ZEBOV-GP antibody titres and a gene signatures associated with reactogenicity (Geneva cohort) was identified correlating gene expression profiles with an adverse event (ie, arthritis). Interpretation: Collectively, our results identify and cross-validate immune-related transcriptomic signatures induced by rVSVΔG-ZEBOV-GP vaccination in four cohorts of adult participants from different genetic and geographical backgrounds. These signatures will aid in the rational development, testing, and evaluation of novel vaccines and will allow evaluation of the effect of host factors such as age, co-infection, and comorbidity on responses to vaccines. Funding: Innovative Medicines Initiative 2 Joint Undertaking. |
| first_indexed | 2024-12-19T11:59:48Z |
| format | Article |
| id | doaj.art-9d0108ac7efd4b3a99b85d9af9182e4b |
| institution | Directory Open Access Journal |
| issn | 2666-5247 |
| language | English |
| last_indexed | 2024-12-19T11:59:48Z |
| publishDate | 2022-02-01 |
| publisher | Elsevier |
| record_format | Article |
| series | The Lancet Microbe |
| spelling | doaj.art-9d0108ac7efd4b3a99b85d9af9182e4b2022-12-21T20:22:31ZengElsevierThe Lancet Microbe2666-52472022-02-0132e113e123Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker studyEleonora Vianello, PhD0Patricia Gonzalez-Dias, MSc1Suzanne van Veen, BSc2Carmen G Engele, BSc3Edwin Quinten, BSc4Thomas P Monath, MD5Donata Medaglini, ProfPhD6Francesco Santoro, PhD7Angela Huttner, MD8Sheri Dubey, PhD9Michael Eichberg, PhD10Francis M Ndungu, PhD11Peter G Kremsner, ProfMD12Paulin N Essone, PhD13Selidji Todagbe Agnandji, MD14Claire-Anne Siegrist, ProfMD15Helder I Nakaya, PhD16Tom H M Ottenhoff, ProfMD17Mariëlle C Haks, PhD18Selidij T AgnandijRafi AhmedJenna AndersonFloriane AudersetPhilip BejonLuisa BorgianniJessica BrosnahanAnnalisa CiabattiniOlivier EnglerMariëlle C HaksAli M HarandiDonald G HeppnerAlice GerliniAngela HuttnerPeter G KremsnerDonata MedagliniThomas P MonathFrancis M NdunguPatricia NjugunaTom H M OttenhoffDavid PejoskiMark PageGianni PozziFrancesco SantoroClaire-Anne SiegristSelidij T AgnandijLuisa BorgianniAnnalisa CiabattiniSheri DubeyMichael EichbergOlivier EnglerEssone P NdongAli M HarandiAlice GerliniAngela HuttnerPeter G KremsnerKabwende LumekaDonata MedagliniHelder I NakayaPatricia Gonzales Dias CarvalhoTom H M OttenhoffGianni PozziSylvia RothenbergerFrancesco SantoroClaire-Anne SiegristEleonora VianelloSravya S NakkaMariëlle C HaksSuzanne van VeenDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, Netherlands; Correspondence to: Dr Eleonora Vianello, Department of Infectious Diseases, Leiden University Medical Center, 2333 ZA Leiden, NetherlandsDepartment of Clinical and Toxicological Analyses, School of Pharmaceutical Sciences, University of São Paulo, São Paulo, BrazilDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsNewLink Genetics Corporation, Devens, MA, USALaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, Italy; Sclavo Vaccines Association, Siena, ItalyLaboratory of Molecular Microbiology and Biotechnology, Department of Medical Biotechnologies, University of Siena, Siena, ItalyDivision of Infectious Diseases, Geneva University Hospitals and Faculty of Medicine, Geneva, Switzerland; Center for Vaccinology, Geneva University Hospitals and Faculty of Medicine, Geneva, SwitzerlandDepartment of Vaccine and Biologics Research, Merck Research Laboratories, West Point, PA, USADepartment of Vaccine and Biologics Research, Merck Research Laboratories, West Point, PA, USADepartment of Biosciences, KEMRI-Wellcome Trust Research Programme, Kilifi, KenyaCentre de Recherches Médicales de Lambaréné, Lambaréné, Gabon; Institut für Tropenmedizin, Universitätsklinikum Tübingen, and German Center for Infection Research, Tübingen, GermanyCentre de Recherches Médicales de Lambaréné, Lambaréné, GabonCentre de Recherches Médicales de Lambaréné, Lambaréné, Gabon; Institut für Tropenmedizin, Universitätsklinikum Tübingen, and German Center for Infection Research, Tübingen, GermanyDivision of Infectious Diseases, Geneva University Hospitals and Faculty of Medicine, Geneva, Switzerland; Center for Vaccinology, Geneva University Hospitals and Faculty of Medicine, Geneva, SwitzerlandDepartment of Clinical and Toxicological Analyses, School of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil; Scientific Platform Pasteur-USP, São Paulo, BrazilDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsSummary: Background: A recombinant vesicular stomatitis virus vector expressing the Zaire Ebola virus glycoprotein (rVSVΔG-ZEBOV-GP) vaccine has been reported as safe, immunogenic, and highly protective in a ring vaccination trial. We aimed to identify transcriptomic immune response biomarker signatures induced by vaccination and associated signatures with its immunogenicity and reactogenicity to better understand the potential mechanisms of action of the vaccine. Methods: 354 healthy adult volunteers were vaccinated in randomised, double-blind, placebo-controlled trials in Europe (Geneva, Switzerland [November, 2014, to January, 2015]) and North America (USA [Dec 5, 2014, to June 23, 2015]), and dose-escalation trials in Africa (Lambaréné, Gabon [November, 2014, to January, 2015], and Kilifi, Kenya [December, 2014, to January, 2015]) using different doses of the recombinant vesicular stomatitis virus vector expressing the Zaire Ebola virus glycoprotein (rVSVΔG-ZEBOV-GP; 3 × 105 to 1 × 108 plaque-forming units [pfu]). Longitudinal transcriptomic responses (days 0, 1, 2, 3, 7, 14, and 28) were measured in whole blood using a targeted gene expression profiling platform (dual-colour reverse-transcriptase multiplex ligation-dependent probe amplification) focusing on 144 immune-related genes. The effect of time and dose on transcriptomic response was also assessed. Logistic regression with lasso regularisation was applied to identify host signatures with optimal discriminatory capability of vaccination at day 1 or day 7 versus baseline, whereas random-effects models and recursive feature elimination combined with regularised logistic regression were used to associate signatures with immunogenicity and reactogenicity. Findings: Our results indicated that perturbation of gene expression peaked on day 1 and returned to baseline levels between day 7 and day 28. The magnitude of the response was dose-dependent, with vaccinees receiving a high dose (≥9 × 106 pfu) of rVSVΔG-ZEBOV-GP exhibiting the largest amplitude. The most differentially expressed genes that were significantly upregulated following vaccination consisted of type I and II interferon-related genes and myeloid cell-associated markers, whereas T cell, natural killer cell, and cytotoxicity-associated genes were downregulated. A gene signature associated with immunogenicity (common to all four cohorts) was identified correlating gene expression profiles with ZEBOV-GP antibody titres and a gene signatures associated with reactogenicity (Geneva cohort) was identified correlating gene expression profiles with an adverse event (ie, arthritis). Interpretation: Collectively, our results identify and cross-validate immune-related transcriptomic signatures induced by rVSVΔG-ZEBOV-GP vaccination in four cohorts of adult participants from different genetic and geographical backgrounds. These signatures will aid in the rational development, testing, and evaluation of novel vaccines and will allow evaluation of the effect of host factors such as age, co-infection, and comorbidity on responses to vaccines. Funding: Innovative Medicines Initiative 2 Joint Undertaking.http://www.sciencedirect.com/science/article/pii/S2666524721002354 |
| spellingShingle | Eleonora Vianello, PhD Patricia Gonzalez-Dias, MSc Suzanne van Veen, BSc Carmen G Engele, BSc Edwin Quinten, BSc Thomas P Monath, MD Donata Medaglini, ProfPhD Francesco Santoro, PhD Angela Huttner, MD Sheri Dubey, PhD Michael Eichberg, PhD Francis M Ndungu, PhD Peter G Kremsner, ProfMD Paulin N Essone, PhD Selidji Todagbe Agnandji, MD Claire-Anne Siegrist, ProfMD Helder I Nakaya, PhD Tom H M Ottenhoff, ProfMD Mariëlle C Haks, PhD Selidij T Agnandij Rafi Ahmed Jenna Anderson Floriane Auderset Philip Bejon Luisa Borgianni Jessica Brosnahan Annalisa Ciabattini Olivier Engler Mariëlle C Haks Ali M Harandi Donald G Heppner Alice Gerlini Angela Huttner Peter G Kremsner Donata Medaglini Thomas P Monath Francis M Ndungu Patricia Njuguna Tom H M Ottenhoff David Pejoski Mark Page Gianni Pozzi Francesco Santoro Claire-Anne Siegrist Selidij T Agnandij Luisa Borgianni Annalisa Ciabattini Sheri Dubey Michael Eichberg Olivier Engler Essone P Ndong Ali M Harandi Alice Gerlini Angela Huttner Peter G Kremsner Kabwende Lumeka Donata Medaglini Helder I Nakaya Patricia Gonzales Dias Carvalho Tom H M Ottenhoff Gianni Pozzi Sylvia Rothenberger Francesco Santoro Claire-Anne Siegrist Eleonora Vianello Sravya S Nakka Mariëlle C Haks Suzanne van Veen Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study The Lancet Microbe |
| title | Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study |
| title_full | Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study |
| title_fullStr | Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study |
| title_full_unstemmed | Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study |
| title_short | Transcriptomic signatures induced by the Ebola virus vaccine rVSVΔG-ZEBOV-GP in adult cohorts in Europe, Africa, and North America: a molecular biomarker study |
| title_sort | transcriptomic signatures induced by the ebola virus vaccine rvsvδg zebov gp in adult cohorts in europe africa and north america a molecular biomarker study |
| url | http://www.sciencedirect.com/science/article/pii/S2666524721002354 |
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