COVID-19 immune signatures in Uganda persist in HIV co-infection and diverge by pandemic phase

Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2...

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Published in:Nature communications Vol. 15; no. 1; pp. 1475 - 18
Main Authors: Cummings, Matthew J., Bakamutumaho, Barnabas, Lutwama, Julius J., Owor, Nicholas, Che, Xiaoyu, Astorkia, Maider, Postler, Thomas S., Kayiwa, John, Kiconco, Jocelyn, Muwanga, Moses, Nsereko, Christopher, Rwamutwe, Emmanuel, Nayiga, Irene, Kyebambe, Stephen, Haumba, Mercy, Bosa, Henry Kyobe, Ocom, Felix, Watyaba, Benjamin, Kikaire, Bernard, Tomoiaga, Alin S., Kisaka, Stevens, Kiwanuka, Noah, Lipkin, W. Ian, O’Donnell, Max R.
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 17.02.2024
Nature Publishing Group
Nature Portfolio
Subjects:
631/250/2502
631/250/2520
631/250/254
631/250/255/2514
692/420/254
Adult
Adults
CD8 antigen
Cell activation
Coinfection - epidemiology
COVID-19
Fibrosis
Growth factors
HIV
HIV Infections - complications
HIV Infections - epidemiology
Human immunodeficiency virus
Humanities and Social Sciences
Humans
Immune response
Immune system
Immunology
Immunopathology
Immunotherapy
Infections
Inflammasomes
Inflammation
Lung diseases
Lymphocytes
Lymphocytes T
Lymphopenia
Lymphotoxin
multidisciplinary
Pandemics
Peripheral blood
Platelet-derived growth factor
Prospective Studies
Protein biosynthesis
Protein synthesis
Proteins
Proteomes
Respiratory tract infection
SARS-CoV-2
Science
Science (multidisciplinary)
Severe acute respiratory syndrome coronavirus 2
Transcriptomes
Tumor necrosis factor-β
Uganda - epidemiology
Viral diseases
Uganda
Africa
ISSN:2041-1723, 2041-1723
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Abstract Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8 + T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity. Less is known about SARS-CoV-2 infection in unstudied geographical areas such as sub-Saharan Africa. Here the authors use multi-omics to characterize the immune response to SARS-CoV-2 in Uganda and consider how people living with HIV immunologically differentially respond to the virus.
AbstractList Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8+ T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity.Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8+ T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity.
Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8 T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity.
Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8 + T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity.
Abstract Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8+ T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity.
Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8 + T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity. Less is known about SARS-CoV-2 infection in unstudied geographical areas such as sub-Saharan Africa. Here the authors use multi-omics to characterize the immune response to SARS-CoV-2 in Uganda and consider how people living with HIV immunologically differentially respond to the virus.
Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world and the immunological landscape is unique. In a prospective cohort study of 306 adults encompassing the entire clinical spectrum of SARS-CoV-2 infection in Uganda, we profile the peripheral blood proteome and transcriptome to characterize the immunopathology of COVID-19 across multiple phases of the pandemic. Beyond the prognostic importance of myeloid cell-driven immune activation and lymphopenia, we show that multifaceted impairment of host protein synthesis and redox imbalance define core biological signatures of severe COVID-19, with central roles for IL-7, IL-15, and lymphotoxin-α in COVID-19 respiratory failure. While prognostic signatures are generally consistent in SARS-CoV-2/HIV-coinfection, type I interferon responses uniquely scale with COVID-19 severity in persons living with HIV. Throughout the pandemic, COVID-19 severity peaked during phases dominated by A.23/A.23.1 and Delta B.1.617.2/AY variants. Independent of clinical severity, Delta phase COVID-19 is distinguished by exaggerated pro-inflammatory myeloid cell and inflammasome activation, NK and CD8+ T cell depletion, and impaired host protein synthesis. Combining these analyses with a contemporary Ugandan cohort of adults hospitalized with influenza and other severe acute respiratory infections, we show that activation of epidermal and platelet-derived growth factor pathways are distinct features of COVID-19, deepening translational understanding of mechanisms potentially underlying SARS-CoV-2-associated pulmonary fibrosis. Collectively, our findings provide biological rationale for use of broad and targeted immunotherapies for severe COVID-19 in sub-Saharan Africa, illustrate the relevance of local viral and host factors to SARS-CoV-2 immunopathology, and highlight underemphasized yet therapeutically exploitable immune pathways driving COVID-19 severity. Less is known about SARS-CoV-2 infection in unstudied geographical areas such as sub-Saharan Africa. Here the authors use multi-omics to characterize the immune response to SARS-CoV-2 in Uganda and consider how people living with HIV immunologically differentially respond to the virus.
ArticleNumber 1475
Author Rwamutwe, Emmanuel
Kikaire, Bernard
Kiwanuka, Noah
O’Donnell, Max R.
Owor, Nicholas
Watyaba, Benjamin
Che, Xiaoyu
Lipkin, W. Ian
Nsereko, Christopher
Ocom, Felix
Lutwama, Julius J.
Cummings, Matthew J.
Muwanga, Moses
Postler, Thomas S.
Kayiwa, John
Bosa, Henry Kyobe
Tomoiaga, Alin S.
Nayiga, Irene
Kyebambe, Stephen
Kiconco, Jocelyn
Bakamutumaho, Barnabas
Haumba, Mercy
Kisaka, Stevens
Astorkia, Maider
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  givenname: Matthew J.
  orcidid: 0000-0003-2906-0966
  surname: Cummings
  fullname: Cummings, Matthew J.
  email: mjc2244@columbia.edu
  organization: Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University, Center for Infection and Immunity, Mailman School of Public Health, Columbia University
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  givenname: Barnabas
  surname: Bakamutumaho
  fullname: Bakamutumaho, Barnabas
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  fullname: Lutwama, Julius J.
  organization: Department of Arbovirology, Emerging and Re-emerging Infectious Diseases, Uganda Virus Research Institute
– sequence: 4
  givenname: Nicholas
  surname: Owor
  fullname: Owor, Nicholas
  organization: Department of Arbovirology, Emerging and Re-emerging Infectious Diseases, Uganda Virus Research Institute
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  givenname: Xiaoyu
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– sequence: 6
  givenname: Maider
  surname: Astorkia
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  organization: Center for Infection and Immunity, Mailman School of Public Health, Columbia University
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  surname: Postler
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  organization: Department of Arbovirology, Emerging and Re-emerging Infectious Diseases, Uganda Virus Research Institute
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  givenname: Henry Kyobe
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  surname: Bosa
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  organization: Uganda Peoples’ Defence Forces, Ministry of Health
– sequence: 17
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  organization: Ministry of Health
– sequence: 18
  givenname: Benjamin
  orcidid: 0000-0003-2512-8425
  surname: Watyaba
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  organization: European and Developing Countries Clinical Trials Partnership-Eastern Africa Consortium for Clinical Research, Uganda Virus Research Institute
– sequence: 19
  givenname: Bernard
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  surname: Kikaire
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  organization: European and Developing Countries Clinical Trials Partnership-Eastern Africa Consortium for Clinical Research, Uganda Virus Research Institute, Department of Pediatrics, Makerere University College of Health Sciences
– sequence: 20
  givenname: Alin S.
  surname: Tomoiaga
  fullname: Tomoiaga, Alin S.
  organization: Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University, Department of Accounting, Business Analytics, Computer Information Systems, and Law, Manhattan College
– sequence: 21
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  organization: Department of Epidemiology and Biostatistics, Makerere University School of Public Health
– sequence: 23
  givenname: W. Ian
  orcidid: 0000-0002-8768-9386
  surname: Lipkin
  fullname: Lipkin, W. Ian
  organization: Center for Infection and Immunity, Mailman School of Public Health, Columbia University, Department of Pathology and Cell Biology, Vagelos College of Physicians and Surgeons, Columbia University, Department of Epidemiology, Mailman School of Public Health, Columbia University
– sequence: 24
  givenname: Max R.
  surname: O’Donnell
  fullname: O’Donnell, Max R.
  organization: Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University, Center for Infection and Immunity, Mailman School of Public Health, Columbia University, Department of Epidemiology, Mailman School of Public Health, Columbia University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38368384$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_3389_fimmu_2025_1575135
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Watyaba, Benjamin
O'Donnell, Max R
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  givenname: Max R
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Copyright The Author(s) 2024
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Copyright_xml – notice: The Author(s) 2024
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– notice: The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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SSID ssj0000391844
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Snippet Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in the world...
Abstract Little is known about the pathobiology of SARS-CoV-2 infection in sub-Saharan Africa, where severe COVID-19 fatality rates are among the highest in...
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StartPage 1475
SubjectTerms 631/250/2502
631/250/2520
631/250/254
631/250/255/2514
692/420/254
Adult
Adults
CD8 antigen
Cell activation
Coinfection - epidemiology
COVID-19
Fibrosis
Growth factors
HIV
HIV Infections - complications
HIV Infections - epidemiology
Human immunodeficiency virus
Humanities and Social Sciences
Humans
Immune response
Immune system
Immunology
Immunopathology
Immunotherapy
Infections
Inflammasomes
Inflammation
Lung diseases
Lymphocytes
Lymphocytes T
Lymphopenia
Lymphotoxin
multidisciplinary
Pandemics
Peripheral blood
Platelet-derived growth factor
Prospective Studies
Protein biosynthesis
Protein synthesis
Proteins
Proteomes
Respiratory tract infection
SARS-CoV-2
Science
Science (multidisciplinary)
Severe acute respiratory syndrome coronavirus 2
Transcriptomes
Tumor necrosis factor-β
Uganda - epidemiology
Viral diseases
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Title COVID-19 immune signatures in Uganda persist in HIV co-infection and diverge by pandemic phase
URI https://link.springer.com/article/10.1038/s41467-024-45204-3
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Volume 15
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