Induction of a Striking Systemic Cytokine Cascade prior to Peak Viremia in Acute Human Immunodeficiency Virus Type 1 Infection, in Contrast to More Modest and Delayed Responses in Acute Hepatitis B and C Virus Infections

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Published in	Journal of Virology Vol. 83; no. 8; pp. 3719 - 3733
Main Authors	Stacey, Andrea R., Norris, Philip J., Qin, Li, Haygreen, Elizabeth A., Taylor, Elizabeth, Heitman, John, Lebedeva, Mila, DeCamp, Allan, Li, Dongfeng, Grove, Douglas, Self, Steven G., Borrow, Persephone
Format	Journal Article
Language	English
Published	Washington, DC American Society for Microbiology 15.04.2009 American Society for Microbiology (ASM)
Subjects	Biological and medical sciences Cytokines - biosynthesis Fundamental and applied biological sciences. Psychology Hepacivirus - immunology Hepatitis B - immunology Hepatitis B - virology Hepatitis B virus Hepatitis B virus - immunology Hepatitis C - immunology Hepatitis C - virology Hepatitis C virus HIV Infections - immunology HIV Infections - virology HIV-1 - immunology Human immunodeficiency virus 1 Humans Longitudinal Studies Microbiology Miscellaneous Pathogenesis and Immunity Plasma - chemistry Plasma - virology Viremia Virology Immunopathology HIV-1 virus Induction Viremia Acute Cytokine Retroviridae Hepatic disease AIDS Immune deficiency Lentivirus Virology Infection Virus Viral hepatitis B Viral disease Digestive diseases Human immunodeficiency virus Viral hepatitis C
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Abstract	Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue JVI About JVI Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JVI RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0022-538X Online ISSN: 1098-5514 Copyright © 2014 by the American Society for Microbiology. For an alternate route to JVI .asm.org, visit: JVI
AbstractList	Characterization of the immune responses induced in the initial stages of human immunodeficiency virus type 1 (HIV-1) infection is of critical importance for an understanding of early viral pathogenesis and prophylactic vaccine design. Here, we used sequential plasma samples collected during the eclipse and exponential viral expansion phases from subjects acquiring HIV-1 (or, for comparison, hepatitis B virus [HBV]or hepatitis C virus [HCV]) to determine the nature and kinetics of the earliest systemic elevations in cytokine and chemokine levels in each infection. Plasma viremia was quantitated over time, and levels of 30 cytokines and chemokines were measured using Luminex-based multiplex assays and enzyme-linked immunosorbent assays. The increase in plasma viremia in acute HIV-1 infection was found to be associated with elevations in plasma levels of multiple cytokines and chemokines, including rapid and transient elevations in alpha interferon (IFN-alpha) and interleukin-15 (IL-15) levels; a large increase in inducible protein 10 (IP-10) levels; rapid and more-sustained increases in tumor necrosis factor alpha and monocyte chemotactic protein 1 levels; more slowly initiated elevations in levels of additional proinflammatory factors including IL-6, IL-8, IL-18, and IFN-gamma; and a late-peaking increase in levels of the immunoregulatory cytokine IL-10. Notably, there was comparatively little perturbation in plasma cytokine levels during the same phase of HBV infection and a delayed response of more intermediate magnitude in acute HCV infection, indicating that the rapid activation of a striking systemic cytokine cascade is not a prerequisite for viral clearance (which occurs in a majority of HBV-infected individuals). The intense early cytokine storm in acute HIV-1 infection may have immunopathological consequences, promoting immune activation, viral replication, and CD4(+) T-cell loss. Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue JVI About JVI Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JVI RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0022-538X Online ISSN: 1098-5514 Copyright © 2014 by the American Society for Microbiology. For an alternate route to JVI .asm.org, visit: JVI Characterization of the immune responses induced in the initial stages of human immunodeficiency virus type 1 (HIV-1) infection is of critical importance for an understanding of early viral pathogenesis and prophylactic vaccine design. Here, we used sequential plasma samples collected during the eclipse and exponential viral expansion phases from subjects acquiring HIV-1 (or, for comparison, hepatitis B virus [HBV]or hepatitis C virus [HCV]) to determine the nature and kinetics of the earliest systemic elevations in cytokine and chemokine levels in each infection. Plasma viremia was quantitated over time, and levels of 30 cytokines and chemokines were measured using Luminex-based multiplex assays and enzyme-linked immunosorbent assays. The increase in plasma viremia in acute HIV-1 infection was found to be associated with elevations in plasma levels of multiple cytokines and chemokines, including rapid and transient elevations in alpha interferon (IFN-) and interleukin-15 (IL-15) levels; a large increase in inducible protein 10 (IP-10) levels; rapid and more-sustained increases in tumor necrosis factor alpha and monocyte chemotactic protein 1 levels; more slowly initiated elevations in levels of additional proinflammatory factors including IL-6, IL-8, IL-18, and IFN-; and a late-peaking increase in levels of the immunoregulatory cytokine IL-10. Notably, there was comparatively little perturbation in plasma cytokine levels during the same phase of HBV infection and a delayed response of more intermediate magnitude in acute HCV infection, indicating that the rapid activation of a striking systemic cytokine cascade is not a prerequisite for viral clearance (which occurs in a majority of HBV-infected individuals). The intense early cytokine storm in acute HIV-1 infection may have immunopathological consequences, promoting immune activation, viral replication, and CD4+ T-cell loss. Characterization of the immune responses induced in the initial stages of human immunodeficiency virus type 1 (HIV-1) infection is of critical importance for an understanding of early viral pathogenesis and prophylactic vaccine design. Here, we used sequential plasma samples collected during the eclipse and exponential viral expansion phases from subjects acquiring HIV-1 (or, for comparison, hepatitis B virus [HBV]or hepatitis C virus [HCV]) to determine the nature and kinetics of the earliest systemic elevations in cytokine and chemokine levels in each infection. Plasma viremia was quantitated over time, and levels of 30 cytokines and chemokines were measured using Luminex-based multiplex assays and enzyme-linked immunosorbent assays. The increase in plasma viremia in acute HIV-1 infection was found to be associated with elevations in plasma levels of multiple cytokines and chemokines, including rapid and transient elevations in alpha interferon (IFN-α) and interleukin-15 (IL-15) levels; a large increase in inducible protein 10 (IP-10) levels; rapid and more-sustained increases in tumor necrosis factor alpha and monocyte chemotactic protein 1 levels; more slowly initiated elevations in levels of additional proinflammatory factors including IL-6, IL-8, IL-18, and IFN-γ; and a late-peaking increase in levels of the immunoregulatory cytokine IL-10. Notably, there was comparatively little perturbation in plasma cytokine levels during the same phase of HBV infection and a delayed response of more intermediate magnitude in acute HCV infection, indicating that the rapid activation of a striking systemic cytokine cascade is not a prerequisite for viral clearance (which occurs in a majority of HBV-infected individuals). The intense early cytokine storm in acute HIV-1 infection may have immunopathological consequences, promoting immune activation, viral replication, and CD4 + T-cell loss. Characterization of the immune responses induced in the initial stages of human immunodeficiency virus type 1 (HIV-1) infection is of critical importance for an understanding of early viral pathogenesis and prophylactic vaccine design. Here, we used sequential plasma samples collected during the eclipse and exponential viral expansion phases from subjects acquiring HIV-1 (or, for comparison, hepatitis B virus [HBV]or hepatitis C virus [HCV]) to determine the nature and kinetics of the earliest systemic elevations in cytokine and chemokine levels in each infection. Plasma viremia was quantitated over time, and levels of 30 cytokines and chemokines were measured using Luminex-based multiplex assays and enzyme-linked immunosorbent assays. The increase in plasma viremia in acute HIV-1 infection was found to be associated with elevations in plasma levels of multiple cytokines and chemokines, including rapid and transient elevations in alpha interferon (IFN-alpha) and interleukin-15 (IL-15) levels; a large increase in inducible protein 10 (IP-10) levels; rapid and more-sustained increases in tumor necrosis factor alpha and monocyte chemotactic protein 1 levels; more slowly initiated elevations in levels of additional proinflammatory factors including IL-6, IL-8, IL-18, and IFN-gamma; and a late-peaking increase in levels of the immunoregulatory cytokine IL-10. Notably, there was comparatively little perturbation in plasma cytokine levels during the same phase of HBV infection and a delayed response of more intermediate magnitude in acute HCV infection, indicating that the rapid activation of a striking systemic cytokine cascade is not a prerequisite for viral clearance (which occurs in a majority of HBV-infected individuals). The intense early cytokine storm in acute HIV-1 infection may have immunopathological consequences, promoting immune activation, viral replication, and CD4(+) T-cell loss.Characterization of the immune responses induced in the initial stages of human immunodeficiency virus type 1 (HIV-1) infection is of critical importance for an understanding of early viral pathogenesis and prophylactic vaccine design. Here, we used sequential plasma samples collected during the eclipse and exponential viral expansion phases from subjects acquiring HIV-1 (or, for comparison, hepatitis B virus [HBV]or hepatitis C virus [HCV]) to determine the nature and kinetics of the earliest systemic elevations in cytokine and chemokine levels in each infection. Plasma viremia was quantitated over time, and levels of 30 cytokines and chemokines were measured using Luminex-based multiplex assays and enzyme-linked immunosorbent assays. The increase in plasma viremia in acute HIV-1 infection was found to be associated with elevations in plasma levels of multiple cytokines and chemokines, including rapid and transient elevations in alpha interferon (IFN-alpha) and interleukin-15 (IL-15) levels; a large increase in inducible protein 10 (IP-10) levels; rapid and more-sustained increases in tumor necrosis factor alpha and monocyte chemotactic protein 1 levels; more slowly initiated elevations in levels of additional proinflammatory factors including IL-6, IL-8, IL-18, and IFN-gamma; and a late-peaking increase in levels of the immunoregulatory cytokine IL-10. Notably, there was comparatively little perturbation in plasma cytokine levels during the same phase of HBV infection and a delayed response of more intermediate magnitude in acute HCV infection, indicating that the rapid activation of a striking systemic cytokine cascade is not a prerequisite for viral clearance (which occurs in a majority of HBV-infected individuals). The intense early cytokine storm in acute HIV-1 infection may have immunopathological consequences, promoting immune activation, viral replication, and CD4(+) T-cell loss.
Author	Steven G. Self John Heitman Li Qin Allan DeCamp Andrea R. Stacey Philip J. Norris Douglas Grove Elizabeth Taylor Dongfeng Li Persephone Borrow Mila Lebedeva Elizabeth A. Haygreen
AuthorAffiliation	The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom, 1 Blood Systems Research Institute, 270 Masonic Avenue, San Francisco, California 94118, 2 University of California, San Francisco, California 94143, 3 Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109, 4 Department of Biostatistics, University of Washington, Seattle, Washington 98105, 5 Department of Probability and Statistics, Peking University, Beijing, China 6
AuthorAffiliation_xml	– name: The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom, 1 Blood Systems Research Institute, 270 Masonic Avenue, San Francisco, California 94118, 2 University of California, San Francisco, California 94143, 3 Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109, 4 Department of Biostatistics, University of Washington, Seattle, Washington 98105, 5 Department of Probability and Statistics, Peking University, Beijing, China 6
Author_xml	– sequence: 1 givenname: Andrea R. surname: Stacey fullname: Stacey, Andrea R. organization: The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom – sequence: 2 givenname: Philip J. surname: Norris fullname: Norris, Philip J. organization: Blood Systems Research Institute, 270 Masonic Avenue, San Francisco, California 94118, University of California, San Francisco, California 94143 – sequence: 3 givenname: Li surname: Qin fullname: Qin, Li organization: Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109, Department of Biostatistics, University of Washington, Seattle, Washington 98105 – sequence: 4 givenname: Elizabeth A. surname: Haygreen fullname: Haygreen, Elizabeth A. organization: The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom – sequence: 5 givenname: Elizabeth surname: Taylor fullname: Taylor, Elizabeth organization: The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom – sequence: 6 givenname: John surname: Heitman fullname: Heitman, John organization: Blood Systems Research Institute, 270 Masonic Avenue, San Francisco, California 94118 – sequence: 7 givenname: Mila surname: Lebedeva fullname: Lebedeva, Mila organization: Blood Systems Research Institute, 270 Masonic Avenue, San Francisco, California 94118 – sequence: 8 givenname: Allan surname: DeCamp fullname: DeCamp, Allan organization: Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109 – sequence: 9 givenname: Dongfeng surname: Li fullname: Li, Dongfeng organization: Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109, Department of Probability and Statistics, Peking University, Beijing, China – sequence: 10 givenname: Douglas surname: Grove fullname: Grove, Douglas organization: Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109 – sequence: 11 givenname: Steven G. surname: Self fullname: Self, Steven G. organization: Statistical Center for HIV/AIDS Research and Prevention, Vaccine and Infectious Disease Institute, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue N., LE-400, Seattle, Washington 98109, Department of Biostatistics, University of Washington, Seattle, Washington 98105 – sequence: 12 givenname: Persephone surname: Borrow fullname: Borrow, Persephone organization: The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom
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Notes	ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 A.R.S. and P.J.N. contributed equally to this study. Corresponding author. Mailing address: The Jenner Institute, University of Oxford, Compton, Berkshire RG20 7NN, United Kingdom. Phone: 44 1635 577913. Fax: 44 1635 577901. E-mail: persephone.borrow@jenner.ac.uk
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Snippet	Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley... Characterization of the immune responses induced in the initial stages of human immunodeficiency virus type 1 (HIV-1) infection is of critical importance for...
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SubjectTerms	Biological and medical sciences Cytokines - biosynthesis Fundamental and applied biological sciences. Psychology Hepacivirus - immunology Hepatitis B - immunology Hepatitis B - virology Hepatitis B virus Hepatitis B virus - immunology Hepatitis C - immunology Hepatitis C - virology Hepatitis C virus HIV Infections - immunology HIV Infections - virology HIV-1 - immunology Human immunodeficiency virus 1 Humans Longitudinal Studies Microbiology Miscellaneous Pathogenesis and Immunity Plasma - chemistry Plasma - virology Viremia Virology
Title	Induction of a Striking Systemic Cytokine Cascade prior to Peak Viremia in Acute Human Immunodeficiency Virus Type 1 Infection, in Contrast to More Modest and Delayed Responses in Acute Hepatitis B and C Virus Infections
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