Overexpression of T-bet in HIV infection is associated with accumulation of B cells outside germinal centers and poor affinity maturation

James W. Austin; Clarisa M. Buckner; Lela Kardava; Wei Wang; Xiaozhen Zhang; Valerie A. Melson; Ryan G. Swanson; Andrew J. Martins; Julian Q. Zhou; Kenneth B. Hoehn; J. Nicholas Fisk; Yiannis Dimopoulos; Alexander Chassiakos; Sijy O’Dell; Margery G. Smelkinson; Catherine A. Seamon; Richard W. Kwan; Michael C. Sneller; Stefania Pittaluga; Nicole A. Doria-Rose; Adrian McDermott; Yuxing Li; Tae-Wook Chun; Steven H. Kleinstein; John S. Tsang; Constantinos Petrovas; Susan Moir

doi:10.1126/scitranslmed.aax0904

Research ArticleHIV

Overexpression of T-bet in HIV infection is associated with accumulation of B cells outside germinal centers and poor affinity maturation

James W. Austin¹,*,
Clarisa M. Buckner¹,*,
Lela Kardava¹,
Wei Wang¹,
Xiaozhen Zhang¹,
Valerie A. Melson¹,
Ryan G. Swanson¹,
Andrew J. Martins²,
Julian Q. Zhou³,
Kenneth B. Hoehn⁴,
J. Nicholas Fisk³,
Yiannis Dimopoulos⁵,
Alexander Chassiakos⁵,
Sijy O’Dell⁵,
Margery G. Smelkinson⁶,
Catherine A. Seamon⁷,
Richard W. Kwan⁷,
Michael C. Sneller¹,
Stefania Pittaluga⁸,
Nicole A. Doria-Rose⁵,
Adrian McDermott⁵,
Yuxing Li ⁹,¹⁰,
Tae-Wook Chun¹,
Steven H. Kleinstein ³,⁴,
John S. Tsang²,¹¹,
Constantinos Petrovas⁵ and
Susan Moir ¹,†

¹Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
²Multiscale Systems Biology Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
³Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511, USA.
⁴Department of Pathology, Yale School of Medicine, New Haven, CT 06520, USA.
⁵Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
⁶Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
⁷Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD 20892, USA.
⁸Laboratory of Pathology, National Cancer Institute, Center for Cancer Research, National Institutes of Health, Bethesda, MD 20892, USA.
⁹Institute for Bioscience and Biotechnology Research, University of Maryland, Rockville, MD 20850, USA.
¹⁰Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.
¹¹NIH Center for Human Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

↵†Corresponding author. Email: smoir{at}niaid.nih.gov

↵* These authors contributed equally to this work.

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Science Translational Medicine 27 Nov 2019:
Vol. 11, Issue 520, eaax0904
DOI: 10.1126/scitranslmed.aax0904

James W. Austin

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Clarisa M. Buckner

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Lela Kardava

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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ORCID record for Lela Kardava

Wei Wang

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Xiaozhen Zhang

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Valerie A. Melson

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Ryan G. Swanson

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Andrew J. Martins

Multiscale Systems Biology Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Julian Q. Zhou

Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511, USA.

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Kenneth B. Hoehn

Department of Pathology, Yale School of Medicine, New Haven, CT 06520, USA.

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J. Nicholas Fisk

Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511, USA.

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Yiannis Dimopoulos

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Alexander Chassiakos

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Sijy O’Dell

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Margery G. Smelkinson

Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Catherine A. Seamon

Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD 20892, USA.

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Richard W. Kwan

Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD 20892, USA.

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Michael C. Sneller

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Stefania Pittaluga

Laboratory of Pathology, National Cancer Institute, Center for Cancer Research, National Institutes of Health, Bethesda, MD 20892, USA.

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Nicole A. Doria-Rose

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Adrian McDermott

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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ORCID record for Adrian McDermott

Yuxing Li

Institute for Bioscience and Biotechnology Research, University of Maryland, Rockville, MD 20850, USA.Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.

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Tae-Wook Chun

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Steven H. Kleinstein

Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511, USA.Department of Pathology, Yale School of Medicine, New Haven, CT 06520, USA.

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John S. Tsang

Multiscale Systems Biology Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.NIH Center for Human Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Constantinos Petrovas

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Susan Moir

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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For correspondence: smoir@niaid.nih.gov

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Overexpression of T-bet in HIV infection is associated with accumulation of B cells outside germinal centers and poor affinity maturation

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