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

View ORCID ProfileJames W. Austin¹,*,
View ORCID ProfileClarisa M. Buckner¹,*,
View ORCID ProfileLela Kardava¹,
View ORCID ProfileWei Wang¹,
Xiaozhen Zhang¹,
View ORCID ProfileValerie A. Melson¹,
Ryan G. Swanson¹,
Andrew J. Martins²,
View ORCID ProfileJulian Q. Zhou³,
Kenneth B. Hoehn⁴,
View ORCID ProfileJ. Nicholas Fisk³,
Yiannis Dimopoulos⁵,
View ORCID ProfileAlexander Chassiakos⁵,
Sijy O’Dell⁵,
View ORCID ProfileMargery G. Smelkinson⁶,
Catherine A. Seamon⁷,
Richard W. Kwan⁷,
View ORCID ProfileMichael C. Sneller¹,
Stefania Pittaluga⁸,
View ORCID ProfileNicole A. Doria-Rose⁵,
View ORCID ProfileAdrian McDermott⁵,
Yuxing Li ⁹,¹⁰,
View ORCID ProfileTae-Wook Chun¹,
View ORCID ProfileSteven H. Kleinstein ³,⁴,
John S. Tsang²,¹¹,
View ORCID ProfileConstantinos Petrovas⁵ and
View ORCID ProfileSusan 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

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Clarisa M. Buckner

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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ORCID record for Clarisa M. Buckner

Lela Kardava

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Wei Wang

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Xiaozhen Zhang

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Valerie A. Melson

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Ryan G. Swanson

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Andrew J. Martins

2Multiscale 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

3Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511, USA.

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Kenneth B. Hoehn

4Department of Pathology, Yale School of Medicine, New Haven, CT 06520, USA.

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J. Nicholas Fisk

3Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511, USA.

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Yiannis Dimopoulos

5Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Alexander Chassiakos

5Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Sijy O’Dell

5Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Margery G. Smelkinson

6Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Catherine A. Seamon

7Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD 20892, USA.

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Richard W. Kwan

7Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD 20892, USA.

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Michael C. Sneller

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Stefania Pittaluga

8Laboratory 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

5Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Adrian McDermott

5Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Yuxing Li

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.

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Tae-Wook Chun

1Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Steven H. Kleinstein

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.

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John S. Tsang

2Multiscale Systems Biology Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

11NIH 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

5Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

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Susan Moir

1Laboratory 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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