CD4 T cells are rapidly depleted from tuberculosis granulomas following acute SIV co-infection

Taylor W Foreman¹, Christine E Nelson¹, Keith D Kauffman¹, Nickiana E Lora¹, Caian L Vinhaes², Danielle E Dorosky¹, Shunsuke Sakai¹, Felipe Gomez³, Joel D Fleegle³, Melanie Parham⁴, Shehan R Perera⁵, Cecilia S Lindestam Arlehamn⁶, Alessandro Sette⁶; Tuberculosis Imaging Program³; Jason M Brenchley⁷, Artur T L Queiroz⁸, Bruno B Andrade², Juraj Kabat⁹, Laura E Via¹⁰, Daniel L Barber¹¹

Affiliations

¹ T lymphocyte Biology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
² Multinational Organization Network Sponsoring Translational and Epidemiological Research (MONSTER) Initiative, Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BA 41810-710, Brazil; Bahiana School of Medicine and Public Health (EBMSP), Salvador, BA 40296, Brazil.
³ Division of Intramural Research, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
⁴ Axle Informatics, National Center for Advancing Translational Sciences, Bethesda, MD 20892, USA.
⁵ Department of Electrical and Computer Engineering, The Ohio State University, Columbus, OH 43201, USA.
⁶ Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA.
⁷ Barrier Immunity Section, Laboratory of Viral Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
⁸ Multinational Organization Network Sponsoring Translational and Epidemiological Research (MONSTER) Initiative, Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BA 41810-710, Brazil; Data and Knowledge Integration Center for Health (CIDACS), Instituto Gonçalo Moniz, Salvador, BA 40296, Brazil.
⁹ Biological Imaging Section, Research Technologies Branch, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁰ Division of Intramural Research, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA; Tuberculosis Research Section, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA; Institute of Infectious Disease & Molecular Medicine and Division of Immunology, Department of Pathology, University of Cape Town, Observatory, Cape Town, 7925, South Africa.
¹¹ T lymphocyte Biology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: barberd@niaid.nih.gov.

PMID: 35649361
DOI: 10.1016/j.celrep.2022.110896

Free article

CD4 T cells are rapidly depleted from tuberculosis granulomas following acute SIV co-infection

Taylor W Foreman et al. Cell Rep. 2022.

Free article

. 2022 May 31;39(9):110896.

doi: 10.1016/j.celrep.2022.110896.

Authors

Affiliations

¹ T lymphocyte Biology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
² Multinational Organization Network Sponsoring Translational and Epidemiological Research (MONSTER) Initiative, Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BA 41810-710, Brazil; Bahiana School of Medicine and Public Health (EBMSP), Salvador, BA 40296, Brazil.
³ Division of Intramural Research, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
⁴ Axle Informatics, National Center for Advancing Translational Sciences, Bethesda, MD 20892, USA.
⁵ Department of Electrical and Computer Engineering, The Ohio State University, Columbus, OH 43201, USA.
⁶ Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA.
⁷ Barrier Immunity Section, Laboratory of Viral Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
⁸ Multinational Organization Network Sponsoring Translational and Epidemiological Research (MONSTER) Initiative, Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BA 41810-710, Brazil; Data and Knowledge Integration Center for Health (CIDACS), Instituto Gonçalo Moniz, Salvador, BA 40296, Brazil.
⁹ Biological Imaging Section, Research Technologies Branch, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁰ Division of Intramural Research, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA; Tuberculosis Research Section, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA; Institute of Infectious Disease & Molecular Medicine and Division of Immunology, Department of Pathology, University of Cape Town, Observatory, Cape Town, 7925, South Africa.
¹¹ T lymphocyte Biology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: barberd@niaid.nih.gov.

PMID: 35649361
DOI: 10.1016/j.celrep.2022.110896

Abstract

HIV/Mycobacterium tuberculosis (Mtb) co-infected individuals have an increased risk of tuberculosis prior to loss of peripheral CD4 T cells, raising the possibility that HIV co-infection leads to CD4 T cell depletion in lung tissue before it is evident in blood. Here, we use rhesus macaques to study the early effects of simian immunodeficiency virus (SIV) co-infection on pulmonary granulomas. Two weeks after SIV inoculation of Mtb-infected macaques, Mtb-specific CD4 T cells are dramatically depleted from granulomas, before CD4 T cell loss in blood, airways, and lymph nodes, or increases in bacterial loads or radiographic evidence of disease. Spatially, CD4 T cells are preferentially depleted from the granuloma core and cuff relative to B cell-rich regions. Moreover, live imaging of granuloma explants show that intralesional CD4 T cell motility is reduced after SIV co-infection. Thus, granuloma CD4 T cells may be decimated before many co-infected individuals experience the first symptoms of acute HIV infection.

Keywords: CD4 T cells; CP: Immunology; CP: Microbiology; SIV; granulomas; live imaging; tuberculosis.

Published by Elsevier Inc.

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Conflict of interest statement

Declaration of interests The contents of this publication do not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the United States government. The authors declare no competing interests.

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CD4 T cells are rapidly depleted from tuberculosis granulomas following acute SIV co-infection

Affiliations

CD4 T cells are rapidly depleted from tuberculosis granulomas following acute SIV co-infection

Authors

Affiliations

Abstract

Conflict of interest statement

Publication types

MeSH terms

LinkOut - more resources

Full Text Sources

Medical

Research Materials

Miscellaneous