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Open Access

Innate Immune Responses and Gut Microbiomes Distinguish HIV-Exposed from HIV-Unexposed Children in a Population-Specific Manner

Nelly Amenyogbe, Pedro Dimitriu, Patricia Cho, Candice Ruck, Edgardo S. Fortuno III, Bing Cai, Ariane Alimenti, Hélène C. F. Côté, Evelyn J. Maan, Amy L. Slogrove, Monika Esser, Arnaud Marchant, Tessa Goetghebuer, Casey P. Shannon, Scott J. Tebbutt, Tobias R. Kollmann, William W. Mohn and Kinga K. Smolen
J Immunol October 16, 2020, ji2000040; DOI: https://doi.org/10.4049/jimmunol.2000040
Nelly Amenyogbe
*Department of Experimental Medicine, The University of British Columbia, Vancouver, British Columbia V5Z 1M9, Canada;
†Telethon Kids Institute, Perth, Western Australia 6009, Australia;
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Pedro Dimitriu
‡Department of Microbiology and Immunology, Life Sciences Institute, The University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada;
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Patricia Cho
*Department of Experimental Medicine, The University of British Columbia, Vancouver, British Columbia V5Z 1M9, Canada;
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Candice Ruck
*Department of Experimental Medicine, The University of British Columbia, Vancouver, British Columbia V5Z 1M9, Canada;
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Edgardo S. Fortuno III
§Division of Infectious Diseases, Department of Pediatrics, The University of British Columbia, Vancouver, British Columbia V6H 3V4, Canada;
¶Division of Palliative, Rehabilitation, and Integrative Medicine, University of Texas MD Anderson Cancer Center, Houston, TX 77030;
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Bing Cai
§Division of Infectious Diseases, Department of Pediatrics, The University of British Columbia, Vancouver, British Columbia V6H 3V4, Canada;
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Ariane Alimenti
‖Department of Pediatrics, BC Women’s Hospital and Health Centre, The University of British Columbia, Vancouver, British Columbia V6H 3V4, Canada;
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Hélène C. F. Côté
#Department of Pathology and Laboratory Medicine, The University of British Columbia, Vancouver, British Columbia V6T 1Z7, Canada;
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Evelyn J. Maan
**Oak Tree Clinic, BC Women’s Hospital, Vancouver, British Columbia V5Z 0A7, Canada;
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Amy L. Slogrove
††Department of Paediatrics and Child Health, Faculty of Medicine and Health Sciences, Stellenbosch University, Worcester 6849, South Africa;
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Monika Esser
‡‡The Immunology Unit, Division of Medical Microbiology, Department of Pathology, National Health Laboratory Service, Stellenbosch University, Cape Town 7505, South Africa;
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Arnaud Marchant
§§Institut d’Immunologie Médicale, Université Libre de Bruxelles, Charleroi B-6041, Belgium;
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Tessa Goetghebuer
¶¶Département de Pédiatrie, Centre Hospitalier Universitaire St Pierre, Université Libre de Bruxelles, B-1000, Belgium;
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Casey P. Shannon
‖‖Prevention of Organ Failure Centre of Excellence, Centre for Heart Lung Innovation, St. Paul’s Hospital, The University of British Columbia, Vancouver, British Columbia V6Z 2K5, Canada;
##Centre for Heart Lung Innovation, St. Paul’s Hospital, The University of British Columbia, Vancouver, British Columbia V6Z 1Y6, Canada;
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Scott J. Tebbutt
‖‖Prevention of Organ Failure Centre of Excellence, Centre for Heart Lung Innovation, St. Paul’s Hospital, The University of British Columbia, Vancouver, British Columbia V6Z 2K5, Canada;
***Department of Medicine, Division of Respiratory Medicine, The University of British Columbia, Vancouver, British Columbia V5Z 1M9, Canada;
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Tobias R. Kollmann
†Telethon Kids Institute, Perth, Western Australia 6009, Australia;
§Division of Infectious Diseases, Department of Pediatrics, The University of British Columbia, Vancouver, British Columbia V6H 3V4, Canada;
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William W. Mohn
‡Department of Microbiology and Immunology, Life Sciences Institute, The University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada;
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Kinga K. Smolen
*Department of Experimental Medicine, The University of British Columbia, Vancouver, British Columbia V5Z 1M9, Canada;
†††Precision Vaccines Program, Division of Infectious Diseases, Boston Children's Hospital, Boston, MA 02115; and
‡‡‡Harvard Medical School, Boston, MA 02115
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Key Points

  • Innate immune and stool microbiome signatures of HEU children are region specific.

  • Differences in HEU immune responses were unrelated to the microbiome.

  • Future immune studies of HEU children must be studied across diverse settings.

Abstract

In both high- and low-income countries, HIV-negative children born to HIV-positive mothers (HIV exposed, uninfected [HEU]) are more susceptible to severe infection than HIV-unexposed, uninfected (HUU) children, with altered innate immunity hypothesized to be a cause. Both the gut microbiome and systemic innate immunity differ across biogeographically distinct settings, and the two are known to influence each other. And although the gut microbiome is influenced by HIV infection and may contribute to altered immunity, the biogeography of immune-microbiome correlations among HEU children have not been investigated. To address this, we compared the innate response and the stool microbiome of 2-y-old HEU and HUU children from Belgium, Canada, and South Africa to test the hypothesis that region-specific immune alterations directly correlate to differences in their stool microbiomes. We did not detect a universal immune or microbiome signature underlying differences between HEU versus HUU that was applicable to all children. But as hypothesized, population-specific differences in stool microbiomes were readily detected and included reduced abundances of short-chain fatty acid–producing bacteria in Canadian HEU children. Furthermore, we did not identify innate immune-microbiome associations that distinguished HEU from HUU children in any population. These findings suggest that maternal HIV infection is independently associated with differences in both innate immunity and the stool microbiome in a biogeographical population-specific way.

Footnotes

  • This work was supported by grants from the Canadian Institutes of Health Research (PJT-148781 and HET-85515) and The University of British Columbia (F0906208).

  • The sequences presented in this article have been submitted to the National Center for Biotechnology Information Sequence Read Archive (https://www.ncbi.nlm.nih.gov/bioproject/) under accession number PRJNA660015.

  • The online version of this article contains supplemental material.

  • Received January 14, 2020.
  • Accepted September 15, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

This article is distributed under The American Association of Immunologists, Inc., Reuse Terms and Conditions for Author Choice articles.

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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Innate Immune Responses and Gut Microbiomes Distinguish HIV-Exposed from HIV-Unexposed Children in a Population-Specific Manner
Nelly Amenyogbe, Pedro Dimitriu, Patricia Cho, Candice Ruck, Edgardo S. Fortuno, Bing Cai, Ariane Alimenti, Hélène C. F. Côté, Evelyn J. Maan, Amy L. Slogrove, Monika Esser, Arnaud Marchant, Tessa Goetghebuer, Casey P. Shannon, Scott J. Tebbutt, Tobias R. Kollmann, William W. Mohn, Kinga K. Smolen
The Journal of Immunology October 16, 2020, ji2000040; DOI: 10.4049/jimmunol.2000040

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Innate Immune Responses and Gut Microbiomes Distinguish HIV-Exposed from HIV-Unexposed Children in a Population-Specific Manner
Nelly Amenyogbe, Pedro Dimitriu, Patricia Cho, Candice Ruck, Edgardo S. Fortuno, Bing Cai, Ariane Alimenti, Hélène C. F. Côté, Evelyn J. Maan, Amy L. Slogrove, Monika Esser, Arnaud Marchant, Tessa Goetghebuer, Casey P. Shannon, Scott J. Tebbutt, Tobias R. Kollmann, William W. Mohn, Kinga K. Smolen
The Journal of Immunology October 16, 2020, ji2000040; DOI: 10.4049/jimmunol.2000040
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Print ISSN 0022-1767        Online ISSN 1550-6606