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CD36 homologs determine microbial resistance to the Lyme disease spirochete

View ORCID ProfileAnya J. O’Neal, Nisha Singh, View ORCID ProfileIain S. Forrest, Agustin Rolandelli, Xiaowei Wang, View ORCID ProfileDana K. Shaw, Brianna D. Young, View ORCID ProfileSukanya Narasimhan, Shraboni Dutta, Greg A. Snyder, Liron Marnin, View ORCID ProfileL. Rainer Butler, View ORCID ProfileSourabh Samaddar, M. Tays Mendes, Francy E. Cabrera Paz, Luisa M. Valencia, View ORCID ProfileEric J. Sundberg, Erol Fikrig, View ORCID ProfileUtpal Pal, David J. Weber, View ORCID ProfileRon Do, View ORCID ProfileJoao H.F. Pedra
doi: https://doi.org/10.1101/2022.02.09.479763
Anya J. O’Neal
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Nisha Singh
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Iain S. Forrest
2Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA
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Agustin Rolandelli
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Xiaowei Wang
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Dana K. Shaw
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Brianna D. Young
3Center for Biomolecular Therapeutics, Department of Biochemistry and Molecular Biology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Sukanya Narasimhan
4Section of Infectious Diseases, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, 06510, USA
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Shraboni Dutta
5Department of Veterinary Medicine, University of Maryland, College Park, MD, 20742, USA
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Greg A. Snyder
6Institute of Human Virology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Liron Marnin
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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L. Rainer Butler
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Sourabh Samaddar
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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M. Tays Mendes
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Francy E. Cabrera Paz
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Luisa M. Valencia
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Eric J. Sundberg
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
6Institute of Human Virology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Erol Fikrig
4Section of Infectious Diseases, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, 06510, USA
7Howard Hughes Medical Institute, Chevy Chase, Maryland, USA
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Utpal Pal
5Department of Veterinary Medicine, University of Maryland, College Park, MD, 20742, USA
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David J. Weber
3Center for Biomolecular Therapeutics, Department of Biochemistry and Molecular Biology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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Ron Do
2Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA
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Joao H.F. Pedra
1Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA
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  • For correspondence: jpedra@som.umaryland.edu
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Abstract

Pattern recognition receptors sense pathogens in arthropods and mammals through distinct immune processes. Whether these molecules share a similar function and recognize the same microbe in evolutionarily distant species remain ill-defined. Here, we establish that the CD36 superfamily is required for Borrelia burgdorferi resistance in both the arthropod vector and humans. Using the blacklegged tick Ixodes scapularis and an electronic health record-linked biobank, we demonstrate that CD36 members elicit immunity to the Lyme disease spirochete. In ticks, the CD36-like protein Croquemort recognizes lipids and initiates the immune deficiency and jun N-terminal kinase pathways against B. burgdorferi. In humans, exome sequencing and clinical information reveal that individuals with CD36 loss-of-function variants have increased prevalence of Lyme disease. Altogether, we discovered a conserved mechanism of anti-bacterial immunity.

One Sentence Summary Lipid receptors belonging to the CD36 superfamily exhibit a shared immune function in both ticks and humans.

Competing Interest Statement

Ron Do reported receiving grants from AstraZeneca, research grants and non-financial support from Goldfinch Bio. Ron Do is also a scientific co-founder, consultant and equity holder (pending) for Pensieve Health and a consultant for Variant Bio. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted February 10, 2022.
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CD36 homologs determine microbial resistance to the Lyme disease spirochete
Anya J. O’Neal, Nisha Singh, Iain S. Forrest, Agustin Rolandelli, Xiaowei Wang, Dana K. Shaw, Brianna D. Young, Sukanya Narasimhan, Shraboni Dutta, Greg A. Snyder, Liron Marnin, L. Rainer Butler, Sourabh Samaddar, M. Tays Mendes, Francy E. Cabrera Paz, Luisa M. Valencia, Eric J. Sundberg, Erol Fikrig, Utpal Pal, David J. Weber, Ron Do, Joao H.F. Pedra
bioRxiv 2022.02.09.479763; doi: https://doi.org/10.1101/2022.02.09.479763
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CD36 homologs determine microbial resistance to the Lyme disease spirochete
Anya J. O’Neal, Nisha Singh, Iain S. Forrest, Agustin Rolandelli, Xiaowei Wang, Dana K. Shaw, Brianna D. Young, Sukanya Narasimhan, Shraboni Dutta, Greg A. Snyder, Liron Marnin, L. Rainer Butler, Sourabh Samaddar, M. Tays Mendes, Francy E. Cabrera Paz, Luisa M. Valencia, Eric J. Sundberg, Erol Fikrig, Utpal Pal, David J. Weber, Ron Do, Joao H.F. Pedra
bioRxiv 2022.02.09.479763; doi: https://doi.org/10.1101/2022.02.09.479763

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