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Multiple stages of evolutionary change in anthrax toxin receptor expression in humans

Author

Listed:
  • Lauren A. Choate

    (Cornell University
    Cornell University)

  • Gilad Barshad

    (Cornell University)

  • Pierce W. McMahon

    (Cornell University)

  • Iskander Said

    (Cornell University)

  • Edward J. Rice

    (Cornell University)

  • Paul R. Munn

    (Cornell University)

  • James J. Lewis

    (Cornell University)

  • Charles G. Danko

    (Cornell University
    Cornell University)

Abstract

The advent of animal husbandry and hunting increased human exposure to zoonotic pathogens. To understand how a zoonotic disease may have influenced human evolution, we study changes in human expression of anthrax toxin receptor 2 (ANTXR2), which encodes a cell surface protein necessary for Bacillus anthracis virulence toxins to cause anthrax disease. In immune cells, ANTXR2 is 8-fold down-regulated in all available human samples compared to non-human primates, indicating regulatory changes early in the evolution of modern humans. We also observe multiple genetic signatures consistent with recent positive selection driving a European-specific decrease in ANTXR2 expression in multiple tissues affected by anthrax toxins. Our observations fit a model in which humans adapted to anthrax disease following early ecological changes associated with hunting and scavenging, as well as a second period of adaptation after the rise of modern agriculture.

Suggested Citation

  • Lauren A. Choate & Gilad Barshad & Pierce W. McMahon & Iskander Said & Edward J. Rice & Paul R. Munn & James J. Lewis & Charles G. Danko, 2021. "Multiple stages of evolutionary change in anthrax toxin receptor expression in humans," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26854-z
    DOI: 10.1038/s41467-021-26854-z
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    References listed on IDEAS

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    1. Ryosuke Kimura & Akihiro Fujimoto & Katsushi Tokunaga & Jun Ohashi, 2007. "A Practical Genome Scan for Population-Specific Strong Selective Sweeps That Have Reached Fixation," PLOS ONE, Public Library of Science, vol. 2(3), pages 1-10, March.
    2. Michael Z. Ludwig & Casey Bergman & Nipam H. Patel & Martin Kreitman, 2000. "Evidence for stabilizing selection in a eukaryotic enhancer element," Nature, Nature, vol. 403(6769), pages 564-567, February.
    3. Fabian H. Leendertz & Heinz Ellerbrok & Christophe Boesch & Emmanuel Couacy-Hymann & Kerstin Mätz-Rensing & Regine Hakenbeck & Carina Bergmann & Pola Abaza & Sandra Junglen & Yasmin Moebius & Linda Vi, 2004. "Anthrax kills wild chimpanzees in a tropical rainforest," Nature, Nature, vol. 430(6998), pages 451-452, July.
    4. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    5. Constanze Hoffmann & Fee Zimmermann & Roman Biek & Hjalmar Kuehl & Kathrin Nowak & Roger Mundry & Anthony Agbor & Samuel Angedakin & Mimi Arandjelovic & Anja Blankenburg & Gregory Brazolla & Katherine, 2017. "Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest," Nature, Nature, vol. 548(7665), pages 82-86, August.
    6. Shihui Liu & Yi Zhang & Mahtab Moayeri & Jie Liu & Devorah Crown & Rasem J. Fattah & Alexander N. Wein & Zu-Xi Yu & Toren Finkel & Stephen H. Leppla, 2013. "Key tissue targets responsible for anthrax-toxin-induced lethality," Nature, Nature, vol. 501(7465), pages 63-68, September.
    7. Pardis C. Sabeti & Patrick Varilly & Ben Fry & Jason Lohmueller & Elizabeth Hostetter & Chris Cotsapas & Xiaohui Xie & Elizabeth H. Byrne & Steven A. McCarroll & Rachelle Gaudet & Stephen F. Schaffner, 2007. "Genome-wide detection and characterization of positive selection in human populations," Nature, Nature, vol. 449(7164), pages 913-918, October.
    8. Tae-Kyung Kim & Martin Hemberg & Jesse M. Gray & Allen M. Costa & Daniel M. Bear & Jing Wu & David A. Harmin & Mike Laptewicz & Kellie Barbara-Haley & Scott Kuersten & Eirene Markenscoff-Papadimitriou, 2010. "Widespread transcription at neuronal activity-regulated enhancers," Nature, Nature, vol. 465(7295), pages 182-187, May.
    9. Augustine Kong & Gudmar Thorleifsson & Daniel F. Gudbjartsson & Gisli Masson & Asgeir Sigurdsson & Aslaug Jonasdottir & G. Bragi Walters & Adalbjorg Jonasdottir & Arnaldur Gylfason & Kari Th. Kristins, 2010. "Fine-scale recombination rate differences between sexes, populations and individuals," Nature, Nature, vol. 467(7319), pages 1099-1103, October.
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