Specialized impulse conduction pathway in the alligator heart

  1. Bjarke Jensen
  2. Bastiaan JD Boukens
  3. Dane A Crossley
  4. Justin Conner
  5. Rajiv Ahmet Mohan
  6. Karel van Duijvenboden
  7. Alex V Postma
  8. Christopher R Gloschat
  9. Ruth M Elsey
  10. David Sedmera
  11. Igor R Efimov
  12. Vincent M Christoffels  Is a corresponding author
  1. Academic Medical Center, University of Amsterdam, Netherlands
  2. University of North Texas, United States
  3. George Washington University, United States
  4. Rockefeller Wildlife Refuge, United States
  5. Charles University, Czech Republic

Abstract

Mammals and birds have a specialized cardiac atrioventricular conduction system enabling rapid activation of both ventricles. This system may have evolved together with high heart rates to support their endothermic state (warm-bloodedness), and is seemingly lacking in ectothermic vertebrates from which first mammals then birds independently evolved. Here, we studied the conduction system in crocodiles (Alligator mississippiensis), the only ectothermic vertebrates with a full ventricular septum. We identified homologues of mammalian conduction system markers (Tbx3-Tbx5, Scn5a, Gja5, Nppa-Nppb) and show the presence of a functional atrioventricular bundle. The ventricular Purkinje network, however, was absent and slow ventricular conduction relied on trabecular myocardium, as it does in other ectothermic vertebrates. We propose the evolution of the atrioventricular bundle followed full ventricular septum formation prior to the development of high heart rates and endothermy. In contrast, the evolution of the ventricular Purkinje network is strongly associated with high heart rates and endothermy.

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Article and author information

Author details

  1. Bjarke Jensen

    Department of Medical Biology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7750-8035
  2. Bastiaan JD Boukens

    Department of Medical Biology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Dane A Crossley

    Department of Biological Sciences, University of North Texas, Denton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Justin Conner

    Department of Biological Sciences, University of North Texas, Denton, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Rajiv Ahmet Mohan

    Department of Medical Biology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3622-1759
  6. Karel van Duijvenboden

    Department of Medical Biology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Alex V Postma

    Department of Medical Biology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Christopher R Gloschat

    Department of Biomedical Engineering, George Washington University, Washington DC, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Ruth M Elsey

    Louisiana Department of Wildlife and Fisheries, Rockefeller Wildlife Refuge, Grand Chenier, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. David Sedmera

    Institute of Anatomy, First Medical Faculty, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  11. Igor R Efimov

    Department of Biomedical Engineering, George Washington University, Washington DC, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1483-5039
  12. Vincent M Christoffels

    Department of Medical Biology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    For correspondence
    v.m.christoffels@amc.uva.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4131-2636

Funding

Carlsbergfondet

  • Bjarke Jensen

Fondation Leducq

  • Vincent M Christoffels

CVON HUSTCARE

  • Vincent M Christoffels

Netherlands Heart Foundation (COBRA3)

  • Vincent M Christoffels

Netherlands Heart Foundation (2016T047)

  • Bastiaan JD Boukens

CVON2014-2018 (CONCOR-genes)

  • Alex V Postma

CVON2014-2018 (CONCOR-genes)

  • Vincent M Christoffels

Czech Science Foundation (16-02972S)

  • David Sedmera

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The investigation conforms with the guide for the Care and Use of Laboratory Animals published by the US National Institutes of Health (NIH Publication No. 8523, revised 1996) and was approved by the Institutional Animal Studies Care and Use Committee of the University of North Texas (IACUC #1403-04).

Reviewing Editor

  1. Deborah Yelon, University of California, San Diego, United States

Version history

  1. Received: September 19, 2017
  2. Accepted: March 20, 2018
  3. Accepted Manuscript published: March 22, 2018 (version 1)
  4. Version of Record published: May 8, 2018 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Bjarke Jensen
  2. Bastiaan JD Boukens
  3. Dane A Crossley
  4. Justin Conner
  5. Rajiv Ahmet Mohan
  6. Karel van Duijvenboden
  7. Alex V Postma
  8. Christopher R Gloschat
  9. Ruth M Elsey
  10. David Sedmera
  11. Igor R Efimov
  12. Vincent M Christoffels
(2018)
Specialized impulse conduction pathway in the alligator heart
eLife 7:e32120.
https://doi.org/10.7554/eLife.32120

Share this article

https://doi.org/10.7554/eLife.32120

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