IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41184-y.html
   My bibliography  Save this article

Sinus venosus adaptation models prolonged cardiovascular disease and reveals insights into evolutionary transitions of the vertebrate heart

Author

Listed:
  • Jacob T. Gafranek

    (University of Cincinnati College of Medicine
    Cincinnati Children’s Hospital Medical Center)

  • Enrico D’Aniello

    (Stazione Zoologica Anton Dohrn)

  • Padmapriyadarshini Ravisankar

    (Cincinnati Children’s Hospital Medical Center)

  • Kairavee Thakkar

    (Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine)

  • Ronald J. Vagnozzi

    (University of Colorado Anschutz Medical Campus)

  • Hee-Woong Lim

    (Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine)

  • Nathan Salomonis

    (Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine)

  • Joshua S. Waxman

    (Cincinnati Children’s Hospital Medical Center
    University of Cincinnati, College of Medicine
    Cincinnati Children’s Hospital Medical Center)

Abstract

How two-chambered hearts in basal vertebrates have evolved from single-chamber hearts found in ancestral chordates remains unclear. Here, we show that the teleost sinus venosus (SV) is a chamber-like vessel comprised of an outer layer of smooth muscle cells. We find that in adult zebrafish nr2f1a mutants, which lack atria, the SV comes to physically resemble the thicker bulbus arteriosus (BA) at the arterial pole of the heart through an adaptive, hypertensive response involving smooth muscle proliferation due to aberrant hemodynamic flow. Single cell transcriptomics show that smooth muscle and endothelial cell populations within the adapting SV also take on arterial signatures. Bulk transcriptomics of the blood sinuses flanking the tunicate heart reinforce a model of greater equivalency in ancestral chordate BA and SV precursors. Our data simultaneously reveal that secondary complications from congenital heart defects can develop in adult zebrafish similar to those in humans and that the foundation of equivalency between flanking auxiliary vessels may remain latent within basal vertebrate hearts.

Suggested Citation

  • Jacob T. Gafranek & Enrico D’Aniello & Padmapriyadarshini Ravisankar & Kairavee Thakkar & Ronald J. Vagnozzi & Hee-Woong Lim & Nathan Salomonis & Joshua S. Waxman, 2023. "Sinus venosus adaptation models prolonged cardiovascular disease and reveals insights into evolutionary transitions of the vertebrate heart," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41184-y
    DOI: 10.1038/s41467-023-41184-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41184-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41184-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Li-Ru You & Fu-Jung Lin & Christopher T. Lee & Francesco J. DeMayo & Ming-Jer Tsai & Sophia Y. Tsai, 2005. "Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity," Nature, Nature, vol. 435(7038), pages 98-104, May.
    2. Rui Diogo & Robert G. Kelly & Lionel Christiaen & Michael Levine & Janine M. Ziermann & Julia L. Molnar & Drew M. Noden & Eldad Tzahor, 2015. "A new heart for a new head in vertebrate cardiopharyngeal evolution," Nature, Nature, vol. 520(7548), pages 466-473, April.
    3. Yong Zhou & Timothy J. Cashman & Kathleen R. Nevis & Pablo Obregon & Sara A. Carney & Yan Liu & Aihua Gu & Christian Mosimann & Samuel Sondalle & Richard E. Peterson & Warren Heideman & Caroline E. Bu, 2011. "Latent TGF-β binding protein 3 identifies a second heart field in zebrafish," Nature, Nature, vol. 474(7353), pages 645-648, June.
    4. Sven Reischauer & Oliver A. Stone & Alethia Villasenor & Neil Chi & Suk-Won Jin & Marcel Martin & Miler T. Lee & Nana Fukuda & Michele Marass & Alec Witty & Ian Fiddes & Taiyi Kuo & Won-Suk Chung & Sh, 2016. "Cloche is a bHLH-PAS transcription factor that drives haemato-vascular specification," Nature, Nature, vol. 535(7611), pages 294-298, July.
    5. Anastasia Felker & Karin D. Prummel & Anne M. Merks & Michaela Mickoleit & Eline C. Brombacher & Jan Huisken & Daniela Panáková & Christian Mosimann, 2018. "Continuous addition of progenitors forms the cardiac ventricle in zebrafish," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Karin D. Prummel & Helena L. Crowell & Susan Nieuwenhuize & Eline C. Brombacher & Stephan Daetwyler & Charlotte Soneson & Jelena Kresoja-Rakic & Agnese Kocere & Manuel Ronner & Alexander Ernst & Zahra, 2022. "Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    2. Hiroko Nomaru & Yang Liu & Christopher De Bono & Dario Righelli & Andrea Cirino & Wei Wang & Hansoo Song & Silvia E. Racedo & Anelisa G. Dantas & Lu Zhang & Chen-Leng Cai & Claudia Angelini & Lionel C, 2021. "Single cell multi-omic analysis identifies a Tbx1-dependent multilineage primed population in murine cardiopharyngeal mesoderm," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Brendan Evano & Diljeet Gill & Irene Hernando-Herraez & Glenda Comai & Thomas M Stubbs & Pierre-Henri Commere & Wolf Reik & Shahragim Tajbakhsh, 2020. "Transcriptome and epigenome diversity and plasticity of muscle stem cells following transplantation," PLOS Genetics, Public Library of Science, vol. 16(10), pages 1-21, October.
    4. Susanne Fleig & Tamar Kapanadze & Jeremiah Bernier-Latmani & Julia K. Lill & Tania Wyss & Jaba Gamrekelashvili & Dustin Kijas & Bin Liu & Anne M. Hüsing & Esther Bovay & Adan Chari Jirmo & Stephan Hal, 2022. "Loss of vascular endothelial notch signaling promotes spontaneous formation of tertiary lymphoid structures," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Thanh Theresa Dinh & Menglan Xiang & Anusha Rajaraman & Yongzhi Wang & Nicole Salazar & Yu Zhu & Walter Roper & Siyeon Rhee & Kevin Brulois & Ed O’Hara & Helena Kiefel & Truc M. Dinh & Yuhan Bi & Dali, 2022. "An NKX-COUP-TFII morphogenetic code directs mucosal endothelial addressin expression," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Xavier Grau-Bové & Lucie Subirana & Lydvina Meister & Anaël Soubigou & Ana Neto & Anamaria Elek & Silvia Naranjo & Oscar Fornas & Jose Luis Gomez-Skarmeta & Juan J. Tena & Manuel Irimia & Stéphanie Be, 2024. "An amphioxus neurula stage cell atlas supports a complex scenario for the emergence of vertebrate head mesoderm," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41184-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.