IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34991-2.html
   My bibliography  Save this article

An NKX-COUP-TFII morphogenetic code directs mucosal endothelial addressin expression

Author

Listed:
  • Thanh Theresa Dinh

    (Stanford University School of Medicine
    Palo Alto Veterans Institute for Research)

  • Menglan Xiang

    (Stanford University School of Medicine
    Palo Alto Veterans Institute for Research)

  • Anusha Rajaraman

    (Stanford University School of Medicine
    Palo Alto Veterans Institute for Research
    Vrije Universiteit Medical Center)

  • Yongzhi Wang

    (Stanford University School of Medicine
    Lund University)

  • Nicole Salazar

    (Stanford University School of Medicine)

  • Yu Zhu

    (Stanford University School of Medicine)

  • Walter Roper

    (Columbia University Vagelos College of Physicians and Surgeons)

  • Siyeon Rhee

    (Stanford University)

  • Kevin Brulois

    (Stanford University School of Medicine
    Palo Alto Veterans Institute for Research)

  • Ed O’Hara

    (Palo Alto Veterans Institute for Research)

  • Helena Kiefel

    (Stanford University School of Medicine)

  • Truc M. Dinh

    (Palo Alto Veterans Institute for Research)

  • Yuhan Bi

    (Stanford University School of Medicine
    Palo Alto Veterans Institute for Research)

  • Dalila Gonzalez

    (University of California, San Diego)

  • Evan P. Bao

    (Palo Alto Veterans Institute for Research)

  • Kristy Red-Horse

    (Stanford University
    Stanford University School of Medicine
    Howard Hughes Medical Institute)

  • Peter Balogh

    (University of Pécs Medical School
    Lymphoid Organogenesis Research Team, Szentágothai Research Center)

  • Fanni Gábris

    (University of Pécs Medical School
    Lymphoid Organogenesis Research Team, Szentágothai Research Center)

  • Balázs Gaszner

    (University of Pécs Medical School)

  • Gergely Berta

    (University of Pécs Medical School)

  • Junliang Pan

    (Palo Alto Veterans Institute for Research
    The Center for Molecular Biology and Medicine, Veterans Affairs Palo Alto Health Care System)

  • Eugene C. Butcher

    (Stanford University School of Medicine
    Palo Alto Veterans Institute for Research
    The Center for Molecular Biology and Medicine, Veterans Affairs Palo Alto Health Care System)

Abstract

Immunoglobulin family and carbohydrate vascular addressins encoded by Madcam1 and St6gal1 control lymphocyte homing into intestinal tissues, regulating immunity and inflammation. The addressins are developmentally programmed to decorate endothelial cells lining gut post-capillary and high endothelial venules (HEV), providing a prototypical example of organ- and segment-specific endothelial specialization. We identify conserved NKX-COUP-TFII composite elements (NCCE) in regulatory regions of Madcam1 and St6gal1 that bind intestinal homeodomain protein NKX2-3 cooperatively with venous nuclear receptor COUP-TFII to activate transcription. The Madcam1 element also integrates repressive signals from arterial/capillary Notch effectors. Pan-endothelial COUP-TFII overexpression induces ectopic addressin expression in NKX2-3+ capillaries, while NKX2-3 deficiency abrogates expression by HEV. Phylogenetically conserved NCCE are enriched in genes involved in neuron migration and morphogenesis of the heart, kidney, pancreas and other organs. Our results define an NKX-COUP-TFII morphogenetic code that targets expression of mucosal vascular addressins.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34991-2
    DOI: 10.1038/s41467-022-34991-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34991-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34991-2?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. Kevin Brulois & Anusha Rajaraman & Agata Szade & Sofia Nordling & Ania Bogoslowski & Denis Dermadi & Milladur Rahman & Helena Kiefel & Edward O’Hara & Jasper J. Koning & Hiroto Kawashima & Bin Zhou & , 2020. "A molecular map of murine lymph node blood vascular endothelium at single cell resolution," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    3. San-Pin Wu & Chung-Yang Kao & Leiming Wang & Chad J. Creighton & Jin Yang & Taraka R. Donti & Romain Harmancey & Hernan G. Vasquez & Brett H. Graham & Hugo J. Bellen & Heinrich Taegtmeyer & Ching-Pin , 2015. "Increased COUP-TFII expression in adult hearts induces mitochondrial dysfunction resulting in heart failure," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    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. 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.
    2. Gopal Chovatiya & Kefei Nina Li & Jonathan Li & Sangeeta Ghuwalewala & Tudorita Tumbar, 2023. "Alk1 acts in non-endothelial VE-cadherin+ perineurial cells to maintain nerve branching during hair homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. 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.
    4. Huihui Liu & Hongchao Liu & Longhao Wang & Lei Song & Guixian Jiang & Qing Lu & Tao Yang & Hu Peng & Ruijie Cai & Xingle Zhao & Ting Zhao & Hao Wu, 2023. "Cochlear transcript diversity and its role in auditory functions implied by an otoferlin short isoform," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Vincent Geldhof & Laura P. M. H. Rooij & Liliana Sokol & Jacob Amersfoort & Maxim Schepper & Katerina Rohlenova & Griet Hoste & Adriaan Vanderstichele & Anne-Marie Delsupehe & Edoardo Isnaldi & Naima , 2022. "Single cell atlas identifies lipid-processing and immunomodulatory endothelial cells in healthy and malignant breast," Nature Communications, Nature, vol. 13(1), pages 1-19, 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:13:y:2022:i:1:d:10.1038_s41467-022-34991-2. 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.