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Complex mammalian-like haematopoietic system found in a colonial chordate

Author

Listed:
  • Benyamin Rosental

    (Stanford University School of Medicine
    Stanford University, Hopkins Marine Station)

  • Mark Kowarsky

    (Stanford University)

  • Jun Seita

    (Stanford University School of Medicine
    Medical Sciences Innovation Hub Program, RIKEN)

  • Daniel M. Corey

    (Stanford University School of Medicine)

  • Katherine J. Ishizuka

    (Stanford University School of Medicine
    Stanford University, Hopkins Marine Station)

  • Karla J. Palmeri

    (Stanford University School of Medicine
    Stanford University, Hopkins Marine Station)

  • Shih-Yu Chen

    (Stanford University School of Medicine)

  • Rahul Sinha

    (Stanford University School of Medicine)

  • Jennifer Okamoto

    (Chan Zuckerberg Biohub)

  • Gary Mantalas

    (Stanford University
    University of California Santa Cruz)

  • Lucia Manni

    (Università degli Studi di Padova)

  • Tal Raveh

    (Stanford University School of Medicine)

  • D. Nathaniel Clarke

    (Stanford University, Hopkins Marine Station)

  • Jonathan M. Tsai

    (Stanford University School of Medicine)

  • Aaron M. Newman

    (Stanford University School of Medicine)

  • Norma F. Neff

    (Chan Zuckerberg Biohub)

  • Garry P. Nolan

    (Stanford University School of Medicine)

  • Stephen R. Quake

    (Chan Zuckerberg Biohub
    Stanford University)

  • Irving L. Weissman

    (Stanford University School of Medicine
    Stanford University, Hopkins Marine Station
    Stanford University School of Medicine)

  • Ayelet Voskoboynik

    (Stanford University School of Medicine
    Stanford University, Hopkins Marine Station)

Abstract

Haematopoiesis is an essential process that evolved in multicellular animals. At the heart of this process are haematopoietic stem cells (HSCs), which are multipotent and self-renewing, and generate the entire repertoire of blood and immune cells throughout an animal’s life1. Although there have been comprehensive studies on self-renewal, differentiation, physiological regulation and niche occupation in vertebrate HSCs, relatively little is known about the evolutionary origin and niches of these cells. Here we describe the haematopoietic system of Botryllus schlosseri, a colonial tunicate that has a vasculature and circulating blood cells, and interesting stem-cell biology and immunity characteristics2–8. Self-recognition between genetically compatible B. schlosseri colonies leads to the formation of natural parabionts with shared circulation, whereas incompatible colonies reject each other3,4,7. Using flow cytometry, whole-transcriptome sequencing of defined cell populations and diverse functional assays, we identify HSCs, progenitors, immune effector cells and an HSC niche, and demonstrate that self-recognition inhibits allospecific cytotoxic reactions. Our results show that HSC and myeloid lineage immune cells emerged in a common ancestor of tunicates and vertebrates, and also suggest that haematopoietic bone marrow and the B. schlosseri endostyle niche evolved from a common origin.

Suggested Citation

  • Benyamin Rosental & Mark Kowarsky & Jun Seita & Daniel M. Corey & Katherine J. Ishizuka & Karla J. Palmeri & Shih-Yu Chen & Rahul Sinha & Jennifer Okamoto & Gary Mantalas & Lucia Manni & Tal Raveh & D, 2018. "Complex mammalian-like haematopoietic system found in a colonial chordate," Nature, Nature, vol. 564(7736), pages 425-429, December.
  • Handle: RePEc:nat:nature:v:564:y:2018:i:7736:d:10.1038_s41586-018-0783-x
    DOI: 10.1038/s41586-018-0783-x
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