Complex mammalian-like haematopoietic system found in a colonial chordate

Nature. 2018 Dec;564(7736):425-429. doi: 10.1038/s41586-018-0783-x. Epub 2018 Dec 5.

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation
  • Cell Lineage
  • Cytotoxicity, Immunologic
  • Female
  • Flow Cytometry
  • Hematopoiesis*
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / immunology
  • Hematopoietic System / cytology*
  • Immunity, Cellular
  • Isoantigens / immunology
  • Male
  • Mammals / anatomy & histology
  • Mammals / blood*
  • Myeloid Cells / cytology
  • Myeloid Cells / immunology
  • Phagocytosis / immunology
  • Phylogeny*
  • Stem Cell Niche
  • Transcriptome / genetics
  • Urochordata / anatomy & histology
  • Urochordata / cytology*
  • Urochordata / genetics
  • Urochordata / immunology

Substances

  • Isoantigens