Complex mammalian-like haematopoietic system found in a colonial chordate

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. Nathaniel Clarke, Jonathan M. Tsai, Aaron M. Newman, Norma F. Neff, Garry P. Nolan, Stephen R. Quake, Irving L. Weissman () and Ayelet Voskoboynik ()
Additional contact information
Benyamin Rosental: Stanford University School of Medicine
Mark Kowarsky: Stanford University
Jun Seita: Stanford University School of Medicine
Daniel M. Corey: Stanford University School of Medicine
Katherine J. Ishizuka: Stanford University School of Medicine
Karla J. Palmeri: Stanford University School of Medicine
Shih-Yu Chen: Stanford University School of Medicine
Rahul Sinha: Stanford University School of Medicine
Jennifer Okamoto: Chan Zuckerberg Biohub
Gary Mantalas: Stanford University
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
Irving L. Weissman: Stanford University School of Medicine
Ayelet Voskoboynik: Stanford University School of Medicine

Nature, 2018, vol. 564, issue 7736, 425-429

Abstract: 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.

Keywords: Schlosseri; Endostyle; Compatible Colonies; Morula Cells; Carboxyfluorescein Succinimidyl Ester (CFSE) (search for similar items in EconPapers)
Date: 2018
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DOI: 10.1038/s41586-018-0783-x

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