TY - JOUR
T1 - Complex mammalian-like haematopoietic system found in a colonial chordate
AU - Rosental, Benyamin
AU - Kowarsky, Mark
AU - Seita, Jun
AU - Corey, Daniel M.
AU - Ishizuka, Katherine J.
AU - Palmeri, Karla J.
AU - Chen, Shih Yu
AU - Sinha, Rahul
AU - Okamoto, Jennifer
AU - Mantalas, Gary
AU - Manni, Lucia
AU - Raveh, Tal
AU - Clarke, D. Nathaniel
AU - Tsai, Jonathan M.
AU - Newman, Aaron M.
AU - Neff, Norma F.
AU - Nolan, Garry P.
AU - Quake, Stephen R.
AU - Weissman, Irving L.
AU - Voskoboynik, Ayelet
N1 - Funding Information: Acknowledgements We thank C. Lowe, C. Anselmi, I. Dimov, S. Karten, C. Patton, J. Thompson, P. Lovelace, R. Voskoboynik, N. Fernhoff, W.-J. Lu, P. Chu, K. Weiskopf, M. Oren, B. Wang, J. Lee, B. Compton, K. Uhlinger, T. Naik and T. Storm for technical advice and help. This study was supported by NIH grants R56AI089968, R01AG037968 and RO1GM100315 (to I.L.W., S.R.Q., and A.V.), the Virginia and D. K. Ludwig Fund for Cancer Research, a grant from the Siebel Stem Cell Institute and a Stinehart-Reed grant (to I.L.W.). L.M. was supported by PRIN - Prot. 2015NSFHXF. B.R. was supported by a Postdoctoral Fellowship of the Human Frontier Science Program Organization LT000591/2014-L, NIH Immunology training grant 5T32AI07290-28 and NIH Hematology training grant T32 HL120824-03. Publisher Copyright: © 2018, Springer Nature Limited.
PY - 2018/12/20
Y1 - 2018/12/20
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85058870446&partnerID=8YFLogxK
U2 - https://doi.org/10.1038/s41586-018-0783-x
DO - https://doi.org/10.1038/s41586-018-0783-x
M3 - Article
C2 - 30518860
SN - 0028-0836
VL - 564
SP - 425
EP - 429
JO - Nature
JF - Nature
IS - 7736
ER -