Tracing the evolutionary history of blood cells to the unicellular ancestor of animals.
Journal
Blood
ISSN: 1528-0020
Titre abrégé: Blood
Pays: United States
ID NLM: 7603509
Informations de publication
Date de publication:
15 12 2022
15 12 2022
Historique:
accepted:
26
08
2022
received:
11
03
2022
pubmed:
17
9
2022
medline:
20
12
2022
entrez:
16
9
2022
Statut:
ppublish
Résumé
Blood cells are thought to have emerged as phagocytes in the common ancestor of animals followed by the appearance of novel blood cell lineages such as thrombocytes, erythrocytes, and lymphocytes, during evolution. However, this speculation is not based on genetic evidence and it is still possible to argue that phagocytes in different species have different origins. It also remains to be clarified how the initial blood cells evolved; whether ancient animals have solely developed de novo programs for phagocytes or they have inherited a key program from ancestral unicellular organisms. Here, we traced the evolutionary history of blood cells, and cross-species comparison of gene expression profiles revealed that phagocytes in various animal species and Capsaspora (C.) owczarzaki, a unicellular organism, are transcriptionally similar to each other. We also found that both phagocytes and C. owczarzaki share a common phagocytic program, and that CEBPα is the sole transcription factor highly expressed in both phagocytes and C. owczarzaki. We further showed that the function of CEBPα to drive phagocyte program in nonphagocytic blood cells has been conserved in tunicate, sponge, and C. owczarzaki. We finally showed that, in murine hematopoiesis, repression of CEBPα to maintain nonphagocytic lineages is commonly achieved by polycomb complexes. These findings indicate that the initial blood cells emerged inheriting a unicellular organism program driven by CEBPα and that the program has also been seamlessly inherited in phagocytes of various animal species throughout evolution.
Identifiants
pubmed: 36112959
pii: S0006-4971(22)01277-0
doi: 10.1182/blood.2022016286
pmc: PMC10653094
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2611-2625Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022 by The American Society of Hematology.
Références
Genes Dev. 1998 Aug 1;12(15):2403-12
pubmed: 9694804
Mol Membr Biol. 1999 Apr-Jun;16(2):195-204
pubmed: 10417985
Science. 2011 Nov 25;334(6059):1091-7
pubmed: 22116879
Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13187-92
pubmed: 9371821
Nucleic Acids Res. 2019 Jan 8;47(D1):D780-D785
pubmed: 30395284
Anat Rec. 1992 Aug;233(4):543-6
pubmed: 1626713
Genome Biol. 2013 Feb 18;14(2):R15
pubmed: 23419129
Nat Immunol. 2006 Oct;7(10):1116-24
pubmed: 16980980
Nature. 2014 Mar 27;507(7493):462-70
pubmed: 24670764
Blood. 1992 Oct 1;80(7):1725-35
pubmed: 1391942
Nature. 2018 Dec;564(7736):425-429
pubmed: 30518860
Nature. 2011 Feb 3;470(7332):90-4
pubmed: 21293377
Genes Dev. 2016 Nov 15;30(22):2475-2485
pubmed: 27913604
Blood. 2006 Jun 1;107(11):4308-16
pubmed: 16469877
Science. 2016 Jun 3;352(6290):aad9780
pubmed: 27257261
Cell. 2016 May 19;165(5):1224-1237
pubmed: 27114036
Nature. 2004 Oct 14;431(7010):873-8
pubmed: 15386022
Mol Biol Evol. 2011 Mar;28(3):1241-1254
pubmed: 21087945
Biol Direct. 2009 Feb 26;4:9
pubmed: 19245710
Zoology (Jena). 2015 Feb;118(1):8-18
pubmed: 25547566
Elife. 2015 Oct 14;4:e08904
pubmed: 26465111
Front Immunol. 2021 May 07;12:637778
pubmed: 34025647
Immunity. 2004 Dec;21(6):853-63
pubmed: 15589173
Biochim Biophys Acta Mol Cell Biol Lipids. 2019 Jun;1864(6):932-940
pubmed: 30077006
Cell. 2006 Feb 24;124(4):815-22
pubmed: 16497590
J Invertebr Pathol. 1979 Mar;33(2):159-70
pubmed: 501126
Open Biol. 2021 Feb;11(2):200359
pubmed: 33622103
Mol Cell Biol. 1994 Jul;14(7):4947-57
pubmed: 8007990
Nature. 2004 Jul 8;430(6996):174-80
pubmed: 15241406
Nature. 2008 Apr 10;452(7188):768-72
pubmed: 18401412
J Immunol. 2007 Sep 15;179(6):3699-706
pubmed: 17785806
Int Rev Immunol. 2001 Feb;20(1):1-20
pubmed: 11342295
Trends Immunol. 2006 Apr;27(4):169-75
pubmed: 16515884
Curr Biol. 2012 Sep 11;22(17):R722-32
pubmed: 22975003
Nat Commun. 2013;4:2325
pubmed: 23942320
Elife. 2013 Dec 24;2:e01287
pubmed: 24368732
Nature. 2019 Jun;570(7762):519-522
pubmed: 31189954
J Immunol. 1999 Nov 1;163(9):4788-95
pubmed: 10528178
Int J Obes Relat Metab Disord. 2001 Sep;25(9):1275-80
pubmed: 11571587
Immunol Rev. 2010 Nov;238(1):23-36
pubmed: 20969582
Br J Haematol. 1971 Apr;20(4):427-35
pubmed: 5551218
Int Immunol. 1997 Jul;9(7):1011-9
pubmed: 9237110
Blood. 2003 Feb 1;101(3):961-9
pubmed: 12393459
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
Annu Rev Cell Dev Biol. 2006;22:677-712
pubmed: 16824014
Cell. 2013 Aug 29;154(5):1112-1126
pubmed: 23993099
Dev Comp Immunol. 2020 Feb;103:103519
pubmed: 31610182
Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):569-74
pubmed: 9012825
Philos Trans R Soc Lond B Biol Sci. 2002 Apr 29;357(1420):531-44
pubmed: 12028790
EMBO J. 2005 Dec 7;24(23):4052-60
pubmed: 16292344
Stem Cell Reports. 2017 Feb 14;8(2):346-359
pubmed: 28111277
Curr Biol. 2015 Sep 21;25(18):2404-10
pubmed: 26365255
Nature. 2021 Aug;596(7870):87-91
pubmed: 34321662
J Invertebr Pathol. 1980 Jan;35(1):26-33
pubmed: 7365267
Nat Cell Biol. 2018 Jul;20(7):836-846
pubmed: 29915358
Front Immunol. 2014 Sep 16;5:445
pubmed: 25278940
Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):297-354
pubmed: 11931142
Cell. 2004 May 28;117(5):663-76
pubmed: 15163413
Proc Natl Acad Sci U S A. 2017 Jun 6;114(23):5792-5799
pubmed: 28584084
Mol Biol Evol. 2012 Feb;29(2):531-44
pubmed: 21771718
Nat Rev Genet. 2017 Aug;18(8):498-512
pubmed: 28479598
FASEB J. 2021 Apr;35(4):e21443
pubmed: 33749877
Immunity. 2006 Nov;25(5):731-44
pubmed: 17088084
Zoolog Sci. 2005 Aug;22(8):837-43
pubmed: 16141696
Mamm Genome. 1994 Apr;5(4):211-5
pubmed: 8012110
J Immunol. 2002 Oct 1;169(7):3519-25
pubmed: 12244141
PLoS One. 2008 May 07;3(5):e2098
pubmed: 18461162
Development. 2004 Aug;131(16):4047-58
pubmed: 15269171
J Mol Evol. 2003 May;56(5):540-63
pubmed: 12698292
Mol Biol Evol. 2006 Jan;23(1):93-106
pubmed: 16151185
iScience. 2021 May 19;24(6):102551
pubmed: 34151224