Exploring Transcriptomic Landscapes in Red Blood Cells, in Their Extracellular Vesicles and on a Single-Cell Level.


Journal

International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791

Informations de publication

Date de publication:
25 Oct 2022
Historique:
received: 26 08 2022
revised: 29 09 2022
accepted: 29 09 2022
entrez: 11 11 2022
pubmed: 12 11 2022
medline: 15 11 2022
Statut: epublish

Résumé

Being enucleated, RBCs lack typical transcriptomes, but are known to contain small amounts of diverse long transcripts and microRNAs. However, the exact role and importance of these RNAs are lacking. Shedding of extracellular vesicles (EVs) from the plasma membrane constitutes an integral mechanism of RBC homeostasis, by which RBCs remove unnecessary cytoplasmic content and cell membrane. To study this further, we explored the transcriptomes of RBCs and extracellular vesicles (EVs) of RBCs using next-generation sequencing. Furthermore, we performed single-cell RNA sequencing on RBCs, which revealed that approximately 10% of the cells contained detectable levels of mRNA and cells formed three subpopulations based on their transcriptomes. A decrease in the mRNA quantity was observed across the populations. Qualitative changes included the differences in the globin transcripts and changes in the expression of ribosomal genes. A specific splice form of a long non-coding RNA, Metastasis Associated Lung Adenocarcinoma Transcript 1 (MALAT1), was the most enriched marker in one subpopulation of RBCs, co-expressing with ribosomal structural transcripts. MALAT1 expression was confirmed by qPCR in CD71-enriched reticulocytes, which were also characterized with imaging flow cytometry at the single cell level. Analysis of the RBC transcriptome shows enrichment of pathways and functional categories required for the maturation of reticulocytes and erythrocyte functions. The RBC transcriptome was detected in their EVs, making these transcripts available for intercellular communication in blood.

Identifiants

pubmed: 36361688
pii: ijms232112897
doi: 10.3390/ijms232112897
pmc: PMC9657499
pii:
doi:

Substances chimiques

RNA, Long Noncoding 0
RNA, Messenger 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Références

Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Blood. 1996 Jun 15;87(12):5314-23
pubmed: 8652847
Blood. 2011 Oct 6;118(14):e101-11
pubmed: 21596849
PLoS One. 2011;6(7):e22838
pubmed: 21829531
Exp Hematol. 2015 May;43(5):382-392
pubmed: 25681748
Wiley Interdiscip Rev RNA. 2011 Jul-Aug;2(4):582-600
pubmed: 21957046
Transfus Apher Sci. 2016 Aug;55(1):92-104
pubmed: 27452642
Nat Biotechnol. 2015 May;33(5):495-502
pubmed: 25867923
RNA. 2002 Dec;8(12):1526-37
pubmed: 12515385
RNA Biol. 2014;11(11):1335-9
pubmed: 25692232
Blood. 2012 Jun 28;119(26):6296-306
pubmed: 22490681
Blood. 2014 Jan 23;123(4):570-81
pubmed: 24200680
BMC Genomics. 2015 Sep 03;16:676
pubmed: 26335021
Cell. 2015 May 21;161(5):1202-1214
pubmed: 26000488
Blood. 1989 Oct;74(5):1844-51
pubmed: 2790208
Nat Methods. 2017 Jul;14(7):687-690
pubmed: 28581496
Nucleic Acids Res. 2002 Jan 1;30(1):207-10
pubmed: 11752295
Front Physiol. 2022 Apr 20;13:828700
pubmed: 35514346
Blood. 2013 Jun 13;121(24):4842-6
pubmed: 23645840
Blood. 2008 Aug 15;112(4):1493-502
pubmed: 18539900
Br J Haematol. 1974 Dec;28(4):463-70
pubmed: 4455300
J Extracell Vesicles. 2013 Dec 23;2:
pubmed: 24376909
Thromb Haemost. 2001 Apr;85(4):639-46
pubmed: 11341498
Biochim Biophys Acta. 2015 Oct;1853(10 Pt B):2775-83
pubmed: 25753537
Cell Tissue Res. 1982;224(2):397-408
pubmed: 7105141
J Biol Chem. 1987 Jul 5;262(19):9412-20
pubmed: 3597417
Autophagy. 2012 Sep;8(9):1325-32
pubmed: 22906961
J Biol Chem. 2009 Dec 4;284(49):34211-22
pubmed: 19801663
Cell. 1976 Aug;8(4):495-503
pubmed: 954102
J Mol Biol. 1977 Feb 25;110(2):191-203
pubmed: 845950
Curr Opin Hematol. 2011 May;18(3):152-7
pubmed: 21423015
Br J Haematol. 2018 Jan;180(1):118-133
pubmed: 29094334
Blood. 2011 Dec 8;118(24):6258-68
pubmed: 21998215
Biochim Biophys Acta Mol Cell Biol Lipids. 2018 Jan;1863(1):1-8
pubmed: 28965917
PLoS One. 2013 Oct 08;8(10):e76062
pubmed: 24116088
Cell. 1976 Jan;7(1):59-65
pubmed: 949743
BMC Genomics. 2015 Nov 16;16:952
pubmed: 26573221
Cell. 2008 Nov 28;135(5):919-32
pubmed: 19041754
Cells. 2022 Aug 03;11(15):
pubmed: 35954235
PLoS One. 2008 Jun 04;3(6):e2360
pubmed: 18523662
Nat Cell Biol. 2007 Jun;9(6):654-9
pubmed: 17486113
J Extracell Vesicles. 2015 May 14;4:27066
pubmed: 25979354
Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):E10018-E10027
pubmed: 29087317
Blood. 2010 Mar 11;115(10):2021-7
pubmed: 20038785
Neuroscience. 2017 Jun 23;354:1-10
pubmed: 28433650
Br J Haematol. 1992 Jul;81(3):432-9
pubmed: 1382547
Physiol Genomics. 2007 Jul 18;30(2):172-8
pubmed: 17405831
Exp Biol Med (Maywood). 2003 Apr;228(4):387-95
pubmed: 12671183
Mol Cell Biol. 2006 Mar;26(6):2419-29
pubmed: 16508016
RNA. 2016 Jun;22(6):867-82
pubmed: 27090285
Dev Cell. 2014 Sep 29;30(6):688-700
pubmed: 25241935
Nat Commun. 2017 Jan 16;8:14049
pubmed: 28091601
Nucleic Acids Res. 2004 Jan 1;32(Database issue):D572-4
pubmed: 14681483
Elife. 2014 Sep 08;3:e01913
pubmed: 25201874
Haematologica. 2004 Dec;89(12):1434-8
pubmed: 15590392
Brief Bioinform. 2013 Mar;14(2):178-92
pubmed: 22517427
Nature. 2008 Jul 10;454(7201):232-5
pubmed: 18454133

Auteurs

Erja Kerkelä (E)

Finnish Red Cross Blood Service, Kivihaantie 7, 00310 Helsinki, Finland.

Jenni Lahtela (J)

Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Tukholmankatu 8, 00290 Helsinki, Finland.

Antti Larjo (A)

Finnish Red Cross Blood Service, Kivihaantie 7, 00310 Helsinki, Finland.

Ulla Impola (U)

Finnish Red Cross Blood Service, Kivihaantie 7, 00310 Helsinki, Finland.

Laura Mäenpää (L)

Research Programs Unit, Molecular Neurology, University of Helsinki, Tukholmankatu 8, 00290 Helsinki, Finland.

Pirkko Mattila (P)

Finnish Red Cross Blood Service, Kivihaantie 7, 00310 Helsinki, Finland.
Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Tukholmankatu 8, 00290 Helsinki, Finland.

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Classifications MeSH