Increasing Upstream Chromatin Long-Range Interactions May Favor Induction of Circular RNAs in LysoPC-Activated Human Aortic Endothelial Cells.

RNA-Seq chromatin long–range interaction circular RNAs human aortic endothelial cell activation proatherogenic lipid lysophosphatidylcholine

Journal

Frontiers in physiology
ISSN: 1664-042X
Titre abrégé: Front Physiol
Pays: Switzerland
ID NLM: 101549006

Informations de publication

Date de publication:
2019
Historique:
received: 16 12 2018
accepted: 28 03 2019
entrez: 7 5 2019
pubmed: 7 5 2019
medline: 7 5 2019
Statut: epublish

Résumé

Circular RNAs (circRNAs) are non-coding RNAs that form covalently closed continuous loops, and act as gene regulators in physiological and disease conditions. To test our hypothesis that proatherogenic lipid lysophosphatidylcholine (LPC) induce a set of circRNAs in human aortic endothelial cell (HAEC) activation, we performed circRNA analysis by searching our RNA-Seq data from LPC-activated HAECs, and found: (1) LPC induces significant modulation of 77 newly characterized cirRNAs, among which 47 circRNAs (61%) are upregulated; (2) 34 (72%) out of 47 upregulated circRNAs are upregulated when the corresponding mRNAs are downregulated, suggesting that the majority of circRNAs are upregulated presumably via LPC-induced "abnormal splicing" when the canonical splicing for generation of corresponding mRNAs is suppressed; (3) Upregulation of 47 circRNAs is temporally associated with mRNAs-mediated LPC-upregulated cholesterol synthesis-SREBP2 pathway and LPC-downregulated TGF-β pathway; (4) Increase in upstream chromatin long-range interaction sites to circRNA related genes is associated with preferred circRNA generation over canonical splicing for mRNAs, suggesting that shifting chromatin long-range interaction sites from downstream to upstream may promote induction of a list of circRNAs in lysoPC-activated HAECs; (5) Six significantly changed circRNAs may have sponge functions for miRNAs; and (6) 74% significantly changed circRNAs contain open reading frames, suggesting that putative short proteins may interfere with the protein interaction-based signaling. Our findings have demonstrated for the first time that a new set of LPC-induced circRNAs may contribute to homeostasis in LPC-induced HAEC activation. These novel insights may lead to identifications of new therapeutic targets for treating metabolic cardiovascular diseases, inflammations, and cancers.

Identifiants

pubmed: 31057422
doi: 10.3389/fphys.2019.00433
pmc: PMC6482593
doi:

Types de publication

Journal Article

Langues

eng

Pagination

433

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL138749
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL117654
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL130233
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK104116
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL132399
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL147565
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK113775
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI145034
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL131460
Pays : United States

Références

Science. 2002 Feb 15;295(5558):1306-11
pubmed: 11847345
J Immunol. 2004 Jan 1;172(1):651-60
pubmed: 14688378
J Allergy Clin Immunol. 2004 Dec;114(6):1463-70
pubmed: 15577853
Oncogene. 2005 Jul 14;24(30):4778-88
pubmed: 15870695
Nat Med. 2006 Feb;12(2):178-80
pubmed: 16462800
J Clin Pathol. 2006 Aug;59(8):855-61
pubmed: 16574722
Hum Mol Genet. 2006 Apr 15;15 Spec No 1:R17-29
pubmed: 16651366
Mol Cell Biol. 2006 Jul;26(14):5528-43
pubmed: 16809785
Clin Immunol. 2006 Nov;121(2):121-33
pubmed: 16890493
Genome Res. 2006 Oct;16(10):1299-309
pubmed: 16954542
J Immunol. 2006 Oct 1;177(7):4907-16
pubmed: 16982933
EMBO J. 2007 Mar 21;26(6):1737-48
pubmed: 17332742
Nature. 2008 Apr 17;452(7189):846-50
pubmed: 18322460
Circulation. 2008 Apr 1;117(13):1649-57
pubmed: 18347211
Atherosclerosis. 2009 Apr;203(2):401-8
pubmed: 18789801
Cell. 2009 Jan 23;136(2):215-33
pubmed: 19167326
Cell. 2009 Feb 20;136(4):701-18
pubmed: 19239890
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
BMC Bioinformatics. 2009 May 27;10:160
pubmed: 19473520
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
Front Biosci (Landmark Ed). 2011 Jun 01;16:3133-45
pubmed: 21622224
Genes Dev. 2011 Jul 1;25(13):1371-83
pubmed: 21690198
Front Biosci (Elite Ed). 2012 Jan 01;4:1478-95
pubmed: 22201969
Front Biosci (Landmark Ed). 2012 Jun 01;17:2327-49
pubmed: 22652782
EMBO Rep. 2012 Sep;13(9):819-26
pubmed: 22836578
Cell Metab. 2012 Oct 3;16(4):414-9
pubmed: 23000402
J Hematol Oncol. 2012 Oct 18;5:66
pubmed: 23078795
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
J Biol Chem. 2013 Feb 1;288(5):2986-93
pubmed: 23166328
Mol Biol Rep. 2013 Apr;40(4):2789-98
pubmed: 23397238
Nat Protoc. 2013 Mar;8(3):509-24
pubmed: 23411633
Nature. 2013 Mar 21;495(7441):384-8
pubmed: 23446346
Nature. 2013 Mar 21;495(7441):333-8
pubmed: 23446348
Science. 2013 Mar 22;339(6126):1448-53
pubmed: 23449998
Mol Genet Genomics. 2013 Sep;288(9):381-9
pubmed: 23783428
J Invest Dermatol. 2014 Mar;134(3):695-703
pubmed: 24005050
Bioinformatics. 2014 Feb 15;30(4):523-30
pubmed: 24336805
Mol Biol Rep. 2014 Mar;41(3):1525-31
pubmed: 24402874
Nature. 2014 Mar 6;507(7490):109-13
pubmed: 24572365
Cell. 2014 Mar 27;157(1):77-94
pubmed: 24679528
Nat Biotechnol. 2014 May;32(5):453-61
pubmed: 24811520
Diabetes. 2014 Dec;63(12):4275-90
pubmed: 25008174
Sci Transl Med. 2014 Aug 20;6(250):250ra114
pubmed: 25143364
Toxicol Appl Pharmacol. 2014 Oct 15;280(2):199-206
pubmed: 25168428
Cancer Res. 2014 Nov 15;74(22):6519-30
pubmed: 25267067
Bioessays. 2015 Jan;37(1):103-12
pubmed: 25345765
Nucleic Acids Res. 2015 Jan;43(Database issue):D1113-6
pubmed: 25361974
J Hematol Oncol. 2014 Oct 31;7:80
pubmed: 25387998
RNA. 2014 Dec;20(12):1829-42
pubmed: 25404635
Front Biosci (Landmark Ed). 2015 Jan 01;20:784-95
pubmed: 25553479
Cell Rep. 2015 Jan 13;10(2):170-7
pubmed: 25558066
Genome Biol. 2015 Jan 13;16:4
pubmed: 25583365
Nucleic Acids Res. 2015 Feb 27;43(4):2454-65
pubmed: 25662225
Arterioscler Thromb Vasc Biol. 2015 Apr;35(4):804-16
pubmed: 25705917
Neoplasia. 2015 Feb;17(2):175-82
pubmed: 25748236
Transcription. 2014;5(3):e28726
pubmed: 25764333
Bioinformatics. 2015 Aug 1;31(15):2560-4
pubmed: 25788621
J Cell Biol. 2015 Apr 13;209(1):13-22
pubmed: 25869663
J Neurosci. 2015 Apr 15;35(15):6153-64
pubmed: 25878287
BMC Bioinformatics. 2015 May 22;16:169
pubmed: 25994840
Sci Transl Med. 2015 Sep 30;7(307):307ra154
pubmed: 26424569
J Cell Physiol. 2016 May;231(5):1142-50
pubmed: 26445298
Nat Rev Immunol. 2015 Nov;15(11):692-704
pubmed: 26471775
Front Biosci (Landmark Ed). 2016 Jan 1;21(1):70-88
pubmed: 26594106
Nucleic Acids Res. 2016 Apr 7;44(6):e58
pubmed: 26657634
RNA Biol. 2016;13(1):34-42
pubmed: 26669964
Front Biosci (Landmark Ed). 2016 Jan 01;21:178-91
pubmed: 26709768
EMBO Rep. 2016 Apr;17(4):570-84
pubmed: 26882547
Circ Res. 2016 Feb 19;118(4):620-36
pubmed: 26892962
J Cardiovasc Transl Res. 2016 Apr;9(2):135-44
pubmed: 26928596
J Immunol. 2016 May 15;196(10):4378-89
pubmed: 27067007
Arterioscler Thromb Vasc Biol. 2016 Jun;36(6):1090-100
pubmed: 27127201
J Cardiovasc Transl Res. 2016 Aug;9(4):343-59
pubmed: 27230673
Development. 2016 Jun 1;143(11):1838-47
pubmed: 27246710
Genome Res. 2016 Sep;26(9):1277-87
pubmed: 27365365
Cardiovasc Res. 2016 Nov 1;112(2):581-589
pubmed: 27389411
J Mol Cell Cardiol. 2016 Sep;98:103-7
pubmed: 27476877
Nat Commun. 2016 Aug 19;7:12429
pubmed: 27539542
Sci Rep. 2016 Oct 11;6:34985
pubmed: 27725737
Lancet. 2016 Oct 8;388(10053):1459-1544
pubmed: 27733281
Nat Rev Genet. 2016 Oct 14;17(11):679-692
pubmed: 27739534
J Biol Chem. 2017 Jan 27;292(4):1267-1287
pubmed: 27856635
FEBS Lett. 2017 Jan;591(1):213-220
pubmed: 27878987
Genes (Basel). 2016 Dec 03;7(12):
pubmed: 27918472
Cancer Lett. 2017 Mar 1;388:208-219
pubmed: 27986464
Clin Lab. 2016 Nov 1;62(11):2257-2265
pubmed: 28164681
Cell Res. 2017 May;27(5):626-641
pubmed: 28281539
Antioxid Redox Signal. 2017 Apr 26;:
pubmed: 28325059
Mol Cell. 2017 Apr 6;66(1):9-21.e7
pubmed: 28344080
Mol Cell. 2017 Apr 6;66(1):22-37.e9
pubmed: 28344082
Sci Rep. 2017 Apr 6;7(1):668
pubmed: 28386100
Cell Death Dis. 2017 May 11;8(5):e2778
pubmed: 28492554
PLoS Comput Biol. 2017 Jun 8;13(6):e1005420
pubmed: 28594838
Cytokine. 2017 Jun 22;:
pubmed: 28648331
RNA Biol. 2017 Dec 2;14(12):1715-1721
pubmed: 28820337
J Mol Med (Berl). 2017 Nov;95(11):1179-1189
pubmed: 28842720
Oncotarget. 2017 Jun 27;8(37):61687-61697
pubmed: 28977896
Nat Rev Cancer. 2018 Jan;18(1):5-18
pubmed: 29170536
Mol Cell. 2017 Dec 7;68(5):940-954.e3
pubmed: 29174924
Oncotarget. 2017 Sep 23;8(56):95704-95718
pubmed: 29221160
Oncol Rep. 2018 Mar;39(3):951-966
pubmed: 29286141
Arterioscler Thromb Vasc Biol. 2018 Mar;38(3):599-609
pubmed: 29371247
Front Immunol. 2018 Jan 26;9:45
pubmed: 29434588
Anatol J Cardiol. 2018 Mar;19(3):192-197
pubmed: 29521313
Biochem Biophys Res Commun. 2018 May 15;499(3):551-555
pubmed: 29596825
Wiley Interdiscip Rev RNA. 2018 Jul;9(4):e1478
pubmed: 29655315
J Biol Chem. 2018 Jul 13;293(28):11033-11045
pubmed: 29769317
Elife. 2018 Jul 10;7:
pubmed: 29988018
Noncoding RNA Res. 2018 Feb 25;3(1):1-11
pubmed: 30159434
Front Physiol. 2018 Oct 12;9:1297
pubmed: 30369883
Nucleic Acids Res. 1987 Oct 26;15(20):8125-48
pubmed: 3313277
Mamm Genome. 1996 Aug;7(8):563-74
pubmed: 8679005
Prog Brain Res. 1996;109:253-64
pubmed: 9009714

Auteurs

Angus Li (A)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.
Department of Biomedical Engineering, Pratt School of Engineering, Duke University, Durham, NC, United States.

Yu Sun (Y)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Charles Drummer (C)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Yifan Lu (Y)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Daohai Yu (D)

Department of Clinical Sciences, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Yan Zhou (Y)

Biostatistics and Bioinformatics Facility, Fox Chase Cancer Center, Temple Health, Philadelphia, PA, United States.

Xinyuan Li (X)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Simone J Pearson (SJ)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Candice Johnson (C)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Catherine Yu (C)

Geisinger Commonwealth School of Medicine, Scranton, PA, United States.

William Y Yang (WY)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Kevin Mastascusa (K)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Xiaohua Jiang (X)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Jianxin Sun (J)

Center for Translational Medicine, Department of Medicine, Sidney Kimmel Medical College, Philadelphia University - Thomas Jefferson University, Philadelphia, PA, United States.

Thomas Rogers (T)

Center for Inflammation, Translational and Clinical Lung Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Wenhui Hu (W)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Hong Wang (H)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Xiaofeng Yang (X)

Center for Metabolic Disease Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.
Center for Inflammation, Translational and Clinical Lung Research, Lewis Katz School of Medicine, Temple University, Philadelphia, PA, United States.

Classifications MeSH