Skip to main content

Advertisement

SpringerLink
Log in

Endothelial long non-coding RNAs regulated by oxidized LDL

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Oxidized low-density lipoprotein (oxLDL) plays a central role in the pathogenesis of atherosclerosis, in part via an effect to promote endothelial dysfunction. In the present study, we evaluated the expression profiles of long non-coding RNAs (lncRNAs) and protein-coding mRNAs in endothelial cells following oxLDL stimulation. LncRNAs and mRNAs from human umbilical vein endothelial cells (HUVECs) were profiled with the Arraystar Human lncRNA Expression Microarray V3.0 following 24 h of oxLDL treatment (100 µg/mL). Of the 30,584 lncRNAs screened, 923 were significantly up-regulated and 975 significantly down-regulated (P < 0.05) in response to oxLDL exposure. In the same HUVEC samples, 518 of the 26,106 mRNAs screened were up-regulated and 572 were down-regulated. Of these differentially expressed lncRNAs, CLDN10-AS1 and CTC-459I6.1 were the most up-regulated (~87-fold) and down-regulated (~28-fold), respectively. Bioinformatic assignment of the differentially regulated genes into functional groups indicated that many are involved in signaling pathways among which are the cytokine receptor, chemokine, TNF, MAPK and Ras signaling pathways, olfactory transduction, and vascular smooth muscle cell function. This is the first report profiling oxLDL-mediated changes in lncRNA and mRNA expression in human endothelial cells. The novel targets revealed substantially extend the list of potential candidate genes involved in atherogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ANRIL:

Antisense non-coding RNA in the INK4

CVD:

Cardiovascular disease

DE:

Differentially expressed

ENCODE:

Encyclopedia of DNA Elements

GO:

Gene ontology

HDL:

High-density lipoprotein

HLA-DPB1:

Major Histocompatibility Complex, Class II, DP Beta-1

HUVECs:

Human umbilical vein endothelial cells

KEGG:

Kyoto Encyclopedia of Genes and Genomes

lncRNA:

Long non-coding RNAs

MIAT:

Myocardial infarction-associated transcript

miRNA:

MicroRNA

ncRNA:

Non-coding RNAs

NO:

Nitric oxide

NQO1:

NAD(P)H dehydrogenase quinone 1

O2 − :

Oxygen radical

oxLDL:

Oxidized low-density lipoprotein

piRNAs:

PIWI-interacting RNAs

ROS:

Reactive oxygen species

SMC:

Smooth muscle cell

snoRNAs:

Small nucleolar RNAs

t-UCRs:

Transcribed ultra-conserved regions

References

  1. Hein TW, Singh U, Vasquez-Vivar J, Devaraj S, Kuo L, Jialal I (2009) Human C-reactive protein induces endothelial dysfunction and uncoupling of eNOS in vivo. Atherosclerosis 206:61–68. doi:10.1016/j.atherosclerosis.2009.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Verma S, Wang CH, Li SH, Dumont AS, Fedak PW, Badiwala MV, Dhillon B, Weisel RD, Li RK, Mickle DA, Stewart DJ (2002) A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 106:913–919

    Article  CAS  PubMed  Google Scholar 

  3. Jialal I, Verma S, Devaraj S (2009) Inhibition of endothelial nitric oxide synthase by C-reactive protein: clinical relevance. Clin Chem 55:206–208. doi:10.1373/clinchem.2008.119206

    Article  CAS  PubMed  Google Scholar 

  4. Hansson GK, Robertson AK, Soderberg-Naucler C (2006) Inflammation and atherosclerosis. Annu Rev Pathol 1:297–329. doi:10.1146/annurev.pathol.1.110304.100100

    Article  CAS  PubMed  Google Scholar 

  5. Szmitko PE, Wang CH, Weisel RD, Jeffries GA, Anderson TJ, Verma S (2003) Biomarkers of vascular disease linking inflammation to endothelial activation: Part II. Circulation 108:2041–2048. doi:10.1161/01.CIR.0000089093.75585.98

    Article  PubMed  Google Scholar 

  6. Szmitko PE, Wang CH, Weisel RD, de Almeida JR, Anderson TJ, Verma S (2003) New markers of inflammation and endothelial cell activation: Part I. Circulation 108:1917–1923. doi:10.1161/01.CIR.0000089190.95415.9F

    Article  PubMed  Google Scholar 

  7. Verma S, Anderson TJ (2002) Fundamentals of endothelial function for the clinical cardiologist. Circulation 105:546–549

    Article  CAS  PubMed  Google Scholar 

  8. Verma S, Buchanan MR, Anderson TJ (2003) Endothelial function testing as a biomarker of vascular disease. Circulation 108:2054–2059. doi:10.1161/01.CIR.0000089191.72957.ED

    Article  PubMed  Google Scholar 

  9. Steinberg D, Witztum JL (2010) Oxidized low-density lipoprotein and atherosclerosis. Arterioscler Thromb Vasc Biol 30:2311–2316. doi:10.1161/ATVBAHA.108.179697

    Article  CAS  PubMed  Google Scholar 

  10. Valente AJ, Irimpen AM, Siebenlist U, Chandrasekar B (2014) OxLDL induces endothelial dysfunction and death via TRAF3IP2: inhibition by HDL3 and AMPK activators. Free Radic Biol Med 70:117–128. doi:10.1016/j.freeradbiomed.2014.02.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Davignon J and Ganz P (2004) Role of endothelial dysfunction in atherosclerosis. Circulation 109:III27-32. doi:10.1161/01.CIR.0000131515.03336.f8

    Google Scholar 

  12. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Roder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See LH, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigo R, Gingeras TR (2012) Landscape of transcription in human cells. Nature 489:101–108. doi:10.1038/nature11233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46. doi:10.1016/j.cell.2013.06.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wang S, Tran EJ (2013) Unexpected functions of lncRNAs in gene regulation. Commun Integr Biol 6:e27610. doi:10.4161/cib.27610

    Article  PubMed  Google Scholar 

  15. Wapinski O, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21:354–361. doi:10.1016/j.tcb.2011.04.001

    Article  CAS  PubMed  Google Scholar 

  16. Uchida S, Dimmeler S (2015) Long noncoding RNAs in cardiovascular diseases. Circ Res 116:737–750. doi:10.1161/CIRCRESAHA.116.302521

    Article  CAS  PubMed  Google Scholar 

  17. Wu CL, Wang Y, Jin B, Chen H, Xie BS, Mao ZB (2015) Senescence-associated Long Non-coding RNA (SALNR) Delays Oncogene-induced Senescence through NF90 Regulation. J Biol Chem 290:30175–30192. doi:10.1074/jbc.M115.661785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Han P, Li W, Lin CH, Yang J, Shang C, Nurnberg ST, Jin KK, Xu W, Lin CY, Lin CJ, Xiong Y, Chien HC, Zhou B, Ashley E, Bernstein D, Chen PS, Chen HS, Quertermous T, Chang CP (2014) A long noncoding RNA protects the heart from pathological hypertrophy. Nature 514:102–106. doi:10.1038/nature13596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Vausort M, Wagner DR, Devaux Y (2014) Long noncoding RNAs in patients with acute myocardial infarction. Circ Res 115:668–677. doi:10.1161/CIRCRESAHA.115.303836

    Article  CAS  PubMed  Google Scholar 

  20. Vilsboll T, Rosenstock J, Yki-Jarvinen H, Cefalu WT, Chen Y, Luo E, Musser B, Andryuk PJ, Ling Y, Kaufman KD, Amatruda JM, Engel SS, Katz L (2010) Efficacy and safety of sitagliptin when added to insulin therapy in patients with type 2 diabetes. Diabetes Obes Metab 12:167–177. doi:10.1111/j.1463-1326.2009.01173.x

    Article  CAS  PubMed  Google Scholar 

  21. Michalik KM, You X, Manavski Y, Doddaballapur A, Zornig M, Braun T, John D, Ponomareva Y, Chen W, Uchida S, Boon RA, Dimmeler S (2014) Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ Res 114:1389–1397. doi:10.1161/CIRCRESAHA.114.303265

    Article  CAS  PubMed  Google Scholar 

  22. Holdt LM, Hoffmann S, Sass K, Langenberger D, Scholz M, Krohn K, Finstermeier K, Stahringer A, Wilfert W, Beutner F, Gielen S, Schuler G, Gabel G, Bergert H, Bechmann I, Stadler PF, Thiery J, Teupser D (2013) Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet 9:e1003588. doi:10.1371/journal.pgen.1003588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lund-Katz S, Phillips MC (2010) High density lipoprotein structure-function and role in reverse cholesterol transport. Subcell Biochem 51:183–227. doi:10.1007/978-90-481-8622-8_7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Singh KK, Matkar PN, Quan A, Mantella L-E, Teoh H, Al-Omran M, Verma S (2016) Investigation of TGFbeta1-induced long noncoding RNAs in endothelial cells. Int J Vasc Med 2016:2459687. doi:10.1155/2016/2459687

    PubMed  PubMed Central  Google Scholar 

  25. Singh KK, Mantella L-E, Pan Y, Quan A, Sabonguia S, Sandhu P, Teoh H, Al-Omran M, verma S (2016) A global profile of glucose-sensitive endothelial-expressed long non-coding RNAs. Can J Physiol Pharmacol 94:1007–1014

    Article  CAS  PubMed  Google Scholar 

  26. Toshima S, Hasegawa A, Kurabayashi M, Itabe H, Takano T, Sugano J, Shimamura K, Kimura J, Michishita I, Suzuki T, Nagai R (2000) Circulating oxidized low density lipoprotein levels. A biochemical risk marker for coronary heart disease. Arterioscler Thromb Vasc Biol 20:2243–2247

    Article  CAS  PubMed  Google Scholar 

  27. Goldstein JL, Brown MS, Krieger M, Anderson RG, Mintz B (1979) Demonstration of low density lipoprotein receptors in mouse teratocarcinoma stem cells and description of a method for producing receptor-deficient mutant mice. Proc Natl Acad Sci U S A 76:2843–2847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Penn MS and Chisolm GM (1994) Oxidized lipoproteins, altered cell function and atherosclerosis. Atherosclerosis 108 :S21–S29

    Article  PubMed  Google Scholar 

  29. Chisolm GM, Ma G, Irwin KC, Martin LL, Gunderson KG, Linberg LF, Morel DW, DiCorleto PE (1994) 7 beta-hydroperoxycholest-5-en-3 beta-ol, a component of human atherosclerotic lesions, is the primary cytotoxin of oxidized human low density lipoprotein. Proc Natl Acad Sci U S A 91:11452–11456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Morel DW, Hessler JR, Chisolm GM (1983) Low density lipoprotein cytotoxicity induced by free radical peroxidation of lipid. J Lipid Res 24:1070–1076

    CAS  PubMed  Google Scholar 

  31. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ (1999) Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J Biol Chem 274:32512–32519

    Article  CAS  PubMed  Google Scholar 

  32. Singh KK, Shukla PC, Quan A, Al-Omran M, Lovren F, Pan Y, Brezden-Masley C, Ingram AJ, Stanford WL, Teoh H, Verma S (2013) BRCA1 is a novel target to improve endothelial dysfunction and retard atherosclerosis. J Thorac Cardiovasc Surg 146(949–960):e4. doi:10.1016/j.jtcvs.2012.12.064

    Google Scholar 

  33. Cominacini L, Rigoni A, Pasini AF, Garbin U, Davoli A, Campagnola M, Pastorino AM, Lo Cascio V, Sawamura T (2001) The binding of oxidized low density lipoprotein (ox-LDL) to ox-LDL receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells through an increased production of superoxide. J Biol Chem 276:13750–13755. doi:10.1074/jbc.M010612200

    Article  CAS  PubMed  Google Scholar 

  34. Li D, Mehta JL (2000) Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of human coronary artery endothelial cells: evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arterioscler Thromb Vasc Biol 20:1116–1122

    Article  CAS  PubMed  Google Scholar 

  35. Salvayre R, Auge N, Benoist H, Negre-Salvayre A (2002) Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585:213–221

    Article  CAS  PubMed  Google Scholar 

  36. Trpkovic A, Resanovic I, Stanimirovic J, Radak D, Mousa SA, Cenic-Milosevic D, Jevremovic D, Isenovic ER (2015) Oxidized low-density lipoprotein as a biomarker of cardiovascular diseases. Crit Rev Clin Lab Sci 52:70–85. doi:10.3109/10408363.2014.992063

    Article  CAS  PubMed  Google Scholar 

  37. Bjorkbacka H, Fredrikson GN, Nilsson J (2013) Emerging biomarkers and intervention targets for immune-modulation of atherosclerosis—a review of the experimental evidence. Atherosclerosis 227:9–17. doi:10.1016/j.atherosclerosis.2012.10.074

    Article  PubMed  Google Scholar 

  38. Galle J, Hansen-Hagge T, Wanner C, Seibold S (2006) Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 185:219–226. doi:10.1016/j.atherosclerosis.2005.10.005

    Article  CAS  PubMed  Google Scholar 

  39. Di Pietro N, Formoso G, Pandolfi A (2016) Physiology and pathophysiology of oxLDL uptake by vascular wall cells in atherosclerosis. Vascul Pharmacol. doi:10.1016/j.vph.2016.05.013

    PubMed  Google Scholar 

  40. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, Kitagawa M, Xiong Y (2011) Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30:1956–1962. doi:10.1038/onc.2010.568

    Article  CAS  PubMed  Google Scholar 

  41. McPherson R, Pertsemlidis A, Kavaslar N, Stewart A, Roberts R, Cox DR, Hinds DA, Pennacchio LA, Tybjaerg-Hansen A, Folsom AR, Boerwinkle E, Hobbs HH, Cohen JC (2007) A common allele on chromosome 9 associated with coronary heart disease. Science 316:1488–1491. doi:10.1126/science.1142447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ishii N, Ozaki K, Sato H, Mizuno H, Saito S, Takahashi A, Miyamoto Y, Ikegawa S, Kamatani N, Hori M, Saito S, Nakamura Y, Tanaka T (2006) Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J Hum Genet 51:1087–1099. doi:10.1007/s10038-006-0070-9

    Article  CAS  PubMed  Google Scholar 

  43. Minta J, Jungwon Yun J, St Bernard R (2010) Microarray analysis of ox-LDL (oxidized low-density lipoprotein)-regulated genes in human coronary artery smooth muscle cells. Cell Biol Int Rep 17:e00007. doi:10.1042/CBR20100006

    Google Scholar 

  44. Deng DX, Spin JM, Tsalenko A, Vailaya A, Ben-Dor A, Yakhini Z, Tsao P, Bruhn L, Quertermous T (2006) Molecular signatures determining coronary artery and saphenous vein smooth muscle cell phenotypes: distinct responses to stimuli. Arterioscler Thromb Vasc Biol 26:1058–1065. doi:10.1161/01.ATV.0000208185.16371.97

    Article  CAS  PubMed  Google Scholar 

  45. Reeve JL, Stenson-Cox C, O’Doherty A, Porn-Ares I, Ares M, O’Brien T, Samali A (2007) OxLDL-induced gene expression patterns in CASMC are mimicked in apoE-/- mice aortas. Biochem Biophys Res Commun 356:681–686. doi:10.1016/j.bbrc.2007.03.027

    Article  CAS  PubMed  Google Scholar 

  46. Encode Project Consortium, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS, Dekker J, Lieb JD, Tullius TD, Crawford GE, Sunyaev S, Noble WS, Dunham I, Denoeud F, Reymond A, Kapranov P, Rozowsky J, Zheng D, Castelo R, Frankish A, Harrow J, Ghosh S, Sandelin A, Hofacker IL, Baertsch R, Keefe D, Dike S, Cheng J, Hirsch HA, Sekinger EA, Lagarde J, Abril JF, Shahab A, Flamm C, Fried C, Hackermuller J, Hertel J, Lindemeyer M, Missal K, Tanzer A, Washietl S, Korbel J, Emanuelsson O, Pedersen JS, Holroyd N, Taylor R, Swarbreck D, Matthews N, Dickson MC, Thomas DJ, Weirauch MT, Gilbert J, Drenkow J, Bell I, Zhao X, Srinivasan KG, Sung WK, Ooi HS, Chiu KP, Foissac S, Alioto T, Brent M, Pachter L, Tress ML, Valencia A, Choo SW, Choo CY, Ucla C, Manzano C, Wyss C, Cheung E, Clark TG, Brown JB, Ganesh M, Patel S, Tammana H, Chrast J, Henrichsen CN, Kai C, Kawai J, Nagalakshmi U, Wu J, Lian Z, Lian J, Newburger P, Zhang X, Bickel P, Mattick JS, Carninci P, Hayashizaki Y, Weissman S, Hubbard T, Myers RM, Rogers J, Stadler PF, Lowe TM, Wei CL, Ruan Y, Struhl K, Gerstein M, Antonarakis SE, Fu Y, Green ED, Karaoz U, Siepel A, Taylor J, Liefer LA, Wetterstrand KA, Good PJ, Feingold EA, Guyer MS, Cooper GM, Asimenos G, Dewey CN, Hou M, Nikolaev S, Montoya-Burgos JI, Loytynoja A, Whelan S, Pardi F, Massingham T, Huang H, Zhang NR, Holmes I, Mullikin JC, Ureta-Vidal A, Paten B, Seringhaus M, Church D, Rosenbloom K, Kent WJ, Stone EA, Program NCS, Baylor College of Medicine Human Genome Sequencing C, Washington University Genome Sequencing C, Broad I, Children’s Hospital Oakland Research I, Batzoglou S, Goldman N, Hardison RC, Haussler D, Miller W, Sidow A, Trinklein ND, Zhang ZD, Barrera L, Stuart R, King DC, Ameur A, Enroth S, Bieda MC, Kim J, Bhinge AA, Jiang N, Liu J, Yao F, Vega VB, Lee CW, Ng P, Shahab A, Yang A, Moqtaderi Z, Zhu Z, Xu X, Squazzo S, Oberley MJ, Inman D, Singer MA, Richmond TA, Munn KJ, Rada-Iglesias A, Wallerman O, Komorowski J, Fowler JC, Couttet P, Bruce AW, Dovey OM, Ellis PD, Langford CF, Nix DA, Euskirchen G, Hartman S, Urban AE, Kraus P, Van Calcar S, Heintzman N, Kim TH, Wang K, Qu C, Hon G, Luna R, Glass CK, Rosenfeld MG, Aldred SF, Cooper SJ, Halees A, Lin JM, Shulha HP, Zhang X, Xu M, Haidar JN, Yu Y, Ruan Y, Iyer VR, Green RD, Wadelius C, Farnham PJ, Ren B, Harte RA, Hinrichs AS, Trumbower H, Clawson H, Hillman-Jackson J, Zweig AS, Smith K, Thakkapallayil A, Barber G, Kuhn RM, Karolchik D, Armengol L, Bird CP, de Bakker PI, Kern AD, Lopez-Bigas N, Martin JD, Stranger BE, Woodroffe A, Davydov E, Dimas A, Eyras E, Hallgrimsdottir IB, Huppert J, Zody MC, Abecasis GR, Estivill X, Bouffard GG, Guan X, Hansen NF, Idol JR, Maduro VV, Maskeri B, McDowell JC, Park M, Thomas PJ, Young AC, Blakesley RW, Muzny DM, Sodergren E, Wheeler DA, Worley KC, Jiang H, Weinstock GM, Gibbs RA, Graves T, Fulton R, Mardis ER, Wilson RK, Clamp M, Cuff J, Gnerre S, Jaffe DB, Chang JL, Lindblad-Toh K, Lander ES, Koriabine M, Nefedov M, Osoegawa K, Yoshinaga Y, Zhu B, de Jong PJ (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799–816. doi:10.1038/nature05874

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by in part by grants from the Canadian Institutes of Health Research and Heart and Stroke Foundation of Canada to S. Verma. S. Verma is the Canada Research Chair in Atherosclerosis at the University of Toronto.

Authors’ contributions

KKS and SV designed the studies and the experiments. KKS, PNM, YP, AQ, and VG conducted the experiments. KKS drafted the manuscript. KKS, AQ, HT, MAO, and SV interpreted the data and critically edited the manuscript. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

  1. Division of Cardiac Surgery, Keenan Research Centre for Biomedical Science of St. Michael’s Hospital, Toronto, ON, M5B 1W8, Canada

    Krishna K. Singh, Yi Pan, Adrian Quan, Vijay Gupta, Hwee Teoh & Subodh Verma

  2. Division of Vascular Surgery, Keenan Research Centre for Biomedical Science of St. Michael’s Hospital, 5E21 KRCBS, 30 Bond Street, Toronto, ON, M5B 1W8, Canada

    Krishna K. Singh & Mohammed Al-Omran

  3. Division of Cardiology, Keenan Research Centre for Biomedical Science of St. Michael’s Hospital, Toronto, ON, Canada

    Pratiek N. Matkar

  4. Division of Endocrinology & Metabolism, Keenan Research Centre for Biomedical Science of St. Michael’s Hospital, Toronto, ON, Canada

    Krishna K. Singh & Hwee Teoh

  5. Department of Surgery, University of Toronto, Toronto, ON, Canada

    Krishna K. Singh, Mohammed Al-Omran & Subodh Verma

  6. Department of Pharmacology & Toxicology, University of Toronto, Toronto, ON, Canada

    Subodh Verma

  7. Department of Surgery, King Saud University and the King Saud University-Li Ka Shing Collaborative Research Program, Riyadh, Saudi Arabia

    Mohammed Al-Omran

Authors
  1. Krishna K. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pratiek N. Matkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adrian Quan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vijay Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hwee Teoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mohammed Al-Omran
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Subodh Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Krishna K. Singh or Subodh Verma.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, K.K., Matkar, P.N., Pan, Y. et al. Endothelial long non-coding RNAs regulated by oxidized LDL. Mol Cell Biochem 431, 139–149 (2017). https://doi.org/10.1007/s11010-017-2984-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-017-2984-2

Keywords

Search

Navigation