A Brief Overview of lncRNAs in Endothelial Dysfunction-Associated Diseases: From Discovery to Characterization
Abstract
:1. Introduction
2. lncRNAs in the Regulation of Gene Expression
3. Functional Roles of lncRNAs in Endothelial Dysfunction
4. Methods for Studying lncRNA: From Discovery to Function
4.1. Methods to Identify/Discover lncRNAs
4.1.1. Tiling Arrays
4.1.2. Serial Analysis of Gene Expression (SAGE)
4.1.3. Cap Analysis of Gene Expression (CAGE)
4.1.4. RNA Sequencing (RNA-Seq)
4.2. Methods to Study the Functional Roles of lncRNAs
4.2.1. RNA Interference (RNAi)
4.2.2. Antisense Oligonucleotides (ASOs)
4.2.3. CRISPR/Cas System
4.2.4. CRISPR Interference (CRISPRi)
4.3. Different Methods to Unveil the Functional Mechanisms of lncRNAs
4.3.1. Localization of lncRNA: Single-Molecule RNA Fluorescence In Situ Hybridization (smRNA-FISH)
4.3.2. Techniques for Investigating lncRNA-DNA Interaction
Capture Hybridization Analysis of RNA Target (CHART)
Chromatin Isolation by RNA Purification (ChIRP)
RNA Antisense Purification (RAP)
4.3.3. Techniques for Investigating lncRNA-RNA Interaction
RNA Antisense purification Followed by RNA Sequencing (RAP-RNA)
Cross-Linking, Ligation and Sequencing of Hybrids (CLASH)
4.3.4. Techniques for Investigating lncRNA-Protein Interaction
RNA Immunoprecipitation (RIP)
High-Throughput Sequencing of RNA Isolated by Cross-Linking Immunoprecipitation (HITS-CLIP)
Photoactivatable Ribonucleotide-Enhanced Cross Linking and Immunoprecipitation (PAR-CLIP)
5. Functional Involvement of lncRNAs in Endothelial Dysfunction-Associated Diseases
5.1. The Correlations of Functional Involvement of lncRNAs in ED and Angiogenesis
5.2. The Correlations of Functional Involvement of lncRNAs in ED and Diabetes
5.3. The Correlations of Functional Involvement of lncRNAs in ED and Hypertension
5.4. The Correlations of Functional Involvement of lncRNAs in ED and Atherosclerosis
6. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
6SG | 6-Thioguanosine |
4SU | 4-Thiouridine |
AAs | Amino acids |
ADAR | Adenosine deaminase acting on RNA |
Akt | AKT serine/threonine kinase 1 |
Alu | Arthrobacter luteus |
AMT | Aminomethyltrioxalen |
ANGPT2 | Angiopoietin 2 |
ASOs | Antisense oligonucleotides |
BACE1 | Beta-secretase 1 |
BACE1AS | BACE1 (beta-secretase 1)-antisense RNA |
BCYRN1 | Brain cytoplasmic RNA 1 |
BP | Blood pressure |
CAGE | Cap analysis of gene expression |
CCNA2 | Cyclin A2 |
CCNB1 | Cyclin B1 |
CCNB2 | Cyclin B2 |
Cdc42 | Cell division cycle 42 |
CeRNA | Competing endogenous RNA |
cGMP | Cyclic guanosine 3′, 5′-monophosphate |
CHART | Capture hybridization analysis of RNA target |
ChIRP | Chromatin isolation by RNA purification |
CLASH | Cross-linking, ligation and sequencing of hybrids |
COUP-TFII | Chicken ovalbumin upstream promoter transcription-factor-2 |
CRISPRi | CRISPR interference |
CTD | Carboxyl-teminal domain |
CTGF | Connective tissue growth factor |
CVD | Cardiovascular disease |
CX3CL1 | C-X3-C motif chemokine ligand 1 |
DSC | Disuccinimidyl glutarate |
EC | Endothelial cell |
ED | Endothelial dysfunction |
EDHF | Endothelium derived hyperpolarizing factor |
EeD | Embryonic ectoderm development |
ERK | Extracellular signal-regulated kinase |
ESM-1 | Endothelial cell specific molecule |
EPC | Endothelial progenitor cell |
EPC2 | Enhancer of polycomb homolog 2 |
ER | Endoplasmic reticulum |
ET-1 | Endothelin-1 |
FA | Formaldehyde |
FAK | Focal adhesion kinase |
FISH | Fluorescence in situ hybridization |
FGF2 | Fibroblast Growth Factor 2 |
GAS5 | Growth arrest specific 5 |
GATA-AS | Antisense transcript of GATA6 |
GRP78 | Glucose regulated protein 78 |
GR | Glucocorticoid receptor |
GTP | Guanosine triphosphate |
H3K4me2 | Demethylation of lysine 4 residue on histone 3 |
H3K4me3 | Trimethylation of lysine 4 of histone H3 |
H3K27me3 | Histone 3 lysine 27 trimethylation |
H19 | H19 imprinted maternally expressed transcript |
HDR | Homology direct repair |
HITS-CLIP | High-throughput sequencing of RNA isolated by cross-linking immunoprecipitation |
HOTAIR | HOX transcript antisense RNA |
HULC | Highly upregulated in liver cancer |
IL-6 | Interleukin-6 |
HUVECs | Human umbilical vein endothelial cells |
IL-1β | Interleukin 1 beta |
KLF2 | Kruppel like factor |
KRAB | Kruppel-associated box |
LDL | Low-density lipoprotein |
lncRNAs | Long non-coding RNAs |
LOX2 | Lysyl oxidase-like 2 |
LRP2BP | LRP2 binding protein |
LSD1 | Lys-specific demethylase 1 |
MALAT1 | Metastasis associated lung adenocarcinoma transcript 1 |
MAPK | Mitogen-activated protein kinases |
MCP-1 | Monocyte chemoattractant protein-1 |
MEG3 | Maternally expressed 3 |
MERFISH | Multiplexed error-robust fluorescence in situ hybridization |
Mhrt | Myosin heavy chain associated RNA transcript |
MIAT | Myocardial infarction associated transcript |
MMP | Matrix metalloproteinase |
MSC | Mesenchymal stem cell |
mTOR | Mammalian target of rapamycin |
NADPH | Nicotinamide adenine dinucleotide phosphate |
NATs | Natural antisense transcripts |
NFAT | Nuclear factor of activated T-cells |
NFkB | Nuclear factor kappa-light-chain-enhancer of activated B cells |
NGS | Next generation sequencing |
NHEJ | Non-homologous end joining |
NO | Nitric oxide |
NOD2 | Nucleotide binding oligomerization domain containing 2 |
eNOS | NO synthase |
NR1 | Notoginsenoside R1 |
NRON | Non-coding repressor of NFAT |
NOX4 | NADPH Oxidase 4 |
OGD | Oxygen-glucose deprivation |
ORF | Open reading frame |
oxLDL | Oxidized low-density lipoprotein |
PAR-CLIP | Photoactivatable ribonucleotide-enhanced cross linking and immunoprecipitation |
PGI2 | Prostacyclin |
PGH2 | ProstaglandinH2 |
PI3K | Phosphatidylinositol 3-kinase |
PKCδ | Protein kinase C delta |
PolII | RNA polymerase II |
PRC2 | Polycomb repressive complex |
PVT1 | Plasmacytoma variant translocation 1 |
RAP | RNA antisense purification |
RAP-RNA | RNA antisense purification followed by RNA sequencing |
RBBP4 | RB binding protein 4, chromatin remodeling factor |
RIP | RNA immunoprecipitation |
RNA-FISH | RNA fluorescence in situ hybridization |
RNA-Seq | RNA sequencing |
RNAi | RNA interference |
RNCR3 | Retinal non-coding RNA3 |
ROS | Reactive oxygen species |
SAGE | Serial analysis of gene expression |
SAA3 | Serum amyloid antigen3 |
sGC | Soluble guanylyl cyclase |
sgRNA | Single guide RNA |
shRNA | Short hairpin RNA |
SINE | Short interspersed elements |
siRNA | Small interfering RNA |
SMAD6 | Mothers against decapentaplegic homologue 6 |
smRNA-FISH | Single molecule RNA in situ hybridization |
SMMECs | Skeletal muscle microvascular endothelial cells |
SNHG12 | Small nucleolar RNA host gene 12 |
SNHG15 | Small nucleolar RNA host gene 15 |
SOX18 | SRY (Sex Determining Region Y)-Box 18 |
SRY | Sex Determining Region Y |
Suz12 | SUZ12 polycomb repressive complex 2 subunit |
T1DM | Type 1 Diabetic Mellitus |
T2DM | Type 2 Diabetic Mellitus |
TAMs | Tumor-associated macrophages |
TSLP | Thymic stromal lymphopoietin |
TNF-α | Tumor necrosis factor-α |
TSS | Transcriptional start site |
TUG1 | Taurine up-regulated 1 |
TXA2 | Thromboxane A2 |
UBE2CP3 | Ubiquitin conjugating enzyme E2 C pseudogene 3 |
UCA-1 | Urothelial cancer associated 1 |
VCAM-1 | Vascular cell adhesion molecule-1 |
VEC | vascular endothelial cells |
VSMC | Vascular smooth muscle cells |
VECs | Vascular endothelial cells |
VEGF | Vascular endothelial growth factor |
VEGFA | Vascular endothelial growth factor A |
VEGFR2 | VEGF receptor 2 |
XIST | X-inactive specific transcript. |
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Method | Advantages | Disadvantages | References |
---|---|---|---|
Tiling arrays |
|
| [86,88,89] |
SAGE |
|
| [90,91] |
CAGE |
|
| [92,93,94,95,96] |
RNA-Seq |
|
| [97,98,99] |
Method | Advantages | Disadvantages | References |
---|---|---|---|
RNAi |
|
| [112,113,114,115] |
ASOs |
|
| [116,117,118,119] |
CRISPR/Cas9 |
|
| [120,121,122,123,124] |
CRISPRi |
|
| [125,126] |
Purpose of Study | Method | Advantages | Disadvantages | References |
---|---|---|---|---|
Identification of subcellular localization | smRNA-FISH |
|
| [149,150] |
Investigation of lncRNA-DNA interaction | CHART |
|
| [86,151,152] |
ChIRP |
|
| [153,154,155] | |
RAP |
|
| [156,157] | |
Investigation of lncRNA-RNA interaction | RAP-RNA |
|
| [158] |
CLASH |
|
| [159,160,161,162] | |
Investigation of lncRNA-protein interaction | RIP |
|
| [163,164,165,166] |
HITS-CLIP |
|
| [167,168,169,170] | |
PAR-CLIP |
|
| [171,172,173] |
Name | Location | Disease Association | Correlations of the Functional Involvement of lncRNAs in ED and Angiogenesis | References |
---|---|---|---|---|
HULC | 6p24.3 | Gliomas | Promotes angiogenesis through regulating endothelial cell specific molecule 1 (ESM-1) via PI3K/AKT/mTOR pathway | [49] |
Angiogenesis | Regulates EC angiogenesis via sequestrating miR-124 | [50] | ||
Small nucleolar RNA host gene 12 (SNHG12) | 1p35.3 | Ischemic stroke | Promotes angiogenesis of oxygen-glucose deprivation (OGD)-treated brain microvascular EC through regulating miR-150/VEGF pathway | [186] |
MALAT1 | 11q13.1 | Hindlimb ischemia | Promotes cell-autonomous angiogenesis of skeletal muscle microvascular endothelial cells (SMMECs) via VEGFR2 regulation | [51] |
Thyroid cancer | Promotes angiogenesis through regulating fibroblast Growth Factor 2 (FGF2) protein secretion from tumor-associated macrophages (TMAs) | [52] | ||
Gastric cancer | Correlated with endothelial vessel density and promotes angiogenesis by regulating VE-cadherin/β-catenin complex, extracellular signal-regulated kinase (ERK)/ matrix metalloproteinase (MMP), and focal adhesion kinase (FAK)/paxillin signalizing pathways | [53] | ||
Neuroblastoma | Promotes hypoxia-induced angiogenesis by increasing FGF2 expression | [54] | ||
Ubiquitin conjugating enzyme E2 C pseudogene 3 (UBE2CP3) | 4q12 | Hepatocellular carcinoma | Stimulates vascular endothelial growth factor A (VEGFA) secretion and promotes HUVEC proliferation, migration and tube formation through activating ERK1/2/ hypoxia inducible factor 1 subunit alpha (HIF-1α)/VEGFA signalling pathways | [187] |
PVT1 | 8q24.21 | Angiogenesis | Regulates connective tissue growth factor (CTGF) and angiopoietin 2 (ANGPT2) expression through interacting with miR-26b and promotes the angiogenesis of HUVEC | [72] |
Glioma | Promotes glioma VEC proliferation, migration and angiogenesis by regulating miR-186 | [73] | ||
Linc00152 | 2p11.2 | Angiogenesis | Promotes oxidized low-density lipoprotein (oxLDL)-treated HUVEC migration and inhibits apoptosis by sponging miR-4767 that regulates angiogenesis | [188] |
TUG1 | 22q12.2 | Glioblastoma | Promotes glioblastoma-induced EC proliferation, migration and angiogenesis by inhibiting miR-299 | [69] |
Angiogenesis | Regulates rapamycin-mediated inhibition of EC proliferation, migration and tube formation | [70] | ||
Hepatoblastoma | Promotes angiogenesis via regulating VEGFA expression by sponging miR-34a | [71] | ||
Urothelial cancer associated 1 (UCA1) | 19p13.12 | Angiogenesis | Promotes human microvascular endothelial cells (HMEC) proliferation, migration and tube formation through inhibiting miR-195 and activating mitogen-activated protein kinase kinase (MEK)/ERK/mTOR pathways | [189] |
MEG3 | 14q32.2 | Breast cancer | Overexpressed MEG3 suppresses tumour growth and angiogenesis via inhibiting AKT pathway | [61] |
Osteoarthritis | Regulates angiogenesis through inversely association of VEGF levels | [62] | ||
Angiogenesis | Overexpressed MEG3 suppresses VEC proliferation, migration and angiogenesis via regulating miR-9 | [63] | ||
Ischemic brain injury | Downregulated MEG3 promotes angiogenesis via negatively regulated Notch pathways | [64] | ||
Cerebral infarction | Downregulated MEG3 promotes angiogenesis of OGD/R-induced rat brain microvascular endothelial cells (RBMVECs) through regulating P53/NOX4 axis | [65] | ||
Angiogenesis | Downregulated MEG3 suppresses VEGF-induced EC migration and angiogenesis through modulating VEGFR2 expression | [66] | ||
Linc00511 | 17q24.3 | Pancreatic ductal adenocarcinoma | Promotes tumour cells proliferation, migration, invasion and angiogenesis through sponging miR-29b-3p | [190] |
Small nucleolar RNA host gene 15 (SNHG15) | 7p13 | Glioma | Promotes glioma VEC proliferation, migration and tube formation by increasing VEGFA and cell division cycle 42 (Cdc42) expression by targeting miR-153 | [191] |
LincRNA-p21 | 6p21.2 | Non–Small Cell Lung Cancer | Enhances VEGFA production and promotes angiogenesis | [192] |
ANRIL | 9p21.3 | Diabetes mellitus | Overexpressed ANRIL promotes angiogenesis by increasing VEGF expression via activating NF-kB pathway | [74] |
HOTAIR | 12q13.13 | Nasopharyngeal carcinoma | Promotes angiogenesis through upregulating VEGFA and angiopoietin 2 (Ang2) expression by glucose regulated protein 78 (GRP78). | [76] |
H19 | 11p15.5 | Glioma | Promotes glioma-induced angiogenesis by increasing miR-29a | [81] |
LINC00657 | 20q11.23 | Angiogenesis | Promotes oxLDL-mediated EC proliferation, migration and tube formation by interacting with miR-590-3p and increasing VEGF, MMP-2 and MMP-9 expression | [193] |
lncRNA | Correlations of the Functional Involvement of lncRNAs in ED and Diabetes | References |
---|---|---|
ANRIL | Up-regulated in DM and alters the EC function through increasing VEGF expression by P300/miR200b/EZH2 | [75] |
MALAT1 | Highly expressed in DM and upregulates inflammatory mediators IL-6 & TNF-α through activating SAA3 and that stimulates DM-induced EC dysfunction via p38MAPK signaling pathway | [55,56,57] |
MEG3 | Down-expressed in DM and enhances DM-mediated EC dysfunctions through altering PI3K/Akt signaling pathway | [67,68] |
Myocardial infarction associated transcript (MIAT) | Induces DM induced EC dysfunction by acting as a competing endogenous RNA (CeRNA) via MIAT/miR-150-5p/VEGF network | [209] |
RNCR3 | Up-regulated in DM and stimulates DM-induced retinal EC dysfunction through regulating RNCR3/ Kruppel like factor 2 (KLF2)/miR-185-5p pathway | [79] |
lncRNA. | Correlations of the Functional Involvement of lncRNAs in ED and Atherosclerosis | References |
---|---|---|
Lnc00113 | Promotes abnormal EC proliferation, survival and migration via activating PI3K/Akt/mTOR pathway that disrupt EC function and develop atherosclerosis | [230] |
MALAT1 | Protects EC from ox-LDL-induced EC dysfunction through inhibiting miR-22-3P and upregulating C-X-C Motif Chemokine Receptor 2 (CXCR2) & AKT expression in the settings of atherosclerosis | [58] |
HOTAIR | Protect EC from injury and enhance EC proliferation, migration and inhibit apoptosis via thymic stromal lymphopoietin (TSLP)-PI3K/AKT-HOTAIR pathway that regulates angiogenesis pathogenesis and progression. | [77] |
RP11-714G18.1 | Suppresses EC migration through RP11-714G18.1/ LRP2 binding protein (LRP2BP)/MMP1 signaling pathway that provide athero-defensive role in atherosclerosis-related EC dysfunction. | [231] |
lincRNA-p21 | Stimulates ox-LDL-induced EC apoptosis and LOX-1 expression via activation of protein kinase C delta (PKCδ) that regulates atherosclerosis pathogenesis | [232] |
TCONS_00024652 | Promotes EC proliferation, migration and angiogenesis via downregulating miR21 expression that stimulates atherosclerosis progression | [233] |
XIST | Promotes ox-LDL-mediated EC injury via miR-320/ nucleotide binding oligomerization domain containing 2 (NOD2) pathway and modulates atherosclerosis | [80] |
RNCR3 | Regulates EC function and accelerates atheroprotective function to the endothelium via acting as a ceRNA and forming a feedback loop with KLF2 and miR-185-5p | [78] |
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Islam, R.; Lai, C. A Brief Overview of lncRNAs in Endothelial Dysfunction-Associated Diseases: From Discovery to Characterization. Epigenomes 2019, 3, 20. https://doi.org/10.3390/epigenomes3030020
Islam R, Lai C. A Brief Overview of lncRNAs in Endothelial Dysfunction-Associated Diseases: From Discovery to Characterization. Epigenomes. 2019; 3(3):20. https://doi.org/10.3390/epigenomes3030020
Chicago/Turabian StyleIslam, Rashidul, and Christopher Lai. 2019. "A Brief Overview of lncRNAs in Endothelial Dysfunction-Associated Diseases: From Discovery to Characterization" Epigenomes 3, no. 3: 20. https://doi.org/10.3390/epigenomes3030020