|Year : 2019 | Volume
| Issue : 2 | Page : 22-26
Factors regulating the change of vascular smooth muscle cells in cardiovascular diseases: A mini review
Haocheng Li1, Qingfeng Sun1, Ye Yao2, Chao Yuan1, Gaoyan Liu1, Bao Jing1, Jingbo Li1, Haiyang Wang1
1 Department of Vascular Surgery, The First Affiliated Hospital of Harbin Medical University, Harbin, China
2 Department of Cardiac Surgery, The First Affiliated Hospital of Harbin Medical University, Harbin, China
|Date of Submission||24-Mar-2019|
|Date of Decision||23-May-2019|
|Date of Acceptance||17-Jun-2019|
|Date of Web Publication||27-Nov-2019|
Department of Vascular Surgery, The First Affiliated Hospital of Harbin Medical University, Harbin 150001
Source of Support: None, Conflict of Interest: None
Vascular smooth muscle cells (VSMCs) are responsible for blood vessel relaxation contraction and hemodynamics. Cardiovascular diseases (CVDs) are a major cause of human death worldwide, and the pathophysiological changes to the VSMCs such as apoptosis, hypertrophy, and migration contribute to these diseases. Herein, we recapitulated the importance of molecular factors relevant to the regulation of VSMCs and how VSMCs are involved in these pathophysiological changes. This is significant to the development of therapeutic treatments for various CVDs. A literature search was conducted to identify studies assessing the regulating factors of VSMCs using the Medline and PubMed databases from inception to February 1, 2019. Search terms were applied either as single or in combination. In the present review, we will discuss some of the influential factors that may affect and regulate the changes of VSMCs in CVDs.
Keywords: Cardiovascular diseases, molecules, noncoding RNAs, signaling pathways, vascular smooth muscle cells
|How to cite this article:|
Li H, Sun Q, Yao Y, Yuan C, Liu G, Jing B, Li J, Wang H. Factors regulating the change of vascular smooth muscle cells in cardiovascular diseases: A mini review. Transl Surg 2019;4:22-6
|How to cite this URL:|
Li H, Sun Q, Yao Y, Yuan C, Liu G, Jing B, Li J, Wang H. Factors regulating the change of vascular smooth muscle cells in cardiovascular diseases: A mini review. Transl Surg [serial online] 2019 [cited 2020 Apr 2];4:22-6. Available from: http://www.translsurg.com/text.asp?2019/4/2/22/271821
| Introduction|| |
Cardiovascular diseases (CVDs) remain the leading cause of death worldwide. CVDs include coronary artery disease, aorticaneurysms, cerebrovascular disease, peripheral artery diseases, pulmonary arterial hypertension, and renal stenosis. The excessive growth of VSMCs involved in several type of CVDs such as atherosclerosis and restenosis. The loss of VSMC contractile functions leads to aortic aneurysms, and the phenotypic switching of VSMCs is associated with pulmonary arterial resistance and remodeling.
VSMCs are components of the blood vessel wall which can maintain blood pressure, vessel integrity, and function. Unlike skeletal muscle and myocardium. VSMCs exhibit high rates of proliferation, migration, and production of extracellular matrix (ECM) components such as collagen, elastin, and proteoglycans. VSMCs are of highly phenotype changes and highly plasticity. Understanding the molecular mechanisms of the pathophysiological changes of VSMCs is essential for the development of therapeutic treatments for various CVDs.
| Literature Search|| |
A literature search was conducted to identify studies assessing the regulating factors of VSMCs using the Medline and PubMed databases from inception to February 1, 2019. The following search terms were applied either as single or in combination: “VSMCs” OR “VSMCs” (Title/Abstract), AND “signal pathways” AND/OR “molecules,” AND/OR “noncoding RNAs” OR “MicroRNAs” OR “Long noncoding RNAs.” Abstracts were analyzed for relevance, and studies describing the regulating factors of VSMCs were retrieved.
| Signaling Pathways and Molecules Affecting Vascular Smooth Muscle Cell Functions|| |
Many signaling pathways and molecules can regulate the functions of VSMCs. The prominent molecule factors include platelet-derived growth factors and their receptors (PDGF and PDGFR); Src; epidermal growth factor (EGF); Angiotensin II (Ang-II) and endothelin I; and thrombin. The signaling pathways such as Ras/MAPK; JAK/STAT; phospholipase C-γ; Signaling pathways of insulin;PTEN/AKT; NOTCH and transforming growth factor β. We will briefly introduce the molecular and pathway functions of VSMCs and elucidate some of them.
PDGFs and their receptors are significant molecules which can regulate VSMC proliferation,, and among the PDFGs, PDGF-BB is the most potent stimulus. Past several decades have found that Src family can mediate the transcription of c-myc. Silencing Src can inhibit VSMC proliferation, and multiple signaling pathways in Ang-II induce VSMC proliferation. Fibroblast growth factors can promotethe VSMCs proliferation by influencing the Ras/MAPKand Src activated signaling pathways., In this part, we will elaborate on the molecule thrombin and reactive oxygen species (ROS).
Thrombin is a crucial molecule in homeostasis with procoagulant and anticoagulant activities., Thrombin can affect various cell types such as VSMCs, fibroblast, T lymphocyte, and monocytes., Studies have found a positive correlation between thrombin and VSMCs. The areas where thrombin bind to its receptor the expression of VSMCs also increased. The active PAR-1 which is induced by thrombin can enhance VSMC expression.,, Further, the study found that this positive regulation is functioned via NF-κB signaling pathway. Thrombin can also stimulate VSMCs proliferation via PI3K/AKT-1, ERK1/2, activating protein1 pathways.,
Reactive oxygen species
ROS include hydrogen peroxide, superoxide anion, and hydroxyl radical. All the species are the production of oxidative stress. ROS are oxygen-derived chemical molecules. these species can implicate in vascular cells dysfunction and DNA damage, lead to permanent cellular damage and death. The imbalance in the mitochondrial respiratory and oxidative enzymes results in excessive ROS. ROS can regulate fibroblast proliferation  and macrophage infiltration. In addition, they can regulate the degradation and remodeling of the ECM by upregulating the matrix metalloproteinases. The apoptosis of VSMCs induced by ROS may via activating NFκB and activator protein 1 signaling pathways.
Signaling pathways such as Ras/MAPK cascade are important in VSMC proliferation by inducing transcription of several genes which are linked to cell progression and proliferation. Phospholipase C-γ pathway can be activated by PDGFR-β. The activated pathway can suppress the mitogenic and chemotactic response to PDGF in VSMCs, thus inhibiting VSMC proliferation., Signal transducers and activators of transcription (STAT) is important in the regulation of cell cycle progression, which can be triggered by various factors, i.e., inflammatory cytokines and EGF., JAK can transduce extracellular signals via STAT pathway and affect VSMC migration and proliferation.
| Noncoding Rnas|| |
Noncoding RNAs which are range from 22 to 24 or >200 nt contribute to complexity regulatory networks. Recent studies have demonstrated that noncoding RNAs (including microRNAs [miRNAs] and long noncoding RNAs (lncRNAs]) are key players in the regulation of VSMC functions.,,
MicroRNAs are highly conserved noncoding RNAs that regulate gene expression at the posttranscriptional level by binding to complementary sequences in the 3' untranslated regions of target mRNA transcripts., They can inhibit or degrade the cleavage and translation of mRNA, exerting posttranscriptional effects and affecting the expression of genes and proteins.,, One microRNA can regulate various kinds of mRNAs, and one mRNA also can be regulated by a variety of miRs. This indicates that microRNAs participate in the pathological and physiological processes of cells in a complex way and play an extremely important regulatory role in cell growth, differentiation, proliferation, apoptosis, and metabolism. Studies have demonstrated that some miRNAs inhibit or promote VSMC proliferation., The following section describes the categories of miRNAs namely inhibition miRNAs and promotion miRNAs.
It was shown that miRNA-34a can significantly inhibit VSMC proliferation and migration, while VSMCs will be dramatically promoted proliferation if miRNA-34a is knocked down., miRNA-141 through targeting pregnancy-associated plasma protein A inhibits VSMC proliferation., It was shown that miRNA-206 can inhibit VSMC proliferation by silencing the expression of the gap junction protein connexin 43.
MicroRNA-17 overexpression in VSMCs by activating NF-κB P65 can promote VSMC proliferation. Furthermore, miRNA-675 promotes VSMC proliferation by targeting phosphatase and the tensin homolog (PTEN). miRNA-29a through downregulation of Fbw7/CDC4 enhances VSMC proliferation, and miRNA146a directly targets KLF4 can promote VSMCs proliferation.,
MicroRNA-21 promotes and inhibits vascular smooth muscle cell proliferation
On the one hand, studies suggest that miRNA-21 promotes VSMC proliferation and anti-apoptosis by silencing PTEN, a lipid and protein phosphatase and an important tumor suppressor protein, and activates the AKT to regulate the activity of a number of targets. On the other hand, some studies demonstrate that the miRNA-21 by silencing programmed cell death protein 4 (PDCD4) inhibits VSMC proliferation., Further studies need to be performed to understand the complicated role of miRNA-21.
Long noncoding RNAs
lncRNAs, classified as larger than 200 nucleotide-lncRNAs, lack distinct open reading frames., The expression of lncRNAs are lower than the protein-coding RNAs. lncRNAs involved in various biological, and have diverse biological functions such as host transcription of miRNAs  and molecule scaffolds for protein complexes; regulate genes expression. lncRNAs involved in VSMCs regulation whether the cells are normal or diseased.,. The overexpressed lncRNA H19 can inhibit VSMC proliferation and promote apoptosis via HIF1α. Another lncRNA, ANRIL, can also regulate VSMC proliferation and apoptosis., Studies have found that knockdown SERCA, a multi-exonic lncRNA, can downregulate the contractile function of VSMCs and upregulate VSMC migration.
| Conclusion|| |
VSMCs are components of the blood vessel wall, and their cell changes contribute to the etiology of many types of CVDs. As a result of extensive research, we have begun to understand their molecular functions and how these processes affect VSMCs. We clarify that the expression of noncoding RNA is related to human vascular diseases, which means that noncoding RNA may be mediating the occurrence and development of CVDs. The study of VSMC molecule is still in its early stage. Many questions such as to what extent these transcripts affect the function of VSMCs and whether they can be effective targets for the treatment of CVDs remain unanswered. Overall, although our research is still in its early stage, it represents a rapidly developing and novel research area. Future research will further clarify our understanding of VSMC biology and help us to use these interesting molecules for the treatment of CVDs.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Bruemmer D, Daugherty A, Lu H, Rateri DL. Relevance of angiotensin II-induced aortic pathologies in mice to human aortic aneurysms. Ann N Y Acad Sci
Silverio A, Cavallo P, De Rosa R, Galasso G. Big health data and cardiovascular diseases: A challenge for research, an opportunity for clinical care. Front Med
Rudijanto A. The role of vascular smooth muscle cells on the pathogenesis of atherosclerosis. Acta Med Indones
Yao Y, Li H, Da X, He Z, Tang B, Li Y, Hu C, Xu C, Chen Q, Wang QK. SUMOylation of Vps34 by SUMO1 promotes phenotypic switching of vascular smooth muscle cells by activating autophagy in pulmonary arterial hypertension. Pulm Pharmacol Ther
Leung A, Stapleton K, Natarajan R. Functional long non-coding RNAs in vascular smooth muscle cells. Curr Top Microbiol Immunol
Wobus AM, Guan K, Yang HT, Boheler KR. Embryonic stem cells as a model to study cardiac, skeletal muscle, and vascular smooth muscle cell differentiation. Methods Mol Biol
Rabkin SW. The role matrix metalloproteinases in the production of aortic aneurysm. Prog Mol Biol Transl Sci
Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev
Wang D, Uhrin P, Mocan A, Waltenberger B, Breuss JM, Tewari D, Mihaly-Bison J, Huminiecki Ł, Starzyński RR, Tzvetkov NT, Horbańczuk J, Atanasov AG. Vascular smooth muscle cell proliferation as a therapeutic target. Part 1: Molecular targets and pathways. Biotechnol Adv
Fredriksson L, Li H, Eriksson U. The PDGF family: Four gene products form five dimeric isoforms. Cytokine Growth Factor Rev
Lu QB, Wan MY, Wang PY, Zhang CX, Xu DY, Liao X, Sun HJ. Chicoric acid prevents PDGF-BB-induced VSMC dedifferentiation, proliferation and migration by suppressing ROS/NFkappaB/mTOR/P70S6K signaling cascade. Redox Biol
Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev
Barone MV, Courtneidge SA. Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src. Nature
Walcher D, Babiak C, Poletek P, Rosenkranz S, Bach H, Betz S, Durst R, Grüb M, Hombach V, Strong J, Marx N. C-Peptide induces vascular smooth muscle cell proliferation: Involvement of SRC-kinase, phosphatidylinositol 3-kinase, and extracellular signal-regulated kinase 1/2. Circ Res
Sayeski PP, Ali MS. The critical role of c-Src and the Shc/Grb2/ERK2 signaling pathway in angiotensin II-dependent VSMC proliferation. Exp Cell Res
Lindner V, Reidy MA. Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc Natl Acad Sci U S A
Seymour KA, Sadowitz B, Stein JJ, Lawler J, Maier KG, Gahtan V. Vascular smooth muscle cell migration induced by domains of thrombospondin-1 is differentially regulated. Am J Surg
Narayanan S. Multifunctional roles of thrombin. Ann Clin Lab Sci
McNamara CA, Sarembock IJ, Bachhuber BG, Stouffer GA, Ragosta M, Barry W, Gimple LW, Powers ER, Owens GK. Thrombin and vascular smooth muscle cell proliferation: Implications for atherosclerosis and restenosis. Semin Thromb Hemost
Martorell L, Martinez-Gonzalez J, Rodriguez C, Gentile M, Calvayrac O, Badimon L. Thrombin and protease-activated receptors (PARs) in atherothrombosis. Thromb Haemost
Chung SW, Park JW, Lee SA, Eo SK, Kim K. Thrombin promotes proinflammatory phenotype in human vascular smooth muscle cell. Biochem Biophys Res Commun
Stoop AA, Lupu F, Pannekoek H. Colocalization of thrombin, PAI-1, and vitronectin in the atherosclerotic vessel wall: A potential regulatory mechanism of thrombin activity by PAI-1/vitronectin complexes. Arterioscler Thromb Vasc Biol
Ko WC, Chen BC, Hsu MJ, Tsai CT, Hong CY, Lin CH. Thrombin induced connective tissue growth factor expression in rat vascular smooth muscle cells via the PAR-1/JNK/AP-1 pathway. Acta Pharmacol Sin
Wang H, Ubl JJ, Stricker R, Reiser G. Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways. Am J Physiol Cell Physiol
Maruyama I, Shigeta K, Miyahara H, Nakajima T, Shin H, Ide S, Kitajima I. Thrombin activates NF-kappa B through thrombin receptor and results in proliferation of vascular smooth muscle cells: Role of thrombin in atherosclerosis and restenosis. Ann N Y Acad Sci
Hsieh HL, Tung WH, Wu CY, Wang HH, Lin CC, Wang TS, Yang CM. Thrombin induces EGF receptor expression and cell proliferation via a PKC (delta)/c-Src-dependent pathway in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol
Smiljanic K, Obradovic M, Jovanovic A, Djordjevic J, Dobutovic B, Jevremovic D, Marche P, Isenovic ER. Thrombin stimulates VSMC proliferation through an EGFR-dependent pathway: Involvement of MMP-2. Mol Cell Biochem
Rampon C, Volovitch M, Joliot A, Vriz S. Hydrogen peroxide and redox regulation of developments. Antioxidants (Basel)
2018;7(11). pii: E159.
Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and mitochondrial DNA damage in heart failure. Circ J
2008;72 Suppl A: A31-7.
Sawada H, Hao H, Naito Y, Oboshi M, Hirotani S, Mitsuno M, Miyamoto Y, Hirota S, Masuyama T. Aortic iron overload with oxidative stress and inflammation in human and murine abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol
Ejiri J, Inoue N, Tsukube T, Munezane T, Hino Y, Kobayashi S, Hirata K, Kawashima S, Imajoh-Ohmi S, Hayashi Y, Yokozaki H, Okita Y, Yokoyama M. Oxidative stress in the pathogenesis of thoracic aortic aneurysm: Protective role of statin and angiotensin II type 1 receptor blocker. Cardiovasc Res
Forstermann U. Nitric oxide and oxidative stress in vascular disease. Pflugers Arch
Forstermann U. Oxidative stress in vascular disease: Causes, defense mechanisms and potential therapies. Nat Clin Pract Cardiovasc Med
Davies KJ. The broad spectrum of responses to oxidants in proliferating cells: A new paradigm for oxidative stress. Iubmb Life
Day RM, Suzuki YJ, Fanburg BL. Regulation of glutathione by oxidative stress in bovine pulmonary artery endothelial cells. Antioxid Redox Signal
Lizarbe TR, Tarin C, Gomez M, Lavin B, Aracil E, Orte LM, Zaragoza C. Nitric oxide induces the progression of abdominal aortic aneurysms through the matrix metalloproteinase inducer EMMPRIN. Am J Pathol
Kumar B, Iqbal MA, Singh RK, Bamezai RN. Resveratrol inhibits TIGAR to promote ROS induced apoptosis and autophagy. Biochimie
Murphy LO, Blenis J. MAPK signal specificity: The right place at the right time. Trends Biochem Sci
Bornfeldt KE, Raines EW, Graves LM, Skinner MP, Krebs EG, Ross R. Platelet-derived growth factor. Distinct signal transduction pathways associated with migration versus proliferation. Ann N Y Acad Sci
Caglayan E, Vantler M, Leppanen O, Gerhardt F, Mustafov L, Ten FH, Kappert K, Odenthal M, Zimmermann WH, Tallquist MD, Rosenkranz S. Disruption of platelet-derived growth factor-dependent phosphatidylinositol 3-kinase and phospholipase C-gamma 1 activity abolishes vascular smooth muscle cell proliferation and migration and attenuates neointima formation in vivo
. J Am Coll Cardiol
Yasunari K, Kohno M, Kano H, Hanehira T, Minami M, Yoshikawa J. Anti-atherosclerotic action of vascular D1 receptors. Clin Exp Pharmacol Physiol Suppl
Sikorski K, Czerwoniec A, Bujnicki JM, Wesoly J, Bluyssen HA. STAT1 as a novel therapeutical target in pro-atherogenic signal integration of IFN-gamma, TLR4 and IL-6 in vascular disease. Cytokine Growth Factor Rev
Henson ES, Gibson SB. Surviving cell death through epidermal growth factor (EGF) signal transduction pathways: Implications for cancer therapy. Cell Signal
International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 2004;431(7011):931-45.
Wang D, Atanasov AG. The microRNAs regulating vascular smooth muscle cell proliferation: A minireview. Int J Mol Sci
2019;20(2). pii: E324.
Song X, Shan D, Chen J, Jing Q. miRNAs and lncRNAs in vascular injury and remodeling. Sci China Life Sci
Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J
Mohr AM, Mott JL. Overview of microRNA biology. Semin Liver Dis
Do DN, Dudemaine PL, Fomenky BE, Ibeagha-Awemu EM. Integration of miRNA weighted gene co-expression network and miRNA-mRNA co-expression analyses reveals potential regulatory functions of miRNAs in calf rumen development. Genomics
2018. pii: S0888-7543(18) 30125-3.
Zhang MJ, Zhou Y, Chen L, Wang YQ, Wang X, Pi Y, Gao CY, Li JC, Zhang LL. An overview of potential molecular mechanisms involved in VSMC phenotypic modulation. Histochem Cell Biol
Ye D, Shen Z, Zhou S. Function of microRNA-145 and mechanisms underlying its role in malignant tumor diagnosis and treatment. Cancer Manag Res
Garavelli S, De Rosa V, de Candia P. The multifaceted interface between cytokines and microRNAs: An ancient mechanism to regulate the good and the bad of inflammation. Front Immunol
Kang H, Hata A. MicroRNA regulation of smooth muscle gene expression and phenotype. Curr Opin Hematol
Vienberg S, Geiger J, Madsen S, Dalgaard LT. MicroRNAs in metabolism. Acta Physiol (Oxf)
Di Leva G, Garofalo M, Croce CM. MicroRNAs in cancer. Annu Rev Pathol
Neller K, Klenov A, Guzman JC, Hudak KA. Integration of the pokeweed miRNA and mRNA transcriptomes reveals targeting of jasmonic acid-responsive genes. Front Plant Sci
Parmacek MS. MicroRNA-modulated targeting of vascular smooth muscle cells. J Clin Invest
Chen Q, Yang F, Guo M, Wen G, Zhang C, Luong LA, Zhu J, Xiao Q, Zhang L. miRNA-34a reduces neointima formation through inhibiting smooth muscle cell proliferation and migration. J Mol Cell Cardiol
Wang H, Jin Z, Pei T, Song W, Gong Y, Chen D, Zhang L, Zhang M, Zhang G. Long noncoding RNAs C2dat1 enhances vascular smooth muscle cell proliferation and migration by targeting MiR-34a-5p. J Cell Biochem
Zhang Y, Chen B, Ming L, Qin H, Zheng L, Yue Z, Cheng Z, Wang Y, Zhang D, Liu C, Bin W, Hao Q, Song F, Ji B. MicroRNA-141 inhibits vascular smooth muscle cell proliferation through targeting PAPP-A. Int J Clin Exp Pathol
Sun Y, Chen D, Cao L, Zhang R, Zhou J, Chen H, Li Y, Li M, Cao J, Wang Z. MiR-490-3p modulates the proliferation of vascular smooth muscle cells induced by ox-LDL through targeting PAPP-A. Cardiovasc Res
Yang D, Sun C, Zhang J, Lin S, Zhao L, Wang L, Lin R, Lv J, Xin S. Proliferation of vascular smooth muscle cells under inflammation is regulated by NF-kappaB p65/microRNA-17/RB pathway activation. Int J Mol Med
Lv J, Wang L, Zhang J, Lin R, Wang L, Sun W, Wu H, Xin S. Long noncoding RNA H19-derived miR-675 aggravates restenosis by targeting PTEN. Biochem Biophys Res Commun
Zheng B, Zheng CY, Zhang Y, Yin WN, Li YH, Liu C, Zhang XH, Nie CJ, Zhang H, Jiang W, Liu SF, Wen JK. Regulatory crosstalk between KLF5, miR-29a and Fbw7/CDC4 cooperatively promotes atherosclerotic development. Biochim Biophys Acta Mol Basis Dis
Joshi SR, Comer BS, McLendon JM, Gerthoffer WT. MicroRNA regulation of smooth muscle phenotype. Mol Cell Pharmacol
Cao J, Zhang K, Zheng J, Dong R. MicroRNA-146a and -21 cooperate to regulate vascular smooth muscle cell proliferation via modulation of the Notch signaling pathway. Mol Med Rep
Oudit GY, Penninger JM. Cardiac regulation by phosphoinositide 3-kinases and PTEN. Cardiovasc Res
Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature
Lin Y, Liu X, Cheng Y, Yang J, Huo Y, Zhang C. Involvement of MicroRNAs in hydrogen peroxide-mediated gene regulation and cellular injury response in vascular smooth muscle cells. J Biol Chem
Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev
Simion V, Haemmig S, Feinberg MW. LncRNAs in vascular biology and disease. Vascul Pharmacol
Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea MD, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A
Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol
Kim YK, Kook H. Diverse roles of noncoding RNAs in vascular calcification. Arch Pharm Res
Turner AW, Wong D, Khan MD, Dreisbach CN, Palmore M, Miller CL. Multi-omics approaches to study long non-coding RNA function in atherosclerosis. Front Cardiovasc Med
Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res
Das S, Zhang E, Senapati P, Amaram V, Reddy MA, Stapleton K, Leung A, Lanting L, Wang M, Chen Z, Kato M, Oh HJ, Guo Q, Zhang X, Zhang B, Zhang H, Zhao Q, Wang W, Wu Y, Natarajan R. A novel angiotensin II-induced long noncoding RNA giver regulates oxidative stress, inflammation, and proliferation in vascular smooth muscle cells. Circ Res
Leung A, Trac C, Jin W, Lanting L, Akbany A, Saetrom P, Schones DE, Natarajan R. Novel long noncoding RNAs are regulated by angiotensin II in vascular smooth muscle cells. Circ Res
Li DY, Busch A, Jin H, Chernogubova E, Pelisek J, Karlsson J, Sennblad B, Liu S, Lao S, Hofmann P, Bäcklund A, Eken SM, Roy J, Eriksson P, Dacken B, Ramanujam D, Dueck A, Engelhardt S, Boon RA, Eckstein HH, Spin JM, Tsao PS, Maegdefessel L. H19 induces abdominal aortic aneurysm development and progression. Circulation
Congrains A, Kamide K, Katsuya T, Yasuda O, Oguro R, Yamamoto K, Ohishi M, Rakugi H. CVD-associated non-coding RNA, ANRIL, modulates expression of atherogenic pathways in VSMC. Biochem Biophys Res Commun
Man H, Bi W. Expression of a novel long noncoding RNA (lncRNA), GASL1, is downregulated in patients with intracranial aneurysms and regulates the proliferation of vascular smooth muscle cells in vitro
. Med Sci Monit
Bell RD, Long X, Lin M, Bergmann JH, Nanda V, Cowan SL, Zhou Q, Han Y, Spector DL, Zheng D, Miano JM. Identification and initial functional characterization of a human vascular cell-enriched long noncoding RNA. Arterioscler Thromb Vasc Biol