MicroRNAs in Hyperglycemia Induced Endothelial Cell Dysfunction

Hyperglycemia is closely associated with prediabetes and Type 2 Diabetes Mellitus. Hyperglycemia increases the risk of vascular complications such as diabetic retinopathy, diabetic nephropathy, peripheral vascular disease and cerebro/cardiovascular diseases. Under hyperglycemic conditions, the endothelial cells become dysfunctional. In this study, we investigated the miRNA expression changes in human umbilical vein endothelial cells exposed to different glucose concentrations (5, 10, 25 and 40 mM glucose) and at various time intervals (6, 12, 24 and 48 h). miRNA microarray analyses showed that there is a correlation between hyperglycemia induced endothelial dysfunction and miRNA expression. In silico pathways analyses on the altered miRNA expression showed that the majority of the affected biological pathways appeared to be associated to endothelial cell dysfunction and apoptosis. We found the expression of ten miRNAs (miR-26a-5p, -26b-5p, 29b-3p, -29c-3p, -125b-1-3p, -130b-3p, -140-5p, -192-5p, -221-3p and -320a) to increase gradually with increasing concentration of glucose. These miRNAs were also found to be involved in endothelial dysfunction. At least seven of them, miR-29b-3p, -29c-3p, -125b-1-3p, -130b-3p, -221-3p, -320a and -192-5p, can be correlated to endothelial cell apoptosis.

[1]  Jing Yang,et al.  Expression of long non-coding RNA and mRNA in the hippocampus of mice with type 2 diabetes , 2018, Molecular medicine reports.

[2]  Hai Jin,et al.  Curcumin inhibits cell proliferation and induces apoptosis of human non-small cell lung cancer cells through the upregulation of miR-192-5p and suppression of PI3K/Akt signaling pathway. , 2015, Oncology reports.

[3]  H. Lan,et al.  miR-140-5p inhibits ovarian cancer growth partially by repression of PDGFRA. , 2015, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[4]  M. Harmsen,et al.  The decrease in histone methyltransferase EZH2 in response to fluid shear stress alters endothelial gene expression and promotes quiescence , 2015, Angiogenesis.

[5]  Lois E. H. Smith,et al.  SOCS3 in retinal neurons and glial cells suppresses VEGF signaling to prevent pathological neovascular growth , 2015, Science Signaling.

[6]  Yang He,et al.  MicroRNA 192 regulates chemo-resistance of lung adenocarcinoma for gemcitabine and cisplatin combined therapy by targeting Bcl-2. , 2015, International journal of clinical and experimental medicine.

[7]  Jianliang Zhang,et al.  MiR-30b Is Involved in the Homocysteine-Induced Apoptosis in Human Coronary Artery Endothelial Cells by Regulating the Expression of Caspase 3 , 2015, International journal of molecular sciences.

[8]  H. Dweep,et al.  miRWalk2.0: a comprehensive atlas of microRNA-target interactions , 2015, Nature Methods.

[9]  Q. Hou,et al.  Interleukin-17 Stimulates STAT3-Mediated Endothelial Cell Activation for Neutrophil Recruitment , 2015, Cellular Physiology and Biochemistry.

[10]  C. Hardin,et al.  ROCK2 primes the endothelium for vascular hyperpermeability responses by raising baseline junctional tension. , 2015, Vascular pharmacology.

[11]  F. Das,et al.  High glucose enhances microRNA-26a to activate mTORC1 for mesangial cell hypertrophy and matrix protein expression. , 2015, Cellular signalling.

[12]  Arunmozhiarasi Armugam,et al.  MiR-335 Regulates Hif-1α to Reduce Cell Death in Both Mouse Cell Line and Rat Ischemic Models , 2015, PloS one.

[13]  Lei Yang,et al.  MiR-26b modulates insulin sensitivity in adipocytes by interrupting the PTEN/PI3K/AKT pathway , 2015, International Journal of Obesity.

[14]  Xiao-yan Xie,et al.  Mcl-1 Is a Novel Target of miR-26b That Is Associated with the Apoptosis Induced by TRAIL in HCC Cells , 2015, BioMed research international.

[15]  Ji-de Lu,et al.  miR-103 Regulates Oxidative Stress by Targeting the BCL2/Adenovirus E1B 19 kDa Interacting Protein 3 in HUVECs , 2015, Oxidative medicine and cellular longevity.

[16]  B. Xiao,et al.  MicroRNA-221/222 regulate ox-LDL-induced endothelial apoptosis via Ets-1/p21 inhibition , 2015, Molecular and Cellular Biochemistry.

[17]  Wei Chen,et al.  Role of sphingosine-1-phosphate receptor 1 and sphingosine-1-phosphate receptor 2 in hyperglycemia-induced endothelial cell dysfunction. , 2015, International journal of molecular medicine.

[18]  Jia Liu,et al.  miR-146a-5p Antagonized AGEs- and P.g-LPS-Induced ABCA1 and ABCG1 Dysregulation in Macrophages via IRAK-1 Downregulation , 2015, Inflammation.

[19]  O. Bakke,et al.  Oligomerized, filamentous surface presentation of RANTES/CCL5 on vascular endothelial cells , 2015, Scientific Reports.

[20]  R. Urrutia,et al.  Gestational Diabetes Mellitus Impairs Fetal Endothelial Cell Functions Through a Mechanism Involving MicroRNA-101 and Histone Methyltransferase Enhancer of Zester Homolog-2 , 2015, Arteriosclerosis, thrombosis, and vascular biology.

[21]  N. Mochizuki,et al.  RhoA and ROCK mediate histamine-induced vascular leakage and anaphylactic shock , 2015, Nature Communications.

[22]  Hongmei Zhu,et al.  Identification of microRNA biomarkers in type 2 diabetes: a meta-analysis of controlled profiling studies , 2015, Diabetologia.

[23]  L. Yao,et al.  Curcumin promotes apoptosis by activating the p53-miR-192-5p/215-XIAP pathway in non-small cell lung cancer. , 2015, Cancer letters.

[24]  B. Göttgens,et al.  The Endothelial Transcription Factor ERG Promotes Vascular Stability and Growth through Wnt/β-Catenin Signaling , 2015, Developmental cell.

[25]  Jiasun Lu,et al.  Regulation of growth of human bladder cancer by miR-192 , 2015, Tumor Biology.

[26]  M. Hirata,et al.  Role of microRNAs 221/222 on Statin Induced Nitric Oxide Release in Human Endothelial Cells , 2014, Arquivos brasileiros de cardiologia.

[27]  Chaodong Wu,et al.  Ginsenoside Rb1 Prevents H2O2-Induced HUVEC Senescence by Stimulating Sirtuin-1 Pathway , 2014, PloS one.

[28]  Qing Zhou,et al.  MicroRNA-29b promotes high-fat diet-stimulated endothelial permeability and apoptosis in apoE knock-out mice by down-regulating MT1 expression. , 2014, International journal of cardiology.

[29]  Qinghua Li,et al.  miR-125b-1-3p inhibits trophoblast cell invasion by targeting sphingosine-1-phosphate receptor 1 in preeclampsia. , 2014, Biochemical and biophysical research communications.

[30]  A. Procopio,et al.  MitomiRs in human inflamm-aging: A hypothesis involving miR-181a, miR-34a and miR-146a , 2014, Experimental Gerontology.

[31]  D. Karolina,et al.  Expression Profiling of RNA Transcripts during Neuronal Maturation and Ischemic Injury , 2014, PloS one.

[32]  E. Gratton,et al.  Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer , 2014, The EMBO journal.

[33]  Nader Sheibani,et al.  Diabetes and Retinal Vascular Dysfunction , 2014, Journal of ophthalmic & vision research.

[34]  Xia Zhao,et al.  MicroRNA-26a regulates glucose metabolism by direct targeting PDHX in colorectal cancer cells , 2014, BMC Cancer.

[35]  Zhongxin Lu,et al.  Huaier suppresses proliferation and induces apoptosis in human pulmonary cancer cells via upregulation of miR‐26b‐5p , 2014, FEBS letters.

[36]  Shitong Li,et al.  Estrogen Rapidly Enhances Incisional Pain of Ovariectomized Rats Primarily through the G Protein-Coupled Estrogen Receptor , 2014, International journal of molecular sciences.

[37]  D. Hua,et al.  MiR-20b, -21, and -130b inhibit PTEN expression resulting in B7-H1 over-expression in advanced colorectal cancer. , 2014, Human immunology.

[38]  Bin Chen,et al.  Autophagy Protects Against Senescence and Apoptosis via the RAS-Mitochondria in High-Glucose-Induced Endothelial Cells , 2014, Cellular Physiology and Biochemistry.

[39]  H. Ding,et al.  Differential role of microRNAs miR‐221/222 and miR‐103/107 in type 2 diabetes and effects of metformin (851.2) , 2014 .

[40]  C. Ruhrberg,et al.  Neuropilin 1 (NRP1) hypomorphism combined with defective VEGF-A binding reveals novel roles for NRP1 in developmental and pathological angiogenesis , 2014, Development.

[41]  K. Zeng,et al.  Advanced Glycation End Products Activate the miRNA/RhoA/ROCK2 Pathway in Endothelial Cells , 2014, Microcirculation.

[42]  J. Sundquist,et al.  Determination of 14 Circulating microRNAs in Swedes and Iraqis with and without Diabetes Mellitus Type 2 , 2014, PloS one.

[43]  Sophie Rome,et al.  Profiling of Circulating MicroRNAs Reveals Common MicroRNAs Linked to Type 2 Diabetes That Change With Insulin Sensitization , 2014, Diabetes Care.

[44]  C. Sena,et al.  Endothelial dysfunction - a major mediator of diabetic vascular disease. , 2013, Biochimica et biophysica acta.

[45]  M. Ivan,et al.  miR-16 and miR-26a target checkpoint kinases Wee1 and Chk1 in response to p53 activation by genotoxic stress , 2013, Cell Death and Disease.

[46]  E. Donadi,et al.  Identifying common and specific microRNAs expressed in peripheral blood mononuclear cell of type 1, type 2, and gestational diabetes mellitus patients , 2013, BMC Research Notes.

[47]  M. Brattain,et al.  MicroRNA-192 Suppresses Liver Metastasis of Colon Cancer , 2013, Oncogene.

[48]  Y. Wang,et al.  Melatonin ameliorates vascular endothelial dysfunction, inflammation, and atherosclerosis by suppressing the TLR4/NF‐κB system in high‐fat‐fed rabbits , 2013, Journal of pineal research.

[49]  K. Ha,et al.  C-Peptide Activates AMPKα and Prevents ROS-Mediated Mitochondrial Fission and Endothelial Apoptosis in Diabetes , 2013, Diabetes.

[50]  Anna M. Krichevsky,et al.  MiR-26b, Upregulated in Alzheimer's Disease, Activates Cell Cycle Entry, Tau-Phosphorylation, and Apoptosis in Postmitotic Neurons , 2013, The Journal of Neuroscience.

[51]  Y. Niu,et al.  MiR-130b Is a Prognostic Marker and Inhibits Cell Proliferation and Invasion in Pancreatic Cancer through Targeting STAT3 , 2013, PloS one.

[52]  K. Porter,et al.  Cellular and molecular mechanisms of endothelial dysfunction in diabetes , 2013, Diabetes & vascular disease research.

[53]  Y. Suárez,et al.  MicroRNAs as pharmacological targets in endothelial cell function and dysfunction. , 2013, Pharmacological research.

[54]  Yi Liu,et al.  miR-29b and miR-29c Are Involved in Toll-Like Receptor Control of Glucocorticoid-Induced Apoptosis in Human Plasmacytoid Dendritic Cells , 2013, PloS one.

[55]  Hailin Tang,et al.  MiR-26a Inhibits Proliferation and Migration of Breast Cancer through Repression of MCL-1 , 2013, PloS one.

[56]  C. Chung,et al.  Peptide-mediated intracellular delivery of miRNA-29b for osteogenic stem cell differentiation. , 2013, Biomaterials.

[57]  Jing Wang,et al.  WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013 , 2013, Nucleic Acids Res..

[58]  Anton J. Enright,et al.  miR-221 affects multiple cancer pathways by modulating the level of hundreds messenger RNAs , 2013, Front. Genet..

[59]  J. Pollard,et al.  NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. , 2013, Blood.

[60]  Dan Li,et al.  Increased expression of microRNA-221 inhibits PAK1 in endothelial progenitor cells and impairs its function via c-Raf/MEK/ERK pathway. , 2013, Biochemical and biophysical research communications.

[61]  K. Copeland,et al.  Current Treatment Options for Type 2 Diabetes Mellitus in Youth: Today’s Realities and Lessons from the TODAY Study , 2013, Current Diabetes Reports.

[62]  Yosuke Okada,et al.  Relationship between fluctuations in glucose levels measured by continuous glucose monitoring and vascular endothelial dysfunction in type 2 diabetes mellitus , 2013, Cardiovascular Diabetology.

[63]  K. Tan,et al.  Blood microRNAs in Low or No Risk Ischemic Stroke Patients , 2013, International journal of molecular sciences.

[64]  V. Scaria,et al.  Reverse Genetics Screen in Zebrafish Identifies a Role of miR-142a-3p in Vascular Development and Integrity , 2012, PloS one.

[65]  F. Camargo,et al.  YAP mediates crosstalk between the Hippo and PI(3)K–TOR pathways by suppressing PTEN via miR-29 , 2012, Nature Cell Biology.

[66]  D. Dykxhoorn,et al.  MicroRNA-10A* and MicroRNA-21 Modulate Endothelial Progenitor Cell Senescence Via Suppressing High-Mobility Group A2 , 2012, Circulation research.

[67]  D. Karolina,et al.  Circulating miRNA profiles in patients with metabolic syndrome. , 2012, The Journal of clinical endocrinology and metabolism.

[68]  M. Yamakuchi MicroRNAs in Vascular Biology , 2012, International journal of vascular medicine.

[69]  A. Fusco,et al.  Downregulation of HMGA-targeting microRNAs has a critical role in human pituitary tumorigenesis , 2012, Oncogene.

[70]  Amir Lerman,et al.  The Assessment of Endothelial Function: From Research Into Clinical Practice , 2012, Circulation.

[71]  Onju Ham,et al.  Up-regulation of miR-26a promotes apoptosis of hypoxic rat neonatal cardiomyocytes by repressing GSK-3β protein expression. , 2012, Biochemical and biophysical research communications.

[72]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[73]  Karthikeyan Chandrasekaran,et al.  Pro-domain in precursor nerve growth factor mediates cell death , 2012, Neurochemistry International.

[74]  Martin Reczko,et al.  DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways , 2012, Nucleic Acids Res..

[75]  T. Münzel,et al.  Hyperglycemia and oxidative stress in cultured endothelial cells--a comparison of primary endothelial cells with an immortalized endothelial cell line. , 2012, Journal of diabetes and its complications.

[76]  J. Bertram,et al.  Role of microRNAs in kidney homeostasis and disease. , 2012, Kidney international.

[77]  Wei-Kang Wu,et al.  Ginsenoside Rb1 Reverses H2O2-induced Senescence in Human Umbilical Endothelial Cells: Involvement of eNOS Pathway , 2012, Journal of cardiovascular pharmacology.

[78]  Hui Zhang,et al.  microRNA-320a inhibits tumor invasion by targeting neuropilin 1 and is associated with liver metastasis in colorectal cancer. , 2012, Oncology reports.

[79]  Manuel Mayr,et al.  MicroRNAs in vascular and metabolic disease. , 2012, Circulation research.

[80]  Lei Yuan,et al.  ETS-related Gene (ERG) Controls Endothelial Cell Permeability via Transcriptional Regulation of the Claudin 5 (CLDN5) Gene* , 2012, The Journal of Biological Chemistry.

[81]  F. Gonzalez,et al.  Disruption of Endothelial Peroxisome Proliferator-Activated Receptor &ggr; Accelerates Diet-Induced Atherogenesis in LDL Receptor-Null Mice , 2012, Arteriosclerosis, thrombosis, and vascular biology.

[82]  Hui Zhang,et al.  [Corrigendum] MicroRNA-320a inhibits tumor invasion by targeting neuropilin 1 and is associated with liver metastasis in colorectal cancer. , 2011, Oncology reports.

[83]  O. Kent,et al.  MicroRNA profiling of diverse endothelial cell types , 2011, BMC Medical Genomics.

[84]  U. Huynh-Do,et al.  The Role of PTEN in Tumor Angiogenesis , 2011, Journal of oncology.

[85]  Arunmozhiarasi Armugam,et al.  MicroRNA 144 Impairs Insulin Signaling by Inhibiting the Expression of Insulin Receptor Substrate 1 in Type 2 Diabetes Mellitus , 2011, PloS one.

[86]  Jianxing He,et al.  MicroRNA-192 targeting retinoblastoma 1 inhibits cell proliferation and induces cell apoptosis in lung cancer cells , 2011, Nucleic acids research.

[87]  Zhen Bian,et al.  miR-29b regulates migration of human breast cancer cells , 2011, Molecular and Cellular Biochemistry.

[88]  A. Schmidt,et al.  Human Vascular Endothelial Cells: A Model System for Studying Vascular Inflammation in Diabetes and Atherosclerosis , 2011, Current diabetes reports.

[89]  P. Kantharidis,et al.  TGF-β Regulates miR-206 and miR-29 to Control Myogenic Differentiation through Regulation of HDAC4 , 2011, The Journal of Biological Chemistry.

[90]  Ming Liu,et al.  Role of MicroRNA-26b in Glioma Development and Its Mediated Regulation on EphA2 , 2011, PloS one.

[91]  Emmette R. Hutchison,et al.  miR-130 Suppresses Adipogenesis by Inhibiting Peroxisome Proliferator-Activated Receptor γ Expression , 2010, Molecular and Cellular Biology.

[92]  D. Popov Endothelial cell dysfunction in hyperglycemia: Phenotypic change, intracellular signaling modification, ultrastructural alteration, and potential clinical outcomes , 2010 .

[93]  M. Mayr,et al.  Plasma MicroRNA Profiling Reveals Loss of Endothelial MiR-126 and Other MicroRNAs in Type 2 Diabetes , 2010, Circulation research.

[94]  Rodica Pop-Busui,et al.  Effect of intensive treatment of hyperglycaemia on microvascular outcomes in type 2 diabetes: an analysis of the ACCORD randomised trial , 2010, The Lancet.

[95]  Jianfeng Xu,et al.  MicroRNA-101 negatively regulates Ezh2 and its expression is modulated by androgen receptor and HIF-1α/HIF-1β , 2010, Molecular Cancer.

[96]  Diederick E. Grobbee,et al.  The global burden of diabetes and its complications: an emerging pandemic , 2010, European journal of cardiovascular prevention and rehabilitation : official journal of the European Society of Cardiology, Working Groups on Epidemiology & Prevention and Cardiac Rehabilitation and Exercise Physiology.

[97]  N. Hamburg,et al.  Endothelial dysfunction in diabetes mellitus: Molecular mechanisms and clinical implications , 2010, Reviews in Endocrine and Metabolic Disorders.

[98]  A. Malik,et al.  Regulation of endothelial permeability via paracellular and transcellular transport pathways. , 2010, Annual review of physiology.

[99]  Wei Huang,et al.  Integrative genome analysis reveals an oncomir/oncogene cluster regulating glioblastoma survivorship , 2010, Proceedings of the National Academy of Sciences.

[100]  Hansjuerg Alder,et al.  miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. , 2009, Cancer cell.

[101]  T. Carpenter,et al.  EphA2 receptor mediates increased vascular permeability in lung injury due to viral infection and hypoxia. , 2009, American journal of physiology. Lung cellular and molecular physiology.

[102]  J. Yun,et al.  Effects of MicroRNA‐29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma , 2009, Hepatology.

[103]  H. Makino,et al.  Endothelial barrier protection by FTY720 under hyperglycemic condition: involvement of focal adhesion kinase, small GTPases, and adherens junction proteins. , 2009, American journal of physiology. Cell physiology.

[104]  Y. Wang,et al.  Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells , 2009, Oncogene.

[105]  Qian Chen,et al.  HDAC4 Represses Vascular Endothelial Growth Factor Expression in Chondrosarcoma by Modulating RUNX2 Activity* , 2009, The Journal of Biological Chemistry.

[106]  Yao‐Hua Song,et al.  MicroRNA-221 regulates high glucose-induced endothelial dysfunction. , 2009, Biochemical and biophysical research communications.

[107]  Katrin J. Svensson,et al.  The polyamines regulate endothelial cell survival during hypoxic stress through PI3K/AKT and MCL-1. , 2009, Biochemical and biophysical research communications.

[108]  Le Yu,et al.  The role of microRNA expression pattern in human intrahepatic cholangiocarcinoma. , 2009, Journal of hepatology.

[109]  Aimee L Jackson,et al.  Coordinated regulation of cell cycle transcripts by p53-Inducible microRNAs, miR-192 and miR-215. , 2008, Cancer research.

[110]  Wenbin Ye,et al.  The Effect of Central Loops in miRNA:MRE Duplexes on the Efficiency of miRNA-Mediated Gene Regulation , 2008, PloS one.

[111]  A. Armugam,et al.  MicroRNA Expression in the Blood and Brain of Rats Subjected to Transient Focal Ischemia by Middle Cerebral Artery Occlusion , 2008, Stroke.

[112]  Y. Yanagi Role of Peroxisome Proliferator Activator Receptor γ on Blood Retinal Barrier Breakdown , 2014 .

[113]  G. Gores,et al.  mir-29 regulates Mcl-1 protein expression and apoptosis , 2007, Oncogene.

[114]  Chung-Hsien Liu,et al.  Ellagic acid inhibits IL-1beta-induced cell adhesion molecule expression in human umbilical vein endothelial cells. , 2007, The British journal of nutrition.

[115]  B. Zinman,et al.  Impaired Fasting Glucose and Impaired Glucose Tolerance , 2007, Diabetes Care.

[116]  B. Wojciak-Stothard,et al.  Rac1 and RhoA as regulators of endothelial phenotype and barrier function in hypoxia-induced neonatal pulmonary hypertension. , 2006, American journal of physiology. Lung cellular and molecular physiology.

[117]  Janet Rossant,et al.  Endothelial cells and VEGF in vascular development , 2005, Nature.

[118]  J. Miyazaki,et al.  The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. , 2005, Genes & development.

[119]  J. Manson,et al.  Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus. , 2004, JAMA.

[120]  Elisabetta Dejana,et al.  Endothelial cell–cell junctions: happy together , 2004, Nature Reviews Molecular Cell Biology.

[121]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[122]  David Botstein,et al.  Endothelial cell diversity revealed by global expression profiling , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[123]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[124]  Doron Aronson,et al.  How hyperglycemia promotes atherosclerosis: molecular mechanisms , 2002, Cardiovascular diabetology.

[125]  G. Molostvov,et al.  Modulation of Bcl-2 Family Proteins in Primary Endothelial Cells during Apoptosis , 2002, Pathophysiology of Haemostasis and Thrombosis.

[126]  A. Verin,et al.  Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. , 2001, The Journal of clinical investigation.

[127]  Shing-Hwa Liu,et al.  High Glucose–Induced Apoptosis in Human Endothelial Cells Is Mediated by Sequential Activations of c-Jun NH2-Terminal Kinase and Caspase-3 , 2000 .

[128]  M. Laakso Hyperglycemia as a risk factor for cardiovascular disease in type 2 diabetes. , 1999, Primary care.

[129]  C. F. Bennett,et al.  The Role of Antiapoptotic Bcl-2 Family Members in Endothelial Apoptosis Elucidated with Antisense Oligonucleotides* , 1999, The Journal of Biological Chemistry.

[130]  M. Corada,et al.  Endothelial cell‐to‐cell junctions , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[131]  J. Revel,et al.  Endothelial cell junctions , 1975, The Journal of cell biology.

[132]  Y. Joo,et al.  Myeloid cell leukemia-1 is associated with tumor progression by inhibiting apoptosis and enhancing angiogenesis in colorectal cancer. , 2015, American journal of cancer research.

[133]  P. Kantharidis,et al.  microRNA in the development of diabetic complications. , 2014, Clinical science.

[134]  M. Christine,et al.  DIABETES AND RETINAL VASCULAR DYSFUNCTION (REVIEW ARTICLE) , 2014 .

[135]  Wei Shen,et al.  Altered microRNA expression profiles in retinas with diabetic retinopathy. , 2012, Ophthalmic research.

[136]  Bo Zhang,et al.  Pathologically decreased miR-26a antagonizes apoptosis and facilitates carcinogenesis by targeting MTDH and EZH2 in breast cancer. , 2011, Carcinogenesis.

[137]  J. Leahy Impaired Fasting Glucose and Impaired Glucose Tolerance: Implications for care , 2008 .

[138]  P. D’Amore,et al.  Arterial versus venous endothelial cells , 2008, Cell and Tissue Research.

[139]  D. Carling,et al.  Hyperglycemia-induced apoptosis in human umbilical vein endothelial cells: inhibition by the AMP-activated protein kinase activation. , 2002, Diabetes.

[140]  Shing-Hwa Liu,et al.  High glucose-induced apoptosis in human endothelial cells is mediated by sequential activations of c-Jun NH(2)-terminal kinase and caspase-3. , 2000, Circulation.

[141]  H. Dvorak,et al.  Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. , 1999, Current topics in microbiology and immunology.

[142]  Hiroyuki Ogata,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 1999, Nucleic Acids Res..

[143]  H. Patel,et al.  O R I G I N a L I N V E S T I G a T I O N Open Access Hyperglycemia Induces Differential Change in Oxidative Stress at Gene Expression and Functional Levels in Huvec and Hmvec , 2022 .