Increased Extracellular Matrix Protein Production in Chronic Diabetic Complications: Implications of Non-Coding RNAs
Abstract
:1. Introduction
2. ECM—The Footprint of Chronic Diabetic Complications
3. Cellular Phenotypic Changes Causing Increased ECM Protein Productions in Chronic Diabetic Complications
4. Hyperglycemia and Gene Transcription
4.1. Transcription Factors and Co-Activators
4.1.1. NF-κB and AP-1
4.1.2. p300 and Histone Acetylation
4.2. Non-Coding RNAs
4.2.1. Non-Coding RNAs
4.2.2. Long Non-Coding RNAs (lncRNAs)
5. Role of miRNAs in Chronic Diabetic Complications in Various Organs
5.1. miRNAs in Diabetic Nephropathy (DN)
5.2. miRNAs in Diabetic Cardiomyopathy (DCM)
5.3. miRNAs in Diabetic Retinopathy (DR)
6. Role of LncRNAs in Chronic Diabetic Complications in Various Organs
6.1. LncRNAs in Diabetic Nephropathy (DN)
6.2. LncRNAs in Diabetic Cardiomyopathy (DCM) and Other Cardiovascular Complications
6.3. lncRNAs in Diabetic Retinopathy (DR)
7. Relationship of lncRNAs, miRNAs, and Other Epigenetic Mechanisms on Causing Increased ECM Protein Production in Diabetes
7.1. Histone Methylation: PRC2 and lncRNAs
8. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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miRNA | Cell/Tissue Type(s) | Reported Function(s) | Disease Model(s) |
---|---|---|---|
miR-192 * | • Mouse mesangial cells • Human proximal tubule cells and kidneys • Rat tubular epithelial cells • Human podocytes | • Elevated expressions associated with increased Col1a2 expressions; targets SIP1 [108] • Loss of miR-192 expression is associated with increased fibrosis and decreased estimated GFR [111] • Decreased in the diabetic kidney, targets ZEB2, and does not affect extracellular matrix (ECM) protein expressions [112] • Increased in high glucose and diabetic conditions [109,110,142] • Can regulate other transcription factors and miRNAs [109,110] | • DN [108,109,110,111,112,142] |
miR-215 | • Proximal tubular cells • Rat mesangial cells • Human podocytes | • Decreased in the diabetic kidney • Ectopic expression of miR-215 increases E-cadherin levels by repressing ZEB2 translation | • DN [112] |
miR-377 | • Human and mouse mesangial cells • Mice kidney tissues | • Up-regulated in hyperglycemic and diabetic conditions • Can indirectly lead to increased fibronectin protein production | • DN [113] |
miR-21 | • Rat mesangial cells • Mice kidney tissues • Rat tubular epithelial cells | • Expression is increased in DN and can enhance the production of high glucose-induced fibrotic and inflammatory markers | • DN [125] |
miR-29* | • Human podocytes • Mouse mesangial cells • Mice kidney tissues • Mouse embryonic fibroblasts and tubular epithelial cells • Mice kidney glomeruli, endothelial cells, and podocytes | • Low levels in early DN and fibrosis and can target collagens I and IV [116] • Lost with progressive renal fibrosis, can reduce collagens I and III, and interact with Smad3 [117] • miR-29c is increased in DN, induces cell apoptosis, and increases ECM protein accumulation [118] | • DN [116,117,118] |
miR-let-7b | • Rat proximal tubular epithelial cells • Mice kidney tissues | • Is reduced in both diabetic and non-diabetic renal fibrosis and can regulate the expression of several ECM genes | • DN [114] |
miR-93 | • Renal microvascular endothelial cells • Mouse podocytes • Mice kidney tissues | • High glucose and diabetic conditions decrease miR-93 expressions • Can target VEGF and negatively regulate it | • DN [115] |
miR-200 * | • Human retinal endothelial cells • Mice and rat retinal tissues • Mice kidney tissues • Mouse mesangial cells • Mouse heart endothelial cells, vascular smooth muscle cells, and cardiac tissues | • miR-200b is reduced under hyperglycemic and diabetic conditions [40,179]; can target VEGF [80,179] • Inhibition of miR-200a-3p can provoke renal fibrosis in DN [121] • Increased levels of miR-200b/c detected in diabetic mouse glomeruli; involved in glomerular mesangial hypertrophy [110,120] • miR-200b overexpression shown to prevent diabetes-induced changes in heart structure and function and reduce EndMT markers [134] • miR-200b shown to have a protective role in the diabetic retina [136,137] • Diabetic VSMCs exhibit increased miR-200 levels, which can contribute to inflammation [129] | • DR [40,80,136,137] • DN [110,120,121,179] • DCM [129,134] |
miR-146a | • Rat and mice retinal tissues • Human umbilical vein endothelial cells • Mice kidney tissues | • miR-146a was shown to be reduced in diabetic tissues; miR-146a mimics can decrease FN expression [55] • miR-146a knockout exacerbates diabetes-induced inflammation and fibrosis in mice kidney tissues [126] • miR-146a mimics can prevent the increased expressions of ECM proteins and inflammatory markers in diabetic tissues [124] | • DR [55] • DCM [55] • DN [124,126] |
miR-1207-5b | • Human renal proximal tubule epithelial cells, podocytes, and mesangial cells | • Hyperglycemia shown to increase miR-1207-5b levels, which contributes to ECM accumulation in the kidney • Knockdown can decrease levels of TGF-β1, FN1, and PAI-1 | • DN [122] |
miR-302d | • Mice kidney tissues • Human mesangial cells, proximal tubular epithelial cells, and HEK-293T | • Capable of attenuating TGF-β-induced fibronectin, thrombospondin, vimentin, and N-cadherin expressions • Can regulate TGF-β -induced EMT | • DN [127] |
miR-216a | • Primary mouse mesangial cells (MMCs) | • Upregulated by TGF-β in MMCs • Also increased in isolated renal glomeruli from type 1 and type 2 diabetic mice • Inhibiting miR-216a in MMCs reverses the effects of TGF-β on Pten and P-Akt levels | • DN [145] |
miR-217 | • Primary mouse mesangial cells | • Upregulated by TGF-β in MMCs • Also increased in diabetic mice kidneys • Along with miR-216a, miR-217 mimics can induce hypertrophy in MMCs | • DN [145] |
miR-133a | • Mice cardiac tissues • Neonatal rat myocytes | • Downregulated in diabetic cardiomyopathy [131,132,133] • Mediates glucose-induced cardiomyocytes hypertrophy [131,132,133] • Cardiac-specific overexpression of miR-133a can significantly decrease cardiac fibrosis [133] | • DCM [131,132,133] |
miR-155 | • Mouse cardiac fibroblasts • Mouse bone marrow progenitor cells (BMPCs) | • Increased expression of miR-155 in MI mice • Transplantation of BMPCs in MI mice can decrease miR-155 expressions and in association, show decreased cardiac fibrosis expressions | • DCM [130] |
lncRNA | Cell/Tissue Type(s) | Reported Function(s) | Disease Model |
---|---|---|---|
PVT1 | • Humanmesangial cells | • Upregulated by glucose treatment in mesangial cells • PVT1 knockdown can significantly reduce the levels of major ECM proteins (FN and COL4A1) | • DN [146] |
MALAT1 | • Mice kidney tissues • Mouse podocytes • Mice and rat cardiac tissues • HRECs • Mice retinal tissues • RF/6A cells • Aqueous and vitreous humors | • MALAT1 levels are increased in the kidney cortices of STZ-induced diabetic mice [147] • MALAT1 regulates diabetes-induced inflammatory gene expressions in the heart and kidneys [148,149] • MALAT1 is upregulated in HG-treated RF/6A cells, aqueous humor samples and in fibrovascular membranes of diabetic patients [167] • MALAT1 has a pathogenetic role in the heart [165,166] • MALAT1 can regulate inflammation through its association with other epigenetic mechanisms in DR [168] | • DN [147,148,149] • DR [167,168] • DCM [148,165,166] |
GM4419 | • Mouse mesangial cells (MMCs) | • Upregulated in MMCs following high glucose culture • Knockdown of GM4419 inhibits the glucose-induced expressions of pro-inflammatory cytokines and renal fibrosis markers • GM4419 can regulate NF-κB signalling | • DN [150] |
GM5524 | • Mice kidney tissues • Mouse podocytes | • Expressions are significantly upregulated in DN • May regulate podocytes apoptosis and autophagy during DN | • DN [151] |
GM15645 | • Mice kidney tissues • Mouse podocytes | • Downregulated in DN • Similar to GM5524, GM15645 may also regulate podocytes apoptosis and autophagy during DN | • DN [151] |
ANRIL | • Human retinal endothelial cells (HRECs) • Mice retinal tissues • Mice kidney and cardiac tissues | • High glucose and diabetic conditions upregulate ANRIL expressions [81,154] • ANRIL can regulate VEGF and ECM expressions through several epigenetic mechanisms (i.e., p300 and PRC2) [81,154] | • DN [154] • DR [81] • DCM [154] |
NR_033515 | • Human blood • HEK293-T • MMCs | • Significantly increased in the serum of DN patients • Overexpression of NR_033515 can accelerate TGF-β1-induced EMT • Promotes cell proliferation and fibrogenesis in high glucose conditions | • DN [152] |
Erbb4-IR | • Mice kidney tissues • Mouse embryonic fibroblasts • MMCs • Mouse tubular epithelial cells | • Significantly upregulated in the kidneys of diabetic mice • A Smad3-dependent lncRNA that promotes renal fibrosis in type 2 DN • Can negatively regulate miR-29b • Kidney-specific silencing of Erbb4-IR shown to prevent renal injury in diabetic mice | • DN [153] |
ASncmtRNA-2 | • Mice kidney tissues • Human mesangial cells | • Expressions are significantly heightened in diabetic mice kidneys and mesangial cells treated with high glucose • May promote glomerular fibrosis in DN | • DN [155] |
Tug1 | • Mice kidney tissues • MMCs | • Suppresses the proliferation of mesangial cells and decreases the expression of ECM-associated proteins in DN • Functions as an endogenous sponge of miR-377, which directly targets PPARγ | • DN [156] |
NONMMUT022554 | • Mice cardiac tissues | • Upregulated in cardiac fibrosis and positively correlated with 6 upregulated genes involved in ECM–receptor interactions and the PI3K–Akt signalling pathway | • Cardiac fibrosis/MI [160] |
PFL (NONMMUT022555) | • Mice cardiac tissues • Mice cardiac fibroblasts and cardiomyocytes | • Upregulated in the hearts of MI mice • Knockdown of PFL can attenuate cardiac interstitial fibrosis and improve cardiac function • Overexpression of PFL promotes proliferation, fibroblast-myofibroblast transition, and mice cardiac fibroblasts • Acts as a competitive endogenous RNA of let-7d | • Cardiac fibrosis/MI [161] |
MIAT | • Mice cardiac tissues • Mouse cardiac fibroblasts | • Significantly upregulated in the infarcted myocardium of mice • Knockdown of MIAT reduces cardiac fibrosis and improves cardiac function • Functions as a sponge of miR-24 in cardiac fibroblasts | • Cardiac fibrosis/MI [162] |
Wisper | • Mice and human cardiac tissues • Mouse cardiac fibroblasts and cardiomyocytes • Human fibroblasts | • Expression of Wisper is strongly correlated with cardiac fibrosis in both animal and human heart tissues • Wisper knockdown affects cardiac fibroblast survival, migration, and proliferation • In vivo depletion of Wisper inhibits cardiac fibrosis and improves function | • Cardiac fibrosis/MI [163] |
Meg3 | • Mice cardiac tissues • Mouse cardiac fibroblasts | • Strongly expressed in adult cardiac fibroblasts • Regulates the production of MMP-2 in vitro • In vivo inhibition of Meg3 after transverse aortic constriction decreases cardiac fibrosis and improves diastolic function | • Cardiac fibrosis [164] |
H19 | • HRECs • Mice retinal tissues • Human vitreous humors | • Downregulated in HG-treated endothelial cells and in the vitreous humors of diabetic patients • Capable of regulating EndMT in vitro and in vivo | • DR [170] |
Lnc-MGC | • Mice kidney tissues • Mouse and human mesangial cells • Human renal biopsies | • Elevated levels of lnc-MGC present in the kidneys during diabetes • Host to a megacluster of miRNAs • CHOP (an ER-stress transcription factor) regulates lnc-MGC expressions • Inhibition of lnc-MGC results in reduced cluster miRNAs, ECM accumulation, and glomerular hypertrophy | • DN [158] |
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Biswas, S.; Chakrabarti, S. Increased Extracellular Matrix Protein Production in Chronic Diabetic Complications: Implications of Non-Coding RNAs. Non-Coding RNA 2019, 5, 30. https://doi.org/10.3390/ncrna5010030
Biswas S, Chakrabarti S. Increased Extracellular Matrix Protein Production in Chronic Diabetic Complications: Implications of Non-Coding RNAs. Non-Coding RNA. 2019; 5(1):30. https://doi.org/10.3390/ncrna5010030
Chicago/Turabian StyleBiswas, Saumik, and Subrata Chakrabarti. 2019. "Increased Extracellular Matrix Protein Production in Chronic Diabetic Complications: Implications of Non-Coding RNAs" Non-Coding RNA 5, no. 1: 30. https://doi.org/10.3390/ncrna5010030