Advertisement

Circular RNAs in β-cell function and type 2 diabetes-related complications: a potential diagnostic and therapeutic approach

  • Hassan Ghasemi
  • Zolfaghar Sabati
  • Hamid Ghaedi
  • Zaker Salehi
  • Behnam AlipoorEmail author
Review
  • 40 Downloads

Abstract

Recent investigations have indicated that altered expression of non-coding RNAs (ncRNAs) could be associated with human diseases such as type 2 diabetes (T2D). Circular RNAs (circRNAs) are a new discovered class of ncRNAs with unique structural characteristics that involved in several molecular and cellular functions. Exploring of the circulating circRNAs as a reliable non-invasive biomarker for monitoring and diagnosing of human diseases has grown significantly. However, the molecular functions and clinical relevance of circRNAs are not yet well clarified in T2D. Accordingly, in this review, the involvement of circRNAs in the β-cell function and T2D-related complications is highlighted. The study also shed light on the possibility of using circRNAs as a biomarker for T2D diagnosis.

Keywords

Non-coding RNAs Circular RNAs Complications Biomarkers Type 2 diabetes 

Notes

Acknowledgements

This work was financially supported by a grant (98U-567) from the Deputy of Research, Abadan Faculty of Medical Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

References

  1. 1.
    Zarrinkalam E et al (2018) Resistance training and hawthorn extract ameliorate cognitive deficits in streptozotocin-induced diabetic rats. Biomed Pharmacother 97:503–510CrossRefPubMedGoogle Scholar
  2. 2.
    Ogurtsova K et al (2017) IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50CrossRefPubMedGoogle Scholar
  3. 3.
    Ramezankhani A et al (2018) Diabetes mellitus: findings from 20 years of the Tehran lipid and glucose study. Int J Endocrinol Metab 16(4 Suppl):e84784PubMedPubMedCentralGoogle Scholar
  4. 4.
    Kumar V et al (2005) Robbins and Cotran pathologic basis of disease. Elsevier Saunders, PhiladelphiaGoogle Scholar
  5. 5.
    Wild S et al (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27(5):1047–1053CrossRefPubMedGoogle Scholar
  6. 6.
    Alberti KGMM, Zimmet PF (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus. Provisional report of a WHO consultation. Diabetes Med 15(7):539–553CrossRefGoogle Scholar
  7. 7.
    Baynes H (2015) Classification, pathophysiology, diagnosis and management of diabetes mellitus. J Diabetes Metab 6(5):1–9Google Scholar
  8. 8.
    World Health Organization (2014) The top 10 causes of death. World Health Organization, GenevaGoogle Scholar
  9. 9.
    Murea M, Ma L, Freedman BI (2012) Genetic and environmental factors associated with type 2 diabetes and diabetic vascular complications. Rev Diabetic Stud: RDS 9(1):6CrossRefPubMedGoogle Scholar
  10. 10.
    Palazzo AF, Lee ES (2015) Non-coding RNA: what is functional and what is junk? Front Genet 6:2CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Adams BD et al (2017) Targeting noncoding RNAs in disease. J Clin Investig 127(3):761–771CrossRefPubMedGoogle Scholar
  12. 12.
    Matsui M, Corey DR (2017) Non-coding RNAs as drug targets. Nat Rev Drug Discov 16(3):167CrossRefPubMedGoogle Scholar
  13. 13.
    Amin N, McGrath A, Chen YPP (2019) Evaluation of deep learning in non-coding RNA classification. Nat Mach Intell 1(5):246CrossRefGoogle Scholar
  14. 14.
    Dahariya S, Paddibhatla I, Kumar S, Raghuwanshi S, Pallepati A, Gutti RK (2019) Long non-coding RNA: classification, biogenesis and functions in blood cells. Mol Immunol 112:82–92CrossRefPubMedGoogle Scholar
  15. 15.
    Alipoor B et al (2018) The rs2910164 variant is associated with reduced miR-146a expression but not cytokine levels in patients with type 2 diabetes. J Endocrinol Invest 41(5):557–566CrossRefPubMedGoogle Scholar
  16. 16.
    Alipoor B et al (2017) Association of miR-146a expression and type 2 diabetes mellitus: a meta-analysis. Int J Mol Cell Med 6(3):156PubMedPubMedCentralGoogle Scholar
  17. 17.
    Ghaedi H et al (2019) Co-expression profiling of plasma miRNAs and long noncoding RNAs in gastric cancer patients. Gene 687:135–142CrossRefPubMedGoogle Scholar
  18. 18.
    Zare A et al (2019) Decreased miR-155-5p, miR-15a, and miR-186 expression in gastric cancer is associated with advanced tumor grade and metastasis. Iran Biomed JGoogle Scholar
  19. 19.
    Qu S et al (2015) Circular RNA: a new star of noncoding RNAs. Cancer Lett 365(2):141–148CrossRefGoogle Scholar
  20. 20.
    Sanger HL et al (1976) Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci 73(11):3852–3856CrossRefPubMedGoogle Scholar
  21. 21.
    Kos A et al (1986) The hepatitis delta (δ) virus possesses a circular RNA. Nature 323(6088):558CrossRefPubMedGoogle Scholar
  22. 22.
    Nigro JM et al (1991) Scrambled exons. Cell 64(3):607–613CrossRefGoogle Scholar
  23. 23.
    Chen L-L (2016) The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Biol 17(4):205CrossRefGoogle Scholar
  24. 24.
    Salzman J (2016) Circular RNA expression: its potential regulation and function. Trends Genet 32(5):309–316CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Burset M, Seledtsov I, Solovyev V (2000) Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res 28(21):4364–4375CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Suñé-Pou M et al (2017) Targeting splicing in the treatment of human disease. Genes 8(3):87CrossRefPubMedCentralGoogle Scholar
  27. 27.
    Memczak S et al (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333CrossRefGoogle Scholar
  28. 28.
    Zhang Y et al (2013) Circular intronic long noncoding RNAs. Mol Cell 51(6):792–806CrossRefPubMedGoogle Scholar
  29. 29.
    Wang Y, Wang Z (2015) Efficient backsplicing produces translatable circular mRNAs. RNA 21(2):172–179CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Starke S et al (2015) Exon circularization requires canonical splice signals. Cell Rep 10(1):103–111CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Jeck WR et al (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19(2):141–157CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Souii A, M’hadheb-Gharbi MB, Gharbi J (2015) Cellular proteins act as bridge between 5′ and 3′ ends of the Coxsackievirus B3 mediating genome circularization during RNA translation. Curr Microbiol 71(3):387–395CrossRefPubMedGoogle Scholar
  33. 33.
    Ivanov A et al (2015) Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep 10(2):170–177CrossRefPubMedGoogle Scholar
  34. 34.
    Yang Z et al (2017) Circular RNAs: regulators of cancer-related signaling pathways and potential diagnostic biomarkers for human cancers. Theranostics 7(12):3106CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Salzman J et al (2012) Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 7(2):e30733CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Liang D, Wilusz JE (2014) Short intronic repeat sequences facilitate circular RNA production. Genes Dev 28(20):2233–2247CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Ashwal-Fluss R et al (2014) circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56(1):55–66CrossRefGoogle Scholar
  38. 38.
    Du WW et al (2017) Identifying and characterizing circRNA-protein interaction. Theranostics 7(17):4183CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Li Z et al (2015) Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 22(3):256CrossRefPubMedGoogle Scholar
  40. 40.
    Salzman J et al (2013) Cell-type specific features of circular RNA expression. PLoS Genet 9(9):e1003777CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lei K et al (2018) The mechanism and function of circular RNAs in human diseases. Exp Cell Res 368(2):147–158CrossRefPubMedGoogle Scholar
  42. 42.
    Chédin F (2016) Nascent connections: R-loops and chromatin patterning. Trends Genet 32(12):828–838CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Holdt LM, Kohlmaier A, Teupser D (2018) Molecular functions and specific roles of circRNAs in the cardiovascular system. Non-Coding RNA Res 3(2):75–98CrossRefGoogle Scholar
  44. 44.
    Rong D et al (2017) An emerging function of circRNA-miRNAs-mRNA axis in human diseases. Oncotarget 8(42):73271CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Saadatian Z et al (2014) Single-nucleotide polymorphisms within micrornas sequences and their 3′utr target sites may regulate gene expression in gastrointestinal tract cancers. Iran Red Crescent Med J 16(7):e16659CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Baek D et al (2008) The impact of microRNAs on protein output. Nature 455:64–71CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Selbach M et al (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455(7209):58CrossRefPubMedGoogle Scholar
  48. 48.
    Liu J et al (2017) Circles reshaping the RNA world: from waste to treasure. Mol Cancer 16(1):58CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Hansen TB et al (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384CrossRefGoogle Scholar
  50. 50.
    Chen Y et al (2016) Circular RNAs: a new frontier in the study of human diseases. J Med Genet 53(6):359–365CrossRefPubMedGoogle Scholar
  51. 51.
    Barrett SP, Salzman J (2016) Circular RNAs: analysis, expression and potential functions. Development 143(11):1838–1847CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Peng L et al (2017) Circular RNA ZNF609 functions as a competitive endogenous RNA to regulate AKT3 expression by sponging miR-150-5p in Hirschsprung’s disease. Oncotarget 8(1):808PubMedGoogle Scholar
  53. 53.
    Wang K et al (2016) A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223. Eur Heart J 37(33):2602–2611CrossRefPubMedGoogle Scholar
  54. 54.
    Guo JU et al (2014) Expanded identification and characterization of mammalian circular RNAs. Genome Biol 15(7):409CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4(9):721CrossRefPubMedGoogle Scholar
  56. 56.
    Tay FC et al (2015) Using artificial microRNA sponges to achieve microRNA loss-of-function in cancer cells. Adv Drug Deliv Rev 81:117–127CrossRefPubMedGoogle Scholar
  57. 57.
    Begemann G et al (1997) Muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins. Development 124(21):4321–4331PubMedGoogle Scholar
  58. 58.
    Lapik YR et al (2004) Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol Cell 15(1):17–29CrossRefPubMedGoogle Scholar
  59. 59.
    Rohrmoser M et al (2007) Interdependence of Pes1, Bop1, and WDR12 controls nucleolar localization and assembly of the PeBoW complex required for maturation of the 60S ribosomal subunit. Mol Cell Biol 27(10):3682–3694CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Holdt LM et al (2016) Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nat Commun 7:12429CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Abdelmohsen K et al (2017) Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol 14(3):361–369CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Du WW et al (2016) Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res 44(6):2846–2858CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Du WW et al (2017) Induction of tumor apoptosis through a circular RNA enhancing Foxo3 activity. Cell Death Differ 24(2):357CrossRefPubMedGoogle Scholar
  64. 64.
    Chen C-Y, Sarnow P (1995) Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 268(5209):415–417CrossRefPubMedGoogle Scholar
  65. 65.
    Legnini I et al (2017) Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell 66:22–37CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Costelli P (2017) Circ-ZNF609: a novel regulator of myogenesis. Non-Coding RNA Investig 1:2CrossRefGoogle Scholar
  67. 67.
    Li S, Mason CE (2014) The pivotal regulatory landscape of RNA modifications. Annu Rev Genom Hum Genet 15:127–150CrossRefGoogle Scholar
  68. 68.
    Wei C-M, Gershowitz A, Moss B (1975) Methylated nucleotides block 5′ terminus of HeLa cell messenger RNA. Cell 4(4):379–386CrossRefPubMedGoogle Scholar
  69. 69.
    Yue Y, Liu J, He C (2015) RNA N6-methyladenosine methylation in post-transcriptional gene expression regulation. Genes Dev 29(13):1343–1355CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Meyer KD, Jaffrey SR (2014) The dynamic epitranscriptome: N 6-methyladenosine and gene expression control. Nat Rev Mol Cell Biol 15(5):313CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Zhou J et al (2015) Dynamic m 6 A mRNA methylation directs translational control of heat shock response. Nature 526(7574):591CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Meyer KD et al (2015) 5′ UTR m 6 A promotes cap-independent translation. Cell 163(4):999–1010CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Pan R-Y et al (2017) Circular RNAs promote TRPM3 expression by inhibiting hsa-miR-130a-3p in coronary artery disease patients. Oncotarget 8(36):60280CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Lukiw W (2013) Circular RNA (circRNA) in Alzheimer’s disease (AD). Front Genet 4:307PubMedPubMedCentralGoogle Scholar
  75. 75.
    Zheng F et al (2017) Circular RNA expression profiles of peripheral blood mononuclear cells in rheumatoid arthritis patients, based on microarray chip technology. Mol Med Rep 16(6):8029–8036CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Zhang Z et al (2018) Circular RNA: new star, new hope in cancer. BMC Cancer 18(1):834CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Thurner M et al (2018) Integration of human pancreatic islet genomic data refines regulatory mechanisms at Type 2 Diabetes susceptibility loci. Elife 7:e31977CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Stoll L et al (2018) Circular RNAs as novel regulators of β-cell functions in normal and disease conditions. Mol Metab 9:69–83CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Kaur S, Mirza A, Pociot F (2018) Cell type-selective expression of circular RNAs in human pancreatic islets. Non-Coding RNA 4(4):38CrossRefPubMedCentralGoogle Scholar
  80. 80.
    Xu H et al (2015) The circular RNA Cdr1as, via miR-7 and its targets, regulates insulin transcription and secretion in islet cells. Sci Rep 5:12453CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Jacobs E et al (2017) Burden of mortality attributable to diagnosed diabetes: a nationwide analysis based on claims data from 65 million people in Germany. Diabetes Care 40(12):1703–1709CrossRefPubMedGoogle Scholar
  82. 82.
    Reddy MA et al (2016) Regulation of vascular smooth muscle cell dysfunction under diabetic conditions by miR-504. Arterioscler Thromb Vasc Biol 36(5):864–873CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Chen J et al (2017) Circular RNA WDR77 target FGF-2 to regulate vascular smooth muscle cells proliferation and migration by sponging miR-124. Biochem Biophys Res Commun 494(1–2):126–132CrossRefPubMedGoogle Scholar
  84. 84.
    Balijepalli C et al (2017) Hypoglycemia: a review of definitions used in clinical trials evaluating antihyperglycemic drugs for diabetes. Clin Epidemiol 9:291CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Bertoluci MC, Rocha VZ (2017) Cardiovascular risk assessment in patients with diabetes. Diabetol Metab Syndr 9(1):25CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Shang F-F et al (2018) Alterations of circular RNAs in hyperglycemic human endothelial cells. Biochem Biophys Res Commun 499(3):551–555CrossRefPubMedGoogle Scholar
  87. 87.
    Liu C et al (2017) Silencing of circular RNA-ZNF609 ameliorates vascular endothelial dysfunction. Theranostics 7(11):2863CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Hamik A, Wang B, Jain MK (2006) Transcriptional regulators of angiogenesis. Arterioscler Thromb Vasc Biol 26(9):1936–1947CrossRefPubMedGoogle Scholar
  89. 89.
    Tang C-M et al (2017) CircRNA_000203 enhances the expression of fibrosis-associated genes by derepressing targets of miR-26b-5p, Col1a2 and CTGF, in cardiac fibroblasts. Sci Rep 7:40342CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Zhou B, Yu J-W (2017) A novel identified circular RNA, circRNA_010567, promotes myocardial fibrosis via suppressing miR-141 by targeting TGF-β1. Biochem Biophys Res Commun 487(4):769–775CrossRefPubMedGoogle Scholar
  91. 91.
    Liebl A et al (2002) Complications, co-morbidity, and blood glucose control in type 2 diabetes mellitus patients in Germany-results from the CODE-2TM study. Exp Clin Endocrinol Diabetes 110(01):10–16CrossRefPubMedGoogle Scholar
  92. 92.
    Wang L et al (2018) Intrathecal circHIPK3 shRNA alleviates neuropathic pain in diabetic rats. Biochem Biophys Res Commun 505(3):644–650CrossRefPubMedGoogle Scholar
  93. 93.
    Shan K et al (2017) Circular noncoding RNA HIPK3 mediates retinal vascular dysfunction in diabetes mellitus. Circulation 136(17):1629–1642CrossRefGoogle Scholar
  94. 94.
    Robitaille J et al (2002) Mutant frizzled-4 disrupts retinal angiogenesis in familial exudative vitreoretinopathy. Nat Genet 32(2):326CrossRefPubMedGoogle Scholar
  95. 95.
    Munoz-Chapuli R, Quesada A, Medina MA (2004) Angiogenesis and signal transduction in endothelial cells. Cell Mol Life Sci CMLS 61(17):2224–2243CrossRefPubMedGoogle Scholar
  96. 96.
    Lukiw WJ, Rogaev EI, Zhao Y (2016) Circular RNA (circRNA) ciRS-7 targets miRNA-7 trafficking and ubiquitin-conjugase E2A (UBE2A)-mediated protein degradation in Alzheimer’s disease (AD) and age-related macular degeneration (AMD). Invest Ophthalmol Vis Sci 57(12):5778Google Scholar
  97. 97.
    Pei X et al (2018) Overexpression of circRNA-001175 promotes proliferation and angiogenesis and inhibits apoptosis of the human umbilical vein endothelial cells (HUVECs) induced by high glucose. Int J Clin Exp Pathol 11(1):359–366Google Scholar
  98. 98.
    Pan L et al (2018) Human circular RNA-0054633 regulates high glucose-induced vascular endothelial cell dysfunction through the microRNA-218/roundabout 1 and microRNA-218/heme oxygenase-1 axes. Int J Mol Med 42(1):597–606PubMedGoogle Scholar
  99. 99.
    Zhang S-J et al (2017) Identification and characterization of circular RNAs as a new class of putative biomarkers in diabetes retinopathy. Invest Ophthalmol Vis Sci 58(14):6500–6509CrossRefPubMedGoogle Scholar
  100. 100.
    Rojiani MV et al (2010) Expression of MMP-2 correlates with increased angiogenesis in CNS metastasis of lung carcinoma. Int J Clin Exp Pathol 3(8):775PubMedPubMedCentralGoogle Scholar
  101. 101.
    Yun JH et al (2017) Endothelial STAT3 activation increases vascular leakage through downregulating tight junction proteins: implications for diabetic retinopathy. J Cell Physiol 232(5):1123–1134CrossRefPubMedGoogle Scholar
  102. 102.
    Zadro-Lamoureux LA et al (2009) Effects on XIAP retinal detachment-induced photoreceptor apoptosis. Invest Ophthalmol Vis Sci 50(3):1448–1453CrossRefPubMedGoogle Scholar
  103. 103.
    Khodabandehloo H et al (2016) Molecular and cellular mechanisms linking inflammation to insulin resistance and β-cell dysfunction. Transl Res 167(1):228–256CrossRefPubMedGoogle Scholar
  104. 104.
    Fang Y et al (2018) Screening of circular RNAs and validation of circANKRD36 associated with inflammation in patients with type 2 diabetes mellitus. Int J Mol Med 42(4):1865–1874PubMedPubMedCentralGoogle Scholar
  105. 105.
    Yang H, Wang Q, Li S (2016) MicroRNA-218 promotes high glucose-induced apoptosis in podocytes by targeting heme oxygenase-1. Biochem Biophys Res Commun 471(4):582–588CrossRefPubMedGoogle Scholar
  106. 106.
    Mahmoud AM et al (2017) Commiphora molmol resin attenuates diethylnitrosamine/phenobarbital-induced hepatocarcinogenesis by modulating oxidative stress, inflammation, angiogenesis and Nrf2/ARE/HO-1 signaling. Chem Biol Interact 270:41–50CrossRefPubMedGoogle Scholar
  107. 107.
    Yang J-H et al (2018) The differentially expressed circular RNAs in the substantia nigra and corpus striatum of Nrf2-knockout mice. Cell Physiol Biochem 50(3):936–951CrossRefPubMedGoogle Scholar
  108. 108.
    Cheng J, Liu Q, Hu N, Zheng F, Zhang X, Ni Y et al (2019) Downregulation of hsa_circ_0068087 ameliorates TLR4/NF-κB/NLRP3 inflammasome-mediated inflammation and endothelial cell dysfunction in high glucose conditioned by sponging miR-197. Gene 709:1–7CrossRefPubMedGoogle Scholar
  109. 109.
    Parveen A, Jin M, Kim SY (2018) Bioactive phytochemicals that regulate the cellular processes involved in diabetic nephropathy. Phytomedicine 39:146–159CrossRefPubMedGoogle Scholar
  110. 110.
    Kölling M et al (2018) The circular RNA ciRs-126 predicts survival in critically ill patients with acute kidney injury. Kidney Int Rep 3(5):1144–1152CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Cheng X, Joe B (2017) Circular RNAs in rat models of cardiovascular and renal diseases. Physiol Genom 49:484–490CrossRefGoogle Scholar
  112. 112.
    Hu W et al (2019) Circular RNA circRNA_15698 aggravates the extracellular matrix of diabetic nephropathy mesangial cells via miR-185/TGF-β1. J Cell Physiol 234(2):1469–1476CrossRefPubMedGoogle Scholar
  113. 113.
    Dangwal S et al (2015) Impairment of wound healing in patients with type 2 diabetes mellitus influences circulating microRNA patterns via inflammatory cytokines. Arterioscler Thromb Vasc Biol 35(6):1480–1488CrossRefPubMedGoogle Scholar
  114. 114.
    Yang Z-G et al (2017) The circular RNA interacts with STAT3, increasing its nuclear translocation and wound repair by modulating Dnmt3a and miR-17 function. Mol Ther 25(9):2062–2074CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Vaishya S, Sarwade RD, Seshadri V (2018) MicroRNA, proteins, and metabolites as novel biomarkers for prediabetes, diabetes, and related complications. Front Endocrinol 9:180CrossRefGoogle Scholar
  116. 116.
    Guay C, Regazzi R (2013) Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol 9(9):513CrossRefGoogle Scholar
  117. 117.
    Enuka Y et al (2015) Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor. Nucleic Acids Res 44(3):1370–1383CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Jeck WR, Sharpless NE (2014) Detecting and characterizing circular RNAs. Nat Biotechnol 32(5):453CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Zhang Z, Yang T, Xiao J (2018) Circular RNAs: promising biomarkers for human diseases. EBioMedicine 34:267–274CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Zhao Z et al (2017) Hsa_circ_0054633 in peripheral blood can be used as a diagnostic biomarker of pre-diabetes and type 2 diabetes mellitus. Acta Diabetol 54(3):237–245CrossRefPubMedGoogle Scholar
  121. 121.
    Sally M et al (2017) Plasma circular RNA (0054633) expression as a biomarker for prediabetes and type 2 diabetes mellitus. Bull Egypt Soc Physiol Sci 38(1):77–88Google Scholar
  122. 122.
    Li X et al (2017) Hsa-circRNA11783-2 in peripheral blood is correlated with coronary artery disease and type 2 diabetes mellitus. Diabetes Vasc Dis Res 14(6):510–515CrossRefGoogle Scholar
  123. 123.
    Gu Y et al (2017) Altered expression profile of circular RNAs in the serum of patients with diabetic retinopathy revealed by microarray. Ophthalmic Res 58(3):176–184CrossRefPubMedGoogle Scholar
  124. 124.
    Wang X et al (2017) Investigating factors associated with depressive symptoms of chronic kidney diseases in china with type 2 diabetes. J Diabetes Res 2017:7Google Scholar
  125. 125.
    Vancampfort D et al (2015) Type 2 diabetes in patients with major depressive disorder: a meta-analysis of prevalence estimates and predictors. Depress Anxiety 32(10):763–773CrossRefPubMedGoogle Scholar
  126. 126.
    Jiang G et al (2017) Relationships of circular RNA with diabetes and depression. Sci Rep 7(1):7285CrossRefPubMedPubMedCentralGoogle Scholar
  127. 127.
    An T, He Z-C, Zhang X-Q, Li J, Chen A-L, Tan F et al (2019) Baduanjin exerts anti-diabetic and anti-depression effects by regulating the expression of mRNA, lncRNA, and circRNA. Chin Med 14(1):3CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Alkan F et al (2017) RIsearch2: suffix array-based large-scale prediction of RNA-RNA interactions and siRNA off-targets. Nucleic Acids Res 45(8):e60PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Clinical BiochemistryAbadan Faculty of Medical SciencesAbadanIran
  2. 2.Student Research CommitteeAbadan Faculty of Medical SciencesAbadanIran
  3. 3.Department of Medical Genetics, Faculty of MedicineShahid Beheshti University of Medical SciencesTehranIran
  4. 4.Department of Radiation SciencesYasuj University of Medical SciencesYasujIran
  5. 5.Department of Laboratory Sciences, Faculty of ParamedicineYasuj University of Medical SciencesYasujIran

Personalised recommendations