Long Noncoding RNAs as Diagnostic and Therapeutic Targets in Type 2 Diabetes and Related Complications
Abstract
:1. Introduction
1.1. Long Noncoding RNAs are Noncoding, Multifunctional Transcripts
1.2. Diabetes Is a Worldwide Health Concern
1.3. LncRNA Profiling in Pancreatic β-Cells and Regulation of Glucose Homeostasis
1.4. LncRNA Profiling in Diabetic Kidney Disease
1.5. LncRNAs Involved in Diabetic Retinopathy
1.6. LncRNAs as Targets for Therapeutic Intervention
2. Conclusions
Conflicts of Interest
References
- The ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489, 57–74. [Google Scholar] [CrossRef]
- Maher, B. ENCODE: The human encyclopaedia. Nature 2012, 489, 46–48. [Google Scholar] [CrossRef] [PubMed]
- Mattick, J.S.; Makunin, I.V. Non-coding RNA. Hum. Mol. Genet. 2006, 15, R17–R29. [Google Scholar] [CrossRef] [PubMed]
- Esteller, M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12, 861–874. [Google Scholar] [CrossRef] [PubMed]
- Kapranov, P.; Cheng, J.; Dike, S.; Nix, D.A.; Duttagupta, R.; Willingham, A.T.; Stadler, P.F.; Hertel, J.; Hackermüller, J.; Hofacker, I.L.; et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007, 316, 1484–1488. [Google Scholar] [CrossRef] [PubMed]
- Guttman, M.; Amit, I.; Garber, M.; French, C.; Lin, M.F.; Feldser, D.; Huarte, M.; Zuk, O.; Carey, B.W.; Cassady, J.P.; et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458, 223–227. [Google Scholar] [CrossRef] [PubMed]
- Wu, Q.; Kim, Y.C.; Lu, J.; Xuan, Z.; Chen, J.; Zheng, Y.; Zhou, T.; Zhang, M.Q.; Wu, C.I.; Wang, S.M. Poly A-transcripts expressed in HeLa cells. PLoS ONE 2008, 3, e2803. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Zhu, H.; Luo, Y. Understanding the Functions of Long Non-Coding RNAs through Their Higher-Order Structures. Int. J. Mol. Sci. 2016, 17, 702. [Google Scholar] [CrossRef] [PubMed]
- Moran, V.A.; Perera, R.J.; Khalil, A.M. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res. 2012, 40, 6391–6400. [Google Scholar] [CrossRef] [PubMed]
- Kornienko, A.E.; Guenzl, P.M.; Barlow, D.P.; Pauler, F.M. Gene regulation by the act of long non-coding RNA transcription. BMC Biol. 2013, 11, 59. [Google Scholar] [CrossRef] [PubMed]
- Wang, K.C.; Chang, H.Y. Molecular mechanisms of long noncoding RNAs. Mol. Cell. 2011, 43, 904–914. [Google Scholar] [CrossRef] [PubMed]
- Cabili, M.N.; Trapnell, C.; Goff, L.; Koziol, M.; Tazon-Vega, B.; Regev, A.; Rinn, J.L. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011, 25, 1915–1927. [Google Scholar] [CrossRef] [PubMed]
- Derrien, T.; Johnson, R.; Bussotti, G.; Tanzer, A.; Djebali, S.; Tilgner, H.; Guernec, G.; Martin, D.; Merkel, A.; Knowles, D.G.; et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012, 22, 1775–1789. [Google Scholar] [CrossRef] [PubMed]
- Kapusta, A.; Kronenberg, Z.; Lynch, V.J.; Zhuo, X.; Ramsay, L.; Bourque, G.; Yandell, M.; Feschotte, C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 2013, 9, e1003470. [Google Scholar] [CrossRef] [PubMed]
- Ponting, C.P.; Oliver, P.L.; Reik, W. Evolution and functions of long noncoding RNAs. Cell 2009, 136, 629–641. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.J.; Nowakowski, T.J.; Pollen, A.A.; Lui, J.H.; Horlbeck, M.A.; Attenello, F.J.; He, D.; Weissman, J.S.; Kriegstein, A.R.; Diaz, A.A.; et al. Single-cell analysis of long non-coding RNAs in the developing human neocortex. Genome Biol. 2016, 17, 67. [Google Scholar] [CrossRef] [PubMed]
- Shalek, A.K.; Satija, R.; Adiconis, X.; Gertner, R.S.; Gaublomme, J.T.; Raychowdhury, R.; Schwartz, S.; Yosef, N.; Malboeuf, C.; Lu, D.; et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 2013, 498, 236–240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chung, S.; Nakagawa, H.; Uemura, M.; Piao, L.; Ashikawa, K.; Hosono, N.; Takata, R.; Akamatsu, S.; Kawaguchi, T.; Morizono, T.; et al. Association of a novel long non-coding RNA in 8q24 with prostate cancer susceptibility. Cancer Sci. 2011, 102, 245–252. [Google Scholar] [CrossRef] [PubMed]
- Guan, Y.; Kuo, W.L.; Stilwell, J.L.; Takano, H.; Lapuk, A.V.; Fridlyand, J.; Mao, J.H.; Yu, M.; Miller, M.A.; Santos, J.L.; et al. Amplification of PVT1 contributes to the pathophysiology of ovarian and breast cancer. Clin. Cancer Res. 2007, 13, 5745–5755. [Google Scholar] [CrossRef] [PubMed]
- Gupta, R.A.; Shah, N.; Wang, K.C.; Kim, J.; Horlings, H.M.; Wong, D.J.; Tsai, M.C.; Hung, T.; Argani, P.; Rinn, J.L.; et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464, 1071–1076. [Google Scholar] [CrossRef] [PubMed]
- Panzitt, K.; Tschernatsch, M.M.; Guelly, C.; Moustafa, T.; Stradner, M.; Strohmaier, H.M.; Buck, C.R.; Denk, H.; Schroeder, R.; Trauner, M.; et al. Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterology 2007, 132, 330–342. [Google Scholar] [CrossRef] [PubMed]
- Pibouin, L.; Villaudy, J.; Ferbus, D.; Muleris, M.; Prosperi, M.-T.; Remvikos, Y.; Goubin, G. Cloning of the mRNA of overexpression in colon carcinoma-1: A sequence overexpressed in a subset of colon carcinomas. Cancer Genet. Cytogenet. 2002, 133, 55–60. [Google Scholar] [CrossRef]
- Bussiere, T.; Gold, G.; Kovari, E.; Giannakopoulos, P.; Bouras, C.; Perl, D.P.; Morrison, J.H.; Hof, P.R. Stereologic analysis of neurofibrillary tangle formation in prefrontal cortex area 9 in aging and Alzheimer’s disease. Neuroscience 2003, 117, 577–592. [Google Scholar] [CrossRef]
- Lukiw, W.J.; Handley, P.; Wong, L.; Crapper McLachlan, D.R. BC200 RNA in normal human neocortex, non-Alzheimer dementia (NAD), and senile dementia of the Alzheimer type (AD). Neurochem. Res. 1992, 17, 591–597. [Google Scholar] [CrossRef] [PubMed]
- Mus, E.; Hof, P.R.; Tiedge, H. Dendritic BC200 RNA in aging and in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA 2007, 104, 10679–10684. [Google Scholar] [CrossRef] [PubMed]
- Nair, M.; Sagar, V.; Pilakka-Kanthikeel, S. Gene-expression reversal of lncRNAs and associated mRNAs expression in active vs latent HIV infection. Sci. Rep. 2016, 6, 34862. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Chen, C.Y.; Yedavalli, V.S.; Jeang, K.T. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 2013, 4, e00596-12. [Google Scholar] [CrossRef] [PubMed]
- Ishii, N.; Ozaki, K.; Sato, H.; Mizuno, H.; Saito, S.; Takahashi, A.; Miyamoto, Y.; Ikegawa, S.; Kamatani, N.; Hori, M.; et al. Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J. Hum. Genet. 2006, 51, 1087–1099. [Google Scholar] [CrossRef] [PubMed]
- Shirasawa, S.; Harada, H.; Furugaki, K.; Akamizu, T.; Ishikawa, N.; Ito, K.; Ito, K.; Tamai, H.; Kuma, K.; Kubota, S.; et al. SNPs in the promoter of a B cell-specific antisense transcript, SAS-ZFAT, determine susceptibility to autoimmune thyroid disease. Hum. Mol. Genet. 2004, 13, 2221–2231. [Google Scholar] [CrossRef] [PubMed]
- Sonkoly, E.; Bata-Csorgo, Z.; Pivarcsi, A.; Polyanka, H.; Kenderessy-Szabo, A.; Molnar, G.; Szentpali, K.; Bari, L.; Megyeri, K.; Mandi, Y.; et al. Identification and characterization of a novel, psoriasis susceptibility-related noncoding RNA gene, PRINS. J. Biol. Chem. 2005, 280, 24159–24167. [Google Scholar] [CrossRef] [PubMed]
- Yu, B.; Liu, L.; Sun, H.; Chen, Y. Long noncoding RNA AK056155 involved in the development of Loeys-Dietz syndrome through AKT/PI3K signaling pathway. Int. J. Clin. Exp. Pathol. 2015, 8, 10768–10775. [Google Scholar] [PubMed]
- Chen, G.; Wang, Z.; Wang, D.; Qiu, C.; Liu, M.; Chen, X.; Zhang, Q.; Yan, G.; Cui, Q. LncRNADisease: A database for long-non-coding RNA-associated diseases. Nucleic Acids Res. 2013, 41, D983–D986. [Google Scholar] [CrossRef] [PubMed]
- Kunej, T.; Obsteter, J.; Pogacar, Z.; Horvat, S.; Calin, G.A. The decalog of long non-coding RNA involvement in cancer diagnosis and monitoring. Crit. Rev. Clin. Lab. Sci. 2014, 51, 344–357. [Google Scholar] [CrossRef] [PubMed]
- Spizzo, R.; Almeida, M.I.; Colombatti, A.; Calin, G.A. Long non-coding RNAs and cancer: A new frontier of translational research? Oncogene 2012, 31, 4577–4587. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, H.; Ma, H.; Zhou, D. Plasma HULC as a promising novel biomarker for the detection of hepatocellular carcinoma. Biomed. Res. Int. 2013, 2013, 136106. [Google Scholar] [CrossRef] [PubMed]
- DeFronzo, R.A.; Abdul-Ghani, M. Type 2 diabetes can be prevented with early pharmacological intervention. Diabetes Care 2011, 34 (Suppl. 2), S202–S209. [Google Scholar] [CrossRef] [PubMed]
- DeFronzo, R.A.; Bonadonna, R.C.; Ferrannini, E. Pathogenesis of NIDDM. A balanced overview. Diabetes Care 1992, 15, 318–368. [Google Scholar] [CrossRef] [PubMed]
- Danaei, G.; Finucane, M.M.; Lu, Y.; Singh, G.M.; Cowan, M.J.; Paciorek, C.J.; Lin, J.K.; Farzadfar, F.; Khang, Y.-H.; Stevens, G.A.; et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: Systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 2011, 378, 31–40. [Google Scholar] [CrossRef]
- Whiting, D.R.; Guariguata, L.; Weil, C.; Shaw, J. IDF diabetes atlas: Global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res. Clin. Pract. 2011, 94, 311–321. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization (WHO). Global Status Report on Noncommunicable Diseases; WHO: Geneva, Switzerland, 2011. [Google Scholar]
- Berends, L.M.; Ozanne, S.E. Early determinants of type-2 diabetes. Best Pract. Res. Clin. Endocrinol. Metab. 2012, 26, 569–580. [Google Scholar] [CrossRef] [PubMed]
- Scott, L.J.; Mohlke, K.L.; Bonnycastle, L.L.; Willer, C.J.; Li, Y.; Duren, W.L.; Erdos, M.R.; Stringham, H.M.; Chines, P.S.; Jackson, A.U.; et al. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 2007, 316, 1341–1345. [Google Scholar] [CrossRef] [PubMed]
- Sladek, R.; Rocheleau, G.; Rung, J.; Dina, C.; Shen, L.; Serre, D.; Boutin, P.; Vincent, D.; Belisle, A.; Hadjadj, S.; et al. A genome-wide association study identified novel risk loci for type 2 diabetes. Nature 2007, 445, 881–885. [Google Scholar] [CrossRef] [PubMed]
- Zeggini, E.; Scott, L.J.; Saxena, R.; Voight, B.F.; Marchini, J.L.; Hu, T.; de Bakker, P.I.W.; Abecasis, G.; Almgren, P.; Andersen, G.; et al. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat. Genet. 2008, 40, 638–645. [Google Scholar] [CrossRef] [PubMed]
- Zeggini, E.; Weedon, M.N.; Lindgren, C.M.; Frayling, T.M.; Elliott, K.S.; Lango, H.; Timpson, N.J.; Perry, J.R.B.; Rayner, N.W.; et al. Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 2007, 316, 1336–1341. [Google Scholar] [CrossRef] [PubMed]
- Hindorff, L.A.; Sethupathy, P.; Junkins, H.A.; Ramos, E.M.; Mehta, J.P.; Collins, F.S.; Manolio, T.A. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc. Natl. Acad. Sci. USA 2009, 106, 9362–9367. [Google Scholar] [CrossRef] [PubMed]
- Ling, C.; Groop, L. Epigenetics: A molecular link between environmental factors and type 2 diabetes. Diabetes 2009, 58, 2718–2725. [Google Scholar] [CrossRef] [PubMed]
- Sun, X.; Wong, D. Long non-coding RNA-mediated regulation of glucose homeostasis and diabetes. Am. J. Cardiovasc. Dis. 2016, 6, 17–25. [Google Scholar] [PubMed]
- Kotake, Y.; Nakagawa, T.; Kitagawa, K.; Suzuki, S.; Liu, N.; Kitagawa, M.; Xiong, Y. Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 2011, 30, 1956–1962. [Google Scholar] [CrossRef] [PubMed]
- Thomas, A.A.; Feng, B.; Chakrabarti, S. ANRIL: A Regulator of VEGF in Diabetic Retinopathy. Invest. Ophthalmol. Vis. Sci. 2017, 58, 470–480. [Google Scholar] [CrossRef] [PubMed]
- Arnes, L.; Akerman, I.; Balderes, D.A.; Ferrer, J.; Sussel, L. betalinc1 encodes a long noncoding RNA that regulates islet beta-cell formation and function. Genes Dev. 2016, 30, 502–507. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Wang, S.; Yao, D.; Yan, Q.; Lu, W. A novel long non-coding RNA CYP4B1-PS1–001 regulates proliferation and fibrosis in diabetic nephropathy. Mol. Cell. Endocrinol. 2016, 426, 136–145. [Google Scholar] [CrossRef] [PubMed]
- Reddy, M.A.; Chen, Z.; Park, J.T.; Wang, M.; Lanting, L.; Zhang, Q.; Bhatt, K.; Leung, A.; Wu, X.; Putta, S.; et al. Regulation of inflammatory phenotype in macrophages by a diabetes-induced long noncoding RNA. Diabetes 2014, 63, 4249–4261. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Yao, D.; Wang, S.; Yan, Q.; Lu, W. Long non-coding RNA ENSMUST00000147869 protects mesangial cells from proliferation and fibrosis induced by diabetic nephropathy. Endocrine 2016, 54, 81–92. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Peng, R.; Peng, H.; Liu, H.; Wen, L.; Wu, T.; Yi, H.; Li, A.; Zhang, Z. miR-451 suppresses the NF-kappaB-mediated proinflammatory molecules expression through inhibiting LMP7 in diabetic nephropathy. Mol. Cell. Endocrinol. 2016, 433, 75–86. [Google Scholar] [CrossRef] [PubMed]
- Gabory, A.; Jammes, H.; Dandolo, L. The H19 locus: Role of an imprinted non-coding RNA in growth and development. Bioessays 2010, 32, 473–480. [Google Scholar] [CrossRef] [PubMed]
- Raveh, E.; Matouk, I.J.; Gilon, M.; Hochberg, A. The H19 Long non-coding RNA in cancer initiation, progression and metastasis - A proposed unifying theory. Mol. Cancer 2015, 14, 184. [Google Scholar] [CrossRef] [PubMed]
- Fadista, J.; Vikman, P.; Laakso, E.O.; Mollet, I.G.; Esguerra, J.L.; Taneera, J.; Storm, P.; Osmark, P.; Landevall, C.; Prasad, R.B.; et al. Global genomic and transcriptomic analysis of human pancreatic islets reveals novel genes influencing glucose metabolism. Proc. Natl. Acad. Sci. USA 2014, 111, 13924–13929. [Google Scholar] [CrossRef] [PubMed]
- Kato, M.; Wang, M.; Chen, Z.; Bhatt, K.; Oh, H.J.; Lanting, L.; Deshpande, S.; Jia, Y.; Lai, J.Y.C.; O’Connor, C.L.; et al. An endoplasmic reticulum stress-regulated lncRNA hosting a microRNA megacluster induces early features of diabetic nephropathy. Nat. Commun. 2016, 7, 12864. [Google Scholar] [CrossRef] [PubMed]
- Puthanveetil, P.; Chen, S.; Feng, B.; Gautam, A.; Chakrabarti, S. Long non-coding RNA MALAT1 regulates hyperglycaemia induced inflammatory process in the endothelial cells. J. Cell. Mol. Med. 2015, 19, 1418–1425. [Google Scholar] [CrossRef] [PubMed]
- Lelli, A.; Nolan, K.A.; Santambrogio, S.; Gonçalves, A.F.; Schonenberger, M.J.; Guinot, A.; Frew, I.J.; Marti, H.H.; Hoogewijs, D.; Wenger, R.H. Induction of long noncoding RNA MALAT1 in hypoxic mice. Hypoxia 2015, 3, 45–52. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.-Y.; Yao, J.; Li, X.-M.; Song, Y.-C.; Wang, X.-Q.; Li, Y.-J.; Yan, B.; Jiang, Q. Pathogenic role of lncRNA-MALAT1 in endothelial cell dysfunction in diabetes mellitus. Cell Death Dis. 2014, 5, e1506. [Google Scholar] [CrossRef] [PubMed]
- Zhou, L.; Xu, D.Y.; Sha, W.G.; Shen, L.; Lu, G.Y.; Yin, X. Long non-coding MIAT mediates high glucose-induced renal tubular epithelial injury. Biochem. Biophys. Res. Commun. 2015, 468, 726–732. [Google Scholar] [CrossRef] [PubMed]
- Yan, B.; Yao, J.; Liu, J.Y.; Li, X.; Wang, X.; Li, Y.; Tao, Z.; Song, Y.; Chen, Q.; Jiang, Q. lncRNA-MIAT regulates microvascular dysfunction by functioning as a competing endogenous RNA. Circ. Res. 2015, 116, 1143–1156. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Wu, Y.B.; Zhou, J.; Kang, D.M. Upregulation of lncRNA MEG3 promotes hepatic insulin resistance via increasing FoxO1 expression. Biochem. Biophys. Res. Commun. 2016, 469, 319–325. [Google Scholar] [CrossRef] [PubMed]
- You, L.; Wang, N.; Yin, D.; Wang, L.; Jin, F.; Zhu, Y.; Yuan, Q.; De, W. Downregulation of Long Noncoding RNA Meg3 Affects Insulin Synthesis and Secretion in Mouse Pancreatic Beta Cells. J. Cell Physiol. 2016, 231, 852–862. [Google Scholar] [CrossRef] [PubMed]
- Qiu, G.Z.; Tian, W.; Fu, H.T.; Li, C.P.; Liu, B. Long noncoding RNA-MEG3 is involved in diabetes mellitus-related microvascular dysfunction. Biochem. Biophys. Res. Commun. 2016, 471, 135–141. [Google Scholar] [CrossRef] [PubMed]
- Lin, Z.; Li, X.; Zhan, X.; Sun, L.; Gao, J.; Cao, Y.; Qiu, H. Construction of competitive endogenous RNA network reveals regulatory role of long non-coding RNAs in type 2 diabetes mellitus. J. Cell. Mol. Med. 2017. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, M.L.; DiStefano, J.K. Functional characterization of the plasmacytoma variant translocation 1 gene (PVT1) in diabetic nephropathy. PLoS ONE 2010, 6, e18671. [Google Scholar] [CrossRef] [PubMed]
- Akerman, I.; Tu, Z.; Beucher, A.; Rolando, D.M.; Sauty-Colace, C.; Benazra, M.; Nakic, N.; Yang, J.; Wang, H.; Pasquali, L.; et al. Human Pancreatic beta Cell lncRNAs Control Cell-Specific Regulatory Networks. Cell Metab. 2017, 25, 400–411. [Google Scholar] [CrossRef] [PubMed]
- Na, H.K.; Surh, Y.J. Oncogenic potential of Nrf2 and its principal target protein heme oxygenase-1. Free Radic. Biol. Med. 2014, 67, 353–365. [Google Scholar] [CrossRef] [PubMed]
- Fu, Z.; Gilbert, E.R.; Liu, D. Regulation of insulin synthesis and secretion and pancreatic Beta-cell dysfunction in diabetes. Curr. Diabetes Rev. 2013, 9, 25–53. [Google Scholar] [CrossRef] [PubMed]
- Moran, I.; Akerman, I.; van de Bunt, M.; Xie, R.; Benazra, M.; Nammo, T.; Arnes, L.; Nakic, N.; García-Hurtado, J.; Rodríguez-Seguí, S.; et al. Human beta cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes. Cell Metab. 2012, 16, 435–448. [Google Scholar] [CrossRef] [PubMed]
- Cho, Y.S.; Chen, C.H.; Hu, C.; Long, J.; Ong, R.T.; Sim, X.; Takeuchi, F.; Wu, Y.; Go, M.J.; Yamauchi, T.; et al. Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians. Nat. Genet. 2012, 44, 67–72. [Google Scholar] [CrossRef] [PubMed]
- Dupuis, J.; Langenberg, C.; Prokopenko, I.; Saxena, R.; Soranzo, N.; Jackson, A.U.; Wheeler, E.; Glazer, N.L.; Bouatia-Naji, N.; Gloyn, A.L.; et al. New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet. 2010, 42, 105–116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kooner, J.S.; Saleheen, D.; Sim, X.; Sehmi, J.; Zhang, W.; Frossard, P.; Been, L.F.; Chia, K.S.; Dimas, A.S.; Hassanali, N.; et al. Genome-wide association study in individuals of South Asian ancestry identifies six new type 2 diabetes susceptibility loci. Nat. Genet. 2011, 43, 984–989. [Google Scholar] [CrossRef] [PubMed]
- Strawbridge, R.J.; Dupuis, J.; Prokopenko, I.; Barker, A.; Ahlqvist, E.; Rybin, D.; Petrie, J.R.; Travers, M.E.; Bouatia-Naji, N.; Dimas, A.S.; et al. Genome-wide association identifies nine common variants associated with fasting proinsulin levels and provides new insights into the pathophysiology of type 2 diabetes. Diabetes 2011, 60, 2624–2634. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voight, B.F.; Scott, L.J.; Steinthorsdottir, V.; Morris, A.P.; Dina, C.; Welch, R.P.; Zeggini, E.; Huth, C.; Aulchenko, Y.S.; Thorleifsson, G.; et al. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat. Genet. 2010, 42, 579–589. [Google Scholar] [CrossRef] [PubMed]
- Pasmant, E.; Sabbagh, A.; Vidaud, M.; Bieche, I. ANRIL, a long, noncoding RNA, is an unexpected major hotspot in GWAS. FASEB J. 2011, 25, 444–448. [Google Scholar] [CrossRef] [PubMed]
- Pullen, T.J.; Rutter, G.A. Could lncRNAs contribute to beta-cell identity and its loss in Type 2 diabetes? Biochem. Soc. Trans. 2013, 41, 797–801. [Google Scholar] [CrossRef] [PubMed]
- Rachmilewitz, J.; Goshen, R.; Ariel, I.; Schneider, T.; de Groot, N.; Hochberg, A. Parental imprinting of the human H19 gene. FEBS Lett. 1992, 309, 25–28. [Google Scholar] [CrossRef]
- Petry, C.J.; Evans, M.L.; Wingate, D.L.; Ong, K.K.; Reik, W.; Constancia, M.; Dunger, D.B. Raised late pregnancy glucose concentrations in mice carrying pups with targeted disruption of H19delta13. Diabetes 2010, 59, 282–286. [Google Scholar] [CrossRef] [PubMed]
- Petry, C.J.; Seear, R.V.; Wingate, D.L.; Acerini, C.L.; Ong, K.K.; Hughes, I.A.; Hughes, I.A.; Dunger, D.B. Maternally transmitted foetal H19 variants and associations with birth weight. Hum. Genet. 2011, 130, 663–670. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.; Wu, F.; Zhou, J.; Yan, L.; Jurczak, M.J.; Lee, H.Y.; Yang, L.; Mueller, M.; Zhou, X.-B.; Dandolo, L.; et al. The H19/let-7 double-negative feedback loop contributes to glucose metabolism in muscle cells. Nucleic Acids Res. 2014, 42, 13799–13811. [Google Scholar] [CrossRef] [PubMed]
- Kallen, A.N.; Zhou, X.B.; Xu, J.; Qiao, C.; Ma, J.; Yan, L.; Lu, L.; Liu, C.; Yi, J.-S.; Zhang, H.; et al. The imprinted H19 lncRNA antagonizes let-7 microRNAs. Mol. Cell 2013, 52, 101–112. [Google Scholar] [CrossRef] [PubMed]
- Miyoshi, N.; Wagatsuma, H.; Wakana, S.; Shiroishi, T.; Nomura, M.; Aisaka, K.; Kohda, T.; Surani, M.A.; Kaneko-Ishino, T.; Ishino, F. Identification of an imprinted gene, Meg3/Gtl2 and its human homologue MEG3, first mapped on mouse distal chromosome 12 and human chromosome 14q. Genes Cell 2000, 5, 211–220. [Google Scholar] [CrossRef]
- Guo, Q.; Qian, Z.; Yan, D.; Li, L.; Huang, L. LncRNA-MEG3 inhibits cell proliferation of endometrial carcinoma by repressing Notch signaling. Biomed. Pharmacother. 2016, 82, 589–594. [Google Scholar] [CrossRef] [PubMed]
- Lu, K.H.; Li, W.; Liu, X.H.; Sun, M.; Zhang, M.L.; Wu, W.Q.; Xie, W.-P.; Hou, Y.-Y. Long non-coding RNA MEG3 inhibits NSCLC cells proliferation and induces apoptosis by affecting p53 expression. BMC Cancer 2013, 13, 461. [Google Scholar] [CrossRef] [PubMed]
- Luo, G.; Wang, M.; Wu, X.; Tao, D.; Xiao, X.; Wang, L.; Min, F.; Zeng, F.; Jiang, G. Long Non-Coding RNA MEG3 Inhibits Cell Proliferation and Induces Apoptosis in Prostate Cancer. Cell. Physiol. Biochem. 2015, 37, 2209–2220. [Google Scholar] [CrossRef] [PubMed]
- Jordan, S.D.; Kruger, M.; Willmes, D.M.; Redemann, N.; Wunderlich, F.T.; Brönneke, H.S.; Merkwirth, C.; Kashkar, H.; Olkkonen, V.M.; Böttger, T.; et al. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Biol. 2011, 13, 434–446. [Google Scholar] [CrossRef] [PubMed]
- Cesana, M.; Cacchiarelli, D.; Legnini, I.; Santini, T.; Sthandier, O.; Chinappi, M.; Tramontano, A.; Bozzoni, I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147, 358–369. [Google Scholar] [CrossRef] [PubMed]
- Costa, V.; Esposito, R.; Aprile, M.; Ciccodicola, A. Non-coding RNA and pseudogenes in neurodegenerative diseases: “The (un)Usual Suspects”. Front. Genet. 2012, 3, 231. [Google Scholar] [CrossRef] [PubMed]
- Sumazin, P.; Yang, X.; Chiu, H.S.; Chung, W.J.; Iyer, A.; Llobet-Navas, D.; Rajbhandari, P.; Bansal, M.; Guarnieri, P.; Silva, J.; et al. An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 2011, 147, 370–381. [Google Scholar] [CrossRef] [PubMed]
- Bichu, P.; Nistala, R.; Khan, A.; Sowers, J.R.; Whaley-Connell, A. Angiotensin receptor blockers for the reduction of proteinuria in diabetic patients with overt nephropathy: Results from the AMADEO study. Vasc. Health Risk Manag. 2009, 5, 129–140. [Google Scholar] [PubMed]
- Dalla Vestra, M.; Saller, A.; Mauer, M.; Fioretto, P. Role of mesangial expansion in the pathogenesis of diabetic nephropathy. J. Nephrol. 2001, 14 (Suppl. 4), S51–S57. [Google Scholar] [PubMed]
- Kanwar, Y.S.; Sun, L.; Xie, P.; Liu, F.Y.; Chen, S. A glimpse of various pathogenetic mechanisms of diabetic nephropathy. Annu. Rev. Pathol. 2011, 6, 395–423. [Google Scholar] [CrossRef] [PubMed]
- Ding, Y.; Choi, M.E. Autophagy in diabetic nephropathy. J. Endocrinol. 2015, 224, R15–R30. [Google Scholar] [CrossRef] [PubMed]
- Prabhakar, S.S. Role of nitric oxide in diabetic nephropathy. Semin. Nephrol. 2004, 24, 333–344. [Google Scholar] [CrossRef] [PubMed]
- Afkarian, M.; Sachs, M.C.; Kestenbaum, B.; Hirsch, I.B.; Tuttle, K.R.; Himmelfarb, J.; de Boer, I.H. Kidney disease and increased mortality risk in type 2 diabetes. J. Am. Soc. Nephrol. 2013, 24, 302–308. [Google Scholar] [CrossRef] [PubMed]
- Gray, S.P.; Cooper, M.E. Diabetic nephropathy in 2010: Alleviating the burden of diabetic nephropathy. Nat. Rev. Nephrol. 2011, 7, 71–73. [Google Scholar] [CrossRef] [PubMed]
- Groop, P.H.; Thomas, M.C.; Moran, J.L.; Waden, J.; Thorn, L.M.; Makinen, V.P.; Rosengard-Bärlund, M.; Saraheimo, M.; Hietala, K.; Heikkilä, O.; et al. The presence and severity of chronic kidney disease predicts all-cause mortality in type 1 diabetes. Diabetes 2009, 58, 1651–1658. [Google Scholar] [CrossRef] [PubMed]
- Orchard, T.J.; Secrest, A.M.; Miller, R.G.; Costacou, T. In the absence of renal disease, 20 year mortality risk in type 1 diabetes is comparable to that of the general population: A report from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetologia 2010, 53, 2312–2319. [Google Scholar] [CrossRef] [PubMed]
- Guariguata, L.; Whiting, D.R.; Hambleton, I.; Beagley, J.; Linnenkamp, U.; Shaw, J.E. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res. Clin. Pract. 2014, 103, 137–149. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Dong, C.; Qian, X.; Huang, S.; Feng, Y.; Ye, X.; Miao, H.; You, Q.; Lu, Y.; Ding, D. Microarray analysis of long noncoding RNA expression patterns in diabetic nephropathy. J. Diabetes Complications 2017, 31, 569–576. [Google Scholar] [CrossRef] [PubMed]
- Yi, H.; Peng, R.; Zhang, L.Y.; Sun, Y.; Peng, H.M.; Liu, H.D.; Yu, L.-J.; Li, A.-L.; Zhang, Y.-J.; Jiang, W.-H.; et al. LincRNA-Gm4419 knockdown ameliorates NF-kappaB/NLRP3 inflammasome-mediated inflammation in diabetic nephropathy. Cell Death Dis. 2017, 8, e2583. [Google Scholar] [CrossRef] [PubMed]
- Alwohhaib, M.; Alwaheeb, S.; Alyatama, N.; Dashti, A.A.; Abdelghani, A.; Hussain, N. Single nucleotide polymorphisms at erythropoietin, superoxide dismutase 1, splicing factor, arginine/serin-rich 15 and plasmacytoma variant translocation genes association with diabetic nephropathy. Saudi J. Kidney Dis. Transpl. 2014, 25, 577–581. [Google Scholar] [CrossRef] [PubMed]
- Millis, M.P.; Bowen, D.; Kingsley, C.; Watanabe, R.M.; Wolford, J.K. Variants in the plasmacytoma variant translocation gene (PVT1) are associated with end-stage renal disease attributed to type 1 diabetes. Diabetes 2007, 56, 3027–3032. [Google Scholar] [CrossRef] [PubMed]
- Huppi, K.; Volfovsky, N.; Runfola, T.; Jones, T.L.; Mackiewicz, M.; Martin, S.E.; Mushinski, J.F.; Stephens, R.; Caplen, N.J. The identification of microRNAs in a genomically unstable region of human chromosome 8q24. Mol. Cancer Res. 2008, 6, 212–221. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, M.L.; Khosroheidari, M.; Eddy, E.; Kiefer, J.; DiStefano, J.K. Role of microRNA 1207–5P and its host gene, the long non-coding RNA Pvt1, as mediators of extracellular matrix accumulation in the kidney: Implications for diabetic nephropathy. PLoS ONE 2013, 8, e77468. [Google Scholar] [CrossRef] [PubMed]
- Kato, M.; Putta, S.; Wang, M.; Yuan, H.; Lanting, L.; Nair, I.; Gunn, A.; Nakagawa, Y.; Shimano, H.; Todorov, I.; et al. TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat. Cell Biol. 2009, 11, 881–889. [Google Scholar] [CrossRef] [PubMed]
- Kato, M.; Dang, V.; Wang, M.; Park, J.T.; Deshpande, S.; Kadam, S.; Mardiros, A.; Zhan, Y.; Oettgen, P.; Putta, S.; et al. TGF-beta induces acetylation of chromatin and of Ets-1 to alleviate repression of miR-192 in diabetic nephropathy. Sci. Signal. 2013, 6, ra43. [Google Scholar] [CrossRef] [PubMed]
- Wong, T.Y.; Cheung, C.M.; Larsen, M.; Sharma, S.; Simo, R. Diabetic retinopathy. Nat. Rev. Dis. Primers 2016, 2, 16012. [Google Scholar] [CrossRef] [PubMed]
- Chew, E.Y.; Klein, M.L.; Ferris, F.L., 3rd; Remaley, N.A.; Murphy, R.P.; Chantry, K.; Hoogwerf, B.J.; Miller, D. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy. Early Treatment Diabetic Retinopathy Study (ETDRS) Report 22. Arch. Ophthalmol. 1996, 114, 1079–1084. [Google Scholar] [CrossRef] [PubMed]
- Fenwick, E.K.; Xie, J.; Man, R.E.K.; Sabanayagam, C.; Lim, L.; Rees, G.; Wong, T.Y.; Lamoureux, E.L. Combined poor diabetes control indicators are associated with higher risks of diabetic retinopathy and macular edema than poor glycemic control alone. PLoS ONE 2017, 12, e0180252. [Google Scholar] [CrossRef] [PubMed]
- Stratton, I.M.; Kohner, E.M.; Aldington, S.J.; Turner, R.C.; Holman, R.R.; Manley, S.E.; Matthews, D.R. UKPDS 50: Risk factors for incidence and progression of retinopathy in Type II diabetes over 6 years from diagnosis. Diabetologia 2001, 44, 156–163. [Google Scholar] [CrossRef] [PubMed]
- Yan, B.; Tao, Z.F.; Li, X.M.; Zhang, H.; Yao, J.; Jiang, Q. Aberrant expression of long noncoding RNAs in early diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 2014, 55, 941–951. [Google Scholar] [CrossRef] [PubMed]
- Zachary, I. VEGF signalling: Integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 2003, 31, 1171–1177. [Google Scholar] [CrossRef] [PubMed]
- McArthur, K.; Feng, B.; Wu, Y.; Chen, S.; Chakrabarti, S. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 2011, 60, 1314–1323. [Google Scholar] [CrossRef] [PubMed]
- Ruiz, M.A.; Feng, B.; Chakrabarti, S. Polycomb repressive complex 2 regulates MiR-200b in retinal endothelial cells: Potential relevance in diabetic retinopathy. PLoS ONE 2015, 10, e0123987. [Google Scholar] [CrossRef] [PubMed]
- Abid, M.R.; Guo, S.; Minami, T.; Spokes, K.C.; Ueki, K.; Skurk, C.; Walsh, K.; Aird, W.C. Vascular endothelial growth factor activates PI3K/Akt/forkhead signaling in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 294–300. [Google Scholar] [CrossRef] [PubMed]
- Li, C.P.; Wang, S.H.; Wang, W.Q.; Song, S.G.; Liu, X.M. Long Noncoding RNA-Sox2OT Knockdown Alleviates Diabetes Mellitus-Induced Retinal Ganglion Cell (RGC) injury. Cell. Mol Neurobiol. 2017, 37, 361–369. [Google Scholar] [CrossRef] [PubMed]
- Sanchez, Y.; Huarte, M. Long non-coding RNAs: Challenges for diagnosis and therapies. Nucleic Acid Ther. 2013, 23, 15–20. [Google Scholar] [CrossRef] [PubMed]
- Li, C.H.; Chen, Y. Targeting long non-coding RNAs in cancers: progress and prospects. Int. J. Biochem. Cell Biol. 2013, 45, 1895–1910. [Google Scholar] [CrossRef] [PubMed]
- Ozcan, G.; Ozpolat, B.; Coleman, R.L.; Sood, A.K.; Lopez-Berestein, G. Preclinical and clinical development of siRNA-based therapeutics. Adv. Drug Deliv. Rev. 2015, 87, 108–119. [Google Scholar] [CrossRef] [PubMed]
- Seth, P.P.; Siwkowski, A.; Allerson, C.R.; Vasquez, G.; Lee, S.; Prakash, T.P.; Wancewicz, E.V.; Witchell, D.; Swayze, E.E. Short antisense oligonucleotides with novel 2’-4’ conformationaly restricted nucleoside analogues show improved potency without increased toxicity in animals. J. Med. Chem. 2009, 52, 10–13. [Google Scholar] [CrossRef] [PubMed]
- Ren, S.; Liu, Y.; Xu, W.; Sun, Y.; Lu, J.; Wang, F.; Wei, M.; Shen, J.; Hou, J.; Gao, X.; et al. Long noncoding RNA MALAT-1 is a new potential therapeutic target for castration resistant prostate cancer. J. Urol. 2013, 190, 2278–2287. [Google Scholar] [CrossRef] [PubMed]
- Gutschner, T.; Hammerle, M.; Eissmann, M.; Hsu, J.; Kim, Y.; Hung, G.; Revenko, A.; Arun, G.; Stentrup, M.; Gross, M.; et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 2013, 73, 1180–1189. [Google Scholar] [CrossRef] [PubMed]
- Michalik, K.M.; You, X.; Manavski, Y.; Doddaballapur, A.; Zornig, M.; Braun, T.; John, D.; Ponomareva, Y.; Chen, W.; Uchida, S.; et al. Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ. Res. 2014, 114, 1389–1397. [Google Scholar] [CrossRef] [PubMed]
- Tsai, M.C.; Spitale, R.C.; Chang, H.Y. Long intergenic noncoding RNAs: New links in cancer progression. Cancer Res. 2011, 71, 3–7. [Google Scholar] [CrossRef] [PubMed]
- Wang, F.; Ren, S.; Chen, R.; Lu, J.; Shi, X.; Zhu, Y.; Zhang, W.; Jing, T.; Zhang, C.; Shen, J.; et al. Development and prospective multicenter evaluation of the long noncoding RNA MALAT-1 as a diagnostic urinary biomarker for prostate cancer. Oncotarget 2014, 5, 11091–11102. [Google Scholar] [CrossRef] [PubMed]
- Carter, G.; Miladinovic, B.; Patel, A.A.; Deland, L.; Mastorides, S.; Patel, N.A. Circulating long noncoding RNA GAS5 levels are correlated to prevalence of type 2 diabetes mellitus. BBA Clin. 2015, 4, 102–107. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Zhao, Z.; Gao, C.; Rao, L.; Hao, P.; Jian, D.; et al. The Diagnostic Value of Whole Blood lncRNA ENST00000550337.1 for Pre-Diabetes and Type 2 Diabetes Mellitus. Exp. Clin. Endocrinol. Diabetes 2017, 125, 377–383. [Google Scholar] [CrossRef] [PubMed]
lncRNA | Name | Phen | Major Findings | Reference |
---|---|---|---|---|
ANRIL | antisense noncoding RNA | T2D | may affect β-cell mass | [49] |
DR | regulates VEGF expression in retina | [50] | ||
βlinc1 | β-cell long intergenic noncoding RNA | T2D | associated with β-cell loss | [51] |
CYP4B1-PS1-001 | cytochrome P450, family 4, subfamily b, polypeptide 1, pseudogene 1 | DKD | may regulate proliferation and fibrosis in mesangial cells | [52] |
E330013P06 (E33) | T2D | promotes macrophage inflammation | [53] | |
ENSMUST-00000147869 | DKD | protects mesangial cells from proliferation and fibrosis | [54] | |
Gm4419 | predicted gene 4419 | DKD | regulates levels of pro-inflammatory cytokines and ECM genes | [55] |
H19 | imprinted maternally expressed transcript | T2D | associated with increased birth weight; higher expression in T2D patients | [56,57] |
HI-LNC901 | T2D | implicated in islet function | [58] | |
Lnc-MGC | lncRNA-megacluster | DKD | affects pro-fibrotic gene expression | [59] |
MALAT1 | metastasis-associated lung adenocarcinoma transcript 1 | DKD | promotes inflammation and hypoxia within the context of diabetes | [60,61] |
DR | associated with markers of visual and retinal vessel function | [62] | ||
MIAT | myocardial infarction associated transcript | DKD | regulates resistance to oxidant exposure | [63] |
DR | attenuates retinal vessel impairment and vascular leakage | [64] | ||
MEG3 | maternally expressed 3 gene | T2D | associated with impaired glucose tolerance, glycogen content, and insulin synthesis and secretion | [65,66] |
DR | modulates angiogenesis by PI3K/Akt | [67] | ||
NEAT1 | nuclear paraspeckle assembly transcript 1 | T2D | regulates mTOR signaling pathway | [68] |
PVT1 | plasmacytoma variant translocation 1 | DKD | regulates ECM components | [69] |
PLUTO | PDX1 associated lncRNA, upregulator of transcription | T2D | regulates PDX1 expression | [70] |
SOX2OT | Sox2 overlapping transcript | DR | mediates glucose-induced retinal injury | [71] |
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Leti, F.; DiStefano, J.K. Long Noncoding RNAs as Diagnostic and Therapeutic Targets in Type 2 Diabetes and Related Complications. Genes 2017, 8, 207. https://doi.org/10.3390/genes8080207
Leti F, DiStefano JK. Long Noncoding RNAs as Diagnostic and Therapeutic Targets in Type 2 Diabetes and Related Complications. Genes. 2017; 8(8):207. https://doi.org/10.3390/genes8080207
Chicago/Turabian StyleLeti, Fatjon, and Johanna K. DiStefano. 2017. "Long Noncoding RNAs as Diagnostic and Therapeutic Targets in Type 2 Diabetes and Related Complications" Genes 8, no. 8: 207. https://doi.org/10.3390/genes8080207