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Published in: BMC Endocrine Disorders 1/2019

Open Access 01-12-2019 | Stroke | Research article

Can MiR-503 be used as a marker in diabetic patients with ischemic stroke?

Authors: Saba Sheikhbahaei, Danesh Manizheh, Saadatnia Mohammad, Tajaddini Mohamad Hasan, Nazemian Saman, Rafiee Laleh, Motieian Mahsa, Amoushahi Khouzani Sanaz, Haghjooy Javanmard Shaghayegh

Published in: BMC Endocrine Disorders | Issue 1/2019

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Abstract

Background

Some microRNAs are involved in diabetes pathology and some are known to have role in stroke. MiR-503 causes endothelial dysfunction in diabetic patients, predisposing to ischemia. There has been no study evaluating Mir-503 level in diabetic patients with or without ischemic stroke.

Methods

We designed a cross-sectional study to assess and compare serum level of MiR-503 in 4 groups of diabetic patients with ischemic stroke (I), non-diabetic patients with stroke (II), diabetic patients (III), and healthy controls (IV) in acute phase and 3 months later.

Results

Our data analysis showed that mean relative expression of MiR-503 in group (I) was significantly higher than 3 other groups (p < 0.05). The level of miR-503 was related to the patients’ fasting blood glucose, Cholesterol level, NIHSS score and acute–phase modified Rankin Scale (mRS) (r = 0.49, p = 0.001, r = 0.5, p = 0.009, r = 0.45, p = 0.009, r = 0.48, p = 0.003, CI = 95%). Relative expression of miR in patients with mRS ≤ 2 (good outcome) was lower than in patients with mRS > 2 (poor outcome) (p = 0.008). After 3 months, level of miR decreased significantly only in group (I) (p = 0.002). Mean relative expression of miR-503 in chronic phase was not significantly different among groups (p-value> 0.05). There was no relation between miRNA level and mRS in chronic phase.

Conclusion

Hyperglycemia and ischemia together raise the level of MiR-503 acutely but it does not remain at high level after 3 months. Although higher miR was related to more disability in acute phase, it does not affect long-term outcome in ischemic patients. As MiR-503 is stable enough in blood it can be used as a potential diagnostic marker of an ischemic stroke in diabetic patient. Its level also is an indicator of stroke severity and patients’ short-term outcome. It is recommended to study whether antagomiR-503 is a new therapeutic agent reducing the severity of and disability due to stroke.
Literature
1.
go back to reference Feigin VL, Lawes CM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. The Lancet Neurology. 2009;8(4):355–69 PubMed PMID: 19233729.PubMedCrossRef Feigin VL, Lawes CM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. The Lancet Neurology. 2009;8(4):355–69 PubMed PMID: 19233729.PubMedCrossRef
2.
go back to reference Krishnamurthi RV, Feigin VL, Forouzanfar MH, Mensah GA, Connor M, Bennett DA, et al. Global and regional burden of first-ever ischaemic and haemorrhagic stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. The Lancet Global health. 2013;1(5):e259–81 PubMed PMID: 25104492. Pubmed Central PMCID: 4181351.PubMedPubMedCentralCrossRef Krishnamurthi RV, Feigin VL, Forouzanfar MH, Mensah GA, Connor M, Bennett DA, et al. Global and regional burden of first-ever ischaemic and haemorrhagic stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. The Lancet Global health. 2013;1(5):e259–81 PubMed PMID: 25104492. Pubmed Central PMCID: 4181351.PubMedPubMedCentralCrossRef
3.
go back to reference Ferreiro JL, Gomez-Hospital JA, Angiolillo DJ. Platelet abnormalities in diabetes mellitus. Diab Vasc Dis Res. 2010;7(4):251–9 PubMed PMID: 20921090.PubMedCrossRef Ferreiro JL, Gomez-Hospital JA, Angiolillo DJ. Platelet abnormalities in diabetes mellitus. Diab Vasc Dis Res. 2010;7(4):251–9 PubMed PMID: 20921090.PubMedCrossRef
4.
go back to reference Shou J, Zhou L, Zhu S, Zhang X. Diabetes is an independent risk factor for stroke recurrence in stroke patients: a meta-analysis. J Stroke Cerebrovasc Dis. 2015;24(9):1961–8 PubMed PMID: 26166420.PubMedCrossRef Shou J, Zhou L, Zhu S, Zhang X. Diabetes is an independent risk factor for stroke recurrence in stroke patients: a meta-analysis. J Stroke Cerebrovasc Dis. 2015;24(9):1961–8 PubMed PMID: 26166420.PubMedCrossRef
5.
go back to reference Chen R, Ovbiagele B, Feng W. Diabetes and stroke: epidemiology, pathophysiology, pharmaceuticals and outcomes. Am J Med Sci. 2016;351(4):380–6 PubMed PMID: 27079344. Pubmed Central PMCID: 5298897.PubMedPubMedCentralCrossRef Chen R, Ovbiagele B, Feng W. Diabetes and stroke: epidemiology, pathophysiology, pharmaceuticals and outcomes. Am J Med Sci. 2016;351(4):380–6 PubMed PMID: 27079344. Pubmed Central PMCID: 5298897.PubMedPubMedCentralCrossRef
6.
go back to reference Capes SE, Hunt D, Malmberg K, Pathak P, Gerstein HC. Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke. 2001;32(10):2426–32 PubMed PMID: 11588337.PubMedCrossRef Capes SE, Hunt D, Malmberg K, Pathak P, Gerstein HC. Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke. 2001;32(10):2426–32 PubMed PMID: 11588337.PubMedCrossRef
7.
go back to reference Kong YW, Cannell IG, de Moor CH, Hill K, Garside PG, Hamilton TL, et al. The mechanism of micro-RNA-mediated translation repression is determined by the promoter of the target gene. Proc Natl Acad Sci U S A. 2008;105(26):8866–71 PubMed PMID: 18579786. Pubmed Central PMCID: 2449332.PubMedPubMedCentralCrossRef Kong YW, Cannell IG, de Moor CH, Hill K, Garside PG, Hamilton TL, et al. The mechanism of micro-RNA-mediated translation repression is determined by the promoter of the target gene. Proc Natl Acad Sci U S A. 2008;105(26):8866–71 PubMed PMID: 18579786. Pubmed Central PMCID: 2449332.PubMedPubMedCentralCrossRef
8.
go back to reference O'Brien J, Hayder H, Zayed Y, Peng C. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402 Pubmed PMID: 30123182.CrossRef O'Brien J, Hayder H, Zayed Y, Peng C. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402 Pubmed PMID: 30123182.CrossRef
9.
go back to reference Koutsis G, Siasos G, Spengos K. The emerging role of microRNA in stroke. Curr Top Med Chem. 2013;13(13):1573–88 PubMed PMID: 23745809.PubMedCrossRef Koutsis G, Siasos G, Spengos K. The emerging role of microRNA in stroke. Curr Top Med Chem. 2013;13(13):1573–88 PubMed PMID: 23745809.PubMedCrossRef
10.
go back to reference Meng S, Cao JT, Zhang B, Zhou Q, Shen CX, Wang CQ. Downregulation of microRNA-126 in endothelial progenitor cells from diabetes patients, impairs their functional properties, via target gene Spred-1. J Mol Cell Cardiol. 2012;53(1):64–72 PubMed PMID: 22525256.PubMedCrossRef Meng S, Cao JT, Zhang B, Zhou Q, Shen CX, Wang CQ. Downregulation of microRNA-126 in endothelial progenitor cells from diabetes patients, impairs their functional properties, via target gene Spred-1. J Mol Cell Cardiol. 2012;53(1):64–72 PubMed PMID: 22525256.PubMedCrossRef
11.
12.
go back to reference Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab. 2009;29(4):675–87 PubMed PMID: 19142192. Pubmed Central PMCID: 2743462.PubMedPubMedCentralCrossRef Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab. 2009;29(4):675–87 PubMed PMID: 19142192. Pubmed Central PMCID: 2743462.PubMedPubMedCentralCrossRef
13.
go back to reference Yin KJ, Deng Z, Huang H, Hamblin M, Xie C, Zhang J, et al. miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis. 2010;38(1):17–26 PubMed PMID: 20053374. Pubmed Central PMCID: 2837803.PubMedPubMedCentralCrossRef Yin KJ, Deng Z, Huang H, Hamblin M, Xie C, Zhang J, et al. miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis. 2010;38(1):17–26 PubMed PMID: 20053374. Pubmed Central PMCID: 2837803.PubMedPubMedCentralCrossRef
14.
go back to reference Ouyang YB, Lu Y, Yue S, Xu LJ, Xiong XX, White RE, et al. miR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis. 2012;45(1):555–63 PubMed PMID: 21983159. Pubmed Central PMCID: 3251314.PubMedCrossRef Ouyang YB, Lu Y, Yue S, Xu LJ, Xiong XX, White RE, et al. miR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis. 2012;45(1):555–63 PubMed PMID: 21983159. Pubmed Central PMCID: 3251314.PubMedCrossRef
15.
go back to reference Buller B, Liu X, Wang X, Zhang RL, Zhang L, Hozeska-Solgot A, et al. MicroRNA-21 protects neurons from ischemic death. The FEBS journal. 2010;277(20):4299–307 PubMed PMID: 20840605. Pubmed Central PMCID: 2957309.PubMedPubMedCentralCrossRef Buller B, Liu X, Wang X, Zhang RL, Zhang L, Hozeska-Solgot A, et al. MicroRNA-21 protects neurons from ischemic death. The FEBS journal. 2010;277(20):4299–307 PubMed PMID: 20840605. Pubmed Central PMCID: 2957309.PubMedPubMedCentralCrossRef
16.
go back to reference Caporali A, Meloni M, Vollenkle C, Bonci D, Sala-Newby GB, Addis R, et al. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation. 2011;123(3):282–91 PubMed PMID: 21220732.PubMedCrossRef Caporali A, Meloni M, Vollenkle C, Bonci D, Sala-Newby GB, Addis R, et al. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation. 2011;123(3):282–91 PubMed PMID: 21220732.PubMedCrossRef
17.
go back to reference V H. The NIH stroke scale: a window into neurological status. Nursing Spectrum 2011;24(15):44–49. V H. The NIH stroke scale: a window into neurological status. Nursing Spectrum 2011;24(15):44–49.
18.
go back to reference Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke. 1993;24(1):35–41 PubMed PMID: 7678184.PubMedCrossRef Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke. 1993;24(1):35–41 PubMed PMID: 7678184.PubMedCrossRef
19.
go back to reference Stary CM, Xu L, Sun X, Ouyang YB, White RE, Leong J, et al. MicroRNA-200c contributes to injury from transient focal cerebral ischemia by targeting Reelin. Stroke. 2015;46(2):551–6 PubMed PMID: 25604249. Pubmed Central PMCID: 4346276.PubMedPubMedCentralCrossRef Stary CM, Xu L, Sun X, Ouyang YB, White RE, Leong J, et al. MicroRNA-200c contributes to injury from transient focal cerebral ischemia by targeting Reelin. Stroke. 2015;46(2):551–6 PubMed PMID: 25604249. Pubmed Central PMCID: 4346276.PubMedPubMedCentralCrossRef
20.
go back to reference Vinciguerra A, Formisano L, Cerullo P, Guida N, Cuomo O, Esposito A, et al. MicroRNA-103-1 selectively downregulates brain NCX1 and its inhibition by anti-miRNA ameliorates stroke damage and neurological deficits. Mol Ther. 2014;22(10):1829–38 PubMed PMID: 24954474. Pubmed Central PMCID: 4428397.PubMedPubMedCentralCrossRef Vinciguerra A, Formisano L, Cerullo P, Guida N, Cuomo O, Esposito A, et al. MicroRNA-103-1 selectively downregulates brain NCX1 and its inhibition by anti-miRNA ameliorates stroke damage and neurological deficits. Mol Ther. 2014;22(10):1829–38 PubMed PMID: 24954474. Pubmed Central PMCID: 4428397.PubMedPubMedCentralCrossRef
21.
go back to reference Zeng L, He X, Wang Y, Tang Y, Zheng C, Cai H, et al. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Ther. 2014;21(1):37–43 PubMed PMID: 24152581.PubMedCrossRef Zeng L, He X, Wang Y, Tang Y, Zheng C, Cai H, et al. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Ther. 2014;21(1):37–43 PubMed PMID: 24152581.PubMedCrossRef
22.
go back to reference Doeppner TR, Doehring M, Bretschneider E, Zechariah A, Kaltwasser B, Muller B, et al. MicroRNA-124 protects against focal cerebral ischemia via mechanisms involving Usp14-dependent REST degradation. Acta Neuropathol. 2013;126(2):251–65 PubMed PMID: 23754622.PubMedCrossRef Doeppner TR, Doehring M, Bretschneider E, Zechariah A, Kaltwasser B, Muller B, et al. MicroRNA-124 protects against focal cerebral ischemia via mechanisms involving Usp14-dependent REST degradation. Acta Neuropathol. 2013;126(2):251–65 PubMed PMID: 23754622.PubMedCrossRef
23.
go back to reference Hughes JM, Seale JP, Temple DM. Ranitidine does not potentiate mediator release from human lung in vitro. Br J Clin Pharmacol. 1985;19(5):711–2 PubMed PMID: 2408646. Pubmed Central PMCID: 1463835.PubMedPubMedCentralCrossRef Hughes JM, Seale JP, Temple DM. Ranitidine does not potentiate mediator release from human lung in vitro. Br J Clin Pharmacol. 1985;19(5):711–2 PubMed PMID: 2408646. Pubmed Central PMCID: 1463835.PubMedPubMedCentralCrossRef
24.
go back to reference Gan CS, Wang CW, Tan KS. Circulatory microRNA-145 expression is increased in cerebral ischemia. Genet Mol Res. 27(11, 1):147–52 PubMed PMID: 22370881. Gan CS, Wang CW, Tan KS. Circulatory microRNA-145 expression is increased in cerebral ischemia. Genet Mol Res. 27(11, 1):147–52 PubMed PMID: 22370881.
25.
go back to reference Zeng L, Liu J, Wang Y, Wang L, Weng S, Chen S, et al. Cocktail blood biomarkers: prediction of clinical outcomes in patients with acute ischemic stroke. Eur Neurol. 2013;69(2):68–75 PubMed PMID: 23154383.PubMedCrossRef Zeng L, Liu J, Wang Y, Wang L, Weng S, Chen S, et al. Cocktail blood biomarkers: prediction of clinical outcomes in patients with acute ischemic stroke. Eur Neurol. 2013;69(2):68–75 PubMed PMID: 23154383.PubMedCrossRef
26.
go back to reference Zeng L, Liu J, Wang Y, Wang L, Weng S, Tang Y, et al. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Frontiers in bioscience 2011 Jun. 1(3):1265–72 PubMed PMID: 21622133.CrossRef Zeng L, Liu J, Wang Y, Wang L, Weng S, Tang Y, et al. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Frontiers in bioscience 2011 Jun. 1(3):1265–72 PubMed PMID: 21622133.CrossRef
27.
go back to reference Sepramaniam S, Tan JR, Tan KS, DeSilva DA, Tavintharan S, Woon FP, et al. Circulating microRNAs as biomarkers of acute stroke. Int J Mol Sci. 2014;15(1):1418–32 PubMed PMID: 24447930. Pubmed Central PMCID: 3907877.PubMedPubMedCentralCrossRef Sepramaniam S, Tan JR, Tan KS, DeSilva DA, Tavintharan S, Woon FP, et al. Circulating microRNAs as biomarkers of acute stroke. Int J Mol Sci. 2014;15(1):1418–32 PubMed PMID: 24447930. Pubmed Central PMCID: 3907877.PubMedPubMedCentralCrossRef
28.
go back to reference Tan KS, Armugam A, Sepramaniam S, Lim KY, Setyowati KD, Wang CW, et al. Expression profile of MicroRNAs in young stroke patients. PLoS One 2009;4(11):e7689. PubMed PMID: 19888324. Pubmed Central PMCID: 2765616.PubMedPubMedCentralCrossRef Tan KS, Armugam A, Sepramaniam S, Lim KY, Setyowati KD, Wang CW, et al. Expression profile of MicroRNAs in young stroke patients. PLoS One 2009;4(11):e7689. PubMed PMID: 19888324. Pubmed Central PMCID: 2765616.PubMedPubMedCentralCrossRef
29.
go back to reference Chen J, Yang T, Yu H, Sun K, Shi Y, Song W, et al. A functional variant in the 3′-UTR of angiopoietin-1 might reduce stroke risk by interfering with the binding efficiency of microRNA 211. Hum Mol Genet. 2010;19(12):2524–33 PubMed PMID: 20378606.PubMedCrossRef Chen J, Yang T, Yu H, Sun K, Shi Y, Song W, et al. A functional variant in the 3′-UTR of angiopoietin-1 might reduce stroke risk by interfering with the binding efficiency of microRNA 211. Hum Mol Genet. 2010;19(12):2524–33 PubMed PMID: 20378606.PubMedCrossRef
30.
go back to reference Vemuganti R. All's well that transcribes well: non-coding RNAs and post-stroke brain damage. Neurochem Int. 2013;63(5):438–49 PubMed PMID: 23954844. Pubmed Central PMCID: 3805745.PubMedPubMedCentralCrossRef Vemuganti R. All's well that transcribes well: non-coding RNAs and post-stroke brain damage. Neurochem Int. 2013;63(5):438–49 PubMed PMID: 23954844. Pubmed Central PMCID: 3805745.PubMedPubMedCentralCrossRef
31.
go back to reference Rubattu S, Stanzione R, Bianchi F, Cotugno M, Forte M, Della Ragione F, et al. Reduced brain UCP2 expression mediated by microRNA-503 contributes to increased stroke susceptibility in the high-salt fed stroke-prone spontaneously hypertensive rat. Cell Death Dis. 2017;8(6):e2891 PubMed PMID: 28640254. Pubmed Central PMCID: 5520932.PubMedPubMedCentralCrossRef Rubattu S, Stanzione R, Bianchi F, Cotugno M, Forte M, Della Ragione F, et al. Reduced brain UCP2 expression mediated by microRNA-503 contributes to increased stroke susceptibility in the high-salt fed stroke-prone spontaneously hypertensive rat. Cell Death Dis. 2017;8(6):e2891 PubMed PMID: 28640254. Pubmed Central PMCID: 5520932.PubMedPubMedCentralCrossRef
32.
go back to reference Caporali A, Emanueli C. MicroRNA-503 and the extended microRNA-16 family in angiogenesis. Trends in cardiovascular medicine. 2011;21(6):162–6 PubMed PMID: 22814423. Pubmed Central PMCID: 3407871.PubMedPubMedCentralCrossRef Caporali A, Emanueli C. MicroRNA-503 and the extended microRNA-16 family in angiogenesis. Trends in cardiovascular medicine. 2011;21(6):162–6 PubMed PMID: 22814423. Pubmed Central PMCID: 3407871.PubMedPubMedCentralCrossRef
33.
go back to reference Llobet-Navas D, Rodriguez-Barrueco R, de la Iglesia-Vicente J, Olivan M, Castro V, Saucedo-Cuevas L, et al. The microRNA 424/503 cluster reduces CDC25A expression during cell cycle arrest imposed by transforming growth factor beta in mammary epithelial cells. Mol Cell Biol. 2014;34(23):4216–31 PubMed PMID: 25266660. Pubmed Central PMCID: 4248740.PubMedPubMedCentralCrossRef Llobet-Navas D, Rodriguez-Barrueco R, de la Iglesia-Vicente J, Olivan M, Castro V, Saucedo-Cuevas L, et al. The microRNA 424/503 cluster reduces CDC25A expression during cell cycle arrest imposed by transforming growth factor beta in mammary epithelial cells. Mol Cell Biol. 2014;34(23):4216–31 PubMed PMID: 25266660. Pubmed Central PMCID: 4248740.PubMedPubMedCentralCrossRef
34.
go back to reference Chen Y, Song Y, Huang J, Qu M, Zhang Y, Geng J, et al. Increased circulating Exosomal miRNA-223 is associated with acute ischemic stroke. Front Neurol. 2017;8:57 PubMed PMID: 28289400. Pubmed Central PMCID: 5326773.PubMedPubMedCentralCrossRef Chen Y, Song Y, Huang J, Qu M, Zhang Y, Geng J, et al. Increased circulating Exosomal miRNA-223 is associated with acute ischemic stroke. Front Neurol. 2017;8:57 PubMed PMID: 28289400. Pubmed Central PMCID: 5326773.PubMedPubMedCentralCrossRef
35.
go back to reference Caporali A, Meloni M, Nailor A, Mitic T, Shantikumar S, Riu F, et al. p75(NTR)-dependent activation of NF-kappaB regulates microRNA-503 transcription and pericyte-endothelial crosstalk in diabetes after limb ischaemia. Nat Commun. 2015;6:8024 PubMed PMID: 26268439. Pubmed Central PMCID: 4538859.PubMedPubMedCentralCrossRef Caporali A, Meloni M, Nailor A, Mitic T, Shantikumar S, Riu F, et al. p75(NTR)-dependent activation of NF-kappaB regulates microRNA-503 transcription and pericyte-endothelial crosstalk in diabetes after limb ischaemia. Nat Commun. 2015;6:8024 PubMed PMID: 26268439. Pubmed Central PMCID: 4538859.PubMedPubMedCentralCrossRef
36.
go back to reference Chang SW, Yue J, Wang BC, Zhang XL. miR-503 inhibits cell proliferation and induces apoptosis in colorectal cancer cells by targeting E2F3, 12853. Int J Clin Exp Pathol. 2015;8(10):–60 PubMed PMID: 26722476. Pubmed Central PMCID: 4680421. Chang SW, Yue J, Wang BC, Zhang XL. miR-503 inhibits cell proliferation and induces apoptosis in colorectal cancer cells by targeting E2F3, 12853. Int J Clin Exp Pathol. 2015;8(10):–60 PubMed PMID: 26722476. Pubmed Central PMCID: 4680421.
37.
go back to reference Zhu X, Zhang C, Fan Q, Liu X, Yang G, Jiang Y, et al. Inhibiting MicroRNA-503 and MicroRNA-181d with Losartan Ameliorates Diabetic Nephropathy in KKAy Mice. Med Sci Monit. 2016;22:3902–9 PubMed PMID: 27770539. Pubmed Central PMCID: 5081237.PubMedPubMedCentralCrossRef Zhu X, Zhang C, Fan Q, Liu X, Yang G, Jiang Y, et al. Inhibiting MicroRNA-503 and MicroRNA-181d with Losartan Ameliorates Diabetic Nephropathy in KKAy Mice. Med Sci Monit. 2016;22:3902–9 PubMed PMID: 27770539. Pubmed Central PMCID: 5081237.PubMedPubMedCentralCrossRef
38.
go back to reference Kavurma MM, Khachigian LM. Sp1 inhibits proliferation and induces apoptosis in vascular smooth muscle cells by repressing p21WAF1/Cip1 transcription and cyclin D1-Cdk4-p21WAF1/Cip1 complex formation. J Biol Chem. 2003;278(35):32537–43 PubMed PMID: 12796485.PubMedCrossRef Kavurma MM, Khachigian LM. Sp1 inhibits proliferation and induces apoptosis in vascular smooth muscle cells by repressing p21WAF1/Cip1 transcription and cyclin D1-Cdk4-p21WAF1/Cip1 complex formation. J Biol Chem. 2003;278(35):32537–43 PubMed PMID: 12796485.PubMedCrossRef
39.
go back to reference Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993;75(4):805–16 PubMed PMID: 8242751.PubMedCrossRef Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993;75(4):805–16 PubMed PMID: 8242751.PubMedCrossRef
40.
go back to reference Duan X, Zhan Q, Song B, Zeng S, Zhou J, Long Y, et al. Detection of platelet microRNA expression in patients with diabetes mellitus with or without ischemic stroke. J Diabetes Complicat. 2014;28(5):705–10 PubMed PMID: 24908639.PubMedCrossRef Duan X, Zhan Q, Song B, Zeng S, Zhou J, Long Y, et al. Detection of platelet microRNA expression in patients with diabetes mellitus with or without ischemic stroke. J Diabetes Complicat. 2014;28(5):705–10 PubMed PMID: 24908639.PubMedCrossRef
41.
go back to reference Yang S, Zhao J, Chen Y, Lei M. Biomarkers associated with ischemic stroke in diabetes mellitus patients. Cardiovasc Toxicol. 2016;16(3):213–22 PubMed PMID: 26175178.PubMedCrossRef Yang S, Zhao J, Chen Y, Lei M. Biomarkers associated with ischemic stroke in diabetes mellitus patients. Cardiovasc Toxicol. 2016;16(3):213–22 PubMed PMID: 26175178.PubMedCrossRef
42.
go back to reference Chen L, Okeke E, Ayalew D, Wang D, Shahid L, Dokun AO. Modulation of miR29a improves impaired post-ischemic angiogenesis in hyperglycemia. Exp Biol Med. 2017;242(14):1432–43 PubMed PMID: 28637396. Pubmed Central PMCID: 5544167.CrossRef Chen L, Okeke E, Ayalew D, Wang D, Shahid L, Dokun AO. Modulation of miR29a improves impaired post-ischemic angiogenesis in hyperglycemia. Exp Biol Med. 2017;242(14):1432–43 PubMed PMID: 28637396. Pubmed Central PMCID: 5544167.CrossRef
43.
go back to reference Tan JR, Tan KS, Koo YX, Yong FL, Wang CW, Armugam A, et al. Blood microRNAs in low or no risk ischemic stroke patients. Int J Mol Sci. 2013;14(1):2072–84 PubMed PMID: 23340648. Pubmed Central PMCID: 3565366.PubMedPubMedCentralCrossRef Tan JR, Tan KS, Koo YX, Yong FL, Wang CW, Armugam A, et al. Blood microRNAs in low or no risk ischemic stroke patients. Int J Mol Sci. 2013;14(1):2072–84 PubMed PMID: 23340648. Pubmed Central PMCID: 3565366.PubMedPubMedCentralCrossRef
Metadata
Title
Can MiR-503 be used as a marker in diabetic patients with ischemic stroke?
Authors
Saba Sheikhbahaei
Danesh Manizheh
Saadatnia Mohammad
Tajaddini Mohamad Hasan
Nazemian Saman
Rafiee Laleh
Motieian Mahsa
Amoushahi Khouzani Sanaz
Haghjooy Javanmard Shaghayegh
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2019
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-019-0371-6

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