Skip to main content
Top
Published in: Clinical Rheumatology 12/2018

01-12-2018 | Original Article

Role of long non-coding RNAs expression (ANRIL, NOS3-AS, and APOA1-AS) in development of atherosclerosis in Egyptian systemic lupus erythematosus patients

Authors: Mai A. Abd-Elmawla, Mary Wadie Fawzy, Sherine M. Rizk, Amira A. Shaheen

Published in: Clinical Rheumatology | Issue 12/2018

Login to get access

Abstract

To quantify the expression level of three lncRNAs which are known to be relevant to atherosclerosis (ANRIL, NOS3-AS, and APOA1-AS) in SLE patients and to assess their relationship with atherogenic and inflammatory biomarkers. The circulating levels of these lncRNAs were assessed using RT-PCR, in addition to measurement of E-selectin, V-CAM1, oxidized low-density lipoprotein (oxLDL), total nitric oxide (NOx), and lipid profile in 65 SLE patients (35 atherosclerotic and 30 non-atherosclerotic) and 35 healthy subjects. The expression levels of these lncRNAs were higher in SLE patients than in healthy controls. Importantly, a higher overexpression of these lncRNAs was noticed in atherosclerotic SLE patients than in non-atherosclerotic ones. In atherosclerotic SLE patients, level of ANRIL was positively associated with menopause, SLE duration, SLEDAI, and SLICC and negatively correlated with C3. Moreover, NOS3-AS expression was negatively correlated with total NOx level and HDL, while it was positively correlated with TC, LDL-C, hypertension, metabolic syndrome, obesity and dyslipidemia, CIMT, VCAM-1, E-selectin, oxLDL, SLEDAI, and SLICC. With respect to APOA1-AS, its expression was negatively correlated with HDL-C, whereas it was positively correlated with TC, LDL-C, hypertension, dyslipidemia, obesity, metabolic syndrome, menopause, CIMT, RI, V-CAM1, E-selectin, oxLDL, and SLICC. ANRIL, NOS3-AS, and APOA1-AS could be used as predictive biomarkers for atherosclerosis in SLE. Multivariate analyses identified these lncRNAs as independent predictors for atherosclerosis in SLE. These lncRNAs play a pivotal role in development of atherosclerosis via their significant repercussions atherogenic and inflammatory indices.
Literature
1.
go back to reference Ward MM (1999) Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 42:338–346CrossRef Ward MM (1999) Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 42:338–346CrossRef
2.
go back to reference Barsalou J, Bradley T, Tyrrell P, Slorach C, Ng L, Levy D, Silverman E (2016) Impact of disease duration on vascular surrogates of early atherosclerosis in childhood-onset systemic lupus erythematosus. Arthritis Rheum 68(1):237–246CrossRef Barsalou J, Bradley T, Tyrrell P, Slorach C, Ng L, Levy D, Silverman E (2016) Impact of disease duration on vascular surrogates of early atherosclerosis in childhood-onset systemic lupus erythematosus. Arthritis Rheum 68(1):237–246CrossRef
4.
go back to reference Gustafsson JT, Svenungsson E (2014) Definitions of and contributions to cardiovascular disease in systemic lupus erythematosus. Autoimmunity 47(2):67–76CrossRef Gustafsson JT, Svenungsson E (2014) Definitions of and contributions to cardiovascular disease in systemic lupus erythematosus. Autoimmunity 47(2):67–76CrossRef
5.
go back to reference Relle M, Foehr B, Schwarting A (2015) Epigenetic aspects of systemic lupus erythematosus. Rheumatol Ther 2:33–46CrossRef Relle M, Foehr B, Schwarting A (2015) Epigenetic aspects of systemic lupus erythematosus. Rheumatol Ther 2:33–46CrossRef
6.
go back to reference Shirodkar AV, Marsden PA (2011) Epigenetics in cardiovascular disease. Curr Opin Cardiol 26:209–215CrossRef Shirodkar AV, Marsden PA (2011) Epigenetics in cardiovascular disease. Curr Opin Cardiol 26:209–215CrossRef
7.
go back to reference Congrains A, Kamide K, Oguro R (2012) Genetic variants at the 9p21 locus contribute to atherosclerosis through modulation of ANRIL and CDKN2A/B. Atherosclerosis 220:449–455CrossRef Congrains A, Kamide K, Oguro R (2012) Genetic variants at the 9p21 locus contribute to atherosclerosis through modulation of ANRIL and CDKN2A/B. Atherosclerosis 220:449–455CrossRef
8.
go back to reference Tsai PC, Liao YC, Lin TH, Hsi E, Yang YH, Juo SH (2012) Additive effect of ANRIL and BRAP polymorphisms on ankle-brachial index in a Taiwanese population. Circ J 76:446–452CrossRef Tsai PC, Liao YC, Lin TH, Hsi E, Yang YH, Juo SH (2012) Additive effect of ANRIL and BRAP polymorphisms on ankle-brachial index in a Taiwanese population. Circ J 76:446–452CrossRef
9.
go back to reference Robb GB, Carson AR, Tai SC, Fish JE, Singh S, Yamada T, Scherer SW, Nakabayashi K, Marsden PA (2004) Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J Biol Chem 279(36):37982–37996CrossRef Robb GB, Carson AR, Tai SC, Fish JE, Singh S, Yamada T, Scherer SW, Nakabayashi K, Marsden PA (2004) Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J Biol Chem 279(36):37982–37996CrossRef
10.
go back to reference Fish JE, Matouk CC, Yeboah E, Bevan SC, Khan M, Patil K, Ohh M, Marsden PA (2007) Hypoxia-inducible expression of a natural cis-antisense transcript inhibits endothelial nitric-oxide synthase. J Biol Chem 282(21):15652–15666CrossRef Fish JE, Matouk CC, Yeboah E, Bevan SC, Khan M, Patil K, Ohh M, Marsden PA (2007) Hypoxia-inducible expression of a natural cis-antisense transcript inhibits endothelial nitric-oxide synthase. J Biol Chem 282(21):15652–15666CrossRef
11.
go back to reference Halley P, Kadakkuzha BM, Faghihi MA, Magistri M, Zeier Z, Khorkova O, Coito O, Hsiao J, Lawrence M, Wahlestedt C (2014) Regulation of the apolipoprotein gene cluster by a long noncoding RNA. Cell Rep 6:222–230CrossRef Halley P, Kadakkuzha BM, Faghihi MA, Magistri M, Zeier Z, Khorkova O, Coito O, Hsiao J, Lawrence M, Wahlestedt C (2014) Regulation of the apolipoprotein gene cluster by a long noncoding RNA. Cell Rep 6:222–230CrossRef
12.
go back to reference Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277CrossRef Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277CrossRef
13.
go back to reference Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT (2010) Bingham 3rd CO. rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62:2569–2581CrossRef Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT (2010) Bingham 3rd CO. rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62:2569–2581CrossRef
14.
go back to reference Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39:363–369CrossRef Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39:363–369CrossRef
15.
go back to reference National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) (2002) Circulation 106(25):3143–3421CrossRef National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) (2002) Circulation 106(25):3143–3421CrossRef
16.
go back to reference Kishikawa K, Kamouchi M, Okada Y, Inoue T, Ibayashi S, Iida M (2004) Transoral carotid ultrasonography as a diagnostic aid in patients with severe carotid stenosis. Cerebrovasc Dis 17:106–111CrossRef Kishikawa K, Kamouchi M, Okada Y, Inoue T, Ibayashi S, Iida M (2004) Transoral carotid ultrasonography as a diagnostic aid in patients with severe carotid stenosis. Cerebrovasc Dis 17:106–111CrossRef
17.
go back to reference Allain CC, Poon LS, Chan CS, Richmond W, Fu PC (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20:470–475PubMed Allain CC, Poon LS, Chan CS, Richmond W, Fu PC (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20:470–475PubMed
18.
go back to reference Lopes-virella ME, Stone P, Elliss S (1977) Cholesterol determination in high density lipoprotein separated by three different methods. Clin Chem 23:882–884PubMed Lopes-virella ME, Stone P, Elliss S (1977) Cholesterol determination in high density lipoprotein separated by three different methods. Clin Chem 23:882–884PubMed
19.
go back to reference Neri BP, Frings CS (1973) Improved method for determination of triglycerides in serum. Clin Chem 19(10):1201–1202PubMed Neri BP, Frings CS (1973) Improved method for determination of triglycerides in serum. Clin Chem 19(10):1201–1202PubMed
20.
go back to reference Friedewald WT, Levy RL, Fredrickson DS (1972) Estimation of the concentration of low density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem 18:499–502 Friedewald WT, Levy RL, Fredrickson DS (1972) Estimation of the concentration of low density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem 18:499–502
21.
go back to reference Vausort M, Wagner DR, Devaux L (2014) Long noncoding RNAs in patients with acute myocardial infarction. Circ Res 115:668–677CrossRef Vausort M, Wagner DR, Devaux L (2014) Long noncoding RNAs in patients with acute myocardial infarction. Circ Res 115:668–677CrossRef
23.
go back to reference Ho CY, Wong CK, Li EK, Tam LS, Lam CW (2003) Elevated plasma concentrations of nitric oxide, soluble thrombomodulin and soluble vascular cell adhesion molecule-1 in patients with systemic lupus erythematosus. Rheumatology (Oxford) 42:117–122CrossRef Ho CY, Wong CK, Li EK, Tam LS, Lam CW (2003) Elevated plasma concentrations of nitric oxide, soluble thrombomodulin and soluble vascular cell adhesion molecule-1 in patients with systemic lupus erythematosus. Rheumatology (Oxford) 42:117–122CrossRef
24.
go back to reference Ahanchi SS, Tsihlis ND, Kibbe MR (2007) The role of nitric oxide in the pathophysiology of intimal hyperplasia. Vasc Surg 45:64–73CrossRef Ahanchi SS, Tsihlis ND, Kibbe MR (2007) The role of nitric oxide in the pathophysiology of intimal hyperplasia. Vasc Surg 45:64–73CrossRef
25.
go back to reference Perl A, Nagy G, Gergely P, Puskas F, Qian Y, Banki K (2004) Apoptosis and mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol Med 102:87–114PubMed Perl A, Nagy G, Gergely P, Puskas F, Qian Y, Banki K (2004) Apoptosis and mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol Med 102:87–114PubMed
26.
go back to reference Li W, Mital S, Ojaimi C, Csiszar A, Kaley G, Hintze TH (2004) Premature deathand age-related cardiac dysfunction in male eNOS-knockout mice. J Mol Cell Cardiol 37(3):671–680CrossRef Li W, Mital S, Ojaimi C, Csiszar A, Kaley G, Hintze TH (2004) Premature deathand age-related cardiac dysfunction in male eNOS-knockout mice. J Mol Cell Cardiol 37(3):671–680CrossRef
28.
go back to reference Proudfoot JM, Barden AE, Loke WM, Croft KD, Puddey IB, Mori TA (2009) HDL is the major lipoprotein carrier of plasma F2-isoprostanes. J Lipid Res 50:716–722CrossRef Proudfoot JM, Barden AE, Loke WM, Croft KD, Puddey IB, Mori TA (2009) HDL is the major lipoprotein carrier of plasma F2-isoprostanes. J Lipid Res 50:716–722CrossRef
29.
go back to reference Baker PW, Rye KA, Gamble JR, Vadas MA, Barter PJ (2000) Phospholipid composition of reconstituted high density lipoproteins influences their ability to inhibit endothelial cell adhesion molecule expression. J Lipid Res 41:1261–1267PubMed Baker PW, Rye KA, Gamble JR, Vadas MA, Barter PJ (2000) Phospholipid composition of reconstituted high density lipoproteins influences their ability to inhibit endothelial cell adhesion molecule expression. J Lipid Res 41:1261–1267PubMed
Metadata
Title
Role of long non-coding RNAs expression (ANRIL, NOS3-AS, and APOA1-AS) in development of atherosclerosis in Egyptian systemic lupus erythematosus patients
Authors
Mai A. Abd-Elmawla
Mary Wadie Fawzy
Sherine M. Rizk
Amira A. Shaheen
Publication date
01-12-2018
Publisher
Springer London
Published in
Clinical Rheumatology / Issue 12/2018
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-018-4269-x

Other articles of this Issue 12/2018

Clinical Rheumatology 12/2018 Go to the issue