Skip to main content
Top
Published in: Archives of Virology 9/2017

01-09-2017 | Original Article

miR-138 promotes migration and tube formation of human cytomegalovirus-infected endothelial cells through the SIRT1/p-STAT3 pathway

Authors: Shanchao Zhang, Lei Liu, Ruijin Wang, Houzhen Tuo, Yanjun Guo, Li Yi, Dexin Wang, Jiawei Wang

Published in: Archives of Virology | Issue 9/2017

Login to get access

Abstract

Human cytomegalovirus (HCMV) has been reported to be linked to vascular disease through the induction of neovessel formation. We have previously reported that microRNA (miR)-217 and miR-199a-5p enhance endothelial angiogenesis via inhibition of sirtuin 1 (SIRT1) in HCMV-infected human umbilical vein endothelial cells (HUVECs). Here, we found that miR-138 also suppressed the expression of the SIRT1 protein and stimulated phosphorylation of signal transducer and activator of transcription 3 (p-STAT3). Moreover, the regulation of p-STAT3 expression mediated by SIRT1 was found to promote HCMV-induced angiogenesis. These findings revealed that miR-138 might promote angiogenesis of HCMV-infected HUVECs by activating the SIRT1-mediated p-STAT3 pathway, and this could provide novel insights into HCMV-induced angiogenesis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Britt W (2008) Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 325:417–470PubMed Britt W (2008) Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 325:417–470PubMed
2.
go back to reference Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA (2008) Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325:397–415PubMedPubMedCentral Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA (2008) Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325:397–415PubMedPubMedCentral
3.
go back to reference Bentz GL, Yurochko AD (2008) Human CMV infection of endothelial cells induces an angiogenic response through viral binding to EGF receptor and beta1 and beta3 integrins. Proc Natl Acad Sci USA 105:5531–5536CrossRefPubMedPubMedCentral Bentz GL, Yurochko AD (2008) Human CMV infection of endothelial cells induces an angiogenic response through viral binding to EGF receptor and beta1 and beta3 integrins. Proc Natl Acad Sci USA 105:5531–5536CrossRefPubMedPubMedCentral
4.
go back to reference Revello MG, Gerna G (2010) Human cytomegalovirus tropism for endothelial/epithelial cells: scientific background and clinical implications. Rev Med Virol 20:136–155CrossRefPubMed Revello MG, Gerna G (2010) Human cytomegalovirus tropism for endothelial/epithelial cells: scientific background and clinical implications. Rev Med Virol 20:136–155CrossRefPubMed
5.
go back to reference Zhang S, Liu L, Wang R, Tuo H, Guo Y, Yi L, Wang D, Wang J (2013) MicroRNA-217 promotes angiogenesis of human cytomegalovirus-infected endothelial cells through downregulation of SIRT1 and FOXO3A. PLoS One 8:e83620CrossRefPubMedPubMedCentral Zhang S, Liu L, Wang R, Tuo H, Guo Y, Yi L, Wang D, Wang J (2013) MicroRNA-217 promotes angiogenesis of human cytomegalovirus-infected endothelial cells through downregulation of SIRT1 and FOXO3A. PLoS One 8:e83620CrossRefPubMedPubMedCentral
6.
go back to reference Zhang S, Liu L, Wang R, Tuo H, Guo Y, Yi L, Wang J, Wang D (2013) MiR-199a-5p promotes migration and tube formation of human cytomegalovirus-infected endothelial cells through downregulation of SIRT1 and eNOS. Arch Virol 158:2443–2452CrossRefPubMed Zhang S, Liu L, Wang R, Tuo H, Guo Y, Yi L, Wang J, Wang D (2013) MiR-199a-5p promotes migration and tube formation of human cytomegalovirus-infected endothelial cells through downregulation of SIRT1 and eNOS. Arch Virol 158:2443–2452CrossRefPubMed
7.
go back to reference Zhang E, Guo Q, Gao H, Xu R, Teng S, Wu Y (2015) Metformin and Resveratrol Inhibited High Glucose-Induced Metabolic Memory of Endothelial Senescence through SIRT1/p300/p53/p21 Pathway. PLoS One 10:e143814 Zhang E, Guo Q, Gao H, Xu R, Teng S, Wu Y (2015) Metformin and Resveratrol Inhibited High Glucose-Induced Metabolic Memory of Endothelial Senescence through SIRT1/p300/p53/p21 Pathway. PLoS One 10:e143814
8.
go back to reference Sen A, Ren S, Lerchenmuller C, Sun J, Weiss N, Most P, Peppel K (2013) MicroRNA-138 regulates hypoxia-induced endothelial cell dysfunction by targeting S100A1. PLoS One 8:e78684CrossRefPubMedPubMedCentral Sen A, Ren S, Lerchenmuller C, Sun J, Weiss N, Most P, Peppel K (2013) MicroRNA-138 regulates hypoxia-induced endothelial cell dysfunction by targeting S100A1. PLoS One 8:e78684CrossRefPubMedPubMedCentral
9.
go back to reference Xu J, Li L, Yun HF, Han YS (2015) MiR-138 promotes smooth muscle cells proliferation and migration in db/db mice through down-regulation of SIRT1. Biochem Biophys Res Commun 463:1159–1164CrossRefPubMed Xu J, Li L, Yun HF, Han YS (2015) MiR-138 promotes smooth muscle cells proliferation and migration in db/db mice through down-regulation of SIRT1. Biochem Biophys Res Commun 463:1159–1164CrossRefPubMed
10.
go back to reference Xing J, Wang S, Lin F, Pan W, Hu CD, Zheng C (2011) Comprehensive characterization of interaction complexes of herpes simplex virus type 1 ICP22, UL3, UL4, and UL20.5. J Virol 85:1881–1886CrossRefPubMed Xing J, Wang S, Lin F, Pan W, Hu CD, Zheng C (2011) Comprehensive characterization of interaction complexes of herpes simplex virus type 1 ICP22, UL3, UL4, and UL20.5. J Virol 85:1881–1886CrossRefPubMed
11.
go back to reference Liu CM, Wang RY, Saijilafu Jiao ZX, Zhang BY, Zhou FQ (2013) MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev 27:1473–1483CrossRefPubMedPubMedCentral Liu CM, Wang RY, Saijilafu Jiao ZX, Zhang BY, Zhou FQ (2013) MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev 27:1473–1483CrossRefPubMedPubMedCentral
12.
go back to reference Conti V, Forte M, Corbi G, Russomanno G, Formisano L, Landolfi A, Izzo V, Filippell A, Vecchione C, Carrizzo A (2017) Sirtuins: a possible clinical implication in cardio and cerebrovascular systems. Curr Drug Targets 18:473–484CrossRefPubMed Conti V, Forte M, Corbi G, Russomanno G, Formisano L, Landolfi A, Izzo V, Filippell A, Vecchione C, Carrizzo A (2017) Sirtuins: a possible clinical implication in cardio and cerebrovascular systems. Curr Drug Targets 18:473–484CrossRefPubMed
13.
go back to reference Soroceanu L, Matlaf L, Bezrookove V, Harkins L, Martinez R, Greene M, Soteropoulos P, Cobbs CS (2011) Human cytomegalovirus US28 found in glioblastoma promotes an invasive and angiogenic phenotype. Cancer Res 71:6643–6653CrossRefPubMedPubMedCentral Soroceanu L, Matlaf L, Bezrookove V, Harkins L, Martinez R, Greene M, Soteropoulos P, Cobbs CS (2011) Human cytomegalovirus US28 found in glioblastoma promotes an invasive and angiogenic phenotype. Cancer Res 71:6643–6653CrossRefPubMedPubMedCentral
14.
go back to reference Li Y, Zhu W, Li J, Liu M, Wei M (2013) Resveratrol suppresses the STAT3 signaling pathway and inhibits proliferation of high glucose-exposed HepG2 cells partly through SIRT1. Oncol Rep 30:2820–2828PubMed Li Y, Zhu W, Li J, Liu M, Wei M (2013) Resveratrol suppresses the STAT3 signaling pathway and inhibits proliferation of high glucose-exposed HepG2 cells partly through SIRT1. Oncol Rep 30:2820–2828PubMed
16.
go back to reference Chen L, Wang J, Wang B, Yang J, Gong Z, Zhao X, Zhang C, Du K (2016) MiR-126 inhibits vascular endothelial cell apoptosis through targeting PI3K/Akt signaling. Ann Hematol 95:365–374CrossRefPubMed Chen L, Wang J, Wang B, Yang J, Gong Z, Zhao X, Zhang C, Du K (2016) MiR-126 inhibits vascular endothelial cell apoptosis through targeting PI3K/Akt signaling. Ann Hematol 95:365–374CrossRefPubMed
17.
go back to reference Climent M, Quintavalle M, Miragoli M, Chen J, Condorelli G, Elia L (2015) TGFbeta triggers miR-143/145 transfer from smooth muscle cells to endothelial cells, thereby modulating vessel stabilization. Circ Res 116:1753–1764CrossRefPubMed Climent M, Quintavalle M, Miragoli M, Chen J, Condorelli G, Elia L (2015) TGFbeta triggers miR-143/145 transfer from smooth muscle cells to endothelial cells, thereby modulating vessel stabilization. Circ Res 116:1753–1764CrossRefPubMed
18.
go back to reference Pankratz F, Bemtgen X, Zeiser R, Leonhardt F, Kreuzaler S, Hilgendorf I, Smolka C, Helbing T, Hoefer I, Esser JS, Kustermann M, Moser M, Bode C, Grundmann S (2015) MicroRNA-155 exerts cell-specific antiangiogenic but proarteriogenic effects during adaptive neovascularization. Circulation 131:1575–1589CrossRefPubMed Pankratz F, Bemtgen X, Zeiser R, Leonhardt F, Kreuzaler S, Hilgendorf I, Smolka C, Helbing T, Hoefer I, Esser JS, Kustermann M, Moser M, Bode C, Grundmann S (2015) MicroRNA-155 exerts cell-specific antiangiogenic but proarteriogenic effects during adaptive neovascularization. Circulation 131:1575–1589CrossRefPubMed
19.
go back to reference Chen HZ, Wang F, Gao P, Pei JF, Liu Y, Xu TT, Tang X, Fu WY, Lu J, Yan YF, Wang XM, Han L, Zhang ZQ, Zhang R, Zou MH, Liu DP (2016) Age-associated sirtuin 1 reduction in vascular smooth muscle links vascular senescence and inflammation to abdominal aortic aneurysm. Circ Res 119:1076–1088CrossRefPubMed Chen HZ, Wang F, Gao P, Pei JF, Liu Y, Xu TT, Tang X, Fu WY, Lu J, Yan YF, Wang XM, Han L, Zhang ZQ, Zhang R, Zou MH, Liu DP (2016) Age-associated sirtuin 1 reduction in vascular smooth muscle links vascular senescence and inflammation to abdominal aortic aneurysm. Circ Res 119:1076–1088CrossRefPubMed
20.
go back to reference Annabi B, Lord-Dufour S, Vezina A, Beliveau R (2012) Resveratrol targeting of carcinogen-induced brain endothelial cell inflammation biomarkers MMP-9 and COX-2 is Sirt1-independent. Drug Target Insights 6:1–11CrossRefPubMedPubMedCentral Annabi B, Lord-Dufour S, Vezina A, Beliveau R (2012) Resveratrol targeting of carcinogen-induced brain endothelial cell inflammation biomarkers MMP-9 and COX-2 is Sirt1-independent. Drug Target Insights 6:1–11CrossRefPubMedPubMedCentral
21.
go back to reference Li Y, Wang P, Yang X, Wang W, Zhang J, He Y, Zhang W, Jing T, Wang B, Lin R (2016) SIRT1 inhibits inflammatory response partly through regulation of NLRP3 inflammasome in vascular endothelial cells. Mol Immunol 77:148–156CrossRefPubMed Li Y, Wang P, Yang X, Wang W, Zhang J, He Y, Zhang W, Jing T, Wang B, Lin R (2016) SIRT1 inhibits inflammatory response partly through regulation of NLRP3 inflammasome in vascular endothelial cells. Mol Immunol 77:148–156CrossRefPubMed
22.
go back to reference Tian Y, Ma J, Wang W, Zhang L, Xu J, Wang K, Li D (2016) Resveratrol supplement inhibited the NF-kappaB inflammation pathway through activating AMPKalpha-SIRT1 pathway in mice with fatty liver. Mol Cell Biochem 422:75–84CrossRefPubMed Tian Y, Ma J, Wang W, Zhang L, Xu J, Wang K, Li D (2016) Resveratrol supplement inhibited the NF-kappaB inflammation pathway through activating AMPKalpha-SIRT1 pathway in mice with fatty liver. Mol Cell Biochem 422:75–84CrossRefPubMed
23.
go back to reference Ye J, Liu Z, Wei J, Lu L, Huang Y, Luo L, Xie H (2013) Protective effect of SIRT1 on toxicity of microglial-derived factors induced by LPS to PC12 cells via the p53-caspase-3-dependent apoptotic pathway. Neurosci Lett 553:72–77CrossRefPubMed Ye J, Liu Z, Wei J, Lu L, Huang Y, Luo L, Xie H (2013) Protective effect of SIRT1 on toxicity of microglial-derived factors induced by LPS to PC12 cells via the p53-caspase-3-dependent apoptotic pathway. Neurosci Lett 553:72–77CrossRefPubMed
24.
go back to reference Salminen A, Kaarniranta K, Kauppinen A (2016) AMPK and HIF signaling pathways regulate both longevity and cancer growth: the good news and the bad news about survival mechanisms. Biogerontology 17:655–680CrossRefPubMed Salminen A, Kaarniranta K, Kauppinen A (2016) AMPK and HIF signaling pathways regulate both longevity and cancer growth: the good news and the bad news about survival mechanisms. Biogerontology 17:655–680CrossRefPubMed
25.
go back to reference Naing Z, Webel R, Hamilton S, Schmeiser C, Scott G, Marschall M, Rawlinson W (2015) Stimulatory effects of human cytomegalovirus tegument protein pp71 lead to increased expression of CCL2 (monocyte chemotactic protein-1) during infection. J Gen Virol 96:1855–1862CrossRefPubMed Naing Z, Webel R, Hamilton S, Schmeiser C, Scott G, Marschall M, Rawlinson W (2015) Stimulatory effects of human cytomegalovirus tegument protein pp71 lead to increased expression of CCL2 (monocyte chemotactic protein-1) during infection. J Gen Virol 96:1855–1862CrossRefPubMed
26.
go back to reference Xing Y, Wang Y, Wang S, Wang X, Fan D, Zhou D, An J (2016) Human cytomegalovirus infection contributes to glioma disease progression via upregulating endocan expression. Transl Res 177:113–126CrossRefPubMed Xing Y, Wang Y, Wang S, Wang X, Fan D, Zhou D, An J (2016) Human cytomegalovirus infection contributes to glioma disease progression via upregulating endocan expression. Transl Res 177:113–126CrossRefPubMed
27.
go back to reference Landais I, Pelton C, Streblow D, DeFilippis V, McWeeney S, Nelson JA (2015) Human cytomegalovirus miR-UL112-3p targets TLR2 and modulates the TLR2/IRAK1/NFkappaB signaling pathway. PLoS Pathog 11:e1004881CrossRefPubMedPubMedCentral Landais I, Pelton C, Streblow D, DeFilippis V, McWeeney S, Nelson JA (2015) Human cytomegalovirus miR-UL112-3p targets TLR2 and modulates the TLR2/IRAK1/NFkappaB signaling pathway. PLoS Pathog 11:e1004881CrossRefPubMedPubMedCentral
28.
go back to reference Potente M, Ghaeni L, Baldessari D, Mostoslavsky R, Rossig L, Dequiedt F, Haendeler J, Mione M, Dejana E, Alt FW, Zeiher AM, Dimmeler S (2007) SIRT1 controls endothelial angiogenic functions during vascular growth. Genes Dev 21:2644–2658CrossRefPubMedPubMedCentral Potente M, Ghaeni L, Baldessari D, Mostoslavsky R, Rossig L, Dequiedt F, Haendeler J, Mione M, Dejana E, Alt FW, Zeiher AM, Dimmeler S (2007) SIRT1 controls endothelial angiogenic functions during vascular growth. Genes Dev 21:2644–2658CrossRefPubMedPubMedCentral
29.
go back to reference Maizel J, Xavier S, Chen J, Lin CH, Vasko R, Goligorsky MS (2014) Sirtuin 1 ablation in endothelial cells is associated with impaired angiogenesis and diastolic dysfunction. Am J Physiol Heart Circ Physiol 307:H1691–H1704CrossRefPubMedPubMedCentral Maizel J, Xavier S, Chen J, Lin CH, Vasko R, Goligorsky MS (2014) Sirtuin 1 ablation in endothelial cells is associated with impaired angiogenesis and diastolic dysfunction. Am J Physiol Heart Circ Physiol 307:H1691–H1704CrossRefPubMedPubMedCentral
30.
go back to reference Price RL, Song J, Bingmer K, Kim TH, Yi JY, Nowicki MO, Mo X, Hollon T, Murnan E, Alvarez-Breckenridge C, Fernandez S, Kaur B, Rivera A, Oglesbee M, Cook C, Chiocca EA, Kwon CH (2013) Cytomegalovirus contributes to glioblastoma in the context of tumor suppressor mutations. Cancer Res 73:3441–3450CrossRefPubMedPubMedCentral Price RL, Song J, Bingmer K, Kim TH, Yi JY, Nowicki MO, Mo X, Hollon T, Murnan E, Alvarez-Breckenridge C, Fernandez S, Kaur B, Rivera A, Oglesbee M, Cook C, Chiocca EA, Kwon CH (2013) Cytomegalovirus contributes to glioblastoma in the context of tumor suppressor mutations. Cancer Res 73:3441–3450CrossRefPubMedPubMedCentral
31.
go back to reference MacManiman JD, Meuser A, Botto S, Smith PP, Liu F, Jarvis MA, Nelson JA, Caposio P (2014) Human cytomegalovirus-encoded pUL7 is a novel CEACAM1-like molecule responsible for promotion of angiogenesis. mBio 5:e2035CrossRef MacManiman JD, Meuser A, Botto S, Smith PP, Liu F, Jarvis MA, Nelson JA, Caposio P (2014) Human cytomegalovirus-encoded pUL7 is a novel CEACAM1-like molecule responsible for promotion of angiogenesis. mBio 5:e2035CrossRef
Metadata
Title
miR-138 promotes migration and tube formation of human cytomegalovirus-infected endothelial cells through the SIRT1/p-STAT3 pathway
Authors
Shanchao Zhang
Lei Liu
Ruijin Wang
Houzhen Tuo
Yanjun Guo
Li Yi
Dexin Wang
Jiawei Wang
Publication date
01-09-2017
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 9/2017
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-017-3423-0

Other articles of this Issue 9/2017

Archives of Virology 9/2017 Go to the issue