Long‑term nicotine exposure induces dysfunction of mouse endothelial progenitor cells

Li,Wei; Du,Da‑Yong; Liu,Yang; Jiang,Feng; Zhang,Pan; Li,Yun‑Tian

doi:10.3892/etm.2016.3916

Long‑term nicotine exposure induces dysfunction of mouse endothelial progenitor cells

Authors:
- Wei Li
- Da‑Yong Du
- Yang Liu
- Feng Jiang
- Pan Zhang
- Yun‑Tian Li
View Affiliations

Affiliations: Department of Cardiology, 305 Hospital of the People's Liberation Army, Beijing 100017, P.R. China
Published online on: November 18, 2016 https://doi.org/10.3892/etm.2016.3916
Pages: 85-90
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Endothelial progenitor cells (EPCs) have an important role in maintaining endothelial homeostasis. Previous studies reported that smoking has detrimental effects on EPCs; however, recent studies revealed that short‑term nicotine exposure may benefit EPCs. As most smokers are exposed to nicotine over an extended time period, the present study aimed to investigate the long‑term effects of nicotine on EPCs. Mice were administered nicotine orally for 1, 3 or 6 months. The mice exposed to nicotine for 1 month demonstrated increased EPC counts and telomerase activity and reduced cell senescence compared with control mice, consistent with previous reports. However, long‑term nicotine exposure resulted in opposing effects on EPCs, causing decreased counts, functional impairment and reduced telomerase activity. Furthermore, the effects of nicotine exposure were correlated with changes in sirtuins type 1 (SIRT1) protein expression. The current study indicated that long‑term nicotine exposure induces dysfunction and senescence of EPCs, which may be associated with impairment of telomerase activity through SIRT1 downregulation. The present results emphasize the necessity of smoking cessation to prevent dysfunction of EPCs.

View Figures

View References

1	Urbich C and Dimmeler S: Endothelial progenitor cells: Characterization and role in vascular biology. Circ Res. 95:343–353. 2004. View Article : Google Scholar : PubMed/NCBI
2	Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Böhm M and Nickenig G: Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med. 353:999–1007. 2005. View Article : Google Scholar : PubMed/NCBI
3	Aicher A, Zeiher AM and Dimmeler S: Mobilizing endothelial progenitor cells. Hypertension. 45:321–325. 2005. View Article : Google Scholar : PubMed/NCBI
4	Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM and Dimmeler S: Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 89:E1–E7. 2001. View Article : Google Scholar : PubMed/NCBI
5	Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP and Gurtner GC: Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 106:2781–2786. 2002. View Article : Google Scholar : PubMed/NCBI
6	Ezzati M, Henley SJ, Thun MJ and Lopez AD: Role of smoking in global and regional cardiovascular mortality. Circulation. 112:489–497. 2005. View Article : Google Scholar : PubMed/NCBI
7	Powell JT: Vascular damage from smoking: Disease mechanisms at the arterial wall. Vasc Med. 3:21–28. 1998. View Article : Google Scholar : PubMed/NCBI
8	Bondjers G, Hansson G, Olsson G and Pettersson K: Smoking, catecholamines and their effects on endothelial cell integrity. Adv Exp Med Biol. 273:51–59. 1990. View Article : Google Scholar : PubMed/NCBI
9	Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, Inden Y and Murohara T: Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol. 24:1442–1447. 2004. View Article : Google Scholar : PubMed/NCBI
10	Puls M, Schroeter MR, Steier J, Stijohann L, Hasenfuss G, Konstantinides S and Schäfer K: Effect of smoking cessation on the number and adhesive properties of early outgrowth endothelial progenitor cells. Int J Cardiol. 152:61–69. 2011. View Article : Google Scholar : PubMed/NCBI
11	Wang X, Zhu J, Chen J and Shang Y: Effects of nicotine on the number and activity of circulating endothelial progenitor cells. J Clin Pharmacol. 44:881–889. 2004. View Article : Google Scholar : PubMed/NCBI
12	Sugimoto A, Masuda H, Eguchi M, Iwaguro H, Tanabe T and Asahara T: Nicotine enlivenment of blood flow recovery following endothelial progenitor cell transplantation into ischemic hindlimb. Stem Cells Dev. 16:649–656. 2007. View Article : Google Scholar : PubMed/NCBI
13	Junhui Z, Xiaojing H, Binquan Z, Xudong X, Junzhu C and Guosheng F: Nicotine-reduced endothelial progenitor cell senescence through augmentation of telomerase activity via the PI3K/Akt pathway. Cytotherapy. 11:485–491. 2009. View Article : Google Scholar : PubMed/NCBI
14	National Institutes of Health (NIH), . Guide for the Care and Use of Laboratory Animals. 7th. NIH; Bethesda, MD, USA: Publication No. 85–23. 1996
15	Li W, Wang H, Kuang CY, Zhu JK, Yu Y, Qin ZX, Liu J and Huang L: An essential role for the Id1/PI3K/Akt/NFkB/survivin signalling pathway in promoting the proliferation of endothelial progenitor cells in vitro. Mol Cell Biochem. 363:135–145. 2012. View Article : Google Scholar : PubMed/NCBI
16	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
17	Reed J, Gunaratnam M, Beltran M, Reszka AP, Vilar R and Neidle S: TRAP-LIG, a modified telomere repeat amplification protocol assay to quantitate telomerase inhibition by small molecules. Anal Biochem. 380:99–105. 2008. View Article : Google Scholar : PubMed/NCBI
18	Vassallo PF, Simoncini S, Ligi I, Chateau AL, Bachelier R, Robert S, Morere J, Fernandez S, Guillet B, Marcelli M, et al: Accelerated senescence of cord blood endothelial progenitor cells in premature neonates is driven by SIRT1 decreased expression. Blood. 123:2116–2126. 2014. View Article : Google Scholar : PubMed/NCBI
19	Stedman RL: The chemical composition of tobacco and tobacco smoke. Chem Rev. 68:153–207. 1968. View Article : Google Scholar : PubMed/NCBI
20	Kannel WB, McGee D and Gordon T: A general cardiovascular risk profile: The Framingham Study. Am J Cardiol. 38:46–51. 1976. View Article : Google Scholar : PubMed/NCBI
21	Strohschneider T, Oberhoff M, Hanke H, Hannekum A and Karsch KR: Effect of chronic nicotine delivery on the proliferation rate of endothelial and smooth muscle cells in experimentally induced vascular wall plaques. Clin Investig. 72:908–912. 1994. View Article : Google Scholar : PubMed/NCBI
22	Leake DS and Bowyer DE: Quantitative studies of pinocytosis by arterial endothelial and smooth muscle cells in culture. Exp Mol Pathol. 35:84–97. 1981. View Article : Google Scholar : PubMed/NCBI
23	Zimmerman M and McGeachie J: The effect of nicotine on aortic endothelial cell turnover. An autoradiographic study. Atherosclerosis. 58:39–47. 1985. View Article : Google Scholar : PubMed/NCBI
24	Banerjee S, Brilakis E, Zhang S, Roesle M, Lindsey J, Philips B, Blewett CG and Terada LS: Endothelial progenitor cell mobilization after percutaneous coronary intervention. Atherosclerosis. 189:70–75. 2006. View Article : Google Scholar : PubMed/NCBI
25	Hristov M, Zernecke A, Liehn EA and Weber C: Regulation of endothelial progenitor cell homing after arterial injury. Thromb Haemost. 98:274–277. 2007.PubMed/NCBI
26	Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA and Finkel T: Circulating endothelial progenitor cells, vascular function and cardiovascular risk. N Engl J Med. 348:593–600. 2003. View Article : Google Scholar : PubMed/NCBI
27	Lin CP, Lin FY, Huang PH, Chen YL, Chen WC, Chen HY, Huang YC, Liao WL, Huang HC, Liu PL and Chen YH: Endothelial progenitor cell dysfunction in cardiovascular diseases: Role of reactive oxygen species and inflammation. Biomed Res Int. 2013:8450372013. View Article : Google Scholar : PubMed/NCBI
28	Counter CM: The roles of telomeres and telomerase in cell life span. Mutat Res. 366:45–63. 1996. View Article : Google Scholar : PubMed/NCBI
29	Imanishi T, Hano T, Sawamura T and Nishio I: Oxidized low-density lipoprotein induces endothelial progenitor cell senescence, leading to cellular dysfunction. Clin Exp Pharmacol Physiol. 31:407–413. 2004. View Article : Google Scholar : PubMed/NCBI
30	Imanishi T, Hano T and Nishio I: Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens. 23:97–104. 2005. View Article : Google Scholar : PubMed/NCBI
31	Kuki S, Imanishi T, Kobayashi K, Matsuo Y, Obana M and Akasaka T: Hyperglycemia accelerated endothelial progenitor cell senescence via the activation of p38 mitogen-activated protein kinase. Circ J. 70:1076–1081. 2006. View Article : Google Scholar : PubMed/NCBI
32	Ota H, Akishita M, Eto M, Iijima K, Kaneki M and Ouchi Y: Sirt1 modulates premature senescence-like phenotype in human endothelial cells. J Mol Cell Cardiol. 43:571–579. 2007. View Article : Google Scholar : PubMed/NCBI
33	Zu Y, Liu L, Lee MY, Xu C, Liang Y, Man RY, Vanhoutte PM and Wang Y: SIRT1 promotes proliferation and prevents senescence through targeting LKB1 in primary porcine aortic endothelial cells. Circ Res. 106:1384–1393. 2010. View Article : Google Scholar : PubMed/NCBI
34	Wan YZ, Gao P, Zhou S, Zhang ZQ, Hao DL, Lian LS, Li YJ, Chen HZ and Liu DP: SIRT1-mediated epigenetic downregulation of plasminogen activator inhibitor-1 prevents vascular endothelial replicative senescence. Aging Cell. 13:890–899. 2014. View Article : Google Scholar : PubMed/NCBI
35	Lemarié CA, Shbat L, Marchesi C, Angulo OJ, Deschênes ME, Blostein MD, Paradis P and Schiffrin EL: Mthfr deficiency induces endothelial progenitor cell senescence via uncoupling of eNOS and downregulation of SIRT1. Am J Physiol Heart Circ Physiol. 300:H745–H753. 2011. View Article : Google Scholar : PubMed/NCBI