Low Shear Stress Inhibited Endothelial Cell Autophagy Through TET2 Downregulation

Annals of Biomedical Engineering

Volumn 44, Issue 7, 2016, Pages 2218-2227

  Yang, Qin ^a   Li, Xiaohong ^a   Li, Rongqing ^a   Peng, Juan ^a   Wang, Zuo ^a   Jiang, Zhisheng ^a   Tang, Xiaoqing ^a   Peng, Zhao ^b   Wang, Yu ^c   Wei, Dangheng ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b Affiliated Hospital Xiang Nan University   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Atherosclerosis; Autophagy; Endothelial cell; Low shear stress; Ten eleven translocation 2 protein

Indexed keywords

CELLS; CYTOLOGY; ENDOTHELIAL CELLS; NITRIC OXIDE; PROTEINS; SHEAR FLOW;

ATHEROGENIC PROCESS; ATHEROSCLEROSIS; ATHEROSCLEROTIC LESIONS; AUTOPHAGY; DOWN-REGULATION; NITRIC-OXIDE SYNTHASE; POTENTIAL MECHANISM; SIRNA TREATMENT;

SHEAR STRESS;

BECLIN 1; BIOLOGICAL MARKER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; LC3I PROTEIN; LC3II PROTEIN; PROTEIN P62; PROTEIN TRANSLOCASE; SMALL INTERFERING RNA; TEN ELEVEN TRANSLOCATION 2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; NOS3 PROTEIN, MOUSE; ONCOPROTEIN; TET2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA SINUS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; AUTOPHAGY; CELL ADHESION; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME INDUCTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LIGHT CHAIN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; WESTERN BLOTTING; ANIMAL; ATHEROSCLEROSIS; BIOSYNTHESIS; GENETICS; KNOCKOUT MOUSE; MECHANICAL STRESS; METABOLISM; PATHOLOGY; SHEAR STRENGTH;

ANIMALS; ATHEROSCLEROSIS; AUTOPHAGY; BECLIN-1; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NITRIC OXIDE SYNTHASE TYPE III; PROTO-ONCOGENE PROTEINS; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 84944916508     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-015-1491-4     Document Type: Article

References (36)

1. Bharath, L. P., R. Mueller, Y. Li, T. Ruan, D. Kunz, R. Goodrich, T. Mills, L. Deeter, and A. Sargsyan. Anandh Babu PV, Graham TE, Symons JD. Impairment of autophagy in endothelial cells prevents shear-stress-induced increases in nitric oxide bioavailability. Can J Physiol Pharmacol. 92(7):605–612, 2014.
2. Chatzizisis, Y. S., A. U. Coskun, M. Jonas, E. R. Edelman, C. L. Feldman, and P. H. Stone. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J. Am. Coll. Cardiol. 49(25):2379–2393, 2007.
3. Chatzizisis, Y. S., M. Jonas, A. U. Coskun, R. Beigel, B. V. Stone, C. Maynard, R. G. Gerrity, W. Daley, C. Rogers, E. R. Edelman, C. L. Feldman, and P. H. Stone. Prediction of the localization of high-risk coronary atherosclerotic plaques on the basis of lowendothelial shear stress: an intravascular ultrasound and histopathology natural history study. Circulation 117(8):993–1002, 2008.
4. Dawlaty, M. M., A. Breiling, T. Le, M. I. Barrasa, G. Raddatz, Q. Gao, B. E. Powell, A. W. Cheng, K. F. Faull, F. Lyko, and R. Jaenisch. Loss of Tet enzymes compromises proper differentiation of embryonic stem cells. Dev Cell. 29(1):102–111, 2014.
5. De Meyer, G. R., M. O. Grootaert, C. F. Michiels, A. Kurdi, D. M. Schrijvers, and W. Martinet. Autophagy in vascular disease. Circ. Res. 116(3):468–479, 2015.
6. Feng, J., N. Shao, K. E. Szulwach, V. Vialou, J. Huynh, C. Zhong, T. Le, D. Ferguson, M. E. Cahill, Y. Li, J. W. Koo, E. Ribeiro, B. Labonte, B. M. Laitman, D. Estey, V. Stockman, P. Kennedy, T. Couroussé, I. Mensah, G. Turecki, K. F. Faull, G. L. Ming, H. Song, G. Fan, P. Casaccia, L. Shen, P. Jin, and E. J. Nestler. Role of Tet1 and 5-hydroxymethylcytosine in cocaine action. Nat. Neurosci. 18(4):536–544, 2015.
7. Green, J., A. Yurdagul, Jr, M. C. McInnis, P. Albert, and A. W. Orr. Flow patterns regulate hyperglycemia-induced subendothelial matrix remodeling during early atherogenesis. Atherosclerosis. 232(2):277–284, 2014.
8. Grimmel, M., C. Backhaus, and T. Proikas-Cezanne. WIPI-mediated autophagy and longevity. Cells. 4(2):202–217, 2015.
9. Guo, F., X. Li, J. Peng, Y. Tang, Q. Yang, L. Liu, Z. Wang, Z. Jiang, M. Xiao, C. Ni, R. Chen, D. Wei, and G. X. Wang. Autophagy regulates vascular endothelial cell eNOS and ET-1 expression induced by laminar shearstress in an ex vivo perfused system. Ann. Biomed. Eng. 42(9):1978–1988, 2014.
10. Harvald, E. B., A. S. Olsen, and N. J. Færgeman. Autophagy in the light of sphingolipid metabolism. Apoptosis 20(5):658–670, 2015.
11. Hon, G. C., C. X. Song, T. Du, F. Jin, S. Selvaraj, A. Y. Lee, C. A. Yen, Z. Ye, S. Q. Mao, B. A. Wang, S. Kuan, L. E. Edsall, B. S. Zhao, G. L. Xu, C. He, and B. Ren. 5mC oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation. Mol Cell. 56(2):286–297, 2014.
12. Kim, K. H., and M. S. Lee. Autophagy—a key player in cellular and body metabolism. Nat Rev Endocrinol. 10(6):322–337, 2014.
13. Ko, M., J. An, W. A. Pastor, S. B. Koralov, K. Rajewsky, and A. Rao. TET proteins and 5-methylcytosine oxidation in hematological cancers. Immunol. Rev. 263(1):6–21, 2015.
14. Koskinas, K. C., C. L. Feldman, Y. S. Chatzizisis, A. U. Coskun, M. Jonas, C. Maynard, A. B. Baker, M. I. Papafaklis, E. R. Edelman, and P. H. Stone. Natural history of experimental coronary atherosclerosis and vascular remodeling in relation to endothelial shear stress: a serial, in vivo intravascular ultrasound study. Circulation 121(19):2092–2101, 2010.
15. Koskinas, K. C., G. K. Sukhova, A. B. Baker, M. I. Papafaklis, Y. S. Chatzizisis, A. U. Coskun, T. Quillard, M. Jonas, C. Maynard, A. P. Antoniadis, G. P. Shi, P. Libby, E. R. Edelman, C. L. Feldman, and P. H. Stone. Thin-capped atheromata with reduced collagen content in pigs develop in coronary arterial regions exposed to persistently low endothelial shear stress. Arterioscler. Thromb. Vasc. Biol. 33(7):1494–1504, 2013.
16. Lavandero, S., M. Chiong, B. A. Rothermel, and J. A. Hill. Autophagy in cardiovascular biology. J. Clin. Invest. 125(1):55–64, 2015.
17. Li, G., J. Peng, Y. Liu, X. Li, Q. Yang, Y. Li, Z. Tang, Z. Wang, Z. Jiang, and D. Wei. Oxidized low-density lipoprotein inhibits HP-1-derived macrophage autophagy via TET2 down-regulation. Lipids 50(2):177–183, 2015.
18. Li, X., Q. Yang, Z. Wang, and D. Wei. Shear stress in atherosclerotic plaque determination. DNA Cell Biol. 33(12):830–838, 2014.
19. Liu, R., Y. Jin, W. H. Tang, L. Qin, X. Zhang, G. Tellides, J. Hwa, J. Yu, and K. A. Martin. Ten-eleven translocation-2 (TET2) is a master regulator of smooth muscle cell plasticity. Circulation 128(18):2047–2057, 2013.
20. Madeo, F., A. Zimmermann, M. C. Maiuri, and G. Kroemer. Essential role for autophagy in life span extension. J. Clin. Invest. 125(1):85–93, 2015.
21. Magné, J., P. Gustafsson, H. Jin, L. Maegdefessel, K. Hultenby, A. Wernerson, P. Eriksson, A. Franco-Cereceda, P. T. Kovanen, I. Gonçalves, and E. Ehrenborg. ATG16L1 expression in carotid atherosclerotic plaques is associated with plaque vulnerability. Arterioscler. Thromb. Vasc. Biol. 35(5):1226–1235, 2015.
22. Nah, J., J. Yuan, and Y. K. Jung. Autophagy in neurodegenerative diseases: from mechanism to therapeutic approach. Mol. Cells 38(5):381–389, 2015.
23. Nakajima, H., and H. Kunimoto. TET2 as an epigenetic master regulator for normal and malignant hematopoiesis. Cancer Sci. 105(9):1093–1099, 2014.
24. Nussenzweig, S. C., S. Verma, and T. Finkel. The role of autophagy in vascular biology. Circ. Res. 116(3):480–488, 2015.
25. Okashita, N., Y. Kumaki, K. Ebi, M. Nishi, Y. Okamoto, M. Nakayama, S. Hashimoto, T. Nakamura, K. Sugasawa, N. Kojima, T. Takada, M. Okano, and Y. Seki. PRDM14 promotes active DNA demethylation through the ten-eleven translocation (TET)-mediated base excision repair pathway in embryonic stem cells. Development. 141(2):269–280, 2014.
26. −/− mice. Sci Rep. 4:5519, 2014.
27. Petersen, M., D. Hofius, and S. U. Andersen. Signaling unmasked: autophagy and catalase promote programmed cell death. Autophagy. 10(3):520–521, 2014.
28. Qi, Y. X., J. Jiang, X. H. Jiang, X. D. Wang, S. Y. Ji, Y. Han, D. K. Long, B. R. Shen, Z. Q. Yan, S. Chien, and Z. L. Jiang. PDGF-BB and TGF-{beta}1 on cross-talk etween endothelial and smooth muscle cells in vascular remodeling induced by low shear stress. Proc. Natl. Acad. Sci. USA 108(5):1908–1913, 2011.
29. Rasmussen, K. D., G. Jia, J. V. Johansen, M. T. Pedersen, N. Rapin, F. O. Bagger, B. T. Porse, O. A. Bernard, J. Christensen, and K. Helin. Loss of TET2 in hematopoietic cells leads to DNA hypermethylation of active enhancers and induction of leukemogenesis. Genes Dev. 29(9):910–922, 2015.
30. Razani, B., C. Fangs, T. Coleman, R. Emanuel, H. Wen, S. Hwang, J. P. Ting, H. W. Virgin, M. B. Kastan, and C. F. Semenkovich. Autophagy links inflammasomes to atherosclerotic progression. Cell Metab. 15(4):534–544, 2012.
31. Robertson, A. B., J. A. Dahl, and A. Klungland. DNA metabolism: bases of DNA repair and regulation. Nat. Chem. Biol. 10(7):487–488, 2014.
32. Santiago, M., C. Antunes, M. Guedes, and N. Sousa. Marques CJ.TET enzymes and DNA hydroxymethylation in neural development and function - how critical are they? Genomics 104(5):334–340, 2014.
33. Stone, P. H., S. Saito, S. Takahashi, Y. Makita, S. Nakamura, T. Kawasaki, A. Takahashi, T. Katsuki, S. Nakamura, A. Namiki, A. Hirohata, T. Matsumura, S. Yamazaki, H. Yokoi, S. Tanaka, S. Otsuji, F. Yoshimachi, J. Honye, D. Harwood, M. Reitman, A. U. Coskun, M. I. Papafaklis, and C. L. Feldman. Prediction of progression of coronary artery disease and clinical outcomes using vascular profiling of endothelial shear stress and arterial plaque characteristics: the prediction study. Circulation 126(2):172–181, 2012.
34. Xiong, Y., G. Yepuri, M. Forbiteh, Y. Yu, J. P. Montani, Z. Yang, and X. F. Ming. ARG2 impairs endothelial autophagy through regulation of MTOR and PRKAA/AMPK signaling in advanced atherosclerosis. Autophagy. 10(12):2223–2238, 2014.
35. Young, A., W. Wu, W. Sun, H. Benjamin Larman, N. Wang, Y. S. Li, J. Y. Shyy, S. Chien, and G. García-Cardeña. Flow activation of AMP-activated protein kinase in vascular endothelium leads to Krüppel-like factor 2 expression. Arterioscler Thromb Vasc Biol. 29(11):1902–1908, 2009.
36. Zhou, J., Y. S. Li, and S. Chien. Shear stress-initiated signaling and its regulation of endothelial function. Arterioscler. Thromb. Vasc. Biol. 34(10):2191–2198, 2014.