MicroRNA-21 blocks abdominal aortic aneurysm development and nicotine-augmented expansion

Science Translational Medicine

Volumn 4, Issue 122, 2012, Pages

  Maegdefessel, Lars ^a   Azuma, Junya ^a   Toh, Ryuji ^a   Deng, Alicia ^a   Merk, Denis R ^a   Raiesdana, Azad ^a   Leeper, Nicholas J ^a   Raaz, Uwe ^a   Schoelmerich, Anke M ^a   McConnell, Michael V ^a   Dalman, Ronald L ^a   Spin, Joshua M ^a   Tsao, Philip S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; ANTAGOMIR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LENTIVIRUS VECTOR; MICRORNA 21; NICOTINE; PANCREATIC ELASTASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; INTERLEUKIN 6; MICRORNA; MIRN21 MICRORNA, HUMAN; MIRN21 MICRORNA, MOUSE; PTEN PROTEIN, HUMAN; PTEN PROTEIN, MOUSE;

ABDOMINAL AORTA ANEURYSM; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLOOD VESSEL WALL; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DESCENDING AORTA SURGERY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE FIBER; ANIMAL; C57BL MOUSE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; SWINE; UPREGULATION;

ANGIOTENSIN II; ANIMALS; AORTIC ANEURYSM, ABDOMINAL; APOPTOSIS; CELL PROLIFERATION; GENE EXPRESSION PROFILING; HUMANS; INFLAMMATION; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICRORNAS; NICOTINE; PANCREATIC ELASTASE; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; SUS SCROFA; UP-REGULATION;

EID: 84857491474     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3003441     Document Type: Article

References (42)

1. C. Fleming, E. P. Whitlock, T. L. Beil, F. A. Lederle, Screening for abdominal aortic aneurysm: A best-evidence systematic review for the U.S. Preventive Services Task Force. Ann. Intern. Med. 142, 203-211 (2005).
2. M. A. Creager,D. W. Jones, J. D. Easton, J. L. Halperin, A. T. Hirsch, A. H. Matsumoto, P. T. O'Gara, R. D. Safian, G. L. Schwartz, J. A. Spittell; American Heart Association, Atherosclerotic Vascular Disease Conference: Writing Group V: Medical decision making and therapy. Circulation 109, 2634-2642 (2004).
3. J. T. Powell, P. Worrell, S. T. MacSweeney, P. J. Franks, R. M. Greenhalgh, Smoking as a risk factor for abdominal aortic aneurysm. Ann. N. Y. Acad. Sci. 800, 246-248 (1996).
4. N. L. Weintraub, Understanding abdominal aortic aneurysm. N. Engl. J. Med. 361, 1114-1116 (2009).
5. F. A. Lederle, D. B. Nelson, A. M. Joseph, Smokers' relative risk for aortic aneurysm compared with other smoking-related diseases: A systematic review. J. Vasc. Surg. 38, 329-334 (2003).
6. E. van Rooij, The art of microRNA research. Circ. Res. 108, 219-234 (2011).
7. A. M. Krichevsky, G. Gabriely, miR-21: A small multi-faceted RNA. J. Cell. Mol. Med. 13, 39-53 (2009).
8. R. Ji, Y. Cheng, J. Yue, J. Yang, X. Liu, H. Chen, D. B. Dean, C. Zhang, MicroRNA expression signature and antisense-mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circ. Res. 100, 1579-1588 (2007).
9. S. Roy, S. Khanna, S. R. Hussain, S. Biswas, A. Azad, C. Rink, S. Gnyawali, S. Shilo, G. J. Nuovo, C. K. Sen, MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc. Res. 82, 21-29 (2009).
10. T. Thum, C. Gross, J. Fiedler, T. Fischer, S. Kissler, M. Bussen, P. Galuppo, S. Just, W. Rottbauer, S. Frantz, M. Castoldi, J. Soutschek, V. Koteliansky, A. Rosenwald, M. A. Basson, J. D. Licht, J. T. Pena, S. H. Rouhanifard, M. U. Muckenthaler, T. Tuschl, G. R. Martin, J. Bauersachs, S. Engelhardt, MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456, 980-984 (2008).
11. X. Liu, Y. Cheng, J. Yang, T. J. Krall, Y. Huo, C. Zhang, An essential role of PDCD4 in vascular smooth muscle cell apoptosis and proliferation: Implications for vascular disease. Am. J. Physiol. Cell Physiol. 298, C1481-C1488 (2010).
12. G. Y. Oudit, J. M. Penninger, Cardiac regulation by phosphoinositide 3-kinases and PTEN. Cardiovasc. Res. 82, 250-260 (2009).
13. T. D. Bunney, M. Katan, Phosphoinositide signalling in cancer: Beyond PI3K and PTEN. Nat. Rev. Cancer 10, 342-352 (2010).
14. J. Lee, J. P. Cooke, The role of nicotine in the pathogenesis of atherosclerosis. Atherosclerosis 215, 281-283 (2011).
15. R. S. Barua, J. A. Ambrose, L. J. Eales-Reynolds, M. C. DeVoe, J. G. Zervas, D. C. Saha, Heavy and light cigarette smokers have similar dysfunction of endothelial vasoregulatory activity: An in vivo and in vitro correlation. J. Am. Coll. Cardiol. 39, 1758-1763 (2002).
16. Z. Wang, W. Wu, X. Fang, Y. Wang, C. Xiao, R. Zhao, L. Wang, Z. Qiao, Protein expression changed by nicotine in rat vascular smooth muscle cells. J. Physiol. Biochem. 63, 161-169 (2007).
17. V. Y. Shin, H. Jin, E. K. Ng, A. S. Cheng, W.W. Chong, C. Y.Wong, W. K. Leung, J. J. Sung, K. M. Chu, NF-κB targets miR-16 and miR-21 in gastric cancer: Involvement of prostaglandin E receptors. Carcinogenesis 32, 240-245 (2011).
18. R. Zhou, G. Hu, A. Y. Gong, X. M. Chen, Binding of NF-kB p65 subunit to the promoter elements is involved in LPS-induced transactivation of miRNA genes in human biliary epithelial cells. Nucleic Acids Res. 38, 3222-3232 (2010).
19. S. B. Furgeson, P. A. Simpson, I. Park, V. Vanputten, H. Horita, C. D. Kontos, R. A. Nemenoff, M. C. Weiser-Evans, Inactivation of the tumour suppressor, PTEN, in smooth muscle promotes a pro-inflammatory phenotype and enhances neointima formation. Cardiovasc. Res. 86, 274-282 (2010).
20. A. Daugherty, L. A. Cassis, Mouse models of abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 24, 429-434 (2004).
21. R. F. Duisters, A. J. Tijsen, B. Schroen, J. J. Leenders, V. Lentink, I. van der Made, V. Herias, R. E. van Leeuwen, M. W. Schellings, P. Barenbrug, J. G. Maessen, S. Heymans, Y. M. Pinto, E. E. Creemers, miR-133 and miR-30 regulate connective tissue growth factor: Implications for a role of microRNAs in myocardial matrix remodeling. Circ. Res. 104, 170-178 (2009).
22. S. Hu, M. Huang, Z. Li, F. Jia, Z. Ghosh, M. A. Lijkwan, P. Fasanaro, N. Sun, X. Wang, F. Martelli, R. C. Robbins, J. C. Wu, MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 122, S124-S131 (2010).
23. E. van Rooij, L. B. Sutherland, J. E. Thatcher, J. M. DiMaio, R. H. Naseem, W. S. Marshall, J. A. Hill, E. N. Olson, Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc. Natl. Acad. Sci. U.S.A. 105, 13027-13032 (2008).
24. J. E. Fish, M. M. Santoro, S. U. Morton, S. Yu, R. F. Yeh, J. D. Wythe, K. N. Ivey, B. G. Bruneau, D. Y. Stainier, D. Srivastava, miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 15, 272-284 (2008).
25. A. Bonauer, G. Carmona, M. Iwasaki, M. Mione, M. Koyanagi, A. Fischer, J. Burchfield, H. Fox, C. Doebele, K. Ohtani, E. Chavakis, M. Potente, M. Tjwa, C. Urbich, A. M. Zeiher, S. Dimmeler, MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324, 1710-1713 (2009).
26. N. J. Leeper, A. Raiesdana, Y. Kojima, H. J. Chun, J. Azuma, L. Maegdefessel, R. K. Kundu, T. Quertermous, P. S. Tsao, J. M. Spin, MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J. Cell. Physiol. 226, 1035-1043 (2011).
27. C. Buckley, C. W. Wyble, M. Borhani, T. L. Ennis, D. K. Kobayashi, J. A. Curci, S. D. Shapiro, R. W. Thompson, Accelerated enlargement of experimental abdominal aortic aneurysms in a mouse model of chronic cigarette smoke exposure. J. Am. Coll. Surg. 199, 896-903 (2004).
28. M. P. Bergoeing, B. Arif, A. E. Hackmann, T. L. Ennis, R. W. Thompson, J. A. Curci, Cigarette smoking increases aortic dilatation without affecting matrix metalloproteinase-9 and -12 expression in a modified mouse model of aneurysm formation. J. Vasc. Surg. 45, 1217-1227 (2007).
29. L. B. Daniels, A. S. Maisel, Natriuretic peptides. J. Am. Coll. Cardiol. 50, 2357-2368 (2007).
30. R. W. Thompson, J. A. Curci, T. L. Ennis, D. Mao, M. B. Pagano, C. T. Pham, Pathophysiology of abdominal aortic aneurysms: Insights from the elastase-induced model in mice with different genetic backgrounds. Ann. N. Y. Acad. Sci. 1085, 59-73 (2006).
31. S. J. Van Vickle-Chavez, W. S. Tung, T. S. Absi, T. L. Ennis, D. Mao, J. P. Cobb, R. W. Thompson, Temporal changes in mouse aortic wall gene expression during the development of elastase-induced abdominal aortic aneurysms. J. Vasc. Surg. 43, 1010-1020 (2006).
32. R. W. Thompson, S. Liao, J. A. Curci, Vascular smooth muscle cell apoptosis in abdominal aortic aneurysms. Coron. Artery Dis. 8, 623-631 (1997).
33. M. S. Hayden, S. Ghosh, Shared principles in NF-kB signaling. Cell 132, 344-362 (2008).
34. S. Watanabe, Y. Horie, E. Kataoka, W. Sato, T. Dohmen, S. Ohshima, T. Goto, A. Suzuki, Non-alcoholic steatohepatitis and hepatocellular carcinoma: Lessons from hepatocyte-specific phosphatase and tensin homolog (PTEN)-deficient mice. J. Gastroenterol. Hepatol. 22 (Suppl. 1), S96-S100 (2007).
35. F. Meng, R. Henson, H. Wehbe-Janek, K. Ghoshal, S. T. Jacob, T. Patel, MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133, 647-658 (2007).
36. A. San Juan, M. Bala, H. Hlawaty, P. Portes, R. Vranckx, L. J. Feldman, D. Letourneur, Development of a functionalized polymer for stent coating in the arterial delivery of small interfering RNA. Biomacromolecules 10, 3074-3080 (2009).
37. J. Elmén, M. Lindow, S. Schütz, M. Lawrence, A. Petri, S. Obad, M. Lindholm, M. Hedtjarn, H. F. Hansen, U. Berger, S. Gullans, P. Kearney, P. Sarnow, E. M. Straarup, S. Kauppinen, LNA-mediated microRNA silencing in non-human primates. Nature 452, 896-899 (2008).
38. P. K. Mishra, N. Tyagi, M. Kumar, S. C. Tyagi, MicroRNAs as a therapeutic target for cardiovascular diseases. J. Cell. Mol. Med. 13, 778-789 (2009).
39. J. Azuma, T. Asagami, R. Dalman, P. S. Tsao, Creation of murine experimental abdominal aortic aneurysms with elastase. J. Vis. Exp. 29, 1280 (2009).
40. C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, J. M. Greve, Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms. Arterioscler. Thromb. Vasc. Biol. 31, 270-279 (2011).
41. H. J. Chun, Z. A. Ali, Y. Kojima, R. K. Kundu, A. Y. Sheikh, R. Agrawal, L. Zheng, N. J. Leeper, N. E. Pearl, A. J. Patterson, J. P. Anderson, P. S. Tsao, M. J. Lenardo, E. A. Ashley, T. Quertermous, Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J. Clin. Invest. 118, 3343-3354 (2008).
42. J. Azuma, L. Maegdefessel, T. Kitagawa, R. L. Dalman, M. V. McConnell, P. S. Tsao, Assessment of elastase-induced murine abdominal aortic aneurysms: Comparison of ultrasound imaging with in situ video microscopy. J. Biomed. Biotechnol. 2011, 252141 (2011).