Butylated hydroxyanisole stimulates heme oxygenase-1 gene expression and inhibits neointima formation in rat arteries

Cardiovascular Research

Volumn 74, Issue 1, 2007, Pages 169-179

  Liu, Xiao ming ^a,b   Azam, Mohammed A ^a,b   Peyton, Kelly J ^a,b   Ensenat, Diana ^b   Keswani, Amit N ^b   Wang, Hong ^c   Durante, William ^a,b  

^a University of Missouri   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEMPLE UNIVERSITY   (United States)

Author keywords

Angioplasty; Arteries; Gene expression; Restenosis; Smooth muscle

Indexed keywords

ANTIOXIDANT; BUTYLATED HYDROXYANISOLE; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA MEDIA; ARTERY INTIMA; ARTICLE; CAROTID ARTERY INJURY; CELL CULTURE; CELL CYCLE PROGRESSION; CELL GROWTH; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA SYNTHESIS; DRUG INHIBITION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME REGULATION; GENE EXPRESSION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANIMALS; ANTIOXIDANTS; ARTERIES; ATHEROSCLEROSIS; BUTYLATED HYDROXYANISOLE; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; MALE; MUSCLE, SMOOTH, VASCULAR; RATS; RATS, SPRAGUE-DAWLEY; STIMULATION, CHEMICAL; TUNICA INTIMA;

EID: 33847753483     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2007.01.017     Document Type: Article

References (45)

1. Schwartz S.M., and Liaw L. Growth control and morphogenesis in the development and pathology of arteries. J Cardiovasc Pharmacol 21 Suppl. 1 (1993) S31-S49
2. Dzau V.J., Braun-Dellaeus R.C., and Shedding D.G. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med 8 (2002) 1249-1256
3. Holmes Jr. D.R. State of the art in coronary interventions. Am J Cardiol 135 (2003) 955-959
4. Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2 (1989) 2557-2568
5. Duckers H.J., Boehm M., True A.L., Yet S.-F., Park J.L., Webb R.C., et al. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med 7 (2001) 693-698
6. Morita T., and Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest 96 (1995) 2676-2682
7. Peyton K.J., Reyna S.V., Chapman G.B., Ensenat D., Liu X., Wang H., et al. Heme oxygenase-1-derived carbon monoxide is an autocrine inhibitor of vascular smooth muscle cell growth. Blood 99 (2002) 4443-4448
8. Togane Y., Toshisuki M., Suematsu M., Ishimura Y., Yamazaki J., and Katayama S. Protective roles of endogenous carbon monoxide in neointimal development elicited by arterial injury. Am J Physiol Heart Circ Physiol 278 (2000) H623-H632
9. Aizawa T., Ishizaka N., Taguchi J., Kimura S., Kurokawa K., and Ohno M. Balloon injury does not induce heme oxygenase-1 gene expression, but administration of hemin inhibits neointimal formation in balloon injured rat carotid arteries. Biochem Biophys Res Commun 261 (1999) 302-307
10. Tulis D.A., Durante W., Peyton K.J., Evans A.J., and Schafer A.I. Heme oxygenase-1 attenuates vascular remodeling following balloon injury in rat carotid arteries. Atherosclerosis 155 (2001) 113-122
11. Tulis D.A., Durante W., Liu X., Evan A.J., Peyton K.J., and Schafer A.I. Adenovirus-mediated heme oxygenase-1 gene delivery inhibits injury-induced vascular neointima formation. Circulation 104 (2001) 2710-2715
12. Yet S.F., Layne M.D., Liu X., Chen Y.H., Ith B., Sibinga N.E., et al. Absence of heme oxygenase-1 exacerbates atherosclerosis lesion formation an vascular remodeling. FASEB J 17 (2003) 1759-1761
13. Exner M., Schillinger M., Minar E., Mlekusch W., Schlerka G., Haumer M., et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with restenosis after percutaneous transluminal angioplasty. J Endovasc Ther 8 (2001) 433-440
14. Chen Y.-H., Chau L.-Y., Lin M.-W., Chen L.-C., Yo M.-H., Chen J.-W., et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with angiographic restenosis after coronary stenting. Eur Heart J 25 (2004) 39-47
15. Kahl R. Synthetic antioxidants: biochemical action and interference with radiation, toxic compounds, chemical mutagens and chemical carcinogens. Toxicology 59 (1984) 179-194
16. Benson A.M., Hunkeler M.J., and Talalay P. Increase of NAD(P)H :quinine reductase by dietary antioxidants: possible role in protection against carcinogenesis and toxicity. Proc Natl Acad Sci U S A 77 (1980) 5216-5220
17. De Long M.J., Prochaska H.J., and Talalay P. Tissue-specific induction patterns of cancer-protective enzymes in mice by tert-butyl-4-hydroxyanisole and related substituted phenols. Cancer Res 45 (1985) 546-551
18. Saito M., Sakagami H., and Fujisawa S. Cytotoxicity and apoptosis induction by butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT). Anticancer Res 23 (2003) 4693-4701
19. Taniguchi S., Furukawa M., Kono T., Hisa T., Ishii M., and Hamada T. Butylated hydroxyanisole blocks the inhibitory effects of tumor necrosis factor-α on collagen production in human dermal fibroblasts. J Dermatol Sci 12 (1996) 44-49
20. Brekke O.L., Shalaby M.R., Sundan A., Espevik T., and Bjerve K.S. Butylated hydroxyanisole specifically inhibits tumor-necrosis factor-induced cytotoxicity and growth enhancement. Cytokine 4 (1992) 269-280
21. Ikezaki S., Nishikawa A., Enami T., Furukawa F., Imazawa T., Uneyama C., et al. Inhibitory effects of the dietary antioxidants butylated hydroxyanisole and butylated hydroxytoluene on bronchioloalveolar cell proliferation during the bleomycin-induced pulmonary fibrosing process in hamsters. Food Chem Toxicol 34 (1996) 327-335
22. Durante W., Schini V.B., Catovsky S., Kroll M.H., Vanhoutte P.M., and Schafer A.I. Plasmin potentiates the induction of nitric oxide synthase by interleukin-1β in vascular smooth muscle. Am J Physiol Heart Circ Physiol 264 (1993) H617-H623
23. Durante W., Kroll M.H., Christodoulides N., Peyton K.J., and Schafer A.I. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res 80 (1997) 557-564
24. Alam J., Wicks C., Stewart D., Gong P., Touchard C., Otterbein S., et al. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells: role of p38 kinase and Nrf2 transcription factor. J Biol Chem 275 (2000) 27694-27702
25. Liu X., Chapman G.B., Peyton K.J., Schafer A.I., and Durante W. Carbon monoxide inhibits apoptosis in vascular smooth muscle cells. Cardiovasc Res 55 (2002) 396-405
26. Granada J.F., Ensenat D., Keswani A.N., Kaluza G.L., Raizner A.E., Liu X.M., et al. Single perivascular delivery of mitomycin C stimulates p21 expression and inhibits neointima formation in rat arteries. Arterioscler Thromb Vasc Biol 25 (2005) 2343-2348
27. Fulton G.J., Davies M.G., Barber L., Svendsen E., and Hagen P.O. Locally applied antisense oligonucleotide to proliferating cell nuclear antigen inhibits intimal thickening in experimental vein grafts. Ann Vasc Surg 12 (1998) 412-417
28. Hu Y., Zou Y., Dietrich H., Wick G., and Xu Q. Inhibition of neointima hyperplasia in mouse vein grafts by locally applied suramin. Circulation 100 (1999) 861-868
29. Abe T., Sasaki M., Nakajima H., Ogita M., Naitou H., Nagase A., et al. Evaluation of pluronic F127 as a gradual release of anticancer drug. Gan To Kagaku Ryoho 17 (1990) 1546-1550
30. Alam J., and Cook J.L. Transcriptional regulation of the heme oxygenase-1 gene via the stress response pathway. Curr Pharm Des 9 (2003) 2499-2511
31. Noda S., Harada N., Hida A., Fujii-Kuriyama Y., Motohashi, and Yamamoto M. Gene expression of detoxifying enzymes in AhR and Nrf2 compound null mutant mice. Biochem Biophys Res Commun 303 (2003) 105-111
32. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M.K., and Cook J.L. Nrf2, a cap'n'collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274 (1999) 26071-26078
33. Balogun E., Hoque M., Gong P., Killeen E., Green C.J., Foresti R., et al. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 371 (2003) 887-895
34. Martin D., Rojo A.I., Salinas M., Diaz R., Gallardo G., Alam J., et al. Regulation of heme oxygenase-1 expression through the phosphatidlyinositol-3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnasol. J Biol Chem 279 (2004) 8919-8929
35. Chen C.Y., Jang J.H., Li M.H., and Surh Y.J. Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem Biophys Res Commun 331 (2005) 993-1000
36. Nguyen T., Yang C.S., and Pickett C.B. The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med 37 (2004) 433-441
37. Yuan X., Xu C., Pan Z., Keum Y.-S., Kim J.-H., Shen G., et al. Butylated hydroxyanisole regulates ARE-mediated gene expression via Nrf2 coupled with ERK and JNK signaling pathway in HepG2 cells. Mol Carcinog 45 (2006) 841-850
38. Yu R., Manlekar S., and Tony Kong A.-N. Molecular mechanisms of butylated hydroxyanisole-induced toxicity: induction of apoptosis through direct release of cytochrome c. Mol Pharmacol 58 (2000) 431-437
39. Otterbein L.E., Zuckerbraun B.S., Haga M., Liu F., Song R., Usheva A., et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 9 (2003) 183-190
40. Ollinger R., Bilban M., Erat A., Froio A., McDaid J., Tyagi S., et al. Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 112 (2005) 1030-1039
41. Yeng Y.-M., Wu B.J., Witting P.K., and Stocker R.S. Probucol protects against smooth muscle cell proliferation by upregulating heme oxygenase-1. Circulation 110 (2004) 1855-1860
42. Wu B.J., Kathir K., Witting P.K., Beck K., Choy K., Li C., et al. Antioxidants protect from atherosclerosis by a heme oxygenase-1 pathway that is independent of free radical scavenging. J Exp Med 203 (2006) 1117-1127
43. Yang X., Thomas D.P., Zhang X., Culver B.W., Alexander B.M., Murdoch W.J., et al. Curcumin inhibits platelet-derived growth factor-stimulated vascular smooth muscle cell function and injury-induced neointima formation. Arterioscler Thromb Vasc Biol 26 (2006) 85-90
44. Zou J., Huang Y., Cao K., Yang G., Yin H., Len J., et al. Effect of resveratrol on intimal hyperplasia after endothelium denudation in an experimental rabbit model. Life Sci 68 (2000) 153-163
45. Zern T.L., and Fernandez M.L. Cardioprotective effects of dietary polyphenols. J Nutr 135 (2005) 2291-2294