Cigarette Smoke Modulates Vascular Smooth Muscle Phenotype: Implications for Carotid and Cerebrovascular Disease

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Starke, Robert M ^a   Ali, Muhammad S ^a   Jabbour, Pascal M ^a   Tjoumakaris, Stavropoula I ^a   Gonzalez, Fernando ^a   Hasan, David M ^b   Rosenwasser, Robert H ^a   Owens, Gary K ^a   Koch, Walter J ^c   Dumont, Aaron S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CIGARETTE SMOKE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; KRUPPEL LIKE FACTOR 4; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYOCARDIN; STROMELYSIN; TRANSGELIN; TUMOR NECROSIS FACTOR ALPHA;

ACETYLATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY; CAROTID ARTERY DISEASE; CEREBROVASCULAR DISEASE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION; MARKER GENE; NONHUMAN; PROMOTER REGION; RAT; VASCULAR SMOOTH MUSCLE;

ACETYLATION; ANIMALS; CAROTID ARTERIES; CELL DIFFERENTIATION; CEREBROVASCULAR DISORDERS; DNA METHYLATION; DOWN-REGULATION; GENETIC MARKERS; HISTONE DEACETYLASE 2; HISTONES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MUSCLE, SMOOTH, VASCULAR; NUCLEAR PROTEINS; PHENOTYPE; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; SMOKE; TOBACCO PRODUCTS; TRANS-ACTIVATORS;

EID: 84881513553     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071954     Document Type: Article

References (64)

1. Talhout R, Schulz T, Florek E, van Benthem J, Wester P, et al. (2011) Hazardous compounds in tobacco smoke. Int J Environ Res Public Health 8: 613-628.
2. He J, Vupputuri S, Allen K, Prerost MR, Hughes J, et al. (1999) Passive smoking and the risk of coronary heart disease-a meta-analysis of epidemiologic studies. N Engl J Med 340: 920-926.
3. You RX, Thrift AG, McNeil JJ, Davis SM, Donnan GA, (1999) Ischemic stroke risk and passive exposure to spouses' cigarette smoking. Melbourne Stroke Risk Factor Study (MERFS) Group. Am J Public Health 89: 572-575.
4. Sacco RL, Adams R, Albers G, Alberts MJ, Benavente O, et al. (2006) Guidelines for prevention of stroke in patients with ischemic stroke or transient ischemic attack: a statement for healthcare professionals from the American Heart Association/American Stroke Association Council on Stroke: co-sponsored by the Council on Cardiovascular Radiology and Intervention: the American Academy of Neurology affirms the value of this guideline. Stroke 37: 577-617.
5. Diez-Roux AV, Nieto FJ, Comstock GW, Howard G, Szklo M, (1995) The relationship of active and passive smoking to carotid atherosclerosis 12-14 years later. Prev Med 24: 48-55.
6. Inoue T, Oku K, Kimoto K, Takao M, Nomoto J, et al. (1995) Relationship of cigarette smoking to the severity of coronary and thoracic aortic atherosclerosis. Cardiology 86: 374-379.
7. Andersen KK, Olsen TS, Dehlendorff C, Kammersgaard LP, (2009) Hemorrhagic and ischemic strokes compared: stroke severity, mortality, and risk factors. Stroke 40: 2068-2072.
8. Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, et al. (2012) Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 32: 1659-1676.
9. Chalouhi N, Ali MS, Starke RM, Jabbour PM, Tjoumakaris SI, et al. (2013) Cigarette smoke and inflammation: role in cerebral aneurysm formation and rupture. Mediators Inflamm 2012: 271582.
10. Goldstein LB, Bushnell CD, Adams RJ, Appel LJ, Braun LT, et al. (2010) Guidelines for the primary prevention of stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42: 517-584.
11. Jha P, Ramasundarahettige C, Landsman V, Rostron B, Thun M, et al. (2013) 21st-century hazards of smoking and benefits of cessation in the United States. N Engl J Med 368: 341-350.
12. Arnson Y, Shoenfeld Y, Amital H, (2010) Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34: J258-265.
13. Mazzone P, Tierney W, Hossain M, Puvenna V, Janigro D, et al. (2010) Pathophysiological impact of cigarette smoke exposure on the cerebrovascular system with a focus on the blood-brain barrier: expanding the awareness of smoking toxicity in an underappreciated area. Int J Environ Res Public Health 7: 4111-4126.
14. Orosz Z, Csiszar A, Labinskyy N, Smith K, Kaminski PM, et al. (2007) Cigarette smoke-induced proinflammatory alterations in the endothelial phenotype: role of NAD(P)H oxidase activation. Am J Physiol Heart Circ Physiol 292: H130-139.
15. Perlstein TS, Lee RT, (2006) Smoking, metalloproteinases, and vascular disease. Arterioscler Thromb Vasc Biol 26: 250-256.
16. Lee J, Taneja V, Vassallo R, (2011) Cigarette smoking and inflammation: cellular and molecular mechanisms. J Dent Res 91: 142-149.
17. Sopori M, (2002) Effects of cigarette smoke on the immune system. Nat Rev Immunol 2: 372-377.
18. Hossain M, Mazzone P, Tierney W, Cucullo L, (2011) In vitro assessment of tobacco smoke toxicity at the BBB: do antioxidant supplements have a protective role? BMC Neurosci 12: 92.
19. Ambrose JA, Barua RS, (2004) The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43: 1731-1737.
20. Schwartz J, Weiss ST, (1994) Cigarette smoking and peripheral blood leukocyte differentials. Ann Epidemiol 4: 236-242.
21. Tracy RP, Psaty BM, Macy E, Bovill EG, Cushman M, et al. (1997) Lifetime smoking exposure affects the association of C-reactive protein with cardiovascular disease risk factors and subclinical disease in healthy elderly subjects. Arterioscler Thromb Vasc Biol 17: 2167-2176.
22. Mendall MA, Patel P, Asante M, Ballam L, Morris J, et al. (1997) Relation of serum cytokine concentrations to cardiovascular risk factors and coronary heart disease. Heart 78: 273-277.
23. Owens GK, (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487-517.
24. Yoshida T, Owens GK, (2005) Molecular determinants of vascular smooth muscle cell diversity. Circ Res 96: 280-291.
25. Creemers EE, Sutherland LB, McAnally J, Richardson JA, Olson EN, (2006) Myocardin is a direct transcriptional target of Mef2, Tead and Foxo proteins during cardiovascular development. Development 133: 4245-4256.
26. Madsen CS, Hershey JC, Hautmann MB, White SL, Owens GK, (1997) Expression of the smooth muscle myosin heavy chain gene is regulated by a negative-acting GC-rich element located between two positive-acting serum response factor-binding elements. J Biol Chem 272: 6332-6340.
27. Pidkovka NA, Cherepanova OA, Yoshida T, Alexander MR, Deaton RA, et al. (2007) Oxidized phospholipids induce phenotypic switching of vascular smooth muscle cells in vivo and in vitro. Circ Res 101: 792-801.
28. Regan CP, Adam PJ, Madsen CS, Owens GK, (2000) Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J Clin Invest 106: 1139-1147.
29. Wamhoff BR, Hoofnagle MH, Burns A, Sinha S, McDonald OG, et al. (2004) A G/C element mediates repression of the SM22alpha promoter within phenotypically modulated smooth muscle cells in experimental atherosclerosis. Circ Res 95: 981-988.
30. Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF,et al. Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab.
31. Wang C, Han M, Zhao XM, Wen JK, (2008) Kruppel-like factor 4 is required for the expression of vascular smooth muscle cell differentiation marker genes induced by all-trans retinoic acid. J Biochem 144: 313-321.
32. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
33. Furnkranz A, Schober A, Bochkov VN, Bashtrykov P, Kronke G, et al. (2005) Oxidized phospholipids trigger atherogenic inflammation in murine arteries. Arterioscler Thromb Vasc Biol 25: 633-638.
34. Isakson BE, Kronke G, Kadl A, Leitinger N, Duling BR, (2006) Oxidized phospholipids alter vascular connexin expression, phosphorylation, and heterocellular communication. Arterioscler Thromb Vasc Biol 26: 2216-2221.
35. Csiszar A, Labinskyy N, Podlutsky A, Kaminski PM, Wolin MS, et al. (2008) Vasoprotective effects of resveratrol and SIRT1: attenuation of cigarette smoke-induced oxidative stress and proinflammatory phenotypic alterations. Am J Physiol Heart Circ Physiol 294: H2721-2735.
36. Alexander MR, Moehle CW, Johnson JL, Yang Z, Lee JK, et al. (2012) Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J Clin Invest 122: 70-79.
37. Alexander MR, Murgai M, Moehle CW, Owens GK, (2012) Interleukin-1beta modulates smooth muscle cell phenotype to a distinct inflammatory state relative to PDGF-DD via NF-kappaB-dependent mechanisms. Physiol Genomics 44: 417-429.
38. Alexander MR, Owens GK, (2012) Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol 74: 13-40.
39. McDonald OG, Owens GK, (2007) Programming smooth muscle plasticity with chromatin dynamics. Circ Res 100: 1428-1441.
40. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK, (2006) Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest 116: 36-48.
41. Celermajer DS, Adams MR, Clarkson P, Robinson J, McCredie R, et al. (1996) Passive smoking and impaired endothelium-dependent arterial dilatation in healthy young adults. N Engl J Med 334: 150-154.
42. Celermajer DS, Sorensen KE, Georgakopoulos D, Bull C, Thomas O, et al. (1993) Cigarette smoking is associated with dose-related and potentially reversible impairment of endothelium-dependent dilation in healthy young adults. Circulation 88: 2149-2155.
43. Owens GK, Kumar MS, Wamhoff BR, (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801.
44. Gunning P, Weinberger R, Jeffrey P, (1997) Actin and tropomyosin isoforms in morphogenesis. Anat Embryol (Berl) 195: 311-315.
45. Snasel J, Pichova I, (1996) The cleavage of host cell proteins by HIV-1 protease. Folia Biol (Praha) 42: 227-230.
46. Di Luozzo G, Pradhan S, Dhadwal AK, Chen A, Ueno H, et al. (2005) Nicotine induces mitogen-activated protein kinase dependent vascular smooth muscle cell migration. Atherosclerosis 178: 271-277.
47. Li JM, Cui TX, Shiuchi T, Liu HW, Min LJ, et al. (2004) Nicotine enhances angiotensin II-induced mitogenic response in vascular smooth muscle cells and fibroblasts. Arterioscler Thromb Vasc Biol 24: 80-84.
48. Stein JJ, Seymour KA, Maier KG, Gahtan V, (2011) The effects of nicotine on vascular smooth muscle cell chemotaxis induced by thrombospondin-1 and fibronectin. Am J Surg 202: 545-548.
49. Chen QW, Edvinsson L, Xu CB, (2010) Cigarette smoke extract promotes human vascular smooth muscle cell proliferation and survival through ERK1/2- and NF-kappaB-dependent pathways. ScientificWorldJournal 10: 2139-2156.
50. Charo IF, Ransohoff RM, (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354: 610-621.
51. Rosenberg GA, (2002) Matrix metalloproteinases in neuroinflammation. Glia 39: 279-291.
52. Ait-Oufella H, Taleb S, Mallat Z, Tedgui A, (2011) Recent advances on the role of cytokines in atherosclerosis. Arterioscler Thromb Vasc Biol 31: 969-979.
53. Tedgui A, Mallat Z, (2006) Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86: 515-581.
54. Ali MS, Yu Z, Jabbour P, Tjoumakaris S, Gonzalez LF, et al. (2012) Tumor Necrosis Factor-alpha Induces Phenotypic Modulation in Cerebral Vascular Smooth Muscle Cells via KLF4: Implications for Cerebral Aneurysm Pathology. Stroke. A110.
55. Bhaskar V, Yin J, Mirza AM, Phan D, Vanegas S,et al. Monoclonal antibodies targeting IL-1 beta reduce biomarkers of atherosclerosis in vitro and inhibit atherosclerotic plaque formation in Apolipoprotein E-deficient mice. Atherosclerosis 216: 313-320.
56. Wang X, Feuerstein GZ, Gu JL, Lysko PG, Yue TL, (1995) Interleukin-1 beta induces expression of adhesion molecules in human vascular smooth muscle cells and enhances adhesion of leukocytes to smooth muscle cells. Atherosclerosis 115: 89-98.
57. Alexander MR, Murgai M, Moehle CW, Owens GK, (2012) Interleukin-1beta modulates smooth muscle cell phenotype to a distinct inflammatory state relative to PDGF-DD via NF-kappaB-dependent mechanisms. Physiol Genomics 44: 417-429.
58. Legein B, Temmerman L, Biessen EA, Lutgens E (2013) Inflammation and immune system interactions in atherosclerosis. Cell Mol Life Sci.
59. Stoll G, Bendszus M, (2006) Inflammation and atherosclerosis: novel insights into plaque formation and destabilization. Stroke 37: 1923-1932.
60. Feinberg MW, Cao Z, Wara AK, Lebedeva MA, Senbanerjee S, et al. (2005) Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J Biol Chem 280: 38247-38258.
61. Trojer P, Reinberg D, (2006) Histone lysine demethylases and their impact on epigenetics. Cell 125: 213-217.
62. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH, et al. (2005) Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J Biol Chem 280: 9719-9727.
63. Kawai-Kowase K, Owens GK, (2007) Multiple repressor pathways contribute to phenotypic switching of vascular smooth muscle cells. Am J Physiol Cell Physiol 292: C59-69.
64. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.