Cigarette smoke components induce matrix metalloproteinase-1 in aortic endothelial cells through inhibition of mTOR signaling

Toxicological Sciences

Volumn 123, Issue 2, 2011, Pages 542-549

  Lemaître, Vincent ^a,b   Dabo, Abdoulaye J ^a   D'Armiento, Jeanine ^a  

^a Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Aortic diseases; Collagenase; Endothelium; Matrix metalloproteinases; Tobacco

Indexed keywords

ACROLEIN; CIGARETTE SMOKE; CIGARETTE SMOKE EXTRACT; INTERSTITIAL COLLAGENASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; RAPAMYCIN; S6 KINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PROTEIN EXPRESSION; RABBIT;

ACROLEIN; ANIMALS; AORTA; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME INDUCTION; GENE EXPRESSION; HUMANS; MATRIX METALLOPROTEINASE 1; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PATHOLOGIC; RABBITS; SIGNAL TRANSDUCTION; SMOKE; TISSUE INHIBITOR OF METALLOPROTEINASE-3; TOBACCO; TOR SERINE-THREONINE KINASES;

MAMMALIA; NICOTIANA TABACUM; ORYCTOLAGUS CUNICULUS;

EID: 80053443687     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr181     Document Type: Article

References (44)

1. Apte, S. S., Olsen, B. R., and Murphy, G. (1995). The gene structure of tissue inhibitor of metalloproteinases (TIMP)-3 and its inhibitory activities define the distinct TIMP gene family. J. Biol. Chem. 270, 14313-14318.
2. Balbin, M., Fueyo, A., Knauper, V., Lopez, J. M., Alvarez, J., Sanchez, L. M., Quesada, V., Bordallo, J., Murphy, G., and López-Otín, C. (2001). Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J. Biol. Chem. 276, 10253-10262.
3. Barnoya, J., and Glantz, S. A. (2005). Cardiovascular effects of secondhand smoke: nearly as large as smoking. Circulation 111, 2684-2698.
4. Blackburn, J. S., and Brinckerhoff, C. E. (2008). Matrix metalloproteinase-1 and thrombin differentially activate gene expression in endothelial cells via PAR-1 and promote angiogenesis. Am. J. Pathol. 173, 1736-1746.
5. Blackburn, J. S., Rhodes, C. H., Coon, C. I., and Brinckerhoff, C. E. (2007). RNA interference inhibition of matrix metalloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis. Cancer Res. 67, 10849-10858.
6. D'Armiento, J., Dalal, S. S., Okada, Y., Berg, R. A., and Chada, K. (1992). Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell 71, 955-961.
7. Deshmukh, H. S., Shaver, C., Case, L. M., Dietsch, M., Wesselkamper, S. C., Hardie, W. D., Korfhagen, T. R., Corradi, M., Nadel, J. A., Borchers, M. T., et al. (2008). Acrolein-activated matrix metalloproteinase 9 contributes to persistent mucin production. Am. J. Respir. Cell Mol. Biol. 38, 446-454.
8. Dunlop, E. A., and Tee, A. R. (2009). Mammalian target of rapamycin complex 1: signalling inputs, substrates and feedback mechanisms. Cell Signal. 21, 827-835.
9. Edirisinghe, I., Yang, S. R., Yao, H., Rajendrasozhan, S., Caito, S., Adenuga, D., Wong, C., Rahman, A., Phipps, R. P., Jin, Z. G., et al. (2008). VEGFR-2 inhibition augments cigarette smoke-induced oxidative stress and inflammatory responses leading to endothelial dysfunction. FASEB J. 22, 2297-2310.
10. Fang, Y., Vilella-Bach, M., Bachmann, R., Flanigan, A., and Chen, J. (2001). Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294, 1942-1945.
11. Fini, M. E., Plucinska, I. M., Mayer, A. S., Gross, R. H., and Brinckerhoff, C. E. (1987). A gene for rabbit synovial cell collagenase: member of a family of metalloproteinases that degrade the connective tissue matrix. Biochemistry 26, 6156-6165.
12. Forsdahl, S. H., Singh, K., Solberg, S., and Jacobsen, B. K. (2009). Risk factors for abdominal aortic aneurysms: a 7-year prospective study: the Tromsø Study, 1994-2001. Circulation 119, 2202-2208.
13. Fujioka, K., and Shibamoto, T. (2006). Determination of toxic carbonyl compounds in cigarette smoke. Environ. Toxicol. 21, 47-54.
14. Galis, Z. S., Sukhova, G. K., Lark, M. W., and Libby, P. (1994). Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J. Clin. Invest. 94, 2493-2503.
15. Gleason, C. E., Lu, D., Witters, L. A., Newgard, C. B., and Birnbaum, M. J. (2007). The role of AMPK and mTOR in nutrient sensing in pancreatic betacells. J. Biol. Chem. 282, 10341-10351.
16. Hardie, D. G. (2004). The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell Sci. 117, 5479-5487.
17. Hashimoto, G., Inoki, I., Fujii, Y., Aoki, T., Ikeda, E., and Okada, Y. (2002). Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165. J. Biol. Chem. 277, 36288-36295.
18. Hoe, H. S., Cooper, M. J., Burns, M. P., Lewis, P. A., van der Brug, M., Chakraborty, G., Cartagena, C. M., Pak, D. T., Cookson, M. R., and Rebeck, G. W. (2007). The metalloprotease inhibitor TIMP-3 regulates amyloid precursor protein and apolipoprotein E receptor proteolysis. J. Neurosci. 27, 10895-10905.
19. Imai, K., Dalal, S. S., Chen, E. S., Downey, R., Schulman, L. L., Ginsburg, M., and D'Armiento, J. (2001). Human collagenase (matrix metalloproteinase-1) expression in the lungs of patients with emphysema. Am. J. Respir. Crit. Care Med. 163, 786-791.
20. Irizarry, E., Newman, K. M., Gandhi, R. H., Nackman, G. B., Halpern, V., Wishner, S., Scholes, J. V., and Tilson, M. D. (1993). Demonstration of interstitial collagenase in abdominal aortic aneurysm disease. J. Surg. Res. 54, 571-574.
21. Lamalice, L., Le Boeuf, F., and Huot, J. (2007). Endothelial cell migration during angiogenesis. Circ. Res. 100, 782-794.
22. Lemaitre, V., O'Byrne, T. K., Borczuk, A. C., Okada, Y., Tall, A. R., and D'Armiento, J. (2001). ApoE knockout mice expressing human matrix metalloproteinase-1 in macrophages have less advanced atherosclerosis. J. Clin. Invest. 107, 1227-1234.
23. Libby, P., Aikawa, M., and Jain, M. K. (2006). Vascular endothelium and atherosclerosis. Handb. Exp. Pharmacol. 176, 285-306.
24. Ma, X. M., and Blenis, J. (2009). Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318.
25. Mahmoodi, M., Sahebjam, S., Smookler, D., Khokha, R., and Mort, J. S. (2005). Lack of tissue inhibitor of metalloproteinases-3 results in an enhanced inflammatory response in antigen-induced arthritis. Am. J. Pathol. 166, 1733-1740.
26. Mercer, B. A., Kolesnikova, N., Sonett, J., and D'Armiento, J. (2004). Extracellular regulated kinase/mitogen activated protein kinase is upregulated in pulmonary emphysema and mediates matrix metalloproteinase-1 induction by cigarette smoke. J. Biol. Chem. 279, 17690-17696.
27. Mercer, B. A., Wallace, A. M., Brinckerhoff, C. E., and D'Armiento, J. M. (2009). Identification of a cigarette smoke-responsive region in the distal MMP-1 promoter. Am. J. Respir. Cell Mol. Biol. 40, 4-12.
28. Mullick, A. E., McDonald, J. M., Melkonian, G., Talbot, P., Pinkerton, K. E., and Rutledge, J. C. (2002). Reactive carbonyls from tobacco smoke increase arterial endothelial layer injury. Am. J. Physiol. Heart Circ. Physiol. 283, H591-H597.
29. Newby, A. C. (2005). Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol. Rev. 85, 1-31.
30. Nikkari, S. T., O'Brien, K. D., Ferguson, M., Hatsukami, T., Welgus, H. G., Alpers, C. E., and Clowes, A. W. (1995). Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation 92, 1393-1398.
31. Park, Y. S., Kim, J., Misonou, Y., Takamiya, R., Takahashi, M., Freeman, M. R., and Taniguchi, N. (2007). Acrolein induces cyclooxygenase-2 and prostaglandin production in human umbilical vein endothelial cells: roles of p38 MAP kinase. Arterioscler. Thromb. Vasc. Biol. 27, 1319-1325.
32. Partridge, C. R., Hawker, J. R., Jr., and Forough, R. J. (2000). Overexpression of a secretory form of FGF-1 promotes MMP-1-mediated endothelial cell migration. J. Cell. Biochem. 78, 487-499.
33. Poulalhon, N., Farge, D., Roos, N., Tacheau, C., Neuzillet, C., Michel, L., Mauviel, A., and Verrecchia, F. (2006). Modulation of collagen and MMP-1 gene expression in fibroblasts by the immunosuppressive drug rapamycin. A direct role as an antifibrotic agent? J. Biol. Chem. 281, 33045-33052.
34. Qi, J. H., Ebrahem, Q., Moore, N., Murphy, G., Claesson-Welsh, L., Bond, M., Baker, A., and Anand-Apte, B. (2003). A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat. Med. 9, 407-415.
35. Raij, L., DeMaster, E. G., and Jaimes, E. A. (2001). Cigarette smoke-induced endothelium dysfunction: role of superoxide anion. J. Hypertens. 19, 891-897.
36. Saunders, W. B., Bayless, K. J., and Davis, G. E. (2005). MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J. Cell Sci. 118, 2325-2340.
37. Saunders, W. B., Bohnsack, B. L., Faske, J. B., Anthis, N. J., Bayless, K. J., Hirschi, K. K., and Davis, G. E. (2006). Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J. Cell. Biol. 175, 179-191.
38. Schonbeck, U., Mach, F., and Libby, P. (1998). Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J. Immunol. 161, 3340-3346.
39. Shao, B., Fu, X., McDonald, T. O., Green, P. S., Uchida, K., O'Brien, K. D., Oram, J. F., and Heinecke, J. W. (2005). Acrolein impairs ATP binding cassette transporter A1-dependent cholesterol export from cells through sitespecific modification of apolipoprotein A-I. J. Biol. Chem. 280, 36386-36396.
40. Staskus, P. W., Masiarz, F. R., Pallanck, L. J., and Hawkes, S. P. (1991). The 21-kDa protein is a transformation-sensitive metalloproteinase inhibitor of chicken fibroblasts. J. Biol. Chem. 266, 449-454.
41. Trivedi, V., Boire, A., Tchernychev, B., Kaneider, N. C., Leger, A. J., O'Callaghan, K., Covic, L., and Kuliopulos, A. (2009). Platelet matrix metalloprotease-1 mediates thrombogenesis by activating PAR1 at a cryptic ligand site. Cell 137, 332-343.
42. Uchida, K., Kanematsu, M., Morimitsu, Y., Osawa, T., Noguchi, N., and Niki, E. (1998). Acrolein is a product of lipid peroxidation reaction. Formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J. Biol. Chem. 273, 16058-16066.
43. Vincenti, M. P., Coon, C. I., Mengshol, J. A., Yocum, S., Mitchell, P., and Brinckerhoff, C. E. (1998). Cloning of the gene for interstitial collagenase-3 (matrix metalloproteinase-13) from rabbit synovial fibroblasts: differential expression with collagenase-1 (matrix metalloproteinase-1). Biochem. J. 331, 341-346.
44. Weber, B. H., Vogt, G., Pruett, R. C., Stohr, H., and Felbor, U. (1994). Mutations in the tissue inhibitor of metalloproteinases-3 (TIMP3) in patients with Sorsby's fundus dystrophy. Nat. Genet. 8, 352-356.