Lysyl oxidase, a critical intra- and extra-cellular target in the lung for cigarette smoke pathogenesis

International Journal of Environmental Research and Public Health

Volumn 8, Issue 1, 2011, Pages 161-184

  Li, Wande ^a   Zhou, Jing ^a   Chen, Lijun ^b   Luo, Zhijun ^a   Zhao, Yinzhi ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

4 (methylnitrosamino) 1 (3 pyridyl) 1 butanone (NNK); Cadmium (CD); Carcinogenesis; Cigarette smoke (CS); CS condensate (CSC); Emphysema; Lysyl oxidase (LO)

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; CADMIUM; CIGARETTE SMOKE; CIGARETTE SMOKE CONDENSATE; CIS ACTING ELEMENT; NUCLEAR FACTOR I; PROTEIN LYSINE 6 OXIDASE;

BINDING AFFINITY; BINDING SITE; CELL PROLIFERATION; CHEMICAL CARCINOGENESIS; DNA RESPONSIVE ELEMENT; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME STRUCTURE; GENE EXPRESSION REGULATION; HUMAN; LUNG CANCER; LUNG CARCINOGENESIS; LUNG EMPHYSEMA; NONHUMAN; ONCOGENE RAS; PATHOGENESIS; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; REVIEW; TRANSCRIPTION REGULATION;

EID: 79851501960     PISSN: None     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph8010161     Document Type: Review

References (126)

1. American Lung Association in Washington. Lung Disease, 2011. Available online: http://www.alaw.org/lung disease (accessed on 17 January 2011).
2. E-Medicine Health. Lung Cancer, 2011. Available online: http://www.emedicinehealth.com/lung_cancer/article_em.htm (accessed on 17 January 2011).
3. Mackay, J.; Eriksen, M. The Tobacco Atlas; WHO: Geneva, Switzerland, 2002.
4. Hecht, S.S. Cigarette smoke and lung cancer: chemical mechanisms and approaches to prevention. Lancet Oncol. 2002, 3, 461-469.
5. Leischow, S.J.; Djordjevic, M.V. Smoking reduction and tobacco-related cancers: The more things change, the more they stay the same. J. Natl. Cancer Inst. 2004, 96, 86-87.
6. American Cancer Society. Tobacco-related Cancers Fact Sheet, 2011. Available online: http://www.cancer.org/Cancer/CancerCauses/TobaccoCancer/tobacco-related-cancer-fact-sheet (accessed on 17 January 2011).
7. Snider, G.L.; Lucey, E.C.; Stone, P.J. Animal models of emphysema. Am. Rev. Respir. Dis. 1986, 133, 149-169.
8. Hautamaki, R.D.; Kobayashi, D.K.; Senior, R.M.; Shapiro, S.D. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 1997, 277, 2002-2004.
9. Shapiro, S.D.; Goldstein, N.M.; Houghton, A.M.; Kobayashi, D.K; Kelley, D.; Belaaouaj, A. Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice. Am. J. Pathol. 2003, 163, 2329-2335.
10. Wright, J.L.; Churg, A. Smoke-induced emphysema in guinea pigs is associated with morphometric evidence of collagen breakdown and repair. Am. J. Physiol. 1995, 268, L17-20.
11. D'Armiento, J.L.; Dalal, S.S.; Okada, Y.; Berg, R.A.; Chada, K. Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell 1992, 71, 955-961.
12. Kuper, H.; Boffetta, P.; Adami, H.O. Tobacco use and cancer causation: association by tumour type. J. Intern. Med. 2002, 252, 206-224.
13. Mulcahy, S. The toxicology of cigarette smoke and environmental tobacco smoke. 2011. Available online: http://www.skynet.ie/~stephen/reports/bc4927.html (accessed on 17 January 2011).
14. Hoffmann, D.; Wynder, E.L. Active and passive smoking. In Toxicology; Marquardt, H., Schaefer, S.G., McClellan, R., Welsch, F., Eds.; Academic Press: New York, NY, USA, 1999; pp. 879-898.
15. Hoffmann, D.; Hoffmann, I.; El-Baypumy, K. The less harmful cigarette: a controversial issue. A tribute to Ernst L. Wynder. Chem. Res. Toxicol. 2001, 14, 767-790.
16. Church, T.; Pryor, W.A. Free-radical chemistry of cigarette smoke and its toxilogical implications. Environ. Health Perspect. 1985, 64, 111-126.
17. Schick, S.; Glantz, S. Philip Morris toxicological experiments with fresh sidestream smoke: More toxic than mainstream smoke. Tob. Control 2005, 14, 396-404.
18. Hecht, S.S. Biochemistry, biology and carcinogenicity of tobacco-specific N-nitrosamines. Chem. Res. Toxicol. 1998, 11, 560-603.
19. Chepiga, T.; Morton, M.; Murphy, P.; Avalos, J.; Bombick, B.; Doolittle, D.; Borgerding, M.; Swauger, J. A comparison of the mainstream smoke chemistry and mutagenicity of a representative sample of the US cigarette market with two Kentucky reference cigarettes (K1R4F and K1R5F). Food Chem. Toxicol. 2000, 38, 949-962.
20. Belinsky, S.A.; Foley, J.F.; White, C.M.; Anderson, M.W.; Maronpot, R.R. Dose-response relationship between O6-methylguanine formation in Clara cells and induction of pulmonary neoplasia in rat by 4-(methyl nitrosamino)-1-(3-pyridyl)-1-butanone. Cancer Res. 1990, 50, 3772-3780.
21. Jalas, J.R.; Ding, X.; Murphy, S.E. Comparative metabolism of the tobacco-specific nitrosamines 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol by rat cytochrome P450 2A3 and human cytochrome P450 2A13. Drug Metab. Dispos. 2003, 31, 1199-1202.
22. Lin, R.K.; Hsieh, Y.S.; Lin, P.; Hsu, H.S.; Chen, C.Y.; Tang, Y.A.; Lee, C.F.; Wang,Y.C. The tobacco-specific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients. J. Clin. Invest. 2010, 120, 521-532.
23. Castonguay, A.; Foiles, P.G.; Trushin, N.; Hecht, S.S. Study of DNA methylation by tobacco-specific N-nitrosamines. Environ. Health Perspect. 1985, 62, 197-202.
24. Pfeifer, G.P.; Denissenko, M.F.; Olivier, M.; Tretyakova, N.; Hecht, S.S.; Hainaut, P. Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 2002, 21, 7435-7451.
25. Beryllin, Cadmium, Mercury and Exposures in the Glass Manufacturing Industry. In Monographs on the Evaluation of Carcinogenic Risk to Humans; IARC: Lyon, France, 1993; Volume 58, pp. 119-236.
26. Tobacco Smoke and Involuntary Smoking. In Monographs on the Evaluation of Carcinogenic Risk of Chemicals to Humans; IARC: Lyon, France, 2004; Volume 83.
27. Post, C.; Johansson, B.; Allenmark, S. Organ distribution and protein binding of cadmium in autopsy material from heavy smokers. Environ. Res. 1984, 34, 29-37.
28. Paakko, P.; Kokkonen, P.; Anttila, S.; Kalliomaki, P.-L. Cadmium and chromium as markers of smoking in human lung tissue. Environ. Res. 1989, 49, 197-207.
29. Coultas, D.B.; Samet, J.M. Cigarette smoking. In Clinical Epidemiology of Chronic Obstractive Pulmonary Disease; Hensley, M.J., Saunders, N.A., Eds.; Marcel Dekker: New York, NY, USA, 1989; pp.109-138.
30. Davision, A.G.; Newman-Taylor, A.J.; Darbyshire, J.; Chettle, D.R.; Guthrie, C.J.G.; O'Malley, D.; Mason, H.J.; Fayers, P.M.; Venables, K.M.; Pickering, C.A.C.; Franklin, D.; Scott, M.C.; Holden, H.; Wright, A.L. Cadmium fume inhalation and emphysema. Lancet 1988, 1, 663-667.
31. Kazantzis, G.; Blacks, R.G. A mortality study of cadmium exposed workers. In Proceedings of the Seventh International Cadmium Conference, New Orleans, LA, USA, 6-8 April 1992; Cook, M.E., Hiscock, S.A., Morrow, H., Volpe, R.A., Eds.; Cadmium Association/Cadmium Council: New Orleans, LA, USA/Reston, VA, USA, 1992; pp. 150-157.
32. Lane, R.E.; Campbell, A.C.P. Fatal emphysema in two men making a copper cadmium alloy. Brit. J. Indust. Med. 1954, 11, 118-122.
33. Kimbel, P. Proteolytic damage and emphysema pathogenesis. In Chronic Obstructive Pulmonary Disease; Petty, T.L., Ed.; Marcel Dekker: New York, NY, USA, 1985; pp. 105-127.
34. Snider, G.L.; Hayes, J.A.; Korthy, A.L.; Lewis, G.P. Centrilobular emphysema experimentally induced by cadmium chloride aerosol. Am. Rev. Respir. Dis. 1973, 108, 40-47.
35. Waisberg, M.; Joseph, P.; Hale, B.; Beyersmann, D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003, 192, 95-117.
36. Ninth Report on Carcinogens; National Toxicology Program: Research Triangle Park, NC, USA, 2000.
37. Glaser, U.; Hochrainer, D.; Otto, F.J.; Oldiges, H. Carcinogenicity and toxicity of four cadmium compounds inhaled by rats. Toxicol. Environ. Chem. 1990, 27, 153-162.
38. Takenaka, S.; Oldiges, H.; Konig, H.; Hochrainer, D.; Oberdorster, G. Carcinogenicity of cadmium chloride aerosols in W. rats. J. Natl. Cancer Inst. 1983, 70, 367-373.
39. Gao, S.; Chen, K.; Zhao, Y.; Rich, C.B.; Chen, L.; Li, S.J.; Toselli, P.; Stone, P.; Li, W. Transcriptional and posttranscriptional inhibition of lysyl oxidase expression by cigarette smoke condensate in cultured rat fetal lung fibroblasts. Toxicol. Sci. 2005, 87, 197-203.
40. Chen, L.-J.; Zhao, Y.; Gao, S.; Chou, I.-N.; Toselli, P.; Stone, P.; Li, W. Downregulation of lysyl oxidase and upregulation of cellular thiols in rat fetal lung fibroblasts treated with cigarette smoke condensate. Toxicol. Sci. 2005, 83, 372-379.
41. Kagan, H.M.; Li, W. Lysyl oxidase: Properties, specificity and biological roles inside of the cell. J. Cell. Biochem. 2003, 88, 660-672.
42. Giampuzzi, M.; Oleggini, R.; Di Donato, A. Demonstration of in vitro interaction between tumor suppressor lysyl oxidase and histone H1 and H2: Definition of the regions involved. Biochim. Biophys. Acta 2003, 1647, 245-251.
43. Kagan, H.M.; Williams, M.A.; Calaman, S.D.; Berkowitz, E.M. Histone H1 is a substrate for lysyl oxidase and contains endogenous sodium borotritide-reducible residues. Biochem. Biophys. Res. Commun. 1983, 115, 186-192.
44. Li, W.; Nugent, M.A.; Zhao, Y.; Chau, A.N.; Li, S.J.; Chou, I.N.; Liu, G.; Kagan, H.M. Lysyl oxidase oxidizes basic fibroblast growth factor and inactivates its mitogenic potential. J. Cell Biochem. 2003, 88, 152-164.
45. Li, W.; Nellaiappan, K.; Strassmaier, T.; Graham, L.; Thomas, K.M.; Kagan, H.M. Localization and activity of lysyl oxidase within nuclei of fibrogenic cells. Proc. Natl. Acad. Sci. USA 1997, 94, 12817-12822.
46. Mello, M.L.S.; Contente, S.; Vidal, B.C.; Planding, W.; Schenck, U. Modulation of ras transformation affecting chromatin supraorganization as assessed by image analysis. Exp. Cell Res. 1995, 220, 374-382.
47. Nellaiappan, K.; Risitano, A.; Liu, G.; Nicklas, G.; Kagan, H.M. Fully processed lysyl oxidase catalyst translocates from the extracellular space into nuclei of aortic smooth muscle cells. J. Cell. Biochem. 2000, 79, 576-582.
48. Lazarus, H.M.; Cruikshank, W.W.; Narasimhan, N.; Kagan, H.M.; Center, D.M. Induction of human monocyte motility by lysyl oxidase. Matrix Biol. 1995, 14, 727-731.
49. Lucero, H.A.; Ravid, K.; Grimsby, J.L.; Rich, C.B.; DiCamillo, S.J.; Mäki, J.M.; Myllyharju, J.; Kagan, H.M. Lysyl oxidase oxidizes cell membrane proteins and enhances the chemotactic response of vascular smooth muscle cells. J. Biol. Chem. 2008, 283, 24103-24117.
50. Li, W.; Liu, G.; Chou, I.-N.; Kagan, H.M. Hydrogen peroxide-mediated, lysyl oxidase-dependent chemotaxis of vascular smooth muscle cells. J. Cell. Biochem. 2000, 78, 550-557.
51. Erler, J.T.; Bennewith, K.L.; Nicolau, M.; Dornhofer, N.; Kong, C.; Le, Q.T.; Chi, J.T.; Jeffrey, S.S.; Giaccia, A.J. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006, 440, 1222-1226.
52. Kenyon, K.; Contente, S.; Trackman, P.C.; Tang, J.; Kagan, H.M.; Friedman, R.M. Lysyl oxidase and rrg messenger RNA. Science 1991, 253, 802.
53. Kosonen, T.; Uriu-Hare, J.Y.; Clegg, M.S.; Keen, C.L.; Rucker, R.B. Incorporation of copper into lysyl oxidase. Biochem. J. 1997, 327, 283-289.
54. Wan, S.X.; Mure, M.; Medzihradszky, K.F.; Burlingame, A.L.; Brown, D.E.; Dooley, D.M.; Smith, A.J.; Kagan, H.M.; Klinman, J.P. A crosslinked cofactor in lysyl oxidase: Redox function for amino acid side chains. Science 1996, 273, 1078-1084
55. Gacheru, S.N.; Trackman, P.C.; Shah, M.A.; O'Gara, C.Y.; Spacciapoli, P.; Greenaway, F.T.; Kagan, H.M. Structural and catalytic properties of copper in lysyl oxidase. J. Biol. Chem. 1990, 265, 19022-19027.
56. Csiszar, K. Lysyl oxidases: A novel multifunctional amine oxidase family. Prog. Nucleic Acid Res. Mol. Biol. 2001, 70, 1-32.
57. Bazan, J.F. A novel family of growth factor receptors: A common binding domain in the growth hormone, prolactin, erythropoietin and IL-6 receptors and the p75 IL-2 receptor β-chain. Biochem. Biophys. Res. Commun. 1989, 164, 788-795.
58. Bazan, J.F, Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. USA 1990, 87, 6934-6938.
59. Gao, S.; Zhao, Y.; Kong, L.; Toselli, P.; Chou, I.-N.; Stone, P.; Li, W. Cloning and characterization of the rat lysyl oxidase gene promoter: Identification of core promoter elements and functional nuclear factor I binding sites. J. Biol. Chem. 2007, 282, 25322-25337.
60. Corden, J.; Wasylyk, B.; Buchwalder, A.; Sassone-Corsi, P.; Kedinger, C.; Chambon, P. Promoter sequences of eukaryotic protein-coding genes. Science 1980, 209, 1406-1414.
61. Smale, S.T.; Kadonaga, J.T. The RNA polymerase II core promoter. Annu. Rev. Biochem. 2003, 72, 449-479.
62. Gronostajski, R.M. Roles of the NFI/CTF gene family in transcription and development. Gene 2000, 249, 31-45.
63. Bandyopadhyay, S.; Gronostajski, R.M. Identification of a conserved oxidation-sensitive cysteine residue in the NFI family of DNA binding proteins. J. Biol. Chem. 1994, 269, 29949-29955.
64. Bandyopadhyay, S.; Starke, D.W.; Mieyal, J.J.; Gronostajski, R.M. Thioltranferase (Glutaredoxin) reactivates the DNA-binding activity of oxidation-inactivated Nuclear Factor I. J. Biol. Chem. 1998, 273, 392-397.
65. Semenza, G.L. Expression of hypoxia-inducible factor 1: Mechanism and consequences. Biochem. Pharmacol. 2000, 59, 47-53.
66. Déry, M.A.; Michaud, M.D.; Richard, D.E. Hypoxia-inducible factor 1: Regulation by hypoxic and non-hypoxic activators. Int. J. Biochem. Cell Biol. 2005, 37, 535-540.
67. Giedroc, D.P.; Chen, X.; Apuy, J.L. Metal response element (MRE) binding transcription factor-1 (MTF-1): Structure, function, and regulation. Antioxid. Redox Signal. 2001, 3, 577-596.
68. Stuart, G.W.; Searle, P.F.; Chen, H.Y.; Brinster, R.; Palmiter, R.D. A 12-base pair DNA motif that is repeated several times in metallothione gene promoters confers metal regulation to a heterologous. Proc. Natl. Acad. Sci. USA 1984, 81, 7318-7322.
69. Lichtlen, P.; Wang, Y.; Belser, T.; Georgiev, O.; Certa, U.; Sack, R.; Schaffner, W. Target gene search for the metal-responsive transcription factor MTF-1. Nuc. Aci. Res. 2001, 29, 1514-1523.
70. Copple, I.M.; Goldring, C.E.; Kitteringham, N.R.; Park, B.K. The Nrf2-Keap1 defence pathway: Role in protection against drug-induced toxicity. Toxicology 2008, 246, 24-33.
71. Wang, G.L.; Jiang, B.-H.; Rue, E.A.; Semenza, G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA. 1995, 92, 5510-5514.
72. Weissmann, N. Hypoxia-driven mechanisms in lung biology and disease: a new review series of the ERS Lung Science Conference. Eur. Respir. J. 2008, 3, 697-698.
73. Yasuo, M.; Mizuno, S.; Kraskauskas, D.; Bogaard, H.J.; Natarajan, R.; Cool, C.D.; Zamora, M.; Voelkel, N.F. Hypoxia inducible factor-1 {alpha} in human emphysema lung tissue. Eur. Respir. J. 2010, doi:10.1183/09031936.00022910, (Epub ahead of print).
74. Wang, G.L.; Semenza, G.L. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: Implications for models of hypoxia signal transduction. Blood 1993, 82, 3610-3615.
75. Epstein, A.C.; Gleadle, J.M.; McNeill, L.A.; Hewitson, K.S.; O'Rourke, J.; Mole, D.R.; Mukherji, M.; Metzen, E.; Wilson, M.I.; Dhanda, A.; Tian, Y.M.; Masson, N.; Hamilton, D.L.; Jaakkola, P.; Barstead, R.; Hodgkin, J.; Maxwell, P.H.; Pugh, C.W.; Schofield, C.J.; Ratcliffe, P.J. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107, 43-54.
76. Zhao, Y.; Gao, S.; Chou, I.-N.; Toselli, P.; Stone, P.; Li, W. Inhibition of the expression of lysyl oxidase and its substrates in cadmium-resistant rat fetal lung fibroblasts. Toxicol. Sci. 2006, 90, 478-489.
77. Chou, D.K.; Zhao, Y.; Gao, S.; Chou, I.-N.; Toselli, P.; Stone, P.; Li, W. Perturbation of copper (Cu) homeostasis and expression of Cu-binding proteins in cadmium-resistant lung fibroblasts. Toxicol Sci. 2007, 99, 267-276.
78. Dubic, M.A.; Keen, C.L.; Rucker, R.B. Elastin metabolism during prenatal lung development in the copper-deficient rat. Exp. Lung Res. 1985, 8, 227-241.
79. Harris, E.D. Biochemical defect in chick lung resulting from copper deficiency. J. Nutr. 1986, 116, 252-258.
80. Soskel, N.T.; Watanabe, S.; Sandberg, L.B. Mechanisms of lung injury in the copper-deficient hamster model of emphysema. Chest 1984, 85, 70s-72s.
81. Richards, M.P. Recent developments in trace element metabolism and function: Role of metallothionein in copper and zinc metabolism. J. Nutr. 1989, 119, 1062-1070.
82. Brouwer, M.; Hoexum-Brouwer, T.; Cashon, R.E. A putative glutathione-binding site in CdZn-metallothionein identified by epuilibrium binding and molecular modelling studies. Biochem. J. 1993, 294, 219-225.
83. Briggs, R.W.; Armitage, I.M. Evidence for site-selective metal binding in calf liver metallothionein. J. Biol. Chem. 1982, 257, 1259-1262.
84. Morris, P.E.; Bernard, G.R. Significance of glutathione in lung disease and implications for therapy. Am. J. Med. Sci. 1994, 307, 119-127.
85. Li, X.Y.; Donaldson, K.; Rahman, I.; MacNee, W. An investigation of the role of glutathione in the increased permeability induced by cigarette smoke in vivo and in vitro. Am. Rev. Respir. Crit. Care Med. 1994, 149, 1518-1525.
86. Rahman, I.; Li, X.Y.; Donaldson, K.; Harrison, H.J.; MacNee, W. Glutathione homeostasis in alveolar epithelial cells in vitro and lung in vivo under oxidative stress. Am. J. Physiol. 1995, 269, L285-L292.
87. Rahman, I. Regulation of glutathione in inflammation and chronic lung diseases. Mutat. Res. 2005, 579, 58-80.
88. Zhao, Y.; Chen, L.; Gao, S.; Toselli, P.; Stone, P.; Li, W. The critical role of the cellular thiol homeostasis in cadmium perturbation of the lung extracellular matrix. Toxicology 2010, 267, 60-69.
89. Li, W.; Chou, I.-N.; Boak, A.; Kagan, H.M. Down-regulation of lysyl oxidase in cadmium-resistant fibroblasts. Am. J. Respir. Cell Mol. Biol. 1995, 13, 418-425.
90. Li, W.; Zhao, Y.; Toselli, P.; Stone, P. Cigarette smoke condensate downregulation of lysyl oxidase transcription mediated by inactivation of nuclear factor I. Toxicologist 2008, 102, 227, (abstract).
91. Li, W.; Zhao, Y.; Gao, S.; Toselli, P. Transcriptional regulation of the lysyl oxidase gene by the hypoxia-inducible factor 1. FASEB J. 2010, 24 (Meeting Abstract Supplement), No. 833.16, (abstract).
92. Galan, A.; Garcia-Bermejo, L.; Troyano, A.; Vilaboa, N.E.; Fernandez, C.; de Blas, E.; Aller, P. The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-ray). Eur. J. Cell Biol. 2001, 80, 312-320.
93. Zhao, Y.; Gao, S.; Zhou, J.; Toselli, P.; Li, W. NNK, a tobacco-specific carcinogen, inhibits the expression of lysyl oxidase, a tumor suppressor gene. Toxicologist 2011, (abstract in press).
94. Bestor, T.H. The DNA methyltransferase of mammals. Hum. Mol. Genet. 2000, 9, 2395-2402.
95. Ng, H.H.; Bird, A. DNA methylation and chromatin modification. Curr. Opin. Genet. Dev. 1999, 9, 158-163.
96. Takiguchi, M.; Achanzar, W.E.; Qu, W.; Li, G.; Waalkes, M.P. Effects of cadmium on DNA-(cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp. Cell Res. 2003, 286, 355-365.
97. Downs, J.A. Histone H3 K56 acetylation, chromatin assembly, and the DNA damage checkpoint. DNA Repair 2008, 7, 2020-2024.
98. Xu, G.-L.; Bestor, T.H.; Bourchis, D.; Hsieh, C.L.; Tommerrup, N.; Bugge, M.; Hulten, M.; Qu, X.; Russo, J.J.; Viegas-Pequignot, E. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 1999, 402, 187-191.
99. Gisselsson, D.; Bjork, J.; Hoglund, M.; Mertens, F.; Cin, P.D.; Akerman, M.; Mandahl, N. Abnormal nuclear shape in solid tumors reflects mitotic instability. Am. J. Pathol. 2001, 158, 199-206.
100. Davidson, J.M. Biochemistry and turnover of lung interstitium. Eur. Respir. J. 1990, 3, 1048-1063.
101. Campa, J.S.; Harrison, N.K.; Laurent, G. Regulation of matrix production in the airways. In T-Lymphocyte and Inflammatory Cell Research in Asthma; Jolles, G., Karlsson, J-A., Taylor, J., Eds.; Academic Press: London, UK, 1993; pp. 221-235.
102. Snider, G.L. Emphysema: the first two centuries-and beyond. Am. Rev. Respir. Dis. 1992, 146, 1615-1622.
103. Soskel, N.T.; Watanabe, S.; Hammond, E.; Sandberg, L.B.; Renzetti, A.D., Jr.; Crapo, J.D. A copper-deficient, zinc-supplemented diet produces emphysema in pig. Am. Rev. Respir. Dis. 1982, 126, 316-325.
104. Chvapil, M.; Misiorowski, R. In vivo inhibition of lysyl oxidase by high dose of zinc. Proc. Soc. Exp. Biol. Med. 1980, 164, 137-141.
105. Grange, D.K.; Kaler, S.G.; Albers, G.M.; Petterchak, J.A.; Thorpe, C.M.; DeMello, D.E. Severe bilateral panlobular emphysema and pulmonary arterial hypoplasia: unusual manifestations of Menkes disease. Am. J. Med. Genet. 2005, 139A, 151-155.
106. Kuhn, C.; Starcher, B.C. The effects of lathyrogens on the evolution of elastase-induced emphysema. Am. Rev. Respir. Dis. 1980, 122, 453-460.
107. Niewoehner, D.E.; Hoidal, J.R. Lung fibrosis and emphysema: Divergent responses to a common injury. Science 1982, 217, 359-360.
108. Fisk, D.E.; Kuhn, C. Emphysema-like changes in the lungs of blotchy mouse. Am. Rev. Respir. Dis. 1976, 113, 787-797.
109. Warburton, D.; Shi, W. Lo, and the niche is knit: Lysyl oxidase activity and maintenance of lung, aorta, and skin integrity. Am. J. Pathol. 2005, 167, 921-922.
110. Liu, X.; Zhao, Y.; Gao, J.; Pawlyk, B.; Starcher, B.; Spencer, J.A.; Yanagisawa, H.; Zuo, J.; Li, T. Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat. Genet. 2004, 36, 178-182.
111. Maki, J.M.; Sormunen, R.; Lippo, S.; Kaarteenaho-Wiik, R.; Soininen, R.; Myllyharju, J. Lysyl oxidase is essential for normal development and function of the respiratory system and for the integrity of elastic and collagen fibers in various tissues. Am. J. Pathol. 2005, 167, 927-936.
112. Laurent, P.; Janoff, A.; Kagan, H.M. Cigarette smoke blocks cross-linking of elastin in vitro. Am. Rev. Respir. Dis. 1983, 127, 189-192.
113. Jackson, L.E.; Faris, B.; Martin, B.M.; Jones, H.V.; Rich, C.B.; Foster, J.A.; Franzblau, C. The effect of β-aminopropionitrile on elastin gene expression in smooth muscle cell cultures. Biochem. Biophys. Res. Commun. 1991, 179, 939-944.
114. Giampuzzi, M.; Botti, G.; Duca, M.D.; Arata, L.; Ghiggeri, G.; Gusmano, R.; Ravazzolo, R.; Donato, A.D. Lysyl oxidase activates the transcription activity of human collagene III promoter. J. Biol. Chem. 2000, 275, 36341-36349.
115. Giampuzzi, M.; Botti, G.; Gilli, M.; Gusmano, R.; Borel, A.; Sommer, P.; Di Donato, A. Down-regulation of lysyl oxidase-induced tumorigenic transformation in NRK-49F cells characterized by constitutive activation of ras-proto-oncogene. J. Biol. Chem. 1995, 276, 29226-29232.
116. Hamalainen, E.R.; Kemppainen, R.; Kuivaniemi, H.; Tromp, G.; Vaheri, A.; Pihlajaniemi, T.; Kivirikko, K.I. Quantitative polymerase chain reaction of lysyl oxidase mRNA in malignantly transformed human cell lines demonstrates that their low lysyl oxidase activity is due to low quantities of its mRNA and low levels of transcription of the respective gene. J. Biol. Chem. 1995, 270, 21590-21593.
117. Woznick, A.R.; Braddock, A.L.; Dulai, M.; Seymour, M.L.; Callahan, R.E.; Welsh, R.J.; Chmielewski, G.W.; Zelenock, G.B.; Shanley, C.J. Lysyl oxidase expression in bronchogenic carcinoma. Am. J. Surg. 2005, 189, 297-301.
118. Kaneda, A.; Wakazono, K.; Tsukamoto, T.; Watanabe, N.; Yagi, Y.; Tatematsu, M.; Kaminishi, M.; Sugimura, T.; Ushijima, T. Lysyl oxidase is a tumor suppressor gene inactivated by methylation and loss of heterozygosity in human gastric cancers. Cancer Res. 2004, 64, 6410-6415.
119. Rost, T.; Pyritz, V.; Rathcke, I.O.; Gorogh, T.; Dunne, A.A.; Werner, J.A. Reduction of LOX- and LOXL2-mRNA expression in head and neck squamous cell carcinomas. Anticancer Res. 2003, 23, 1565-1573.
120. Wu, M.; Min, C.; Wang, X.; Yu, Z.; Kirsch, K.H.; Trackman, P.C.; Sonenshein, G.E. Repression of BCL2 by the tumor suppressor activity of the lysyl oxidase propeptide inhibits transformed phenotype of lung and pancreatic cancer cells. Cancer Res. 2007, 67, 6278-6285.
121. Ren, C.; Yang, G.; Timme, T.L.; Wheeler, T.M.; Thompson, T.C. Reduced lysyl oxidase messenger RNA levels in experimental and human prostate cancer. Cancer Res. 1998, 58, 1285-1290.
122. Decitre, M.; Gleyzal, C.; Raccurt, M.; Peyrol, S.; Aubert-Foucher, E.; Csiszar, K.; Sommer, P. Lysyl oxidase-like protein localizes to sites of de novo fibrinogenesis and in the early stromal reaction of ductal breast carcinomas. Lab. Invest. 1998, 78, 143-151.
123. Peyrol, S.; Raccurt, M.; Gerard, F.; Gleyzal, C.; Grimaud, J.A.; Sommer, P. Lysyl oxidase gene expression in the stromal reaction to in situ and invasive ductal breast carcinoma. Am. J. Pathol. 1997, 150, 497-507.
124. Bouez, C.; Reynaud, C.; Noblesse, E.; Thépot, A.; Gleyzal, C.; Kanitakis, J.; Perrier, E.; Damour, O.; Sommer, P. The lysyl oxidase (LOX) is absent in basal and squamous cell carcinomas and its knockdown induces an invading phenotype in a skin equivalent model. Clin. Cancer Res. 2006, 12, 1463-1469.
125. Csiszar, K.; Fong, F.S.T.; Ujfalusi, A; Krawetz, S.A.; Salvati, E.P.; Mackenzie, J.W.; Boyd, C.D. Somatic mutations of the lysyl oxidase gene on chromosome 5q23.1 in colorectal tumors. Int. J. Cancer 2002, 97, 636-642.
126. Li, W.; Li, S.J.; Zhao, Y.; Kagan, H.M. Oxidation of histone H1 within cell nuclei by lysyl oxidase: Implications for changes in chromosomal stability. The First Meeting Bulletin of the American Society for Matrix Biology, 2002, 1, 119, (abstract).