The kinetics of transcriptomic changes induced by cigarette smoke in rat lungs reveals a specific program of defense, inflammation, and circadian clock gene expression

Toxicological Sciences

Volumn 93, Issue 2, 2006, Pages 422-431

  Gebel, Stephan ^a   Gerstmayer, Bernhard ^b   Kuhl, Peter ^a   Borlak, Jürgen ^c   Meurrens, Kris ^d   Müller, Thomas ^a  

^a Philip Morris Research Laboratories GmbH   (Germany)

^b MILTENYI BIOTEC GMBH   (Germany)

^c FRAUNHOFER INSTITUTE FOR TOXICOLOGY AND EXPERIMENTAL MEDICINE   (Germany)

^d Philip Morris Research Laboratories   (Belgium)

Author keywords

Cigarette smoke; Circadian rhythm; Gene expression; Inflammation; Oxidative stress; Rat lung

Indexed keywords

ANTIOXIDANT; ARGINASE; CHITINASE; CIGARETTE SMOKE; GALECTIN 3; XENOBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR IMMUNITY; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME DEGRADATION; GENE EXPRESSION; INNATE IMMUNITY; LUNG DISEASE; MALE; NONHUMAN; PARTICULATE MATTER; PATHOGENESIS; RAT; TOXICITY TESTING; TOXICOKINETICS; TRANSCRIPTOMICS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; GENE EXPRESSION; IMMUNITY, NATURAL; INFLAMMATION; LUNG; MALE; RATS; RATS, SPRAGUE-DAWLEY; SMOKE; TOBACCO; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; XENOBIOTICS;

ANIMALIA;

EID: 33748753955     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfl071     Document Type: Article

References (51)

1. Anwar, A., Dehn, D., Siegel, D., Kepa, J. K., Tang, L. J., Pietenpol, J. A., and Ross, D. (2003). Interaction of Human NAD(P)H:qUinone oxidoreductase 1 (NQO1) with the tumor suppressor protein p53 in cells and cell-free systems. J. Biol. Chem. 278(12), 10368-10373.
2. Asher, G., Lotem, J., Kama, R., Sachs, L., and Shaul, Y. (2002). NQO1 stabilizes p53 through a distinct pathway. Proc. Natl. Acad. Sci. U.S.A. 99(5), 3099-3104.
3. Barnes, P. J., Shapiro, S. D., and Pauwels, R. A. (2003). Chronic obstructive pulmonary disease: Molecular and cellular mechanisms. Eur. Respir. J. 22(4), 672-688.
4. Benowitz, N. L., Hansson, A., and Jacob, P., III. (2002). Cardiovascular effects of nasal and transdermal nicotine and cigarette smoking. Hypertension 39(6), 1107-1112.
5. Bosio, A., Knörr, C., Janssen, U., Gebel, S., Haussmann, H. J., and Müller, T. (2002). Kinetics of gene expression profiling in Swiss 3T3 cells exposed to aqueous extracts of cigarette smoke. Carcinogenesis 23(5), 741-748.
6. Carroll, M. C. (2004). The complement system in regulation of adaptive immunity. Nat. Immunol. 5(10), 981-986.
7. Dickerson, T. J., and Janda, K. D. (2002). A previously undescribed chemical link between smoking and metabolic disease. Proc. Natl. Acad. Sci. U.S.A. 99(23), 15084-15088.
8. Fireman, P. (2003). Understanding asthma pathophysiology. Allergy Asthma Proc. 24(2), 79-83.
9. Friedrichs, B., Miert, E. V., and Vanscheeuwijk, P. M. (2006). Lung inflammation in rats following subchronic exposure to cigarette mainstream smoke. Exp. Lung Res. 32, 1-29.
10. Gebel, S., Gerstmayer, B., Bosio, A., Haussmann, H. J., Miert, E. V., and Müller, T. (2004). Gene expression profiling in respiratory tissues from rats exposed to mainstream cigarette smoke. Carcinogenesis 25(2), 169-178.
11. Goetz, D. H., Holmes, M. A., Borregaard, N., Bluhm, M. E., Raymond, K. N., and Strong, R. K. (2002). The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell 10(5), 1033-1043.
12. Haussmann, H. J., Anskeit, E., Becker, D., Kuhl, P., Stinn, W., Teredesai, A., Voncken, P., and Walk, R. A. (1998). Comparison of fresh and room-aged cigarette sidestream smoke in a subchronic inhalation study on rats. Toxicol. Sci. 41(1), 100-116.
13. Hirayama, J., and Sassone-Corsi, P. (2005). Structural and functional features of transcription factors controlling the circadian clock. Curr. Opin. Gen. Dev. 15(5), 548-556.
14. Hoyt, J. C., Robbins, R. A., Habib, M., Springall, D. R., Buttery, L. D. K., Polak, J. M., and Barnes, P. J. (2003). Cigarette smoke decreases inducible nitric oxide synthase in lung epithelial cells. Exp. Lung Res. 29(1), 17-28.
15. Hukkanen, J., Jacob, P., III, and Benowitz, N. L. (2005). Metabolism and disposition kinetics of nicotine. Pharmacol. Rev. 57(1), 79-115.
16. Kelly, E. A. B., Houtman, J. J., and Jarjour, N. N. (2004). Inflammatory changes associated with circadian variation in pulmonary function in subjects with mild asthma. Clin. Exp. Allergy 34(2), 227-233.
17. Kharitonov, S. A., Robbins, R. A., Yates, D., Keatings, V., and Barnes, P. J. (1995). Acute and chronic effects of cigarette smoking on exhaled nitric oxide. Am. J. Respir. Crit. Care Med. 152(2), 609-612.
18. King, N. E., Rothenberg, M. E., and Zimmermann, N. (2004). Arginine in asthma and lung inflammation. J. Nutr. 134(10), 2830S-2836S.
19. Klaassen, C. D., and Liu, J. (1998). Metallothionein transgenic and knock-out mouse models in the study of cadmium toxicity. J. Toxicol. Sci. 23(Suppl. 2), 97-102.
20. Knörr-Wittmann, C., Hengstermann, A., Gebel, S., Alam, J., and Müller, T. (2005). Characterization of Nrf2 activation and heme oxygenase-1 expression in NIH3T3 cells exposed to aqueous extracts of cigarette smoke. Free Radic. Biol. Med. 39(11), 1438-1448.
21. Kobayashi, M., and Yamamoto, M. (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 7(3-4), 385-394.
22. Kunkel, S. L., and Strieter, R. M. (2005). Cytokines and chemokines in lung inflammation and injury. In Fishman's Pulmonary Diseases and Disorders (A. P. Fishman and J. A. Elias, Eds.), 3rd ed., pp. 315-324. McGraw-Hill, New York.
23. Lin, Y. H., and Yang-Yen, H. F. (2001). The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. J. Biol. Chem. 276(49), 46024-46030.
24. Liu, C., and Gillette, M. U. (1996). Cholinergic regulation of the suprachiasmatic nucleus circadian rhythm via a muscarinic mechanism at night. J. Neurosci. 16(2), 744-751.
25. Müller, T., and Gebel, S. (2006). Cigarette smoke-induced redox signaling and gene expression in in vitro and in vivo models. In Cigarette Smoke & Oxidative Stress. (B. B. Halliwell and H. E. Poulsen, Eds.), pp. 75-111. Springer, Heidelberg.
26. Nebert, D. W., Dalton, T. P., Okey, A. B., and Gonzalez, F. J. (2004). Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 279(23), 23847-23850.
27. Oishi, K., Miyazaki, K., Mesaki, M., Kobayashi, H., Iitaka, C., Kudo, T., Shimizu, Y., Ishida, N., Kadota, K., Kikuno, R., et al. (2003). Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 278(42), 41519-41527.
28. Oka, N., Nakahara, S., Takenaka, Y., Fukumori, T., Hogan, V., Kanayama, H., Yanagawa, T., and Raz, A. (2005). Galectin-3 inhibits tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells. Cancer Res. 65(17), 7546-7553.
29. O'Regan, A. (2003). The role of osteopontin in lung disease. Cytokine & Growth Factor Reviews 14(6), 479-488.
30. Peto, R., Lopez, A. D., Boreham, J., Thun, M., and Heath, C., Jr. (1992). Mortality from tobacco in developed countries: Indirect estimation from national vital statistics. Lancet 339(8804), 1268-1278.
31. Pittendrigh, C. S. (1993). Temporal organization: Reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55(1), 17-54.
32. Rahman, I. (2005). Smoking-induced inflammation, injury, and disease - Molecular mechanisms. In Oxygen/Nitrogen Radicals - Lung Injury and Disease (V. Vallyathan, V. Castranova, and X. Shi, Eds.), pp. 211-255. Marcel Dekker, New York.
33. Rangasamy, T., Cho, C. Y., Thimmulappa, R. K., Zhen, L., Srisuma, S. S., Kensler, T. W., Yamamoto, M., Petrache, I., Tuder, R. M., and Biswal, S. (2004). Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 114(9), 1248-1259.
34. Roth, J., Teigelkamp, S., Wilke, M., Grun, L., Tummler, B., and Sorg, C. (1992). Complex pattern of the myelo-monocytic differentiation antigens MRP8 and MRP14 during chronic airway inflammation. Immunobiology 186(3-4), 304-314.
35. Rutter, J., Reick, M., Wu, L. C., and McKnight, S. L. (2001). Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293(5529), 510-514.
36. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., et al. (2003). TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34(2), 374-378.
37. Spira, A., Beane, J., Pinto-Plata, V., Kadar, A., Liu, G., Shah, V., Celli, B., and Brody, J. S. (2004a). Gene expression profiling of human lung tissue from smokers with severe emphysema. Am. J. Respir. Cell Mol. Biol. 31(6), 601-610.
38. Spira, A., Beane, J., Shah, V., Liu, G., Schembri, F., Yang, X., Palma, J., and Brody, J. S. (2004b). Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc. Natl. Acad. Sci. U.S.A. 101(27), 10143-10148.
39. Tauchi, M., Hida, A., Negishi, T., Katsuoka, F., Noda, S., Mimura, J., Hosoya, T., Yanaka, A., Aburatani, H., Fujii-Kuriyama, Y., et al. (2005). Constitutive expression of aryl hydrocarbon receptor in keratinocytes causes inflammatory skin lesions. Mol. Cell. Biol. 25(21), 9360-9368.
40. Theocharis, S. E., Margeli, A. P., and Koutselinis, A. (2003). Metallothionein: A multifunctional protein from toxicity to cancer. Int. J. Biol. Markers 18(3), 162-169.
41. US Department of Health and Human Services. (1989a). Chronic Obstructive Pulmonary Disease (US Department of Health and Human Services, Ed.), pp. 66-68. Public Health Service, Centers for Disease Control, Center for Chronic Disease Prevention and Health Promotion Office on Smoking and Health, Rockville, MD. DHHS Publication No. (CDC) 89-8411.
42. US Department of Health and Human Services. (1989b). Coronary Heart Disease. (US Department of Health and Human Services, Ed.), pp. 58-65. Public Health Service, Centers for Disease Control, Center for Chronic Disease Prevention and Health Promotion Office on Smoking and Health, Rockville, MD. DHHS Publication No. (CDC) 89-8411.
43. Vandal, K., Rouleau, P., Boivin, A., Ryckman, C., Talbot, M., and Tessier, P. A. (2003). Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J. Immunol. 171(5), 2602-2609.
44. Vanscheeuwijk, P. M., Teredesai, A., Terpstra, P. M., Verbeek, J., Kuhl, P., Gerstenberg, B., Gebel, S., and Carmines, E. L. (2002). Evaluation of the potential effects of ingredients added to cigarettes. Part 4: Subchronic inhalation toxicity. Food Chem. Toxicol. 40, 113-131.
45. Vercelli, D. (2003). Arginase: Marker, effector, or candidate gene for asthma? J. Clin. Invest. 111(12), 1815-1817.
46. Woodruff, P. G., Koth, L. L., Yang, Y. H., Rodriguez, M. W., Favoreto, S., Dolganov, G. M., Paquet, A. C., and Erle, D. J. (2005). A distinctive alveolar macrophage activation state induced by cigarette smoking. Am. J. Respir. Crit. Care Med. 172(11), 1383-1392.
47. Yang, R. Y., Hsu, D. K., and Liu, F. T. (1996). Expression of galectin-3 modulates T-cell growth and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 93(13), 6737-6742.
48. Zhu, W., Sano, H., Nagai, R., Fukuhara, K., Miyazaki, A., and Horiuchi, S. (2001). The role of galectin-3 in endocytosis of advanced glycation end products and modified low density lipoproteins. Biochem. Biophys. Res. Commun. 280(4), 1183-1188.
49. Zhu, Y., Denhardt, D. T., Cao, H., Sutphin, P. D., Koong, A. C., Giaccia, A. J., and Le, Q. T. (2005). Hypoxia upregulates osteopontin expression in NIH-3T3 cells via a Ras-activated enhancer. Oncogene 24(43), 6555-6563.
50. Zhu, Z., Zheng, T., Homer, R. J., Kim, Y. K., Chen, N. Y., Cohn, L., Hamid, Q., and Elias, J. A. (2004). Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304(5677), 1678-1682.
51. Zimmermann, N., King, N. E., Laporte, J., Yang, M., Mishra, A., Pope, S. M., Muntel, E. E., Witte, D. P., Pegg, A. A., Foster, P. S., et al. (2003). Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis. J. Clin. Invest. 111(12), 1863-1874.