IKKα causes chromatin modification on pro-inflammatory genes by cigarette smoke in mouse lung

American Journal of Respiratory Cell and Molecular Biology

Volumn 38, Issue 6, 2008, Pages 689-698

  Yang, Se Ran ^a   Valvo, Samantha ^a   Yao, Hongwei ^a   Kode, Aruna ^a   Rajendrasozhan, Saravanan ^a   Edirisinghe, Indika ^a   Caito, Samuel ^a   Adenuga, David ^a   Henry, Ryan ^a   Fromm, George ^a   Maggirwar, Sanjay ^a   Li, Jian Dong ^a   Bulger, Michael ^a   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Chronic obstructive pulmonary disease; Histone acetylation; Inflammation; Macrophages; NF B

Indexed keywords

CIGARETTE SMOKE; HISTONE; HISTONE H3; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; INTERLEUKIN 6; TRANSCRIPTION FACTOR RELA;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINE; CHROMATIN; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; GENE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTERLEUKIN 6 GENE; MACROPHAGE; MALE; MIP 2 GENE; MONOCYTE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE; CHROMATIN; CULTURE MEDIA; EPIGENESIS, GENETIC; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HISTONES; HUMANS; I-KAPPA B KINASE; INFLAMMATION; INTERLEUKIN-6; INTERLEUKIN-8; LUNG; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; PROMOTER REGIONS (GENETICS); SMOKING; TRANSCRIPTION FACTOR RELA;

MUS;

EID: 45249105749     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2007-0379OC     Document Type: Article

References (47)

1. Burchfiel CM, Marcus EB, Curb JD, Maclean CJ, Vollmer WM, Johnson LR, Fong KO, Rodriguez BL, Masaki KH, Buist AS. Effects of smoking and smoking cessation on longitudinal decline in pulmonary function. Am J Respir Crit Care Med 1995;151:1778-1785.
2. Yang SR, Chida AS, Bauter MR, Shafiq N, Seweryniak K, Maggirwar SB, Kilty I, Rahman I. Cigarette smoke induces proinflammatory cytokine release by activation of NF-kappaB and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol 2006;291:L46-L57.
3. Ito K, Ito M, Elliott WM, Cosio B, Caramori G, Kon OM, Barczyk A, Hayashi S, Adcock IM, Hogg JC, et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 2005;352:1967-1976.
4. Rahman I, Adcock IM. Oxidative stress and redox regulation of lung inflammation in COPD. Eur Respir J 2006;28:219-242.
5. Di Stefano A, Caramori G, Oates T, Capelli A, Lusuardi M, Gnemmi I, Ioli F, Chung KF, Donner CF, Barnes PJ, et al. Increased expression of nuclear factor-kappaB in bronchial biopsies from smokers and patients with COPD. Eur Respir J 2002;20:556-563.
6. Szulakowski P, Crowther AJ, Jimenez LA, Donaldson K, Mayer R, Leonard TB, Macnee W, Drost EM. The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006;174:41-50.
7. Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, Butler K, Donaldson K, Macnee W, Rahman I. Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 2004;31:633-642.
8. Morrison D, Rahman I, Lannan S, MacNee W. Epithelial permeability, inflammation, and oxidant stress in the air spaces of smokers. Am J Respir Crit Care Med 1999;159:473-479.
9. Clayton AL, Hazzalin CA, Mahadevan LC. Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 2006;23:289-296.
10. Yamamoto Y, Verma UN, Prajapati S, Kwak YT, Gaynor RB. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 2003;423:655-659.
11. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 2007;447:972-978.
12. Jeffery P. Remodeling and inflammation of bronchi in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc 2004;1:176-183.
13. Yang SR, Wright J, Bauter M, Seweryniak K, Kode A, Rahman I. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am J Physiol Lung Cell Mol Physiol 2007;292:L567-L576.
14. Chen LF, Mu Y, Greene WC. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 2002;21:6539-6548.
15. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NFkappaB action regulated by reversible acetylation. Science 2001;293:1653-1657.
16. Chen LF, Williams SA, Mu Y, Nakano H, Duerr JM, Buckbinder L, Greene WC. NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol Cell Biol 2005;25:7966-7975.
17. Vermeulen L, De Wilde G, Notebaert S, Vanden Berghe W, Haegeman G. Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit. Biochem Pharmacol 2002;64:963-970.
18. Rahman I, MacNee W. Role of transcription factors in inflammatory lung diseases. Thorax 1998;53:601-612.
19. Schmitz ML, Bacher S, Kracht M. I kappa B-independent control of NF-kappa B activity by modulatory phosphorylations. Trends Biochem Sci 2001;26:186-190.
20. Hu Y, Baud V, Delhase M, Zhang P, Deerinck T, Ellisman M, Johnson R, Karin M. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 1999;284:316-320.
21. Matsushima A, Kaisho T, Rennert PD, Nakano H, Kurosawa K, Uchida D, Takeda K, Akira S, Matsumoto M. Essential role of nuclear factor (NF)-kappaB-inducing kinase and inhibitor of kappaB (IkappaB) kinase alpha in NF-kappaB activation through lymphotoxin beta receptor, but not through tumor necrosis factor receptor I. J Exp Med 2001;193:631-636.
22. Takeda K, Takeuchi O, Tsujimura T, Itami S, Adachi O, Kawai T, Sanjo H, Yoshikawa K, Terada N, Akira S. Limb and skin abnormalities in mice lacking IKKalpha. Science 1999;284:313-316.
23. Li Q, Lu Q, Hwang JY, Buscher D, Lee KF, Izpisua-Belmonte JC, Verma IM. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev 1999;13:1322-1328.
24. Sizemore N, Lerner N, Dombrowski N, Sakurai H, Stark GR. Distinct roles of the Ikappa B kinase alpha and beta subunits in liberating nuclear factor kappa B (NF-kappa B) from Ikappa B and in phosphorylating the p65 subunit of NF-kappa B. J Biol Chem 2002;277:3863-3869.
25. Anest V, Hanson JL, Cogswell PC, Steinbrecher KA, Strahl BD, Baldwin AS. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 2003;423:659-663.
26. Park GY, Wang X, Hu N, Pedchenko TV, Blackwell TS, Christman JW. NIK is involved in nucleosomal regulation by enhancing histone H3 phosphorylation by IKKalpha. J Biol Chem 2006;281:18684-18690.
27. Gloire G, Horion J, El Mjiyad N, Bex F, Chariot A, Dejardin E, Piette J. Promoter-dependent effect of IKKalpha on NF-kappa B/p65 DNA binding. J Biol Chem 2007;282:21308-21318.
28. Vandel L, Trouche D. Physical association between the histone acetyl transferase CBP and a histone methyl transferase. EMBO Rep 2001;2:21-26.
29. Foronjy RF, Mirochnitchenko O, Propokenko O, Lemaitre V, Jia Y, Inouye M, Okada Y, D'Armiento JM. Superoxide dismutase expression attenuates cigarette smoke- or elastase-generated emphysema in mice. Am J Respir Crit Care Med 2006;173:623-631.
30. Thatcher TH, McHugh NA, Egan RW, Chapman RW, Hey JA, Turner CK, Redonnet MR, Seweryniak KE, Sime PJ, Phipps RP. Role of CXCR2 in cigarette smoke-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol 2005;289:L322-L328.
31. Thatcher TH, Maggirwar SB, Baglole CJ, Lakatos HF, Gasiewicz TA, Phipps RP, Sime PJ. Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-kappaB component RelB. Am J Pathol 2007;170:855-864.
32. Moesby L, Jensen S, Hansen EW, Christensen JD.Acomparative study of Mono Mac 6 cells, isolated mononuclear cells and Limulus amoebocyte lysate assay in pyrogen testing. Int J Pharm 1999;191:141-149.
33. Ziegler-Heitbrock HW, Thiel E, Futterer A, Herzog V, Wirtz A, Riethmuller G. Establishment of a human cell line (MonoMac6) with characteristics of mature monocytes. Int J Cancer 1988;41:456-461.
34. Carp H, Janoff A. Possible mechanisms of emphysema in smokers. In vitro suppression of serum elastase-inhibitory capacity by fresh cigarette smoke and its prevention by antioxidants. Am Rev Respir Dis 1978;118:617-621.
35. Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I. Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 2004;18:1897-1899.
36. Kode A, Yang SR, Rahman I. Differential effects of cigarette smoke on oxidative stress and proinflammatory cytokine release in primary human airway epithelial cells and in a variety of transformed alveolar epithelial cells. Respir Res 2006;7:132-152.
37. Kweon SM, Wang B, Rixter D, Lim JH, Koga T, Ishinaga H, Chen LF, Jono H, Xu H, Li JD. Synergistic activation of NF-kappaB by nontypeable H. influenzae and S. pneumoniae is mediated by CK2, IKKbeta-IkappaBalpha, and p38 MAPK. Biochem Biophys Res Commun 2006;351:368-375.
38. Bulger M, Schubeler D, Bender MA, Hamilton J, Farrell CM, Hardison RC, Groudine M. A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse beta-globin locus. Mol Cell Biol 2003;23:5234-5244.
39. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403:41-45.
40. Barnes PJ. Alveolar macrophages as orchestrators of COPD. COPD 2004;1:59-70.
41. Shapiro SD. The macrophage in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999;160:S29-S32.
42. Natoli G, Saccani S, Bosisio D, Marazzi I. Interactions of NF-kappaB with chromatin: the art of being at the right place at the right time. Nat Immunol 2005;6:439-445.
43. Vermeulen L, DeWilde G, Van Damme P, Vanden Berghe W, Haegeman G. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 2003;22:1313-1324.
44. Soloaga A, Thomson S, Wiggin GR, Rampersaud N, Dyson MH, Hazzalin CA, Mahadevan LC, Arthur JS. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J 2003;22:2788-2797.
45. Duncan EA, Anest V, Cogswell P, Baldwin AS. The kinases MSK1 and MSK2 are required for epidermal growth factor-induced, but not tumor necrosis factor-induced, histone H3 Ser10 phosphorylation. J Biol Chem 2006;281:12521-12525.
46. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M. IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature 2005;434:1138-1143.
47. Deak M, Clifton AD, Lucocq LM, Alessi DR. Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J 1998;17:4426-4441.