Mitogen- and stress-activated kinase 1 (MSK1) regulates cigarette smoke-induced histone modifications on NF-κB-dependent genes

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Sundar, Isaac K ^a   Chung, Sangwoon ^a   Hwang, Jae woong ^a   Lapek, John D ^a   Bulger, Michael ^a   Friedman, Alan E ^a   Yao, Hongwei ^a   Davie, James R ^b   Rahman, Irfan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CIGARETTE SMOKE; I KAPPA B KINASE ALPHA; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR RELA; HISTONE; HISTONE ACETYLTRANSFERASE PCAF; MITOGEN AND STRESS ACTIVATED PROTEIN KINASE 1; MITOGEN AND STRESS-ACTIVATED PROTEIN KINASE 1; S6 KINASE;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CIGARETTE SMOKING; CONTROLLED STUDY; GENE FUNCTION; GENE PRODUCT; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NF KAPPAB GENE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; ANIMAL; CELL LINE; DRUG EFFECT; ENZYME ACTIVATION; GENE SILENCING; GENETICS; METABOLISM; PHOSPHORYLATION; PROMOTER REGION; SMOKE; SMOKING;

ACETYLATION; ANIMALS; CELL LINE; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; HISTONES; HUMANS; MICE; P300-CBP TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SMOKE; SMOKING; TRANSCRIPTION FACTOR RELA;

EID: 84856409891     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031378     Document Type: Article

References (66)

1. Rahman I, Adcock IM, (2006) Oxidative stress and redox regulation of lung inflammation in COPD. Eur Respir J 28: 219-242.
2. Rajendrasozhan S, Chung S, Sundar IK, Yao H, Rahman I, (2010) Targeted disruption of NF-{kappa}B1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling. Am J Physiol Lung Cell Mol Physiol 298: L197-209.
3. Rajendrasozhan S, Yao H, Rahman I, (2009) Current perspectives on role of chromatin modifications and deacetylases in lung inflammation in COPD. COPD 6: 291-297.
4. Barnes PJ, Shapiro SD, Pauwels RA, (2003) Chronic obstructive pulmonary disease: molecular and cellular mechanisms. Eur Respir J 22: 672-688.
5. Yao H, Edirisinghe I, Rajendrasozhan S, Yang SR, Caito S, et al. (2008) Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol 294: L1174-1186.
6. Kode A, Yang SR, Rahman I, (2006) 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 7: 132.
7. Chen LF, Williams SA, Mu Y, Nakano H, Duerr JM, et al. (2005) NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol Cell Biol 25: 7966-7975.
8. Yang SR, Wright J, Bauter M, Seweryniak K, Kode A, et al. (2007) 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 292: L567-576.
9. Vermeulen L, De Wilde G, Van Damme P, Vanden Berghe W, Haegeman G, (2003) Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 22: 1313-1324.
10. Yang SR, Valvo S, Yao H, Kode A, Rajendrasozhan S, et al. (2008) IKK alpha causes chromatin modification on pro-inflammatory genes by cigarette smoke in mouse lung. Am J Respir Cell Mol Biol 38: 689-698.
11. Soloaga A, Thomson S, Wiggin GR, Rampersaud N, Dyson MH, et al. (2003) MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J 22: 2788-2797.
12. Kefaloyianni E, Gaitanaki C, Beis I, (2006) ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-kappaB transactivation during oxidative stress in skeletal myoblasts. Cell Signal 18: 2238-2251.
13. McCoy CE, Campbell DG, Deak M, Bloomberg GB, Arthur JS, (2005) MSK1 activity is controlled by multiple phosphorylation sites. Biochem J 387: 507-517.
14. Zhong H, Voll RE, Ghosh S, (1998) Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1: 661-671.
15. Reddel RR, Ke Y, Gerwin BI, McMenamin MG, Lechner JF, et al. (1988) Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Research 48: 1904-1909.
16. Drobic B, Perez-Cadahia B, Yu J, Kung SK, Davie JR, (2010) Promoter chromatin remodeling of immediate-early genes is mediated through H3 phosphorylation at either serine 28 or 10 by the MSK1 multi-protein complex. Nucleic Acids Res 38: 3196-3208.
17. Deak M, Clifton AD, Lucocq LM, Alessi DR, (1998) Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J 17: 4426-4441.
18. Kim YM, Cao D, Reed W, Wu W, Jaspers I, et al. (2007) Zn2+-induced NF-kappaB-dependent transcriptional activity involves site-specific p65/RelA phosphorylation. Cell Signal 19: 538-546.
19. Kode A, Rajendrasozhan S, Caito S, Yang SR, Megson IL, et al. (2008) Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 294: L478-488.
20. Carp H, Janoff A, (1978) 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 118: 617-621.
21. Fujioka K, Shibamoto T, (2006) Determination of toxic carbonyl compounds in cigarette smoke. Environ Toxicol 21: 47-54.
22. Lambert C, McCue J, Portas M, Ouyang Y, Li J, et al. (2005) Acrolein in cigarette smoke inhibits T-cell responses. J Allergy Clin Immunol 116: 916-922.
23. Carnevali S, Nakamura Y, Mio T, Liu X, Takigawa K, et al. (1998) Cigarette smoke extract inhibits fibroblast-mediated collagen gel contraction. Am J Physiol 274: L591-598.
24. Smith CJ, Hansch C, (2000) The relative toxicity of compounds in mainstream cigarette smoke condensate. Food Chem Toxicol 38: 637-646.
25. Mauderly JL, Gigliotti AP, Barr EB, Bechtold WE, Belinsky SA, et al. (2004) Chronic inhalation exposure to mainstream cigarette smoke increases lung and nasal tumor incidence in rats. Toxicol Sci 81: 280-292.
26. Arthur JS, (2008) MSK activation and physiological roles. Front Biosci 13: 5866-5879.
27. Strahl BD, Allis CD, (2000) The language of covalent histone modifications. Nature 403: 41-45.
28. Yamamoto Y, Verma UN, Prajapati S, Kwak YT, Gaynor RB, (2003) Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423: 655-659.
29. Ito K, Charron CE, Adcock IM, (2007) Impact of protein acetylation in inflammatory lung diseases. Pharmacol Ther 116: 249-265.
30. Yao H, Hwang JW, Moscat J, Diaz-Meco MT, Leitges M, et al. (2010) Protein kinase C zeta mediates cigarette smoke/aldehyde- and lipopolysaccharide-induced lung inflammation and histone modifications. J Biol Chem 285: 5405-5416.
31. Yang SR, Yao H, Rajendrasozhan S, Chung S, Edirisinghe I, et al. (2009) RelB is differentially regulated by IkappaB Kinase-alpha in B cells and mouse lung by cigarette smoke. Am J Respir Cell Mol Biol 40: 147-158.
32. Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, et al. (2004) Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 31: 633-642.
33. Yang SR, Chida AS, Bauter MR, Shafiq N, Seweryniak K, et al. (2006) 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 291: L46-57.
34. Vermeulen L, Vanden Berghe W, Beck IM, De Bosscher K, Haegeman G, (2009) The versatile role of MSKs in transcriptional regulation. Trends Biochem Sci 34: 311-318.
35. Wiggin GR, Soloaga A, Foster JM, Murray-Tait V, Cohen P, et al. (2002) MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol Cell Biol 22: 2871-2881.
36. Markou T, Lazou A, (2002) Phosphorylation and activation of mitogen- and stress-activated protein kinase-1 in adult rat cardiac myocytes by G-protein-coupled receptor agonists requires both extracellular-signal-regulated kinase and p38 mitogen-activated protein kinase. Biochem J 365: 757-763.
37. Pierrat B, Correia JS, Mary JL, Tomas-Zuber M, Lesslauer W, (1998) RSK-B, a novel ribosomal S6 kinase family member, is a CREB kinase under dominant control of p38alpha mitogen-activated protein kinase (p38alphaMAPK). J Biol Chem 273: 29661-29671.
38. New L, Zhao M, Li Y, Bassett WW, Feng Y, et al. (1999) Cloning and characterization of RLPK, a novel RSK-related protein kinase. J Biol Chem 274: 1026-1032.
39. Jamaluddin M, Tian B, Boldogh I, Garofalo RP, Brasier AR, (2009) Respiratory syncytial virus infection induces a reactive oxygen species-MSK1-phospho-Ser-276 RelA pathway required for cytokine expression. J Virol 83: 10605-10615.
40. Reber L, Vermeulen L, Haegeman G, Frossard N, (2009) Ser276 phosphorylation of NF-kB p65 by MSK1 controls SCF expression in inflammation. PLoS One 4: e4393.
41. Joo JH, Jetten AM, (2008) NF-kappaB-dependent transcriptional activation in lung carcinoma cells by farnesol involves p65/RelA(Ser276) phosphorylation via the MEK-MSK1 signaling pathway. J Biol Chem 283: 16391-16399.
42. Jacks KA, Koch CA, (2010) Differential regulation of mitogen- and stress-activated protein kinase-1 and-2 (MSK1 and MSK2) by CK2 following UV radiation. J Biol Chem 285: 1661-1670.
43. Beck IM, Vanden Berghe W, Vermeulen L, Bougarne N, Vander Cruyssen B, et al. (2008) Altered subcellular distribution of MSK1 induced by glucocorticoids contributes to NF-kappaB inhibition. EMBO J 27: 1682-1693.
44. Zhong S, Jansen C, She QB, Goto H, Inagaki M, et al. (2001) Ultraviolet B-induced phosphorylation of histone H3 at serine 28 is mediated by MSK1. J Biol Chem 276: 33213-33219.
45. Perez-Cadahia B, Drobic B, Espino PS, He S, Mandal S, et al. (2011) Role of MSK1 in the malignant phenotype of Ras-transformed mouse fibroblasts. J Biol Chem 286: 42-49.
46. Ananieva O, Darragh J, Johansen C, Carr JM, McIlrath J, et al. (2008) The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat Immunol 9: 1028-1036.
47. Darragh J, Ananieva O, Courtney A, Elcombe S, Arthur JS, (2010) MSK1 regulates the transcription of IL-1ra in response to TLR activation in macrophages. Biochem J 425: 595-602.
48. Anest V, Hanson JL, Cogswell PC, Steinbrecher KA, Strahl BD, et al. (2003) A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 423: 659-663.
49. Gloire G, Horion J, El Mjiyad N, Bex F, Chariot A, et al. (2007) Promoter-dependent effect of IKKalpha on NF-kappaB/p65 DNA binding. J Biol Chem 282: 21308-21318.
50. Chung S, Sundar IK, Yao H, Ho YS, Rahman I, (2010) Glutaredoxin 1 regulates cigarette smoke-mediated lung inflammation through differential modulation of I{kappa}B kinases in mice: impact on histone acetylation. Am J Physiol Lung Cell Mol Physiol 299: L192-203.
51. Anest V, Cogswell PC, Baldwin AS Jr, (2004) IkappaB kinase alpha and p65/RelA contribute to optimal epidermal growth factor-induced c-fos gene expression independent of IkappaBalpha degradation. J Biol Chem 279: 31183-31189.
52. Duncan EA, Anest V, Cogswell P, Baldwin AS, (2006) 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 281: 12521-12525.
53. Chung S, Sundar IK, Hwang JW, Yull FE, Blackwell TS, et al. (2011) NF-kappaB Inducing Kinase, NIK Mediates Cigarette Smoke/TNFalpha-Induced Histone Acetylation and Inflammation through Differential Activation of IKKs. PLoS One 6: e23488.
54. Chadee DN, Hendzel MJ, Tylipski CP, Allis CD, Bazett-Jones DP, et al. (1999) Increased Ser-10 phosphorylation of histone H3 in mitogen-stimulated and oncogene-transformed mouse fibroblasts. J Biol Chem 274: 24914-24920.
55. Dunn KL, Davie JR, (2005) Stimulation of the Ras-MAPK pathway leads to independent phosphorylation of histone H3 on serine 10 and 28. Oncogene 24: 3492-3502.
56. Garcia BA, Barber CM, Hake SB, Ptak C, Turner FB, et al. (2005) Modifications of human histone H3 variants during mitosis. Biochemistry 44: 13202-13213.
57. Thomson S, Clayton AL, Hazzalin CA, Rose S, Barratt MJ, et al. (1999) The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J 18: 4779-4793.
58. Kannan-Thulasiraman P, Katsoulidis E, Tallman MS, Arthur JS, Platanias LC, (2006) Activation of the mitogen- and stress-activated kinase 1 by arsenic trioxide. J Biol Chem 281: 22446-22452.
59. Kim HG, Lee KW, Cho YY, Kang NJ, Oh SM, et al. (2008) Mitogen- and stress-activated kinase 1-mediated histone H3 phosphorylation is crucial for cell transformation. Cancer Res 68: 2538-2547.
60. Janknecht R, (2003) Regulation of the ER81 transcription factor and its coactivators by mitogen- and stress-activated protein kinase 1 (MSK1). Oncogene 22: 746-755.
61. Chen L, Fischle W, Verdin E, Greene WC, (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293: 1653-1657.
62. Berger SL, (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12: 142-148.
63. Chen LF, Mu Y, Greene WC, (2002) Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 21: 6539-6548.
64. Gilmour PS, Rahman I, Donaldson K, MacNee W, (2003) Histone acetylation regulates epithelial IL-8 release mediated by oxidative stress from environmental particles. Am J Physiol Lung Cell Mol Physiol 284: L533-540.
65. Okazaki T, Sakon S, Sasazuki T, Sakurai H, Doi T, et al. (2003) Phosphorylation of serine 276 is essential for p65 NF-kappaB subunit-dependent cellular responses. Biochem Biophys Res Commun 300: 807-812.
66. Caivano M, Cohen P, (2000) Role of mitogen-activated protein kinase cascades in mediating lipopolysaccharide-stimulated induction of cyclooxygenase-2 and IL-1 beta in RAW264 macrophages. J Immunol 164: 3018-3025.