Acetylation modulates the STAT signaling code

Cytokine and Growth Factor Reviews

Volumn 23, Issue 6, 2012, Pages 293-305

  Wieczorek, Martin ^a   Ginter, Torsten ^a   Brand, Peter ^a   Heinzel, Thorsten ^a   Krämer, Oliver H ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Acetylation; Cytokine; HAT; HDAC; Phosphorylation; SIRT; STAT; Sumoylation

Indexed keywords

ANACARDIC ACID; BUTYRIC ACID; CISPLATIN; ENTINOSTAT; FLUDARABINE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 13; INTERLEUKIN 4; NICOTINAMIDE; PANOBINOSTAT; RESVERATROL; SIRTUIN; STAT PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN; STAT5 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN; STAT6 PROTEIN; TAMOXIFEN; TERIFLUNOMIDE; TRICHOSTATIN A; UNINDEXED DRUG; VORINOSTAT;

ACETYLATION; APOPTOSIS; CANCER INHIBITION; CARCINOGENESIS; CELL GROWTH; DRUG SELECTIVITY; DRUG SENSITIVITY; DRUG TARGETING; HUMAN; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

ACETYLATION; ANIMALS; HUMANS; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84869872190     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2012.06.005     Document Type: Review

References (142)

1. Mertens C., Darnell J.E. SnapShot: JAK-STAT signaling. Cell 2007, 131:612.
2. Hiscott J., Ware C. Cytokines. Current Opinion in Immunology 2011, 23:561-563.
3. Yang J., Stark G.R. Roles of unphosphorylated STATs in signaling. Cell Research 2008, 18:443-451.
4. Liongue C., O'Sullivan L.A., Trengove M.C., Ward A.C. Evolution of JAK-STAT pathway components: mechanisms and role in immune system development. PloS ONE 2012, 7:e32777.
5. Harrison D.A. The Jak/STAT pathway. Cold Spring Harbor Perspectives in Biology 2012, 4.
6. Kiu H., Nicholson S.E. Biology and significance of the JAK/STAT signalling pathways. Growth Factors 2012, 30:88-106.
7. Reich N.C. STAT dynamics. Cytokine & Growth Factor Reviews 2007, 18:511-518.
8. Mohr A., Chatain N., Domoszlai T., Rinis N., Sommerauer M., Vogt M., et al. Dynamics and non-canonical aspects of JAK/STAT signalling. European Journal of Cell Biology 2011.
9. Mertens C., Zhong M., Krishnaraj R., Zou W., Chen X., Darnell J.E. Dephosphorylation of phosphotyrosine on STAT1 dimers requires extensive spatial reorientation of the monomers facilitated by the N-terminal domain. Genes & Development 2006, 20:3372-3381.
10. Grivennikov S.I., Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine & Growth Factor Reviews 2010, 21:11-19.
11. Hennighausen L., Robinson G.W. Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes & Development 2008, 22:711-721.
12. Kim H.S., Lee M.S. STAT1 as a key modulator of cell death. Cellular Signalling 2007, 19:454-465.
13. Gough D.J., Levy D.E., Johnstone R.W., Clarke C.J. IFNgamma signaling - does it mean JAK-STAT?. Cytokine & Growth Factor Reviews 2008, 19:383-394.
14. Krämer O.H., Heinzel T. Phosphorylation-acetylation switch in the regulation of STAT1 signaling. Molecular and Cellular Endocrinology 2010, 315:40-48.
15. Hu X., Ivashkiv L.B. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 2009, 31:539-550.
16. Yang X.J., Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Molecular Cell 2008, 31:449-461.
17. Spange S., Wagner T., Heinzel T., Krämer O.H. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. International Journal of Biochemistry & Cell Biology 2009, 41:185-198.
18. Bannister A.J., Kouzarides T. Regulation of chromatin by histone modifications. Cell Research 2011, 21:381-395.
19. Aka J.A., Kim G.W., Yang X.J. K-Acetylation and its enzymes: overview and new developments. Handbook of Experimental Pharmacology 2011, 206:1-12.
20. Krämer O.H. HDAC2: a critical factor in health and disease. Trends in Pharmacological Sciences 2009, 30:647-655.
21. Yang X.J., Seto E. HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 2007, 26:5310-5318.
22. Nguyen T.L., Wilson M.G., Hiscott J. Oncolytic viruses and histone deacetylase inhibitors-a multi-pronged strategy to target tumor cells. Cytokine & Growth Factor Reviews 2010, 21:153-159.
23. Delcuve G.P., Khan D.H., Davie J.R. Roles of histone deacetylases in epigenetic regulation: emerging paradigms from studies with inhibitors. Clinical Epigenetics 2012, 4:5.
24. Müller S., Krämer O.H. Inhibitors of HDACs - effective drugs against cancer?. Current Cancer Drug Targets 2010.
25. Leng C., Gries M., Ziegler J., Lokshin A., Mascagni P., Lentzsch S., et al. Reduction of graft-versus-host disease by histone deacetylase inhibitor suberonylanilide hydroxamic acid is associated with modulation of inflammatory cytokine milieu and involves inhibition of STAT1. Experimental Hematology 2006, 34:776-787.
26. Zhou W., Zhu W.G. The changing face of HDAC inhibitor depsipeptide. Current Cancer Drug Targets 2009, 9:91-100.
27. Hebenstreit D., Wirnsberger G., Horejs-Hoeck J., Duschl A. Signaling mechanisms, interaction partners, and target genes of STAT6. Cytokine & Growth Factor Reviews 2006, 17:173-188.
28. Roth M., Black J.L. Transcription factors in asthma: are transcription factors a new target for asthma therapy?. Current Drug Targets 2006, 7:589-595.
29. Bruns H.A., Kaplan M.H. The role of constitutively active Stat6 in leukemia and lymphoma. Critical Reviews in Oncology/Hematology 2006, 57:245-253.
30. Shankaranarayanan P., Chaitidis P., Kuhn H., Nigam S. Acetylation by histone acetyltransferase CREB-binding protein/p300 of STAT6 is required for transcriptional activation of the 15-lipoxygenase-1 gene. The Journal of Biological Chemistry 2001, 276:42753-42760.
31. Ferrari R., Pellegrini M., Horwitz G.A., Xie W., Berk A.J., Kurdistani S.K. Epigenetic reprogramming by adenovirus e1a. Science 2008, 321:1086-1088.
32. Grausenburger R., Bilic I., Boucheron N., Zupkovitz G., El-Housseiny L., Tschismarov R., et al. Conditional deletion of histone deacetylase 1 in T cells leads to enhanced airway inflammation and increased Th2 cytokine production. Journal of Immunology 2010, 185:3489-3497.
33. Buglio D., Georgakis G.V., Hanabuchi S., Arima K., Khaskhely N.M., Liu Y.J., et al. Vorinostat inhibits STAT6-mediated TH2 cytokine and TARC production and induces cell death in Hodgkin lymphoma cell lines. Blood 2008, 112:1424-1433.
34. Dietrich S., Krämer O.H., Hahn E., Schäfer C., Giese T., Hess M., et al. Leflunomide induces apoptosis in fludarabine-resistant and clinically refractory CLL cells. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2012, 18:417-431.
35. Sikorski K., Czerwoniec A., Bujnicki J.M., Wesoly J., Bluyssen H.A. STAT1 as a novel therapeutical target in pro-atherogenic signal integration of IFNgamma TLR4 and IL-6 in vascular disease. Cytokine & Growth Factor Reviews 2011, 22:211-219.
36. Kimura A., Naka T., Nakahama T., Chinen I., Masuda K., Nohara K., et al. Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. The Journal of Experimental Medicine 2009, 206:2027-2035.
37. Krämer O.H., Baus D., Knauer S.K., Stein S., Jager E., Stauber R.H., et al. Acetylation of Stat1 modulates NF-kappaB activity. Genes & Development 2006, 20:473-485.
38. Shankar E., Vykhovanets E.V., Vykhovanets O.V., Maclennan G.T., Singh R., Bhaskaran N., et al. High-fat diet activates pro-inflammatory response in the prostate through association of Stat-3 and NF-kappaB. The Prostate 2012, 72:233-243.
39. Strebovsky J., Walker P., Lang R., Dalpke A.H. Suppressor of cytokine signaling 1 (SOCS1) limits NFkappaB signaling by decreasing p65 stability within the cell nucleus. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2011, 25:863-874.
40. Nadiminty N., Lou W., Lee S.O., Lin X., Trump D.L., Gao A.C. Stat3 activation of NF-{kappa}B p100 processing involves CBP/p300-mediated acetylation. Proceedings of the National Academy of Sciences of the United States of America 2006, 7264-7269.
41. Hayashi T., Ishida Y., Kimura A., Iwakura Y., Mukaida N., Kondo T. IFN-gamma protects cerulein-induced acute pancreatitis by repressing NF-kappa B activation. Journal of Immunology 2007, 178:7385-7394.
42. http://www.phosida.com/.
43. http://www.phosphosite.org/.
44. Gao S.P., Mark K.G., Leslie K., Pao W., Motoi N., Gerald W.L., et al. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. The Journal of Clinical Investigation 2007, 117:3846-3856.
45. Nelson E.A., Sharma S.V., Settleman J., Frank D.A. A chemical biology approach to developing STAT inhibitors: molecular strategies for accelerating clinical translation. Oncotarget 2011, 2:518-524.
46. Groner B., Lucks P., Borghouts C. The function of Stat3 in tumor cells and their microenvironment. Seminars in Cell & Developmental Biology 2008, 19:341-350.
47. Wang R., Cherukuri P., Luo J. Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation. The Journal of Biological Chemistry 2005, 280:11528-11534.
48. Yuan Z.L., Guan Y.J., Chatterjee D., Chin Y.E. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 2005, 307:269-273.
49. Li T., Du Y., Wang L., Huang L., Li W., Lu M., et al. Characterization and prediction of lysine (K)-acetyl-transferase specific acetylation sites. Molecular & Cellular Proteomics 2012, 11:011080. M111.
50. Choudhary C., Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nature Reviews Molecular Cell Biology 2010, 11:427-439.
51. Ma L., Gao J.S., Guan Y., Shi X., Zhang H., Ayrapetov M.K., et al. Acetylation modulates prolactin receptor dimerization. Proceedings of the National Academy of Sciences of the United States of America 2010, 19314-19319.
52. Schiavone D., Avalle L., Dewilde S., Poli V. The immediate early genes Fos and Egr1 become STAT1 transcriptional targets in the absence of STAT3. FEBS Letters 2011, 585:2455-2460.
53. Ray S., Boldogh I., Brasier A.R. STAT3 NH2-terminal acetylation is activated by the hepatic acute-phase response and required for IL-6 induction of angiotensinogen. Gastroenterology 2005, 129:1616-1632.
54. Hou T., Ray S., Lee C., Brasier A.R. The STAT3 NH2-terminal domain stabilizes enhanceosome assembly by interacting with the p300 bromodomain. The Journal of Biological Chemistry 2008, 283:30725-30734.
55. Ray S., Lee C., Hou T., Boldogh I., Brasier A.R. Requirement of histone deacetylase1 (HDAC1) in signal transducer and activator of transcription 3 (STAT3) nucleocytoplasmic distribution. Nucleic Acids Research 2008, 36:4510-4520.
56. Lee J.L., Wang M.J., Chen J.Y. Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. The Journal of Cell Biology 2009, 185:949-957.
57. Gires O. Lessons from common markers of tumor-initiating cells in solid cancers. Cellular and Molecular Life Sciences: CMLS 2011, 68:4009-4022.
58. Zöller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nature Reviews Cancer 2011, 11:254-267.
59. Page B.D., Fletcher S., Yue P., Li Z., Zhang X., Sharmeen S., et al. Identification of a non-phosphorylated, cell permeable, small molecule ligand for the Stat3 SH2 domain. Bioorganic & Medicinal Chemistry Letters 2011, 21:5605-5609.
60. Nie Y., Erion D.M., Yuan Z., Dietrich M., Shulman G.I., Horvath T.L., et al. STAT3 inhibition of gluconeogenesis is downregulated by SirT1. Nature Cell Biology 2009, 11:492-500.
61. Sestito R., Madonna S., Scarponi C., Cianfarani F., Failla C.M., Cavani A., et al. STAT3-dependent effects of IL-22 in human keratinocytes are counterregulated by sirtuin 1 through a direct inhibition of STAT3 acetylation. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2011, 25:916-927.
62. Lee H., Zhang P., Herrmann A., Yang C., Xin H., Wang Z., et al. Acetylated STAT3 is crucial for methylation of tumor-suppressor gene promoters and inhibition by resveratrol results in demethylation. Proceedings of the National Academy of Sciences of the United States of America 2012.
63. Peng L., Yuan Z., Ling H., Fukasawa K., Robertson K., Olashaw N., et al. SIRT1 deacetylates the DNA methyltransferase 1 (DNMT1) protein and alters its activities. Molecular and Cellular Biology 2011, 31:4720-4734.
64. Fantin V.R., Loboda A., Paweletz C.P., Hendrickson R.C., Pierce J.W., Roth J.A., et al. Constitutive activation of signal transducers and activators of transcription predicts vorinostat resistance in cutaneous T-cell lymphoma. Cancer Research 2008, 68:3785-3794.
65. Edwards A., Li J., Atadja P., Bhalla K., Haura E.B. Effect of the histone deacetylase inhibitor LBH589 against epidermal growth factor receptor-dependent human lung cancer cells. Molecular Cancer Therapeutics 2007, 6:2515-2524.
66. Tang Y.A., Wen W.L., Chang J.W., Wei T.T., Tan Y.H., Salunke S., et al. A novel histone deacetylase inhibitor exhibits antitumor activity via apoptosis induction F-actin disruption and gene acetylation in lung cancer. PloS ONE 2010, 5:e12417.
67. Hubaux R., Vandermeers F., Crisanti M.C., Kapoor V., Burny A., Mascaux C., et al. Preclinical evidence for a beneficial impact of valproate on the response of small cell lung cancer to first-line chemotherapy. European Journal of Cancer 2010, 46:1724-1734.
68. Chai G., Li L., Zhou W., Wu L., Zhao Y., Wang D., et al. HDAC inhibitors act with 5-aza-2'-deoxycytidine to inhibit cell proliferation by suppressing removal of incorporated abases in lung cancer cells. PloS ONE 2008, 3:e2445.
69. Han S., Fukazawa T., Yamatsuji T., Matsuoka J., Miyachi H., Maeda Y., et al. Anti-tumor effect in human lung cancer by a combination treatment of novel histone deacetylase inhibitors: SL142 or SL325 and retinoic acids. PloS ONE 2010, 5:e13834.
70. Karelia N., Desai D., Hengst J.A., Amin S., Rudrabhatla S.V., Yun J. Selenium-containing analogs of SAHA induce cytotoxicity in lung cancer cells. Bioorganic & Medicinal Chemistry Letters 2010, 20:6816-6819.
71. Pang M., Kothapally J., Mao H., Tolbert E., Ponnusamy M., Chin Y.E., et al. Inhibition of histone deacetylase activity attenuates renal fibroblast activation and interstitial fibrosis in obstructive nephropathy. American Journal of Physiology Renal Physiology 2009, 297:F996-F1005.
72. Gupta M., Han J.J., Stenson M., Wellik L., Witzig T.E. Regulation of STAT3 by histone deacetylase-3 in diffuse large B-cell lymphoma: implications for therapy. Leukemia: Official Journal of the Leukemia Society of America, Leukemia Research Fund, UK 2011.
73. Klampfer L., Huang J., Swaby L.A., Augenlicht L. Requirement of histone deacetylase activity for signaling by STAT1. The Journal of Biological Chemistry 2004, 279:30358-30368.
74. Roos W.P., Jöst E., Belohlavek C., Nagel G., Fritz G., Kaina B. Intrinsic anticancer drug resistance of malignant melanoma cells is abrogated by IFN-beta and valproic acid. Cancer Research 2011, 71:4150-4160.
75. Häcker S., Dittrich A., Mohr A., Schweitzer T., Rutkowski S., Krauss J., et al. Histone deacetylase inhibitors cooperate with IFN-gamma to restore caspase-8 expression and overcome TRAIL resistance in cancers with silencing of caspase-8. Oncogene 2009, 28:3097-3110.
76. Hudak L., Tezeeh P., Wedel S., Makarevic J., Juengel E., Tsaur I., et al. Low dosed interferon alpha augments the anti-tumor potential of histone deacetylase inhibition on prostate cancer cell growth and invasion. The Prostate 2012.
77. Kreuzaler P.A., Staniszewska A.D., Li W., Omidvar N., Kedjouar B., Turkson J., et al. Stat3 controls lysosomal-mediated cell death in vivo. Nature Cell Biology 2011, 13:303-309.
78. Bauer K., Kretzschmar A.K., Cvijic H., Blumert C., Löffler D., Brocke-Heidrich K., et al. Cyclophilins contribute to Stat3 signaling and survival of multiple myeloma cells. Oncogene 2009, 28:2784-2795.
79. Szczepanek K., Chen Q., Larner A.C., Lesnefsky E.J. Cytoprotection by the modulation of mitochondrial electron transport chain: the emerging role of mitochondrial STAT3. Mitochondrion 2012, 12:180-189.
80. Reich N.C. STAT3 revs up the powerhouse. Science Signaling 2009, 2:pe61.
81. Shen L., Ciesielski M., Ramakrishnan S., Miles K.M., Ellis L., Sotomayor P., et al. Class I histone deacetylase inhibitor entinostat suppresses regulatory T cells and enhances immunotherapies in renal and prostate cancer models. PloS ONE 2012, 7:e30815.
82. Gough D.J., Messina N.L., Clarke C.J., Johnstone R.W., Levy D.E. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 2012, 36:166-174.
83. Hosui A., Klover P., Tatsumi T., Uemura A., Nagano H., Doki Y., et al. Suppression of signal transducers and activators of transcription 1 (STAT1) in hepatocellular carcinoma is associated with tumor progression. International Journal of Cancer Journal International du Cancer 2012.
84. Schneckenleithner C., Bago-Horvath Z., Dolznig H., Neugebauer N., Kollmann K., Kolbe T., et al. Putting the brakes on mammary tumorigenesis: loss of STAT1 predisposes to intraepithelial neoplasias. Oncotarget 2011, 2:1043-1054.
85. Kovacic B., Stoiber D., Moriggl R., Weisz E., Ott R.G., Kreibich R., et al. STAT1 acts as a tumor promoter for leukemia development. Cancer Cell 2006, 10:77-87.
86. Stronach E.A., Alfraidi A., Rama N., Datler C., Studd J.B., Agarwal R., et al. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Research 2011, 71:4412-4422.
87. Guo L., Guo H., Gao C., Mi Z., Russell W.B., Kuo P.C. Stat1 acetylation inhibits inducible nitric oxide synthase expression in interferon-gamma-treated RAW264.7 murine macrophages. Surgery 2007, 142:156-162.
88. Krämer O.H., Knauer S.K., Greiner G., Jandt E., Reichardt S., Gührs K.H., et al. A phosphorylation-acetylation switch regulates STAT1 signaling. Genes & Development 2009, 23:223-235.
89. Tang X., Gao J.S., Guan Y.J., McLane K.E., Yuan Z.L., Ramratnam B., et al. Acetylation-dependent signal transduction for type I interferon receptor. Cell 2007, 131:93-105.
90. Cudejko C., Wouters K., Fuentes L., Hannou S.A., Paquet C., Bantubungi K., et al. p16INK4a deficiency promotes IL-4-induced polarization and inhibits proinflammatory signaling in macrophages. Blood 2011, 118:2556-2566.
91. Ginter T., Bier C., Knauer S.K., Sughra K., Hildebrand D., Münz T., et al. Histone deacetylase inhibitors block IFNgamma-induced STAT1 phosphorylation. Cellular Signalling 2012, 24:1453-1460.
92. Zupkovitz G., Tischler J., Posch M., Sadzak I., Ramsauer K., Egger G., et al. Negative and positive regulation of gene expression by mouse histone deacetylase 1. Molecular and Cellular Biology 2006, 26:7913-7928.
93. Nguyen T.L., Abdelbary H., Arguello M., Breitbach C., Leveille S., Diallo J.S., et al. Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proceedings of the National Academy of Sciences of the United States of America 2008, 14981-14986.
94. Vlasáková J., Nováková Z., Rossmeislová L., Kahle M., Hozák P., Hodny Z. Histone deacetylase inhibitors suppress IFNalpha-induced up-regulation of promyelocytic leukemia protein. Blood 2007, 109:1373-1380.
95. Klampfer L., Huang J., Sasazuki T., Shirasawa S., Augenlicht L. Inhibition of interferon gamma signaling by the short chain fatty acid butyrate. Molecular Cancer Research: MCR 2003, 1:855-862.
96. Chang H.M., Paulson M., Holko M., Rice C.M., Williams B.R., Marie I., et al. Induction of interferon-stimulated gene expression and antiviral responses require protein deacetylase activity. Proceedings of the National Academy of Sciences of the United States of America 2004, 9578-9583.
97. Nusinzon I., Horvath C.M. Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1. Proceedings of the National Academy of Sciences of the United States of America 2003, 14742-14747.
98. Schneider G., Krämer O.H. NFkappaB/p53 crosstalk-a promising new therapeutic target. Biochimica et Biophysica Acta 2011, 1815:90-103.
99. Kim K.S., Kang K.W., Seu Y.B., Baek S.H., Kim J.R. Interferon-gamma induces cellular senescence through p53-dependent DNA damage signaling in human endothelial cells. Mechanisms of Ageing and Development 2009, 130:179-188.
100. Moiseeva O., Mallette F.A., Mukhopadhyay U.K., Moores A., Ferbeyre G. DNA damage signaling and p53-dependent senescence after prolonged beta-interferon stimulation. Molecular Biology of the Cell 2006, 17:1583-1592.
101. Brandl A., Wagner T., Uhlig K.M., Knauer S.K., Stauber R.H., Melchior F., et al. Dynamically regulated sumoylation of HDAC2 controls p53 deacetylation and restricts apoptosis following genotoxic stress. Journal of Molecular Cell Biology 2012.
102. Knights C.D., Catania J., Di Giovanni S., Muratoglu S., Perez R., Swartzbeck A., et al. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. The Journal of Cell Biology 2006, 173:533-544.
103. Sadzak I., Schiff M., Gattermeier I., Glinitzer R., Sauer I., Saalmuller A., et al. Recruitment of Stat1 to chromatin is required for interferon-induced serine phosphorylation of Stat1 transactivation domain. Proceedings of the National Academy of Sciences of the United States of America 2008, 8944-8949.
104. Antunes F., Marg A., Vinkemeier U. STAT1 signaling is not regulated by a phosphorylation-acetylation switch. Molecular and Cellular Biology 2011, 31:3029-3037.
105. Regis G., Pensa S., Boselli D., Novelli F., Poli V. Ups and downs: the STAT1:STAT3 seesaw of Interferon and gp130 receptor signalling. Seminars in Cell & Developmental Biology 2008, 19:351-359.
106. Novac N., Heinzel T. Nuclear receptors: overview and classification. Current Drug Targets Inflammation and Allergy 2004, 3:335-346.
107. Niedenthal R. Ubc9 fusion-directed SUMOylation (UFDS). Biochemical Society Transactions 2007, 35:1430-1432.
108. Rogers R.S., Horvath C.M., Matunis M.J. SUMO modification of STAT1 and its role in PIAS-mediated inhibition of gene activation. The Journal of Biological Chemistry 2003, 278:30091-30097.
109. Song L., Bhattacharya S., Yunus A.A., Lima C.D., Schindler C. Stat1 and SUMO modification. Blood 2006, 108:3237-3244.
110. Van Nguyen T., Angkasekwinai P., Dou H., Lin F.M., Lu L.S., Cheng J., et al. SUMO-specific protease 1 is critical for early lymphoid development through regulation of STAT5 activation. Molecular Cell 2012, 45:210-221.
111. Wang Y., Levy D.E.C., elegans S.T.A.T. evolution of a regulatory switch. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2006, 20:1641-1652.
112. Lin J., Buettner R., Yuan Y.C., Yip R., Horne D., Jove R., et al. Molecular dynamics simulations of the conformational changes in signal transducers and activators of transcription, Stat1 and Stat3. Journal of Molecular Graphics & Modelling 2009, 28:347-356.
113. Genin P., Morin P., Civas A. Impairment of interferon-induced IRF-7 gene expression due to inhibition of ISGF3 formation by trichostatin A. Journal of Virology 2003, 77:7113-7119.
114. Icardi L., Lievens S., Mori R., Piessevaux J., De Cauwer L., De Bosscher K., et al. Opposed regulation of type I IFN-induced STAT3 and ISGF3 transcriptional activities by histone deacetylases (HDACS) 1 and 2. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2012, 26:240-249.
115. Ferbeyre G., Moriggl R. The role of Stat5 transcription factors as tumor suppressors or oncogenes. Biochimica et Biophysica Acta 2011, 1815:104-114.
116. Wang Z., Li G., Tse W., Bunting K.D. Conditional deletion of STAT5 in adult mouse hematopoietic stem cells causes loss of quiescence and permits efficient nonablative stem cell replacement. Blood 2009, 113:4856-4865.
117. Friedbichler K., Hoelbl A., Li G., Bunting K.D., Sexl V., Gouilleux F., et al. Serine phosphorylation of the Stat5a C-terminus is a driving force for transformation. Frontiers in Bioscience: A Journal and Virtual Library 2012, 17:3043-3056.
118. Friedbichler K., Kerenyi M.A., Kovacic B., Li G., Hoelbl A., Yahiaoui S., et al. Stat5a serine 725 and 779 phosphorylation is a prerequisite for hematopoietic transformation. Blood 2010, 116:1548-1558.
119. Page B.D., Khoury H., Laister R.C., Fletcher S., Vellozo M., Manzoli A., et al. Small molecule STAT5-SH2 domain inhibitors exhibit potent antileukemia activity. Journal of Medicinal Chemistry 2012, 55:1047-1055.
120. Tang Y., Zhao W., Chen Y., Zhao Y., Gu W. Acetylation is indispensable for p53 activation. Cell 2008, 133:612-626.
121. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
122. Ryan C.M., Harries J.C., Kindle K.B., Collins H.M., Heery D.M. Functional interaction of CREB binding protein (CBP) with nuclear transport proteins and modulation by HDAC inhibitors. Cell Cycle 2006, 5:2146-2152.
123. Gareau J.R., Lima C.D. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nature Reviews Molecular Cell Biology 2010, 11:861-871.
124. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nature Reviews Molecular Cell Biology 2007, 8:947-956.
125. Bawa-Khalfe T., Yeh E.T. SUMO losing balance: SUMO proteases disrupt SUMO homeostasis to facilitate cancer development and progression. Genes & Cancer 2010, 1:748-752.
126. Cheng J., Kang X., Zhang S., Yeh E.T. SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 2007, 131:584-595.
127. Rascle A., Johnston J.A., Amati B. Deacetylase activity is required for recruitment of the basal transcription machinery and transactivation by STAT5. Molecular and Cellular Biology 2003, 23:4162-4173.
128. Alvarez-Breckenridge C.A., Yu J., Price R., Wei M., Wang Y., Nowicki M.O., et al. The histone deacetylase inhibitor valproic acid lessens NK cell action against oncolytic virus-infected glioblastoma cells by inhibition of STAT5/T-BET signaling and generation of gamma interferon. Journal of Virology 2012, 86:4566-4577.
129. Nguyen T., Dai Y., Attkisson E., Kramer L., Jordan N., Nguyen N., et al. HDAC inhibitors potentiate the activity of the BCR/ABL kinase inhibitor KW-2449 in imatinib-sensitive or -resistant BCR/ABL+ leukemia cells in vitro and in vivo. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2011, 17:3219-3232.
130. Inks E.S., Josey B.J., Jesinkey S.R., Chou C.J. A novel class of small molecule inhibitors of HDAC6. ACS Chemical Biology 2012, 7:331-339.
131. Kosan C., Saba I., Godmann M., Herold S., Herkert B., Eilers M., et al. Transcription factor miz-1 is required to regulate interleukin-7 receptor signaling at early commitment stages of B cell differentiation. Immunity 2010, 33:917-928.
132. Saba I., Kosan C., Vassen L., Möröy T. IL-7R-dependent survival and differentiation of early T-lineage progenitors is regulated by the BTB/POZ domain transcription factor Miz-1. Blood 2011, 117:3370-3381.
133. Moriggl R., Sexl V., Kenner L., Duntsch C., Stangl K., Gingras S., et al. Stat5 tetramer formation is associated with leukemogenesis. Cancer Cell 2005, 7:87-99.
134. Tenoever B.R., Ng S.L., Chua M.A., McWhirter S.M., García-Sastre A., Maniatis T. Multiple functions of the IKK-related kinase IKKepsilon in interferon-mediated antiviral immunity. Science 2007, 315:1274-1278.
135. Ng S.L., Friedman B.A., Schmid S., Gertz J., Myers R.M., Tenoever B.R., et al. IkappaB kinase epsilon (IKK(epsilon)) regulates the balance between type I and type II interferon responses. Proceedings of the National Academy of Sciences of the United States of America 2011, 21170-21175.
136. Buchwald M., Pietschmann K., Müller J.P., Böhmer F.D., Heinzel T., Krämer O.H. Ubiquitin conjugase UBCH8 targets active FMS-like tyrosine kinase 3 for proteasomal degradation. Leukemia: Official Journal of the Leukemia Society of America, Leukemia Research Fund, UK 2010, 24:1412-1421.
137. Lin T.Y., Fenger J., Murahari S., Bear M.D., Kulp S.K., Wang D., et al. AR-42, a novel HDAC inhibitor, exhibits biologic activity against malignant mast cell lines via down-regulation of constitutively activated Kit. Blood 2010, 115:4217-4225.
138. Oestreich K.J., Weinmann A.S. Transcriptional mechanisms that regulate T helper 1 cell differentiation. Current Opinion in Immunology 2012, 24:191-195.
139. Dawson M.A., Bannister A.J., Gottgens B., Foster S.D., Bartke T., Green A.R., et al. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 2009, 461:819-822.
140. Yan S.J., Lim S.J., Shi S., Dutta P., Li W.X. Unphosphorylated STAT and heterochromatin protect genome stability. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2011, 25:232-241.
141. Wang H., Zhou W., Zheng Z., Zhang P., Tu B., He Q., et al. The HDAC inhibitor depsipeptide transactivates the p53/p21 pathway by inducing DNA damage. DNA Repair (Amst) 2012, 11:146-156.
142. Sakamoto S., Potla R., Larner A.C. Histone deacetylase activity is required to recruit RNA polymerase II to the promoters of selected interferon-stimulated early response genes. The Journal of Biological Chemistry 2004, 279:40362-40367.