Post-translational control of transcription factors: Methylation ranks highly

FEBS Journal

Volumn 282, Issue 23, 2015, Pages 4450-4465

  Carr, Simon M ^a   Poppy Roworth, A ^a   Chan, Cheryl ^a   La Thangue, Nicholas B ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

arginine methylation; E2F 1; lysine methylation; NF B; p53; PKMT; pRB; PRMT; transcription

Indexed keywords

HISTONE DEMETHYLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYLTRANSFERASE; PROTEIN P53; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F1; ARGININE; LYSINE;

APOPTOSIS; CARCINOGENESIS; CELL CYCLE REGULATION; DIFFERENTIATION; DNA REPAIR; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PROCESSING; REVIEW; SENESCENCE; STRUCTURE ANALYSIS; CHEMISTRY; METABOLISM; METHYLATION;

ARGININE; HUMANS; LYSINE; METHYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTION FACTORS;

EID: 84959128134     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13524     Document Type: Review

References (90)

1. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128, 693-705.
2. Tessarz P, &, Kouzarides T, (2014) Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol 15, 703-708.
3. Hamamoto R, Saloura V, &, Nakamura Y, (2015) Critical roles of non-histone protein lysine methylation in human tumorigenesis. Nat Rev Cancer 15, 110-124.
4. Biggar KK, &, Li SSC, (2015) Non-histone protein methylation as a regulator of cellular signalling and function. Nat Rev Mol Cell Biol 16, 5-17.
5. Yang Y, &, Bedford MT, (2013) Protein arginine methyltransferases and cancer. Nat Rev Cancer 13, 37-50.
6. Klose RJ, &, Zhang Y, (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8, 307-318.
7. Johansson C, Tumber A, Che K, Cain P, Nowak R, Gileadi C, &, Oppermann U, (2014) The roles of Jumonji-type oxygenases in human disease. Epigenomics 6, 89-120.
8. Bottger A, Islam MS, Chowdhury R, Schofield CJ, &, Wolf A, (2015) The oxygenase Jmjd6-a case study in conflicting assignments. Biochem J 468, 191-202.
9. Musselman CA, Lalonde ME, Cote J, &, Kutateladze TG, (2012) Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 19, 1218-1227.
10. Gayatri S, &, Bedford MT, (2014) Readers of histone methylarginine marks. Biochim Biophys Acta 1839, 702-710.
11. Poppy Roworth A, Ghari F, &, La Thangue NB, (2015) To live or let die-complexity within the E2F1 pathway. Mol Cell Oncol 2, e970480.
12. DeGregori J, Leone G, Miron A, Jakoi L, &, Nevins JR, (1997) Distinct roles for E2F proteins in cell growth control and apoptosis. Proc Natl Acad Sci U S A 94, 7245-7250.
13. Cho EC, Zheng S, Munro S, Liu G, Carr SM, Moehlenbrink J, Lu YC, Stimson L, Khan O, Konietzny R, et al,. (2012) Arginine methylation controls growth regulation by E2F-1. EMBO J 31, 1785-1797.
14. Zheng S, Moehlenbrink J, Lu YC, Zalmas LP, Sagum CA, Carr S, McGouran JF, Alexander L, Fedorov O, Munro S, et al,. (2013) Arginine methylation-dependent reader-writer interplay governs growth control by E2F-1. Mol Cell 52, 37-51.
15. Yang J, Valineva T, Hong J, Bu T, Yao Z, Jensen ON, Frilander MJ, &, Silvennoinen O, (2007) Transcriptional co-activator protein p100 interacts with snRNP proteins and facilitates the assembly of the spliceosome. Nucleic Acids Res 35, 4485-4494.
16. Valineva T, Yang J, Palovuori R, &, Silvennoinen O, (2005) The transcriptional co-activator protein p100 recruits histone acetyltransferase activity to STAT6 and mediates interaction between the CREB-binding protein and STAT6. J Biol Chem 280, 14989-14996.
17. Bao X, Zhao S, Liu T, Liu Y, Liu Y, &, Yang X, (2013) Overexpression of PRMT5 promotes tumor cell growth and is associated with poor disease prognosis in epithelial ovarian cancer. J Histochem Cytochem 61, 206-217.
18. Kontaki H, &, Talianidis I, (2010) Lysine methylation regulates E2F1-induced cell death. Mol Cell 39, 152-160.
19. Xie Q, Bai Y, Wu J, Sun Y, Wang Y, Zhang Y, Mei P, &, Yuan Z, (2011) Methylation-mediated regulation of E2F1 in DNA damage-induced cell death. J Rec Signal Transd Res 31, 139-146.
20. Loftus SJ, Liu G, Carr SM, Munro S, &, La Thangue NB, (2012) NEDDylation regulates E2F-1-dependent transcription. EMBO Rep 13, 811-818.
21. Aoki I, Higuchi M, &, Gotoh Y, (2013) NEDDylation controls the target specificity of E2F1 and apoptosis induction. Oncogene 32, 3954-3964.
22. Montenegro MF, Saez-Ayala M, Pinero-Madrona A, Cabezas-Herrera J, &, Rodriguez-Lopez JN, (2012) Reactivation of the tumour suppressor RASSF1A in breast cancer by simultaneous targeting of DNA and E2F1 methylation. PLoS One 7, e52231.
23. van den Heuvel S, &, Dyson NJ, (2008) Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Biol 9, 713-724.
24. Longworth MS, &, Dyson NJ, (2010) pRb, a local chromatin organizer with global possibilities. Chromosoma 119, 1-11.
25. Sherr CJ, &, McCormick F, (2002) The RB and p53 pathways in cancer. Cancer Cell 2, 103-112.
26. Indovina P, Marcelli E, Casini N, Rizzo V, &, Giordano A, (2013) Emerging roles of RB family: new defense mechanisms against tumor progression. J Cell Physiol 228, 525-535.
27. Kim KY, Wang DH, Campbell M, Huerta SB, Shevchenko B, Izumiya C, &, Izumiya Y, (2015) PRMT4-mediated arginine methylation negatively regulates retinoblastoma tumor suppressor protein and promotes E2F-1 dissociation. Mol Cell Biol 35, 238-248.
28. Munro S, Khaire N, Inche A, Carr S, &, La Thangue NB, (2010) Lysine methylation regulates the pRb tumour suppressor protein. Oncogene 29, 2357-2367.
29. Hediger F, &, Gasser SM, (2006) Heterochromatin protein 1: don't judge the book by its cover!. Curr Opin Genet Dev 16, 143-150.
30. Carr SM, Munro S, Kessler B, Oppermann U, &, La Thangue NB, (2011) Interplay between lysine methylation and Cdk phosphorylation in growth control by the retinoblastoma protein. EMBO J 30, 317-327.
31. Carr SM, Munro S, Zalmas LP, Fedorov O, Johansson C, Krojer T, Sagum CA, Bedford MT, Oppermann U, &, La Thangue NB, (2014) Lysine methylation-dependent binding of 53BP1 to the pRb tumor suppressor. Proc Natl Acad Sci U S A 111, 11341-11346.
32. Panier S, &, Boulton SJ, (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15, 7-18.
33. Cook R, Zoumpoulidou G, Luczynski MT, Rieger S, Moquet J, Spanswick VJ, Hartley JA, Rothkamm K, Huang PH, &, Mittnacht S, (2015) Direct Involvement of retinoblastoma family proteins in DNA repair by non-homologous end-joining. Cell Rep 10, 2006-2018.
34. Barradas M, Anderton E, Acosta JC, Li S, Banito A, Rodriguez-Niedenfuhr M, Maertens G, Banck M, Zhou MM, Walsh MJ, et al,. (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 23, 1177-1182.
35. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, Christensen J, &, Helin K, (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev 23, 1171-1176.
36. Zhao L, Zhang Y, Gao Y, Geng P, Lu Y, Liu X, Yao R, Hou P, Liu D, Lu J, et al,. (2015) JMJD3 promotes SAHF formation in senescent WI38 cells by triggering an interplay between demethylation and phosphorylation of RB protein. Cell Death Differ 22, 1630-1640.
37. Saddic LA, West LE, Aslanian A, Yates JR 3rd, Rubin SM, Gozani O, &, Sage J, (2010) Methylation of the retinoblastoma tumor suppressor by SMYD2. J Biol Chem 285, 37733-37740.
38. Cho HS, Hayami S, Toyokawa G, Maejima K, Yamane Y, Suzuki T, Dohmae N, Kogure M, Kang D, Neal DE, et al,. (2012) RB1 methylation by SMYD2 enhances cell cycle progression through an increase of RB1 phosphorylation. Neoplasia (New York, NY) 14, 476-486.
39. Trojer P, Li G, Sims RJ 3rd, Vaquero A, Kalakonda N, Boccuni P, Lee D, Erdjument-Bromage H, Tempst P, Nimer SD, et al,. (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129, 915-928.
40. Brown MA, Sims RJ, Gottlieb PD, &, Tucker PW, (2006) Identification and characterization of Smyd2: a split SET/MYND domain-containing histone H3 lysine 36-specific methyltransferase that interacts with the Sin3 histone deacetylase complex. Mol Cancer 5, 26.
41. Lawrence T, (2009) The nuclear factor NF-κB pathway in inflammation. Cold Spring Harbor Pers Biol 1, a001651.
42. Hoesel B, &, Schmid JA, (2013) The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer 12, 86.
43. Wei H, Wang B, Miyagi M, She Y, Gopalan B, Huang DB, Ghosh G, Stark GR, &, Lu T, (2013) PRMT5 dimethylates R30 of the p65 subunit to activate NF-kappaB. Proc Natl Acad Sci U S A 110, 13516-13521.
44. Lu T, Jackson MW, Wang B, Yang M, Chance MR, Miyagi M, Gudkov AV, &, Stark GR, (2010) Regulation of NF-kappaB by NSD1/FBXL11-dependent reversible lysine methylation of p65. Proc Natl Acad Sci U S A 107, 46-51.
45. Ea C-K, &, Baltimore D, (2009) Regulation of NF-κB activity through lysine monomethylation of p65. Proc Natl Acad Sci U S A 106, 18972-18977.
46. Lu T, Yang M, Huang DB, Wei H, Ozer GH, Ghosh G, &, Stark GR, (2013) Role of lysine methylation of NF-kappaB in differential gene regulation. Proc Natl Acad Sci U S A 110, 13510-13515.
47. Yang X-D, Huang B, Li M, Lamb A, Kelleher NL, &, Chen L-F, (2009) Negative regulation of NF-κB action by Set9-mediated lysine methylation of the RelA subunit. EMBO J 28, 1055-1066.
48. Levy D, Kuo AJ, Chang Y, Schaefer U, Kitson C, Cheung P, Espejo A, Zee BM, Liu CL, Tangsombatvisit S, et al,. (2011) Lysine methylation of the NF-kappaB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-kappaB signaling. Nat Immunol 12, 29-36.
49. Li Y, Reddy MA, Miao F, Shanmugam N, Yee JK, Hawkins D, Ren B, &, Natarajan R, (2008) Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. J Biol Chem 283, 26771-26781.
50. Lu T, Jackson MW, Singhi AD, Kandel ES, Yang M, Zhang Y, Gudkov AV, &, Stark GR, (2009) Validation-based insertional mutagenesis identifies lysine demethylase FBXL11 as a negative regulator of NFkappaB. Proc Natl Acad Sci U S A 106, 16339-16344.
51. Zhang T, Park KA, Li Y, Byun HS, Jeon J, Lee Y, Hong JH, Kim JM, Huang SM, Choi SW, et al,. (2013) PHF20 regulates NF-kappaB signalling by disrupting recruitment of PP2A to p65. Nat Commun 4, 2062.
52. Riley T, Sontag E, Chen P, &, Levine A, (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9, 402-412.
53. Murray-Zmijewski F, Slee EA, &, Lu X, (2008) A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol 9, 702-712.
54. Jansson M, Durant ST, Cho EC, Sheahan S, Edelmann M, Kessler B, &, La Thangue NB, (2008) Arginine methylation regulates the p53 response. Nat Cell Biol 10, 1431-1439.
55. Li Y, Chitnis N, Nakagawa H, Kita Y, Natsugoe S, Yang Y, Li Z, Wasik M, Klein-Szanto AJ, Rustgi AK, et al,. (2015) PRMT5 is required for lymphomagenesis triggered by multiple oncogenic drivers. Cancer Discov 5, 288-303.
56. Chuikov S, Kurash JK, Wilson JR, Xiao B, Justin N, Ivanov GS, McKinney K, Tempst P, Prives C, Gamblin SJ, et al,. (2004) Regulation of p53 activity through lysine methylation. Nature 432, 353-360.
57. Ivanov GS, Ivanova T, Kurash J, Ivanov A, Chuikov S, Gizatullin F, Herrera-Medina EM, Rauscher F 3rd, Reinberg D, &, Barlev NA, (2007) Methylation-acetylation interplay activates p53 in response to DNA damage. Mol Cell Biol 27, 6756-6769.
58. Kurash JK, Lei H, Shen Q, Marston WL, Granda BW, Fan H, Wall D, Li E, &, Gaudet F, (2008) Methylation of p53 by Set7/9 mediates p53 acetylation and activity in vivo. Mol Cell 29, 392-400.
59. Campaner S, Spreafico F, Burgold T, Doni M, Rosato U, Amati B, &, Testa G, (2011) The methyltransferase Set7/9 (Setd7) is dispensable for the p53-mediated DNA damage response in vivo. Mol Cell 43, 681-688.
60. Lehnertz B, Rogalski JC, Schulze FM, Yi L, Lin S, Kast J, &, Rossi FM, (2011) p53-dependent transcription and tumor suppression are not affected in Set7/9-deficient mice. Mol Cell 43, 673-680.
61. Huang J, Perez-Burgos L, Placek BJ, Sengupta R, Richter M, Dorsey JA, Kubicek S, Opravil S, Jenuwein T, &, Berger SL, (2006) Repression of p53 activity by Smyd2-mediated methylation. Nature 444, 629-632.
62. Huang J, Sengupta R, Espejo AB, Lee MG, Dorsey JA, Richter M, Opravil S, Shiekhattar R, Bedford MT, Jenuwein T, et al,. (2007) p53 is regulated by the lysine demethylase LSD1. Nature 449, 105-108.
63. Shi X, Kachirskaia I, Yamaguchi H, West LE, Wen H, Wang EW, Dutta S, Appella E, &, Gozani O, (2007) Modulation of p53 function by SET8-mediated methylation at lysine 382. Mol Cell 27, 636-646.
64. West LE, Roy S, Lachmi-Weiner K, Hayashi R, Shi X, Appella E, Kutateladze TG, &, Gozani O, (2010) The MBT repeats of L3MBTL1 link SET8-mediated p53 methylation at lysine 382 to target gene repression. J Biol Chem 285, 37725-37732.
65. Kachirskaia I, Shi X, Yamaguchi H, Tanoue K, Wen H, Wang EW, Appella E, &, Gozani O, (2008) Role for 53BP1 Tudor domain recognition of p53 dimethylated at lysine 382 in DNA damage signaling. J Biol Chem 283, 34660-34666.
66. Cui G, Park S, Badeaux AI, Kim D, Lee J, Thompson JR, Yan F, Kaneko S, Yuan Z, Botuyan MV, et al,. (2012) PHF20 is an effector protein of p53 double lysine methylation that stabilizes and activates p53. Nat Struct Mol Biol 19, 916-924.
67. Huang J, Dorsey J, Chuikov S, Perez-Burgos L, Zhang X, Jenuwein T, Reinberg D, &, Berger SL, (2010) G9a and Glp methylate lysine 373 in the tumor suppressor p53. J Biol Chem 285, 9636-9641.
68. Chen L, Li Z, Zwolinska AK, Smith MA, Cross B, Koomen J, Yuan ZM, Jenuwein T, Marine JC, Wright KL, et al,. (2010) MDM2 recruitment of lysine methyltransferases regulates p53 transcriptional output. EMBO J 29, 2538-2552.
69. DeHart CJ, Chahal JS, Flint SJ, &, Perlman DH, (2014) Extensive post-translational modification of active and inactivated forms of endogenous p53. Mol Cell Proteomics 13, 1-17.
70. McGrath J, &, Trojer P, (2015) Targeting histone lysine methylation in cancer. Pharmacol Ther 150, 1-22.
71. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, Paul JE, Boyle M, Woolcock BW, Kuchenbauer F, et al,. (2010) Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet 42, 181-185.
72. Gui Y, Guo G, Huang Y, Hu X, Tang A, Gao S, Wu R, Chen C, Li X, Zhou L, et al,. (2011) Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet 43, 875-878.
73. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, et al,. (2011) The genetic landscape of the childhood cancer medulloblastoma. Science 331, 435-439.
74. He J, Nguyen AT, &, Zhang Y, (2011) KDM2b/JHDM1b, an H3K36me2-specific demethylase, is required for initiation and maintenance of acute myeloid leukemia. Blood 117, 3869-3880.
75. van Haaften G, Dalgliesh GL, Davies H, Chen L, Bignell G, Greenman C, Edkins S, Hardy C, O'Meara S, Teague J, et al,. (2009) Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat Genet 41, 521-523.
76. Maes T, Carceller E, Salas J, Ortega A, &, Buesa C, (2015) Advances in the development of histone lysine demethylase inhibitors. Curr Opin Pharmacol 23, 52-60.
77. Kaniskan HÜ, Konze KD, &, Jin J, (2015) Selective inhibitors of protein methyltransferases. J Med Chem 58, 1596-1629.
78. Musselman CA, Khorasanizadeh S, &, Kutateladze TG, (2014) Towards understanding methyllysine readout. Biochim Biophys Acta 1839, 686-693.
79. James LI, Barsyte-Lovejoy D, Zhong N, Krichevsky L, Korboukh VK, Herold JM, MacNevin CJ, Norris JL, Sagum CA, Tempel W, et al,. (2013) Discovery of a chemical probe for the L3MBTL3 methyllysine reader domain. Nat Chem Biol 9, 184-191.
80. Avasarala S, Van Scoyk M, Karuppusamy Rathinam MK, Zerayesus S, Zhao X, Zhang W, Pergande MR, Borgia JA, DeGregori J, Port JD, et al,. (2015) PRMT1 is a novel regulator of epithelial-mesenchymal-transition in non-small cell lung cancer. J Biol Chem 290, 13479-13489.
81. Yamagata K, Daitoku H, Takahashi Y, Namiki K, Hisatake K, Kako K, Mukai H, Kasuya Y, &, Fukamizu A, (2008) Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol Cell 32, 221-231.
82. Davies CC, Chakraborty A, Diefenbacher ME, Skehel M, &, Behrens A, (2013) Arginine methylation of the c-Jun coactivator RACO-1 is required for c-Jun/AP-1 activation. EMBO J 32, 1556-1567.
83. Hosokawa H, Kato M, Tohyama H, Tamaki Y, Endo Y, Kimura MY, Tumes DJ, Motohashi S, Matsumoto M, Nakayama KI, et al,. (2015) Methylation of gata3 protein at arg-261 regulates transactivation of the il5 gene in T helper 2 cells. J Biol Chem 290, 13095-13103.
84. Bandyopadhyay S, Harris DP, Adams GN, Lause GE, McHugh A, Tillmaand EG, Money A, Willard B, Fox PL, &, Dicorleto PE, (2012) HOXA9 methylation by PRMT5 is essential for endothelial cell expression of leukocyte adhesion molecules. Mol Cell Biol 32, 1202-1213.
85. Zhao X, Jankovic V, Gural A, Huang G, Pardanani A, Menendez S, Zhang J, Dunne R, Xiao A, Erdjument-Bromage H, et al,. (2008) Methylation of RUNX1 by PRMT1 abrogates SIN3A binding and potentiates its transcriptional activity. Genes Dev 22, 640-653.
86. Naeem H, Cheng D, Zhao Q, Underhill C, Tini M, Bedford MT, &, Torchia J, (2007) The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol Cell Biol 27, 120-134.
87. Le Romancer M, Treilleux I, Leconte N, Robin-Lespinasse Y, Sentis S, Bouchekioua-Bouzaghou K, Goddard S, Gobert-Gosse S, &, Corbo L, (2008) Regulation of estrogen rapid signaling through arginine methylation by PRMT1. Mol Cell 31, 212-221.
88. Maganti AV, Maier B, Tersey SA, Sampley ML, Mosley AL, Ozcan S, Pachaiyappan B, Woster PM, Hunter CS, Stein R, et al,. (2015) Transcriptional activity of the islet beta cell factor Pdx1 is augmented by lysine methylation catalyzed by the methyltransferase Set7/9. J Biol Chem 290, 9812-9822.
89. Dasgupta M, Dermawan JK, Willard B, &, Stark GR, (2015) STAT3-driven transcription depends upon the dimethylation of K49 by EZH2. Proc Natl Acad Sci U S A 112, 3985-3990.
90. Fang L, Zhang L, Wei W, Jin X, Wang P, Tong Y, Li J, Du JX, &, Wong J, (2014) A methylation-phosphorylation switch determines Sox2 stability and function in ESC maintenance or differentiation. Mol Cell 55, 537-551.