EGFR Modulates DNA Synthesis and Repair through Tyr Phosphorylation of Histone H4

Developmental Cell

Volumn 30, Issue 2, 2014, Pages 224-237

  Chou, Ruey Hwang ^a,b   Wang, Ying Nai ^a,c   Hsieh, Yi Hsien ^a   Li, Long Yuan ^a,b   Xia, Weiya ^c   Chang, Wei Chao ^a,d   Chang, Ling Chu ^a   Cheng, Chien Chia ^c   Lai, Chien Chen ^a   Hsu, Jennifer L ^a,c   Chang, Wei Jung ^a   Chiang, Shu Ya ^a   Lee, Hong Jen ^e   Liao, Hsin Wei ^e   Chuang, Pei Huan ^a   Chen, Hui Yu ^a   Wang, Hung Ling ^a   Kuo, Sheng Chu ^a   Chen, Chung Hsuan ^d   Yu, Yung Luen ^a,b   Hung, Mien Chie ^a,b,c,e   more..

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b ASIA UNIVERSITY   (Taiwan)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d GENOMICS RESEARCH CENTER   (Taiwan)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; HISTONE H4; HISTONE METHYLTRANSFERASE; KI 67 ANTIGEN; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DNA METHYLATION; DNA REPAIR; DNA SYNTHESIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANIMALS; CELL LINE, TUMOR; DNA REPLICATION; FEMALE; HEK293 CELLS; HISTONES; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINATIONAL DNA REPAIR; TYROSINE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904884937     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.06.008     Document Type: Article

References (55)

1. Beck D.B., Burton A., Oda H., Ziegler-Birling C., Torres-Padilla M.E., Reinberg D. The role of PR-Set7 in replication licensing depends on Suv4-20h. Genes Dev. 2012, 26:2580-2589.
2. Blagoev B., Kratchmarova I., Ong S.E., Nielsen M., Foster L.J., Mann M. A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat. Biotechnol. 2003, 21:315-318.
3. Botuyan M.V., Lee J., Ward I.M., Kim J.E., Thompson J.R., Chen J., Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 2006, 127:1361-1373.
4. Chen H.C., Appeddu P.A., Isoda H., Guan J.L. Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J. Biol. Chem. 1996, 271:26329-26334.
5. Chen Y.J., Huang W.C., Wei Y.L., Hsu S.C., Yuan P., Lin H.Y., Wistuba I.I., Lee J.J., Yen C.J., Su W.C., et al. Elevated BCRP/ABCG2 expression confers acquired resistance to gefitinib in wild-type EGFR-expressing cells. PLoS ONE 2011, 6:e21428.
6. Dawson M.A., Bannister A.J., Göttgens B., Foster S.D., Bartke T., Green A.R., Kouzarides T. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 2009, 461:819-822.
7. Dittmann K., Mayer C., Fehrenbacher B., Schaller M., Raju U., Milas L., Chen D.J., Kehlbach R., Rodemann H.P. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J. Biol. Chem. 2005, 280:31182-31189.
8. Dittmann K., Mayer C., Kehlbach R., Rodemann H.P. Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol. Cancer 2008, 7:69.
9. Dittmann K., Mayer C., Fehrenbacher B., Schaller M., Kehlbach R., Rodemann H.P. Nuclear EGFR shuttling induced by ionizing radiation is regulated by phosphorylation at residue Thr654. FEBS Lett. 2010, 584:3878-3884.
10. Fang J., Feng Q., Ketel C.S., Wang H., Cao R., Xia L., Erdjument-Bromage H., Tempst P., Simon J.A., Zhang Y. Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 2002, 12:1086-1099.
11. Fukuda H., Sano N., Muto S., Horikoshi M. Simple histone acetylation plays a complex role in the regulation of gene expression. Brief. Funct. Genomics Proteomics 2006, 5:190-208.
12. Gomes D.A., Rodrigues M.A., Leite M.F., Gomez M.V., Varnai P., Balla T., Bennett A.M., Nathanson M.H. c-Met must translocate to the nucleus to initiate calcium signals. J. Biol. Chem. 2008, 283:4344-4351.
13. Han W., Lo H.W. Landscape of EGFR signaling network in human cancers: biology and therapeutic response in relation to receptor subcellular locations. Cancer Lett. 2012, 318:124-134.
14. He W., Rose D.W., Olefsky J.M., Gustafson T.A. Grb10 interacts differentially with the insulin receptor, insulin-like growth factor I receptor, and epidermal growth factor receptor via the Grb10 Src homology 2 (SH2) domain and a second novel domain located between the pleckstrin homology and SH2 domains. J. Biol. Chem. 1998, 273:6860-6867.
15. Hsu S.C., Hung M.C. Characterization of a novel tripartite nuclear localization sequence in the EGFR family. J. Biol. Chem. 2007, 282:10432-10440.
16. Hsu S.C., Miller S.A., Wang Y., Hung M.C. Nuclear EGFR is required for cisplatin resistance and DNA repair. Am. J. Transl. Res. 2009, 1:249-258.
17. Huang W.C., Chen Y.J., Li L.Y., Wei Y.L., Hsu S.C., Tsai S.L., Chiu P.C., Huang W.P., Wang Y.N., Chen C.H., et al. Nuclear translocation of epidermal growth factor receptor by Akt-dependent phosphorylation enhances breast cancer-resistant protein expression in gefitinib-resistant cells. J. Biol. Chem. 2011, 286:20558-20568.
18. Huen M.S., Sy S.M., van Deursen J.M., Chen J. Direct interaction between SET8 and proliferating cell nuclear antigen couples H4-K20 methylation with DNA replication. J. Biol. Chem. 2008, 283:11073-11077.
19. Huo L., Wang Y.N., Xia W., Hsu S.C., Lai C.C., Li L.Y., Chang W.C., Wang Y., Hsu M.C., Yu Y.L., et al. RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc. Natl. Acad. Sci. USA 2010, 107:16125-16130.
20. Jørgensen S., Elvers I., Trelle M.B., Menzel T., Eskildsen M., Jensen O.N., Helleday T., Helin K., Sørensen C.S. The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 2007, 179:1337-1345.
21. Lee T.H., Seng S., Sekine M., Hinton C., Fu Y., Avraham H.K., Avraham S. Vascular endothelial growth factor mediates intracrine survival in human breast carcinoma cells through internally expressed VEGFR1/FLT1. PLoS Med. 2007, 4:e186.
22. Li C., Iida M., Dunn E.F., Ghia A.J., Wheeler D.L. Nuclear EGFR contributes to acquired resistance to cetuximab. Oncogene 2009, 28:3801-3813.
23. Lin S.Y., Makino K., Xia W., Matin A., Wen Y., Kwong K.Y., Bourguignon L., Hung M.C. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat. Cell Biol. 2001, 3:802-808.
24. Lo H.W. Nuclear mode of the EGFR signaling network: biology, prognostic value, and therapeutic implications. Discov. Med. 2010, 10:44-51.
25. Lo H.W., Hsu S.C., Ali-Seyed M., Gunduz M., Xia W., Wei Y., Bartholomeusz G., Shih J.Y., Hung M.C. Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell 2005, 7:575-589.
26. Mahajan K., Fang B., Koomen J.M., Mahajan N.P. H2B Tyr37 phosphorylation suppresses expression of replication-dependent core histone genes. Nat. Struct. Mol. Biol. 2012, 19:930-937.
27. Martin C., Zhang Y. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 2005, 6:838-849.
28. Munshi A., Shafi G., Aliya N., Jyothy A. Histone modifications dictate specific biological readouts. J. Genet. Genomics 2009, 36:75-88.
29. Oda H., Hübner M.R., Beck D.B., Vermeulen M., Hurwitz J., Spector D.L., Reinberg D. Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 2010, 40:364-376.
30. Pesavento J.J., Mizzen C.A., Kelleher N.L. Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: human histone H4. Anal. Chem. 2006, 78:4271-4280.
31. Peterson C.L., Laniel M.A. Histones and histone modifications. Curr. Biol. 2004, 14:R546-R551.
32. Qu Y.Y., Hu S.L., Xu X.Y., Wang R.Z., Yu H.Y., Xu J.Y., Chen L., Dong G.L. Nimotuzumab enhances the radiosensitivity of cancer cells in vitro by inhibiting radiation-induced DNA damage repair. PLoS ONE 2013, 8:e70727.
33. Reilly J.F., Maher P.A. Importin beta-mediated nuclear import of fibroblast growth factor receptor: role in cell proliferation. J. Cell Biol. 2001, 152:1307-1312.
34. Sanders S.L., Portoso M., Mata J., Bähler J., Allshire R.C., Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 2004, 119:603-614.
35. Schlessinger J., Lemmon M.A. SH2 and PTB domains in tyrosine kinase signaling. Sci. STKE 2003, 2003:RE12. 10.1126/stke.2003.191.re12.
36. Sehat B., Tofigh A., Lin Y., Trocmé E., Liljedahl U., Lagergren J., Larsson O. SUMOylation mediates the nuclear translocation and signaling of the IGF-1 receptor. Sci. Signal. 2010, 3:ra10.
37. Singh R.K., Kabbaj M.H., Paik J., Gunjan A. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 2009, 11:925-933.
38. Stachowiak E.K., Maher P.A., Tucholski J., Mordechai E., Joy A., Moffett J., Coons S., Stachowiak M.K. Nuclear accumulation of fibroblast growth factor receptors in human glial cells-association with cell proliferation. Oncogene 1997, 14:2201-2211.
39. Toulany M., Kasten-Pisula U., Brammer I., Wang S., Chen J., Dittmann K., Baumann M., Dikomey E., Rodemann H.P. Blockage of epidermal growth factor receptor-phosphatidylinositol 3-kinase-AKT signaling increases radiosensitivity of K-RAS mutated human tumor cells in vitro by affecting DNA repair. Clin. Cancer Res. 2006, 12:4119-4126.
40. Van Aller G.S., Reynoird N., Barbash O., Huddleston M., Liu S., Zmoos A.F., McDevitt P., Sinnamon R., Le B., Mas G., et al. Smyd3 regulates cancer cell phenotypes and catalyzes histone H4 lysine 5 methylation. Epigenetics 2012, 7:340-343.
41. Wang S.C., Hung M.C. Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin. Cancer Res. 2009, 15:6484-6489.
42. Wang Y.N., Hung M.C. Nuclear functions and subcellular trafficking mechanisms of the epidermal growth factor receptor family. Cell Biosci. 2012, 2:13.
43. Wang S.C., Nakajima Y., Yu Y.L., Xia W., Chen C.T., Yang C.C., McIntush E.W., Li L.Y., Hawke D.H., Kobayashi R., Hung M.C. Tyrosine phosphorylation controls PCNA function through protein stability. Nat. Cell Biol. 2006, 8:1359-1368.
44. Wang Y.N., Wang H., Yamaguchi H., Lee H.J., Lee H.H., Hung M.C. COPI-mediated retrograde trafficking from the Golgi to the ER regulates EGFR nuclear transport. Biochem. Biophys. Res. Commun. 2010, 399:498-504.
45. Wang Y.N., Yamaguchi H., Hsu J.M., Hung M.C. Nuclear trafficking of the epidermal growth factor receptor family membrane proteins. Oncogene 2010, 29:3997-4006.
46. Wang Y.N., Yamaguchi H., Huo L., Du Y., Lee H.J., Lee H.H., Wang H., Hsu J.M., Hung M.C. The translocon Sec61beta localized in the inner nuclear membrane transports membrane-embedded EGF receptor to the nucleus. J. Biol. Chem. 2010, 285:38720-38729.
47. Wang Y.N., Lee H.H., Lee H.J., Du Y., Yamaguchi H., Hung M.C. Membrane-bound trafficking regulates nuclear transport of integral epidermal growth factor receptor (EGFR) and ErbB-2. J. Biol. Chem. 2012, 287:16869-16879.
48. Wang Y.N., Hsu J.L., Hung M.C. Nuclear functions and trafficking of receptor tyrosine kinases. Vesicle Trafficking in Cancer 2013, 159-176. Springer, New York. Y. Yarden, G. Tarcic (Eds.).
49. Wheeler D.L., Dunn E.F., Harari P.M. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat. Rev. Clin. Oncol. 2010, 7:493-507.
50. Xiao A., Li H., Shechter D., Ahn S.H., Fabrizio L.A., Erdjument-Bromage H., Ishibe-Murakami S., Wang B., Tempst P., Hofmann K., et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 2009, 457:57-62.
51. Yaffe M.B. Phosphotyrosine-binding domains in signal transduction. Nat. Rev. Mol. Cell Biol. 2002, 3:177-186.
52. Yang H., Mizzen C.A. The multiple facets of histone H4-lysine 20 methylation. Biochem. Cell Biol. 2009, 87:151-161.
53. Yang H., Pesavento J.J., Starnes T.W., Cryderman D.E., Wallrath L.L., Kelleher N.L., Mizzen C.A. Preferential dimethylation of histone H4 lysine 20 by Suv4-20. J. Biol. Chem. 2008, 283:12085-12092.
54. Yu Y.L., Chou R.H., Wu C.H., Wang Y.N., Chang W.J., Tseng Y.J., Chang W.C., Lai C.C., Lee H.J., Huo L., et al. Nuclear EGFR suppresses ribonuclease activity of polynucleotide phosphorylase through DNAPK-mediated phosphorylation at serine 776. J. Biol. Chem. 2012, 287:31015-31026.
55. Zhong Q., Chen C.F., Chen P.L., Lee W.H. BRCA1 facilitates microhomology-mediated end joining of DNA double strand breaks. J. Biol. Chem. 2002, 277:28641-28647.