Phosphoproteomics study on the activated PKCδ-induced cell death

Journal of Proteome Research

Volumn 12, Issue 10, 2013, Pages 4280-4301

  Xia, Li ^a   Wang, Tong Dan ^a   Shen, Shao Ming ^a   Zhao, Meng ^a   Sun, Han ^c   He, Ying ^c   Xie, Lu ^c   Wu, Zhao Xia ^a   Han, San Feng ^a   Wang, Li Shun ^a   Chen, Guo Qiang ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI UNIVERSITY OF MEDICINE AND HEALTH SCIENCES   (China)

^c SHANGHAI CENTER FOR BIOINFORMATION TECHNOLOGY   (China)

Author keywords

cell death; kinase substrates; phosphoproteomics; Protein kinase C (PKC )

Indexed keywords

PHOSPHOPEPTIDE; PROTEIN KINASE C DELTA;

ARTICLE; CELL DEATH; CELL ENGINEERING; DYNAMICS; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; UPREGULATION;

AMINO ACID SEQUENCE; APOPTOSIS; CELL LINE, TUMOR; CONSENSUS SEQUENCE; CULLIN PROTEINS; GENE ONTOLOGY; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN INTERACTION MAPS; PROTEIN KINASE C-DELTA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84885212552     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400089v     Document Type: Article

References (111)

1. Nishizuka, Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation Nature 1988, 334 (6184) 661-5
2. Emoto, Y.; Manome, Y.; Meinhardt, G.; Kisaki, H.; Kharbanda, S.; Robertson, M.; Ghayur, T.; Wong, W. W.; Kamen, R.; Weichselbaum, R. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells EMBO J. 1995, 14 (24) 6148-56
3. Brodie, C.; Blumberg, P. M. Regulation of cell apoptosis by protein kinase c delta Apoptosis 2003, 8 (1) 19-27
4. Kanthasamy, A. G.; Kitazawa, M.; Kanthasamy, A.; Anantharam, V. Role of proteolytic activation of protein kinase Cdelta in oxidative stress-induced apoptosis Antioxid Redox Signal 2003, 5 (5) 609-20
5. Kikkawa, U.; Matsuzaki, H.; Yamamoto, T. Protein kinase C delta (PKC delta): activation mechanisms and functions J. Biochem. 2002, 132 (6) 831-9
6. Song, M. G.; Gao, S. M.; Du, K. M.; Xu, M.; Yu, Y.; Zhou, Y. H.; Wang, Q.; Chen, Z.; Zhu, Y. S.; Chen, G. Q. Nanomolar concentration of NSC606985, a camptothecin analog, induces leukemic-cell apoptosis through protein kinase Cdelta-dependent mechanisms Blood 2005, 105 (9) 3714-21
7. Emoto, Y.; Kisaki, H.; Manome, Y.; Kharbanda, S.; Kufe, D. Activation of protein kinase Cdelta in human myeloid leukemia cells treated with 1-beta-D-arabinofuranosylcytosine Blood 1996, 87 (5) 1990-6
8. DeVries, T. A.; Neville, M. C.; Reyland, M. E. Nuclear import of PKCdelta is required for apoptosis: identification of a novel nuclear import sequence EMBO J. 2002, 21 (22) 6050-60
9. Zhao, M.; Duan, X. F.; Zhao, X. Y.; Zhang, B.; Lu, Y.; Liu, W.; Cheng, J. K.; Chen, G. Q. Protein kinase Cdelta stimulates proteasome-dependent degradation of C/EBPalpha during apoptosis induction of leukemic cells PLoS One 2009, 4 (8) e6552
10. D'Costa, A. M.; Denning, M. F. A caspase-resistant mutant of PKC-delta protects keratinocytes from UV-induced apoptosis Cell Death Differ. 2005, 12 (3) 224-32
11. Sun, F.; Kanthasamy, A.; Song, C.; Yang, Y.; Anantharam, V.; Kanthasamy, A. G. Proteasome inhibitor-induced apoptosis is mediated by positive feedback amplification of PKCdelta proteolytic activation and mitochondrial translocation J. Cell. Mol. Med. 2008, 12 (6A) 2467-81
12. Murriel, C. L.; Churchill, E.; Inagaki, K.; Szweda, L. I.; Mochly-Rosen, D. Protein kinase Cdelta activation induces apoptosis in response to cardiac ischemia and reperfusion damage: a mechanism involving BAD and the mitochondria J. Biol. Chem. 2004, 279 (46) 47985-91
13. Lomonaco, S. L.; Kahana, S.; Blass, M.; Brody, Y.; Okhrimenko, H.; Xiang, C.; Finniss, S.; Blumberg, P. M.; Lee, H. K.; Brodie, C. Phosphorylation of protein kinase Cdelta on distinct tyrosine residues induces sustained activation of Erk1/2 via down-regulation of MKP-1: role in the apoptotic effect of etoposide J. Biol. Chem. 2008, 283 (25) 17731-9
14. Basu, A.; Tu, H. Activation of ERK during DNA damage-induced apoptosis involves protein kinase Cdelta Biochem. Biophys. Res. Commun. 2005, 334 (4) 1068-73
15. Yoshida, K.; Miki, Y.; Kufe, D. Activation of SAPK/JNK signaling by protein kinase Cdelta in response to DNA damage J. Biol. Chem. 2002, 277 (50) 48372-8
16. Efimova, T.; Broome, A. M.; Eckert, R. L. Protein kinase Cdelta regulates keratinocyte death and survival by regulating activity and subcellular localization of a p38delta-extracellular signal-regulated kinase 1/2 complex Mol. Cell. Biol. 2004, 24 (18) 8167-83
17. Lee, Y. J.; Soh, J. W.; Dean, N. M.; Cho, C. K.; Kim, T. H.; Lee, S. J.; Lee, Y. S. Protein kinase Cdelta overexpression enhances radiation sensitivity via extracellular regulated protein kinase 1/2 activation, abolishing the radiation-induced G(2)-M arrest Cell Growth Differ 2002, 13 (5) 237-46
18. Hu, Y.; Kang, C.; Philp, R. J.; Li, B. PKC delta phosphorylates p52ShcA at Ser29 to regulate ERK activation in response to H2O2 Cell Signal 2007, 19 (2) 410-8
19. Yoshida, K.; Liu, H.; Miki, Y. Protein kinase C delta regulates Ser46 phosphorylation of p53 tumor suppressor in the apoptotic response to DNA damage J. Biol. Chem. 2006, 281 (9) 5734-40
20. Lee, S. J.; Kim, D. C.; Choi, B. H.; Ha, H.; Kim, K. T. Regulation of p53 by activated protein kinase C-delta during nitric oxide-induced dopaminergic cell death J. Biol. Chem. 2006, 281 (4) 2215-24
21. Ren, J.; Datta, R.; Shioya, H.; Li, Y.; Oki, E.; Biedermann, V.; Bharti, A.; Kufe, D. p73beta is regulated by protein kinase Cdelta catalytic fragment generated in the apoptotic response to DNA damage J. Biol. Chem. 2002, 277 (37) 33758-65
22. Park, C. H.; Choi, B. H.; Jeong, M. W.; Kim, S.; Kim, W.; Song, Y. S.; Kim, K. T. Protein kinase Cdelta regulates vaccinia-related kinase 1 in DNA damage-induced apoptosis Mol. Biol. Cell 2011, 22 (8) 1398-408
23. Majumder, P. K.; Pandey, P.; Sun, X.; Cheng, K.; Datta, R.; Saxena, S.; Kharbanda, S.; Kufe, D. Mitochondrial translocation of protein kinase C delta in phorbol ester-induced cytochrome c release and apoptosis J. Biol. Chem. 2000, 275 (29) 21793-6
24. Li, L.; Lorenzo, P. S.; Bogi, K.; Blumberg, P. M.; Yuspa, S. H. Protein kinase Cdelta targets mitochondria, alters mitochondrial membrane potential, and induces apoptosis in normal and neoplastic keratinocytes when overexpressed by an adenoviral vector Mol. Cell. Biol. 1999, 19 (12) 8547-58
25. von Burstin, V. A.; Xiao, L.; Kazanietz, M. G. Bryostatin 1 inhibits phorbol ester-induced apoptosis in prostate cancer cells by differentially modulating protein kinase C (PKC) delta translocation and preventing PKCdelta-mediated release of tumor necrosis factor-alpha Mol. Pharmacol. 2010, 78 (3) 325-32
26. Kajimoto, T.; Shirai, Y.; Sakai, N.; Yamamoto, T.; Matsuzaki, H.; Kikkawa, U.; Saito, N. Ceramide-induced apoptosis by translocation, phosphorylation, and activation of protein kinase Cdelta in the Golgi complex J. Biol. Chem. 2004, 279 (13) 12668-76
27. Kajimoto, T.; Ohmori, S.; Shirai, Y.; Sakai, N.; Saito, N. Subtype-specific translocation of the delta subtype of protein kinase C and its activation by tyrosine phosphorylation induced by ceramide in HeLa cells Mol. Cell. Biol. 2001, 21 (5) 1769-83
28. Zrachia, A.; Dobroslav, M.; Blass, M.; Kazimirsky, G.; Kronfeld, I.; Blumberg, P. M.; Kobiler, D.; Lustig, S.; Brodie, C. Infection of glioma cells with Sindbis virus induces selective activation and tyrosine phosphorylation of protein kinase C delta. Implications for Sindbis virus-induced apoptosis J. Biol. Chem. 2002, 277 (26) 23693-701
29. Parent, N.; Scherer, M.; Liebisch, G.; Schmitz, G.; Bertrand, R. Protein kinase C-delta isoform mediates lysosome labilization in DNA damage-induced apoptosis Int. J. Oncol. 2011, 38 (2) 313-24
30. Gomel, R.; Xiang, C.; Finniss, S.; Lee, H. K.; Lu, W.; Okhrimenko, H.; Brodie, C. The localization of protein kinase Cdelta in different subcellular sites affects its proapoptotic and antiapoptotic functions and the activation of distinct downstream signaling pathways Mol. Cancer Res. 2007, 5 (6) 627-39
31. Liu, J.; Chen, J.; Dai, Q.; Lee, R. M. Phospholipid scramblase 3 is the mitochondrial target of protein kinase C delta-induced apoptosis Cancer Res. 2003, 63 (6) 1153-6
32. Liu, J.; Dai, Q.; Chen, J.; Durrant, D.; Freeman, A.; Liu, T.; Grossman, D.; Lee, R. M. Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response Mol. Cancer Res. 2003, 1 (12) 892-902
33. Sitailo, L. A.; Tibudan, S. S.; Denning, M. F. The protein kinase C delta catalytic fragment targets Mcl-1 for degradation to trigger apoptosis J. Biol. Chem. 2006, 281 (40) 29703-10
34. Sitailo, L. A.; Tibudan, S. S.; Denning, M. F. Bax activation and induction of apoptosis in human keratinocytes by the protein kinase C delta catalytic domain J. Invest. Dermatol. 2004, 123 (3) 434-43
35. Frank, S.; Gaume, B.; Bergmann-Leitner, E. S.; Leitner, W. W.; Robert, E. G.; Catez, F.; Smith, C. L.; Youle, R. J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis Dev. Cell 2001, 1 (4) 515-25
36. Qi, X.; Disatnik, M. H.; Shen, N.; Sobel, R. A.; Mochly-Rosen, D. Aberrant mitochondrial fission in neurons induced by protein kinase C{delta} under oxidative stress conditions in vivo Mol. Biol. Cell 2011, 22 (2) 256-65
37. Bharti, A.; Kraeft, S. K.; Gounder, M.; Pandey, P.; Jin, S.; Yuan, Z. M.; Lees-Miller, S. P.; Weichselbaum, R.; Weaver, D.; Chen, L. B.; Kufe, D.; Kharbanda, S. Inactivation of DNA-dependent protein kinase by protein kinase Cdelta: implications for apoptosis Mol. Cell. Biol. 1998, 18 (11) 6719-28
38. Cross, T.; Griffiths, G.; Deacon, E.; Sallis, R.; Gough, M.; Watters, D.; Lord, J. M. PKC-delta is an apoptotic lamin kinase Oncogene 2000, 19 (19) 2331-7
39. Yoshida, K.; Wang, H. G.; Miki, Y.; Kufe, D. Protein kinase Cdelta is responsible for constitutive and DNA damage-induced phosphorylation of Rad9 EMBO J. 2003, 22 (6) 1431-41
40. Yoshida, K.; Yamaguchi, T.; Shinagawa, H.; Taira, N.; Nakayama, K. I.; Miki, Y. Protein kinase C delta activates topoisomerase IIalpha to induce apoptotic cell death in response to DNA damage Mol. Cell. Biol. 2006, 26 (9) 3414-31
41. Gao, F. H.; Wu, Y. L.; Zhao, M.; Liu, C. X.; Wang, L. S.; Chen, G. Q. Protein kinase C-delta mediates down-regulation of heterogeneous nuclear ribonucleoprotein K protein: involvement in apoptosis induction Exp. Cell Res. 2009, 315 (19) 3250-8
42. Mayr, M.; Chung, Y. L.; Mayr, U.; McGregor, E.; Troy, H.; Baier, G.; Leitges, M.; Dunn, M. J.; Griffiths, J. R.; Xu, Q. Loss of PKC-delta alters cardiac metabolism Am. J. Physiol. Heart Circ. Physiol. 2004, 287 (2) H937-45
43. Mayr, M.; Metzler, B.; Chung, Y. L.; McGregor, E.; Mayr, U.; Troy, H.; Hu, Y.; Leitges, M.; Pachinger, O.; Griffiths, J. R.; Dunn, M. J.; Xu, Q. Ischemic preconditioning exaggerates cardiac damage in PKC-delta null mice Am. J. Physiol. Heart Circ. Physiol. 2004, 287 (2) H946-56
44. Boer, J.; Bonten-Surtel, J.; Grosveld, G. Overexpression of the nucleoporin CAN/NUP214 induces growth arrest, nucleocytoplasmic transport defects, and apoptosis Mol. Cell. Biol. 1998, 18 (3) 1236-47
45. Beausoleil, S. A.; Jedrychowski, M.; Schwartz, D.; Elias, J. E.; Villen, J.; Li, J.; Cohn, M. A.; Cantley, L. C.; Gygi, S. P. Large-scale characterization of HeLa cell nuclear phosphoproteins Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (33) 12130-5
46. Yates, J. R., 3rd; Eng, J. K.; McCormack, A. L.; Schieltz, D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database Anal. Chem. 1995, 67 (8) 1426-36
47. Beausoleil, S. A.; Villen, J.; Gerber, S. A.; Rush, J.; Gygi, S. P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization Nat. Biotechnol. 2006, 24 (10) 1285-92
48. Park, S. K.; Venable, J. D.; Xu, T.; Yates, J. R., 3rd. A quantitative analysis software tool for mass spectrometry-based proteomics Nat. Methods 2008, 5 (4) 319-22
49. Huang da, W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2009, 4 (1) 44-57
50. Szklarczyk, D.; Franceschini, A.; Kuhn, M.; Simonovic, M.; Roth, A.; Minguez, P.; Doerks, T.; Stark, M.; Muller, J.; Bork, P.; Jensen, L. J.; von Mering, C. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Nucleic Acids Res. 2011, 39 (Database issue) D561-8
51. Smoot, M. E.; Ono, K.; Ruscheinski, J.; Wang, P. L.; Ideker, T. Cytoscape 2.8: new features for data integration and network visualization Bioinformatics 2011, 27 (3) 431-2
52. Scardoni, G.; Petterlini, M.; Laudanna, C. Analyzing biological network parameters with CentiScaPe Bioinformatics 2009, 25 (21) 2857-9
53. Schwartz, D.; Gygi, S. P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets Nat. Biotechnol. 2005, 23 (11) 1391-8
54. Xue, Y.; Ren, J.; Gao, X.; Jin, C.; Wen, L.; Yao, X. GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy Mol. Cell. Proteomics 2008, 7 (9) 1598-608
55. Wang, L. H.; Li, D. Q.; Fu, Y.; Wang, H. P.; Zhang, J. F.; Yuan, Z. F.; Sun, R. X.; Zeng, R.; He, S. M.; Gao, W. pFind 2.0: a software package for peptide and protein identification via tandem mass spectrometry Rapid Commun. Mass Spectrom. 2007, 21 (18) 2985-91
56. Matsuoka, S.; Ballif, B. A.; Smogorzewska, A.; McDonald, E. R., 3rd; Hurov, K. E.; Luo, J.; Bakalarski, C. E.; Zhao, Z.; Solimini, N.; Lerenthal, Y.; Shiloh, Y.; Gygi, S. P.; Elledge, S. J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 2007, 316 (5828) 1160-6
57. Bensimon, A.; Schmidt, A.; Ziv, Y.; Elkon, R.; Wang, S. Y.; Chen, D. J.; Aebersold, R.; Shiloh, Y. ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage Sci. Signal. 2010, 3 (151) rs3
58. Bennetzen, M. V.; Larsen, D. H.; Bunkenborg, J.; Bartek, J.; Lukas, J.; Andersen, J. S. Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response Mol. Cell. Proteomics 2010, 9 (6) 1314-23
59. de Graauw, M.; Hensbergen, P.; Van de Water, B. Phospho-proteomic analysis of cellular signaling Electrophoresis 2006, 27 (13) 2676-86
60. Dix, M. M.; Simon, G. M.; Cravatt, B. F. Global mapping of the topography and magnitude of proteolytic events in apoptosis Cell 2008, 134 (4) 679-91
61. Kondo, S.; Perrimon, N. A genome-wide RNAi screen identifies core components of the G(2)-M DNA damage checkpoint Sci. Signal. 2011, 4 (154) rs1
62. Ernst, J.; Bar-Joseph, Z. STEM: a tool for the analysis of short time series gene expression data BMC Bioinf. 2006, 7, 191
63. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13 (11) 2498-504
64. Linding, R.; Jensen, L. J.; Ostheimer, G. J.; van Vugt, M. A.; Jorgensen, C.; Miron, I. M.; Diella, F.; Colwill, K.; Taylor, L.; Elder, K.; Metalnikov, P.; Nguyen, V.; Pasculescu, A.; Jin, J.; Park, J. G.; Samson, L. D.; Woodgett, J. R.; Russell, R. B.; Bork, P.; Yaffe, M. B.; Pawson, T. Systematic discovery of in vivo phosphorylation networks Cell 2007, 129 (7) 1415-26
65. Miller, M. L.; Jensen, L. J.; Diella, F.; Jorgensen, C.; Tinti, M.; Li, L.; Hsiung, M.; Parker, S. A.; Bordeaux, J.; Sicheritz-Ponten, T.; Olhovsky, M.; Pasculescu, A.; Alexander, J.; Knapp, S.; Blom, N.; Bork, P.; Li, S.; Cesareni, G.; Pawson, T.; Turk, B. E.; Yaffe, M. B.; Brunak, S.; Linding, R. Linear motif atlas for phosphorylation-dependent signaling Sci. Signal. 2008, 1 (35) ra2
66. Blom, N.; Sicheritz-Ponten, T.; Gupta, R.; Gammeltoft, S.; Brunak, S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence Proteomics 2004, 4 (6) 1633-49
67. Amanchy, R.; Periaswamy, B.; Mathivanan, S.; Reddy, R.; Tattikota, S. G.; Pandey, A. A curated compendium of phosphorylation motifs Nat. Biotechnol. 2007, 25 (3) 285-6
68. Fujii, K.; Zhu, G.; Liu, Y.; Hallam, J.; Chen, L.; Herrero, J.; Shaw, S. Kinase peptide specificity: improved determination and relevance to protein phosphorylation Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (38) 13744-9
69. Yasuda, I.; Kishimoto, A.; Tanaka, S.; Tominaga, M.; Sakurai, A.; Nishizuka, Y. A synthetic peptide substrate for selective assay of protein kinase C Biochem. Biophys. Res. Commun. 1990, 166 (3) 1220-7
70. Kemp, B. E.; Pearson, R. B. Design and use of peptide substrates for protein kinases Methods Enzymol. 1991, 200, 121-34
71. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 2006, 127 (3) 635-48
72. Yu, Y.; Yoon, S. O.; Poulogiannis, G.; Yang, Q.; Ma, X. M.; Villen, J.; Kubica, N.; Hoffman, G. R.; Cantley, L. C.; Gygi, S. P.; Blenis, J. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling Science 2011, 332 (6035) 1322-6
73. Hsu, P. P.; Kang, S. A.; Rameseder, J.; Zhang, Y.; Ottina, K. A.; Lim, D.; Peterson, T. R.; Choi, Y.; Gray, N. S.; Yaffe, M. B.; Marto, J. A.; Sabatini, D. M. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling Science 2011, 332 (6035) 1317-22
74. Olsen, J. V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M. L.; Jensen, L. J.; Gnad, F.; Cox, J.; Jensen, T. S.; Nigg, E. A.; Brunak, S.; Mann, M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis Sci. Signal. 2010, 3 (104) ra3
75. Nishizuka, Y. The role of protein kinase C in cell surface signal transduction and tumour promotion Nature 1984, 308 (5961) 693-8
76. Nishizuka, Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C Science 1992, 258 (5082) 607-14
77. Yoshida, K. PKCdelta signaling: mechanisms of DNA damage response and apoptosis Cell. Signal. 2007, 19 (5) 892-901
78. Smith, G. C.; Jackson, S. P. The DNA-dependent protein kinase Genes Dev. 1999, 13 (8) 916-34
79. Kharbanda, S.; Pandey, P.; Jin, S.; Inoue, S.; Bharti, A.; Yuan, Z. M.; Weichselbaum, R.; Weaver, D.; Kufe, D. Functional interaction between DNA-PK and c-Abl in response to DNA damage Nature 1997, 386 (6626) 732-5
80. Liu, H.; Lu, Z. G.; Miki, Y.; Yoshida, K. Protein kinase C delta induces transcription of the TP53 tumor suppressor gene by controlling death-promoting factor Btf in the apoptotic response to DNA damage Mol. Cell. Biol. 2007, 27 (24) 8480-91
81. Blois, J. T.; Mataraza, J. M.; Mecklenbrauker, I.; Tarakhovsky, A.; Chiles, T. C. B cell receptor-induced cAMP-response element-binding protein activation in B lymphocytes requires novel protein kinase Cdelta J. Biol. Chem. 2004, 279 (29) 30123-32
82. Kurita, S.; Higuchi, H.; Saito, Y.; Nakamoto, N.; Takaishi, H.; Tada, S.; Saito, H.; Gores, G. J.; Hibi, T. DNMT1 and DNMT3b silencing sensitizes human hepatoma cells to TRAIL-mediated apoptosis via up-regulation of TRAIL-R2/DR5 and caspase-8 Cancer Sci. 2010, 101 (6) 1431-9
83. Lavoie, G.; Esteve, P. O.; Laulan, N. B.; Pradhan, S.; St-Pierre, Y. PKC isoforms interact with and phosphorylate DNMT1 BMC Biol. 2011, 9 (1) 31
84. Goodrich, D. W.; Wang, N. P.; Qian, Y. W.; Lee, E. Y.; Lee, W. H. The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle Cell 1991, 67 (2) 293-302
85. Robertson, K. D.; Ait-Si-Ali, S.; Yokochi, T.; Wade, P. A.; Jones, P. L.; Wolffe, A. P. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters Nat. Genet. 2000, 25 (3) 338-42
86. McCabe, M. T.; Davis, J. N.; Day, M. L. Regulation of DNA methyltransferase 1 by the pRb/E2F1 pathway Cancer Res. 2005, 65 (9) 3624-32
87. Andrews, P. D.; Knatko, E.; Moore, W. J.; Swedlow, J. R. Mitotic mechanics: the auroras come into view Curr. Opin. Cell. Biol. 2003, 15 (6) 672-83
88. den Hollander, J.; Rimpi, S.; Doherty, J. R.; Rudelius, M.; Buck, A.; Hoellein, A.; Kremer, M.; Graf, N.; Scheerer, M.; Hall, M. A.; Goga, A.; von Bubnoff, N.; Duyster, J.; Peschel, C.; Cleveland, J. L.; Nilsson, J. A.; Keller, U. Aurora kinases A and B are up-regulated by Myc and are essential for maintenance of the malignant state Blood 2010, 116 (9) 1498-505
89. Addepalli, M. K.; Ray, K. B.; Kumar, B.; Ramnath, R. L.; Chile, S.; Rao, H. RNAi-mediated knockdown of AURKB and EGFR shows enhanced therapeutic efficacy in prostate tumor regression Gene Ther. 2010, 17 (3) 352-9
90. Mourtada-Maarabouni, M.; Williams, G. T. RBM5/LUCA-15 - tumour suppression by control of apoptosis and the cell cycle? Sci. World J. 2002, 2, 1885-90
91. Shu, Y.; Rintala-Maki, N. D.; Wall, V. E.; Wang, K.; Goard, C. A.; Langdon, C. E.; Sutherland, L. C. The apoptosis modulator and tumour suppressor protein RBM5 is a phosphoprotein Cell. Biochem. Funct. 2007, 25 (6) 643-53
92. Reyland, M. E.; Barzen, K. A.; Anderson, S. M.; Quissell, D. O.; Matassa, A. A. Activation of PKC is sufficient to induce an apoptotic program in salivary gland acinar cells Cell Death Differ. 2000, 7 (12) 1200-9
93. Weishaupt, J. H.; Neusch, C.; Bahr, M. Cyclin-dependent kinase 5 (CDK5) and neuronal cell death Cell Tissue Res. 2003, 312 (1) 1-8
94. Sahin, B.; Hawasli, A. H.; Greene, R. W.; Molkentin, J. D.; Bibb, J. A. Negative regulation of cyclin-dependent kinase 5 targets by protein kinase C Eur. J. Pharmacol. 2008, 581 (3) 270-5
95. Zhao, C. T.; Li, K.; Li, J. T.; Zheng, W.; Liang, X. J.; Geng, A. Q.; Li, N.; Yuan, X. B. PKCdelta regulates cortical radial migration by stabilizing the Cdk5 activator p35 Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (50) 21353-8
96. Zhang, L.; Yun, H.; Murray, F.; Lu, R.; Wang, L.; Hook, V.; Insel, P. A. Cytotoxic T lymphocyte antigen-2 alpha induces apoptosis of murine T-lymphoma cells and cardiac fibroblasts and is regulated by cAMP/PKA Cell. Signal. 2011, 23 (10) 1611-6
97. Zambon, A. C.; Wilderman, A.; Ho, A.; Insel, P. A. Increased Expression of the Pro-apoptotic Protein BIM, a Mechanism for cAMP/Protein Kinase A (PKA)-induced Apoptosis of Immature T Cells J. Biol. Chem. 2011, 286 (38) 33260-7
98. Ojeda, F.; Folch, H.; Guarda, M. I.; Jastorff, B.; Diehl, H. A. Induction of apoptosis in thymocytes: new evidence for an interaction of PKC and PKA pathways Biol. Chem. Hoppe-Seyler 1995, 376 (6) 389-93
99. Ahmad, K. A.; Wang, G.; Unger, G.; Slaton, J.; Ahmed, K. Protein kinase CK2 - a key suppressor of apoptosis Adv. Enzyme Regul. 2008, 48, 179-87
100. Di Maira, G.; Brustolon, F.; Tosoni, K.; Belli, S.; Kramer, S. D.; Pinna, L. A.; Ruzzene, M. Comparative analysis of CK2 expression and function in tumor cell lines displaying sensitivity vs. resistance to chemical induced apoptosis Mol. Cell. Biochem. 2008, 316 (1-2) 155-61
101. Wang, G.; Unger, G.; Ahmad, K. A.; Slaton, J. W.; Ahmed, K. Downregulation of CK2 induces apoptosis in cancer cells - a potential approach to cancer therapy Mol. Cell. Biochem. 2005, 274 (1-2) 77-84
102. Pospisilova, S.; Brazda, V.; Kucharikova, K.; Luciani, M. G.; Hupp, T. R.; Skladal, P.; Palecek, E.; Vojtesek, B. Activation of the DNA-binding ability of latent p53 protein by protein kinase C is abolished by protein kinase CK2 Biochem. J. 2004, 378 (Pt 3) 939-47
103. Sugasawa, K. The CUL4 enigma: culling DNA repair factors Mol. Cell 2009, 34 (4) 403-4
104. Kielbassa, K.; Muller, H. J.; Meyer, H. E.; Marks, F.; Gschwendt, M. Protein kinase C delta-specific phosphorylation of the elongation factor eEF-alpha and an eEF-1 alpha peptide at threonine 431 J. Biol. Chem. 1995, 270 (11) 6156-62
105. DeVries, T. A.; Kalkofen, R. L.; Matassa, A. A.; Reyland, M. E. Protein kinase Cdelta regulates apoptosis via activation of STAT1 J. Biol. Chem. 2004, 279 (44) 45603-12
106. Obenauer, J. C.; Cantley, L. C.; Yaffe, M. B. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs Nucleic Acids Res. 2003, 31 (13) 3635-41
107. Gao, J.; Thelen, J. J.; Dunker, A. K.; Xu, D. Musite, a tool for global prediction of general and kinase-specific phosphorylation sites Mol. Cell. Proteomics 2010, 9 (12) 2586-600
108. Statsuk, A. V.; Maly, D. J.; Seeliger, M. A.; Fabian, M. A.; Biggs, W. H., 3rd; Lockhart, D. J.; Zarrinkar, P. P.; Kuriyan, J.; Shokat, K. M. Tuning a three-component reaction for trapping kinase substrate complexes J. Am. Chem. Soc. 2008, 130 (51) 17568-74
109. Berwick, D. C.; Tavare, J. M. Identifying protein kinase substrates: hunting for the organ-grinder's monkeys Trends Biochem. Sci. 2004, 29 (5) 227-32
110. Liu, L.; Lee, S.; Zhang, J.; Peters, S. B.; Hannah, J.; Zhang, Y.; Yin, Y.; Koff, A.; Ma, L.; Zhou, P. CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis Mol. Cell 2009, 34 (4) 451-60
111. Jia, L.; Sun, Y. SCF E3 ubiquitin ligases as anticancer targets Curr. Cancer Drug Targets 2011, 11 (3) 347-56