Life and death decisions: Regulation of apoptosis by proteolysis of signaling molecules

Cell Death and Differentiation

Volumn 7, Issue 7, 2000, Pages 589-602

  Utz, P J ^a   Anderson, P ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Apoptosis; Caspase; Kinase; Signaling

Indexed keywords

CALPAIN; CASPASE; KERATIN; LAMIN; PROTEIN KINASE; PROTEINASE; REGULATOR PROTEIN; RNA BINDING PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR;

APOPTOSIS; CELL CYCLE; CELL DAMAGE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME SUBSTRATE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 0033938117     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400696     Document Type: Review

References (150)

1. Andrade F, Roy S, Nicholson D, Thornberry N, Rosen A and Casciola-Rosen LA (1998) Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis. Immunity 8: 451-460
2. Casciola-Rosen LA, Andrade F, Ulanet D, Wong W and Rosen A (1999) Cleavage by granzyme B is strongly predictive of autoantigen status. Implications for initiation of autoimmunity. J. Exp. Med. 190: 815-826
3. Utz PJ, Gensler TJ and Anderson P (2000) Death, autoantigen modifications, and tolerance. Arthritis Res. 2: 101-114
4. Utz PJ and Anderson P (1998) Posttranslational modifications, apoptosis, and bypass of tolerance to autoantigens. Arthritis Rheum. 41: 1152-1160
5. Bokoch G (1998) Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction. Cell Death Differ. 5: 637-645
6. Nicholson D and Thornberry N (1997) Caspases: killer proteases. TIBS 22: 299-306
7. Anderson P (1997) Kinase cascades regulating entry into apoptosis. Microbiol. Mol. Biol. Rev. 61: 33-46
8. Kerr J, Wyllie A and Currie A (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26: 239-257
9. Rudel T and Bokoch G (1997) Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276: 1571-1574
10. Lee N, MacDonald H, Reinhard C, Halenbeck R, Roulston A, Shi T and Williams L (1997) Activation of hPAK65 by caspase cleavage induces some of the morphological and biochemical changes of apoptosis. Proc. Natl. Acad. Sci. USA 94: 13642-13647
11. Schlaepfer D, Hauck C and Sieg D (1999) Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol. 71: 435-478
12. van de Water B, Nagelkerke J and Stevens J (1999) Dephosphorylation of focal adhesion kinase (FAK) and loss of focal contacts precede caspase-mediated cleavage of FAK during apoptosis in renal epithelial cells. J. Biol. Chem. 274: 13328-13337
13. Chan P, Lai J, Cheng C, Tang M, Chiu C and Chen H (1999) Suppression of ultraviolet irradiation-induced apoptosis by overexpression of focal adhesion kinase in Madin-Darby canine kidney cells. J. Biol. Chem. 274: 26901-26906
14. Wen L, Fahrni J, Troie S, Guan J, Orth K and Rosen G (1997) Cleavage of focal adhesion kinase by caspases during apoptosis. J. Biol. Chem. 272: 26056-26061
15. Gervais F, Thornberry N, Ruffolo S, Nicholson D and Roy S (1998) Caspases cleave focal adhesion kinase during apoptosis to generate FRNK-like polypeptide. J. Biol. Chem. 273: 17102-17108
16. Wen L, Madani K, Martin G and Rosen G (1998) Proteolytic cleavage of ras GTPase-activating protein during apoptosis. Cell Death Differ. 5: 729-734
17. Widmann C, Gibson S and Johnson G (1998) Caspase-dependent cleavage of signaling proteins during apoptosis. J. Biol. Chem. 273: 7141-7147
18. Henkemeyer M, Rossi D, Holmyard D, Puri M, Mbamalu G, Harpal K, Shih T, Jacks T and Pawson T (1995) Vascular system defects and neuronal apoptosis in mice lacking ras GTPase-activating protein. Nature 377: 695-701
19. McGlade J, Brunkhorst B, Anderson D, Mbamalu G, Settleman J, Dedhar S, Rozakis-Adcock M, Chen L and Pawson T (1993) The N-terminal region of GAP regulates cytoskeletal structure and cell adhesion. EMBO J. 12: 3073-3081
20. Sabourin L, Seale P, Wagner J and Rudnicki M (2000) Caspase 3 cleavage of the Ste20-related kinase SLK releases and activates an apoptosis-inducing kinase domain and an actin-disassembling region. Mol. Cell. Biol. 20: 684-696
21. Sabourin L and Rudnicki M (1999) Induction of apoptosis by SLK, a Ste20-related kinase. Oncogene 18: 7566-7575
22. Casciola-Rosen LA, Anhalt GJ and Rosen A (1995) DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182: 1625-1634
23. Song Q, Lees-Miller S, Kumar S, Zhang Z, Chan D, Smith G, Jackson S, Alnemri E, Litwack G, Khanna K and Lavin M (1996) DNA-dependent protein kinase catalytic subunit: a target for an ICE-like protease in apoptosis. EMBO J. 15: 3238-3246
24. Le Romancer M, Cosulich S, Jackson S and Clarke P (1996) Cleavage and inactivation of DNA-dependent protein kinase catalytic subunit during apoptosis in Xenopus egg extracts. J. Cell Sci. 109: 3121-3127
25. Molz L, Booher R, Young P and Beach D (1989) cdc2 and the regulation of mitosis: six interacting mcs genes. Genetics 122: 773-782
26. Morgan D (1995) Principles of CDK regulation. Nature 374: 131-134
27. Zhou B, Li H, Yuan J and Kirschner M (1998) Caspase-deper dent activation of cyclin-dependent kinases during Fas-induced apoptosis in Jurkat cells. Proc. Natl. Acad. Sci. USA 95: 6785-6790
28. Yao S, McKenna K, Sharkis S and Bedi A (1996) Requirement of p34cdc2 kinase for apoptosis mediated by the Fas/APO-1 receptor and interleukin 1beta-converting enzyme-related proteases. Cancer Res. 56:4551-4555
29. Chen G, Shi L, Litchfield D and Greenberg A (1995) Rescue from granzyme B-induced apoptosis by Wee1 kinase. J. Exp. Med. 181: 2295-2300
30. Hiromura K, Pippi J, Fero M, Roberts J and Shankland S (1999) Modulation of apoptosis by the cyclin-dependent kinase inhibitor p27(Kip1). J. Clin. Invest. 103: 597-604
31. Eymin B, Haugg M, Drain N, Sordet O, Dimanche-Boìtrel M and Solary E (1999) p27Kip1 induces drug resistance by preventing apoptosis upstream of cytochrome c release and procaspase-3 activation in leukemic cells. Oncogene 18: 1411-1418
32. Dimanche-Boitrel M, Micheau O, Hamman A, Haugg M, Eymin B, Chauffert B and Solary E (1998) Contribution of the cyclin-dependent kinase inhibitor p27KIP1 to the confluence-dependent resistance of HT29 human colon carcinoma cells. Int. J. Cancer 77:796-802
33. Levkau B, Koyama H, Raines E, Clurman B, Herren B, Orth K, Roberts J and Ross R (1998) Cleavage of p21/Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol. Cell 1: 553-563
34. Eymin B, Sordet O, Droin N, Munsch B, Haugg M, van de Craen M, Vandenabeele P and Solary E (1999) Caspase-induced proteolysis of the cyclin-dependent kinase inhibitor p27kip1 mediates its anti-apoptotic activity. Oncogene 18: 4839-4847
35. Sheikh M, Garcia M, Zhan Q, Liu Y and Fornace A (1996) Cell cycle-independent regulation of p21Waf1/Cip1 and retinoblastoma protein during okadaic acid-induced apoptosis is coupled with induction of Bax protein in human breast carcinoma cells. Cell Growth Differ. 7: 1599-1607
36. Wang J and Walsh K (1996) Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273: 359-361
37. Park J, Kim K, Kim S and Lee S (1998) Caspase 3 specifically cleaves p21WAF1/CIP1 in the earlierstage of apoptosis in SK-HEP-1 human hepatoma cells. Eur. J. Biochem. 257: 242-248
38. Zhang Y, Fujita N and Tsuruo T (1999) Caspase-mediated cleavage of p21Waf1/Cip1 converts cancer cells from growth arrest to undergoing apoptosis. Oncogens 18: 1131-1138
39. Lahti J, Xiang J and Kidd V (1995) The PITSLRE protein kinase family. Prog. Cell Cycle Res. 1: 329-338
40. Lahti J, Xiang J, Heath L, Campana D and Kidd V (1995) PITSLRE protein kinase activity is associated with apoptosis. Mol. Cell. Biol. 15: 1-11
41. Beyaert R, Kidd V, Cornelis S, van de Craen M, Denecker G, Lahti J, Gururajan R, Vandenabeele P and Friers W (1997) Cleavage of PITSLRE kinase by ICE/ CASP-1 and CPP32/CASP-3 during apoptosis induced by tumor necrosis factor. J. Biol. Chem. 272: 11694-11697
42. Tang D, Gururajan R and Kidd V (1998) Phosphorylation of PITSLRE p110 isoforms accompanies their processing by cas pases during Fas-mediated cell death. J. Biol. Chem. 273: 16601-16607
43. Barkett M, Xue D, Horvitz H and Gilmore T (1997) Phosphorylation of IkappaB-alpha inhibits its cleavage by caspase CPP32 in vitro. J. Biol. Chem. 272: 29419-29422
44. Bunnell B, Heath L, Adams D, Lahti J and Kidd V (1990) Increased expression of a 58-kDa protein kinase leads to changes in the CHO cell cycle. Proc. Natl. Acad. Sci. USA 87: 7467-7471
45. Wu M, Ao Z, Prasad K, Wu R and Schlossman S (1998) IEX-1L, an apoptosis inhibitor involved in NF-κB-mediated cell survival. Science 281: 998-1001
46. Lin Y, Devin A, Rodriguez Y and Liu Z (1999) Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13: 2514-2526
47. Stanger B, Leder P, Lee T, Kim E and Seed B (1995) RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 81: 513-523
48. Kelliher M, Grimm S, Ishida Y, Kuo F, Stanger B and Leder P (1998) The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 8: 297-303
49. Ting A, Pimental-Muiños F and Seed B (1996) RIP mediates tumor necrosis factor receptor-1 activation of NF-κB but not Fas/Apo-1-initiated apoptosis. EMBO J. 15: 6189-6196
50. Hsu H, Huang J, Shu H, Baichwal V and Goeddel D (1996) TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4: 387-396
51. Thome M, Hofmann K, Burns K, Martinon F, Bodmer J, Mattmann C and Tschopp J (1998) Identification of CARDIAK, a RIP-like kinase that associates with caspase-1. Curr. Biol. 8: 885-888
52. Yu P, Huang B, Shen M, Quast J, Chan E, Xu X, Nolan G, Payan D and Luo Y (1999) Identification of RIP3, a RIP-like kinase that activates apoptosis and NF-κB. Curr. Biol. 9: 539-542
53. Pimentel-Muiños F and Seed B (1999) Regulated commitment of TNF receptor signaling: a molecular switch for death or activation. Immunity 11: 783-793
54. Lee K, Murakawa M, Nishida E, Tsubuki S, Kawashima S, Sakamaki K and Yonehara S (1998) Proteolytic activation of MST/Krs, STE20-related protein kinase, by caspase during apoptosis. Oncogene 16: 3029-3037
55. Graves J, Gotoh Y, Draves K, Ambrose D, Han D, Wright M, Chernoff J, Clark E and Krebs E (1998) Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J. 17: 2224-2234
56. Creasy C, Ambrose D and Chernoff J (1996) The Ste20-like protein kinase, Mst1, dimerizes and contains an inhibitory domain. J. Biol. Chem. 271: 21049-21053
57. Watabe M, Kakeya H and Osada H (1999) Requirement of protein kinase (Krs/ MST) activation for MT-21-induced apoptosis. Oncogene 18:5211-5220
58. Widmann C, Gerwins P, Johnson N, Jarpe M and Johnson G (1998) MEK kinase-1, a substrate for DEVD-directed caspases, is involved in genotoxin-induced apoptosis. Mol. Cell. Biol. 18: 2416-2429
59. Cardone M, Salvesen G, Widmann C, Johnson G and Frische S (1997) The regulation of anoikis: MEKK-1 activation requires cleavage by caspases. Cell 90: 315-323
60. Deak J, Cross J, Lewis M, Qian Y, Parrott L, Distelhorst C and Templeton D (1998) Fas-induced proteolytic activation and intracellular redistribution of the stress-signaling kinase MEKK1. Proc. Natl. Acad. Sci. USA 95: 5585-5600
61. Francois F and Grimes M (1999) Phosphorylation-dependent Akt cleavage in neural cell in vitro reconstitution of apoptosis. J. Neurochem. 73: 1773-1776
62. Cardone M, Roy N, Stennike H, Salvesen G, Franke T, Stanbridge E, Frische S and Reed J (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282: 1318-1321
63. Alberola-lla J, Takaki S, Kerner J and Perlmutter R (1997) Differential signaling by lymphocyte antigen receptors. Ann. Rev. Immunol. 15: 125-154
64. Atkinson E, Ostergaard H, Kane K, Pinkowski M, Caputo A, Olszowy M and Bleakley C (1996) A physical interaction between the cell death protein Fas and the tyrosine kinase p59fynT. J. Biol. Chem. 271: 5968-5971
65. Mari B, Guerin S, Farahi F, Breittmayer J, Belhacene N, Peyron J, Rossi B and Auberger P (1996) Thrombin and trypsin-induced Ca(2+) mobilization in human T cell lines through interaction with different protease-activated receptors. FASEB J. 10: 309-316
66. Campbell K, Cooper S, Dessing M, Yates S and Buder A (1998) Interaction of p59fyn kinase with the dynein light chain, Tctex-1, and colocalization during cytokinesis. J. Immunol. 161: 1728-1737
67. Finke J Zea A, Stanley J, Longo D, Mizoguchi H, Tubbs R, Wiltrout R, O'Shea J, Kudoh S, Klein E, et al. (1993) Loss of T cell receptor ζ chain and p56lck in T-cell infiltrating human renal cell carcinoma. Cancer Res. 53: 5613-5616
68. Gastman B, Johnson D, Whiteside T and Rabinowich H (1999) Caspase-mediated degradation of T-cell receptor ζ chain. Cancer Res. 59: 1422-1427
69. Kersh E, Shaw E and Allen P (1998) Fidelity of T cell activation through multistep T cell receptor ζ chain phosphorylation. Science 281: 572-575
70. Penna D, Müller S, Martinon F, Demotz S, Iwashima M and Valitutti S (1999) Degradation of ZAP-70 following antigenic Stimulation in human T lymphocytes: role of calpain proteolytic activity. J. Immunol. 163: 50-56
71. Sarin A, Nakajima H and Henkart P (1995) A protease-dependent TCR-induced death pathway in mature lymphocytes. J. Immunol. 154: 5806-5812
72. Squier M and Cohen J (1997) Calpain, an upstream regulator of thymocyte apoptosis. J. Immunol. 158: 3690-3697
73. Datta R, Kojima H, Yoshida Kand Kufe D (1997) Caspase-3-mediatedcleavage of protein kinase C theta in induction of apoptosis. J. Biol. Chem. 272: 20317-20320
74. McGinnis K, Whitton M, Gnegy M and Wang K (1998) Calcium/calmodulin-dependent protein kinase IV is cleaved by caspase-3 and calpain in SH-SY5Y human neuroblastoma cells undergoing apoptosis. J. Biol. Chem. 273: 19993-20000
75. Boise L, Gottschallk A, Quintans J and Thompson C (1995) Bcl-2 and Bcl-2-related proteins in apoptosis regulation. Curr. Top. Microbiol. Immunol. 200: 107-121
76. Yang E and Korsmeyer S (1996) Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood 88: 386-401
77. Kyriakis J and Avruch J (1996) Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18: 567-577
78. Boise L, Gonzalez-Garcia M, Postema C, Ding L, Lindsten T, Turka L, Mao X, Nunez G and Thompson C (1993) Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74: 597-608
79. Fang W, Rivard J, Mueller D and Behrens T (1994) Cloning and molecular characterization of mouse bcl-x in B and T lymphocytes. J. Immunol. 153: 4388-4398
80. Shaham S and Horvitz H (1996) An alternatively spliced C. elegans ced-4 RNA encodes a novel cell death inhibitor. Cell 86: 201-208
81. Screaton G, Xu X-N, Olsen A, Cowper A, Tan R, McMichael A and Bell J (1997) LARD: A new lymphoid-specific death domain containing receptor regulated by alternative pre-mRNA splicing. Proc. Natl. Acad. Sci. USA 94: 4615-4619
82. Wang L, Miura M, Bergeron L, Zhu H and Yuan J (1994) lch-1, an ICE/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78: 739-750
83. Jiang Z and Wu J (1999) Alternative splicing and apoptosis. Proc. Soc. Exp. Biol. Med. 220: 64-72
84. Rutjes SA, Utz PJ, Broekhuis C, van der Heijden A, van Venrooij WJ and Pruijn GJM (1999) The La (SS-B) autoantigen, a key protein in RNA biogenesis, is dephosphorylated and cleaved early during apoptosis. Cell Death Differ. 6: 976-986
85. Casciola-Rosen LA, Miller DK, Anhalt GJ and Rosen A (1994) Specific cleavage of the 70 kDa protein component of the U1 small nuclear riboprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem. 269: 30757-30760
86. Utz PJ, Hottelet M, van Venrooij WJ and Anderson P (1998) The 72 kDa component of the signal recognition particle is cleaved during apoptosis. J. Biol. Chem. 273: 35299-35361
87. Utz PJ, Hottelet M, Schur P and Anderson P (1997) Proteins phosphorylated during stress-induced apoptosis are common targets for autoantibody production in patients with systemic lupus erythematosus. J. Exp. Med. 185: 843-854
88. Utz PJ, Hottelet M, van Venrooij WJ and Anderson P (1998) Association of phosphorylated SR proteins and the U1-small nuclear ribonuclear protein autoantigen complex accompanies apoptotic cell death. J. Exp. Med. 187: 547-560
89. Fu XD (1995) The superfamily of arginine/serine-rich splicing factors. RNA. 1: 663-680
90. Colwill K, Pawson T, Andrews B, Prasad J, Manley J, Bell J and Duncan P (1996) The clk/sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15: 265-275
91. Colwill K, Feng L, Yeakley J, Gish G, Caceres J, Pawson T and Fu XD (1996) SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol. Chem. 271: 24569-24575
92. Gui J, Lane W and Fu XD (1994) A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369: 678-682
93. Gui J, Tronchere H, Chandler S and Fu XD (1994) Purification and characterization of a serine kinase specific for the serine-and arginine-rich pre-mRNA splicing factors. Proc. Natl. Acad. Sci. USA 91: 10824-10828
94. Kuroyanagi N, Onogi H, Wakabayashi T and Hagiwara M (1998) Novel SR-protein-specific kinase, SRPK2, disassembles nuclear speckles. Biochem. Biophys. Res. Comm. 242: 357-364
95. Wang H, Lin W, Dyck J, Yeakley J, Songyang Z, Cantley L and Fu XD (1998) SRPK2: A differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J. Cell. Biol. 140: 737-750
96. Rossi F, Labourier E, Forne T, Divita G, Derancourt J, Riou J, Antoine E, Cathala G, Brunei C and Tazi J (1996) Specific phosphorylation of SR proteins by mammalian DNA topoisomerase I. Nature 381: 80-82
97. Casiano CA, Martin SJ, Green DR and Tan EM (1996) Selective cleavage of nuclear autoantigens during CD95 (Fas/Apo-1)-mediated T cell apoptosis. J. Exp. Med. 184: 765-770
98. Samejima K, Svingen P, Basi G, Kottke T, Mesner P, Stewart L, Durrieu F, Poirier G, Alnemri E, Champoux J, Kaufmann S and Earnshaw W (1999) Caspase-mediated cleavage of DNA topoisomerase I at unconventional sites during apoptosis. J. Biol. Chem. 274: 4335-4340
99. Jiang Z, Zhang W, Rao Y and Wu J (1998) Regulation of lch-1 pre-mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl. Acad. Sci. USA 95: 9155-9160
100. Nishizuka Y (1995) Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9: 484-496
101. Tanabe F, Cui S and Ito M (1998) Ceramide promotes calpain-mediated proteolysis of protein kinase C beta in murine polymorphonuclear leukocytes. Biochem. Biophys. Res. Commun. 242: 129-133
102. Santoro M, Annand R, Robertson M, Peng Y, Brady M, Mankovich J, Hackett M, Ghayur T, Walter G, Wong W and Giegel D (1998) Regulation of protein phosphatase 2A activity by caspase-3 during apoptosis. J. Biol. Chem. 273: 13119-13128
103. Tschopp J, Irmler M and Thome M (1998) Inhibition of fas death signals by FLIPs. Curr. Opin. Immunol. 10: 552-558
104. Jackson S, MacDonald J, Lees-Miller S and Tjian R (1990) GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell 63: 155-165
105. Lees-Miller S, Sakaguchi K, Ullrich S, Appella E and Anderson C (1992) Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell Biol. 12: 5041-5049
106. Shieh S, Ikeda M, Taya Y and Prives C (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334
107. Yan M, Dai T, Deak J, Kyriakis J, Zon L, Woodgett J and Templeton D (1994) Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature 371: 798-800
108. Chan W, Yu J and Yang S (1998) Heat-shock stress induces cleavage and activation of PAK2 in apoptotic cells. J. Protein Chem. 17: 485-494
109. Frost J (1997) Cross-cascade activation of ERKs and ternary complex factors by Rho family proteins. EMBO J. 21: 6426-6438
110. Tuazon P, Spanos W, Gump E, Monnig C and Traugh J (1997) Determinants for substrate phosphorylation by p21-activated protein kinase (gamma-PAK). Biochemistry 36: 16059-16064
111. Ramos E, Wysolmerski R and Masaracchia R (1997) Myosin phosphorylation by human cdc42-dependent S6H4/kinase/yPAK from placenta and lymphoid cells. Receptors and Signal Trans. 7: 99-110
112. Enslen H, Tokumitsu H and Soderling T (1995) Phosphorylation of CREB by CaM-kinase IV activated by CaM-kinase IV kinase. Biochem. Biophys. Res. Commun. 207: 1038-1043
113. Sun P, Lou Land Maurer R (1996) Regulation of activating transcription factor-1 and the cAMP response element-binding protein by Ca2+/calmodulin-dependent protein kinases type I, II, and IV. J. Biol. Chem. 271: 3066-3073
114. Miranti C, Ginty D, Huang G, Chatila T and Greenberg M (1995) Calcium activates serum response factor-dependent transcription by a Ras-and Elk-1-independent mechanism that involves a Ca2+/calmodulin-dependent kinase. Mol. Cell. Biol. 15: 3672-3684
115. Ho N, Gullberg M and Chatila T (1996) Activation protein 1-dependent transcriptional activation of interleukin 2 gene by Ca2+/calmodulin kinase type IV/Gr. J. Exp. Med. 184: 101-112
116. Alevizopoulos A, Dusserre Y, Ruegg U and Mermod N (1997) Regulation of the transforming growth factor beta-responsive transcription factor CTF-1 by calcineurin and calcium/calmodulin-dependent protein kinase IV. J. Biol. Chem. 272: 23597-23605
117. Alevizopoulos A and Mermod N (1997) Transforming growth factor-beta: the breaking open of a black box. Bioessays 19: 581-591
118. Sahyoun N, McDonald O, Farrell F and Lapetina E (1991) Phosphorylation of a Ras-related GTP-binding protein, Rap-1b, by a neuronal Ca2+/calmodulin-dependent protein kinase, CaM kinase Gr. Proc. Natl. Acad. Sci. USA 88: 2643-2647
119. Madhavan R and Jarrett H (1999) Phosphorylation of dystrophin and alpha-syntrophin by Ca(2+)-calmodulin dependent protein kinase II. Biochim. Biophys. Acta. 1434: 260-274
120. Feinmesser R, Wicks S, Taverner C and Chantry A (1999) Ca2+/calmodulin-dependent kinase Il phosphorylates the epidermal growth factor receptor on rrultiple sites in the cytoplasmic tail and serine 744 within the kinase domain to regulate signal generation. J. Biol. Chem. 274: 16168-16173
121. Banin S, Gout I and Brickell P (1999) Interaction between Wiskott-Aldrich Syndrome protein (WASP) and the Fyn protein-tyrosine kinase. Mol. Biol. Rep. 26: 173-177
122. Kanda H, Mimura T, Hamasaki K, Yamamoto K, Yazaki Y, Hirai H and Nojima Y (1999) Fyn and Lck tyrosine kinases regulate tyrosine phosphorylation of p105CasL, a member of the p130Cas docking protein family, in T-cell receptor-mediated signalling. Immunology 97: 56-61
123. Hunter S, Burton E, Wu S and Anderson S (1999) Fyn assoc ates with Cbl and phosphorylates tyrosine 731 in Cbl, a binding site for phosphatidylinositol 3-kinase. J. Biol. Chem. 274: 2097-2106
124. Ron D, Napolitano E, Voronova A, Vasquez N, Roberts D, Calio B, Caothien R, Pettiford S, Wellik S, Mandac J and Kauvar L (1999) Direct interaction in T-cells between theta PKC and the tyrosine kinase p59fyn. J. Biol. Chem. 274: 19003-19010
125. Yeakley J, Tronchere H, Diesen J, Dyck J, Wang H and Fu XD (1999) Phosphorylation regulates in vivo interaction and molecular targeting of serine/ arginine-rich pre-mRNA splicing factors. J. Cell. Biol. 145: 447-455
126. Mou T, Kraas J, Fung E and Swope S (1998) Identification of a dynein molecular motor component in Torpedo electroplax; binding and phosphorylation of Tctex-1 by Fyn. FEBS Letters 435: 275-281
127. Ricci J, Maulon L, Luciano F, Guerin S, Livolsi A, Mari B, Breittmayer J, Peyron J and Auberger P (1999) Cleavage and relocation of the tyrosine kinase P59FYN during Fas-mediated apoptosis in T lymphocytes. Oncogene 18: 3963-3969
128. Deckert M, Tartare-Deckert S, Couture C, Mustelin T and Altman A (1996) Functional and physical interactions of Syk family kinases with the Vav protooncogene product. Immunity 5: 591-604
129. Wardenburg J, Fu C, Jackman J, Flotow H, Wilkinson S, Williams D, Johnson R, Kong G, Chan A and Findell P (1996) Phosphorylation of SLP 76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271: 19641-19644
130. Zhang W, Sloan-LancasterJ, Kitchen J, Trible R and Samelson L (1998) LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92: 83-92
131. Schlapfer D, Hauck C and Sieg D (1999) Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol. 71: 435-478
132. Burridge K and Chrznowsky-Wodnicka M (1996) Focal adhesions, contractility, and signaling. Ann. Rev. Cell. Biol. 12: 463-519
133. Macdonald S, Crews C, Wu L, Driller J, Clark R, Erikson R and McCormick F (1993) Reconstitution of the Raf-1-MEK-ERK signal transduction pathway in vitro. Mol. Cell. Biol. 13: 6615-6620
134. Huang W, Alessandrini A, Crews C and Erikson R (1993) Raf-1 forms a stable complex with Mek1 and activates Mek1 by serine phosphorylation. Proc. Natl. Acad. Sci. USA 90: 10947-10951
135. Datta S, Dudek H, Tao X, Masters S, Fu H, Gotoh Y and Greenberg M (1997)Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241
136. Dekker L and Parker P (1997) Regulated binding of the protein kinase C substrate GAP-43 to the V0/C2 region of protein kinase C-delta. J. Biol. Chem. 272: 12747-12753
137. Ghayur T, Hugunin M, Talanian R, Ratnofsky S, Quinlan C, Emoto Y. Pandey P, Datta R, Huang Y, Kharbanda S, Allen H, Kamen R, Wong W and Kufe D (1996) Proteolytic activation of protein kinase C delta by an ICE/CED2-like protease induces characteristics of apoptosis. J. Exp. Med. 184: 2399-2404
138. Municio M, Lozano J, Sanchez P, Moscat J and Diaz-Meco M (1995) Identification of heterogenous ribonucleoprotein A1 as a novel substrate for protein kinase Czeta. J. Biol. Chem. 270: 15884-15891
139. Frutos S, Moscat J and Diaz-Meco M (1999) Cleavage of zetaPKC but not lambda/iotaPKC by caspase-3 during UV-induced apoptosis. J. Biol. Chem. 274: 10765-10770
140. Häussermann S, Kittstein W, Rincke G, Johannes F-J, Marks FandGschwendt M (1999) Proteolytic cleavage of protein kinase Cμ upon induction of apoptosis in U937 cells. FEBS Letters 462: 442-446
141. Cryns V, Byun Y, Rana A, Mellor H, Lustig K, Ghanem L, Parker P, Kirschner M and Yuan J (1997) Specific proteolysis of the kinase protein kinase C-related kinase 2 by caspase-3 during apoptosis. Identification by a novel, small pool expression cloning strategy. J. Biol. Chem. 272: 29449-29453
142. Mukai H, Toshimori M. Shibata H, Kitagawa M, Shimakawa M, Miyahara M, Sunakawa H and Ono Y (1996) PKN associates and phosphorylates the headrod domain of neurofilament protein. J. Biol. Chem. 271: 9816-9822
143. Mukai H, Toshimori M, Shibata H, Takanag H, Kitagawa M, Miyahara M, Shimakawa M and Ono Y (1997) Interaction of PKN with alpha-actinin. J. Biol. Chem. 272: 4740-4746
144. Matsuzawa K, Kosako H, Inagaki N, Shibata H, Mukai H, Ono Y, Amano M, Kaibuchi K, Matsuura Y, Azuma I and Inagaki M (1997) Domain-specific phosphorylation of vimentin and glial fibrillary acidic protein by PKN. Biochem. Biophys. Res. Commun. 234: 621-625
145. Takahashi M, Mukai H, Toshimori M, Miyamoto M and Ono Y (1998) Proteolytic activation of PKN by caspase-3 or related protease during apoptosis. Proc. Natl. Acad. Sci. USA 95: 11566-11571
146. McGowan C and Russell P (1993) Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. EMBO J. 12: 75-85
147. Lupher M, Rao N, Eck M and Band H (1999) The Cbl protooncoprotein: a negative regulator of immune receptor signal transduction. Immunol Today 20: 375-382
148. Meisner H, Conway B, Hartley D and Czech M (1995) Interactions of Cbl with Grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol. Cell. Biol. 15: 3571-3578
149. Elly C, Witte S, Zhang Z, Rosnet O, Lipkowitz S, Altman A and Liu Y (1999) Tyrosine phosphorylation and complex formation of Cbl-b upon T cell receptor stimulation. Oncogene 18: 1147-1156
150. Zhang Z, Elly C, Qiu L, Altman A and Liu Y (1999) A direct interaction between the adaptor protein Cbl-b and the kinase ZAP-70 induces a positive signal in T cells. Curr. Biol. 9: 203-206