Proteomic and biochemical analysis of 14-3-3-binding proteins during C2-ceramide-induced apoptosis

FEBS Journal

Volumn 277, Issue 16, 2010, Pages 3321-3342

  Pozuelo Rubio, Mercedes ^a  

^a CSIC   (Spain)

Author keywords

14 3 3; apoptosis; C2 ceramide; Hela cells; proteomics

Indexed keywords

BINDING PROTEIN; CALMODULIN; CERAMIDE; DNA DEPENDENT PROTEIN KINASE; NUCLEOPHOSMIN; PROTEIN 14 3 3; PROTEIN 14 3 3 BINDING PROTEIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

AFFINITY CHROMATOGRAPHY; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

14-3-3 PROTEINS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 8; CELL LINE, TUMOR; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MITOCHONDRIA; PROTEIN BINDING; PROTEOMICS; REPRODUCIBILITY OF RESULTS; RNA, SMALL INTERFERING; SPHINGOSINE;

EID: 77955250361     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07730.x     Document Type: Article

References (104)

1. Chaudhri M, Scarabel M Aitken A (2003) Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem Biophys Res Commun 300, 679 685.
2. Jones DH, Ley S Aitken A (1995) Isoforms of 14-3-3 protein can form homo- and heterodimers in vivo and in vitro: implications for function as adapter proteins. FEBS Lett 368, 55 58.
3. Aitken A, Howell S, Jones D, Madrazo J Patel Y (1995) 14-3-3 alpha and delta are the phosphorylated forms of raf-activating 14-3-3 beta and zeta. In vivo stoichiometric phosphorylation in brain at a Ser-Pro-Glu-Lys MOTIF. J Biol Chem 270, 5706 5709.
4. Moreira JM, Shen T, Ohlsson G, Gromov P, Gromova I Celis JE (2008) A combined proteome and ultrastructural localization analysis of 14-3-3 proteins in transformed human amnion (AMA) cells: definition of a framework to study isoform-specific differences. Mol Cell Proteomics 7, 1225 1240.
5. Mackintosh C (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381, 329 342.
6. Muslin AJ, Tanner JW, Allen PM Shaw AS (1996) Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84, 889 897.
7. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ Cantley LC (1997) The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961 971.
8. Aitken A (2002) Functional specificity in 14-3-3 isoform interactions through dimer formation and phosphorylation. Chromosome location of mammalian isoforms and variants. Plant Mol Biol 50, 993 1010.
9. Henriksson ML, Francis MS, Peden A, Aili M, Stefansson K, Palmer R, Aitken A Hallberg B (2002) A nonphosphorylated 14-3-3 binding motif on exoenzyme S that is functional in vivo. Eur J Biochem 269, 4921 4929.
10. Yaffe MB (2002) How do 14-3-3 proteins work? - Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett 513, 53 57.
11. Wilker E Yaffe MB (2004) 14-3-3 Proteins - a focus on cancer and human disease. J Mol Cell Cardiol 37, 633 642.
12. Pozuelo Rubio M, Geraghty KM, Wong BH, Wood NT, Campbell DG, Morrice N Mackintosh C (2004) 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem J 379, 395 408.
13. Meek SE, Lane WS Piwnica-Worms H (2004) Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J Biol Chem 279, 32046 32054.
14. Jin J, Smith FD, Stark C, Wells CD, Fawcett JP, Kulkarni S, Metalnikov P, O'Donnell P, Taylor P, Taylor L et al. (2004) Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr Biol 14, 1436 1450.
15. Benzinger A, Muster N, Koch HB, Yates JR III. Hermeking H (2005) Targeted proteomic analysis of 14-3-3 sigma, a p53 effector commonly silenced in cancer. Mol Cell Proteomics 4, 785 795.
16. Angrand PO, Segura I, Volkel P, Ghidelli S, Terry R, Brajenovic M, Vintersten K, Klein R, Superti-Furga G, Drewes G et al. (2006) Transgenic mouse proteomics identifies new 14-3-3-associated proteins involved in cytoskeletal rearrangements and cell signaling. Mol Cell Proteomics 5, 2211 2227.
17. Ballif BA, Cao Z, Schwartz D, Carraway KL III. Gygi SP (2006) Identification of 14-3-3epsilon substrates from embryonic murine brain. J Proteome Res 5, 2372 2379.
18. Satoh J, Nanri Y Yamamura T (2006) Rapid identification of 14-3-3-binding proteins by protein microarray analysis. J Neurosci Methods 152, 278 288.
19. Puri P, Myers K, Kline D Vijayaraghavan S (2008) Proteomic analysis of bovine sperm YWHA binding partners identify proteins involved in signaling and metabolism. Biol Reprod 79, 1183 1191.
20. Liang S, Yu Y, Yang P, Gu S, Xue Y Chen X (2009) Analysis of the protein complex associated with 14-3-3 epsilon by a deuterated-leucine labeling quantitative proteomics strategy. J Chromatogr B Analyt Technol Biomed Life Sci 877, 627 634.
21. Masters SC, Subramanian RR, Truong A, Yang H, Fujii K, Zhang H Fu H (2002) Survival-promoting functions of 14-3-3 proteins. Biochem Soc Trans 30, 360 365.
22. Williams GT (1991) Programmed cell death: apoptosis and oncogenesis. Cell 65, 1097 1098.
23. Zha J, Harada H, Yang E, Jockel J Korsmeyer SJ (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87, 619 628.
24. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T, Matsuda H Tsujimoto Y (2003) 14-3-3 Interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem 278, 2058 2065.
25. Zhang L, Chen J Fu H (1999) Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc Natl Acad Sci USA 96, 8511 8515.
26. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857 868.
27. Woodcock JM, Murphy J, Stomski FC, Berndt MC Lopez AF (2003) The dimeric versus monomeric status of 14-3-3zeta is controlled by phosphorylation of Ser58 at the dimer interface. J Biol Chem 278, 36323 36327.
28. Obeid LM, Linardic CM, Karolak LA Hannun YA (1993) Programmed cell death induced by ceramide. Science 259, 1769 1771.
29. Suzuki E, Handa K, Toledo MS Hakomori S (2004) Sphingosine-dependent apoptosis: a unified concept based on multiple mechanisms operating in concert. Proc Natl Acad Sci USA 101, 14788 14793.
30. Fillet M, Cren-Olive C, Renert AF, Piette J, Vandermoere F, Rolando C Merville MP (2005) Differential expression of proteins in response to ceramide-mediated stress signal in colon cancer cells by 2-D gel electrophoresis and MALDI-TOF-MS. J Proteome Res 4, 870 880.
31. Pandey S, Murphy RF Agrawal DK (2007) Recent advances in the immunobiology of ceramide. Exp Mol Pathol 82, 298 309.
32. Ogretmen B Hannun YA (2004) Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 4, 604 616.
33. Jaffrezou JP Laurent G (2004) Ceramide: a new target in anticancer research? Bull Cancer 91, E133 E161.
34. Kok JW Sietsma H (2004) Sphingolipid metabolism enzymes as targets for anticancer therapy. Curr Drug Targets 5, 375 382.
35. Sawai H, Domae N Okazaki T (2005) Current status and perspectives in ceramide-targeting molecular medicine. Curr Pharm Des 11, 2479 2487.
36. Dimanche-Boitrel MT, Meurette O, Rebillard A Lacour S (2005) Role of early plasma membrane events in chemotherapy-induced cell death. Drug Resist Updat 8, 5 14.
37. Masters SC Fu H (2001) 14-3-3 proteins mediate an essential anti-apoptotic signal. J Biol Chem 276, 45193 45200.
38. Cao W, Yang X, Zhou J, Teng Z, Cao L, Zhang X Fei Z (2010) Targeting 14-3-3 protein, difopein induces apoptosis of human glioma cells and suppresses tumor growth in mice. Apoptosis 15, 230 241.
39. Kumar AP, Garcia GE, Orsborn J, Levin VA Slaga TJ (2003) 2-Methoxyestradiol interferes with NF kappa B transcriptional activity in primitive neuroectodermal brain tumors: implications for management. Carcinogenesis 24, 209 216.
40. Qi W Martinez JD (2003) Reduction of 14-3-3 proteins correlates with increased sensitivity to killing of human lung cancer cells by ionizing radiation. Radiat Res 160, 217 223.
41. Niemantsverdriet M, Wagner K, Visser M Backendorf C (2008) Cellular functions of 14-3-3 zeta in apoptosis and cell adhesion emphasize its oncogenic character. Oncogene 27, 1315 1319.
42. Neal CL, Yao J, Yang W, Zhou X, Nguyen NT, Lu J, Danes CG, Guo H, Lan KH, Ensor J et al. (2009) 14-3-3zeta overexpression defines high risk for breast cancer recurrence and promotes cancer cell survival. Cancer Res 69, 3425 3432.
43. Shoji M, Kawamoto S, Setoguchi Y, Mochizuki K, Honjoh T, Kato M, Hashizume S, Hanagiri T, Yoshimatsu T, Nakanishi K et al. (1994) The 14-3-3 protein as the antigen for lung cancer-associated human monoclonal antibody AE6F4. Hum Antibodies Hybridomas 5, 123 130.
44. Qi W, Liu X, Qiao D Martinez JD (2005) Isoform-specific expression of 14-3-3 proteins in human lung cancer tissues. Int J Cancer 113, 359 363.
45. Jang JS, Cho HY, Lee YJ, Ha WS Kim HW (2004) The differential proteome profile of stomach cancer: identification of the biomarker candidates. Oncol Res 14, 491 499.
46. Zang L, Palmer Toy D, Hancock WS, Sgroi DC Karger BL (2004) Proteomic analysis of ductal carcinoma of the breast using laser capture microdissection, LC-MS, and 16O/18O isotopic labeling. J Proteome Res 3, 604 612.
47. Somiari RI, Somiari S, Russell S Shriver CD (2005) Proteomics of breast carcinoma. J Chromatogr B Analyt Technol Biomed Life Sci 815, 215 225.
48. Silveira LR, Fiamoncini J, Hirabara SM, Procopio J, Cambiaghi TD, Pinheiro CH, Lopes LR Curi R (2008) Updating the effects of fatty acids on skeletal muscle. J Cell Physiol 217, 1 12.
49. Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, Birrer MJ, Szabo E, Zon LI, Kyriakis JM et al. (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380, 75 79.
50. Byun Y, Chen F, Chang R, Trivedi M, Green KJ Cryns VL (2001) Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ 8, 443 450.
51. Chen F, Chang R, Trivedi M, Capetanaki Y Cryns VL (2003) Caspase proteolysis of desmin produces a dominant-negative inhibitor of intermediate filaments and promotes apoptosis. J Biol Chem 278, 6848 6853.
52. Yang X, Wang J, Liu C, Grizzle WE, Yu S, Zhang S, Barnes S, Koopman WJ, Mountz JD, Kimberly RP et al. (2005) Cleavage of p53-vimentin complex enhances tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis of rheumatoid arthritis synovial fibroblasts. Am J Pathol 167, 705 719.
53. Schietke R, Brohl D, Wedig T, Mucke N, Herrmann H Magin TM (2006) Mutations in vimentin disrupt the cytoskeleton in fibroblasts and delay execution of apoptosis. Eur J Cell Biol 85, 1 10.
54. Lee SB, Xuan Nguyen TL, Choi JW, Lee KH, Cho SW, Liu Z, Ye K, Bae SS Ahn JY (2008) Nuclear Akt interacts with B23/NPM and protects it from proteolytic cleavage, enhancing cell survival. Proc Natl Acad Sci USA 105, 16584 16589.
55. Nutt LK, Buchakjian MR, Gan E, Darbandi R, Yoon SY, Wu JQ, Miyamoto YJ, Gibbon JA, Andersen JL, Freel CD et al. (2009) Metabolic control of oocyte apoptosis mediated by 14-3-3zeta-regulated dephosphorylation of caspase-2. Dev Cell 16, 856 866.
56. Zhou J, Shao Z, Kerkela R, Ichijo H, Muslin AJ, Pombo C Force T (2009) Serine 58 of 14-3-3zeta is a molecular switch regulating ASK1 and oxidant stress-induced cell death. Mol Cell Biol 29, 4167 4176.
57. Susin SA, Zamzami N Kroemer G (1998) Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta 1366, 151 165.
58. Basu S, Bayoumy S, Zhang Y, Lozano J Kolesnick R (1998) BAD enables ceramide to signal apoptosis via Ras and Raf-1. J Biol Chem 273, 30419 30426.
59. Zundel W Giaccia A (1998) Inhibition of the anti-apoptotic PI(3)K/Akt/Bad pathway by stress. Genes Dev 12, 1941 1946.
60. Zhou H, Summers SA, Birnbaum MJ Pittman RN (1998) Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J Biol Chem 273, 16568 16575.
61. Cuvillier O, Edsall L Spiegel S (2000) Involvement of sphingosine in mitochondria-dependent Fas-induced apoptosis of type II Jurkat T cells. J Biol Chem 275, 15691 15700.
62. Martin SJ, Takayama S, McGahon AJ, Miyashita T, Corbeil J, Kolesnick NR, Reed JC Green DR (1995) Inhibition of ceramide-induced apoptosis by Bcl-2. Cell Death Differ 2, 253 257.
63. Zhang J, Alter N, Reed JC, Borner C, Obeid LM Hannun YA (1996) Bcl-2 interrupts the ceramide-mediated pathway of cell death. Proc Natl Acad Sci USA 93, 5325 5328.
64. Sprick MR, Weigand MA, Rieser E, Rauch CT, Juo P, Blenis J, Krammer PH Walczak H (2000) FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity 12, 599 609.
65. Darios F, Lambeng N, Troadec JD, Michel PP Ruberg M (2003) Ceramide increases mitochondrial free calcium levels via caspase 8 and Bid: role in initiation of cell death. J Neurochem 84, 643 654.
66. Wang J, Zhen L, Klug MG, Wood D, Wu X Mizrahi J (2000) Involvement of caspase 3- and 8-like proteases in ceramide-induced apoptosis of cardiomyocytes. J Card Fail 6, 243 249.
67. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M Seraphin B (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17, 1030 1032.
68. Al-Hakim AK, Goransson O, Deak M, Toth R, Campbell DG, Morrice NA, Prescott AR Alessi DR (2005) 14-3-3 cooperates with LKB1 to regulate the activity and localization of QSK and SIK. J Cell Sci 118, 5661 5673.
69. van Hemert MJ, Niemantsverdriet M, Schmidt T, Backendorf C Spaink HP (2004) Isoform-specific differences in rapid nucleocytoplasmic shuttling cause distinct subcellular distributions of 14-3-3 sigma and 14-3-3 zeta. J Cell Sci 117, 1411 1420.
70. Obenauer JC, Cantley LC Yaffe MB (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31, 3635 3641.
71. Tzivion G, Luo ZJ Avruch J (2000) Calyculin A-induced vimentin phosphorylation sequesters 14-3-3 and displaces other 14-3-3 partners in vivo. J Biol Chem 275, 29772 29778.
72. Liu MY, Cai S, Espejo A, Bedford MT Walker CL (2002) 14-3-3 interacts with the tumor suppressor tuberin at Akt phosphorylation site(s). Cancer Res 62, 6475 6480.
73. Li Z, Shi Z, Park HR, Li Z Fu H (2009) Identification of the 14-3-3/HIP-55 protein complex as a negative regulator of HPK1 in the Akt signaling. FASEB J 23, 581 583.
74. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB Korsmeyer SJ (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727 730.
75. Gingras AC, Aebersold R Raught B (2005) Advances in protein complex analysis using mass spectrometry. J Physiol 563, 11 21.
76. Li J, Zhang X, Sejas DP Pang Q (2005) Negative regulation of p53 by nucleophosmin antagonizes stress-induced apoptosis in human normal and malignant hematopoietic cells. Leuk Res 29, 1415 1423.
77. Pozuelo Rubio M, Peggie M, Wong BH, Morrice N MacKintosh C (2003) 14-3-3s regulate fructose-2,6-bisphosphate levels by binding to PKB-phosphorylated cardiac fructose-2,6-bisphosphate kinase/phosphatase. EMBO J 22, 3514 3523.
78. Cotelle V, Meek SE, Provan F, Milne FC, Morrice N MacKintosh C (2000) 14-3-3s regulate global cleavage of their diverse binding partners in sugar-starved Arabidopsis cells. EMBO J 19, 2869 2876.
79. Benz PM, Feller SM, Sickmann A, Walter U Renne T (2008) Prostaglandin-induced VASP phosphorylation controls alpha II-spectrin breakdown in apoptotic cells. Int Immunopharmacol 8, 319 324.
80. Mukherjee B, Kessinger C, Kobayashi J, Chen BP, Chen DJ, Chatterjee A Burma S (2006) DNA-PK phosphorylates histone H2AX during apoptotic DNA fragmentation in mammalian cells. DNA Repair (Amst) 5, 575 590.
81. Collis SJ, DeWeese TL, Jeggo PA Parker AR (2005) The life and death of DNA-PK. Oncogene 24, 949 961.
82. Chakravarthy BR, Walker T, Rasquinha I, Hill IE MacManus JP (1999) Activation of DNA-dependent protein kinase may play a role in apoptosis of human neuroblastoma cells. J Neurochem 72, 933 942.
83. Munoz-Pinedo C, Ruiz-Ruiz C, Ruiz de Almodovar C, Palacios C Lopez-Rivas A (2003) Inhibition of glucose metabolism sensitizes tumor cells to death receptor-triggered apoptosis through enhancement of death-inducing signaling complex formation and apical procaspase-8 processing. J Biol Chem 278, 12759 12768.
84. Galluzzi L, Zamzami N, de La Motte Rouge T, Lemaire C, Brenner C Kroemer G (2007) Methods for the assessment of mitochondrial membrane permeabilization in apoptosis. Apoptosis 12, 803 813. (Pubitemid 46653289)
85. Moorhead G, Douglas P, Cotelle V, Harthill J, Morrice N, Meek S, Deiting U, Stitt M, Scarabel M, Aitken A et al. (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J 18, 1 12.
86. Sarker M, Ruiz-Ruiz C Lopez-Rivas A (2001) Activation of protein kinase C inhibits TRAIL-induced caspase activation, mitochondrial events and apoptosis in a human leukemic T cell line. Cell Death Differ 8, 172 181.
87. Perkins DN, Pappin DJ, Creasy DM Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551 3567.
88. Wakeyama H, Akiyama T, Takahashi K, Amano H, Kadono Y, Nakamura M, Oshima Y, Itabe H, Nakayama KI, Nakayama K et al. (2007) Negative feedback loop in the Bim-caspase-3 axis regulating apoptosis and activity of osteoclasts. J Bone Miner Res 22, 1631 1639.
89. Huang M, Kozlowski P, Collins M, Wang Y, Haystead TA Graves LM (2002) Caspase-dependent cleavage of carbamoyl phosphate synthetase II during apoptosis. Mol Pharmacol 61, 569 577.
90. Mills JC, Stone NL, Erhardt J Pittman RN (1998) Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol 140, 627 636.
91. Du MR, Zhou WH, Yan FT, Zhu XY, He YY, Yang JY Li DJ (2007) Cyclosporine A induces titin expression via MAPK/ERK signalling and improves proliferative and invasive potential of human trophoblast cells. Hum Reprod 22, 2528 2537.
92. Takadera T Ohyashiki T (2007) Calmodulin inhibitor-induced apoptosis was prevented by glycogen synthase kinase-3 inhibitors in PC12 cells. Cell Mol Neurobiol 27, 783 790.
93. Han M, Liew CT, Zhang HW, Chao S, Zheng R, Yip KT, Song ZY, Li HM, Geng XP, Zhu LX et al. (2008) Novel blood-based, five-gene biomarker set for the detection of colorectal cancer. Clin Cancer Res 14, 455 460.
94. Lee TH, Huang Q, Oikemus S, Shank J, Ventura JJ, Cusson N, Vaillancourt RR, Su B, Davis RJ Kelliher MA (2003) The death domain kinase RIP1 is essential for tumor necrosis factor alpha signaling to p38 mitogen-activated protein kinase. Mol Cell Biol 23, 8377 8385.
95. Holcik M, Gordon BW Korneluk RG (2003) The internal ribosome entry site-mediated translation of antiapoptotic protein XIAP is modulated by the heterogeneous nuclear ribonucleoproteins C1 and C2. Mol Cell Biol 23, 280 288.
96. Konishi A, Shimizu S, Hirota J, Takao T, Fan Y, Matsuoka Y, Zhang L, Yoneda Y, Fujii Y, Skoultchi AI Tsujimoto Y (2003) Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114, 673 688.
97. Okamura H, Yoshida K, Amorim BR Haneji T (2008) Histone H1.2 is translocated to mitochondria and associates with Bak in bleomycin-induced apoptotic cells. J Cell Biochem 103, 1488 1496.
98. Ruiz-Vela A Korsmeyer SJ (2007) Proapoptotic histone H1.2 induces CASP-3 and -7 activation by forming a protein complex with CYT c, APAF-1 and CASP-9. FEBS Lett 581, 3422 3428.
99. Freilinger A, Rosner M, Krupitza G, Nishino M, Lubec G, Korsmeyer SJ Hengstschlager M (2006) Tuberin activates the proapoptotic molecule BAD. Oncogene 25, 6467 6479.
100. Freilinger A, Rosner M Hengstschlager M (2006) Tuberin negatively affects BCL-2's cell survival function. Amino Acids 30, 391 396.
101. Kolb TM, Duan L Davis MA (2005) Tsc2 expression increases the susceptibility of renal tumor cells to apoptosis. Toxicol Sci 88, 331 339.
102. Yu PW, Huang BC, Shen M, Quast J, Chan E, Xu X, Nolan GP, Payan DG Luo Y (1999) Identification of RIP3, a RIP-like kinase that activates apoptosis and NFκB. Curr Biol 9, 539 542.
103. Sun X, Lee J, Navas T, Baldwin DT, Stewart TA Dixit VM (1999) RIP3, a novel apoptosis-inducing kinase. J Biol Chem 274, 16871 16875.
104. Kasof GM, Prosser JC, Liu D, Lorenzi MV Gomes BC (2000) The RIP-like kinase, RIP3, induces apoptosis and NF-κB nuclear translocation and localizes to mitochondria. FEBS Lett 473, 285 291.