Calphostin C-induced apoptosis is mediated by a tissue transglutaminase-dependent mechanism involving the DLK/JNK signaling pathway

Cell Death and Differentiation

Volumn 15, Issue 9, 2008, Pages 1522-1531

  Robitaille, K ^a   Daviau, A ^a   Lachance, G ^a   Couture, J P ^a   Blouin, R ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CALPHOSTIN C; CASPASE 3; DUAL LEUCINE ZIPPER BEARING KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHOTRANSFERASE; PROTEIN BAX; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL STRAIN 3T3; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; FIBROBLAST; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HYPOTHESIS; MOUSE; NONHUMAN; OLIGOMERIZATION; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; GTP-BINDING PROTEINS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICE; NAPHTHALENES; NIH 3T3 CELLS; POLY(ADP-RIBOSE) POLYMERASES; RNA INTERFERENCE; TRANSGLUTAMINASES;

EID: 49949098410     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2008.77     Document Type: Article

References (41)

1. Kobayashi E, Nakano H, Morimoto M, Tamaoki T. Calphostin C (UNC-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 1989; 159: 548-553.
2. Ikemoto H, Tani E, Matsumoto T, Nakano A, Furuyama J. Apoptosis of human glioma cells in response to calphostin C, a specific protein kinase C inhibitor. J Neurosurg 1995; 83: 1008-1016.
3. Zhu DM, Narla RK, Fang WH, Chia NC, Uckun FM. Calphostin C triggers calcium-dependent apoptosis in human acute lymphoblastic leukemia cells. Clin Cancer Res 1998; 4: 2967-2976.
4. Ozaki I, Tani E, Ikemoto H, Kitagawa H, Fujikawa H. Activation of stress-activated protein kinase/c-Jun NH2-terminal kinase and p38 kinase in calphostin C-induced apoptosis requires caspase-3-like proteases but is dispensable for cell death. J Biol Chem 1999; 274: 5310-5317.
5. Ikemoto H, Tani E, Ozaki I, Kitagawa H, Arita N. Calphostin C-mediated translocation and integration of Bax into mitochondria induces cytochrome c release before mitochondrial dysfunction. Cell Death Differ 2000; 7: 511-520.
6. Zheng XL, Gui Y, Du G, Frohman MA, Peng DQ. Calphostin-C induction of vascular smooth muscle cell apoptosis proceeds through phospholipase D and microtubule inhibition. J Biol Chem 2004; 279: 7112-7118.
7. Oliverio S, Amendola A, Di Sano F, Farrace MG, Fesus L, Nemes Z et al Tissue transglutaminase-dependent posttranslational modification of the retinoblastoma gene product in promonocytic cells undergoing apoptosis. Mol Cell Biol 1997; 17: 6040-6048.
8. Hébert SS, Daviau A, Grondin G, Latreille M, Aubin RA, Blouin R. The mixed lineage kinase DLK is oligomerized by tissue transglutaminase during apoptosis. J Biol Chem 2000; 275: 32482-32490.
9. Robitaille K, Daviau A, Tucholski J, Johnson GV, Rancourt C, Blouin R. Tissue transglutaminase triggers oligomerization and activation of dual leucine zipper-bearing kinase in calphostin C-treated cells to facilitate apoptosis. Cell Death Differ 2004; 11: 542-549.
10. Lorand L, Graham RM. Transglutaminases: Crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 2003; 4: 140-156.
11. Esposito C, Caputo I. Mammalian transglutaminases. Identification of substrates as a key to physiological function and physiopathological relevance. FEBS J 2005; 272: 615-631.
12. Fésüs L, Szondy Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 2005; 579: 3297-3302.
13. Tucholski J, Johnson GVW. Tissue transglutaminase differentially modulates apoptosis in a stimuli-dependent manner. J Neurochem 2002; 81: 780-791.
14. Antonyak MA, Singh US, Lee DA, Boehm JE, Combs C, Zgola MM et al. Effects of tissue transglutaminase on retinoic acid-induced cellular differentiation and protection against apoptosis. J Biol Chem 2001; 276: 33582-33587.
15. Antonyak MA, Boehm JE, Cerione RA. Phosphoinositide 3-kinase activity is required for retinoic acid-induced expression and activation of the tissue transglutaminase. J Biol Chem 2002; 277: 14712-14716.
16. Nemes Jr Z, Adány R, Balázs M, Boross P, Fésüs L. Identification of cytoplasmic actin as an abundant glutaminyl substrate for tissue transglutaminase in HL-60 and U937 cells undergoing apoptosis. J Biol Chem 1997; 272: 20577-20583.
17. Ballestar E, Abad C, Franco L. Core histones are glutaminyl substrates for tissue transglutaminase. J Biol Chem 1996; 271: 18817-18824.
18. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000; 103: 239-252.
19. Harper SJ, LoGrasso P. Signalling for survival and death in neurones - The role of stress-activated kinases, JNK and P38. Cell Signalling 2001; 13: 299-310.
20. Yang DD, Kuan CY, Whitmarsh AJ, Rincon M, Zheng TS, Davis RJ et al Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 1997; 389: 865-870.
21. Troy CM, Rabacchi SA, Xu Z, Maroney AC, Connors TJ, Shelanski ML et al. beta-Amyloid-induced neuronal apoptosis requires c-Jun N-terminal kinase activation. J Neurochem 2001; 77: 157-164.
22. Maroney AC, Finn JP, Bozyczko-Coyne D, O'Kane TM, Neff NT, Tolkovsky AM et al. CEP-1347 (KT7515), an inhibitor of JNK activation, rescues sympathetic neurons and neuronally differentiated PC12 cells from death evoked by three distinct insults. J Neurochem 1999; 73: 1901-1912.
23. Mayne GC, Murray AW. Evidence that protein kinase C epsilon mediates phorbol ester inhibition of calphostin C- and tumor necrosis factor-alpha-induced apoptosis in U937 histiocytic lymphoma cells. J Biol Chem 1998; 273: 24115-24121.
24. Pollack IF, Kawecki S. The effect of calphostin C, a potent photodependent protein kinase C inhibitor, on the proliferation of glioma cells in vitro. J Neurooncol 1997; 31: 255-266.
25. Porter AG, Jänicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 1999; 6: 99-104.
26. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994; 371: 346-347.
27. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W et al SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 2001; 98: 13681-13686.
28. Kim BJ, Ryu SW, Song BJ. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 2006; 281 21256-21265.
29. Mehta K, Fok J, Miller FR, Koul D, Sahin AA. Prognostic significance of tissue transglutaminase in drug resistant and metastatic breast cancer. Clin Cancer Res 2004; 10: 8068-8076.
30. Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Genet Dev 2002; 12: 14-21.
31. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000; 288: 870-874.
32. Shin DM, Jeon JH, Kim CW, Cho SY, Kwon JC, Lee HJ et al. Cell type-specific activation of intracellular transglutaminase 2 by oxidative stress or ultraviolet irradiation: Implications of transglutaminase 2 in age-related cataractogenesis. J Biol Chem 2004; 279: 15032-15039.
33. Fan G, Merritt SE, Kortenjann M, Shaw PE, Holzman LB. Dual leucine zipper-bearing kinase (DLK) activates p46SAPK and p38mapk but not ERK2. J Biol Chem 1996; 271: 24788-24793.
34. Gallo KA, Johnson GL. Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat Rev Mol Cell Biol 2002; 3: 663-672.
35. Johnson GV, Cox TM, Lockhart JP, Zinnerman MD, Miller ML, Powers RE. Transglutaminase activity is increased in Alzheimer's disease brain. Brain Res 1997; 751: 323-329.
36. Rasmussen LK, Sorensen ES, Petersen TE, Gliemann J, Jensen PH. Identification of glutamine and lysine residues in Alzheimer amyloid β A4 peptide responsible for transglutaminase-catalysed homopolymerization and cross-linking to alpha 2M receptor. FEBS Lett 1994; 338: 161-166.
37. Tucholski J, Kuret J, Johnson GV. Tau is modified by tissue transglutaminase in situ: Possible functional and metabolic effects of polyamination. J Neurochem 1999; 73: 1871-1880.
38. Chen JSK, Konopleva M, Andreeff M, Multani AS, Pathak S, Mehta K. Drug-resistant breast carcinoma (MCF-7) cells are paradoxically sensitive to apoptosis. J Cell Physiol 2004; 200: 223-234.
39. Fok JY, Mehta K. Tissue transglutaminase induces the release of apoptosis inducing factor and results in apoptotic death of pancreatic cells. Apoptosis 2007; 12: 1455-1463.
40. Douziech M, Laberge G, Grondin G, Daigle N, Blouin R. Localization of the mixed-lineage kinase DLK/MUK/ZPK to the Golgi apparatus in NIH 3T3 cells. J Histochem Cytochem 1999; 47: 1287-1296.
41. Zhang J, Lesort M, Guttmann RP, Johnson GVW. Modulation of the in situ activity of tissue transglutaminase by calcium and GTP. J Biol Chem 1998; 273: 2288-2295.