Hexokinase II detachment from the mitochondria potentiates cisplatin induced cytotoxicity through a caspase-2 dependent mechanism

Cell Cycle

Volumn 8, Issue 20, 2009, Pages 3355-3364

  Shulga, Nataly ^a   Wilson Smith, Robin ^b   Pastorino, John G ^a  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b Department of Anesthesiology   (United States)

Author keywords

Caspase 2; Cisplatin; Hexokinase II; Mitochondria

Indexed keywords

CASPASE 2; CASPASE 3; CASPASE 9; CISPLATIN; CYTOCHROME C; HEXOKINASE; HEXOKINASE ISOENZYME; PROTEIN BAK; PROTEIN BID; PROTEIN P53; UNCLASSIFIED DRUG;

ARTICLE; CELL DAMAGE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME LOCALIZATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRION; OLIGOMERIZATION;

EID: 70350220872     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.20.9853     Document Type: Article

References (50)

1. Chu G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J Biol Chem 1994; 269:787-790 (Pubitemid 24981963)
2. Yang Z, Faustino PJ, Andrews PA, Monastra R, Rasmussen AA, Ellison CD, et al. Decreased cisplatin/ DNA adduct formation is associated with cisplatin resistance in human head and neck cancer cell lines. Cancer Chemother Pharmacol 2000; 46:255-262 (Pubitemid 30764108)
3. Zhivotovsky B, Orrenius S. Caspase-2 function in response to DNA damage. Biochem Biophys Res Commun 2005; 331:859-867 (Pubitemid 40615517)
4. Basu A, Akkaraju GR. Regulation of caspase activation and cis-diamminedichloroplatinum(II)-induced cell death by protein kinase C. Biochemistry 1999; 38:4245-4251 (Pubitemid 29172183)
5. Seth R, Yang C, Kaushal V, Shah SV, Kaushal GP. p53-dependent caspase-2 activation in mitochondrial release of apoptosis-inducing factor and its role in renal tubular epithelial cell injury. J Biol Chem 2005; 280:31230-31239 (Pubitemid 41291860)
6. Cao X, Bennett RL, May WS. c-Myc and caspase-2 are involved in activating Bax during cytotoxic drug-induced apoptosis. J Biol Chem 2008; 283:14490-14496
7. Cuenin S, Tinel A, Janssens S, Tschopp J. p53-induced protein with a death domain (PIDD) isoforms differentially activate nuclear factor-kappaB and caspase-2 in response to genotoxic stress. Oncogene 2008; 27:387-396
8. Baliga BC, Read SH, Kumar S. The biochemical mechanism of caspase-2 activation. Cell Death Differ 2004; 11:1234-1241
9. Tinel A, Tschopp J. The PIDDosome, a protein complex implicated in activation of caspase-2 in response to genotoxic stress. Science 2004; 304:843-846 (Pubitemid 38620177)
10. Taghiyev AF, Guseva NV, Glover RA, Rokhlin OW, Cohen MB. TSA-induced cell death in prostate cancer cell lines is caspase-2 dependent and involves the PIDDosome. Cancer Biol Ther 2006; 5:1199-1205
11. Baptiste-Okoh N, Barsotti AM, Prives C. Caspase 2 is both required for p53-mediated apoptosis and down-regulated by p53 in a p21-dependent manner. Cell Cycle 2008; 7:1133-1138 (Pubitemid 351749262)
12. Baptiste-Okoh N, Barsotti AM, Prives C. A role for caspase 2 and PIDD in the process of p53-mediated apoptosis. Proc Natl Acad Sci USA 2008; 105:1937-1942
13. Berube C, Boucher LM, Ma W, Wakeham A, Salmena L, Hakem R, et al. Apoptosis caused by p53-induced protein with death domain (PIDD) depends on the death adapter protein RAIDD. Proc Natl Acad Sci USA 2005; 102:14314-14320 (Pubitemid 41429695)
14. Tinel A, Janssens S, Lippens S, Cuenin S, Logette E, Jaccard B, et al. Autoproteolysis of PIDD marks the bifurcation between pro-death caspase-2 and prosurvival NFkappaB pathway. EMBO J 2007; 26:197-208. (Pubitemid 46094711)
15. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 2002; 297:1352-1354 (Pubitemid 34913174)
16. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES. Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 2002; 277:13430-13437 (Pubitemid 34967937)
17. Upton JP, Austgen K, Nishino M, Coakley KM, Hagen A, Han D, et al. Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol Cell Biol 2008; 28:3943-3951 (Pubitemid 351812981)
18. Wagner KW, Engels IH, Deveraux QL. Caspase-2 can function upstream of bid cleavage in the TRAIL apoptosis pathway. J Biol Chem 2004; 279:35047-35052
19. Robertson JD, Gogvadze V, Kropotov A, Vakifahmetoglu H, Zhivotovsky B, Orrenius S. Processed caspase-2 can induce mitochondria-mediated apoptosis independently of its enzymatic activity. EMBO Rep 2004; 5:643-648 (Pubitemid 39136428)
20. Nathan Majewski VNR, Brooks Robey, Nissim Hay. Akt inhibits apoptosis downstream of BID cleavage via a glucose-dependent mechanism involving mitochondrial hexokinases. Mol Cell Biol 2004; 24:730-740
21. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K, et al. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 2004; 16:819-830 (Pubitemid 39586539)
22. Zaid H, Abu-Hamad S, Israelson A, Nathan I, Shoshan-Barmatz V. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ 2005; 12:751-760 (Pubitemid 40945982)
23. Pastorino JG, Shulga N, Hoek JB. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J Biol Chem 2002; 277:7610-7618 (Pubitemid 34953160)
24. Miyamoto S, Murphy AN, Brown JH. Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ 2008; 15:521-529 (Pubitemid 351267303)
25. Cartron PF, Juin P, Oliver L, Martin S, Meflah K, Vallette FM. Nonredundant role of Bax and Bak in Bid-mediated apoptosis. Mol Cell Biol 2003; 23:4701-4712 (Pubitemid 36734757)
26. Vakifahmetoglu H, Olsson M, Orrenius S, Zhivotovsky B. Functional connection between p53 and caspase-2 is essential for apoptosis induced by DNA damage. Oncogene 2006; 25:5683-5692 (Pubitemid 44389351)
27. Niizuma K, Endo H, Nito C, Myer DJ, Kim GS, Chan PH. The PIDDosome mediates delayed death of hippocampal CA1 neurons after transient global cerebral ischemia in rats. Proc Natl Acad Sci USA 2008; 105:16368-16373
28. Gao Z, Shao Y, Jiang X. Essential roles of the Bcl-2 family of proteins in caspase-2-induced apoptosis. J Biol Chem 2005; 280:38271-38275 (Pubitemid 43853724)
29. Bonzon C, Bouchier-Hayes L, Pagliari LJ, Green DR, Newmeyer DD. Caspase-2-induced apoptosis requires bid cleavage: a physiological role for bid in heat shock-induced death. Mol Biol Cell 2006; 17:2150-2157 (Pubitemid 44011731)
30. Slee EA, Keogh SA, Martin SJ. Cleavage of BID during cytotoxic drug and UV radiation-induced apoptosis occurs downstream of the point of Bcl-2 action and is catalysed by caspase-3: a potential feedback loop for amplification of apoptosis-associated mitochondrial cytochrome c release. Cell Death Differ 2000; 7:556-565
31. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998; 94:491-501. (Pubitemid 28391865)
32. Tang D, Lahti JM, Kidd VJ. Caspase-8 activation and bid cleavage contribute to MCF7 cellular execution in a caspase-3-dependent manner during staurosporine-mediated apoptosis. J Biol Chem 2000; 275:9303-9307 (Pubitemid 30185152)
33. Tsujimoto Y. Bcl-2 family of proteins: life-or-death switch in mitochondria. Biosci Rep 2002; 22:47-58. (Pubitemid 35217479)
34. Scorrano L, Korsmeyer SJ. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 2003; 304:437-444
35. Newmeyer DD, Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003; 112:481-490 (Pubitemid 36263081)
36. Degli Esposti M, Dive C. Mitochondrial membrane permeabilisation by Bax/Bak. Biochem Biophys Res Commun 2003; 304:455-461
37. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 2000; 7:1166-1173 (Pubitemid 32042223)
38. Pedersen PL. Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 2007; 39:211-222
39. Pedersen PL, Mathupala S, Rempel A, Geschwind JF, Ko YH. Mitochondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys Acta 2002; 1555:14-20. (Pubitemid 35245999)
40. Majewski N, Nogueira V, Robey RB, Hay N. Akt inhibits apoptosis downstream of BID cleavage via a glucose-dependent mechanism involving mitochondrial hexokinases. Mol Cell Biol 2004; 24:730-740 (Pubitemid 38057924)
41. Shimizu S, Konishi A, Kodama T, Tsujimoto Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci USA 2000; 97:3100-3105 (Pubitemid 30183262)
42. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 1999; 399:483-487
43. Banerjee J, Ghosh S. Bax increases the pore size of rat brain mitochondrial voltage-dependent anion channel in the presence of tBid. Biochem Biophys Res Commun 2004; 323:310-314 (Pubitemid 39206288)
44. Adachi M, Higuchi H, Miura S, Azuma T, Inokuchi S, Saito H, et al. Bax interacts with the voltage-dependent anion channel and mediates ethanol-induced apoptosis in rat hepatocytes. Am J Physiol Gastrointest Liver Physiol 2004; 287:695-705. (Pubitemid 39096637)
45. Chandra D, Choy G, Daniel PT, Tang DG. Bax-dependent regulation of Bak by voltage-dependent anion channel 2. J Biol Chem 2005; 280:19051-19061 (Pubitemid 41379611)
46. Abu-Hamad S, Sivan S, Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc Natl Acad Sci USA 2006; 103:5787-5792
47. 2+-dependent cell survival and death. Mol Cell 2009; 33:377-388
48. Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 2008; 321:1206-1210
49. L protein activates endogenous mitochondrial channels in living synaptic terminals. Proc Natl Acad Sci USA 2004; 101:13590-13595
50. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 2007; 9:550-555 (Pubitemid 46696536)