N-benzyladriamycin-14-valerate (AD198) induces apoptosis through protein kinase C-δ-induced phosphorylation of phospholipid scramblase 3

Cancer Research

Volumn 65, Issue 21, 2005, Pages 10016-10023

  He, Yongwen ^a   Liu, Jihua ^a   Durrant, David ^a   Yang, Hung Sheng ^a   Sweatman, Trevor ^b   Lothstein, Leonard ^b   Lee, Ray M ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF TENNESSEE CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACYCLINE DERIVATIVE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CYCLOSPORIN A; N BENZYLDOXORUBICIN 14 VALERATE; PROTEIN KINASE C GAMMA; SCRAMBLASE; SCRAMBLASE 3; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MITOCHONDRION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CASPASES; CELL MEMBRANE PERMEABILITY; DOXORUBICIN; ENZYME ACTIVATION; HELA CELLS; HUMANS; INTRACELLULAR MEMBRANES; MITOCHONDRIA; PHOSPHOLIPID TRANSFER PROTEINS; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; THREONINE;

EID: 27544457225     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-1688     Document Type: Article

References (32)

1. Bevers EM, Comfurius P, Dekkers DW, Zwaal RF. Lipid translocation across the plasma membrane of mammalian cells Biochim Biophys Acta 1999;1439:317-30.
2. Williamson P, Schlegel RA. Transbilayer phospholipid movement and the clearance of apoptotic cells. Biochim Biophys Acta 2002;1585:53-63.
3. Wiedmer T, Zhou Q, Kwoh DY, Sims PJ. Identification of three new members of the phospholipid scramblase gene family. Biochim Biophys Acta 2000; 1467:244-53.
4. Wiedmer T, Zhao J, Nanjundan M, Sims PJ. Palmitoylation of phospholipid scramblase 1 controls its distribution between nucleus and plasma membrane. Biochemistry 2003;42:1227-33.
5. Ben-Efraim I, Zhou Q, Wiedmer T, Gerace L, Sims PJ. Phospholipid scramblase 1 is imported into the nucleus by a receptor-mediated pathway and interacts with DNA. Biochemistry 2004;43:3518-26.
6. Yu A, McMaster CR, Byers DM, Ridgway ND, Cook HW. Stimulation of phosphatidylserine biosynthesis and facilitation of UV-induced apoptosis in Chinese hamster ovary cells overexpressing phospholipid scramblase 1. J Biol Chem 2003;278:9706-14.
7. Liu J, Dai Q, Chen J, et al. Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response. Mol Cancer Res 2003;1:892-902.
8. Liu J, Chen J, Dai Q, Lee RM. Phospholipid scramblase 3 is the mitochondrial target of protein kinase C δ-induced apoptosis. Cancer Res 2003;63:1153-6.
9. Wiedmer T, Zhao J, Li L, et al. Adiposity, dyslipidemia, and insulin resistance in mice with targeted deletion of phospholipid scramblase 3 (PLSCR3). Proc Natl Acad Sci U S A 2004;101:13296-301.
10. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 1992;258:607-14.
11. Ohno S. The distinct biological potential of PKC isotypes. In: Parker PJ, Dekker LV, editors. Protein kinase C. Georgetown: Lendes Bioscience; 1977. p. 75-95.
12. Brodie C, Blumberg PM. Regulation of cell apoptosis by protein kinase Cδ. Apoptosis 2003;8:19-27.
13. Liu J, Durrant D, Lee RM. Protein kinase C-δ and its downstream effectors as potential targets for cancer therapy. Cancer Therapy 2003;1:289-95.
14. Blass M, Kronfeld I, Kazimirsky G, Blumberg PM, Brodie C. Tyrosine phosphorylation of protein kinase Cδ is essential for its apoptotic effect in response to etoposide. Mol Cell Biol 2002;22:182-95.
15. Denning MF, Wang Y, Tibudan S, Alkan S, Nickoloff BJ, Qin JZ. Caspase activation and disruption of mitochondrial membrane potential during UV radiation-induced apoptosis of human keratinocytes requires activation of protein kinase C. Cell Death Differ 2002; 9:40-52.
16. DeVries TA, Neville MC, Reyland ME. Nuclear import of PKCδ is required for apoptosis: identification of a novel nuclear import sequence. EMBO J 2002;21:6050-60.
17. Emoto Y, Manome Y, Meinhardt G, et al. Proteolytic activation of protein kinase Cδ by an ICE-like protease in apoptotic cells. EMBO J 1995;14:6148-56.
18. Yoshida K, Wang HG, Miki Y, Kufe D. Protein kinase Cδ is responsible for constitutive and DNA damage-induced phosphorylation of Rad9. EMBO J 2003;22: 1431-41.
19. Yuan ZM, Utsugisawa T, Ishiko T, et al. Activation of protein kinase Cδ by the c-Abl tyrosine kinase in response to ionizing radiation. Oncogene 1998;16: 1643-8.
20. Volkmer E, Karnitz LM. Human homologs of Schizosaccharomyces pombe rad1, hus1, and rad9 form a DNA damage-responsive protein complex. J Biol Chem 1999;274:567-70.
21. Frasch SC, Henson PM, Kailey JM, et al. Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cδ. J Biol Chem 2000; 275:23065-73.
22. Lothstein L, Sweatman TW, Dockter ME, Israel M. Resistance to N-benzyladriamycin-14-valerate in mouse J774.2 cells: P-glycoprotein expression without reduced N-benzyladriamycin-14-valerate accumulation. Cancer Res 1992;52:3409-17.
23. Lothstein L, Wright HM, Sweatman TW, Israel M. N-benzyladriamycin-14- valerate and drug resistance: correlation of anthracycline structural modification with intracellular accumulation and distribution in multidrug resistant cells. Oncol Res 1992;4:341-7.
24. Roaten JB, Kazanietz MG, Sweatman TW, Lothstein L, Israel M, Parrill AL. Molecular models of N-benzyladriamycin-14-valerate (AD 198) in complex with the phorbol ester-binding C1b domain of protein kinase C-δ. J Med Chem 2001;44:1028-34.
25. Barrett CM, Lewis FL, Roaten JB, et al. Novel extranuclear-targeted anthracyclines override the anti-apoptotic functions of Bcl-2 and target protein kinase C pathways to induce apoptosis. Mol Cancer Ther 2002; 1:469-81.
26. Roaten JB, Kazanietz MG, Caloca MJ, et al. Interaction of the novel anthracycline antitumor agent N-benzyladriamycin-14-valerate with the C1-regulatory domain of protein kinase C: structural requirements, isoform specificity, and correlation with drug cytotoxicity. Mol Cancer Ther 2002;1: 483-92.
27. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 2004;56:185-229.
28. Lothstein L, Koseki Y, Sweatman TW. P-glycoprotein overexpression in mouse cells does not correlate with resistance to N-benzyladriamycin-14-valerate (AD 198). Anticancer Drugs 1994;5:623-33.
29. Lothstein L, Rodrigues PJ, Sweatman TW, Israel M. Cytotoxicity and intracellular biotransformation of N-benzyladriamycin-14-valerate (AD 198) are modulated by changes in 14-O-acyl chain length. Anticancer Drugs 1998;9:58-66.
30. Bilyeu JD, Panta GR, Cavin LG, et al. Circumvention of nuclear factor κB-induced chemoresistance by cytoplasmic-targeted anthracyclines. Mol Pharmacol 2004;65:1038-47.
31. Gong XM, Choi J, Franzin CM, Zhai D, Reed JC, Marassi FM. Conformation of membrane-associated proapoptotic tBid. J Biol Chem 2004;279: 28954-60.
32. Oh KJ, Barbuto S, Meyer N, Kim RS, Collier RJ, Korsmeyer SJ. Conformational changes in BID, a pro-apoptotic BCL-2 family member, upon membrane binding. A site-directed spin labeling study. J Biol Chem 2005;280:753-67.