Antitumor triptycene analogs directly interact with isolated mitochondria to rapidly trigger markers of permeability transition

Anticancer Research

Volumn 27, Issue 5 A, 2007, Pages 3259-3271

  Perchellet, Elisabeth M ^a   Wang, Yang ^a   Lou, Kaiyan ^a   Zhao, Huiping ^a   Battina, Srinivas K ^a   Hua, Duy H ^a   Perchellet, Jean Pierre H ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Antitumor triptycenes; Isolated mitochondria; Mitochondrial Ca2+ release; Mitochondrial swelling; Tumor cell proliferation

Indexed keywords

ADENOSINE DIPHOSPHATE; ALAMETHICIN; ARSENIC TRIOXIDE; ARSENOSOBENZENE; ATRACTYLOSIDE; BONGKREKIC ACID; CYCLOSPORIN A; RUTHENIUM; TRIPTYCENE DERIVATIVE; UBIQUINONE DERIVATIVE;

ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; DOSE RESPONSE; DRUG INHIBITION; DRUG MECHANISM; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRION SWELLING; PRIORITY JOURNAL; TUMOR CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; CALCIUM; CARCINOMA, LEWIS LUNG; CELL GROWTH PROCESSES; CELL MEMBRANE PERMEABILITY; FEMALE; HL-60 CELLS; HUMANS; LEUKEMIA L1210; MICE; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANES; QUINONES;

EID: 35349023186     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Perchellet EM, Magill MJ, Huang X, Brantis CE, Hua DH and Perchellet JP: Triptycenes: a novel synthetic class of bifunctional anticancer drugs that inhibit nucleoside transport, induce DNA cleavage and decrease the viability of leukemic cells in the nanomolar range in vitro. Anti-Cancer Drugs 10: 749-766, 1999.
2. Wang B, Wu M, Perchellet EM, McIlvain CJ, Sperfslage BJ, Huang X, Tamura M, Stephany HA, Hua DH and Perchellet JP: A synthetic triptycene bisquinone, which blocks nucleoside transport and induces DNA fragmentation, retains its cytotoxic efficacy in daunorubicin-resistant HL-60 cell lines. Int J Oncology 19: 1169-1178, 2001.
3. Hua DH, Tamura M, Huang X, Stephany HA, Helfrich BA, Perchellet EM, Sperfslage BJ, Perchellet JP, Jiang S, Kyle DE and Chiang PK: Syntheses and bioactivities of substituted 9,10-dihydro-9,10-[1,2]benzenoanthra-cene-1,4,5,8- tetraones. Unusual reactivities with amines. J Org Chem 67: 2907-2912, 2002.
4. Perchellet EM, Sperfslage BJ, Wang Y, Huang X, Tamura M, Hua DH and Perchellet JP: Among substituted 9,10-dihydro-9,10-[1,2]benzenoanthracene-1,4,5, 8-tetraones, the lead antitumor triptycene bisquinone TT24 blocks nucleoside transport, induces apoptotic DNA fragmentation and decreases the viability of L1210 leukemic cells in the nanomolar range of daunorubicin in vitro. Anti- Cancer Drugs 13: 567-582, 2002.
5. Wang Y, Perchellet EM, Tamura M, Hua DH and Perchellet JP: Induction of poly(ADP-ribose) polymerase-1 cleavage by antitumor triptycene bisquinones in wild-type and daunorubicin-resistant HL-60 cell lines. Cancer Letters 188: 73-83, 2002.
6. Wang B, Perchellet EM, Wang Y, Tamura M, Hua DH and Perchellet JP: Antitumor triptycene bisquinones: a novel synthetic class of dual inhibitors of DNA topoisomerase I and II activities. Anti- Cancer Drugs 14: 503-514, 2003.
7. Perchellet EM, Wang Y, Weber RL, Lou K, Hua DH and Perchellet JP: Antitumor triptycene bisquinones induce a caspase-independent release of mitochondrial cytochrome c and a caspase-2- mediated activation of initiator caspase-8 and -9 in HL-60 cells by a mechanism which does not involve Fas signaling. Anti-Cancer Drugs 15: 929-946, 2004.
8. Wang Y, Perchellet EM, Ward MM, Lou K, Zhao H, Battina SK, Wiredu B, Hua DH and Perchellet JP: Antitumor triptycene analogs induce a rapid collapse of mitochondrial transmembrane potential in HL-60 cells and isolated mitochondria. Int J Oncol 28: 161-172, 2006.
9. Hua DH, Lou K, Battina SK, Zhao H, Perchellet EM, Wang Y and Perchellet JP: Syntheses, molecular targets and antitumor activities of novel triptycene bisquinones and 1,4-anthracenedione analogs. Anti-Cancer Agents Med Chem 6: 303-318, 2006.
10. Fulda S, Scaffidi C, Susin SA, Krammer PH, Kroemer G, Peter ME and Debatin KM: Activation of mitochondria and release of mitochondrial apoptogenic factors by betulinic acid. J Biol Chem 273: 33942-33948, 1998.
11. Blattner JR, He L and Lemasters JJ: Screening assays for the mitochondrial permeability transition using a fluorescence multiwell plate reader. Anal Biochem 295: 220-226, 2001.
12. Custodio JBA, Cardoso CMP and Almeida LM: Thiol protecting agents and antioxidants inhibit the mitochondrial permeability transition promoted by etoposide: implications in the prevention of etoposide-induced apoptosis. Chem-Biol Interac 140: 169-184, 2002.
13. Gottlieb E, Armour SM, Harris MH and Thompson CB: Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis. Cell Death Differ 10: 709-717, 2003.
14. Zamzami N, Maisse C, Metivier D and Kroemer G: Measurement of membrane permeability and permeability transition of mitochondria. Methods Cell Biol 65: 147-158, 2001.
15. Henry TR, Solem LE and Wallace KB: Channel-specific induction of the cyclosporine A-sensitive mitochondrial permeability transition by menadione. J Toxicol Environ Health 45: 489-504, 1995.
16. Bernardi P: Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155, 1999.
17. Zoratti M and Szabo I: The mitochondrial permeability transition. Biochim Biophys Acta 1241: 139-176, 1995.
18. Ly JD, Grubb DR and Lawen A: The mitochondrial membrane potential (Δψm) in apoptosis; an update. Apoptosis 8: 115-128, 2003.
19. Bernardi P and Petronilli V: The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J Bioenerg Biomembr 28: 131-138, 1996.
20. Grad JM, Cepero E and Boise LH: Mitochondria as targets for established and novel anti-cancer agents. Drug Resistance Updates 4: 85-91, 2001.
21. Joseph B, Marchetti P, Formstecher P, Kroemer G, Lewensohn R and Zhivotovsky B: Mitochondrial dysfunction is an essential step for killing of non-small cell lung carcinomas resistant to conventional treatment. Oncogene 21: 65-77, 2002.
22. Solary E, Bettaieb A, Dubrez-Daloz L and Corcos L: Mitochondria as a target for inducing death of malignant hematopoietic cells. Leukemia & Lymphoma 44: 563-574, 2003.
23. Dias N and Bailly C: Drugs targeting mitochondrial functions to control tumor cell growth. Biochem Pharmacol 70: 1-12, 2005.
24. Robertson JD, Gogvadze V, Zhivotovsky B and Orrenius S: Distinct pathways for stimulation of cytochrome c release. J Biol Chem 275: 32438-32443, 2000.
25. Huigsloot M, Tijdens IB, Mulder GJ, and van de Water B: Differential regulation of doxorubicin-induced mitochondrial dysfunction and apoptosis by Bcl-2 in mammary adenocarcinoma (MTLn3) cells. J Biol Chem 277: 35869-35879, 2002.
26. Tong X, Lin S, Fujii M and Hou D-X: Echinocystic acid induces apoptosis in HL-60 cells through mitochondria-mediated death pathway. Cancer Lett 212: 21-32, 2004.
27. Zhang S, Ong C-N and Shen H-M: Involvement of proapoptotic Bcl-2 family members in parthenolide-induced mitochondrial dysfunction and apoptosis. Cancer Lett 211: 175-188, 2004.
28. Kim JS, Lee JM, Chwae YJ, Kim YH, Lee JH, Kim K, Lee TH, Kim SJ and Park JH: Cisplatin-induced apoptosis in Hep3B cells: mitochondria- dependent and -independent pathways. Biochem Pharmacol 67: 1459-1468, 2004.
29. Ahn HJ, Kim YS, Kim J-U, Han SM, Shin JW and Yang HO: Mechanism of taxol-induced apoptosis in human SKOV3 ovarian carcinoma cells. J Cell Biochem 91: 1043-1052, 2004.
30. Shibata M-A, Ito Y, Morimoto J and Otsuki Y: Lovastatin inhibits tumor growth and lung metastasis in mouse mammary carcinoma model: a p53-independent mitochondrial-mediated apoptotic mechanism. Carcinogenesis 25: 1887-1898, 2004.
31. Hsu MJ, Chao Y, Chang YH, Ho FM, Huang LJ, Huang YL, Luh TY, Chen CP and Lin WW: Cell apoptosis induced by a synthetic carbazole compound LCY-2-CHO is mediated through activation of caspase and mitochondrial pathways. Biochem Pharmacol 70: 102-112, 2005.
32. Ko CH, Shen S-C, Hsu C-S and Chen Y-C: Mitochondrial-dependent, reactive oxygen species- independent apoptosis by myricetin: roles of protein kinase C, cytochrome c, and caspases. Biochem Pharmacol 69: 913-927, 2005.
33. Sen N, Das BB, Ganguly A, Mukherjee T, Tripathi G, Bandyopadhyay S, Rakshit S, Sen T and Majumder HK: Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. Cell Death Differ 11: 924-936, 2004.
34. Piret J-P, Arnould T, Fuks B, Chatelain P, Remade J and Michiels C: Mitochondria permeability transition-dependent tert-butyl hydroperoxide-induced apoptosis in hepatoma HepG2 cells. Biochem Pharmacol 67: 611-620, 2004.
35. Schempp CM, Kirkin V, Simon-Haarhaus B, Kersten A, Kiss J, Termeer CC, Gilb B, Kaufmann T, Borner C, Sleeman JP and Simon JC: Inhibition of tumour cell growth by hyperforin, a novel anticancer drug from St. John's wort that acts by induction of apoptosis. Oncogene 21: 1242-1250, 2002.
36. Marchetti P, Zamzami N, Joseph B, Schraen-Maschke S, Mereau-Richard C, Costantini P, Metivier D, Susin SA, Kroemer G and Formstecher P: The novel retinoid 6-[3-(1-adamantyl)-4- hydroxyphenyl]-2-naphtalene carboxylic acid can trigger apoptosis through a mitochondrial pathway independent of the nucleus. Cancer Res 59: 6257-6266, 1999.
37. Ricci J-E, Waterhouse N and Green DR: Mitochondrial functions during cell death, a complex (I-V) dilemma. Cell Death Differ 10: 488-492, 2003.
38. Donovan M and Cotter TG: Control of mitochondrial integrity by Bcl-2 family members and caspase-independent cell death. Biochim Biophys Acta 1644: 133-147, 2004.
39. Shimizu S, Narita M and Tsujimoto Y: Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487, 1999.
40. Gogvadze V, Robertson JD, Enoksson M, Zhivotovsky B and Orrenius S: Mitochondrial cytochrome c release may occur by volume-dependent mechanisms not involving permeability transition. Biochem J 378: 213-217, 2004.
41. Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y and Tsujimoto Y: Essential role of voltage- dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol 152: 237-250, 2001.
42. Bossy-Wetzel E, Newmeyer DD and Green DR: Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 17: 37-49, 1998.
43. Hearps AC, Burrows J, Connor CE, Woods GM, Lowenthal RM and Ragg SJ: Mitochondrial cytochrome c release precedes transmembrane depolarization and caspase-3 activation during ceramide-induced apoptosis of Jurkat T cells. Apoptosis 7: 387-394, 2002.
44. Scorrano L and Korsmeyer SJ: Mechanisms of cytochrome c release by proapoptotic Bcl-2 family members. Biochem Biophys Res Commun 304: 437-444, 2003.
45. Machida K, Hayashi Y and Osada H: A novel adenine nucleotide translocase inhibitor, MT-21, induces cytochrome c release by a mitochondrial permeability transition-independent mechanism. J Biol Chem 277: 31243-31248, 2002.
46. Bauer MK, Schubert A, Rocks O and Grimm S: Adenine nucleotide translocase-1, a component of the permeability transition pore, can dominantly induce apoptosis. J Cell Biol 147: 1493-1502, 1999.
47. Zoratti M, Szabò I and De Marchi U: Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 1706: 40-52, 2005.
48. Walter L, Miyoshi H, Leverve X, Bernardi P and Fontaine E: Regulation of the mitochondrial permeability transition pore by ubiquinone analogs. A progress report. Free Radical Res 36: 405- 412, 2002.
49. Henry TR and Wallace KB: Differential mechanisms of induction of the mitochondrial permeability transition by quinones of varying chemical reactivities. Toxicol Appl Pharmacol 134: 195-203, 1995.
50. Fontaine E, Ichas F and Bernardi P: A ubiquinone-binding site regulates the mitochondrial permeability transition pore. J Biol Chem 273: 25734-25740, 1998.
51. Kristián T, Gertsch J, Bates TE and Siesjö BK: Characteristics of the calcium-triggered mitochondrial permeability transition in nonsynaptic brain mitochondria: effect of cyclosporin A and ubiquinone 0. J Neurochem 74: 1999-2009, 2000.
52. Ichas F and Mazat JP: From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366: 33-50, 1998.