Cell-centric view of apoptosis and apoptotic cell death-inducing antitumoral strategies

Cancers

Volumn 3, Issue 1, 2011, Pages 1042-1080

  Apraiz, Aintzane ^a   Boyano, Maria Dolores ^a   Asumendi, Aintzane ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Apoptosis; Classical chemotherapy; Targeted chemotherapy

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; 7 HYDROXYSTAUROSPORINE; 8 FLUORO 3,4 DIHYDRO 2 [4 (METHYLAMINOMETHYL)PHENYL]PYRROLO[3,4,5 E,F][2]BENZAZEPIN 6(5H) ONE; A 779024; ANTHRACYCLINE; AZD 7762; AZD 7792; CAMPTOTHECIN DERIVATIVE; CISPLATIN; CYCLIN DEPENDENT KINASE INHIBITOR; DACTINOMYCIN; DNA TOPOISOMERASE INHIBITOR; DOCETAXEL; DOXORUBICIN; EPOTHILONE DERIVATIVE; FOLIC ACID DERIVATIVE; GOSSYPOL; GYRASE INHIBITOR; IMATINIB; LOMEGUATRIB; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; NAVELBINE; OBLIMERSEN; OLAPARIB; PACLITAXEL; PHOSPHOTRANSFERASE INHIBITOR; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VELIPARIB; VINBLASTINE; VINCRISTINE; XL 844;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; APOPTOTIC CELL DEATH; CANCER CELL; CANCER CHEMOTHERAPY; CELL DEATH; CELL NUCLEUS; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHRONIC MYELOID LEUKEMIA; CYTOSKELETON; DNA ADDUCT; DNA DAMAGE; DNA REPAIR; DRUG CLASSIFICATION; DRUG TARGETING; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; NONHUMAN; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION;

EID: 79953701064     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers3011042     Document Type: Review

References (173)

1. Majno, G.; Joris, I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 1995, 146, 3-15.
2. Buchdunger, E.; Zimmermann, J.; Mett, H.; Meyer, T.; Müller, M.; Druker, B.; Lydon, N. Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res. 1996, 56, 100-104.
3. Kerr, J.; Wyllie, A.; Currie, A. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26, 239-257.
4. Diamantis, A.; Magiorkinis, E.; Sakorafas, G.; Androutsos, G. A brief history of apoptosis: From ancient to modern times. Onkologie 2008, 31, 702-706.
5. Proskuryakov, S.Y.; Konoplyannikov, A.G.; Gabai, V.L. Necrosis: A specific form of programmed cell death? Exp. Cell Res. 2003, 283, 1-16.
6. Golstein, P.; Kroemer, G. Cell death by necrosis: Towards a molecular definition. Trends Biochem. Sci. 2007, 32, 37-43.
7. Festjens, N.; Vanden Berghe, T.; Vandenabeele, P. Necrosis, a well-orchestrated form of cell demise: Signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta 2006, 1757, 1371-1387.
8. Kroemer, G.; Galluzzi, L.; Vandenabeele, P.; Abrams, J.; Alnemri, E.S.; Baehrecke, E.H.; Blagosklonny, M.V.; El-Deiry, W.S.; Golstein, P.; Green, D.R.; Hengartner, M.; Knight, R.A.; Kumar, S.; Lipton, S.A.; Malorni, W.; Nunez, G.; Peter, M.E.; Tschopp, J.; Yuan, J.; Piacentini, M.; Zhivotovsky, B.; Melino, G. Classification of cell death: Recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Difer. 2009, 16, 3-11.
9. Schlegel, R.A.; Williamson, P. Phosphatidylserine, a death knell. Cell Death Difer. 2001, 8, 551-563.
10. Balasubramanian, K.; Mirnikjoo, B.; Schroit, A.J. Regulated externalization of phosphatidylserine at the cell surface: Implications for apoptosis. J. Biol. Chem. 2007, 282, 18357-18364.
11. Fadok, V.A.; Voelker, D.R.; Campbell, P.A.; Cohen, J.J.; Bratton, D.L.; Henson, P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 1992, 148, 2207-2216.
12. Savill, J.; Gregory, C. Apoptotic PS to phagocyte TIM-4: Eat me. Immunity 2007, 27, 830-832.
13. Danial, N.N.; Korsmeyer, S.J. Cell death: Critical control points. Cell 2004, 116, 205-219.
14. Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol. 2007, 35, 495-516.
15. Ashkenazi, A.; Dixit, V. Death receptors: Signaling and modulation. Science 1998, 281, 1305-1308.
16. Guicciardi, M.E.; Gores, G.J. Life and death by death receptors. FASEB J. 2009, 23, 1625-1637.
17. Meylan, E.; Tschopp, J. The RIP kinases: Crucial integrators of cellular stress. Trends Biochem. Sci. 2005, 30, 151-159.
18. O'Donnell, M.A.; Legarda-Addison, D.; Skountzos, P.; Yeh, W.C.; Ting, A.T. Ubiquitination of RIP1 regulates an NF-B-independent cell death switch in TNF signaling. Curr. Biol. 2007, 17, 418-424.
19. Li, J.; Yuan, J. Caspases in apoptosis and beyond. Oncogene 2008, 27 (48), 6194-6206.
20. Moffitt, K.L.; Martin, S.L.; Walker, B. Proteases implicated in apoptosis: Old and new. J. Pharm. Pharmacol. 2010, 62, 563-576.
21. Green, D.; Kroemer, G. Pharmacological manipulation of cell death: Clinical applications in sight? J. Clin. Invest. 2005, 115, 2610-2617.
22. Heath-Engel, H.M.; Chang, N.C.; Shore, G.C. The endoplasmic reticulum in apoptosis and autophagy: Role of the BCL-2 protein family. Oncogene 2008, 27, 6419-6433.
23. Ferri, K.F.; Kroemer, G. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 2001, 3, E255-E263.
24. Breckenridge, D.G.; Germain, M.; Mathai, J.P.; Nguyen, M.; Shore, G.C. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003, 22, 8608-8618.
25. de Bruin, E.C.; Medema, J.P. Apoptosis and non-apoptotic deaths in cancer development and treatment response. Cancer Treat Rev. 2008, 34, 737-749.
26. Crompton, M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341, 233-249.
27. Tsujimoto, Y.; Shimizu, S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 2007, 12, 835-840.
28. Baines, C.P.; Kaiser, R.A.; Sheiko, T.; Craigen, W.J.; Molkentin, J.D. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 2007, 9, 550-555.
29. Baines, C.P.; Kaiser, R.A.; Purcell, N.H.; Blair, N.S.; Osinska, H.; Hambleton, M.A.; Brunskill, E.W.; Sayen, M.R.; Gottlieb, R.A.; Dorn, G.W.; Robbins, J.; Molkentin, J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434, 658-662.
30. Nakagawa, T.; Shimizu, S.; Watanabe, T.; Yamaguchi, O.; Otsu, K.; Yamagata, H.; Inohara, H.; Kubo, T.; Tsujimoto, Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005, 434, 652-658.
31. Baines, C.P. The molecular composition of the mitochondrial permeability transition pore. J. Mol. Cell Cardiol. 2009, 46, 850-857.
32. Brunelle, J.K.; Letai, A. Control of mitochondrial apoptosis by the Bcl-2 family. J. Cell Sci. 2009, 122, 437-441.
33. Tsujimoto, Y.; Jaffe, E.; Cossman, J.; Gorham, J.; Nowell, P.C.; Croce, C.M. Clustering of breakpoints on chromosome 11 in human B-cell neoplasms with the t(1 1;14) chromosome translocation. Nature 1985, 315, 340-343.
34. Cleary, M.L.; Smith, S.D.; Sklar, J. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14;18) translocation. Cell 1986, 47, 19-28.
35. Vaux, D.L.; Cory, S.; Adams, J.M. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988, 335, 440-442.
36. Oltvai, Z.N.; Milliman, C.L.; Korsmeyer, S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993, 74, 609-619.
37. Cory, S.; Huang, D.C.; Adams, J.M. The Bcl-2 family: Roles in cell survival and oncogenesis. Oncogene 2003, 22, 8590-8607.
38. Korsmeyer, S.J.; Shutter, J.R.; Veis, D.J.; Merry, D.E.; Oltvai, Z.N. Bcl-2/Bax: A rheostat that regulates an anti-oxidant pathway and cell death. Semin. Cancer Biol. 1993, 4, 327-332.
39. Wei, M.C.; Lindsten, T.; Mootha, V.K.; Weiler, S.; Gross, A.; Ashiya, M.; Thompson, C.B.; Korsmeyer, S.J. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 2000, 14, 2060-2071.
40. Wolter, K.G.; Hsu, Y.T.; Smith, C.L.; Nechushtan, A.; Xi, X.G.; Youle, R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 1997, 139, 1281-1292.
41. Hill, M.; Adrain, C.; Martin, S. Portrait of a killer: The mitochondrial apoptosome emerges from the shadows. Mol. Interv. 2003, 3, 19-26.
42. Deveraux, Q.L.; Roy, N.; Stennicke, H.R.; Van Arsdale, T.; Zhou, Q.; Srinivasula, S.M.; Alnemri, E.S.; Salvesen, G.S.; Reed, J.C. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 1998, 17, 2215-2223.
43. Ogata, M.; Hino, S.; Saito, A.; Morikawa, K.; Kondo, S.; Kanemoto, S.; Murakami, T.; Taniguchi, M.; Tanii, I.; Yoshinaga, K.; Shiosaka, S.; Hammarback, J.A.; Urano, F.; Imaizumi, K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell Biol. 2006, 26, 9220-9231.
44. Roos, W.P.; Kaina, B. DNA damage-induced cell death by apoptosis. Trends Mol. Med. 2006, 12, 440-450.
45. Hong, S.J.; Dawson, T.M.; Dawson, V.L. Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol. Sci. 2004, 25, 259-264.
46. Shall, S.; de Murcia, G. Poly (ADP-ribose) polymerase-1: What have we learned from the deficient mouse model? Mutat. Res. 2000, 460, 1-15.
47. Ha, H.C.; Snyder, S.H. Poly(ADP-ribose) polymerase-1 in the nervous system. Neurobiol. Dis. 2000, 7, 225-239.
48. Abraham, R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001, 15, 2177-2196.
49. Mancini, M.; Machamer, C.; Roy, S.; Nicholson, D.; Thornberry, N.; Casciola-Rosen, L.; Rosen, A. Caspase-2 is localized at the Golgi complex and cleaves golgin-160 during apoptosis. J. Cell Biol. 2000, 149, 603-612.
50. Malisan, F.; Testi, R. GD3 ganglioside and apoptosis. Biochim. Biophys. Acta 2002, 1585, 179-187.
51. Hannun, Y.A.; Obeid, L.M. Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 2008, 9, 139-150.
52. Hicks, S.W.; Machamer, C.E. Golgi structure in stress sensing and apoptosis. Biochim. Biophys. Acta 2005, 1744, 406-414.
53. Rippo, M.R.; Malisan, F.; Ravagnan, L.; Tomassini, B.; Condo, I.; Costantini, P.; Susin, S.A.; Rufini, A.; Todaro, M.; Kroemer, G.; Testi, R. GD3 ganglioside directly targets mitochondria in a bcl-2-controlled fashion. FASEB J. 2000, 14, 2047-2054.
54. Garcia-Ruiz, C.; Colell, A.; Morales, A.; Calvo, M.; Enrich, C.; Fernandez-Checa, J.C. Trafficking of ganglioside GD3 to mitochondria by tumor necrosis factor-alpha. J. Biol. Chem. 2002, 277, 36443-36448.
55. Tomassini, B.; Malisan, F.; Franchi, L.; Nicolo, C.; Calvo, G.B.; Saito, T.; Testi, R. Calnexin suppresses GD3 synthase-induced apoptosis. FASEB J. 2004, 18, 1553-1555.
56. Jones, S.; Ledgerwood, E.; Prins, J.; Galbraith, J.; Johnson, D.; Pober, J.; Bradley, J. TNF recruits TRADD to the plasma membrane but not the trans-Golgi network, the principal subcellular location of TNF-R1. J. Immunol. 1999, 162, 1042-1048.
57. Bennett, M.; Macdonald, K.; Chan, S.W.; Luzio, J.P.; Simari, R.; Weissberg, P. Cell surface trafficking of Fas: A rapid mechanism of p53-mediated apoptosis. Science 1998, 282, 290-293.
58. Schutze, S.; Schneider-Brachert, W. Impact of TNF-R1 and CD95 internalization on apoptotic and antiapoptotic signaling. Results Probl. Cell Difer. 2009, 49, 63-85.
59. Boya, P.; Kroemer, G. Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27, 6434-6451.
60. Li, W.; Yuan, X.; Nordgren, G.; Dalen, H.; Dubowchik, G.M.; Firestone, R.A.; Brunk, U.T. Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett. 2000, 470, 35-39.
61. Erdal, H.; Berndtsson, M.; Castro, J.; Brunk, U.; Shoshan, M.; Linder, S. Induction of lysosomal membrane permeabilization by compounds that activate p53-independent apoptosis. Proc. Natl. Acad. Sci. USA 2005, 102, 192-197.
62. Park, J.H.; Schuchman, E.H. Acid ceramidase and human disease. Biochim. Biophys. Acta 2006, 1758, 2133-2138.
63. Chwieralski, C.; Welte, T.; Bühling, F. Cathepsin-regulated apoptosis. Apoptosis 2006, 11, 143-149.
64. Turk, B.; Stoka, V. Protease signalling in cell death: Caspases versus cysteine cathepsins. FEBS Lett. 2007, 581, 2761-2767.
65. Heinrich, M.; Wickel, M.; Winoto-Morbach, S.; Schneider-Brachert, W.; Weber, T.; Brunner, J.; Saftig, P.; Peters, C.; Kronke, M.; Schutze, S. Ceramide as an activator lipid of cathepsin D. Adv. Exp. Med. Biol. 2000, 477, 305-315.
66. Guicciardi, M.; Deussing, J.; Miyoshi, H.; Bronk, S.; Svingen, P.; Peters, C.; Kaufmann, S.; Gores, G. Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest. 2000, 106, 1127-1137.
67. Foghsgaard, L.; Wissing, D.; Mauch, D.; Lademann, U.; Bastholm, L.; Boes, M.; Elling, F.; Leist, M.; Jaattela, M. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 2001, 153, 999-1010.
68. Nagaraj, N.S.; Vigneswaran, N.; Zacharias, W. Cathepsin B mediates TRAIL-induced apoptosis in oral cancer cells. J. Cancer Res. Clin. Oncol. 2006, 132, 171-183.
69. Turk, B.; Turk, V. Lysosomes as "suicide bags" in cell death: myth or reality? J. Biol. Chem. 2009, 284, 21783-21787.
70. Klaric, M.; Tao, S.; Stoka, V.; Turk, B.; Turk, V. Cysteine cathepsins are not critical for TNF-alpha-induced cell death in T98G and U937 cells. Biochim. Biophys. Acta 2009, 1794, 1372-1377.
71. Cirman, T.; Oresic, K.; Mazovec, G.D.; Turk, V.; Reed, J.C.; Myers, R.M.; Salvesen, G.S.; Turk, B. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J. Biol. Chem. 2004, 279, 3578-3587.
72. Blomgran, R.; Zheng, L.; Stendahl, O. Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J. Leukoc. Biol. 2007, 81, 1213-1223.
73. Houseweart, M.; Vilaythong, A.; Yin, X.; Turk, B.; Noebels, J.; Myers, R. Apoptosis caused by cathepsins does not require Bid signaling in an in vivo model of progressive myoclonus epilepsy (EPM1). Cell Death Difer. 2003, 10, 1329-1335.
74. Droga-Mazovec, G.; Bojic, L.; Petelin, A.; Ivanova, S.; Romih, R.; Repnik, U.; Salvesen, G.S.; Stoka, V.; Turk, V.; Turk, B. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J. Biol. Chem. 2008, 283, 19140-19150.
75. Trapani, J.A.; Smyth, M.J. Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2002, 2, 735-747.
76. Bolitho, P.; Voskoboinik, I.; Trapani, J.; Smyth, M. Apoptosis induced by the lymphocyte effector molecule perforin. Curr. Opin. Immunol. 2007, 19, 339-347.
77. Pardo, J.; Bosque, A.; Brehm, R.; Wallich, R.; Naval, J.; Müllbacher, A.; Anel, A.; Simon, M.M. Apoptotic pathways are selectively activated by granzyme A and/or granzyme B in CTL-mediated target cell lysis. J. Cell Biol. 2004, 167, 457-468.
78. Talanian, R.V.; Yang, X.; Turbov, J.; Seth, P.; Ghayur, T.; Casiano, C.A.; Orth, K.; Froelich, C.J. Granule-mediated killing: pathways for granzyme B-initiated apoptosis. J. Exp. Med. 1997, 186, 1323-1331.
79. Thomas, D.A.; Du, C.; Xu, M.; Wang, X.; Ley, T.J. DFF45/ICAD can be directly processed by granzyme B during the induction of apoptosis. Immunity 2000, 12, 621-632.
80. Sakahira, H.; Enari, M.; Nagata, S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 1998, 391, 96-99.
81. Barry, M.; Heibein, J.A.; Pinkoski, M.J.; Lee, S.F.; Moyer, R.W.; Green, D.R.; Bleackley, R.C. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol. Cell Biol. 2000, 20, 3781-3794.
82. Goping, I.S.; Barry, M.; Liston, P.; Sawchuk, T.; Constantinescu, G.; Michalak, K.M.; Shostak, I.; Roberts, D.L.; Hunter, A.M.; Korneluk, R.; Bleackley, R.C. Granzyme B-induced apoptosis requires both direct caspase activation and relief of caspase inhibition. Immunity 2003, 18, 355-365.
83. Fan, Z.; Beresford, P.J.; Oh, D.Y.; Zhang, D.; Lieberman, J. Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell 2003, 112, 659-672.
84. DeVita, V.J.; Chu, E. A history of cancer chemotherapy. Cancer Res 2008, 68, 8643-8653.
85. Cho, K.; Wang, X.; Nie, S.; Chen, Z.G.; Shin, D.M. Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer Res. 2008, 14, 1310-1316.
86. Maurer, B.J.; Metelitsa, L.S.; Seeger, R.C.; Cabot, M.C.; Reynolds, C.P. Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)-retinamide in neuroblastoma cell lines. J. Natl. Cancer Inst. 1999, 91, 1138-1146.
87. Tiwari, M.; Bajpai, V.; Sahasrabuddhe, A.; Kumar, A.; Sinha, R.; Behari, S.; Godbole, M. Inhibition of N-(4-hydroxyphenyl)retinamide-induced autophagy at a lower dose enhances cell death in malignant glioma cells. Carcinogenesis 2008, 29, 600-609.
88. Chu, E.; DeVita, V.T., Jr. Physicians Cancer Chemotherapy Drug Manual 2009; Jones & Bartlett Publishers: London, UK, 2009.
89. Chen, D.; Milacic, V.; Frezza, M.; Dou, Q.P. Metal complexes, their cellular targets and potential for cancer therapy. Curr. Pharm. Des. 2009, 15, 777-791.
90. Wang, X.; Guo, Z. The role of sulfur in platinum anticancer chemotherapy. Anticancer Agents Med. Chem. 2007, 7, 19-34.
91. Kasherman, Y.; Sturup, S.; Gibson, D. Is glutathione the major cellular target of cisplatin? A study of the interactions of cisplatin with cancer cell extracts. J. Med. Chem. 2009, 52 (14), 4319-4328.
92. Dedon, P.C.; Borch, R.F. Characterization of the reactions of platinum antitumor agents with biologic and nonbiologic sulfur-containing nucleophiles. Biochem. Pharmacol. 1987, 36, 1955-1964.
93. Boulikas, T. Clinical overview on Lipoplatin: A successful liposomal formulation of cisplatin. Expert Opin. Invest. Drugs 2009, 18, 1197-1218.
94. Zhang, J.; Wang, L.; Xing, Z.; Liu, D.; Sun, J.; Li, X.; Zhang, Y. Status of bi-and multi-nuclear platinum anticancer drug development. Anticancer Agents Med. Chem. 2010, 10, 272-282.
95. Siddik, Z.H. Biochemical and molecular mechanisms of cisplatin resistance. Cancer Treat. Res. 2002, 112, 263-284.
96. 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.
97. Kang, H.J.; Park, H.J. Novel molecular mechanism for actinomycin D activity as an oncogenic promoter G-quadruplex binder. Biochemistry 2009, 48, 7392-7398.
98. Galm, U.; Hager, M.H.; Van Lanen, S.G.; Ju, J.; Thorson, J.S.; Shen, B. Antitumor antibiotics: Bleomycin, enediynes, and mitomycin. Chem. Rev. 2005, 105, 739-758.
99. Bradner, W.T. Mitomycin C: A clinical update. Cancer Treat. Rev. 2001, 27, 35-50.
100. Schumacker, P.T. Reactive oxygen species in cancer cells: Live by the sword, die by the sword. Cancer Cell 2006, 10, 175-176.
101. Magnusson, M.; Höglund, P.; Johansson, K.; Jönsson, C.; Killander, F.; Malmström, P.; Weddig, A.; Kjellén, E. Pentoxifylline and vitamin E treatment for prevention of radiation-induced side-effects in women with breast cancer: A phase two, double-blind, placebo-controlled randomised clinical trial (Ptx-5). Eur. J. Cancer 2009, 45, 2488-2495.
102. Pace, A.; Giannarelli, D.; Galiè, E.; Savarese, A.; Carpano, S.; Della Giulia, M.; Pozzi, A.; Silvani, A.; Gaviani, P.; Scaioli, V.; Jandolo, B.; Bove, L.; Cognetti, F. Vitamin E neuroprotection for cisplatin neuropathy: a randomized, placebo-controlled trial. Neurology 2010, 74, 762-766.
103. De Larco, J.E.; Park, C.A.; Dronava, H.; Furcht, L.T. Paradoxical roles for antioxidants in tumor prevention and eradication. Cancer Biol. Ther. 2010, 9, 362-370.
104. Wang, J.; Yi, J. Cancer cell killing via ROS: To increase or decrease, that is the question. Cancer Biol. Ther. 2008, 7, 1875-1884.
105. Asumendi, A.; Morales, M.C.; Alvarez, A.; Aréchaga, J.; Pérez-Yarza, G. Implication of mitochondria-derived ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl)retinamideinduced apoptosis. Br. J. Cancer 2002, 86, 1951-1956.
106. Coleman, M.C.; Asbury, C.R.; Daniels, D.; Du, J.; Aykin-Burns, N.; Smith, B.J.; Li, L.; Spitz, D.R.; Cullen, J.J. 2-deoxy-D-glucose causes cytotoxicity, oxidative stress, and radiosensitization in pancreatic cancer. Free Radic. Biol. Med. 2008, 44, 322-331.
107. Wei, X.; Guo, W.; Wu, S.; Wang, L.; Huang, P.; Liu, J.; Fang, B. Oxidative stress in NSC-741909-induced apoptosis of cancer cells. J. Transl. Med. 2010, 8, 37.
108. Ralph, S.J.; Rodríguez-Enríquez, S.; Neuzil, J.; Moreno-Sánchez, R. Bioenergetic pathways in tumor mitochondria as targets for cancer therapy and the importance of the ROS-induced apoptotic trigger. Mol. Aspects Med. 2010, 31, 29-59.
109. Buchdunger, E.; Zimmermann, J.; Mett, H.; Meyer, T.; Müller, M.; Druker, B.J.; Lydon, N.B. Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res. 1996, 56, 100-104.
110. Kitada, S.; Leone, M.; Sareth, S.; Zhai, D.; Reed, J.C.; Pellecchia, M. Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/leukemia-2 proteins. J. Med. Chem. 2003, 46, 4259-4264.
111. Vermel, E.M. The search for antitumour substances of plan origin. Acta Unio. Int. Contra. Cancrum. 1964, 20, 211-213.
112. Tanphaichitr, N.; Fitzgerald, L.M.; Matlin, S.A. Differential effects of () and (-) gossypol enantiomers on mitochondrial function and proliferation of cultured TM4 cells. J. Androl. 1988, 9, 270-277.
113. Kang, M.H.; Reynolds, C.P. Bcl-2 inhibitors: Targeting mitochondrial apoptotic pathways in cancer therapy. Clin. Cancer Res. 2009, 15, 1126-1132.
114. Oltersdorf, T.; Elmore, S.W.; Shoemaker, A.R.; Armstrong, R.C.; Augeri, D.J.; Belli, B.A.; Bruncko, M.; Deckwerth, T.L.; Dinges, J.; Hajduk, P.J.; Joseph, M.K.; Kitada, S.; Korsmeyer, S.J.; Kunzer, A.R.; Letai, A.; Li, C.; Mitten, M.J.; Nettesheim, D.G.; Ng, S.; Nimmer, P.M.; O'Connor, J.M.; Oleksijew, A.; Petros, A.M.; Reed, J.C.; Shen, W.; Tahir, S.K.; Thompson, C.B.; Tomaselli, K.J.; Wang, B.; Wendt, M.D.; Zhang, H.; Fesik, S.W.; Rosenberg, S.H. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435, 677-681.
115. Tse, C.; Shoemaker, A.R.; Adickes, J.; Anderson, M.G.; Chen, J.; Jin, S.; Johnson, E.F.; Marsh, K.C.; Mitten, M.J.; Nimmer, P.; Roberts, L.; Tahir, S.K.; Xiao, Y.; Yang, X.; Zhang, H.; Fesik, S.; Rosenberg, S.H.; Elmore, S.W. ABT-263: A potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res. 2008, 68, 3421-3428.
116. Tsujimoto, Y.; Finger, L.R.; Yunis, J.; Nowell, P.C.; Croce, C.M. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;1 8) chromosome translocation. Science 1984, 226, 1097-1099.
117. Reed, J.C.; Stein, C.; Subasinghe, C.; Haldar, S.; Croce, C.M.; Yum, S.; Cohen, J. Antisensemediated inhibition of BCL2 protooncogene expression and leukemic cell growth and survival: comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. Cancer Res. 1990, 50, 6565-6570.
118. Hallek, M. State-of-the-art treatment of chronic lymphocytic leukemia. Hematol. Am. Soc. Hematol. Educ. Program 2009, 440-449.
119. Cole, P.D.; Zebala, J.A.; Alcaraz, M.J.; Smith, A.K.; Tan, J.; Kamen, B.A. Pharmacodynamic properties of methotrexate and Aminotrexate during weekly therapy. Cancer Chemot her. Pharmacol. 2006, 57, 826-834.
120. Wyman, C.; Kanaar, R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 2006, 40, 363-383.
121. Sinha, B.K. Topoisomerase inhibitors. A review of their therapeutic potential in cancer. Drugs 1995, 49, 11-19.
122. Nitiss, J.L. Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer 2009, 9, 338-350.
123. Champoux, J.J. DNA topoisomerases: Structure, function, and mechanism. Annu. Rev. Biochem. 2001, 70, 369-413.
124. Cragg, G.M.; Newman, D.J. A tale of two tumor targets: Topoisomerase I and tubulin. The Wall and Wani contribution to cancer chemotherapy. J. Nat. Prod. 2004, 67, 232-244.
125. Pommier, Y.; Barcelo, J.M.; Rao, V.A.; Sordet, O.; Jobson, A.G.; Thibaut, L.; Miao, Z.H.; Seiler, J.A.; Zhang, H.; Marchand, C.; Agama, K.; Nitiss, J.L.; Redon, C. Repair of topoisomerase I-mediated DNA damage. Prog. Nucl. Acid. Res. Mol. Biol. 2006, 81, 179-229.
126. Lieberman, H.B. DNA damage repair and response proteins as targets for cancer therapy. Curr. Med. Chem. 2008, 15, 360-367.
127. Ashwell, S.; Zabludoff, S. DNA damage detection and repair pathways--recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin. Cancer Res. 2008, 14, 4032-4037.
128. de Murcia, G.; Ménissier de Murcia, J. Poly(ADP-ribose) polymerase: A molecular nick-sensor. Trends Biochem. Sci. 1994, 19, 172-176.
129. Drew, Y.; Plummer, R. PARP inhibitors in cancer therapy: Two modes of attack on the cancer cell widening the clinical applications. Drug Resist. Updates 2009, 12, 153-156.
130. Canan Koch, S.S.; Thoresen, L.H.; Tikhe, J.G.; Maegley, K.A.; Almassy, R.J.; Li, J.; Yu, X.H.; Zook, S.E.; Kumpf, R.A.; Zhang, C.; Boritzki, T.J.; Mansour, R.N.; Zhang, K.E.; Ekker, A.; Calabrese, C.R.; Curtin, N.J.; Kyle, S.; Thomas, H.D.; Wang, L.Z.; Calvert, A.H.; Golding, B.T.; Griffin, R.J.; Newell, D.R.; Webber, S.E.; Hostomsky, Z. Novel tricyclic poly(ADP-ribose) polymerase-1 inhibitors with potent anticancer chemopotentiating activity: Design, synthesis, and X-ray cocrystal structure. J. Med. Chem. 2002, 45, 4961-4974.
131. Rabik, C.A.; Njoku, M.C.; Dolan, M.E. Inactivation of O6-alkylguanine DNA alkyltransferase as a means to enhance chemotherapy. Cancer Treat. Rev. 2006, 32, 261-276.
132. Dolan, M.E.; Corsico, C.D.; Pegg, A.E. Exposure of HeLa cells to 0(6)-alkylguanines increases sensitivity to the cytotoxic effects of alkylating agents. Biochem. Biophys. Res. Commun. 1985, 132, 178-185.
133. Yarosh, D.B.; Hurst-Calderone, S.; Babich, M.A.; Day, R.S. Inactivation of O6-methylguanine-DNA methyltransferase and sensitization of human tumor cells to killing by chloroethylnitrosourea by O6-methylguanine as a free base. Cancer Res. 1986, 46, 1663-1668.
134. Dolan, M.E.; Moschel, R.C.; Pegg, A.E. Depletion of mammalian O6-alkylguanine-DNA alkyltransferase activity by O6-benzylguanine provides a means to evaluate the role of this protein in protection against carcinogenic and therapeutic alkylating agents. Proc. Natl. Acad. Sci. USA 1990, 87, 5368-5372.
135. Kaina, B.; Mühlhausen, U.; Piee-Staffa, A.; Christmann, M.; Garcia Boy, R.; Rösch, F.; Schirrmacher, R. Inhibition of O6-methylguanine-DNA methyltransferase by glucose-conjugated inhibitors: comparison with nonconjugated inhibitors and effect on fotemustine and temozolomide-induced cell death. J. Pharmacol. Exp. Ther. 2004, 311, 585-593.
136. McMurry, T.B. MGMT inhibitors-The Trinity College-Paterson Institute experience, a chemist's perception. DNA Repair (Amst) 2007, 6, 1161-1169.
137. Kim, S.H.; Kaminker, P.; Campisi, J. Telomeres, aging and cancer: In search of a happy ending. Oncogene 2002, 21, 503-511.
138. Deng, Y.; Chan, S.S.; Chang, S. Telomere dysfunction and tumour suppression: The senescence connection. Nat. Rev. Cancer 2008, 8, 450-458.
139. Shay, J.W.; Bacchetti, S. A survey of telomerase activity in human cancer. Eur. J. Cancer 1997, 33, 787-791.
140. Folini, M.; Gandellini, P.; Zaffaroni, N. Targeting the telosome: Therapeutic implications. Biochim. Biophys. Acta 2009, 1792, 309-316.
141. Neidle, S. Human telomeric G-quadruplex: The current status of telomeric G-quadruplexes as therapeutic targets in human cancer. FEBS J. 2010, 277, 1118-1125.
142. Schmidt, M.; Bastians, H. Mitotic drug targets and the development of novel anti-mitotic anticancer drugs. Drug Resist. Updates 2007, 10, 162-181.
143. Harrison, M.R.; Holen, K.D.; Liu, G. Beyond taxanes: A review of novel agents that target mitotic tubulin and microtubules, kinases, and kinesins. Clin. Adv. Hematol. Oncol. 2009, 7, 54-64.
144. Gallastegui, N.; Groll, M. The 26S proteasome: Assembly and function of a destructive machine. Trends Biochem. Sci. 2010, 35, 634-642.
145. Orlowski, M.; Wilk, S. Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch. Biochem. Biophys. 2000, 383, 1-16.
146. Delic, J.; Masdehors, P.; Omura, S.; Cosset, J.M.; Dumont, J.; Binet, J.L.; Magdelénat, H. The proteasome inhibitor lactacystin induces apoptosis and sensitizes chemo-and radioresistant human chronic lymphocytic leukaemia lymphocytes to TNF-alpha-initiated apoptosis. Br. J. Cancer 1998, 77, 1103-1107.
147. Myung, J.; Kim, K.B.; Crews, C.M. The ubiquitin-proteasome pathway and proteasome inhibitors. Med. Res. Rev. 2001, 21, 245-273.
148. Hoeller, D.; Dikic, I. Targeting the ubiquitin system in cancer therapy. Nature 2009, 458, 438-444.
149. Orlowski, R.Z.; Kuhn, D.J. Proteasome inhibitors in cancer therapy: Lessons from the first decade. Clin. Cancer Res. 2008, 14, 1649-1657.
150. Kim, P.K.; Hailey, D.W.; Mullen, R.T.; Lippincott-Schwartz, J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc. Natl. Acad. Sci. USA 2008, 105, 20567-20574.
151. Lee, A.S. GRP78 induction in cancer: Therapeutic and prognostic implications. Cancer Res. 2007, 67, 3496-3499.
152. Park, H.R.; Tomida, A.; Sato, S.; Tsukumo, Y.; Yun, J.; Yamori, T.; Hayakawa, Y.; Tsuruo, T.; Shin-ya, K. Effect on tumor cells of blocking survival response to glucose deprivation. J. Natl. Cancer Inst. 2004, 96, 1300-1310.
153. Zhao, P.; Ueda, J.Y.; Kozone, I.; Chijiwa, S.; Takagi, M.; Kudo, F.; Nishiyama, M.; Shin-ya, K.; Kuzuyama, T. New glycosylated derivatives of versipelostatin, the GRP78/Bip molecular chaperone down-regulator, from Streptomyces versipellis 4083-SVS6. Org. Biomol. Chem. 2009, 7, 1454-1460.
154. Cohen, P. The role of protein phosphorylation in human health and disease. The Sir Hans Krebs Medal Lecture. Eur. J. Biochem. 2001, 268, 5001-5010.
155. Perrotti, D.; Jamieson, C.; Goldman, J.; Skorski, T. Chronic myeloid leukemia: Mechanisms of blastic transformation. J. Clin. Invest. 2010, 120, 2254-2264.
156. Giamas, G.; Man, Y.L.; Hirner, H.; Bischof, J.; Kramer, K.; Khan, K.; Ahmed, S.S.; Stebbing, J.; Knippschild, U. Kinases as targets in the treatment of solid tumors. Cell Signal 2010, 22, 984-1002.
157. Shchemelinin, I.; Sefc, L.; Necas, E. Protein kinases, their function and implication in cancer and other diseases. Folia Biol. (Praha) 2006, 52, 81-100.
158. Arora, A.; Scholar, E.M. Role of tyrosine kinase inhibitors in cancer therapy. J. Pharmacol. Exp. Ther. 2005, 315, 971-979.
159. Janeway, K.A.; Albritton, K.H.; Van Den Abbeele, A.D.; D'Amato, G.Z.; Pedrazzoli, P.; Siena, S.; Picus, J.; Butrynski, J.E.; Schlemmer, M.; Heinrich, M.C.; Demetri, G.D. Sunitinib treatment in pediatric patients with advanced GIST following failure of imatinib. Pediatr. Blood Cancer 2009, 52, 767-771.
160. Wang, C.M.; Huang, K.; Zhou, Y.; Du, C.Y.; Ye, Y.W.; Fu, H.; Zhou, X.Y.; Shi, Y.Q. Molecular mechanisms of secondary imatinib resistance in patients with gastrointestinal stromal tumors. J. Cancer Res. Clin. Oncol. 2010, 136, 1065-1071.
161. Gorre, M.E.; Mohammed, M.; Ellwood, K.; Hsu, N.; Paquette, R.; Rao, P.N.; Sawyers, C.L. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001, 293, 876-880.
162. Jarkowski, A.; Sweeney, R.P. Nilotinib: A new tyrosine kinase inhibitor for the treatment of chronic myelogenous leukemia. Pharmacotherapy 2008, 28, 1374-1382.
163. Gautschi, O.; Heighway, J.; Mack, P.C.; Purnell, P.R.; Lara, P.N.; Gandara, D.R. Aurora kinases as anticancer drug targets. Clin. Cancer Res. 2008, 14, 1639-1648.
164. Yuan, R.; Kay, A.; Berg, W.J.; Lebwohl, D. Targeting tumorigenesis: Development and use of mTOR inhibitors in cancer therapy. J. Hematol. Oncol. 2009, 2, 45.
165. Sehgal, S.N.; Baker, H.; Vézina, C. Rapamycin (AY-22,989), a new antifungal antibiotic. II. Fermentation, isolation and characterization. J. Antibiot. (Tokyo) 1975, 28, 727-732.
166. Hay, N.; Sonenberg, N. Upstream and downstream of mTOR. Genes Dev. 2004, 18, 1926-1945.
167. Mannhold, R.; Fulda, S.; Carosati, E. IAP antagonists: Promising candidates for cancer therapy. Drug Discov. Today 2010, 15, 210-219.
168. De Duve, C.; Pressman, B.C.; Gianetto, R.; Wattiaux, R.; Appelmans, F. Tissue fractionation studies. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem. J. 1955, 60, 604-617.
169. Lübke, T.; Lobel, P.; Sleat, D.E. Proteomics of the lysosome. Biochim. Biophys. Acta 2009, 1793, 625-635.
170. Groth-Pedersen, L.; Jäättelä, M. Combating apoptosis and multidrug resistant cancers by targeting lysosomes. Cancer Lett. 2010, in press.
171. Warburg, O. On respiratory impairment in cancer cells. Science 1956, 124, 269-270.
172. Hockenbery, D.M. Targeting mitochondria for cancer therapy. Environ. Mol. Mutagen. 2010, 51, 476-489.
173. Ralph, S.J.; Rodríguez-Enríquez, S.; Neuzil, J.; Saavedra, E.; Moreno-Sánchez, R. The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation-why mitochondria are targets for cancer therapy. Mol. Aspects Med. 2010, 31, 145-170.