Targeting Cell Survival Proteins for Cancer Cell Death
Abstract
:1. Introduction
1.1. Bcl-2 Family
1.1.1. Bcl-2
1.1.2. Bcl-xL
1.1.3. Mcl-1
1.1.4. Pro-Apoptotic Proteins
1.2. IAP Family
1.2.1. Class 1 IAPs
1.2.2. Class 2 IAPs
1.2.3. Class 3 IAPs
1.3. HSP Family
2. Inhibitors of Survival Proteins
2.1. Inhibitors of Bcl-2 Proteins
2.1.1. Peptide-Based Inhibitors
2.1.2. ASOs
2.1.3. Small-Molecule Inhibitors
2.2. Inhibitors of IAP Family Proteins
2.2.1. Selective IAP Inhibitors
2.2.2. Inhibitors Mimicking SMAC
2.2.3. SMAC-Derived Peptides
2.3. Inhibitors of Hsp90
2.3.1. Derivatives of Geldanamycin
2.3.2. Resorcinol and Its Derivatives
2.3.3. Purine-Based Inhibitors
2.4. Natural Agents as Survival Protein Inhibitors
3. Conclusions and Perspectives
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Tsujimoto, Y.; Cossman, J.; Jaffe, E.; Croce, C.M. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985, 228, 1440–1443. [Google Scholar] [CrossRef] [PubMed]
- Reed, J.C.; Pellecchia, M. Apoptosis-based therapies for hematologic malignancies. Blood 2005, 106, 408–418. [Google Scholar] [CrossRef] [PubMed]
- Packham, G.; Stevenson, F.K. Bodyguards and assassins: Bcl-2 family proteins and apoptosis control in chronic lymphocytic leukaemia. Immunology 2005, 114, 441–449. [Google Scholar] [CrossRef] [PubMed]
- Kang, M.H.; Reynolds, C.P. Bcl-2 inhibitors: Targeting mitochondrial apoptotic pathways in cancer therapy. Clin. Cancer Res. 2009, 15, 1126–1132. [Google Scholar] [CrossRef] [PubMed]
- Reed, J.C. Apoptosis-based therapies. Nat. Rev. Drug Discov. 2002, 1, 111–121. [Google Scholar] [CrossRef] [PubMed]
- Thomas, S.; Quinn, B.A.; Das, S.K.; Dash, R.; Emdad, L.; Dasgupta, S.; Wang, X.Y.; Dent, P.; Reed, J.C.; Pellecchia, M.; et al. Targeting the bcl-2 family for cancer therapy. Expert Opin. Ther. Targets 2013, 17, 61–75. [Google Scholar] [CrossRef] [PubMed]
- Reed, J.C. Bcl-2-family proteins and hematologic malignancies: History and future prospects. Blood 2008, 111, 3322–3330. [Google Scholar] [CrossRef] [PubMed]
- Sinicrope, F.A.; Hart, J.; Michelassi, F.; Lee, J.J. Prognostic value of bcl-2 oncoprotein expression in stage II colon carcinoma. Clin. Cancer Res. 1995, 1, 1103–1110. [Google Scholar] [PubMed]
- Jiang, S.X.; Sato, Y.; Kuwao, S.; Kameya, T. Expression of bcl-2 oncogene protein is prevalent in small cell lung carcinomas. J. Pathol. 1995, 177, 135–138. [Google Scholar] [CrossRef] [PubMed]
- McDonnell, T.J.; Troncoso, P.; Brisbay, S.M.; Logothetis, C.; Chung, L.W.; Hsieh, J.T.; Tu, S.M.; Campbell, M.L. Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res. 1992, 52, 6940–6944. [Google Scholar] [PubMed]
- Joensuu, H.; Pylkkanen, L.; Toikkanen, S. Bcl-2 protein expression and long-term survival in breast cancer. Am. J. Pathol. 1994, 145, 1191–1198. [Google Scholar] [PubMed]
- Campos, L.; Rouault, J.P.; Sabido, O.; Oriol, P.; Roubi, N.; Vasselon, C.; Archimbaud, E.; Magaud, J.P.; Guyotat, D. High expression of bcl-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Blood 1993, 81, 3091–3096. [Google Scholar] [PubMed]
- Hermine, O.; Haioun, C.; Lepage, E.; d’Agay, M.F.; Briere, J.; Lavignac, C.; Fillet, G.; Salles, G.; Marolleau, J.P.; Diebold, J.; et al. Prognostic significance of bcl-2 protein expression in aggressive non-hodgkin’s lymphoma. Groupe d’etude des lymphomes de l’adulte (gela). Blood 1996, 87, 265–272. [Google Scholar] [PubMed]
- Grover, R.; Wilson, G.D. Bcl-2 expression in malignant melanoma and its prognostic significance. Eur. J. Surg. Oncol. 1996, 22, 347–349. [Google Scholar] [CrossRef]
- Weller, M.; Malipiero, U.; Aguzzi, A.; Reed, J.C.; Fontana, A. Protooncogene bcl-2 gene transfer abrogates Fas/APO-1 antibody-mediated apoptosis of human malignant glioma cells and confers resistance to chemotherapeutic drugs and therapeutic irradiation. J. Clin. Investig. 1995, 95, 2633–2643. [Google Scholar] [CrossRef] [PubMed]
- Cimmino, A.; Calin, G.A.; Fabbri, M.; Iorio, M.V.; Ferracin, M.; Shimizu, M.; Wojcik, S.E.; Aqeilan, R.I.; Zupo, S.; Dono, M.; et al. Mir-15 and mir-16 induce apoptosis by targeting bcl2. Proc. Natl. Acad. Sci. USA 2005, 102, 13944–13949. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; Saini, N. Downregulation of bcl2 by mirnas augments drug-induced apoptosis—a combined computational and experimental approach. J. Cell Sci. 2012, 125, 1568–1578. [Google Scholar] [CrossRef] [PubMed]
- Rao, P.H.; Houldsworth, J.; Dyomina, K.; Parsa, N.Z.; Cigudosa, J.C.; Louie, D.C.; Popplewell, L.; Offit, K.; Jhanwar, S.C.; Chaganti, R.S. Chromosomal and gene amplification in diffuse large b-cell lymphoma. Blood 1998, 92, 234–240. [Google Scholar] [PubMed]
- Hanada, M.; Delia, D.; Aiello, A.; Stadtmauer, E.; Reed, J.C. Bcl-2 gene hypomethylation and high-level expression in B-cell chronic lymphocytic leukemia. Blood 1993, 82, 1820–1828. [Google Scholar] [PubMed]
- Yano, T.; Jaffe, E.S.; Longo, D.L.; Raffeld, M. Myc rearrangements in histologically progressed follicular lymphomas. Blood 1992, 80, 758–767. [Google Scholar] [PubMed]
- Strasser, A.; Harris, A.W.; Bath, M.L.; Cory, S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 1990, 348, 331–333. [Google Scholar] [CrossRef] [PubMed]
- Strasser, A.; Elefanty, A.G.; Harris, A.W.; Cory, S. Progenitor tumours from Emu-bcl-2-myc transgenic mice have lymphomyeloid differentiation potential and reveal developmental differences in cell survival. EMBO J. 1996, 15, 3823–3834. [Google Scholar] [PubMed]
- Jager, R.; Herzer, U.; Schenkel, J.; Weiher, H. Overexpression of Bcl-2 inhibits alveolar cell apoptosis during involution and accelerates c-myc-induced tumorigenesis of the mammary gland in transgenic mice. Oncogene 1997, 15, 1787–1795. [Google Scholar] [CrossRef] [PubMed]
- Naik, P.; Karrim, J.; Hanahan, D. The rise and fall of apoptosis during multistage tumorigenesis: Down-modulation contributes to tumor progression from angiogenic progenitors. Genes Dev. 1996, 10, 2105–2116. [Google Scholar] [CrossRef] [PubMed]
- Boise, L.H.; Gonzalez-Garcia, M.; Postema, C.E.; Ding, L.; Lindsten, T.; Turka, L.A.; Mao, X.; Nunez, G.; Thompson, C.B. Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993, 74, 597–608. [Google Scholar] [CrossRef]
- Kirsh, E.J.; Baunoch, D.A.; Stadler, W.M. Expression of bcl-2 and bcl-x in bladder cancer. J. Urol. 1998, 159, 1348–1353. [Google Scholar] [CrossRef]
- Castilla, C.; Congregado, B.; Chinchon, D.; Torrubia, F.J.; Japon, M.A.; Saez, C. Bcl-xl is overexpressed in hormone-resistant prostate cancer and promotes survival of lncap cells via interaction with proapoptotic bak. Endocrinology 2006, 147, 4960–4967. [Google Scholar] [CrossRef] [PubMed]
- Kozopas, K.M.; Yang, T.; Buchan, H.L.; Zhou, P.; Craig, R.W. Mcl1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to bcl2. Proc. Natl. Acad. Sci. USA 1993, 90, 3516–3520. [Google Scholar] [CrossRef] [PubMed]
- Day, C.L.; Smits, C.; Fan, F.C.; Lee, E.F.; Fairlie, W.D.; Hinds, M.G. Structure of the BH3 domains from the p53-inducible BH3-only proteins Noxa and Puma in complex with mcl-1. J. Mol. Biol. 2008, 380, 958–971. [Google Scholar] [CrossRef] [PubMed]
- Rinkenberger, J.L.; Horning, S.; Klocke, B.; Roth, K.; Korsmeyer, S.J. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 2000, 14, 23–27. [Google Scholar] [PubMed]
- Opferman, J.T.; Iwasaki, H.; Ong, C.C.; Suh, H.; Mizuno, S.; Akashi, K.; Korsmeyer, S.J. Obligate role of anti-apoptotic mcl-1 in the survival of hematopoietic stem cells. Science 2005, 307, 1101–1104. [Google Scholar] [CrossRef] [PubMed]
- Opferman, J.T.; Letai, A.; Beard, C.; Sorcinelli, M.D.; Ong, C.C.; Korsmeyer, S.J. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003, 426, 671–676. [Google Scholar] [CrossRef] [PubMed]
- Arbour, N.; Vanderluit, J.L.; Le Grand, J.N.; Jahani-Asl, A.; Ruzhynsky, V.A.; Cheung, E.C.; Kelly, M.A.; MacKenzie, A.E.; Park, D.S.; Opferman, J.T.; et al. Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J. Neurosci. 2008, 28, 6068–6078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perciavalle, R.M.; Opferman, J.T. Delving deeper: Mcl-1’s contributions to normal and cancer biology. Trends Cell Biol. 2013, 23, 22–29. [Google Scholar] [CrossRef] [PubMed]
- Beroukhim, R.; Mermel, C.H.; Porter, D.; Wei, G.; Raychaudhuri, S.; Donovan, J.; Barretina, J.; Boehm, J.S.; Dobson, J.; Urashima, M.; et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463, 899–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Glaser, S.P.; Lee, E.F.; Trounson, E.; Bouillet, P.; Wei, A.; Fairlie, W.D.; Izon, D.J.; Zuber, J.; Rappaport, A.R.; Herold, M.J.; et al. Anti-apoptotic mcl-1 is essential for the development and sustained growth of acute myeloid leukemia. Genes Dev. 2012, 26, 120–125. [Google Scholar] [CrossRef] [PubMed]
- Wei, L.H.; Kuo, M.L.; Chen, C.A.; Chou, C.H.; Cheng, W.F.; Chang, M.C.; Su, J.L.; Hsieh, C.Y. The anti-apoptotic role of interleukin-6 in human cervical cancer is mediated by up-regulation of mcl-1 through a pi 3-k/akt pathway. Oncogene 2001, 20, 5799–5809. [Google Scholar] [CrossRef] [PubMed]
- Shigemasa, K.; Katoh, O.; Shiroyama, Y.; Mihara, S.; Mukai, K.; Nagai, N.; Ohama, K. Increased mcl-1 expression is associated with poor prognosis in ovarian carcinomas. Jpn. J. Cancer Res. 2002, 93, 542–550. [Google Scholar] [CrossRef] [PubMed]
- Stewart, D.P.; Koss, B.; Bathina, M.; Perciavalle, R.M.; Bisanz, K.; Opferman, J.T. Ubiquitin-independent degradation of antiapoptotic mcl-1. Mol. Cell. Biol. 2010, 30, 3099–3110. [Google Scholar] [CrossRef] [PubMed]
- Zhong, Q.; Gao, W.; Du, F.; Wang, X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of mcl-1 and regulates apoptosis. Cell 2005, 121, 1085–1095. [Google Scholar] [CrossRef] [PubMed]
- Schwickart, M.; Huang, X.; Lill, J.R.; Liu, J.; Ferrando, R.; French, D.M.; Maecker, H.; O’Rourke, K.; Bazan, F.; Eastham-Anderson, J.; et al. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 2010, 463, 103–107. [Google Scholar] [CrossRef] [PubMed]
- Inuzuka, H.; Shaik, S.; Onoyama, I.; Gao, D.; Tseng, A.; Maser, R.S.; Zhai, B.; Wan, L.; Gutierrez, A.; Lau, A.W.; et al. SCFFBW7 regulates cellular apoptosis by targeting MCL1 for ubiquitylation and destruction. Nature 2011, 471, 104–109. [Google Scholar] [CrossRef] [PubMed]
- Rampino, N.; Yamamoto, H.; Ionov, Y.; Li, Y.; Sawai, H.; Reed, J.C.; Perucho, M. Somatic frameshift mutations in the bax gene in colon cancers of the microsatellite mutator phenotype. Science 1997, 275, 967–969. [Google Scholar] [CrossRef] [PubMed]
- Meijerink, J.P.; Raemaekers, J.M.; Mensink, E.J. New type of t(14;18) in a non-Hodgkin’s lymphoma provides insight in molecular events in early B-cell differentiation. Br. J. Haematol. 1995, 91, 630–639. [Google Scholar] [CrossRef] [PubMed]
- Shibue, T.; Takeda, K.; Oda, E.; Tanaka, H.; Murasawa, H.; Takaoka, A.; Morishita, Y.; Akira, S.; Taniguchi, T.; Tanaka, N. Integral role of Noxa in p53-mediated apoptotic response. Genes Dev. 2003, 17, 2233–2238. [Google Scholar] [CrossRef] [PubMed]
- Nakano, K.; Vousden, K.H. Puma, a novel proapoptotic gene, is induced by p53. Mol. Cell 2001, 7, 683–694. [Google Scholar] [CrossRef]
- Fulda, S.; Vucic, D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 2012, 11, 109–124. [Google Scholar] [CrossRef] [PubMed]
- Birnbaum, M.J.; Clem, R.J.; Miller, L.K. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with cys/his sequence motifs. J. Virol. 1994, 68, 2521–2528. [Google Scholar] [PubMed]
- Crook, N.E.; Clem, R.J.; Miller, L.K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 1993, 67, 2168–2174. [Google Scholar] [PubMed]
- Salvesen, G.S.; Duckett, C.S. IAP proteins: Blocking the road to death’s door. Nat. Rev. Mol. Cell Biol. 2002, 3, 401–410. [Google Scholar] [CrossRef] [PubMed]
- Sanna, M.G.; da Silva Correia, J.; Ducrey, O.; Lee, J.; Nomoto, K.; Schrantz, N.; Deveraux, Q.L.; Ulevitch, R.J. IAP suppression of apoptosis involves distinct mechanisms: The TAK1/JNK1 signaling cascade and caspase inhibition. Mol. Cell. Biol. 2002, 22, 1754–1766. [Google Scholar] [CrossRef] [PubMed]
- Hofer-Warbinek, R.; Schmid, J.A.; Stehlik, C.; Binder, B.R.; Lipp, J.; de Martin, R. Activation of NF-κb by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J. Biol. Chem. 2000, 275, 22064–22068. [Google Scholar] [CrossRef] [PubMed]
- Levkau, B.; Garton, K.J.; Ferri, N.; Kloke, K.; Nofer, J.R.; Baba, H.A.; Raines, E.W.; Breithardt, G. XIAP induces cell-cycle arrest and activates nuclear factor-κb: New survival pathways disabled by caspase-mediated cleavage during apoptosis of human endothelial cells. Circ. Res. 2001, 88, 282–290. [Google Scholar] [CrossRef] [PubMed]
- Varfolomeev, E.; Vucic, D. (Un)expected roles of c-IAPs in apoptotic and nfkappab signaling pathways. Cell Cycle 2008, 7, 1511–1521. [Google Scholar] [CrossRef] [PubMed]
- Vaux, D.L.; Silke, J. Iaps, rings and ubiquitylation. Nat. Rev. Mol. Cell. Biol. 2005, 6, 287–297. [Google Scholar] [CrossRef] [PubMed]
- Schimmer, A.D. Inhibitor of apoptosis proteins: Translating basic knowledge into clinical practice. Cancer Res. 2004, 64, 7183–7190. [Google Scholar] [CrossRef] [PubMed]
- Duckett, C.S.; Nava, V.E.; Gedrich, R.W.; Clem, R.J.; Van Dongen, J.L.; Gilfillan, M.C.; Shiels, H.; Hardwick, J.M.; Thompson, C.B. A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J. 1996, 15, 2685–2694. [Google Scholar] [PubMed]
- Deveraux, Q.L.; Leo, E.; Stennicke, H.R.; Welsh, K.; Salvesen, G.S.; Reed, J.C. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J. 1999, 18, 5242–5251. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Vucic, D.; Stennicke, H.R.; Pisabarro, M.T.; Salvesen, G.S.; Dixit, V.M. Ml-IAP, a novel inhibitor of apoptosis that is preferentially expressed in human melanomas. Curr. Biol. 2000, 10, 1359–1366. [Google Scholar] [CrossRef]
- Richter, B.W.; Mir, S.S.; Eiben, L.J.; Lewis, J.; Reffey, S.B.; Frattini, A.; Tian, L.; Frank, S.; Youle, R.J.; Nelson, D.L.; et al. Molecular cloning of ILP-2, a novel member of the inhibitor of apoptosis protein family. Mol. Cell. Biol. 2001, 21, 4292–4301. [Google Scholar] [CrossRef] [PubMed]
- Roy, N.; Mahadevan, M.S.; McLean, M.; Shutler, G.; Yaraghi, Z.; Farahani, R.; Baird, S.; Besner-Johnston, A.; Lefebvre, C.; Kang, X.; et al. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 1995, 80, 167–178. [Google Scholar] [CrossRef]
- Maier, J.K.; Lahoua, Z.; Gendron, N.H.; Fetni, R.; Johnston, A.; Davoodi, J.; Rasper, D.; Roy, S.; Slack, R.S.; Nicholson, D.W.; et al. The neuronal apoptosis inhibitory protein is a direct inhibitor of caspases 3 and 7. J. Neurosci. 2002, 22, 2035–2043. [Google Scholar] [PubMed]
- Tanaka, K.; Iwamoto, S.; Gon, G.; Nohara, T.; Iwamoto, M.; Tanigawa, N. Expression of survivin and its relationship to loss of apoptosis in breast carcinomas. Clin. Cancer Res. 2000, 6, 127–134. [Google Scholar] [PubMed]
- Gianani, R.; Jarboe, E.; Orlicky, D.; Frost, M.; Bobak, J.; Lehner, R.; Shroyer, K.R. Expression of survivin in normal, hyperplastic, and neoplastic colonic mucosa. Hum. Pathol. 2001, 32, 119–125. [Google Scholar] [CrossRef] [PubMed]
- Sarela, A.I.; Macadam, R.C.; Farmery, S.M.; Markham, A.F.; Guillou, P.J. Expression of the antiapoptosis gene, survivin, predicts death from recurrent colorectal carcinoma. Gut 2000, 46, 645–650. [Google Scholar] [CrossRef] [PubMed]
- Grabowski, P.; Kuhnel, T.; Muhr-Wilkenshoff, F.; Heine, B.; Stein, H.; Hopfner, M.; Germer, C.T.; Scherubl, H. Prognostic value of nuclear survivin expression in oesophageal squamous cell carcinoma. Br. J. Cancer 2003, 88, 115–119. [Google Scholar] [CrossRef] [PubMed]
- Ambrosini, G.; Adida, C.; Altieri, D.C. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med. 1997, 3, 917–921. [Google Scholar] [CrossRef] [PubMed]
- Powers, M.V.; Workman, P. Inhibitors of the heat shock response: Biology and pharmacology. FEBS Lett. 2007, 581, 3758–3769. [Google Scholar] [CrossRef] [PubMed]
- Young, J.C.; Agashe, V.R.; Siegers, K.; Hartl, F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 2004, 5, 781–791. [Google Scholar] [CrossRef] [PubMed]
- Scaltriti, M.; Dawood, S.; Cortes, J. Molecular pathways: Targeting hsp90--who benefits and who does not. Clin. Cancer Res. 2012, 18, 4508–4513. [Google Scholar] [CrossRef] [PubMed]
- Banerji, U. Heat shock protein 90 as a drug target: Some like it hot. Clin. Cancer Res. 2009, 15, 9–14. [Google Scholar] [CrossRef] [PubMed]
- Whitesell, L.; Lindquist, S.L. Hsp90 and the chaperoning of cancer. Nat. Rev. Cancer 2005, 5, 761–772. [Google Scholar] [CrossRef] [PubMed]
- Pick, E.; Kluger, Y.; Giltnane, J.M.; Moeder, C.; Camp, R.L.; Rimm, D.L.; Kluger, H.M. High hsp90 expression is associated with decreased survival in breast cancer. Cancer Res. 2007, 67, 2932–2937. [Google Scholar] [CrossRef] [PubMed]
- Conroy, S.E.; Latchman, D.S. Do heat shock proteins have a role in breast cancer? Br. J. Cancer 1996, 74, 717–721. [Google Scholar] [CrossRef] [PubMed]
- Taipale, M.; Jarosz, D.F.; Lindquist, S. Hsp90 at the hub of protein homeostasis: Emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11, 515–528. [Google Scholar] [CrossRef] [PubMed]
- Biamonte, M.A.; Van de Water, R.; Arndt, J.W.; Scannevin, R.H.; Perret, D.; Lee, W.C. Heat shock protein 90: Inhibitors in clinical trials. J. Med. Chem. 2010, 53, 3–17. [Google Scholar] [CrossRef] [PubMed]
- Neckers, L.; Workman, P. Hsp90 molecular chaperone inhibitors: Are we there yet? Clin. Cancer Res. 2012, 18, 64–76. [Google Scholar] [CrossRef] [PubMed]
- Sattler, M.; Liang, H.; Nettesheim, D.; Meadows, R.P.; Harlan, J.E.; Eberstadt, M.; Yoon, H.S.; Shuker, S.B.; Chang, B.S.; Minn, A.J.; et al. Structure of bcl-xl-bak peptide complex: Recognition between regulators of apoptosis. Science 1997, 275, 983–986. [Google Scholar] [CrossRef] [PubMed]
- Willis, S.N.; Chen, L.; Dewson, G.; Wei, A.; Naik, E.; Fletcher, J.I.; Adams, J.M.; Huang, D.C. Proapoptotic bak is sequestered by mcl-1 and bcl-xl, but not bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005, 19, 1294–1305. [Google Scholar] [CrossRef] [PubMed]
- Kolluri, S.K.; Zhu, X.; Zhou, X.; Lin, B.; Chen, Y.; Sun, K.; Tian, X.; Town, J.; Cao, X.; Lin, F.; et al. A short nur77-derived peptide converts bcl-2 from a protector to a killer. Cancer Cell 2008, 14, 285–298. [Google Scholar] [CrossRef] [PubMed]
- LaBelle, J.L.; Katz, S.G.; Bird, G.H.; Gavathiotis, E.; Stewart, M.L.; Lawrence, C.; Fisher, J.K.; Godes, M.; Pitter, K.; Kung, A.L.; et al. A stapled bim peptide overcomes apoptotic resistance in hematologic cancers. J. Clin. Investig. 2012, 122, 2018–2031. [Google Scholar] [CrossRef] [PubMed]
- Reed, J.C.; Stein, C.; Subasinghe, C.; Haldar, S.; Croce, C.M.; Yum, S.; Cohen, J. Antisense-mediated inhibition of bcl2 protooncogene expression and leukemic cell growth and survival: Comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. Cancer Res. 1990, 50, 6565–6570. [Google Scholar] [PubMed]
- Olie, R.A.; Zangemeister-Wittke, U. Targeting tumor cell resistance to apoptosis induction with antisense oligonucleotides: Progress and therapeutic potential. Drug Resist. Updates 2001, 4, 9–15. [Google Scholar] [CrossRef] [PubMed]
- O’Brien, S.; Moore, J.O.; Boyd, T.E.; Larratt, L.M.; Skotnicki, A.B.; Koziner, B.; Chanan-Khan, A.A.; Seymour, J.F.; Gribben, J.; Itri, L.M.; et al. 5-year survival in patients with relapsed or refractory chronic lymphocytic leukemia in a randomized, phase III trial of fludarabine plus cyclophosphamide with or without oblimersen. J. Clin. Oncol. 2009, 27, 5208–5212. [Google Scholar] [CrossRef] [PubMed]
- Bedikian, A.Y.; Millward, M.; Pehamberger, H.; Conry, R.; Gore, M.; Trefzer, U.; Pavlick, A.C.; DeConti, R.; Hersh, E.M.; Hersey, P.; et al. Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: The oblimersen melanoma study group. J. Clin. Oncol. 2006, 24, 4738–4745. [Google Scholar] [CrossRef] [PubMed]
- Zangemeister-Wittke, U.; Leech, S.H.; Olie, R.A.; Simoes-Wust, A.P.; Gautschi, O.; Luedke, G.H.; Natt, F.; Haner, R.; Martin, P.; Hall, J.; et al. A novel bispecific antisense oligonucleotide inhibiting both bcl-2 and bcl-xl expression efficiently induces apoptosis in tumor cells. Clin. Cancer Res. 2000, 6, 2547–2555. [Google Scholar] [PubMed]
- Sieghart, W.; Losert, D.; Strommer, S.; Cejka, D.; Schmid, K.; Rasoul-Rockenschaub, S.; Bodingbauer, M.; Crevenna, R.; Monia, B.P.; Peck-Radosavljevic, M.; et al. Mcl-1 overexpression in hepatocellular carcinoma: A potential target for antisense therapy. J. Hepatol. 2006, 44, 151–157. [Google Scholar] [CrossRef] [PubMed]
- Dean, N.M.; Bennett, C.F. Antisense oligonucleotide-based therapeutics for cancer. Oncogene 2003, 22, 9087–9096. [Google Scholar] [CrossRef] [PubMed]
- Doi, K.; Li, R.; Sung, S.S.; Wu, H.; Liu, Y.; Manieri, W.; Krishnegowda, G.; Awwad, A.; Dewey, A.; Liu, X.; et al. Discovery of marinopyrrole A (maritoclax) as a selective Mcl-1 antagonist that overcomes ABT-737 resistance by binding to and targeting Mcl-1 for proteasomal degradation. J. Biol. Chem. 2012, 287, 10224–10235. [Google Scholar] [CrossRef]
- Pandey, M.K.; Gowda, K.; Doi, K.; Sharma, A.K.; Wang, H.G.; Amin, S. Proteasomal degradation of Mcl-1 by maritoclax induces apoptosis and enhances the efficacy of ABT-737 in melanoma cells. PLoS ONE 2013, 8. [Google Scholar] [CrossRef]
- Tzung, S.P.; Kim, K.M.; Basanez, G.; Giedt, C.D.; Simon, J.; Zimmerberg, J.; Zhang, K.Y.; Hockenbery, D.M. Antimycin a mimics a cell-death-inducing bcl-2 homology domain 3. Nat. Cell Biol. 2001, 3, 183–191. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Witham, J.; Valenti, M.R.; De-Haven-Brandon, A.K.; Vidot, S.; Eccles, S.A.; Kaye, S.B.; Richardson, A. The bcl-2/bcl-xl family inhibitor ABT-737 sensitizes ovarian cancer cells to carboplatin. Clin. Cancer Res. 2007, 13, 7191–7198. [Google Scholar] [CrossRef] [PubMed]
- Hikita, H.; Takehara, T.; Shimizu, S.; Kodama, T.; Shigekawa, M.; Iwase, K.; Hosui, A.; Miyagi, T.; Tatsumi, T.; Ishida, H.; et al. The bcl-xl inhibitor, ABT-737, efficiently induces apoptosis and suppresses growth of hepatoma cells in combination with sorafenib. Hepatology 2010, 52, 1310–1321. [Google Scholar] [CrossRef] [PubMed]
- Hann, C.L.; Daniel, V.C.; Sugar, E.A.; Dobromilskaya, I.; Murphy, S.C.; Cope, L.; Lin, X.; Hierman, J.S.; Wilburn, D.L.; Watkins, D.N.; et al. Therapeutic efficacy of ABT-737, a selective inhibitor of bcl-2, in small cell lung cancer. Cancer Res. 2008, 68, 2321–2328. [Google Scholar] [CrossRef] [PubMed]
- 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.; et al. An inhibitor of bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435, 677–681. [Google Scholar] [CrossRef] [PubMed]
- Roberts, A.W.; Seymour, J.F.; Brown, J.R.; Wierda, W.G.; Kipps, T.J.; Khaw, S.L.; Carney, D.A.; He, S.Z.; Huang, D.C.; Xiong, H.; et al. Substantial susceptibility of chronic lymphocytic leukemia to bcl2 inhibition: Results of a phase I study of navitoclax in patients with relapsed or refractory disease. J. Clin. Oncol. 2012, 30, 488–496. [Google Scholar] [CrossRef] [PubMed]
- Wilson, W.H.; O’Connor, O.A.; Czuczman, M.S.; LaCasce, A.S.; Gerecitano, J.F.; Leonard, J.P.; Tulpule, A.; Dunleavy, K.; Xiong, H.; Chiu, Y.L.; et al. Navitoclax, a targeted high-affinity inhibitor of bcl-2, in lymphoid malignancies: A phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol. 2010, 11, 1149–1159. [Google Scholar] [CrossRef]
- Billard, C. BH3 mimetics: Status of the field and new developments. Mol. Cancer Ther. 2013, 12, 1691–1700. [Google Scholar] [CrossRef] [PubMed]
- Yecies, D.; Carlson, N.E.; Deng, J.; Letai, A. Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood 2010, 115, 3304–3313. [Google Scholar] [CrossRef] [PubMed]
- Van Delft, M.F.; Wei, A.H.; Mason, K.D.; Vandenberg, C.J.; Chen, L.; Czabotar, P.E.; Willis, S.N.; Scott, C.L.; Day, C.L.; Cory, S.; et al. The BH3 mimetic ABT-737 targets selective bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if mcl-1 is neutralized. Cancer Cell 2006, 10, 389–399. [Google Scholar] [CrossRef]
- Lucas, K.M.; Mohana-Kumaran, N.; Lau, D.; Zhang, X.D.; Hersey, P.; Huang, D.C.; Weninger, W.; Haass, N.K.; Allen, J.D. Modulation of Noxa and mcl-1 as a strategy for sensitizing melanoma cells to the BH3-mimetic ABT-737. Clin. Cancer Res. 2012, 18, 783–795. [Google Scholar] [CrossRef] [PubMed]
- Smoot, R.L.; Blechacz, B.R.; Werneburg, N.W.; Bronk, S.F.; Sinicrope, F.A.; Sirica, A.E.; Gores, G.J. A Bax-mediated mechanism for obatoclax-induced apoptosis of cholangiocarcinoma cells. Cancer Res. 2010, 70, 1960–1969. [Google Scholar] [CrossRef] [PubMed]
- Konopleva, M.; Watt, J.; Contractor, R.; Tsao, T.; Harris, D.; Estrov, Z.; Bornmann, W.; Kantarjian, H.; Viallet, J.; Samudio, I.; et al. Mechanisms of antileukemic activity of the novel bcl-2 homology domain-3 mimetic GX15–070 (obatoclax). Cancer Res. 2008, 68, 3413–3420. [Google Scholar] [CrossRef] [PubMed]
- Pan, J.; Cheng, C.; Verstovsek, S.; Chen, Q.; Jin, Y.; Cao, Q. The BH3-mimetic GX15–070 induces autophagy, potentiates the cytotoxicity of carboplatin and 5-fluorouracil in esophageal carcinoma cells. Cancer Lett. 2010, 293, 167–174. [Google Scholar] [CrossRef]
- Joudeh, J.; Claxton, D. Obatoclax mesylate : Pharmacology and potential for therapy of hematological neoplasms. Expert Opin. Investig. Drugs 2012, 21, 363–373. [Google Scholar] [CrossRef] [PubMed]
- Hwang, J.J.; Kuruvilla, J.; Mendelson, D.; Pishvaian, M.J.; Deeken, J.F.; Siu, L.L.; Berger, M.S.; Viallet, J.; Marshall, J.L. Phase I dose finding studies of obatoclax (GX15–070), a small molecule pan-bcl-2 family antagonist, in patients with advanced solid tumors or lymphoma. Clin. Cancer Res. 2010, 16, 4038–4045. [Google Scholar] [CrossRef] [PubMed]
- Hughes, C.C.; Prieto-Davo, A.; Jensen, P.R.; Fenical, W. The marinopyrroles, antibiotics of an unprecedented structure class from a marine Streptomyces sp. Org. Lett. 2008, 10, 629–631. [Google Scholar] [CrossRef] [PubMed]
- Doi, K.; Liu, Q.; Gowda, K.; Barth, B.M.; Claxton, D.; Amin, S.; Loughran, T.P., Jr.; Wang, H.G. Maritoclax induces apoptosis in acute myeloid leukemia cells with elevated mcl-1 expression. Cancer Biol. Ther. 2014, 15. [Google Scholar] [CrossRef] [PubMed]
- Wei, J.; Kitada, S.; Stebbins, J.L.; Placzek, W.; Zhai, D.; Wu, B.; Rega, M.F.; Zhang, Z.; Cellitti, J.; Yang, L.; et al. Synthesis and biological evaluation of apogossypolone derivatives as pan-active inhibitors of antiapoptotic B-cell lymphoma/leukemia-2 (bcl-2) family proteins. J. Med. Chem. 2010, 53, 8000–8011. [Google Scholar] [CrossRef] [PubMed]
- Baggstrom, M.Q.; Qi, Y.; Koczywas, M.; Argiris, A.; Johnson, E.A.; Millward, M.J.; Murphy, S.C.; Erlichman, C.; Rudin, C.M.; Govindan, R. A phase II study of AT-101 (gossypol) in chemotherapy-sensitive recurrent extensive-stage small cell lung cancer. J. Thorac. Oncol. 2011, 6, 1757–1760. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Song, W.; Aboukameel, A.; Mohammad, M.; Wang, G.; Banerjee, S.; Kong, D.; Wang, S.; Sarkar, F.H.; Mohammad, R.M. Tw-37, a small-molecule inhibitor of bcl-2, inhibits cell growth and invasion in pancreatic cancer. Int. J. Cancer 2008, 123, 958–966. [Google Scholar] [CrossRef] [PubMed]
- Mohammad, R.M.; Goustin, A.S.; Aboukameel, A.; Chen, B.; Banerjee, S.; Wang, G.; Nikolovska-Coleska, Z.; Wang, S.; Al-Katib, A. Preclinical studies of TW-37, a new nonpeptidic small-molecule inhibitor of bcl-2, in diffuse large cell lymphoma xenograft model reveal drug action on both bcl-2 and mcl-1. Clin. Cancer Res. 2007, 13, 2226–2235. [Google Scholar] [CrossRef] [PubMed]
- Zeitlin, B.D.; Joo, E.; Dong, Z.; Warner, K.; Wang, G.; Nikolovska-Coleska, Z.; Wang, S.; Nor, J.E. Antiangiogenic effect of TW37, a small-molecule inhibitor of bcl-2. Cancer Res. 2006, 66, 8698–8706. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Li, Z.M.; Hu, Z.Y.; Zeng, Z.L.; Yang, D.J.; Jiang, W.Q. Apogossypolone inhibits cell growth by inducing cell cycle arrest in u937 cells. Oncol. Rep. 2009, 22, 193–198. [Google Scholar] [PubMed]
- Paoluzzi, L.; Gonen, M.; Gardner, J.R.; Mastrella, J.; Yang, D.; Holmlund, J.; Sorensen, M.; Leopold, L.; Manova, K.; Marcucci, G.; et al. Targeting bcl-2 family members with the BH3 mimetic AT-101 markedly enhances the therapeutic effects of chemotherapeutic agents in in vitro and in vivo models of b-cell lymphoma. Blood 2008, 111, 5350–5358. [Google Scholar] [CrossRef] [PubMed]
- Wei, J.; Stebbins, J.L.; Kitada, S.; Dash, R.; Placzek, W.; Rega, M.F.; Wu, B.; Cellitti, J.; Zhai, D.; Yang, L.; et al. BI-97C1, an optically pure apogossypol derivative as pan-active inhibitor of antiapoptotic B-cell lymphoma/leukemia-2 (bcl-2) family proteins. J. Med. Chem. 2010, 53, 4166–4176. [Google Scholar] [CrossRef] [PubMed]
- Dash, R.; Azab, B.; Quinn, B.A.; Shen, X.; Wang, X.Y.; Das, S.K.; Rahmani, M.; Wei, J.; Hedvat, M.; Dent, P.; et al. Apogossypol derivative BI-97C1 (Sabutoclax) targeting mcl-1 sensitizes prostate cancer cells to mda-7/IL-24-mediated toxicity. Proc. Natl. Acad. Sci. USA 2011, 108, 8785–8790. [Google Scholar] [CrossRef] [PubMed]
- Kazi, A.; Sun, J.; Doi, K.; Sung, S.S.; Takahashi, Y.; Yin, H.; Rodriguez, J.M.; Becerril, J.; Berndt, N.; Hamilton, A.D.; et al. The BH3 α-helical mimic BH3-m6 disrupts bcl-x(l), bcl-2, and mcl-1 protein-protein interactions with bax, bak, bad, or bim and induces apoptosis in a bax- and bim-dependent manner. J. Biol. Chem. 2011, 286, 9382–9392. [Google Scholar] [CrossRef] [PubMed]
- Varfolomeev, E.; Blankenship, J.W.; Wayson, S.M.; Fedorova, A.V.; Kayagaki, N.; Garg, P.; Zobel, K.; Dynek, J.N.; Elliott, L.O.; Wallweber, H.J.; et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-κb activation, and TNFα-dependent apoptosis. Cell 2007, 131, 669–681. [Google Scholar] [CrossRef] [PubMed]
- Vince, J.E.; Wong, W.W.; Khan, N.; Feltham, R.; Chau, D.; Ahmed, A.U.; Benetatos, C.A.; Chunduru, S.K.; Condon, S.M.; McKinlay, M.; et al. IAP antagonists target ciap1 to induce TNFα-dependent apoptosis. Cell 2007, 131, 682–693. [Google Scholar] [CrossRef] [PubMed]
- Ndubaku, C.; Varfolomeev, E.; Wang, L.; Zobel, K.; Lau, K.; Elliott, L.O.; Maurer, B.; Fedorova, A.V.; Dynek, J.N.; Koehler, M.; et al. Antagonism of c-IAP and XIAP proteins is required for efficient induction of cell death by small-molecule IAP antagonists. ACS Chem. Biol. 2009, 4, 557–566. [Google Scholar] [CrossRef] [PubMed]
- Schimmer, A.D.; Dalili, S.; Batey, R.A.; Riedl, S.J. Targeting XIAP for the treatment of malignancy. Cell Death Differ. 2006, 13, 179–188. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Thomas, R.M.; Suzuki, H.; De Brabander, J.K.; Wang, X.; Harran, P.G. A small molecule smac mimic potentiates trail- and TNFα-mediated cell death. Science 2004, 305, 1471–1474. [Google Scholar] [CrossRef] [PubMed]
- Ndubaku, C.; Cohen, F.; Varfolomeev, E.; Vucic, D. Targeting inhibitor of apoptosis proteins for therapeutic intervention. Future Med. Chem. 2009, 1, 1509–1525. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; Nikolovska-Coleska, Z.; Lu, J.; Meagher, J.L.; Yang, C.Y.; Qiu, S.; Tomita, Y.; Ueda, Y.; Jiang, S.; Krajewski, K.; et al. Design, synthesis, and characterization of a potent, nonpeptide, cell-permeable, bivalent smac mimetic that concurrently targets both the BIR2 and BIR3 domains in XIAP. J. Am. Chem. Soc. 2007, 129, 15279–15294. [Google Scholar] [CrossRef] [PubMed]
- Petersen, S.L.; Wang, L.; Yalcin-Chin, A.; Li, L.; Peyton, M.; Minna, J.; Harran, P.; Wang, X. Autocrine TNFα signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007, 12, 445–456. [Google Scholar] [CrossRef] [PubMed]
- Chai, J.; Du, C.; Wu, J.W.; Kyin, S.; Wang, X.; Shi, Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 2000, 406, 855–862. [Google Scholar] [PubMed]
- Verhagen, A.M.; Ekert, P.G.; Pakusch, M.; Silke, J.; Connolly, L.M.; Reid, G.E.; Moritz, R.L.; Simpson, R.J.; Vaux, D.L. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000, 102, 43–53. [Google Scholar] [CrossRef]
- Wu, G.; Chai, J.; Suber, T.L.; Wu, J.W.; Du, C.; Wang, X.; Shi, Y. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000, 408, 1008–1012. [Google Scholar] [PubMed]
- Franklin, M.C.; Kadkhodayan, S.; Ackerly, H.; Alexandru, D.; Distefano, M.D.; Elliott, L.O.; Flygare, J.A.; Mausisa, G.; Okawa, D.C.; Ong, D.; et al. Structure and function analysis of peptide antagonists of melanoma inhibitor of apoptosis (ML-IAP). Biochemistry 2003, 42, 8223–8231. [Google Scholar] [CrossRef] [PubMed]
- Vucic, D.; Deshayes, K.; Ackerly, H.; Pisabarro, M.T.; Kadkhodayan, S.; Fairbrother, W.J.; Dixit, V.M. Smac negatively regulates the anti-apoptotic activity of melanoma inhibitor of apoptosis (ML-IAP). J. Biol. Chem. 2002, 277, 12275–12279. [Google Scholar] [CrossRef] [PubMed]
- Fulda, S.; Wick, W.; Weller, M.; Debatin, K.M. Smac agonists sensitize for APO2L/trail- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 2002, 8, 808–815. [Google Scholar] [CrossRef] [PubMed]
- Schulte, T.W.; Neckers, L.M. The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to hsp90 and shares important biologic activities with geldanamycin. Cancer Chemother. Pharmacol. 1998, 42, 273–279. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.S.; Alarcon, S.V.; Lee, S.; Lee, M.J.; Giaccone, G.; Neckers, L.; Trepel, J.B. Update on hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 2009, 9, 1479–1492. [Google Scholar] [CrossRef] [PubMed]
- Sydor, J.R.; Normant, E.; Pien, C.S.; Porter, J.R.; Ge, J.; Grenier, L.; Pak, R.H.; Ali, J.A.; Dembski, M.S.; Hudak, J.; et al. Development of 17-allylamino-17-demethoxygeldanamycin hydroquinone hydrochloride (IPI-504), an anti-cancer agent directed against hsp90. Proc. Natl. Acad. Sci. USA 2006, 103, 17408–17413. [Google Scholar] [CrossRef] [PubMed]
- Ge, J.; Normant, E.; Porter, J.R.; Ali, J.A.; Dembski, M.S.; Gao, Y.; Georges, A.T.; Grenier, L.; Pak, R.H.; Patterson, J.; et al. Design, synthesis, and biological evaluation of hydroquinone derivatives of 17-amino-17-demethoxygeldanamycin as potent, water-soluble inhibitors of hsp90. J. Med. Chem. 2006, 49, 4606–4615. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.Q.; Geng, X.; Solit, D.; Pratilas, C.A.; Rosen, N.; Danishefsky, S.J. New efficient synthesis of resorcinylic macrolides via ynolides: Establishment of cycloproparadicicol as synthetically feasible preclinical anticancer agent based on hsp90 as the target. J. Am. Chem. Soc. 2004, 126, 7881–7889. [Google Scholar] [CrossRef] [PubMed]
- Jhaveri, K.; Taldone, T.; Modi, S.; Chiosis, G. Advances in the clinical development of heat shock protein 90 (hsp90) inhibitors in cancers. Biochim. Biophys. Acta 2012, 1823, 742–755. [Google Scholar] [CrossRef] [PubMed]
- Chiosis, G.; Timaul, M.N.; Lucas, B.; Munster, P.N.; Zheng, F.F.; Sepp-Lorenzino, L.; Rosen, N. A small molecule designed to bind to the adenine nucleotide pocket of hsp90 causes her2 degradation and the growth arrest and differentiation of breast cancer cells. Chem. Biol. 2001, 8, 289–299. [Google Scholar] [CrossRef]
- Caldas-Lopes, E.; Cerchietti, L.; Ahn, J.H.; Clement, C.C.; Robles, A.I.; Rodina, A.; Moulick, K.; Taldone, T.; Gozman, A.; Guo, Y.; et al. Hsp90 inhibitor PU-H71, a multimodal inhibitor of malignancy, induces complete responses in triple-negative breast cancer models. Proc. Natl. Acad. Sci. USA 2009, 106, 8368–8373. [Google Scholar] [CrossRef] [PubMed]
- Kasibhatla, S.R.; Hong, K.; Biamonte, M.A.; Busch, D.J.; Karjian, P.L.; Sensintaffar, J.L.; Kamal, A.; Lough, R.E.; Brekken, J.; Lundgren, K.; et al. Rationally designed high-affinity 2-amino-6-halopurine heat shock protein 90 inhibitors that exhibit potent antitumor activity. J. Med. Chem. 2007, 50, 2767–2778. [Google Scholar] [CrossRef] [PubMed]
- Bao, R.; Lai, C.J.; Qu, H.; Wang, D.; Yin, L.; Zifcak, B.; Atoyan, R.; Wang, J.; Samson, M.; Forrester, J.; et al. CUDC-305, a novel synthetic HSP90 inhibitor with unique pharmacologic properties for cancer therapy. Clin. Cancer Res. 2009, 15, 4046–4057. [Google Scholar] [CrossRef] [PubMed]
- Lundgren, K.; Zhang, H.; Brekken, J.; Huser, N.; Powell, R.E.; Timple, N.; Busch, D.J.; Neely, L.; Sensintaffar, J.L.; Yang, Y.C.; et al. BIIB021, an orally available, fully synthetic small-molecule inhibitor of the heat shock protein hsp90. Mol. Cancer Ther. 2009, 8, 921–929. [Google Scholar] [CrossRef] [PubMed]
- Aggarwal, B.B.; Van Kuiken, M.E.; Iyer, L.H.; Harikumar, K.B.; Sung, B. Molecular targets of nutraceuticals derived from dietary spices: Potential role in suppression of inflammation and tumorigenesis. Exp. Biol. Med. 2009, 234, 825–849. [Google Scholar] [CrossRef] [PubMed]
- Dhillon, N.; Aggarwal, B.B.; Newman, R.A.; Wolff, R.A.; Kunnumakkara, A.B.; Abbruzzese, J.L.; Ng, C.S.; Badmaev, V.; Kurzrock, R. Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin. Cancer Res. 2008, 14, 4491–4499. [Google Scholar] [CrossRef] [PubMed]
- Sonpavde, G.; Matveev, V.; Burke, J.M.; Caton, J.R.; Fleming, M.T.; Hutson, T.E.; Galsky, M.D.; Berry, W.R.; Karlov, P.; Holmlund, J.T.; et al. Randomized phase II trial of docetaxel plus prednisone in combination with placebo or AT-101, an oral small molecule bcl-2 family antagonist, as first-line therapy for metastatic castration-resistant prostate cancer. Ann. Oncol. 2012, 23, 1803–1808. [Google Scholar] [CrossRef] [PubMed]
- Liu, B.; Bai, Q.X.; Chen, X.Q.; Gao, G.X.; Gu, H.T. Effect of curcumin on expression of survivin, bcl-2 and bax in human multiple myeloma cell line. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2007, 15, 762–766. [Google Scholar] [PubMed]
- Kolettas, E.; Thomas, C.; Leneti, E.; Skoufos, I.; Mbatsi, C.; Sisoula, C.; Manos, G.; Evangelou, A. Rosmarinic acid failed to suppress hydrogen peroxide-mediated apoptosis but induced apoptosis of jurkat cells which was suppressed by bcl-2. Mol. Cell. Biochem. 2006, 285, 111–120. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, N.; Laverick, L.; Sammons, J.; Zhang, H.; Maslin, D.J.; Hassan, H.T. Ajoene, a garlic-derived natural compound, enhances chemotherapy-induced apoptosis in human myeloid leukaemia CD34-positive resistant cells. Anticancer Res. 2001, 21, 3519–3523. [Google Scholar] [PubMed]
- Goy, A.; Hernandez-Ilzaliturri, F.J.; Kahl, B.; Ford, P.; Protomastro, E.; Berger, M. A phase I/II study of the pan bcl-2 inhibitor obatoclax mesylate plus bortezomib for relapsed or refractory mantle cell lymphoma. Leuk. Lymphoma 2014, 55, 2761–2768. [Google Scholar] [CrossRef] [PubMed]
- Wiechno, P.; Somer, B.G.; Mellado, B.; Chlosta, P.L.; Cervera Grau, J.M.; Castellano, D.; Reuter, C.; Stockle, M.; Kamradt, J.; Pikiel, J.; et al. A randomised phase 2 study combining ly2181308 sodium (survivin antisense oligonucleotide) with first-line docetaxel/prednisone in patients with castration-resistant prostate cancer. Eur. Urol. 2014, 65, 516–520. [Google Scholar] [CrossRef] [PubMed]
- Sinicrope, F.A.; Penington, R.C.; Tang, X.M. Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis is inhibited by bcl-2 but restored by the small molecule bcl-2 inhibitor, HA 14–1, in human colon cancer cells. Clin. Cancer Res. 2004, 10, 8284–8292. [Google Scholar] [CrossRef] [PubMed]
- Mesri, M.; Wall, N.R.; Li, J.; Kim, R.W.; Altieri, D.C. Cancer gene therapy using a survivin mutant adenovirus. J. Clin. Investig. 2001, 108, 981–990. [Google Scholar] [CrossRef] [PubMed]
- Arisan, E.D.; Kutuk, O.; Tezil, T.; Bodur, C.; Telci, D.; Basaga, H. Small inhibitor of bcl-2, HA14–1, selectively enhanced the apoptotic effect of cisplatin by modulating bcl-2 family members in MDA-MB-231 breast cancer cells. Breast Cancer Res. Treat. 2010, 119, 271–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raetz, E.A.; Morrison, D.; Romanos-Sirakis, E.; Gaynon, P.; Sposto, R.; Bhojwani, D.; Bostrom, B.C.; Brown, P.; Eckroth, E.; Cassar, J.; et al. A phase I study of EZN-3042, a novel survivin messenger ribonucleic acid (mRNA) antagonist, administered in combination with chemotherapy in children with relapsed acute lymphoblastic leukemia (ALL): A report from the therapeutic advances in childhood leukemia and lymphoma (TACL) consortium. J. Pediatr. Hematol. Oncol. 2013. [Google Scholar] [CrossRef]
- Mitsiades, C.S.; Hayden, P.; Kotoula, V.; McMillin, D.W.; McMullan, C.; Negri, J.; Delmore, J.E.; Poulaki, V.; Mitsiades, N. Bcl-2 overexpression in thyroid carcinoma cells increases sensitivity to bcl-2 homology 3 domain inhibition. J. Clin. Endocrinol. Metab. 2007, 92, 4845–4852. [Google Scholar] [CrossRef] [PubMed]
- Hansen, J.B.; Fisker, N.; Westergaard, M.; Kjaerulff, L.S.; Hansen, H.F.; Thrue, C.A.; Rosenbohm, C.; Wissenbach, M.; Orum, H.; Koch, T. Spc3042: A proapoptotic survivin inhibitor. Mol. Cancer Ther. 2008, 7, 2736–2745. [Google Scholar] [CrossRef] [PubMed]
- Al-Karaawi, M.A. Interaction studies to evaluate 2-carboxyphenolate analogues as inhibitor of anti-apoptotic protein bcl-2. Bioinformation 2013, 9, 477–480. [Google Scholar] [CrossRef] [PubMed]
- Kelly, R.J.; Thomas, A.; Rajan, A.; Chun, G.; Lopez-Chavez, A.; Szabo, E.; Spencer, S.; Carter, C.A.; Guha, U.; Khozin, S.; et al. A phase I/II study of sepantronium bromide (YM155, survivin suppressor) with paclitaxel and carboplatin in patients with advanced non-small-cell lung cancer. Ann. Oncol. 2013, 24, 2601–2606. [Google Scholar] [CrossRef] [PubMed]
- Felix, S.; Sandjo, L.P.; Opatz, T.; Erkel, G. SF002–96–1, a new drimane sesquiterpene lactone from an aspergillus species, inhibits survivin expression. Beilstein J. Org. Chem. 2013, 9, 2866–2876. [Google Scholar] [CrossRef] [PubMed]
- Shanafelt, T.D.; Call, T.G.; Zent, C.S.; Leis, J.F.; LaPlant, B.; Bowen, D.A.; Roos, M.; Laumann, K.; Ghosh, A.K.; Lesnick, C.; et al. Phase 2 trial of daily, oral polyphenon e in patients with asymptomatic, RAI stage 0 to II chronic lymphocytic leukemia. Cancer 2013, 119, 363–370. [Google Scholar] [CrossRef] [PubMed]
- Wadegaonkar, V.P.; Wadegaonkar, P.A. Withanone as an inhibitor of survivin: A potential drug candidate for cancer therapy. J. Biotechnol. 2013, 168, 229–233. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.; Braun, C.R.; Bird, G.H.; Walensky, L.D. Photoreactive stapled peptides to identify and characterize bcl-2 family interaction sites by mass spectrometry. Methods Enzymol. 2014, 544, 25–48. [Google Scholar] [PubMed]
- Shi, X.; Wang, D.; Ding, K.; Lu, Z.; Jin, Y.; Zhang, J.; Pan, J. GDP366, a novel small molecule dual inhibitor of survivin and Op18, induces cell growth inhibition, cellular senescence and mitotic catastrophe in human cancer cells. Cancer Biol. Ther. 2010, 9, 640–650. [Google Scholar] [CrossRef] [PubMed]
- Real, P.J.; Cao, Y.; Wang, R.; Nikolovska-Coleska, Z.; Sanz-Ortiz, J.; Wang, S.; Fernandez-Luna, J.L. Breast cancer cells can evade apoptosis-mediated selective killing by a novel small molecule inhibitor of bcl-2. Cancer Res. 2004, 64, 7947–7953. [Google Scholar] [CrossRef] [PubMed]
- Kaneko, M.; Nakashima, T.; Uosaki, Y.; Hara, M.; Ikeda, S.; Kanda, Y. Synthesis of tetrocarcin derivatives with specific inhibitory activity towards bcl-2 functions. Bioorg. Med. Chem. Lett. 2001, 11, 887–890. [Google Scholar] [CrossRef]
- Chan, S.L.; Lee, M.C.; Tan, K.O.; Yang, L.K.; Lee, A.S.; Flotow, H.; Fu, N.Y.; Butler, M.S.; Soejarto, D.D.; Buss, A.D.; et al. Identification of chelerythrine as an inhibitor of bclxl function. J. Biol. Chem. 2003, 278, 20453–20456. [Google Scholar] [CrossRef] [PubMed]
- Varadarajan, S.; Vogler, M.; Butterworth, M.; Dinsdale, D.; Walensky, L.D.; Cohen, G.M. Evaluation and critical assessment of putative mcl-1 inhibitors. Cell Death Differ. 2013, 20, 1475–1484. [Google Scholar] [CrossRef] [PubMed]
- Lessene, G.; Czabotar, P.E.; Sleebs, B.E.; Zobel, K.; Lowes, K.N.; Adams, J.M.; Baell, J.B.; Colman, P.M.; Deshayes, K.; Fairbrother, W.J.; et al. Structure-guided design of a selective bcl-x(l) inhibitor. Nat. Chem. Biol. 2013, 9, 390–397. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Goulet, R., 3rd; Stanton, K.J.; Sadaria, M.; Nakshatri, H. Differential effect of anti-apoptotic genes bcl-xl and c-flip on sensitivity of mcf-7 breast cancer cells to paclitaxel and docetaxel. Anticancer Res. 2005, 25, 2367–2379. [Google Scholar] [PubMed]
- Wu, T.Y.; Wagner, K.W.; Bursulaya, B.; Schultz, P.G.; Deveraux, Q.L. Development and characterization of nonpeptidic small molecule inhibitors of the xiap/caspase-3 interaction. Chem. Biol. 2003, 10, 759–767. [Google Scholar] [CrossRef]
- Bai, L.; Chen, J.; McEachern, D.; Liu, L.; Zhou, H.; Aguilar, A.; Wang, S. BM-1197: A novel and specific bcl-2/bcl-xl inhibitor inducing complete and long-lasting tumor regression in vivo. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [PubMed]
- Aguilar, A.; Zhou, H.; Chen, J.; Liu, L.; Bai, L.; McEachern, D.; Yang, C.Y.; Meagher, J.; Stuckey, J.; Wang, S. A potent and highly efficacious bcl-2/bcl-xl inhibitor. J. Med. Chem. 2013, 56, 3048–3067. [Google Scholar] [CrossRef] [PubMed]
- Ling, X.; Cao, S.; Cheng, Q.; Keefe, J.T.; Rustum, Y.M.; Li, F. A novel small molecule FL118 that selectively inhibits survivin, mcl-1, XIAP and cIAP2 in a p53-independent manner, shows superior antitumor activity. PLoS ONE 2012, 7. [Google Scholar] [CrossRef] [PubMed]
- Melkko, S.; Mannocci, L.; Dumelin, C.E.; Villa, A.; Sommavilla, R.; Zhang, Y.; Grutter, M.G.; Keller, N.; Jermutus, L.; Jackson, R.H.; et al. Isolation of a small-molecule inhibitor of the antiapoptotic protein bcl-xl from a DNA-encoded chemical library. ChemMedChem 2010, 5, 584–590. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.; Zheng, Z.; Li, Y.; Yu, W.; Zhong, W.; Tian, S.; Zhao, F.; Ren, X.; Xiao, J.; Wang, N.; et al. A novel bcl-xl inhibitor z36 that induces autophagic cell death in hela cells. Autophagy 2009, 5, 314–320. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Wang, X.; Du, Z.; Liu, Y.; Huang, D.; Zheng, K.; Liu, K.; Zhang, Y.; Zhong, X.; Wang, Y. SNX-25a, a novel hsp90 inhibitor, inhibited human cancer growth more potently than 17-AAG. Biochem. Biophys. Res. Commun. 2014, 450, 73–80. [Google Scholar] [CrossRef] [PubMed]
- Ponassi, R.; Biasotti, B.; Tomati, V.; Bruno, S.; Poggi, A.; Malacarne, D.; Cimoli, G.; Salis, A.; Pozzi, S.; Miglino, M.; et al. A novel Bim-BH3-derived bcl-XL inhibitor: Biochemical characterization, in vitro, in vivo and ex-vivo anti-leukemic activity. Cell Cycle 2008, 7, 3211–3224. [Google Scholar] [CrossRef] [PubMed]
- Burlison, J.A.; Neckers, L.; Smith, A.B.; Maxwell, A.; Blagg, B.S. Novobiocin: Redesigning a DNA gyrase inhibitor for selective inhibition of hsp90. J. Am. Chem. Soc. 2006, 128, 15529–15536. [Google Scholar] [CrossRef] [PubMed]
- Shoemaker, A.R.; Oleksijew, A.; Bauch, J.; Belli, B.A.; Borre, T.; Bruncko, M.; Deckwirth, T.; Frost, D.J.; Jarvis, K.; Joseph, M.K.; et al. A small-molecule inhibitor of bcl-XL potentiates the activity of cytotoxic drugs in vitro and in vivo. Cancer Res. 2006, 66, 8731–8739. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Q.; Wu, C.Z.; Lee, J.K.; Zhao, S.R.; Li, H.M.; Huo, Q.; Ma, T.; Zhang, J.; Hong, Y.S.; Liu, H. Anticancer effects of the hsp90 inhibitor 17-demethoxy-reblastatin in human breast cancer MDA-MB-231 cells. J. Microbiol. Biotechnol. 2014, 24, 914–920. [Google Scholar] [PubMed]
- Broome, H.E.; Yu, A.L.; Diccianni, M.; Camitta, B.M.; Monia, B.P.; Dean, N.M. Inhibition of bcl-xl expression sensitizes t-cell acute lymphoblastic leukemia cells to chemotherapeutic drugs. Leuk. Res. 2002, 26, 311–316. [Google Scholar] [CrossRef]
- Stenderup, K.; Rosada, C.; Gavillet, B.; Vuagniaux, G.; Dam, T.N. DEBIO 0932, a new oral hsp90 inhibitor, alleviates psoriasis in a xenograft transplantation model. Acta Derm. Venereol. 2014, 94, 672–676. [Google Scholar] [CrossRef] [PubMed]
- Wacheck, V.; Selzer, E.; Gunsberg, P.; Lucas, T.; Meyer, H.; Thallinger, C.; Monia, B.P.; Jansen, B. Bcl-x(l) antisense oligonucleotides radiosensitise colon cancer cells. Br. J. Cancer 2003, 89, 1352–1357. [Google Scholar] [CrossRef] [PubMed]
- Chandarlapaty, S.; Sawai, A.; Ye, Q.; Scott, A.; Silinski, M.; Huang, K.; Fadden, P.; Partdrige, J.; Hall, S.; Steed, P.; et al. SNX2112, a synthetic heat shock protein 90 inhibitor, has potent antitumor activity against her kinase-dependent cancers. Clin. Cancer Res. 2008, 14, 240–248. [Google Scholar] [CrossRef] [PubMed]
- Yin, H.; Lee, G.I.; Sedey, K.A.; Kutzki, O.; Park, H.S.; Orner, B.P.; Ernst, J.T.; Wang, H.G.; Sebti, S.M.; Hamilton, A.D. Terphenyl-based Bak BH3 α-helical proteomimetics as low-molecular-weight antagonists of bcl-xl. J. Am. Chem. Soc. 2005, 127, 10191–10196. [Google Scholar] [CrossRef] [PubMed]
- Fotsop, D.F.; Roussi, F.; Leverrier, A.; Breteche, A.; Gueritte, F. Biomimetic total synthesis of meiogynin a, an inhibitor of bcl-xl and bak interaction. J. Org. Chem. 2010, 75, 7412–7415. [Google Scholar] [CrossRef] [PubMed]
- Woodhead, A.J.; Angove, H.; Carr, M.G.; Chessari, G.; Congreve, M.; Coyle, J.E.; Cosme, J.; Graham, B.; Day, P.J.; Downham, R.; et al. Discovery of (2,4-dihydroxy-5-isopropylphenyl)-[5-(4-methylpiperazin-1-ylmethyl)-1,3-dihydrois oindol-2-yl]methanone (AT13387), a novel inhibitor of the molecular chaperone hsp90 by fragment based drug design. J. Med. Chem. 2010, 53, 5956–5969. [Google Scholar] [CrossRef] [PubMed]
- Fogliatto, G.; Gianellini, L.; Brasca, M.G.; Casale, E.; Ballinari, D.; Ciomei, M.; Degrassi, A.; De Ponti, A.; Germani, M.; Guanci, M.; et al. NMS-E973, a novel synthetic inhibitor of hsp90 with activity against multiple models of drug resistance to targeted agents, including intracranial metastases. Clin. Cancer Res. 2013, 19, 3520–3532. [Google Scholar] [CrossRef] [PubMed]
- Rudin, C.M.; Hann, C.L.; Garon, E.B.; Ribeiro de Oliveira, M.; Bonomi, P.D.; Camidge, D.R.; Chu, Q.; Giaccone, G.; Khaira, D.; Ramalingam, S.S.; et al. Phase II study of single-agent navitoclax (ABT-263) and biomarker correlates in patients with relapsed small cell lung cancer. Clin. Cancer Res. 2012, 18, 3163–3169. [Google Scholar] [CrossRef] [PubMed]
- Bhat, R.; Tummalapalli, S.R.; Rotella, D.P. Progress in the discovery and development of heat shock protein 90 (hsp90) inhibitors. J. Med. Chem. 2014, 57, 8718–8728. [Google Scholar] [CrossRef] [PubMed]
- Souers, A.J.; Leverson, J.D.; Boghaert, E.R.; Ackler, S.L.; Catron, N.D.; Chen, J.; Dayton, B.D.; Ding, H.; Enschede, S.H.; Fairbrother, W.J.; et al. ABT-199, a potent and selective bcl-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 2013, 19, 202–208. [Google Scholar] [CrossRef] [PubMed]
- Vassallo, A.; Vaccaro, M.C.; De Tommasi, N.; Dal Piaz, F.; Leone, A. Identification of the plant compound geraniin as a novel hsp90 inhibitor. PLoS ONE 2013, 8. [Google Scholar] [CrossRef]
- Ono, N.; Yamazaki, T.; Nakanishi, Y.; Fujii, T.; Sakata, K.; Tachibana, Y.; Suda, A.; Hada, K.; Miura, T.; Sato, S.; et al. Preclinical antitumor activity of the novel heat shock protein 90 inhibitor CH5164840 against human epidermal growth factor receptor 2 (HER2)-overexpressing cancers. Cancer Sci. 2012, 103, 342–349. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Zhou, H.; Aguilar, A.; Liu, L.; Bai, L.; McEachern, D.; Yang, C.Y.; Meagher, J.L.; Stuckey, J.A.; Wang, S. Structure-based discovery of BM-957 as a potent small-molecule inhibitor of bcl-2 and bcl-xl capable of achieving complete tumor regression. J. Med. Chem. 2012, 55, 8502–8514. [Google Scholar] [CrossRef] [PubMed]
- Khandelwal, A.; Hall, J.A.; Blagg, B.S. Synthesis and structure-activity relationships of EGCG analogues, a recently identified hsp90 inhibitor. J. Org. Chem. 2013, 78, 7859–7884. [Google Scholar] [CrossRef] [PubMed]
- Chauhan, D.; Velankar, M.; Brahmandam, M.; Hideshima, T.; Podar, K.; Richardson, P.; Schlossman, R.; Ghobrial, I.; Raje, N.; Munshi, N.; et al. A novel bcl-2/bcl-x(l)/bcl-w inhibitor ABT-737 as therapy in multiple myeloma. Oncogene 2007, 26, 2374–2380. [Google Scholar] [CrossRef] [PubMed]
- Margarucci, L.; Monti, M.C.; Cassiano, C.; Mozzicafreddo, M.; Angeletti, M.; Riccio, R.; Tosco, A.; Casapullo, A. Chemical proteomics-driven discovery of oleocanthal as an hsp90 inhibitor. Chem. Commun. 2013, 49, 5844–5846. [Google Scholar] [CrossRef]
- Lyman, S.K.; Crawley, S.C.; Gong, R.; Adamkewicz, J.I.; McGrath, G.; Chew, J.Y.; Choi, J.; Holst, C.R.; Goon, L.H.; Detmer, S.A.; et al. High-content, high-throughput analysis of cell cycle perturbations induced by the hsp90 inhibitor xl888. PLoS ONE 2011, 6. [Google Scholar] [CrossRef]
- Best, O.G.; Singh, N.; Forsyth, C.; Mulligan, S.P. The novel hsp-90 inhibitor SNX7081 is significantly more potent than 17-AAG against primary cll cells and a range of haematological cell lines, irrespective of lesions in the tp53 pathway. Br. J. Haematol. 2010, 151, 185–188. [Google Scholar] [CrossRef] [PubMed]
- Menezes, D.L.; Taverna, P.; Jensen, M.R.; Abrams, T.; Stuart, D.; Yu, G.K.; Duhl, D.; Machajewski, T.; Sellers, W.R.; Pryer, N.K.; et al. The novel oral hsp90 inhibitor NVP-HSP990 exhibits potent and broad-spectrum antitumor activities in vitro and in vivo. Mol. Cancer Ther. 2012, 11, 730–739. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Li, Y.; Zhang, S.; Perry, B.; Zhao, T.; Wang, Y.; Sun, C. Radicicol, a heat shock protein 90 inhibitor, inhibits differentiation and adipogenesis in 3T3-L1 preadipocytes. Biochem. Biophys. Res. Commun. 2013, 436, 169–174. [Google Scholar] [CrossRef] [PubMed]
- Oost, T.K.; Sun, C.; Armstrong, R.C.; Al-Assaad, A.S.; Betz, S.F.; Deckwerth, T.L.; Ding, H.; Elmore, S.W.; Meadows, R.P.; Olejniczak, E.T.; et al. Discovery of potent antagonists of the antiapoptotic protein xiap for the treatment of cancer. J. Med. Chem. 2004, 47, 4417–4426. [Google Scholar] [CrossRef] [PubMed]
- Liston, P.; Fong, W.G.; Kelly, N.L.; Toji, S.; Miyazaki, T.; Conte, D.; Tamai, K.; Craig, C.G.; McBurney, M.W.; Korneluk, R.G. Identification of XAF1 as an antagonist of xiap anti-caspase activity. Nat. Cell Biol. 2001, 3, 128–133. [Google Scholar] [CrossRef] [PubMed]
- Ju, H.Q.; Xiang, Y.F.; Xin, B.J.; Pei, Y.; Lu, J.X.; Wang, Q.L.; Xia, M.; Qian, C.W.; Ren, Z.; Wang, S.Y.; et al. Synthesis and in vitro anti-HSV-1 activity of a novel hsp90 inhibitor BJ-B11. Bioorg. Med. Chem. Lett. 2011, 21, 1675–1677. [Google Scholar] [CrossRef] [PubMed]
- Schimmer, A.D.; Welsh, K.; Pinilla, C.; Wang, Z.; Krajewska, M.; Bonneau, M.J.; Pedersen, I.M.; Kitada, S.; Scott, F.L.; Bailly-Maitre, B.; et al. Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 2004, 5, 25–35. [Google Scholar] [CrossRef]
- Nakashima, T.; Ishii, T.; Tagaya, H.; Seike, T.; Nakagawa, H.; Kanda, Y.; Akinaga, S.; Soga, S.; Shiotsu, Y. New molecular and biological mechanism of antitumor activities of KW-2478, a novel nonansamycin heat shock protein 90 inhibitor, in multiple myeloma cells. Clin. Cancer Res. 2010, 16, 2792–2802. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.H.; Bajji, A.; Tangallapally, R.; Markovitz, B.; Trovato, R.; Shenderovich, M.; Baichwal, V.; Bartel, P.; Cimbora, D.; McKinnon, R.; et al. Discovery of (2S)-1-[4-(2-{6-amino-8-[(6-bromo-1,3-benzodioxol-5-yl)sulfanyl]-9h-purin-9-yl}et hyl)piperidin-1-yl]-2-hydroxypropan-1-one (MPC-3100), a purine-based hsp90 inhibitor. J. Med. Chem. 2012, 55, 7480–7501. [Google Scholar] [CrossRef] [PubMed]
- Lee, F.A.; Zee, B.C.; Cheung, F.Y.; Kwong, P.; Chiang, C.L.; Leung, K.C.; Siu, S.W.; Lee, C.; Lai, M.; Kwok, C.; et al. Randomized phase II study of the X-linked inhibitor of apoptosis (XIAP) antisense AEG35156 in combination with sorafenib in patients with advanced hepatocellular carcinoma (HCC). Am. J. Clin. Oncol. 2014. [Google Scholar] [CrossRef] [PubMed]
- Sessa, C.; Shapiro, G.I.; Bhalla, K.N.; Britten, C.; Jacks, K.S.; Mita, M.; Papadimitrakopoulou, V.; Pluard, T.; Samuel, T.A.; Akimov, M.; et al. First-in-human phase I dose-escalation study of the hsp90 inhibitor auy922 in patients with advanced solid tumors. Clin. Cancer Res. 2013, 19, 3671–3680. [Google Scholar] [CrossRef] [PubMed]
- Nikolovska-Coleska, Z.; Xu, L.; Hu, Z.; Tomita, Y.; Li, P.; Roller, P.P.; Wang, R.; Fang, X.; Guo, R.; Zhang, M.; et al. Discovery of embelin as a cell-permeable, small-molecular weight inhibitor of XIAP through structure-based computational screening of a traditional herbal medicine three-dimensional structure database. J. Med. Chem. 2004, 47, 2430–2440. [Google Scholar] [CrossRef] [PubMed]
- Pacey, S.; Wilson, R.H.; Walton, M.; Eatock, M.M.; Hardcastle, A.; Zetterlund, A.; Arkenau, H.T.; Moreno-Farre, J.; Banerji, U.; Roels, B.; et al. A phase I study of the heat shock protein 90 inhibitor alvespimycin (17-DMAG) given intravenously to patients with advanced solid tumors. Clin. Cancer Res. 2011, 17, 1561–1570. [Google Scholar] [CrossRef] [PubMed]
- Reddy, N.; Voorhees, P.M.; Houk, B.E.; Brega, N.; Hinson, J.M., Jr.; Jillela, A. Phase I trial of the hsp90 inhibitor PF-04929113 (SNX5422) in adult patients with recurrent, refractory hematologic malignancies. Clin. Lymphoma Myeloma Leuk. 2013, 13, 385–391. [Google Scholar] [CrossRef] [PubMed]
- Flygare, J.A.; Beresini, M.; Budha, N.; Chan, H.; Chan, I.T.; Cheeti, S.; Cohen, F.; Deshayes, K.; Doerner, K.; Eckhardt, S.G.; et al. Discovery of a potent small-molecule antagonist of inhibitor of apoptosis (IAP) proteins and clinical candidate for the treatment of cancer (GDC-0152). J. Med. Chem. 2012, 55, 4101–4113. [Google Scholar] [CrossRef] [PubMed]
- Dickson, M.A.; Okuno, S.H.; Keohan, M.L.; Maki, R.G.; D’Adamo, D.R.; Akhurst, T.J.; Antonescu, C.R.; Schwartz, G.K. Phase II study of the hsp90-inhibitor BIIB021 in gastrointestinal stromal tumors. Ann. Oncol. 2013, 24, 252–257. [Google Scholar] [CrossRef] [PubMed]
- Pacey, S.; Gore, M.; Chao, D.; Banerji, U.; Larkin, J.; Sarker, S.; Owen, K.; Asad, Y.; Raynaud, F.; Walton, M.; et al. A phase II trial of 17-allylamino, 17-demethoxygeldanamycin (17-AAG, tanespimycin) in patients with metastatic melanoma. Investig. New Drugs 2012, 30, 341–349. [Google Scholar] [CrossRef] [PubMed]
- Dhuria, S.; Einolf, H.; Mangold, J.; Sen, S.; Gu, H.; Wang, L.; Cameron, S. Time-dependent inhibition and induction of human cytochrome P4503A4/5 by an oral iap antagonist, LCL161, in vitro and in vivo in healthy subjects. J. Clin. Pharmacol. 2013, 53, 642–653. [Google Scholar] [CrossRef] [PubMed]
- Jhaveri, K.; Chandarlapaty, S.; Lake, D.; Gilewski, T.; Robson, M.; Goldfarb, S.; Drullinsky, P.; Sugarman, S.; Wasserheit-Leiblich, C.; Fasano, J.; et al. A phase II open-label study of ganetespib, a novel heat shock protein 90 inhibitor for patients with metastatic breast cancer. Clin. Breast Cancer 2014, 14, 154–160. [Google Scholar] [CrossRef] [PubMed]
- Asano, M.; Hashimoto, K.; Saito, B.; Shiokawa, Z.; Sumi, H.; Yabuki, M.; Yoshimatsu, M.; Aoyama, K.; Hamada, T.; Morishita, N.; et al. Design, stereoselective synthesis, and biological evaluation of novel tri-cyclic compounds as inhibitor of apoptosis proteins (IAP) antagonists. Bioorg. Med. Chem. 2013, 21, 5725–5737. [Google Scholar] [CrossRef] [PubMed]
- Oh, W.K.; Galsky, M.D.; Stadler, W.M.; Srinivas, S.; Chu, F.; Bubley, G.; Goddard, J.; Dunbar, J.; Ross, R.W. Multicenter phase II trial of the heat shock protein 90 inhibitor, retaspimycin hydrochloride (IPI-504), in patients with castration-resistant prostate cancer. Urology 2011, 78, 626–630. [Google Scholar] [CrossRef] [PubMed]
- Abd-Elrahman, I.; Hershko, K.; Neuman, T.; Nachmias, B.; Perlman, R.; Ben-Yehuda, D. The inhibitor of apoptosis protein livin (ML-IAP) plays a dual role in tumorigenicity. Cancer Res. 2009, 69, 5475–5480. [Google Scholar] [CrossRef] [PubMed]
Compound | Reference | Compound | Reference |
---|---|---|---|
Bcl-2 inhibitor | Survivin inhibitor | ||
GX15-070 ** | [152] | LY2181308 ** | [153] |
HA-14 | [154] | Ad-Survivin T34A | [155] |
HA14-1 | [156] | EZN-3042 * | [157] |
BH3I-1/BH3I-2 | [158] | SPC3042 | [159] |
2-carboxyphenolate | [160] | YM155 ** | [161] |
Genasense *** | [85] | SF002-96-1 | [162] |
Polyphenon E ** | [163] | Withanone | [164] |
SAHBs | [165] | GDP366 | [166] |
YC137 | [167] | Gambogic acid | [113] |
Tetrocarcin-A derivatives | [168] | Mcl-1 inhibitor | |
Bcl-xL inhibitor | Maritoclax | [90] | |
Chelerythrine | [169] | MIM-1 | [170] |
Compound 6 | [171] | BIR2 inhibitor | |
2-Methoxyantimycin A3 | [172] | TWX024 | [173] |
BM-1197 | [174] | Survivin/XIAP/Mcl-1/cIAP2 inhibitor | |
BM-1074 | [175] | FL118 | [176] |
Compound 19/93 | [177] | HSP90 inhibitor | |
Z36 | [178] | SNX-25a | [179] |
072RB | [180] | Novobiocin | [181] |
A-385358 | [182] | 17-DR | [183] |
Antisense (ISIS 15999) | [184] | Debio 0932 | [185] |
Antisense (ISIS 22783) | [186] | SNX-2112 | [187] |
Terphenyl derivatives | [188] | PU-H71 | [142] |
Meiogynin A | [189] | AT13387 | [190] |
BCl-2/Bcl-xL inhibitor | NMS-E973 | [191] | |
Nativoclax (ABT-263) ** | [192] | NXD30001 | [193] |
ABT-199 ** | [194] | Geraniin | [195] |
Antimycin A | [92] | CH5164840 | [196] |
BM-957 | [197] | EGC-3-gallate | [198] |
ABT-737 | [199] | Oleocanthal | [200] |
Bcl-2/Bcl-xL/Mcl-1 inhibitor | XL888 | [201] | |
Gossypol (AT-101) ** | [148] | SNX-7081 | [202] |
BI-97C1 | [118] | NVP-HSP990 | [203] |
XIAP inhibitor | Radicicol | [204] | |
BIR3 antagonists | [205,206] | BJ-B11 | [207] |
PPU derivatives | [208] | KW-2478 | [209] |
Capped tripeptides 205 | MPC-3100 | [210] | |
SM-164 | [127] | Peptide PEP73 | [195] |
AEG35156 ** | [211] | AUY922 * | [212] |
Embelin | [213] | 17-DMAG * | [214] |
XIAP/BIR3 inhibitor | SNX5422 * | [215] | |
GDC-0152 | [216] | BIIB021 ** | [217] |
IAIAP inhibitor | 17-AAG ** | [218] | |
LCL161 | [219] | Ganetespib ** | [220] |
OHPPA | [221] | IPI-504 ** | [222] |
Livin (ML-IAP) | [223] |
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Pandey, M.K.; Prasad, S.; Tyagi, A.K.; Deb, L.; Huang, J.; Karelia, D.N.; Amin, S.G.; Aggarwal, B.B. Targeting Cell Survival Proteins for Cancer Cell Death. Pharmaceuticals 2016, 9, 11. https://doi.org/10.3390/ph9010011
Pandey MK, Prasad S, Tyagi AK, Deb L, Huang J, Karelia DN, Amin SG, Aggarwal BB. Targeting Cell Survival Proteins for Cancer Cell Death. Pharmaceuticals. 2016; 9(1):11. https://doi.org/10.3390/ph9010011
Chicago/Turabian StylePandey, Manoj K., Sahdeo Prasad, Amit Kumar Tyagi, Lokesh Deb, Jiamin Huang, Deepkamal N. Karelia, Shantu G. Amin, and Bharat B. Aggarwal. 2016. "Targeting Cell Survival Proteins for Cancer Cell Death" Pharmaceuticals 9, no. 1: 11. https://doi.org/10.3390/ph9010011