Anti-malaria drug blocks proteotoxic stress response: Anti-cancer implications

Cell Cycle

Volumn 8, Issue 23, 2009, Pages 3960-3970

  Neznanov, Nickolay ^a   Gorbachev, Anton V ^b   Neznanova, Lubov ^a   Komarov, Andrei P ^c   Gurova, Katerina V ^a   Gasparian, Alexander V ^d   Banerjee, Amiya K ^b   Almasan, Alexandru ^b   Fairchild, Robert L ^b   Gudkov, Andrei V ^a,d  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c Cellecta Inc   (United States)

^d CLEVELAND BIOLABS INC   (United States)

Author keywords

Apoptosis; Bortezomib; Geldanamycin; Heat shock; Hsp90; Hyperthermia; Proteasomal inhibitors

Indexed keywords

17 DEMETHOXY 17 (2 DIMETHYLAMINOETHYLAMINO)GELDANAMYCIN; AMINOACRIDINE DERIVATIVE; BORTEZOMIB; EMETINE; GELDANAMYCIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90 INHIBITOR; HEAT SHOCK TRANSCRIPTION FACTOR 1; MEPACRINE; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; DNA BINDING; DRUG EFFECT; DRUG EFFICACY; DRUG INHIBITION; DRUG POTENTIATION; HEAT SHOCK RESPONSE; HUMAN; HUMAN CELL; HYPERTHERMIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SENSITIZATION; STRESS;

EID: 74849113809     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.23.10179     Document Type: Article

References (66)

1. Kampinga HH. Chaperones in preventing protein denaturation in living cells and protecting against cellular stress. Handb Exp Pharmacol 2006; 1-42.
2. Chang YS, Lee LC, Sun FC, Chao CC, Fu HW, Lai YK. Involvement of calcium in the differential induction of heat shock protein 70 by heat shock protein 90 inhibitors, geldanamycin and radicicol, in human non-small cell lung cancer H460 cells. J Cell Biochem 2006; 97:156-65.
3. Kawazoe Y, Nakai A, Tanabe M, Nagata K. Proteasome inhibition leads to the activation of all members of the heat-shock-factor family. Eur J Biochem 1998; 255:356-62.
4. Kim D, Kim SH, Li GC. Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce hsp70 and hsp27 expression. Biochem Biophys Res Commun 1999; 254:264-8.
5. Morimoto RI, Sarge KD, Abravaya K. Transcriptional regulation of heat shock genes. A paradigm for inducible genomic responses. J Biol Chem 1992; 267:21987-90.
6. Shen HY, He JC, Wang Y, Huang QY, Chen JF. Geldanamycin induces heat shock protein 70 and protects against MPTP-induced dopaminergic neurotoxicity in mice. J Biol Chem 2005; 280:39962-9.
7. Davenport EL, Moore HE, Dunlop AS, Sharp SY, Workman P, Morgan GJ, et al. Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood 2007; 110:2641-9.
8. Davenport EL, Morgan GJ, Davies FE. Untangling the unfolded protein response. Cell Cycle 2008; 7:865-9.
9. Mathew A, Mathur SK, Jolly C, Fox SG, Kim S, Morimoto RI. Stress-specific activation and repression of heat shock factors 1 and 2. Mol Cell Biol 2001; 21:7163-71.
10. Noonan EJ, Place RF, Giardina C, Hightower LE. Hsp70B' regulation and function. Cell Stress Chaperones 2007; 12:393-402.
11. Shringarpure R, Catley L, Bhole D, Burger R, Podar K, Tai YT, et al. Gene expression analysis of B-lymphoma cells resistant and sensitive to bortezomib. Br J Haematol 2006; 134:145-56.
12. Imai J, Yashiroda H, Maruya M, Yahara I, Tanaka K. Proteasomes and molecular chaperones: cellular machinery responsible for folding and destruction of unfolded proteins. Cell Cycle 2003; 2:585-90.
13. Wang J, Maldonado MA. The ubiquitin-proteasome system and its role in inflammatory and autoimmune diseases. Cell Mol Immunol 2006; 3:255-61.
14. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 1997; 89:239-50.
15. Weissman AM. Regulating protein degradation by ubiquitination. Immunol Today 1997; 18:189-98.
16. Stravopodis DJ, Margaritis LH, Voutsinas GE. Drug-mediated targeted disruption of multiple protein activities through functional inhibition of the Hsp90 chaperone complex. Curr Med Chem 2007; 14:3122-38.
17. Cowan JL, Morley SJ. The proteasome inhibitor, MG132, promotes the reprogramming of translation in C2C12 myoblasts and facilitates the association of hsp25 with the eIF4F complex. Eur J Biochem 2004; 271:3596-611.
18. Rahmani M, Davis EM, Bauer C, Dent P, Grant S. Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves downregulation of Mcl-1 through inhibition of translation. J Biol Chem 2005; 280:35217-27.
19. Proud CG. eIF2 and the control of cell physiology. Semin Cell Dev Biol 2005; 16:3-12.
20. Clemens MJ. Translational control in virus-infected cells: models for cellular stress responses. Semin Cell DevBiol 2005; 16:13-20.
21. He B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 2006; 13:393-403.
22. Solimini NL, Luo J, Elledge SJ. Non-oncogene addiction and the stress phenotype of cancer cells. Cell 2007; 130:986-8.
23. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007; 130:1005-18.
24. Munshi NC, Tricot G, Desikan R, Badros A, Zangari M, Toor A, et al. Clinical activity of arsenic trioxide for the treatment of multiple myeloma. Leukemia 2002; 16:1835-7.
25. Hayden PJ, Mitsiades CS, Anderson KC, Richardson PG. Novel therapies in myeloma. Curr Opin Hematol 2007; 14:609-15.
26. Perez CA, Pajak T, Emami B, Hornback NB, Tupchong L, Rubin P. Randomized phase III study comparing irradiation and hyperthermia with irradiation alone in superficial measurable tumors. Final report by the Radiation Therapy Oncology Group. Am J Clin Oncol 1991; 14:133-41.
27. McCollum AK, TenEyck CJ, Stensgard B, Morlan BW, Ballman KV, Jenkins RB, et al. P-Glycoprotein-mediated resistance to Hsp90-directed therapy is eclipsed by the heat shock response. Cancer Res 2008; 68:7419-27.
28. Nowakowski GS, McCollum AK, Ames MM, Mandrekar SJ, Reid JM, et al. A phase I trial of twice-weekly 17-allylamino-demethoxy-geldanamycin in patients with advanced cancer. Clin Cancer Res 2006; 12:6087-93.
29. McCollum AK, Lukasiewicz KB, Teneyck CJ, Lingle WL, Toft DO, Erlichman C. Cisplatin abrogates the geldanamycin-induced heat shock response. Mol Cancer Ther 2008; 7:3256-64.
30. Polla BS. Heat shock proteins in host-parasite interactions. Immunol Today 1991; 12:38-41.
31. Zaarur N, Gabai VL, Porco JA Jr, Calderwood S, Sherman MY. Targeting heat shock response to sensitize cancer cells to proteasome and Hsp90 inhibitors. Cancer Res 2006; 66:1783-91.
32. Grollman AP. Inhibitors of protein biosynthesis. V. Effects of emetine on protein and nucleic acid biosynthesis in HeLa cells. J Biol Chem 1968; 243:4089-94.
33. Gurova KV, Hill JE, Guo C, Prokvolit A, Burdelya LG, Samoylova E, et al. Small molecules that reactivate p53 in renal cell carcinoma reveal a NFkappaB-dependent mechanism of p53 suppression in tumors. Proc Natl Acad Sci USA 2005; 102:17448-53.
34. Chiosis G, Caldas LE, Solit D. Heat shock protein-90 inhibitors: a chronicle from geldanamycin to today's agents. Curr Opin Investig Drugs 2006; 7:534-41.
35. Drysdale MJ, Brough PA, Massey A, Jensen MR, Schoepfer J. Targeting Hsp90 for the treatment of cancer. Curr Opin Drug Discov Devel 2006; 9:483-95.
36. Schulte TW, Neckers LM. The benzoquinone ansamycin 17-allylamino-17- demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother Pharmacol 1998; 42:273-9.
37. Sharp S, Workman P. Inhibitors of the HSP90 molecular chaperone: current status. Adv Cancer Res 2006; 95:323-48.
38. Weber SM, Levitz SM. Chloroquine interferes with lipopolysaccharide- induced TNFalpha gene expression by a nonlysosomotropic mechanism. J Immunol 2000; 165:1534-40.
39. Demidenko ZN, Vivo C, Halicka HD, Li CJ, Bhalla K, Broude EV, et al. Pharmacological induction of Hsp70 protects apoptosis-prone cells from doxorubicin: comparison with caspase-inhibitor- and cycle-arrest-mediated cytoprotection. Cell Death Differ 2006; 13:1434-41.
40. Guo F, Rocha K, Bali P, Pranpat M, Fiskus W, Boyapalle S, et al. Abrogation of heat shock protein 70 induction as a strategy to increase antileukemia activity of heat shock protein 90 inhibitor 17-allylamino-demethoxy geldanamycin. Cancer Res 2005; 65:10536-44.
41. Xiao L, Lu X, Ruden DM. Effectiveness of hsp90 inhibitors as anti-cancer drugs. Mini Rev Med Chem 2006; 6:1137-43.
42. Voellmy R. On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 2004; 9:122-33.
43. Arya R, Mallik M, Lakhotia SC. Heat shock genes - integrating cell survival and death. J Biosci 2007; 32:595-610.
44. Latchman DS. HSP27 and cell survival in neurones. Int J Hyperthermia 2005; 21:393-402.
45. Jaattela M. Escaping cell death: survival proteins in cancer. Exp Cell Res 1999; 248:30-43.
46. Costlow N, Lis JT. High-resolution mapping of DNase I-hypersensitive sites of Drosophila heat shock genes in Drosophila melanogaster and Saccharomyces cerevisiae. Mol Cell Biol 1984; 4:1853-63.
47. Bonner JJ, Pardue ML. The effect of heat shock on RNA synthesis in Drosophila tissues. Cell 1976; 8:43-50.
48. Spradling A, Penman S, Pardue ML. Analysis of drosophila mRNA by in situ hybridization: sequences transcribed in normal and heat shocked cultured cells. Cell 1975; 4:395-404.
49. McKenzie SL, Henikoff S, Meselson M. Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster. Proc Natl Acad Sci USA 1975; 72:1117-21.
50. Subjeck JR, Shyy TT. Stress protein systems of mammalian cells. Am J Physiol 1986; 250:1-17.
51. Lindquist S. The heat-shock response. Annu Rev Biochem 1986; 55:1151-91.
52. Neidhardt FC, VanBogelen RA, Vaughn V. The genetics and regulation of heat-shock proteins. Annu Rev Genet 1984; 18:295-329.
53. Jiang HY, Wek RC. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 2005; 280:14189-202.
54. Neznanov N, Dragunsky EM, Chumakov KM, Neznanova L, Wek RC, Gudkov AV, et al. Different effect of proteasome inhibition on vesicular stomatitis virus and poliovirus replication. PLoS ONE 2008; 3:1887.
55. Kim YH, Park EJ, Han ST, Park JW, Kwon TK. Arsenic trioxide induces Hsp70 expression via reactive oxygen species and JNK pathway in MDA231 cells. Life Sci 2005; 77:2783-93.
56. Powers MV, Clarke PA, Workman P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 2008; 14:250-62.
57. Kwiatkowski D, Bate CA, Scragg IG, Beattie P, Udalova I, Knight JC. The malarial fever response - pathogenesis, polymorphism and prospects for intervention. Ann Trop Med Parasitol 1997; 91:533-42.
58. Senanayake N, Roman GC. Neurological complications of malaria. Southeast Asian J Trop Med Public Health 1992; 23:672-80.
59. Smith T, Felger I, Tanner M, Beck HP. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg 1999; 93:59-64.
60. Pavithra SR, Kumar R, Tatu U. Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol 2007; 3:1701-15.
61. Acharya P, Kumar R, Tatu U. Chaperoning a cellular upheaval in malaria: heat shock proteins in Plasmodium falciparum. Mol Biochem Parasitol 2007; 153:85-94.
62. Silva MD, Cooke BM, Guillotte M, Buckingham DW, Sauzet JP, Le Scanf C, et al. A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Mol Microbiol 2005; 56:990-1003.
63. Stuhlmeier KM, Pollaschek C. Quinacrine but not chloroquine inhibits PMA induced upregulation of matrix metalloproteinases in leukocytes: quinacrine acts at the transcriptional level through a PLA2-independent mechanism. J Rheumatol 2006; 33:472-80.
64. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983; 11:1475-89.
65. Trinklein ND, Chen WC, Kingston RE, Myers RM. Transcriptional regulation and binding of heat shock factor 1 and heat shock factor 2 to 32 human heat shock genes during thermal stress and differentiation. Cell Stress Chaperones 2004; 9:21-8.
66. Harrison EM, Sharpe E, Bellamy CO, McNally SJ, Devey L, Garden OJ, et al. Heat shock protein 90-binding agents protect renal cells from oxidative stress and reduce kidney ischemia-reperfusion injury. Am J Physiol Renal Physiol 2008; 295:397-405.