Oxidative inhibition of Hsp90 disrupts the super-chaperone complex and attenuates pancreatic adenocarcinoma in vitro and in vivo

International Journal of Cancer

Volumn 132, Issue 3, 2013, Pages 695-706

  Mandal, Chitra ^a   Sarkar, Sayantani ^a   Dutta, Devawati ^a   Samanta, Suman Kumar ^a   Bhattacharya, Kaushik ^a   Pal, Bikas Chandra ^a   Li, Jinping ^b   Datta, Kaustubh ^c   Mandal, Chhabinath ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

apoptosis; Cdc37; Hsp90; mahanine; pancreatic cancer; reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ALKALOID DERIVATIVE; ANTINEOPLASTIC AGENT; CELL CYCLE PROTEIN 37; CHAPERONE; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; MAHANINE; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; TANESPIMYCIN; THIOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BIOACCUMULATION; CANCER INHIBITION; CARCINOMA CELL; CELL MIGRATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION;

ACETYLCYSTEINE; ADENOCARCINOMA; ADENOSINE TRIPHOSPHATE; ALKALOIDS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARBAZOLES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CHAPERONINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LEUPEPTINS; MICE; MICE, NUDE; OXIDATIVE STRESS; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; SULFHYDRYL COMPOUNDS;

EID: 84870245054     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27687     Document Type: Article

References (48)

1. Wang Z, Ahmad A, Li Y, et al. Targeting notch to eradicate pancreatic cancer stem cells for cancer therapy. Anticancer Res 2011; 31: 1105-13.
2. Niederhuber JE, Brennan MF, Menck HR,. The National Cancer Data Base report on pancreatic cancer. Cancer 1995; 76: 1671-77.
3. Bardeesy N, DePinho RA,. Pancreatic cancer biology and genetics. Nat Rev Cancer 2002; 2: 897-909.
4. Li D, Xie K, Wolff R, Abbruzzese JL,. Pancreatic cancer. Lancet 2004; 363: 1049-57.
5. Poyton RO, Ball KA, Castello PR,. Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol Metab 2009; 20: 332-40.
6. Li N, Ragheb K, Lawler G, et al. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 2003; 278: 8516-25.
7. Dias N, Bailly C,. Drugs targeting mitochondrial functions to control tumour cell growth. Biochem Pharmacol 2005; 70: 1-12.
8. Pan JS, Hong MZ, Ren JL,. Reactive oxygen species: a double edged sword in oncogenesis. World J Gastroenterol 2009; 15: 1702-07.
9. Sreedhar AS, Soti C, Csermely P,. Inhibition of Hsp90: a new strategy for inhibiting protein kinases. Biochim Biophys Acta 2004; 1697: 233-42.
10. Richter K, Buchner J,. Hsp90: chaperoning signal transduction. J Cell Physiol 2001; 188: 281-90.
11. Mann J,. Natural products in cancer chemotherapy: past, present and future. Nat Rev Cancer 2002; 2: 143-48.
12. Newman DJ, Cragg GM, Snader KM,. The influence of natural products upon drug discovery. Nat Prod Rep 2000; 17: 215-34.
13. Ramsewak RS, Nair MG, Strasburg GM, et al. Biologically active carbazole alkaloids from Murraya koenigii. J Agric Food Chem 1999; 47: 444-47.
14. Tachibana Y, Kikuzaki H, Lajis NH, et al. Antioxidative activity of carbazoles from Murraya koenigii leaves. J Agric Food Chem 2001; 49: 5589-94.
15. Nakahara K, Trakoontivakorn G, Alzoreky NS, et al. Antimutagenicity of some edible Thai plants, and a bioactive carbazole alkaloid, mahanine, isolated from Micromelum minsutum. J Agric Food Chem 2002; 50: 4796-802.
16. Ito C, Itoigawa M, Nakao K, et al. Induction of apoptosis by carbazole alkaloids isolated from Murraya koenigii. Phytomedicine 2006; 13: 359-65.
17. Roy MK, Thalang VN, Trakoontivakorn G, et al. Mahanine, a carbazole alkaloid from Micromelum minsutum, inhibits cell growth and induces apoptosis in U937 cells through a mitochondrial dependent pathway. Br J Pharmacol 2005; 145: 145-55.
18. Roy MK, Thalang VN, Trakoontivakorn G, et al. Mechanism of mahanine-induced apoptosis in human leukemia cells (HL-60). Biochem Pharmacol 2004; 67: 41-51.
19. Sinha S, Pal BC, Jagadeesh S, et al. Mahanine inhibits growth and induces apoptosis in prostate cancer cells through the deactivation of Akt and activation of caspases. Prostate 2006; 66: 1257-65.
20. Bhattacharya K, Samanta SK, Tripathi R, et al. Apoptotic effects of mahanine on human leukemic cells are mediated through crosstalk between Apo-1/Fas signaling and the Bid protein and via mitochondrial pathways. Biochem Pharmacol 2010; 79: 361-72.
21. Jagadeesh S, Sinha S, Pal BC, et al. Mahanine reverses an epigenetically silenced tumor suppressor gene RASSF1A in human prostate cancer cells. Biochem Biophys Res Commun 2007; 362: 212-17.
22. Mosman T,. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63.
23. Bai J, Cederbaum AI,. Catalase protects HepG2 cells from apoptosis induced by DNA-damaging agents by accelerating the degradation of p53. J Biol Chem 2003; 278: 4660-67.
24. Cumming RC, Andon NL, Haynes PA, et al. Protein disulfide bond formation in the cytoplasm during oxidative stress. J Biol Chem 2004; 279: 21749-58.
25. Csermely P, Kahn CR,. The 90-kDa heat shock protein (hsp-90) possesses an ATP binding site and autophosphorylating activity. J Biol Chem 1991; 266: 4943-50.
26. Csermely P, Kajtár J, Hollósi M, et al. The 90 kDa heat shock protein (hsp90) induces the condensation of the chromatin structure. Biochem Biophys Res Commun 1994; 202: 1657-63.
27. Zhang T, Hamza A, Cao X, et al. A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Mol Cancer Ther 2008; 7: 162-70.
28. Ghoshal A, Mukhopadhyay S, Deminse R, et al. Detection and characterization of a sialoglycosylated bacterial ABC-type phosphate transporter protein from patients with visceral leishmaniasis. Glycoconj J 2009; 26: 675-89.
29. Morris GM, Huey R, Lindstrom W, et al. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 2009; 30: 2785-91.
30. Van der Spoel D, Lindahl E, Hess B, et al. GROMACS: fast, flexible, and free. J Comput Chem 2005; 26: 1701-18.
31. Lu SY, Jiang YJ, Lv J, et al. Molecular docking and molecular dynamics simulation studies of GPR40 receptor-agonist interactions. J Mol Graph Model 2010; 28: 766-74.
32. Schüttelkopf AW, Van Aalten DM,. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr D Biol Crystallogr 2004; 60: 1355-63.
33. Humphrey W, Dalke A, Schulten K,. VMD-visual molecular dynamics. J Mol Graph 1996; 14: 33-8.
34. Aqvist J, Marelius J,. The linear interaction energy method for predicting ligand binding free energies. Comb Chem HighThroughput Screen 2001; 4: 613-26.
35. Aqvist J, Luzhkov VB, Brandsdal BO,. Ligand binding affinities from MD simulations. Acc Chem Res 2002; 35: 358-65.
36. Hansson T, Aqvist J,. Estimation of binding free energies for HIV proteinase inhibitors by molecular dynamics simulations. Protein Eng 1995; 8: 1137-44.
37. Seeliger D, de Groot BL,. Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J Comput Aided Mol Des 2010; 24: 417-22.
38. Liang CC, Park AY, Guan JL,. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2007; 2: 329-33.
39. Sipos B, Möser S, Kalthoff H, et al. A comprehensive characterization of pancreatic ductal carcinoma cell lines: towards the establishment of an in vitro research platform. Virchows Arch 2003; 442: 444-52.
40. Fan TJ, Han LH, Cong RS, et al. Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 2005; 37: 719-27.
41. Clark CB, Rane MJ, El Mehdi D, et al. Role of oxidative stress in geldanamycin-induced cytotoxicity and disruption of Hsp90 signaling complex. Free Radic Biol Med 2009; 47: 1440-9.
42. Fukuyo Y, Inoue M, Nakajima T, et al. Oxidative stress plays a critical role in inactivating mutant BRAF by geldanamycin derivatives. Cancer Res 2008; 68: 6324-30.
43. Chen G, Zhang X, Zhao M, et al. Celastrol targets mitochondrial respiratory chain complex I to induce reactive oxygen species-dependent cytotoxicity in tumor cells. BMC Cancer 2011; 11: 170-82.
44. Tsutsumi S, Beebe K, Neckers L,. Impact of heat-shock protein 90 on cancer metastasis. Future Oncol 2009; 5: 679-88.
45. Ogata M, Naito Z, Tanaka S, et al. Overexpression and localization of heat shock proteins mRNA in pancreatic carcinoma. J Nippon Med Sch 2000; 67: 177-85.
46. Richardson PG, Mitsiades CS, Laubach JP, et al. Inhibition of heat shock protein 90 (HSP90) as a therapeutic strategy for the treatment of myeloma and other cancers. Br J Hematol 2011; 152: 367-79.
47. Eccles SA, Massey A, Raynaud FI, et al. NVPAUY922: a novel heat shock protein 90 inhibitor active against xenograft tumour growth, angiogenesis, and metastasis. Cancer Res 2008; 68: 2850-60.
48. Rao RV, Niazi K, Mollahan P, et al. Coupling endoplasmic reticulum stress to the cell-death program: a novel HSP90-independent role for the small chaperone protein p23. Cell Death Differ 2006; 13: 415-25.