Natural product celastrol destabilizes tubulin heterodimer and facilitates mitotic cell death triggered by microtubule-targeting anti-cancer drugs

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Jo, Hakryul ^a   Loison, Fabien ^a   Hattori, Hidenori ^a   Silberstein, Leslie E ^a   Yu, Hongtao ^b   Luo, Hongbo R ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CASPASE; CELASTROL; DIMETHYL SULFOXIDE; HETERODIMER; PROTEASOME; PURVALANOL A; TANESPIMYCIN; TUBULIN; VINBLASTINE; ANTINEOPLASTIC AGENT; BIOLOGICAL PRODUCT; TRIPTERINE; TRITERPENE;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL DEATH; CELL MIGRATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; DEPOLYMERIZATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG STRUCTURE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOSIS INHIBITION; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; OLIGOMERIZATION; PROTEIN PHOSPHORYLATION; PURIFICATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; DRUG RESISTANCE; HELA CELL; MICROTUBULE; MITOSIS; PROTEIN MULTIMERIZATION; PROTEIN STABILITY;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BIOLOGICAL PRODUCTS; CELLS, CULTURED; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HELA CELLS; HUMANS; MICROTUBULES; MITOSIS; NEUTROPHILS; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; TRITERPENES; TUBULIN;

EID: 77956397168     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010318     Document Type: Article

References (44)

1. Luders J, Stearns T (2007) Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8: 161-167.
2. Hammond JW, Cai D, Verhey KJ (2008) Tubulin modifications and their cellular functions. Curr Opin Cell Biol 20: 71-76.
3. Janke C, Rogowski K, Wloga D, Regnard C, Kajava AV, et al. (2005) Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science 308: 1758-1762.
4. Gaertig J, Wloga D (2008) Ciliary tubulin and its post-translational modifications. Curr Top Dev Biol 85: 83-113.
5. Weisbrich A, Honnappa S, Jaussi R, Okhrimenko O, Frey D, et al. (2007) Structure-function relationship of CAP-Gly domains. Nat Struct Mol Biol 14: 959-967.
6. Steinmetz MO, Akhmanova A (2008) Capturing protein tails by CAP-Gly domains. Trends Biochem Sci 33: 535-545.
7. Fukasawa K (2007) Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7: 911-924.
8. Hunt JT (2009) Discovery of ixabepilone. Mol Cancer Ther 8: 275-281.
9. Mooberry SL (2007) Strategies for the development of novel Taxol-like agents. Methods Mol Med 137: 289-302.
10. Burris HA, 3rd (2008) Preclinical investigations with epothilones in breast cancer models. Semin Oncol 35: S15-S21; quiz S39.
11. Nagle A, Hur W, Gray NS (2006) Antimitotic agents of natural origin. Curr Drug Targets 7: 305-326.
12. Shi J, Orth JD, Mitchison T (2008) Cell type variation in responses to antimitotic drugs that target microtubules and kinesin-5. Cancer Res 68: 3269-3276.
13. Symmans WF, Volm MD, Shapiro RL, Perkins AB, Kim AY, et al. (2000) Paclitaxel-induced apoptosis and mitotic arrest assessed by serial fine-needle aspiration: implications for early prediction of breast cancer response to neoadjuvant treatment. Clin Cancer Res 6: 4610-4617.
14. Milross CG, Mason KA, Hunter NR, Chung WK, Peters LJ, et al. (1996) Relationship of mitotic arrest and apoptosis to antitumor effect of paclitaxel. J Natl Cancer Inst 88: 1308-1314.
15. Zhu D, Hattori H, Jo H, Jia Y, Subramanian KK, et al. (2006) Deactivation of phosphatidylinositol 3,4,5-trisphosphate/Akt signaling mediates neutrophil spontaneous death. Proc Natl Acad Sci U S A 103: 14836-14841.
16. Jo H, Jia Y, Subramanian KK, Hattori H, Luo HR (2008) Cancer cell-derived clusterin modulates the phosphatidylinositol 39-kinase-Akt pathway through attenuation of insulin-like growth factor 1 during serum deprivation. Mol Cell Biol 28: 4285-4299.
17. Whitfield ML, Zheng LX, Baldwin A, Ohta T, Hurt MM, et al. (2000) Stem-loop binding protein, the protein that binds the 39 end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol Cell Biol 20: 4188-4198.
18. Corson TW, Crews CM (2007) Molecular understanding and modern application of traditional medicines: triumphs and trials. Cell 130: 769-774.
19. Yang H, Chen D, Cui QC, Yuan X, Dou QP (2006) Celastrol, a triterpene extracted from the Chinese ''Thunder of God Vine,'' is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice. Cancer Res 66: 4758-4765.
20. Hieronymus H, Lamb J, Ross KN, Peng XP, Clement C, et al. (2006) Gene expression signature-based chemical genomic prediction identifies a novel class of HSP90 pathway modulators. Cancer Cell 10: 321-330.
21. Zhang T, Hamza A, Cao X, Wang B, Yu S, et al. (2008) A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Mol Cancer Ther 7: 162-170.
22. Sethi G, Ahn KS, Pandey MK, Aggarwal BB (2007) Celastrol, a novel triterpene, potentiates TNF-induced apoptosis and suppresses invasion of tumor cells by inhibiting NF-kappaB-regulated gene products and TAK1-mediated NF-kappaB activation. Blood 109: 2727-2735.
23. de Carcer G (2004) Heat shock protein 90 regulates the metaphase-anaphase transition in a polo-like kinase-dependent manner. Cancer Res 64: 5106-5112.
24. de Carcer G, do Carmo Avides M, Lallena MJ, Glover DM, Gonzalez C (2001) Requirement of Hsp90 for centrosomal function reflects its regulation of Polo kinase stability. Embo J 20: 2878-2884.
25. Prosser SL, Straatman KR, Fry AM (2009) Molecular dissection of the centrosome overduplication pathway in S-phase-arrested cells. Mol Cell Biol 29: 1760-1773.
26. Toyoshima F, Matsumura S, Morimoto H, Mitsushima M, Nishida E (2007) PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells. Dev Cell 13: 796-811.
27. Martin SR, Clark DC, Mayley PM (1982) Interactions of tubulin and microtubule-associated proteins. Conformation and stability of the oligomeric species from glycerol-cycled microtubule protein of bovine brain. Biochem J 203: 643-652.
28. Correia JJ, Lipscomb LD, Dabrowiak JC, Isern N, Zubieta J (1994) Cleavage of tubulin by vanadateion. Arch Biochem Biophys 309: 94-104.
29. Carlier MF, Simon C, Pantaloni D (1984) Polymorphism of tubulin oligomers in the presence of microtubule-associated proteins. Implications in microtubule assembly. Biochemistry 23: 1582-1590.
30. Barton JS, Riazi GH (1982) Evidence against tubulin oligomer dissociation to tubulin dimer at assembly temperatures. Biochim Biophys Acta 705: 8-11.
31. Correia JJ, Lipscomb LD, Lobert S (1993) Nondisulfide crosslinking and chemical cleavage of tubulin subunits: pH and temperature dependence. Arch Biochem Biophys 300: 105-114.
32. Lewis SA, Tian G, Cowan NJ (1997) The alpha- and beta-tubulin folding pathways. Trends Cell Biol 7: 479-484.
33. O'Connor DS, Wall NR, Porter AC, Altieri DC (2002) A p34(cdc2) survival checkpoint in cancer. Cancer Cell 2: 43-54.
34. Morgan DO (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 13: 261-291.
35. Hassane DC, Guzman ML, Corbett C, Li X, Abboud R, et al. (2008) Discovery of agents that eradicate leukemia stem cells using an in silico screen of public gene expression data. Blood 111: 5654-5662.
36. Jin HZ, Hwang BY, Kim HS, Lee JH, Kim YH, et al. (2002) Antiinflammatory constituents of Celastrus orbiculatus inhibit the NF-kappaB activation and NO production. J Nat Prod 65: 89-91.
37. Miyata N, Gon Y, Nunomura S, Endo D, Yamashita K, et al. (2008) Inhibitory effects of parthenolide on antigen-induced microtubule formation and degranulation in mast cells. Int Immunopharmacol 8: 874-880.
38. Fonrose X, Ausseil F, Soleilhac E, Masson V, David B, et al. (2007) Parthenolide inhibits tubulin carboxypeptidase activity. Cancer Res 67: 3371-3378.
39. Mi L, Gan N, Cheema A, Dakshanamurthy S, Yang DC, et al. (2009) Cancer preventive isothiocyanates induce selective degradation of cellular alpha- and beta-tubulins by proteasomes. J Biol Chem.
40. Mi L, Xiao Z, Hood BL, Dakshanamurthy S, Wang X, et al. (2008) Covalent binding to tubulin by isothiocyanates. A mechanism of cell growth arrest and apoptosis. J Biol Chem 283: 22136-22146.
41. Banerjee M, Poddar A, Mitra G, Surolia A, Owa T, et al. (2005) Sulfonamide drugs binding to the colchicine site of tubulin: thermodynamic analysis of the drug-tubulin interactions by isothermal titration calorimetry. J Med Chem 48: 547-555.
42. Ross-Macdonald P, de Silva H, Guo Q, Xiao H, Hung CY, et al. (2008) Identification of a nonkinase target mediating cytotoxicity of novel kinase inhibitors. Mol Cancer Ther 7: 3490-3498.
43. Lin YF, Tsai WP, Liu HG, Liang PH (2009) Intracellular beta-tubulin/ chaperonin containing TCP1-beta complex serves as a novel chemotherapeutic target against drug-resistant tumors. Cancer Res 69: 6879-6888.
44. Peris L, Thery M, Faure J, Saoudi Y, Lafanechere L, et al. (2006) Tubulin tyrosination is a major factor affecting the recruitment of CAP-Gly proteins at microtubule plus ends. J Cell Biol 174: 839-849.