Celastrol induces unfolded protein response-dependent cell death in head and neck cancer

Experimental Cell Research

Volumn 330, Issue 2, 2015, Pages 412-422

  Fribley, Andrew M ^a,b,d   Miller, Justin R ^a,d   Brownell, Amy L ^a,d   Garshott, Danielle M ^a,b   Zeng, Qinghua ^a,b,d   Reist, Tyler E ^c   Narula, Neha ^d   Cai, Peter ^d   Xi, Yue ^a,d   Callaghan, Michael U ^a,d   Kodali, Vamsi ^e   Kaufman, Randal J ^e  

^a CHILDREN'S HOSPITAL OF MICHIGAN   (United States)

^b KARMANOS CANCER INSTITUTE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BURNHAM INSTITUTE   (United States)

Author keywords

Apoptosis; Celastrol; Chaperone; Drug discovery; ER stress; Oral cancer; Protein folding; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CELASTROL; DIHYDROCELASTROL; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; LUCIFERASE; PROTEIN IRE1; TRITERPENOID; UNCLASSIFIED DRUG; ATF4 PROTEIN, HUMAN; DDIT3 PROTEIN, HUMAN; DNA BINDING PROTEIN; EIF2AK3 PROTEIN, HUMAN; INITIATION FACTOR 2; MESSENGER RNA; PLANT EXTRACT; PROTEIN KINASE R; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR; TRIPTERINE; TRITERPENE;

APOPTOSIS; ARTICLE; CANCER CELL LINE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENETIC TRANSFECTION; HEAD AND NECK CANCER; HOMEOSTASIS; HUMAN; HUMAN CELL; MOUTH SQUAMOUS CELL CARCINOMA; SIGNAL TRANSDUCTION; SURVIVAL RATE; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOSYNTHESIS; CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; MOUTH NEOPLASMS; PATHOLOGY; PHYSIOLOGY; TRIPTERYGIUM; TUMOR CELL LINE; UBIQUITINATION;

MURINAE;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CHO CELLS; CRICETULUS; DNA-BINDING PROTEINS; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; HUMANS; MICE; MOUTH NEOPLASMS; PLANT EXTRACTS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; TRIPTERYGIUM; TRITERPENES; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE;

EID: 84919782859     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.08.014     Document Type: Article

References (50)

1. Fribley A.M., Cruz P.G., Miller J.R., Callaghan M.U., Cai P., Narula N., Neubig R.R., Showalter H.D., Larsen S.D., Kirchhoff P.D., Larsen M.J., Burr D.A., Schultz P.J., Jacobs R.R., Tamayo-Castillo G., Ron D., Sherman D.H., Kaufman R.J. Complementary cell-based high-throughput screens identify novel modulators of the unfolded protein response. J. Biomol. Screen. 2011, 16:825-835.
2. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics, 2009. CA: Cancer J. Clin. 2009, 59:225-249.
3. Han J., Back S.H., Hur J., Lin Y.H., Gildersleeve R., Shan J., Yuan C.L., Krokowski D., Wang S., Hatzoglou M., Kilberg M.S., Sartor M.A., Kaufman R.J. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 2013, 15:481-490.
4. Larsson O., Li S., Issaenko O.A., Avdulov S., Peterson M., Smith K., Bitterman P.B., Polunovsky V.A. Eukaryotic translation initiation factor 4E induced progression of primary human mammary epithelial cells along the cancer pathway is associated with targeted translational deregulation of oncogenic drivers and inhibitors. Cancer Res. 2007, 67:6814-6824.
5. Kerekatte V., Smiley K., Hu B., Smith A., Gelder F., De Benedetti A. The proto-oncogene/translation factor eIF4E: a survey of its expression in breast carcinomas. Int. J. Cancer 1995, 64:27-31.
6. Crew J.P., Fuggle S., Bicknell R., Cranston D.W., de Benedetti A., Harris A.L. Eukaryotic initiation factor-4E in superficial and muscle invasive bladder cancer and its correlation with vascular endothelial growth factor expression and tumour progression. Br J Cancer 2000, 82:161-166.
7. Rosenwald I.B., Hutzler M.J., Wang S., Savas L., Fraire A.E. Expression of eukaryotic translation initiation factors 4E and 2alpha is increased frequently in bronchioloalveolar but not in squamous cell carcinomas of the lung. Cancer 2001, 92:2164-2171.
8. Wang S., Lloyd R.V., Hutzler M.J., Rosenwald I.B., Safran M.S., Patwardhan N.A., Khan A. Expression of eukaryotic translation initiation factors 4E and 2alpha correlates with the progression of thyroid carcinoma. Thyroid 2001, 11:1101-1107.
9. Wang S., Rosenwald I.B., Hutzler M.J., Pihan G.A., Savas L., Chen J.J., Woda B.A. Expression of the eukaryotic translation initiation factors 4E and 2alpha in non-Hodgkin[U+05F3]s lymphomas. Am J. Pathol. 1999, 155:247-255.
10. Rosenwald I.B., Chen J.J., Wang S., Savas L., London I.M., Pullman J. Upregulation of protein synthesis initiation factor eIF-4E is an early event during colon carcinogenesis. Oncogene 1999, 18:2507-2517.
11. Assouline S., Culjkovic B., Cocolakis E., Rousseau C., Beslu N., Amri A., Caplan S., Leber B., Roy D.C., Miller W.H., Borden K.L. Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): a proof-of-principle clinical trial with ribavirin. Blood 2009, 114:257-260.
12. Franklin S., Pho T., Abreo F.W., Nassar R., De Benedetti A., Stucker F.J., Nathan C.O. Detection of the proto-oncogene eIF4E in larynx and hypopharynx cancers. Arch. Otolaryngol. Head Neck Surg. 1999, 125:177-182.
13. Altman B.J., Wofford J.A., Zhao Y., Coloff J.L., Ferguson E.C., Wieman H.L., Day A.E., Ilkayeva O., Rathmell J.C. Autophagy provides nutrients but can lead to Chop-dependent induction of Bim to sensitize growth factor-deprived cells to apoptosis. Mol. Biol. Cell 2009, 20:1180-1191.
14. Nathan C.O., Liu L., Li B.D., Abreo F.W., Nandy I., De Benedetti A. Detection of the proto-oncogene eIF4E in surgical margins may predict recurrence in head and neck cancer. Oncogene 1997, 15:579-584.
15. He D., Xu Q., Yan M., Zhang P., Zhou X., Zhang Z., Duan W., Zhong L., Ye D., Chen W. The NF-kappa B inhibitor, celastrol, could enhance the anti-cancer effect of gambogic acid on oral squamous cell carcinoma. BMC Cancer 2009, 9:343.
16. Feldman D.E., Chauhan V., Koong A.C. The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol. Cancer Res.: MCR 2005, 3:597-605.
17. Romero-Ramirez L., Cao H., Nelson D., Hammond E., Lee A.H., Yoshida H., Mori K., Glimcher L.H., Denko N.C., Giaccia A.J., Le Q.T., Koong A.C. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res. 2004, 64:5943-5947.
18. Bi M., Naczki C., Koritzinsky M., Fels D., Blais J., Hu N., Harding H., Novoa I., Varia M., Raleigh J., Scheuner D., Kaufman R.J., Bell J., Ron D., Wouters B.G., Koumenis C. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 2005, 24:3470-3481.
19. Abbott A. Neurologists strike gold in drug screen effort. Nature 2002, 417:109.
20. Raja S.M., Clubb R.J., Ortega-Cava C., Williams S.H., Bailey T.A., Duan L., Zhao X., Reddi A.L., Nyong A.M., Natarajan A., Band V., Band H. Anticancer activity of Celastrol in combination with ErbB2-targeted therapeutics for treatment of ErbB2-overexpressing breast cancers. Cancer Biol. Ther. 2011, 11:263-276.
21. Pang X., Yi Z., Zhang J., Lu B., Sung B., Qu W., Aggarwal B.B., Liu M. Celastrol suppresses angiogenesis-mediated tumor growth through inhibition of AKT/mammalian target of rapamycin pathway. Cancer Res. 2010, 70:1951-1959.
22. Abbas S., Bhoumik A., Dahl R., Vasile S., Krajewski S., Cosford N.D., Ronai Z.A. Preclinical studies of celastrol and acetyl isogambogic acid in melanoma. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2007, 13:6769-6778.
23. Peng B., Xu L., Cao F., Wei T., Yang C., Uzan G., Zhang D. HSP90 inhibitor, celastrol, arrests human monocytic leukemia cell U937 at G0/G1 in thiol-containing agents reversible way. Mol. Cancer 2010, 9:79.
24. Chen M., Rose A.E., Doudican N., Osman I., Orlow S.J. Celastrol synergistically enhances temozolomide cytotoxicity in melanoma cells. Mol Cancer Res: MCR 2009, 7:1946-1953.
25. Chow A.M., Brown I.R. Induction of heat shock proteins in differentiated human and rodent neurons by celastrol. Cell Stress Chaperones 2007, 12:237-244.
26. Fribley, A.M., Miller, J.R., Reist, T.E., Callaghan, M.U., and Kaufman, R.J. Large-Scale Analysis of UPR-Mediated Apoptosis in Human Cells. Methods Enzymol. 491, 57-71.
27. Park J.W., Woo K.J., Lee J.T., Lim J.H., Lee T.J., Kim S.H., Choi Y.H., Kwon T.K. Resveratrol induces pro-apoptotic endoplasmic reticulum stress in human colon cancer cells. Oncol Rep. 2007, 18:1269-1273.
28. D.P. Flaherty, J.E. Golden, C. Liu, M. Hedrick, P. Gosalia, Y. Li, M. Milewski, E. Sugarman, E. Suyama, K. Nguyen, S. Vasile, S. Salaniwal, D. Stonich, Y. Su, A. Mangravita-Novo, M. Vicchiarelli, L.H. Smith, J. Diwan, T.D.Y. Chung, A.B. Pinkerton, J. Aube, J.R. Miller, D.M. Garshott, M.U. Callaghan, A.M. Fribley, R.J. Kaufman, (2010) Selective small molecule activator of the apoptotic arm of the UPR. in Probe Reports from the NIH Molecular Libraries Program, Bethesda (MD). pp.
29. Yang H.S., Kim J.Y., Lee J.H., Lee B.W., Park K.H., Shim K.H., Lee M.K., Seo K.I. Celastrol isolated from Tripterygium regelii induces apoptosis through both caspase-dependent and -independent pathways in human breast cancer cells. Food Chem Toxicol: Int J. published Br.Indus. Biol. Res. Assoc. 2011, 49:527-532.
30. Ge P., Ji X., Ding Y., Wang X., Fu S., Meng F., Jin X., Ling F., Luo Y. Celastrol causes apoptosis and cell cycle arrest in rat glioma cells. Neurol. Res. 2010, 32:94-100.
31. Fribley A., Zeng Q., Wang C.Y. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol. Cell Biol. 2004, 24:9695-9704.
32. Bush K.T., Goldberg A.L., Nigam S.K. Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J. BiolChem. 1997, 272:9086-9092.
33. Perez-Galan P., Roue G., Villamor N., Montserrat E., Campo E., Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood 2006, 107:257-264.
34. Sung B., Park B., Yadav V.R., Aggarwal B.B. Celastrol, a triterpene, enhances TRAIL-induced apoptosis through the down-regulation of cell survival proteins and up-regulation of death receptors. J. Biol. Chem. 2010, 285:11498-11507.
35. Sethi G., Ahn K.S., Pandey M.K., Aggarwal B.B. 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 2007, 109:2727-2735.
36. Zhu H., Yang W., He L.J., Ding W.J., Zheng L., Liao S.D., Huang P., Lu W., He Q.J., Yang B. Upregulating Noxa by ER stress, celastrol exerts synergistic anti-cancer activity in combination with ABT-737 in human hepatocellular carcinoma cells. PLoS One 2012, 7:e52333.
37. Yang H., Chen D., Cui Q.C., Yuan X., Dou Q.P. 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. 2006, 66:4758-4765.
38. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 2001, 7:1165-1176.
39. Setty A.R., Sigal L.H. Herbal medications commonly used in the practice of rheumatology: mechanisms of action, efficacy, and side effects. Sem. Arthr. Rheum. 2005, 34:773-784.
40. Westerheide S.D., Bosman J.D., Mbadugha B.N., Kawahara T.L., Matsumoto G., Kim S., Gu W., Devlin J.P., Silverman R.B., Morimoto R.I. Celastrols as inducers of the heat shock response and cytoprotection. J. Biol. Chem. 2004, 279:56053-56060.
41. Mu T.W., Ong D.S., Wang Y.J., Balch W.E., Yates J.R., Segatori L., Kelly J.W. Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell 2008, 134:769-781.
42. Dai Y., Desano J., Tang W., Meng X., Meng Y., Burstein E., Lawrence T.S., Xu L. Natural proteasome inhibitor celastrol suppresses androgen-independent prostate cancer progression by modulating apoptotic proteins and NF-kappaB. PLoS One 2010, 5:e14153.
43. Zhou L.L., Lin Z.X., Fung K.P., Cheng C.H., Che C.T., Zhao M., Wu S.H., Zuo Z. Celastrol-induced apoptosis in human HaCaT keratinocytes involves the inhibition of NF-kappaB activity. EurJ. pharmacol. 2011, 670:399-408.
44. Huang Y., Zhou Y., Fan Y., Zhou D. Celastrol inhibits the growth of human glioma xenografts in nude mice through suppressing VEGFR expression. Cancer Lett. 2008, 264:101-106.
45. Wang W.B., Feng L.X., Yue Q.X., Wu W.Y., Guan S.H., Jiang B.H., Yang M., Liu X., Guo D.A. Paraptosis accompanied by autophagy and apoptosis was induced by celastrol, a natural compound with influence on proteasome, ER stress and Hsp90. J. Cell. Physiol. 2011.
46. Trott A., West J.D., Klaic L., Westerheide S.D., Silverman R.B., Morimoto R.I., Morano K.A. Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol. Biol. Cell 2008, 19:1104-1112.
47. Menendez-Benito V., Verhoef L.G., Masucci M.G., Dantuma N.P. Endoplasmic reticulum stress compromises the ubiquitin-proteasome system. Human Mol. Genet. 2005, 14:2787-2799.
48. Fribley A., Wang C.Y. Proteasome inhibitor induces apoptosis through induction of endoplasmic reticulum stress. Cancer Biol. Ther. 2006, 5:745-748.
49. Nawrocki S.T., Carew J.S., Dunner K., Boise L.H., Chiao P.J., Huang P., Abbruzzese J.L., McConkey D.J. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res. 2005, 65:11510-11519.
50. Fels D.R., Ye J., Segan A.T., Kridel S.J., Spiotto M., Olson M., Koong A.C., Koumenis C. Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways. Cancer Res. 2008, 68:9323-9330.