Liposomal honokiol induced lysosomal degradation of Hsp90 client proteins and protective autophagy in both gefitinib-sensitive and gefitinib-resistant NSCLC cells

Biomaterials

Volumn 141, Issue , 2017, Pages 188-198

  Yang, Jianhong ^a   Wu, Wenshuang ^a   Wen, Jiaolin ^a   Ye, Haoyu ^a   Luo, Hong ^b   Bai, Peng ^a   Tang, Minghai ^a   Wang, Fang ^a   Zheng, Li ^a   Yang, Shengyong ^a   Li, Weimin ^a   Peng, Aihua ^a   Yang, Li ^a   Wan, Li ^c   Chen, Lijuan ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

^c CHENGDU UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Autophagy; EGFR; Gefitinib resistance; Honokiol; HSP90

Indexed keywords

CELL CULTURE; CELL MEMBRANES; CELLS; DISEASES; ELECTRIC RESISTANCE; MOLECULAR BIOLOGY; PROTEINS;

AUTOPHAGY; EGFR; GEFITINIB; HONOKIOL; HSP90;

CYTOLOGY;

4 PHENYLBUTYRIC ACID; AUTOPHAGY RELATED PROTEIN 7; BECLIN 1; CASPASE 3; CASPASE 8; CISPLATIN; CYTOTOXIC AGENT; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; GELATINASE A; GELATINASE B; HEAT SHOCK PROTEIN 90; HONOKIOL; HYPOXIA INDUCIBLE FACTOR 1ALPHA; I KAPPA B BETA; I KAPPA B KINASE ALPHA; INITIATION FACTOR 2ALPHA; LIPOSOME; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PACLITAXEL; PROTEIN KINASE B; RAF PROTEIN; SMALL INTERFERING RNA; SURVIVIN; VASCULOTROPIN RECEPTOR 2; ANTINEOPLASTIC AGENT; BIPHENYL DERIVATIVE; LIGNAN; LIPOSOMAL HONOKIOL; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER RESISTANCE; CELL DEATH; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; HISTONE ACETYLATION; IC50; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUNG CANCER CELL LINE; LYSOSOME; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MISFOLDING; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT; UBIQUITINATION; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; DRUG RESISTANCE; HUMAN; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; BIPHENYL COMPOUNDS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LIGNANS; LUNG NEOPLASMS; MICE, INBRED BALB C; MICE, NUDE; QUINAZOLINES; SIGNAL TRANSDUCTION;

EID: 85021752286     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2017.07.002     Document Type: Article

References (48)

1. Pao, W., Miller, V.A., Politi, K.A., Riely, G.J., Somwar, R., Zakowski, M.F., et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. Plos Med. 2 (2005), 225–235.
2. Trepel, J., Mollapour, M., Giaccone, G., Neckers, L., Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 10 (2010), 537–549.
3. Scroggins, B.T., Robzyk, K., Wang, D., Marcu, M.G., Tsutsumi, S., Beebe, K., et al. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol. Cell, 25, 2007, 151.
4. Rao, R., Fiskus, W., Yang, Y., Lee, P., Joshi, R., Fernandez, P., et al. HDAC6 inhibition enhances 17-AAG–mediated abrogation of hsp90 chaperone function in human leukemia cells. Blood, 112, 2008, 1886.
5. Shimamura, T., Li, D., Ji, H., Haringsma, H.J., Liniker, E., Borgman, C.L., et al. Hsp90 inhibition suppresses mutant EGFR-T790M signaling and overcomes kinase inhibitor resistance. Cancer Res., 68, 2008, 5827.
6. Koizumi, H., Yamada, T., Takeuchi, S., Nakagawa, T., Kita, K., Nakamura, T., et al. Hsp90 inhibition overcomes HGF-triggering resistance to EGFR-TKIs in EGFR-mutant lung cancer by decreasing client protein expression and angiogenesis. J. Thorac. Oncol. Off. Publ. Int. Assoc. Study Lung Cancer 7 (2012), 1078–1085.
7. Shintani, T., Klionsky, D.J., Autophagy in health and disease: a double-edged sword. Science, 306, 2004, 990.
8. Yorimitsu, T., Nair, U., Yang, Z., Klionsky, D.J., Endoplasmic reticulum stress triggers autophagy. J. Biol. Chem. 281 (2006), 30299–30304.
9. Ishida, Y., Nagata, K., Autophagy eliminates a specific species of misfolded procollagen and plays a protective role in cell survival against ER stress. Autophagy 5 (2009), 1217–1219.
10. Ciechanover, A., The ubiquitin–proteasome pathway: on protein death and cell life. Embo J. 17 (1998), 7151–7160.
11. Zhang, H., Burrows, F., Targeting multiple signal transduction pathways through inhibition of Hsp90. J. Mol. Med., 82, 2004, 488.
12. Shen, S., Zhang, P., Lovchik, M.A., Li, Y., Tang, L., Chen, Z., et al. Cyclodepsipeptide toxin promotes the degradation of Hsp90 client proteins through chaperone-mediated autophagy. J. Cell Biol., 185, 2009, 629.
13. Guoliang, Qing, Pengrong, Gutian, Xiao. Hsp90 inhibition results in autophagy-mediated proteasome-independent degradation of IκB kinase (IKK). Cell Res. 16 (2006), 895–901.
14. Chen, L., Zhang, Q., Yang, G., Fan, L., Tang, J., Garrard, I., et al. Rapid purification and scale-up of honokiol and magnolol using high-capacity high-speed counter-current chromatography. J. Chromatogr. A 1142 (2007), 115–122.
15. Pillai, V.B., Samant, S., Sundaresan, N.R., Raghuraman, H., Kim, G., Bonner, M.Y., et al. Honokiol blocks and reverses cardiac hypertrophy in mice by activating mitochondrial Sirt3. Nat. Commun., 6, 2015, 6656.
16. Scheepstra, M., Nieto, L., Hirsch, A.K., Fuchs, S., Leysen, S., Lam, C.V., et al. A natural-product switch for a dynamic protein interface. Angew. Chem. 53 (2014), 6443–6448.
17. Chen, X., Hyphenrui, Lu R., Dan, H., Hyphenxia, Liao G., et al. Honokiol: a promising small molecular weight natural agent for the growth inhibition of oral squamous cell carcinoma cells., 3, 2011, 34–42.
18. Ken-Hu Chang, M.-D.Y., Chih-Jung, Yao, Pei-Chun, Lin, Gi-Ming, Lai, Honokiol-induced apoptosis and autophagy in glioblastoma multiforme cells. Oncol. Lett. 6 (2013), 1435–1438.
19. Shigemura, K., Arbiser, J.L., Sun, S.Y., Zayzafoon, M., Johnstone, P.A., Fujisawa, M., et al. Honokiol, a natural plant product, inhibits the bone metastatic growth of human prostate cancer cells. Cancer 109 (2007), 1279–1289.
20. Bai, X., Cerimele, F., Ushiofukai, M., Waqas, M., Campbell, P.M., Govindarajan, B., et al. Honokiol, a small molecular weight natural product, inhibits angiogenesis in vitro and tumor growth in vivo. J. Biol. Chem., 278, 2003, 35501.
21. Tse, A.K., Wan, C.K., Shen, X.L., Yang, M., Fong, W.F., Honokiol inhibits TNF-alpha-stimulated NF-kappaB activation and NF-kappaB-regulated gene expression through suppression of IKK activation. Biochem. Pharmacol. 70 (2005), 1443–1457.
22. Battle, T.E., Arbiser, J., Frank, D.A., The natural product honokiol induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia (B-CLL) cells., 106, 2005, 690–697.
23. Ishitsuka, K., Hideshima, T., Hamasaki, M., Raje, N., Kumar, S., Hideshima, H., et al. Honokiol overcomes conventional drug resistance in human multiple myeloma by induction of caspase-dependent and -independent apoptosis. Blood, 106, 2005, 1794.
24. Crane, C., Panner, A., Pieper, R.O., Arbiser, J., Parsa, A.T., Honokiol mediated inhibition of PI3K/mTOR pathway: a potential strategy to overcome immunoresistance in glioma, breast and prostate carcinoma without impacting T cell function. J. Immunother., 32, 2009, 585.
25. Hahm, E.R., Sakao, K., Singh, S.V., Honokiol activates reactive oxygen species-mediated cytoprotective autophagy in human prostate cancer cells. Prostate 74 (2014), 1209–1221.
26. Wen, J., Fu, A.F., Chen, L.J., Xie, X.J., Yang, G.L., Chen, X.C., et al. Liposomal honokiol inhibits VEGF-D-induced lymphangiogenesis and metastasis in xenograft tumor model. Int. J. Cancer J. Int. Du Cancer 124 (2009), 2709–2718.
27. Yang, J., Zhou, Y., Cheng, X., Fan, Y., He, S., Li, S., et al. Isogambogenic acid induces apoptosis-independent autophagic cell death in human non-small-cell lung carcinoma cells. Sci. Rep., 5, 2015, 7697.
28. Lamark, T., Johansen, T., Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int. J. Cell Biol., 2012, 2012 736905.
29. Ling, B., Liang, S.F., Xu, Y.H., Zhao, X.Y., Tang, M.H., Liu, X.Y., et al. Differential proteomic analysis of HeLa cells treated with Honokiol using a quantitative proteomic strategy. Amino Acids 35 (2008), 115–122.
30. Marcu, M.G., Doyle, M., Bertolotti, A., Ron, D., Hendershot, L., Neckers, L., Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha. Mol. Cell. Biol., 22, 2002, 8506.
31. Davenport, E.L., Moore, H.E., Dunlop, A.S., Sharp, S.Y., Workman, P., Morgan, G.J., et al. Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood 110 (2007), 2641–2649.
32. Vincenz, L., Jäger, R., O'Dwyer, M., Samali, A., Endoplasmic reticulum stress and the unfolded protein response: targeting the Achilles heel of multiple myeloma. Mol. Cancer Ther. 12 (2013), 831–843.
33. Schröder, M., Kaufman, R.J., The mammalian unfolded protein response. Annu. Rev. Biochem., 74, 2005, 739.
34. Klionsky, D.J., Cuervo, A.M., Seglen, P.O., Methods for monitoring autophagy from yeast to human. Autophagy, 3, 2007, 181.
35. Moscat, J., Diazmeco, T.M., p62 at the crossroads of autophagy, apoptosis, and cancer. Cell, 137, 2009, 1001.
36. Yang, Z., Klionsky, D.J., An Overview of the Molecular Mechanism of Autophagy: Springer Berlin Heidelberg. 2009.
37. Puthalakath, H., O'Reilly, L.A., Gunn, P., Lee, L., Kelly, P.N., Huntington, N.D., et al. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell, 129, 2007, 1337.
38. Young, M.M., Takahashi, Y., Khan, O., Park, S., Hori, T., Yun, J., et al. Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis. J. Biol. Chem. 287 (2012), 12455–12468.
39. Kim, Y.S., Alarcon, S.V., Lee, S., Lee, M.J., Giaccone, G., Neckers, L., et al. Update on Hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 9 (2009), 1479–1492.
40. Liou, S.F., Hua, K.T., Hsu, C.Y., Weng, M.S., Honokiol from Magnolia spp. induces G1 arrest via disruption of EGFR stability through repressing HDAC6 deacetylated Hsp90 function in lung cancer cells. J. Funct. Foods 15 (2015), 84–96.
41. Singh, T., Prasad, R., Katiyar, S.K., Inhibition of class I histone deacetylases in non-small cell lung cancer by honokiol leads to suppression of cancer cell growth and induction of cell death in vitro and in vivo. Epigenetics Off. J. Dna Methylation Soc., 8, 2012, 54.
42. Leemanneill, R.J., Cai, Q., Joyce, S.C., Thomas, S.M., Bhola, N.E., Neill, D.B., et al. Honokiol inhibits epidermal growth factor receptor signaling and enhances the antitumor effects of epidermal growth factor receptor inhibitors. Clin. Cancer Res. 16 (2010), 2571–2579.
43. Mortimore, G.E., Poso, A.R., Intracellular protein catabolism and its control during nutrient deprivation and supply. Annu. Rev. Nutr. 7 (1987), 539–564.
44. Fuertes, G., Villarroya, A., Knecht, E., Role of proteasomes in the degradation of short-lived proteins in human fibroblasts under various growth conditions. Int. J. Biochem. Cell Biol., 35, 2003, 651.
45. Korac, J., Schaeffer, V., Kovacevic, I., Clement, A.M., Jungblut, B., Behl, C., et al. Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J. Cell Sci., 126, 2013, 580.
46. Bustamante, H.A., Rivera-Dictter, A., Cavieres, V.A., Muñoz, V.C., González, A., Lin, Y., et al. Turnover of C99 is controlled by a crosstalk between ERAD and ubiquitin-independent lysosomal degradation in human neuroglioma cells. Plos One, 8, 2013 e83096.
47. Taiyab, A., Sreedhar, A.S., Rao, C., Hsp90 inhibitors, GA and 17AAG, lead to ER stress-induced apoptosis in rat histiocytoma. Biochem. Pharmacol., 78, 2009, 142.
48. Manni, S., Brancalion, A., Tubi, L.Q., Colpo, A., Pavan, L., Cabrelle, A., et al. Protein kinase CK2 protects multiple myeloma cells from ER stress-induced apoptosis and from the cytotoxic effect of HSP90 inhibition through regulation of the unfolded protein response. Clin. Cancer Res., 18, 2012, 1888.