Clusterin facilitates stress-induced lipidation of LC3 and autophagosome biogenesis to enhance cancer cell survival

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zhang, Fan ^a   Kumano, Masafumi ^a   Beraldi, Eliana ^a   Fazli, Ladan ^a   Du, Caigan ^a   Moore, Susan ^a   Sorensen, Poul ^a   Zoubeidi, Amina ^a   Gleave, Martin E ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO N [1 (4 CHLOROPHENYL) 3 HYDROXYPROPYL] 1 (7H PYRROLO[2,3 D]PYRIMIDIN 4 YL) 4 PIPERIDINECARBOXAMIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CHLOROQUINE; CLUSTERIN; CUSTIRSEN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; OLIGONUCLEOTIDE; RAPAMYCIN; SCRB OLIGONUCLEOTIDE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; 4-AMINO-N-(1-(4-CHLOROPHENYL)-3-HYDROXYPROPYL)-1-(7H-PYRROLO(2,3-D)PYRIMIDIN-4-YL)PIPERIDINE-4-CARBOXAMIDE; ATG3 PROTEIN, HUMAN; CLU PROTEIN, HUMAN; LIGHT CHAIN 3, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEOTIDE; OGX-011; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE; UBIQUITIN CONJUGATING ENZYME;

CANCER; CHEMICAL BINDING; CYTOLOGY; MEMBRANE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; BIOGENESIS; CANCER CELL LINE; CANCER INHIBITION; CELL SURVIVAL; CELL VACUOLE; CELL VIABILITY; CELL VIABILITY ASSAY; CLONOGENIC ASSAY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MALE; MITOPHAGY; MOUSE; NONHUMAN; SELECTIVE AUTOPHAGY; STRESS; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; NUDE MOUSE; PATHOLOGY; PHAGOSOME; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

MUS;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; CLUSTERIN; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; MICROTUBULE-ASSOCIATED PROTEINS; PHAGOSOMES; PROSTATIC NEOPLASMS; PYRIMIDINES; PYRROLES; SIGNAL TRANSDUCTION; THIONUCLEOTIDES; UBIQUITIN-CONJUGATING ENZYMES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84923277945     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6775     Document Type: Article

References (60)

1. Garrido, C. et al. Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 5, 2592-2601 (2006).
2. Kopito, R. R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530 (2000).
3. Ding, W. X. et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 171, 513-524 (2007).
4. Zhu, K., Dunner, Jr. K. & McConkey, D. J. Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene 29, 451-462 (2010).
5. Criswell, T. et al. Delayed activation of insulin-like growth factor-1 receptor/Src/MAPK/Egr-1 signaling regulates clusterin expression, a pro-survival factor. J. Biol. Chem. 280, 14212-14221 (2005).
6. Lamoureux, F. et al. Clusterin inhibition using OGX-011 synergistically enhances Hsp90 inhibitor activity by suppressing the heat shock response in castrate-resistant prostate cancer. Cancer Res. 71, 5838-5849 (2011).
7. Shiota, M. et al. Clusterin is a critical downstream mediator of stress-induced YB-1 transactivation in prostate cancer. Mol. Cancer Res. 9, 1755-1766 (2011).
8. Li, N., Zoubeidi, A., Beraldi, E. & Gleave, M. E. GRP78 regulates clusterin stability, retrotranslocation and mitochondrial localization under ER stress in prostate cancer. Oncogene 32, 1933-1942 (2012).
9. Poon, S. et al. Mildly acidic pH activates the extracellular molecular chaperone clusterin. J. Biol. Chem. 277, 39532-39540 (2002).
10. Trougakos, I. P. et al. Intracellular clusterin inhibits mitochondrial apoptosis by suppressing p53-activating stress signals and stabilizing the cytosolic Ku70-Bax protein complex. Clin. Cancer Res. 15, 48-59 (2009).
11. Zhang, H. et al. Clusterin inhibits apoptosis by interacting with activated Bax. Nat. Cell Biol. 7, 909-915 (2005).
12. Ammar, H. & Closset, J. L. Clusterin activates survival through the phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem. 283, 12851-12861 (2008).
13. Zoubeidi, A. et al. Clusterin facilitates COMMD1 and I-kappaB degradation to enhance NF-kappaB activity in prostate cancer cells. Mol. Cancer Res. 8, 119-130 (2010).
14. Shiota, M. et al. Clusterin mediates TGF-beta-induced epithelial-mesenchymal transition and metastasis via Twist1 in prostate cancer cells. Cancer Res. 72, 5261-5272 (2012).
15. Yom, C. K., Woo, H. Y., Min, S. Y., Kang, S. Y. & Kim, H. S. Clusterin overexpression and relapse-free survival in breast cancer. Anticancer Res. 29, 3909-3912 (2009).
16. July, L. V. et al. Clusterin expression is significantly enhanced in prostate cancer cells following androgen withdrawal therapy. Prostate 50, 179-188 (2002).
17. Sowery, R. D. et al. Clusterin knockdown using the antisense oligonucleotide OGX-011 re-sensitizes docetaxel-refractory prostate cancer PC-3 cells to chemotherapy. BJU Int. 102, 389-397 (2008).
18. Zoubeidi, A., Chi, K. & Gleave, M. Targeting the cytoprotective chaperone, clusterin, for treatment of advanced cancer. Clin. Cancer Res. 16, 1088-1093 (2010).
19. Chi, K. N. et al. Randomized phase II study of docetaxel and prednisone with or without OGX-011 in patients with metastatic castration-resistant prostate cancer. J. Clin. Oncol. 28, 4247-4254 (2010).
20. Meijer, A. J. & Codogno, P. Autophagy: regulation and role in disease. Crit. Rev. Clin. Lab. Sci. 46, 210-240 (2009).
21. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (2008).
22. Gozuacik, D. & Kimchi, A. Autophagy and cell death. Curr. Top. Dev. Biol. 78, 217-245 (2007).
23. Bettuzzi, S. et al. Genetic inactivation of ApoJ/clusterin: effects on prostate tumourigenesis and metastatic spread. Oncogene 28, 4344-4352 (2009).
24. Chayka, O. et al. Clusterin, a haploinsufficient tumor suppressor gene in neuroblastomas. J. Natl Cancer Inst. 101, 663-677 (2009).
25. Mizushima, N., Yoshimori, T. & Levine, B. Methods in mammalian autophagy research. Cell 140, 313-326 (2010).
26. He, C. & Klionsky, D. J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93 (2009).
27. Perry, C. N. et al. Novel methods for measuring cardiac autophagy in vivo. Methods Enzymol. 453, 325-342 (2009).
28. Ni, H. M. et al. Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy 7, 188-204 (2011).
29. Mizushima, N. & Kuma, A. Autophagosomes in GFP-LC3 Transgenic Mice. Methods Mol. Biol. 445, 119-124 (2008).
30. Kuma, A. & Mizushima, N. Chromosomal mapping of the GFP-LC3 transgene in GFP-LC3 mice. Autophagy 4, 61-62 (2008).
31. Ding, W. X. & Yin, X. M. Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol. Chem. 393, 547-564 (2012).
32. Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145 (2007).
33. Mizushima, N., Ohsumi, Y. & Yoshimori, T. Autophagosome formation in mammalian cells. Cell. Struct. Funct. 27, 421-429 (2002).
34. Yamada, Y. et al. The crystal structure of Atg3, an autophagy-related ubiquitin carrier protein (E2) enzyme that mediates Atg8 lipidation. J. Biol. Chem. 282, 8036-8043 (2007).
35. Johansen, T. & Lamark, T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7, 279-296 (2011).
36. Behrends, C., Sowa, M. E., Gygi, S. P. & Harper, J. W. Network organization of the human autophagy system. Nature 466, 68-76 (2010).
37. Kraft, C., Peter, M. & Hofmann, K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12, 836-841 (2010).
38. Chen, N. & Debnath, J. Autophagy and tumorigenesis. FEBS Lett. 584, 1427-1435 (2010).
39. Ryter, S. W., Cloonan, S. M. & Choi, A. M. Autophagy: a critical regulator of cellular metabolism and homeostasis. Mol. Cells 36, 7-16 (2013).
40. Nakatogawa, H., Suzuki, K., Kamada, Y. & Ohsumi, Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 10, 458-467 (2009).
41. Roy, S. & Debnath, J. Autophagy and tumorigenesis. Semin. Immunopathol. 32, 383-396 (2010).
42. Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676 (1999).
43. Hu, Y. L. et al. Hypoxia-induced autophagy promotes tumor cell survival and adaptation to antiangiogenic treatment in glioblastoma. Cancer Res. 72, 1773-1783 (2012).
44. Shi, Z. et al. A systems biology analysis of autophagy in cancer therapy. Cancer Lett. 337, 149-160 (2013).
45. Boutin, B. et al. Androgen deprivation and androgen receptor competition by bicalutamide induce autophagy of hormone-resistant prostate cancer cells and confer resistance to apoptosis. Prostate 73, 1090-1102 (2013).
46. Lamoureux, F. et al. Blocked autophagy using lysosomotropic agents sensitizes resistant prostate tumor cells to the novel Akt inhibitor AZD5363. Clin. Cancer Res. 19, 833-844 (2013).
47. Kimura, T., Takabatake, Y., Takahashi, A. & Isaka, Y. Chloroquine in cancer therapy: a double-edged sword of autophagy. Cancer Res. 73, 3-7 (2013).
48. Solomon, V. R. & Lee, H. Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies. Eur. J. Pharmacol. 625, 220-233 (2009).
49. Wyatt, A. R. et al. Clusterin facilitates in vivo clearance of extracellular misfolded proteins. Cell. Mol. Life. Sci. 68, 3919-3931 (2011).
50. Jones, S. E. & Jomary, C. Clusterin. Int. J. Biochem. Cell Biol. 34, 427-431 (2002).
51. Carver, J. A., Rekas, A., Thorn, D. C. & Wilson, M. R. Small heat-shock proteins and clusterin: intra-and extracellular molecular chaperones with a common mechanism of action and function? IUBMB Life 55, 661-668 (2003).
52. Rozenknop, A. et al. Characterization of the interaction of GABARAPL-1 with the LIR motif of NBR1. J. Mol. Biol. 410, 477-487 (2011).
53. Nezis, I. P. & Stenmark, H. p62 at the interface of autophagy, oxidative stress signaling, and cancer. Antioxid. Redox Signal 17, 786-793 (2012).
54. Su, H. & Wang, X. p62 Stages an interplay between the ubiquitin-proteasome system and autophagy in the heart of defense against proteotoxic stress. Trends Cardiovasc. Med. 21, 224-228 (2011).
55. Matsumoto, H. et al. Cotargeting androgen receptor and clusterin delays castrate-resistant prostate cancer progression by inhibiting adaptive stress response and AR stability. Cancer Res. 73, 5206-5217 (2013).
56. Ammar, H. & Closset, J. L. Clusterin activates survival through the phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem. 283, 12851-12861 (2008).
57. Miyake, H., Nelson, C., Rennie, P. S. & Gleave, M. E. Testosterone-repressed prostate message-2 is an antiapoptotic gene involved in progression to androgen independence in prostate cancer. Cancer Res. 60, 170-176 (2000).
58. Yla-Anttila, P., Vihinen, H., Jokitalo, E. & Eskelinen, E. L. Monitoring autophagy by electron microscopy in Mammalian cells. Methods Enzymol. 452, 143-164 (2009).
59. Eskelinen, E. L. Fine structure of the autophagosome. Methods Mol. Biol. 445, 11-28 (2008).
60. Li, S. et al. Reduction of cold ischemia-reperfusion injury by graft-expressing clusterin in heart transplantation. J Heart Lung Transplant 30, 819-826 (2011).