Hsp70 inhibition induces myeloma cell death via the intracellular accumulation of immunoglobulin and the generation of proteotoxic stress

Cancer Letters

Volumn 339, Issue 1, 2013, Pages 49-59

  Zhang, Lei ^a   Fok, Jacqueline J L ^a   Mirabella, Fabio ^a   Aronson, Lauren I ^a   Fryer, Rosemary A ^a   Workman, Paul ^a   Morgan, Gareth J ^a   Davies, Faith E ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

ER stress; Haematology; Hsp70; Multiple myeloma; Protein folding

Indexed keywords

HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 72; IMMUNOGLOBULIN; PROTEASOME; SHORT HAIRPIN RNA; UBIQUITIN;

ARTICLE; CELL DEATH; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM STRESS; ENZYME DEGRADATION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MULTIPLE MYELOMA; MYELOMA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN TARGETING;

ER STRESS; HAEMATOLOGY; HSP70; MULTIPLE MYELOMA; PROTEIN FOLDING;

CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; GENE SILENCING; HSC70 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOGLOBULINS; INTRACELLULAR SPACE; MULTIPLE MYELOMA; RNA INTERFERENCE; STRESS, PHYSIOLOGICAL; UBIQUITIN;

EID: 84883456569     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.07.023     Document Type: Article

References (49)

1. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295(5561):1852-1858.
2. Craig E.A. Chaperones: helpers along the pathways to protein folding. Science 1993, 260(5116):1902-1903.
3. Hartl F.U. Molecular chaperones in cellular protein folding. Nature 1996, 381(6583):571-579.
4. Robert J. Evolution of heat shock protein and immunity. Dev. Comp. Immunol. 2003, 27(6-7):449-464.
5. Travers J., Sharp S., Workman P. HSP90 inhibition: two-pronged exploitation of cancer dependencies. Drug Discov. Today 2012, 17(5-6):242-252.
6. Powers M.V., et al. Targeting HSP70: the second potentially druggable heat shock protein and molecular chaperone?. Cell Cycle 2010, 9(8):1542-1550.
7. Trepel J., et al. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 2010, 10(8):537-549.
8. A.R. Goloudina, O.N. Demidov, C. Garrido, Inhibition of HSP70: a challenging anti-cancer strategy. Cancer Lett., vol. 325, no. 2, (2012) pp. 117-24.
9. Voss A.K., Thomas T., Gruss P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development 2000, 127(1):1-11.
10. Palumbo A., Anderson K. Multiple myeloma. N. Engl. J. Med. 2011, 364(11):1046-1060.
11. Davenport E.L., et al. Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood 2007, 110(7):2641-2649.
12. Clarke P.A., et al. Gene expression profiling of human colon cancer cells following inhibition of signal transduction by 17-allylamino-17-demethoxygeldanamycin, an inhibitor of the hsp90 molecular chaperone. Oncogene 2000, 19(36):4125-4133.
13. Maloney A., et al. Gene and protein expression profiling of human ovarian cancer cells treated with the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res. 2007, 67(7):3239-3253.
14. Dittmar K.D., Pratt W.B. Folding of the glucocorticoid receptor by the reconstituted Hsp90-based chaperone machinery. The initial hsp90.p60.hsp70-dependent step is sufficient for creating the steroid binding conformation. J. Biol. Chem. 1997, 272(20):13047-13054.
15. Arispe N., De Maio A. ATP and ADP modulate a cation channel formed by Hsc70 in acidic phospholipid membranes. J. Biol. Chem. 2000, 275(40):30839-30843.
16. Jiang R., et al. Hsc70 chaperones clathrin and primes it to interact with vesicle membranes. J. Biol. Chem. 2000, 275(12):8439-8447.
17. Gao Y., et al. Heat shock protein 70 together with its co-chaperone CHIP inhibits TNF-alpha induced apoptosis by promoting proteasomal degradation of apoptosis signal-regulating kinase1. Apoptosis 2010, 15(7):822-833.
18. Moore H.E., et al. Aminopeptidase inhibition as a targeted treatment strategy in myeloma. Mol. Cancer Ther. 2009, 8(4):762-770.
19. Szulc J., Aebischer P. Conditional gene expression and knockdown using lentivirus vectors encoding shRNA. Meth. Mol. Biol. 2008, 434:291-309. (Clifton, NJ).
20. Obeng E.A., et al. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006, 107(12):4907-4916.
21. Meister S., et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res. 2007, 67(4):1783-1792.
22. Klausner R.D., Sitia R. Protein degradation in the endoplasmic reticulum. Cell 1990, 62(4):611-614.
23. Mancini R., et al. Degradation of unassembled soluble Ig subunits by cytosolic proteasomes: evidence that retrotranslocation and degradation are coupled events. FASEB J. 2000, 14(5):769-778.
24. Fagioli C., Mezghrani A., Sitia R. Reduction of interchain disulfide bonds precedes the dislocation of Ig-mu chains from the endoplasmic reticulum to the cytosol for proteasomal degradation. J. Biol. Chem. 2001, 276(44):40962-40967.
25. Jiang J., et al. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J. Biol. Chem. 2001, 276(46):42938-42944.
26. Pirkkala L., Nykanen P., Sistonen L. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 2001, 15(7):1118-1131.
27. Davenport E.L., Morgan G.J., Davies F.E. Untangling the unfolded protein response. Cell Cycle 2008, 7(7):865-869.
28. Chiang H.L., et al. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 1989, 246(4928):382-385.
29. Agarraberes F.A., Terlecky S.R., Dice J.F. An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J. Cell. Biol. 1997, 137(4):825-834.
30. Hoang B., et al. Effect of autophagy on multiple myeloma cell viability. Mol. Cancer Ther. 2009, 8(7):1974-1984.
31. Aronson L.I., Davies F.E. DangER: protein ovERload. Targeting protein degradation to treat myeloma. Haematologica 2012, 97(8):1119-1130.
32. Aronson L.I., et al. Understanding the interplay between the proteasome pathway and autophagy in response to dual PI3K/mTOR inhibition in myeloma cells is essential for their effective clinical application. Leukemia 2013.
33. Massey A.J., et al. A novel, small molecule inhibitor of Hsc70/Hsp70 potentiates Hsp90 inhibitor induced apoptosis in HCT116 colon carcinoma cells. Cancer Chemother. Pharmacol. 2010, 66(3):535-545.
34. Powers M.V., Clarke P.A., Workman P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 2008, 14(3):250-262.
35. Park S.H., et al. The cytoplasmic Hsp70 chaperone machinery subjects misfolded and endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitin-proteasome system. Mol. Biol. Cell 2007, 18(1):153-165.
36. Evans C.G., Chang L., Gestwicki J.E. Heat shock protein 70 (hsp70) as an emerging drug target. J. Med. Chem. 2010, 53(12):4585-4602.
37. Chatterjee M., et al. The PI3K/Akt signalling pathway regulates the expression of Hsp70, which critically contributes to Hsp90-chaperone function and tumor cell survival in multiple myeloma. Haematologica 2012.
38. O'Hare T., et al. Cutting edge: proteasome involvement in the degradation of unassembled Ig light chains. J. Immunol. 1999, 163(1):11-14.
39. Ho S.C., et al. Accelerated proteasomal degradation of membrane Ig heavy chains. J. Immunol. 2000, 164(9):4713-4719.
40. Dice J.F. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem. Sci. 1990, 15(8):305-309.
41. Cuervo A.M., Dice J.F. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 1996, 273(5274):501-503.
42. Majeski A.E., Dice J.F. Mechanisms of chaperone-mediated autophagy. Int. J. Biochem. Cell. Biol. 2004, 36(12):2435-2444.
43. Massey A., Kiffin R., Cuervo A.M. Pathophysiology of chaperone-mediated autophagy. Int. J. Biochem. Cell. Biol. 2004, 36(12):2420-2434.
44. Neckers L., Workman P. Hsp90 molecular chaperone inhibitors: are we there yet?. Clin. Cancer Res. 2012, 18(1):64-76.
45. Ahn S.G., et al. Heat-shock cognate 70 is required for the activation of heat-shock factor 1 in mammalian cells. Biochem. J. 2005, 392(Pt 1):145-152.
46. Shi Y., Mosser D.D., Morimoto R.I. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 1998, 12(5):654-666.
47. Ciocca D.R., Arrigo A.P., Calderwood S.K. Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update. Arch. Toxicol. 2013, 87(1):19-48.
48. Workman P., Collins I. Probing the probes: fitness factors for small molecule tools. Chem. Biol. 2010, 17(6):561-577.
49. Davenport E.L., et al. Targeting heat shock protein 72 enhances Hsp90 inhibitor-induced apoptosis in myeloma. Leukemia 2010, 24(10):1804-1807.