Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways

Cancer Research

Volumn 68, Issue 22, 2008, Pages 9323-9330

  Fels, Diane R ^a,b   Ye, Jiangbin ^a   Segan, Andrew T ^a   Kridel, Steven J ^b   Spiotto, Michael ^c   Olson, Michael ^c   Koong, Albert C ^c   Koumenis, Constantinos ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; CYCLOHEXIMIDE; THAPSIGARGIN;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER INHIBITION; CELL DEATH; COLORECTAL CARCINOMA; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; HELA CELL; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; TUMOR CELL; UNFOLDED PROTEIN RESPONSE; UTERINE CERVIX CARCINOMA;

ACTIVATING TRANSCRIPTION FACTOR 4; ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BORONIC ACIDS; CELL HYPOXIA; CELL LINE, TUMOR; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NECROSIS; PROTEASE INHIBITORS; PROTEIN FOLDING; PYRAZINES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; THAPSIGARGIN; TRANSCRIPTION FACTORS;

EID: 56449087512     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2873     Document Type: Article

References (48)

1. Brown JM. Tumor hypoxia in cancer therapy. Methods Enzymol 2007;435:297-321.
2. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32.
3. Le QT, Denko NC, Giaccia AJ. Hypoxic gene expression and metastasis. Cancer Metastasis Rev 2004;23:293-310.
4. Koumenis C, Naczki C, Koritzinsky M, et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2a. Mol Cell Biol 2002;22:7405-16.
5. Blais JD, Filipenko V, Bi M, et al. Activating Transcription Factor 4 Is Translationally Regulated by Hypoxic Stress. Mol Cell Biol 2004;24:7469-82.
6. Koritzinsky M, Magagnin MG, van den Beucken T, et al. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J 2006;25:1114-25.
7. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell 2006;21: 521-31.
8. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-29.
9. Bi M, Naczki C, Koritzinsky M, et al. ER stressregulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005;24: 3470-81.
10. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001;107:881-91.
11. Calfon M, Zeng H, Urano F, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002;415:92-6.
12. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998;12:982-95.
13. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000;101:249-58.
14. Richardson PG, Mitsiades C, Hideshima T, Anderson KC. BORTEZOMIB: proteasome inhibition as an effective anticancer therapy. Annu Rev Med 2006;57:33-47.
15. Hideshima T, Richardson P, Chauhan D, et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 2001;61:3071-6.
16. Lee A-H, Iwakoshi NN, Anderson KC, Glimcher LH. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Natl Acad Sci U S A 2003;100:9946-51.
17. 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;24:9695-704.
18. Nawrocki ST, Carew JS, Dunner K, Jr., et al. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res 2005;65: 11510-9.
19. Obeng E, Carlson L, Gutman D, Harrington JW, Lee K, LH. B. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006;107:4907-16.
20. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003; 278:20915-24. Epub 2003 Mar 28.
21. Dong D, Ni M, Li J, et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res 2008;68:498-505.
22. Pyrko P, Schonthal AH, Hofman FM, Chen TC, Lee AS. The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res 2007;67:9809-16.
23. Ameri K, Lewis CE, Raida M, Sowter H, Hai T, Harris AL. Anoxic induction of ATF-4 through HIF-1-independent pathways of protein stabilization in human cancer cells. Blood 2004;103:1876-82.
24. Koditz J, Nesper J, Wottawa M, et al. Oxygendependent ATF-4 stability is mediated by the PHD3 oxygen sensor. Blood 2007;110:3610-7.
25. Romero-Ramirez L, Cao H, Nelson D, et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 2004;64:5943-7.
26. Denmeade SR, Jakobsen CM, Janssen S, et al. Prostate-specific antigen-activated thapsigargin prodrug as targeted therapy for prostate cancer. J Natl Cancer Inst 2003;95:990-1000.
27. Veschini L, Belloni D, Foglieni C, et al. Hypoxiainducible transcription factor-1 α determines sensitivity of endothelial cells to the proteosome inhibitor bortezomib. Blood 2007;109:2565-70.
28. Novoa I ZY, Zeng H, Jungreis R, Harding HP, Ron D. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 2003;22: 1180-7.
29. Ma Y, Hendershot LM. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 2003;278:34864-73.
30. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000;5:897-904.
31. Scheuner D, Song B, McEwen E, et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 2001;7: 1165-76.
32. Hitomi J, Katayama T, Eguchi Y, et al. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and A{h}-induced cell death. J Cell Biol 2004;165:347-56.
33. Bernales S MK, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 2006;4:e423.
34. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem 2006;281:30299-304.
35. Kouroku Y, Fujita E, Tanida I, et al. ER stress (PERK/ eIF2α phosphorylation) mediates the polyglutamineinduced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007;14:230-9. Epub 2006 Jun 23.
36. Ogata M, Hino S-I, Saito A, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006;26:9220-31.
37. Degenhardt K, Mathew R, Beaudoin B, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006;10:51-64.
38. Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000;19:5720-8.
39. Amaravadi RK, Thompson CB. The roles of therapyinduced autophagy and necrosis in cancer treatment. Clin Cancer Res 2007;13:7271-9.
40. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999;402:672-6.
41. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418:191-5.
42. Jiang H-Y, Wek RC. Phosphorylation of the {α}-subunit of the eukaryotic initiation factor-2 (eIF2{α}) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 2005; 280:14189-202.
43. Karantza-Wadsworth V, Patel S, Kravchuk O, et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 2007; 21:1621-35.
44. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000;287: 664-6.
45. Ding W-X, Ni H-M, Gao W, et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007;171:513-24.
46. Shin DH, Chun YS, Lee DS, Huang LE, Park JW. Bortezomib inhibits tumor adaptation to hypoxia by stimulating the FIH-mediated repression of hypoxiainducible factor-1. Blood 2008;111:3131-6. Epub 2008 Jan 3.
47. Fu Y, Lee AS. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol Ther 2006;5:741-4. Epub 2006 Jul 1.
48. Ma Y, Hendershot LM. The role of the unfolded protein response in tumour development: friend or foe? Nat Rev Cancer 2004;4:966-77.