Targeting endoplasmic reticulum signaling pathways in cancer

Acta Oncologica

Volumn 51, Issue 7, 2012, Pages 822-830

  Martinon, Fabio ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ANTINEOPLASTIC AGENT; BORTEZOMIB; CALRETICULIN; ENDONUCLEASE; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; INDINAVIR; INITIATION FACTOR 2ALPHA; MESSENGER RNA; NELFINAVIR; PROTEIN IRE1; RITONAVIR; X BOX BINDING PROTEIN 1;

5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; APOPTOSIS; CANCER CELL; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CELL PH; CELL SURVIVAL; CELLULAR STRESS SIGNAL; DRUG APPROVAL; DRUG EFFICACY; DRUG INDICATION; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; EUKARYOTE; HYPOXIA; IMMUNOGENICITY; MULTIPLE MYELOMA; NEOPLASM; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BORONIC ACIDS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HIV PROTEASE INHIBITORS; HUMANS; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PYRAZINES; SIGNAL TRANSDUCTION;

EID: 84866359928     PISSN: 0284186X     EISSN: 1651226X     Source Type: Journal    
DOI: 10.3109/0284186X.2012.689113     Document Type: Review

References (78)

1. Hetz C, Martinon F, Rodriguez D, Glimcher LH. The unfolded protein response: Integrating stress signals through the stress sensor IRE1. Physiol Rev 2011;91: 1219-43.
2. Stevens FJ, Argon Y. Protein folding in the ER. Semin Cell Dev Biol 1999;10:443-54. (Pubitemid 129513232)
3. Walter P, Ron D. The unfolded protein response: From stress pathway to homeostatic regulation. Science 2011;334: 1081-6.
4. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011;13:184-90.
5. Matus S, Glimcher LH, Hetz C. Protein folding stress in neurodegenerative diseases: A glimpse into the ER. Curr Opin Cell Biol 2011;23:239-52.
6. Fonseca SG, Gromada J, Urano F. Endoplasmic reticulum stress and pancreatic α-cell death. Trends Endocrinol Metab 2011;22:266-74.
7. Martinon F, Glimcher LH. Regulation of innate immunity by signaling pathways emerging from the endoplasmic reticulum. Curr Opin Immunol 2011;23:35-40.
8. Hotamisligil GS. Endoplasmic reticulum stress and the infl ammatory basis of metabolic disease. Cell 2010;140:900-17.
9. Healy SJM, Gorman AM, Mousavi-Shafaei P, Gupta S, Samali A. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur J Pharmacol 2009;625:234-46.
10. Maiuolo J, Bulotta S, Verderio C, Benfante R, Borgese N. Selective activation of the transcription factor ATF6 mediates endoplasmic reticulum proliferation triggered by a membrane protein. Proc Natl Acad Sci USA 2011;108:7832-7.
11. Glimcher LH, Lee A-H. From sugar to fat: How the transcription factor XBP1 regulates hepatic lipogenesis. Ann N Y Acad Sci 2009;1173(Suppl 1):E2-9.
12. Lin JH, Walter P, Yen TSB. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol 2008;3:399-425. (Pubitemid 351488287)
13. Hetz C, Glimcher LH. Fine-tuning of the unfolded protein response: assembling the IRE1α Interactome. Mol Cell 2009;35:551-61.
14. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009;186:323-31.
15. Han D, Lerner AG, Vande Walle L, Upton J-P, Xu W, Hagen A, et al. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009;138:562-75.
16. Proud CG. eIF2 and the control of cell physiology. Semin Cell Dev Biol 2005;16:3-12.
17. Fels DR, Koumenis C. The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biol Ther 2006;5:723-8. (Pubitemid 44794028)
18. Ameri K, Harris AL. Activating transcription factor 4. Int J Biochem Cell Biol 2008;40:14-21. (Pubitemid 350064577)
19. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: The PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 2006;38:317-32. (Pubitemid 41821881)
20. Maiuolo J, Bulotta S, Verderio C, Benfante R, Borgese N. Selective activation of the transcription factor ATF6 mediates endoplasmic reticulum proliferation triggered by a membrane protein. Proc Natl Acad Sci USA 2011;108:7832-7.
21. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007;13:351-64. (Pubitemid 47308675)
22. Yamamoto K, Sato T, Matsui T, Sato M, Okada T, Yoshida H, et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 2007;13:365-76. (Pubitemid 47308680)
23. Ma Y, Hendershot LM. The role of the unfolded protein response in tumour development: Friend or foe? Nat Rev Cancer 2004;4:966-77. (Pubitemid 39626220)
24. Koong AC, Chauhan V, Romero-Ramirez L. Targeting XBP-1 as a novel anti-cancer strategy. Cancer Biol Ther 2006;5: 756-9. (Pubitemid 44775129)
25. Romero-Ramirez L, Cao H, Nelson D, Hammond E, Lee A-H, Yoshida H, et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 2004;64:5943-7. (Pubitemid 39129389)
26. Kurata M, Yamazaki Y, Kanno Y, Ishibashi S, Takahara T, Kitagawa M, et al. Anti-apoptotic function of Xbp1 as an IL-3 signaling molecule in hematopoietic cells. Cell Death Disease 2011;2:e118.
27. Carrasco DR, Sukhdeo K, Protopopova M, Sinha R, Enos M, Carrasco DE, et al. The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 2007;11:349-60. (Pubitemid 46518314)
28. Auf G, Jabouille A, Gué rit S, Pineau R, Delugin M, Bouchecareilh M, et al. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma. Proc Natl Acad Sci USA 2010;107:15553-8.
29. Martinon F, Chen X, Lee A-H, Glimcher LH. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol 2010;11:411-8.
30. Duan Q, Wang X, Gong W, Ni L, Chen C, He X, et al. ER stress negatively modulates the expression of the miR-199a/214 cluster to regulates tumor survival and progression in human hepatocellular cancer. PLoS ONE 2012;7:e31518.
31. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N, et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 2002;22:7405-16.
32. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, et a l. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005;24: 3470-81. (Pubitemid 41486784)
33. Blais JD, Addison CL, Edge R, Falls T, Zhao H, Wary K, et a l. Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol Cell Biol 2006;26:9517-32. (Pubitemid 44904443)
34. Stockwell SR, Platt G, Barrie SE, Zoumpoulidou G, Poele te RH, Aherne GW, et al. Mechanism-based screen for G1/S checkpoint activators identifi es a selective activator of EIF2AK3/PERK signalling. PLoS ONE 2012;7:e28568.
35. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011;144:646-74.
36. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the infl ammatory response. Nature 2008;454:455-62.
37. Mahadevan NR, Rodvold J, Sepulveda H, Rossi S, Drew AF, Zanetti M. Transmission of endoplasmic reticulum stress and pro-infl ammation from tumor cells to myeloid cells. Proc Natl Acad Sci USA 2011;108:6561-6.
38. Mahadevan NR, Zanetti M. Tumor stress inside out: Cellextrinsic effects of the unfolded protein response in tumor cells modulate the immunological landscape of the tumor microenvironment. J Immunol 2011;187:4403-9.
39. Kepp O, Galluzzi L, Martins I, Schlemmer F, Adjemian S, Michaud M, et al. Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metast Rev 2011;30:61-9.
40. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011;334:1573-7.
41. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini J-L, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007;13:54-61. (Pubitemid 46067386)
42. Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J Epub 2012 Jan 17.
43. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund A-C, Chapman DC, et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009;28:578-90.
44. Kraskiewicz H, FitzGerald U. InterfERing with endoplasmic reticulum stress. Trends Pharmacol Sci 2012;33:53-63.
45. Schleicher SM, Moretti L, Varki V, Lu B. Progress in the unraveling of the endoplasmic reticulum stress/autophagy pathway and cancer: Implications for future therapeutic approaches. Drug Resist Update 2010;13:79-86.
46. Iwakoshi NN, Lee A-H, Glimcher LH. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol Rev 2003;194:29-38. (Pubitemid 36886426)
47. Mahindra A, Laubach J, Raje N, Munshi N, Richardson PG, Anderson K. Latest advances and current challenges in the treatment of multiple myeloma. Nat Rev Clin Oncol Epub 2012 Feb 21.
48. Obeng EA, Carlson LM, Gutman DM, Harrington WJ, Lee KP, Boise LH. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006;107:4907-16. (Pubitemid 43882644)
49. Lee A-H, Iwakoshi NN, Anderson KC, Glimcher LH. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Natl Acad Sci USA 2003;100: 9946-51. (Pubitemid 37087048)
50. Nawrocki ST, Carew JS, Pino MS, Highshaw RA, Dunner K, Huang P, et al. Bortezomib sensitizes pancreatic cancer cells to endoplasmic reticulum stress-mediated apoptosis. Cancer Res 2005;65:11658-66. (Pubitemid 41821726)
51. Fels DR, Ye J, Segan AT, Kridel SJ, Spiotto M, Olson M, et al. Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways. Cancer Res 2008;68:9323-30.
52. D'Arcy P, Brnjic S, Olofsson MH, Fryknä s M, Lindsten K, De Cesare M, et al. Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nat Med 2011;17: 1636-40.
53. Cvek B, Dvorak Z. The ubiquitin-proteasome system (UPS) and the mechanism of action of bortezomib. Curr Pharm Des 2011;17:1483-99.
54. Palella FJ, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, et al. Declining morbidity and mortality among patients with advanced human immunodefi ciency virus infection. HIV Outpatient Study Investigators. N Engl J Med 1998;338:853-60. (Pubitemid 28135961)
55. International Collaboration on HIV and Cancer. Highly active antiretroviral therapy and incidence of cancer in human immunodefi ciency virus-infected adults. J Natl Cancer Inst 2000;92:1823-30.
56. Ledergerber B, Telenti A, Egger M. Risk of HIV related Kaposi ' s sarcoma and non-Hodgkin ' s lymphoma with potent antiretroviral therapy: Prospective cohort study. Swiss HIV Cohort Study. BMJ 1999;319:23-4. (Pubitemid 29304340)
57. Lebbé C, Blum L, Pellet C, Blanchard G, Vé rola O, Morel P, et al. Clinical and biological impact of antiretroviral therapy with protease inhibitors on HIV-related Kaposi's sarcoma. AIDS 1998;12:F45-9.
58. Bower M, Fox P, Fife K, Gill J, Nelson M, Gazzard B. Highly active anti-retroviral therapy (HAART) prolongs time to treatment failure in Kaposi's sarcoma. AIDS 1999;13: 2105-11. (Pubitemid 29509588)
59. Chen L, Jarujaron S, Wu X, Sun L, Zha W, Liang G, et al. HIV protease inhibitor lopinavir-induced TNF-alpha and IL-6 expression is coupled to the unfolded protein response and ERK signaling pathways in macrophages. Biochem Pharmacol 2009;78:70-7.
60. Ikezoe T, Saito T, Bandobashi K, Yang Y, Koeffl er HP, Taguchi H. HIV-1 protease inhibitor induces growth arrest and apoptosis of human multiple myeloma cells via inactivation of signal transducer and activator of transcription 3 and extracellular signal-regulated kinase 1/2. 2004;3:473-9.
61. Yang Y, Ikezoe T, Takeuchi T, Adachi Y, Ohtsuki Y, Takeuchi S, et al. HIV-1 protease inhibitor induces growth arrest and apoptosis of human prostate cancer LNCaP cells in vitro and in vivo in conjunction with blockade of androgen receptor STAT3 and AKT signaling. Cancer Sci 2005;96: 425-33. (Pubitemid 41179744)
62. Jiang W, Mikochik PJ, Ra JH, Lei H, Flaherty KT, Winkler JD, et al. HIV protease inhibitor nelfi navir inhibits growth of human melanoma cells by induction of cell cycle arrest. Cancer Res 2007;67:1221-7.
63. Srirangam A, Mitra R, Wang M, Gorski JC, Badve S, Baldridge L, et al. Effects of HIV protease inhibitor ritonavir on Akt-regulated cell proliferation in breast cancer. Clin Cancer Res 2006;12:1883-96.
64. Maggiorella L, Wen B, Frascogna V, Opolon P, Bourhis J, Deutsch E. Combined radiation sensitizing and anti-angiogenic effects of ionizing radiation and the protease inhibitor ritonavir in a head and neck carcinoma model. Anticancer Res 2005;25:4357-62. (Pubitemid 41665228)
65. Esposito V, Palescandolo E, Spugnini EP, Montesarchio V, De Luca A, Cardillo I, et al. Evaluation of antitumoral properties of the protease inhibitor indinavir in a murine model of hepatocarcinoma. Clin Cancer Res 2006;12:2634-9.
66. Gaedicke S, Firat-Geier E, Constantiniu O, Lucchiari-Hartz M, Freudenberg M, Galanos C, et al. Antitumor effect of the human immunodefi ciency virus protease inhibitor ritonavir: Induction of tumor-cell apoptosis associated with perturbation of proteasomal proteolysis. Cancer Res 2002;62:6901-8. (Pubitemid 35424079)
67. Pyrko P, Kardosh A, Wang W, Xiong W, Schö n thal AH, Chen TC. HIV-1 protease inhibitors nelfi navir and atazanavir induce malignant glioma death by triggering endoplasmic reticulum stress. Cancer Res 2007;67:10920-8. (Pubitemid 350145921)
68. Monini P, Sgadari C, Toschi E, Barillari G, Ensoli B. Antitumour effects of antiretroviral therapy. Nat Rev Cancer 2004;4:861-75. (Pubitemid 39472953)
69. Yang Y, Ikezoe T, Nishioka C, Bandobashi K, Takeuchi T, Adachi Y, et al. NFV, an HIV-1 protease inhibitor, induces growth arrest, reduced Akt signalling, apoptosis and docetaxel sensitisation in NSCLC cell lines. Br J Cancer 2006;95: 1653-62. (Pubitemid 44950790)
70. Gupta AK, Cerniglia GJ, Mick R, McKenna WG, Muschel RJ. HIV protease inhibitors block Akt signaling and radiosensitize tumor cells both in vitro and in vivo. Cancer Res 2005;65:8256-65. (Pubitemid 41330590)
71. Pore N, Gupta AK, Cerniglia GJ, Jiang Z, Bernhard EJ, Evans SM, et al. Nelfi navir down-regulates hypoxia-inducible factor 1alpha and VEGF expression and increases tumor oxygenation: Implications for radiotherapy. Cancer Res 2006;66: 9252-9. (Pubitemid 44521147)
72. Andr é P, Groettrup M, Klenerman P, de Giuli R, Booth BL, Cerundolo V, et al. An inhibitor of HIV-1 protease modulates proteasome activity, antigen presentation, and T cell responses. Proc Natl Acad Sci USA 1998;95:13120-4.
73. Gupta AK, Li B, Cerniglia GJ, Ahmed MS, Hahn SM, Maity A. The HIV protease inhibitor nelfi navir downregulates Akt phosphorylation by inhibiting proteasomal activity and inducing the unfolded protein response. Neoplasia 2007;9: 271-8. (Pubitemid 46608294)
74. Wu W, Zhang R, Salahub DR. Nelfi navir: A magic bullet to annihilate cancer cells? Cancer Biol Ther 2009;8:233-5.
75. Gills JJ, Lopiccolo J, Dennis PA. Nelfi navir, a new anti-cancer drug with pleiotropic effects and many paths to autophagy. Autophagy 2008;4:107-9.
76. Fribley AM, Cruz PG, Miller JR, Callaghan MU, Cai P, Narula N, et al. Complementary cell-based high-throughput screens identify novel modulators of the unfolded protein response. J Biomol Screen 2011;16:825-35.
77. Papandreou I, Denko NC, Olson M, Van Melckebeke H, Lust S, Tam A, et al. Identifi cation of an Ire1alpha endonuclease specifi c inhibitor with cytotoxic activity against human multiple myeloma. Blood 2011;117:1311-4.
78. Volkmann K, Lucas JL, Vuga D, Wang X, Brumm D, Stiles C, et al. Potent and selective inhibitors of the inositolrequiring enzyme 1 endoribonuclease. J Biol Chem 2011;286: 12743-55.