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PMID: 17353921 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Targeting homeostatic mechanisms of endoplasmic reticulum stress to increase susceptibility of cancer cells to fenretinide-induced apoptosis: the role of stress proteins ERdj5 and ERp57.

British journal of cancer ·Vol. 96 ·No. 7 ·2007-04-10 ·Pages 1062-71

Corazzari M, Lovat PE, Armstrong JL, Fimia GM, Hill DS, Birch-Machin M, Redfern CP, Piacentini M

Abstract

Endoplasmic reticulum (ER) malfunction, leading to ER stress, can be a consequence of genome instability and hypoxic tissue environments. Cancer cells survive by acquiring or enhancing survival mechanisms to counter the effects of ER stress and these homeostatic responses may be new therapeutic targets. Understanding the links between ER stress and apoptosis may be approached using drugs specifically to target ER stress responses in cancer cells. The retinoid analogue fenretinide [N-(4-hydroxyphenyl) retinamide] is a new cancer preventive and chemotherapeutic drug, that induces apoptosis of some cancer cell types via oxidative stress, accompanied by induction of an ER stress-related transcription factor, GADD153. The aim of this study was to test the hypothesis that fenretinide induces ER stress in neuroectodermal tumour cells, and to elucidate the role of ER stress responses in fenretinide-induced apoptosis. The ER stress genes ERdj5, ERp57, GRP78, calreticulin and calnexin were induced in neuroectodermal tumour cells by fenretinide. In contrast to the apoptosis-inducing chemotherapeutic drugs vincristine and temozolomide, fenretinide induced the phosphorylation of eIF2alpha, expression of ATF4 and splicing of XBP-1 mRNA, events that define ER stress. In these respects, fenretinide displayed properties similar to the ER stress inducer thapsigargin. ER stress responses were inhibited by antioxidant treatment. Knockdown of ERp57 or ERdj5 by RNA interference in these cells increased the apoptotic response to fenretinide. These data suggest that downregulating homeostatic ER stress responses may enhance apoptosis induced by oxidative stress-inducing drugs acting through the ER stress pathway. Therefore, ER-resident proteins such as ERdj5 and ERp57 may represent novel chemotherapeutic targets.

MeSH Terms
Activating Transcription Factor 4/genetics,metabolism Alternative Splicing Antineoplastic Agents/pharmacology Apoptosis/drug effects Biomarkers, Tumor/metabolism DNA-Binding Proteins/genetics,metabolism Endoplasmic Reticulum/metabolism Endoplasmic Reticulum Chaperone BiP Eukaryotic Initiation Factor-2/genetics,metabolism Fenretinide/pharmacology HSP40 Heat-Shock Proteins Humans Molecular Chaperones/antagonists & inhibitors,genetics,metabolism Neuroblastoma/drug therapy,metabolism,pathology Neuroectodermal Tumors/drug therapy,metabolism,pathology Nuclear Proteins/genetics,metabolism Oligonucleotide Array Sequence Analysis Oxidative Stress Phosphorylation/drug effects Protein Disulfide-Isomerases/antagonists & inhibitors,genetics,metabolism RNA, Messenger/genetics,metabolism RNA, Small Interfering/pharmacology Reactive Oxygen Species/metabolism Regulatory Factor X Transcription Factors Transcription Factors Tumor Cells, Cultured/drug effects X-Box Binding Protein 1
Chemicals
ATF4 protein, human Antineoplastic Agents Biomarkers, Tumor DNA-Binding Proteins DNAJC10 protein, human Endoplasmic Reticulum Chaperone BiP Eukaryotic Initiation Factor-2 HSP40 Heat-Shock Proteins HSPA5 protein, human Molecular Chaperones Nuclear Proteins RNA, Messenger RNA, Small Interfering Reactive Oxygen Species Regulatory Factor X Transcription Factors Transcription Factors X-Box Binding Protein 1 XBP1 protein, human Activating Transcription Factor 4 Fenretinide Protein Disulfide-Isomerases PDIA3 protein, human
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Corazzari M
1INMI-IRCCS Lazzaro Spallanzani, Rome 00149, Italy.
Lovat P E
Armstrong J L
Fimia G M
Hill D S
Birch-Machin M
Redfern C P F
Piacentini M
References (40)
40 references, click to expand
  1. ERdj5, an endoplasmic reticulum (ER)-resident protein containing DnaJ and thioredoxin domains, is expressed in secretory cells or following ER stress.
    J Biol Chem. 2003 Jan 10;278(2):1059-66 PMID: 12411443
  2. Effector mechanisms of fenretinide-induced apoptosis in neuroblastoma.
    Exp Cell Res. 2000 Oct 10;260(1):50-60 PMID: 11010810
  3. Possible involvement of both endoplasmic reticulum-and mitochondria-dependent pathways in thapsigargin-induced apoptosis in human neuroblastoma SH-SY5Y cells.
    J Pharmacol Sci. 2003 Jul;92(3):228-36 PMID: 12890888
  4. Fenretinide: a prototype cancer prevention drug.
    Expert Opin Investig Drugs. 2003 Nov;12(11):1829-42 PMID: 14585058
  5. Growth and DNA damage-inducible transcription factor 153 mediates apoptosis in response to fenretinide but not synergy between fenretinide and chemotherapeutic drugs in neuroblastoma.
    Mol Pharmacol. 2003 Dec;64(6):1370-8 PMID: 14645667
  6. The fusion oncoprotein PML-RARalpha induces endoplasmic reticulum (ER)-associated degradation of N-CoR and ER stress.
    J Biol Chem. 2004 Mar 19;279(12):11814-24 PMID: 14701861
  7. Coupling endoplasmic reticulum stress to the cell death program.
    Cell Death Differ. 2004 Apr;11(4):372-80 PMID: 14765132
  8. ERp57 is a multifunctional thiol-disulfide oxidoreductase.
    J Biol Chem. 2004 Apr 30;279(18):18277-87 PMID: 14871896
  9. Gangliosides link the acidic sphingomyelinase-mediated induction of ceramide to 12-lipoxygenase-dependent apoptosis of neuroblastoma in response to fenretinide.
    J Natl Cancer Inst. 2004 Sep 1;96(17):1288-99 PMID: 15339967
  10. Molecular mechanisms of neurotoxicity of pathological prion protein.
    Curr Mol Med. 2004 Jun;4(4):397-403 PMID: 15354870
  11. 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 Nov;24(22):9695-704 PMID: 15509775
  12. A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice.
    J Natl Cancer Inst. 1984 Apr;72(4):913-7 PMID: 6584666
  13. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA.
    Nature. 2002 Jan 3;415(6867):92-6 PMID: 11780124
  14. N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes.
    Leukemia. 2002 May;16(5):902-10 PMID: 11986953
  15. GADD153 and 12-lipoxygenase mediate fenretinide-induced apoptosis of neuroblastoma.
    Cancer Res. 2002 Sep 15;62(18):5158-67 PMID: 12234979
  16. Neuronal apoptosis induced by endoplasmic reticulum stress.
    Neurochem Res. 2002 Sep;27(9):891-8 PMID: 12396099
  17. Regulation of translational initiation during cellular responses to stress.
    Prog Nucleic Acid Res Mol Biol. 1998;58:79-125 PMID: 9308364
  18. N-(4-hydroxyphenyl) retinamide is cytotoxic to melanoma cells in vitro through induction of programmed cell death.
    Int J Cancer. 1999 Apr 12;81(2):262-7 PMID: 10188729
  19. Signal transduction from the endoplasmic reticulum to the cell nucleus.
    Physiol Rev. 1999 Jul;79(3):683-701 PMID: 10390516
  20. Calcium signaling and cytotoxicity.
    Environ Health Perspect. 1999 Feb;107 Suppl 1:25-35 PMID: 10229704
  21. Apoptosis and carcinogenesis.
    Br J Cancer. 1999 Jul;80 Suppl 1:34-7 PMID: 10466759
  22. Chaperone proteins involved in troglitazone-induced toxicity in human hepatoma cell lines.
    Toxicol Sci. 2005 Feb;83(2):293-302 PMID: 15525695
  23. The NF-kappaB pathway mediates fenretinide-induced apoptosis in SH-SY5Y neuroblastoma cells.
    Apoptosis. 2005 May;10(3):493-8 PMID: 15909111
  24. Differential regulation of noxa in normal melanocytes and melanoma cells by proteasome inhibition: therapeutic implications.
    Cancer Res. 2005 Jul 15;65(14):6294-304 PMID: 16024631
  25. Cellular functions of endoplasmic reticulum chaperones calreticulin, calnexin, and ERp57.
    Int Rev Cytol. 2005;245:91-121 PMID: 16125546
  26. Lysosomes and endoplasmic reticulum: targets for improved, selective anticancer therapy.
    Drug Resist Updat. 2005 Aug;8(4):199-204 PMID: 16055370
  27. Activation of the unfolded protein response is necessary and sufficient for reducing topoisomerase IIalpha protein levels and decreasing sensitivity to topoisomerase-targeted drugs.
    Mol Pharmacol. 2005 Dec;68(6):1699-707 PMID: 16141312
  28. Proteasome inhibition: a new approach for the treatment of malignancies.
    Bull Cancer. 2005 Nov;92(11):E61-6, 945-52 PMID: 16316823
  29. The unfolded protein response: a novel component of the hypoxic stress response in tumors.
    Mol Cancer Res. 2005 Nov;3(11):597-605 PMID: 16317085
  30. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells.
    Cancer Res. 2005 Dec 15;65(24):11510-9 PMID: 16357160
  31. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status.
    Blood. 2006 Jan 1;107(1):257-64 PMID: 16166592
  32. Hypoxia selects for high-metastatic Lewis lung carcinoma cells overexpressing Mcl-1 and exhibiting reduced apoptotic potential in solid tumors.
    Oncogene. 2006 Feb 9;25(6):917-28 PMID: 16247470
  33. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells.
    Blood. 2006 Jun 15;107(12):4907-16 PMID: 16507771
  34. Proteasome inhibitor induces apoptosis through induction of endoplasmic reticulum stress.
    Cancer Biol Ther. 2006 Jul;5(7):745-8 PMID: 16861900
  35. Inhibition of Ca2+ influx is required for mitochondrial reactive oxygen species-induced endoplasmic reticulum Ca2+ depletion and cell death in leukemia cells.
    Mol Pharmacol. 2006 Oct;70(4):1424-34 PMID: 16849592
  36. Bax and the mitochondrial permeability transition cooperate in the release of cytochrome c during endoplasmic reticulum-stress-induced apoptosis.
    Cell Death Differ. 2007 Apr;14(4):703-15 PMID: 17170750
  37. Induction of apoptosis by cancer chemotherapy.
    Exp Cell Res. 2000 Apr 10;256(1):42-9 PMID: 10739650
  38. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response.
    Nat Cell Biol. 2000 Jun;2(6):326-32 PMID: 10854322
  39. Cell cycle arrest and apoptosis of melanoma cells by docosahexaenoic acid: association with decreased pRb phosphorylation.
    Cancer Res. 2000 Aug 1;60(15):4139-45 PMID: 10945621
  40. Induction of GADD153 and Bak: novel molecular targets of fenretinide-induced apoptosis of neuroblastoma.
    Cancer Lett. 2003 Jul 18;197(1-2):157-63 PMID: 12880976
Article Info
Journal
British journal of cancer
Abbr.
Br J Cancer
ISSN
0007-0920
Published
2007-04-10
Epub
2007-00-13
Pages
1062-71
Language
English
Region
England
NLM ID
0370635
PMCID
PMC2360126
Subset
IM
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