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PMID: 17823654 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

G1P3, an IFN-induced survival factor, antagonizes TRAIL-induced apoptosis in human myeloma cells.

The Journal of clinical investigation ·Vol. 117 ·No. 10 ·2007-10-00 ·Pages 3107-17

Cheriyath V, Glaser KB, Waring JF, Baz R, Hussein MA, Borden EC

Abstract

The effectiveness of IFN-alpha2b for human multiple myeloma has been variable. TRAIL has been proposed to mediate IFN-alpha2b apoptosis in myeloma. In this study we assessed the effects of IFN-alpha2b signaling on the apoptotic activity of TRAIL and human myeloma cell survival. While TRAIL was one of the most potently induced proapoptotic genes in myeloma cells following IFN-alpha2b treatment, less than 20% of myeloma cells underwent apoptosis. Thus, we hypothesized that an IFN-stimulated gene (ISG) with prosurvival activity might suppress TRAIL-mediated apoptosis. Consistent with this, IFN-alpha2b stabilized mitochondria and inhibited caspase-3 activation, which antagonized TRAIL-mediated apoptosis and cytotoxicity after 24 hours of cotreatment in cell lines and in fresh myeloma cells, an effect not evident after 72 hours. Induced expression of G1P3, an ISG with largely unknown function, was correlated with the antiapoptotic activity of IFN-alpha2b. Ectopically expressed G1P3 localized to mitochondria and antagonized TRAIL-mediated mitochondrial potential loss, cytochrome c release, and apoptosis, suggesting specificity of G1P3 for the intrinsic apoptosis pathway. Furthermore, RNAi-mediated downregulation of G1P3 restored IFN-alpha2b-induced apoptosis. Our data identify the direct role of a mitochondria-localized prosurvival ISG in antagonizing the effect of TRAIL. Curtailing G1P3-mediated antiapoptotic signals could improve therapies for myeloma or other malignancies.

MeSH Terms
Antineoplastic Agents/pharmacology Apoptosis/genetics Caspase 3/metabolism Cell Line, Tumor Cytochromes c/metabolism Gene Expression Regulation Gene Expression Regulation, Leukemic Humans Interferon alpha-2 Interferon-alpha/pharmacology Mitochondria/chemistry,metabolism Mitochondrial Proteins/antagonists & inhibitors,genetics,metabolism Multiple Myeloma/genetics,metabolism Recombinant Proteins TNF-Related Apoptosis-Inducing Ligand/antagonists & inhibitors,metabolism
Chemicals
Antineoplastic Agents IFI6 protein, human Interferon alpha-2 Interferon-alpha Mitochondrial Proteins Recombinant Proteins TNF-Related Apoptosis-Inducing Ligand TNFSF10 protein, human Cytochromes c Caspase 3
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Cheriyath Venugopalan
Center for Hematology and Oncology Molecular Therapeutics, The Cleveland Clinic, Taussig Cancer Center, Cleveland, Ohio, USA.
Glaser Keith B
Waring Jeffrey F
Baz Rachid
Hussein Mohamad A
Borden Ernest C
References (45)
45 references, click to expand
  1. Chromosome translocations in multiple myeloma.
    Oncogene. 2001 Sep 10;20(40):5611-22 PMID: 11607813
  2. Viral interference with apoptosis.
    Semin Cell Dev Biol. 1998 Jun;9(3):339-49 PMID: 9665871
  3. Multiple myeloma: evolving genetic events and host interactions.
    Nat Rev Cancer. 2002 Mar;2(3):175-87 PMID: 11990854
  4. IFN-beta pretreatment sensitizes human melanoma cells to TRAIL/Apo2 ligand-induced apoptosis.
    J Immunol. 2002 Jul 15;169(2):847-55 PMID: 12097388
  5. Genomic abnormalities in monoclonal gammopathy of undetermined significance.
    Blood. 2002 Aug 15;100(4):1417-24 PMID: 12149226
  6. Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines.
    Mol Cancer Ther. 2003 Feb;2(2):151-63 PMID: 12589032
  7. Second-generation interferons for cancer: clinical targets.
    Semin Cancer Biol. 2000 Apr;10(2):125-44 PMID: 10936063
  8. The biochemistry of apoptosis.
    Nature. 2000 Oct 12;407(6805):770-6 PMID: 11048727
  9. Regulation of Bcl-2-family proteins in myeloma cells by three myeloma survival factors: interleukin-6, interferon-alpha and insulin-like growth factor 1.
    Cell Death Differ. 2000 Dec;7(12):1244-52 PMID: 11175262
  10. High, intermittent dose of all-trans retinoic acid in combination with alpha-interferon for advanced multiple myeloma.
    Haematologica. 2001 Jul;86(7):776-7 PMID: 11454541
  11. TRAIL/Apo2L ligand selectively induces apoptosis and overcomes drug resistance in multiple myeloma: therapeutic applications.
    Blood. 2001 Aug 1;98(3):795-804 PMID: 11468181
  12. Apo2L/TRAIL and Bcl-2-related proteins regulate type I interferon-induced apoptosis in multiple myeloma.
    Blood. 2001 Oct 1;98(7):2183-92 PMID: 11568006
  13. TRAIL-induced eradication of primary tumour cells from multiple myeloma patient bone marrows is not related to TRAIL receptor expression or prior chemotherapy.
    Leukemia. 2001 Oct;15(10):1650-7 PMID: 11587225
  14. Reciprocal expression of TRAIL and CD95L in Th1 and Th2 cells: role of apoptosis in T helper subset differentiation.
    Cell Death Differ. 2003 Feb;10(2):203-10 PMID: 12700648
  15. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis.
    Apoptosis. 2003 Jun;8(3):237-49 PMID: 12766484
  16. Quantitative real-time RT-PCR analysis of eight novel estrogen-regulated genes in breast cancer.
    Int J Biol Markers. 2003 Apr-Jun;18(2):123-9 PMID: 12841681
  17. Interferon-alpha-induced apoptosis in U266 cells is associated with activation of the proapoptotic Bcl-2 family members Bak and Bax.
    Oncogene. 2003 Jul 17;22(29):4543-56 PMID: 12881711
  18. Insights into the multistep transformation of MGUS to myeloma using microarray expression analysis.
    Blood. 2003 Dec 15;102(13):4504-11 PMID: 12947006
  19. Targeting death receptors in cancer with Apo2L/TRAIL.
    Curr Opin Pharmacol. 2004 Aug;4(4):333-9 PMID: 15251125
  20. Characterization of a human gene inducible by alpha- and beta-interferons and its expression in mouse cells.
    EMBO J. 1986 Jul;5(7):1601-6 PMID: 3017706
  21. Targeted breakage of a human chromosome mediated by cloned human telomeric DNA.
    Nat Genet. 1992 Dec;2(4):283-7 PMID: 1303280
  22. Interferons for the treatment of hematological malignancies.
    Oncology. 1994 Mar-Apr;51(2):137-41 PMID: 7515169
  23. Innovative treatment strategies for non-Hodgkin's lymphoma and multiple myeloma.
    Semin Oncol. 1994 Dec;21(6 Suppl 14):14-22 PMID: 7992095
  24. Cytokine therapy in multiple myeloma.
    Br J Haematol. 1996 Sep;94(3):425-32 PMID: 8790137
  25. In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine.
    J Immunol. 1996 Nov 1;157(9):4100-8 PMID: 8892645
  26. Regulation of apoptosis by viral gene products.
    J Virol. 1997 Mar;71(3):1739-46 PMID: 9032302
  27. The apoptotic cysteine protease CPP32.
    Int J Biochem Cell Biol. 1997 Mar;29(3):393-6 PMID: 9202418
  28. The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8461-6 PMID: 9671700
  29. Mitochondria and apoptosis.
    Science. 1998 Aug 28;281(5381):1309-12 PMID: 9721092
  30. IFN-alpha is a survival factor for human myeloma cells and reduces dexamethasone-induced apoptosis.
    J Immunol. 1998 Sep 15;161(6):2692-9 PMID: 9743325
  31. Human myeloma cell apoptosis induced by interferon-alpha.
    Br J Haematol. 1998 Nov;103(2):518-29 PMID: 9827928
  32. Interferon-alpha protects myeloma cell lines from dexamethasone-induced apoptosis.
    Leukemia. 1999 Mar;13(3):473-80 PMID: 10086739
  33. In silico identification of breast cancer genes by combined multiple high throughput analyses.
    Int J Mol Med. 2005 Feb;15(2):205-12 PMID: 15647832
  34. PML mediates IFN-alpha-induced apoptosis in myeloma by regulating TRAIL induction.
    Blood. 2005 Feb 1;105(3):1280-7 PMID: 15459016
  35. Mechanisms of resistance to TRAIL-induced apoptosis in cancer.
    Cancer Gene Ther. 2005 Mar;12(3):228-37 PMID: 15550937
  36. Interferon-alpha as maintenance therapy in patients with multiple myeloma.
    Ann Oncol. 2005 Apr;16(4):634-9 PMID: 15741226
  37. Involvement of Noxa in cellular apoptotic responses to interferon, double-stranded RNA, and virus infection.
    J Biol Chem. 2005 Apr 22;280(16):15561-8 PMID: 15705586
  38. G1P3, an interferon inducible gene 6-16, is expressed in gastric cancers and inhibits mitochondrial-mediated apoptosis in gastric cancer cell line TMK-1 cell.
    Cancer Immunol Immunother. 2005 Aug;54(8):729-40 PMID: 15685448
  39. Ectopic and IFN-induced expression of Fas overcomes resistance to Fas-mediated apoptosis in multiple myeloma cells.
    Blood. 2005 Aug 15;106(4):1346-54 PMID: 15860671
  40. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3.
    Cell. 2005 Sep 9;122(5):669-82 PMID: 16125763
  41. Apo2L/TRAIL is an indirect mediator of apoptosis induced by interferon-alpha in human myeloma cells.
    FEBS Lett. 2005 Nov 7;579(27):6217-22 PMID: 16246331
  42. The many shapes of mitochondrial death.
    Oncogene. 2006 Aug 7;25(34):4717-24 PMID: 16892085
  43. Multiple myeloma: increasing evidence for a multistep transformation process.
    Blood. 1998 Jan 1;91(1):3-21 PMID: 9414264
  44. Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1.
    EMBO J. 1998 Apr 15;17(8):2224-34 PMID: 9545236
  45. Molecular cross-talk between the TRAIL and interferon signaling pathways.
    J Biol Chem. 2002 Jan 4;277(1):575-85 PMID: 11677236
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2007-10-00
Pages
3107-17
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC1964509
Subset
IM
Grants
NCI NIH HHS · R01 CA090914 · United States
NCI NIH HHS · R01 CA090914-04 · United States
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