Home LiteratureArticle Details
PMID: 17032924 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Targeting mitochondrial factor Smac/DIABLO as therapy for multiple myeloma (MM).

Blood ·Vol. 109 ·No. 3 ·2007-02-01 ·Pages 1220-7

Chauhan D, Neri P, Velankar M, Podar K, Hideshima T, Fulciniti M, Tassone P, Raje N, Mitsiades C, Mitsiades N, Richardson P, Zawel L, Tran M, Munshi N, Anderson KC

Abstract

Second mitochondria-derived activator of caspases (Smac) promotes apoptosis via activation of caspases. Here we show that a low-molecular-weight Smac mimetic LBW242 induces apoptosis in multiple myeloma (MM) cells resistant to conventional and bortezomib therapies. Examination of purified patient MM cells demonstrated similar results, without significant cytotoxicity against normal lymphocytes and bone marrow stromal cells (BMSCs). Importantly, LBW242 abrogates paracrine MM cell growth triggered by their adherence to BMSCs and overcomes MM cell growth and drug-resistance conferred by interleukin-6 or insulinlike growth factor-1. Overexpression of Bcl-2 similarly does not affect LBW242-induced cytotoxicity. Mechanistic studies show that LBW242-induced apoptosis in MM cells is associated with activation of caspase-8, caspase-9, and caspase-3, followed by PARP cleavage. In human MM xenograft mouse models, LBW242 is well tolerated, inhibits tumor growth, and prolongs survival. Importantly, combining LBW242 with novel agents, including tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) or the proteasome inhibitors bortezomib and NPI-0052, as well as with the conventional anti-MM agent melphalan, induces additive/synergistic anti-MM activity. Our study therefore provides the rationale for clinical protocols evaluating LBW242, alone and together with other anti-MM agents, to improve patient outcome in MM.

MeSH Terms
Animals Antineoplastic Agents/administration & dosage,pharmacology Apoptosis/drug effects Apoptosis Regulatory Proteins Cell Proliferation/drug effects Coculture Techniques Drug Synergism Humans Intracellular Signaling Peptides and Proteins/agonists Melphalan/pharmacology Mice Mitochondrial Proteins/agonists Molecular Mimicry Multiple Myeloma/drug therapy,pathology Paracrine Communication/drug effects Stromal Cells/cytology Survival Rate Transplantation, Heterologous Tumor Cells, Cultured
Chemicals
Antineoplastic Agents Apoptosis Regulatory Proteins DIABLO protein, human Intracellular Signaling Peptides and Proteins Mitochondrial Proteins Melphalan
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Chauhan Dharminder
The Jerome Lipper Multiple Myeloma Center, Department of Medical Oncology, Dana Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA.
Neri Paola
Velankar Mugdha
Podar Klaus
Hideshima Teru
Fulciniti Mariateresa
Tassone Pierfrancesco
Raje Noopur
Mitsiades Constantine
Mitsiades Nicholas
Richardson Paul
Zawel Leigh
Tran Mary
Munshi Nikhil
Anderson Kenneth C
References (65)
65 references, click to expand
  1. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins.
    Cell. 2000 Jul 7;102(1):43-53 PMID: 10929712
  2. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked.
    Science. 1997 Feb 21;275(5303):1129-32 PMID: 9027314
  3. 2-Methoxyestradiol overcomes drug resistance in multiple myeloma cells.
    Blood. 2002 Sep 15;100(6):2187-94 PMID: 12200384
  4. Cell death: the significance of apoptosis.
    Int Rev Cytol. 1980;68:251-306 PMID: 7014501
  5. Chromatin condensation during apoptosis is accompanied by degradation of lamin A+B, without enhanced activation of cdc2 kinase.
    J Cell Biol. 1994 Aug;126(4):827-37 PMID: 8051209
  6. A JNK-dependent pathway is required for TNFalpha-induced apoptosis.
    Cell. 2003 Oct 3;115(1):61-70 PMID: 14532003
  7. Aureoverticillactam, a novel 22-atom macrocyclic lactam from the marine actinomycete Streptomyces aureoverticillatus.
    J Nat Prod. 2004 Aug;67(8):1400-2 PMID: 15332863
  8. 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
  9. Structural basis of IAP recognition by Smac/DIABLO.
    Nature. 2000 Dec 21-28;408(6815):1008-12 PMID: 11140638
  10. Non-peptidic small molecule inhibitors of XIAP.
    Bioorg Med Chem Lett. 2005 Feb 1;15(3):771-5 PMID: 15664855
  11. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain.
    Nature. 2000 Dec 21-28;408(6815):1004-8 PMID: 11140637
  12. Proteasome inhibitor PS-341 inhibits human myeloma cell growth in vivo and prolongs survival in a murine model.
    Cancer Res. 2002 Sep 1;62(17):4996-5000 PMID: 12208752
  13. Molecular mechanisms of novel therapeutic approaches for multiple myeloma.
    Nat Rev Cancer. 2002 Dec;2(12):927-37 PMID: 12459731
  14. Caspases: enemies within.
    Science. 1998 Aug 28;281(5381):1312-6 PMID: 9721091
  15. Mechanisms of cell death and survival in multiple myeloma (MM): Therapeutic implications.
    Apoptosis. 2003 Aug;8(4):337-43 PMID: 12815276
  16. Interleukin-6 inhibits Fas-induced apoptosis and stress-activated protein kinase activation in multiple myeloma cells.
    Blood. 1997 Jan 1;89(1):227-34 PMID: 8978296
  17. A role for insulin-like growth factor in the regulation of IL-6-responsive human myeloma cell line growth.
    J Immunol. 1997 Jul 1;159(1):487-96 PMID: 9200490
  18. Molecular sequelae of proteasome inhibition in human multiple myeloma cells.
    Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14374-9 PMID: 12391322
  19. Activation of NF-kappaB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications.
    Oncogene. 2002 Aug 22;21(37):5673-83 PMID: 12173037
  20. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors.
    Adv Enzyme Regul. 1984;22:27-55 PMID: 6382953
  21. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death.
    Mol Cell. 2001 Sep;8(3):613-21 PMID: 11583623
  22. Moving disease biology from the lab to the clinic.
    Cancer. 2003 Feb 1;97(3 Suppl):796-801 PMID: 12548578
  23. Bcl-2 overexpression is associated with resistance to dexamethasone, but not melphalan, in multiple myeloma cells.
    Int J Oncol. 1998 Aug;13(2):397-405 PMID: 9664139
  24. IAP family proteins--suppressors of apoptosis.
    Genes Dev. 1999 Feb 1;13(3):239-52 PMID: 9990849
  25. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death.
    Science. 2004 Sep 3;305(5689):1471-4 PMID: 15353805
  26. The expanding role of mitochondria in apoptosis.
    Genes Dev. 2001 Nov 15;15(22):2922-33 PMID: 11711427
  27. Multiple myeloma cells are protected against dexamethasone-induced apoptosis by insulin-like growth factors.
    Br J Haematol. 1997 May;97(2):429-40 PMID: 9163610
  28. A lively meeting on a deathly topic.
    Apoptosis. 1997;2(3):337-42 PMID: 14692410
  29. Cytochrome c-dependent and -independent induction of apoptosis in multiple myeloma cells.
    J Biol Chem. 1997 Nov 28;272(48):29995-7 PMID: 9374472
  30. Structure-based design, synthesis and biochemical testing of novel and potent Smac peptido-mimetics.
    Bioorg Med Chem Lett. 2005 Feb 1;15(3):793-7 PMID: 15664859
  31. Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiple myeloma, other hematologic malignancies, and solid tumors.
    Cancer Cell. 2004 Mar;5(3):221-30 PMID: 15050914
  32. Mitochondrial control of cell death.
    Nat Med. 2000 May;6(5):513-9 PMID: 10802706
  33. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo.
    Nat Med. 2002 Aug;8(8):808-15 PMID: 12118245
  34. Heterogeneity in therapeutic response of genetically altered myeloma cell lines to interleukin 6, dexamethasone, doxorubicin, and melphalan.
    Blood. 2000 Nov 1;96(9):3175-80 PMID: 11050000
  35. Interleukin-6 prevents dexamethasone-induced myeloma cell death.
    Blood. 1994 Nov 1;84(9):3063-70 PMID: 7949178
  36. Structural and biochemical basis of apoptotic activation by Smac/DIABLO.
    Nature. 2000 Aug 24;406(6798):855-62 PMID: 10972280
  37. Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer.
    J Med Chem. 2004 Aug 26;47(18):4417-26 PMID: 15317454
  38. Predominant suppression of apoptosome by inhibitor of apoptosis protein in non-small cell lung cancer H460 cells: therapeutic effect of a novel polyarginine-conjugated Smac peptide.
    Cancer Res. 2003 Feb 15;63(4):831-7 PMID: 12591734
  39. The role of tumor necrosis factor alpha in the pathophysiology of human multiple myeloma: therapeutic applications.
    Oncogene. 2001 Jul 27;20(33):4519-27 PMID: 11494147
  40. Synthetic Smac/DIABLO peptides enhance the effects of chemotherapeutic agents by binding XIAP and cIAP1 in situ.
    J Biol Chem. 2002 Nov 15;277(46):44236-43 PMID: 12218061
  41. Apoptosis regulators.
    Rev Clin Exp Hematol. 2003 Jun;7(2):117-38 PMID: 14763159
  42. Fibroblast growth factor 2-mediated translational control of IAPs blocks mitochondrial release of Smac/DIABLO and apoptosis in small cell lung cancer cells.
    Mol Cell Biol. 2003 Nov;23(21):7600-10 PMID: 14560006
  43. Targeting p38 MAPK inhibits multiple myeloma cell growth in the bone marrow milieu.
    Blood. 2003 Jan 15;101(2):703-5 PMID: 12393542
  44. Vascular endothelial growth factor-induced migration of multiple myeloma cells is associated with beta 1 integrin- and phosphatidylinositol 3-kinase-dependent PKC alpha activation.
    J Biol Chem. 2002 Mar 8;277(10):7875-81 PMID: 11751905
  45. Targeting the mitochondria: an exciting new approach to myeloma therapy. Commentary re: N. J. Bahlis et al., Feasibility and correlates of arsenic trioxide combined with ascorbic acid-mediated depletion of intracellular glutathione for the treatment of relapsed/refractory multiple myeloma. Clin. Cancer Res., 8: 3658-3668, 2002.
    Clin Cancer Res. 2002 Dec;8(12):3643-5 PMID: 12473572
  46. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition.
    Cell. 2000 Jul 7;102(1):33-42 PMID: 10929711
  47. Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-kappa B.
    Blood. 1996 Feb 1;87(3):1104-12 PMID: 8562936
  48. Targeting mitochondria to overcome conventional and bortezomib/proteasome inhibitor PS-341 resistance in multiple myeloma (MM) cells.
    Blood. 2004 Oct 15;104(8):2458-66 PMID: 15217830
  49. Apoptosis: checkpoint at the mitochondrial frontier.
    Mutat Res. 1999 Jul 30;434(3):243-51 PMID: 10486595
  50. Development of Peptidomimetics Targeting IAPs.
    Int J Pept Res Ther. 2006 Mar;12(1):21-32 PMID: 19617919
  51. SHP2 mediates the protective effect of interleukin-6 against dexamethasone-induced apoptosis in multiple myeloma cells.
    J Biol Chem. 2000 Sep 8;275(36):27845-50 PMID: 10880513
  52. Synthetic Smac peptide enhances the effect of etoposide-induced apoptosis in human glioblastoma cell lines.
    J Neurooncol. 2006 May;77(3):247-55 PMID: 16575541
  53. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib.
    Cancer Cell. 2005 Nov;8(5):407-19 PMID: 16286248
  54. Biologic sequelae of nuclear factor-kappaB blockade in multiple myeloma: therapeutic applications.
    Blood. 2002 Jun 1;99(11):4079-86 PMID: 12010810
  55. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2.
    EMBO J. 2001 Dec 3;20(23):6627-36 PMID: 11726499
  56. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis.
    Nature. 2001 Mar 1;410(6824):112-6 PMID: 11242052
  57. Elevated expression of inhibitor of apoptosis proteins in prostate cancer.
    Clin Cancer Res. 2003 Oct 15;9(13):4914-25 PMID: 14581366
  58. Ectopic overexpression of second mitochondria-derived activator of caspases (Smac/DIABLO) or cotreatment with N-terminus of Smac/DIABLO peptide potentiates epothilone B derivative-(BMS 247550) and Apo-2L/TRAIL-induced apoptosis.
    Blood. 2002 May 1;99(9):3419-26 PMID: 11964312
  59. Apaf-1/cytochrome c-independent and Smac-dependent induction of apoptosis in multiple myeloma (MM) cells.
    J Biol Chem. 2001 Jul 6;276(27):24453-6 PMID: 11356822
  60. Endonuclease G is an apoptotic DNase when released from mitochondria.
    Nature. 2001 Jul 5;412(6842):95-9 PMID: 11452314
  61. Proteasome inhibition in multiple myeloma: therapeutic implication.
    Annu Rev Pharmacol Toxicol. 2005;45:465-76 PMID: 15822185
  62. Adhesion of human myeloma-derived cell lines to bone marrow stromal cells stimulates interleukin-6 secretion.
    Blood. 1993 Dec 15;82(12):3712-20 PMID: 8260708
  63. NF-kappa B as a therapeutic target in multiple myeloma.
    J Biol Chem. 2002 May 10;277(19):16639-47 PMID: 11872748
  64. Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils: up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia.
    Blood. 2003 Feb 1;101(3):1164-71 PMID: 12393423
  65. Molecular characterization of mitochondrial apoptosis-inducing factor.
    Nature. 1999 Feb 4;397(6718):441-6 PMID: 9989411
Article Info
Journal
Blood
Abbr.
Blood
ISSN
0006-4971
Published
2007-02-01
Epub
2006-00-10
Pages
1220-7
Language
English
Region
United States
NLM ID
7603509
PMCID
PMC1785138
Subset
IM
Grants
NCI NIH HHS · R01 CA050947 · United States
NCI NIH HHS · CA 50947 · United States
NCI NIH HHS · CA 78373 · United States
NCI NIH HHS · CA10070 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com