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PMID: 19775282 Published · ppublish English Journal Article

Down-regulation of the Notch pathway mediated by a gamma-secretase inhibitor induces anti-tumour effects in mouse models of T-cell leukaemia.

British journal of pharmacology ·Vol. 158 ·No. 5 ·2009-11-00 ·Pages 1183-95

Tammam J, Ware C, Efferson C, O'Neil J, Rao S, Qu X, Gorenstein J, Angagaw M, Kim H, Kenific C, Kunii K, Leach KJ, Nikov G, Zhao J, Dai X, Hardwick J, Scott M, Winter C, Bristow L, Elbi C, Reilly JF, Look T, Draetta G, Van der Ploeg L, Kohl NE, Strack PR, Majumder PK

Abstract

gamma-Secretase inhibitors (GSIs) block NOTCH receptor cleavage and pathway activation and have been under clinical evaluation for the treatment of malignancies such as T-cell acute lymphoblastic leukaemia (T-ALL). The ability of GSIs to decrease T-ALL cell viability in vitro is a slow process requiring >8 days, however, such treatment durations are not well tolerated in vivo. Here we study GSI's effect on tumour and normal cellular processes to optimize dosing regimens for anti-tumour efficacy. Inhibition of the Notch pathway in mouse intestinal epithelium was used to evaluate the effect of GSIs and guide the design of dosing regimens for xenograft models. Serum Abeta(40) and Notch target gene modulation in tumours were used to evaluate the degree and duration of target inhibition. Pharmacokinetic and pharmacodynamic correlations with biochemical, immunohistochemical and profiling data were used to demonstrate GSI mechanism of action in xenograft tumours. Three days of >70% Notch pathway inhibition was sufficient to provide an anti-tumour effect and was well tolerated. GSI-induced conversion of mouse epithelial cells to a secretory lineage was time- and dose-dependent. Anti-tumour efficacy was associated with cell cycle arrest and apoptosis that was in part due to Notch-dependent regulation of mitochondrial homeostasis. Intermittent but potent inhibition of Notch signalling is sufficient for anti-tumour efficacy in these T-ALL models. These findings provide support for the use of GSI in Notch-dependent malignancies and that clinical benefits may be derived from transient but potent inhibition of Notch.

MeSH Terms
Amyloid Precursor Protein Secretases/antagonists & inhibitors Amyloid beta-Peptides/blood Animals Antineoplastic Agents/administration & dosage,adverse effects,pharmacology Apoptosis Cell Differentiation Cell Line, Tumor Colon/cytology,drug effects Cyclic S-Oxides/administration & dosage,adverse effects,pharmacology Down-Regulation Drug Administration Schedule Humans Intestinal Mucosa/cytology,drug effects Membrane Potential, Mitochondrial/drug effects Mice Mice, Nude Mitochondrial Proteins/biosynthesis,genetics Neoplasm Transplantation Peptide Fragments/blood Precursor T-Cell Lymphoblastic Leukemia-Lymphoma/drug therapy,metabolism,pathology Receptor, Notch1/genetics,physiology Signal Transduction Thiadiazoles/administration & dosage,adverse effects,pharmacology Transplantation, Heterologous
Chemicals
Amyloid beta-Peptides Antineoplastic Agents Cyclic S-Oxides MRK 003 Mitochondrial Proteins Peptide Fragments Receptor, Notch1 Thiadiazoles amyloid beta-protein (1-40) Amyloid Precursor Protein Secretases
Authors & Affiliations
27 authors, click to expand affiliations / ORCID
Tammam J
Department of Oncology/Pharmacology, Merck Research Laboratories, Boston, MA 02115, USA.
Ware C
Efferson C
O'Neil J
Rao S
Qu X
Gorenstein J
Angagaw M
Kim H
Kenific C
Kunii K
Leach K J
Nikov G
Zhao J
Dai X
Hardwick J
Scott M
Winter C
Bristow L
Elbi C
Reilly J F
Look T
Draetta G
Van der Ploeg Lht
Kohl N E
Strack P R
Majumder P K
References (52)
52 references, click to expand
  1. Apoptosis-based therapies.
    Nat Rev Drug Discov. 2002 Feb;1(2):111-21 PMID: 12120092
  2. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia.
    Science. 2004 Oct 8;306(5694):269-71 PMID: 15472075
  3. Gamma-secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia.
    Nat Med. 2009 Jan;15(1):50-8 PMID: 19098907
  4. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors.
    J Exp Med. 2007 Aug 6;204(8):1813-24 PMID: 17646409
  5. Alzheimer's APP mangles mitochondria.
    Nat Med. 2006 Nov;12(11):1241-3 PMID: 17088888
  6. Apoptosis in T cell acute lymphoblastic leukemia cells after cell cycle arrest induced by pharmacological inhibition of notch signaling.
    Chem Biol. 2007 Feb;14(2):209-19 PMID: 17317574
  7. A loss of function mutation of presenilin-2 interferes with amyloid beta-peptide production and notch signaling.
    J Biol Chem. 1999 Oct 1;274(40):28669-73 PMID: 10497236
  8. Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis.
    J Cell Biol. 2004 Oct 25;167(2):215-21 PMID: 15492044
  9. The BCL-2 protein family: opposing activities that mediate cell death.
    Nat Rev Mol Cell Biol. 2008 Jan;9(1):47-59 PMID: 18097445
  10. Activating NOTCH1 mutations predict favorable early treatment response and long-term outcome in childhood precursor T-cell lymphoblastic leukemia.
    Blood. 2006 Aug 15;108(4):1151-7 PMID: 16614245
  11. Modulation of notch processing by gamma-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation.
    Toxicol Sci. 2004 Nov;82(1):341-58 PMID: 15319485
  12. Quantitative measurement of changes in amyloid-beta(40) in the rat brain and cerebrospinal fluid following treatment with the gamma-secretase inhibitor LY-411575 [N2-[(2S)-2-(3,5-difluorophenyl)-2-hydroxyethanoyl]-N1-[(7S)-5-methyl-6-oxo-6,7-dihydro-5H-dibenzo[b,d]azepin-7-yl]-L-alaninamide].
    J Pharmacol Exp Ther. 2005 May;313(2):902-8 PMID: 15743924
  13. Global identification of Myc target genes reveals its direct role in mitochondrial biogenesis and its E-box usage in vivo.
    PLoS One. 2008 Mar 12;3(3):e1798 PMID: 18335064
  14. The action of the notchlocus in Drosophila melanogaster. II. Biochemical effects of recessive lethals on mitochondrial enzymes.
    Genetics. 1981 Sep;99(1):65-74 PMID: 6804303
  15. Notch signaling in vascular development and physiology.
    Development. 2007 Aug;134(15):2709-18 PMID: 17611219
  16. A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1.
    Mol Cell. 2000 Feb;5(2):197-206 PMID: 10882062
  17. Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2.
    EMBO Rep. 2008 Apr;9(4):377-83 PMID: 18274550
  18. Mitochondrial dysfunction associated with a mutation in the Notch3 gene in a CADASIL family.
    Neurology. 2001 Oct 9;57(7):1235-8 PMID: 11591842
  19. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth.
    Proc Natl Acad Sci U S A. 2006 Nov 28;103(48):18261-6 PMID: 17114293
  20. Mitochondrial membrane potential monitored by JC-1 dye.
    Methods Enzymol. 1995;260:406-17 PMID: 8592463
  21. NOTCH1 mutations in T-cell acute lymphoblastic leukemia: prognostic significance and implication in multifactorial leukemogenesis.
    Clin Cancer Res. 2006 May 15;12(10):3043-9 PMID: 16707600
  22. Inhibition of NOTCH signaling by gamma secretase inhibitor engages the RB pathway and elicits cell cycle exit in T-cell acute lymphoblastic leukemia cells.
    Cancer Res. 2009 Apr 1;69(7):3060-8 PMID: 19318552
  23. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis.
    Cancer Cell. 2008 Dec 9;14(6):485-93 PMID: 19061839
  24. Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo.
    J Clin Invest. 2008 Jan;118(1):217-28 PMID: 18079963
  25. In vitro validation of gamma-secretase inhibitors alone or in combination with other anti-cancer drugs for the treatment of T-cell acute lymphoblastic leukemia.
    Haematologica. 2008 Apr;93(4):533-42 PMID: 18322257
  26. Direct response to Notch activation: signaling crosstalk and incoherent logic.
    Sci Signal. 2009 Jan 27;2(55):ra1 PMID: 19176515
  27. Mammary stem cells and breast cancer--role of Notch signalling.
    Stem Cell Rev. 2007 Jun;3(2):169-75 PMID: 17873349
  28. New genetic abnormalities and treatment response in acute lymphoblastic leukemia.
    Semin Hematol. 2009 Jan;46(1):16-23 PMID: 19100364
  29. Dominant-negative Notch3 receptor inhibits mitogen-activated protein kinase pathway and the growth of human lung cancers.
    Cancer Res. 2005 May 1;65(9):3555-61 PMID: 15867348
  30. Growth suppression of pre-T acute lymphoblastic leukemia cells by inhibition of notch signaling.
    Mol Cell Biol. 2003 Jan;23(2):655-64 PMID: 12509463
  31. ChIP-on-chip significance analysis reveals large-scale binding and regulation by human transcription factor oncogenes.
    Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):244-9 PMID: 19118200
  32. Downregulation of Notch signaling by gamma-secretase inhibition can abrogate chemotherapy-induced apoptosis in T-ALL cell lines.
    Ann Hematol. 2009 Jul;88(7):613-21 PMID: 19057901
  33. Requirement of Notch activation during regeneration of the intestinal epithelia.
    Am J Physiol Gastrointest Liver Physiol. 2009 Jan;296(1):G23-35 PMID: 19023031
  34. Significance analysis of time course microarray experiments.
    Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12837-42 PMID: 16141318
  35. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain.
    Nature. 1998 May 28;393(6683):382-6 PMID: 9620803
  36. Notch signals positively regulate activity of the mTOR pathway in T-cell acute lymphoblastic leukemia.
    Blood. 2007 Jul 1;110(1):278-86 PMID: 17363738
  37. Intermittent target inhibition with dasatinib 100 mg once daily preserves efficacy and improves tolerability in imatinib-resistant and -intolerant chronic-phase chronic myeloid leukemia.
    J Clin Oncol. 2008 Jul 1;26(19):3204-12 PMID: 18541900
  38. Notch1 contributes to mouse T-cell leukemia by directly inducing the expression of c-myc.
    Mol Cell Biol. 2006 Nov;26(21):8022-31 PMID: 16954387
  39. Diagnosing and exploiting cancer's addiction to blocks in apoptosis.
    Nat Rev Cancer. 2008 Feb;8(2):121-32 PMID: 18202696
  40. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation.
    Cancer Res. 2005 Mar 15;65(6):2353-63 PMID: 15781650
  41. Notch signaling regulates the differentiation of post-mitotic intestinal epithelial cells.
    Genes Dev. 2005 Jul 15;19(14):1686-91 PMID: 16024658
  42. Targeting the Notch1 and mTOR pathways in a mouse T-ALL model.
    Blood. 2009 Jun 11;113(24):6172-81 PMID: 19246562
  43. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma.
    Genes Dev. 2006 Aug 1;20(15):2096-109 PMID: 16847353
  44. Notch signaling in development and cancer.
    Endocr Rev. 2007 May;28(3):339-63 PMID: 17409286
  45. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3671-5 PMID: 2023917
  46. Direct regulation of intestinal fate by Notch.
    Proc Natl Acad Sci U S A. 2005 Aug 30;102(35):12443-8 PMID: 16107537
  47. Mitochondrial translocation of protein kinase C delta in phorbol ester-induced cytochrome c release and apoptosis.
    J Biol Chem. 2000 Jul 21;275(29):21793-6 PMID: 10818086
  48. Notch signals control the fate of immature progenitor cells in the intestine.
    Nature. 2005 Jun 16;435(7044):964-8 PMID: 15959516
  49. Inhibition of gamma-secretase activity inhibits tumor progression in a mouse model of pancreatic ductal adenocarcinoma.
    Gastroenterology. 2009 May;136(5):1741-9.e6 PMID: 19208345
  50. Introduction and expression of the 400 kilobase amyloid precursor protein gene in transgenic mice [corrected].
    Nat Genet. 1993 Sep;5(1):22-30 PMID: 8220418
  51. Prognostic significance of molecular-cytogenetic abnormalities in pediatric T-ALL is not explained by immunophenotypic differences.
    Leukemia. 2008 Jan;22(1):124-31 PMID: 17928886
  52. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells.
    Nature. 2005 Jun 16;435(7044):959-63 PMID: 15959515
Article Info
Journal
British journal of pharmacology
Abbr.
Br J Pharmacol
ISSN
1476-5381
Published
2009-11-00
Epub
2009-00-23
Pages
1183-95
Language
English
Region
England
NLM ID
7502536
PMCID
PMC2782329
Subset
IM
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