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PMID: 20530696 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Review

Targeting Notch to target cancer stem cells.

Pannuti A, Foreman K, Rizzo P, Osipo C, Golde T, Osborne B, Miele L

Abstract

The cellular heterogeneity of neoplasms has been at the center of considerable interest since the "cancer stem cell hypothesis", originally formulated for hematologic malignancies, was extended to solid tumors. The origins of cancer "stem" cells (CSC) or tumor-initiating cells (TIC; henceforth referred to as CSCs) and the methods to identify them are hotly debated topics. Nevertheless, the existence of subpopulations of tumor cells with stem-like characteristics has significant therapeutic implications. The stem-like phenotype includes indefinite self-replication, pluripotency, and, importantly, resistance to chemotherapeutics. Thus, it is plausible that CSCs, regardless of their origin, may escape standard therapies and cause disease recurrences and/or metastasis after apparently complete remissions. Consequently, the idea of selectively targeting CSCs with novel therapeutics is gaining considerable interest. The Notch pathway is one of the most intensively studied putative therapeutic targets in CSC, and several investigational Notch inhibitors are being developed. However, successful targeting of Notch signaling in CSC will require a thorough understanding of Notch regulation and the context-dependent interactions between Notch and other therapeutically relevant pathways. Understanding these interactions will increase our ability to design rational combination regimens that are more likely to prove safe and effective. Additionally, to determine which patients are most likely to benefit from treatment with Notch-targeting therapeutics, reliable biomarkers to measure pathway activity in CSC from specific tumors will have to be identified and validated. This article summarizes the most recent developments in the field of Notch-targeted cancer therapeutics, with emphasis on CSC.

MeSH Terms
Animals Antineoplastic Agents/therapeutic use Drug Delivery Systems Drug Resistance, Neoplasm Humans Ligands Mice Neoplasms/drug therapy,metabolism,pathology Neoplastic Stem Cells/pathology Receptors, Notch/antagonists & inhibitors Signal Transduction/drug effects
Chemicals
Antineoplastic Agents Ligands Receptors, Notch
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Pannuti Antonio
University of Mississippi Cancer Institute, Jackson, MS 39216, USA.
Foreman Kimberly
Rizzo Paola
Osipo Clodia
Golde Todd
Osborne Barbara
Miele Lucio
References (108)
108 references, click to expand
  1. Notch inhibitors as a new tool in the war on cancer: a pathway to watch.
    Curr Pharm Biotechnol. 2009 Feb;10(2):154-60 PMID: 19199947
  2. Make room for dedifferentiation.
    Fly (Austin). 2009 Oct-Dec;3(4):283-5 PMID: 19923919
  3. Possible mechanisms of action of NSAIDs and related compounds that modulate gamma-secretase cleavage.
    Curr Top Med Chem. 2008;8(1):47-53 PMID: 18220932
  4. The epithelial-mesenchymal transition generates cells with properties of stem cells.
    Cell. 2008 May 16;133(4):704-15 PMID: 18485877
  5. Chronic DLL4 blockade induces vascular neoplasms.
    Nature. 2010 Feb 11;463(7282):E6-7 PMID: 20147986
  6. Efficient tumour formation by single human melanoma cells.
    Nature. 2008 Dec 4;456(7222):593-8 PMID: 19052619
  7. Notch signaling in cancer.
    Curr Mol Med. 2006 Dec;6(8):905-18 PMID: 17168741
  8. Regulation of Notch signalling by non-visual beta-arrestin.
    Nat Cell Biol. 2005 Dec;7(12):1191-201 PMID: 16284625
  9. Notch promotes radioresistance of glioma stem cells.
    Stem Cells. 2010 Jan;28(1):17-28 PMID: 19921751
  10. De novo discovery of a gamma-secretase inhibitor response signature using a novel in vivo breast tumor model.
    Cancer Res. 2009 Dec 1;69(23):8949-57 PMID: 19903844
  11. DLL4 blockade inhibits tumor growth and reduces tumor-initiating cell frequency.
    Cell Stem Cell. 2009 Aug 7;5(2):168-77 PMID: 19664991
  12. Notch-activated signaling cascade interacts with mitochondrial remodeling proteins to regulate cell survival.
    Proc Natl Acad Sci U S A. 2010 Apr 13;107(15):6882-7 PMID: 20339081
  13. The difficulty of targeting cancer stem cell niches.
    Clin Cancer Res. 2010 Jun 15;16(12):3121-9 PMID: 20530700
  14. Exploitation of the Notch signaling pathway as a novel target for cancer therapy.
    Anticancer Res. 2008 Nov-Dec;28(6A):3621-30 PMID: 19189643
  15. Emerging role of Notch in stem cells and cancer.
    Cancer Lett. 2009 Jun 28;279(1):8-12 PMID: 19022563
  16. Regulation of Notch signaling by dynamic changes in the precision of S3 cleavage of Notch-1.
    Mol Cell Biol. 2008 Jan;28(1):165-76 PMID: 17967888
  17. Nemo-like kinase suppresses Notch signalling by interfering with formation of the Notch active transcriptional complex.
    Nat Cell Biol. 2010 Mar;12(3):278-85 PMID: 20118921
  18. Notch2 signaling induces apoptosis and inhibits human MDA-MB-231 xenograft growth.
    Am J Pathol. 2007 Sep;171(3):1023-36 PMID: 17675579
  19. Notch activation induces Akt signaling via an autocrine loop to prevent apoptosis in breast epithelial cells.
    Cancer Res. 2009 Jun 15;69(12):5015-22 PMID: 19491273
  20. Functional diversity among Notch1, Notch2, and Notch3 receptors.
    Biochem Biophys Res Commun. 2002 Mar 8;291(4):775-9 PMID: 11866432
  21. Hit 'em where they live: targeting the cancer stem cell niche.
    Cancer Cell. 2007 Jan;11(1):3-5 PMID: 17222787
  22. Breast cancer, stem/progenitor cells and the estrogen receptor.
    Trends Endocrinol Metab. 2004 Jul;15(5):193-7 PMID: 15223047
  23. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy.
    J Natl Cancer Inst. 2008 May 7;100(9):672-9 PMID: 18445819
  24. The big brain aquaporin is required for endosome maturation and notch receptor trafficking.
    Cell. 2008 May 30;133(5):852-63 PMID: 18510929
  25. Notch-1 associates with IKKalpha and regulates IKK activity in cervical cancer cells.
    Oncogene. 2008 Oct 2;27(44):5833-44 PMID: 18560356
  26. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors.
    Cancer Res. 2006 Aug 1;66(15):7445-52 PMID: 16885340
  27. Mammary stem cells and breast cancer--role of Notch signalling.
    Stem Cell Rev. 2007 Jun;3(2):169-75 PMID: 17873349
  28. Identification of a cancer stem cell in human brain tumors.
    Cancer Res. 2003 Sep 15;63(18):5821-8 PMID: 14522905
  29. Direct inhibition of the NOTCH transcription factor complex.
    Nature. 2009 Nov 12;462(7270):182-8 PMID: 19907488
  30. Notch-1 activates estrogen receptor-alpha-dependent transcription via IKKalpha in breast cancer cells.
    Oncogene. 2010 Jan 14;29(2):201-13 PMID: 19838210
  31. Identification and expansion of human colon-cancer-initiating cells.
    Nature. 2007 Jan 4;445(7123):111-5 PMID: 17122771
  32. Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches.
    Cancer Res. 2008 Jul 1;68(13):5226-35 PMID: 18593923
  33. Circulating tumor cells: detection, molecular profiling and future prospects.
    Expert Rev Proteomics. 2007 Dec;4(6):741-56 PMID: 18067413
  34. Circulating tumor cells (CTC) detection: clinical impact and future directions.
    Cancer Lett. 2007 Aug 18;253(2):180-204 PMID: 17314005
  35. Therapeutic implications of cancer stem cells.
    Curr Opin Genet Dev. 2004 Feb;14(1):43-7 PMID: 15108804
  36. Cancer stem cells persist in many cancer cell lines.
    Cell Cycle. 2004 Apr;3(4):414-5 PMID: 15004528
  37. Structural requirements for assembly of the CSL.intracellular Notch1.Mastermind-like 1 transcriptional activation complex.
    J Biol Chem. 2003 Jun 6;278(23):21232-9 PMID: 12644465
  38. Identification of human brain tumour initiating cells.
    Nature. 2004 Nov 18;432(7015):396-401 PMID: 15549107
  39. Notch and cancer: a double-edged sword.
    Cell Mol Life Sci. 2007 Nov;64(21):2746-62 PMID: 17687513
  40. Cancer stem cells: implications for cancer treatment and prevention.
    Cancer J. 2007 Sep-Oct;13(5):271-5 PMID: 17921723
  41. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland.
    J Clin Invest. 2007 Dec;117(12):3988-4002 PMID: 18060036
  42. The multifaceted role of Notch in cancer.
    Curr Opin Genet Dev. 2007 Feb;17(1):52-9 PMID: 17178457
  43. Targeting Hedgehog--a cancer stem cell pathway.
    Clin Cancer Res. 2010 Jun 15;16(12):3130-40 PMID: 20530699
  44. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features.
    Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13820-5 PMID: 19666588
  45. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway.
    Cancer Res. 2009 Mar 15;69(6):2400-7 PMID: 19276344
  46. Oxygen concentration determines the biological effects of NOTCH-1 signaling in adenocarcinoma of the lung.
    Cancer Res. 2007 Sep 1;67(17):7954-9 PMID: 17804701
  47. Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression.
    J Cell Physiol. 2007 Nov;213(2):374-83 PMID: 17680632
  48. Cooperative assembly of higher-order Notch complexes functions as a switch to induce transcription.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2103-8 PMID: 17284587
  49. The canonical Notch signaling pathway: unfolding the activation mechanism.
    Cell. 2009 Apr 17;137(2):216-33 PMID: 19379690
  50. 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
  51. Identification of cells initiating human melanomas.
    Nature. 2008 Jan 17;451(7176):345-9 PMID: 18202660
  52. A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition.
    Nat Struct Mol Biol. 2008 Aug;15(8):849-57 PMID: 18660822
  53. Cancer stem cells and self-renewal.
    Clin Cancer Res. 2010 Jun 15;16(12):3113-20 PMID: 20530701
  54. Prospective identification of tumorigenic prostate cancer stem cells.
    Cancer Res. 2005 Dec 1;65(23):10946-51 PMID: 16322242
  55. Targeting Wnt signaling: can we safely eradicate cancer stem cells?
    Clin Cancer Res. 2010 Jun 15;16(12):3153-62 PMID: 20530697
  56. Identification and expansion of the tumorigenic lung cancer stem cell population.
    Cell Death Differ. 2008 Mar;15(3):504-14 PMID: 18049477
  57. The anti-apoptotic effect of Notch-1 requires p56lck-dependent, Akt/PKB-mediated signaling in T cells.
    J Biol Chem. 2004 Jan 23;279(4):2937-44 PMID: 14583609
  58. Targeting the NF-kappaB signaling pathway in Notch1-induced T-cell leukemia.
    Nat Med. 2007 Jan;13(1):70-7 PMID: 17173050
  59. Hypoxia requires notch signaling to maintain the undifferentiated cell state.
    Dev Cell. 2005 Nov;9(5):617-28 PMID: 16256737
  60. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts.
    Stem Cells. 2010 Jan;28(1):5-16 PMID: 19904829
  61. Notch3 and pre-TCR interaction unveils distinct NF-kappaB pathways in T-cell development and leukemia.
    EMBO J. 2006 Mar 8;25(5):1000-8 PMID: 16498412
  62. Off the beaten pathway: the complex cross talk between Notch and NF-kappaB.
    Lab Invest. 2008 Jan;88(1):11-7 PMID: 18059366
  63. T cell leukemia-associated human Notch/translocation-associated Notch homologue has I kappa B-like activity and physically interacts with nuclear factor-kappa B proteins in T cells.
    J Exp Med. 1996 May 1;183(5):2025-32 PMID: 8642313
  64. The prolyl-isomerase Pin1 is a Notch1 target that enhances Notch1 activation in cancer.
    Nat Cell Biol. 2009 Feb;11(2):133-42 PMID: 19151708
  65. HER-2, notch, and breast cancer stem cells: targeting an axis of evil.
    Clin Cancer Res. 2009 Mar 15;15(6):1845-7 PMID: 19276254
  66. Targeting transcription factors in acute leukemia in children.
    Curr Drug Targets. 2007 Jun;8(6):727-37 PMID: 17584028
  67. Skin-derived TSLP triggers progression from epidermal-barrier defects to asthma.
    PLoS Biol. 2009 May 19;7(5):e1000067 PMID: 19557146
  68. Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling.
    Mol Cell Biol. 2009 Nov;29(21):5679-95 PMID: 19704010
  69. Opposite effects of Notch-1 and Notch-2 on mesothelioma cell survival under hypoxia are exerted through the Akt pathway.
    Cancer Res. 2008 Dec 1;68(23):9678-85 PMID: 19047145
  70. Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways.
    J Natl Cancer Inst. 2007 Apr 18;99(8):616-27 PMID: 17440163
  71. Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis.
    Cell Stem Cell. 2009 Aug 7;5(2):191-203 PMID: 19664993
  72. Let me do more than count the ways: what circulating tumor cells can tell us about the biology of cancer.
    Mol Pharm. 2009 Sep-Oct;6(5):1307-10 PMID: 19634916
  73. Cancer stem cells and hepatocellular carcinoma.
    Cancer Biol Ther. 2009 Sep;8(18):1691-8 PMID: 19901516
  74. Nuclear signalling by tumour-associated antigen EpCAM.
    Nat Cell Biol. 2009 Feb;11(2):162-71 PMID: 19136966
  75. Involvement of Notch-1 signaling in bone marrow stroma-mediated de novo drug resistance of myeloma and other malignant lymphoid cell lines.
    Blood. 2004 May 1;103(9):3503-10 PMID: 14670925
  76. Regulation of the ERBB-2 promoter by RBPJkappa and NOTCH.
    J Biol Chem. 1997 May 30;272(22):14110-4 PMID: 9162037
  77. Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis.
    J Clin Pharmacol. 2005 Aug;45(8):872-7 PMID: 16027397
  78. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres.
    Stem Cells. 2007 Mar;25(3):807-15 PMID: 17158237
  79. Notch signaling.
    Clin Cancer Res. 2006 Feb 15;12(4):1074-9 PMID: 16489059
  80. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo.
    Science. 2004 May 28;304(5675):1331-4 PMID: 15143218
  81. Cancerous stem cells can arise from pediatric brain tumors.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15178-83 PMID: 14645703
  82. Cancer metastasis facilitated by developmental pathways: Sonic hedgehog, Notch, and bone morphogenic proteins.
    J Cell Biochem. 2007 Nov 1;102(4):829-39 PMID: 17914743
  83. The Notch pathway in prostate development and cancer.
    Differentiation. 2008 Jul;76(6):699-716 PMID: 18565101
  84. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line.
    Cancer Res. 2007 Apr 15;67(8):3716-24 PMID: 17440084
  85. Notch signaling: the core pathway and its posttranslational regulation.
    Dev Cell. 2009 May;16(5):633-47 PMID: 19460341
  86. ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a gamma-secretase inhibitor.
    Oncogene. 2008 Aug 28;27(37):5019-32 PMID: 18469855
  87. Cancer stem cells in human gastrointestinal cancers.
    Hum Cell. 2006 Feb;19(1):24-9 PMID: 16643604
  88. Modulation of Notch signaling by antibodies specific for the extracellular negative regulatory region of NOTCH3.
    J Biol Chem. 2008 Mar 21;283(12):8046-54 PMID: 18182388
  89. Ligand endocytosis drives receptor dissociation and activation in the Notch pathway.
    Development. 2000 Apr;127(7):1373-85 PMID: 10704384
  90. Induction of pluripotent stem cells from adult human fibroblasts by defined factors.
    Cell. 2007 Nov 30;131(5):861-72 PMID: 18035408
  91. Selective targeting of cancer stem cells: a new concept in cancer therapeutics.
    BioDrugs. 2007;21(5):299-310 PMID: 17896836
  92. Cancer stem cells--an old idea that's new again: implications for the diagnosis and treatment of breast cancer.
    Expert Opin Biol Ther. 2007 Apr;7(4):431-8 PMID: 17373895
  93. Human Notch-1 inhibits NF-kappa B activity in the nucleus through a direct interaction involving a novel domain.
    J Immunol. 2001 Jul 1;167(1):289-95 PMID: 11418662
  94. Monoubiquitination and endocytosis direct gamma-secretase cleavage of activated Notch receptor.
    J Cell Biol. 2004 Jul 5;166(1):73-83 PMID: 15240571
  95. Drosophila deltex mediates suppressor of Hairless-independent and late-endosomal activation of Notch signaling.
    Development. 2004 Nov;131(22):5527-37 PMID: 15496440
  96. Number crunching in the cancer stem cell market.
    Breast Cancer Res. 2009;11(2):302 PMID: 19439026
  97. The possible correlation of Notch-1 and Notch-2 with clinical outcome and tumour clinicopathological parameters in human breast cancer.
    Int J Mol Med. 2004 Nov;14(5):779-86 PMID: 15492845
  98. Notch signaling in cancer.
    Cancer Biol Ther. 2002 Sep-Oct;1(5):466-76 PMID: 12496471
  99. Notch1 and notch2 have opposite effects on embryonal brain tumor growth.
    Cancer Res. 2004 Nov 1;64(21):7787-93 PMID: 15520184
  100. Notch signaling, gamma-secretase inhibitors, and cancer therapy.
    Cancer Res. 2007 Mar 1;67(5):1879-82 PMID: 17332312
  101. Gamma-secretase: proteasome of the membrane?
    Nat Rev Mol Cell Biol. 2004 Jun;5(6):499-504 PMID: 15173829
  102. ADAM10, the rate-limiting protease of regulated intramembrane proteolysis of Notch and other proteins, is processed by ADAMS-9, ADAMS-15, and the gamma-secretase.
    J Biol Chem. 2009 Apr 24;284(17):11738-47 PMID: 19213735
  103. Endocytic regulation of Notch signaling.
    Curr Opin Genet Dev. 2009 Aug;19(4):323-8 PMID: 19447603
  104. gamma-Secretase inhibitors abrogate oxaliplatin-induced activation of the Notch-1 signaling pathway in colon cancer cells resulting in enhanced chemosensitivity.
    Cancer Res. 2009 Jan 15;69(2):573-82 PMID: 19147571
  105. Induced pluripotent stem cell lines derived from human somatic cells.
    Science. 2007 Dec 21;318(5858):1917-20 PMID: 18029452
  106. Rational targeting of Notch signaling in cancer.
    Oncogene. 2008 Sep 1;27(38):5124-31 PMID: 18758481
  107. Notch1 and Notch2 inhibit myeloid differentiation in response to different cytokines.
    Mol Cell Biol. 1998 Apr;18(4):2324-33 PMID: 9528802
  108. Stem cell-like cancer cells in cancer cell lines.
    Cancer Biomark. 2007;3(4-5):245-50 PMID: 17917153
Article Info
Journal
Clinical cancer research : an official journal of the American Association for Cancer Research
Abbr.
Clin Cancer Res
ISSN
1557-3265
Published
2010-06-15
Epub
2010-00-08
Pages
3141-52
Language
English
Region
United States
NLM ID
9502500
PMCID
PMC3008160
Subset
IM
Grants
NIA NIH HHS · P01 AG025531 · United States
NIA NIH HHS · P01 AG025531-040003 · United States
NIA NIH HHS · P01 AG2553101 · United States
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