Targeting Notch pathway induces growth inhibition and differentiation of neuroblastoma cells

Neuro-Oncology

Volumn 12, Issue 12, 2010, Pages 1231-1243

  Ferrari Toninelli, Giulia ^a   Bonini, Sara Anna ^a   Uberti, Daniela ^a   Buizza, Laura ^a   Bettinsoli, Paola ^a   Poliani, Pietro Luigi ^b   Facchetti, Fabio ^b   Memo, Maurizio ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

Author keywords

secretase inhibitors; 13 cis retinoic acid; Cell migration; Differentiation; Neuroblastoma

Indexed keywords

2 CHLORO 3 (3,4 DICHLOROPHENYL) 1 ISOPROPYL 4 METHYLIMIDAZOLIUM CHLORIDE; ANTINEOPLASTIC AGENT; DAPT; GAMMA SECRETASE INHIBITOR; JAGGED1; NOTCH BLOCKING GAMMA SECRETASE INHIBITOR; NOTCH RECEPTOR; RETINOIC ACID; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA CELL; PROTEIN TARGETING; TUMOR DIFFERENTIATION;

AMYLOID PRECURSOR PROTEIN SECRETASES; APOPTOSIS; BENZODIAZEPINONES; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; DERMATOLOGIC AGENTS; DRUG THERAPY, COMBINATION; FLOW CYTOMETRY; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOTRETINOIN; MEMBRANE PROTEINS; NEUROBLASTOMA; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; WOUND HEALING;

EID: 78650096138     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/noq101     Document Type: Article

References (56)

1. Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet.2007;369(9579):2106-2120.
2. Lau L, Tai D, Weitzman S, Grant R, Baruchel S, Malkin D. Factors influencingsurvival in children with recurrent neuroblastoma. J PediatrHematol Oncol. 26:227-232.
3. Matthay KK, Villablanca JC, Seeger RCS, et al. Treatment of high-riskneuroblastoma with intensive chemotherapy, radiotherapy, autologousbone marrow transplantation, and 13-cis-retinoic acid. Children'sCancer Group. N Engl J Med. 1999;341(16):1165-1173.
4. Garattini E, Gianni M, Terao M. Cytodifferentiation by retinoids, anovel therapeutic option in oncology: rational combinations withother therapeutic agents. Vitam Horm. 2007;75:301-354.
5. De los Santos M, Zambrano A, Aranda A. Combined effects of retinoicacid and histone deacetylase inhibitors on human neuroblastomaSH-SY5Y cells. Mol Cancer Ther. 2007;6(4):1425-1432.
6. Guzhova I, Hultquist A, Cetinkaya C, Nilsson K, Påhlman S, Larsson LG.Interferon-gamma cooperates with retinoic acid and phorbol ester toinduce differentiation and growth inhibition of human neuroblastomacells. Int J Cancer. 2001;94(1):97-108.
7. Hahn CK, Ross KN, Warrington IM, et al. Expression-based screeningidentifies the combination of histone deacetylase inhibitors and retinoidsfor neuroblastoma differentiation. Proc Natl Acad Sci USA.2008;105(28):9751-9756.
8. Brodeur GM. Neuroblastoma: biological insights into a clinical enigma.Nat Rev Cancer. 2003;3(3):203-216.
9. Wagner LM, Danks MK. New therapeutic targets for the treatment ofhigh-risk neuroblastoma. J Cell Biochem. 2009;107:46-57.
10. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat RevMol Cell Biol. 2006;7(9):678-689.
11. Louvi A, Artavanis-Tsakonas S. Notch signalling in vertebrate neuraldevelopment. Nat Rev Neurosci. 2006;7(2):93-100.
12. Sestan N, Artavanis-Tsakonas S, Rakic P. Contact-dependent inhibitionof cortical neurite growth mediated by Notch signaling. Science.1999;286(5440):741- 746.
13. Ferrari-Toninelli G, Bonini SA, Bettinsoli P, Uberti D, Memo M.Microtubule stabilizing effect of Notch activation in primary corticalneurons. Neuroscience. 2008;154(3):946-952.
14. Ferrari-Toninelli G, Bonini SA, Uberti D, et al. Notch activation inducesneurite remodeling and functional modifications in SH-SY5Y neuronalcells. Dev Neurobiol. 2009;69(6):378-391.
15. Leong KG, Karsan A. Recent insights into the role of Notch signaling intumorigenesis. Blood. 2006;107(6):2223-2233.
16. Såhlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signallingmediates hypoxia-induced tumor cell migration and invasion. ProcNatl Acad Sci USA. 2008;105(17):6392-6397.
17. Rehman AO, Wang CY. Notch signaling in the regulation of tumorangiogenesis. Trends Cell Biol. 2006;16(6):293-300.
18. Dufraine J, Funahashi Y, Kitajewski J. Notch signaling regulatestumor angiogenesis by diverse mechanisms. Oncogene. 2008;27(38):5132-5137.
19. Bolós V, Blanco M, Medina V, Aparicio G, Díaz-Prado S, Grande E.Notch signalling in cancer stem cells. Clin Transl Oncol.2009;11(1):11- 19.
20. Miele L, Miao H, Nickoloff BJ. Notch signaling as a novel cancer therapeutictarget. Curr Cancer Drug Targets. 2006;6(4):313-323.
21. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B, Miele L. Rationaltargeting of Notch signaling in cancer. Oncogene. 2008;27(38):5124-5131.
22. De Keersmaecker K, Lahortiga I, Mentens N, et al. In vitro validation ofgamma secretase inhibitors alone or in combination with otheranti-cancer drugs for treatment of T-cell acute lymphoblastic leukaemia.Haematologica. 2008;93(4):533-542.
23. Baliko F, Bright T, Poon R, Cohen B, Egan SE, Alman BA. Inhibition ofNotch signaling induces neural differentiation in Ewing sarcoma. Am JPathol. 2007;170(5):1686-1694.
24. Hallahan AR, Pritchard JI, Hansen S, et al. The SmoA1 mouse modelreveals that Notch signaling is critical for the growth and survival ofsonic hedgehog-induced medulloblastoma. Cancer Res. 2004;64(21):7794-7800.
25. Shih IeM, Wang TL. Notch signaling, gamma-secretase inhibitors, andcancer therapy. Cancer Res. 2007;67(5):1879-1882.
26. Påhlman S, Stockhausen MT, Fredlund E, Axelson H. Notch signaling inneuroblastoma. Semin Cancer Biol. 2004;14:365-373.
27. Sarovina K, Schellenberger J, Schneider C, et al. Progenitor cell maintenanceand neurogenesis in sympathetic ganglia involves Notch signalling.Mol Cell Neurosci. 2008;37:20-31.
28. Revet I, Huizenga G, Chan A, et al. The MSX1 homeobox transcriptionfactor is a downstream target of PHOX2B and activates theDelta-Notch pathway in neuroblastoma. Exp Cell Res. 2008;314(4):707-719.
29. Grynfeld A, Påhlman S, Axelson H. Induced neuroblastoma cell differentiation,associated with transient HES-1 activity and reducedHASH-1 expression, is inhibited by Notch1. Int J Cancer. 2000;88:401-410.
30. Hooper C, Tavassoli M, Chapple PJ, et al. TAp73 isoforms antagonizeNotch signalling in SH-SY5Y neuroblastomas and in primary neurones.J Neurochem. 2006;99:989-999.
31. Stockhausen MT, Sjölund J, Axelson H. Regulation of the Notch targetgene Hes-1 by TGFa induced Ras/MAPK signalling in human neuroblastomacells. Exp Cell Res. 2005;310:218-228.
32. Kim Y, Lin Q, Zelterman D, et al. Hypoxia regulated Delta-like 1 homologueenhance cancer cell stemness and tumorigenicity. Cancer Res.2009;69(24):9271-9280.
33. Pession A, Tonelli R. The MYCN oncogene as a specific and selectivedrug target for peripheral and central nervous system tumors. CurrCancer Drug Targets. 2005;5(4):273-283.
34. Zhao X, D'Arca D, Lim WK, et al. The N-Myc-DLL3 cascade is suppressedby the ubiquitin ligase Huwe1 to inhibit proliferation and promote neurogenesisin the developing brain. Dev Cell. 2009;17(2):210-221.
35. Janardhanan R, Banik NL, Ray SK. N-Myc down regulation induceddifferentiation, early cell cycle exit, and apoptosis in human malignantneuroblastoma cells having wild type or mutant p53 BiochemPharmacol. 2009;78:1105-1114.
36. Funahashi Y, Hernandez SL, Das I, et al. A Notch1 ectodomain constructinhibits endothelial Notch signaling, tumor growth, and angiogenesis.Cancer Res. 2008;68(12):4727-4735.
37. Nickoloff BJ, Quin JZ, Chaturvedi V, Denning MF, Bonish B, Miele L.Jagged-1 mediated activation of Notch signalling induces completematuration of human keratinocytes through NF-kB and PPARg. CellDeath Diff. 2002;9:842-855.
38. Bordow SB, Haber M, Madafiglio J, Cheung B, Marshall GM, Norris MD.Expression of the multidrug resistance-associated protein (MRP) gene correlateswith amplification and overexpression of the N-myc oncogene inchildhood neuroblastoma. Cancer Res. 1994;54(19):5036-5040.
39. Lleò A. Activity of g-secretase on substrate other than APP. Curr TopMed Chem. 2008;8:9-16.
40. Zampagni M, Evangelisti E, Cascella R, et al. Lipid rafts are primarymediators of amyloid oxidative attack on plasma membrane. J MolMed. 2010;88(6):597-608.
41. Petit A, Pasini A, Alves da Costa C, et al. JLK isocoumarin inhibitors:selective g-secretase inhibitors that do not interfere with Notchpathway in vitro or in vivo. J Neurosci Res. 2003;74:370-377.
42. Hellström M, Phng LK, Hofmann JJ, et al. Dll4 signalling throughNotch1 regulates formation of tip cells during angiogenesis. Nature.2007;445(7129):776-780.
43. Joshi S, Guleria RS, Pan J, Dipette D, Singh US. Heterogeneity in retinoicacid signaling in neuroblastomas: Role of matrix metalloproteinases inretinoic acid-induced differentiation. Biochim Biophys Acta. 2007;1772(9):1093-1102.
44. Joshi S, Guleria R, Pan J, DiPette D, Singh US. Retinoic acid receptorsand tissue-transglutaminase mediate short-term effect of retinoic acidon migration and invasion of neuroblastoma SH-SY5Y cells.Oncogene. 2006;25(2):240-247.
45. Zaizen Y, Taniguchi S, Suita S. The role of cellular motility in the invasionof human neuroblastoma cells with or without N-myc amplification andexpression. J Pediatr Surg. 1998;33(12):1765-1770.
46. Rao SS, O'Neil J, Liberator CD, et al. Inhibition of NOTCH signaling bygamma secretase inhibitor engages the RB pathway and elicits cell cycleexit in T-cell acute lymphoblastic leukaemia cells. Cancer Res.2009;69(7):3060-3068.
47. Rasul S, Balasubramanian R, Filipović A, Slade MJ, Yagüe E, CoombesRC. Inhibition of gamma-secretase induces G2/M arrest andtriggers apoptosis in breast cancer cells. Br J Cancer. 2009;100(12):1879-1888.
48. Berezovska O, McLean P, Knowles R, et al. Notch1 inhibits neurite outgrowthin postmitotic primary neurons. Neuroscience. 1999;93(2):433-439.
49. Liao YF, Wang BJ, Hsu WM, et al. Unnatural substituted (hydroxyethylurea) peptidomimetics inhibit gamma secretase and promote theneuronal differentiation of neuroblastoma cells. Mol Pharmacol.2007;71(2):588-601.
50. Nefedova Y, Sullivan DM, Bolick SC, Dalton WS, Gabrilovich DI.Inhibition of Notch signaling induces apoptosis of myeloma cells andenhances sensitivity chemotherapy. Blood. 2008;111(4):2220-2229.
51. Real PJ, Tosello V, Palomero T, Castillo M, et al. Gamma- secretaseinhibitors reverse glucocorticoid resistance in T cell acute lymphoblasticleukemia. Nat Med. 2009;15(1):50-58.
52. Bailey JM, Singh PK, Hollingsworth MA. Cancer metastasis facilitated bydevelopmental pathways: Sonic hedgehog, Notch, and bone morphogenicproteins. J Cell Biochem. 2007;102(4):829-839.
53. Garaventa A, Perilongo G. High risk neuroblastoma: a persistent therapeuticchallenge. Pediatr Blood Cancer. 2008;51:722-723.
54. Nara K, Kusafuka T, Yoneda A, Oue T, Sangkhathat S, Fukuzawa M.Silencing of MYCN by RNA interference induces growth inhibition,apoptotic activity and cell differentiation in a neuroblastoma cell linewith MYCN amplification. Int J Oncol. 2007;30(5):1189-1196.
55. EdsjöA, Nilsson H, Vandesompele J, Karlsson J, Pattyn F, Culp LA, et al.Neuroblastoma cells with overexpressed MYCN retain their capacityto undergo neuronal differentiation. Lab Invest. 2004;84(4):406-417.
56. Yang T, Arslanova D, Gu Y, Augelli-Szafran C, Xia W. Quantification ofgamma-secretase modulation differentiates inhibitor compound selectivitybetween two substrates Notch and amyloid precursor protein.Mol Brain. 2008;1(1):15.