Notch1-induced brain tumor models the sonic hedgehog subgroup of human medulloblastoma

Cancer Research

Volumn 73, Issue 17, 2013, Pages 5381-5390

  Natarajan, Sivaraman ^a   Li, Yaochen ^a   Miller, Emily E ^a   Shih, David J ^e   Taylor, Michael D ^e   Stearns, Timothy M ^a   Bronson, Roderick T ^d   Ackerman, Susan L ^a,b   Yoon, Jeong K ^c   Yun, Kyuson ^a  

^a JACKSON LABORATORY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Maine Medical Center Research Institute   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; PROTEIN P53; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATAXIA; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; MEDULLOBLASTOMA; MOUSE; MOUSE EMBRYO; NONHUMAN; NOTCH1 GENE; ONCOGENE; PRIORITY JOURNAL; SEIZURE; TRANSGENIC MOUSE; TUMOR MODEL;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLAR NEOPLASMS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HEDGEHOG PROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; MEDULLOBLASTOMA; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 84883474106     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-0033     Document Type: Article

References (43)

1. Allenspach EJ, Maillard I, Aster JC, Pear WS. Notch signaling in cancer. Cancer Biol Ther 2002;1:466-76.
2. Koch U, Radtke F. Notch signaling in solid tumors. Curr Top Dev Biol 2010;92:411-55.
3. Pierfelice TJ, Schreck KC, Eberhart CG, Gaiano N. Notch, neural stem cells, and brain tumors. Cold Spring Harb Symp Quant Biol 2008;73: 367 -75.
4. Pierfelice T, Alberi L, Gaiano N. Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 2011;69:840-55.
5. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009;137:216-33.
6. Aster JC, Pear WS, Blacklow SC. Notch signaling in leukemia. Annu Rev Pathol 2008;3:587-613. (Pubitemid 351488294)
7. Weng AP, Ferrando AA, Lee W, Morris JPt, Silverman LB, Sanchez-Irizarry C, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004;306:269-71. (Pubitemid 39336870)
8. Purow BW, Haque RM, Noel MW, Su Q, Burdick MJ, Lee J, et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 2005;65: 2353-63. (Pubitemid 40490146)
9. Behesti H, Marino S. Cerebellar granule cells: insights into proliferation, differentiation, and role in medulloblastoma pathogenesis. Int J Biochem Cell Biol 2009;41:435-45.
10. Yang ZJ, Ellis T, Markant SL, Read TA, Kessler JD, Bourboulas M, et al. Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 2008;14: 135-45.
11. Schuller U, Heine VM, Mao J, Kho AT, Dillon AK, Han YG, et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 2008;14:123-34.
12. Hamilton SR, Liu B, Parsons RE, Papadopoulos N, Jen J, Powell SM, et al. The molecular basis of Turcot's syndrome. N Engl J Med 1995;332:839-47.
13. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM, et al. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 1996;272:1668-71. (Pubitemid 26200029)
14. Fan X, Mikolaenko I, Elhassan I, Ni X, Wang Y, Ball D, et al. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 2004;64:7787-93. (Pubitemid 39446911)
15. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012;488: 106-10.
16. Jones DT, Jager N, Kool M, Zichner T, Hutter B, Sultan M, et al. Dissecting the genomic complexity underlying medulloblastoma. Nature 2012;488:100-5.
17. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006;66:7445-52. (Pubitemid 44289197)
18. Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010;28:5-16.
19. Hovinga KE, Shimizu F, Wang R, Panagiotakos G, Van Der Heijden M, Moayedpardazi H, et al. Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 2010;28:1019-29.
20. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, et al. Notch promotes radioresistance of glioma stem cells. Stem Cells 2010;28:17-28.
21. Dang L, Fan X, Chaudhry A, Wang M, Gaiano N, Eberhart CG. Notch3 signaling initiates choroid plexus tumor formation. Oncogene 2006;25: 487-91. (Pubitemid 43117634)
22. Pierfelice TJ, Schreck KC, Dang L, Asnaghi L, Gaiano N, Eberhart CG. Notch3 activation promotes invasive glioma formation in a tissue site-specific manner. Cancer Res 2011;71:1115-25.
23. Tchorz JS, Tome M, Cloetta D, Sivasankaran B, Grzmil M, Huber RM, et al. Constitutive Notch2 signaling in neural stem cells promotes tumorigenic features and astroglial lineage entry. Cell Death Dis 2012;3:e325.
24. Li Y, Hibbs MA, Gard AL, Shylo NA, Yun K. Genome-wide analysis of N1ICD/RBPJ targets in vivo reveals direct transcriptional regulation of Wnt, SHH, and Hippo pathway effectors by Notch1. Stem Cells 2012;30:741-52.
25. Yang X, Klein R, Tian X, Cheng HT, Kopan R, Shen J. Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev Biol 2004;269:81-94. (Pubitemid 38471825)
26. Venkatesh DA, Park KS, Harrington A, Miceli-Libby L, Yoon JK, Liaw L. Cardiovascular and hematopoietic defects associated with Notch1 activation in embryonic Tie2-expressing populations. Circ Res 2008;103:423-31.
27. 2/M arrest in response to DNA damage and in growth control after damage recovery. Oncogene 2001;20:3290-300.
28. Okamoto K, Beach D. Cyclin G is a transcriptional target of the p53 tumor suppressor protein. EMBO J 1994;13:4816-22. (Pubitemid 24319363)
29. Brosh R, Sarig R, Natan EB, Molchadsky A, Madar S, Bornstein C, et al. p53-dependent transcriptional regulation of EDA2R and its involvement in chemotherapy-induced hair loss. FEBS Lett 2010;584:2473-7.
30. Morrison SJ, Perez SE, Qiao Z, Verdi JM, Hicks C, Weinmaster G, et al. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 2000;101: 499-510.
31. Taylor MD, Northcott PA, Korshunov A, Remke M, Cho YJ, Clifford SC, et al. Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol 2012;123:465-72.
32. Kool M, Koster J, Bunt J, Hasselt NE, Lakeman A, van Sluis P, et al. Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PLoS One 2008;3:e3088.
33. Solecki DJ, Liu XL, Tomoda T, Fang Y, Hatten ME. Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 2001;31:557-68. (Pubitemid 32835111)
34. Lee Y, McKinnon PJ. DNA ligase IV suppresses medulloblastoma formation. Cancer Res 2002;62:6395-9. (Pubitemid 35364093)
35. Tong WM, Ohgaki H, Huang H, Granier C, Kleihues P, Wang ZQ. Null mutation of DNA strand break-binding molecule poly(ADP-ribose) polymerase causes medulloblastomas in p53(-/-) mice. Am J Pathol 2003;162:343-52. (Pubitemid 36042016)
36. Frappart PO, Lee Y, Russell HR, Chalhoub N, Wang YD, Orii KE, et al. Recurrent genomic alterations characterize medulloblastoma arising from DNA double-strand break repair deficiency. Proc Natl Acad Sci U S A 2009;106:1880-5.
37. Yan CT, Kaushal D, Murphy M, Zhang Y, Datta A, Chen C, et al. XRCC4 suppresses medulloblastomas with recurrent translocations in p53- deficient mice. Proc Natl Acad Sci U S A 2006;103:7378-83. (Pubitemid 43727841)
38. Julian E, Dave RK, Robson JP, Hallahan AR, Wainwright BJ. Canonical Notch signaling is not required for the growth of Hedgehog pathway-induced medulloblastoma. Oncogene 2010;29:3465-76.
39. Hatton BA, Villavicencio EH, Pritchard J, LeBlanc M, Hansen S, Ulrich M, et al. Notch signaling is not essential in sonic hedgehog-activated medulloblastoma. Oncogene 2010;29:3865-72.
40. Northcott PA, Jones DT, Kool M, Robinson GW,Gilbertson RJ, Cho YJ, et al. Medulloblastomics: the end of the beginning. Nat Rev Cancer 2012;12:818-34.
41. Aster JC, Xu L, Karnell FG, Patriub V, Pui JC, Pear WS. Essential roles for ankyrin repeat and transactivation domains in induction of T-cell leukemia by notch1. Mol Cell Biol 2000;20: 7505 -15.
42. Aster JC, Robertson ES, Hasserjian RP, Turner JR, Kieff E, Sklar J. Oncogenic forms of NOTCH1 lacking either the primary binding site for RBP-Jkappa or nuclear localization sequences retain the ability to associate with RBP-Jkappa and activate transcription. J Biol Chem 1997;272:11336-43. (Pubitemid 27184136)
43. Lujambio A, Akkari L, Simon J, Grace D, Tschaharganeh DF, Bolden JE, et al. Non-cell-autonomous tumor suppression by p53. Cell 2013; 153:449-60.