NOTCH ligands JAG1 and JAG2 as critical pro-survival factors in childhood medulloblastoma

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Fiaschetti, Giulio ^a   Schroeder, Christina ^c   Castelletti, Deborah ^a   Arcaro, Alexandre ^c   Westermann, Frank ^b   Baumgartner, Martin ^a   Shalaby, Tarek ^a   Grotzer, Michael A ^a  

^a UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

JAG1; JAG2; Medulloblastoma; NOTCH; Pediatric cancer

Indexed keywords

CALCIUM BINDING PROTEIN; JAG2 PROTEIN, HUMAN; MEMBRANE PROTEIN; MYC PROTEIN; MYC PROTEIN, HUMAN; NOTCH RECEPTOR; SERRATE PROTEINS; SIGNAL PEPTIDE; SMALL INTERFERING RNA;

APOPTOSIS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLUM TUMOR; CHILD; CHROMATIN IMMUNOPRECIPITATION; COHORT ANALYSIS; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; MEDULLOBLASTOMA; METABOLISM; PATHOLOGY;

APOPTOSIS; CALCIUM-BINDING PROTEINS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLAR NEOPLASMS; CHILD; CHROMATIN IMMUNOPRECIPITATION; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEDULLOBLASTOMA; MEMBRANE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, NOTCH; RNA, SMALL INTERFERING;

EID: 84921367324     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-2-39     Document Type: Article

References (45)

1. Dennis M, Spiegler BJ, Hetherington CR, Greenberg ML: Neuropsychological sequelae of the treatment of children with medulloblastoma. J Neurooncol 1996, 29: 91-101. 10.1007/BF00165522
2. Taylor MD, Northcott PA, Korshunov A, Remke M, Cho YJ, Clifford SC, Eberhart CG, Parsons DW, Rutkowski S, Gajjar A, Ellison DW, Lichter P, Gilbertson RJ, Pomeroy SL, Kool M, Pfister SM: Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol 2012, 123(4):465-472. 10.1007/s00401-011-0922-z
3. Gilbertson R: Paediatric embryonic brain tumours. biological and clinical relevance of molecular genetic abnormalities. Eur J Cancer 2002, 38(5):675-685. 10.1016/S0959-8049(01)00315-X
4. Gilbertson RJ, Ellison DW: The origins of medulloblastoma subtypes. Annu Rev Pathol 2008, 3: 341-365. 10.1146/annurev.pathmechdis.3.121806.151518
5. Fiuza UM, Arias AM: Cell and molecular biology of Notch. J Endocrinol 2007, 194(3):459-474. 10.1677/JOE-07-0242
6. Yoon K, Gaiano N: Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 2005, 8(6):709-715. 10.1038/nn1475
7. Radtke F, Raj K: The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer 2003, 3(10):756-767. 10.1038/nrc1186
8. Bray SJ: Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 2006, 7(9):678-689. 10.1038/nrm2009
9. Guruharsha KG, Kankel MW, Artavanis-Tsakonas S: The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat Rev Genet 2012, 13(9):654-666. 10.1038/nrg3272
10. D'Souza B, Miyamoto A, Weinmaster G: The many facets of Notch ligands. Oncogene 2008, 27(38):5148-5167. 10.1038/onc.2008.229
11. Allenspach EJ, Maillard I, Aster JC, Pear WS: Notch signaling in cancer. Cancer Biol Ther 2002, 1(5):466-476. 10.4161/cbt.1.5.162
12. Zweidler-McKay PA: Notch signaling in pediatric malignancies. Curr Oncol Rep 2008, 10(6):459-468. 10.1007/s11912-008-0071-2
13. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA: Notch promotes radioresistance of glioma stem cells. Stem cells (Dayton, Ohio) 2010, 28(1):17-28.
14. Miele L, Miao H, NickoloffBJ: NOTCH signaling as a novel cancer therapeutic target. Current cancer drug targets 2006, 6(4):313-323. 10.2174/156800906777441771
15. Wang Z, Li Y, Banerjee S, Kong D, Ahmad A, Nogueira V, Hay N, Sarkar FH: Down-regulation of Notch-1 and Jagged-1 inhibits prostate cancer cell growth, migration and invasion, and induces apoptosis via inactivation of Akt, mTOR, and NF-kappaB signaling pathways. J Cell Biochem 2010, 109(4):726-736.
16. Koch U, Radtke F: Notch and cancer: a double-edged sword. Cell Mol Life Sci 2007, 64(21):2746-2762. 10.1007/s00018-007-7164-1
17. Fan X, Mikolaenko I, Elhassan I, Ni X, Wang Y, Ball D, Brat DJ, Perry A, Eberhart CG: Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 2004, 64(21):7787-7793. 10.1158/0008-5472.CAN-04-1446
18. Fiaschetti G, Castelletti D, Zoller S, Schramm A, Schroeder C, Nagaishi M, Stearns D, Mittelbronn M, Eggert A, Westermann F, Ohgaki H, Shalaby T, Pruschy M, Arcaro A, Grotzer MA: Bone morphogenetic protein-7 is a MYC target with prosurvival functions in childhood medulloblastoma. Oncogene 2011, 30(25):2823-2835. 10.1038/onc.2011.10
19. Kunkele A, De Preter K, Heukamp L, Thor T, Pajtler KW, Hartmann W, Mittelbronn M, Grotzer MA, Deubzer HE, Speleman F, Schramm A, Eggert A, Schulte JH: Pharmacological activation of the p53 pathway by nutlin-3 exerts anti-tumoral effects in medulloblastomas. Neuro-oncology 2012, 14(7):859-869. 10.1093/neuonc/nos115
20. Stearns D, Chaudhry A, Abel TW, Burger PC, Dang CV, Eberhart CG: c-myc overexpression causes anaplasia in medulloblastoma. Cancer res 2006, 66(2):673-681. 10.1158/0008-5472.CAN-05-1580
21. Thompson MC, Fuller C, Hogg TL, Dalton J, Finkelstein D, Lau CC, Chintagumpala M, Adesina A, Ashley DM, Kellie SJ, Taylor MD, Curran T, Gajjar A, Gilbertson RJ: Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations. J Clin Oncol 2006, 24(12):1924-1931. 10.1200/JCO.2005.04.4974
22. Fattet S, Haberler C, Legoix P, Varlet P, Lellouch-Tubiana A, Lair S, Manie E, Raquin MA, Bours D, Carpentier S, Barillot E, Grill J, Doz F, Puget S, Janoueix-Lerosey I, Delattre O: Beta-catenin status in paediatric medulloblastomas: correlation of immunohistochemical expression with mutational status, genetic profiles, and clinical characteristics. J Pathol 2009, 218(1):86-94. 10.1002/path.2514
23. Kool M, Koster J, Bunt J, Hasselt NE, Lakeman A, van Sluis P, Troost D, Meeteren NS, Caron HN, Cloos J, Mrsic A, Ylstra B, Grajkowska W, Hartmann W, Pietsch T, Ellison D, Clifford SC, Versteeg R: Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PloS one 2008, 3(8):e3088. 10.1371/journal.pone.0003088
24. Northcott PA, Shih DJ, Peacock J, Garzia L, Morrissy AS, Zichner T, Stutz AM, Korshunov A, Reimand J, Schumacher SE, Beroukhim R, Ellison DW, Marshall CR, Lionel AC, Mack S, Dubuc A, Yao Y, Ramaswamy V, Luu B, Rolider A, Cavalli FM, Wang X, Remke M, Wu X, Chiu RY, Chu A, Chuah E, Corbett RD, Hoad GR, Jackman SD, et al.: Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature 2012, 488(7409):49-56. 10.1038/nature11327
25. Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, Mack S, Bouffet E, Clifford SC, Hawkins CE, French P, Rutka JT, Pfister S, Taylor MD: Medulloblastoma comprises four distinct molecular variants. J Clin Oncol 2011, 29(11):1408-1414. 10.1200/JCO.2009.27.4324
26. Robinson G, Parker M, Kranenburg TA, Lu C, Chen X, Ding L, Phoenix TN, Hedlund E, Wei L, Zhu X, Chalhoub N, Baker SJ, Huether R, Kriwacki R, Curley N, Thiruvenkatam R, Wang J, Wu G, Rusch M, Hong X, Becksfort J, Gupta P, Ma J, Easton J, Vadodaria B, Onar-Thomas A, Lin T, Li S, Pounds S, Paugh S, et al.: Novel mutations target distinct subgroups of medulloblastoma. Nature 2012, 488(7409):43-48. 10.1038/nature11213
27. Kool M, Korshunov A, Remke M, Jones DT, Schlanstein M, Northcott PA, Cho YJ, Koster J, Schouten-van Meeteren A, van Vuurden D, Clifford SC, Pietsch T, von Bueren AO, Rutkowski S, McCabe M, Collins VP, Backlund ML, Haberler C, Bourdeaut F, Delattre O, Doz F, Ellison DW, Gilbertson RJ, Pomeroy SL, Taylor MD, Lichter P, Pfister SM: Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol 2012, 123(4):473-484. 10.1007/s00401-012-0958-8
28. Roth RB, Hevezi P, Lee J, Willhite D, Lechner SM, Foster AC, Zlotnik A: Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics 2006, 7(2):67-80. 10.1007/s10048-006-0032-6
29. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA: miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nature cell biology 2010, 12(3):247-256.
30. Snuderl M, Batista A, Kirkpatrick ND, Ruiz de Almodovar C, Riedemann L, Walsh EC, Anolik R, Huang Y, Martin JD, Kamoun W, Knevels E, Schmidt T, Farrar CT, Vakoc BJ, Mohan N, Chung E, Roberge S, Peterson T, Bais C, Zhelyazkova BH, Yip S, Hasselblatt M, Rossig C, Niemeyer E, Ferrara N, Klagsbrun M, Duda DG, Fukumura D, Xu L, Carmeliet P, et al.: Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell 2013, 152(5):1065-1076. 10.1016/j.cell.2013.01.036
31. Cho YJ, Tsherniak A, Tamayo P, Santagata S, Ligon A, Greulich H, Berhoukim R, Amani V, Goumnerova L, Eberhart CG, Lau CC, Olson JM, Gilbertson RJ, Gajjar A, Delattre O, Kool M, Ligon K, Meyerson M, Mesirov JP, Pomeroy SL: Integrative genomic analysis of medulloblastoma identifies a molecular subgroup that drives poor clinical outcome. J Clin Oncol 2011, 29(11):1424-1430. 10.1200/JCO.2010.28.5148
32. Lin CY, Loven J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA: Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012, 151(1):56-67. 10.1016/j.cell.2012.08.026
33. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, Eberhart CG: Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006, 66(15):7445-7452. 10.1158/0008-5472.CAN-06-0858
34. Yustein JT, Liu YC, Gao P, Jie C, Le A, Vuica-Ross M, Chng WJ, Eberhart CG, Bergsagel PL, Dang CV: Induction of ectopic Myc target gene JAG2 augments hypoxic growth and tumorigenesis in a human B-cell model. Proc Natl Acad Sci U S A 2010, 107(8):3534-3539. 10.1073/pnas.0901230107
35. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J, Cocito A, Amati B: Genomic targets of the human c-Myc protein. Genes Dev 2003, 17(9):1115-1129. 10.1101/gad.1067003
36. Pei Y, Moore CE, Wang J, Tewari AK, Eroshkin A, Cho YJ, Witt H, Korshunov A, Read TA, Sun JL, Schmitt EM, Miller CR, Buckley AF, McLendon RE, Westbrook TF, Northcott PA, Taylor MD, Pfister SM, Febbo PG, Wechsler-Reya RJ: An animal model of MYC-driven medulloblastoma. Cancer cell 2012, 21(2):155-167. 10.1016/j.ccr.2011.12.021
37. Kawauchi D, Robinson G, Uziel T, Gibson P, Rehg J, Gao C, Finkelstein D, Qu C, Pounds S, Ellison DW, Gilbertson RJ, Roussel MF: A mouse model of the most aggressive subgroup of human medulloblastoma. Cancer cell 2012, 21(2):168-180. 10.1016/j.ccr.2011.12.023
38. Nam DH, Jeon HM, Kim S, Kim MH, Lee YJ, Lee MS, Kim H, Joo KM, Lee DS, Price JE, Bang SI, Park WY: Activation of notch signaling in a xenograft model of brain metastasis. Clin Cancer Res 2008, 14(13):4059-4066. 10.1158/1078-0432.CCR-07-4039
39. de Bont JM, Packer RJ, Michiels EM, den Boer ML, Pieters R: Biological background of pediatric medulloblastoma and ependymoma: a review from a translational research perspective. J Neurooncol 2008, 10(6):1040-1060.
40. Ingram WJ, McCue KI, Tran TH, Hallahan AR, Wainwright BJ: Sonic Hedgehog regulates Hes1 through a novel mechanism that is independent of canonical Notch pathway signalling. Oncogene 2008, 27(10):1489-1500. 10.1038/sj.onc.1210767
41. Dakubo GD, Mazerolle CJ, Wallace VA: Expression of Notch and Wnt pathway components and activation of Notch signaling in medulloblastomas from heterozygous patched mice. J Neurooncol 2006, 79(3):221-227. 10.1007/s11060-006-9132-2
42. Hallahan AR, Pritchard JI, Hansen S, Benson M, Stoeck J, Hatton BA, Russell TL, Ellenbogen RG, Bernstein ID, Beachy PA, Olson JM: The SmoA1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas. Cancer res 2004, 64(21):7794-7800. 10.1158/0008-5472.CAN-04-1813
43. Shih Ie M, Wang TL: Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer res 2007, 67(5):1879-1882. 10.1158/0008-5472.CAN-06-3958
44. Beel AJ, Sanders CR: Substrate specificity of gamma-secretase and other intramembrane proteases. Cell Mol Life Sci 2008, 65(9):1311-1334. 10.1007/s00018-008-7462-2
45. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H: Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005, 435(7044):959-963. 10.1038/nature03659