Oncogenic YAP promotes radioresistance and genomic instability in medulloblastoma through IGF2-mediated Akt activation

Oncogene

Volumn 31, Issue 15, 2012, Pages 1923-1937

  Fernandez L, A ^a   Squatrito, M ^a   Northcott, P ^b   Awan, A ^c   Holland, E C ^a   Taylor, M D ^b   Nahle Z ^c   Kenney, A M ^c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

cerebellum; DNA damage; IGF; medulloblastoma; sonic hedgehog; YAP

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; PROTEIN KINASE B; SOMATOMEDIN B; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME INACTIVATION; GENOMIC INSTABILITY; HUMAN; HUMAN TISSUE; MEDULLOBLASTOMA; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY; TUMOR GROWTH; TUMOR RECURRENCE;

ANIMALS; CELL CYCLE CHECKPOINTS; CEREBELLAR NEOPLASMS; DNA DAMAGE; GENOMIC INSTABILITY; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MEDULLOBLASTOMA; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RADIATION TOLERANCE; TRANSCRIPTION FACTORS;

ERINACEIDAE;

EID: 84859777450     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.379     Document Type: Article

References (52)

1. Berman DM, Karhadkar SS, Hallahan AR, Pritchard JI, EberhartCG, Watkins DN et al. (2002). Medulloblastoma growth inhibitionby hedgehog pathway blockade. Science 297: 1559-1561. (Pubitemid 34971004)
2. Bertini E, Oka T, Sudol M, Strano S, Blandino G. (2009). YAP: at thecrossroad between transformation and tumor suppression. CellCycle 8: 49-57.
3. Bhatia B, Hsieh M, Kenney AM, Nahle Z. (2011). Mitogenic Sonichedgehog signaling drives E2F1-dependent lipogenesis in progenitorcells and medulloblastoma. Oncogene 30: 410-422.
4. Brunet A, Datta SR, Greenberg ME. (2001). Transcription-dependentand- independent control of neuronal survival by the PI3K-Aktsignaling pathway. Curr Opin Neurobiol 11: 297-305. (Pubitemid 32524094)
5. Burgering BM, Kops GJ. (2002). Cell cycle and death control: long liveForkheads. Trends Biochem Sci 27: 352-360. (Pubitemid 34756518)
6. Castedo M, Roumier T, Blanco J, Ferri KF, Barretina J, Tintignac LAet al. (2002). Sequential involvement of Cdk1, mTOR andp53 in apoptosis induced by the HIV-1 envelope. EMBO J 21:4070-4080. (Pubitemid 34857439)
7. Chrysis DC, Alexandrides TK, Koromantzou E, Georgopoulos N, Vassilakos P, Kiess W et al. (2001). Novel application of IGF-I andIGFBP-3 generation tests in the diagnosis of growth hormone axisdisturbances in children with beta-thalassaemia. Clin Endocrinol(Oxf) 54: 253-259. (Pubitemid 32193528)
8. Corcoran RB, Bachar Raveh T, Barakat MT, Lee EY, Scott MP.(2008). Insulin-like growth factor 2 is required for progression toadvanced medulloblastoma in patched1 heterozygous mice. CancerRes 68: 8788-8795.
9. Dahmane N, Ruiz i Altaba A. (1999). Sonic hedgehog regulatesthe growth and patterning of the cerebellum. Development 126:3089-3100. (Pubitemid 29378174)
10. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GMet al. (1997). Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661-665. (Pubitemid 27061332)
11. Duronio V. (2008). The life of a cell: apoptosis regulation by thePI3K/PKB pathway. Biochem J 415: 333-344.
12. Eberhart CG. (2008). Even cancers want commitment: lineage identityand medulloblastoma formation. Cancer Cell 14: 105-107.
13. Fernandez-L A, Kenney AM. (2010). The Hippo in the room: a newlook at a key pathway in cell growth and transformation. Cell Cycle9: 2292-2299.
14. Fernandez-L A, Northcott PA, Dalton J, Fraga C, Ellison D, Angers Set al. (2009). YAP1 is amplified and up-regulated in hedgehogassociatedmedulloblastomas and mediates Sonic hedgehog-drivenneural precursor proliferation. Genes Dev 23: 2729-2741.
15. Frappart PO, Lee Y, Russell HR, Chalhoub N, Wang YD, Orii KEet al. (2009). Recurrent genomic alterations characterize medulloblastomaarising from DNA double-strand break repair deficiency.Proc Natl Acad Sci USA 106: 1880-1885.
16. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. (1997). Alteredneural cell fates and medulloblastoma in mouse patched mutants.Science 277: 1109-1113. (Pubitemid 27371635)
17. Hahn H, Wojnowski L, Specht K, Kappler R, Calzada-Wack J, Potter D et al. (2000). Patched target Igf2 is indispensable forthe formation of medulloblastoma and rhabdomyosarcoma. J BiolChem 275: 28341-28344.
18. Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, Holland EC. (2008). PI3K pathway regulatessurvival of cancer stem cells residing in the perivascular nichefollowing radiation in medulloblastoma in vivo. Genes Dev 22:436-448. (Pubitemid 351272752)
19. Hartmann W, Koch A, Brune H, Waha A, Schuller U, Dani I et al.(2005). Insulin-like growth factor II is involved in the proliferationcontrol of medulloblastoma and its cerebellar precursor cells. Am JPathol 166: 1153-1162. (Pubitemid 40524439)
20. Hatton BA, Villavicencio EH, Tsuchiya KD, Pritchard JI, Ditzler S, Pullar B et al. (2008). The Smo/Smo model: hedgehog-inducedmedulloblastoma with 90% incidence and leptomeningeal spread.Cancer Res 68: 1768-1776. (Pubitemid 351416562)
21. Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M et al. (2004). Rb inactivation promotes genomicinstability by uncoupling cell cycle progression from mitotic control.Nature 430: 797-802. (Pubitemid 39071352)
22. Hirose Y, Katayama M, Mirzoeva OK, Berger MS, Pieper RO. (2005).Akt activation suppresses Chk2-mediated, methylating agentinducedG2 arrest and protects from temozolomide-induced mitoticcatastrophe and cellular senescence. Cancer Res 65: 4861-4869. (Pubitemid 40740825)
23. Kandel ES, Skeen J, Majewski N, Di Cristofano A, Pandolfi PP, Feliciano CS et al. (2002). Activation of Akt/protein kinase Bovercomes a G(2)/m cell cycle checkpoint induced by DNA damage.Mol Cell Biol 22: 7831-7841. (Pubitemid 35217294)
24. Kenney AM, Rowitch DH. (2000). Sonic hedgehog promotes G(1)cyclin expression and sustained cell cycle progression in mammalianneuronal precursors. Mol Cell Biol 20: 9055-9067. (Pubitemid 32245934)
25. Kenney AM, Widlund HR, Rowitch DH. (2004). Hedgehog and PI-3kinase signaling converge on Nmyc1 to promote cell cycleprogression in cerebellar neuronal precursors. Development 131:217-228. (Pubitemid 38111428)
26. Kool M, Koster J, Bunt J, Hasselt NE, Lakeman A, van Sluis P et al.(2008). Integrated genomics identifies five medulloblastoma subtypeswith distinct genetic profiles, pathway signatures andclinicopathological features. PLoS One 3: e3088.
27. Leonard JM, Ye H, Wetmore C, Karnitz LM. (2008). Sonic Hedgehogsignaling impairs ionizing radiation-induced checkpoint activationand induces genomic instability. J Cell Biol 183: 385-391.
28. Mueller S, Chang S. (2009). Pediatric brain tumors: current treatmentstrategies and future therapeutic approaches. Neurotherapeutics 6:570-586.
29. Nahle Z, Hsieh M, Pietka T, Coburn CT, Grimaldi PA, Zhang MQet al. (2008). CD36-dependent regulation of muscle FoxO1 andPDK4 in the PPAR delta/beta-mediated adaptation to metabolicstress. J Biol Chem 283: 14317-14326.
30. Negrini S, Gorgoulis VG, Halazonetis TD. (2010). Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11:220-228.
31. Northcott PA, Fernandez LA, Hagan JP, Ellison DW, GrajkowskaW, Gillespie Y et al. (2009a). The miR-17/92 polycistron is up-regulatedin sonic hedgehog-driven medulloblastomas and induced by N-mycin sonic hedgehog-treated cerebellar neural precursors. Cancer Res69: 3249-3255.
32. Northcott PA, Nakahara Y, Wu X, Feuk L, Ellison DW, Croul S et al.(2009b). Multiple recurrent genetic events converge on controlof histone lysine methylation in medulloblastoma. Nat Genet 41:465-472.
33. Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, Mack S et al. (2011). Medulloblastoma comprises four distinctmolecular variants. J Clin Oncol 29: 1408-1414.
34. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, LinSM et al. (2003). Transcriptional profiling of the Sonic hedgehogresponse: a critical role for N-myc in proliferation of neuronalprecursors. Proc Natl Acad Sci USA 100: 7331-7336. (Pubitemid 36706438)
35. Overholtzer M, Zhang J, Smolen GA, Muir B, Li W, Sgroi DC et al.(2006). Transforming properties of YAP, a candidate oncogene onthe chromosome 11q22 amplicon. Proc Natl Acad Sci USA 103:12405-12410. (Pubitemid 44267272)
36. Parathath SR, Mainwaring LA, Fernandez LA, Campbell DO, Kenney AM. (2008). Insulin receptor substrate 1 is an effector ofsonic hedgehog mitogenic signaling in cerebellar neural precursors.Development 135: 3291-3300.
37. Pazzaglia S, Tanori M, Mancuso M, Rebessi S, Leonardi S, Di Majo Vet al. (2006). Linking DNA damage to medulloblastoma tumorigenesisin patched heterozygous knockout mice. Oncogene 25:1165-1173.
38. Plo I, Laulier C, Gauthier L, Lebrun F, Calvo F, Lopez BS. (2008).AKT1 inhibits homologous recombination by inducing cytoplasmicretention of BRCA1 and RAD51. Cancer Res 68: 9404-9412.
39. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME et al. (2002). Prediction of central nervous systemembryonal tumour outcome based on gene expression. Nature 415:436-442. (Pubitemid 34100955)
40. Rao G, Pedone CA, Del Valle L, Reiss K, Holland EC, Fults DW.(2004). Sonic hedgehog and insulin-like growth factor signalingsynergize to induce medulloblastoma formation from nestinexpressingneural progenitors in mice. Oncogene 23: 6156-6162. (Pubitemid 39178868)
41. Reinhardt HC, Yaffe MB. (2009). Kinases that control the cell cycle inresponse to DNA damage: Chk1, Chk2, and MK2. Curr Opin CellBiol 21: 245-255.
42. Ruiz i Altaba A. (1999). Gli proteins encode context-dependentpositive and negative functions: implications for development anddisease. Development 126: 3205-3216. (Pubitemid 29378183)
43. Shtivelman E, Sussman J, Stokoe D. (2002). A role for PI 3-kinaseand PKB activity in the G2/M phase of the cell cycle. Curr Biol 12:919-924. (Pubitemid 34689227)
44. Sieber OM, Heinimann K, Tomlinson IP. (2003). Genomic instability-the engine of tumorigenesis? Nat Rev Cancer 3: 701-708.
45. Tanori M, Mancuso M, Pasquali E, Leonardi S, Rebessi S, Di Majo V et al. (2008). PARP-1 cooperates with Ptc1 to suppressmedulloblastoma and basal cell carcinoma. Carcinogenesis 29:1911-1919.
46. Tanori M, Santone M, Mancuso M, Pasquali E, Leonardi S, Di Majo V et al. (2010). Developmental and oncogenic effects ofinsulin-like growth factor-I in Ptc1 +mouse cerebellum. MolCancer 9: 53.
47. Wallace VA. (1999). Purkinje-cell-derived Sonic hedgehog regulatesgranule neuron precursor cell proliferation in the developing mousecerebellum. Curr Biol 9: 445-448. (Pubitemid 29205791)
48. Wechsler-Reya RJ, Scott MP. (1999). Control of neuronal precursorproliferation in the cerebellum by Sonic Hedgehog. Neuron 22:103-114. (Pubitemid 29070097)
49. Xu N, Hegarat N, Black EJ, Scott MT, Hochegger H, Gillespie DA.(2010). Akt/PKB suppresses DNA damage processing and checkpointactivation in late G2. J Cell Biol 190: 297-305.
50. Yuan M, Tomlinson V, Lara R, Holliday D, Chelala C, Harada Tet al. (2008). Yes-associated protein (YAP) functions as a tumorsuppressor in breast. Cell Death Differ 15: 1752-1759.
51. Zeng Q, Hong W. (2008). The emerging role of the hippo pathway incell contact inhibition, organ size control, and cancer developmentin mammals. Cancer Cell 13: 188-192. (Pubitemid 351318373)
52. Zhao B, Ye X, Yu J, Li L, Li W, Li S et al. (2008). TEAD mediatesYAP-dependent gene induction and growth control. Genes Dev 22:1962-1971. (Pubitemid 352008643)