Genome sequencing of SHH medulloblastoma predicts genotype-related response to smoothened inhibition

Cancer Cell

Volumn 25, Issue 3, 2014, Pages 393-405

  Kool, Marcel ^a   Jones, David T W ^a   Jäger, Natalie ^a   Northcott, Paul A ^a   Pugh, Trevor J ^b   Hovestadt, Volker ^a   Piro, Rosario M ^a   Esparza, L Adriana ^a   Markant, Shirley L ^c   Remke, Marc ^d   Milde, Till ^e   Bourdeaut, Franck ^f   Ryzhova, Marina ^g   Sturm, Dominik ^a   Pfaff, Elke ^a   Stark, Sebastian ^a   Hutter, Sonja ^a   Sxeker Cin, Huriye ^a   Johann, Pascal ^a   Bender, Sebastian ^a   Schmidt, Christin ^a   Rausch, Tobias ^h   Shih, David ^d   Reimand, Jüri ⁱ   Sieber, Laura ^a   Wittmann, Andrea ^a   Linke, Linda ^a   Witt, Hendrik ^a,e   Weber, Ursula D ^a   Zapatka, Marc ^a   Konig Rainer ^a,j,k   Beroukhim, Rameen ^b,l,m   Bergthold, Guillaume ^b,l,n   Van Sluis, Peter ^o   Volckmann, Richard ^o   Koster, Jan ^o   Versteeg, Rogier ^o   Schmidt, Sabine ^a   Wolf, Stephan ^a   Lawerenz, Chris ^a   Bartholomae, Cynthia C ^a   Von Kalle, Christof ^a   Unterberg, Andreas ^a   Herold Mende, Christel ^a   Hofer, Silvia ^p   Kulozik, Andreas E ^e   Von Deimling, Andreas ^a,q   Scheurlen, Wolfram ^r   Felsberg, Jörg ^s   Reifenberger, Guido ^s   Hasselblatt, Martin ^t   Crawford, John R ^u,v   Grant, Gerald A ^w   Jabado, Nada ^x   Perry, Arie ^y   Cowdrey, Cynthia ^y   Croul, Sydney ^z   Zadeh, Gelareh ^z   Korbel, Jan O ^h   Doz, Francois ^f,aa   Delattre, Olivier ^f   Bader, Gary D ⁱ   McCabe, Martin G ^ab   Collins, V Peter ^ac   Kieran, Mark W ^l   Cho, Yoon Jae ^ad   Pomeroy, Scott L ^ae   Witt, Olaf ^a   Brors, Benedikt ^a   Taylor, Michael D ^d   Schüller, Ulrich ^af   Korshunov, Andrey ^a,q   Eils, Roland ^a   Wechsler Reya, Robert J ^c   Lichter, Peter ^a   Pfister, Stefan M ^a,e   more..

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c BURNHAM INSTITUTE   (United States)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^f INSTITUT CURIE   (France)

^g BURDENKO NEUROSURGICAL INSTITUTE   (Russian Federation)

^h EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

ⁱ UNIVERSITY OF TORONTO   (Canada)

^j JENA UNIVERSITY HOSPITAL   (Germany)

^k HANS KNÖLL INSTITUTE   (Germany)

^l DANA FARBER CANCER INSTITUTE   (United States)

^m BRIGHAM AND WOMEN S HOSPITAL   (United States)

ⁿ INSTITUT GUSTAVE ROUSSY   (France)

^o ACADEMIC MEDICAL CENTER   (Netherlands)

^p UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^q UNIVERSITY OF HEIDELBERG   (Germany)

^r Cnopf'Sche Kinderklinik Nü Rnberg Children's Hospital   (Germany)

^s HEINRICH HEINE UNIVERSITY   (Germany)

^t UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^u UNIVERSITY OF CALIFORNIA   (United States)

^v RADY CHILDREN'S HOSPITAL   (United States)

^w DUKE UNIVERSITY MEDICAL CENTER   (United States)

^x RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^y UNIVERSITY OF CALIFORNIA   (United States)

^z Arthur and Sonia Labatt Brain Tumour Research Centre   (Canada)

^aa UNIVERSITÉ PARIS DESCARTES   (France)

^ab UNIVERSITY OF MANCHESTER   (United Kingdom)

^ac UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^ad STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^ae BOSTON CHILDREN S HOSPITAL   (United States)

^af UNIVERSITY OF MUNICH   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN PATCHED 1; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; SONIDEGIB; TRANSCRIPTION FACTOR GLI2;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CHILD; CHROMOSOME 17P; CHROMOSOME LOSS; CONTROLLED STUDY; DNA HISTONE INTERACTION; DRUG RESPONSE; ENZYME INHIBITION; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENOMIC INSTABILITY; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INFANT; MAJOR CLINICAL STUDY; MALE; MEDULLOBLASTOMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRESCHOOL CHILD; PRIORITY JOURNAL; PROMOTER REGION; SCHOOL CHILD; SEQUENCE ANALYSIS; TUMOR XENOGRAFT; CHROMOSOME 10Q; CHROMOSOME 9Q; COHORT ANALYSIS; DNA METHYLATION; EPIGENETICS; GENE; GENE EXPRESSION; GERMLINE MUTATION; GLI2 GENE; GROUPS BY AGE; HUMAN TISSUE; MYCN GENE; PREDICTION; PTCH1 GENE; SIGNAL TRANSDUCTION; SMO GENE; SOMATIC MUTATION; SUFU GENE; TP53 GENE; TREATMENT OUTCOME;

ADOLESCENT; ADULT; ANIMALS; BASE SEQUENCE; BIPHENYL COMPOUNDS; CEREBELLAR NEOPLASMS; CHILD; CHILD, PRESCHOOL; DEAD-BOX RNA HELICASES; DNA COPY NUMBER VARIATIONS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION PROFILING; HEDGEHOG PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MEDULLOBLASTOMA; MICE; MICE, INBRED NOD; MICE, SCID; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TELOMERASE; TUMOR SUPPRESSOR PROTEIN P53; YOUNG ADULT;

ERINACEIDAE;

EID: 84896096387     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.02.004     Document Type: Article

References (45)

1. Amakye D.D., Robinson D., Rose K., Cho Y., Ligon K., Sharp T., Haider A., Bandaru R., Ando Y., Geoerger B., et al. Abstract 4818: The predictive value of a 5-gene signature as a patient pre-selection tool in medulloblastoma for Hedgehog pathway inhibitor therapy. Cancer Res. 2012, 72. 10.1158/1538-7445.AM2012-4818.
2. Beauchamp E.M., Ringer L., Bulut G., Sajwan K.P., Hall M.D., Lee Y.C., Peaceman D., Ozdemirli M., Rodriguez O., Macdonald T.J., et al. Arsenic trioxide inhibits human cancer cell growth and tumor development in mice by blocking Hedgehog/GLI pathway. J.Clin. Invest. 2011, 121:148-160.
3. Brandes A.A., Franceschi E., Tosoni A., Reni M., Gatta G., Vecht C., Kortmann R.D. Adult neuroectodermal tumors of posterior fossa (medulloblastoma) and of supratentorial sites (stPNET). Crit. Rev. Oncol. Hematol. 2009, 71:165-179.
4. Brugières L., Remenieras A., Pierron G., Varlet P., Forget S., Byrde V., Bombled J., Puget S., Caron O., Dufour C., et al. High frequency of germline SUFU mutations in children with desmoplastic/nodular medulloblastoma younger than 3 years of age. J.Clin. Oncol. 2012, 30:2087-2093.
5. Buonamici S., Williams J., Morrissey M., Wang A., Guo R., Vattay A., Hsiao K., Yuan J., Green J., Ospina B., et al. Interfering with resistance to smoothened antagonists by inhibition of the PI3K pathway in medulloblastoma. Sci. Transl. Med. 2010, 2:51ra70.
6. Dijkgraaf G.J., Alicke B., Weinmann L., Januario T., West K., Modrusan Z., Burdick D., Goldsmith R., Robarge K., Sutherlin D., et al. Small molecule inhibition of GDC-0449 refractory smoothened mutants and downstream mechanisms of drug resistance. Cancer Res. 2011, 71:435-444.
7. Ellison D.W., Dalton J., Kocak M., Nicholson S.L., Fraga C., Neale G., Kenney A.M., Brat D.J., Perry A., Yong W.H., et al. Medulloblastoma: clinicopathological correlates of SHH, WNT, and non-SHH/WNT molecular subgroups. Acta Neuropathol. 2011, 121:381-396.
8. Geoerger B., Aerts I., Casanova M., Chisholm J.C., Hargrave D., Leary S., Ashley D.M., Bouffet E., MacDonald T.J., Hurh E., et al. A phase I/II study of LDE225, a smoothened (Smo) antagonist, in pediatric patients with recurrent medulloblastoma (MB) or other solid tumors. J.Clin. Oncol. 2012, 30:9519.
9. Grammel D., Warmuth-Metz M., von Bueren A.O., Kool M., Pietsch T., Kretzschmar H.A., Rowitch D.H., Rutkowski S., Pfister S.M., Schüller U. Sonic hedgehog-associated medulloblastoma arising from the cochlear nuclei of the brainstem. Acta Neuropathol. 2012, 123:601-614.
10. Jones D.T., Jäger N., Kool M., Zichner T., Hutter B., Sultan M., Cho Y.J., Pugh T.J., Hovestadt V., Stütz A.M., et al. Dissecting the genomic complexity underlying medulloblastoma. Nature 2012, 488:100-105.
11. Killela P.J., Reitman Z.J., Jiao Y., Bettegowda C., Agrawal N., Diaz L.A., Friedman A.H., Friedman H., Gallia G.L., Giovanella B.C., et al. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc. Natl. Acad. Sci. USA 2013, 110:6021-6026.
12. Kim J., Tang J.Y., Gong R., Kim J., Lee J.J., Clemons K.V., Chong C.R., Chang K.S., Fereshteh M., Gardner D., et al. Itraconazole, a commonly used antifungal that inhibits Hedgehog pathway activity and cancer growth. Cancer Cell 2010, 17:388-399.
13. Kim J., Aftab B.T., Tang J.Y., Kim D., Lee A.H., Rezaee M., Kim J., Chen B., King E.M., Borodovsky A., et al. Itraconazole and arsenic trioxide inhibit Hedgehog pathway activation and tumor growth associated with acquired resistance to smoothened antagonists. Cancer Cell 2013, 23:23-34.
14. Kimura H., Ng J.M., Curran T. Transient inhibition of the Hedgehog pathway in young mice causes permanent defects in bone structure. Cancer Cell 2008, 13:249-260.
15. Koelsche C., Sahm F., Capper D., Reuss D., Sturm D., Jones D.T., Kool M., Northcott P.A., Wiestler B., Böhmer K., et al. Distribution of TERT promoter mutations in pediatric and adult tumors of the nervous system. Acta Neuropathol. 2013, 126:907-915.
16. Kool M., Korshunov A., Remke M., Jones D.T., Schlanstein M., Northcott P.A., Cho Y.J., Koster J., Schouten-van Meeteren A., van Vuurden D., et al. 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, 123:473-484.
17. Korshunov A., Remke M., Kool M., Hielscher T., Northcott P.A., Williamson D., Pfaff E., Witt H., Jones D.T., Ryzhova M., et al. Biological and clinical heterogeneity of MYCN-amplified medulloblastoma. Acta Neuropathol. 2012, 123:515-527.
18. Lee Y., Kawagoe R., Sasai K., Li Y., Russell H.R., Curran T., McKinnon P.J. Loss of suppressor-of-fused function promotes tumorigenesis. Oncogene 2007, 26:6442-6447.
19. Lin T.L., Matsui W. Hedgehog pathway as a drug target: Smoothened inhibitors in development. OncoTargets and therapy 2012, 5:47-58.
20. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109.
21. Low J.A., de Sauvage F.J. Clinical experience with Hedgehog pathway inhibitors. J.Clin. Oncol. 2010, 28:5321-5326.
22. Metcalfe C., Alicke B., Crow A., Lamoureux M., Dijkgraaf G.J., Peale F., Gould S.E., de Sauvage F.J. PTEN loss mitigates the response of medulloblastoma to Hedgehog pathway inhibition. Cancer Res. 2013, 73:7034-7042.
23. Milenkovic L., Scott M.P. Not lost in space: trafficking in the hedgehog signaling pathway. Sci. Signal. 2010, 3:pe14.
24. Ng J.M., Curran T. The Hedgehog's tale: developing strategies for targeting cancer. Nat. Rev. Cancer 2011, 11:493-501.
25. Northcott P.A., Hielscher T., Dubuc A., Mack S., Shih D., Remke M., Al-Halabi H., Albrecht S., Jabado N., Eberhart C.G., et al. Pediatric and adult sonic hedgehog medulloblastomas are clinically and molecularly distinct. Acta Neuropathol. 2011, 122:231-240.
26. Northcott P.A., Korshunov A., Witt H., Hielscher T., Eberhart C.G., Mack S., Bouffet E., Clifford S.C., Hawkins C.E., French P., et al. Medulloblastoma comprises four distinct molecular variants. J.Clin. Oncol. 2011, 29:1408-1414.
27. Northcott P.A., Jones D.T., Kool M., Robinson G.W., Gilbertson R.J., Cho Y.J., Pomeroy S.L., Korshunov A., Lichter P., Taylor M.D., Pfister S.M. Medulloblastomics: the end of the beginning. Nat. Rev. Cancer 2012, 12:818-834.
28. Northcott P.A., Shih D.J., Peacock J., Garzia L., Morrissy A.S., Zichner T., Stütz A.M., Korshunov A., Reimand J., Schumacher S.E., et al. Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature 2012, 488:49-56.
29. Padovani L., Sunyach M.P., Perol D., Mercier C., Alapetite C., Haie-Meder C., Hoffstetter S., Muracciole X., Kerr C., Wagner J.P., et al. Common strategy for adult and pediatric medulloblastoma: a multicenter series of 253 adults. Int. J. Radiat. Oncol. Biol. Phys. 2007, 68:433-440.
30. Parsons D.W., Li M., Zhang X., Jones S., Leary R.J., Lin J.C., Boca S.M., Carter H., Samayoa J., Bettegowda C., et al. The genetic landscape of the childhood cancer medulloblastoma. Science 2011, 331:435-439.
31. Pugh T.J., Weeraratne S.D., Archer T.C., Pomeranz Krummel D.A., Auclair D., Bochicchio J., Carneiro M.O., Carter S.L., Cibulskis K., Erlich R.L., et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012, 488:106-110.
32. Rausch T., Jones D.T.W., Zapatka M., Stütz A.M., Zichner T., Weischenfeldt J., Jäger N., Remke M., Shih D., Northcott P.A., et al. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations. Cell 2012, 148:59-71.
33. Remke M., Ramaswamy V., Peacock J., Shih D.J., Koelsche C., Northcott P.A., Hill N., Cavalli F.M., Kool M., Wang X., et al. TERT promoter mutations are highly recurrent in SHH subgroup medulloblastoma. Acta Neuropathol. 2013, 126:917-929.
34. Robinson G., Parker M., Kranenburg T.A., Lu C., Chen X., Ding L., Phoenix T.N., Hedlund E., Wei L., Zhu X., et al. Novel mutations target distinct subgroups of medulloblastoma. Nature 2012, 488:43-48.
35. Rudin C.M., Hann C.L., Laterra J., Yauch R.L., Callahan C.A., Fu L., Holcomb T., Stinson J., Gould S.E., Coleman B., et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N.Engl. J. Med. 2009, 361:1173-1178.
36. Ryan S.L., Schwalbe E.C., Cole M., Lu Y., Lusher M.E., Megahed H., O'Toole K., Nicholson S.L., Bognar L., Garami M., et al. MYC family amplification and clinical risk-factors interact to predict an extremely poor prognosis in childhood medulloblastoma. Acta Neuropathol. 2012, 123:501-513.
37. Shu Q., Wong K.K., Su J.M., Adesina A.M., Yu L.T., Tsang Y.T., Antalffy B.C., Baxter P., Perlaky L., Yang J., et al. Direct orthotopic transplantation of fresh surgical specimen preserves CD133+ tumor cells in clinically relevant mouse models of medulloblastoma and glioma. Stem Cells 2008, 26:1414-1424.
38. Spreafico F., Massimino M., Gandola L., Cefalo G., Mazza E., Landonio G., Pignoli E., Poggi G., Terenziani M., Pedrazzoli P., et al. Survival of adults treated for medulloblastoma using paediatric protocols. Eur. J. Cancer 2005, 41:1304-1310.
39. Taylor M.D., Northcott P.A., Korshunov A., Remke M., Cho Y.J., Clifford S.C., Eberhart C.G., Parsons D.W., Rutkowski S., Gajjar A., et al. Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 2012, 123:465-472.
40. Wang Y., Ding Q., Yen C.J., Xia W., Izzo J.G., Lang J.Y., Li C.W., Hsu J.L., Miller S.A., Wang X., et al. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 2012, 21:374-387.
41. Welch J.S., Ley T.J., Link D.C., Miller C.A., Larson D.E., Koboldt D.C., Wartman L.D., Lamprecht T.L., Liu F., Xia J., et al. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012, 150:264-278.
42. Yauch R.L., Dijkgraaf G.J., Alicke B., Januario T., Ahn C.P., Holcomb T., Pujara K., Stinson J., Callahan C.A., Tang T., et al. Smoothened mutation confers resistance to a Hedgehog pathway inhibitor in medulloblastoma. Science 2009, 326:572-574.
43. Yeh-Nayre L.A., Malicki D.M., Vinocur D.N., Crawford J.R. Medulloblastoma with excessive nodularity: radiographic features and pathologic correlate. Case reports in radiology 2012, 2012:310359.
44. Zhao X., Liu Z., Yu L., Zhang Y., Baxter P., Voicu H., Gurusiddappa S., Luan J., Su J.M., Leung H.C., Li X.N. Global gene expression profiling confirms the molecular fidelity of primary tumor-based orthotopic xenograft mouse models of medulloblastoma. Neuro-oncol. 2012, 14:574-583.
45. Zhukova N., Ramaswamy V., Remke M., Pfaff E., Shih D.J., Martin D.C., Castelo-Branco P., Baskin B., Ray P.N., Bouffet E., et al. Subgroup-specific prognostic implications of TP53 mutation in medulloblastoma. J.Clin. Oncol. 2013, 31:2927-2935.