Mutations in the SIX1/2 Pathway and the DROSHA/DGCR8 miRNA Microprocessor Complex Underlie High-Risk Blastemal Type Wilms Tumors

Cancer Cell

Volumn 27, Issue 2, 2015, Pages 298-311

  Wegert, Jenny ^a   Ishaque, Naveed ^b   Vardapour, Romina ^a   Geörg, Christina ^b   Gu, Zuguang ^b   Bieg, Matthias ^b   Ziegler, Barbara ^a   Bausenwein, Sabrina ^a   Nourkami, Nasenien ^c   Ludwig, Nicole ^c   Keller, Andreas ^c   Grimm, Clemens ^a   Kneitz, Susanne ^a   Williams, Richard D ^d   Chagtai, Tas ^d   Pritchard Jones, Kathy ^d   vanSluis, Peter ^e   Volckmann, Richard ^e   Koster, Jan ^e   Versteeg, Rogier ^e   Acha, Tomas ^f   O'Sullivan, Maureen J ^g   Bode, PeterK ^h   Niggli, Felix ^h   Tytgat, Godelieve A ^e   vanTinteren, Harm ^e   vandenHeuvel Eibrink, Marry M ⁱ   Meese, Eckart ^c   Vokuhl, Christian ^j   Leuschner, Ivo ^j   Graf, Norbert ^c   Eils, Roland ^b,k   Pfister, Stefan M ^b   Kool, Marcel ^b   Gessler, Manfred ^a   more..

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f HOSPITAL MATERNO INFANTIL   (Spain)

^g OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^h UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

ⁱ ERASMUS MEDICAL CENTER   (Netherlands)

^j UNIVERSITY OF KIEL   (Germany)

^k UNIVERSITY OF HEIDELBERG   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; PROTEIN P53; SOMATOMEDIN B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SIX1; TRANSCRIPTION FACTOR SIX2; TRANSCRIPTOME; UNCLASSIFIED DRUG; DGCR8 PROTEIN, HUMAN; DROSHA PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; NERVE PROTEIN; RIBONUCLEASE III; RNA BINDING PROTEIN; SIX1 PROTEIN, HUMAN; SIX2 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; BLASTEMA; CANCER RISK; CONTROLLED STUDY; DGCR8 GENE; DICER1 GENE; DIS3L2 GENE; DROSHA GENE; EMBRYO; EXOME; GENE MUTATION; GENE REPLICATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC RISK; HIGH RISK PATIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; NEPHROBLASTOMA; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; RNA PROCESSING; TUMOR GENE; TUMOR GROWTH; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; MUTATION; PATHOLOGY;

GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICRORNAS; MUTATION; NEOPLASM PROTEINS; NERVE TISSUE PROTEINS; RIBONUCLEASE III; RNA-BINDING PROTEINS; TRANSCRIPTOME; WILMS TUMOR;

EID: 84922769850     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.01.002     Document Type: Article

References (51)

1. Anglesio M.S., Wang Y., Yang W., Senz J., Wan A., Heravi-Moussavi A., Salamanca C., Maines-Bandiera S., Huntsman D.G., Morin G.B. Cancer-associated somatic DICER1 hotspot mutations cause defective miRNA processing and reverse-strand expression bias to predominantly mature 3p strands through loss of 5p strand cleavage. J.Pathol. 2013, 229:400-409.
2. Astuti D., Morris M.R., Cooper W.N., Staals R.H., Wake N.C., Fews G.A., Gill H., Gentle D., Shuib S., Ricketts C.J., et al. Germline mutations in DIS3L2 cause the Perlman syndrome of overgrowth and Wilms tumor susceptibility. Nat. Genet. 2012, 44:277-284.
3. Bardeesy N., Falkoff D., Petruzzi M.J., Nowak N., Zabel B., Adam M., Aguiar M.C., Grundy P., Shows T., Pelletier J. Anaplastic Wilms' tumour, a subtype displaying poor prognosis, harbours p53 gene mutations. Nat. Genet. 1994, 7:91-97.
4. Bjornsson H.T., Brown L.J., Fallin M.D., Rongione M.A., Bibikova M., Wickham E., Fan J.B., Feinberg A.P. Epigenetic specificity of loss of imprinting of the IGF2 gene in Wilms tumors. J.Natl. Cancer Inst. 2007, 99:1270-1273.
5. Brodbeck S., Englert C. Genetic determination of nephrogenesis: the Pax/Eya/Six gene network. Pediatr. Nephrol. 2004, 19:249-255.
6. Call K.M., Glaser T., Ito C.Y., Buckler A.J., Pelletier J., Haber D.A., Rose E.A., Kral A., Yeger H., Lewis W.H., et al. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 1990, 60:509-520.
7. Dome J.S., Fernandez C.V., Mullen E.A., Kalapurakal J.A., Geller J.I., Huff V., Gratias E.J., Dix D.B., Ehrlich P.F., Khanna G., et al. Children's Oncology Group's 2013 blueprint for research: renal tumors. Pediatr. Blood Cancer 2013, 60:994-1000. COG Renal Tumors Committee.
8. Foulkes W.D., Priest J.R., Duchaine T.F. DICER1: mutations, microRNAs and mechanisms. Nat. Rev. Cancer 2014, 14:662-672.
9. Gan J., Tropea J.E., Austin B.P., Court D.L., Waugh D.S., Ji X. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 2006, 124:355-366.
10. Gan J., Shaw G., Tropea J.E., Waugh D.S., Court D.L., Ji X. A stepwise model for double-stranded RNA processing by ribonuclease III. Mol. Microbiol. 2008, 67:143-154.
11. Gessler M., Poustka A., Cavenee W., Neve R.L., Orkin S.H., Bruns G.A. Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 1990, 343:774-778.
12. Grundy P.E., Breslow N.E., Li S., Perlman E., Beckwith J.B., Ritchey M.L., Shamberger R.C., Haase G.M., D'Angio G.J., Donaldson M., et al. Loss of heterozygosity for chromosomes 1p and 16q is an adverse prognostic factor in favorable-histology Wilms tumor: a report from the National Wilms Tumor Study Group. J.Clin. Oncol. 2005, 23:7312-7321. National Wilms Tumor Study Group.
13. Hendry C.E., Vanslambrouck J.M., Ineson J., Suhaimi N., Takasato M., Rae F., Little M.H. Direct transcriptional reprogramming of adult cells to embryonic nephron progenitors. J.Am. Soc. Nephrol. 2013, 24:1424-1434.
14. Huff V. Wilms' tumours: about tumour suppressor genes, an oncogene and a chameleon gene. Nat. Rev. Cancer 2011, 11:111-121.
15. Klamt B., Schulze M., Thäte C., Mares J., Goetz P., Kodet R., Scheulen W., Weirich A., Graf N., Gessler M. Allele loss in Wilms tumors of chromosome arms 11q, 16q, and 22q correlate with clinicopathological parameters. Genes Chromosomes Cancer 1998, 22:287-294.
16. Kohlhase J., Wischermann A., Reichenbach H., Froster U., Engel W. Mutations in the SALL1 putative transcription factor gene cause Townes-Brocks syndrome. Nat. Genet. 1998, 18:81-83.
17. Kozomara A., Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014, 42:D68-D73.
18. Lahoti C., Thorner P., Malkin D., Yeger H. Immunohistochemical detection of p53 in Wilms' tumors correlates with unfavorable outcome. Am. J. Pathol. 1996, 148:1577-1589.
19. Lawrence M.S., Stojanov P., Polak P., Kryukov G.V., Cibulskis K., Sivachenko A., Carter S.L., Stewart C., Mermel C.H., Roberts S.A., et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013, 499:214-218.
20. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 1000 Genome Project Data Processing Subgroup.
21. Melton C., Judson R.L., Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 2010, 463:621-626.
22. Natrajan R., Williams R.D., Hing S.N., Mackay A., Reis-Filho J.S., Fenwick K., Iravani M., Valgeirsson H., Grigoriadis A., Langford C.F., et al. Array CGH profiling of favourable histology Wilms tumours reveals novel gains and losses associated with relapse. J.Pathol. 2006, 210:49-58.
23. Patrick A.N., Cabrera J.H., Smith A.L., Chen X.S., Ford H.L., Zhao R. Structure-function analyses of the human SIX1-EYA2 complex reveal insights into metastasis and BOR syndrome. Nat. Struct. Mol. Biol. 2013, 20:447-453.
24. Piper D.E., Batchelor A.H., Chang C.P., Cleary M.L., Wolberger C. Structure of a HoxB1-Pbx1 heterodimer bound to DNA: role of the hexapeptide and a fourth homeodomain helix in complex formation. Cell 1999, 96:587-597.
25. Pode-Shakked N., Shukrun R., Mark-Danieli M., Tsvetkov P., Bahar S., Pri-Chen S., Goldstein R.S., Rom-Gross E., Mor Y., Fridman E., et al. The isolation and characterization of renal cancer initiating cells from human Wilms' tumour xenografts unveils new therapeutic targets. EMBO Mol. Med. 2013, 5:18-37.
26. Pugh T.J., Morozova O., Attiyeh E.F., Asgharzadeh S., Wei J.S., Auclair D., Carter S.L., Cibulskis K., Hanna M., Kiezun A., et al. The genetic landscape of high-risk neuroblastoma. Nat. Genet. 2013, 45:279-284.
27. Rakheja D., Chen K.S., Liu Y., Shukla A.A., Schmid V., Chang T.C., Khokhar S., Wickiser J.E., Karandikar N.J., Malter J.S., et al. Somatic mutations in DROSHA and DICER1 impair microRNA biogenesis through distinct mechanisms in Wilms tumours. Nat. Commun. 2014, 2:4802.
28. Rausch T., Jones D.T., 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.
29. Rivera M.N., Kim W.J., Wells J., Driscoll D.R., Brannigan B.W., Han M., Kim J.C., Feinberg A.P., Gerald W.L., Vargas S.O., et al. An X chromosome gene, WTX, is commonly inactivated in Wilms tumor. Science 2007, 315:642-645.
30. Ruf R.G., Xu P.X., Silvius D., Otto E.A., Beekmann F., Muerb U.T., Kumar S., Neuhaus T.J., Kemper M.J., Raymond R.M., et al. SIX1 mutations cause branchio-oto-renal syndrome by disruption of EYA1-SIX1-DNA complexes. Proc. Natl. Acad. Sci. USA 2004, 101:8090-8095.
31. Ruteshouser E.C., Robinson S.M., Huff V. Wilms tumor genetics: mutations in WT1, WTX, and CTNNB1 account for only about one-third of tumors. Genes Chromosomes Cancer 2008, 47:461-470.
32. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
33. Scott R.H., Murray A., Baskcomb L., Turnbull C., Loveday C., Al-Saadi R., Williams R., Breatnach F., Gerrard M., Hale J., et al. Stratification of Wilms tumor by genetic and epigenetic analysis. Oncotarget 2012, 3:327-335.
34. Segers H., van den Heuvel-Eibrink M.M., Williams R.D., van Tinteren H., Vujanic G., Pieters R., Pritchard-Jones K., Bown N. Gain of 1q is a marker of poor prognosis in Wilms' tumors. Genes Chromosomes Cancer 2013, 52:1065-1074. Children's Cancer and Leukaemia Group and the UK Cancer Cytogenetics Group.
35. Sehic D., Karlsson J., Sandstedt B., Gisselsson D. SIX1 protein expression selectively identifies blastemal elements in Wilms tumor. Pediatr. Blood Cancer 2012, 59:62-68.
36. Senanayake U., Koller K., Pichler M., Leuschner I., Strohmaier H., Hadler U., Das S., Hoefler G., Guertl B. The pluripotent renal stem cell regulator SIX2 is activated in renal neoplasms and influences cellular proliferation and migration. Hum. Pathol. 2013, 44:336-345.
37. Slade I., Stephens P., Douglas J., Barker K., Stebbings L., Abbaszadeh F., Pritchard-Jones K., Cole R., Pizer B., Stiller C., et al. Constitutional translocation breakpoint mapping by genome-wide paired-end sequencing identifies HACE1 as a putative Wilms tumour susceptibility gene. J.Med. Genet. 2010, 47:342-347. FACT collaboration.
38. Smyth G.K. limma: Linear Models for Microarray Data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005, 397-420. Springer. R. Gentleman, V. Carey, W. Huber, R. Irizarry, S. Dudoit (Eds.).
39. Stefl R., Oberstrass F.C., Hood J.L., Jourdan M., Zimmermann M., Skrisovska L., Maris C., Peng L., Hofr C., Emeson R.B., Allain F.H. The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell 2010, 143:225-237.
40. Torrezan G.T., Ferreira E.N., Nakahata A.M., Barros B.D., Castro M.T., Correa B.R., Krepischi A.C., Olivieri E.H., Cunha I.W., Tabori U., et al. Recurrent somatic mutation in DROSHA induces microRNA profile changes in Wilms tumour. Nat. Commun. 2014, 5:4039.
41. Urbach A., Yermalovich A., Zhang J., Spina C.S., Zhu H., Perez-Atayde A.R., Shukrun R., Charlton J., Sebire N., Mifsud W., et al. Lin28 sustains early renal progenitors and induces Wilms tumor. Genes Dev. 2014, 28:971-982.
42. Viswanathan S.R., Powers J.T., Einhorn W., Hoshida Y., Ng T.L., Toffanin S., O'Sullivan M., Lu J., Phillips L.A., Lockhart V.L., et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat. Genet. 2009, 41:843-848.
43. Vujanić G.M., Sandstedt B. The pathology of Wilms' tumour (nephroblastoma): the International Society of Paediatric Oncology approach. J.Clin. Pathol. 2010, 63:102-109.
44. Walz A.L., Ooms A., Gadd S., Gerhard D.S., Smith M.A., GuidryAuvil J.M., Daoud Meerzaman, Chen Q.-R., Hsu C.H., Yan C., et al. Recurrent DGCR8, DROSHA, and SIX homeodomain mutations in favorable histology Wilms tumors. Cancer Cell 2015, 27:286-297. this issue.
45. Wegert J., Wittmann S., Leuschner I., Geissinger E., Graf N., Gessler M. WTX inactivation is a frequent, but late event in Wilms tumors without apparent clinical impact. Genes Chromosomes Cancer 2009, 48:1102-1111.
46. Weirich A., Leuschner I., Harms D., Vujanic G.M., Troger J., Abel U., Graf N., Schmidt D., Ludwig R., Voute P.A. Clinical impact of histologic subtypes in localized non-anaplastic nephroblastoma treated according to the trial and study SIOP-9/GPOH. Ann. Oncol. 2001, 12:311-319.
47. Weirich A., Ludwig R., Graf N., Abel U., Leuschner I., Vujanic G.M., Mehls O., Boos J., Beck J., Royer-Pokora B., Voute P.A. Survival in nephroblastoma treated according to the trial and study SIOP-9/GPOH with respect to relapse and morbidity. Ann. Oncol. 2004, 15:808-820.
48. Williams R.D., Al-Saadi R., Chagtai T., Popov S., Messahel B., Sebire N., Gessler M., Wegert J., Graf N., Leuschner I., et al. Subtype-specific FBXW7 mutation and MYCN copy number gain in Wilms' tumor. Clin. Cancer Res. 2010, 16:2036-2045.
49. Wu M.K., Sabbaghian N., Xu B., Addidou-Kalucki S., Bernard C., Zou D., Reeve A.E., Eccles M.R., Cole C., Choong C.S., et al. Biallelic DICER1 mutations occur in Wilms tumours. J.Pathol. 2013, 230:154-164.
50. Yu J., McMahon A.P., Valerius M.T. Recent genetic studies of mouse kidney development. Curr. Opin. Genet. Dev. 2004, 14:550-557.
51. Zirn B., Hartmann O., Samans B., Krause M., Wittmann S., Mertens F., Graf N., Eilers M., Gessler M. Expression profiling of Wilms tumors reveals new candidate genes for different clinical parameters. Int. J. Cancer 2006, 118:1954-1962.