Deficiency of splicing factor 1 suppresses the occurrence of testicular germ cell tumors

Cancer Research

Volumn 70, Issue 18, 2010, Pages 7264-7272

  Zhu, Rui ^a   Heaney, Jason ^b   Nadeau, Joseph H ^b   Ali, Sara ^a   Matin, Angabin ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; MESSENGER RNA; SPLICING FACTOR 1; TUMOR PROMOTER; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; DNA BINDING PROTEIN; TRANSCRIPTION FACTOR; ZFP162 PROTEIN, MOUSE;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER INCIDENCE; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EUKARYOTIC CELL; GERM CELL TUMOR; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC CELL; TESTIS; TESTIS CELL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL TRANSFORMATION; DEFICIENCY; FEMALE; GENETICS; KNOCKOUT MOUSE; METABOLISM; NEOPLASM; TESTIS TUMOR;

ALTERNATIVE SPLICING; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASMS, GERM CELL AND EMBRYONAL; RNA, MESSENGER; TESTICULAR NEOPLASMS; TRANSCRIPTION FACTORS;

EID: 77956923246     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0820     Document Type: Article

References (49)

1. Skakkebaek NE, Berthelsen JG, Giwercman A, Muller J. Carcinoma-in-situ of the testis: possible origin from gonocytes and precursor of all types of germ cell tumours except spermatocytoma. Int J Androl 1987;10:19-28.
2. Oosterhuis JW, Looijenga LHJ. Testicular germ-cell tumours in a broader perspective. Nat Rev Cancer 2005;5:210-22.
3. Dieckmann KP, Skakkebaek NE. Carcinoma in situ of the testis: review of biological and clinical features. Int J Cancer 1999;83:815-22.
4. Lutke Holzik MF, Sijmons RH, Sleijfer DT, et al. Syndromic aspects of testicular carcinoma. Cancer 2003;97:984-92.
5. Crockford GP, Linger R, Hockley S, et al. Genome-wide linkage screen for testicular germ cell tumour susceptibility loci. Hum Mol Genet 2006;15:443-51.
6. Linger R, Dudakia D, Huddart R, et al. A physical analysis of the Y chromosome shows no additional deletions, other than Gr/Gr, associated with testicular germ cell tumour. Br J Cancer 2007;96:357-61.
7. Kanetsky PA, Mitra N, Vardhanabhuti S, et al. Common variation in KITLG and at 5q31.3 predisposes to testicular germ cell cancer. Nat Genet 2009;41:811-5.
8. Rapley EA, Turnbull C, Olama AAA, et al. A genome-wide association study of testicular germ cell tumor. Nat Genet 2009;41:807-10.
9. Stevens LC. Embryology of testicular teratomas in strain 129 mice. J Natl Cancer Inst 1959;23:1249-95.
10. Krentz AD, Murphy MW, Kim S, et al. The DM domain protein DMRT1 is a dose- sensitive regulator of fetal germ cell proliferation and pluripotency. Proc Natl Acad Sci U S A 2009;106:22323-8.
11. Youngren KK, Coveney D, Peng X, et al. The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 2005;435:360-4.
12. Kimura T, Suzuki A, Fujita Y, et al. Conditional loss of PTEN leads to testicular teratoma and enhances embryonic germ cell production. Development 2003;130:1691-700.
13. Heaney JD, Lam M-YJ, Michelson MV, Nadeau JH. Loss of the transmembrane but not the soluble Kit ligand isoform increases testicular germ cell tumor susceptibility in mice. Cancer Res 2008;68:5193-7.
14. Donehower LA, Harvey M, Vogel H, et al. Effects of genetic background on tumorigenesis in p53-deficient mice. Mol Carcinog 1995;14:16-22.
15. Heaney JD, Michelson MV, Youngren KK, Lam M-YJ, Nadeau JH. Deletion of eIF2β suppresses testicular cancer incidence and causes recessive lethality in agouti-yellow mice. Hum Mol Genet 2009;18:1395-404.
16. Rescorla FJ. Pediatric germ cell tumors. Semin Surg Oncol 1999;16:144-58.
17. Weidinger G, Stebler J, Slanchev K, et al. Dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 2003;13:1429-34.
18. Cook MS, Coveney D, Batchvarov I, Nadeau JH, Capel B. BAX-mediated cell death affects early germ cell loss and incidence of testicular teratomas in Dnd1(Ter/Ter) mice. Dev Biol 2009;328:377-83.
19. Noguchi T, Noguchi M. A recessive mutation (ter) causing germ cell deficiency and a high incidence of congenital testicular teratomas in 129/Sv-ter mice. J Natl Cancer Inst 1985;75:385-92.
20. Noguchi T, Stevens LC. Primordial germ cell proliferation in fetal testes in mouse strains with high and low incidences of congenital testicular teratomas. J Natl Cancer Inst 1982;69:907-13.
21. Matin A, Collin GB, Asada Y, Varnum D, Nadeau JH. Susceptibility to testicular germ-cell tumours in a 129.MOLF-Chr 19 chromosome substitution strain. Nat Genet 1999;23:237-40.
22. Youngren KK, Nadeau JH, Matin A. Testicular cancer susceptibility in the 129.MOLF-Chr 19 mouse strain: additive effects, gene interactions and epigenetic modifications. Hum Mol Genet 2003;12:389-98.
23. Zhu R, Ji Y, Xiao L, Matin A. Testicular germ cell tumor susceptibility genes from the consomic 129.MOLF-Chr 19 mouse strain. Mamm Genome 2007;18:584-95.
24. Liu Z, Luyten I, Bottomley MJ, et al. Structural basis for recognition of the intronbranch site RNA by splicing factor 1.Science 2001;294:1098-102.
25. Selenko P, Gregorovic G, Sprangers R, et al. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol Cell 2003;11:965-76.
26. Das R, Reed R. Resolution of the mammalian E complex and the ATP-dependent spliceosome complexes on native agarose minigels. RNA 1999;5:1504-8.
27. Michaud S, Reed R. An ATP-independent complex commits pre-mRNA to the mammalian spliceosome assembly pathway. Genes Dev 1991;5:2534-46.
28. Berglund JA, Chua K, Abovich N, Reed R, Rosbash M. The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell 1997;89:781-7.
29. Kramer A. Purification of splicing factor SF1, a heat stable protein that functions in the assembly of a presplicing complex. Mol Cell Biol 1992;12:4545-52.
30. Berglund JA, Abovich N, Rosbash M. A cooperative interaction between U2AF65 and mBBP/SF1 facilitates branchpoint region recognition. Genes Dev 1998;12:858-67.
31. Tanackovic G, Kramer A. Human splicing factor SF3a, but not SF1, is essential for pre-mRNA splicing in vivo. Mol Biol Cell 2005;16:1366-77.
32. Shitashige M, Satow R, Honda K, Ono M, Hirohashi S, Yamada T. Increased susceptibility of Sf1+/- mice to azoxymethane-induced colon tumorigenesis. Cancer Sci 2007;98:1862-7.
33. Nagy A, Gertsenstein M, Vintersten K, Behringer R, editors. Manipulating the mouse embryo: a laboratory manual. New York: Cold Spring Harbor Laboratory Press; 2003, p. 687-9.
34. Dejosez M, Kreumenacker JS, Zitur LJ, et al. Ronin is essential for embryogenesis and the pluripotency of mouse embryonic stem cells. Cell 2008;133:1162-74.
35. Simpson EM, Linder CC, Sargent EE, Davisson MT, Mobraaten LE, Sharp JJ. Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat Genet 1997;16:19-27.
36. Qiu TH, Chandramouli GV, Hunter KW, Alkharouf NW, Green JE, Liu ET. Global expression profiling identifies signatures of tumor virulence in MMTV-PyMT-transgenic mice: correlation to human disease. Cancer Res 2004;64:5973-81.
37. Shitashige M, Naishiro Y, Idogawa M, et al. Involvement of splicing factor-1 in β-catenin/T-cell factor-4-mediated gene transactivation and pre-mRNA splicing. Gastroenterology 2007;132:1039-54.
38. Yeo G, Holste D, Kreiman G, Burge CB. Variation in alternative splicing across human tissues. Genome Biol 2004;5:R74.
39. Srebrow A, Kornblihtt AR. The connection between splicing and cancer. J Cell Sci 2006;119:2635-41.
40. Kim E, Goren A, Ast G. Insights into the connection between cancer and alternative splicing. Trends Genet 2008;24:7-10.
41. Ritchie W, Granjeaud S, Puthier D, Gautheret D. Entropy measures quantify global splicing disorders in cancer. PLoS Comput Biol 2008;4:e1000011.
42. Grosso AR, Martins S, Carmo-Fonseca M. The emerging role of splicing factors in cancer. EMBO Rep 2008;9:1087-93.
43. Zerbe LK, Pino I, Pio R, et al. Relative amounts of antagonistic splicing factors, hnRNPA1 and ASF/SF2, change during neoplastic lung growth: implications for pre-mRNA processing. Mol Carcinog 2004;41:187-96.
44. He C, Zuo Z, Chen H, et al. Genome-wide detection of testis- and testicular cancer-specific alternative splicing. Carcinogenesis 2007;28:2484-90.
45. Kempkensteffen C, Hinz S, Krause H, et al. Expression of splicing variants of the inhibitor of apoptosis Livin in testicular germ cell tumors. Tumor Biol 2008;29:76-82.
46. Kralovicova J, Houngninou-Molango S, Kramer A, Vorechovsky I. Branch site haplotypes that control alternative splicing. Hum Mol Genet 2004;24:3189-202.
47. Coulombe-Huntington J, Lam KCL, Dias C, Majewski J. Fine-scale variation and genetic determinants of alternative splicing across individuals. PLoS Genet 2009;5:e1000766.
48. Toda T, Iida A, Miwa T, Nakamura Y, Imai T. Isolation and characterization of a novel gene encoding nuclear protein at a locus (D11S636) tightly linked to multiple endocrine neoplasia type 1 (MEN1). Hum Mol Genet 1994;3:465-70.
49. Wrehlke C, Wiedemeyer WR, Schmitt-Wrede HP, Mincheva A, Lichter P, Wunderlich F. Genomic organization of mouse gene zfp162. DNA Cell Biol 1999;18:419-28.