Splicing factor hnRNP A2/B1 regulates tumor suppressor gene splicing and is an oncogenic driver in glioblastoma

Cancer Research

Volumn 71, Issue 13, 2011, Pages 4464-4472

  Golan Gerstl, Regina ^a   Cohen, Michal ^a   Shilo, Asaf ^a   Suh, Sung Suk ^b   Bakàcs, Arianna ^c   Coppola, Luigi ^c   Karni, Rotem ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b OHIO STATE UNIVERSITY   (United States)

^c SAN FILIPPO NERI HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIN1 GENE; C FLIP GENE; CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; CELL IMMORTALIZATION; CONTROLLED STUDY; GENE CONTROL; GENE DELETION; GENE OVEREXPRESSION; GLIOBLASTOMA; HNRNPA2B1 GENE; HUMAN; HUMAN TISSUE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTO ONCOGENE; RNA SPLICING; RON GENE; TUMOR SUPPRESSOR GENE; WWOX GENE;

ALTERNATIVE SPLICING; ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; GENE DOSAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENES, TUMOR SUPPRESSOR; GLIOBLASTOMA; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; MICE; NIH 3T3 CELLS; RECEPTOR PROTEIN-TYROSINE KINASES; UP-REGULATION;

EID: 79959892321     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-4410     Document Type: Article

References (43)

1. Venables JP, Klinck R, Koh C, Gervais-Bird J, Bramard A, Inkel L, et al. Cancer-associated regulation of alternative splicing. Nat Struct Mol Biol 2009;16:670-6.
2. Xi L, Feber A, Gupta V, Wu M, Bergemann AD, Landreneau RJ, et al. Whole genome exon arrays identify differential expression of alternatively spliced, cancer-related genes in lung cancer. Nucleic Acids Res 2008;36:6535-47.
3. Roy M, Xu Q, Lee C. Evidence that public database records for many cancer-associated genes reflect a splice form found in tumors and lack normal splice forms. Nucleic Acids Res 2005;33:5026-33. (Pubitemid 41487810)
4. Venables JP. Aberrant and alternative splicing in cancer. Cancer Res 2004;64:7647-54. (Pubitemid 39446889)
5. Srebrow A, Kornblihtt AR. The connection between splicing and cancer. J Cell Sci 2006;119:2635-41. (Pubitemid 44184000)
6. Kim E, Goren A, Ast G. Insights into the connection between cancer and alternative splicing. Trends Genet 2008;24:7-10. (Pubitemid 350298628)
7. Karni R, de Stanchina E, Lowe SW, Sinha R, Mu D, Krainer AR. The gene coding for the splicing factor SF2/ASF is a proto-oncogene. Nat Struct Mol Biol 2007;14:185-93. (Pubitemid 46355578)
8. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell 2009;136:777-93.
9. Hanamura A, Cáceres JF, Mayeda A, Franza BR Jr, Krainer AR. Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 1998;4:430-44. (Pubitemid 28160784)
10. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002;3:195-205.
11. Mayeda A, Krainer AR. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 1992;68:365-75.
12. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003;72:291-336. (Pubitemid 36930448)
13. Cartegni L, Chew SL, Krainer AR. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 2002;3:285-98. (Pubitemid 34279797)
14. Guil S, Cáceres JF. The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat Struct Mol Biol 2007;14:591-6. (Pubitemid 47037061)
15. Michlewski G, Guil S, Semple CA, Cáceres JF. Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 2008;32:383-93.
16. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al. A microRNA polycistron as a potential human oncogene. Nature 2005;435:828-33. (Pubitemid 40839734)
17. Fielding P, Turnbull L, Prime W, Walshaw M, Field JK. Heterogeneous nuclear ribonucleoprotein A2/B1 up-regulation in bronchial lavage specimens: a clinical marker of early lung cancer detection. Clin Cancer Res 1999;5:4048-52. (Pubitemid 30013783)
18. Zhou J, Nong L, Wloch M, Cantor A, Mulshine JL, Tockman MS. Expression of early lung cancer detection marker: hnRNP-A2/B1 and its relation to microsatellite alteration in non-small cell lung cancer. Lung Cancer 2001;34:341-50. (Pubitemid 33048796)
19. Patry C, Bouchard L, Labrecque P, Gendron D, Lemieux B, Toutant J, et al. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res 2003;63:7679-88. (Pubitemid 37466696)
20. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010;463:364-8.
21. Clower CV, Chatterjee D, Wang Z, Cantley LC, Vander Heiden MG, Krainer AR. The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism. Proc Natl Acad Sci U S A 2010;107:1894-9.
22. Mayeda A, Munroe SH, Cáceres JF, Krainer AR. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J 1994;13:5483-95. (Pubitemid 24351827)
23. Karni R, Hippo Y, Lowe SW, Krainer AR. The splicing factor oncoprotein SF2/ASF activates the mTORC1. Proc Natl Acad Sci U S A 2008;105:15323-7.
24. Zhu Y, Parada LF. The molecular and genetic basis of neurological tumours. Nat Rev Cancer 2002;2:616-26. (Pubitemid 37328928)
25. Ghigna C, Giordano S, Shen H, Benvenuto F, Castiglioni F, Comoglio PM, et al. Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol Cell 2005;20:881-90. (Pubitemid 41814877)
26. Benvenuti S, Comoglio PM. The MET receptor tyrosine kinase in invasion and metastasis. J Cell Physiol 2007;213:316-25. (Pubitemid 47509708)
27. Denley A, Wallace JC, Cosgrove LJ, Forbes BE. The insulin receptor isoform exon 11- (IR-A) in cancer and other diseases: a review. Horm Metab Res 2003;35:778-85. (Pubitemid 38058183)
28. Frasca F, Pandini G, Scalia P, Sciacca L, Mineo R, Costantino A, et al. Insulin receptor isoform A, a newly recognized, high-affinity insulin-like growth factor II receptor in fetal and cancer cells. Mol Cell Biol 1999;19:3278-88. (Pubitemid 29193789)
29. Hietakangas V, Poukkula M, Heiskanen KM, Karvinen JT, Sistonen L, Eriksson JE. Erythroid differentiation sensitizes K562 leukemia cells to TRAIL-induced apoptosis by downregulation of c-FLIP. Mol Cell Biol 2003;23:1278-91. (Pubitemid 36177037)
30. Fricker N, Beaudouin J, Richter P, Eils R, Krammer PH, Lavrik IN. Model-based dissection of CD95 signaling dynamics reveals both a pro- and antiapoptotic role of c-FLIPL. J Cell Biol 2010;190:377-89.
31. Lüschen S, Falk M, Scherer G, Ussat S, Paulsen M, Adam-Klages S. The Fas-associated death domain protein/caspase-8/c-FLIP signaling pathway is involved in TNF-induced activation of ERK. Exp Cell Res 2005;310:33-42. (Pubitemid 41393685)
32. Park D, Shim E, Kim Y, Kim YM, Lee H, Choe J, et al. C-FLIP promotes the motility of cancer cells by activating FAK and ERK, and increasing MMP-9 expression. Mol Cells 2008;25:184-95. (Pubitemid 351818994)
33. Ge K, DuHadaway J, Du W, Herlyn M, Rodeck U, Prendergast GC. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc Natl Acad Sci U S A 1999;96:9689-94. (Pubitemid 29398793)
34. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med 2005;11:312-9. (Pubitemid 40460560)
35. Srinivasula SM, Ahmad M, Guo Y, Zhan Y, Lazebnik Y, Fernandes-Alnemri T, et al. Identification of an endogenous dominant-negative short isoform of caspase-9 that can regulate apoptosis. Cancer Res 1999;59:999-1002. (Pubitemid 29135957)
36. Johnson CR, Jarvis WD. Caspase-9 regulation: an update. Apoptosis 2004;9:423-7. (Pubitemid 38987578)
37. Salah Z, Aqeilan R, Huebner K. WWOX gene and gene product: tumor suppression through specific protein interactions. Future Oncol 2010;6:249-59.
38. Kosla K, Pluciennik E, Kurzyk A, Jesionek-Kupnicka D, Kordek R, Potemski P, et al. Molecular analysis of WWOX expression correlation with proliferation and apoptosis in glioblastoma multiforme. J Neurooncol 2011;101:207-13.
39. Driouch K, Prydz H, Monese R, Johansen H, Lidereau R, Frengen E. Alternative transcripts of the candidate tumor suppressor gene, WWOX, are expressed at high levels in human breast tumors. Oncogene 2002;21:1832-40. (Pubitemid 34259185)
40. Chabot B, Blanchette M, Lapierre I, La Branche H. An intron element modulating 50 splice site selection in the hnRNP A1 pre-mRNA interacts with hnRNP A1. Mol Cell Biol 1997;17:1776-86. (Pubitemid 27133262)
41. Moran-Jones K, Grindlay J, Jones M, Smith R, Norman JC. hnRNP A2 regulates alternative mRNA splicing of TP53INP2 to control invasive cell migration. Cancer Res 2009;69:9219-27.
42. Michlewski G, Cáceres JF. Antagonistic role of hnRNP A1 and KSRP in the regulation of let-7a biogenesis. Nat Struct Mol Biol 2010;17:1011-8.
43. Pioli PA, Rigby WF. The von Hippel-Lindau protein interacts with heteronuclear ribonucleoprotein a2 and regulates its expression. J Biol Chem 2001;276:40346-52.