c-Myc regulates RNA splicing of the A-Raf kinase and its activation of the ERK pathway

Cancer Research

Volumn 71, Issue 13, 2011, Pages 4664-4674

  Rauch, Jens ^a,b   Moran Jones, Kim ^b,c   Albrecht, Valerie ^d   Schwarzl, Thomas ^a   Hunter, Keith ^e   Gires, Olivier ^d   Kolch, Walter ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

A RAF KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PROTEIN MST2; RAS PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HNRNP H; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; APOPTOSIS; ARTICLE; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; DRUG ACTIVITY; ENZYME ACTIVATION; ENZYME REGULATION; GENE SEQUENCE; GENETIC TRANSFECTION; GENETIC TRANSFORMATION; HEAD AND NECK CANCER; HNRNP H ONCOGENE; HUMAN; HUMAN CELL; INTRON; ONCOGENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA SPLICING; SIGNAL TRANSDUCTION;

ALTERNATIVE SPLICING; ANIMALS; DOWN-REGULATION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HCT116 CELLS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP F-H; HUMANS; ISOENZYMES; MAP KINASE SIGNALING SYSTEM; MICE; NIH 3T3 CELLS; PROTO-ONCOGENE PROTEINS A-RAF; PROTO-ONCOGENE PROTEINS C-MYC; RAS PROTEINS; TRANSFORMATION, GENETIC;

EID: 79959863480     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-4447     Document Type: Article

References (49)

1. Yoon S, Seger R. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 2006;24:21-44.
2. Wellbrock C, Karasarides M, Marais R. The RAF proteins take centre stage. Nat Rev Mol Cell Biol 2004;5:875-85.
3. Dhillon AS, Hagan S, Rath O, Kolch W. MAP kinase signalling pathways in cancer. Oncogene 2007;26:3279-90.
4. Rauch J, Kolch W. A-Raf/v-raf murine sarcoma 3611 viral oncogene homolog. UCSD-Nature Molecule Pages (2010). (doi:10.1038/mp. a000307.01). [cited]; Available from: http://www.signaling-gateway. org/molecule/query?afcsid=A000307.
5. Baljuls A, Mueller T, Drexler HC, Hekman M, Rapp UR.Unique N-region determines low basal activity and limited inducibility of A-RAF kinase: the role of N-region in the evolutionary divergence of RAF kinase function in vertebrates. J Biol Chem 2007;282:26575-90.
6. Rauch J, O'Neill E, Mack B, Matthias C, Munz M, Kolch W, et al. Heterogeneous nuclear ribonucleoprotein H blocks MST2-mediated apoptosis in cancer cells by regulating a-raf transcription. Cancer Res 2010;70:1679-88.
7. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 2003;3:11-22.
8. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 2008;9:517-31.
9. Pratilas CA, Solit DB. Targeting the mitogen-activated protein kinase pathway: physiological feedback and drug response. Clin Cancer Res 2010;16:3329-34.
10. Niault TS, Baccarini M. Targets of Raf in tumorigenesis. Carcinogenesis 2010;31:1165-74.
11. Zebisch A, Troppmair J. Back to the roots: the remarkable RAF oncogene story. Cell Mol Life Sci 2006;63:1314-30.
12. Hagemann C, Gloger J, Anacker J, Said HM, Gerngras S, Kühnel S, et al. RAF expression in human astrocytic tumors. Int J Mol Med 2009;23:17-31.
13. Kisanuki H, Choi YL, Wada T, Moriuchi R, Fujiwara S, Kaneda R, et al. Retroviral expression screening of oncogenes in pancreatic ductal carcinoma. Eur J Cancer 2005;41:2170-5.
14. Mark GE, Seeley TW, Shows TB, Mountz JD. Pks, a raf-related sequence in humans. Proc Natl Acad Sci U S A 1986;83:6312-6.
15. Rauch J, Ahlemann M, Schaffrik M, Mack B, Ertongur S, Andratschke M, et al. Allogenic antibody-mediated identification of head and neck cancer antigens. Biochem Biophys Res Commun 2004;323:156-62.
16. Papin C, Denouel-Galy A, Laugier D, Calothy G, Eychene A. Modulation of kinase activity and oncogenic properties by alternative splicing reveals a novel regulatory mechanism for B-Raf. J Biol Chem 1998;273:24939-47.
17. Papin C, Eychene A, Brunet A, Pagès G, Pouysségur J, Calothy G, et al. B-Raf protein isoforms interact with and phosphorylate Mek-1 on serine residues 218 and 222. Oncogene 1995;10:1647-51.
18. Baitei EY, Zou M, Al-Mohanna F, Collison K, Alzahrani AS, Farid NR, et al. Aberrant BRAF splicing as an alternative mechanism for oncogenic B-Raf activation in thyroid carcinoma. J Pathol 2009;217: 707-15.
19. He C, Zhou F, Zuo Z, Cheng H, Zhou R. A global view of cancer-specific transcript variants by subtractive transcriptome-wide analysis. PLoS One 2009;4:e4732.
20. Yokoyama T, Takano K, Yoshida A, Katada F, Sun P, Takenawa T, et al. DA-Raf1, a competent intrinsic dominant-negative antagonist of the Ras-ERK pathway, is required for myogenic differentiation. J Cell Biol 2007;177:781-93.
21. Nekhoroshkova E, Albert S, Becker M, Rapp UR. A-RAF kinase functions in ARF6 regulated endocytic membrane traffic. PLoS ONE 2009;4:e4647.
22. Pelengaris S, Khan M, Evan G. c-MYC: more than just a matter of life and death. Nat Rev Cancer 2002;2:764-76.
23. Adhikary S, Eilers M. Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 2005;6:635-45.
24. Zeller KI, Jegga AG, Aronow BJ, O'Donnell KA, Dang CV. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol 2003;4:R69.
25. Zeller KI, Zhao X, Lee CW, Chiu KP, Yao F, Yustein JT, et al. Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc Natl Acad Sci U S A 2006;103:17834-9.
26. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Semin Cancer Biol 2006;16:253-64.
27. Mayer A, Andratschke M, Pauli C, Graefe H, Kristina K, Wollenberg B. Generation of an autologous cell system for immunotherapy of squamous cell carcinoma of the head and neck. Anticancer Res 2005;25:4075-80.
28. Matallanas D, Sanz-Moreno V, Arozarena I, Calvo F, Agudo- Ibáñez L, Santos E, et al. Distinct utilization of effectors and biological outcomes resulting from site-specific Ras activation: Ras functions in lipid rafts and Golgi complex are dispensable for proliferation and transformation. Mol Cell Biol 2006;26:100-16.
29. O'Neill E, Rushworth L, Baccarini M, Kolch W. Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1. Science 2004;306:2267-70.
30. Weischenfeldt J, Lykke-Andersen J, Porse B. Messenger RNA surveillance: neutralizing natural nonsense. Curr Biol 2005;15:R559-62.
31. Kolch W, Heidecker G, Lloyd P, Rapp UR. Raf-1 protein kinase is required for growth of induced NIH/3T3 cells. Nature 1991;349:426-8.
32. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 2007;7:295-308.
33. Littlewood TD, Hancock DC, Danielian PS, Parker MG, Evan GI. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res 1995;23:1686-90.
34. Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, et al. The UCSC genome browser database. Nucleic Acids Res 2003;31:51-4.
35. Birney E, Stamatoyannopoulos JA, Dutta A, Kent WJ, Guigó R, Gingeras TR, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007;447:799-816.
36. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008;456:470-6.
37. Garcia-Blanco MA, Baraniak AP, Lasda EL. Alternative splicing in disease and therapy. Nat Biotechnol 2004;22:535-46.
38. Wang GS, Cooper TA. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 2007;8:749-61.
39. Venables JP. Aberrant and alternative splicing in cancer. Cancer Res 2004;64:7647-54.
40. Venables JP. Unbalanced alternative splicing and its significance in cancer. Bioessays 2006;28:378-86.
41. Carpenter B, MacKay C, Alnabulsi A, MacKay M, Telfer C, Melvin WT, et al. The roles of heterogeneous nuclear ribonucleoproteins in tumour development and progression. Biochim Biophys Acta 2006;1765:85-100.
42. Garneau D, Revil T, Fisette JF, Chabot B. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 2005;280:22641-50.
43. Rooke N, Markovtsov V, Cagavi E, Black DL. Roles for SR proteins and hnRNP A1 in the regulation of c-src exon N1. Mol Cell Biol 2003;23:1874-84.
44. Markovtsov V, Nikolic JM, Goldman JA, Turck CW, Chou MY, Black DL. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol Cell Biol 2000;20:7463-79.
45. Pan Q, Saltzman AL, Kim YK, Misquitta C, Shai O, Maquat LE, et al. Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes Dev 2006;20:153-8.
46. Kolch W, Philipp A, Mischak H, Dutil EM, Mullen TM, Feramisco JR, et al. Inhibition of Raf-1 signaling by a monoclonal antibody, which interferes with Raf-1 activation and with Mek substrate binding. Oncogene 1996;13:1305-14.
47. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2009;463:364-8.
48. Mazurek S, Boschek CB, Hugo F, Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Semin Cancer Biol 2005;15:300-8.
49. Mazurek S, Drexler HC, Troppmair J, Eigenbrodt E, Rapp UR. Regulation of pyruvate kinase typeM2 by A-Raf: a possible glycolytic stop or go mechanism. Anticancer Res 2007;27:3963-71.