AGenome-wide aberrantRNASplicing in patients with acute myeloid leukemia identifies novel potential disease markers and therapeutic targets

Clinical Cancer Research

Volumn 20, Issue 5, 2014, Pages 1135-1145

  Adamia, Sophia ^a   Haibe Kains, Benjamin ^b   Pilarski, Patrick M ^c   Bar Natan, Michal ^d   Pevzner, Samuel ^e   Avet Loiseau, Herve ^f   Lode, Laurence ^g   Verselis, Sigitas ^a   Fox, Edward A ^a   Burke, John ^h   Galinsky, Ilene ^a   Dagogo Jack, Ibiayi ⁱ   Wadleigh, Martha ^a   Steensma, David P ^a   Motyckova, Gabriela ^a   Deangelo, Daniel J ^a   Quackenbush, John ^a   Stone, Richard ^a   Griffin, James D ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BOSTON UNIVERSITY   (United States)

^f TOULOUSE UNIVERSITY HOSPITAL   (France)

^g Team 12   (France)

^h Biotique Systems Inc Wwwbiotiquesystemscom   (United States)

ⁱ BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; TUMOR SUPPRESSOR PROTEIN; MICROSOMAL AMINOPEPTIDASE; TUMOR MARKER;

ACUTE GRANULOCYTIC LEUKEMIA; ALTERNATIVE RNA SPLICING; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE MARKER; DRUG TARGETING; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKEMOGENESIS; MAJOR CLINICAL STUDY; ONCOGENE; PRIORITY JOURNAL; RNA SEQUENCE; SPLICEOSOME; TUMOR SUPPRESSOR GENE; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENETIC ASSOCIATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MOLECULARLY TARGETED THERAPY; REPRODUCIBILITY; RNA SPLICING; SIGNAL TRANSDUCTION;

ALTERNATIVE SPLICING; ANTIGENS, CD13; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LEUKEMIA, MYELOID, ACUTE; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR TARGETED THERAPY; REPRODUCIBILITY OF RESULTS; RNA SPLICING; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84895817817     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-0956     Document Type: Article

References (44)

1. Ast G. How did alternative splicing evolve? Nat Rev Genet 2004;5: 773-82.
2. Cartegni L, Chew SL, Krainer AR. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 2002;3:285-98.
3. Jurica MS, Moore MJ. Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 2003;12:5-14.
4. Jurica MS. Searching for a wrench to throw into the splicing machine. Nat Chem Biol 2008;4:3-6.
5. Hastings ML, Krainer AR. Pre-mRNA splicing in the new millennium. Curr Opin Cell Biol 2001;13:302-9.
6. Matlin AJ, Moore MJ. Spliceosome assembly and composition. Adv Exp Med Biol 2007;623:14-35.
7. Abrahamsson AE, Geron I, Gotlib J, Dao KH, Barroga CF, Newton IG, et al. Glycogen synthase kinase 3beta missplicing contributes to leukemia stem cell generation. Proc Natl Acad Sci U S A 2009;106: 3925-9.
8. Vassen L, Khandanpour C, Ebeling P, van der Reijden BA, Jansen JH, Mahlmann S, et al. Growth factor independent 1b (Gfi1b) and a new splice variant of Gfi1b are highly expressed in patients with acute and chronic leukemia. Int J Hematol 2009;89:422-30.
9. Liu X, Zhang Q, Zhang DE, Zhou C, Xing H, Tian Z, et al. Overexpression of an isoform of AML1 in acute leukemia and its potential role in leukemogenesis. Leukemia 2009;23:739-45.
10. Meyer D, Seth S, Albrecht J, Maier MK, du Pasquier L, Ravens I, et al. CD96 interaction with CD155 via its first Ig-like domain is modulated by alternative splicing or mutations in distal Ig-like domains. J Biol Chem 2009;284:2235-44.
11. Wagner M, Schmelz K, Wuchter C, Ludwig WD, Dorken B, Tamm I. In vivo expression of survivin and its splice variant survivin-2B: impact on clinical outcome in acute myeloid leukemia. Int J Cancer 2006;119: 1291-7.
12. Mannari D, Gascoyne D, Dunne J, Chaplin T, Young B. A novel exon in AML1-ETOnegatively influences the clonogenic potential of the t(8;21) in acute myeloid leukemia. Leukemia 2010;24:891-4.
13. Ommen HB, Ostergaard M, Yan M, Braendstrup K, Zhang DE, Hokland P. Persistent altered fusion transcript splicing identifies RUNX1-RUNX1T1+ AML patients likely to relapse. Eur J Haematol 2010;84: 128-32.
14. Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, et al. CD44 splice isoformswitching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Invest 2011;121:1064-74.
15. Lu X, Feng X, Man X, Yang G, Tang L, Du D, et al. Aberrant splicing of Hugl-1 is associated with hepatocellular carcinoma progression. Clin Cancer Res 2009;15:3287-96.
16. Tazi J, Bakkour N, Stamm S. Alternative splicing and disease. Biochim Biophys Acta 2009;1792:14-26.
17. Caballero OL, de Souza SJ, Brentani RR, Simpson AJ. Alternative spliced transcripts as cancer markers. Dis Markers 2001;17:67-75.
18. Barta A, Schumperli D. Editorial on alternative splicing and disease. RNA Biol 2010;7:388-9.
19. David A, Mabjeesh N, Azar I, Biton S, Engel S, Bernstein J, et al. Unusual alternative splicing within the human kallikrein genes KLK2 and KLK3 gives rise to novel prostate-specific proteins. J Biol Chem 2002;277:18084-90.
20. Kote-Jarai Z, Amin Al Olama A, Leongamornlert D, Tymrakiewicz M, Saunders E, Guy M, et al. Identification of a novel prostate cancer susceptibility variant in the KLK3 gene transcript. Hum Genet 2011; 129:687-94.
21. Yoshida K, Sanada M, Shiraishi Y, Nowak D, Nagata Y, Yamamoto R, et al. Frequent pathway mutations of splicing machinery in myelodysplasia. Nature 2011;478:64-9.
22. Graubert TA, Shen D, Ding L, Okeyo-Owuor T, Lunn CL, Shao J, et al. Recurrent mutations in the U2AF1 splicing factor in myelodysplastic syndromes. Nat Genet 2011;44:53-7.
23. Malcovati L, Papaemmanuil E, Bowen DT, Boultwood J, Della Porta MG, Pascutto C, et al. Clinical significance of SF3B1 mutations in myelodysplastic syndromes and myelodysplastic/myeloproliferative neoplasms. Blood 2011;118:6239-46.
24. Zhang SJ, Rampal R, Manshouri T, Patel J, Mensah N, Kayserian A, et al. Genetic analysis of patients with leukemic transformation of myeloproliferative neoplasms shows recurrent SRSF2 mutations that are associated with adverse outcome. Blood 2012;119:4480-5.
25. Mansouri L, Gunnarsson R, Sutton LA, Ameur A, Hooper SD, Mayrhofer M, et al. Next generation RNA-sequencing in prognostic subsets of chronic lymphocytic leukemia. Am J Hematol 2012;87:737-40.
26. Damm F, Nguyen-Khac F, Fontenay M, Bernard OA. Spliceosome and other novel mutations in chronic lymphocytic leukemia and myeloid malignancies. Leukemia 2012;26:2027-31.
27. Quesada V, Conde L, Villamor N, Ordonez GR, Jares P, Bassaganyas L, et al. Exome sequencing identifies recurrent mutations of the splicing factor SF3B1 gene in chronic lymphocytic leukemia. Nat Genet 2012;44:47-52.
28. Rossi D, Bruscaggin A, Spina V, Rasi S, Khiabanian H, Messina M, et al. Mutations of the SF3B1 splicing factor in chronic lymphocytic leukemia: association with progression and fludarabine-refractoriness. Blood 2011;118:6904-8.
29. Dolnik A, Engelmann JC, Scharfenberger-Schmeer M, Mauch J, Kelkenberg-Schade S, Haldemann B, et al. Commonly altered genomic regions in acute myeloid leukemia are enriched for somatic mutations involved in chromatinremodeling andsplicing. Blood2012;120:e83-92.
30. Ogawa S. Splicing factor mutations in myelodysplasia. Int J Hematol 2012;96:438-42.
31. Adamia S, Reiman T,CrainieM, MantMJ, Belch AR, PilarskiLM. Intronic splicing of hyaluronansynthase1 (HAS1): a biologically relevant indicator of poor outcome in multiple myeloma. Blood 2005;105:4836-44.
32. Caldenhoven E, van Dijk TB, Solari R, Armstrong J, Raaijmakers JA, Lammers JW, et al. STAT3beta, a splice variant of transcription factor STAT3, is a dominant negative regulator of transcription. J Biol Chem 1996;271:13221-7.
33. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P, Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 2002;16:3074-86.
34. Fridman JS, Hernando E, Hemann MT, de Stanchina E, Cordon-Cardo C, Lowe SW. Tumor promotion byMdm2 splice variants unable to bind p53. Cancer Res 2003;63:5703-6.
35. Bourdon JC, Fernandes K, Murray-Zmijewski F, Liu G, Diot A, Xirodimas DP, et al. p53 isoforms can regulate p53 transcriptional activity. Genes Dev 2005;19:2122-37.
36. Evans SC, Viswanathan M, Grier JD, Narayana M, El-Naggar AK, Lozano G. An alternatively spliced HDM2 product increases p53 activity by inhibiting HDM2. Oncogene 2001;20:4041-9.
37. Thorsen K, Sorensen KD, Brems-Eskildsen AS, Modin C, Gaustadnes M, Hein AM, et al. Alternative splicing in colon, bladder, and prostate cancer identified by exon array analysis. Mol Cell Proteomics 2008;7: 1214-24.
38. Andre F, Michiels S, Dessen P, Scott V, Suciu V, Uzan C, et al. Exonic expression profiling of breast cancer and benign lesions: a retrospective analysis. Lancet Oncol 2009;10:381-90.
39. 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.
40. Cheung HC, Baggerly KA, Tsavachidis S, Bachinski LL, Neubauer VL, Nixon TJ, et al. Global analysis of aberrant pre-mRNA splicing in glioblastoma using exon expression arrays. BMC Genomics 2008; 9:216.
41. Raghavachari N, Barb J, Yang Y, Liu P, Woodhouse K, Levy D, et al. A systematic comparison and evaluation of high density exon arrays and RNA-seq technology used to unravel the peripheral blood transcriptome of sickle cell disease. BMC Med Genomics 2012;5:28.
42. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 2008;18:1509-17.
43. Bartel F, Taubert H, Harris LC. Alternative and aberrant splicing of MDM2 mRNA in human cancer. Cancer Cell 2002;2:9-15.
44. Bartel F, Taylor AC, Taubert H, Harris LC. Novel mdm2 splice variants identified in pediatric rhabdomyosarcoma tumors and cell lines. Oncol Res 2001;12:451-7.