The Splicing Efficiency of Activating HRAS Mutations Can Determine Costello Syndrome Phenotype and Frequency in Cancer

PLoS Genetics

Volumn 12, Issue 5, 2016, Pages

  Hartung, Anne Mette ^a   Swensen, Jeff ^b,c,d   Uriz, Inaki E ^a   Lapin, Morten ^a   Kristjansdottir, Karen ^a   Petersen, Ulrika S S ^a   Bang, Jeanne Mari V ^a   Guerra, Barbara ^a   Andersen, Henriette Skovgaard ^a   Dobrowolski, Steven F ^c   Carey, John C ^e   Yu, Ping ^d   Vaughn, Cecily ^d   Calhoun, Amy ^f   Larsen, Martin R ^a   Dyrskjøt, Lars ^g   Stevenson, David A ^h   Andresen, Brage S ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b CARIS LIFE SCIENCES   (United States)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^d ARUP LABORATORIES   (United States)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^g AARHUS UNIVERSITY HOSPITAL   (Denmark)

^h STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GLYCINE; GROWTH HORMONE; GUANOSINE TRIPHOSPHATE; MESSENGER RNA; OLIGONUCLEOTIDE; SPLICE SWITCHING OLIGONUCLEOTIDE; TELOMERIC REPEAT BINDING FACTOR 2; THREONINE; UNCLASSIFIED DRUG; VALINE; CODON; HRAS PROTEIN, HUMAN; PROTEIN P21; RNA SPLICING;

AORTA VALVE REGURGITATION; ARNOLD CHIARI MALFORMATION; ARTICLE; CANCER CELL; CASE REPORT; CELL PROLIFERATION; CELL VIABILITY; CHILD; CLINICAL FEATURE; CODON; COSTELLO SYNDROME; CROWDING (TOOTH); DNA SEQUENCE; DNA STRUCTURE; EAR MALFORMATION; ENHANCER REGION; ENZYME ACTIVE SITE; EXON SKIPPING; EXONIC SPLICING ENHANCER; EXONIC SPLICING SILENCER; GASTROSTOMY; GENE FREQUENCY; GENE MUTATION; GENE SWITCHING; GERMLINE MUTATION; GROWTH HORMONE DEFICIENCY; HEART LEFT VENTRICLE HYPERTROPHY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MALE; MASS SPECTROMETRY; NEOPLASM; NEVUS; NOSE SEPTUM PERFORATION; NUCLEOTIDE SEQUENCE; ONCOGENE H RAS; PHENOTYPE; PROTEIN MOTIF; PTOSIS; RETROGNATHIA; SEIZURE; SEQUENCE ANALYSIS; SILENCER ELEMENT; START CODON; STOMACH FUNDOPLICATION; TELECANTHUS; WESTERN BLOTTING; EXON; GENETICS; GENOTYPE; PATHOLOGY; RNA SPLICING;

CHILD; CODON; COSTELLO SYNDROME; EXONS; GENOTYPE; GERM-LINE MUTATION; HUMANS; MALE; NEOPLASMS; PHENOTYPE; PROTO-ONCOGENE PROTEINS P21(RAS); RNA SPLICE SITES; RNA SPLICING;

EID: 84974606803     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006039     Document Type: Article

References (37)

1. Parada LF, Tabin CJ, Shih C, Weinberg RA, (1982) Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature297: 474–478. 6283357
2. Reddy EP, Reynolds RK, Santos E, Barbacid M, (1982) A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma oncogene. Nature300: 149–152. 7133135
3. Tabin CJ, Bradley SM, Bargmann CI, Weinberg RA, Papageorge AG, et al. (1982) Mechanism of activation of a human oncogene. Nature300: 143–149. 6290897
4. Colby WW, Hayflick JS, Clark SG, Levison AD, (1986) Biochemical characterization of polypeptides encoded by mutated human Ha-ras1 genes. Mol Cell Biol6(2): 730–734. 3537694
5. Seeburg PH, Colby WW, Capon DJ, Goeddel DV, Levinson AD, (1984) Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature312: 71–75. 6092966
6. Fasano O, Aldrich T, Tamanoi F, Taparowsky E, Furth M, et al. (1984) Analysis of the transforming potential of the human H-ras gene by random mutagenesis. Proc Nat Acad Sci USA81: 4008–4012. 6330729
7. Gripp KW, Lin AE, Stabley DL, Nicholson L, Scott CI, Jret al. (2006) HRAS mutation analysis in Costello syndrome: genotype and phenotype correlation. Am J Med Genet140A: 1–7.
8. Giannoulatou E, McVean G, Taylor IB, McGowan SJ, Maher GJ, et al. (2013) Contributions of intrinsic mutation rate and selfish selection to levels of de novo HRAS mutations in the paternal germline. Proc Natl Acad Sci USA110: 20152–20157. doi: 10.1073/pnas.131138111024259709
9. Aoki Y, Niihori T, Kawame H, Kurosawa K, Ohashi H, et al. (2005) Germline mutations in HRAS proto-oncogene cause Costello syndrome. Nat Genet37: 1038–1040. 16170316
10. Burkitt-Wright EM, Bradley L, Shorto J, McConnell VP, Gannon C, et al. (2012) Neonatal lethal Costello syndrome and unusual dinucleotide deletion/insertion mutations in HRAS predicting p.Gly12Val. Am J Med Genet A158A: 1102–1110. doi: 10.1002/ajmg.a.3529622495892
11. Lo IFM, Brewer C, Shannon N, Shorto J, Tang B, (2008) Severe neonatal manifestations of Costello syndrome. J Med Genet45: 167–171. 18039947
12. Lorenz S, Petersen C, Kordaß U, Seidel H, Zenker M, et al. (2012) Two cases with severe lethal course of Costello syndrome associated with HRAS p.G12C and p.G12D. Eur J Med Genet55: 615–619. doi: 10.1016/j.ejmg.2012.07.00722926243
13. Wang GS, Cooper TA, (2007) Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet8(10): 749–761. 17726481
14. Supek F, Miñana B, Valcárcel J, Gabaldón T, Lehner B, (2014) Synonymous mutations frequently act as driver mutations in human cancers. Cell156: 1324–1335. doi: 10.1016/j.cell.2014.01.05124630730
15. Kim E, Ilagan JO, Liang Y, Daubner GM, Lee SC, et al. (2015) SRSF2 Mutations Contribute to Myelodysplasia by Mutant-Specific Effects on Exon Recognition. Cancer Cell27: 617–630. doi: 10.1016/j.ccell.2015.04.00625965569
16. Karni R, de Stanchina E, Lowe SW, Sinha R, Mu D, et al. (2007) The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat Struct Mol Biol14: 185–193. 17310252
17. Jia R, Li C, McCoy JP, Deng CX, Zheng ZM, (2010) SRp20 is a proto-oncogene critical for cell proliferation and tumor induction and maintenance. Int J Biol Sci6: 806–826. 21179588
18. Cohen-Eliav M, Golan-Gerstl R, Siegfried Z, Andersen CL, Thorsen K, et al. (2013) The splicing factor SRSF6 is amplified and is an oncoprotein in lung and colon cancers. J Pathol229: 630–639. doi: 10.1002/path.412923132731
19. Nielsen KB, Sørensen S, Cartegni L, Corydon TJ, Doktor TK, et al. (2007) Seemingly Neutral Polymorphic Variations May Confer Immunity to Splicing-Inactivating Mutations: A synonymous SNP in Exon 5 of MCAD Protects from Deleterious Mutations in a flaking Exonic Splicing Enhancer. Am J Hum Genet80: 416–432. 17273963
20. Manley JL, Krainer AR, (2010) A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins). Genes Dev24: 1073–1074. doi: 10.1101/gad.193491020516191
21. Dreyfuss G, Kim VN, Kataoka N, (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol3: 195–205. 11994740
22. Matern D, He M, Berry SA, Rinaldo P, Whitley CB, et al. (2003) Prospective diagnosis of 2-methylbutyryl-CoA dehydrogenase deficiency in the Hmong population by newborn screening using tandem mass spectrometry. Pediatrics112: 74–78. 12837870
23. Santoro M, Modoni A, Sabatelli M, Madia F, Piemonte F, et al. (2007) Chronic GM2 gangliosidosis type Sandhoff associated with a novel missense HEXB gene mutation causing a double pathogenic effect. Mol Genet Metab91: 111–114. 17251047
24. Theophilus BD, Enayat MS, Williams MD, Hill FG, (2001) Site and type of mutations in the factor VIII gene in patients and carriers of haemophilia A. Haemophilia7: 381–91. 11442643
25. Masuda A, Shen XM, Ito M, Matsuura T, Engel AG, et al. (2008) hnRNP H enhances skipping of a nonfunctional exon P3A in CHRNA1 and a mutation disrupting its binding causes congenital myasthenic syndrome. Hum Mol Genet17: 4022–4035. doi: 10.1093/hmg/ddn30518806275
26. Dobrowolski SF, Andersen HS, Doktor TK, Andresen BS, (2010) The phenylalanine hydroxylase c.30C>G synonymous variation (p.G10G) creates a common exonic splicing silencer. Mol Genet Metab100: 316–323. doi: 10.1016/j.ymgme.2010.04.00220457534
27. Talukdar I, Sen S, Urbano R, Thompson J, Yates JR, 3rdet al. (2011) hRNP A1 and hnRNP F modulate the alternative splicing of exon 11 of the insulin receptor gene. PLoS One6: e27869. doi: 10.1371/journal.pone.002786922132154
28. Olsen RK, Brøner S, Sabaratnam R, Doktor TK, Andersen HS, et al. (2014) The ETFDH c.158A>G Variation Disrupts the Balanced Interplay of ESE- and ESS-Binding Proteins thereby Causing Missplicing and Multiple Acyl-CoA Dehydrogenation Deficiency. Hum Mutat35: 86–95. doi: 10.1002/humu.2245524123825
29. Schaub MC, Lopez SR, Caputi M, (2007) Members of the heterogeneous nuclear ribonucleoprotein H family activate splicing of an HIV-1 splicing substrate by promoting formation of ATP-dependent spliceosomal complexes. J Biol Chem282: 13617–13626. 17337441
30. Coulter LR, Landree MA, Cooper TA, (1997) Identification of a new class of exonic splicing enhancers by in vivo selection. Mol Cell Biol17: 2143–2150. 9121463
31. Singh G, Cooper TA, (2006) Minigene reporter for identification and analysis of cis elements and trans factors affecting pre-mRNA splicing. BioTechniques41: 177–181. 16925019
32. Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR, (2003) ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res31: 3568–3571. 12824367
33. Ellis PD, Smith CW, Kemp P, (2004) Regulated tissue-specific alternative splicing of enhanced green fluorescent protein transgenes conferred by a-tropomyosin regulatory elements in transgenic mice. J Biol Chem279: 36660–36669. 15194683
34. Rimoldi V, Soldà G, Asselta R, Spena S, Stuani C, et al. (2013) Dual role of G-runs and hnRNP F in the regulation of a mutation-activated pseudoexon in the fibrinogen gamma-chain transcript. PLoS One8:e59333. doi: 10.1371/journal.pone.005933323533617
35. Bauman JA, Li SD, Yang A, Huang L, Kole R, (2010) Anti-tumor activity of splice-switching oligonucleotides. Nucleic Acids Res38: 8348–8356. doi: 10.1093/nar/gkq73120719743
36. Zammarchi F, de Stanchina E, Bournazou E, Supakorndej T, Martires K, et al. (2011) Antitumorigenic potential of STAT3 alternative splicing modulation. Proc Natl Acad Sci USA108: 17779–17784. doi: 10.1073/pnas.110848210822006329
37. Dewaele M, Tabaglio T, Willekens K, Bezzi M, Teo SX, et al. (2016) Antisense oligonucleotide-mediated MDM4 exon 6 skipping impairs tumor growth. J Clin Invest126: 68–84. doi: 10.1172/JCI8253426595814