From whole gene deletion to point mutations of EP300-positive rubinstein-taybi patients: New insights into the mutational spectrum and peculiar clinical hallmarks

Human Mutation

Volumn 37, Issue 2, 2016, Pages 175-183

  Negri, Gloria ^a   Magini, Pamela ^b   Milani, Donatella ^c   Colapietro, Patrizia ^a   Rusconi, Daniela ^a   Scarano, Emanuela ^b   Bonati, Mariateresa ^d   Priolo, Manuela ^e   Crippa, Milena ^d   Mazzanti, Laura ^b   Wischmeijer, Anita ^b   Tamburrino, Federica ^b   Pippucci, Tommaso ^b   Finelli, Palma ^a,d   Larizza, Lidia ^a,d   Gervasini, Cristina ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^d ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^e BIANCHI MELACRINO MORELLI HOSPITAL   (Italy)

Author keywords

Deletion; EP300; Genotype phenotype correlation; RSTS; Rubinstein Taybi syndrome

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; GENOMIC DNA; GROWTH HORMONE; CREBBP PROTEIN, HUMAN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; EP300 PROTEIN, HUMAN;

ADOLESCENT; ADULT; ANXIETY DISORDER; ARTICLE; BRACHYCEPHALY; CASE REPORT; CHILD; CLINICAL ARTICLE; CLINICAL FEATURE; COLOBOMA; COMPARATIVE GENOMIC HYBRIDIZATION; CROWDING (TOOTH); DISEASE PREDISPOSITION; EXON; FEEDING DIFFICULTY; FEMALE; FOCAL EPILEPSY; FOLLOW UP; GENE DELETION; GENOTYPE PHENOTYPE CORRELATION; GROWTH HORMONE DEFICIENCY; HUMAN; HYPERTENSION; INTELLECTUAL IMPAIRMENT; INTRAUTERINE GROWTH RETARDATION; KELOID; KYPHOSIS; LANGUAGE DELAY; MALE; MALOCCLUSION; MICROCEPHALY; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; NEVUS; NUCLEOTIDE SEQUENCE; OBESITY; OTITIS; POINT MUTATION; PREGNANCY TOXEMIA; PRIORITY JOURNAL; RESPIRATORY TRACT INFECTION; RUBINSTEIN SYNDROME; SCHOOL CHILD; SCOLIOSIS; SKIN MANIFESTATION; SPONTANEOUS ABORTION; STEATOSIS; STRABISMUS; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENETIC ASSOCIATION STUDY; GENETIC VARIATION; GENETICS; HUMAN GENOME; MUTATION; PATHOLOGY; PHENOTYPE; YOUNG ADULT;

ADOLESCENT; CHILD; CREB-BINDING PROTEIN; E1A-ASSOCIATED P300 PROTEIN; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENOME, HUMAN; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MUTATION; PHENOTYPE; RUBINSTEIN-TAYBI SYNDROME; SEQUENCE ANALYSIS, DNA; YOUNG ADULT;

EID: 84949032396     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22922     Document Type: Article

References (58)

1. An Q, Burke GA, Dainton M, Harrison CJ, Kempski H, Konn Z, Myooren W, Stewart A, Taj M, Webb D, Strefford JC, Martineau M. 2010. Haploinsufficiency of the MLL and TOB2 genes in lymphoid malignancy. Leukemia 24:649-652.
2. Bartholdi D, Roelfsema JH, Papadia F, Breuning MH, Niedrist D, Hennekam RC, Schinzel A, Peters DJ. 2007. Genetic heterogeneity in Rubinstein-Taybi syndrome: delineation of the phenotype of the first patients carrying mutations in EP300. J Med Genet 44:327-333.
3. Bartsch O, Labonté J, Albrecht B, Wieczorek D, Lechno S, Zechner U, Haaf T. 2010. Two patients with EP300 mutations and facial dysmorphism different from the classic Rubinstein-Taybi syndrome. Am J Med Genet A 152A:181-184.
4. Bartsch O, Locher K, Meinecke P, Kress W, Seemanová E, Wagner A, Ostermann K, Rödel G. 2002. Molecular studies in 10 cases of Rubinstein-Taybi syndrome, including amild variant showing amissensemutation in codon 1175 of CREBBP. J Med Genet 39:496-501.
5. Bartsch O, Schmidt S, Richter M, Morlot S, Seemanová E, Wiebe G, Rasi S. 2005. DNA sequencing of CREBBP demonstrates mutations in 56% of patients with Rubinstein-Taybi syndrome (RSTS) and in another patient with incomplete RSTS. Hum Genöet 117:485-493.
6. Bartsch O, Wagner A, Hinkel GK, Krebs P, Stumm M, Schmalenberger B, Böhm S, Balci S, Majewski F. 1999. FISH studies in 45 patients with Rubinstein-Taybi syndrome: deletions associated with polysplenia, hypoplastic left heart and death in infancy. Eur J Hum Genet 7:748-756.
7. Beets L, Rodríguez-Fonseca C, Hennekam RC. 2014.Growth charts for individualswith Rubinstein-Taybi syndrome. Am J Med Genet A 164A:2300-2309.
8. Bentivegna A, Milani D, Gervasini C, Castronovo P, Mottadelli F, Manzini S, Colapietro P, Giordano L, Atzeri F, Divizia MT, Uzielli ML, Neri G, et al. 2006. Rubinstein-Taybi Syndrome: spectrum of CREBBP mutations in Italian patients. BMC Med Genet 7:77.
9. Bischoff FR, Krebber H, Kempf T, Hermes I, Ponstingl H. 1995. Human RanGTPaseactivating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport. Proc Natl Acad Sci USA 92:1749-1753.
10. Blough RI, Petrij F, Dauwerse JG, Milatovich-Cherry A, Weiss L, Saal HM, Rubinstein JH. 2000. Variation in microdeletions of the cyclic AMP-responsive elementbinding protein gene at chromosome band 16p13.3 in the Rubinstein-Taybi syndrome. Am J Med Genet 90:29-34.
11. Bounakis N, Karampalis C, Sharp H, Tsirikos AI. 2015. Surgical treatment of scoliosis in Rubinstein-Taybi syndrome type 2: a case report. J Med Case Rep 9:10.
12. Brunak S, Engelbrecht J, Knudsen S. 1991. Prediction of human mRNA donor and acceptor sites from the DNA sequence. J Mol Biol 220:49-65.
13. Chan HM, La Thangue NB. 2001. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci 114:2363-2373.
14. Coupry I, Roudaut C, Stef M, Delrue MA, Marche M, Burgelin I, Taine L, Cruaud C, Lacombe D, Arveiler B. 2002. Molecular analysis of the CBP gene in 60 patients with Rubinstein-Taybi syndrome. J Med Genet 39:415-421.
15. Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, Beroud C. 2009. Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 37:e67.
16. Drolet DW, Scully KM, Simmons DM, Wegner M, Chu KT, Swanson LW, Rosenfeld MG.1991.TEF, a transcription factor expressed specifically inthe anterior pituitary during embryogenesis, defines a new class of leucine zipper proteins. Genes Dev 5:1739-1753.
17. Foley P, Bunyan D, Stratton J, Dillon M, Lynch SA. 2009. Further case of Rubinstein-Taybi syndrome due to a deletion in EP300. Am J Med Genet A 149A:997-1000.
18. Galéra C, Taupiac E, Fraisse S, Naudion S, Toussaint E, Rooryck-Thambo C, Delrue MA, Arveiler B, Lacombe D, Bouvard MP. 2009. Socio-behavioral characteristics of children with Rubinstein-Taybi syndrome. J Autism Dev Disord 39:1252-1260.
19. Gervasini C, Castronovo P, Bentivegna A, Mottadelli F, Faravelli F, Giovannucci-Uzielli ML, Pessagno A, Lucci-Cordisco E, Pinto AM, Salviati L, Selicorni A, Tenconi R, et al. 2007. High frequency of mosaic CREBBP deletions in Rubinstein-Taybi syndrome patients and mapping of somatic and germ-line breakpoints. Genomics 90:567-573.
20. Gu W, Zhang F, Lupski JR. 2008. Mechanisms for human genomic rearrangements. Pathogenetics 1:4.
21. Harb M, Becker MM, Vitour D, Baron CH, Vende P, Brown SC, Bolte S, Arold ST, Poncet D. 2008.Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3with eIF4G and RoXaN. JVirol 82:11283-11293.
22. Hebsgaard PG, Korning N, Tolstrup J, Engelbrech P, Rouze S, Brunak S. 1996. Splice site prediction in Arabidopsis thaliana DNA by combining local and global sequence information. Nucleic Acids Res 24:3439-3452.
23. Hennekam RC. 2006. Rubinstein-Taybi syndrome. Eur J Hum Genet 14:981-985.
24. Kalkhoven E. 2004. CBP and p300: HATs for different occasions. Biochem Pharmacol 68:1145-1155.
25. Kline AD, Krantz ID, Sommer A, Kliewer M, Jackson LG, FitzPatrick DR, Levin AV, Selicorni A. 2007. Cornelia de Lange syndrome: clinical review, diagnostic and scoring systems, and anticipatory guidance. Am J Med Genet A 143A:1287-1296.
26. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, InternationalHuman Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
27. Lopez-Atalaya JP, Valor LM, Barco A. 2014. Epigenetic factors in intellectual disability: the Rubinstein-Taybi syndrome as a paradigm of neurodevelopmental disorder with epigenetic origin. Prog Mol Biol Transl Sci 128:139-176.
28. Marzuillo P, Grandone A, Coppola R, Cozzolino D, Festa A, Messa F, Luongo C, Del Giudice EM, Perrone L. 2013. Novel cAMP binding protein-BP (CREBBP) mutation in a girl with Rubinstein-Taybi syndrome, GH deficiency, Arnold Chiari malformation and pituitary hypoplasia. BMC Med Genet 14:28.
29. Masuda K, Akiyama K, Arakawa M, Nishi E, Kitazawa N, Higuchi T, Katou Y, Shirahige K, Izumi K. 2015. Exome sequencing identification of EP300 mutation in a proband with coloboma and imperforate anus: possible expansion of the phenotypic spectrum of Rubinstein-Taybi syndrome. Mol Syndromol 6:99-103.
30. Masuno M, Imaizumi K, Ishii T, Kuroki Y, Baba N, Tanaka Y. 1998. Pilomatrixomas in Rubinstein-Taybi syndrome. Am J Med Genet 77:81-82.
31. Milani D, Manzoni FM, Pezzani L, Ajmone P, Gervasini C, Menni F, Esposito S. 2015. Rubinstein-Taybi syndrome: clinical features, genetic basis, diagnosis, and management. Ital J Pediatr 41:4.
32. Miller RW, Rubinstein JH. 1995. Tumors in Rubinstein-Taybi syndrome. Am J Med Genet 56:112-115.
33. Murata T, Kurokawa R, Krones A, Tatsumi K, Ishii M, Taki T, Masuno M, Ohashi H, Yanagisawa M, Rosenfeld MG, Glass CK, Hayashi Y. 2001. Defect of histone acetyltransferase activity of the nuclear transcriptional coactivator CBP in Rubinstein-Taybi syndrome. Hum Mol Genet 10:1071-1076.
34. Negri G and Gervasini C. 2014. EP300 (E1A binding protein p300) Atlas Genet Cytogenet Oncol Haematol. Retrieved from http://atlasgeneticsoncology.org//Genes/P300ID97.html.
35. Negri G, Milani D, Colapietro P, Forzano F, Della Monica M, Rusconi D, Consonni L, Caffi LG, Finelli P, Scarano G, Magnani C, Selicorni A, et al. 2015 Clinical and molecular characterization of Rubinstein-Taybi syndrome patients carrying distinct novel mutations of the EP300 gene. Clin Genet 87:148-154.
36. Papathemeli D, Schulzendorff N, Kohlhase J, Göppner D, Franke I, Gollnick H. 2015. Pilomatricomas in Rubinstein-Taybi syndrome. J Dtsch Dermatol Ges 13:240-242.
37. Park E, Kim Y, Ryu H, Kowall NW, Lee J, Ryu H. 2014. Epigenetic mechanisms of Rubinstein-Taybi syndrome. Neuromolecular Med 16:16-24.
38. Petrij F, Dauwerse HG, Blough RI, Giles RH, van der Smagt JJ, Wallerstein R, Maaswinkel-Mooy PD, van Karnebeek CD, van Ommen GJ, van Haeringen A, Rubinstein JH, Saal HM, et al. 2000a. Diagnostic analysis of the Rubinstein-Taybi syndrome: five cosmids should be used for microdeletion detection and low number of protein truncating mutations. J Med Genet 37:168-176.
39. Petrij F, Dorsman JC, Dauwerse HG, Giles RH, Peeters T, Hennekam RC, Breuning MH, Peters DJ. 2000b. Rubinstein-Taybi syndrome caused by a de novo reciprocal translocation t(2;16)(q36.3;p13.3). Am J Med Genet 92:47-52.
40. Petrij F, Giles RH, Dauwerse HG, Saris JJ, Hennekam RC, Masuno M, Tommerup N, van Ommen GJ, Goodman RH, Peters DJ. 1995. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 376:348-351.
41. Roelfsema JH, White SJ, Ariyürek Y, Bartholdi D, Niedrist D, Papadia F, Bacino CA, den Dunnen JT, van Ommen GJ, Breuning MH, Hennekam RC, Peters DJ. 2005. Genetic heterogeneity in Rubinstein-Taybi syndrome: mutations in both the CBP and EP300 genes cause disease. Am J Hum Genet 76:572-580.
42. Rubinstein JH, Taybi H. 1963. Broad thumbs and toes and facial abnormalities. A possible mental retardation syndrome. Am J Dis Child 105:588-608.
43. Rusconi D, Negri G, Colapietro P, Picinelli C, Milani D, Spena S, Magnani C, Silengo MC, Sorasio L, Curtisova V, Cavaliere ML, Prontera P, et al. 2015. Characterization of 14 novel deletions underlying Rubinstein-Taybi syndrome: an update of the CREBBP deletion repertoire. Hum Genet 134:613-626.
44. Sharma N, Mali AM, Bapat SA. 2010. SpectrumofCREBBPmutations in Indian patients with Rubinstein-Taybi syndrome. J Biosci 35:187-202.
45. Solomon BD, Bodian DL, Khromykh A, Mora GG, Lanpher BC, Iyer RK, Baveja R, Vockley JG, Niederhuber JE. 2015. Expanding the phenotypic spectrum in EP300-related Rubinstein-Taybi syndrome. Am J Med Genet A 167:1111-1116.
46. Spena S, Milani D, Rusconi D, Negri G, Colapietro P, Elcioglu N, Bedeschi F, Pilotta A, Spaccini L, Ficcadenti A, Magnani C, Scarano G, et al. 2014. Insights into genotype-phenotype correlations from CREBBP point mutation screening in a cohort of 46 Rubinstein-Taybi syndrome patients. Clin Genet 88:431-440.
47. Stef M, Simon D, Mardirossian B, Delrue MA, Burgelin I, Hubert C, Marche M, Bonnet F, Gorry P, Longy M, Lacombe D, Coupry I, et al. 2007. Spectrum of CREBBP gene dosage anomalies in Rubinstein-Taybi syndrome patients. Eur J Hum Genet 15:843-847.
48. Tillgren V, Ho JC, Önnerfjord P, Kalamajski S. 2015. The novel small leucine-rich protein chondroadherin-like (CHADL) is expressed in cartilage and modulates chondrocyte differentiation. J Biol Chem 290:918-925.
49. Trojer P, Cao AR, Gao Z, Li Y, Zhang J, Xu X, Li G, Losson R, Erdjument-Bromage H, Tempst P, Farnham PJ, Reinberg D. 2011. L3MBTL2 protein acts in concert with PcG protein-mediated monoubiquitination of H2A to establish a repressive chromatin structure. Mol Cell 42:438-450.
50. Tsai AC, Dossett CJ, Walton CS, Cramer AE, Eng PA, Nowakowska BA, Pursley AN, Stankiewicz P, Wiszniewska J, Cheung SW. 2011. Exon deletions of the EP300 and CREBBP genes in two children with Rubinstein-Taybi syndrome detected by aCGH. Eur J Hum Genet 19:43-49.
51. Udaka T, Samejima H, Kosaki R, Kurosawa K, Okamoto N, Mizuno S, Makita Y, Numabe H, Toral JF, Takahashi T, Kosaki K. 2005. Comprehensive screening of CREB-binding protein gene mutations among patients with Rubinstein-Taybi syndrome using denaturing high-performance liquid chromatography. Congenit Anom (Kyoto) 45:125-131.
52. van Belzen M, Bartsch O, Lacombe D, Peters DJ, Hennekam RC. 2011.Rubinstein-Taybi syndrome (CREBBP, EP300). Eur J Hum Genet 19:121.
53. Viosca J, Lopez-Atalaya JP, Olivares R, Eckner R, Barco A. 2010. Syndromic features and mild cognitive impairment in mice with genetic reduction on p300 activity: Differential contribution of p300 andCBP toRubinstein-Taybi syndrome etiology. Neurobiol Dis 37:186-194.
54. Waite J, Moss J, Beck SR, Richards C, Nelson L, Arron K, Burbidge C, Berg K, Oliver C. 2015. Repetitive behavior in rubinstein-taybi syndrome: parallels with autism spectrum phenomenology. J Autism Dev Disord 45:1238-1253.
55. Winkler GS. 2010. The mammalian anti-proliferative BTG/Tob protein family. J Cell Physiol 222:66-72.
56. Wong MM, Byun JS, Sacta M, Jin Q, Baek S, Gardner K. 2014. Promoter-bound p300 complexes facilitate post-mitotic transmission of transcriptional memory. PLoS One 9:e99989.
57. Woods SA, Robinson HB, Kohler LJ, Agamanolis D, Sterbenz G, Khalifa M. 2013. Exome sequencing identifies a novel EP300 frame shiftmutation in a patient with features that overlap Cornelia de Lange syndrome. Am J Med Genet A 164A:251-258.
58. Zimmermann N, Acosta AM, Kohlhase J, Bartsch O. 2007. Confirmation of EP300 gene mutations as a rare cause of Rubinstein-Taybi syndrome. Eur J Hum Genet 15:837-842.