RNA-Seq analysis of Gtf2ird1 knockout epidermal tissue provides potential insights into molecular mechanisms underpinning Williams-Beuren syndrome

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Corley, Susan M ^a   Canales, Cesar P ^a   Carmona Mora, Paulina ^a   Mendoza Reinosa, Veronica ^a   Beverdam, Annemiek ^a   Hardeman, Edna C ^a   Wilkins, Marc R ^a   Palmer, Stephen J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Neurodevelopmental disorder; RNA Seq; Transcriptomics; Williams Beuren syndrome

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR HEY1; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR MYF6; TRANSCRIPTION FACTOR MYOG; TRANSCRIPTION FACTOR POU3F3; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; GTF2IRD1 PROTEIN, MOUSE; MUSCLE PROTEIN; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENT; DOWN REGULATION; EPIDERMIS; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INTERACTION; GENE ONTOLOGY; GTF2IRD1 GENE; MOLECULAR MODEL; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SKIN DEVELOPMENT; UPREGULATION; VALIDATION PROCESS; WILLIAMS BEUREN SYNDROME; WNT SIGNALING PATHWAY; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CLUSTER ANALYSIS; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDY; GENETICS; HIGH THROUGHPUT SEQUENCING; KNOCKOUT MOUSE; METABOLISM; PHENOTYPE; PROCEDURES; REPRODUCIBILITY; SIGNAL TRANSDUCTION; WILLIAMS SYNDROME;

ANIMALS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DISEASE MODELS, ANIMAL; EPIDERMIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETIC ASSOCIATION STUDIES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUSCLE PROTEINS; NUCLEAR PROTEINS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; WILLIAMS SYNDROME;

EID: 84978044238     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2801-4     Document Type: Article

References (70)

1. Osborne LR, Mervis CB. Rearrangements of the Williams-Beuren syndrome locus: molecular basis and implications for speech and language development. Expert Rev Mol Med. 2007;9(15):1-16.
2. Antonell A, Del Campo M, Magano LF, Kaufmann L, de la Iglesia JM, Gallastegui F, Flores R, Schweigmann U, Fauth C, Kotzot D, et al. Partial 7q11.23 deletions further implicate GTF2I and GTF2IRD1 as the main genes responsible for the Williams-Beuren syndrome neurocognitive profile. J Med Genet. 2010;47(5):312-20.
3. Enkhmandakh B, Makeyev AV, Erdenechimeg L, Ruddle FH, Chimge NO, Tussie-Luna MI, et al. Essential functions of the Williams-Beuren syndrome-associated TFII-I genes in embryonic development. Proc Natl Acad Sci U S A. 2009;106(1):181-6.
4. Lucena J, Pezzi S, Aso E, Valero MC, Carreiro C, Dubus P, Sampaio A, Segura M, Barthelemy I, Zindel MY, et al. Essential role of the N-terminal region of TFII-I in viability and behavior. BMC Med Genet. 2010;11:61.
5. Young EJ, Lipina T, Tam E, Mandel A, Clapcote SJ, Bechard AR, Chambers J, Mount HT, Fletcher PJ, Roder JC, et al. Reduced fear and aggression and altered serotonin metabolism in Gtf2ird1-targeted mice. Genes Brain Behav. 2008;7(2):224-34.
6. Howard ML, Palmer SJ, Taylor KM, Arthurson GJ, Spitzer MW, Du X, et al. Mutation of Gtf2ird1 from the Williams-Beuren syndrome critical region results in facial dysplasia, motor dysfunction, and altered vocalisations. Neurobiol Dis. 2012;45(3):913-22.
7. Schneider T, Skitt Z, Liu Y, Deacon RM, Flint J, Karmiloff-Smith A, Rawlins JN, Tassabehji M. Anxious, hypoactive phenotype combined with motor deficits in Gtf2ird1 null mouse model relevant to Williams syndrome. Behav Brain Res. 2012;233(2):458-73.
8. Tassabehji M, Hammond P, Karmiloff-Smith A, Thompson P, Thorgeirsson SS, Durkin ME, Popescu NC, Hutton T, Metcalfe K, Rucka A, et al. GTF2IRD1 in craniofacial development of humans and mice. Science. 2005;310(5751):1184-7.
9. Palmer SJ, Tay ES, Santucci N, Cuc Bach TT, Hook J, Lemckert FA, Jamieson RV, Gunnning PW, Hardeman EC. Expression of Gtf2ird1, the Williams syndrome-associated gene, during mouse development. Gene Expr Patterns. 2007;7(4):396-404.
10. Canales CP, Wong AC, Gunning PW, Housley GD, Hardeman EC, Palmer SJ. The role of GTF2IRD1 in the auditory pathology of Williams-Beuren Syndrome. Eur J Hum Genet. 2015;23(6):774-80.
11. Polly P, Haddadi LM, Issa LL, Subramaniam N, Palmer SJ, Tay ES, Hardeman EC. hMusTRD1alpha1 represses MEF2 activation of the troponin I slow enhancer. J Biol Chem. 2003;278(38):36603-10.
12. Vullhorst D, Buonanno A. Multiple GTF2I-like repeats of general transcription factor 3 exhibit DNA binding properties. Evidence for a common origin as a sequence-specific DNA interaction module. J Biol Chem. 2005;280(36):31722-31.
13. Issa LL, Palmer SJ, Guven KL, Santucci N, Hodgson VR, Popovic K, Joya JE, Hardeman EC. MusTRD can regulate postnatal fiber-specific expression. Dev Biol. 2006;293(1):104-15.
14. Palmer SJ, Santucci N, Widagdo J, Bontempo SJ, Taylor KM, Tay ES, Hook J, Lemckert F, Gunning PW, Hardeman EC. Negative autoregulation of GTF2IRD1 in Williams-Beuren syndrome via a novel DNA binding mechanism. J Biol Chem. 2010;285(7):4715-24.
15. O'Leary J, Osborne LR. Global analysis of gene expression in the developing brain of Gtf2ird1 knockout mice. PLoS One. 2011;6(8):e23868.
16. Chimge NO, Mungunsukh O, Ruddle F, Bayarsaihan D. Expression profiling of BEN regulated genes in mouse embryonic fibroblasts. J Exp Zool B Mol Dev Evol. 2007;308(3):209-24.
17. Chimge NO, Makeyev AV, Ruddle FH, Bayarsaihan D. Identification of the TFII-I family target genes in the vertebrate genome. Proc Natl Acad Sci U S A. 2008;105(26):9006-10.
18. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139-40.
19. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
20. Peukert D, Weber S, Lumsden A, Scholpp S. Lhx2 and Lhx9 determine neuronal differentiation and compartition in the caudal forebrain by regulating Wnt signaling. PLoS Biol. 2011;9(12):e1001218.
21. Rhee H, Polak L, Fuchs E. Lhx2 maintains stem cell character in hair follicles. Science. 2006;312(5782):1946-9.
22. Beer HD, Bittner M, Niklaus G, Munding C, Max N, Goppelt A, Werner S. The fibroblast growth factor binding protein is a novel interaction partner of FGF-7, FGF-10 and FGF-22 and regulates FGF activity: implications for epithelial repair. Oncogene. 2005;24(34):5269-77.
23. Miyazono K, Kamiya Y, Morikawa M. Bone morphogenetic protein receptors and signal transduction. Am J Biochem. 2010;147(1):35-51.
24. Croce JC, McClay DR. Evolution of the Wnt pathways. Methods Mol Biol. 2008;469:3-18.
25. Doi T, Puri P, Bannigan J, Thompson J. Disruption of noncanonical Wnt/CA2+ pathway in the cadmium-induced omphalocele in the chick model. J Pediatr Surg. 2010;45(8):1645-9.
26. Ouji Y, Yoshikawa M, Shiroi A, Ishizaka S. Wnt-10b secreted from lymphocytes promotes differentiation of skin epithelial cells. Biochem Biophys Res Commun. 2006;342(4):1063-9.
27. Carmona-Mora P, Widagdo J, Tomasetig F, Canales CP, Cha Y, Lee W, Alshawaf A, Dottori M, Whan RM, Hardeman EC, et al. The nuclear localization pattern and interaction partners of GTF2IRD1 demonstrate a role in chromatin regulation. Hum Genet. 2015;134(10):1099-115.
28. Peterson LF, Boyapati A, Ranganathan V, Iwama A, Tenen DG, Tsai S, Tsai S, Zhang DE. The hematopoietic transcription factor AML1 (RUNX1) is negatively regulated by the cell cycle protein cyclin D3. Mol Cell Biol. 2005;25(23):10205-19.
29. Zong H, Chi Y, Wang Y, Yang Y, Zhang L, Chen H, Jiang J, Li Z, Hong Y, Wang H, et al. Cyclin D3/CDK11p58 complex is involved in the repression of androgen receptor. Mol Cell Biol. 2007;27(20):7125-42.
30. Sarruf DA, Iankova I, Abella A, Assou S, Miard S, Fajas L. Cyclin D3 promotes adipogenesis through activation of peroxisome proliferator-activated receptor gamma. Mol Cell Biol. 2005;25(22):9985-95.
31. Despouy G, Bastie JN, Deshaies S, Balitrand N, Mazharian A, Rochette-Egly C, Chomienne C, Delva L. Cyclin D3 is a cofactor of retinoic acid receptors, modulating their activity in the presence of cellular retinoic acid-binding protein II. J Biol Chem. 2003;278(8):6355-62.
32. Jian Y, Yan J, Wang H, Chen C, Sun M, Jiang J, Lu J, Yang Y, Gu J. Cyclin D3 interacts with vitamin D receptor and regulates its transcription activity. Biochem Biophys Res Commun. 2005;335(3):739-48.
33. Weiss A, Attisano L. The TGFbeta superfamily signaling pathway. Wiley Interdiscip Rev Dev Biol. 2013;2(1):47-63.
34. Ichimura T, Watanabe S, Sakamoto Y, Aoto T, Fujita N, Nakao M. Transcriptional repression and heterochromatin formation by MBD1 and MCAF/AM family proteins. J Biol Chem. 2005;280(14):13928-35.
35. Sasai N, Saitoh N, Saitoh H, Nakao M. The transcriptional cofactor MCAF1/ATF7IP is involved in histone gene expression and cellular senescence. PLoS One. 2013;8(7), e68478.
36. Piao L, Nakagawa H, Ueda K, Chung S, Kashiwaya K, Eguchi H, Ohigashi H, Ishikawa O, Daigo Y, Matsuda K, et al. C12orf48, termed PARP-1 binding protein, enhances poly(ADP-ribose) polymerase-1 (PARP-1) activity and protects pancreatic cancer cells from DNA damage. Genes Chromosomes Cancer. 2011;50(1):13-24.
37. Alshareeda AT, Negm OH, Green AR, Nolan CC, Tighe P, Albarakati N, et al. KPNA2 is a nuclear export protein that contributes to aberrant localisation of key proteins and poor prognosis of breast cancer. Br J Cancer. 2015;112(12):1929-37.
38. Follit JA, San Agustin JT, Xu F, Jonassen JA, Samtani R, Lo CW, Pazour GJ. The Golgin GMAP210/TRIP11 anchors IFT20 to the Golgi complex. PLoS Genet. 2008;4(12), e1000315.
39. Infante C, Ramos-Morales F, Fedriani C, Bornens M, Rios RM. GMAP-210, A cis-Golgi network-associated protein, is a minus end microtubule-binding protein. J Cell Biol. 1999;145(1):83-98.
40. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-8.
41. Henrichsen CN, Csardi G, Zabot MT, Fusco C, Bergmann S, Merla G, Reymond A. Using transcription modules to identify expression clusters perturbed in Williams-Beuren syndrome. PLoS Comput Biol. 2011;7(1), e1001054.
42. O'Mahoney JV, Guven KL, Lin J, Joya JE, Robinson CS, Wade RP, Hardeman EC. Identification of a novel slow-muscle-fiber enhancer binding protein, MusTRD1. Mol Cell Biol. 1998;18(11):6641-52.
43. Tantin D, Tussie-Luna MI, Roy AL, Sharp PA. Regulation of immunoglobulin promoter activity by TFII-I class transcription factors. J Biol Chem. 2004;279(7):5460-9.
44. Yan X, Zhao X, Qian M, Guo N, Gong X, Zhu X. Characterization and gene structure of a novel retinoblastoma-protein-associated protein similar to the transcription regulator TFII-I. Biochem J. 2000;345(Pt 3):749-57.
45. Tussie-Luna MI, Bayarsaihan D, Seto E, Ruddle FH, Roy AL. Physical and functional interactions of histone deacetylase 3 with TFII-I family proteins and PIASxbeta. Proc Natl Acad Sci U S A. 2002;99(20):12807-12.
46. Folgueras AR, Guo X, Pasolli HA, Stokes N, Polak L, Zheng D, Fuchs E. Architectural niche organization by LHX2 is linked to hair follicle stem cell function. Cell Stem Cell. 2013;13(3):314-27.
47. Mardaryev AN, Meier N, Poterlowicz K, Sharov AA, Sharova TY, Ahmed MI, Rapisarda V, Lewis C, Fessing MY, Ruenger TM, et al. Lhx2 differentially regulates Sox9, Tcf4 and Lgr5 in hair follicle stem cells to promote epidermal regeneration after injury. Development. 2011;138(22):4843-52.
48. Birk E, Har-Zahav A, Manzini CM, Pasmanik-Chor M, Kornreich L, Walsh CA, Noben-Trauth K, Albin A, Simon AJ, Colleaux L, et al. SOBP is mutated in syndromic and nonsyndromic intellectual disability and is highly expressed in the brain limbic system. Am J Hum Genet. 2010;87(5):694-700.
49. Godoy JA, Rios JA, Zolezzi JM, Braidy N, Inestrosa NC. Signaling pathway cross talk in Alzheimer's disease. Cell Commun Signal. 2014;12:23.
50. Collu GM, Hidalgo-Sastre A, Brennan K. Wnt-Notch signalling crosstalk in development and disease. Cell Mol Life Sci. 2014;71(18):3553-67.
51. Katoh M, Katoh M. Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther. 2006;5(9):1059-64.
52. Itoh N, Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem. 2011;149(2):121-30.
53. Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer. 2010;10(2):116-29.
54. Yun YR, Won JE, Jeon E, Lee S, Kang W, Jo H, Jang JH, Shin US, Kim HW. Fibroblast growth factors: biology, function, and application for tissue regeneration. J Tissue Eng. 2010;2010:218142.
55. van Scheltinga AF T, Bakker SC, Kahn RS, Kas MJ. Fibroblast growth factors in neurodevelopment and psychopathology. Neuroscientist. 2013;19(5):479-94.
56. Stevens HE, Smith KM, Maragnoli ME, Fagel D, Borok E, Shanabrough M, Horvath TL, Vaccarino FM. Fgfr2 is required for the development of the medial prefrontal cortex and its connections with limbic circuits. J Neurosci. 2010;30(16):5590-602.
57. Yamanaka Y, Kitano A, Takao K, Prasansuklab A, Mushiroda T, Yamazaki K, Kumada T, Shibata M, Takaoka Y, Awaya T, et al. Inactivation of fibroblast growth factor binding protein 3 causes anxiety-related behaviors. Mol Cell Neurosci. 2011;46(1):200-12.
58. Szebenyi G, Fallon JF. Fibroblast growth factors as multifunctional signaling factors. Int Rev Cytol. 1999;185:45-106.
59. Bikle DD, Xie Z, Tu CL. Calcium regulation of keratinocyte differentiation. Expert Rev Endocrinol Metab. 2012;7(4):461-72.
60. Kim J, Kim J, Kim DW, Ha Y, Ihm MH, Kim H, Song K, Lee I. Wnt5a induces endothelial inflammation via beta-catenin-independent signaling. J Immunol. 2010;185(2):1274-82.
61. Flavell SW, Greenberg ME. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci. 2008;31:563-90.
62. Rosso SB, Inestrosa NC. WNT signaling in neuronal maturation and synaptogenesis. Front Cell Neurosci. 2013;7:103.
63. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E. Oxytocin increases trust in humans. Nature. 2005;435(7042):673-6.
64. Dai L, Carter CS, Ying J, Bellugi U, Pournajafi-Nazarloo H, Korenberg JR. Oxytocin and vasopressin are dysregulated in Williams Syndrome, a genetic disorder affecting social behavior. PLoS One. 2012;7(6), e38513.
65. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14(4):R36.
66. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357-9.
67. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11(3):R25.
68. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T. A travel guide to Cytoscape plugins. Nat Methods. 2012;9(11):1069-76.
69. Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6(7), e21800.
70. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-50.