Disruption of SATB2 or its long-range cis-regulation by SOX9 causes a syndromic form of Pierre Robin sequence

Human Molecular Genetics

Volumn 23, Issue 10, 2014, Pages 2569-2579

  Rainger, Jacqueline K ^a   Bhatia, Shipra ^a   Bengani, Hemant ^a   Gautier, Philippe ^a   Rainger, Joe ^a   Pearson, Matt ^a   Ansari, Morad ^a   Crow, Jayne ^b   Mehendale, Felicity ^c   Palinkasova, Bozena ^d   Dixon, Michael J ^d   Thompson, Pamela J ^e,f   Matarin, Mar ^e   Sisodiya, Sanjay M ^e,f   Kleinjan, Dirk A ^a   Fitzpatrick, David R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b NHS LOTHIAN   (United Kingdom)

^c ROYAL HOSPITAL FOR SICK CHILDREN   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^f EPILEPSY SOCIETY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; DNA BINDING PROTEIN; HISTONE H3; HISTONE H3K4; PROTEIN PLCL1; PROTEIN SATB2; SPACER DNA; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; MATRIX ATTACHMENT REGION BINDING PROTEIN; SATB2 PROTEIN, HUMAN; SOX9 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADULT; AGGRESSION; ANIMAL CELL; ANOPHTHALMIA; ANTERIOR COMMISSURE; APRAXIA; ARACHNODACTYLY; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BINDING SITE; CASE REPORT; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME 11; CHROMOSOME 2Q; CLEFT PALATE; COMPARATIVE GENOMIC HYBRIDIZATION; COMPUTER MODEL; CONTROLLED STUDY; COPY NUMBER VARIATION; ENHANCER REGION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE IDENTIFICATION; GENE TARGETING; HEMISPHERE; HUMAN; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; INTERPHASE; LATERAL BRAIN VENTRICLE; LEARNING DISORDER; LOSS OF FUNCTION MUTATION; MALE; METAPHASE; MICROGNATHIA; MICROPHTHALMIA; MICROSTOMIA; MOUTH MALFORMATION; NEUROPSYCHOLOGY; NONHUMAN; NOSE MALFORMATION; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODONTIA; PATHOGENESIS; PHENOTYPE; PIERRE ROBIN SYNDROME; POLYADENYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RECIPROCAL CHROMOSOME TRANSLOCATION; WORKING MEMORY; ZEBRA FISH; ANIMAL; CELL CULTURE; CHILD; EPISTASIS; GENETICS; INFANT; MOUSE; MUTATION; PRESCHOOL CHILD; REGULATORY SEQUENCE; YOUNG ADULT;

ADULT; ANIMALS; BINDING SITES; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; EPISTASIS, GENETIC; FEMALE; HUMANS; INFANT; MALE; MATRIX ATTACHMENT REGION BINDING PROTEINS; MICE; MUTATION; PIERRE ROBIN SYNDROME; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; YOUNG ADULT; ZEBRAFISH;

EID: 84898800698     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt647     Document Type: Article

References (46)

1. Robin, P. (1923) La chute de la base de la langue consideree comme une nouvelle cause de gene dans la respiration naso-pharyngienne. Bull. Acad. Med. Paris, 89, 37-41.
2. Robin, P. (1934) Glossoptosis due to atresia and hypotrophy of the mandible. Arch. Pediatr. Adolesc. Med., 48, 541.
3. Warkany, J. (1971) Congenital malformations. 655, Year Book Medical Publishers, Chicago, IL.
4. Lee, K.H. and Hayward, P. (2008) Retrospective review of Stickler syndrome patients with cleft palate 1997-2004. ANZ J. Surg., 78, 764-766.
5. Marques, I.L., Barbieri, M.A. and Bettiol, H. (1998) Etiopathogenesis of isolated Robin sequence. Cleft Palate Craniofac. J., 35, 517-525.
6. Sheffield, L.J., Reiss, J.A., Strohm, K. and Gilding, M. (1987) A genetic follow-up study of 64 patients with the Pierre Robin complex. Am. J. Med. Genet., 28, 25-36.
7. Benko, S., Fantes, J.A., Amiel, J., Kleinjan, D.J., Thomas, S., Ramsay, J., Jamshidi, N., Essafi, A., Heaney, S., Gordon, C.T. et al. (2009) Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nat. Genet., 41, 359-364.
8. Bridgewater, L.C., Lefebvre, V. and de Crombrugghe, B. (1998) Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J. Biol. Chem., 273, 14998-15006.
9. Brewer, C.M., Leek, J.P., Green, A.J., Holloway, S., Bonthron, D.T., Markham, A.F. and Fitz Patrick, D.R. (1999) Alocus for isolated cleft palate, located on human chromosome 2q32. Am. J. Hum. Genet., 65, 387-396.
10. FitzPatrick, D.R., Carr, I.M., McLaren, L., Leek, J.P., Wightman, P., Williamson, K., Gautier, P., McGill, N., Hayward, C., Firth, H. et al. (2003) Identification of SATB2 as the cleft palate gene on 2q32-q33. Hum. Mol. Genet., 12, 2491-2501.
11. Tegay, D.H., Chan, K.K., Leung, L., Wang, C., Burkett, S., Stone, G., Stanyon, R., Toriello, H.V. and Hatchwell, E. (2009) Toriello-Carey syndrome in a patient with a de novo balanced translocation [46, XY, t(2;14)(q33;q22)] interrupting SATB2. Clin. Genet., 75, 259-264.
12. Baptista, J., Mercer, C., Prigmore, E., Gribble, S.M., Carter, N.P., Maloney, V., Thomas, N.S., Jacobs, P.A. and Crolla, J.A. (2008) Breakpoint mapping and arrayCGHin translocations: comparison of a phenotypically normal and an abnormal cohort. Am. J. Hum. Genet., 82, 927-936.
13. Balasubramanian, M., Smith, K., Basel-Vanagaite, L., Feingold, M.F., Brock, P., Gowans, G.C., Vasudevan, P.C., Cresswell, L., Taylor, E.J., Harris, C.J. et al. (2011) Case series: 2q33.1 microdeletion syndrome-further delineation of the phenotype. J. Med. Genet., 48, 290-298.
14. Urquhart, J., Black, G.C. and Clayton-Smith, J. (2009) 4.5Mbmicrodeletion in chromosome band 2q33.1 associated with learning disability and cleft palate. Eur. J. Med. Genet., 52, 454-457.
15. Van Buggenhout, G., Van Ravenswaaij-Arts, C., Mc Maas, N., Thoelen, R., Vogels, A., Smeets, D., Salden, I., Matthijs, G., Fryns, J.P. and Vermeesch, J.R. (2005) The del(2)(q32.2q33) deletion syndrome defined by clinical and molecular characterization of four patients. Eur. J. Med. Genet., 48, 276-289.
16. Rosenfeld, J.A., Ballif, B.C., Lucas, A., Spence, E.J., Powell, C., Aylsworth, A.S., Torchia, B.A. and Shaffer, L.G. (2009) Small deletions of SATB2 cause some of the clinical features of the 2q33.1 microdeletion syndrome. PLoS ONE, 4, e6568.
17. Leoyklang, P., Suphapeetiporn, K., Siriwan, P., Desudchit, T., Chaowanapanja, P., Gahl, W.A. and Shotelersuk, V. (2007) Heterozygous nonsense mutation SATB2 associated with cleft palate, osteoporosis, and cognitive defects. Hum. Mutat., 28, 732-738.
18. Dobreva, G., Dambacher, J. and Grosschedl, R. (2003) SUMO modification of a novel MAR-binding protein, SATB2, modulates immunoglobulin mu gene expression. Genes Dev., 17, 3048-3061.
19. Dobreva, G., Chahrour, M., Dautzenberg, M., Chirivella, L., Kanzler, B., Farinas, I., Karsenty, G. and Grosschedl, R. (2006) SATB2 is a multifunctional determinant of craniofacial patterning and osteoblast differentiation. Cell, 125, 971-986.
20. Alcamo, E.A., Chirivella, L., Dautzenberg, M., Dobreva, G., Farinas, I., Grosschedl, R. and McConnell, S.K. (2008) Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron, 57, 364-377.
21. Fishell, G. and Hanashima, C. (2008) Pyramidal neuronsgrowup and change their mind. Neuron, 57, 333-338.
22. Kolzer, S., Fuss, B., Hoch, M. and Klein, T. (2003) Defective proventriculus is required for pattern formation along the proximodistal axis, cell proliferation and formation of veins in the Drosophila wing. Development, 130, 4135-4147.
23. Shirai, T., Yorimitsu, T., Kiritooshi, N., Matsuzaki, F. and Nakagoshi, H. (2007) Notch signaling relieves the joint-suppressive activity of defective proventriculus in the Drosophila leg. Dev. Biol., 312, 147-156.
24. Yorimitsu, T., Kiritooshi, N. and Nakagoshi, H. (2011) Defective proventriculus specifies the ocellar region in the Drosophila head. Dev. Biol., 356, 598-607.
25. Fantes, J.A., Boland, E., Ramsay, J., Donnai, D., Splitt, M., Goodship, J.A., Stewart, H., Whiteford, M., Gautier, P., Harewood, L. et al. (2008) FISH mapping of de novo apparently balanced chromosome rearrangements identifies characteristics associated with phenotypic abnormality. Am. J. Hum. Genet., 82, 916-926.
26. Ragge, N.K., Lorenz, B., Schneider, A., Bushby, K., de Sanctis, L., de Sanctis, U., Salt, A., Collin, J.R., Vivian, A.J., Free, S.L. et al. (2005) SOX2 anophthalmia syndrome. Am. J. Med. Genet. A, 135, 1-7. discussion 8.
27. Ghassibe-Sabbagh, M., Desmyter, L., Langenberg, T., Claes, F., Boute, O., Bayet, B., Pellerin, P., Hermans, K., Backx, L., Mansilla, M.A. et al. (2011) FAF1, a gene that is disrupted in cleft palate and has conserved function in zebrafish. Am. J. Hum. Genet., 88, 150-161.
28. Ghassibé, M.(2007) Fas-associated factor-1, a protein involved in apoptosis, causes cleft lip and palate. PhD Thesis. de Duve Institute.
29. Rauch, A., Wieczorek, D., Graf, E., Wieland, T., Endele, S., Schwarzmayr, T., Albrecht, B., Bartholdi, D., Beygo, J., Di Donato, N. et al. (2012) Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exomesequencing study. Lancet, 380, 1674-1682.
30. Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S.A., Flynn, R.A. and Wysocka, J. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature, 470, 279-283.
31. Oh, C.D., Maity, S.N., Lu, J.F., Zhang, J., Liang, S., Coustry, F., de Crombrugghe, B. and Yasuda, H. (2010) Identification of SOX9 interaction sites in the genome of chondrocytes. PLoS ONE, 5, e10113.
32. Kleinjan, D.J. and van Heyningen, V. (1998) Position effect in human genetic disease. Hum. Mol. Genet., 7, 1611-1618.
33. Roessler, E., Ward, D.E., Gaudenz, K., Belloni, E., Scherer, S.W., Donnai, D., Siegel-Bartelt, J., Tsui, L.C. and Muenke, M. (1997) Cytogenetic rearrangements involving the loss of the Sonic Hedgehog gene at 7q36 cause holoprosencephaly. Hum. Genet., 100, 172-181.
34. Clarke, S.L., VanderMeer, J.E., Wenger, A.M., Schaar, B.T., Ahituv, N. and Bejerano, G. (2012) Human developmental enhancers conserved between deuterostomes and protostomes. PLoS Genet., 8, e1002852.
35. Woolfe, A., Goodson, M., Goode, D.K., Snell, P., McEwen, G.K., Vavouri, T., Smith, S.F., North, P., Callaway, H., Kelly, K. et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol., 3, e7.
36. Visel, A., Blow, M.J., Li, Z., Zhang, T., Akiyama, J.A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F. et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature, 457, 854-858.
37. Schmidt, D., Wilson, M.D., Ballester, B., Schwalie, P.C., Brown, G.D., Marshall, A., Kutter, C., Watt, S., Martinez-Jimenez, C.P., Mackay, S. et al. (2010) Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science, 328, 1036-1040.
38. Chattopadhyay, S., Whitehurst, C.E. and Chen, J. (1998) A nuclear matrix attachment region upstream of the T cell receptor beta gene enhancer binds Cux/CDP and SATB1 and modulates enhancer-dependent reporter gene expression but not endogenous gene expression. J. Biol. Chem., 273, 29838-29846.
39. Gordon, C.T., Tan, T.Y., Benko, S., Fitzpatrick, D., Lyonnet, S. and Farlie, P.G. (2009) Long-range regulation at the SOX9 locus in development and disease. J. Med. Genet., 46, 649-656.
40. Chong, S.S., Pack, S.D., Roschke, A.V., Tanigami, A., Carrozzo, R., Smith, A.C., Dobyns, W.B. and Ledbetter, D.H. (1997) A revision of the lissencephaly and Miller-Dieker syndrome critical regions in chromosome 17p13.3. Hum. Mol. Genet., 6, 147-155.
41. Chambeyron, S., Da Silva, N.R., Lawson, K.A. and Bickmore, W.A. (2005) Nuclear re-organisation of the Hoxb complex during mouse embryonic development. Development, 132, 2215-2223.
42. Finlan, L.E., Sproul, D., Thomson, I., Boyle, S., Kerr, E., Perry, P., Ylstra, B., Chubb, J.R. and Bickmore, W.A. (2008) Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet., 4, e1000039.
43. Soutoglou, E. and Talianidis, I. (2002) Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science, 295, 1901-1904.
44. Sheehan-Rooney, K., Palinkasova, B., Eberhart, J.K. and Dixon, M.J. (2010) A cross-species analysis of Satb2 expression suggests deep conservation across vertebrate lineages. Dev. Dyn., 239, 3481-3491.
45. Thisse, C. and Thisse, B. (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc., 3, 59-69.
46. Ravi, V., Bhatia, S., Gautier, P., Loosli, F., Tay, B.H., Tay, A., Murdoch, E., Coutinho, P., van Heyningen, V., Brenner, S. et al. (2013) Sequencing of Pax6 loci from the elephant shark reveals a family of Pax6 genes in vertebrate genomes, forged by ancient duplications and divergences. PLoS Genet., 9, e1003177.