A LINE-1 Insertion in DLX6 Is Responsible for Cleft Palate and Mandibular Abnormalities in a Canine Model of Pierre Robin Sequence

PLoS Genetics

Volumn 10, Issue 4, 2014, Pages

  Wolf, Zena T ^a   Leslie, Elizabeth J ^b   Arzi, Boaz ^c   Jayashankar, Kartika ^a   Karmi, Nili ^a   Jia, Zhonglin ^b,d   Rowland, Douglas J ^a   Young, Amy ^a   Safra, Noa ^a   Sliskovic, Saundra ^a   Murray, Jeffrey C ^b   Wade, Claire M ^e   Bannasch, Danika L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SICHUAN UNIVERSITY   (China)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR DLX5; HOMEODOMAIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANINE MODEL; CHROMOSOME 14; CLEFT PALATE; CONTROLLED STUDY; DISTAL LESS HOMEOBOX 5 GENE; DISTAL LESS HOMEOBOX 6 GENE; GENE; GENE FREQUENCY; GENE SEQUENCE; GENETIC ASSOCIATION; HUMAN; JAW MALFORMATION; LONG INTERSPERSED REPEAT; MAJOR CLINICAL STUDY; MICRO-COMPUTED TOMOGRAPHY; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PIERRE ROBIN SYNDROME; SEQUENCE ANALYSIS; STOP CODON; ANIMAL; DOG; GENETICS; HOMEOBOX; MANDIBLE; METABOLISM; PHENOTYPE; PROCEDURES; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; CLEFT PALATE; DOGS; GENE FREQUENCY; GENES, HOMEOBOX; GENOME-WIDE ASSOCIATION STUDY; HOMEODOMAIN PROTEINS; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MANDIBLE; MUTATION, MISSENSE; PHENOTYPE; PIERRE ROBIN SYNDROME; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84901323341     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004257     Document Type: Article

References (60)

1. Parker SE, Mai CT, Canfield MA, Rickard R, Wang Y, et al. (2010) Updated National Birth Prevalence estimates for selected birth defects in the United States, 2004-2006. Birth Defects Res A Clin Mol Teratol 88: 1008-1016.
2. Persson C, Elander A, Lohmander-Agerskov A, E S, (2002) Speech outcomes in isolated cleft palate: impact of cleft extent and additional malformations. Cleft Palate Craniofac J 39: 397-408.
3. Christensen K, PB M, (2002) Facial clefting and psychiatric diseases: a follow-up of the Danish 1936-1987 Facial Cleft cohort. Cleft Palate Craniofac J 39: 392-396.
4. Conrad AL, Canady J, Richman L, P N, (2008) Incidence of neurological soft signs in children with isolated cleft of the lip or palate. Percept Mot Skills 106: 197-206.
5. Bush JO, R J, (2012) Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development 139: 231-243.
6. Bush PG, Williams AJ, (1983) Incidence of the Robin Anomalad (Pierre Robin syndrome). Br J Plast Surg 36: 434-437.
7. Ricks JE, Ryder VM, Bridgewater LC, Schaalje B, RE S, (2002) Altered mandibular development precedes the time of palate closure in mice homozygous for disproportionate micromelia: an oral clefting model supporting the Pierre-Robin sequence. Teratology 65: 116-120.
8. Cohen MM, (1999) Robin sequences and complexes: causal heterogeneity and pathogenetic/phenotypic variability. Am J Med Genet 84: 311-315.
9. Printzlau A, M A, (2004) Pierre Robin sequence in Denmark: a retrospective population-based epidemiological study. Cleft Palate Craniofac J 41: 47-52.
10. Jakobsen LP, Ullmann R, Christensen SB, Jensen KE (2007) Pierre Robin sequence may be caused by dysregulation of SOX9 and KCNJ2. J Med Genet 44: 381-386.
11. Benko S, Fantes JA, Amiel J, Kleinjan DJ, Thomas S, et al. (2009) Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nat Genet 41: 359-364.
12. Jakobsen LP, Knudsen MA, Lespinasse J, Garcia Ayuso C, Ramos C, et al. (2006) The genetic basis of the Pierre Robin Sequence. Cleft Palate Craniofac J 43: 155-159.
13. Holder-Espinasse M, Abadie V, Cormier-Daire V, Beyler C, Manach Y, et al. (2001) Pierre Robin sequence: a series of 117 consecutive cases. J Pediatr 139: 588-590.
14. Poswillo D, (1966) Observations of fetal posture and causal mechanisms of congenital deformity of palate, mandible and limbs. J Dent Res 45: 584-596.
15. Richtsmeier JT, Sack GH Jr, Grausz HM, LC C, (1994) Cleft palate with autosomal recessive transmission in Brittany spaniels. Cleft Palate Craniofac J 31: 364-371.
16. Moura E, Cirio SM, CT P, (2011) Non-Syndromic Cleft Lip and Palate in Boxer Dogs: Evidence of Monogenic Autosomal Recessive Inheritance. Cleft Palate Craniofac J 49: 759-60 doi:10.1597/11-110.
17. Kemp C, Thiele H, Dankof A, Schmidt G, Lauster C, et al. (2009) Cleft lip and/or palate with monogenic autosomal recessive transmission in Pyrenees shepherd dogs. Cleft Palate Craniofac J 46: 81-88.
18. Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, et al. (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8: e1000451.
19. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803-819.
20. Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, et al. (1999) Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126: 3795-3809.
21. Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, et al. (1999) Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126: 3831-3846.
22. Jeong J, Li X, McEvilly RJ, Rosenfeld MG, Lufkin T, et al. (2008) Dlx genes pattern mammalian jaw primordium by regulating both lower jaw-specific and upper jaw-specific genetic programs. Development 135: 2905-2916.
23. Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, et al. (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24: 1757-1764.
24. Pfaffl MW, Horgan GW, L D, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
25. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, et al. (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56-65.
26. Exome Variant Server. In: (ESP) NGESP, editor. Seattle, WA.
27. Simeone A, Acampora D, Pannese M, D'Esposito M, Stornaiuolo A, et al. (1994) Cloning and characterization of two members of the vertebrate Dlx gene family. Proc Natl Acad Sci U S A 91: 2250-2254.
28. Robledo RF, Rajan L, Li X, T L, (2002) The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev 16: 1089-1101.
29. Beverdam A, Merlo GR, Paleari L, Mantero S, Genova F, et al. (2002) Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: mirror of the past? Genesis 34: 221-227.
30. Hedge S, Praveen BN (2013) Morphological and Radiological Variation of Mandibular Condyles in Health and Diseases: A Systematic Review. Dentistry 3: 154 doi:10.4172/2161-1122.1000154.
31. Johnson JM, Moonis G, Green GE, Carmody R, HN B, (2011) Syndromes of the first and second branchial arches, part 2: syndromes. AJNR Am J Neuroradiol 32: 230-237.
32. Clarke L, Hepworth WB, Carey JC, RE S, (1988) Chondrodystrophic mice with coincidental agnathia: evidence for the tongue obstruction hypothesis in cleft palate. Teratology 38: 565-570.
33. Lavrin IO, McLean W, Seegmiller RE, Olsen BR, ED H, (2001) The mechanism of palatal clefting in the Col11a1 mutant mouse. Arch Oral Biol 46: 865-869.
34. Seegmiller RE, FC F, (1977) Mandibular growth retardation as a cause of cleft palate in mice homozygous for the chondrodysplasia gene. J Embryol Exp Morphol 38: 227-238.
35. Cohen MM Jr, (1978) Syndromes with cleft lip and cleft palate. Cleft Palate J 15: 306-328.
36. D'Elia AV, Tell G, Paron I, Pellizzari L, Lonigro R, et al. (2001) Missense mutations of human homeoboxes: A review. Hum Mutat 18: 361-374.
37. Samee N, Geoffroy V, Marty C, Schiltz C, Vieux-Rochas M, et al. (2009) Increased bone resorption and osteopenia in Dlx5 heterozygous mice. J Cell Biochem 107: 865-872.
38. Damante G, Pellizzari L, Esposito G, Fogolari F, Viglino P, et al. (1996) A molecular code dictates sequence-specific DNA recognition by homeodomains. EMBO J 15: 4992-5000.
39. Shamseldin HE, Faden MA, Alashram W, FS A, (2012) Identification of a novel DLX5 mutation in a family with autosomal recessive split hand and foot malformation. J Med Genet 49: 16-20.
40. Han J, Mayo J, Xu X, Li J, Bringas P Jr, et al. (2009) Indirect modulation of Shh signaling by Dlx5 affects the oral-nasal patterning of palate and rescues cleft palate in Msx1-null mice. Development 136: 4225-4233.
41. Poitras L, Yu M, Lesage-Pelletier C, Macdonald RB, Gagne JP, et al. (2010) An SNP in an ultraconserved regulatory element affects Dlx5/Dlx6 regulation in the forebrain. Development 137: 3089-3097.
42. Brown KK, Reiss JA, Crow K, Ferguson HL, Kelly C, et al. (2010) Deletion of an enhancer near DLX5 and DLX6 in a family with hearing loss, craniofacial defects, and an inv(7)(q21.3q35). Hum Genet 127: 19-31.
43. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
44. Kirkness EF, Bafna V, Halpern AL, Levy S, Remington K, et al. (2003) The dog genome: survey sequencing and comparative analysis. Science 301: 1898-1903.
45. Szak ST, Pickeral OK, Makalowski W, Boguski MS, Landsman D, et al. (2002) Molecular archeology of L1 insertions in the human genome. Genome Biol 3: research0052.
46. Smith BF, Yue Y, Woods PR, Kornegay JN, Shin JH, et al. (2011) An intronic LINE-1 element insertion in the dystrophin gene aborts dystrophin expression and results in Duchenne-like muscular dystrophy in the corgi breed. Lab Invest 91: 216-231.
47. Meischl C, Boer M, Ahlin A, D R, (2000) A new exon created by intronic insertion of a rearranged LINE-1 element as the cause of chronic granulomatous disease. Eur J Hum Genet 8: 697-703.
48. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
49. Kouwenhoven EN, van Heeringen SJ, Tena JJ, Oti M, Dutilh BE, et al. (2010) Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet 6: e1001065.
50. Zerucha T, Stuhmer T, Hatch G, Park BK, Long Q, et al. (2000) A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci 20: 709-721.
51. Feng J, Bi C, Clark BS, Mady R, Shah P, et al. (2006) The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev 20: 1470-1484.
52. K M, (2010) Population structure and genetic diversity of worldwide Nova Scotia Duck Tolling Retriever and Lancashire Heeler dog populations. Journal of Animal Breeding and Genetics 127: 318-326.
53. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575.
54. R Development Core Team. (2012) R: A Language and Environment for Statistical Computing. 2.15.1 ed. Vienna, Austria.
55. Rozen S, H S, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
56. Toonen RJ, S H, (2001) Increased throughput for fragment analysis on an ABI PRISM 377 automated sequencer using a membrane comb and STRand software. Biotechniques 31: 1320-1324.
57. Lange K, Cantor R, Horvath S, Perola M, Sabatti C, et al. (2001) MENDEL version 4.0: A complete package for the exact genetic analysis of discrete traits in pedigree and population data sets. American Journal of Human Genetics 69 (supplement):: 504.
58. Brinkhof B, Spee B, Rothuizen J, LC P, (2006) Development and evaluation of canine reference genes for accurate quantification of gene expression. Anal Biochem 356: 36-43.
59. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, et al. (2010) Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics 26: 2069-2070.
60. StataCorp (2011) Stata Statistical Software. Release 12 ed. College Station, TX: StataCorp LP.