Haploinsufficiency of the NOTCH1 Receptor as a Cause of Adams-Oliver Syndrome with Variable Cardiac Anomalies

Circulation: Cardiovascular Genetics

Volumn 8, Issue 4, 2015, Pages 572-581

  Southgate, Laura ^b   Sukalo, Maja ^b   Karountzos, Anastasios S V ^b   Taylor, Edward J ^b   Collinson, Claire S ^b   Ruddy, Deborah ^b   Snape, Katie M ^b   Dallapiccola, Bruno ^b   Tolmie, John L ^b   Joss, Shelagh ^b   Brancati, Francesco ^b   Digilio, Maria Cristina ^b   Graul Neumann, Luitgard M ^b   Salviati, Leonardo ^b   Coerdt, Wiltrud ^b   Jacquemin, Emmanuel ^b   Wuyts, Wim ^b   Zenker, Martin ^b   Machado, Rajiv D ^b   Trembath, Richard C ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b NONE

Author keywords

Adams Oliver syndrome; genetics; haploinsufficiency; heart defects, congenital; receptor, NOTCH1

Indexed keywords

MESSENGER RNA; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HEY1; UNCLASSIFIED DRUG;

ADAMS OLIVER SYNDROME; ADOLESCENT; ADULT; AMINO ACID SUBSTITUTION; AORTA COARCTATION; AORTA STENOSIS; AORTA VALVE REGURGITATION; AORTA VALVE STENOSIS; AORTIC VALVE REPAIR; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; BRACHYDACTYLY; CHILD; CONGENITAL BLOOD VESSEL MALFORMATION; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; CUTIS MARMORATA TELANGIECTATICA CONGENITA; DISULFIDE BOND; DOWN REGULATION; ECHOCARDIOGRAPHY; EXOME; FEMALE; FRAMESHIFT MUTATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC SCREENING; HAPLOINSUFFICIENCY; HEART DISEASE; HEART VENTRICLE SEPTUM DEFECT; HUMAN; LEUKOCYTE; LIGAND BINDING; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MISSENSE MUTATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA DEGRADATION; RNA TRANSCRIPTION; SCHOOL CHILD; SIGNAL TRANSDUCTION; SKIN APLASIA; STOP CODON; SYNDACTYLY; TRANSIENT TRANSFECTION; YOUNG ADULT; CHEMISTRY; DNA SEQUENCE; ECTODERMAL DYSPLASIA; FAMILY HEALTH; GENETIC PREDISPOSITION; GENETICS; LIMB MALFORMATION; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PEDIGREE; PROCEDURES; PROTEIN TERTIARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCALP DERMATOSES;

ADOLESCENT; ADULT; BASE SEQUENCE; CHILD; ECTODERMAL DYSPLASIA; EXOME; FAMILY HEALTH; FEMALE; GENE EXPRESSION; GENETIC PREDISPOSITION TO DISEASE; HAPLOINSUFFICIENCY; HEART DEFECTS, CONGENITAL; HUMANS; LIMB DEFORMITIES, CONGENITAL; MALE; MIDDLE AGED; MODELS, MOLECULAR; PEDIGREE; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCALP DERMATOSES; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 84940045054     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.115.001086     Document Type: Article

References (44)

1. Adams FH, Oliver CP. Hereditary deformities in man due to arrested development. J Hered. 1945; 36: 3-7.
2. Martínez-Frías ML, Arroyo Carrera I, Muñoz-Delgado NJ, Nieto Conde C, Rodríguez-Pinilla E, Urioste Azcorra M, et al. The Adams-Oliver syndrome in Spain: The epidemiological aspects. An Esp Pediatr. 1996; 45: 57-61.
3. Lin AE, Westgate MN, van der Velde ME, Lacro RV, Holmes LB. Adams-Oliver syndrome associated with cardiovascular malformations. Clin Dysmorphol. 1998; 7: 235-241.
4. Digilio MC, Marino B, Dallapiccola B. Autosomal dominant inheritance of aplasia cutis congenita and congenital heart defect: A possible link to the Adams-Oliver syndrome. Am J Med Genet A. 2008; 146A: 2842-2844.doi: 10. 1002/ajmg. a. 32526.
5. Snape KM, Ruddy D, Zenker M, Wuyts W, Whiteford M, Johnson D, et al. The spectra of clinical phenotypes in aplasia cutis congenita and terminal transverse limb defects. Am J Med Genet A. 2009; 149A: 1860-1881.doi: 10. 1002/ajmg. a. 32708.
6. Southgate L, Machado RD, Snape KM, Primeau M, Dafou D, Ruddy DM, et al. Gain-of-function mutations of ARHGAP31, a Cdc42/Rac1 GTPase regulator, cause syndromic cutis aplasia and limb anomalies. Am J Hum Genet. 2011; 88: 574-585.doi: 10. 1016/j. ajhg. 2011. 04. 013.
7. Shaheen R, Faqeih E, Sunker A, Morsy H, Al-Sheddi T, Shamseldin HE, et al. Recessive mutations in DOCK6, encoding the guanidine nucleotide exchange factor DOCK6, lead to abnormal actin cytoskeleton organization and Adams-Oliver syndrome. Am J Hum Genet. 2011; 89: 328-333. doi: 10. 1016/j. ajhg. 2011. 07. 009.
8. Hassed SJ, Wiley GB, Wang S, Lee JY, Li S, Xu W, et al. RBPJ mutations identified in two families affected by Adams-Oliver syndrome. Am J Hum Genet. 2012; 91: 391-395.doi: 10. 1016/j. ajhg. 2012. 07. 005.
9. Shaheen R, Aglan M, Keppler-Noreuil K, Faqeih E, Ansari S, Horton K, et al. Mutations in EOGT confirm the genetic heterogeneity of autosomalrecessive Adams-Oliver syndrome. Am J Hum Genet. 2013; 92: 598-604. doi: 10. 1016/j. ajhg. 2013. 02. 012.
10. Cohen I, Silberstein E, Perez Y, Landau D, Elbedour K, Langer Y, et al. Autosomal recessive Adams-Oliver syndrome caused by homozygous mutation in EOGT, encoding an EGF domain-specific O-GlcNAc transferase. Eur J Hum Genet. 2014; 22: 374-378.doi: 10. 1038/ejhg. 2013. 159.
11. Stittrich AB, Lehman A, Bodian DL, Ashworth J, Zong Z, Li H, et al. Mutations in NOTCH1 cause Adams-Oliver syndrome. Am J Hum Genet. 2014; 95: 275-284.doi: 10. 1016/j. ajhg. 2014. 07. 011.
12. Isrie M, Wuyts W, Van Esch H, Devriendt K. Isolated terminal limb reduction defects: extending the clinical spectrum of Adams-Oliver syndrome and ARHGAP31 mutations. Am J Med Genet A. 2014; 164A: 1576-1579. doi: 10. 1002/ajmg. a. 36486.
13. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010; 38: e164.doi: 10. 1093/nar/gkq603.
14. Nagase T, Yamakawa H, Tadokoro S, Nakajima D, Inoue S, Yamaguchi K, et al. Exploration of human ORFeome: high-throughput preparation of ORF clones and efficient characterization of their protein products. DNA Res. 2008; 15: 137-149.doi: 10. 1093/dnares/dsn004.
15. Dallapiccola B, Giannotti A, Marino B, Digilio C, Obregon G. Familial aplasia cutis congenita and coarctation of the aorta. Am J Med Genet. 1992; 43: 762-763.doi: 10. 1002/ajmg. 1320430423.
16. Girard M, Amiel J, Fabre M, Pariente D, Lyonnet S, Jacquemin E. Adams-Oliver syndrome and hepatoportal sclerosis: occasional association or common mechanism? Am J Med Genet A. 2005; 135: 186-189.doi: 10. 1002/ajmg. a. 30724.
17. Franchi-Abella S, Fabre M, Mselati E, De Marsillac ME, Bayari M, Pariente D, et al. Obliterative portal venopathy: A study of 48 children. J Pediatr. 2014; 165: 190-193. e2.doi: 10. 1016/j. jpeds. 2014. 03. 025.
18. Shone JD, Sellers RD, Anderson RC, Adams P Jr, Lillehei CW, Edwards JE. The developmental complex of "parachute mitral valve, " supravalvular ring of left atrium, subaortic stenosis, and coarctation of aorta. Am J Cardiol. 1963; 11: 714-725.
19. Schwarz JM, Cooper DN, Schuelke M, Seelow D. MutationTaster2: mutation prediction for the deep-sequencing age. Nat Methods. 2014; 11: 361-362.doi: 10. 1038/nmeth. 2890.
20. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010; 7: 248-249.doi: 10. 1038/nmeth0410-248.
21. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009; 4: 1073-1081.doi: 10. 1038/nprot. 2009. 86.
22. Cordle J, Johnson S, Tay JZ, Roversi P, Wilkin MB, de Madrid BH, et al. A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition. Nat Struct Mol Biol. 2008; 15: 849-857. doi: 10. 1038/nsmb. 1457.
23. Zenker M. Clinical manifestations of mutations in RAS and related intracellular signal transduction factors. Curr Opin Pediatr. 2011; 23: 443-451. doi: 10. 1097/MOP. 0b013e32834881dd.
24. Davis EE, Katsanis N. The ciliopathies: A transitional model into systems biology of human genetic disease. Curr Opin Genet Dev. 2012; 22: 290-303.doi: 10. 1016/j. gde. 2012. 04. 006.
25. Patel MS, Taylor GP, Bharya S, Al-Sanna'a N, Adatia I, Chitayat D, et al. Abnormal pericyte recruitment as a cause for pulmonary hypertension in Adams-Oliver syndrome. Am J Med Genet A. 2004; 129A: 294-299. doi: 10. 1002/ajmg. a. 30221.
26. Algaze C, Esplin ED, Lowenthal A, Hudgins L, Tacy TA, Selamet Tierney ES. Expanding the phenotype of cardiovascular malformations in Adams-Oliver syndrome. Am J Med Genet A. 2013; 161A: 1386-1389.doi: 10. 1002/ajmg. a. 35864.
27. High FA, Epstein JA. The multifaceted role of Notch in cardiac development and disease. Nat Rev Genet. 2008; 9: 49-61.doi: 10. 1038/nrg2279.
28. Oda T, Elkahloun AG, Pike BL, Okajima K, Krantz ID, Genin A, et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet. 1997; 16: 235-242.doi: 10. 1038/ng0797-235.
29. High FA, Lu MM, Pear WS, Loomes KM, Kaestner KH, Epstein JA. Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc Natl Acad Sci U S A. 2008; 105: 1955-1959.doi: 10. 1073/pnas. 0709663105.
30. McDaniell R, Warthen DM, Sanchez-Lara PA, Pai A, Krantz ID, Piccoli DA, et al. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am J Hum Genet. 2006; 79: 169-173.doi: 10. 1086/505332.
31. Isidor B, Lindenbaum P, Pichon O, Bézieau S, Dina C, Jacquemont S, et al. Truncating mutations in the last exon of NOTCH2 cause a rare skeletal disorder with osteoporosis. Nat Genet. 2011; 43: 306-308.doi: 10. 1038/ ng. 778.
32. Simpson MA, Irving MD, Asilmaz E, Gray MJ, Dafou D, Elmslie FV, et al. Mutations in NOTCH2 cause Hajdu-Cheney syndrome, a disorder of severe and progressive bone loss. Nat Genet. 2011; 43: 303-305. doi: 10. 1038/ng. 779.
33. Jiang R, Lan Y, Chapman HD, Shawber C, Norton CR, Serreze DV, et al. Defects in limb, craniofacial, and thymic development in Jagged2 mutant mice. Genes Dev. 1998; 12: 1046-1057.
34. Francis JC, Radtke F, Logan MP. Notch1 signals through Jagged2 to regulate apoptosis in the apical ectodermal ridge of the developing limb bud. Dev Dyn. 2005; 234: 1006-1015.doi: 10. 1002/dvdy. 20590.
35. Pan Y, Liu Z, Shen J, Kopan R. Notch1 and 2 cooperate in limb ectoderm to receive an early Jagged2 signal regulating interdigital apoptosis. Dev Biol. 2005; 286: 472-482.doi: 10. 1016/j. ydbio. 2005. 08. 037.
36. Ramasamy SK, Kusumbe AP, Wang L, Adams RH. Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature. 2014; 507: 376-380.doi: 10. 1038/nature13146.
37. Gridley T. Notch signaling in vascular development and physiology. Development. 2007; 134: 2709-2718.doi: 10. 1242/dev. 004184.
38. Hambleton S, Valeyev NV, Muranyi A, Knott V, Werner JM, McMichael AJ, et al. Structural and functional properties of the human notch-1 ligand binding region. Structure. 2004; 12: 2173-2183.doi: 10. 1016/j. str. 2004. 09. 012.
39. de Celis JF, Barrio R, del Arco A, García-Bellido A. Genetic and molecular characterization of a Notch mutation in its Delta-and Serrate-binding domain in Drosophila. Proc Natl Acad Sci U S A. 1993; 90: 4037-4041.
40. Lu L, Stanley P. Roles of O-fucose glycans in notch signaling revealed by mutant mice. Methods Enzymol. 2006; 417: 127-136.doi: 10. 1016/ S0076-6879(06)17010-X.
41. Alfaro JF, Gong CX, Monroe ME, Aldrich JT, Clauss TR, Purvine SO, et al. Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci U S A. 2012; 109: 7280-7285.doi: 10. 1073/ pnas. 1200425109.
42. Sakaidani Y, Ichiyanagi N, Saito C, Nomura T, Ito M, Nishio Y, et al. Olinked-N-acetylglucosamine modification of mammalian Notch receptors by an atypical O-GlcNAc transferase Eogt1. Biochem Biophys Res Commun. 2012; 419: 14-19.doi: 10. 1016/j. bbrc. 2012. 01. 098.
43. Cartegni L, Chew SL, Krainer AR. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet. 2002; 3: 285-298.doi: 10. 1038/nrg775.
44. Fischer A, Schumacher N, Maier M, Sendtner M, Gessler M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 2004; 18: 901-911.doi: 10. 1101/gad. 291004.