De novo Alu-element insertions in FGFR2 identify a distinct pathological basis for Apert syndrome

American Journal of Human Genetics

Volumn 64, Issue 2, 1999, Pages 446-461

  Oldridge, Michael ^a   Zackai, Elaine H ^c   McDonald McGinn, Donna M ^c   Iseki, Sachiko ^e   Morriss Kay, Gillian M ^e   Twigg, Stephen R F ^a   Johnson, David ^a   Wall, Steven A ^b   Jiang, Wen ^d   Theda, Christiane ^d   Jabs, Ethylin Wang ^d   Wilkie, Andrew O M ^a,b  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b RADCLIFFE INFIRMARY   (United Kingdom)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

FGF2 PROTEIN, MOUSE; FGFR2 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE;

ACROCEPHALOSYNDACTYLY; ALU SEQUENCE; ANIMAL; ARTICLE; CASE REPORT; CHILD; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GENOME IMPRINTING; HUMAN; LIMB; MALE; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PEDIGREE; PRENATAL DEVELOPMENT; RADIOGRAPHY; RNA SPLICING;

ACROCEPHALOSYNDACTYLIA; ALU ELEMENTS; ANIMALS; BASE SEQUENCE; CHILD; EXTREMITIES; FEMALE; GENE EXPRESSION; GENOMIC IMPRINTING; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PEDIGREE; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTORS, FIBROBLAST GROWTH FACTOR; RECEPTORS, GROWTH FACTOR; RNA SPLICING;

EID: 0033073850     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/302245     Document Type: Article

References (60)

1. Abdelhak S, Kalatzis V, Heilig R, Compain S, Samson D, Vincent C, Levi-Acobas F, et al (1997) Clustering of mutations responsible for branchio-oto-renal (BOR) syndrome in the eyes absent homologous region (eyaHR) of EYA1. Hum Mol Genet 6:2247-2255
2. Anderson J, Burns HD, Enriquez-Harris P, Wilkie AOM, Heath JK (1998a) Apert syndrome mutations in fibroblast growth factor receptor 2 exhibit increased affinity for FGF ligand. Hum Mol Genet 7:1475-1483
3. Anderson PJ, Hall CM, Evans RD, Jones BM, Hayward RD (1998b) The feet in Pfeiffer's syndrome. J Craniofac Surg 9: 83-87
4. Batzer MA, Deininger PL, Hellmann-Blumberg U, Jurka J, Labuda D, Rubin CM, Schmid CW, et al (1996) Standardized nomenclature for Alu repeats. J Mol Evol 42:3-6
5. Batzer MA, Rubin CM, Hellmann-Blumberg U, Alegria-Hartman M, Leeflang EP, Stern JD, Bazan HA, et al (1995) Dispersion and insertion polymorphism in two small subfamilies of recently amplified human Alu repeats. J Mol Biol 247:418-427
6. Bellus GA, Gaudenz K, Zackai EH, Clark LA, Szabo J, Francomano CA, Muenke M (1996) Identical mutations in three different fibroblast growth factor receptor genes in autosomal dominant craniosynostosis syndromes. Nat Genet 14: 174-176
7. Boeke JD (1997) LINEs and Alus - the poly A connection. Nat Genet 16:6-7
8. Carstens RP, McKeehan WL, Garcia-Blanco MA (1998) An intronic sequence element mediates both activation and repression of rat fibroblast growth factor receptor 2 premRNA splicing. Mol Cell Biol 18:2205-2217
9. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159
10. Deininger PL, Batzer MA (1995) SINE master genes and population biology. In: Maraia R (ed) The impact of short, interspersed elements (SINES) on the host genome. RG Landes, Georgetown, TX, pp 43-60
11. Del Gatto F, Plet A, Gesnel M-C, Fort C, Breathnach R (1997) Multiple interdependent sequence elements control splicing of a fibroblast growth factor receptor 2 alternative exon. Mol Cell Biol 17:5106-5116
12. Dell KR, Williams LT (1992) A novel form of fibroblast growth factor receptor 2: alternative splicing of the third immunoglobulin like domain confers ligand binding specificity. J Biol Chem 267:21225-21229
13. Dib C, Fauré S, Fizames C, Samson D, Drouot N, Vignal A, Millasseau P, et al (1996) A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 380:152-154
14. Dionne CA, Crumley G, Bellot F, Kaplow JM, Searfoss G, Ruta M, Burgess WH, et al (1990) Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J 9:2685-2692
15. Escobar V, Bixler D (1977) On the classification of the acrocephalosyndactyly syndromes. Clin Genet 12:169-178
16. Finch PW, Cunha GR, Rubin JS, Wong J, Ron D (1995) Pattern of keratinocyte growth factor and keratinocyte growth factor receptor expression during mouse fetal development suggests a role in mediating morphogenetic mesenchymal-epithelial interactions. Dev Dyn 203:223-240
17. Gilbert E, Del Gatto F, Champion-Arnaud P, Gesnel M-C, Breathnach R (1993) Control of BEK and K-SAM splice sites in alternative splicing of the fibroblast growth factor receptor 2 pre-mRNA. Mol Cell Biol 13:5461-5468
18. Gorlin RJ, Cohen MM Jr, Levin LS (1990) Syndromes with craniosynostosis: general aspects and well-known syndromes. In: Gorlin RJ, Cohen MM Jr, Levin LS (eds) Syndromes of the head and neck, 2d ed. Oxford University Press, New York, pp 519-539
19. Halling KC, Honchel R, Lazzaro CR, Bufill JA, Arndt C, Lindor NM (1997) A germline AluI repeat insertion of the APC gene leading to hereditary desmoid disease in an Amish family. Am J Hum Genet Suppl 61:A67
20. Hu MC-T, Qiu WR, Wang Y-P, Hill D, Ring BD, Scully S, Bolon B, et al (1998) FGF-18, a novel member of the fibroblast growth factor family, stimulates hepatic and intestinal proliferation. Mol Cell Biol 18:6063-6074
21. Hughes AE, Armstrong DKB, Dawson JF, Nevin NC (1998) Syndromic acanthosis nigricans - evidence of aberrant fibroblast growth factor receptor function. Am J Hum Genet Suppl 63:A183
22. Iseki S, Wilkie AOM, Heath JK, Ishimaru T, Eto K, Morriss-Kay GM (1997) Fgfr2 and osteopontin domains in the developing skull vault are mutually exclusive and can be altered by locally applied FGF2. Development 124: 3375-3384
23. 2 +-sensing receptor gene in familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism. Am J Hum Genet 56:880-886
24. Johnson DE, Williams LT (1993) Structural and functional diversity in the FGF receptor multigene family. In: Vande Woude GF, Klein G (eds) Advances in cancer research. Vol 60. Academic Press, San Diego, pp 1-41
25. Johnston CL, Cox HC, Gomm JJ, Coombes RC (1995) Fibroblast growth factor receptors (FGFRs) localize in different cellular compartments. J Biol Chem 270:30643-30650
26. Jurka J (1997) Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci USA 94:1872-1877
27. Katoh M, Hattori Y, Sasaki H, Tanaka M, Sugano K, Yazaki Y, Sugimura T, et al (1992) K-sam gene encodes secreted as well as transmembrane receptor tyrosine kinase. Proc Natl Acad Sci USA 89:2960-2964
28. Lajeunie E, Ma HW, Bonaventure J, Munnich A, Le Merrer M, Renier D (1995) FGFR2 mutations in Pfeiffer syndrome. Nat Genet 9:108
29. Lester T, McMahon C, Van Regemorter N, Jones A, Genet S (1997) X-linked immunodeficiency caused by insertion of Alu repeat sequences. J Med Genet 34 Suppl 1:S81
30. Makalowski W, Mitchell GA, Labuda D (1994) Alu sequences in the coding regions of mRNA: a source of protein variability. Trends Genet 10:188-193
31. Martin GR (1998) The roles of FGFs in the early development of vertebrate limbs. Genes Dev 12:1571-1586
32. Mason IJ, Fuller-Pace F, Smith R, Dickson C (1994) FGF7 (keratinocyte growth factor) expression during mouse de velopment suggests roles in myogenesis, forebrain regionalisation and cpithelial-mesenchymal interactions. Mech Dev 45:15-30
33. Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, Chan AM-L, Aaronson SA (1992) Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci USA 89:246-250
34. Miki Y, Katagiri T, Kasumi F, Yoshimoto T, Nakamura Y (1996) Mutation analysis in the BRCA2 gene in primary breast cancers. Nat Genet 13:245-247
35. Moloney DM, Slaney SF, Oldridge M, Wall SA, Sahlin P, Stenman G, Wilkie AOM (1996) Exclusive paternal origin of new mutations in Apert syndrome. Nat Genet 13:48-53
36. Muenke M, Schell U, Hehr A, Robin NH, Losken HW, Schinzel A, Pulleyn LJ, et al (1994) A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome. Nat Genet 8:269-274
37. Muratani K, Hada T, Yamamoto Y, Kaneko T, Shigeto Y, Ohue T, Furuyama J, et al (1991) Inactivation of the cholinesterase gene by Alu insertion: possible mechanism for human gene transposition. Proc Natl Acad Sci USA 88:11315-11319
38. Neilson KM, Friesel R (1996) Ligand-independent activation of fibroblast growth factor receptors by point mutations in the extracellular, transmembrane, and kinase domains. J Biol Chem 271:25049-25057
39. Ohbayashi N, Hoshikawa M, Kimura S, Yamasaki M, Fukui S, Itoh N (1998) Structure and expression of the mRNA encoding a novel fibroblast growth factor, FGF-18. J Biol Chem 273:18161-18164
40. Ohuchi H, Nakagawa T, Yamamoto A, Araga A, Ohata T, Ishimaru Y, Yoshioka H, et al (1997) The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124:2235-2244
41. Oldridge M, Lunt PW, Zackai EH, McDonald-McGinn DM, Muenke M, Moloney DM, Twigg SRF, et al (1997) Genotype-phenotype correlation for nucleotide substitutions in the IgII-IgIII linker of FGFR2. Hum Mol Genet 6:137-143
42. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, et al (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271: 15292-15297
43. Orr-Urtreger A, Bedford MT, Burakova T, Arman E, Zimmer Y, Yayon A, Givol D, et al (1993) Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev Biol 158:475-486
44. Park W-J, Theda C, Maestri NE, Meyers GA, Fryburg JS, Dufresne C, Cohen MM Jr, et al (1995) Analysis of phenotypic features and FGFR2 mutations in Apert syndrome. Am J Hum Genet 57:321-328
45. Passos-Bueno MR, Richieri-Costa A, Sertié AL, Kneppers A (1998) Presence of the Apert canonical S252W FGFR2 mutation in a patient without severe syndactyly. J Med Genet 35:677-679
46. Passos-Bueno MR, Sertié AL, Zatz M, Richieri-Costa A (1997) Pfeiffer mutation in an Apert patient: how wide is the spectrum of variability due to mutations in the FGFR2 gene? Am J Med Genet 71:243-245
47. Przylepa KA, Paznekas W, Zhang M, Golabi M, Bias W, Bamshad MJ, Carey JC, et al (1996) Fibroblast growth factor receptor 2 mutations in Beare-Stevenson cutis gyrata syndrome. Nat Genet 13:492-494
48. Robertson SC, Meyer AN, Hart KC, Galvin BD, Webster MK, Donoghue DJ (1998) Activating mutations in the extracellular domain of the fibroblast growth factor receptor 2 function by disruption of the disulfide bond in the third immunoglobulin-like domain. Proc Natl Acad Sci USA 95: 4567-4572
49. Schell U, Hehr A, Feldman GJ, Robin NH, Zackai EH, de Die-Smulders C, Viskochil DH, et al (1995) Mutations in FGFR1 and FGFR2 cause familial and sporadic Pfeiffer syndrome. Hum Mol Genet 4:323-328
50. Schmid CW (1996) Alu: structure, origin, evolution, significance, and function of one-tenth of human DNA. Prog Nucleic Acid Res Mol Biol 53:283-319
51. Slaney SF, Oldridge M, Hurst JA, Morriss-Kay GM, Hall CM, Poole MD, Wilkie AOM (1996) Differential effects of FGFR2 mutations on syndactyly and cleft palate in Aperr syndrome. Am J Hum Genet 58:923-932
52. Spivak-Kroizman T, Lemmon MA, Dikic I, Ladbury JE, Pinchasi D, Huang J, Jaye M, et al (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 79:1015-1024
53. Twigg SRF, Burns HD, Oldridge M, Heath JK, Wilkie AOM (1998) Conserved use of a non-canonical 5′splice site (/GA) in alternative splicing by fibroblast growth factor receptors 1, 2 and 3. Hum Mol Genet 7:685-691
54. Upton J (1991) Classification and pathologic anatomy of limb anomalies. Clin Plast Surg 18:321-355
55. Upton J, Zuker RM (eds) (1991) Clinics in plastic surgery. Vol 18: Apert syndrome. WB Saunders, Philadelphia
56. Vidaud D, Vidaud M, Bahnak BR, Siguret V, Sanchez SG, Laurian Y, Meyer D, et al (1993) Haemophilia B due to a de novo insertion of a human-specific Alu subfamily member within the coding region of the factor IX gene. Eur J Hum Genet 1:30-36
57. Wallace MR, Anderson LB, Saulino AM, Gregory PE, Glover TW, Collins FS (1991) A de novo Alu insertion results in neurofibromatosis type 1. Nature 353:864-866
58. Wilkie AOM (1997) Craniosynostosis: genes and mechanisms. Hum Mol Genet 6:1647-1656
59. Wilkie AOM, Slaney SF, Oldridge M, Poole MD, Ashworth GJ, Hockley AD, Hayward RD, et al (1995) Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat Genet 9:165-172
60. Xu X, Weinstein M, Li C, Naski M, Cohen RI, Ornitz DM, Leder P, et al (1998) Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125:753-765