Characterization of a novel missense mutation in the prodomain of GDF5, which underlies brachydactyly type C and mild Grebe type chondrodysplasia in a large Pakistani family

Human Genetics

Volumn 132, Issue 11, 2013, Pages 1253-1264

  Farooq, Muhammad ^a,b   Nakai, Hiroyuki ^c   Fujimoto, Atsushi ^a   Fujikawa, Hiroki ^a   Kjaer, Klaus Wilbrandt ^d   Baig, Shahid Mahmood ^b   Shimomura, Yutaka ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b NATIONAL INSTITUTE FOR BIOTECHNOLOGY AND GENETIC ENGINEERING NIBGE   (Pakistan)

^c NIIGATA UNIVERSITY   (Japan)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 5; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 1; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 2; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BRACHYDACTYLY; CHONDRODYSPLASIA; CLINICAL ARTICLE; CONTROLLED STUDY; GREBE TYPE CHONDRODYSPLASIA; HUMAN; HUMAN CELL; MISSENSE MUTATION; MOLECULAR STABILITY; NUCLEOTIDE SEQUENCE; PAKISTAN; PEDIGREE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ASIAN CONTINENTAL ANCESTRY GROUP; BRACHYDACTYLY; GENOTYPE; GROWTH DIFFERENTIATION FACTOR 5; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; LATENT TGF-BETA BINDING PROTEINS; MOLECULAR SEQUENCE DATA; MUSCULOSKELETAL ABNORMALITIES; MUTATION, MISSENSE; OSTEOCHONDRODYSPLASIAS; PAKISTAN; PEDIGREE; PHENOTYPE; PROTEIN CONFORMATION; SEQUENCE ANALYSIS, DNA;

EID: 84888312517     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-013-1330-3     Document Type: Article

References (50)

1. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201
2. Asai-Coakwell M, French CR, Ye M, Garcha K, Bigot K, Perera AG, Staehling-Hampton K, Mema SC, Chanda B, Mushegian A, Bamforth S, Doschak MR, Li G, Dobbs MB, Giampietro PF, Brooks BP, Vijayalakshmi P, Sauve Y, Abitbol M, Sundaresan P, van Heyningen V, Pourquie O, Underhill TM, Waskiewicz AJ, Lehmann OJ (2009) Incomplete penetrance and phenotypic variability characterize Gdf6-attributable oculo-skeletal phenotypes. Hum Mol Genet 18:1110-1121
3. Bakrania P, Efthymiou M, Klein JC, Salt A, Bunyan DJ, Wyatt A, Ponting CP, Martin A, Williams S, Lindley V, Gilmore J, Restori M, Robson AG, Neveu MM, Holder GE, Collin JR, Robinson DO, Farndon P, Johansen-Berg H, Gerrelli D, Ragge NK (2008) Mutations in BMP4 cause eye, brain, and digit developmental anomalies: overlap between the BMP4 and hedgehog signaling pathways. Am J Hum Genet 82:304-319
4. Bell J (1951) On hereditary digital anomalies, Part 1: On brachydactyly and symphalangism. In: The Treasury of Human Inheritance. Cambridge Univ. Press, Cambridge
5. Buxton P, Edwards C, Archer CW, Francis-West P (2001) Growth/differentiation factor-5 (GDF-5) and skeletal development. J Bone Joint Surg Am 83-A(Suppl 1):S23-S30
6. Chang SC, Hoang B, Thomas JT, Vukicevic S, Luyten FP, Ryba NJ, Kozak CA, Reddi AH, Moos M Jr (1994) Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development. J Biol Chem 269:28227-28234
7. Dawson K, Seeman P, Sebald E, King L, Edwards M, Williams J 3rd, Mundlos S, Krakow D (2006) GDF5 is a second locus for multiple-synostosis syndrome. Am J Hum Genet 78:708-712
8. Di Pasquale E, Beck-Peccoz P, Persani L (2004) Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet 75:106-111
9. Drews F, Knobel S, Moser M, Muhlack KG, Mohren S, Stoll C, Bosio A, Gressner AM, Weiskirchen R (2008) Disruption of the latent transforming growth factor-beta binding protein-1 gene causes alteration in facial structure and influences TGF-beta bioavailability. Biochim Biophys Acta 1783:34-48
10. Everman DB, Bartels CF, Yang Y, Yanamandra N, Goodman FR, Mendoza-Londono JR, Savarirayan R, White SM, Graham JM Jr, Gale RP, Svarch E, Newman WG, Kleckers AR, Francomano CA, Govindaiah V, Singh L, Morrison S, Thomas JT, Warman ML (2002) The mutational spectrum of brachydactyly type C. Am J Med Genet 112:291-296
11. Faiyaz-Ul-Haque M, Ahmad W, Wahab A, Haque S, Azim AC, Zaidi SH, Teebi AS, Ahmad M, Cohn DH, Siddique T, Tsui LC (2002a) Frameshift mutation in the cartilage-derived morphogenetic protein 1 (CDMP1) gene and severe acromesomelic chondrodysplasia resembling Grebe-type chondrodysplasia. Am J Med Genet 111:31-37
12. Faiyaz-Ul-Haque M, Ahmad W, Zaidi SH, Haque S, Teebi AS, Ahmad M, Cohn DH, Tsui LC (2002b) Mutation in the cartilage-derived morphogenetic protein-1 (CDMP1) gene in a kindred affected with fibular hypoplasia and complex brachydactyly (DuPan syndrome). Clin Genet 61:454-458
13. Fitch N, Jequier S, Costom B (1979) Brachydactyly C, short stature, and hip dysplasia. Am J Med Genet 4:157-166
14. Francis-West PH, Abdelfattah A, Chen P, Allen C, Parish J, Ladher R, Allen S, MacPherson S, Luyten FP, Archer CW (1999) Mechanisms of GDF-5 action during skeletal development. Development 126:1305-1315
15. Gray AM, Mason AJ (1990) Requirement for activin A and transforming growth factor-beta 1 pro-regions in homodimer assembly. Science 247:1328-1330
16. Harrison CA, Al-Musawi SL, Walton KL (2011) Prodomains regulate the synthesis, extracellular localisation and activity of TGF-beta superfamily ligands. Growth Factors 29:174-186
17. Hotten GC, Matsumoto T, Kimura M, Bechtold RF, Kron R, Ohara T, Tanaka H, Satoh Y, Okazaki M, Shirai T, Pan H, Kawai S, Pohl JS, Kudo A (1996) Recombinant human growth/differentiation factor 5 stimulates mesenchyme aggregation and chondrogenesis responsible for the skeletal development of limbs. Growth Factors 13:65-74
18. Janssens K, Vanhoenacker F, Bonduelle M, Verbruggen L, Van Maldergem L, Ralston S, Guanabens N, Migone N, Wientroub S, Divizia MT, Bergmann C, Bennett C, Simsek S, Melancon S, Cundy T, Van Hul W (2006) Camurati-Engelmann disease: review of the clinical, radiological, and molecular data of 24 families and implications for diagnosis and treatment. J Med Genet 43:1-11
19. Lorda-Diez CI, Montero JA, Garcia-Porrero JA, Hurle JM (2010) Tgfbeta2 and 3 are coexpressed with their extracellular regulator Ltbp1 in the early limb bud and modulate mesodermal outgrowth and BMP signaling in chicken embryos. BMC Dev Biol 10:69
20. Luyten FP (1997) Cartilage-derived morphogenetic protein-1. Int J Biochem Cell Biol 29:1241-1244
21. Merino R, Macias D, Ganan Y, Economides AN, Wang X, Wu Q, Stahl N, Sampath KT, Varona P, Hurle JM (1999) Expression and function of Gdf-5 during digit skeletogenesis in the embryonic chick leg bud. Dev Biol 206:33-45
22. Miyamoto Y, Mabuchi A, Shi D, Kubo T, Takatori Y, Saito S, Fujioka M, Sudo A, Uchida A, Yamamoto S, Ozaki K, Takigawa M, Tanaka T, Nakamura Y, Jiang Q, Ikegawa S (2007) A functional polymorphism in the 5′ UTR of GDF5 is associated with susceptibility to osteoarthritis. Nat Genet 39:529-533
23. Miyazono K, Hellman U, Wernstedt C, Heldin CH (1988) Latent high molecular weight complex of transforming growth factor beta 1. Purification from human platelets and structural characterization. J Biol Chem 263:6407-6415
24. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199
25. Noguchi K, Ishii S, Shimizu T (2003) Identification of p2y9/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family. J Biol Chem 278:25600-25606
26. Olofsson A, Miyazono K, Kanzaki T, Colosetti P, Engstrom U, Heldin CH (1992) Transforming growth factor-beta 1, -beta 2, and -beta 3 secreted by a human glioblastoma cell line. Identification of small and different forms of large latent complexes. J Biol Chem 267:19482-19488
27. Ploger F, Seemann P, Schmidt-von Kegler M, Lehmann K, Seidel J, Kjaer KW, Pohl J, Mundlos S (2008) Brachydactyly type A2 associated with a defect in proGDF5 processing. Hum Mol Genet 17:1222-1233
28. Polinkovsky A, Robin NH, Thomas JT, Irons M, Lynn A, Goodman FR, Reardon W, Kant SG, Brunner HG, van der Burgt I, Chitayat D, McGaughran J, Donnai D, Luyten FP, Warman ML (1997) Mutations in CDMP1 cause autosomal dominant brachydactyly type C. Nat Genet 17:18-19
29. Robertson I, Jensen S, Handford P (2011) TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs. Biochem J 433:263-276
30. Saharinen J, Keski-Oja J (2000) Specific sequence motif of 8-Cys repeats of TGF-beta binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-beta. Mol Biol Cell 11:2691-2704
31. Saharinen J, Taipale J, Keski-Oja J (1996) Association of the small latent transforming growth factor-beta with an eight cysteine repeat of its binding protein LTBP-1. EMBO J 15:245-253
32. Saharinen J, Hyytiainen M, Taipale J, Keski-Oja J (1999) Latent transforming growth factor-beta binding proteins (LTBPs)-structural extracellular matrix proteins for targeting TGF-beta action. Cytokine Growth Factor Rev 10:99-117
33. Schwabe GC, Turkmen S, Leschik G, Palanduz S, Stover B, Goecke TO, Mundlos S (2004) Brachydactyly type C caused by a homozygous missense mutation in the prodomain of CDMP1. Am J Med Genet A 124A:356-363
34. Seemann P, Schwappacher R, Kjaer KW, Krakow D, Lehmann K, Dawson K, Stricker S, Pohl J, Ploger F, Staub E, Nickel J, Sebald W, Knaus P, Mundlos S (2005) Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J Clin Invest 115:2373-2381
35. Sengle G, Charbonneau NL, Ono RN, Sasaki T, Alvarez J, Keene DR, Bachinger HP, Sakai LY (2008) Targeting of bone morphogenetic protein growth factor complexes to fibrillin. J Biol Chem 283:13874-13888
36. Settle SH Jr, Rountree RB, Sinha A, Thacker A, Higgins K, Kingsley DM (2003) Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol 254:116-130
37. Sha X, Yang L, Gentry LE (1991) Identification and analysis of discrete functional domains in the pro region of pre-pro-transforming growth factor beta 1. J Cell Biol 114:827-839
38. Shi M, Zhu J, Wang R, Chen X, Mi L, Walz T, Springer TA (2011) Latent TGF-beta structure and activation. Nature 474:343-349
39. Shimomura Y, Agalliu D, Vonica A, Luria V, Wajid M, Baumer A, Belli S, Petukhova L, Schinzel A, Brivanlou AH, Barres BA, Christiano AM (2010) APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex. Nature 464:1043-1047
40. Storm EE, Kingsley DM (1999) GDF5 coordinates bone and joint formation during digit development. Dev Biol 209:11-27
41. Suzuki S, Marazita ML, Cooper ME, Miwa N, Hing A, Jugessur A, Natsume N, Shimozato K, Ohbayashi N, Suzuki Y, Niimi T, Minami K, Yamamoto M, Altannamar TJ, Erkhembaatar T, Furukawa H, Daack-Hirsch S, L'Heureux J, Brandon CA, Weinberg SM, Neiswanger K, Deleyiannis FW, de Salamanca JE, Vieira AR, Lidral AC, Martin JF, Murray JC (2009) Mutations in BMP4 are associated with subepithelial, microform, and overt cleft lip. Am J Hum Genet 84:406-411
42. Taipale J, Koli K, Keski-Oja J (1992) Release of transforming growth factor-beta 1 from the pericellular matrix of cultured fibroblasts and fibrosarcoma cells by plasmin and thrombin. J Biol Chem 267:25378-25384
43. Taipale J, Miyazono K, Heldin CH, Keski-Oja J (1994) Latent transforming growth factor-beta 1 associates to fibroblast extracellular matrix via latent TGF-beta binding protein. J Cell Biol 124:171-181
44. Thomas JT, Lin K, Nandedkar M, Camargo M, Cervenka J, Luyten FP (1996) A human chondrodysplasia due to a mutation in a TGF-beta superfamily member. Nat Genet 12:315-317
45. Thomas JT, Kilpatrick MW, Lin K, Erlacher L, Lembessis P, Costa T, Tsipouras P, Luyten FP (1997) Disruption of human limb morphogenesis by a dominant negative mutation in CDMP1. Nat Genet 17:58-64
46. Thomas JT, Prakash D, Weih K, Moos M Jr (2006) CDMP1/GDF5 has specific processing requirements that restrict its action to joint surfaces. J Biol Chem 281:26725-26733
47. Vidricaire G, Denault JB, Leduc R (1993) Characterization of a secreted form of human furin endoprotease. Biochem Biophys Res Commun 195:1011-1018
48. Wakefield LM, Smith DM, Flanders KC, Sporn MB (1988) Latent transforming growth factor-beta from human platelets. A high molecular weight complex containing precursor sequences. J Biol Chem 263:7646-7654
49. Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomkinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, Lee SJ (2003) Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA 100:15842-15846
50. Yang W, Cao L, Liu W, Jiang L, Sun M, Zhang D, Wang S, Lo WH, Luo Y, Zhang X (2008) Novel point mutations in GDF5 associated with two distinct limb malformations in Chinese: brachydactyly type C and proximal symphalangism. J Hum Genet 53:368-374