The brachydactylies: A molecular disease family

Clinical Genetics

Volumn 76, Issue 2, 2009, Pages 123-136

  Mundlos, S ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

BMP pathway; Brachydactyly; Disease family; Molecular network

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ACROMESOMELIC CHONDRODYSPLASIA; BRACHYDACTYLY; BRACHYDACTYLY TYPE A1; BRACHYDACTYLY TYPE A2; BRACHYDACTYLY TYPE A3; BRACHYDACTYLY TYPE B1; BRACHYDACTYLY TYPE B2; BRACHYDACTYLY TYPE C; BRACHYDACTYLY TYPE D; BRACHYDACTYLY TYPE E; CHONDRODYSPLASIA; CLINICAL FEATURE; DISEASE MODEL; GENE FUNCTION; GENE REGULATORY NETWORK; GENETIC LINKAGE; GENITAL MALFORMATION; HAND FOOT GENITAL SYNDROME; HUMAN; LIMB DEVELOPMENT; LIMB MALFORMATION; MISSENSE MUTATION; MOLECULAR GENETICS; MULTIPLE SYNOSTOSIS SYNDROME; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; ROBINOW SYNDROME; SIGNAL TRANSDUCTION; SYMPHALANGIA;

ABNORMALITIES, MULTIPLE; HUMANS; LIMB DEFORMITIES, CONGENITAL; SYNDROME; SYNOSTOSIS;

ANIMALIA;

EID: 70349989289     PISSN: 00099163     EISSN: 13990004     Source Type: Journal    
DOI: 10.1111/j.1399-0004.2009.01238.x     Document Type: Review

References (81)

1. Bell J. On brachydactyly and syphalangism. The treasury of human inheritance 1951, In: , Cambridge, Cambridge University Press
2. Farabee WC. Hereditary and sexual influence in meristic variation: a study of malformations in man. PhD thesis, Harvard University. 1903
3. Gao B, Guo J, She C. Mutations in IHH, encoding Indian hedgehog, cause brachydactyly type A-1. Nat Genet 2001, 28(4):386-388.
4. McCready ME, Sweeney E, Fryer AE. A novel mutation in the IHH gene causes brachydactyly type A1: a 95-year-old mystery resolved. Hum Genet 2002, 111(4-5):368-375.
5. Gao B, Hu J, Stricker S. A mutation in Ihh that causes digit abnormalities alters its signalling capacity and range. Nature 2009, (in press)
6. Niedermaier M, Schwabe GC, Fees S. An inversion involving the mouse Shh locus results in brachydactyly through dysregulation of Shh expression. J Clin Invest 2005, 115(4):900-909.
7. Armour CM, McCready ME, Baig A, Hunter AG, Bulman DE. A novel locus for brachydactyly type A1 on chromosome 5p13.3-p13.2. J Med Genet 2002, 39(3):186-188.
8. Seemann P, Schwappacher R, Kjaer KW. Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J Clin Invest 2005, 115(9):2373-2381.
9. Kjaer KW, Eiberg H, Hansen L. A mutation in the receptor binding site of GDF5 causes Mohr-Wriedt brachydactyly type A2. J Med Genet 2006, 43(3):225-231.
10. Lehmann K, Seemann P, Boergermann J. A novel R486Q mutation in BMPR1B resulting in either a brachydactyly type C/symphalangism-like phenotype or brachydactyly type A2. Eur J Hum Genet 2006, 14(12):1248-1254.
11. Lehmann K, Seemann P, Stricker S. Mutations in bone morphogenetic protein receptor 1B cause brachydactyly type A2. Proc Natl Acad Sci USA 2003, 100(21):12277-12282.
12. Ploger F, Seemann P, Schmidt-von Kegler M. Brachydactyly type A2 associated with a defect in proGDF5 processing. Hum Mol Genet 2008, 17(9):1222-1233.
13. Dathe K, Kjaer KW, Brehm A. Duplicatons involving a conserved regulatory element downstream of BMP2 are associated with brachydydactyly type A2. Am J Hum Genet 2009, (in press)
14. Oldridge M, Fortuna AM, Maringa M. Dominant mutations in ROR2, encoding an orphan receptor tyrosine kinase, cause brachydactyly type B. Nat Genet 2000, 24(3):275-278.
15. Schwabe GC, Tinschert S, Buschow C. Distinct mutations in the receptor tyrosine kinase gene ROR2 cause brachydactyly type B. Am J Hum Genet 2000, 67(4):822-831.
16. Stricker S, Verhey van Wijk N, Witte F, Brieske N, Seidel K, Mundlos S. Cloning and expression pattern of chicken Ror2 and functional characterization of truncating mutations in brachydactyly type B and Robinow syndrome. Dev Dyn 2006, 235(12):3456-3465.
17. Hikasa H, Shibata M, Hiratani I, Taira M. The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 2002, 129(22):5227-5239.
18. Oishi I, Suzuki H, Onishi N. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 2003, 8(7):645-654.
19. Akbarzadeh S, Wheldon LM, Sweet SM, Talma S, Mardakheh FK, Heath JK. The deleted in brachydactyly B domain of ROR2 is required for receptor activation by recruitment of Src. PLoS ONE 2008, 3(3):e1873.
20. Winkel A, Stricker S, Tylzanowski P. Wnt-ligand-dependent interaction of TAK1 (TGF-beta-activated kinase-1) with the receptor tyrosine kinase Ror2 modulates canonical Wnt-signalling. Cell Signal 2008, 20(11):2134-2144.
21. DeChiara TM, Kimble RB, Poueymirou WT. Ror2, encoding a receptor-like tyrosine kinase, is required for cartilage and growth plate development. Nat Genet 2000, 24(3):271-274.
22. Takeuchi S, Takeda K, Oishi I. Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells 2000, 5(1):71-78.
23. Raz R, Stricker S, Gazzerro E. The mutation ROR2W749X, linked to human BDB, is a recessive mutation in the mouse, causing brachydactyly, mediating patterning of joints and modeling recessive Robinow syndrome. Development 2008, 135(9):1713-1723.
24. Sammar M, Stricker S, Schwabe G. Modulation of GDF5/BRI-b signaling through interaction with the tyrosine kinase receptor Ror2. Genes Cells 2004, (in press)
25. Lehmann K, Seemann P, Silan F. A new subtype of brachydactyly type B caused by point mutations in the bone morphogenetic protein antagonist NOGGIN. Am J Hum Genet 2007, 81(2):388-396.
26. Smith WC, Harland RM. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 1992, 70(5):829-840.
27. Brunet LJ, McMahon JA, McMahon AP, Harland RM. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 1998, 280(5368):1455-1457.
28. McMahon JA, Takada S, Zimmerman LB, Fan CM, Harland RM, McMahon AP. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev 1998, 12(10):1438-1452.
29. Groppe J, Greenwald J, Wiater E. Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 2002, 420(6916):636-642.
30. Gong Y, Krakow D, Marcelino J. Heterozygous mutations in the gene encoding noggin affect human joint morphogenesis. Nat Genet 1999, 21(3):302-304.
31. Polinkovsky A, Robin NH, Thomas JT. Mutations in CDMP1 cause autosomal dominant brachydactyly type C. Nat Genet 1997, 17(1):18-19.
32. Savarirayan R, White SM, Goodman FR. Broad phenotypic spectrum caused by an identical heterozygous CDMP-1 mutation in three unrelated families. Am J Med Genet 2003, 117A(2):136-142.
33. Schwabe GC, Turkmen S, Leschik G. Brachydactyly type C caused by a homozygous missense mutation in the prodomain of CDMP1. Am J Med Genet 2004, 124A(4):356-363.
34. Nohe A, Keating E, Knaus P, Petersen NO. Signal transduction of bone morphogenetic protein receptors. Cell Signal 2004, 16(3):291-299.
35. Gazzerro E, Canalis E. Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord 2006, 7(1-2):51-65.
36. Storm EE, Kingsley DM. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 1996, 122(12):3969-3979.
37. Francis-West PH, Parish J, Lee K, Archer CW. BMP/GDF-signalling interactions during synovial joint development. Cell Tissue Res 1999, 296(1):111-119.
38. Johnson D, Kan SH, Oldridge M. Missense mutations in the homeodomain of HOXD13 are associated with brachydactyly types D and E. Am J Hum Genet 2003, 72(4):984-997.
39. Dawson K, Seeman P, Sebald E. GDF5 is a second locus for multiple-synostosis syndrome. Am J Hum Genet 2006, 78(4):708-712.
40. Yang W, Cao L, Liu W. Novel point mutations in GDF5 associated with two distinct limb malformations in Chinese: brachydactyly type C and proximal symphalangism. J Hum Genet 2008, 53(4):368-374.
41. Mortlock DP, Innis JW. Mutation of HOXA13 in hand-foot-genital syndrome. Nat Genet 1997, 15(2):179-180.
42. Innis JW, Goodman FR, Bacchelli C. A HOXA13 allele with a missense mutation in the homeobox and a dinucleotide deletion in the promoter underlies Guttmacher syndrome. Hum Mutat 2002, 19(5):573-574.
43. Tufan F, Cefle K, Turkmen S. Clinical and molecular characterization of two adults with autosomal recessive Robinow syndrome. Am J Med Genet A 2005, 136(2):185-189.
44. Balci S, Ercal MD, Say B, Atasu M. Robinow syndrome: with special emphasis on dermatoglyphics and hand malformations (split hand). Clin Dysmorphol 1993, 2(3):199-207.
45. Patton MA, Afzal AR. Robinow syndrome. J Med Genet 2002, 39(5):305-310.
46. Mazzeu JF, Pardono E, Vianna-Morgante AM. Clinical characterization of autosomal dominant and recessive variants of Robinow syndrome. Am J Med Genet A 2007, 143(4):320-325.
47. Afzal AR, Rajab A, Fenske CD. Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat Genet 2000, 25(4):419-422.
48. van Bokhoven H, Celli J, Kayserili H. Mutation of the gene encoding the ROR2 tyrosine kinase causes autosomal recessive Robinow syndrome. Nat Genet 2000, 25(4):423-426.
49. Demirhan O, Turkmen S, Schwabe GC. A homozygous BMPR1B mutation causes a new subtype of acromesomelic chondrodysplasia with genital anomalies. J Med Genet 2005, 42(4):314-317.
50. Thomas JT, Kilpatrick MW, Lin K. Disruption of human limb morphogenesis by a dominant negative mutation in CDMP1. Nat Genet 1997, 17(1):58-64.
51. Thomas JT, Lin K, Nandedkar M, Camargo M, Cervenka J, Luyten FP. A human chondrodysplasia due to a mutation in a TGF-beta superfamily member. Nat Genet 1996, 12(3):315-317.
52. Faiyaz-Ul-Haque M, Ahmad W, Zaidi SH. Mutation in the cartilage-derived morphogenetic protein-1 (CDMP1) gene in a kindred affected with fibular hypoplasia and complex brachydactyly (DuPan syndrome). Clin Genet 2002, 61(6):454-458.
53. Douzgou S, Lehmann K, Mingarelli R, Mundlos S, Dallapiccola B. Compound heterozygosity for GDF5 in Du Pan type chondrodysplasia. Am J Med Genet A 2008, 146A(16):2116-2121.
54. Storm EE, Huynh TV, Copeland NG, Jenkins NA, Kingsley DM, Lee SJ. Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature 1994, 368(6472):639-643.
55. van Bokhoven H, Celli J, van Reeuwijk J. MYCN haploinsufficiency is associated with reduced brain size and intestinal atresias in Feingold syndrome. Nat Genet 2005, 37(5):465-467.
56. Kenney AM, Cole MD, Rowitch DH. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 2003, 130(1):15-28.
57. Ota S, Zhou ZQ, Keene DR, Knoepfler P, Hurlin PJ. Activities of N-Myc in the developing limb link control of skeletal size with digit separation. Development 2007, 134(8):1583-1592.
58. Kornak U, Mundlos S. Genetic disorders of the skeleton: a developmental approach. Am J Hum Genet 2003, 73(3):447-474.
59. Zou H, Wieser R, Massague J, Niswander L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev 1997, 11(17):2191-2203.
60. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, Tabin CJ. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2006, 2(12):e216.
61. Ovchinnikov DA, Selever J, Wang Y. BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev Biol 2006, 295(1):103-115.
62. Yoon BS, Pogue R, Ovchinnikov DA. BMPs regulate multiple aspects of growth-plate chondrogenesis through opposing actions on FGF pathways. Development 2006, 133(23):4667-4678.
63. de Crombrugghe B, Lefebvre V, Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr Opin Cell Biol 2001, 13(6):721-727.
64. Kuss P, Villavicencio-Lorini P, Witte F. Mutant Hoxd13 induces extra digits in a mouse model of synpolydactyly directly and by decreasing retinoic acid synthesis. J Clin Invest 2009, 119(1):146-156.
65. Albrecht AN, Schwabe GC, Stricker S, Boddrich A, Wanker EE, Mundlos S. The synpolydactyly homolog (spdh) mutation in the mouse -a defect in patterning and growth of limb cartilage elements. Mech Dev 2002, 112(1-2):53-67.
66. Koyama E, Ochiai T, Rountree RB. Synovial joint formation during mouse limb skeletogenesis: roles of Indian hedgehog signaling. Ann N Y Acad Sci 2007, 1116:100-112.
67. St-Jacques B, Hammerschmidt M, McMahon AP. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 1999, 13(16):2072-2086.
68. Pacifici M, Koyama E, Shibukawa Y. Cellular and molecular mechanisms of synovial joint and articular cartilage formation. Ann N Y Acad Sci 2006, 1068:74-86.
69. Hartmann C, Tabin CJ. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 2001, 104(3):341-351.
70. Pitsillides AA, Ashhurst DE. A critical evaluation of specific aspects of joint development. Dev Dyn 2008, 237(9):2284-2294.
71. Knosp WM, Scott V, Bachinger HP, Stadler HS. HOXA13 regulates the expression of bone morphogenetic proteins 2 and 7 to control distal limb morphogenesis. Development 2004, 131(18):4581-4592.
72. Li X, Nie S, Chang C, Qiu T, Cao X. Smads oppose Hox transcriptional activities. Exp Cell Res 2006, 312(6):854-864.
73. Williams TM, Williams ME, Heaton JH, Gelehrter TD, Innis JW. Group 13 HOX proteins interact with the MH2 domain of R-Smads and modulate Smad transcriptional activation functions independent of HOX DNA-binding capability. Nucleic Acids Res 2005, 33(14):4475-4484.
74. Spranger J. Pattern recognition in bone dysplasias. Prog Clin Biol Res 1985, 200:315-342.
75. Spranger J, Winterpacht A, Zabel B. The type II collagenopathies: a spectrum of chondrodysplasias. Eur J Pediatr 1994, 153(2):56-65.
76. Oltvai ZN, Barabasi AL. Systems biology. Life's complexity pyramid. Science 2002, 298(5594):763-764.
77. Stelzl U, Worm U, Lalowski M. A human protein-protein interaction network: a resource for annotating the proteome. Cell 2005, 122(6):957-968.
78. Barabasi AL, Oltvai ZN. Network biology: understanding the cell's functional organization. Nat Rev Genet 2004, 5(2):101-113.
79. Hartwell LH, Hopfield JJ, Leibler S, Murray AW. From molecular to modular cell biology. Nature 1999, 402(Suppl. 6761):C47-C52.
80. Alon U. Network motifs: theory and experimental approaches. Nat Rev Genet 2007, 8(6):450-461.
81. Oti M, Brunner HG. The modular nature of genetic diseases. Clin Genet 2007, 71(1):1-11.