Deregulated bone morphogenetic protein receptor signaling underlies fibrodysplasia ossificans progressiva

Current Pharmaceutical Design

Volumn 18, Issue 27, 2012, Pages 4087-4092

  de Gorter, David J J ^a,b   Jankipersadsing, Vishant ^a   Dijke, Peter Ten ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Activin receptor like kinase 2; ALK2 R206H; BMP; Fibrodysplasia ossificans progressiva; Heterotopic ossification; Osteoblast differentiation

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 2; BONE MORPHOGENETIC PROTEIN RECEPTOR; PROCOLLAGEN C PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME 2; CHROMOSOME MUTATION; CLINICAL FEATURE; CONGENITAL BONE DISEASE; DIAGNOSTIC PROCEDURE; DISEASE COURSE; GENETIC CODE; HALLUX; HETEROTOPIC OSSIFICATION; HUMAN; OSSIFYING MYOSITIS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACTIVIN RECEPTORS, TYPE I; ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; HUMANS; MUTATION; MYOSITIS OSSIFICANS; OSSIFICATION, HETEROTOPIC; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84866314332     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161212802430495     Document Type: Article

References (69)

1. Connor JM, Skirton H, Lunt PW. A three generation family with fibrodysplasia ossificans progressiva. J Med Genet 1993; 30(8): 687-689.
2. Kaplan FS, McCluskey W, Hahn G, Tabas JA, Muenke M, Zasloff MA. Genetic transmission of fibrodysplasia ossificans progressiva. Report of a family. J Bone Joint Surg Am 1993; 75(8): 1214-1220.
3. Shore EM, Xu M, Feldman GJ, et al. A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Genet 2006; 38(5): 525-527.
4. Groppe JC, Shore EM, Kaplan FS. Functional modeling of the ACVR1 (R206H) mutation in FOP. Clin Orthop Relat Res 2007; 462: 87-92.
5. Shen Q, Little SC, Xu M, et al. The fibrodysplasia ossificans progressiva R206H ACVR1 mutation activates BMP-independent chondrogenesis and zebrafish embryo ventralization. J Clin Invest 2009; 119(11): 3462-3472.
6. van Dinther M, Visser N, de Gorter DJJ, et al. ALK2 R206H mutation linked to fibrodysplasia ossificans progressiva confers constitutive activity to the BMP type I receptor and sensitizes mesenchymal cells to BMP-induced osteoblast differentiation and bone formation. J Bone Miner Res 2010; 25(6): 1208-1215.
7. Kaplan FS, Xu M, Seemann P, et al. Classic and atypical fibrodysplasia ossificans progressiva (FOP) phenotypes are caused by mutations in the bone morphogenetic protein (BMP) type I receptor ACVR1. Hum Mutat 2009; 30(3): 379-390.
8. Shore EM, Kaplan FS. Insights from a rare genetic disorder of extra-skeletal bone formation, fibrodysplasia ossificans progressive (FOP). Bone 2008; 43(3): 427-433.
9. Bocciardi R, Bordo D, Di DM, Di RM, Ravazzolo R. Mutational analysis of the ACVR1 gene in Italian patients affected with fibrodysplasia ossificans progressiva: confirmations and advancements. Eur J Hum Genet 2009; 17(3): 311-318.
10. Carvalho DR, Navarro MM, Martins BJ, et al. Mutational screening of ACVR1 gene in Brazilian fibrodysplasia ossificans progressiva patients. Clin Genet 2010; 77(2): 171-176.
11. Furuya H, Ikezoe K, Wang L, et al. A unique case of fibrodysplasia ossificans progressiva with an ACVR1 mutation, G356D, other than the common mutation (R206H). Am J Med Genet A 2008; 146A(4): 459-463.
12. Schober P, Krage R, Thone D, Loer SA, Schwarte LA. Ultrasoundguided ankle block in stone man disease, fibrodysplasia ossificans progressiva. Anesth Analg. 2009; 109(3): 988-990.
13. Smith R. Fibrodysplasia (myositis) ossificans progressiva. Clinical lessons from a rare disease. Clin Orthop Relat Res 1998; (346): 7-14.
14. Cohen RB, Hahn GV, Tabas JA, et al. The natural history of heterotopic ossification in patients who have fibrodysplasia ossificans progressiva. A study of forty-four patients. J Bone Joint Surg Am 1993; 75(2): 215-219.
15. Connor JM, Evans DA. Fibrodysplasia ossificans progressiva. The clinical features and natural history of 34 patients. J Bone Joint Surg Br 1982; 64(1): 76-83.
16. Kaplan FS, Le MM, Glaser DL, et al. Fibrodysplasia ossificans progressiva. Best Pract Res Clin Rheumatol 2008; 22(1): 191-205.
17. Glaser DL, Rocke DM, Kaplan FS. Catastrophic falls in patients who have fibrodysplasia ossificans progressiva. Clin Orthop Relat Res. 1998; (346): 110-116.
18. Lanchoney TF, Cohen RB, Rocke DM, Zasloff MA, Kaplan FS. Permanent heterotopic ossification at the injection site after diphtheria-tetanus-pertussis immunizations in children who have fibrodysplasia ossificans progressiva. J Pediatr 1995; 126(5 Pt 1): 762-764.
19. Scarlett RF, Rocke DM, Kantanie S, Patel JB, Shore EM, Kaplan FS. Influenza-like viral illnesses and flare-ups of fibrodysplasia ossificans progressiva. Clin Orthop Relat Res 2004; (423): 275-279.
20. Kaplan FS, Shen Q, Lounev V, et al. Skeletal metamorphosis in fibrodysplasia ossificans progressiva (FOP). J Bone Miner Metab 2008; 26(6): 521-530.
21. Kaplan FS, Zasloff MA, Kitterman JA, Shore EM, Hong CC, Rocke DM. Early mortality and cardiorespiratory failure in patients with fibrodysplasia ossificans progressiva. J Bone Joint Surg Am 2010; 92(3): 686-691.
22. Kaplan FS, Glaser D, Shore EM, et al. The Phenotype of Fibrodysplasia Ossificans Progressiva. Clin Rev Bone Miner Metab 2005;3(3/4): 183-188.
23. Bridges AJ, Hsu KC, Singh A, Churchill R, Miles J. Fibrodysplasia (myositis) ossificans progressiva. Semin Arthritis Rheum 1994; 24(3): 155-164.
24. Connor JM, Evans DA. Genetic aspects of fibrodysplasia ossificans progressiva. J Med Genet 1982; 19(1): 35-39.
25. Kaplan FS, Tabas JA, Zasloff MA. Fibrodysplasia ossificans progressiva: a clue from the fly? Calcif Tissue Int 1990; 47(2): 117-125.
26. Shafritz AB, Shore EM, Gannon FH, et al. Overexpression of an osteogenic morphogen in fibrodysplasia ossificans progressiva. N Engl J Med 1996; 335(8): 555-561.
27. Kan L, Hu M, Gomes WA, Kessler JA. Transgenic mice overexpressing BMP4 develop a fibrodysplasia ossificans progressive (FOP)-like phenotype. Am J Pathol 2004; 165(4): 1107-1115.
28. de la Pena LS, Billings PC, Fiori JL, Ahn J, Kaplan FS, Shore EM. Fibrodysplasia ossificans progressiva (FOP), a disorder of ectopic osteogenesis, misregulates cell surface expression and trafficking of BMPRIA. J Bone Miner Res 2005; 20(7): 1168-1176.
29. Fiori JL, Billings PC, de La Pena LS, Kaplan FS, Shore EM. Dysregulation of the BMP-p38 MAPK signaling pathway in cells from patients with fibrodysplasia ossificans progressiva (FOP). J Bone Miner Res 2006; 21(6): 902-909.
30. Kaplan FS, Fiori J, de La Pena LS, Ahn J, Billings PC, Shore EM. Dysregulation of the BMP-4 signaling pathway in fibrodysplasia ossificans progressiva. Ann NY Acad Sci 2006; 1068: 54-65.
31. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J. Mechanism of activation of the TGF-[1] receptor. Nature 1994; 370(6488): 341-347.
32. Franzen P, Heldin CH, Miyazono K. The GS domain of the transforming growth factor-[1] type I receptor is important in signal transduction. Biochem Biophys Res Commun 1995; 207(2): 682-689.
33. Wieser R, Wrana JL, Massague J. GS domain mutations that constitutively activate T β R-I, the downstream signaling component in the TGF-β receptor complex. EMBO J 1995; 14(10): 2199-208.
34. Chen YG, Liu F, Massague J. Mechanism of TGF β receptor inhibition by FKBP12. EMBO J. 1997; 16(13): 3866-3876.
35. Huse M, Chen YG, Massague J, Kuriyan J. Crystal structure of the cytoplasmic domain of the type I TGF β receptor in complex with FKBP12. Cell 1999; 96(3): 425-436.
36. Yamaguchi T, Kurisaki A, Yamakawa N, Minakuchi K, Sugino H. FKBP12 functions as an adaptor of the Smad7-Smurf1 complex on activin type I receptor. J Mol Endocrinol 2006; 36(3): 569-579.
37. Yao D, Dore JJ, Jr., Leof EB. FKBP12 is a negative regulator of transforming growth factor-[1] receptor internalization. J Biol Chem 2000; 275(17): 13149-13154.
38. Fujii M, Takeda K, Imamura T, et al. Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol Biol Cell 1999; 10(11): 3801-3813.
39. Fukuda T, Kohda M, Kanomata K, et al. Constitutively activated ALK2 and increased SMAD1/5 cooperatively induce bone morphogenetic protein signaling in fibrodysplasia ossificans progressiva. J Biol Chem 2009; 284(11): 7149-7156.
40. Yu PB, Deng DY, Lai CS, et al. BMP type I receptor inhibition reduces heterotopic ossification. Nat Med 2008; 14(12): 1363-1369.
41. Gannon FH, Glaser D, Caron R, Thompson LD, Shore EM, Kaplan FS. Mast cell involvement in fibrodysplasia ossificans progressiva. Hum Pathol 2001; 32(8): 842-848.
42. Gannon FH, Valentine BA, Shore EM, Zasloff MA, Kaplan FS. Acute lymphocytic infiltration in an extremely early lesion of fibrodysplasia ossificans progressiva. Clin Orthop Relat Res 1998(346): 19-25.
43. Kan L, Liu Y, McGuire TL, et al. Dysregulation of local stem/progenitor cells as a common cellular mechanism for heterotopic ossification. Stem Cells 2009; 27(1): 150-156.
44. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. Conversion of vascular endothelial cells into multipotent stemlike cells. Nat Med 2010; 16(12): 1400-1406.
45. Jackson WM, Aragon AB, Onodera J, et al. Cytokine expression in muscle following traumatic injury. J Orthop Res 2011; 29(10): 1613-1620.
46. Shen W, Li Y, Zhu J, Schwendener R, Huard J. Interaction between macrophages, TGF-β1, and the COX-2 pathway during the inflammatory phase of skeletal muscle healing after injury. J Cell Physiol 2008; 214(2): 405-412.
47. Lounev VY, Ramachandran R, Wosczyna MN, et al. Identification of progenitor cells that contribute to heterotopic skeletogenesis. J Bone Joint Surg Am 2009; 91(3): 652-663.
48. Suda RK, Billings PC, Egan KP, et al. Circulating osteogenic precursor cells in heterotopic bone formation. Stem Cells 2009; 27(9): 2209-2219.
49. Lin GT, Chang HW, Liu CS, Huang PJ, Wang HC, Cheng YM. De novo 617G-A nucleotide mutation in the ACVR1 gene in a Taiwanese patient with fibrodysplasia ossificans progressiva. J Hum Genet 2006; 51(12): 1083-1086.
50. Nakajima M, Haga N, Takikawa K, Manabe N, Nishimura G, Ikegawa S. The ACVR1 617G>A mutation is also recurrent in three Japanese patients with fibrodysplasia ossificans progressiva. J Hum Genet 2007; 52(5): 473-475.
51. Fukuda T, Kanomata K, Nojima J, et al. A unique mutation of ALK2, G356D, found in a patient with fibrodysplasia ossificans progressiva is a moderately activated BMP type I receptor. Biochem Biophys Res Commun 2008; 377(3): 905-909.
52. Ratbi I, Borcciadi R, Regragui A, Ravazzolo R, Sefiani A. Rarely occurring mutation of ACVR1 gene in Moroccan patient with fibrodysplasia ossificans progressiva. Clin Rheumatol 2010; 29(1): 119-121.
53. Petrie KA, Lee WH, Bullock AN, et al. Novel mutations in ACVR1 result in atypical features in two fibrodysplasia ossificans progressiva patients. PLoS One 2009; 4(3): e5005.
54. Tung CH, Lai NS. Fibrodysplasia ossificans progressiva seen on three-dimensional computed tomography. Arthritis Rheum 2008; 58(1): 250.
55. Tulchinsky M. Diagnostic features of fibrodysplasia (myositis) ossificans progressiva on bone scan. Clin Nucl Med 2007; 32(8): 616-619.
56. Kulwin R, Binkovitz LA. PET/CT of fibrodysplasia ossificans progressiva. Pediatr Radiol 2009; 39(9): 991-994.
57. Kaplan FS, Xu M, Glaser DL, et al. Early diagnosis of fibrodysplasia ossificans progressiva. Pediatrics. 2008; 121(5): e1295-e1300.
58. Lee DY, Cho TJ, Lee HR, et al. ACVR1 gene mutation in sporadic Korean patients with fibrodysplasia ossificans progressiva. J Korean Med Sci 2009; 24(3): 433-437.
59. Sun Y, Xia W, Jiang Y, et al. A recurrent mutation c.617G>A in the ACVR1 gene causes fibrodysplasia ossificans progressiva in two Chinese patients. Calcif Tissue Int 2009; 84(5): 361-365.
60. Glaser D, Kaplan F. Treatment Considerations for the Management of Fibrodysplasia Ossificans Progressiva. Clin Rev Bone Miner Metab 2005; 3(3/4): 243-250.
61. Yu PB, Hong CC, Sachidanandan C, et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 2008; 4(1): 33-41.
62. Hao J, Ho JN, Lewis JA, et al. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol 2010; 5(2): 245-253.
63. Shi S, Hoogaars WM, de Gorter DJJ, et al. BMP antagonists enhance myogenic differentiation and ameliorate the dystrophic phenotype in a DMD mouse model. Neurobiol Dis 2011; 41(2): 353-360.
64. Cuny GD, Yu PB, Laha JK, et al. Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg Med Chem Lett 2008; 18(15): 4388-4392.
65. Kaplan J, Kaplan FS, Shore EM. Restoration of normal BMP signaling levels and osteogenic differentiation in FOP mesenchymal progenitor cells by mutant allele-specific targeting. Gene Ther 2011; doi:10.1038/gt.2011.152.
66. Takahashi M, Katagiri T, Furuya H, Hohjoh H. Disease-causing allele-specific silencing against the ALK2 mutants, R206H and G356D, in fibrodysplasia ossificans progressiva. Gene Ther 2011; doi: 10.1038/gt.2011.193.
67. van Ommen GJ, van Deutekom J, Aartsma-Rus A. The therapeutic potential of antisense-mediated exon skipping. Curr Opin Mol Ther 2008; 10(2): 140-149.
68. van Deutekom JC, Janson AA, Ginjaar IB, et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007; 357(26): 2677-2686.
69. Shimono K, Tung WE, Macolino C, et al. Potent inhibition of heterotopic ossification by nuclear retinoic acid receptor-γ agonists. Nat Med 2011; 17(4): 454-460.