Fibrodysplasia ossificans progressiva (FOP), a disorder of ectopic osteogenesis, misregulates cell surface expression and trafficking of BMPRIA

Journal of Bone and Mineral Research

Volumn 20, Issue 7, 2005, Pages 1168-1176

  Serrano De La Peña, Lourdes ^a,b   Billings, Paul C ^a   Fiori, Jennifer L ^a   Ahn, Jaimo ^a   Kaplan, Frederick S ^a   Shore, Eileen M ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

BMP; BMP receptors; Fibrodysplasia ossificans progressiva; Heterotopic ossification

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; CELL SURFACE PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BMPR1A; UNCLASSIFIED DRUG;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL GROWTH; CELL SURFACE; CONTROLLED STUDY; DISEASE COURSE; DNA BINDING; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTERNALIZATION; LYMPHOCYTE; OSSIFYING MYOSITIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CELL MEMBRANE; CELLS, CULTURED; HUMANS; MYOSITIS OSSIFICANS; OSTEOGENESIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 20844450082     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/JBMR.050305     Document Type: Article

References (42)

1. Kaplan FS, Shore EM, Connor JM 2002 Fibrodysplasia ossificans progressiva. In: Royce P, Steinmann B (eds.) Connective Tissue and Its Heritable Disorders, 2nd ed. Wiley-Liss. New York. NY, USA, pp. 827-840.
2. Kaplan FS, Shore EM, Zasloff MA 1996 Fibrodysplasia ossificans progressiva: Searching for the skeleton key. Calcif Tissue Int 59:75-78.
3. Kaplan FS, Tabas JA, Gannon FH, Finkel G, Hahn GV, Zasloff MA 1993 The histopathology of fibrodysplasia ossificans progressiva. An endochondral process. J Bone Joint Surg Am 75:220-230.
4. Gannon FH, Valentine BA, Shore EM, Zasloff MA, Kaplan FS 1998 Acute lymphocytic infiltration in an extremely early lesion of fibrodysplasia ossificans progressiva. Clin Orthop 346:19-25.
5. Cohen RB, Hahn GV, Tabas JA, Peeper J, Levitz CL, Sando A, Sando N, Zasloff M, Kaplan FS 1993 The natural history of heterotopic ossification in patients who have fibrodysplasia ossificans progressiva. A study of forty-four patients. J Bone Joint Surg Am 75:215-219.
6. Connor JM, Evans DAP 1982 Fibrodysplasia ossificans progressiva. The clinical features and natural history of 34 patients. J Bone Joint Surg Br 64:76-83.
7. Lanchoney TF, Cohen RB, Rocke DM, Zasloff MA, Kaplan FS 1995 Permanent heterotopic ossification at the injection site after diphtheria-tetanus- pertussis immunizations in children who have fibrodysplasia ossificans progressiva. J Pediatr 126:762-764.
8. Luchetti W, Cohen RB, Hahn GV, Rocke DM, Helpin M, Zasloff M, Kaplan FS 1996 Severe restriction in jaw movement after routine injection of local anesthetic in patients who have fibrodysplasia ossificans progressiva. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 81:21-25.
9. Glaser DL, Rocks DM, Kaplan FS 1998 Catastrophic falls in patients who have fibrodysplasia ossificans progressiva. Clin Orthop 346:110-116.
10. Kaplan FS, McCluskey W, Hahn G, Tabas JA, Muenke M, Zasloff MA 1993 Genetic transmission of fibrodysplasia ossificans progressiva. Report of a family. J Bone Joint Surg Am 75:1214-1220.
11. Feldman G, Li M, Martin S, Urbanek M, Urtizberea JA, Fardeau M, LeMerrer M, Connor JM, Triffitt J, Smith R, Muenke M, Kaplan FS, Shore EM 2000 Fibrodysplasia ossificans progressiva, a heritable disorder of severe heterotopic ossification, maps to human chromosome 4q27-31. Am J Hum Genet 66:128-135.
12. Xu M, Feldman G, Le Merrer M, Shugart YY, Glaser D, Urtizberea JA, Fardeau M, Connor JM, Triffitt J. Smith R, Shore EM, Kaplan FS 2000 Linkage exclusion and mutational analy-sis of the noggin gene in patients with fibrodysplasia ossificans progressiva. Clin Genet 58:291-298.
13. Sandhu HS, Khan SN 2002 Animal models for preclinical assessment of bone morphogenetic proteins in the spine. Spine 27:S32-S38.
14. Seeherman H, Wozney J, Li R 2002 Bone morphogenetic protein delivery systems. Spine 27:S16-S23.
15. Urist MR 1965 Bone formation by autoinduction. Science 150:893-899.
16. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA 1988 Novel regulators of bone formation: Molecular clones and activities. Science 242:1528-1534.
17. Kan L, Hu M, Gomes WA, Kessler JA 2004 Transgenic mice overexpressing BMP4 develop a fibrodysplasia ossificans progressiva (FOP)-like phenotype. Am J Pathol 165:1107-1115.
18. Hoffmann A, Gross G 2001 BMP signaling pathways in cartilage and bone formation. Crit Rev Eukaryot Gene Expr 11:23-45.
19. Glaser DL, Economides AN, Wang L, Liu X, Kimble RD, Fandl JP, Wilson JM, Stahl N, Kaplan FS, Shore EM 2003 In vivo somatic cell gene transfer of an engineered Noggin mutein prevents BMP4-induced heterotopic ossification. J Bone Joint Surg Am 85:2332-2342.
20. Massagué J, Blain SW, Lo RS 2000 TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103:295-309.
21. Derynck R, Zhang YE 2003 Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425:577-584.
22. Shi Y, Massague J 2003 Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700.
23. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J 1994 Mechanism of activation of the TGF-beta receptor. Nature 370:341-347.
24. Gilboa L, Nohe A, Geissendorfer T, Sebald W, Henis YI, Knaus P 2000 Bone morphogenetic protein receptor complexes on the surface of live cells: A new oligomerization mode for serine/threonine kinase receptors. Mol Biol Cell 11:1023-1035.
25. von Bubnoff A, Cho KW 2001 Intracellular BMP signaling regulation in vertebrates: Pathway or network? Dev Biol 239:1-14.
26. Attisano L, Wrana JL 2000 Smads as transcriptional comodulators. Curr Opin Cell Biol 12:235-243.
27. Canalis E, Economides AN, Gazzerro E 2003 Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24:218-235.
28. Shafritz AB, Shore EM, Gannon FH, Zasloff MA, Taub R, Muenke M, Kaplan FS 1996 Overexpression of an osteogenic morphogen in fibrodysplasia ossificans progressiva. N Engl J Med 335:555-561.
29. Gannon FH, Kaplan FS, Olmsted E, Finkel GC, Zasloff M, Shore E 1997 Bone morphogenetic protein (BMP) 2/4 in early fibromatous lesions of fibrodysplasia ossificans progressiva. Hum Pathol 28:339-343.
30. Olmsted EA, Kaplan FS, Shore EM 2003 Bone morphogenetic protein-4 regulation in fibrodysplasia ossificans progressiva. Clin Orthop 408:331-343.
31. Ahn J, Serrano de la Pena L, Shore EM, Kaplan FS 2003 Paresis of a bone morphogenetic protein antagonist response in a genetic disorder of heterotopic skeletogenesis. J Bone Joint Surg Am 85:667-674.
32. Ishisaki A, Yamato K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, ten Dijke P, Sugino H, Nishihara T 1999 Differential inhibition of Smado and SmadV on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. J Biol Chem 274:13637-13642.
33. Zimmerman LB, De Jesus-Escobar JM, Harland RM L996 The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86:599-606.
34. Bennett D, Alphey L 2002 PP1 binds Sara and negatively regulates Dpp signaling in Drosophila melanogaster. Nat Genet 31:419-423.
35. Haj FG, Verveer PJ, Squire A, Neel BG, Bastiaens PI 2002 Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science 295:1708-1711.
36. Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL 1998 SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 95:779-791.
37. Itoh F, Divecha N, Brocks L, Oomen L, Janssen H, Calafat J, Itoh S, Dijke Pt P 2002 The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signalling. Genes Cells 7:321-331.
38. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL 2003 Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5:410-421.
39. Rauch C, Brunet AC, Deleule J, Farge E 2002 C2C12 myoblast/osteoblast transdifferentiation steps enhanced by epigenetic inhibition of BMP2 endocytosis. Am J Physiol Cell Physiol 283:C235-C243.
40. Gilboa L, Wells RG, Lodish HF, Henis YI 1998 Oligomeric structure of type I and type II transforming growth factor beta receptors: Homodimers form in the ER and persist at the plasma membrane. J Cell Biol 140:767-777.
41. Dore JJ Jr, Edens M, Garamszegi N, Leof EB 1998 Heteromeric and homomeric transforming growth factor-beta receptors show distinct signaling and endocytic responses in epithelial cells. J Biol Chem 273:31770-31777.
42. Nohe A, Kassel S, Ehrlich M, Neubauer F, Sebald W, Henis YI, Knaus P 2002 The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem 277:5330-5338.