Bone morphogenetic protein receptors and activin receptors are highly expressed in ossified ligament tissues of patients with ossification of the posterior longitudinal ligament

American Journal of Pathology

Volumn 150, Issue 4, 1997, Pages 1335-1347

  Yonemori, Koji ^a   Imamura, Takeshi ^a,b,c   Ishidou, Yasuhiro ^a   Okano, Toshihiro ^a   Matsunaga, Shunji ^a   Yoshida, Hiroki ^a   Kato, Mitsuyasu ^b,c   Sampath, T Kuber ^d   Miyazono, Kohei ^b,c   Dijke, Peter Ten ^e   Sakou, Takashi ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b CANCER INSTITUTE   (Japan)

^c CANCER CHEMOTHERAPY CENTER   (Japan)

^d CURIS INC   (United States)

^e LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; CYTOKINE RECEPTOR;

AGED; ARTICLE; AUTOPSY; CASE REPORT; CELL DIFFERENTIATION; GROWTH REGULATION; HUMAN; IMMUNOHISTOCHEMISTRY; LIGAMENT CALCINOSIS; MALE; PATHOGENESIS; POSTERIOR LONGITUDINAL LIGAMENT; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN SYNTHESIS REGULATION; RECEPTOR DENSITY; TISSUE DISTRIBUTION;

ACTIVIN RECEPTORS; ADULT; AGED; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; FEMALE; HUMANS; LONGITUDINAL LIGAMENTS; MALE; MIDDLE AGED; OSSIFICATION, HETEROTOPIC; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 0030895267     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Key CA: On paraplegia depending on disease of ligaments of the spine. Guy's Hosp Rep 1838, 3:17-34
2. Tsukimoto H: A case report: autopsy of syndrome of compression of spinal cord owing to ossification within spinal canal of cervical spine, Arch Jap Chir 1960, 29:1003-1007 (in Japanese)
3. Sakou T, Matsunaga S, Epstein N: OPLL, ossification of the posterior longitudinal ligaments: epidemiology, pathology, pathogenesis, diagnosis, and treatment. Cervical Spondylosis and Similar Disorders of the Spine. Edited by K Yonenobu, T Sakou, K Ono. Tokyo, Springer, 1996, pp 29-37
4. Tsuyama N: Ossification of the posterior longitudinal ligament of the spine. Clin Orthop 1984, 184:71-84
5. Taketomi E, Sakou T, Matsunaga S, Yamaguchi M: Family study of a twin with ossification of the posterior longitudinal ligament in the cervical spine. Spine 1992, 17:55-56
6. Terayama K: Genetic studies on ossification of the posterior longitudinal ligament of the spine. Spine 1989, 14:1184-1191
7. Sakou T, Taketomi E, Matsunaga S, Yamaguchi M, Sonoda S, Yashiki S: Genetic study of ossification of the posterior longitudinal ligament in the cervical spine with human leukocyte antigen haplotype. Spine 1991, 16:1249-1252
8. Koga H, Hayashi K, Taketomi E, Matsunaga S, Yashiki S, Fujiyoshi T, Sonoda S, Sakou T: Restriction fragment length polymorphism of genes of the α2(XI) collagen, bone morphogenetic protein-2, alkaline phosphatase, and tumor necrosis factcr-α among patients with ossification of posterior longitudinal ligament and controls from the Japanese population. Spine 1996, 21:469-473
9. Okazaki T, Takuwa Y, Yamamoto M, Matsumoto T, Igarashi T, Kurokawa T, Ogata E: Ossification of the paravertebral ligaments: a frequent complication of hypoparathyroidism. Metabolism 1984, 33:710-713
10. Seichi A, Hoshino Y, Ohnishi I, Kurokawa T: The role of calcium metabolism abnormalities in the development of ossification of the posterior longitudinal ligament of the cervical spine. Spine 1992, 17:30-32
11. Yoshikawa S, Shiba M, Suzuki A: Spinal-cord compres- sion in untreated adult cases of vitamin-D resistant rickets. J Bone Joint Surg 1968, 50:743-752
12. Takeuchi Y, Matsumoto T, Takuwa Y, Hoshino Y, Kurokawa T, Shibuya N, Ogata E: High incidence of obesity and elevated serum immunoreactive insulin level in patients with paravertebral ligamentous ossification: a relationship to the development of ectopic ossification. J Bone Miner Metab 1989, 7:17-21
13. Matsunaga S, Sakou T, Taketomi E, Nakanishi K: Effects of strain distribution in the intervertebral discs on the progression of ossification of the posterior longitudinal ligaments, Spine 1996, 21:184-189
14. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA: Novel regulators of bone formation: molecular clones and activities. Science 1988, 242:1528-1534
15. Wang EA, Rosen V, D'Alessandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, LaPan P, Luxemberg DP, McQuaid D, Moutsatsos IK, Move J, Wozney JM: Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 1990, 87:2220-2224
16. Reddi AH: Bone and cartilage differentiation. Curr Opin Genet Dev 1994, 4:737-744
17. Wozney JM: Bone morphogenetic proteins. Prog Growth Factor Res 1989, 1:267-280
18. Vukicevic S, Luyten FP, Reddi AH: Stimulation of the expression of osteogenic and chondrogenic phenotypes in vitro by osteogenin, Proc Natl Acad Sci USA 1989, 86:8793-8797
19. Sampath TK, Maliakal JC, Hauschka PV, Jones WK, Sasak H, Tucker RF, White KH, Coughlin JE, Tucker MM, Pang RHL, Corbett C, Özkaynak E, Oppermann H, Rueger DC: Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation In vitro. J Biol Chem 1992, 267:20352-20362
20. Lyons KM, Jones CM, Hogan BLM: The DVR gene family in embryonic development. Trends Genet 1991, 7:408-412
21. Kingsley DM, Bland AE, Grubber JM, Marker PC, Russell LB, Copeland NG, Jenkins NA: The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF-β superfamily. Cell 1992, 71:399-410
22. Winnier G, Blessing M, Labosky PA, Hogan BLM: Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 1995, 9:2105-2116
23. Luo G, Hofmann C, Bronckers ALJJ, Sohocki M, Bradley A, Karsenty G: BMP-7 is an inducer of nephrogenesis and is also required for eye development and skeletal patterning. Genes Dev 1995, 9:2808-2820
24. Dudley AT, Lyons KM, Robertson EJ: A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 1995, 9:2795-2807
25. Vale W, Hsueh A, Rivier C, Yu J: The inhibin/activin family of hormones and growth factors. Peptide Growth Factors and Their Receptors, part II. Edited by MB Sporn, AB Roberts. Berlin, Springer-Verlag, 1990, pp 211-248
26. Feijen A, Goumans MJ, van den Eijnden-van Raaij AJM: Expression of activin subunits, activin receptors, and follistatin in postimplantation mouse embryos suggests specific developmental functions for different activins. Development 1994, 120:3621-3637
27. Murata M, Eto Y, Shibai H, Sakai M, Muramatsu M: Erythroid differentiation factor is encoded by the same mRNA as that of the inhibin βA chain. Proc Natt Acad Sci USA 1988, 85:2434-2438
28. Smith JC, Price BMJ, van Nimmen K, Huylebroeck D: Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 1990, 345:729-731
29. Thomsen G, Woolf T, Whitman M, Sokol S, Vaughan J, Vale W, Melton DA: Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 1990, 63:485-493
30. Centrella M, McCarthy TL, Canalis E: Activin-A binding and biochemical effects in osteoblasts-enriched cultures from fetal-rat parietal bone. Mol Cell Biol 1991, 11:250-258
31. Ogawa Y, Schmidt DK, Nathan RM, Armstrong RM, Miller KL, Sawamura SJ, Ziman JM, Erickson KL, de Leon ER, Rosen DM, Seyedin SM, Glaser CB, Chang R-J, Corrigan AZ, Vale W: Bovine bone activin enhances bone morphogenetic protein-induced ectopic bone formation, J Biol Chem 1992, 267:14233-14237
32. Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R, Bradley A: Functional analysis of activins during mammalian development. Nature 1995, 374:354-356
33. Vassalli A, Matzuk MM, Gardner HAR, Lee K-F, Jaenisch R: Activin/inhibin βB subunit gene disruption leads to defects in eyelid development and female reproduction, Genes Dev 1994, 8:414-427
34. Kingsley DM: The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 1994, 8:133-146
35. Massagué J, Attisano L, Wrana JL: The TGF-β family and its composite receptors. Trends Cell Biol 1994, 4:172-178
36. ten Dijke P, Miyazono K, Heldin C-H: Signaling via hetero-oligomeric complexes of type I and type II serine/threonine kinase receptors, Curr Opin Cell Biol 1996, 8:139-145
37. ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, Riddle DL, Ichijo H, Heldin C-H, Miyazono K: Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4, J Biol Chem 1994, 269:16985-16988
38. Koenig BB, Cook JS, Wolsing DH, Ting J, Tiesman JP, Correa PE, Oison CA, Pecquet AL, Ventura F, Grant RA, Chen G-X, Wrana JL, Massagué J, Rosenbaum JS: Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol Cell Biol 1994, 14:5961-5974
39. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, Heldin C-H, Miyazono K: Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 1995, 92:7632-7636
40. Liu F, Ventura F, Doody J, Massagué J: Human type II receptor for bone morphogenetic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol Cell Biol 1995, 15:3479-3486
41. Nohno T, Ishikawa T, Saito T, Hosokawa K, Noji S, Wolsing DH, Rosenbaum JS: Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogenetic protein type I receptors. J Biol Chem 1995, 270:22522-22526
42. Dewulf N, Verschueren K, Lonnoy O, Morén A, Grimsby S, vande Spiegle K, Miyazono K, Huylebroeck D, ten Dijke P: Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 1995, 136:2652-2663
43. Ishidou Y, Kitajima I, Obama H, Maruyama I, Murata F, Imamura T, Yamada N, ten Dijke P, Miyazono K, Sakou T: Enhanced expression of type I receptors for bone morphogenetic proteins during bone formation. J Bone Miner Res 1995, 10:1651-1659
44. Attisano L, Carcamo J, Ventura F, Weis FMB, Massagué J, Wrana JL: Identification of human activin and TGF-β type I receptors that form heteromeric kinase complexes with type II receptors. Cell 1993, 75:671-680
45. Attisano L, Wrana, JL, Cheifetz S, Massagué J: Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 1992, 68:97-108
46. Mathews LS, Vale WW: Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 1991, 65:973-982
47. Tsuchida K, Mathews LS, Vale WW: Cloning and characterization of a transmembrane serine kinase that acts as an activin type I receptor. Proc Natl Acad Sci USA 1993, 90:11242-11246
48. Cárcamo J, Weis FMB, Ventura F, Wieser R, Wrana JL, Attisano L, Massagué J: Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor-β and activin. Mol Cell Biol 1994, 14:3810-3821
49. ten Dijke P, Yamashita H, Ichijo H, Franzén P, Laiho M, Miyazono K, Heldin C-H: Characterization of type I receptors for transforming growth factor-β and activin. Science 1994, 264:101-104
50. Tsuchida K, Vangham JM, Wiater E, Gaddy-Kurten D, Vale WW: Inactivation of activin-dependent transcrip- tion by kinase-deficient activin receptors. Endocrinology 1995, 136:5493-5503
51. Yamashita H, ten Dijke P, Huylebroeck D, Sampath TK, Andries M, Smith JC, Heldin C-H, Miyazono K: Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J Cell Biol 1995, 130:217-226
52. Matzuk MM, Kumar TR, Bradley A: Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 1995, 374:356-360
53. Ichijo H, Yamashita H, ten Dijke P, Eto Y, Heldin C-H, Miyazono K: Characterization of in vivo phosphorylation of activin type II receptor. Biochem Biophys Res Commun 1993, 194:1508-1514
54. Waltenberger J, Lundin L, Öberg K, Wilander E, Miyazono K, Heldin C-H, Funa K: Involvement of transforming growth factor-β in the formation of fibrotic lesions in carcinoid heart disease. Am J Pathol 1993, 142:71-78
55. Vukicevic S, Latin V, Chen P, Batorsky R, Reddi AH, Sampath TK: Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: high affinity binding to basement membranes, Biochem Biophys Res Commun 1994, 198:693-700
56. Hsu SM, Raine L, Fanger H: Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 1981, 29:577-580
57. Sampath TK, Coughlin JE, Whetstone RM, Banach D, Corbett C, Ridge RJ, Özkaynak E, Oppermann H, Rueger DC: Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-β superfamily. J Biol Chem 1990, 265:13198-13205
58. Ishida Y, Kawai S: Effects of bone-seeking hormones on DNA synthesis, cyclic AMP level, and alkaline phosphatase activity in cultured cells from human posterior longitudinal ligament of the spine. J Bone Miner Res 1993, 8:1291-1300
59. Kon T, Yamazaki M, Tagawa M, Goto S, Terakado A, Moriya H, Fujimura S: Bone morphogenetic protein-2 stimulates differentiation of cultured spinal ligament cells from patients with ossification of the posterior longitudinal ligament. Calcif Tissue Int 1997 (in press)
60. Resnick D, Guerra J Jr, Robinson CA, Vint VC: Association of diffuse idiopathic skeletal hyperostosis (DISH) and calcification and ossification of the posterior longitudinal ligament. Am J Roentgenol 1978, 131:1049-1053
61. Asahina I, Sampath TK, Hauschka PV: Human osteogenic protein-1 induces chondroblastic, osteoblastic, and/or adipocytic differentiation of clonal murine target cells. Exp Cell Res 1996, 222:38-47
62. Kawaguchi H, Kurokawa T, Hoshino Y, Kawahara H, Ogata E, Matsumoto T: Immunohistochemical demonstration of bone morphogenetic protein-2 and trans- forming growth factor-β in the ossification of the posterior longitudinal ligament of the cervical spine. Spine 1992, 17:33-36
63. Asahina I, Sampath TK, Nishimura I, Hauschka PV: Human osteogenic protein-1 induces both chondroblastic and osteoblastic differentiation of osteoprogenitor cells derived from newborn rat calvaria. J Cell Biol 1993, 123:921-933
64. Miyamoto S, Takaoka K, Yonenobu K, Ono K: Ossification of the ligamentum flavum induced by bone morphogenetic protein. J Bone Joint Surg 1992, 74-B:279-283
65. Takeda K, Oida S, Ichijo H, Iimura T, Maruoka Y, Ama- gasa T, Sasaki S: Molecular cloning of rat bone morphogenetic protein (BMP) type IA receptor and its expression during ectopic bone formation induced by BMP, Biochem Biophys Res Commun 1994, 204:203-209
66. Tanno T: Experimental study on the spinal lesions in hyperostotic mouse (twy/twy): Special reference to the pathogenesis of the ossification of the spinal ligaments and to the action of ethane-1 hydroxy-1, 1-diphosphonate (EHDP), Nippon-Seikeigeka-Gakkai-Zasshi 1992, 66:1073-1083 (in Japanese)
67. Zucker LM, Zucker TF: Fatty, a new mutation in the rat. J Hered 1961, 52: 275-278