Fibrodysplasia ossificans progressiva-related activated activin-like kinase signaling enhances osteoclast formation during heterotopic ossification in muscle tissues

Journal of Biological Chemistry

Volumn 289, Issue 24, 2014, Pages 16966-16977

  Yano, Masato ^a   Kawao, Naoyuki ^a   Okumoto, Katsumi ^a   Tamura, Yukinori ^a   Okada, Kiyotaka ^a   Kaji, Hiroshi ^a  

^a KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; ENZYMES; GLYCOPROTEINS; HISTOLOGY; MAMMALS; MOLECULAR BIOLOGY; MUSCLE;

BONE MORPHOGENETIC PROTEINS; CONDITIONED MEDIUM; HETEROTOPIC OSSIFICATION; MOLECULAR PATHOGENESIS; OSTEOCLAST FORMATION; RAW 264.7 CELLS; SUBCUTANEOUS TISSUES; TRANSFORMING GROWTH FACTORS;

CELL SIGNALING;

ACTIVIN LIKE KINASE 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; GENE ACTIVATION; GENE MUTATION; GENETIC TRANSFECTION; HETEROTOPIC OSSIFICATION; MOLECULAR PATHOLOGY; MOUSE; MUSCLE TISSUE; NONHUMAN; OSSIFYING MYOSITIS; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE; TISSUE DISTRIBUTION;

BONE; BONE MORPHOGENETIC PROTEIN (BMP); MUSCLE; OSTEOCLAST; TRANSFORMING GROWTH FACTOR Β (TGF-Β);

ACTIVIN RECEPTORS, TYPE I; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MUSCLE, SKELETAL; MUTATION, MISSENSE; MYOBLASTS; MYOSITIS OSSIFICANS; NIH 3T3 CELLS; OSSIFICATION, HETEROTOPIC; OSTEOCLASTS; OSTEOGENESIS; RATS; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84902438329     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526038     Document Type: Article

References (44)

1. Shore, E. M., and Kaplan, F. S. (2008) Insights from a rare genetic disorder of extra-skeletal bone formation, fibrodysplasia ossificans progressiva (FOP). Bone 43, 427-433
2. Shore, E. M., Xu, M., Feldman, G. J., Fenstermacher, D. A., Cho, T. J., Choi, I. H., Connor, J. M., Delai, P., Glaser, D. L., LeMerrer, M., Morhart, R., Rogers, J. G., Smith, R., Triffitt, J. T., Urtizberea, J. A., Zasloff, M., Brown, M. A., and Kaplan, F. S. (2006) A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat. Genet. 38, 525-527
3. Fukuda, T., Kohda, M., Kanomata, K., Nojima, J., Nakamura, A., Kamizono, J., Noguchi, Y., Iwakiri, K., Kondo, T., Kurose, J., Endo, K., Awakura, T., Fukushi, J., Nakashima, Y., Chiyonobu, T., Kawara, A., Nishida, Y., Wada, I., Akita, M., Komori, T., Nakayama, K., Nanba, A., Maruki, Y., Yoda, T., Tomoda, H., Yu, P. B., Shore, E. M., Kaplan, F. S., Miyazono, K., Matsuoka, M., Ikebuchi, K., Ohtake, A., Oda, H., Jimi, E., Owan, I., Okazaki, Y., and Katagiri, T. (2009) Constitutively activated ALK2 and increased SMAD1/5 cooperatively induce bone morphogenetic protein signaling in fibrodysplasia ossificans progressiva. J. Biol. Chem. 284, 7149-7156
4. Kaplan, F. S., Chakkalakal, S. A., and Shore, E. M. (2012) Fibrodysplasia ossificans progressiva: mechanisms and models of skeletal metamorphosis. Dis. Model. Mech. 5, 756-762
5. Nakaoka, D., Sugimoto, T., Kaji, H., Kanzawa, M., Yano, S., Yamauchi, M., Sugishita, T., and Chihara, K. (2001) Determinants of bone mineral density and spinal fracture risk in postmenopausal Japanese women. Osteoporos. Int. 12, 548-554 (Pubitemid 32777430)
6. Lang, T. F. (2011) The bone-muscle relationship in men and women. J. Osteoporos. 2011, 702735-702739
7. Richards, R. R., McKee, M. D., Paitich, C. B., Anderson, G. I., and Bertoia, J. T. (1991) A comparison of the effects of skin coverage and muscle flap coverage on the early strength of union at the site of osteotomy after devascularization of a segment of canine tibia. J. Bone Joint Surg. Am. 73, 1323-1330
8. Hisa, I., Inoue, Y., Hendy, G. N., Canaff, L., Kitazawa, R., Kitazawa, S., Komori, T., Sugimoto, T., Seino, S., and Kaji, H. (2011) Parathyroid hormone-responsive Smad3-related factor, Tmem119, promotes osteoblast differentiation and interacts with the bone morphogenetic protein-Runx2 pathway. J. Biol. Chem. 286, 9787-9796
9. Tanaka, K., Inoue, Y., Hendy, G. N., Canaff, L., Katagiri, T., Kitazawa, R., Komori, T., Sugimoto, T., Seino, S., and Kaji, H. (2012) Interaction of Tmem119 and the bone morphogenetic protein pathway in the commitment of myoblastic into osteoblastic cells. Bone 51, 158-167
10. Tanaka, K., Matsumoto, E., Higashimaki, Y., Katagiri, T., Sugimoto, T., Seino, S., and Kaji, H. (2012) Role of osteoglycin in the linkage between muscle and bone. J. Biol. Chem. 287, 11616-11628
11. Tanaka, K., Matsumoto, E., Higashimaki, Y., Sugimoto, T., Seino, S., and Kaji, H. (2012) FAM5C is a soluble osteoblast differentiation factor linking muscle to bone. Biochem. Biophys. Res. Commun. 418, 134-139
12. Henriksen, K., Bollerslev, J., Everts, V., and Karsdal, M. A. (2011) Osteoclast activity and subtypes as a function of physiology and pathology-implications for future treatments of osteoporosis. Endocr. Rev. 32, 31-63
13. O'Brien, C. A., Nakashima, T., and Takayanagi, H. (2013) Osteocyte control of osteoclastogenesis. Bone 54, 258-263
14. Yasui, T., Kadono, Y., Nakamura, M., Oshima, Y., Matsumoto, T., Masuda, H., Hirose, J., Omata, Y., Yasuda, H., Imamura, T., Nakamura, K., and Tanaka, S. (2011) Regulation of RANKL-induced osteoclastogenesis by TGF-β through molecular interaction between Smad3 and Traf6. J. Bone Miner. Res. 26, 1447-1456
15. Jensen, E. D., Pham, L., Billington, C. J., Jr., Espe, K., Carlson, A. E., Westendorf, J. J., Petryk, A., Gopalakrishnan, R., and Mansky, K. (2010) Bone morphogenic protein 2 directly enhances differentiation of murine osteoclast precursors. J. Cell. Biochem. 109, 672-682
16. Walker, E. C., McGregor, N. E., Poulton, I. J., Pompolo, S., Allan, E. H., Quinn, J. M., Gillespie, M. T., Martin, T. J., and Sims, N. A. (2008) Cardiotrophin-1 is an osteoclast-derived stimulus of bone formation required for normal bone remodeling. J. Bone Miner. Res. 23, 2025-2032
17. Henriksen, K., Andreassen, K. V., Thudium, C. S., Gudmann, K. N., Moscatelli, I., Crüger-Hansen, C. E., Schulz, A. S., Dziegiel, M. H., Richter, J., Karsdal, M. A., and Neutzsky-Wulff, A. V. (2012) A specific subtype of osteoclasts secretes factors inducing nodule formation by osteoblasts. Bone 51, 353-361
18. Henriksen, K., Karsdal, M. A., and Martin, T. J. (2014) Osteoclast-derived coupling factors in bone remodeling. Calcif. Tissue Int. 94, 88-97
19. Brantus, J. F., and Meunier, P. J. (1998) Effects of intravenous etidronate and oral corticosteroids in fibrodysplasia ossificans progressiva. Clin. Orthop. Rel. Res. 346, 117-120
20. Ulusoy, H. (2012) Fibrodysplasia ossificans progressiva without characteristic skeletal anomalies. Rheumatol. Int. 32, 1379-1382
21. Kaji, H. (2013) Linkage between muscle and bone: common catabolic signals resulting in osteoporosis and sarcopenia. Curr. Opin. Clin. Nutr. Metab. Care 16, 272-277
22. Kawao, N., Tamura, Y., Okumoto, K., Yano, M., Okada, K., Matsuo, O., and Kaji, H. (2013) Plasminogen plays a crucial role in bone repair. J. Bone Miner. Res. 28, 1561-1574
23. Bouxsein, M. L., Boyd, S. K., Christiansen, B. A., Guldberg, R. E., Jepsen, K. J., and Müller, R. (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 25, 1468-1486
24. Quinn, J. M., Horwood, N. J., Elliott, J., Gillespie, M. T., and Martin, T. J. (2000) Fibroblastic stromal cells express receptor activator of NF-κB ligand and support osteoclast differentiation. J. Bone Miner. Res. 15, 1459-1466 (Pubitemid 30484515)
25. Hotokezaka, H., Sakai, E., Kanaoka, K., Saito, K., Matsuo, K., Kitaura, H., Yoshida, N., and Nakayama, K. (2002) U0126 and PD98059, specific inhibitors of MEK, accelerate differentiation of RAW264.7 cells into osteoclast-like cells. J. Biol. Chem. 277, 47366-47372 (Pubitemid 36159251)
26. Tobimatsu, T., Kaji, H., Sowa, H., Naito, J., Canaff, L., Hendy, G. N., Sugimoto, T., and Chihara, K. (2006) Parathyroid hormone increases β-catenin levels through Smad3 in mouse osteoblastic cells. Endocrinology 147, 2583-2590
27. Inoue, Y., Canaff, L., Hendy, G. N., Hisa, I., Sugimoto, T., Chihara, K., and Kaji, H. (2009) Role of Smad3, acting independently of transforming growth factor-β, in the early induction of Wnt-β-catenin signaling by parathyroid hormone in mouse osteoblastic cells. J. Cell. Biochem. 108, 285-294
28. Utvåg, S. E., Grundnes, O., Rindal, D. B., and Reikerås, O. (2003) Influence of extensive muscle injury on fracture healing in rat tibia. J. Orthop. Trauma 17, 430-435
29. Glass, G. E., Chan, J. K., Freidin, A., Feldmann, M., Horwood, N. J., and Nanchahal, J. (2011) TNF-α promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells. Proc. Natl. Acad. Sci. U.S.A. 108, 1585-1590
30. Leblanc, E., Trensz, F., Haroun, S., Drouin, G., Bergeron, E., Penton, C. M., Montanaro, F., Roux, S., Faucheux, N., and Grenier, G. (2011) BMP-9-induced muscle heterotopic ossification requires changes to the skeletal muscle microenvironment. J. Bone Miner. Res. 26, 1166-1177
31. Sims, N. A., and Walsh, N. C. (2012) Intercellular cross-talk among bone cells: new factors and pathways. Curr. Osteoporos. Rep. 10, 109-117
32. Kanatani, M., Sugimoto, T., Kaji, H., Kobayashi, T., Nishiyama, K., Fukase, M., Kumegawa, M., and Chihara, K. (1995) Stimulatory effect of bone morphogenetic protein-2 on osteoclast-like cell formation and bone-resorbing activity. J. Bone Miner. Res. 10, 1681-1690
33. Abe, E., Yamamoto, M., Taguchi, Y., Lecka-Czernik, B., O'Brien, C. A., Economides, A. N., Stahl, N., Jilka, R. L., and Manolagas, S. C. (2000) Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin. J. Bone Miner. Res. 15, 663-673 (Pubitemid 30174020)
34. Okamoto, M., Murai, J., Yoshikawa, H., and Tsumaki, N. (2006) Bone morphogenetic proteins in bone stimulate osteoclasts and osteoblasts during bone development. J. Bone Miner. Res. 21, 1022-1033 (Pubitemid 43962831)
35. Otsuka, E., Notoya, M., and Hagiwara, H. (2003) Treatment of myoblastic C2C12 cells with BMP-2 stimulates vitamin D-induced formation of osteoclasts. Calcif. Tissue Int. 73, 72-77 (Pubitemid 37022082)
36. Hisa, I., Kawara, A., Katagiri, T., Sugimoto, T., and Kaji, H. (2012) Effects of serum from a fibrodysplasia ossificans progressiva patient on osteoblastic cells. Open J. Endocr. Metab. Dis. 2, 1-6
37. Pederson, L., Ruan, M., Westendorf, J. J., Khosla, S., and Oursler, M. J. (2008) Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine 1-phosphate. Proc. Natl. Acad. Sci. U.S.A. 105, 20764-20769
38. Koseki, T., Gao, Y., Okahashi, N., Murase, Y., Tsujisawa, T., Sato, T., Yamato, K., and Nishihara, T. (2002) Role of TGF-β family in osteoclastogenesis induced by RANKL. Cell. Signal. 14, 31-36 (Pubitemid 34020826)
39. Janssens, K., ten Dijke, P., Janssens, S., and Van Hul, W. (2005) Transforming growth factor-β1 to the bone. Endocr. Rev. 26, 743-774
40. Matsumoto, M., Sudo, T., Saito, T., Osada, H., and Tsujimoto, M. (2000) Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-κB ligand (RANKL). J. Biol. Chem. 275, 31155-31161
41. Li, X., Udagawa, N., Takami, M., Sato, N., Kobayashi, Y., and Takahashi, N. (2003) p38 mitogen-activated protein kinase is crucially involved in osteoclast differentiation but not in cytokine production, phagocytosis, or dendritic cell differentiation of bone marrow macrophages. Endocrinology 144, 4999-5005 (Pubitemid 37378415)
42. Ishida, A., Fujita, N., Kitazawa, R., and Tsuruo, T. (2002) Transforming growth factor-β induces expression of receptor activator of NF-κB ligand in vascular endothelial cells derived from bone. J. Biol. Chem. 277, 26217-26224 (Pubitemid 34967109)
43. Karsdal, M. A., Hjorth, P., Henriksen, K., Kirkegaard, T., Nielsen, K. L., Lou, H., Delaissé, J. M., and Foged, N. T. (2003) Transforming growth factor-β controls human osteoclastogenesis through the p38 MAPK and regulation of RANK expression. J. Biol. Chem. 278, 44975-44987 (Pubitemid 37377257)
44. Song, G. A., Kim, H. J., Woo, K. M., Baek, J. H., Kim, G. S., Choi, J. Y., and Ryoo, H. M. (2010) Molecular consequences of the ACVR1(R206H) mutation of fibrodysplasia ossificans progressiva. J. Biol. Chem. 285, 22542-22553