Altered fracture callus formation in chondromodulin-I deficient mice

Bone

Volumn 43, Issue 6, 2008, Pages 1047-1056

  Yukata, Kiminori ^a   Matsui, Yoshito ^a   Shukunami, Chisa ^b   Takimoto, Aki ^b   Goto, Tomohiro ^a   Nishizaki, Yuriko ^b   Nakamichi, Yuko ^c   Kubo, Takahiro ^a   Sano, Toshiaki ^a   Kato, Shigeaki ^c   Hiraki, Yuji ^b   Yasui, Natsuo ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Chondrogenesis; Chondromodulin I; Fracture callus; Fracture healing; Periosteum

Indexed keywords

CHONDROMODULIN I; COLLAGEN TYPE 10; COLLAGEN TYPE 10 ALPHA 1; GLYCOPROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MATURATION; BONE RADIOGRAPHY; BONE REMODELING; BONE STRESS; CALLUS; CARTILAGE CELL; CARTILAGE MATRIX; CHM 1 GENE; CONTROLLED STUDY; FRACTURE HEALING; FRACTURE NONUNION; GENE; GENE LOCATION; GENE MUTATION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; OSSIFICATION; PERIOSTEUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TIBIA FRACTURE; WILD TYPE;

ANIMALS; BONE RESORPTION; BONY CALLUS; FRACTURE HEALING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 57049128175     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2008.08.111     Document Type: Article

References (51)

1. Hiraki Y., Tanaka H., Inoue H., Kondo J., Kamizono A., and Suzuki F. Molecular cloning of a new class of cartilage-specific matrix, chondromodulin-I, which stimulates growth of cultured chondrocytes. Biochem. Biophys. Res. Commun. 175 (1991) 971-977
2. Inoue H., Kondo J., Koike T., Shukunami C., and Hiraki Y. Identification of an autocrine chondrocyte colony-stimulating factor: chondromodulin-I stimulates the colony formation of growth plate chondrocytes in agarose culture. Biochem. Biophys. Res. Commun. 241 (1997) 395-400
3. Hiraki Y., Mitsui K., Endo N., Takahashi K., Hayami T., Inoue H., Shukunami C., Tokunaga K., Kono T., Yamada M., Takahashi H.E., and Kondo J. Molecular cloning of human chondromodulin-I, a cartilage-derived growth modulating factor, and its expression in Chinese hamster ovary cells. Eur. J. Biochem. 260 (1999) 869-878
4. Shukunami C., Iyama K., Inoue H., and Hiraki Y. Spatiotemporal pattern of the mouse chondromodulin-I gene expression and its regulatory role in vascular invasion into cartilage during endochondral bone formation. Int. J. Dev. Biol. 43 (1999) 39-49
5. Azizan A., Holaday N., and Neame P.J. Post-translational processing of bovine chondromodulin-I. J. Biol. Chem. 276 (2001) 23632-23638
6. Shukunami C., and Hiraki Y. Expression of cartilage-specific functional matrix chondromodulin-I mRNA in rabbit growth plate chondrocytes and its responsiveness to growth stimuli in vitro. Biochem. Biophys. Res. Commun. 249 (1998) 885-890
7. Kitahara H., Hayami T., Tokunaga K., Endo N., Funaki H., Yoshida Y., Yaoita E., and Yamamoto T. Chondromodulin-I expression in rat articular cartilage. Arch. Histol. Cytol. 66 (2003) 221-228
8. Hiraki Y., Inoue H., Iyama K., Kamizono A., Ochiai M., Shukunami C., Iijima S., Suzuki F., and Kondo J. Identification of chondromodulin I as a novel endothelial cell growth inhibitor. Purification and its localization in the avascular zone of epiphyseal cartilage. J. Biol. Chem. 272 (1997) 32419-32426
9. Hiraki Y., Kono T., Sato M., Shukunami C., and Kondo J. Inhibition of DNA synthesis and tube morphogenesis of cultured vascular endothelial cells by chondromodulin-I. FEBS Lett. 415 (1997) 321-324
10. Nakamichi Y., Shukunami C., Yamada T., Aihara K., Kawano H., Sato T., Nishizaki Y., Yamamoto Y., Shindo M., Yoshimura K., Nakamura T., Takahashi N., Kawaguchi H., Hiraki Y., and Kato S. Chondromodulin I is a bone remodeling factor. Mol. Cell. Biol. 23 (2003) 636-644
11. Yoshioka M., Yuasa S., Matsumura K., Kimura K., Shiomi T., Kimura N., Shukunami C., Okada Y., Mukai M., Shin H., Yozu R., Sata M., Ogawa S., Hiraki Y., and Fukuda K. Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nat. Med. 12 (2006) 1151-1159
12. Einhorn T.A. The cell and molecular biology of fracture healing. Clin. Orthop. Relat. Res. (1998) 7-21
13. Gerstenfeld L.C., Cullinane D.M., Barnes G.L., Graves D.T., and Einhorn T.A. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J. Cell. Biochem. 88 (2003) 873-884
14. Foster J.W., Dominguez-Steglich M.A., Guioli S., Kowk G., Weller P.A., Stevanovic M., Weissenbach J., Mansour S., Young I.D., Goodfellow P.N., et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372 (1994) 525-530
15. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., and Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 (1997) 755-764
16. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., and de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108 (2002) 17-29
17. Edwall D., Prisell P.T., Levinovitz A., Jennische E., and Norstedt G. Expression of insulin-like growth factor I messenger ribonucleic acid in regenerating bone after fracture: influence of indomethacin. J. Bone Miner. Res. 7 (1992) 207-213
18. Nakamura T., Hara Y., Tagawa M., Tamura M., Yuge T., Fukuda H., and Nigi H. Recombinant human basic fibroblast growth factor accelerates fracture healing by enhancing callus remodeling in experimental dog tibial fracture. J. Bone Miner. Res. 13 (1998) 942-949
19. Zehentner B.K., Dony C., and Burtscher H. The transcription factor Sox9 is involved in BMP-2 signaling. J. Bone Miner. Res. 14 (1999) 1734-1741
20. Tuli R., Tuli S., Nandi S., Huang X., Manner P.A., Hozack W.J., Danielson K.G., Hall D.J., and Tuan R.S. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J. Biol. Chem. 278 (2003) 41227-41236
21. Iwaki A., Jingushi S., Oda Y., Izumi T., Shida J.I., Tsuneyoshi M., and Sugioka Y. Localization and quantification of proliferating cells during rat fracture repair: detection of proliferating cell nuclear antigen by immunohistochemistry. J. Bone Miner. Res. 12 (1997) 96-102
22. Barnes G.L., Kostenuik P.J., Gerstenfeld L.C., and Einhorn T.A. Growth factor regulation of fracture repair. J. Bone Miner. Res. 14 (1999) 1805-1815
23. Rundle C.H., Wang H., Yu H., Chadwick R.B., Davis E.I., Wergedal J.E., Lau K.H., Mohan S., Ryaby J.T., and Baylink D.J. Microarray analysis of gene expression during the inflammation and endochondral bone formation stages of rat femur fracture repair. Bone 38 (2006) 521-529
24. Isefuku S., Joyner C.J., and Simpson A.H. A murine model of distraction osteogenesis. Bone 27 (2000) 661-665
25. Metsaranta M., Toman D., De Crombrugghe B., and Vuorio E. Specific hybridization probes for mouse type I, II, III and IX collagen mRNAs. Biochim. Biophys. Acta. 1089 (1991) 241-243
26. Inada M., Yasui T., Nomura S., Miyake S., Deguchi K., Himeno M., Sato M., Yamagiwa H., Kimura T., Yasui N., Ochi T., Endo N., Kitamura Y., Kishimoto T., and Komori T. Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev. Dyn. 214 (1999) 279-290
27. Apte S.S., Seldin M.F., Hayashi M., and Olsen B.R. Cloning of the human and mouse type X collagen genes and mapping of the mouse type X collagen gene to chromosome 10. Eur. J. Biochem. 206 (1992) 217-224
28. Arai F., Ohneda O., Miyamoto T., Zhang X.Q., and Suda T. Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J. Exp. Med. 195 (2002) 1549-1563
29. Emans P.J., Surtel D.A., Frings E.J., Bulstra S.K., and Kuijer R. In vivo generation of cartilage from periosteum. Tissue Eng. 11 (2005) 369-377
30. Shafer J., Davis A.R., Gannon F.H., Fouletier-Dilling C.M., Lazard Z., Moran K., Gugala Z., Ozen M., Ittmann M., Heggeness M.H., and Olmsted-Davis E. Oxygen tension directs chondrogenic differentiation of myelo-monocytic progenitors during endochondral bone formation. Tissue Eng. 13 (2007) 2011-2019
31. Yoo J.U., and Johnstone B. The role of osteochondral progenitor cells in fracture repair. Clin. Orthop. Relat. Res. (1998) S73-81
32. Huang J.I., Kazmi N., Durbhakula M.M., Hering T.M., Yoo J.U., and Johnstone B. Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: a patient-matched comparison. J. Orthop. Res. 23 (2005) 1383-1389
33. Loboa E.G., Beaupre G.S., and Carter D.R. Mechanobiology of initial pseudarthrosis formation with oblique fractures. J. Orthop. Res. 19 (2001) 1067-1072
34. Hankemeier S., Grassel S., Plenz G., Spiegel H.U., Bruckner P., and Probst A. Alteration of fracture stability influences chondrogenesis, osteogenesis and immigration of macrophages. J. Orthop. Res. 19 (2001) 531-538
35. Le A.X., Miclau T., Hu D., and Helms J.A. Molecular aspects of healing in stabilized and non-stabilized fractures. J. Orthop. Res. 19 (2001) 78-84
36. Buckwalter J.A., Einhorn T.A., Bolander M.E., and Cruess R.L. Healing of musculoskeletal tissues. In: Rockwood C.A., Green D.P., Buchholz R.W., and Heckmann J.D. (Eds). Fractures in adults (1996), Lippincott-Raven, Philadelphia 261-304
37. Thompson Z., Miclau T., Hu D., and Helms J.A. A model for intramembranous ossification during fracture healing. J. Orthop. Res. 20 (2002) 1091-1098
38. Cheung K.M., Kaluarachi K., Andrew G., Lu W., Chan D., and Cheah K.S. An externally fixed femoral fracture model for mice. J. Orthop. Res. 21 (2003) 685-690
39. Hiltunen A., Vuorio E., and Aro H.T. A standardized experimental fracture in the mouse tibia. J. Orthop. Res. 11 (1993) 305-312
40. Hiltunen A., Metsaranta M., Perala M., Saamanen A.M., Aro H.T., and Vuorio E. Expression of type VI, IX and XI collagen genes and alternative splicing of type II collagen transcripts in fracture callus tissue in mice. FEBS Lett. 364 (1995) 171-174
41. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., and de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol. Cell Biol. 17 (1997) 2336-2346
42. Lefebvre V., Li P., and de Crombrugghe B. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. Embo. J. 17 (1998) 5718-5733
43. Bell D.M., Leung K.K., Wheatley S.C., Ng L.J., Zhou S., Ling K.W., Sham M.H., Koopman P., Tam P.P., and Cheah K.S. SOX9 directly regulates the type-II collagen gene. Nat. Genet. 16 (1997) 174-178
44. Ng L.J., Wheatley S., Muscat G.E., Conway-Campbell J., Bowles J., Wright E., Bell D.M., Tam P.P., Cheah K.S., and Koopman P. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 183 (1997) 108-121
45. Bosserhoff A.K., Moser M., Hein R., Landthaler M., and Buettner R. In situ expression patterns of melanoma-inhibiting activity (MIA) in melanomas and breast cancers. J. Pathol. 187 (1999) 446-454
46. Ikeda T., Kamekura S., Mabuchi A., Kou I., Seki S., Takato T., Nakamura K., Kawaguchi H., Ikegawa S., and Chung U.I. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum. 50 (2004) 3561-3573
47. Bi W., Huang W., Whitworth D.J., Deng J.M., Zhang Z., Behringer R.R., and de Crombrugghe B. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc. Natl. Acad. Sci. U S A 98 (2001) 6698-6703
48. Uusitalo H., Hiltunen A., Ahonen M., Gao T.J., Lefebvre V., Harley V., Kahari V.M., and Vuorio E. Accelerated up-regulation of L-Sox5, Sox6, and Sox9 by BMP-2 gene transfer during murine fracture healing. J. Bone Miner. Res. 16 (2001) 1837-1845
49. Uusitalo H., Hiltunen A., Ahonen M., Kahari V.M., Aro H., and Vuorio E. Induction of periosteal callus formation by bone morphogenetic protein-2 employing adenovirus-mediated gene delivery. Matrix. Biol. 20 (2001) 123-127
50. Fujii T., Ueno T., Kagawa T., Sugahara T., and Yamamoto T. Immunohistochemical analysis of Sox9 expression in periosteum of tibia and calvaria after surgical release of the periosteum. Acta. Histochem. 106 (2005) 427-437
51. Hadjiargyrou M., Lombardo F., Zhao S., Ahrens W., Joo J., Ahn H., Jurman M., White D.W., and Rubin C.T. Transcriptional profiling of bone regeneration. Insight into the molecular complexity of wound repair. J. Biol. Chem. 277 (2002) 30177-30182