Expression of osteoblastic and osteoclastic genes during spontaneous regeneration and autotransplantation of goldfish scale: A new tool to study intramembranous bone regeneration

Bone

Volumn 50, Issue 6, 2012, Pages 1240-1249

  Thamamongood, Thiparpa Aime ^a,b   Furuya, Ryo ^b,c   Fukuba, Shunsuke ^b   Nakamura, Masahisa ^c   Suzuki, Nobuo ^d   Hattori, Atsuhiko ^b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c WASEDA UNIVERSITY   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

Author keywords

Cell to cell contact; Intramembranous bone regeneration; Osteoblastic genes; Osteoclastic genes; Scale autotransplantation; Teleost scale regeneration

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; UNCLASSIFIED DRUG;

ALP GENE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOTRANSPLANTATION; BONE REGENERATION; CATHEPSIN K GENE; CONTROLLED STUDY; DLX5 GENE; GENE; GENE EXPRESSION; GOLDFISH; HISTOLOGY; INTRAMEMBRANOUS BONE REGENERATION; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCALCIN GENE; OSTEOLYSIS; OSTERIX GENE; RANKL GENE; RUNX2A GENE; RUNX2B GENE; SEQUENCE ANALYSIS; TRAP GENE; TYPE 1 COLLAGEN GENE;

ANIMAL STRUCTURES; ANIMALS; BASE SEQUENCE; BONE REGENERATION; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FISH PROTEINS; GENE EXPRESSION REGULATION; GOLDFISH; MODELS, ANIMAL; OSTEOBLASTS; OSTEOCLASTS; REGENERATION; RNA, MESSENGER; TRANSPLANTATION, AUTOLOGOUS;

EID: 84859799071     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.03.021     Document Type: Article

References (70)

1. Azuma K., Kobayashi M., Nakamura M., Suzuki N., Yashima S., Iwamuro S., et al. Two osteoclastic markers expressed in multinucleate osteoclasts of goldfish scales. Biochem Biophys Res Commun 2007, 362:594-600.
2. Yoshikubo H., Suzuki N., Takemura K., Hoso M., Yashima S., Iwamuro S., et al. Osteoblastic activity and estrogenic response in the regenerating scale of goldfish, a good model of osteogenesis. Life Sci 2005, 76:2699-2709.
3. Suzuki N., Kitamura K., Nemoto T., Shimizu N., Wada S., Kondo T., et al. Effect of vibration on osteoblastic and osteoclastic activities: analysis of bone metabolism using goldfish scale as a model for bone. Adv Space Res 2007, 40:1711-1721.
4. Suzuki N., Somei M., Seki A., Reiter R.J., Hattori A. Novel bromomelatonin derivatives as potentially effective drugs to treat bone diseases. J Pineal Res 2008, 45:229-234.
5. Ejiri S. The preosteoclast and its cytodifferentiation into the osteoclast: ultrastructural and histochemical studies of rat fetal parietal bone. Arch Histol Jpn 1983, 46:533-557.
6. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
7. Rice D.P., Rice R., Thesleff I. Molecular mechanisms in calvarial bone and suture development, and their relation to craniosynostosis. Eur J Orthod 2003, 25:139-148.
8. Lian J.B., Balint E., Javed A., Drissi H., Vitti R., Quinlan E.J., et al. Runx1/AML1 hematopoietic transcription factor contributes to skeletal development in vivo. J Cell Physiol 2003, 196:301-311.
9. Ito Y., Yeo J.Y., Chytil A., Han J., Bringas P., Nakajima A., et al. Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 2003, 130:5269-5280.
10. Suzuki N., Danks J.A., Maruyama Y., Ikegame M., Sasayama Y., Hattori A., et al. Parathyroid hormone 1 (1-34) acts on the scales and involves calcium metabolism in goldfish. Bone 2011, 48:1186-1193.
11. Witten P.E., Bendahmane M., Abou-Haila A. Enzyme histochemical characteristics of osteoblasts and mononucleated osteoclasts in a teleost fish with acellular bone (Oreochromis niloticus, Cichlidae). Cell Tissue Res 1997, 287:591-599.
12. Flores M., Tsang V., Hu W., Kalev-Zylinska M., Postlethwait J., Crosier P., et al. Duplicate zebrafish runx2 orthologues are expressed in developing skeletal elements. Gene Expr Patterns 2004, 4:573-581.
13. Glenney G.W., Wiens G.D. Early diversification of the TNF superfamily in teleosts: genomic characterization and expression analysis. J Immunol 2007, 178:7955-7973.
14. Zylberberg L., Bonaventure J., Cohen-Solal L., Hartmann D., Bereiterhahn J. Organization and characterization of fibrillar collagens in fish scales in situ and in vitro. J Cell Sci 1992, 103:273.
15. Renn J., Winkler C. Osterix-mCherry transgenic medaka for in vivo imaging of bone formation. Dev Dyn 2009, 238:241-248.
16. Gavaia P.J., Simes D.C., Ortiz-Delgado J.B., Viegas C.S., Pinto J.P., Kelsh R.N., et al. Osteocalcin and matrix Gla protein in zebrafish (Danio rerio) and Senegal sole (Solea senegalensis): comparative gene and protein expression during larval development through adulthood. Gene Expr Patterns 2006, 6:637-652.
17. Pinto J.P., Conceicao N., Gavaia P.J., Cancela M.L. Matrix Gla protein gene expression and protein accumulation colocalize with cartilage distribution during development of the teleost fish Sparus aurata. Bone 2003, 32:201-210.
18. Aubin J.E., Gupta A.K., Bhargava U., Turksen K. Expression and regulation of galectin 3 in rat osteoblastic cells. J Cell Physiol 1996, 169:468-480.
19. Nishimoto S.K., Araki N., Robinson F.D., Waite J.H. Discovery of bone gamma-carboxyglutamic acid protein in mineralized scales. The abundance and structure of Lepomis macrochirus bone gamma-carboxyglutamic acid protein. J Biol Chem 1992, 267:11600-11605.
20. Li H., Marijanovic I., Kronenberg M.S., Erceg I., Stover M.L., Velonis D., et al. Expression and function of Dlx genes in the osteoblast lineage. Dev Biol 2008, 316:458-470.
21. Lee M.H., Kim Y.J., Kim H.J., Park H.D., Kang A.R., Kyung H.M., et al. BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-beta 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J Biol Chem 2003, 278:34387-34394.
22. Harris S.E., Guo D., Harris M.A., Krishnaswamy A., Lichtler A. Transcriptional regulation of BMP-2 activated genes in osteoblasts using gene expression microarray analysis: role of Dlx2 and Dlx5 transcription factors. Front Biosci 2003, 8:s1249-s1265.
23. Verreijdt L., Debiais-Thibaud M., Borday-Birraux V. Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): differential involvement in the visceral skeleton and braincase. Dev Dyn 2006, 235:1371-1389.
24. Abe G., Ide H., Tamura K. Function of FGF signaling in the developmental process of the median fin fold in zebrafish. Dev Biol 2007, 304:355-366.
25. Sire J.Y. The same cell lineage is involved in scale formation and regeneration in the teleost fish Hemichromis bimaculatus. Tissue Cell 1989, 21:447-462.
26. Squier C., Ghoneim S., Kremenak C. Ultrastructure of the periosteum from membrane bone. J Anat 1990, 171:233.
27. Fell H. The osteogenic capacity in vitro of periosteum and endosteum isolated from the limb skeleton of fowl embryos and young chicks. J Anat 1932, 66:157.
28. Ito Y., Fitzsimmons J., Sanyal A., Mello M., Mukherjee N., O'driscoll S. Localization of chondrocyte precursors in periosteum. Osteoarthritis Cartilage 2001, 9:215-223.
29. Dwek J.R. The periosteum: what is it, where is it, and what mimics it in its absence?. Skeletal Radiol 2010, 39:319-323.
30. Sire J.Y., Géraudie J. Fine structure of regenerating scales and their associated cells in the cichlid Hemichromis bimaculatus (Gill). Cell Tissue Res 1984, 237:537-547.
31. Neave F. On the histology and regeneration of the teleost scale. Q J Microsc Sci NS 1940, 81:541-568.
32. Zhao Q., Wang X., Liu Y., He A., Jia R. NFATc1: functions in osteoclasts. Int J Biochem Cell Biol 2010, 42:576-579.
33. DR S. Fixation of implants. The adult knee 2003, 289-296. Lippincott Williams & Wilkins, Philadelphia. J.J. Callaghan, A.G. Rosenberg, H.E. Rubash, P.T. Simonian, T.A. Wickiewicz (Eds.).
34. Amsel S., Maniatis A., Tavassoli M., Crosby W.H. The significance of intramedullary cancellous bone formation in the repair of bone marrow tissue. Anat Rec 1969, 164:101-111.
35. Patt H.M., Maloney M.A. Bone marrow regeneration after local injury: a review. Exp Hematol 1975, 3:135-148.
36. Liang C.T., Barnes J., Seedor J.G., Quartuccio H.A., Bolander M., Jeffrey J.J., et al. Impaired bone activity in aged rats: alterations at the cellular and molecular levels. Bone 1992, 13:435-441.
37. Suva L.J., Seedor J.G., Endo N., Quartuccio H.A., Thompson D.D., Bab I., et al. Pattern of gene expression following rat tibial marrow ablation. J Bone Miner Res 1993, 8:379-388.
38. Bab I.A. Postablation bone marrow regeneration: an in vivo model to study differential regulation of bone formation and resorption. Bone 1995, 17:437S-441S.
39. Lu H., Kraut D., Gerstenfeld L.C., Graves D.T. Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology 2003, 144:346-352.
40. Boabaid F., Berry J.E., Koh A.J., Somerman M.J., McCcauley L.K. The role of parathyroid hormone-related protein in the regulation of osteoclastogenesis by cementoblasts. J Periodontol 2004, 75:1247-1254.
41. Kuroda S., Virdi A.S., Dai Y., Shott S., Sumner D.R. Patterns and localization of gene expression during intramembranous bone regeneration in the rat femoral marrow ablation model. Calcif Tissue Int 2005, 77:212-225.
42. van der Meulen T., Kranenbarg S., Schipper H., Samallo J., van Leeuwen J.L., Franssen H. Identification and characterisation of two runx2 homologues in zebrafish with different expression patterns. Biochim Biophys Acta 2005, 1729:105-117.
43. Suzuki N., Hattori A. Melatonin suppresses osteoclastic and osteoblastic activities in the scales of goldfish. J Pineal Res 2002, 33:253-258.
44. Milona M., Gough J., Edgar A. Expression of alternatively spliced isoforms of human Sp7 in osteoblast-like cells. BMC Genomics 2003, 4:43.
45. Weiss M.J., Henthorn P.S., Lafferty M.A., Slaughter C., Raducha M., Harris H. Isolation and characterization of a cDNA encoding a human liver/bone/kidney-type alkaline phosphatase. Proc Natl Acad Sci 1986, 83:7182.
46. Dohi Y., Tabata S., Yamaguchi M., Ohgushi H., Yonemasu K. Characterization of the cDNA encoding bullfrog, Rana catesbeiana, osteocalcin and two forms of the protein isolated from bone*. Biochimie 2004, 86:471-480.
47. Nishimoto S.K., Waite J.H., Nishimoto M., Kriwacki R.W. Structure, activity, and distribution of fish osteocalcin. J Biol Chem 2003, 278:11843.
48. Maeda T., Matsunuma A., Kurahashi I., Yanagawa T., Yoshida H., Horiuchi N. Induction of osteoblast differentiation indices by statins in MC3T3-E1 cells. J Cell Biochem 2004, 92:458-471.
49. Komori T. Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 2006, 99:1233-1239.
50. Lee M., Kim Y., Yoon W., Kim J., Kim B., Hwang Y., et al. Dlx5 specifically regulates Runx2 type II expression by binding to homeodomain-response elements in the Runx2 distal promoter. J Biol Chem 2005, 280:35579-35587.
51. Samee N., Geoffroy V., Marty C., Schiltz C., Vieux-Rochas M., Levi G., et al. Dlx5, a positive regulator of osteoblastogenesis, is essential for osteoblast-osteoclast coupling. Am J Pathol 2008, 173:773-780.
52. Lee M.H., Kwon T.G., Park H.S., Wozney J.M., Ryoo H.M. BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2. Biochem Biophys Res Commun 2003, 309:689-694.
53. Ulsamer A., Ortuño M., Ruiz S., Susperregui A., Osses N., Rosa J., et al. BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J Biol Chem 2008, 283:3816-3826.
54. Ducy P., Zhang R., Geoffroy V., Ridall A.L., Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997, 89:747-754.
55. Karsenty G., Kronenberg H., Settembre C. Genetic control of bone formation. Annual Review of Cell and Developmental 2009, 25:629-648.
56. Suda T., Takahashi N., Martin T.J. Modulation of osteoclast differentiation. Endocr Rev 1992, 13:66-80.
57. Suda T., Udagawa N., Nakamura I., Miyaura C., Takahashi N. Modulation of osteoclast differentiation by local factors. Bone 1995, 17:87S-91S.
58. Roodman G.D. Advances in bone biology: the osteoclast. Endocr Rev 1996, 17:308-332.
59. Lerner U.H. Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis. J Dent Res 2006, 85:596-607.
60. Romas E., Gillespie M.T., Martin T.J. Involvement of receptor activator of NFkappaB ligand and tumor necrosis factor-alpha in bone destruction in rheumatoid arthritis. Bone 2002, 30:340-346.
61. Weitzmann M.N., Pacifici R. The role of T lymphocytes in bone metabolism. Immunol Rev 2005, 208:154-168.
62. Quinn J.M., Gillespie M.T. Modulation of osteoclast formation. Biochem Biophys Res Commun 2005, 328:739-745.
63. Romas E., Bakharevski O., Hards D.K., Kartsogiannis V., Quinn J.M., Ryan P.F., et al. Expression of osteoclast differentiation factor at sites of bone erosion in collagen-induced arthritis. Arthritis Rheum 2000, 43:821-826.
64. Martin T.J., Gillespie M.T. Receptor activator of nuclear factor [kappa] B ligand (RANKL): another link between breast and bone. Trends Endocrinol Metab 2001, 12:2-4.
65. Srivastava S., Matsuda M., Hou Z., Bailey J.P., Kitazawa R., Herbst M.P., et al. Receptor activator of NF-κB ligand induction via Jak2 and Stat5a in mammary epithelial cells. J Biol Chem 2003, 278:46171.
66. Nakatsuji Y., Miller R.H. Homotypic cell contact-dependent inhibition of astrocyte proliferation. Glia 1998, 22:379-389.
67. Koguchi K., Nakatsuji Y., Nakayama K., Sakoda S. Modulation of astrocyte proliferation by cyclin-dependent kinase inhibitor p27(Kip1). Glia 2002, 37:93-104.
68. Nakatsuji Y., Miller R.H. Density dependent modulation of cell cycle protein expression in astrocytes. J Neurosci Res 2001, 66:487-496.
69. Liu M.L., Mars W.M., Zarnegar R., Michalopoulos G.K. Collagenase pretreatment and the mitogenic effects of hepatocyte growth factor and transforming growth factor-alpha in adult rat liver. Hepatology 1994, 19:1521-1527.
70. Thompson J.S., Saxena S.K., Sharp J.G. Regulation of intestinal regeneration: new insights. Microsc Res Tech 2000, 51:129-137.