Different roles of Runx2 during early neural crest-derived bone and tooth development

Journal of Bone and Mineral Research

Volumn 21, Issue 7, 2006, Pages 1034-1044

  James, Martyn J ^a   Järvinen, Elina ^a   Wang, Xiu Ping ^a,b   Thesleff, Irma ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Bambi; Bmp4; Bono1; Dickkopf1; Epithelial mesenchymal interactions; Fgf receptor1; Gli1; Intramembranous ossification; Lef1; Mandibular bone; Patched; Prostaglandin F receptor; Runx2; Tcf1; Tgf 1; Tooth; Wnt10a; Wnt10b

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; GROWTH FACTOR; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BAMBI GENE; BMP4 GENE; BONE DEVELOPMENT; BONO1 GENE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DKK1 GENE; DOWN REGULATION; DUSP6 GENE; ENPP1 GENE; EPITHELIUM CELL; FGF RECEPTOR 1 GENE; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE INDUCTION; GENE TARGETING; GENETIC TRANSCRIPTION; GLI1 GENE; IGFBP3 GENE; IN SITU HYBRIDIZATION; IN VITRO STUDY; LEF1 GENE; MESENCHYME; MESENCHYME CELL; MICROARRAY ANALYSIS; MOUSE; MUTANT; NEURAL CREST; NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; PATCHED GENE; PROSTAGLANDIN F RECEPTOR 1 GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RUNX2 GENE; SIGNAL TRANSDUCTION; TCF1 GENE; TGFBETA1 GENE; TISSUE SECTION; TISSUE SPECIFICITY; TOOTH DEVELOPMENT; WILD TYPE; WNT10A GENE; WNT10B GENE;

ANIMALS; BONE DEVELOPMENT; CELL COMMUNICATION; CORE BINDING FACTOR ALPHA 1 SUBUNIT; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESODERM; MICE; MICE, MUTANT STRAINS; NEURAL CREST; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TOOTH;

EID: 33745486966     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.060413     Document Type: Article

References (53)

1. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JH, Owen MJ, Mertelsmann R, Zabel BU, Olsen BR 1997 Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773-779.
2. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T 1997 Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
3. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ 1997 Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771.
4. D'Souza RN, Aberg T, Gaikwad J, Cavender A, Owen M, Karsenty G, Thesleff I 1999 Cbfa1 is required for epithelial-mesenchymal interactions regulating tooth development in mice. Development 126:2911-2920.
5. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B 2002 The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108:17-29.
6. Tyler MS, Hall BK 1977 Epithelial influences on skeletogenesis in the mandible of the embryonic chick. Anat Rec 18:229-240.
7. Sperber GH 2001 The mandible. In: Sperber GH (ed.) Craniofacial Development. BC Decker, Hamilton, Ontario, Canada, pp. 127-138.
8. Chai Y, Jiang X, Ito Y, Bringas P Jr, Han J, Rowitch DH, Soriano P, McMahon AP, Sucov HM 2000 Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127:1671-1679.
9. Karsenty G, Wagner EF 2002 Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2:389-406.
10. Thesleff I 2003 Epithelial-mesenchymal signalling regulating tooth morphogenesis. J Cell Sci 116:1467-1468.
11. Åberg T, Wang XP, Kim JH, Yamashiro T, Bei M, Rice R, Ryoo HM, Thesleff I 2004 Runx2 mediates FGF signaling from epithelium to mesenchyme during tooth morphogenesis. Dev Biol 270:76-93.
12. Chen D, Ji X, Harris MA, Feng JQ, Karsenty G, Celeste AJ, Rosen V, Mundy GR, Harris SE 1998 Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA is differentiation and specification of mesenchymal precursor cells to osteoblasts and adipocyte lineages. J Cell Biol 142:295-305.
13. Lian JB, Javed A, Zaidi SK, Lengner C, Montecino M, van Wijnen AJ, Stein JL, Stein GS 2004 Regulatory controls for osteoblast growth arid differentiation: Role of Runx/Cbfa/AML factors. Crit Rev Eukaryot Gene Expr 14:1-41.
14. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G 1997 Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:747-754.
15. Ducy P, Karsenty G 1995 Two distinct osteoblast-specific cis-acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol 15:1858-1869.
16. Ogawa E, Inuzuka M, Maruyama M, Satake M, Naito-Fujimoto M, Ito Y, Shigesada K 1993 Molecular cloning and characterization of PEBP2 beta, the heterodimeric partner of a novel Drosophila runt-related DNA binding protein PEBP2 alpha. Virology 194:314-331.
17. Westendorf JJ, Zaidi SK, Cascino JE, Kahler R, van Wijnen AJ, Lian JB, Yoshida M, Stein GS, Li X 2002 Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol Cell Biol 22:7982-7992.
18. Zaidi SK, Sullivan AJ, Medina R, Ito Y, Van Wijnen AJ, Stein JL, Lian JB, Stein GS 2004 Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription. EMBO J 23:790-799.
19. Pratap J, Galindo M, Zaidi SK, Vradii D, Bhat BM, Robinson JA, Choi JY, Komori T, Stein JL, Lian JB, Stein GS, van Wijnen AJ 2003 Cell growth regulatory role of Runx2 during proliferative expansion of preosteoblasts. Cancer Res 63:5357-5362.
20. Scheidl SJ, Nilsson S, Kalen M, Hellstrom M, Takemoto M, Hakansson J, Lindahl P 2002 mRNA expression profiling of laser microbeam microdissected cells from slender embryonic structures. Am J Pathol 160:801-813.
21. Wilkinson D, Green J 1990 In situ hybridization and the three-dimensional reconstruction of serial sections. In: Copp AJ, Cole DE (eds.) Postimplantation Mammalian Embryos. Oxford University Press, London, UK, pp. 155-171.
22. Rozen S, Skaletsky HJ 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds.) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ, USA, pp. 365-386.
23. Bianco P, Fisher LW, Young MF, Termine JD, Robey PG 1990 Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J Histochem Cytochem 38:1549-1563.
24. Mark MP, Bloch-Zupan A, Wolf C, Ruberte E, Ruch JV 1991 Involvement of cellular retinoic acid-binding proteins I and II (CRABPI and CRABPII) and of the cellular retinol-binding protein I (CRBPI) in odontogenesis in the mouse. Differentiation 48:89-98.
25. Wang X-P, Åberg T, James MJ, Levanon D, Groner Y, Thesleff I 2005 Runx2 (Cbfa1) Inhibits Shh signaling in the lower but not upper molars of mouse embryos and prevents the budding of putative successional teeth. J Dent Res 84:138-143.
26. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA 2005 Regulation of osteogenesis and bone mass by Wnt10b. Proc Natl Acad Sci USA 102:3324-3329.
27. Hu H, Hilton MJ, Tu X, Yu K, Ornitz DM, Long F 2005 Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 132:49-60.
28. Mukhopadhyay M, Shtrom S, Rodriguez-Esteban C, Chen L, Tsukui T, Gomer L, Dorward DW, Glinka A, Grinberg A, Huang SP, Niehrs C, Belmonte JC, Westphal H 2001 Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev Cell 1:423-434.
29. Eblaghie MC, Lunn JS, Dickinson RJ, Munsterberg AE, Sanz-Ezquerro JJ, Farrell ER, Mathers J, Keyse SM, Storey K, Tickle C 2003 Negative feedback regulation of FGF signaling levels by Pyst1/MKP3 in chick embryos. Curr Biol 13:1009-1018.
30. Kawakami Y, Rodriguez-Leon J, Koth CM, Buscher D, Itoh T, Raya A, Ng JK, Esteban CR, Takahashi S, Henrique D, Schwarz MF, Asahara H, Izpisua Belmonte JC 2003 MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nat Cell Biol 5:513-519.
31. Okawa A, Nakamura I, Goto S, Moriya H, Nakamura Y, Ikegawa S 1998 Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat Genet 19:271-273.
32. Jones JI, Clemmons DR 1995 Insulin-like growth factors and their binding proteins: Biological actions. Endocr Rev 16:3-34.
33. Grotewold L, Ruther U 2002 The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and and c-Jun and modulates programmed cell death. EMBO J 21:966-975.
34. Villaudy J, Delbe J, Blat C, Desauty G, Golde A, Harel L 1991 An IGF binding protein is an inhibitor of FGF stimulation. J Cell Physiol 149:492-496.
35. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, Massague J, Niehrs C 1999 Silencing of TGF-beta signaling by the pseudoreceptor BAMBI. Nature 401:480-485.
36. Dunn NR, Winnier GE, Hargett LK, Schrick JJ, Fogo AB, Hogan BL 1997 Haploinsufficient phenotypes in Bmp4 heterozygous null mice and modification by mutations in Gli3 and Alx4. Dev Biol 188:235-247.
37. James MJ, Jarvinen E, Thesleff I 2004 Bono1: A gene associated with regions of deposition of bone and dentine. Gene Expr Patterns 4:595-599.
38. Shibata Y, Tsukazaki T, Hirata K, Xin C, Yamaguchi A 2004 Role of a new member of IGFBP superfamily, IGFBP-rP10, in proliferation and differentiation of osteoblastic cells. Biochem Biophys Res Commun 325:1194-1200.
39. Ornitz DM, Marie PJ 2002 FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev 16:1446-1465.
40. Yang Y, Guillot P, Boyd Y, Lyon MF, McMahon AP 1998 Evidence that preaxial polydactyly in the Doublefoot mutant is due to ectopic Indian Hedgehog signaling. Development 125:3123-3132.
41. Van Genderen C, Okamura RM, Farinas I, Quo RG, Parslow TG, Bruhn L, Grosschedl R 1994 Development of several organ that require inductive epithelial-mesenchymal interactions is impaired in LEF1-deficient mice. Genes Dev 8:2691-2703.
42. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM, Quinn AG, Myers RM, Cox DR, Epstein EH Jr, Scott MP 1996 Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272:1668-1671.
43. Caverzasio J, Palmer G, Suzuki A, Bonjour JP 2000 Evidence for the involvement of two pathways in activation of extracellular signal-regulated kinase (Erk) and cell proliferation by Gi and Gq protein-coupled receptors in osteoblast-like cells. J Bone Miner Res 15:1697-1706.
44. Verbeek S, Izon D, Hofhuis F, Robanus-Maandag E, te Riele H, van de Wetering M, Oosterwegel M, Wilson A, MacDonald HR, Clevers H 1995 An HMG-box-containing T-cell factor required for thymocyte differentiation. 374:70-74.
45. Kinoshita A, Saito T, Tomita H, Makita Y, Yoshida K, Ghadami M, Yamada K, Kondo S, Ikegawa S, Nishimura G, Fukushima Y, Nakagomi T, Saito H, Sugimoto T, Kamegaya M, Hisa K, Murray JC, Taniguchi N, Niikawa N, Yoshiura K 2000 Domain-specific mutations in TGFB1 result in Camurati-Engelmann disease. Nat Genet 26:19-20.
46. Wang J, Shackleford GM 1996 Murine Wnt10a and Wnt10b: Cloning and expression in developing limbs, face and skin of embryos and in adults. Oncogene 13:1537-1544.
47. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C 2005 Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8:727-738.
48. Gaur T, Lengner CJ, Hovhannisyan H, Bhat RA, Bodine PV, Komm BS, Javed A, van Wijnen AJ, Stein, Stein GS, Lian JB 2005 Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem 280:3132-3140.
49. Wozney JM 1992 The bone morphogenetic protein family and osteogenesis. Mol Reprod Dev 32:160-167.
50. Barlow AJ, Francis-West PH 1997 Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial promordia. Development 124:391-398.
51. St-Jacques B, Hammerschmidt M, McMahon AP 1999 Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13:2072-2086.
52. Seki K, Hata A 2004 Indian hedgehog gene is a target of the bone morphogenetic protein signaling pathway. J Biol Chem 279:18544-18549.
53. Yosida CA, Yamamoto H, Fujita T, Ito K, Inoue K, Yamana K, Zanma A, Takada K, Ito Y, Koraori T 2004 Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev 18:952-963.