Leucine rich amelogenin peptide alters ameloblast differentiation in vivo

Matrix Biology

Volumn 32, Issue 7-8, 2013, Pages 432-442

  Stahl, Jonathan ^a   Nakano, Yukiko ^a   Kim, Seong Oh ^b   Gibson, Carolyn W ^c   Le, Thuan ^a   DenBesten, Pamela ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Yonsei University College of Dentistry   (South Korea)

^c UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Ameloblasts; Amelogenin; Enamel; Leucine rich amelogenin peptide (LRAP); MMP20; SATB1; Transgenic mice

Indexed keywords

AMELOBLASTIN; AMELOGENIN; LEUCINE; MATRIX METALLOPROTEINASE 20; MESSENGER RNA; TRANSCRIPTION FACTOR;

ALVEOLAR BONE; AMELOBLAST; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL POLARITY; CHROMATIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; DEVELOPMENTAL STAGE; ENAMEL; EXON; IMMUNOLOCALIZATION; IN SITU HYBRIDIZATION; IN VIVO STUDY; MOLAR TOOTH; MOUSE; NONHUMAN; ODONTOBLAST; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETORY CELL; STEM CELL; STOP CODON; THICKNESS; TOOTH DEVELOPMENT; UPREGULATION;

MURINAE; MUS MUSCULUS; RODENTIA;

AMELOBLASTS; AMELOGENIN; ENAMEL; LEUCINE RICH AMELOGENIN PEPTIDE; LEUCINE RICH AMELOGENIN PEPTIDE (LRAP); LRAP; MATRIX METALLOPROTEINASE 20; MMP20; SATB1; TRANSGENIC MICE;

AMELOBLASTS; AMELOGENESIS; ANIMALS; CELL DIFFERENTIATION; DENTAL ENAMEL PROTEINS; DNA PRIMERS; GENE EXPRESSION REGULATION; HISTOLOGICAL TECHNIQUES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MATRIX ATTACHMENT REGION BINDING PROTEINS; MATRIX METALLOPROTEINASE 20; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; X-RAY MICROTOMOGRAPHY;

EID: 84889085791     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.05.004     Document Type: Article

References (45)

1. Agrelo R., Souabni A., Novatchkova M., Haslinger C., Leeb M., Komnenovic V., Kishimoto H., Gresh L., Kohwi-Shigematsu T., Kenner L., Wutz A. SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev. Cell 2009, 16:507-516.
2. Albrecht B.E., Breitenbach U., Stuhmer T., Harvey R.J., Darlison M.G. In situ hybridization and reverse transcription-polymerase chain reaction studies on the expression of the GABA(C) receptor rho1- and rho2-subunit genes in avian and rat brain. Eur. J. Neurosci. 1997, 9:2414-2422.
3. Boabaid F., Gibson C.W., Kuehl M.A., Berry J.E., Snead M.L., Nociti F.H., Katchburian E., Somerman M.J. Leucine-rich amelogenin peptide: a candidate signaling molecule during cementogenesis. J. Periodontol. 2004, 75:1126-1136.
4. Cai S., Han H.J., Kohwi-Shigematsu T. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat. Genet. 2003, 34:42-51.
5. Cai S., Lee C.C., Kohwi-Shigematsu T. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 2006, 38:1278-1288.
6. Chen E., Yuan Z.A., Wright J.T., Hong S.P., Li Y., Collier P.M., Hall B., D'Angelo M., Decker S., Piddington R., Abrams W.R., Kulkarni A.B., Gibson C.W. The small bovine amelogenin LRAP fails to rescue the amelogenin null phenotype. Calcif. Tissue Int. 2003, 73:487-495.
7. Ferguson C., Alpern E., Miclau T., Helms J.A. Does adult fracture repair recapitulate embryonic skeletal formation?. Mech. Dev. 1999, 87:57-66.
8. Fessing M.Y., Mardaryev A.N., Gdula M.R., Sharov A.A., Sharova T.Y., Rapisarda V., Gordon K.B., Smorodchenko A.D., Poterlowicz K., Ferone G., Kohwi Y., Missero C., Kohwi-Shigematsu T., Botchkarev V.A. p63 regulates Satb1 to control tissue-specific chromatin remodeling during development of the epidermis. J. Cell Biol. 2011, 194:825-839.
9. Fincham A.G., Moradian-Oldak J. Amelogenin post-translational modifications: carboxy-terminal processing and the phosphorylation of bovine and porcine "TRAP" and "LRAP" amelogenins. Biochem. Biophys. Res. Commun. 1993, 197:248-255.
10. Fincham A.G., Belcourt A.B., Termine J.D., Butler W.T., Cothran W.C. Dental enamel matrix: sequences of two amelogenin polypeptides. Biosci. Rep. 1981, 1:771-778.
11. Fincham A.G., Moradian-Oldak J., Simmer J.P., Sarte P., Lau E.C., Diekwisch T., Slavkin H.C. Self-assembly of a recombinant amelogenin protein generates supramolecular structures. J. Struct. Biol. 1994, 112:103-109.
12. Gibson C.W., Golub E., Ding W.D., Shimokawa H., Young M., Termine J., Rosenbloom J. Identification of the leucine-rich amelogenin peptide (LRAP) as the translation product of an alternatively spliced transcript. Biochem. Biophys. Res. Commun. 1991, 174:1306-1312.
13. Gibson C.W., Yuan Z.A., Hall B., Longenecker G., Chen E., Thyagarajan T., Sreenath T., Wright J.T., Decker S., Piddington R., Harrison G., Kulkarni A.B. Amelogenin-deficient mice display an amelogenesis imperfecta phenotype. J. Biol. Chem. 2001, 276:31871-31875.
14. Gibson C.W., Yuan Z.A., Li Y., Daly B., Suggs C., Aragon M.A., Alawi F., Kulkarni A.B., Wright J.T. Transgenic mice that express normal and mutated amelogenins. J. Dent. Res. 2007, 86:331-335.
15. Gibson C.W., Li Y., Daly B., Suggs C., Yuan Z.A., Fong H., Simmons D., Aragon M., Kulkarni A.B., Wright J.T. The leucine-rich amelogenin peptide alters the amelogenin null enamel phenotype. Cells Tissues Organs 2009, 189:169-174.
16. Gruenbaum-Cohen Y., Tucker A.S., Haze A., Shilo D., Taylor A.L., Shay B., Sharpe P.T., Mitsiadis T.A., Ornoy A., Blumenfeld A., Deutsch D. Amelogenin in cranio-facial development: the tooth as a model to study the role of amelogenin during embryogenesis. J. Exp. Zool. B Mol. Dev. Evol. 2009, 312B:445-457.
17. Habelitz S., DenBesten P.K., Marshall S.J., Marshall G.W., Li W. Self-assembly and effect on crystal growth of the leucine-rich amelogenin peptide. Eur. J. Oral Sci. 2006, 114(Suppl. 1):315-319. (discussion 327-319, 382).
18. Han H.J., Russo J., Kohwi Y., Kohwi-Shigematsu T. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 2008, 452:187-193.
19. Hu C.C., Ryu O.H., Qian Q., Zhang C.H., Simmer J.P. Cloning, characterization, and heterologous expression of exon-4-containing amelogenin mRNAs. J. Dent. Res. 1997, 76:641-647.
20. Iacob S., Veis A. Identification of the functional activity of the [A-4] amelogenin gene splice product in newborn mouse ameloblasts. Bone 2008, 42:1072-1079.
21. Iwasaki K., Bajenova E., Somogyi-Ganss E., Miller M., Nguyen V., Nourkeyhani H., Gao Y., Wendel M., Ganss B. Amelotin-a novel secreted, ameloblast-specific protein. J. Dent. Res. 2005, 84:1127-1132.
22. Kumar P.P., Bischof O., Purbey P.K., Notani D., Urlaub H., Dejean A., Galande S. Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat. Cell Biol. 2007, 9:45-56.
23. Le T.Q., Zhang Y., Li W., Denbesten P.K. The effect of LRAP on enamel organ epithelial cell differentiation. J. Dent. Res. 2007, 86:1095-1099.
24. Lee S.K., Kim S.M., Lee Y.J., Yamada K.M., Yamada Y., Chi J.G. The structure of the rat ameloblastin gene and its expression in amelogenesis. Mol. Cells 2003, 15:216-225.
25. Li R., Li W., DenBesten P.K. Alternative splicing of amelogenin mRNA from rat incisor ameloblasts. J. Dent. Res. 1995, 74:1880-1885.
26. Li W., Mathews C., Gao C., DenBesten P.K. Identification of two additional exons at the 3' end of the amelogenin gene. Arch. Oral Biol. 1998, 43:497-504.
27. Lu Y., Papagerakis P., Yamakoshi Y., Hu J.C., Bartlett J.D., Simmer J.P. Functions of KLK4 and MMP-20 in dental enamel formation. Biol. Chem. 2008, 389:695-700.
28. Nebgen D.R., Inoue H., Sabsay B., Wei K., Ho C.S., Veis A. Identification of the chondrogenic-inducing activity from bovine dentin (bCIA) as a low-molecular-mass amelogenin polypeptide. J. Dent. Res. 1999, 78:1484-1494.
29. Pavan Kumar P., Purbey P.K., Sinha C.K., Notani D., Limaye A., Jayani R.S., Galande S. Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol. Cell. 2006, 22:231-243.
30. Ravindranath R.M., Devarajan A., Bringas P. Enamel formation in vitro in mouse molar explants exposed to amelogenin polypeptides ATMP and LRAP on enamel development. Arch. Oral Biol. 2007, 52:1161-1171.
31. Reith E.J., Cotty V.F. The absorptive activity of ameloblasts during the maturation of enamel. Anat. Rec. 1967, 157:577-587.
32. Simmer J.P. Alternative splicing of amelogenins. Connect. Tissue Res. 1995, 32:131-136.
33. Simmer J.P., Hu C.C., Lau E.C., Sarte P., Slavkin H.C., Fincham A.G. Alternative splicing of the mouse amelogenin primary RNA transcript. Calcif. Tissue Int. 1994, 55:302-310.
34. Smith C.E. Ameloblasts: secretory and resorptive functions. J. Dent. Res. 1979, 58:695-707.
35. Smith C.E., Warshawsky H. Quantitative analysis of cell turnover in the enamel organ of the rat incisor. Evidence for ameloblast death immediately after enamel matrix secretion. Anat. Rec. 1977, 187:63-98.
36. Sundin O.H., Busse H.G., Rogers M.B., Gudas L.J., Eichele G. Region-specific expression in early chick and mouse embryos of Ghox-lab and Hox 1.6, vertebrate homeobox-containing genes related to Drosophila labial. Development 1990, 108:47-58.
37. Termine J.D., Belcourt A.B., Christner P.J., Conn K.M., Nylen M.U. Properties of dissociatively extracted fetal tooth matrix proteins I. Principal molecular species in developing bovine enamel. J. Biol. Chem. 1980, 255:9760-9768.
38. Thomsen R., Solvsten C.A., Linnet T.E., Blechingberg J., Nielsen A.L. Analysis of qPCR data by converting exponentially related Ct values into linearly related X0 values. J. Bioinforma. Comput. Biol. 2010, 8:885-900.
39. Tompkins K., Alvares K., George A., Veis A. Two related low molecular mass polypeptide isoforms of amelogenin have distinct activities in mouse tooth germ differentiation in vitro. J. Bone Miner. Res. 2005, 20:341-349.
40. Uchida T., Tanabe T., Fukae M., Shimizu M. Immunocytochemical and immunochemical detection of a 32kDa nonamelogenin and related proteins in porcine tooth germs. Arch. Histol. Cytol. 1991, 54:527-538.
41. Warotayanont R., Frenkel B., Snead M.L., Zhou Y. Leucine-rich amelogenin peptide induces osteogenesis by activation of the Wnt pathway. Biochem. Biophys. Res. Commun. 2009, 387:558-563.
42. Wen H.B., Fincham A.G., Moradian-Oldak J. Progressive accretion of amelogenin molecules during nanospheres assembly revealed by atomic force microscopy. Matrix Biol. 2001, 20:387-395.
43. Wen X., Cawthorn W.P., MacDougald O.A., Stupp S.I., Snead M.L., Zhou Y. The influence of leucine-rich amelogenin peptide on MSC fate by inducing Wnt10b expression. Biomaterials 2011, 32:6478-6486.
44. Xu L., Harada H., Taniguchi A. The exon 6ABC region of amelogenin mRNA contribute to increased levels of amelogenin mRNA through amelogenin protein-enhanced mRNA stabilization. J. Biol. Chem. 2006, 281:32439-32444.
45. Xu L., Harada H., Yokohama-Tamaki T., Matsumoto S., Tanaka J., Taniguchi A. Reuptake of extracellular amelogenin by dental epithelial cells results in increased levels of amelogenin mRNA through enhanced mRNA stabilization. J. Biol. Chem. 2006, 281:2257-2262.