A solution NMR investigation into the murine amelogenin splice-variant LRAP (Leucine-Rich Amelogenin Protein)

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 9, 2010, Pages 1768-1774

  Buchko, Garry W ^a   Tarasevich, Barbara J ^a   Roberts, Jacky ^a   Snead, Malcolm L ^b   Shaw, Wendy J ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Amelogenesis; Biomineralization; Cell signaling; Dynamic light scattering; Enamel; Intrinsic disorder; LRAP; Nanosphere self assembly; NMR spectroscopy

Indexed keywords

ACETIC ACID; AMELOGENIN; LEUCINE RICH AMELOGENIN PROTEIN; NANOSPHERE; PROLINE; SODIUM CHLORIDE; UNCLASSIFIED DRUG; AMIDE; ENAMEL PROTEIN; LEUCINE-RICH AMELOGENIN PEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; ISOMERIZATION; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION; ALTERNATIVE RNA SPLICING; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MOUSE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

MURINAE;

ALTERNATIVE SPLICING; AMELOGENIN; AMIDES; ANIMALS; DENTAL ENAMEL PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; SODIUM CHLORIDE;

EID: 77955174627     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.03.006     Document Type: Article

References (51)

1. Ten Cate A.R. Oral Histology: Development, Structure, and Function 1994, St. Louis, Mosby. 4th ed.
2. White S.N., Luo W., Paine M.L., Fong H., Sarikaya M., Snead M.L. Biological organization of hydroxyapatite crystallites into a fibrous continuum toughens and controls anisotrophy in human enamel. J. Dent. Res. 2001, 80:321-326.
3. Hunter G. Interfacial aspects of biomineralization. Curr. Opin. Mat. Sci. 1996, 1:430-435.
4. Margolis H.C., Beniash E., Fowler C.E. Role of macromolecular assembly of enamel matrix proteins in enamel formation. Crit. Rev. Oral Biol. Med. 2006, 85:775-793.
5. Termine J.D., Belcourt A.B., Christner P.J., Conn K.M., Nylen M.U. Properties of dissociatively extracted fetal tooth matrix proteins. J. Biol. Chem. 1990, 255:9760-9768.
6. 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.
7. Fincham A.G., Moradian-Oldak J., Diekwisch T.G.H., Lyaruu D.M., Wright J.T., P.B., Slavkin H.C. Evidence for amelogenin "nanospheres" as functional components of secretory-stage enamel matrix. J. Struct. Biol. 1995, 115:50-59.
8. Uchida T., Tanabe T., Fukae M., Shimizu M., Yamada M., Miake K., Kobayashi S. Immunochemical and immunohistochemical studies, using antisera against porcine 25kDa amelogenin, 89kDa enamelin and the 12-17kDa nonamelogenins, on immature enamel of the pig and rat. Histochemistry 1991, 96:129-138.
9. Ravassipour D., Hart P.S., Hart T.C., Ritter A.V., Yamauchi M., Gibson C., Wright J.T. Unique enamel phenotype associated with amelogenin gene (AMELX) codon 41 point mutation. J. Dent. Res. 2000, 79:1476-1481.
10. Gibson C.W., Yaun Z.A., Hall B., Longenecker G., Chen E.H., Thyagarajan T., Sreenath T., Wright J.T., Decker S., Piddington R., Harrison G., Kulkarni A.B. Amelogenin-deficient mice display an amelogenesis imperfecta type phenotype. J. Biol. Chem. 2001, 276:31871.
11. Moradian-Oldak J., Paine M.L., Lei Y.P., Fincham A.G., Snead M.L. Self-assembly properties of recombinant engineered amelogenin proteins analyzed by dynamic light scattering and atomic force microscopy. J. Struct. Biol. 2000, 131:27-37.
12. Paine M.L., White S.N., Luo W., Fong H., Sarikaya M., Snead M.L. Regulated gene expression dictates enamel structure and tooth function. Matrix Biol. 2001, 20:273-292.
13. Wen H.B., Fincham A.G., Moradian-Oldak J. Progressive accretion of amelogenin molecules during nanosphere assembly revealed by atomic force microscopy. Matrix Biol. 2001, 20:387-395.
14. Du C., Falini G., Fermani S., Abbott C., Moradian-Oldak J. Supramolecular assembly of amelogenin nanospheres into birefringent microribbons. Science 2005, 307:1450-1454.
15. Moradian-Oldak J., Simmer J.P., Lau E.C., Sarte P.E., Slavkin H.C., Fincham A.G. Detection of monodisperse aggregates of a recombinant amelogenin by dynamic light scattering. Biopolymers 1994, 34:1339-1347.
16. Moradian-Oldak J., Leung W., Fincham A.G. Temperature and pH-dependence of amelogenin self-assembly: a particle size distribution study. J. Struct. Biol. 1998, 122:320-327.
17. Buchko G.W., Tarasevich B.J., Bekhazi J., Snead M.L., Shaw W.J. A solution NMR investigation into the early events of amelogenin nanosphere self-assembly initiated with sodium chloride or calcium chloride. Biochemistry 2008, 47:6571-6582.
18. Dempsey C.E. The actions of melittin on membranes. Biochim. Biophys. Acta 1990, 1031:143-161.
19. Moradian-Oldak J. Amelogenins: assembly, processing and control of crystal morphology. Matrix Biol. 2001, 20:293-305.
20. Paine M.L., Snead M.L. Protein interactions during assembly of the enamel organic extracellular matrix. J. Bone Miner. Res. 1997, 12:221-227.
21. Toyosawa S., O'hUigin F., Figueroa F., Tichy H., Klein J. Identification and characterization of amelogenin genes in monotremes, reptiles, and amphibians. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13056-13061.
22. Buchko G.W., McAteer K., Wallace S.S., Kennedy M.A. Solution-state NMR investigation of DNA binding interactions in Escherichia coli formamidopyrimidine-DNA glycosylase (Fpg): a dynamic description of the DNA/protein interface. DNA Repair 2005, 4:327-339.
23. Moradian-Oldak J., Tan J., Fincham A.G. Interaction of amelogenin with hydroxyapatite crystals: an adherence effect through amelogenin self-association. Biopolymers 1998, 46:225-238.
24. Aoba T., Moreno E.C. The enamel fluid in the early secretory stage of porcine amelogenesis: chemical composition and saturation with respect to enamel mineral. Calcif. Tissue Int. 1987, 41:86-94.
25. Moradian-Oldak J., Bouropoulos N., Wang L., Gharakhanian N. Analysis of the self-assembly and appetite binding properties of amelogenin proteins lacking the hydrophilic C-terminal. Matrix Biol. 2002, 21:197-205.
26. Gibson C.W. The amelogenin "enamel proteins" and cells in the periodontium. Cells Tissues Organs 2008, 18:345-360.
27. Veis A., Tompkinds K., Alvares K., Wei K., Wang L., Wang S., Brown A.G., Jengh S.-M., Healy K.E. Specific amelogenin gene splice products have signaling effects on cells in culture and in implants in vivo. J. Biol. Chem. 2000, 275:41263-41272.
28. Boabaid F., Gibson C.W., Kuehl M.A., Berry J.E., Snead M.L., Nociti F.H.J., Katchburian E., Sommerman M.J. Leucine-rich amelogenin peptide: a candidate signalling molecule during cementogenesis. J. Periodontol. 2004, 75:1126-1136.
29. Warotayanont R., Zhu D., Snead M.L., Zhou Y. Leucine-rich amelogenin peptide induces osteogenesis in mouse embryonic stem cells. Biochem. Biophys. Res. Commum. 2008, 367:1-6.
30. Habelitz S., Kullar A., Marshall S.J., DenBesten P.K., Balooch M., Marshall G.W., Li W. Amelogenin-guided crystal growth on fluoroapatite glass-ceramics. J. Dent. Res. 2004, 83:698-702.
31. Shaw W.J., Ferris K. Structure, orientation, and dynamics of the C-terminal hexapeptide of LRAP determined using solid-state NMR. J. Phys. Chem. B 2008, 112:16975-16981.
32. Shaw W.J., Ferris K., Tarasevich B.J., Larson J.L. The structure and orientation of the C-terminus of LRAP. Biophysical J. 2008, 94:3247-3257.
33. Chen E.H., 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.
34. 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 2008, 189:169-174.
35. Ravindranath R.M.H., Devarajan A., Bringas, Jr.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.
36. Goto Y., Kogure E., Takagi T., Aimoto S., Aoba T. Molecular conformation of porcine amelogenin in solution: three folding units at the N-terminal, central, and C-terminal regions. J. Biochem. (Tokyo) 1993, 113:55-60.
37. Snead M.L., Lau E.C., Zeichner-David M., Fincham A.G., Woo S.L., Slavkin H.C. DNA sequence for cloned cDNA for murine amelogenin reveals the amino acid sequence for enamel-specific proteins. Biochem. Biophys. Res. Commum. 1986, 129:812-818.
38. 15N resonance assignments of murine amelogenin, an enamel biomineralization protein. Biomol. NMR Assign. 2008, 2:89-91.
39. Zuiderweg E.R.P. Mapping protein-protein interactions in solution using NMR spectroscopy. Biochemistry 2002, 41:1-7.
40. Simmer J.P., Lau E.C., Hu C.C., Bringas P., Santos V., Aoba T., Lacey M., Nelson D., Zeichner-David M., Snead M.L., Slavkin H.C., Fincham A.G. Isolation and characterization of a mouse amelogenin expressed in Escherichia coli. Calcif. Tissue Int. 1994, 54:312-319.
41. Goddard T.D., Kneller D.G. Sparky 3 2004, University of California, San Francisco.
42. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 1995, 6:135-140.
43. Buchko G.W., Ni S., Lourette N.M., Reeves R., Kennedy M.A. NMR resonance assignments of the high mobility group protein HMGA1. J. Biomol. NMR 2007, 38:185.
44. Ishima R., Torchia D.A. Protein dynamics from NMR. Nat. Struct. Biol. 2000, 7:740-743.
45. Delak K., Harcup C., Lakshminarayanan R., Sun Z., Fan Y., Moradian-Oldak J., Evans J.S. The tooth enamel protein, procine amelogenin, is an intrinsically disordered protein with an extended molecular configuration in the monomeric form. Biochemistry 2009, 48:2272-2281.
46. Schubert M., Labudde D., Oschkinat H., Schmieder P. A software tool for prediction of Xaa-Pro peptide bond conformations in proteins based on 13C chemical shift statistics. J. Biomol. NMR 2002, 24:149-154.
47. Lee D., Hilty C., Wider G., Wuthrich K. Effective rotational correlation times of proteins from NMR relaxation interference. J. Magn. Reson. 2006, 178:72-76.
48. Mulder F.A.A., Hon G., Muhandiram D.R., Dahlquist F.W., Kay L.E. Flexibility and ligand exchange in a buried cavity mutant of T4 lysozyme studied by multinuclear NMR. Biochemistry 2000, 39:12614-12622.
49. Le T.Q., Gochin M., Featherstone J.D.B., Li W., DenBesten P.K. Comparative calcium binding of leucine-rich amelogenin peptide and full-length amelogenin. Eur. J. Oral Sci. 2006, 114(Suppl. 1):320-326.
50. Miller S., Janin J., Lesk A.M., Chothia C. Interior and surface of monomeric proteins. J. Mol. Biol. 1987, 196:641-656.
51. Kohn W.D., Kay C.M., Hodges R.S. Salt effects on protein stability: two-stranded alpha-helical coiled-coils containing inter- or intrahelical ion pairs. J. Mol. Biol. 1997, 267:1039-1052.