A solution NMR investigation into the early events of amelogenin nanosphere self-assembly initiated with sodium chloride or calcium chloride

Biochemistry

Volumn 47, Issue 50, 2008, Pages 13215-13222

  Buchko, Garry W ^a   Tarasevich, Barbara J ^a   Bekhazi, 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

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM ALLOYS; CALCIUM CHLORIDE; MOLECULAR DYNAMICS; NANOSPHERES; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; QUANTUM CHEMISTRY; SELF ASSEMBLY; SODIUM CHLORIDE; THEOREM PROVING;

AMELOGENIN; HSQC SPECTRUMS; INTERACTION MECHANISMS; NACL CONCENTRATIONS; NMR SPECTROSCOPIES; ROTATIONAL CORRELATION TIMES; SOLUTION CONDITIONS;

DYNAMICS;

ACETIC ACID; AMELOGENIN; CALCIUM CHLORIDE; CARBON 13; DIMER; HYDROGEN; NANOSPHERE; NITROGEN 15; SODIUM CHLORIDE;

ARTICLE; CONCENTRATION (PARAMETERS); CORRELATION ANALYSIS; DIMERIZATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; INTROSPECTION; LIGHT SCATTERING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; SPECIES;

AMELOGENIN; ANIMALS; CALCIUM CHLORIDE; LIGHT; MICE; NANOSPHERES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SCATTERING, RADIATION; SODIUM CHLORIDE; SOLUTIONS;

MURINAE;

EID: 57649120771     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8018288     Document Type: Article

References (52)

1. Ten Cate, A. R. (1994) Oral histology: Developement, Structure, and Function, 4th ed., Mosby, St. Louis, MO.
2. Landis, W. J. (1995) The strength of calcified tissue depends in part on the molecular structure and organization of its constituent mineral crystals in their organix matrix. Bone 16, 533-544.
3. White, S. N., Luo, W., Paine, M. L., Fong, H., Sarikaya, M., and Snead, M. L. (2001) Biological organization of hydroxyapatite crystallites into a fibrous continuum toughens and controls anisotrophy in human enamel. J. Dent. Res. 80, 321-326.
4. Hunter, G. (1996) Interfacial aspects of biomineralization. Curr. Opin. Mat. Sci. 1, 430-435.
5. Margolis, H. C., Beniash, E., and Fowler, C. E. (2006) Role of macromoleculare assembly of enamel matrix proteins in enamel formation. Crit. Rev. Oral Biol. Med. 85, 775-793.
6. Termine, J. D., Belcourt, A. B., Christner, P. J., Conn, K. M., and Nylen, M. U. (1990) Properties of dissociatively extracted fetal tooth matrix proteins. J. Biol. Chem. 255, 9760-9768.
7. Fincham, A. G., Moradian-Oldak, J., Simmer, J. P., Sarte, P., Lau, E. C., Diekwisch, T., and Slavkin, H. C. (1994) Self-assembly of a recombinant amelogenin protein generates supramolecular structures. J. Struct. Biol. 112, 103-109.
8. Fincham, A. G., Moradian-Oldak, J., Diekwisch, T. G. H., Lyaruu, D. M., Wright, J. T., Jr., P. B., and Slavkin, H. C. (1995) Evidence for amelogenein "nanospheres" as functional components of secretory-stage enamel matrix. J. Struct. Biol. 115, 50-59.
9. Uchida, T., Tanabe, T., Fukae, M., Shimizu, M., Yamada, M., Miake, K., and Kobayashi, S. (1991) Immunochemical and immunohistochemical studies, using antisera against porcine 25 kDa amelogenin, 89 kDa enamelin and the 12-17 kDa nonamelogenins, on immature enamel of the pig and rat. Histochemistry 96, 129-138.
10. Toyosawa, S., O'hUigin, F., Figueroa, F., Tichy, H., and Klein, J. (1998) Identification and characterization of amelogenin genes in monotremes, reptiles, and amphibians. Proc. Natl. Acad. Sci. U.S.A. 95, 13056-13061.
11. Snead, M. L., Lau, E. C., Zeichner-David, M., Fincham, A. G., Woo, S. L., and Slavkin, H. C. (1986) DNA sequence for cloned cDNA for murine amelogenin reveals the amino acid sequence for enamel-specific proteins. Biochem. Biophys. Res. Commum. 129, 812-818.
12. Renugopalakrishnan, V., Strawich, E. S., Horowitz, P. M., and Glimcher, M. J. (1986) Studies of the secondary structure of amelogenin from bovin tooth enamel. Biochemistry 25, 4879-4887.
13. Goto, Y., Kogure, E., Takagi, T., Aimoto, S., and Aoba, T. (1993) Molecular conformation of porcine amelogenin in solution: three folding units at the N-terminal, central, and C-termininal regions. J. Biochem. (Toyko) 113, 55-60.
14. Lakshminarayanan, R., Fan, D., Du, C., and Moradian-Oldak, J. (2007) The role of secondary structure in the entropically driven amelogenin self-assembly. Biophys. J. 93, 3664-3674.
15. Matsushima, N., Izumi, Y., and Aoba, T. (1998) Small-angle X-ray scattering and computer-aided molecular modeling studies of 20 kDa fragment of porcine amelogenin: does amelogenin adopt an elongated bundle structure? J. Biochem. 123, 150-156.
16. Robinson, S., Fuchs, P., and Weatherell, J. A. (1981) The appearance of developing rat incisor enamel using a freeze fracturing technique. J. Cryst. Growth 53, 160-165.
17. Moradian-Oldak, J., Simmer, J. P., Lau, E. C., Sarte, P. E., Slavkin, H. C., and Fincham, A. G. (1994) Detection of monodisperse aggregates of a recombinant amelogenin by dynamic light scattering. Biopolymers 34, 1339-1347.
18. Moradian-Oldak, J., Leung, W., and Fincham, A. G. (1998) Temperature and pH-dependence of amelogin self-assembly: A particle size distribution study. J. Struct. Biol. 122, 320-327.
19. Du, C., Falini, G., Fermani, S., Abbott, C., and Moradian-Oldak, J. (2005) Supramolecular assembly of amelogenin nanospheres into birefringent microribbons. Science 307, 1450-1454.
20. Moradian-Oldak, J., Paine, M. L., Lei, Y. P., Fincham, A. G., and Snead, M. L. (2000) Self-assembly properties of recombinant engineered amelogenin proteins analyzed by dynamic light scattering and atomic force microscopy. J. Struct. Biol. 131, 27-37.
21. Paine, M. L., White, S. N., Luo, W., Fong, H., Sarikaya, M., and Snead, M. L. (2001) Regulated gene expression dictates enamel structure and tooth function. Matrix Biol. 20, 273-292.
22. Moradian-Oldak, J., Jiminez, I., Maltby, D., and Fincham, A. G. (2001) Controlled proteolysis of amelogenins reveals exposure of both carboxy- and amino terminal regions. Biopolymers 58, 606-616.
23. Paine, M. L., and Snead, M. L. (1997) Protein interactions during assembly of the enamel organic extracellular matrix. J. Bone Min. Res. 12, 221-227.
24. Wen, H. B., Fincham, A. G., and Moradian-Oldak, J. (2001) Progressive accretion of amelgenin molecules during nanosphere assembly revealed by atomic force microscopy. Matrix Biol. 20, 387-395.
25. Dempsey, C. E. (1990) The actions of melittin on membranes. Biochim. Biophys. Acta 1031, 143-161.
26. Moradian-Oldak, J. (2001) Amelogenins: assembly, processing and control of crystal morphology. Matrix Biol. 20, 293-305.
27. 15N Resonance assignments of murine amelogenin, an enamel biomineralization protein. Biomol. NMR Ass. 2, 89-91.
28. Buchko, G. W., McAteer, K., Wallace, S. S., and Kennedy, M. A. (2005) 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 4, 327-339.
29. Zuiderweg, E. R. P. (2002) Mapping protein-protein interactions in solution using NMR spectroscopy. Biochemistry 41, 1-7.
30. Ishima, R., and Torchia, D. A. (2000) Protein dynamics from NMR. Nat. Struct. Biol. 7, 740-743.
31. 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., and Fincham, A. G. (1994) Isolation and characterization of a mouse amelogenin expressed in Escherichia coli. Calcif. Tissue Int. 54, 312-319.
32. Szyperski, T., Yeh, D., Sukumaran, D., Moseley, H., and Montelione, G. (2002) Reduced-dimensionality NMR spectroscopy for high-throughput protein resonance assignment. Proc. Natl. Acad. Sci. U.S.A. 99, 8009-8014.
33. 15N Chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6, 135-140.
34. Lee, D., Hilty, C., Wider, G., and Wuthrich, K. (2006) Effective rotational correlation times of proteins from NMR relaxation interference. J. Magn. Reson. 178, 72-76.
35. Mulder, F. A. A., Hon, G., Muhandiram, D. R., Dahlquist, F. W., and Kay, L. E. (2000) Flexibility and ligand exchange in a buried cavity mutant of T4 lysozyme studied by multinuclear NMR. Biochemistry 39, 12614-12622.
36. Sogah, D. Y., Perle-Treves, D., Voyer, N., and DeGrado, W. F. (1994) Design and synthesis of polytripeptide (LeuGlnPro) based upon the matrix protein amelogenin. Macromol. Symp. 88, 149-163.
37. Aoba, T., and Moreno, E. C. (1987) The enamel fluid in the early secretory stage of porcine amelogenesis: chemical composition and saturation with respect to enamel mineral. Calcif. Tissue Int. 41, 86-94.
38. Krishnan, V. V., and Cosman, M. (1998) An emperical relationship between rotational correlation time and solvent accesible area. J. Biomol. NMR 12, 177-182.
39. Bhattacharjya, S., Ping, X., Gingras, R., Shaykhutdinov, R., Wu, C., Whiteway, M., and Ni, F. (2004) Solution structure of the dimeric SAM domain of MAPKKK Ste11 and its interactions with the adaptor protein STE50 from the budding yeast: implications for Ste11 activitation and signal transmission through the Ste50-Ste11 complex. J. Mol. Biol. 344, 1071-1087.
40. Squire, P. G., and Himmel, M. E. (1979) Hydrodynamics and protein hydration. Arch. Biochem. Biophys. 196, 165-177.
41. Fincham, A. G., Leung, W., Tan, J., and Moradian-Oldak, J. (1998) Does amelogenin nanosphere assembly proceed through intermediary-sized structures? Conn. Tis. Res. 38, 237-240.
42. Aichmayer, B., Margolis, H. C., Sigel, R., Yamakoshi, Y., Simmer, J. P., and Fratzl, P. (2005) The onset of amelogenin nanosphere aggregation studied by small-angle x-ray scattering and dynamic light scattering. J. Struct. Biol. 151, 239-249.
43. Tan, J., Leung, W., Moradian-Oldak, J., Zeichner-David, M., and Fincham, A. G. (1998) Quantitative analysis of amelogenin solubility. J. Dent. Res. 77, 1388-1396.
44. Tan, J., Leung, W., Moradian-Oldak, J., Zeichner-David, M., and Fincham, A. G. (1998) The pH dependent amelogenin solubility and its biological signficance. Conn. Tis. Res. 38, 215-221.
45. Miller, S., Janin, J., Lesk, A. M., and Chothia, C. (1987) Interior and surface of monomeric proteins. J. Mol. Biol. 196, 641-656.
46. Habelitz, S., Kullar, A., Marshall, S. J., DenBesten, P. K., Balooch, M., Marshall, G. W., and Li, W. (2004) Amelogenin-guided crystal growth on fluoroapatite glass-ceramics. J. Dent. Res. 83, 698-702.
47. Kohn, W. D., Kay, C. M., and Hodges, R. S. (1997) Salt effects on protein stability: two-stranded α-helical coiled-coils containing inter- or intrahelical ion pairs. J. Mol. Biol. 267, 1039-1052.
48. Shaw, W. J., Campbell, A. A., Paine, M. L., and Snead, M. L. (2004) The COOH terminus of the amelogenin, LRAP, is oriented next to the hydroxyapatite surface. J. Biol. Chem. 279, 40263-40266.
49. Shaw, W. J., Ferris, K., Tarasevich, B. J., and Larson, J. L. (2008) The structure and orientation of the C-terminus of LRAP. Biophys. J. 94, 3247-3257.
50. Shaw, W. J., and Ferris, K. (2008) Structure, orientation and dynamics of the C-terminal hexapeptide of LRAP determined using solid state NMR, J. Phys. Chem. B, in press.
51. Ravassipour, D., Hart, P. S., Hart, T. C., Ritter, A. V., Yamauchi, M., Gibson, C., and Wright, J. T. (2000) Unique enamel phenotype associated with amelogenin gene (AMELX) codon 41 point mutation. J. Dent. Res. 79, 1476-1481.
52. Hopp, T. P., and Woods, K. R. (1981) Prediction of protein antigenic determinants from amino acid sequences. Proc. Natl. Acad. Sci. U.S.A. 75, 3824-3828.