Polyelectrolyte domains and intrinsic disorder within the prismatic asprich protein family

Biochemistry

Volumn 48, Issue 16, 2009, Pages 3669-3677

  Delak, Katya ^a   Collino, Sebastiano ^a   Evans, John Spencer ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIONIC SURFACES; BETA-STRAND; BIOMINERAL; C-TERMINAL REGIONS; CONFORMATIONAL RESPONSE; DISORDERED PROTEINS; DISORDERED STATE; EXPERIMENTAL CHARACTERIZATION; FUNCTIONAL PROTEINS; INTRINSIC DISORDER; METAL ION COMPLEXATION; POLYANIONIC; PREDICTION ALGORITHMS; PROTEIN FAMILY; PROTEIN SEQUENCES; RANDOM-COIL STRUCTURES; SOLVENT ACCESSIBILITY; SYNTHETIC PEPTIDE;

AMINES; BIOINFORMATICS; BIOMINERALIZATION; CALCIUM; CHARGED PARTICLES; GROWTH KINETICS; METAL IONS; MINING; POLYELECTROLYTES; SURFACE CHARGE;

PROTEINS;

ASPARAGINE; ASPARTIC ACID; ASPRICH PROTEIN; CALCIUM; GLUTAMINE; INTRINSICALLY DISORDERED PROTEIN; METAL ION; PEPTIDES AND PROTEINS; POLYELECTROLYTE; UNCLASSIFIED DRUG; METAL; PEPTIDE FRAGMENT; PROTEIN;

ALGORITHM; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; BIOMINERALIZATION; CARBOXY TERMINAL SEQUENCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; MOLECULAR GENETICS; PROTEIN CONFORMATION; SEQUENCE ANALYSIS; SYNTHESIS;

ALGORITHMS; AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; METALS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEINS; SEQUENCE ANALYSIS, PROTEIN;

EID: 65449165696     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900113v     Document Type: Article

References (51)

1. (a) Dyson, H. J., and Wright, P. E. (1998) Equilibrium NMR studies of unfolded and partially folded proteins. Nat. Struct. Biol. 7, 499-503.
2. (b) Dyson, H. J., and Wright, P. E. (1998) Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Methods Enzymol. 339, 258-270
3. (a) Uversky, V. N. (2002) Natively unfolded proteins: A point where biology waits for physics. Protein Sci. 11, 739-756.
4. (b) Tompa, P. (2002) Intrinsically unstructured proteins. Trends Biochem. Sci. 27, 527-533.
5. Meszaros, B., Tompa, P., Simon, I., and Dosztanyi, Z. (2007) Molecular principles of the interactions of disordered proteins. J. Mol. Biol. 372, 549-561.
6. Tran, H. T., Mao, A., and Pappu, R. V. (2008) Role of backbone-solvent interactions in determining conformational equilibria of intrinsically disordered proteins. J. Am. Chem. Soc. 130, 7380-7382
7. Oldfield, C. J., Cheng, Y., Cortese, M. S., Brown, C. J., Uversky, V. N., and Dunker, A. K. (2005) Comparing and combining predictors of mostly disordered proteins. Biochemistry 44, 1989-2000 (Pubitemid 40227474)
8. Kapłon, T. M., Rymarczyk, G., Nocula-Ługowska, M., Jakób, M., Kochman, M., Lisowski, M., Szewczuk, Z., and Ozẏhar, A. (2008) Starmaker exhibits properties of an intrinsically disordered protein. Biomacromolecules 9, 2118-2125.
9. Delak, K., Harcup, C., Lakshminarayanan, R., Sun, Z., Fan, Y., Moradian-Oldak, J., and Evans, J. S. (2009) The tooth enamel protein, amelogenin, is an intrinsically disordered protein with an extended molecular configuration in the monomeric form. Biochemistry 48, 2272-2281.
10. Amos, F. F., and Evans, J. S. (2009) AP7, a partially disordered pseudo C-RING protein, is capable of forming stabilized aragonite in vitro. Biochemistry 48, 1332-1339.
11. (a) Evans, J. S. (2008) "Tuning in" to mollusk shell nacre- and prismatic-associated protein terminal sequences. Implications for biomineralization and the construction of high performance inorganic-organic composites. Chem. Rev. 108, 4455-4462.
12. (b) Wustman, B. A., Weaver, J. C., Morse, D. E., and Evans, J. S. (2003) Characterization of a Ca(II)-, mineral-interactive polyelectrolyte sequence from the adhesive elastomeric biomineralization protein Lustrin A. Langmuir 19, 9373-9381.
13. (c) Wustman, B. A., Weaver, J. C., Morse, D. E., and Evans, J. S. (2002) Structural analyses of polyelectrolyte sequence domains within the adhesive elastomeric biomineralization protein Lustrin A. Langmuir 18, 9901-9906.
14. (a) Collino, S., Kim, I. W., and Evans, J. S. (2006) Identification of an "Acidic" C-Terminal mineral modification sequence from the mollusk shell protein Asprich. Cryst. Growth Des. 6, 839-842.
15. (b) Kim, I. W., Giocondi, J. L., Orme, C., Collino, S., and Evans, J. S. (2008) Morphological and kinetic transformation of calcite crystal growth by prismatic-associated Asprich sequences. Cryst. Growth Des. 8, 1154-1160.
16. (c) Delak, K., Giocondi, J., Orme, C., and Evans, J. S. (2008) Modulation of crystal growth by the terminal sequences of the prismatic-associated Asprich protein. Cryst. Growth Des. 8, 4481-4486.
17. Gotliv, B.-A., Kessler, N., Sumerel, J. L., Morse, D. E., Tuross, N., Addadi, L., and Weiner, S. (2005) Asprich: A novel aspartic acid rich protein family from the prismatic shell matrix of the bivalve Atrina rigida. ChemBioChem 6, 304-314 (Pubitemid 40879743)
18. Politi, Y., Mahamid, J., Goldberg, H., Weiner, S., and Addadi, L. (2007) Asprich mollusk shell protein: In vitro experiments aimed at elucidating function in CaCO3 crystallization. CrystEngComm 9, 1171-1177.
19. Sethi, D., Garg, A., and Raghava, G. P. S. (2008) DPROT: Prediction of disordered proteins using evolutionary information. Amino Acids 35, 599-605.
20. Linding, R., Russell, R. B., Neduva, V., and Gibson, T. J. (2003) GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701-3708 (Pubitemid 37442227)
21. (a) Li, X., Romero, P., Rani, M., Dunker, A. K., and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions. Genome Informatics 10, 30-40.
22. (b) Romero, P., Obradovic, Z., Li, X., Garner, E., Brown, C., and Dunker, A. K. (2001) Sequence complexity of disordered protein. Proteins: Struct., Funct., Genet. 42, 38-48.
23. (c) Romero, P., Obradovic, Z., and Dunker, A. K. (1997) Sequence data analysis for long disordered regions prediction in the calcineurin family. Genome Informatics 8, 110-124.
24. Yi, S., Boys, B. L., Brickenden, A., Konermann, L., and Choy, W. Y. (2007) Effects of zinc binding on the structure and dynamics of the intrinsically disordered protein prothymosin alpha: Evidence for metalation as an entropic switch. Biochemistry 46, 13120-13130 (Pubitemid 350089907)
25. Li, M., Liu, J., Ran, X., Fang, M., Shi, J., Qin, H., Goh, J. M., and Song, J. (2006) Resurrecting abandoned proteins with pure water: CD and NMR studies of protein fragments solubilized in salt-free water. Biophys. J. 91, 4201-4209.
26. (a) Collino, S., and Evans, J. S. (2008) The molecular specifications of a mineral modulation sequence derived from the aragnotepromoting protein, n16. Biomacromolecules 9, 1909-1918.
27. (b) Collino, S., Kim, I. W., and Evans, J. S. (2008) Identification and structural characterization of an unusual RING-like sequence within an extracellular biomineralization protein, AP7. Biochemistry 47, 3745-3755
28. Collino, S., and Evans, J. S. (2007) Structural features that distinguish kinetically distinct biomineralization polypeptides. Biomacromolecules 8, 1686-1694 (Pubitemid 46876287)
29. Wang, Y., Nip, A. M., and Wishart, D. S. (1997) A simple method to quantitatively measure polypeptide JHNHR coupling constants from TOCSY or NOESY spectra. J. Biomol. NMR 10, 373-382 (Pubitemid 127505377)
30. MacKerell, A. D., Brooks, B., Brooks, C. L., Nilsson, L., Roux, B., Won, Y., and Karplus, M. (1998) CHARMM: The Energy Function and Its Parameterization with an Overview of the Program, in The Encyclopedia of Computational Chemistry (Schleyer, P. v. R., et al., Eds.) Vol.1, pp 271-277, John Wiley & Sons, Chichester.
31. (a) Kumar, A., Wagner, G., Ernst, R. R., and Wuthrich, K. (1981) Buildup rates of the nuclear Overhauser effect measured by twodimensional proton magnetic resonance spectroscopy: Implications for studies of protein conformations. J. Am. Chem. Soc. 103, 3654-3658.
32. (b) Wuthrich, K. (1986) NMR of proteins and nucleic acids, Wiley-Interscience, New York, NY.
33. (c) Braun, W., and Go, N. (1985) Calculation of protein conformations by proton-proton distance constraints. A new efficient algorithm. J. Mol. Biol. 186, 611-626.
34. Wüthrich, K., Billeter, M., and Braun, W. (1993) Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance. J. Mol. Biol. 169, 949-961.
35. Baker, N. H., Sept, D., Joseph, S., Holst, N. J., and McCammon, J. A. (2001) Proc. Natl. Acad. Sci U.S.A. 98, 10037-10041.
36. (a) Uversky, V. N., Permyakov, S. E., Zagranichny, V. E., Rodionov, I. L., Fink, A. L., Cherskaya, A. M., and Permyakov, E. A. (2002) Effect of zinc and temperature on the conformation of the alpha subunit of retinal phosphodiesterases: A natively unfolded protein. J. Proteome Res. 1, 149-159.
37. (b) Uversky, V. N., Li, J., and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. J. Biol. Chem. 276, 44284-44296.
38. (c) Uversky, V. N., Gillespie, J. R., Millett, I. S., Khodyakova, A. V., Vasilenko, R. N., Vasiliev, A. M., Rodionov, I. L., Kozlovskaya, G. D., Dolgikh, D. A., Fink, A. L., Doniach, S., Permyakov, G. D., and Abramov, V. M. (2000) Zn(II)-mediated structure formation and compaction of the "natively unfolded" human prothymosin alpha. Biochem. Biophys. Res. Commun. 267, 663-668.
39. (d) Munishkina, L. A., Fink, A. L., and Uversky, V. N. (2004) Conformational prerequisites for formation of amyloid fibrils from histones. J. Mol. Biol. 342, 1305-1324
40. Markley, J. L., Bax, A., Arata, Y., Hilbers, C. W., Kaptein, R., Sykes, B. D., Wright, P. E., and Wüthrich, K. (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids. J. Biomol. NMR 12, 1-23.
41. Ma, K., San, L. S., and Wang, K. (2001) Polyproline II helix is a key structural motif of the elastic PEVK segment of titin. Biochemistry 40, 3427-3438 (Pubitemid 32242799)
42. (a) Serrano, L. (1995) Comparison between the phi distribution of the amino acids in the protein database and NMR data indicates that amino acids have various phi propensities in the random coil conformation. J. Mol. Biol. 254, 322-333.
43. (b) Smith, L. J., Bolin, K. A., Schwalbe, H., MacArthur, M. W., Thornton, J. M., and Dobson, C. M. (1996) Analysis of main chain torsion angles in proteins: Prediction of NMR coupling constants for native and random coil conformations. J. Mol. Biol. 255, 494-506
44. Fiebig, K. M., Schwalbe, H., Buck, M., Smith, L. J., and Dobson, C. M. (1996) Towards a description of the conformations of denatured states of proteins. Comparison of a random coil model with NMR measurements. J. Phys. Chem. 100, 2661-2666 (Pubitemid 126793219)
45. Eker, F., Griebenow, K., Cao, X., Nafie, L. A., and Schweitzer- Stenner, R. (2004) Tripeptides with ionizable side chains adopt a perturbed Polyproline II structure in water. Biochemistry 43, 613-621.
46. (a) Sarkar, P., Reichman, C., Saleh, T., Birge, R., and Kalodimos, C. G. (2007) Proline cis-trans isomerization controls autoinhibition of a signalling protein. Mol. Cell 25, 413-426.
47. (b) Andreotti, A. H. (2003) Native state proline isomerization: An intrinsic molecular switch. Biochemistry 42, 9515-9524.
48. (c) Nicholson, L. K., and Lu, K. P. (2007) Prolyl cis-trans isomerization as a molecular timer in Crk signaling. Mol. Cell 25, 483-486.
49. Kulp, J. L., Shiba, K., and Evans, J. S. (2005) Probing the conformational features of a phage display polypeptide sequence directed against single-walled carbon nanohorn surfaces. Langmuir 21, 11907-11914 (Pubitemid 43011535)
50. Pai, R. K., and Pillai, S. (2008) Divalent cation-induced variations in polyelectrolyte conformation and controlling calcite morphologies: Direct observation of the phase transition by atomic force microscopy. J. Am. Chem. Soc. 130, 13074-13078.
51. Dunker, A. K., Oldfield, C. J., Meng, J., Romero, P., Yang, J. Y., Walton, J., Vacic, V., Obradovic, Z., and Uversky, V. N. (2008) The unfoldomics decade: An update on intrinsically disordered proteins. BMC Genomics 9, 1-26.