A C-RING-like domain participates in protein self-assembly and mineral nucleation

Biochemistry

Volumn 50, Issue 41, 2011, Pages 8880-8887

  Amos, Fairland F ^a   Ndao, Moise ^a   Ponce, Christopher B ^a   Evans, John Spencer ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; EXTRACELLULAR PROTEINS; IN-VITRO; MINERAL FORMATION; MOLECULAR SURFACES; MOLLUSK SHELL; N-TERMINAL DOMAINS; PARTICLE MORPHOLOGIES; PH RANGE; RANDOM COIL; SELF-ASSOCIATIONS; SEQUENCE HOMOLOGY; SINGLE-CRYSTAL ARAGONITE; SUPRAMOLECULAR ASSEMBLIES; TWO DOMAINS;

AMINO ACIDS; ASSOCIATION REACTIONS; AZOBENZENE; CALCIUM CARBONATE; CARBONATE MINERALS; DYES; ENZYME ACTIVITY; NUCLEATION; OLIGOMERS; PH; PROTEINS; RESONANCE; SELF ASSEMBLY; SILICATE MINERALS; SINGLE CRYSTAL SURFACES; SUPRAMOLECULAR CHEMISTRY;

MAGNETIC DOMAINS;

AP7 PROTEIN; AP7C PROTEIN; AP7N PROTEIN; RING FINGER PROTEIN; UNCLASSIFIED DRUG;

ACIDITY; ALKALINITY; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; MINERALIZATION; NUCLEAR MAGNETIC RESONANCE; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; SEQUENCE ANALYSIS; STATIC ELECTRICITY;

ANIMALS; ANIONS; CALCIUM CARBONATE; CARRIER PROTEINS; CATIONS; HYDROGEN-ION CONCENTRATION; LIGHT; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, ELECTRON, TRANSMISSION; MINERALS; MOLLUSCA; NACRE; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SCATTERING, RADIATION; STATIC ELECTRICITY;

EID: 80054753936     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201346d     Document Type: Article

References (41)

1. Shen, X., Belcher, A. M., Hansma, P. K., Stucky, G. D., and Morse, D. E. (1997) Molecular cloning and characterization of Lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens J. Biol. Chem. 272, 32472-32481 (Pubitemid 28011932)
2. Samata, T., Hayashi, N., Kono, M., Hasegawa, K., Horita, C., and Akera, S. (1999) A new matrix protein family related to the nacreous layer formation of Pinctada fucata FEBS Lett. 462, 225-232
3. Ma, Z., Huang, J., Sun, J., Wang, G., Li, C., Xi, L., and Zhang, R. (2007) A novel extrapallial fluid protein controls the morphology of nacre lamellae in the pearl oyster, Pinctada fucata J. Biol. Chem. 282, 23253-23260
4. Suzuki, M., Saruwatari, K., Kogure, T., Yamamoto, Y., Nishimura, T., Kato, T., and Nagasawa, H. (2009) An acidic matrix protein, Pif, is a key macromolecule for nacre formation Science 325, 1388-1390
5. Michenfelder, M., Fu, G., Lawrence, C., Weaver, J. C., Wustman, B. A., Taranto, L., and Evans, J. S. (2003) Characterization of two molluscan crystal-modulating biomineralization proteins and identification of putative mineral binding domains Biopolymers 70, 522-533 (Pubitemid 37531835)
6. 2004, 73, 291. (erratum)
7. Fu, G., Qiu, S. R., Orme, C. A., Morse, D. E., and DeYoreo, J. J. (2007) Acceleration of calcite kinetics by nacre proteins Adv. Mater. 17, 2678-2683
8. Falini, G., Albeck, S., Weiner, S., and Addadi, L. (1996) Control of aragonite or calcite polymorphism by mollusk shell macromolecules Science 271, 67-69
9. Ndao, M., Keene, E., Amos, F. A., Rewari, G., Ponce, C. B., Estroff, L., and Evans, J. S. (2010) Intrinsically disordered mollusk shell prismatic protein that modulates calcium carbonate crystal growth Biomacromolecules 11, 2539-2544
10. Delak, K., Harcup, C., Lakshminarayanan, R., Zhi, S., Fan, Y., Moradian-Oldak, J., and Evans, J. S. (2009) The tooth enamel protein, porcine amelogenin, is an intrinsically disordered protein with an extended molecular configuration in the monomeric form Biochemistry 48, 2272-2281
11. Mann, K., Siedler, F., Treccani, L., Heinemann, F., and Fritz, M. (2007) Perlinhibin, a cysteine, histidine, and arginine-rich miniprotein from abalone (Haliotis laevigata) nacre, inhibits in vitro calcium carbonate crystallization Biophys. J. 93, 1246-1252
12. 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
13. Uversky, V. N. (2002) Natively unfolded proteins: A point where biology waits for physics Protein Sci. 11, 739-756 (Pubitemid 34241284)
14. Uversky, V. N., Gillespie, J. R., and Fink, A. L. (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41, 415-427
15. Meng, J., Romero, P., Yang, J. Y., Chen, J. W., Vacic, V., Obradovic, Z., and Uversky, V. N. (2008) The unfoldomics decade: An update on intrinsically disordered proteins BMC Genomics 9, 1-26
16. 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 (Pubitemid 351431364)
17. Kim, I. W., Collino, S., Morse, D. E., and Evans, J. S. (2006) A crystal modulating protein from molluscan nacre that limits the growth of calcite in vitro Cryst. Growth Des. 6, 1078-1082 (Pubitemid 43823567)
18. Collino, S. and Evans, J. S. (2007) Structural features that distinguish kinetically distinct biomineralization polypeptides Biomacromolecules 7, 1686-1694 (Pubitemid 46876287)
19. Amos, F. F., Ponce, C. B., and Evans, J. S. (2011) Formation of framework nacre polypeptide supramolecular assemblies that nucleate polymorphs Biomacromolecules 12, 1883-1889
20. Keene, E. C., Evans, J. S., and Estroff, L. A. (2010) Silk fibroin hydrogels coupled with the n16N-β-chitin complex: An in vitro organic matrix for controlling calcium carbonate mineralization Cryst. Growth Des. 10, 5169-5175
21. Amos, F. F., Destine, E., Ponce, C. B., and Evans, J. S. (2010) The N- and C-terminal regions of the pearl-associated EF hand protein, PFMG1, promote the formation of the aragonite polymorph in vitro Cryst. Growth Des. 10, 4211-4216
22. Saurin, A. J., Borden, K. L. B., Boddy, M. N., and Freemont, P. S. (1996) Does this have a familiar RING? Trends Biochem. Sci. 21, 208-215
23. Freemont, P. S. (2000) Ubiquitination: RING for destruction? Curr. Biol. 10, R84-R87
24. Capili, A. D., Edghill, E. L., Wu, K., and Borden, K. L. B. (2004) Structure of the C-terminal RING finger from a RING-IBR-RING/TRIAD motif reveals a novel zinc-binding domain distinct from a RING J. Mol. Biol. 340, 1117-1129 (Pubitemid 38968705)
25. Borden, K. L. B. (2000) RING domains: Master builders of molecular scaffolds? J. Mol. Biol. 295, 1103-1112
26. Schärtl, W. (2007) Light scattering from polymer solutions and nanoparticle dispersions, 1st ed., Springer-Verlag, Heidelberg, Germany.
27. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: An automated pipeline for the setup, execution, and analysis of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32, 665-667
28. Baker, N. H., Sept, D., Joseph, S., Holst, N. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041 (Pubitemid 32802969)
29. Ndao, M., Dutta, K., Bromley, K., Sun, Z., Lakshminarayanan, R., Rewari, G., Moradian-Oldak, J., and Evans, J. S. (2011) Probing the self-association, intermolecular contacts, and folding propensity of amelogenin Protein Sci. 20, 724-734
30. Buchko, G. W., Tarasevich, B. J., Bekhazi, J., Snead, M. L., and Shaw, W. J. (2008) A solution NMR investigation into the early events of amelogenin nanosphere self-assembly Biochemistry 47, 13215-13222
31. 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 (Pubitemid 44887278)
32. Shera, J. N. and Sun, X. S. (2009) Effect of peptide sequence on surface properties and self-assembly of an amphipathic pH-responsive peptide Biomacromolecules 10, 2446-2450
33. Zimenkov, Y., Dublin, S. N., Ni, R., Tu, R. S., Breedveld, V., Apkarian, R. P., and Conticello, V. P. (2006) Rational design of a reversible pH-responsive switch for peptide self-assembly J. Am. Chem. Soc. 126, 6770-6771 (Pubitemid 43830548)
34. Dalmau, M., Lim, S., and Wang, S. W. (2009) pH-triggered disassembly in a caged protein complex Biomacromolecules 10, 3199-3206
35. Kayser, V., Turton, D. A., Aggeli, A., Beevers, A., Reid, G. D., and Beddard, G. S. (2004) Energy migration in novel pH-triggered self-assembled β-sheet ribbons J. Am. Chem. Soc. 126, 336-343 (Pubitemid 38090374)
36. Rajagopal, K., Lamm, M. S., Haines-Butterick, L. A., Pochan, D. J., and Schneider, J. P. (2009) Tuning the pH responsiveness of β-hairpin peptide folding, self-assembly, and hydrogel material formation Biomacromolecules 10, 2619-2625
37. Chichagov, A. V., Varlamov, D. A., Dilanyan, R. A., Dokina, T. N., Drozhzhina, N. A., Samokhvalova, O. L., and Ushakovskaya, T. V. (2001) MINCRYST: A crystallographic database for minerals, local and network (WWW) versions Crystallogr. Rep. 46, 876-879
38. Ndao, M., Keene, E., Amos, F. A., Rewari, G., Ponce, C. B., Estroff, L., and Evans, J. S. (2010) Intrinsically disordered mollusk shell prismatic protein that modulates calcium carbonate crystal growth Biomacromolecules 11, 2539-2544
39. Song, Y., Mao, J., and Gunner, M. R. (2009) MCCE2: Improving protein pKa calculations with extensive side chain rotamer sampling J. Comput. Chem. 30, 2231-2247
40. Merz, K. M. (1991) Determination of pKas of ionizable groups in proteins: The pKa of Glu 7 and 35 in hen egg white lysozyme and Glu 106 in human carbonic anhydrase J. Am. Chem. Soc. 113, 3572-3575
41. Li, H., Robertson, A. D., and Jensen, J. H. (2005) Very fast empirical prediction and rationalization of protein pKa values Proteins: Struct., Funct., Bioinf. 61, 704-721 (Pubitemid 41753142)