De novo self-assembling collagen heterotrimers using explicit positive and negative design

Biochemistry

Volumn 49, Issue 11, 2010, Pages 2307-2316

  Xu, Fei ^a   Zhang, Lei ^b   Koder, Ronald L ^b   Nanda, Vikas ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; CIRCULAR DICHROISM; COLLAGEN PEPTIDES; COLLAGEN STABILITY; COLLAGEN-LIKE PEPTIDES; COMPUTATIONAL DESIGN; COMPUTATIONAL MODEL; DESIGN APPROACHES; DESIGN MODELS; FIBROUS PROTEINS; HETEROTRIMERS; PAIR INTERACTIONS; POLYPEPTIDE CHAIN; PROTEIN FOLDS; SELF-ASSEMBLING; THERMAL STABILITY; TRIPLE HELICAL STRUCTURES; TRIPLE-HELICES;

COLLAGEN; DICHROISM; OLIGOMERIZATION; OLIGOMERS; PEPTIDES; PROTEIN FOLDING; THERMOGRAVIMETRIC ANALYSIS;

DESIGN;

COLLAGEN; OLIGOMER; POLYPEPTIDE; SELF ASSEMBLED MONOLAYER;

ARTICLE; CIRCULAR DICHROISM; ELECTRICITY; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; THERMOSTABILITY;

AMINO ACID SEQUENCE; COLLAGEN; COMPUTER SIMULATION; DRUG DESIGN; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; STATIC ELECTRICITY; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 77949503842     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902077d     Document Type: Article

References (50)

1. Kalluri, R. (2003) Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3, 422-433.
2. Heino, J. (2007) The collagen family members as cell adhesion proteins. BioEssavs 29. 1001-1010.
3. Khoshnoodi, J., Pedchenko, V., and Hudson, B. G. (2008) Mammalian collagen IV. Micros. Res. Tech. 71, 357-370.
4. Rich, A., and Crick, F. H. (1961) The molecular structure of collagen. J. Mol. Biol. 3, 483-506.
5. Bella, J., Eaton, M., Brodsky, B., and Berman, H. M. (1994) Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution. Science 266. 75-81.
6. Bella, J., Brodsky, B., and Berman, H. M. (1995) Hydration structure of a collagen peptide. Structure 3, 893-906.
7. Kuznetsova, N., Rau, D. C., Parsegian, V. A., and Leikin, S. (1997) Solvent hydrogen-bond network in protein self-assembly: solvation of collagen triple helices in nonaqueous solvents. Biophys. J. 72, 353-362.
8. Jaramillo, A., and Wodak, S. J. (2005) Computational protein design is a challenge for implicit solvation models. Biophys. J. 88, 156-171.
9. Pokala, N., and Handel, T. M. (2004) Energy functions for protein design I: efficient and accurate continuum electrostatics and solvation. Protein Sci. 13, 925-936.
10. Bretscher, L. E., Jenkins, C. L., Taylor, K. M., DeRider, M. L., and Raines, R. T. (2001) Conformational stability of collagen relies on a stereoelectronic effect. J. Am. Chem. Soc. 123, 111-778.
11. Holmgren, S. K., Taylor, K. M., Bretscher, L. E., and Raines, R. T. (1998) Code for collagen's stability deciphered. Nature 392, 666-667.
12. Baum., J., and Brodsky, B. (1997) Real-time NMR investigations of triple-helix, folding and collagen folding diseases. Folding Des. 2, R53R60.
13. Persikov, A. V., Xu, Y., and Brodsky, B. (2004) Equilibrium thermal transitions of collagen, model peptides. Protein Sci. 13, 893-902.
14. Salem, G., and Traub, W. (1975) Conformational implications of amino acid sequence regularities in collagen. FEBS Lett. 51, 94-99.
15. Traub, W., and Fietzek, P. P. (1976) Contribution of the A2 chain to the molecular stability of collagen. FEHS Lett. 68, 245-249.
16. Hulmes, D. J., Miller, A., Parry, D. A., Piez, K. A., and WoodheadGalloway, J. (1973) Analysis of the primary structure of collagen for the origins of molecular packing. J. Mol. Biol 79, 137-148.
17. Venugopal, M. G., Ramshaw, J. A., Braswell, E., Zhu, D., and Brodsky, B. (1994) Electrostatic interactions in collagen-like triplehelical peptides. Biocnhemistry 33, 7948-7956.
18. Yang, W., Chan, V. C., Kirkpatrick, A., Ramshaw, J. A., and Brodsky, B. (1997) Gly-Pro-Arg confers stability similar to GlyPro-Hyp in the collagen triple-helix of host-guest peptides. J. Biol. Chem. 272, 28837-28840.
19. Persikov, A. V., Ramshaw, J. A., Kirkpatrick, A., and Brodsky, B. (2005) Electrostatic interactions involving lysine make major contributions to collagen, triple-helix stability. Biochemistry 44, 1414-1422.
20. Ottl, J., Battistuta, R., Pieper, M., Tschesche, H., Bode, W., Kuhn, K., and Moroder, L. (.1996) Design and synthesis of heterotrimeric collagen peptides with a built-in cystine-knot. Models for collagen catabolism by matrix-metalloproteases. FEBS Lett. 398, 31-36.
21. Fiori, S., Sacca, B., and Moroder, L. (2002) Structural properties of a collagenous heterotrimer that mimics the collagenase cleavage site of collagen type I. J. Mol. Biol. 319, 1235-1242.
22. Gauba, V., and Hartgerink, J. D. (2007) Surprisingly high stability of collagen ABC heterotrimer: evaluation of side chain charge pairs, J. Am, Chem. Soc. 129, 15034-15041.
23. Gauba, V., and Hartgerink, J. D. (2007) Self-assembled, heterotrimeric collagen, triple helices directed through electrostatic interactions. J. Am. Chem. Soc.129, 2683-2690.
24. Gauba, V., and Hartgerink, J. D. (2008) Synthetic collagen heterotrimers: structural mimics of wild-type and mutant collagen type I. J. Am. Chem. Soc. 130, 7509-7515.
25. Nautiyal, S., Woolfson, D. N., King, D. S., and Alber, T. (1995) A. designed heterotrimeric coiled coil. Biochemistry 34, 11645-11651.
26. Kirkpatrick, S., Gelatt, C. D., and Vecchi, M. P. (1983) Optimization by simulated, annealing. Science 220, 671-680.
27. Hellinga, H. W., and Richards, F. M. (1994) Optimal sequence selection in proteins of known structure by simulated evolution. Proc. Natl. Acad. Sci. U.S.A. 91, 5803-5807.
28. Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H., and Teller, E. (1951) Equations of state calculations by fast computing machines. J. Chem. Phys. 21, 1087-1092.
29. Huang, C. Y. (1982) Determination, of binding stoichiometry by the continuous variation method: the Job plot. Methods Enjzymol. 87, 509-525.
30. Huang, S. S., Koder, R. L., Lewis, M., Wand, A. J., and Dutton, P. L. (2004) The HP-1 maquette: from an apoprotein structure to a structured hemoprotein designed to promote redox-coupled proton exchange. Proc. Natl. Acad. Sci. U.S.A. 101, 5536-5541.
31. Summa, C. M., Rosenblatt, M. M., Hong, J. K., Lear, J. D., and DeGrado, W. F. (2002) Computational de novo design, and characterization of an A(2)B(2) diiron protein. J. MoL Biol. 321, 923-938.
32. Sindelar, C. V., Hendsch, Z. S., and Tidor, B. (1998) Effects of salt bridges on protein structure and design. Protein Sci. 7, 1898-1914.
33. Berezovsky, I. N., Zeldovich, K. B., and Shakhnovich, E. I. (2007) Positive and negative design in stability and thermal adaptation of natural proteins. PLoS Comnut. Biol. 3, e52.
34. Morrissey, M. P., and Shakhnovich, E. I. (1996) Design of proteins with selected thermal properties. Folding Des. 1, 391-405.
35. Shakhnovich, E. I., and Gutin, A. M. (1993) A. new approach, to the design of stable proteins. Protien Eng. 6, 793-800.
36. Shakhnovich, E. I., and Gutin, A. M. (1993) Engineering of stable and fast-folding sequences of model proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 7195-7199.
37. Seno, F., Vendruscolo, M., Maritan, A., and Banavar, J. R. (1996) Optimal protein design procedure. Phys. Rev. Lett. 77, 1901-1904.
38. Persikov, A. V., Ramshaw, J. A. M., Kirkpatrick, A., and Brodsky, B. (2000) Amino acid propensities for the collagen triple-helix. Biochemistry 39, 14960-14967.
39. Koehl, P., and Levitt, M. (1999) De novo protein design. II. Plasticity in sequence space. J. Mol. Biol. 293, 1183-1193.
40. Bolon, D. N., Grant, R. A., Baker, T. A., and Sauer, R. T. (2005) Specificity versus stability in computational protein design. Proc. Natl. Acad. Sci. U.S.A. 102, 12724-12729.
41. Havranek, J. J., and Harbury, P. B. (2003) Automated design, of specificity in molecular recognition. Natl. Struct. Biol. 10, 45-52.
42. Grigoryan, G., Reinke, A. W., and Keating, A. E. (2009) Design of protein-interaction specificity gives selective bZIP-binding peptides. Nature 458, 859-864.
43. Chan, V. C., Ramshaw, J. A., Kirkpatrick, A., Beck, K., and Brodsky, B. (1997) Positional preferences of ionizable residues in GIy-X-Y triplets of the collagen triple-helix. J. Biol. Chem. 272, 31441-31446.
44. Hulmes, D. J., Miller, A., Parry, D. A., and Woodhead-Galloway, J. (1977) Fundamental periodicities in the amino acid sequence of the collagen alphal chain. Biochem. Biophys. Res. Commun. 77, 574-580.
45. Strickler, S. S., Gribenko, A. V., Keiffer, T. R., Tomlinson, J., Reihle, T., Loladze, V. V., and Makhatadze, G. I. (2006) Protein stability and surface electrostatics: a charged relationship. Biochemistry 45, 2761-2766.
46. Mechling, D. E., and Bachinger, H. P. (2000) The collagen-like peptide (GER) 15GPCCG forms pH-dependent covalently linked triple helical trimers. J. Biol. Chem. 275, 14532-14536.
47. Persikov, A. V., Ramshaw, J. A., and Brodsky, B. (2005) Prediction of collagen stability from amino acid sequence. J. Biol. Chem. 280, 19343-19349.
48. Knupp, C., and Squire, J. M. (2001) A new twist in the collagen story-the type VI segmented supercoil. EMBO J. 20, 372-376.
49. ReIe, S., Song, Y., Apkarian, R. P., Qu, Z., Conticello, V. P., and Chaikof, E. L. (2007) D-periodic collagen-mimetic microfibers. J. Am. Chem. Soc. 129, 14780-14787.
50. Pandya, M. J., Spooner, G. M., Sunde, M., Thorpe, J. R., Rodger, A., and Woolfson, D. N. (2000) Sticky-end assembly of a designed, peptide fiber provides insight into protein fibrillogenesis. Biochemistry 39, 8728-8734.