Kinetics and morphology of self-assembly of an elastin-like polypeptide based on the alternating domain arrangement of human tropoelastin.

Biochemistry

Volumn 49, Issue 27, 2010, Pages 5726-5733

  Cirulis, Judith T ^a   Keeley, Fred W ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTERIAL BLOOD; EFFECTS OF TEMPERATURE; ELASTIC MATRIX; ELASTIC RECOIL; ELASTIN-LIKE POLYPEPTIDES; EXTENDED NETWORKS; EXTRACELLULAR; EXTRACELLULAR MATRIX PROTEIN; HYDROPHOBIC DOMAINS; IN-VIVO; MONOMERIC FORMS; MULTISTEP PROCESS; NETWORK FORMATION; NETWORK STRUCTURES; SELF ASSEMBLY PROCESS; SOLUTION CONDITIONS; TEMPERATURE-INDUCED PHASE SEPARATION; TROPOELASTIN;

BLOOD VESSELS; GLYCOPROTEINS; POLYPEPTIDES; SELF ASSEMBLY; TEMPERATURE;

PHASE SEPARATION;

ELASTIN; ELASTIN LIKE POLYPEPTIDE EP20 24 24; POLYPEPTIDE; TROPOELASTIN; UNCLASSIFIED DRUG; PEPTIDE;

ARTICLE; COACERVATION; CONCENTRATION RESPONSE; HUMAN; KINETICS; MATHEMATICAL ANALYSIS; PARAMETER; PHASE SEPARATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROCESSING; TEMPERATURE SENSITIVITY; CHEMISTRY; EXTRACELLULAR MATRIX; GENE; GENETICS; HYDROPHOBICITY; MACROMOLECULE; METABOLISM; NUCLEOTIDE SEQUENCE; TEMPERATURE;

BASE SEQUENCE; ELASTIN; EXTRACELLULAR MATRIX; GENES; HUMANS; HYDROPHOBICITY; KINETICS; MACROMOLECULAR SUBSTANCES; PEPTIDES; TEMPERATURE; TROPOELASTIN;

EID: 77954730534     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100468v     Document Type: Article

References (56)

1. Trask, T. M., Trask, B. C., Ritty, T. M., Abrams, W. R., Rosenbloom, J., and Mecham, R. P. (2000) Interaction of tropoelastin with the amino-terminal domains of fibrillin-1 and fibrillin-2 suggests a role for the fibrillins in elastic fiber assembly. J. Biol. Chem. 275, 24400-24406.
2. Jensen, S. A., Reinhardt,D. P., Gibson, M. A., and Weiss, A. S. (2001) Protein interaction studies ofMAGP-1 with tropoelastin and fibrillin-1. J. Biol. Chem. 276, 39661-139616
3. Nakamura, T., Lozano, P. R., Ikeda, Y., Iwanaga, Y., Hinek, A., Minamisawa, S., Cheng, C. F., Kobuke, K., Dalton, N., Takada, Y., Tashiro, K., Ross, J., Jr., Honjo, T., and Chien, K. R. (2002) Fibulin- 5/DANCE is essential for elastogenesis in vivo. Nature 415, 171-175.
4. Reinboth, B., Hanssen, E., Cleary, E. G., and Gibson, M. A. (2002) Molecular interactions of biglycan and decorin with elastic fiber components: Biglycan forms a ternary complex with tropoelastin and microfibril-associated glycoprotein 1. J. Biol. Chem. 277, 3950-3957.
5. Yanagisawa, H., Davis, E. C., Starcher, B. C., Ouchi, T., Yanagisawa, M., Richardson, J. A., and Olson, E. N. (2002) Fibulin-5 is an elastinbinding protein essential for elastic fiber development in vivo. Nature 415, 168-171.
6. Clarke, A. W., Wise, S. G., Cain, S. A., Kielty, C. M., and Weiss, A. S. (2005) Coacervation is promoted by molecular interactions between the PF2 segment of fibrillin-1 and the domain 4 region of tropoelastin. Biochemistry 44, 10271-10281.
7. Hirai, M., Ohbayashi, T., Horiguchi, M., Okawa, K., Hagiwara, A., Chien, K. R., Kita, T., and Nakamura, T. (2007) Fibulin-5/DANCE has an elastogenic organizer activity that is abrogated by proteolytic cleavage in vivo. J. Cell Biol. 176, 1061-1071.
8. Zheng, Q., Davis, E. C., Richardson, J. A., Starcher, B. C., Li, T., Gerard, R. D., and Yanagisawa, H. (2007) Molecular analysis of fibulin-5 function during de novo synthesis of elastic fibers. Mol. Cell. Biol. 27, 1083-1095.
9. Lemaire, R., Bayle, J., Mecham, R. P., and Lafyatis, R. (2007) Microfibril-associated MAGP-2 stimulates elastic fiber assembly. J. Biol. Chem. 282, 800-808.
10. Brown-Augsburger, P., Broekelmann, T., Rosenbloom, J., and Mecham, R. P. (1996) Functional domains on elastin and microfibrilassociated glycoprotein involved in elastic fiber assembly. Biochem. J. 318, 149-155.
11. Trask, B. C., Trask, T. M., Broekelmann, T., and Mecham, R. P. (2000) The microfibrillar proteins MAGP-1 and fibrillin-1 form a ternary complex with the chondroitin sulfate proteoglycan decorin. Mol. Biol. Cell 11, 1499-1507.
12. Wachi, H., Nonaka, R., Sato, F., Shibata-Sato, K., Ishida, M., Iketani, S., Maeda, I., Okamoto, K., Urban, Z., Onoue, S., and Seyama, Y. (2008) Characterization of the molecular interaction between tropoelastin and DANCE/fibulin-5. J. Biochem. 143, 633-639.
13. Cox, B. A., Starcher, B. C., and Urry, D. W. (1974) Coacervation of tropoelastin results in fiber formation. J. Biol. Chem. 249, 997-998.
14. Bressan, G. M., Castellani, I., Giro, M. G., Volpin, D., Fornieri, C., and Pasquali Ronchetti, I. (1983) Banded fibers in tropoelastin coacervates at physiological temperatures. J. Ultrastruct. Res. 82, 335-340.
15. Bressan, G. M., Pasquali-Ronchetti, I., Fornieri, C., Mattioli, F., Castellani, I., and Volpin, D. (1986) Relevance of aggregation properties of tropoelastin to the assembly and structure of elastic fibers. J. Ultrastruct. Mol. Struct. Res. 94, 209-216.
16. Bedell-Hogan, D., Trackman, P., Abrams, W., Rosenbloom, J., and Kagan, H. (1993) Oxidation, cross-linking, and insolubilization of recombinant tropoelastin by purified lysyl oxidase. J. Biol. Chem. 268, 10345-10350.
17. Mithieux, S. M., Rasko, J. E., and Weiss, A. S. (2004) Synthetic elastin hydrogels derived from massive elastic assemblies of self-organized human protein monomers. Biomaterials 25, 4921-4927.
18. Kozel, B. A., Rongish, B. J., Czirok, A., Zach, J., Little, C. D., Davis, E. C., Knutsen, R. H., Wagenseil, J. E., Levy, M. A., and Mecham, R. P. (2006) Elastic fiber formation: A dynamic view of extracellular matrix assembly using timer reporters. J. Cell. Physiol. 207, 87-96.
19. Czirok, A., Zach, J., Kozel, B. A., Mecham, R. P., Davis, E. C., and Rongish, B. J. (2006) Elastic fiber macro-assembly is a hierarchical, cell motion-mediated process. J. Cell. Physiol. 207, 97-106.
20. Bellingham, C. M., Woodhouse, K. A., Robson, P., Rothstein, S. J., and Keeley, F. W. (2001) Self-aggregation characteristics of recombinantly expressed human elastin polypeptides. Biochim. Biophys. Acta 1550, 6-19.
21. Bellingham, C. M., Lillie, M. A., Gosline, J. M., Wright, G. M., Starcher, B. C., Bailey, A. J., Woodhouse, K. A., and Keeley, F. W. (2003) Recombinant human elastin polypeptides self-assemble into biomaterials with elastin-like properties. Biopolymers 70, 445-455.
22. Luan, C. H., Parker, T. M., Prasad, K. U., and Urry, D. W. (1991) Differential scanning calorimetry studies of NaCl effect on the inverse temperature transition of some elastin-based polytetra-, polypenta-, and polynonapeptides. Biopolymers 31, 465-475.
23. Vrhovski, B., Jensen, S., and Weiss, A. S. (1997) Coacervation characteristics of recombinant human tropoelastin. Eur. J. Biochem. 250, 92-98.
24. Miao, M., Bellingham, C. M., Stahl, R. J., Sitarz, E. E., Lane, C. J., and Keeley, F. W. (2003) Sequence and structure determinants for the self-aggregation of recombinant polypeptides modeled after human elastin. J. Biol. Chem. 278, 48553-48562.
25. Miao, M., Cirulis, J. T., Lee, S., and Keeley, F. W. (2005) Structural determinants of cross-linking and hydrophobic domains for selfassembly of elastin-like polypeptides. Biochemistry 44, 14367-14375.
26. Reguera, J., Urry, D. W., Parker, T. M., McPherson, D. T., and Rodriguez-Cabello, J. C. (2007) Effect of NaCl on the exothermic and endothermic components of the inverse temperature transition of a model elastin-like polymer. Biomacromolecules 8, 354-358.
27. Cox, B. A., Starcher, B. C., and Urry, D. W. (1973) Coacervation of alpha-elastin results in fiber formation. Biochim. Biophys. Acta 317, 209-213.
28. Urry, D. W., and Long, M. M. (1977) On the conformation, coacervation and function of polymeric models of elastin. Adv. Exp. Med. Biol. 79, 685-714.
29. Clarke, A. W., Arnspang, E. C., Mithieux, S. M., Korkmaz, E., Braet, F., and Weiss, A. S. (2006) Tropoelastin massively associates during coacervation to form quantized protein spheres. Biochemistry 45, 9989-9996.
30. Cirulis, J. T., and Keeley, F. W. (2009) Viscoelastic properties and gelation of an elastin-like polypeptide. J. Rheol. 53, 1215-1228.
31. Tu, Y., Wise, S. G., and Weiss, A. S. (2010) Stages in tropoelastin coalescence during synthetic elastin hydrogel formation. Micron 41, 268-272.
32. Cirulis, J. T., Bellingham, C. M., Davis, E. C., Hubmacher, D., Reinhardt,D. P., Mecham, R. P., and Keeley, F. W. (2008) Fibrillins, fibulins, and matrix-associated glycoprotein modulate the kinetics and morphology of in vitro self-assembly of a recombinant elastin-like polypeptide. Biochemistry 47, 12601-12613.
33. Pepe, A., Guerra, D., Bochicchio, B., Quaglino, D., Gheduzzi, D., Pasquali Ronchetti, I., and Tamburro, A. M. (2005) Dissection of human tropoelastin: Supramolecular organization of polypeptide sequences coded by particular exons. Matrix Biol. 24, 96-109.
34. Muiznieks, L. D., Jensen, S. A., and Weiss, A. S. (2003) Structural changes and facilitated association of tropoelastin. Arch. Biochem. Biophys. 410, 317-323.
35. Scalley,M. L., and Baker, D. (1997) Protein folding kinetics exhibit an Arrhenius temperature dependence when corrected for the temperature dependence of protein stability. Proc. Natl. Acad. Sci. U.S.A. 94, 10636-10640.
36. Schreiner, E., Nicolini, C., Ludolph, B., Ravindra, R., Otte, N., Kohlmeyer, A., Rousseau, R., Winter, R., and Marx, D. (2004) Folding and unfolding of an elastin-like oligopeptide: "inverse temperature transition," reentrance, and hydrogen-bond dynamics. Phys. Rev. Lett. 92, 1481011-1481014
37. Reguera, J., Lagaron, J. M., Alonso, M., Reboto, V., Calvo, B., and Rodriguez-Cabello, J. C. (2003) Thermal behavior and kinetic analysis of the chain unfolding and refolding and of the concomitant nonpolar solvation and desolvation of two elastin-like polymers. Macromolecules 36, 8470-8476.
38. Ribeiro, A., Arias, F. J., Reguera, J., Alonso, M., and Rodriguez- Cabello, J. C. (2009) Influence of the amino-acid sequence on the inverse temperature transition of elastin-like polymers. Biophys. J. 97, 312-320.
39. Zhang, Y., Mao, H., and Cremer, P. S. (2003) Probing the mechanism of aqueous two-phase system formation for alpha-elastin on-chip. J. Am. Chem. Soc. 125, 15630-15635.
40. Zhang, Y., Trabbic-Carlson, K., Albertorio, F., Chilkoti, A., and Cremer, P. S. (2006) Aqueous two-phase system formation kinetics for elastin-like polypeptides of varying chain length. Biomacromolecules 7, 2192-2199.
41. Vitale, S. A., and Katz, J. L. (2003) Liquid droplet dispersions formed by homogeneous liquid-liquid nucleation: "the ouzo effect. Langmuir 19, 4105-4110.
42. Nichols, M. R., Moss, M. A., Reed, D. K., Hoh, J. H., and Rosenberry, T. L. (2005) Rapid assembly of amyloid-β peptide at a liquid/liquid interface produces unstable β-sheet fibers. Biochemistry 44, 165-173.
43. Dreher, M. R., Simnick, A. J., Fischer, K., Smith, R. J., Patel, A., Schmidt, M., and Chilkoti, A. (2008) Temperature triggered selfassembly of polypeptides into multivalent spherical micelles. J. Am. Chem. Soc. 130, 687-694.
44. Yamaoka, T., Tamura, T., Seto, Y., Tada, T., Kunugi, S., and Tirrell, D. A. (2003) Mechanism for the phase transition of a genetically engineered elastin model peptide (VPGIG)40 in aqueous solution. Biomacromolecules 4, 1680-1685.
45. Kurková, D., Kríz, J., Schmidt, P., Dybal, J., Rodríguez-Cabello, J. C., and Alonso, M. (2003) Structure and dynamics of two elastinlike polypentapeptides studied by NMR spectroscopy. Biomacromolecules 4, 589-601.
46. Li, B., and Daggett, V. (2003) The molecular basis of the temperatureand pH-induced conformational transitions in elastin-based peptides. Biopolymers 68, 121-129.
47. Tamburro, A. M., Bochicchio, B., and Pepe, A. (2003) Dissection of human tropoelastin: Exon-by-exon chemical synthesis and related conformational studies. Biochemistry 42, 13347-13362.
48. Bochicchio, B., Floquet, N., Pepe, A., Alix, A. J., and Tamburro, A. M. (2004) Dissection of human tropoelastin: Solution structure, dynamics, and self-assembly of the exon 5 peptide. Chemistry 10, 3166-3176.
49. Rousseau, R., Schreiner, E., Kohlmeyer, A., and Marx, D. (2004) Temperature-dependent conformational transitions and hydrogenbond dynamics of the elastin-like octapeptide GVG(VPGVG): A molecular-dynamics study. Biophys. J. 86, 1393-1407.
50. Pepe, A., Guerra, D., Bochicchio, B., Quaglino, D., Gheduzzi, D., Pasquali Ronchetti, I., and Tamburro, A. M. (2005) Dissection of human tropoelastin: Supramolecular organization of polypeptide sequences coded by particular exons. Matrix Biol. 24, 96-109.
51. Rauscher, S., Baud, S., Miao, M., Keeley, F. W., and Pomès, R. (2006) Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. Structure 14, 1667-1676.
52. Krukau, A., Brovchenko, I., and Geiger, A. (2007) Temperatureinduced conformational transition of a model elastin-like peptide GVG(VPGVG)(3) in water. Biomacromolecules 8, 2196-2202.
53. Sönnichsen, F. D., Van Eyk, J. E., Hodges, R. S., and Sykes, B. D. (1992) Effect of trifluoroethanol on protein secondary structure: An NMR and CD study using a synthetic actin peptide. Biochemistry 31, 8790-8798.
54. Buck,M. (1998)Trifluoroethanol and colleagues: Cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 31, 297-355.
55. Kentsis, A., and Sosnick, T. R. (1998) Trifluoroethanol promotes helix formation by destabilizing backbone exposure: Desolvation rather than native hydrogen bonding defines the kinetic pathway of dimeric coiled coil folding. Biochemistry 37, 14613-14622.
56. Reiersen, H., and Rees, A. R. (2000) Trifluoroethanol may form a solvent matrix for assisted hydrophobic interactions between peptide side chains. Protein Eng. 13, 739-743.