Folding studies of pH-dependent collagen peptides

Chemical Biology and Drug Design

Volumn 75, Issue 2, 2010, Pages 161-168

  Lee, Jeeyeon ^a   Chmielewski, Jean ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Collagen; Folding; Nucleation; Peptide; PH dependent

Indexed keywords

CARBOXYL GROUP; COLLAGEN; GLYCINE; HYDROXYPROLINE; PROLINE; SYNTHETIC PEPTIDE;

ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; PEPTIDE SYNTHESIS; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; COLLAGEN; HYDROGEN-ION CONCENTRATION; HYDROXYPROLINE; KINETICS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

EID: 74549189458     PISSN: 17470277     EISSN: 17470285     Source Type: Journal    
DOI: 10.1111/j.1747-0285.2009.00929.x     Document Type: Article

References (55)

1. Lee S.G., Lee J.Y., Chmielewski J. (2008) Investigation of pH-dependent collagen triple-helix formation. Angew Chem 47 : 8429 8432.
2. Kielty C.M., Hopkins I., Grant M.E. (1993) Connective tissue and its heritable disorders: molecular, genetic, and medical aspects. In : Royce P.M., Steinmann B., editor. Wiley Liss Inc., New York, USA, p. 159 221.
3. Prockop D.J., Kivirikko K.I. (1995) Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64 : 403 434.
4. Ramachandran G.N., Ambady G.K. (1954) Elements of the helical structure of collagen. Curr Sci 23 : 349 350.
5. Rich A., Crick F.H. (1961) The molecular structure of collagen. J Mol Biol 3 : 483 506.
6. Bella J., Eaton M., Brodsky B., Berman H.M. (1994) Crystal and molecular structure of a collagen-like peptide at 1.9 A resolution. Science 266 : 75 81.
7. Kobayashi Y., Sakai R., Kakiuchi K. (1970) Stabilization mechanism of triple helical structure of collagen molecules. Biopolymers 10 : 415 425.
8. Berg R.A., Prockop D.J. (1973) The thermal transition of a nonhydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple helix of collagen. Biochem Biophys Res Commun 52 : 115 120.
9. n of defined molecular weights. Evidence for the stabilization of collagen triple helix by hydroxyproline. Biochim Biophys Acta 3 : 198 202.
10. Shoulders M.D., Raines R.T. (2009) Collagen structure and stability. Annu Rev Biochem 78 : 929 958.
11. McLaughlin S.H., Bulleid N.J. (1998) Molecular recognition in procollagen chain assembly. Matrix Biol 16 : 369 377.
12. Lamande S.R., Bateman J.F. (1999) Procollagen folding and assembly: the role of endoplasmic reticulum enzymes and molecular chaperones. Semin Cell Dev Biol 10 : 455 464.
13. Byers P.H., Click E.M., Harper E., Bornstein P. (1975) Interchain disulfide bonds in procollagen are located in a large nonotriple-helical COOH-terminal domain. Proc Natl Acad Sci USA 72 : 3009 3013.
14. Lees J.F., Tasab M., Bulleid N.J. (1997) Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J 16 : 908 916.
15. Bulleid N.J., Dalley J.A., Lees J.F. (1997) The C-propeptide domain of procollagen can be replaced with a transmembrane domain without affecting trimer formation or collagen triple helix folding during biosynthesis. EMBO J 16 : 6694 6701.
16. Lukens L. (1976) Time of occurrence of disulfide linking between prollagen chains. J Biol Chem 251 : 3530 3538.
17. Engel J. (1991) The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu Rev Biophys Biophys Chem 20 : 137 152.
18. Bächinger H.P., Bruckner P., Timpl R., Prockop D.J., Engel J. (1980) Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen. Role of disulfide bridges and peptide bond isomerization. Eur J Biochem 106 : 619 632.
19. Dölz R., Engel J., Kühn K. (1988) Folding of collagen IV. Eur J Biochem 178 : 357 366.
20. Snellman A., Tu H., Vaisanen T., Kvist A.P., Huhtala P., Pihlajaniemi T. (2000) A short sequence in the N-terminal region is required for the trimerization of type XIII collagen and is conserved in other collagenous transmembrane proteins. EMBO J 19 : 5051 5059.
21. Areida S.K., Reinhardt D.P., Müller P.K., Fietzek P.P., Köwitz J., Marinkovich M.P., Notbohm H. (2001) Properties of the collagen type XVII ectodomain. Evidence for N- to C-terminal triple helix folding. J Biol Chem 276 : 1594 1601.
22. Lesage A., Penin F., Geourjon C., Marion D., van der Rest M. (1996) Trimeric assembly and three-dimensional structure model of the FACIT collagen COL1-NC1 junction from CD and NMR analysis. Biochemistry 35 : 9647 9660.
23. Mazzorana M., Cogne S., Goldschmidt D., Aubert-Foucher E. (2001) Collagenous sequence governs the trimeric assembly of collagen XII. J Biol Chem 276 : 27989 27998.
24. Mechling D.E., Gambee J.E., Morris N.P., Sakai L.Y., Keene D.R., Mayne R., Bächinger H.P. (1996) Type IX collagen NC1 domain peptides can trimerize in vitro without forming a triple helix. J Biol Chem 271 : 13781 13785.
25. Zhang Y., Chen Q. (1999) The noncollagenous domain 1 of type X collagen. A novel motif for trimer and higher order multimer formation without a triple helix. J Biol Chem 274 : 22409 22413.
26. Södar S., Pöschl E. (2004) The NC1 domain of human collagen IV is necessary to initiate triple helix formation. Biochem Biophys Res Comm 325 : 276 280.
27. Persikov A.V., Xu Y., Brodsky B. (2004) Equilibrium thermal transitions of collagen model peptides. Protein Sci 13 : 893 902.
28. Bächinger H.P., Engel J. (2001) Thermodynamic vs. kinetic stability of collagen triple helices. Matrix Biol 20 : 267 269.
29. Leikina E., Mertts M.V., Kuznetsova N., Leikin S. (2002) Type I collagen is thermally unstable at body temperature. Proc Natl Acad Sci USA 99 : 1314 1318.
30. Miles C.A. (1993) Kinetics of collagen denaturation in mammalian lens capsules studied by differential scanning calorimetry. Int J Biol Macromol 15 : 265 271.
31. Miles C.A., Burjanadze T.V., Bailey A.J. (1995) The kinetics of the thermal denaturation of collagen in unrestrained rat tail tendon determined by differential scanning calorimetry. J Mol Biol 245 : 437 446.
32. Frank S., Boudko S., Mizuno K., Schulthess T., Engel J., Bächinger H.P. (2003) Collagen triple helix formation can be nucleated at either end. J Biol Chem 278 : 7747 7750.
33. Ottl J., Moroder L. (1999) Disulfide-bridged heterotrimeric collagen peptides containing the collagenase cleavage site of collagen type I. Synthesis and conformational properties. J Am Chem Soc 121 : 653 661.
34. McAlinden A., Smith T.A., Sandell L.J., Ficheux D., Parry D.A., Hulmes D.J. (2003) Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily. J Biol Chem 278 : 42200 42207.
35. Boudko S.P., Frank S., Kammerer R.A., Stetefeld J., Schulthess T., Landwehr R., Lustig A., Bächinger H.P., Engel J. (2002) Nucleation and propagation of the collagen triple helix in single-chain and trimerized peptides: transition from third to first order kinetics. J Mol Biol 317 : 459 470.
36. Goodman M., Feng Y., Melacini G., Taulane J.P. (1996) A template-induced incipient collagen-like triple-helical structure. J Am Chem Soc 118 : 5156 5157.
37. Buevich A.V., Dai Q.-H., Liu X., Brodsky B., Baum J. (2000) Site-specific NMR monitoring of cis-trans isomerization in the folding of the proline-rich collagen triple helix. Biochemistry 39 : 4299 4308.
38. Hyde T.J., Bryan M.A., Brodsky B., Baum J. (2006) Sequence dependence of renucleation after a Gly mutation in model collagen peptides. J Biol Chem 281 : 36937 36943.
39. Liu X., Siegel D.L., Fan P., Brodsky B., Baum J. (1996) Direct NMR measurement of the folding kinetics of a trimeric peptide. Biochemistry 35 : 4306 4313.
40. Buevich A.V., Silva T., Brodsky B., Baum J. (2004) Transformation of the mechanism of triple-helix peptide folding in the absence of a C-terminal nucleation domain and its implications for mutations in collagen disorders. J Biol Chem 279 : 46890 46895.
41. Xu Y., Bhate M., Brodsky B. (2002) Characterization of the nucleation step and folding of a collagen triple-helix peptide. Biochemistry 41 : 8143 8151.
42. Bansal M., Ananthanarayanan V.S. (1988) The role of hydroxyproline in collagen folding: conformational energy calculations on oligopeptides containing proline and hydroxyproline. Biopolymers 27 : 299 312.
43. Bulleid N.J., Wilson R., Lees J.F. (1996) Type-III procollagen assembly in semi-intact cells: chain association, nucleation and triple helix folding do not require formation of inter-chain disulphide bonds but triple -helix nucleation does require hydroxylation. Biochem J 317 : 195 202.
44. Ackerman M.S., Bhate M., Shenoy N., Beck K., Ramshaw J.A., Brodsky B. (1999) Sequence dependence of the folding of collagen-like peptides. Single amino acids affect the rate of triple-helix nucleation. J Biol Chem 274 : 7668 7673.
45. Bächinger H.P., Engel J. (2005) Thermodynamics and kinetics of collagen folding. In : Buchner J., Kiefhaber T., editor. Handbook of Protein Folding. Wiley-VCH, Weinheim, Germany, p. 1059 1110.
46. Xu Y., Hyde T., Wang X., Bhate M., Brodsky B., Baum J. (2003) NMR and CD spectroscopy show that imino acid restriction of the unfolded state leads to efficient folding. Biochemistry 42 : 8696 8703.
47. Chopra R.K., Ananthanarayanan V.S. (1982) Conformational implications of enzymatic proline hydroxylation in collagen. Proc Natl Acad Sci USA 79 : 7180 7184.
48. Persikov A.V., Ramshaw J.A.M., Broadsky B. (2000) Collagen model peptides: sequence dependence of triple-helix stability. Biopolymers 55 : 436 450.
49. Yang W., Chan V.C., Kirkpatrick A., Ramshaw J.A., Brodsky B. (1997) Gly-Pro-Arg confers stability similar to Gly-Pro-Hyp in the collagen triple-helix of host-guest peptides. J Biol Chem 272 : 28837 28840.
50. Babu R., Ganesh K.N. (2001) Enhanced triple helix stability of collagen peptides with 4R-Aminoprolyl (AMP) residues. Relative roles of electrostatic and hydrogen bonding effects. J Am Chem Soc 123 : 2079 2080.
51. Bansal M. (1977) Stereochemical restrictions on the occurrence of amino acid residues in the collagen structure. Int J Pept Protein Res 9 : 224 234.
52. Chan V.C., Ramshaw J.A., Kirkpatrick A., Beck K., Brodsky B. (1997) Positional preferences of ionizable residues in Gly-X-Y triplets of the collagen triple-helix. J Biol Chem 272 : 31441 31446.
53. Shah N.K., Ramshaw J.A., Kirkpatrick A., Shah C., Brodsky B. (1996) A host-guest set of triple-helical peptides: stability of Gly-X-Y triplets containing common nonpolar residues. Biochemistry 35 : 10262 10268.
54. Kotch F.W., Guzei I.A., Raines R.T. (2008) Stabilization of the collagen triple helix by O-Methylation of hydroxyproline residues. J Am Chem Soc 130 : 2952 2953.
55. Persikov A.V., Ramshaw J.A., Brodsky B. (2005) Prediction of collagen stability from amino acid sequence. J Biol Chem 280 : 19343 19349.