Thermostability gradient in the collagen triple helix reveals its multi-domain structure

Journal of Molecular Biology

Volumn 338, Issue 5, 2004, Pages 989-998

  Steplewski, Andrzej ^a   Majsterek, Ireneusz ^a   McAdams, Erin ^a   Rucker, Eileen ^a   Brittingham, Raymond J ^a   Ito, Hidetoshi ^a   Hirai, Kazuya ^b   Adachi, Eijiro ^b   Jimenez, Sergio A ^a   Fertala, Andrzej ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b KITASATO UNIVERSITY   (Japan)

Author keywords

CD, circular dichroism spectroscopy; Collagen mutations; Extracellular matrix; Hsp47, heat shock protein 47; Protein engineering; Recombinant collagen; Thermostability

Indexed keywords

ARGININE; CARBON; COLLAGEN TYPE 2; CYSTEINE; MUTANT PROTEIN; NITROGEN;

ARTICLE; CONFORMATION; GENETIC ENGINEERING; MELTING POINT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN STRUCTURE; TANDEM REPEAT; TEMPERATURE; THERMOSTABILITY;

EID: 11144357161     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.03.037     Document Type: Article

References (43)

1. Rich A., Crick F.H. The molecular structure of collagen. J. Mol. Biol. 3:1961;483-506.
2. Fraser R.D., MacRae T.P., Suzuki E. Chain conformation in the collagen molecule. J. Mol. Biol. 129:1979;463-481.
3. Privalov P.L. Stability of proteins. Proteins which do not present a single cooperative system. Advan. Protein Chem. 35:1982;1-104.
4. Di Lullo G.A., Sweeney S.M., Korkko J., Ala-Kokko L., San Antonio J.D. Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J. Biol. Chem. 277:2002;4223-4231.
5. Prockop D.J., Fertala A. Inhibition of the self-assembly of collagen I into fibrils with synthetic peptides. Demonstration that assembly is driven by specific binding sites on the monomers. J. Biol. Chem. 273:1998;15598-15604.
6. Prockop D.J., Berg R.A., Kivirikko K.I., Uitto J. Intracellular steps in the biosynthesis of collagen. Ramachandran G.N., Reddi A.H. Biochemistry of Collagen. 1976;163-237 Plenum, New York.
7. Rosenbloom J., Harsch M., Jimenez S. Hydroxyproline content determines the denaturation temperature of chick tendon collagen. Arch. Biochem. Biophys. 158:1973;478-484.
8. Berg R.A., Prockop D.J. The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen. Biochem. Biophys. Res. Commun. 52:1973;115-120.
9. Jimenez S., Harsch M., Rosenbloom J. Hydroxyproline stabilizes the triple helix of chick tendon collagen. Biochem. Biophys. Res. Commun. 52:1973;106-114.
10. Prockop D.J., Kivirikko K.I. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64:1995;403-434.
11. Olsen B.R. Mutations in collagen genes resulting in metaphyseal and epiphyseal dysplasias. Bone. 17:1995;45S-49S.
12. Kuivaniemi H., Tromp G., Prockop D.J. Mutations in collagen genes: causes of rare and some common diseases in humans. FASEB J. 5:1991;2052-2060.
13. Beck K., Chan V.C., Shenoy N., Kirkpatrick A., Ramshaw J.A., Brodsky B. Destabilization of osteogenesis imperfecta collagen-like model peptides correlates with the identity of the residue replacing glycine. Proc. Natl Acad. Sci. USA. 97:2000;4273-4278.
14. Fertala A., Westerhausen A., Morris G., Rooney J.E., Prockop D.J. Two cysteine substitutions in procollagen I: a glycine replacement near the N-terminus of alpha 1(I) chain causes lethal osteogenesis imperfecta and a glycine replacement in the alpha 2(I) chain markedly destabilizes the triple helix. Biochem. J. 289:1993;195-199.
15. Byers P.H., Cole W.G. Osteogenesis imperfecta. Royce P.M., Steinmann B. Connective Tissue and Its Heritable Disorders: Molecular, Genetic, and Medical Aspects. 2nd edit. 2002;385-430 Wiley-Liss, New York.
16. Persikov A.V., Ramshaw J.A., Kirkpatrick A., Brodsky B. Amino acid propensities for the collagen triple-helix. Biochemistry. 39:2000;14960-14967.
17. Arnold W.V., Fertala A., Sieron A.L., Hattori H., Mechling D., Bachinger H.P., Prockop D.J. Recombinant procollagen II: deletion of D period segments identifies sequences that are required for helix stabilization and generates a temperature-sensitive N-proteinase cleavage site. J. Biol. Chem. 273:1998;31822-31828.
18. Arnold W.V., Sieron A.L., Fertala A., Bachinger H.P., Mechling D., Prockop D.J. A cDNA cassette system for the synthesis of recombinant procollagens. Variants of procollagen II lacking a D-period are secreted as triple-helical monomers. Matrix Biol. 16:1997;105-116.
19. Majsterek I., McAdams E., Adachi E., Dhume S.T., Fertala A. Prospects and limitations of the rational engineering of fibrillar collagens. Protein Sci. 12:2003;2063-2072.
20. Frank S., Kammerer R.A., Mechling D., Schulthess T., Landwehr R., Bann J., et al. Stabilization of short collagen-like triple helices by protein engineering. J. Mol. Biol. 308:2001;1081-1089.
21. Bulleid N.J., Dalley J.A., Lees J.F. 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. 16:1997;6694-6701.
22. Lees J.F., Tasab M., Bulleid N.J. Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J. 16:1997;908-916.
23. McLaughlin S.H., Bulleid N.J. Molecular recognition in procollagen chain assembly. Matrix Biol. 16:1998;369-377.
24. Williams C.J., Considine E.L., Knowlton R.G., Reginato A., Neumann G., Harrison D., et al. Spondyloepiphyseal dysplasia and precocious osteoarthritis in a family with an Arg75→Cys mutation in the procollagen type II gene (COL2A1). Hum. Genet. 92:1993;499-505.
25. Chan D., Taylor T.K., Cole W.G. Characterization of an arginine 789 to cysteine substitution in alpha 1 (II) collagen chains of a patient with spondyloepiphyseal dysplasia. J. Biol. Chem. 268:1993;15238-15245.
26. Tanzawa K., Berger J., Prockop D.J. Type I procollagen N-proteinase from whole chick embryos. Cleavage of a homotrimer of pro-alpha 1(I) chains and the requirement for procollagen with a triple-helical conformation. J. Biol. Chem. 260:1985;1120-1126.
27. Berger J., Tanzawa K., Prockop D.J. Sequential cleavage of type I procollagen by procollagen N-proteinase. An intermediate containing an uncleaved pro alpha 1(I) chain. Biochemistry. 24:1985;600-605.
28. Tuderman L., Kivirikko K.I., Prockop D.J. Partial purification and characterization of a neutral protease which cleaves the N-terminal propeptides from procollagen. Biochemistry. 17:1978;2948-2954.
29. Lightfoot S.J., Holmes D.F., Brass A., Grant M.E., Byers P.H., Kadler K.E. Type I procollagens containing substitutions of aspartate, arginine, and cysteine for glycine in the pro alpha 1 (I) chain are cleaved slowly by N-proteinase, but only the cysteine substitution introduces a kink in the molecule. J. Biol. Chem. 267:1992;25521-25528.
30. Vogel B.E., Doelz R., Kadler K.E., Hojima Y., Engel J., Prockop D.J. A substitution of cysteine for glycine 748 of the alpha 1 chain produces a kink at this site in the procollagen I molecule and an altered N-proteinase cleavage site over 225 nm away. J. Biol. Chem. 263:1988;19249-19255.
31. Rossi A., Zanaboni G., Cetta G., Tenni R. Stability of type I collagen CNBr peptide trimers. J. Mol. Biol. 269:1997;488-493.
32. Zafarullah K., Sieron A.L., Fertala A., Tromp G., Kuivaniemi H., Prockop D.J. A recombinant homotrimer of type I procollagen that lacks the central two D-periods. The thermal stability of the triple helix is decreased by 2 to 4 degrees C. Matrix Biol. 16:1997;245-253.
33. Sieron A.L., Fertala A., Ala-Kokko L., Prockop D.J. Deletion of a large domain in recombinant human procollagen II does not alter the thermal stability of the triple helix. J. Biol. Chem. 268:1993;21232-21237.
34. Royce P.M., Steinmann B. Connective Tissue and Its Heritable Disorders: Molecular, Genetic, and Medical Aspects. 2nd edit. 2002;Wiley-Liss, New York.
35. Fertala A., Ala-Kokko L., Wiaderkiewicz R., Prockop D.J. Collagen II containing a Cys substitution for arg-alpha1-519. Homotrimeric monomers containing the mutation do not assemble into fibrils but alter the self-assembly of the normal protein. J. Biol. Chem. 272:1997;6457-6464.
36. Thomson C.A., Tenni R., Ananthanarayanan V.S. Mapping Hsp47 binding site(s) using CNBr peptides derived from type I and type II collagen. Protein Sci. 12:2003;1792-1800.
37. Tasab M., Batten M.R., Bulleid N.J. Hsp47: a molecular chaperone that interacts with and stabilizes correctly-folded procollagen. EMBO J. 19:2000;2204-2211.
38. Baldwin C.T., Reginato A.M., Smith C., Jimenez S.A., Prockop D.J. Structure of cDNA clones coding for human type II procollagen. The alpha 1(II) chain is more similar to the alpha 1(I) chain than two other alpha chains of fibrillar collagens. Biochem. J. 262:1989;521-528.
39. Fertala A., Sieron A.L., Ganguly A., Li S.W., Ala-Kokko L., Anumula K.R., Prockop D.J. Synthesis of recombinant human procollagen II in a stably transfected tumour cell line (HT1080). Biochem. J. 298:1994;31-37.
40. Davis J.M., Bächinger H.P. Hysteresis in the triple helix-coil transition of type III collagen. J. Biol. Chem. 268:1993;25965-25972.
41. Bruckner P., Bachinger H.P., Timpl R., Engel J. Three conformationally distinct domains in the amino-terminal segment of type III procollagen and its rapid triple helix leads to and comes from coil transition. Eur. J. Biochem. 90:1978;595-603.
42. Tyler J.M., Branton D. Rotary shadowing of extended molecules dried from glycerol. J. Ultrastruct. Res. 71:1980;95-102.
43. Hojima Y., McKenzie J.A., van der Rest M., Prockop D.J. Type I procollagen N-proteinase from chick embryo tendons. Purification of a new 500-kDa form of the enzyme and identification of the catalytically active polypeptides. J. Biol. Chem. 264:1989;11336-11345.