A thermodynamic analysis of the contribution of hydroxyproline to the structural stability of the collagen triple helix

Connective Tissue Research

Volumn 36, Issue 4, 1997, Pages 347-365

  Burjanadze, Thengiz V ^a   Veis, Arthur ^b  

^a INSTITUTE OF PHYSICS   (Georgia)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA;

EID: 0031421465     PISSN: 03008207     EISSN: None     Source Type: Journal    
DOI: 10.3109/03008209709160233     Document Type: Short Survey

References (92)

1. Takahashi, T. and Tanaka, T. (1953). Physico-chemical studies on the skin and leathers of marine animals. VIII. On the heat stability of fish skin in leather, Bull. Jup. Soc. Sci. Fisheries, 19, 603-610.
2. Gustavson, K. H. (1954). Hydroxyproline and stability of collagens, Acta Chem. Scand., 8, 1298-1299.
3. Burge, R. E. and Hynes, R. D. (1959). The thermal denaturation of collagen in solution and its structural implications, J. Mol. Biol., 1, 155-164.
4. Harrington, W. F. and Rao, N. V. (1967). Pyrrolidine ring stability of collagen. In: Conformation of Biopolymers, G. N. Ramachandran, (ed.) pp. 513-531. (Academic Press, New York.)
5. Rigby, B. J. (1971). The thermal stability of collagen: Its significance in biology and physiology. In: Chemical Dynamics, G. W. Hirshenfelder (ed), pp. 537-555. (Wiley, New York.)
6. Mathews, M. B. (1975). Connective tissue. Macromolecular structure and evolution. (Springer-Verlag, Berlin.)
7. Burjanadze, T. V. (1979). Hydroxyproline content and location in relation to collagen thermal stability, Biopolymers, 18, 931-938.
8. Burjanadze, T. V. (1982). Evidence for the role of 4-hydroxyproline localized in the third position of the triplet (Gly-X-Y) in adaptional changes of thermostability of a collagen molecule and collagen fibrils, Biopolymers, 21, 1489-1501.
9. Vogel, B. E., Minor, R. R., Freund, M. and Prockop, D. J. (1987). A point mutation in a type I procollagen gene converts glycine 748 of the α1 chain to cysteine and destabilizes the triple helix in a lethal variant of osteogenesis imperfecta, J. Biol. Chem., 262, 14737-14744.
10. Bachinger, H. P., Morris, N. P. and Davis, J. M. (1993). Thermal stability and folding of the collagen triple helix and the effects of mutations in osteogenesis imperfecta on the triple helix of type I collagen, Amer. J. Med. Genet., 45, 152-162.
11. Harrington, W. F. and Rao, N. V. (1970). Collagen structure in solution. I. Kinetics of helix regeneration in single-chain gelatins. Biochemistry, 9, 3714-3724.
12. Harrington, W. F. and Karr, G. M. (1970). Collagen structure in solution. II. Analysis of refolding kinetics in terms of nucleation and growth processes, Biochemistry, 9, 3725-3733.
13. Haushka, P. V. and Harrington, W. F. (1970). Collagen structure in solution. III. Effect of cross-links on thermal stability and refolding kinetics, Biochemistry, 9, 3734-3745.
14. Burjanadze, T. V. and Bezhitadze, M. O. (1992). Presence of a thermostable domain in the helical part of the type I collagen molecule and its role in the mechanism of triple helix folding, Biopolymers, 32, 951-956.
15. Burjanadze, T. V. (1992). Thermodynamic substantiation of water-bridged collagen structure. Biopolymers, 32, 941-949.
16. Burjanadze, T. V., Bezhitadze, M. O., Giorgadze, A. G. and Babakishvili, G. M. (1990). Thermodynamic parameters of fibril formation activation of evolutionary differentiated collagens. Biofizika (USSR), 35, 933-937.
17. 2O demonstrates that collagen monomers undergo a conformational transition prior to thermal self-assembly in vitro, Biochemistry, 30, 2372-2377.
18. Von Hippel, P. H. (1967). Collagen structure in solution. In: Treatise on Collagen I, G. N. Ramachandran (ed). pp. 253-338. (Academic Press, New York.)
19. Privalov, P. L., Tiktopulo, E. I. and Tischenko, V. M. (1979). Stability and mobility of the collagen structure, J. Mol. Biol., 127, 203-216.
20. Burjanadze, T. V., Tiktopulo, E. I. and Privalov, P. L. (1987). Enthalpy and entropy of the denaturation of collagen with different degrees of thermostability, Doklady Akad. Nauk USSR., 293, 720-724.
21. Paterlini, M. G., Nemethy, G. and Scheraga, H. A. (1995). The energy of formation of internal loops in triple-helical collagen polypeptides, Biopolymers, 35, 607-619.
22. Miller, E. J. (1988). Collagen types. In: Collagen, vol. I., M. Nimmi (ed.). (CRC Press, Boca Raton.)
23. Miura, S. and Kimura, S. (1985). Jellyfish mesogloea collagen. Characterization of molecules as α1α2α3 heterotrimers, J. Biol. Chem., 260, 15352-15356.
24. Morris, N. P., Watt, S. L., Davis, J. M. and Bachinger, H. P. (1990). Unfolding intermediates in the triple helix to coil transition of bovine type XI collagen and human type V collagens α1(2)α2 and α1α2α3, J. Biol. Chem., 265, 10081-10087.
25. Van der Rest, M. and Bruckner, P. (1993). Collagens: Diversity at the molecular and supramolecular levels, Current Opinion in Structural Biol., 3, 430-436.
26. Piez, K. A. (1976). Primary structure of collagen, In: Biochemistry of Collagen, G. N. Ramachandran and A. H. Reddi, (ed.) pp. 1-42. (Plenum, New York.)
27. Brazel, D., Oberbaumer, I., Dieringer, H., Babel, W., Glanville, R. W., Deutzmann, R. and Kuhn, K. (1987). Completion of the amino acid sequence of the α1 of human basement membrane collagen (type IV) reveals 21 non-triplet interruptions located within the collagenous domain, Eur. J. Biochem., 168, 529-536.
28. Suzuki, E., Fraser, R. D. B. and MacRae, T. P. (1980). Role of hydroxyproline in the stabilization of the collagen molecule via water molecules, Int. J. Biol. Macromolec., 2, 54-56.
29. Bhatnagar, R. S., Pattabiraman, N., Sorensen, K. R., Langridge, R., MacElroy, R. D. and Renugopalakrishnan, V. (1988). Interchain proline: proline contacts contribute to the stability of the triple helical conformation, J. Bio. Struc. Dyn., 6, 223-233.
30. Rich, A. and Crick, F. H. S. (1961). The molecular structure of collagen, J. Mol. Biol., 3, 483-506.
31. Ramachandran, G. N. and Chandrasekharan, R. (1968). Interchain hydrogen bonds via bound water molecules in the collagen triple helix, Biopolymers, 6, 1649-1658.
32. Burjanadze, T. V. (1982). Stabilization of collagen structure: Dependence of collagen denaturation enthalpy on the imino acid content, Biopolymers, 21, 1587-1595.
33. Miles, C. A., Burjanadze, T. V. and 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.
34. Veis, A. (1964). The macromolecular chemistry of gelatin. (Academic Press, New York.)
35. Doty, P. and Nishihara, T. (1958). The molecular properties and thermal stability of soluble collagen. In: Recent Advances in Gelatin and Glue Research, G. Stainsby (ed.), pp. 92-99. (Pergamon Press, New York.)
36. Esipova, N. G. (1957). Hydroxyproline and thermostability of collagen, Biofizika (USSR), 2, 445-450.
37. Piez, K. A. and Gross, J. (1960). The amino acid composition of some fish collagens. The relation between composition and structure, J. Biol. Chem., 235, 995-998.
38. Masser, M. D. and Rice, R. V. (1963). The denaturation and renaturation of earthworm cuticle collagen, Biochem. Biophys. Acta, 74, 283-294.
39. Josse, J. and Harrington, W. F. (1964). Role of pyrrolidine residues in the structure and stabilization of collagen, J. Mol. Biol., 9, 269-287.
40. Privalov, P. L. and Tiktopulo, E. I. (1970). Thermal conformational transformation of tropocollagen. I. Calorimetric study, Biopolymers, 9, 127-139.
41. Berg, R. A. and Prockop, D. J. (1973). 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, 115-120.
42. Rosenbloom, J., Harsch, M. and Jimenez, S. (1973). Hydroxyproline content determines the denaturation temperature of chick tendon collagen, Arch. Biochem. Biophvs., 158, 478-484.
43. Ward, A. R. and Mason, P. (1973). Influence of proline hydroxylation upon the thermal stability of collagen fragments α1CB2, J. Mol. Biol., 79, 431-435.
44. Goldstein, A. and Adams, E. (1968). Occurrence of glycylhydyroxyprolyl sequences in earthworm cuticle collagen, J. Biol. Chem., 243, 3550-3552.
45. Goldstein, A. and Adams, E. (1970). Glycylhydroxyprolyl sequences in earthworm cuticle collagen: glycylhydroxyprolylserine, J. Biol. Chem., 245, 5478-5483.
46. Gryder, R. M., Lamon, M. and Adams, E. (1975). Sequence position of 3-hydroxyproline in basement membrane collagen. Isolation of glycyl-3-hydroxypolyl-4-hydroxyproline from swine kidney, J. Biol. Chem., 250, 2470-2474.
47. Francois, J. (1985). Biochemical and biophysical characterization of collagen in Tenebrio molitor L. (Coleoptera, Tenebrionidae), Biochimie, 67, 1035-1042.
48. Engel, J. (1987). Folding and unfolding of collagen triple helices, Adv. Meat. Research, 4, 145-161.
49. Rose, C., Kumar, M. and Mandai, A. B. (1988). A study of the hydration and thermodynamics of warm-water and cold-water fish collagen, Biochem. J., 249, 127-133.
50. Rigby, B. J. (1967). Relation between the shrinkage of native collagen in acid solution and the melting temperature of the tropocollagen molecule, Biochim. Biophys. Acta., 133, 272-277.
51. McBride, O. W. and Harrington, W. F. (1967). Helix-coil transition in collagen. Evidence for a single-stranded triple helix, Biochemistry, 6, 1499-1514.
52. Veis, A. (1982). Collagen Fibrillogenesis, Connective Tissue Research, 10, 11-24.
53. Veis, A. and George, A. (1994). Fundamentals of interstitial collagen self-assembly. In Extracellular Matrix assembly and Structure, P.D. Yurchenko, D.E. Birk, and R.P. Mecham. (eds.), pp. 15-45, (Academic Press, N.Y.)
54. Leiken, S., Rau, D. C. and Parsegian, V. A. (1995). Temperature-favoured assembly of collagen is driven by hydrophilic not hydrophobic interactions, Struct. Biol., 2, 205-210.
55. Vasquez, M., Nemethy, G. and Scheraga, H. A. (1994). Conformational Energy Calculations on polypeptides and proteins, Chem. Rev, 94, 2183-2239.
56. Privalov, P. L. (1979). Stability of proteins: small globular proteins, Adv. Prot. Chem., 33, 167-241.
57. Privalov, P. L. (1982). Stability of proteins. Proteins which do not present a single cooperative system, Adv. Prot. Chem., 35, 1-104.
58. Murphy, K. P., Privalov, P. L. and Gill, S. J. (1990). Common features of protein unfolding and dissolution of hydrophobic compounds, Science, 247, 559-561.
59. Ramachandran, G. N., Bansal, M. and Bhatnagar, R. S. (1973). A hypothesis on the role of hydroxyproline in stabilizing collagen structure, Biochim. Biophys. Acta., 322, 166-171.
60. 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.
61. Burjanadze, T. V. and Kisiriya, E. L. (1982). Dependence of thermal stability on the number of hydrogen bonds in water-bridged collagen structure, Biopolymers, 21, 695-701.
62. Schellman, J. A. (1955). The stability of hydrogen bonded peptide structures in aqueous solution, Compt. rend. lab. Carlsberg, Ser. chim., 29, 230-259.
63. Mrevlishvili, G. M. and Sharimanov, Iu. G. (1978). Study of hydration and intramolecular fusion of collagen by the NMR and calorimetric methods, Biofizika (USSR), 23, 717-719.
64. Grigera, J. R. and Berendsen, H. J. C. (1979). The molecular details of collagen hydration, Biopolymers, 18, 47-57.
65. von Hippel, P. H. and Schlich, T. (1969). The effect of neutral salts on the structure and conformation stability of biological macromolecules In: Structure and stability of biological macromolecules, S. Timasheff and G. D. Fasman, (eds.) pp. 417-474. (Marcel Dekker, New York.)
66. Esipova, N. G., Andreeva, N. S. and Gatovska, T. V. (1958). The stabilizing role of water in the structure of collagen, Biofizika (USSR), 3, 505-511.
67. Berendsen, H. J. C. and Migchelsen, C. (1965). Hydration structure of fibrous macromolecules, Ann N. Y. Acad. Sciences, 125, 365-379.
68. 15N solid-state NMR study of collagen and related polypeptides. The effect of hydration on formation of interchain hydrogen bonds as the primary source of stability of the collagen helix, Eur. J. Biochem., 224, 729-734.
69. 2O. Chem. Phys., 59, 296-305.
70. 10, J. Mol. Biol., 152, 427-443.
71. Esipova, N. G., Grigolava, M. V., Shchegoleva, T. Iu., Rogulenkova, V. N. and Maleev, V. Ia. (1981). Why must the collagen denaturation temperature be close to the temperature at which the species developed?, Biofizika (USSR), 26, 355-356.
72. Fessler, J. H. and Hodge, A. J. (1962). Ultracentrifugal observation of phase transition in density gradients, J. Mol. Biol., 15, 446-449.
73. n, Biopolymers, 16, 601-622.
74. Nordwig, A. and Hayduk, U. (1969). Invertebrate collagens: isolation, characterization and phylogenetic aspects, J. Mol. Biol., 44, 161-172.
75. Ramirez, F. (1988). Organization and evolution of the fibrillar collagen genes. In: Collagen: IV. Molecular Biology, B.R. Olsen and M. Nimni (eds.), pp. 22-30, (CRC Press, Boca Raton, Florida.)
76. Gaill, F., Mann, K., Wiedemann, H., Engel, J. and Timpl, R. (1995). Structural comparison of cuticle and interstitial collagens from annelids living in shallow sea-water and at deep-sea hydrothermal vents, J. Mol. Biol., 246, 284-294.
77. Venugopal, M. G., Ramshaw, J. A. M., Braswell, E., Zhu, D. and Brodsky, B. (1994). Electrostatic interactions in collagen-like triple helical peptides, Biochemistry, 33, 7948-7956.
78. Vitagliano, L., Nemethy, G. and Scheraga, H. A. (1993). Stabilization of the triple-helical structure of natural collagen by side chain interactions, Biochemistry, 32, 7354-7359.
79. Bruckner, P. and Eikenberry, E. F. (1984). Procollagen is more stable in cellulo than in vitro, Eur. J. Biochem., 140, 397-399.
80. Gura, T., Hu, G. and Veis, A. (1996). Posttranscriptional aspects of the biosynthesis of type I collagen pro-alpha chains: The effects of posttranslational modifications on synthesis pauses during elongation of the pro α1(I) chain, J Cellular Biochem., 61, 194-215.
81. Bruckner, P., Eikenberry, E. F. and Prockop, D. J. (1981). Formation of the triple helix in type I collagen in cellulo. A kinetic model based on cis-trans isomerization of peptide bonds, Eur. J. Biochem., 118, 607-613.
82. Bailey, A. J. (1968). The nature of collagen, Comp. Biochem., 26B, 297-423.
83. Alexandrov, V. Ja. (1977). Cell, Macromolecules and Temperature. (Springer-Verlag, New York.)
84. Bernengo, J. C., Ronziere, M. C., Bezot, P., Bezot, C., Herbage, D. and Veis, A. (1983). A hydrodynamic study of collagen fibrillogenesis by electric birefringence and quasielastic light scattering, J. Biol Chem., 258, 1001-1006.
85. Hofmann, H., Voss, T., Kuhn, K. and Engel, J. (1984). Localization of flexible sites in thread-like molecules from electron micrographs. Comparison of interstitial, basement membrane and intima collagens, J. Mol. Biol., 172, 325-343.
86. Nikitin, V. N., Perskii, E. E. and Utevskaia, L. A. (1977). Age and evolutionary biochemistry of collagen structures. (Naukova Dumka, Kiev.)
87. Uitto, J. (1986). Interstitial collagens, Biol. Integument, 2, 800-809.
88. Sakai, T. and Gross, J. (1967). Some properties of the products of reaction of tadpole collagenase with collagen, Biochemistry, 6, 518-528.
89. Danielsen, C. C. (1987). Thermal stability of human-fibroblast-collagenase-cleavage products of type-I and type-III collagens, Biochem. J., 247, 725-729.
90. Privolov, P. L. (1968). Thermal transconformation of procollagen. I. Denaturation enthalpy of procollagens with different imino acid content, Biofizika (USSR), 13, 955-963.
91. Burjanadze, T. V. (1971). Calorimetric determination of the denaturation heat of collagens different in imino acid content, Bull. Georgia Acad. Sci., 65, 445-448.
92. Menashi, S., Finch, A., Gardner, P. J. and Ledward, D. A. (1976). Enthalpy changes associated with the denaturation of collagens of different imino acid content, Biochem. Biophys. Acta, 444, 623-625.