Predicting protein decomposition: The case of aspartic-acid racemization kinetics

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1379, 1999, Pages 51-64

  Collins, M J ^a   Waite, E R ^a   Van Duin, A C T ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Aspartic acid racemization; Bone; Collagen; Dating; Deamidation; Kinetics

Indexed keywords

EID: 0033613646     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0359     Document Type: Article

References (100)

1. Bada, J. L. 1971 Kinetics of the non-biological decomposition and racemization of amino acids in natural waters. Adv. Chem. Ser. 106, 309-331.
2. Bada, J. L. 1972 Kinetics of racemization of amino acids as a function of pH. J. Am. Chem. Soc. 94, 1371-1373.
3. Bada, J. L. 1985 Aspartic acid racemization ages of California Paleoindian skeletons. Am. Antiquity 50, 645-647.
4. Bada, J. L. & Protsch, R. 1973 Racemization reaction of aspartic acid and its use in dating fossil bones. Proc. Natn. Acad. Sci. USA 70, 1331-1334.
5. Bada, J. L., Wang, X. S., Poinar, H. N., Pääbo, S. & Poinar, G. O. 1994 Amino acid racemization in amber-entombed insects - implications for DNA preservation. Geochim. Cosmochim. Acta 58, 3131-3135.
6. Bender, M. L. 1974 Reliability of amino acid racemisation dating and palaeotemperature analysis on bones. Nature 252, 378-379.
7. Bongers, J., Heimer, E. P., Lambros, T., Pan, Y. C. E., Campbell, R. M. & Felix, A. M. 1992 Degradation of aspartic acid and asparagine residues in human growth hormone releasing factor. Int. J. Peptide Prot. Res. 39, 364-374.
8. Brennan, T. V. & Clarke, S. 1993 Spontaneous degradation of polypeptides at aspartyl and asparaginyl residues - effects of the solvent dielectric. Prot. Sci. 2, 331-338.
9. Brennan, T. V. & Clarke, S. 1995 Effect of adjacent histidine and cysteine residues on the spontaneous degradation of aspartyl and asparaginyl containing peptides. Int. J. Peptide Prot. Res. 45, 547-553.
10. Brinton, K. L. & Bada, J. L. 1995 Aspartic acid racemization and protein diagenesis in corals over the last 350 years-comment, Geochim. Cosmochim. Acta 59, 415-416.
11. Brooks, A. S., Hare, P. E., Kokis, J. E., Miller, G. H., Ernst, R. D. & Wendorf, F. 1990 Dating Pleistocene archaeological sites by protein diagenesis in ostrich eggshell. Science 248, 60-64.
12. Brunauer, L. S. & Clarke, S. 1986 Age-dependent accumulation of protein residues which can be hydrolyzed to Daspartic acid in human crythrocytes. J. Biol. Chem. 261, 12538-12543.
13. Burkert, U. & Allinger, N. L. 1982 Molecular mechanics. Washington, DC: American Chemical Society.
14. Capasso, S., Mazzarella, L. & Zagari, A. 1991 Deamidation via cyclic imide of asparaginyl peptides: dependence on salts, buffers and organic solvents. Peptide Res. 4, 234-238.
15. Capasso, S., Mazzarella, L., Sica, F., Zagari, A. & Salvadori, S. 1992 Spontaneous cyclization of the aspartic acid side chain to the succinimide derivative. J. Chem. Soc. Chem. Comm. II, 919-921.
16. Capasso, S., Mazzarella, L., Sica, F., Zagari, A. & Salvadori, S. 1993 Kinetics and mechanism of succinimide ring formation in the deamidation process of asparagine residues. J. Chem. Soc. Perkin Trans. II, 679-682.
17. Carolan, V. A., Gardner, M. L. G., Lucy, D. & Pollard, A. M. 1997 Some considerations regarding the use of amino acid racemization in human dentine as an indicator of age at death. J. Forensic Sci. 42, 10-16.
18. Child, A. M., Gillard, R. D. & Pollard, A. M. 1993 Microbially induced promotion of amino acid racemization in bone: isolation of the micro-organisms and detection of their enzymes. J. Archaeol. Sci. 20, 159-168.
19. Cleland, J. L., Powell, M. F. & Shire, S. J. 1993 The development of stable protein formulations: a close look at protein aggregation, deamidation, and oxidation. Crit. Rev. Therapeut. Drug Carrier Syst. 10, 307-377.
20. Cloos, P. A. C. 1995 Age related changes in proteins in human dentine. MPhil thesis, Det Kongelige Danske Kunstakademi.
21. Collins, M. J. & Galley, P. 1998 Towards an optimal method of archaeological collagen extraction; the influence of pH and grinding. Ancient Biomolecules. (In the press.)
22. Collins, M. J., Westbrock, P., Muyzer, G. & de Leeuw, J. W. 1992 Experimental evidence for condensation reactions between sugars and proteins in carbonate skeletons. Geochim. Cosmochim. Acta 56, 1539-1544.
23. Collins, M. J., Riley, M., Child, A. M. & Turner-Walker, G. 1995 A basic mathematical simulation of the chemical degradation of ancient collagen. J. Arch. Sci. 22, 175-183.
24. Csapo; J., Csapó-Kiss, Némethy, S., Folestad S., Tivesten, A. & Martin, T. G. 1994 Age determination based on amino acid racemization: a new possibility. Amino Acids 7, 317-325.
25. Daniel, R. M., Dines, M. & Petach, H. H. 1996 The denaturation and degradation of stable enzymes at high temperatures. Biochem. J. 317, 1-11.
26. de Sol, B. S. 1978 Factors affecting the extent of racemization of peptide and protein bound amino acids: positioning effects and kinetic studies. MS thesis, Utah State University, Logan, UT.
27. Druffel, E. R. M., Griffin, S., Witter, A., Nelson, E., Southson, J., Kashgarian, M. & Vogel, J. 1995 Gerardia: bristlecone pine of the deep sea? Geochim. Cosmochim. Acta 59, 5031-5036.
28. Elster, H., Gil-Av, E. & Weiner, S. 1991 Amino acid racemization of fossil bone. J. Arch. Sci. 18, 605-617.
29. Fujii, N., Satoh, K., Harada, K. & Ishibashi, Y. 1994 Simultaneous stereoinversion and isomerization at specific aspartic acid residues in α-a-crystallin from human lens. J. Biochem. 116, 663-669.
30. Fujii, N., Momose, Y. & Harada, K. 1996 Kinetic study of racemization of aspartyl residues in model peptides of α-a-crystallin. Int. J. Peptide Prot. Res. 48, 118-122.
31. Fujisawa, R., Zhou, H.-Y. & Kuboki, Y. 1994 In vitro and in vivo association of dentin phosphophoryn with α1CB6 peptide of type I collagen. Connective Tissue Res. 31, 1-10.
32. Garner, W. H. & Spector, A. 1978 Racemization in human lens: evidence of rapid insolubilization of specific polypeptides in cataract formation. Proc. Natn. Acad. Sci. USA 75, 3618-3620.
33. Garnero, P., Fledelius, C., Ginetys, E., Serre, C.-M., Vignot, E. & Delmas, P. D. 1997 Decreased β-isomerization of the C-terminal telopeptide of type I collagen α1 chain in Paget's disease of bone. J. Bone Mineral Res. 12, 1407-1415.
34. Geiger, T. & Clarke, S. 1987 Deamidation, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J. Biol. Chem. 262, 785-794.
35. Gillard, R. D., Hardman, S. M., Pollard, A. M., Sutton, P. A. & Whittaker, D. K. 1991 Determinations of age at death in archaeological populations using the D/L ratio of aspartic acid in dental collagen. Archaeometry 1990, 637-644.
36. Goodfriend, G. A. 1991 Patterns of racemization and epimerization of amino acids in land snail shells over the course of the Holocene. Geochim. Cosmochim. Acta 55, 293-302.
37. Goodfriend, G. A. 1992 Rapid racemization of aspartic acid in mollusc shells and potential for dating over recent centuries. Nature 357, 399-401.
38. Goodfriend, G. A. 1997 Aspartic acid racemization and amino acid composition of the organic endoskeleton of the deep-water colonial anemone Gerardia: determination of longevity from kinetic experiments. Geochim. Cosmochim. Acta 61, 1931-1939.
39. Goodfriend, G. A. & Hare, P. E. 1995 Reply to comment by K. L. F. Brinton and J. E. Bada on 'Aspartic acid racemization and protein diagenesis in corals over the last 350 years'. Geochim. Cosmochim. Acta 59, 417-418.
40. Goodfriend, G. A. & Meyer, V. R. 1991 A comparative-study of the kinetics of amino-acid racemization epimerization in fossil and modern mollusk shells. Geochim. Cosmochim. Acta 55, 3355-3367.
41. Goodfriend, G. A., Hare, P. E. & Druffel, E. R. M. 1992 Aspartic acid racemization and protein diagenesis in corals over the last 350 years. Geochim. Cosmochim. Acta 56, 3847-3850.
42. Goodfriend, G. A., Kashgarian, M. & Harasewych, M. G. 1995 Aspartic acid racemization and the life history of deep-water slit shells. Geochim. Cosmochim. Acta 59, 1125-1129.
43. Goodfriend, G. A., Brigham-Grette, J. & Miller, G. H. 1996 Enhanced age resolution of the marine quaternary record in the arctic using aspartic acid racemization dating of bivalve shells. Quaternary Res. 45, 176-187.
44. Harada, N., Handa, N., Ito, M., Oba, T. & Matsumoto, E. 1996 Chronology of marine sediments by the racemization reaction of aspartic acid in planktonic foraminifera. Org. Geochem. 24, 921-930.
45. Hare, P. E. 1980 Organic geochemistry of bone and its relation to the survival of bone in the natural environment. In Fossils in the making (ed. A. K. Behrensmeyer & A. Hill), pp. 208-219. University of Chicago Press.
46. Hensel, R., Jakob, I., Scheer, H. & Lottspeich, F. 1992 Proteins from hyperthermophilic Archaea - stability towards covalent modification of the peptide-chain. Biochem. Soc. Symp. 58, 127-133.
47. Hirst, K. L., Ibaraki-O'Connor, I., Young, M. F. & Dixon, M. J. 1997 Cloning and expression analysis of the bovine dentin matrix acidic phosphoprotein gene. J. Dental Res. 76, 754-760.
48. Johnson, B. J. & Miller, G. H. 1997 Archaeological applications of amino acid racemization. Archaeometry 39, 265-287.
49. Julg, A., Lafont, R. & Perinett, G. 1987 Mechanisms of collagen racemizationin fossil bones: application to absolute dating. Quaternary Sci. Rev. 6, 25-28.
50. Kimber, R. W. L. & Hare, P. E. 1992 Wide range of racemization of amino-acids in peptides from human fossil bone and its implications for amino acid racemization dating. Geochim. Cosmochim. Acta 56, 739-743.
51. King, K. & Bada, J. L. 1979 Effect of in situ leaching on amino acid racemisation rates in fossil bone. Nature 281, 135-137.
52. Kossiakoff, A. A. 1988 Tertiary structure is a principal determinant to protein deamidation. Science 240, 191-194.
53. Krings, M., Stone, A., Schmitz, R. W., Krainitzki, H., Stoncking, M. & Pääbo, S. 1997 Neanderthal DNA sequences and the origin of modern humans. Cell 90, 19-30.
54. Linde, A. 1989 Dentin matrix proteins: composition and possible functions in calcification. Anat. Rec. 224, 154-166.
55. Lura, R. & Schirch, V. 1988 Role of peptide conformation in the rate and mechanism of deamidation of asparaginyl residues. Biochemistry 27, 7671-7677.
56. McKerrow, J. H. 1973 Non-enzymatic deamidation of asparingyl residues in model peptides and proteins. PhD thesis, University of California, San Diego.
57. 14-C ages and aspartic acid racemization at the Upper Palaeolithic site of the Abri Pataud (Dordogne, France). J. Arch. Sci. 23, 803-809.
58. Maroudas, A., Bayliss, M. T., Uchitel-Kaushansky, N., Schneiderman, R. & Gilav, E. 1998 Aggrecan turnover in human articular cartilage: use of aspartic acid racemization as a marker of molecular age. Arch. Biochem. Biophys. 350, 61-71.
59. Masters, P. M. 1982 Amino acid racemization in structural proteins. In Biological markers of ageing (ed. M. E. Raff & M. D. Schneider), pp. 120-137. Washington, DC: NIH Publications.
60. Masters, P. M. 1985 Jn vivo decomposition of phosphoserine and serine in noncollagenous protein from human dentine. Calcified Tissue Int. 37, 236-241.
61. Matsu'ura, S. & Ueta, N. 1980 Fraction dependent variation of aspartic acid racemization age in fossil bone. Nature 286, 883-884.
62. Meeson, B. W., Corprew, F. E., McManus, J. M P., Myers, D. M., Closs, J. W., Sun, K.-J., Sunday, D. J. & Sellers, P. J. 1995 ISLSCP Initiative I - global data sets for land-atmosphere models 1987-1988. Volumes 1-5. Published on CD-ROM by NASA (USA_NASA_GDAAC_ISLSCP_001-USA_NASA_GDAAC_ISLSCP_005).
63. Metwalli, A. A. M. & van Bockel, M. A. J. S. 1998 On the kinetics of heat-induced deamidation and breakdown of caseinate. Food Chem. 61, 53-61.
64. Miller, G. H., Magee, J. W. & Jull, A. J. T. 1997 Low-latitude glacial cooling in the Southern Hemisphere from amino-acid racemization in Emu eggshells. Nature 385, 241-244.
65. Müller, H. T. & Heidemann, E. 1993 Untersuchung der Gesetzmässigkeitein für den Säureabbau von Hautkollagen und Indentifizierung der Kollagenspaltstellen biem sauren Gelatineprozess. Das Leder 44, 69-79.
66. Némethy, S. 1995 Molecular palaeotological studies of shelled marine organisms and mammal bones. PhD thesis, Göteborg University, Göteborg.
67. Ohtani, S. & Yamamoto, K. 1991 Age estimation using the racemization of amino acid in human dentin. J. Forensic Sci 36, 792-800.
68. Ohtani, S. & Yamamoto, K. 1992 Estimation of age from a tooth by means of racemization of an amino-acid, especially aspartic-acid - comparison of enamel and dentin. J. Forensic Sci. 37, 1061-1067.
69. Ohtani, S., Matsushima, Y., Ohhira, H. & Watanabe, A. 1995 Age-related changes in D-aspartic acid of rat teeth. Growth, Development and Aging 59, 55-61.
70. Oliyai, C. & Borchardt, R. T. 1994 Chemical pathways of peptide degradation. 6. Effect of the primary sequence on the pathways of degradation of aspartyl residues in model hexapeptides. Pharmaceut. Res. 11, 751-758.
71. Patel, K. & Borchardt, R. T. 1990a Chemical pathways of peptide degradation. 3. Effect of primary sequence on the pathways of deamidation of asparaginyl residues in hexapeptides. Pharmaceut. Res. 7, 787-793.
72. Patel, K. & Borchardt, R. T. 1990b Chemical pathways of peptide degradation. 2. Kinetics of deamidation of an asparaginyl residue in a model hexapeptide. Pharmaceut. Res. 7, 703-711.
73. Poinar, H. N., Höss, M., Bada, J. L. & Pääbo, S. 1996 Amino acid racemization and the preservation of ancient DNA. Science 272, 864-866.
74. Pollard, A. M. & Heron, C. 1996 Amino acid stereochemistry and the first Americans. In Archaeological chemistry (ed. A. M. Pollard & C. Heron), pp. 271-301. London: RSC Paperbacks.
75. Radkiewicz, J. L., Zipse, H., Clarke, S. & Houk, K. N. 1996 Accelerated racemization of aspartic acid and asparagine residues via succinimide intermediates: an ab initio theoretical exploration of mechanism. J. Am. Chem. Soc. 118, 9148-9155.
76. Ritchie, H. H. & Wang, L. H. 1996 Sequence determination of an extremely acidic rat dentin phosphoprotein. J. Biol. Chem. 271, 21695-21698.
77. Ritz, S. & Kaatsch, H.-J. 1996 Methoden der altersbestimmung an lebendon personon: Mobgliichkeiten, Grenzen, Zuliissigkeit & Ethische. Vertretbarkeit. Rerhtsmed. 6, 171-176.
78. Ritz, S. & Schutz, H. W. 1993 Aspartic acid racemization in intervertebral disks as an aid to postmortem estimation of age at death. J. Forensic Sci. 38, 633-640.
79. Ritz, S., Schutz, H. W. & Peper, C. 1993 Postmortem estimation of age at death based on aspartic-acid racemization in dentin - its applicability for root dentin. Int. J. Legal Med. 105, 289-293.
80. Saleh, N., Deutsch, D. & Gil-Av, E. 1993 Racemization of aspartic acid in the extracellular matrix proteins of primary and secondary dentin. Calcified Tissue Int. 53, 103-110.
81. Sellers, P. J. (and 14 others) 1995 An overview of the ISLSCP Initiative I - global data sets. On ISLSCP Initiative I global data sets for land atmosphere models 1987-1988. Volumes 1 5. Published on CD-ROM by NASA. Volume 1: USA_NASA_GDAAC_ISLSCP_001. OVERVIEW.DOC.
82. Senderoff, R. I., Wootton, S. C., Boctor, A. M., Chen, T. M., Giordani, A. B., Julian, T. N. & Radebaugh, G. W. 1994 Aqueous stability of human epidermal growth factor 1-48. Pharmaceut. Res. 11, 1712-1720.
83. Shimoyama, A. & Harada, K. 1984 An age determination of an ancient burial mound man by apparent racemization reaction of aspartic acid in tooth dentine. Chem. Lett. 10, 1661-1664.
84. Sinex, F. M. 1960 Ageing and the lability of irreplaceable molecules. II. The amide groups of collagen. J. Gerontol. 15, 15-18.
85. Skelton, R. R. 1983 Amino acid racemization dating: a test of its reliability for North American archaeology. PhD thesis, University of California, Davis, CA.
86. Smith, G. G. & Evans, R. C. 1980 The effect of structure and conditions on the rate of racemization of free and bound amino acids. In Biogeochemistry of amino acids (ed. P. E. Hare, T. C Hoering & K. King Jr). pp. 257-282. New York: Wiley.
87. Steinberg, S. M., Masters, P. M. & Bada, J. L. 1984 The racemization of free and peptide bound serine and aspartic acid at 100°C as a function of pH - implications for in vivo racemization. Bioorganic Chem. 12, 349-355.
88. Stetler-Stevenson, W. G. & Veis, A. 1986 Type I collagen shows a specific binding affinity for bovine dentin phosphoryn. Calcified Tissue Int. 38, 135-141.
89. Stevenson, C. L., Friedman, A. R., Kubiak.T. M., Donlan, M. E. & Borchardt, R. T. 1993 Effect of secondary structure on the rate of deamidation of several growth hormone releasing factor analogues. Int. J. Peptide Prot. Res. 42, 497-503.
90. Sykes, G. A., Collins, M. J. & Walton, D. I. 1995 The significance of a geochemically isolated (intra-crystalline) organic fraction within biominerals. Org. Geochem. 23, 1059-1066.
91. Tomizawa, H., Yamada, H., Wada, K. & Imoto, T. 1995 Stabilization of lysozyme against irreversible inactivation by suppression of chemical reactions. J. Biochem. 117, 635-640.
92. Triffit, J. T. 1980 The organic matrix of bone tissue. In Fundamental and clinical bone physiology (ed. M. R. Urist), pp. 45-82. Lippincott, PA: Lippincott.
93. Tyler-Cross, R. & Schirch, V. 1991 Effects of amino acid sequence, buffers, and ionic strength on the rate and mechanism of deamidation of asparagine residues in small peptides. J. Biol. Chem. 266, 22549-22556.
94. Van Duin, A. C. T. & Collins, M. J. 1998 The effects of conformational constraints on aspartic acid racemization. Org. Geochem. (In the press.)
95. Von Endt, D. W. 1980 Protein hydrolysis and amino acid racemization in sized bone. In Biogeochemistry of amino acids (ed. P. E. Hare, T. C. Hoering & K. King Jr), pp. 297-304. New York: Wiley.
96. Weiner, S., Kustanovich, Z., Gil-Av, E. & Traub, W. 1980 Dead Sea scrolls parchments: unfolding of the collagen molecules and racemization of aspartic acid. Nature 287, 820-823.
97. Wonnacott, D. M. 1979 The application of gas Chromatography to the resolution of enantiomeric mixtures of amino acids. Factors affecting the racemization of amino acids. PhD thesis, Utah State University, Logan, Utah, as cited in Smith G. G. & Evans R. C. 1980 The effect of structure and conditions on the rate of racemization of free and bound amino acids. In Biogeochemistry of amino acids (ed. P. E. Hare, T. C. Hoering & K. King Jr). pp. 257-282. New York: Wiley.
98. Wonnacott, D. M. 1979 The application of gas Chromatography to the resolution of enantiomeric mixtures of amino acids. Factors affecting the racemization of amino acids. PhD thesis, Utah State University, Logan, Utah, as cited in Smith G. G. & Evans R. C. 1980 The effect of structure and conditions on the rate of racemization of free and bound amino acids. In Biogeochemistry of amino acids (ed. P. E. Hare, T. C. Hoering & K. King Jr). pp. 257-282. New York: Wiley.
99. Zhang, J., Lee, T. C. & Ho, C. T. 1993 Comparative study on kinetics of nonenzymatic deamidation of soy protein and egg white lysozyme. J. Agric. Food Chem. 41, 2286-2290.
100. Zhao, M. X., Bada, J. L. & Ahern, T. J. 1989 Racemization rates of asparagine and aspartic-acid residues in lysozyme at 100°C as a function of pH. Bioorganic Chem. 17, 36-40.