Chemical Synthesis of Peptides Containing Site-Specific Advanced Glycation Endproducts

Accounts of Chemical Research

Volumn 49, Issue 10, 2016, Pages 2199-2208

  Kaur, Harveen ^a   Kamalov, Meder ^b   Brimble, Margaret A ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; PEPTIDE;

CHEMICAL STRUCTURE; CHEMISTRY; GLYCOSYLATION; SYNTHESIS;

GLYCATION END PRODUCTS, ADVANCED; GLYCOSYLATION; MOLECULAR STRUCTURE; PEPTIDES;

EID: 84991764297     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.6b00366     Document Type: Article

References (62)

1. Maillard, L. C. The action of amino acids on sugar; The formation of melanoidin by a methodic route Cr. Hebd. Acad. Sci. 1912, 154, 66-68
2. Prasad, K.; Dhar, I.; Caspar-Bell, G. Role of advanced glycation end Products and its receptors in the pathogenesis of cigarette smoke-induced cardiovascular disease Int. J. Angiol. 2015, 24, 75-80 10.1055/s-0034-1396413
3. Singh, R.; Barden, A.; Mori, T.; Beilin, L. Advanced glycation end-products: a review Diabetologia 2001, 44, 129-146 10.1007/s001250051591
4. Vlassara, H.; Palace, M. R. Diabetes and advanced glycation endproducts J. Intern. Med. 2002, 251, 87-101 10.1046/j.1365-2796.2002.00932.x
5. Monnier, V. M.; Stevens, V. J.; Cerami, A. Non-enzymatic glycosylation, sulfhydryl oxidation, and aggregation of lens proteins in experimental sugar cataracts J. Exp. Med. 1979, 150, 1098-1107 10.1084/jem.150.5.1098
6. Lee, A. T.; Cerami, A. Role of glycation in aging Ann. N. Y. Acad. Sci. 1992, 663, 63-70 10.1111/j.1749-6632.1992.tb38649.x
7. Goldin, A.; Beckman, J. A.; Schmidt, A. M.; Creager, M. A. Advanced glycation end products-Sparking the development of diabetic vascular injury Circulation 2006, 114, 597-605 10.1161/CIRCULATIONAHA.106.621854
8. Koschinsky, T.; He, C. J.; Mitsuhashi, T.; Bucala, R.; Liu, C.; Buenting, C.; Heitmann, K.; Vlassara, H. Orally absorbed reactive glycation products (glycotoxins): An environmental risk factor in diabetic nephropathy Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 6474-6479 10.1073/pnas.94.12.6474
9. Semba, R. D.; Nicklett, E. J.; Ferrucci, L. Does accumulation of advanced glycation end products contribute to the aging phenotype? J. Gerontol., Ser. A 2010, 65, 963-975 10.1093/gerona/glq074
10. Dyer, D. G.; Dunn, J. A.; Thorpe, S. R.; Bailie, K. E.; Lyons, T. J.; Mccance, D. R.; Baynes, J. W. Accumulation of Maillard reaction-products in skin collagen in diabetes and aging J. Clin. Invest. 1993, 91, 2463-2469 10.1172/JCI116481
11. Ledesma, M. D.; Bonay, P.; Colaco, C.; Avila, J. Analysis of microtubule-associated protein-Tau glycation in paired helical filaments J. Biol. Chem. 1994, 269, 21614-21619
12. Yan, H.; Harding, J. J. Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase Biochem. J. 1997, 328, 599-605 10.1042/bj3280599
13. Kikuchi, S.; Shinpo, K.; Takeuchi, M.; Yamagishi, S.; Makita, Z.; Sasaki, N.; Tashiro, K. Glycation-a sweet tempter for neuronal death Brain Res. Rev. 2003, 41, 306-323 10.1016/S0165-0173(02)00273-4
14. Kizer, J. R.; Benkeser, D.; Arnold, A. M.; Ix, J. H.; Mukamal, K. J.; Djousse, L.; Tracy, R. P.; Siscovick, D. S.; Psaty, B. M.; Zieman, S. J. Advanced glycation/glycoxidation endproduct carboxymethyl-lysine and incidence of coronary heart disease and stroke in older adults Atherosclerosis 2014, 235, 116-121 10.1016/j.atherosclerosis.2014.04.013
15. Arsov, S.; Graaff, R.; van Oeveren, W.; Stegmayr, B.; Sikole, A.; Rakhorst, G.; Smit, A. J. Advanced glycation end-products and skin autofluorescence in end-stage renal disease: a review Clin. Chem. Lab. Med. 2014, 52, 11-20 10.1515/cclm-2012-0832
16. Basta, G.; Schmidt, A. M.; De Caterina, R. Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes Cardiovasc. Res. 2004, 63, 582-592 10.1016/j.cardiores.2004.05.001
17. Munch, G.; Thome, J.; Foley, P.; SChinzel, R.; Riederer, P. Advanced glycation endproducts in ageing and Alzheimer's disease Brain Res. Rev. 1997, 23, 134-143 10.1016/S0165-0173(96)00016-1
18. Kouidrat, Y.; Amad, A.; Arai, M.; Miyashita, M.; Lalau, J. D.; Loas, G.; Itokawa, M. Advanced glycation end products and schizophrenia: A systematic review J. Psychiatr. Res. 2015, 66-67, 112-117 10.1016/j.jpsychires.2015.04.023
19. Viguet-Carrin, S.; Roux, J. P.; Arlot, M. E.; Merabet, Z.; Leeming, D. J.; Byrjalsen, I.; Delmas, P. D.; Bouxsein, M. L. Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae Bone 2006, 39, 1073-1079 10.1016/j.bone.2006.05.013
20. Paul, R. G.; Bailey, A. J. Glycation of collagen: The basis of its central role in the late complications of ageing and diabetes Int. J. Biochem. Cell Biol. 1996, 28, 1297-1310 10.1016/S1357-2725(96)00079-9
21. Wadman, S. K.; Debree, P. K.; Vansprang, F. J.; Kamerling, J. P.; Haverkamp, J.; Vliegenthart, J. F. G. Nϵ-(Carboxymethyl)lysine, a constituent of human urine Clin. Chim. Acta 1975, 59, 313-320 10.1016/0009-8981(75)90007-8
22. Ahmed, M. U.; Thorpe, S. R.; Baynes, J. W. Identification of N-Epsilon-carboxymethyllysine as a degradation product of fructoselysine in glycated protein J. Biol. Chem. 1986, 261, 4889-4894
23. Glomb, M. A.; Monnier, V. M. Mechanism of protein modification by glyoxal and glycolaldehyde, reactive intermediates of the Maillard reaction J. Biol. Chem. 1995, 270, 10017-10026 10.1074/jbc.270.17.10017
24. Hellerma, L.; Coffey, D. S. Studies on crystalline D-amino acid oxidase.V. Characterization of borohydride-reduced enzyme-substrate intermediate synthesis of epsilon-N-(1-Carboxyethyl)-L-Lysine J. Biol. Chem. 1967, 242, 582
25. Biemann, K.; Lioret, C.; Asselineau, J.; Lederer, E.; Polonsky, J. On the structure of lysopine, a new amino acid isolated from crown gall tissue Biochim. Biophys. Acta 1960, 40, 369-370 10.1016/0006-3002(60)91370-6
26. Fujioka, M.; Tanaka, M. Enzymic and chemical synthesis of epsilon-N-(L-Propionyl-2)-L-Lysine Eur. J. Biochem. 1978, 90, 297-300 10.1111/j.1432-1033.1978.tb12603.x
27. Liardon, R.; Deweckgaudard, D.; Philippossian, G.; Finot, P. A. Identification of N-Epsilon-Carboxymethyllysine-a New Maillard Reaction-Product, in Rat Urine J. Agric. Food Chem. 1987, 35, 427-431 10.1021/jf00075a035
28. Csuk, R.; Stark, S.; Barthel, A.; Kluge, R.; Strohl, D. A Robust Synthesis of N-epsilon-(Carboxymethyl)-L-lysine (CML) Synthesis 2009, 2009, 1933-1934 10.1055/s-0028-1088064
29. Krause, R.; Knoll, K.; Henle, T. Studies on the formation of furosine and pyridosine during acid hydrolysis of different Amadori products of lysine Eur. Food Res. Technol. 2003, 216, 277-283
30. Gruber, P.; Hofmann, T. Chemoselective synthesis of peptides containing major advanced glycation end-products of lysine and arginine J. Pept. Res. 2005, 66, 111-124 10.1111/j.1399-3011.2005.00279.x
31. Woods, T. M.; Kamalov, M.; Harris, P. W. R.; Cooper, G. J. S.; Brimble, M. Synthesis of monolysyl advanced glycation endproducts and their incorporation into collagen model peptides Org. Lett. 2012, 14, 5740-5743 10.1021/ol302745f
32. Kihlberg, J.; Bergman, R.; Wickberg, B. Synthesis of strombine-a new method for monocarboxymethylation of primary amines Acta Chem. Scand. 1983, 37, 911-916 10.3891/acta.chem.scand.37b-0911
33. Kamalov, M. AGEing Peptides: Synthesis and analysis of peptides site-specifically modified by advanced glycation endproducts. Doctoral Thesis, The University of Auckland, New Zealand, 2014.
34. Erdmann, R. S.; Wennemers, H. Functionalizable collagen model peptides J. Am. Chem. Soc. 2010, 132, 13957-13959 10.1021/ja103392t
35. Kamalov, M.; Yang, S.; Harris, P. W. R.; Cooper, G. J. S.; Brimble, M. A. Expedient synthesis of peptides containing N-epsilon-carboxymethyllysine Synlett 2014, 25, 1835-1838 10.1055/s-0033-1378305
36. Xue, J.; Rai, V.; Singer, D.; Chabierski, S.; Xie, J. J.; Reverdatto, S.; Burz, D. S.; Schmidt, A. M.; Hoffmann, R.; Shekhtman, A. Advanced glycation end product recognition by the receptor for AGEs Structure 2011, 19, 722-732 10.1016/j.str.2011.02.013
37. Pashikanti, S.; de Alba, D. R.; Boissonneault, G. A.; Cervantes-Laurean, D. Rutin metabolites: Novel inhibitors of nonoxidative advanced glycation end products Free Radical Biol. Med. 2010, 48, 656-663 10.1016/j.freeradbiomed.2009.11.019
38. Chace, K. V.; Carubelli, R.; Nordquist, R. E. The role of nonenzymatic glycosylation, transition-metals, and free-radicals in the formation of collagen aggregates Arch. Biochem. Biophys. 1991, 288, 473-480 10.1016/0003-9861(91)90223-6
39. Seifert, S. T.; Krause, R.; Gloe, K.; Henle, T. Metal complexation by the peptide-bound Maillard reaction products N-epsilon-fructoselysine and N-epsilon-carboxymethyllysine J. Agric. Food Chem. 2004, 52, 2347-2350 10.1021/jf035223y
40. Kamalov, M.; Harris, P. W. R.; Hartinger, C. G.; Miskelly, G. M.; Cooper, G. J. S.; Brimble, M. A. Physicochemical studies on the copper(II) binding by glycated collagen telopeptides Org. Biomol. Chem. 2015, 13, 3058-3063 10.1039/C4OB02536A
41. Nakayama, T.; Hayase, F.; Kato, H. Formation of epsilon-(2-formyl-5-hydroxymethyl-pyrrol-1-yl)-L-norleucine in the Maillard Reaction between D-glucose and L-lysine Agric. Biol. Chem. 1980, 44, 1201-1202 10.1080/00021369.1980.10864104
42. Chiang, G. H. High-Performance Liquid-Chromatographic determination of epsilon-pyrrole-lysine in processed food J. Agric. Food Chem. 1988, 36, 506-509 10.1021/jf00081a025
43. Henle, T.; Bachmann, A. Synthesis of pyrraline reference material Z. Lebensm.-Unters. Forsch. 1996, 202, 72-74 10.1007/BF01229689
44. Madson, M. A.; Feather, M. S. An improved preparation of 3-deoxy-D-erythro-hex-2-ulose via the bis(benzoylhydrazone) and some related constitutional studies Carbohydr. Res. 1981, 94, 183-191 10.1016/S0008-6215(00)80716-8
45. Miller, R.; Olsson, K. Synthesis of (±)-2-Formyl-5-(hydroxymethyl)pyrrole-1-norleucine-a biologically-active Maillard reaction-product derived from glucose and lysine Acta Chem. Scand. 1985, 39, 717-723 10.3891/acta.chem.scand.39b-0717
46. Schüßler, U.; Ledl, F. Synthesis of 2-amino-6-(2-formyl-5-hydroxymethyl-1-pyrrolyl)hexanoic Acid Z. Lebensm.-Unters. Forsch. 1989, 189, 138-140 10.1007/BF01332948
47. Geng, H. M.; Chen, J. L. Y.; Furkert, D. P.; Jiang, S. D.; Brimble, M. A. A convergent synthesis of the 2-formylpyrrole spiroketal natural product Acortatarin A Synlett 2012, 23, 855-858 10.1055/s-0031-1290508
48. Kamalov, M.; Harris, P. W. R.; Wood, J. M.; Brimble, M. A. On resin synthesis and cross-linking of collagen peptides containing the advanced glycation end-product pyrraline via Maillard condensation Chem. Commun. 2015, 51, 9475-9478 10.1039/C5CC03052H
49. Yuen, T. Y.; Eaton, S. E.; Woods, T. M.; Furkert, D. P.; Choi, K. W.; Brimble, M. A. A Maillard approach to 2-formylpyrroles: Synthesis of magnolamide, lobechine and funebral Eur. J. Org. Chem. 2014, 2014, 1431-1437 10.1002/ejoc.201301639
50. Brinkmann, E.; Wellsknecht, K. J.; Thorpe, S. R.; Baynes, J. W. Characterization of an imidazolium compound formed by reaction of methylglyoxal and N-Alpha-hippuryllysine J. Chem. Soc., Perkin Trans. 1 1995, 2817-2818 10.1039/P19950002817
51. Wellsknecht, K. J.; Brinkmann, E.; Baynes, J. W. Characterization of an imidazolium salt formed from glyoxal and N-alpha-hippuryllysine-a model for Maillard reaction cross-links in proteins J. Org. Chem. 1995, 60, 6246-6247 10.1021/jo00125a001
52. Nagaraj, R. H.; Shipanova, I. N.; Faust, F. M. Protein cross-linking by the Maillard reaction-Isolation, characterization, and in vivo detection of a lysine-lysine cross-link derived from methylglyoxal J. Biol. Chem. 1996, 271, 19338-19345 10.1074/jbc.271.32.19338
53. Linetsky, M. D.; Shipova, E. V. Convenient synthesis of GOLD and MOLD and identification of their oxidation products in vitro and in vivo Amino Acids 2007, 32, 285-289 10.1007/s00726-006-0338-6
54. Esposito, D.; Kirchhecker, S.; Antonietti, M. A sustainable route towards imidazolium building blocks based on biomass molecules Chem.-Eur. J. 2013, 19, 15097-15100 10.1002/chem.201302806
55. Yamada, H.; Sasaki, T.; Niwa, S.; Oishi, T.; Murata, M.; Kawakami, T.; Aimoto, S. Intact glycation end products containing carboxymethyl-lysine and glyoxal lysine dimer obtained from synthetic collagen model peptide Bioorg. Med. Chem. Lett. 2004, 14, 5677-5680 10.1016/j.bmcl.2004.08.044
56. Kamalov, M.; Harris, P. W. R.; Cooper, G. J. S.; Brimble, M. A. Site-specific cross-linking of collagen peptides by lysyl advanced glycation endproducts Chem. Commun. 2014, 50, 4944-4946 10.1039/c4cc02003k
57. Bhatnagar, P. K.; Agner, E. K.; Alberts, D.; Arbo, B. E.; Callahan, J. F.; Cuthbertson, A. S.; Engelsen, S. J.; Fjerdingstad, H.; Hartmann, M.; Heerding, D.; Hiebl, J.; Huffman, W. F.; Hysben, M.; King, A. G.; Kremminger, P.; Kwon, C.; LoCastro, S.; Lovhaug, D.; Pelus, L. M.; Petteway, S.; Takata, J. S. Structure-activity relationships of novel hematoregulatory peptides J. Med. Chem. 1996, 39, 3814-3819 10.1021/jm960099d
58. Lange, M.; Cuthbertson, A. S.; Towart, R.; Fischer, P. M. Synthesis and activity of dimeric bradykinin antagonists containing diaminodicarboxylic acid bridge residues J. Pept. Sci. 1998, 4, 289-293 10.1002/(SICI)1099-1387(199806)4:4<289::AID-PSC146>3.0.CO;2-T
59. Kamalov, M.; Kaur, H.; Brimble, M. A. Intermolecular peptide cross-linking by using diaminodicarboxylic Acids Chem.-Eur. J. 2016, 22, 3622-3631 10.1002/chem.201503458
60. Kok, W. M.; Scanlon, D. B.; Karas, J. A.; Miles, L. A.; Tew, D. J.; Parker, M. W.; Barnham, K. J.; Hutton, C. A. Solid-phase synthesis of homodimeric peptides: preparation of covalently-linked dimers of amyloid beta peptide Chem. Commun. 2009, 6228-6230 10.1039/b912784d
61. Kok, W. M.; Cottam, J. M.; Ciccotosto, G. D.; Miles, L. A.; Karas, J. A.; Scanlon, D. B.; Roberts, B. R.; Parker, M. W.; Cappai, R.; Barnham, K. J.; Hutton, C. A. Synthetic dityrosine-linked beta-amyloid dimers form stable, soluble, neurotoxic oligomers Chem. Sci. 2013, 4, 4449-4454 10.1039/c3sc22295k
62. Drake, M. P.; Davison, P. F.; Bump, S.; Schmitt, F. O. Action of proteolytic enzymes on tropocollagen and insoluble collagen Biochemistry 1966, 5, 301-312 10.1021/bi00865a039