Carbohydrate-mimetic peptides: Structural aspects of mimicry and therapeutic implications

Expert Opinion on Biological Therapy

Volumn 11, Issue 2, 2011, Pages 211-224

  Agostino, Mark ^a   Sandrin, Mauro S ^b   Thompson, Philip E ^a   Farrugia, William ^c   Ramsland, Paul A ^a,b,c   Yuriev, Elizabeth ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BURNET INSTITUTE   (Australia)

Author keywords

molecular modeling; molecular recognition; peptide carbohydrate mimicry; peptide immunogenicity; X ray crystallography

Indexed keywords

2G12.1 PEPTIDE; ANTIBODY; BACTERIUM ANTIBODY; CARBOHYDRATE BINDING PROTEIN; CARBOHYDRATE MIMETIC PEPTIDE; CONCANAVALIN A; GALACTOSE ANTIBODY; ISOGLOBOTRIAOSYLCERAMIDE SYNTHASE; MANNOSE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2G12; MONOCLONAL ANTIBODY SYA J6; OSELTAMIVIR; SHIGELLA ANTIBODY; SYNTHETASE; TETANUS TOXOID; UNCLASSIFIED DRUG; ZANAMIVIR;

AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; ANTIGEN RECOGNITION; BINDING SITE; CRYSTAL STRUCTURE; DRUG MECHANISM; DRUG TARGETING; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; MOLECULAR DOCKING; MOLECULAR MIMICRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHAGE DISPLAY; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SHIGELLA; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CARBOHYDRATES; HUMANS; MODELS, MOLECULAR; MOLECULAR MIMICRY; NEOPLASMS; PEPTIDE FRAGMENTS;

EID: 78651373160     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.2011.542140     Document Type: Review

References (104)

1. Todeschini AR, Hakomori S-I. Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim Biophys Acta-Gen Subj 2008;1780:421-33
2. Werz DB, Ranzinger R, Herget S, et al Exploring the structural diversity of mammalian carbohydrates (glycospace) by statistical databank analysis. ACS Chem Biol 2007;2:685-91
3. Gabius H-J, Siebert H-C, Andre S, et al Chemical biology of the sugar code. Chembiochem 2004;5:740-64
4. Gabius H-J. Glycans: bioactive signals decoded by lectins. Biochem Soc Trans 2008;36:1491-6
5. Ernst B, Magnani JL. From carbohydrate leads to glycomimetic drugs. Nat Rev Drug Disc 2009;8:661-77
6. von Itzstein M, Wu W-Y, Kok GB, et al Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 1993;363:418-23
7. Lew W, Chen X, Kim UC. Discovery and development of GS 4104 (oseltamivir): an orally active influenza neuraminidase inhibitor. Curr Med Chem 2000;7:663-72
8. Johnson MA, Pinto BM. Structural and functional studies of peptide-carbohydrate mimicry. Top Curr Chem 2008;273:55-116
9. Cunto-Amesty G, Dam TK, Luo P, et al Directing the immune response to carbohydrate antigens. J Biol Chem 2001;276:30490-8
10. Johnson MA, Pinto BM. Molecular mimicry of carbohydrates by peptides. Aust J Chem 2002;55:13-25
11. Seeberger PH. Automated carbohydrate synthesis as platform to address fundamental aspects of glycobiology - current status and future challenges. Carbohyd Res 2008;343:1889-96
12. Koester DC, Holkenbrink A, Werz DB. Recent advances in the synthesis of carbohydrate mimetics. Synthesis 2010;42:3217-42
13. Werle M, Bernkop-Schnurch A. Strategies to improve plasma half life of peptide and protein drugs. Amino Acids 2006;30:351-67
14. Aguilar M-I, Purcell AW, Devi R, et al Beta-amino acid-containing hybrid peptides - new opportunities in peptidomimetics. Org Biomol Chem 2007;5:2884-90
15. Geysen HM, Rodda SJ, Mason TJ, et al Strategies for epitope analysis using peptide synthesis. J Immunol Methods 1987;102:259-74
16. Kehoe JW, Kay BK. Filamentous phage display in the new millenium. Chem Rev 2005;105:4056-72
17. Oldenburg KR, Loganathan D, Goldstein IJ, et al Peptide ligands for a sugar-binding protein isolated from a random peptide library. Proc Nat Acad Sci USA 1992;89:5393-7
18. Mertens P, Walgraffe D, Laurent T, et al Selection of phage-displayed peptides recognised by monoclonal antibodies directed against the lipopolysaccharide of Brucella. Int Rev Immunol 2001;20:181-99
19. Beninati C, Garibaldi M, Lo Passo C, et al Immunogenic mimics of Brucella lipopolysaccharide epitopes. Peptides 2009;30:1936-9
20. Jouault T, Fradin C, Dzierszinski F, et al Peptides that mimic Candida albicans-derived beta-1,2-linked mannosides. Glycobiology 2001;11:693-701
21. Beenhouwer DO, May RJ, Valadon P, et al High affinity mimotope of the polysaccharide capsule of Cryptococcus neoformans identified from an evolutionary phage peptide library. J Immunol 2002;169:6992-9
22. Hou Y, Gu XX. Development of peptide mimotopes of lipooligosaccharide from nontypeable Haemophilus influenzae as vaccine candidates. J Immunol 2003;170:4373-9
23. Gevorkian G, Segura E, Acero G, et al Peptide mimotopes of Mycobacterium tuberculosis carbohydrate immunodeterminants. Biochem J 2005;387:411-17
24. Sharma A, Saha A, Bhattacharjee S, et al Specific and randomly derived immunoactive peptide mimotopes of mycobacterial antigens. Clin Vacc Immunol 2006;13:1143-54
25. Brett PJ, Tiwana H, Feavers IM, et al Characterization of oligopeptides that cross-react with carbohydrate-specific antibodies by real time kinetics, in-solution competition enzyme-linked immunosorbent assay, and immunological analyses. J Biol Chem 2002;277:20468-76
26. Lauvrak V, Berntzen G, Heggelund U, et al Selection and characterization of cyclic peptides that bind to a monoclonal antibody against meningococcal L3,7,9 lipopolysaccharides. Scand J Immunol 2004;59:373-84
27. Lo Passo C, Romeo A, Pernice I, et al Peptide mimics of the group B meningococcal capsule induce bactericidal and protective antibodies after immunization. J Immunol 2007;178:4417-23
28. Prinz DM, Smithson SL, Westerink MAJ. Two different methods result in the selection of peptides that induce a protective antibody response to Neisseria meningitidis serogroup C. J Immunol Methods 2004;285:1-14
29. Ngampasutadol J, Rice PA, Walsh MT, et al Characterization of a peptide vaccine candidate mimicking an oligosaccharide epitope of Neisseria gonorrhoeae and resultant immune responses and function. Vaccine 2006;24:157-70
30. Tang SS, Tan WS, Devi S, et al Mimotopes of the Vi antigen of Salmonella enterica serovar Typhi identified from phage display peptide library. Clin Vacc Immunol 2003;10:1078-84
31. Theillet FX, Saul FA, Vulliez-Le Normand B, et al Structural mimicry of O-antigen by a peptide revealed in a complex with an antibody raised againstShigella flexneri serotype 2a. J Mol Biol 2009;388:839-50
32. Buchwald UK, Lees A, Steinitz M, et al A peptide mimotope of type 8 pneumococcal capsular polysaccharide induces a protective immune response in mice. Infect Immun 2005;73:325-33
33. Dharmasena MN, Jewell DA, Taylor RK. Development of peptide mimics of a protective epitope of Vibrio cholerae Ogawa O-antigen and investigation of the structural basis of peptide mimicry. J Biol Chem 2007;282:33805-16
34. Doleckova-Maresova L, Pavlik M, Horn M, et al De novo design of alpha-amylase inhibitor: a small linear mimetic of macromolecular proteinaceous ligands. Chem Biol 2005;12:1349-57
35. Yu L, Yu PS, Yee Yen Mui E, et al Phage display screening against a set of targets to establish peptide-based sugar mimetics and molecular docking to predict binding site. Bioorg Med Chem 2009;17:4825-32
36. Arnusch CJ, Andre S, Valentini P, et al Interference of the galactose-dependent binding of lectins by novel pentapeptide ligands. Bioorg Med Chem Lett 2004;14:1437-40
37. Andre S, Arnusch CJ, Kuwabara I, et al Identification of peptide ligands for malignancy- and growth-regulating galectins using random phage-display and designed combinatorial peptide libraries. Bioorg Med Chem 2005;13:563-73
38. Tang Z, Wang L, Hu L, et al Identification and characterization of peptide mimics of blood group A antigen. J Huazhong Univ Sci Tech Med Sci 2008;28:222-6
39. Kumar A, Rao M. A novel bifunctional peptidic aspartic protease inhibitor inhibits chitinase A from Serratia marcescens: kinetic analysis of inhibition and binding affinity. Biochim Biophys Acta-Gen Subj 2010;1800:526-36
40. Zhan J, Xia Z, Xu L, et al A peptide mimetic of Gal-alpha1,3-Gal is able to block human natural antibodies. Biochem Biophys Res Commun 2003;308:19-22
41. Lang J, Zhan J, Xu L, et al Identification of peptide mimetics of xenoreactive alpha-Gal antigenic epitope by phage display. Biochem Biophys Res Commun 2006;344:214-20
42. Wondimu A, Zhang TQ, Kieber-Emmons T, et al Peptides mimicking GD2 ganglioside elicit cellular, humoral and tumor-protective immune responses in mice. Cancer Immunol Immunother 2008;57:1079-89
43. Miura Y, Sasao Y, Kamihira M, et al Peptides binding to a Gb3 mimic selected from a phage library. Biochim Biophys Acta-Gen Subj 2004;1673:131-8
44. Simon-Haldi M, Mantei N, Franke J, et al Identification of a peptide mimic of the L2/HNK-1 carbohydrate epitope. J Neurochem 2002;83:1380-8
45. Heimburg-Molinaro J, Almogren A, Morey S, et al Development, characterization, and immunotherapeutic use of peptide mimics of the Thomsen-Friedenreich carbohydrate antigen. Neoplasia 2009;11:780-92
46. Dinglasan RR, Porter-Kelley JM, Alam U, et al Peptide mimics as surrogate immunogens of mosquito midgut carbohydrate malaria transmission blocking targets. Vaccine 2005;23:2717-24
47. Jain D, Kaur KJ, Salunke DM. Enhanced binding of a rationally designed peptide ligand of concanavalin A arises from improved geometrical complementarity. Biochemistry 2001;40:12059-66
48. Johnson MA, Eniade AA, Pinto BM. Rational design and synthesis of peptide ligands for an anti-carbohydrate antibody and their immunochemical characterization. Bioorg Med Chem 2003;11:781-8
49. Hoess R, Brinkmann U, Handel T, et al Identification of a peptide which binds to the carbohydrate-specific monoclonal antibody B3. Gene 1993;128:43-9
50. Rodi DJ, Soares AS, Makowski L. Quantitative assessment of peptide sequence diversity in M13 combinatorial phage peptide libraries. J Mol Biol 2002;322:1039-52
51. The UniProt Consortium. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res 2010;38:D142-8
52. Agostino M, Sandrin MS, Thompson PE, et al Peptide inhibitors of xenoreactive antibodies mimic the interaction profile of the native carbohydrate antigens. Biopolymers: Peptide Sci 2010:published online 21 August 2010, doi: 10.1002/bip.21427
53. Krishnan L, Sahni G, Kaur KJ, et al Role of antibody paratope conformational flexibility in the manifestation of molecular mimicry. Biophys J 2008;94:1367-76
54. DeMarco ML, Woods RJ. Structural glycobiology: a game of snakes and ladders. Glycobiology 2008;18:426-40
55. Lutteke T. Analysis and validation of carbohydrate three-dimensional structures. Acta Crystallogr 2009;D65:156-68
56. Yuriev E, Sandrin MS, Ramsland PA. Antibody-ligand docking: insights into peptide-carbohydrate mimicry. Mol Simul 2008;34:461-8
57. Clement MJ, Fortune A, Phalipon A, et al Toward a better understanding of the basis of the molecular mimicry of polysaccharide antigens by peptides - the example of Shigella flexneri 5A. J Biol Chem 2006;281:2317-32
58. Agostino M, Sandrin MS, Thompson PE, et al In silico analysis of antibody-carbohydrate interactions and its application to xenoreactive antibodies. Mol Immunol 2009;47:233-46
59. Nurisso A, Kozmon S, Imberty A. Comparison of docking methods forcarbohydrate binding in calcium-dependent lectins and prediction of the carbohydrate binding mode to sea cucumber lectin CEL-III. Mol Simul 2008;34:469-79
60. Agostino M, Jene C, Boyle T, et al Molecular docking of carbohydrate ligands to antibodies: structural validation against crystal structures. J Chem Inf Model 2009;49:2749-60
61. Gattegno L, Ramdani A, Jouault T, et al Lectin-carbohydrate interactions and infectivity of human immunodeficiency virus type-1 (HIV-1). AIDS Res Hum Retrovir 1992;8:27-37
62. Pashov A, Canziani G, Monzavi-Karbassi B, et al Antigenic properties of peptide mimotopes of HIV-1-associated carbohydrate antigens. J Biol Chem 2005;280:28959-65
63. Harrop SJ, Helliwell JR, Wan TCM, et al Structure solution of a cubic crystal of concanavalin A complexed with methyl alpha-d-glucopyransoide. Acta Crystallogr 1996;D52:143-55
64. Agrawal BBL, Goldstein IJ. Specific binding of concanavalin A to cross-linked dextran gels. Biochem J 1965;96:23C-25C
65. Sharon N, Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 2004;14:53R-63R
66. Naismith JH, Emmerich C, Habash J, et al Refined structure of concanavalin A complexed with methyl alpha-d-mannopyranoside at 2.0 A°resolution and comparison with the saccharide-free structure. Acta Crystallogr 1994;D50:847-58
67. Sanders DAR, Moothoo DN, Raftery J, et al The 1.2 A° resolution structure of the Con A-dimannose complex. J Mol Biol 2001;310:875-84
68. Bouckaert J, Hamelryck TW, Wyns L, et al The crystal structures of Man (alpha1,3)Man(alpha1-O)Me and Man (alpha1,6)Man(alpha1-O)Me in complex with concanavalin A. J Biol Chem 1999;274:29188-195
69. Moothoo DN, Naismith JH. Concanavalin A distorts the beta- GlcNAc-(1!2)-Man linkage of beta- GlcNAc-(1!2)-alpha-Man-(1!3)-[beta- GlcNAc-(1!2)-alpha-Man-(1!6)]-Man upon binding. Glycobiology 1998;8:173-81
70. Naismith JH, Field RA. Structural basis of trimannoside recognition by concanavalin A. J Biol Chem 1996;271:972-6
71. Jain D, Kaur K, Sundaravadivel B, et al Structural and functional consequences of peptide-carbohydrate mimicry - crystal structure of a carbohydrate-mimicking peptide bound to concanavalin A. J Biol Chem 2000;275:16098-102
72. Jain D, Kaur KJ, Salunke DM. Plasticity in protein-peptide recognition: crystal structures of two different peptides bound to concanavalin A. Biophys J 2001;80:2912-21
73. Zhang Z, Qian M, Huang Q, et al Crystal structure of the complex of concanavalin A and hexapeptide. J Prot Chem 2001;20:423-9
74. Evans DM, Herman LW. Identification of peptide ligands specific for the sugar-binding site of concanavalin a by screening a synthetic peptide combinatorial library. J Biomol Screen 1997;2:225-33
75. Kaur KJ, Khurana S, Salunke DM. Topological analysis of the functional mimicry between a peptide and a carbohydrate moiety. J Biol Chem 1997;272:5539-43
76. Jain D, Kaur KJ, Goel M, et al Structural basis of functional mimicry between carbohydrate and peptide ligands of Con A. Biochem Biophys Res Commun 2000;272:843-9
77. Kaur KJ, Jain D, Goel M, et al Immunological implications of structural mimicry between a dodecapeptide and a carbohydrate moiety. Vaccine 2001;19:3124-30
78. Cao Y, Qin L, Zhang L, et al Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med 1995;332:201-8
79. Stiegler G, Katinger H. Therapeutic potential of neutralizing antibodies in the treatment of HIV-1 infection. J Antimicrob Chemother 2003;51:757-9
80. Scanlan CN, Pantophlet R, Wormald M, et al The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of a1-2 mannose residues on the outer face of gp120. J Virol 2002;76:7306-21
81. Calarese DA, Scanlan CN, Zwick MB, et al Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 2003;300:2065-71
82. Calarese DA, Lee H-K, Huang C-Y, et al Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12. Proc Nat Acad Sci USA 2005;102:13372-7
83. Menendez A, Calarese DA, Stanfield RL, et al A peptide inhibitor of HIV-1 neutralizing antibody 2G12 is not a structural mimic of the natural carbohydrate epitope on gp120. FASEB J 2008;22:1380-92
84. Phalipon A, Folgori A, Arondel J, et al Induction of anti-carbohydrate antibodies by phage library-selected peptide mimics. Eur J Immunol 1997;27:2620-5
85. Vyas NK, Vyas MN, Chervenak MC, et al Molecular recognition of oligosaccharide epitopes by a monoclonal Fab specific for Shigella flexneri Y lipopolysaccharide: X-ray structures and thermodynamics. Biochemistry 2002;41:13575-86
86. Carlin NIA, Gidney MAJ, Lindberg AA, et al Characterization of Shigellaflexneri-specific murine monoclonal antibodies by chemically defined glycoconjugates. J Immunol 1986;137:2361-6
87. Hossany RB, Johnson MA, Eniade AA, et al Synthesis and immunochemical characterization of protein conjugates of carbohydrate and carbohydrate-mimetic peptides as experimental vaccines. Bioorg Med Chem 2004;12:3743-54
88. Hossany BR, Johnston BD, Wen X, et al Design, synthesis, and immunochemical characterization of a chimeric glycopeptide corresponding to the Shigella flexneri Y O-polysaccharide and its peptide mimic MDWNMHAA. Carbohyd Res 2009;344:1412-27
89. Clement M-J, Imberty A, Phalipon A, et al Conformational studies of the O-specific polysaccharide of Shigella flexneri 5a and of four related synthetic pentasaccharide fragments using NMR and molecular modelling. J Biol Chem 2003;278:47928-36
90. Vyas NK, Vyas MN, Chervenak MC, et al Structural basis of peptide-carbohydrate mimicry in an antibody-combining site. Proc Nat Acad Sci USA 2003;100:15023-8
91. Borrelli S, Hossany RB, Pinto BM. Immunological evidence for functional rather than structural mimicry by a Shigella flexneri Y polysaccharide-mimetic peptide. Clin Vacc Immunol 2008;15:1106-14
92. Phalipon A, Costachel C, Grandjean C, et al Characterization of functional oligosaccharide mimics of the Shigella flexneri serotype 2a O-antigen: implications for the development of a chemically defined glycoconjugate vaccine. J Immunol 2006;176:1686-94
93. Vulliez-Le Normand B, Saul FA, Phalipon A, et al Structures of synthetic O-antigen fragments from serotype 2a Shigella flexneri in complex with a protective monoclonal antibody. Proc Nat Acad Sci USA 2008;105:9976-81
94. Yuriev E, Agostino M, Farrugia W, et al Structural biology of carbohydrate xenoantigens. Expert Opin Biol Ther 2009;9:1017-29
95. Ezzelarab M, Ayares D, Cooper DK. Carbohydrates in xenotransplantation. Immunol Cell Biol 2005;83:396-404
96. Lai L, Kolber-Simonds D, Park K-W, et al Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 2002;295:1089-92
97. Milland J, Christensen D, Lazarus BD, et al The molecular basis for Galalpha (1,3)Gal expression in animals with a deletion of the alpha1,3galactosyltransferase gene. J Immunol 2006;176:2448-54
98. Vaughan HA, Oldenburg KR, Gallop MA, et al Recognition of an octapeptide sequence by multiple Galalpha(1,3)Gal-binding proteins. Xenotransplantation 1996;3:18-23
99. Kooyman DL, McClellan SB, Parker W, et al Identification and characterization of a galactosyl peptide mimetic. Implications for use in removing xenoreactive anti-alpha gal antibodies. Transplantation 1996;61:851-5
100. Sandrin MS, Vaughan HA, Xing PX, et al Natural human anti-Gala(1,3)Gal antibodies react with human mucin peptides. Glycoconj J 1997;14:97-105
101. Xian M, Fatima Z, Zhang W, et al Identification of alpha-galactosyl epitope mimetics through rapid generation and screening of C-linked glycopeptides library. J Comb Chem 2004;6:126-34
102. Tempel W, Tschampel S, Woods RJ. The xenograft antigen bound to Griffonia simplicifolia lectin 1-B(4). X-ray crystal structure of the complex and molecular dynamics characterization of the binding site. J Biol Chem 2002;277:6615-21
103. Milland J, Yuriev E, Xing P-X, et al Carbohydrate residues downstream of the terminal Galalpha(1,3)Gal epitope modulate the specificity of xenoreactive antibodies. Immunol Cell Biol 2007;85:623-32
104. Agostino M, Sandrin MS, Thompson PE, et al Identification of preferred carbohydrate binding modes in xenoreactive antibodies by combining conformational filters and binding site maps. Glycobiology 2010;20:724-35