Groove-type recognition of chlamydiaceae-specific lipopolysaccharide antigen by a family of antibodies possessing an unusual variable heavy chain N-linked glycan

Journal of Biological Chemistry

Volumn 289, Issue 24, 2014, Pages 16644-16661

  Haji Ghassemi, Omid ^a   Mul̈ler Loennies, Sven ^b   Saldova, Radka ^c   Muniyappa, Mohankumar ^c   Brade, Lore ^b   Rudd, Pauline M ^c   Harvey, David J ^e   Kosma, Paul ^d   Brade, Helmut ^b   Evans, Stephen V ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b RESEARCH CENTER BORSTEL   (Germany)

^c NATIONAL INSTITUTE FOR BIOPROCESSING RESEARCH AND TRAINING   (Ireland)

^d UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIBODIES; POLYSACCHARIDES;

ALLERGIC RESPONSE; ANTIGEN BINDING; CROSS REACTIVITY; HETEROGENEOUS MIXTURES; LIPOPOLYSACCHARIDES; N-LINKED GLYCANS; THERAPEUTIC ANTIBODIES; THREE-DIMENSIONAL STRUCTURE;

EPITOPES;

ANTIGEN; ASPARAGINE; BACTERIUM LIPOPOLYSACCHARIDE; CETUXIMAB; EPITOPE; GALACTOSYLGALACTOSE; GLYCOSAMINOGLYCAN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN HEAVY CHAIN;

ALLERGIC REACTION; AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; CHLAMYDIACEAE; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GLYCOSYLATION; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MICROCALORIMETRY; NONHUMAN; PRIORITY JOURNAL; RESIDUE ANALYSIS; STRUCTURE ANALYSIS;

ANTIBODIES; ANTIGEN; CARBOHYDRATE COMPLEX; GLYCOSYLATION; X-RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANTIBODIES, BACTERIAL; ANTIBODY AFFINITY; BINDING SITES, ANTIBODY; CHLAMYDIA; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; LIPOPOLYSACCHARIDES; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA;

EID: 84902531881     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.528224     Document Type: Article

References (77)

1. Sharon, J. (1990) Structural correlates of high antibody-affinity: three engineered amino-acid substitutions can increase the affinity of an anti-para-azophenylarsonate antibody 200-fold. Proc. Natl. Acad. Sci. U.S.A. 87, 4814-4817
2. Li, Z., Woo, C. J., Iglesias-Ussel, M. D., Ronai, D., and Scharff, M. D. (2004) The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 18, 1-11 (Pubitemid 38090682)
3. Teng, G., and Papavasiliou, F. N. (2007) Immunoglobulin somatic hypermutation. Annu. Rev. Genet. 41, 107-120
4. Gaspal, F. M., McConnell, F. M., Kim, M. Y., Gray, D., Kosco-Vilbois, M. H., Raykundalia, C. R., Botto, M., and Lane, P. J. (2006) The generation of thymus-independent germinal centers depends on CD40 but not on CD154, the T cell-derived CD40-ligand. Eur. J. Immunol. 36, 1665-1673 (Pubitemid 44089034)
5. Greenspan, N. S., Dacek, D. A., and Cooper, L. J. (1988) Fc region-dependence of IgG3 anti-streptococcal Group A carbohydrate antibody functional affinity. 1. The effect of temperature. J. Immunol. 141, 4276-4282 (Pubitemid 19018217)
6. Ullrich, M. (2009) Bacterial Polysaccharides: Current Innovations and Future Trends, pp. 105-123, Chapter 6, Caister Academic Press, Norfolk,UK
7. Stein, K. E. (1992) Thymus-independent and thymus-dependent responses to polysaccharide antigens. J. Infect. Dis. 165, S49-S52
8. Andersson, B., and Blomgren, H. (1971) Evidence for thymus-independent humoral antibody production in mice against polyvinylpyrrolidone and E. coli lipopolysaccharide. Cell. Immunol. 2, 411-424
9. Deleted in proof
10. Kimura, H., Buescher, E. S., Ball, E. D., and Marcus, D. M. (1989) Restricted usage of VH and V K genes by murine monoclonal antibodies against 3-fucosyllactosamine. Eur. J. Immunol. 19, 1741-1746 (Pubitemid 19243897)
11. Brooks, C. L., Müller-Loennies, S., Borisova, S. N., Brade, L., Kosma, P., Hirama, T., Mackenzie, C. R., Brade, H., and Evans, S. V. (2010) Antibodies raised against chlamydial lipopolysaccharide antigens reveal convergence in germ-line gene usage and differential epitope recognition. Biochemistry 49, 570-581
12. Zhou, J., Lottenbach, K. R., Barenkamp, S. J., and Reason, D. C. (2004) Somatic hypermutation and diverse immunoglobulin gene usage in the human antibody response to the capsular polysaccharide of Streptococcus pneumoniae type 6B. Infect Immun. 72, 3505-3514 (Pubitemid 38697777)
13. Pascual, V., Victor, K., Spellerberg, M., Hamblin, T. J., Stevenson, F. K., and Capra, J. D. (1992) Vh restriction among human cold agglutinins. The Vh4-21 gene segment is required to encode anti-I and anti-I specificities. J. Immunol. 149, 2337-2344
14. Nguyen, H. P., Seto, N. O., MacKenzie, C. R., Brade, L., Kosma, P., Brade, H., and Evans, S. V. (2003) Germ line antibody recognition of distinct carbohydrate epitopes. Nat. Struct. Biol. 10, 1019-1025 (Pubitemid 37500494)
15. Mariotti, S. P., Pascolini, D., and Rose-Nussbaumer, J. (2009) Trachoma: global magnitude of a preventable cause of blindness. Br. J. Ophthalmol. 93, 563-568
16. Brade, H., Brade, L., and Nano, F. E. (1987) Chemical and serological investigations on the genus-specific lipopolysaccharide epitope of Chlamydia. Proc. Natl. Acad. Sci. U.S.A. 84, 2508-2512 (Pubitemid 17075895)
17. Kosma, P. (1999) Chlamydial lipopolysaccharide. Biochim. Biophys. Acta 1455, 387-402
18. Brade, L., Zych, K., Rozalski, A., Kosma, P., Bock, K., and Brade, H. (1997) Structural requirements of synthetic oligosaccharides to bind monoclonal antibodies against Chlamydia lipopolysaccharide. Glycobiology 7, 819-827 (Pubitemid 27385379)
19. Kosma, P., Brade, H., and Evans, S. (2008) Lipopolysaccharide antigens of Chlamydia. In Carbohydrate-based vaccines (Roy, R., ed.), pp. 211-224, American Chemical Society (distributed by Oxford University Press), Washington, D. C.
20. Müller-Loennies, S., MacKenzie, C. R., Patenaude, S. I., Evans, S. V., Kosma, P., Brade, H., Brade, L., and Narang, S. (2000) Characterization of high affinity monoclonal antibodies specific for chlamydial lipopolysaccharide. Glycobiology 10, 121-130 (Pubitemid 30193012)
21. Holst, O., Bock, K., Brade, L., and Brade, H. (1995) The structures of oligosaccharide bisphosphates isolated from the lipopolysaccharide of a recombinant Escherichia coli strain expressing the gene gsea (3-deoxy-D-manno- octulopyranosonic acid (Kdo) transferase) of Chlamydia psittaci 6BC. Eur. J. Biochem. 229, 194-200
22. Brade, L., Rozalski, A., Kosma, P., and Brade, H. (2000) A monoclonal antibody recognizing the 3-deoxy-D-manno-oct-2-ulosonic acid (Kdo) trisaccharide αKdo(2→4)αKdo(2→4)αKdo of Chlamydophila psittaci 6BC lipopolysaccharide. J. Endotoxin Res. 6, 361-368 (Pubitemid 32241945)
23. Brade, L., Brunnemann, H., Ernst, M., Fu, Y., Holst, O., Kosma, P., Näher, H., Persson, K., and Brade, H. (1994) Occurrence of antibodies against chlamydial lipopolysaccharide in human sera as measured by ELISA using an artificial glycoconjugate antigen. FEMS Immunol. Med. Microbiol. 8, 27-41
24. Igietseme, J. U., Eko, F. O., and Black, C. M. (2011) Chlamydia vaccines: recent developments and the role of adjuvants in future formulations. Expert Rev. Vaccines 10, 1585-1596
25. Brooks, C. L., Müller-Loennies, S., Brade, L., Kosma, P., Hirama, T., Mac-Kenzie, C. R., Brade, H., and Evans, S. V. (2008) Exploration of specificity in germ line monoclonal antibody recognition of a range of natural and synthetic epitopes. J. Mol. Biol. 377, 450-468
26. Blackler, R. J., Müller-Loennies, S., Brooks, C. L., Evans, D. W., Brade, L., Kosma, P., Brade, H., and Evans, S. V. (2011)Acommon NH53K mutation in the combining site of antibodies raised against chlamydial LPS glycoconjugates significantly increases avidity. Biochemistry 50, 3357-3368
27. Blackler, R. J., Müller-Loennies, S., Brade, L., Kosma, P., Brade, H., and Evans, S. V. (2012) Antibody recognition of Chlamydia LPS: Structural insights of inherited immune responses. In Anticarbohydrate Antibodies: From Molecular Basis to Clinical Application (Kosma, P., and Müller-Loennies, S. eds.) pp. 75-120, Springer, Vienna
28. Evans, D. W., Müller-Loennies, S., Brooks, C. L., Brade, L., Kosma, P., Brade, H., and Evans, S. V. (2011) Structural insights into parallel strategies for germ line antibody recognition of lipopolysaccharide from Chlamydia. Glycobiology 21, 1049-1059
29. Müller-Loennies, S., Gronow, S., Brade, L., MacKenzie, R., Kosma, P., and Brade, H. (2006)Amonoclonal antibody against a carbohydrate epitope in lipopolysaccharide differentiates Chlamydophila psittaci from Chlamydophila pecorum, Chlamydophila pneumoniae, and Chlamydia trachomatis. Glycobiology 16, 184-196 (Pubitemid 43264685)
30. Nguyen, H. P., Seto, N. O., Brade, L., Kosma, P., Brade, H., and Evans, S. V. (2001) Crystallization and preliminary x-ray diffraction analysis of two homologous antigen-binding fragments in complex with different carbohydrate antigens. Acta Crystallogr. D Biol. Crystallogr. 57, 1872-1876 (Pubitemid 33145606)
31. Fu, Y., Baumann, M., Kosma, P., Brade, L., and Brade, H. (1992) A synthetic glycoconjugate representing the genus-specific epitope of chlamydial lipopolysaccharide exhibits the same specificity as its natural counterpart. Infect Immun. 60, 1314-1321
32. Brooks, C. L., Wimmer, K., Kosma, P., Müller-Loennies, S., Brade, L., Brade, H., and Evans, S. V. (2013) Exploring the cross-reactivity of S25-2: complex with a 5,6-dehydro-Kdo disaccharide. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69, 2-5
33. Holst, O., Broer, W., Thomas-Oates, J. E., Mamat, U., and Brade, H. (1993) Structural analysis of oligosaccharide bisphosphates isolated from the lipopolysaccharide of a recombinant strain of Escherichia coli F515 (Re Chemotype) expressing the genus-specific epitope of Chlamydia lipopolysaccharide. Eur. J. Biochem. 214, 703-710 (Pubitemid 23188145)
34. Holst, O., Thomas-Oates, J. E., and Brade, H. (1994) Preparation and structural analysis of oligosaccharide monophosphates obtained from the lipopolysaccharide of recombinant strains of Salmonella Minnesota and Escherichia coli expressing the genus-specific epitope of Chlamydia lipopolysaccharide. Eur. J. Biochem. 222, 183-194 (Pubitemid 24161340)
35. Kosma, P., Bahnmüller, R., Schulz, G., and Brade, H. (1990) Synthesis of a tetrasaccharide of the genus-specific lipopolysaccharide epitope of Chlamydia. Carbohydr. Res. 208, 37-50
36. Kosma, P., Gass, J., Schulz, G., Christian, R., and Unger, F. M. (1987) Artificial antigens. Synthesis of polyacrylamide copolymers containing 3-deoxy-D-manno-2-octulo-pyranosylonic acid (Kdo) residues. Carbohydr. Res. 167, 39-54
37. Kosma, P., Schulz, G., and Brade, H. (1988) Synthesis of a trisaccharide of 3-deoxy-D-manno-2-octulopyranosylonic acid (Kdo) residues related to the genus-specific lipopolysaccharide epitope of Chlamydia. Carbohydr. Res. 183, 183-199
38. Kosma, P., Schulz, G., Unger, F. M., and Brade, H. (1989) Synthesis of trisaccharides containing 3-deoxy-D-manno-2-octulosonic acid residues related to the Kdo region of enterobacterial lipopolysaccharides. Carbohydr. Res. 190, 191-201
39. Kosma, P., Reiter, A., Hofinger, A., Brade, L., and Brade, H. (2000) Synthesis of neoglycoproteins containing Kdo epitopes specific for Chlamydophila psittaci lipopolysaccharide. J. Endotoxin Res. 6, 57-69 (Pubitemid 30440497)
40. Müller-Loennies, S., Grimmecke, D., Brade, L., Lindner, B., Kosma, P., and Brade, H. (2002) A novel strategy for the synthesis of neoglycoconjugates from deacylated deep rough lipopolysaccharides. J. Endotoxin Res. 8, 295-305
41. Brochet, X., Lefranc, M. P., and Giudicelli, V. (2008) IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36, W503-W508
42. Yousfi Monod, M., Giudicelli, V., Chaume, D., and Lefranc, M. P. (2004) IMGT/junction analysis: the first tool for the analysis of the immunoglobulin and T cell receptor complex V-J and V-D-J junctions. Bioinformatics 20, i379-i385 (Pubitemid 41296713)
43. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
44. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
45. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
46. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321 (Pubitemid 37531815)
47. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
48. DeLano, W. L. (2012) The PyMOL Molecular Graphics System, Version 1.5.0.4, Schrödinger, LLC, New York
49. Royle, L., Radcliffe, C. M., Dwek, R. A., and Rudd, P. M. (2006) Detailed structural analysis of N-glycans released from glycoproteins in SDS-PAGE gel bands using HPLC combined with exoglycosidase array digestions. In Glycobiology Protocols (Brockhausen, I., ed.) Humana Press, Totowa, NJ
50. Royle, L., Campbell, M. P., Radcliffe, C. M., White, D. M., Harvey, D. J., Abrahams, J. L., Kim, Y. G., Henry, G. W., Shadick, N. A., Weinblatt, M. E., Lee, D. M., Rudd, P. M., and Dwek, R. A. (2008) HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Anal. Biochem. 376, 1-12
51. Bigge, J. C., Patel, T. P., Bruce, J. A., Goulding, P. N., Charles, S. M., and Parekh, R. B. (1995) Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid. Anal. Biochem. 230, 229-238
52. Börnsen, K. O., Mohr, M. D., and Widmer, H. M. (1995) Ion-exchange and purification of carbohydrates on a nafion(R) membrane as a new sample pretreatment for matrix-assisted laser-desorption ionization mass-spectrometry. Rapid Commun. Mass Spectrom. 9, 1031-1034
53. Harvey, D. J., Sobott, F., Crispin, M., Wrobel, A., Bonomelli, C., Vasiljevic, S., Scanlan, C. N., Scarff, C. A., Thalassinos, K., and Scrivens, J. H. (2011) Ion mobility mass spectrometry for extracting spectra of N-glycans directly from incubation mixtures following glycan release: application to glycans from engineered glycoforms of intact, folded HIV gp120. J. Am. Soc. Mass Spectrom. 22, 568-581
54. Harvey, D. J., Royle, L., Radcliffe, C. M., Rudd, P. M., and Dwek, R. A. (2008) Structural and quantitative analysis of N-linked glycans by matrixassisted laser desorption ionization and negative ion nanospray mass spectrometry. Anal. Biochem. 376, 44-60
55. Brade, L., Gronow, S., Wimmer, N., Kosma, P., and Brade, H. (2002) Monoclonal antibodies against 3-deoxy-α-D-manno-oct-2-ulosonic acid (Kdo) and D-glycero-α-D-talo-oct-2-ulosonic acid (Ko). J. Endotoxin Res. 8, 357-364 (Pubitemid 35460670)
56. Theillet, F. X., Saul, F. A., Vulliez-Le Normand, B., Hoos, S., Felici, F., Weintraub, A., Mulard, L. A., Phalipon, A., Delepierre, M., and Bentley, G. A. (2009) Structural mimicry of O-antigen by a peptide revealed in a complex with an antibody raised against Shigella flexneri serotype 2a. J. Mol. Biol. 388, 839-850
57. Murase, T., Zheng, R. B., Joe, M., Bai, Y., Marcus, S. L., Lowary, T. L., and Ng, K. K. (2009) Structural insights into antibody recognition of mycobacterial polysaccharides. J. Mol. Biol. 392, 381-392
58. Cygler, M., Rose, D. R., and Bundle, D. R. (1991) Recognition of a cellsurface oligosaccharide of pathogenic Salmonella by an antibody Fab fragment. Science 253, 442-445 (Pubitemid 21917173)
59. Sigurskjold, B. W., and Bundle, D. R. (1992) Thermodynamics of oligosaccharide binding to a monoclonal-antibody specific for a Salmonella O-antigen point to hydrophobic interactions in the binding site. J. Biol. Chem. 267, 8371-8376
60. Gerstenbruch, S., Brooks, C. L., Kosma, P., Brade, L., Mackenzie, C. R., Evans, S. V., Brade, H., and Müller-Loennies, S. (2010) Analysis of crossreactive and specific anti-carbohydrate antibodies against lipopolysaccharide from Chlamydophila psittaci. Glycobiology 20, 461-472
61. Kosma, P., Strobl, M., Allmaier, G., Schmid, E., and Brade, H. (1994) Synthesis of pentasaccharide core structures corresponding to the genusspecific lipopolysaccharide epitope of Chlamydia. Carbohydr. Res. 254, 105-132 (Pubitemid 24077858)
62. Xie, K., Song, S. C., Spitalnik, S. L., and Wedekind, J. E. (2005) Crystallographic analysis of the NNA7 Fab and proposal for the mode of human blood-group recognition. Acta Crystallogr. D Biol. Crystallogr. 61, 1386-1394 (Pubitemid 43943138)
63. Sheriff, S., Chang, C. Y., Jeffrey, P. D., and Bajorath, J. (1996) X-ray structure of the uncomplexed anti-tumor antibody BR96 and comparison with its antigen-bound form. J. Mol. Biol. 259, 938-946 (Pubitemid 26229860)
64. García-Ojeda, P. A., Hardy, S., Kozlowski, S., Stein, K. E., and Feavers, I. M. (2004) Surface plasmon resonance analysis of antipolysaccharide antibody specificity: responses to meningococcal group C conjugate vaccines and bacteria. Infect. Immun. 72, 3451-3460 (Pubitemid 38697771)
65. Bogart, J. A., and Govindan, R. (2006) A randomized phase II study of radiation therapy, pemetrexed, and carboplatin with or without Cetuximab in stage III non-small-cell lung cancer. Clin. Lung Cancer 7, 285-287 (Pubitemid 43280035)
66. Van Cutsem, E., Köhne, C. H., Hitre, E., Zaluski, J., Chang Chien, C. R., Makhson, A., D'Haens, G., Pintér, T., Lim, R., Bodoky, G., Roh, J. K., Folprecht, G., Ruff, P., Stroh, C., Tejpar, S., Schlichting, M., Nippgen, J., and Rougier, P. (2009) Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N. Engl. J. Med. 360, 1408-1417
67. Qian, J., Liu, T., Yang, L., Daus, A., Crowley, R., and Zhou, Q. (2007) Structural characterization of N-linked oligosaccharides on monoclonal antibody Cetuximab by the combination of orthogonal matrix-assisted laser desorption/ionization hybrid quadrupole-quadrupole time-of-flight tandem mass spectrometry and sequential enzymatic digestion. Anal. Biochem. 364, 8-18 (Pubitemid 46497948)
68. Patel, T. P., Parekh, R. B., Moellering, B. J., and Prior, C. P. (1992) Different culture methods lead to differences in glycosylation of a murine IgG monoclonal-antibody. Biochem. J. 285, 839-845
69. Sheeley, D. M., Merrill, B. M., and Taylor, L. C. (1997) Characterization of monoclonal antibody glycosylation: comparison of expression systems and identification of terminal α-linked galactose. Anal. Biochem. 247, 102-110 (Pubitemid 27161500)
70. Borrebaeck, C. K., Malmborg, A. C., and Ohlin, M. (1993) Does endogenous glycosylation prevent the use of mouse monoclonal-antibodies as cancer therapeutics. Immunol. Today 14, 477-479
71. Leibiger, H., Wüstner, D., Stigler, R. D., and Marx, U. (1999) Variable domain-linked oligosaccharides of a human monoclonal IgG: structure and influence on antigen binding. Biochem. J. 338, 529-538
72. Jacquemin, M., Radcliffe, C. M., Lavend'homme, R., Wormald, M. R., Vanderelst, L., Wallays, G., Dewaele, J., Collen, D., Vermylen, J., Dwek, R. A., Saint-Remy, J. M., Rudd, P. M., and Dewerchin, M. (2006) Variable region heavy chain glycosylation determines the anticoagulant activity of a factor VIII antibody. J. Thromb. Haemost. 4, 1047-1055
73. Jacquemin, M. (2010) Variable region heavy chain glycosylation determines the anticoagulant activity of a factor VIII antibody. Haemophilia 16, 16-19
74. Heine, H.,Müller-Loennies, S., Brade, L., Lindner, B., and Brade, H. (2003) Endotoxic activity and chemical structure of lipopolysaccharides from Chlamydia trachomatis serotypes E and L-2 and Chlamydophila psittaci 6BC. Eur. J. Biochem. 270, 440-450 (Pubitemid 36177311)
75. Rund, S., Lindner, B., Brade, H., and Holst, O. (2000) Structural analysis of the lipopolysaccharide from Chlamydophila psittaci strain 6BC. Eur. J. Biochem. 267, 5717-5726
76. Harvey, D. J., Merry, A. H., Royle, L., Campbell, M. P., Dwek, R. A., and Rudd, P. M. (2009) Proposal for a standard system for drawing structural diagrams of N- and O-linked carbohydrates and related compounds. Proteomics 9, 3796-3801
77. Hellström, I., Garrigues, H. J., Garrigues, U., and Hellström, K. E. (1990) Highly tumor-reactive, internalizing, mouse monoclonal-antibodies to ley-related cell-surface antigens. Cancer Res. 50, 2183-2190