Utilizing complement evasion strategies to design complement-based antibacterial immunotherapeutics: Lessons from the pathogenic Neisseriae

Immunobiology

Volumn 221, Issue 10, 2016, Pages 1110-1123

  Ram, Sanjay ^a   Shaughnessy, Jutamas ^a   DeOliveira, Rosane B ^a   Lewis, Lisa A ^a   Gulati, Sunita ^a   Rice, Peter A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Complement; Factor H; Immunotherapeutics; Neisseria; Sialic acid

Indexed keywords

ANTIINFECTIVE AGENT; COMPLEMENT FACTOR H; CYTIDINE PHOSPHATE; GLYCAN; IMMUNOGLOBULIN FC FRAGMENT; N ACETYLNEURAMINIC ACID; NONULOSONATE; SIALIC ACID DERIVATIVE; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; COMPLEMENT; HYBRID PROTEIN; IMMUNOLOGIC FACTOR;

BACTEREMIA; COMPLEMENT ACTIVATION; COMPLEMENT EVASION; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; GONORRHEA; HAEMOPHILUS INFLUENZAE; HEMOLYSIS; IN VITRO STUDY; NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; REVIEW; ANIMAL; BACTERIAL INFECTION; BACTERIUM; CHEMISTRY; DRUG DESIGN; DRUG EFFECTS; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR MIMICRY;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; BACTERIA; BACTERIAL INFECTIONS; COMPLEMENT ACTIVATION; COMPLEMENT FACTOR H; COMPLEMENT SYSTEM PROTEINS; DRUG DESIGN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOLOGIC FACTORS; MOLECULAR MIMICRY; NEISSERIA; RECOMBINANT FUSION PROTEINS; SIALIC ACIDS;

EID: 84991218430     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2016.05.016     Document Type: Review

References (169)

1. Amdahl, H., Jarva, H., Haanpera, M., Mertsola, J., He, Q., Jokiranta, T.S., Meri, S., Interactions between Bordetella pertussis and the complement inhibitor factor H. Mol. Immunol., 48, 2011, 697.
2. Anderson, R.M., May, R.M., 1991. Infectious Diseases of Humans: Dynamics and Control Oxford Science Publications, 768.
3. Aspinall, G.O., McDonald, A.G., Pang, H., Kurjanczyk, L.A., Penner, J.L., Lipopolysaccharides of Campylobacter jejuni serotype O:19: structures of core oligosaccharide regions from the serostrain and two bacterial isolates from patients with the Guillain-Barre syndrome. Biochemistry, 33, 1994, 241.
4. Barnett, T.C., Lim, J.Y., Soderholm, A.T., Rivera-Hernandez, T., West, N.P., Walker, M.J., Host-pathogen interaction during bacterial vaccination. Curr. Opin. Immunol., 36, 2015, 1.
5. Behnsen, J., Hartmann, A., Schmaler, J., Gehrke, A., Brakhage, A.A., Zipfel, P.F., The opportunistic human pathogenic fungus Aspergillus fumigatus evades the host complement system. Infect. Immun., 76, 2008, 820.
6. Ben Nasr, A., Klimpel, G.R., Subversion of complement activation at the bacterial surface promotes serum resistance and opsonophagocytosis of Francisella tularensis. J. Leukoc. Biol., 84, 2008, 77.
7. Bernhard, S., Fleury, C., Su, Y.C., Zipfel, P.F., Koske, I., Nordstrom, T., Riesbeck, K., Outer membrane protein OlpA contributes to moraxella catarrhalis serum resistance via interaction with factor H and the alternative pathway. J. Infect. Dis. 210:8 (2014), 1306–1310.
8. Bhattacharjee, A., Oeemig, J.S., Kolodziejczyk, R., Meri, T., Kajander, T., Lehtinen, M.J., Iwai, H., Jokiranta, T.S., Goldman, A., Structural basis for complement evasion by Lyme disease pathogen Borrelia burgdorferi. J. Biol. Chem., 288, 2013, 18685.
9. Bhide, M., Bhide, K., Pulzova, L., Madar, M., Mlynarcik, P., Bencurova, E., Hresko, S., Mucha, R., Variable regions in the sushi domains 6–7 and 19–20 of factor H in animals and human lead to change in the affinity to factor H binding protein of Borrelia. J. Proteom., 75, 2012, 4520.
10. Biedzka-Sarek, M., Jarva, H., Hyytiainen, H., Meri, S., Skurnik, M., Characterization of complement factor H binding to Yersinia enterocolitica serotype O:3. Infect. Immun., 76, 2008, 4100.
11. Blacklow, R.S., Warren, L., Biosynthesis of sialic acids by Neisseria meningitidis. J. Biol. Chem., 237, 1962, 3520.
12. Blaum, B.S., Hannan, J.P., Herbert, A.P., Kavanagh, D., Uhrin, D., Stehle, T., Structural basis for sialic acid-mediated self-recognition by complement factor H. Nat. Chem. Biol., 11, 2015, 77.
13. Borrow, R., Carlone, G.M., Rosenstein, N., Blake, M., Feavers, I., Martin, D., Zollinger, W., Robbins, J., Aaberge, I., Granoff, D.M., Miller, E., Plikaytis, B., van Alphen, L., Poolman, J., Rappuoli, R., Danzig, L., Hackell, J., Danve, B., Caulfield, M., Lambert, S., Stephens, D., Neisseria meningitidis group B correlates of protection and assay standardization—international meeting report emory university, Atlanta, Georgia, United States, 16–17 march 2005. Vaccine, 24, 2006, 5093.
14. CDC, Antibiotic resistance threats in the United States, 2013, department of health and human services. Cent. Dis. Control Prev., 2013.
15. Carreno, M.P., Labarre, D., Maillet, F., Jozefowicz, M., Kazatchkine, M.D., Regulation of the human alternative complement pathway: formation of a ternary complex between factor H, surface-bound C3b and chemical groups on nonactivating surfaces. Eur. J. Immunol., 19, 1989, 2145.
16. Castiblanco-Valencia, M.M., Fraga, T.R., Silva, L.B., Monaris, D., Abreu, P.A., Strobel, S., Jozsi, M., Isaac, L., Barbosa, A.S., Leptospiral immunoglobulin-like proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP. J. Infect. Dis., 205, 2012, 995.
17. Chava, A.K., Chatterjee, M., Sharma, V., Sundar, S., Mandal, C., Variable degree of alternative complement pathway-mediated hemolysis in Indian visceral leishmaniasis induced by differential expression of 9-O-acetylated sialoglycans. J. Infect. Dis., 189, 2004, 1257.
18. Chung, K.M., Liszewski, M.K., Nybakken, G., Davis, A.E., Townsend, R.R., Fremont, D.H., Atkinson, J.P., Diamond, M.S., West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proc. Natl. Acad. Sci. U. S. A., 103, 2006, 19111.
19. Cress, B.F., Englaender, J.A., He, W., Kasper, D., Linhardt, R.J., Koffas, M.A., Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules. FEMS Microbiol. Rev., 38, 2014, 660.
20. de la Paz, H., Cooke, S.J., Heckels, J.E., Effect of sialylation of lipopolysaccharide of Neisseria gonorrhoeae on recognition and complement-mediated killing by monoclonal antibodies directed against different outer-membrane antigens. Microbiology, 141, 1995, 913.
21. Devyatyarova-Johnson, M., Rees, I.H., Robertson, B.D., Turner, M.W., Klein, N.J., Jack, D.L., The lipopolysaccharide structures of Salmonella enterica serovar Typhimurium and Neisseria gonorrhoeae determine the attachment of human mannose-binding lectin to intact organisms. Infect. Immun., 68, 2000, 3894.
22. Dave, S., Pangburn, M.K., Pruitt, C., McDaniel, L.S., Interaction of human factor H with PspC of Streptococcus pneumoniae. Indian J. Med. Res., 119(Suppl), 2004, 66.
23. de Cordoba, S.R., de Jorge, E.G., Translational mini-review series on complement factor H: genetics and disease associations of human complement factor H. Clin. Exp. Immunol., 151, 2008, 1.
24. de Cordoba, S.R., Tortajada, A., Harris, C.L., Morgan, B.P., Complement dysregulation and disease: from genes and proteins to diagnostics and drugs. Immunobiology, 217, 2012, 1034.
25. Degn, S.E., Thiel, S., Humoral pattern recognition and the complement system. Scand. J. Immunol., 78, 2013, 181.
26. Delmas, Y., Vendrely, B., Clouzeau, B., Bachir, H., Bui, H.N., Lacraz, A., Helou, S., Bordes, C., Reffet, A., Llanas, B., Skopinski, S., Rolland, P., Gruson, D., Combe, C., Outbreak of Escherichia coli O104:H4 haemolytic uraemic syndrome in France: outcome with eculizumab. Nephrol. Dial. Transplant., 29, 2014, 565.
27. Dinh, A., Anathasayanan, A., Rubin, L.M., Safe and effective use of eculizumab in the treatment of severe Shiga toxin Escherichia coli-associated hemolytic uremic syndrome. Am. J. Health Syst. Pharm., 72, 2015, 117.
28. Duthy, T.G., Ormsby, R.J., Giannakis, E., Ogunniyi, A.D., Stroeher, U.H., Paton, J.C., Gordon, D.L., The human complement regulator factor H binds pneumococcal surface protein PspC via short consensus repeats 13–15. Infect. Immun., 70, 2002, 5604.
29. Edwards, A.O., Ritter, R. 3rd, Abel, K.J., Manning, A., Panhuysen, C., Farrer, L.A., Complement factor H polymorphism and age-related macular degeneration. Science, 308, 2005, 421.
30. Elkins, C., Carbonetti, N.H., Varela, V.A., Stirewalt, D., Klapper, D.G., Sparling, P.F., Antibodies to N-terminal peptides of gonococcal porin are bactericidal when gonococcal lipopolysaccharide is not sialylated. Mol. Microbiol., 6, 1992, 2617.
31. Emond, J.P., Dublanchet, A., Goldner, M., Kinetics of conversion of Neisseria gonorrhoeae to resistance to complement by cytidine 5'-monophospho-N-acetyl neuraminic acid. Antonie Van Leeuwenhoek, 67, 1995, 281.
32. Esparza-Gordillo, J., Goicoechea de Jorge, E., Buil, A., Carreras Berges, L., Lopez-Trascasa, M., Sanchez-Corral, P., Rodriguez de Cordoba, S., Predisposition to atypical hemolytic uremic syndrome involves the concurrence of different susceptibility alleles in the regulators of complement activation gene cluster in 1q32. Hum. Mol. Genet., 14, 2005, 703.
33. Esparza-Gordillo, J., Jorge, E.G., Garrido, C.A., Carreras, L., Lopez-Trascasa, M., Sanchez-Corral, P., de Cordoba, S.R., Insights into hemolytic uremic syndrome: segregation of three independent predisposition factors in a large, multiple affected pedigree. Mol. Immunol., 43, 2006, 1769.
34. Fearon, D.T., Regulation by membrane sialic acid of beta1H-dependent decay- dissociation of amplification C3 convertase of the alternative complement pathway. Proc. Natl. Acad. Sci. U. S. A., 75, 1978, 1971.
35. Ferreira, V.P., Herbert, A.P., Cortes, C., McKee, K.A., Blaum, B.S., Esswein, S.T., Uhrin, D., Barlow, P.N., Pangburn, M.K., Kavanagh, D., The binding of factor H to a complex of physiological polyanions and C3b on cells is impaired in atypical hemolytic uremic syndrome. J. Immunol., 182, 2009, 7009.
36. Figueroa, J.E., Densen, P., Infectious diseases associated with complement deficiencies. Clin. Microbiol. Rev., 4, 1991, 359.
37. Figueroa, J., Andreoni, J., Densen, P., Complement deficiency states and meningococcal disease. Immunol. Res., 12, 1993, 295.
38. Fleury, C., Su, Y.C., Hallstrom, T., Sandblad, L., Zipfel, P.F., Riesbeck, K., Identification of a Haemophilus influenzae factor H-binding lipoprotein involved in serum resistance. J. Immunol., 192, 2014, 5913.
39. Fremeaux-Bacchi, V., Miller, E.C., Liszewski, M.K., Strain, L., Blouin, J., Brown, A.L., Moghal, N., Kaplan, B.S., Weiss, R.A., Lhotta, K., Kapur, G., Mattoo, T., Nivet, H., Wong, W., Gie, S., Hurault de Ligny, B., Fischbach, M., Gupta, R., Hauhart, R., Meunier, V., Loirat, C., Dragon-Durey, M.A., Fridman, W.H., Janssen, B.J., Goodship, T.H., Atkinson, J.P., Mutations in complement C3 predispose to development of atypical hemolytic uremic syndrome. Blood, 112, 2008, 4948.
40. Friberg, N., Carlson, P., Kentala, E., Mattila, P.S., Kuusela, P., Meri, S., Jarva, H., Factor H binding as a complement evasion mechanism for an anaerobic pathogen, Fusobacterium necrophorum. J. Immunol., 181, 2008, 8624.
41. Fries, L.F., Gaither, T.A., Hammer, C.H., Frank, M.M., C3b covalently bound to IgG demonstrates a reduced rate of inactivation by factors H and I. J. Exp. Med., 160, 1984, 1640.
42. Frosch, M., Weisgerber, C., Meyer, T.F., Molecular characterization and expression in Escherichia coli of the gene complex encoding the polysaccharide capsule of Neisseria meningitidis group B. Proc. Natl. Acad. Sci. U. S. A., 86, 1989, 1669.
43. Garnett, G.P., Anderson, R.M., Sexually transmitted diseases and sexual behavior: insights from mathematical models. J. Infect. Dis., 174(Suppl. 2), 1996, S150.
44. Giuntini, S., Pajon, R., Ram, S., Granoff, D.M., Binding of complement factor H to PorB3 and NspA enhances resistance of Neisseria meningitidis to anti-factor H binding protein bactericidal activity. Infect. Immun., 83, 2015, 1536.
45. Gulati, S., McQuillen, D.P., Mandrell, R.E., Jani, D.B., Rice, P.A., Immunogenicity of Neisseria gonorrhoeae lipooligosaccharide epitope 2C7, widely expressed in vivo with no immunochemical similarity to human glycosphingolipids. J. Infect. Dis., 174, 1996, 1223 [published erratum appears in J Infect Dis 1997 Apr;175(4):1027].
46. Gulati, S., Sastry, K., Jensenius, J.C., Rice, P.A., Ram, S., Regulation of the Mannan-binding lectin pathway of complement on Neisseria gonorrhoeae by C1-inhibitor and alpha(2)-macroglobulin. J. Immunol., 168, 2002, 4078.
47. Gulati, S., Cox, A., Lewis, L.A., Michael, F.S., Li, J., Boden, R., Ram, S., Rice, P.A., Enhanced factor H binding to sialylated Gonococci is restricted to the sialylated lacto-N-neotetraose lipooligosaccharide species: implications for serum resistance and evidence for a bifunctional lipooligosaccharide sialyltransferase in Gonococci. Infect. Immun., 73, 2005, 7390.
48. Gulati, S., Agarwal, S., Vasudhev, S., Rice, P.A., Ram, S., Properdin is critical for antibody-dependent bactericidal activity against Neisseria gonorrhoeae that recruit C4b-binding protein. J. Immunol., 188, 2012, 3416.
49. Gulati, S., Zheng, B., Reed, G.W., Su, X., Cox, A.D., St Michael, F., Stupak, J., Lewis, L.A., Ram, S., Rice, P.A., Immunization against a saccharide epitope accelerates clearance of experimental Gonococcal infection. PLoS Pathog., 9, 2013, e1003559.
50. Gulati, S., Schoenhofen, I.C., Whitfield, D.M., Cox, A.D., Li, J., St Michael, F., Vinogradov, E.V., Stupak, J., Zheng, B., Ohnishi, M., Unemo, M., Lewis, L.A., Taylor, R.E., Landig, C.S., Diaz, S., Reed, G.W., Varki, A., Rice, P.A., Ram, S., Utilizing CMP-sialic acid analogs to unravel Neisseria gonorrhoeae lipooligosaccharide-mediated complement resistance and design novel therapeutics. PLoS Pathog., 11, 2015, e1005290.
51. Haines, J.L., Hauser, M.A., Schmidt, S., Scott, W.K., Olson, L.M., Gallins, P., Spencer, K.L., Kwan, S.Y., Noureddine, M., Gilbert, J.R., Schnetz-Boutaud, N., Agarwal, A., Postel, E.A., Pericak-Vance, M.A., Complement factor H variant increases the risk of age-related macular degeneration. Science, 308, 2005, 419.
52. Hajishengallis, G., Maekawa, T., Abe, T., Hajishengallis, E., Lambris, J.D., Complement involvement in periodontitis: molecular mechanisms and rational therapeutic approaches. Adv. Exp. Med. Biol., 865, 2015, 57.
53. Hallstrom, T., Zipfel, P.F., Blom, A.M., Lauer, N., Forsgren, A., Riesbeck, K., Haemophilus influenzae interacts with the human complement inhibitor factor H. J. Immunol., 181, 2008, 537.
54. Hallstrom, T., Morgelin, M., Barthel, D., Raguse, M., Kunert, A., Hoffmann, R., Skerka, C., Zipfel, P.F., Dihydrolipoamide dehydrogenase of Pseudomonas aeruginosa is a surface-exposed immune evasion protein that binds three members of the factor H family and plasminogen. J. Immunol., 189, 2012, 4939.
55. Hammerschmidt, S., Agarwal, V., Kunert, A., Haelbich, S., Skerka, C., Zipfel, P.F., The host immune regulator factor H interacts via two contact sites with the PspC protein of Streptococcus pneumoniae and mediates adhesion to host epithelial cells. J. Immunol., 178, 2007, 5848.
56. Hellwage, J., Meri, T., Heikkila, T., Alitalo, A., Panelius, J., Lahdenne, P., Seppala, I.J., Meri, S., The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem., 276, 2001, 8427.
57. Hill, D.J., Griffiths, N.J., Borodina, E., Virji, M., Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin. Sci. (Lond.), 118, 2010, 547.
58. Ho, D.K., Jarva, H., Meri, S., Human complement factor H binds to outer membrane protein Rck of Salmonella. J. Immunol., 185, 2010, 1763.
59. Ho, D.K., Riva, R., Skurnik, M., Meri, S., The Yersinia pseudotuberculosis outer membrane protein Ail recruits the human complement regulatory protein factor H. J. Immunol., 189, 2012, 3593.
60. Hofer, J., Giner, T., Jozsi, M., Complement factor H-antibody-associated hemolytic uremic syndrome: pathogenesis, clinical presentation, and treatment. Semin. Thromb. Hemost., 40, 2014, 431.
61. Hong, S., Beja-Glasser, V.F., Nfonoyim, B.M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K.M., Shi, Q., Rosenthal, A., Barres, B.A., Lemere, C.A., Selkoe, D.J., Stevens, B., Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science 352:6286 (2016), 712–716.
62. Houliston, R.S., Vinogradov, E., Dzieciatkowska, M., Li, J., St Michael, F., Karwaski, M.F., Brochu, D., Jarrell, H.C., Parker, C.T., Yuki, N., Mandrell, R.E., Gilbert, M., Lipooligosaccharide of Campylobacter jejuni: similarity with multiple types of mammalian glycans beyond gangliosides. J. Biol. Chem., 286, 2011, 12361.
63. Ingwer, I., Petersen, B.H., Brooks, G., Serum bactericidal action and activation of the classic and alternate complement pathways by Neisseria gonorrhoeae. J. Lab. Clin. Med., 92, 1978, 211.
64. Inzana, T.J., Balyan, R., Howard, M.D., Decoration of Histophilus somni lipooligosaccharide with N-acetyl-5-neuraminic acid enhances bacterial binding of complement factor H and resistance to killing by serum and polymorphonuclear leukocytes. Vet. Microbiol., 161, 2012, 113.
65. Jarva, H., Janulczyk, R., Hellwage, J., Zipfel, P.F., Bjorck, L., Meri, S., Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hic protein that binds to short consensus repeats 8–11 of factor H. J. Immunol., 168, 2002, 1886.
66. Jelezarova, E., Lutz, H.U., Assembly and regulation of the complement amplification loop in blood: the role of C3b-C3b-IgG complexes. Mol. Immunol., 36, 1999, 837.
67. Jelezarova, E., Vogt, A., Lutz, H.U., Interaction of C3b(2)—IgG complexes with complement proteins properdin, factor B and factor H: implications for amplification. Biochem. J., 349, 2000, 217.
68. Jerse, A.E., Wu, H., Packiam, M., Vonck, R.A., Begum, A.A., Garvin, L.E., Estradiol-treated female mice as surrogate hosts for Neisseria gonorrhoeae genital tract infections. Front. Microbiol., 2, 2011, 107.
69. Kajander, T., Lehtinen, M.J., Hyvarinen, S., Bhattacharjee, A., Leung, E., Isenman, D.E., Meri, S., Goldman, A., Jokiranta, T.S., Dual interaction of factor H with C3d and glycosaminoglycans in host-nonhost discrimination by complement. Proc. Natl. Acad. Sci. U. S. A., 108, 2011, 2897.
70. Kamerling, J., Pneumococcal Polysaccharides: A Chemical View. 2000, Mary Ann Liebert, Inc., Larchmont, NY (81 pp.).
71. Kavanagh, D., Goodship, T., Genetics and complement in atypical HUS. Pediatr. Nephrol., 25, 2010, 2431.
72. Kazatchkine, M.D., Fearon, D.T., Silbert, J.E., Austen, K.F., Surface-associated heparin inhibits zymosan-induced activation of the human alternative complement pathway by augmenting the regulatory action of the control proteins on particle-bound C3b. J. Exp. Med., 150, 1979, 1202.
73. Kim, S.W., Choi, C.H., Moon, D.C., Jin, J.S., Lee, J.H., Shin, J.H., Kim, J.M., Lee, Y.C., Seol, S.Y., Cho, D.T., Lee, J.C., Serum resistance of Acinetobacter baumannii through the binding of factor H to outer membrane proteins. FEMS Microbiol. Lett., 301, 2009, 224.
74. Klein, R.J., Zeiss, C., Chew, E.Y., Tsai, J.Y., Sackler, R.S., Haynes, C., Henning, A.K., SanGiovanni, J.P., Mane, S.M., Mayne, S.T., Bracken, M.B., Ferris, F.L., Ott, J., Barnstable, C., Hoh, J., Complement factor H polymorphism in age-related macular degeneration. Science, 308, 2005, 385.
75. Kraiczy, P., Skerka, C., Kirschfink, M., Brade, V., Zipfel, P.F., Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and Factor H. Eur. J. Immunol., 31, 2001, 1674.
76. Kunert, A., Losse, J., Gruszin, C., Huhn, M., Kaendler, K., Mikkat, S., Volke, D., Hoffmann, R., Jokiranta, T.S., Seeberger, H., Moellmann, U., Hellwage, J., Zipfel, P.F., Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J. Immunol., 179, 2007, 2979.
77. Lapeyraque, A.L., Malina, M., Fremeaux-Bacchi, V., Boppel, T., Kirschfink, M., Oualha, M., Proulx, F., Clermont, M.J., Le Deist, F., Niaudet, P., Schaefer, F., Eculizumab in severe shiga-toxin-associated HUS. N. Engl. J. Med., 364, 2011, 2561.
78. Lewis, L.A., Ram, S., Prasad, A., Gulati, S., Getzlaff, S., Blom, A.M., Vogel, U., Rice, P.A., Defining targets for complement components C4b and C3b on the pathogenic neisseriae. Infect. Immun., 76, 2008, 339.
79. Lewis, L.A., Choudhury, B., Balthazar, J.T., Martin, L.E., Ram, S., Rice, P.A., Stephens, D.S., Carlson, R., Shafer, W.M., Phosphoethanolamine substitution of lipid A and resistance of Neisseria gonorrhoeae to cationic antimicrobial peptides and complement-mediated killing by normal human serum. Infect. Immun., 77, 2009, 1112.
80. Lewis, L.A., Ngampasutadol, J., Wallace, R., Reid, J.E., Vogel, U., Ram, S., The meningococcal vaccine candidate neisserial surface protein a (NspA) binds to factor H and enhances meningococcal resistance to complement. PLoS Pathog., 6, 2010, e1001027.
81. Lewis, L.A., Carter, M., Ram, S., The relative roles of factor H binding protein, neisserial surface protein A, and lipooligosaccharide sialylation in regulation of the alternative pathway of complement on meningococci. J. Immunol., 188, 2012, 5063.
82. Lewis, L.A., Carter, M., Burbage, J., Chaves, B., Beluchukwu, A., Gulati, S., Rice, P.A., Ram, S., 2012. The role of gonococcal Neisserial surface protein A in serum resistance and comparison of its factor H binding properties with that of its meningococcal counterpart, Wuerzburg, Germany, 389 pp.
83. Lewis, L.A., Vu, D.M., Vasudhev, S., Shaughnessy, J., Granoff, D.M., Ram, S., Factor H-dependent alternative pathway inhibition mediated by porin B contributes to virulence of Neisseria meningitidis. MBio, 4, 2013, e00339.
84. Lewis, L.A., Gulati, S., Burrowes, E., Zheng, B., Ram, S., Rice, P.A., Alpha-2,3-sialyltransferase expression level impacts the kinetics of lipooligosaccharide sialylation, complement resistance, and the ability of Neisseria gonorrhoeae to colonize the murine genital tract. MBio, 6, 2015, e02465.
85. Lipsitch, M., O'Hagan, J.J., Patterns of antigenic diversity and the mechanisms that maintain them. J. R. Soc. Interface, 4, 2007, 787.
86. Liszewski, M.K., Atkinson, J.P., Complement regulator CD46: genetic variants and disease associations. Hum. Genom., 9, 2015, 7.
87. Loirat, C., Fremeaux-Bacchi, V., Atypical hemolytic uremic syndrome. Orphanet J. Rare Dis., 6, 2011, 60.
88. Lucidarme, J., Tan, L., Exley, R.M., Findlow, J., Borrow, R., Tang, C.M., Characterization of Neisseria meningitidis isolates that do not express the virulence factor and vaccine antigen factor H binding protein. Clin. Vaccine Immunol., 18, 2011, 1002.
89. Meri, T., Jokiranta, T.S., Hellwage, J., Bialonski, A., Zipfel, P.F., Meri, S., Onchocerca volvulus microfilariae avoid complement attack by direct binding of factor H. J. Infect. Dis., 185, 2002, 1786.
90. Madico, G., Welsch, J.A., Lewis, L.A., McNaughton, A., Perlman, D.H., Costello, C.E., Ngampasutadol, J., Vogel, U., Granoff, D.M., Ram, S., The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol., 177, 2006, 501.
91. Madico, G., Ngampasutadol, J., Gulati, S., Vogel, U., Rice, P.A., Ram, S., Factor H binding and function in sialylated pathogenic neisseriae is influenced by gonococcal, but not meningococcal, porin. J. Immunol., 178, 2007, 4489.
92. Mandrell, R.E., Apicella, M.A., Lipo-oligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS. Immunobiology, 187, 1993, 382.
93. Mandrell, R.E., Griffiss, J.M., Macher, B.A., Lipooligosaccharides (LOS) of Neisseria gonorrhoeae and Neisseria meningitidis have components that are immunochemically similar to precursors of human blood group antigens. Carbohydrate sequence specificity of the mouse monoclonal antibodies that recognize crossreacting antigens on LOS and human erythrocytes. J. Exp. Med., 168, 1988, 107.
94. Mandrell, R.E., Lesse, A.J., Sugai, J.V., Shero, M., Griffiss, J.M., Cole, J.A., Parsons, N.J., Smith, H., Morse, S.A., Apicella, M.A., In vitro and in vivo modification of Neisseria gonorrhoeae lipooligosaccharide epitope structure by sialylation. J. Exp. Med., 171, 1990, 1649.
95. Mandrell, R.E., Kim, J.J., John, C.M., Gibson, B.W., Sugai, J.V., Apicella, M.A., Griffiss, J.M., Yamasaki, R., Endogenous sialylation of the lipooligosaccharides of Neisseria meningitidis. J. Bacteriol., 173, 1991, 2823.
96. Mandrell, R.E., Further antigenic similarities of Neisseria gonorrhoeae lipooligosaccharides and human glycosphingolipids. Infect. Immun., 60, 1992, 3017.
97. Maruvada, R., Prasadarao, N.V., Rubens, C.E., Acquisition of factor H by a novel surface protein on group B Streptococcus promotes complement degradation. FASEB J., 23, 2009, 3967.
98. McDowell, J.V., Lankford, J., Stamm, L., Sadlon, T., Gordon, D.L., Marconi, R.T., Demonstration of factor H-like protein 1 binding to Treponema denticola, a pathogen associated with periodontal disease in humans. Infect. Immun., 73, 2005, 7126.
99. McHarg, S., Clark, S.J., Day, A.J., Bishop, P.N., Age-related macular degeneration and the role of the complement system. Mol. Immunol., 67, 2015, 43.
100. McQuillen, D.P., Gulati, S., Ram, S., Turner, A.K., Jani, D.B., Heeren, T.C., Rice, P.A., Complement processing and immunoglobulin binding to Neisseria gonorrhoeae determined in vitro simulates in vivo effects. J. Infect. Dis., 179, 1999, 124.
101. Meri, S., Pangburn, M.K., Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc. Natl. Acad. Sci. U. S. A., 87, 1990, 3982.
102. Meri, S., Pangburn, M.K., Regulation of alternative pathway complement activation by glycosaminoglycans: specificity of the polyanion binding site on factor H. Biochem. Biophys. Res. Commun., 198, 1994, 52.
103. Meri, T., Cutler, S.J., Blom, A.M., Meri, S., Jokiranta, T.S., Relapsing fever spirochetes Borrelia recurrentis and B. duttonii acquire complement regulators C4b-binding protein and factor H. Infect. Immun., 74, 2006, 4157.
104. Meri, T., Amdahl, H., Lehtinen, M.J., Hyvarinen, S., McDowell, J.V., Bhattacharjee, A., Meri, S., Marconi, R., Goldman, A., Jokiranta, T.S., Microbes bind complement inhibitor factor H via a common site. PLoS Pathog., 9, 2013, e1003308.
105. Michalek, M.T., Mold, C., Bremer, E.G., Inhibition of the alternative pathway of human complement by structural analogues of sialic acid. J. Immunol., 140, 1988, 1588.
106. Nairn, C.A., Cole, J.A., Patel, P.V., Parsons, N.J., Fox, J.E., Smith, H., Cytidine 5'-monophospho-N-acetylneuraminic acid or a related compound is the low Mr factor from human red blood cells which induces gonococcal resistance to killing by human serum. J. Gen. Microbiol., 134, 1988, 3295.
107. Nester, C.M., Barbour, T., de Cordoba, S.R., Dragon-Durey, M.A., Fremeaux-Bacchi, V., Goodship, T.H., Kavanagh, D., Noris, M., Pickering, M., Sanchez-Corral, P., Skerka, C., Zipfel, P., Smith, R.J., Atypical aHUS: State of the art. Mol. Immunol., 67, 2015, 31.
108. Ngampasutadol, J., Ram, S., Gulati, S., Agarwal, S., Li, C., Visintin, A., Monks, B., Madico, G., Rice, P.A., Human factor H interacts selectively with Neisseria gonorrhoeae and results in species-specific complement evasion. J. Immunol., 180, 2008, 3426.
109. Nicholson-Weller, A., Spicer, D.B., Austen, K.F., Deficiency of the complement regulatory protein, decay-accelerating factor, on membranes of granulocytes, monocytes, and platelets in paroxysmal nocturnal hemoglobinuria. N. Engl. J. Med., 312, 1985, 1091.
110. Pandiripally, V., Wei, L., Skerka, C., Zipfel, P.F., Cue, D., Recruitment of complement factor H-like protein 1 promotes intracellular invasion by group A streptococci. Infect. Immun., 71, 2003, 7119.
111. Pangburn, M.K., Muller-Eberhard, H.J., Complement C3 convertase: cell surface restriction of beta1 H control and generation of restriction on neuraminidase-treated cells. Proc. Natl. Acad. Sci. U. S. A., 75, 1978, 2416.
112. Pangburn, M.K., Schreiber, R.D., Muller-Eberhard, H.J., Deficiency of an erythrocyte membrane protein with complement regulatory activity in paroxysmal nocturnal hemoglobinuria. Proc. Natl. Acad. Sci. U. S. A., 80, 1983, 5430.
113. Parsons, N.J., Patel, P.V., Tan, E.L., Andrade, J.R.C., Nairn, C.A., Goldner, M., Cole, J.A., Smith, H., Cytidine 5'-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human red blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum. Microb. Pathog., 5, 1988, 303.
114. Parsons, N.J., Andrade, J.R., Patel, P.V., Cole, J.A., Smith, H., Sialylation of lipopolysaccharide and loss of absorption of bactericidal antibody during conversion of gonococci to serum resistance by cytidine 5'-monophospho-N-acetyl neuraminic acid. Microb. Pathog., 7, 1989, 63.
115. Parsons, N.J., Ashton, P.R., Constantinidou, C., Cole, J.A., Smith, H., Identification by mass spectrometry of CMP-NANA in diffusible material released from high M(r) blood cell fractions that confers serum resistance on gonococci. Microb. Pathog., 14, 1993, 329.
116. Parsons, N.J., Constantinidou, C., Cole, J.A., Smith, H., Sialylation of lipopolysaccharide by CMP-NANA in viable gonococci is enhanced by low Mr material released from blood cell extracts but not by some UDP sugars. Microb. Pathog., 16, 1994, 413.
117. Pavliak, V., Brisson, J.R., Michon, F., Uhrin, D., Jennings, H.J., Structure of the sialylated L3 lipopolysaccharide of Neisseria meningitidis. J. Biol. Chem., 268, 1993, 14146.
118. Pian, Y., Gan, S., Wang, S., Guo, J., Wang, P., Zheng, Y., Cai, X., Jiang, Y., Yuan, Y., Fhb, a novel factor H-binding surface protein, contributes to the antiphagocytic ability and virulence of Streptococcus suis. Infect. Immun., 80, 2012, 2402.
119. Pickering, M.C., Cook, H.T., Translational mini-review series on complement factor H: renal diseases associated with complement factor H: novel insights from humans and animals. Clin. Exp. Immunol., 151, 2008, 210.
120. Poltermann, S., Kunert, A., von der Heide, M., Eck, R., Hartmann, A., Zipfel, P.F., Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem., 282, 2007, 37537.
121. Ram, S., Sharma, A.K., Simpson, S.D., Gulati, S., McQuillen, D.P., Pangburn, M.K., Rice, P.A., A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med., 187, 1998, 743.
122. Ram, S., Lewis, L.A., Rice, P.A., Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin. Microbiol. Rev., 23, 2010, 740.
123. Ram, S., Lewis, L.A., Agarwal, S., Meningococcal group W-135 and Y capsular polysaccharides paradoxically enhance activation of the alternative pathway of complement. J. Biol. Chem., 286, 2011, 8297.
124. Ray, T.D., Lewis, L.A., Gulati, S., Rice, P.A., Ram, S., Novel blocking human IgG directed against the pentapeptide repeat motifs of Neisseria meningitidis Lip/H.8 and Laz lipoproteins. J. Immunol., 186, 2011, 4881.
125. Reis, E.S., Mastellos, D.C., Yancopoulou, D., Risitano, A.M., Ricklin, D., Lambris, J.D., Applying complement therapeutics to rare diseases. Clin. Immunol., 161, 2015, 225.
126. Rice, P.A., Vayo, H., Tam, M., Blake, M.S., Immunoglobulin G antibodies directed against protein III block killing of serum-resistant Neisseria gonorrhoeae by immune serum. J. Exp. Med., 164, 1986, 1735.
127. Rodriguez de Cordoba, S., Hidalgo, M.S., Pinto, S., Tortajada, A., Genetics of atypical hemolytic uremic syndrome (aHUS). Semin. Thromb. Hemost., 40, 2014, 422.
128. Rodriguez, E., Rallapalli, P.M., Osborne, A.J., Perkins, S.J., New functional and structural insights from updated mutational databases for complement factor H factor I, membrane cofactor protein and C3. Biosci. Rep., 2014, p34.
129. Rosa, T.F., Flammersfeld, A., Ngwa, C.J., Kiesow, M., Fischer, R., Zipfel, P.F., Skerka, C., Pradel, G., The Plasmodium falciparum blood stages acquire factor h family proteins to evade destruction by human complement. Cell. Microbiol., 2015.
130. Rossmann, E., Kraiczy, P., Herzberger, P., Skerka, C., Kirschfink, M., Simon, M.M., Zipfel, P.F., Wallich, R., Dual binding specificity of a Borrelia hermsii-associated complement regulator-acquiring surface protein for factor H and plasminogen discloses a putative virulence factor of relapsing fever spirochetes. J. Immunol., 178, 2007, 7292.
131. Sahagun-Ruiz, A., Granados Martinez, A.P., Breda, L.C., Fraga, T.R., Castiblanco Valencia, M.M., Barbosa, A.S., Isaac, L., Pasteurella pneumotropica evades the human complement system by acquisition of the complement regulators factor H and C4BP. PLoS One, 9, 2014, e111194.
132. Schneider, H., Griffiss, J.M., Boslego, J.W., Hitchcock, P.J., Zahos, K.M., Apicella, M.A., Expression of paragloboside-like lipooligosaccharides may be a necessary component of gonococcal pathogenesis in men. J. Exp. Med., 174, 1991, 1601.
133. Schneider, M.C., Prosser, B.E., Caesar, J.J., Kugelberg, E., Li, S., Zhang, Q., Quoraishi, S., Lovett, J.E., Deane, J.E., Sim, R.B., Roversi, P., Johnson, S., Tang, C.M., Lea, S.M., Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature, 458, 2009, 890.
134. Schott, M., Grosskinsky, S., Brenner, C., Kraiczy, P., Wallich, R., Molecular characterization of the interaction of Borrelia parkeri and Borrelia turicatae with human complement regulators. Infect. Immun., 78, 2010, 2199.
135. Schramm, E.C., Clark, S.J., Triebwasser, M.P., Raychaudhuri, S., Seddon, J.M., Atkinson, J.P., Genetic variants in the complement system predisposing to age-related macular degeneration: a review. Mol. Immunol., 61, 2014, 118.
136. Schweinle, J.E., Hitchcock, P.J., Tenner, A.J., Hammer, C.H., Frank, M.M., Joiner, K.A., Interaction of Neisseria gonorrhoeae with classical complement components, C1-inhibitor, and a monoclonal antibody directed against the Neisserial H.8 antigen. J. Clin. Invest., 83, 1989, 397.
137. Sekar, A., Bialas, A.R., de Rivera, H., Davis, A., Hammond, T.R., Kamitaki, N., Tooley, K., Presumey, J., Baum, M., Van Doren, V., Genovese, G., Rose, S.A., Handsaker, R.E., Daly, M.J., Carroll, M.C., Stevens, B., McCarroll, S.A., Schizophrenia risk from complex variation of complement component 4. Nature, 530, 2016, 177.
138. Seling, A., Siegel, C., Fingerle, V., Jutras, B.L., Brissette, C.A., Skerka, C., Wallich, R., Zipfel, P.F., Stevenson, B., Kraiczy, P., Functional characterization of Borrelia spielmanii outer surface proteins that interact with distinct members of the human factor H protein family and with plasminogen. Infect. Immun., 78, 2010, 39.
139. Sharma, A.K., Pangburn, M.K., Localization by site-directed mutagenesis of the site in human complement factor H that binds to Streptococcus pyogenes M protein. Infect. Immun., 65, 1997, 484.
140. Sharp, J.A., Echague, C.G., Hair, P.S., Ward, M.D., Nyalwidhe, J.O., Geoghegan, J.A., Foster, T.J., Cunnion, K.M., Staphylococcus aureus surface protein SdrE binds complement regulator factor H as an immune evasion tactic. PLoS One, 7, 2012, e38407.
141. Shaughnessy, J., Lewis, L.A., Jarva, H., Ram, S., Functional comparison of the binding of factor H short consensus repeat 6 (SCR 6) to factor H binding protein from Neisseria meningitidis and the binding of factor H SCR 18–20 to Neisseria gonorrhoeae porin. Infect. Immun., 77, 2009, 2094.
142. Shaughnessy, J., Ram, S., Bhattacharjee, A., Pedrosa, J., Tran, C., Horvath, G., Monks, B., Visintin, A., Jokiranta, T.S., Rice, P.A., Molecular characterization of the interaction between sialylated Neisseria gonorrhoeae and factor H. J. Biol. Chem., 286, 2011, 22235.
143. Shaughnessy, J., Vu, D.M., Punjabi, R., Serra-Pladevall, J., DeOliveira, R.B., Granoff, D.M., Ram, S., Fusion protein comprising factor H domains 6 and 7 and human IgG1 Fc as an antibacterial immunotherapeutic. Clin. Vaccine Immunol., 21, 2014, 1452.
144. Shaughnessy, J., Gulati, S., Agarwal, S., Unemo, M., Ohnishi, M., Su, X.H., Monks, B.G., Visintin, A., Madico, G., Lewis, L.A., Golenbock, D.T., Reed, G.W., Rice, P.A., Ram, S., A novel factor H-Fc chimeric immunotherapeutic molecule against Neisseria gonorrhoeae. J. Immunol., 196, 2016, 1732.
145. Simon, N., Lasonder, E., Scheuermayer, M., Kuehn, A., Tews, S., Fischer, R., Zipfel, P.F., Skerka, C., Pradel, G., Malaria parasites co-opt human factor H to prevent complement-mediated lysis in the mosquito midgut. Cell Host Microbe, 13, 2013, 29.
146. Smith, H., Cole, J.A., Parsons, N.J., The sialylation of gonococcal lipopolysaccharide by host factors: a major impact on pathogenicity. FEMS Microbiol. Lett., 79, 1992, 287.
147. Steele, N.P., Munson, R.S. Jr., Granoff, D.M., Cummins, J.E., Levine, R.P., Antibody-dependent alternative pathway killing of Haemophilus influenzae type b. Infect. Immun., 44, 1984, 452.
148. Stoiber, H., Ebenbichler, C., Schneider, R., Janatova, J., Dierich, M.P., Interaction of several complement proteins with gp120 and gp41, the two envelope glycoproteins of HIV-1. AIDS, 9, 1995, 19.
149. Swartley, J.S., Marfin, A.A., Edupuganti, S., Liu, L.J., Cieslak, P., Perkins, B., Wenger, J.D., Stephens, D.S., Capsule switching of Neisseria meningitidis. Proc. Natl. Acad. Sci. U. S. A., 94, 1997, 271.
150. Tarr, P.I., Hosea, S.W., Brown, E.J., Schneerson, R., Sutton, A., Frank, M.M., The requirement of specific anticapsular IgG for killing of Haemophilus influenzae by the alternative pathway of complement activation. J. Immunol., 128, 1982, 1772.
151. Telford, J.L., Bacterial genome variability and its impact on vaccine design. Cell Host Microbe, 3, 2008, 408.
152. Thiel, S., Gadjeva, M., Humoral pattern recognition molecules: Mannan-binding lectin and ficolins. Adv. Exp. Med. Biol., 653, 2009, 58.
153. Thurman, J.M., Holers, V.M., The central role of the alternative complement pathway in human disease. J. Immunol., 176, 2006, 1305.
154. Tsai, C.M., Civin, C.I., Eight lipooligosaccharides of Neisseria meningitidis react with a monoclonal antibody which binds lacto-N-neotetraose (Gal beta 1–4GlcNAc beta 1–3 Gal beta 1–4Glc). Infect. Immun., 59, 1991, 3604.
155. Unemo, M., Shafer, W.M., Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin. Microbiol. Rev., 27, 2014, 587.
156. Varki, A., Kornfeld, S., An autosomal dominant gene regulates the extent of 9-O-acetylation of murine erythrocyte sialic acids. A probable explanation for the variation in capacity to activate the human alternate complement pathway. J. Exp. Med., 152, 1980, 532.
157. van Alphen, L., van den Dobbelsteen, G., Meningococcal B vaccine development and evaluation of efficacy. Hum. Vaccin, 4, 2008, 158.
158. Wakarchuk, W.W., Gilbert, M., Martin, A., Wu, Y., Brisson, J.R., Thibault, P., Richards, J.C., Structure of an alpha-2,6-sialylated lipooligosaccharide from Neisseria meningitidis immunotype L1. Eur. J. Biochem., 254, 1998, 626.
159. Wallich, R., Pattathu, J., Kitiratschky, V., Brenner, C., Zipfel, P.F., Brade, V., Simon, M.M., Kraiczy, P., Identification and functional characterization of complement regulator-acquiring surface protein 1 of the Lyme disease spirochetes Borrelia afzelii and Borrelia garinii. Infect. Immun., 73, 2005, 2351.
160. Ward, M.E., Watt, P.J., Glynn, A.A., Gonococci in urethral exudates possess a virulence factor lost on subculture. Nature, 227, 1970, 382.
161. Warren, L., Blacklow, R.S., The biosynthesis of cytidine 5'-monophospho-n-acetylneuraminic acid by an enzyme from Neisseria meningitidis. J. Biol. Chem., 237, 1962, 3527.
162. Watson, D.C., Wakarchuk, W.W., Gervais, C., Durocher, Y., Robotham, A., Fernandes, S.M., Schnaar, R.L., Young, N.M., Gilbert, M., Preparation of legionaminic acid analogs of sialo-glycoconjugates by means of mammalian sialyltransferases. Glycoconj. J., 32, 2015, 729.
163. Weismann, D., Hartvigsen, K., Lauer, N., Bennett, K.L., Scholl, H.P., Charbel Issa, P., Cano, M., Brandstatter, H., Tsimikas, S., Skerka, C., Superti-Furga, G., Handa, J.T., Zipfel, P.F., Witztum, J.L., Binder, C.J., Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature, 478, 2011, 76.
164. Wetzler, L.M., Barry, K., Blake, M.S., Gotschlich, E.C., Gonococcal lipooligosaccharide sialylation prevents complement- dependent killing by immune sera. Infect. Immun., 60, 1992, 39.
165. Wong, S.M., Shaughnessy, J., Ram, S., Akerley, B.J., Defining the binding region in factor H to develop a therapeutic factor H-Fc fusion protein against nontypeable Haemophilus influenzae. Front. Cell. Infect. Microbiol., 2016.
166. Wu, H., Jerse, A.E., Alpha-2,3-sialyltransferase enhances Neisseria gonorrhoeae survival during experimental murine genital tract infection. Infect. Immun., 74, 2006, 4094.
167. Yuki, N., Taki, T., Inagaki, F., Kasama, T., Takahashi, M., Saito, K., Handa, S., Miyatake, T., A bacterium lipopolysaccharide that elicits Guillain-Barre syndrome has a GM1 ganglioside-like structure. J. Exp. Med., 178, 1993, 1771.
168. Yuki, N., Susuki, K., Koga, M., Nishimoto, Y., Odaka, M., Hirata, K., Taguchi, K., Miyatake, T., Furukawa, K., Kobata, T., Yamada, M., Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain-Barre syndrome. Proc. Natl. Acad. Sci. U. S. A., 101, 2004, 11404.
169. Zaleski, A., Densen, P., Sialylation of LOS Inhibits Gonococcal Killing Primarily Through an Effect on Classical Pathway Activation. 1996, National Institutes of Health Baltimore, MD (114 pp.).