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Roles of Carbohydrates in the Interaction of Pathogens with Neural Cells

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Glycobiology of the Nervous System

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 9))

Abstract

Numerous pathogens that can affect neural function utilize oligosaccharide–protein interactions as a first step in the infection process. The variability in carbohydrate structures as well as the presence of carbohydrate binding receptors on the surface of cells provides a plethora of potential binding sites for viruses, bacteria, and bacterial toxins. This chapter discusses scenarios for how carbohydrates may affect the ability of infectious agents to interact with neural cells, provides examples of problems that may result from development of antibodies to carbohydrate antigens found on pathogens that are similar to epitopes expressed on mammalian cells, and presents approaches either in use or under consideration for translational uses of this information.

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Abbreviations

BBB:

Blood–brain barrier

Bgp:

Borrelia GAG-binding protein

BoNT:

Botulinum neurotoxin

CaMKII:

Ca2+/calmodulin-dependent kinase II

CNS:

Central nervous system

CTx:

Cholera toxin

DC-SIGN:

Dendritic cell-specific intercellular molecule-grabbing nonintegrin

GABA:

Gamma-aminobutyric acid

GAG:

Glycosaminoglycan

Gb3:

Globotriaosylceramide

GBS:

Guillain–Barre syndrome

GSL:

Glycosphingolipid

H:

Hemagglutinin

HIV:

Human immunodeficiency virus

Iv:

Intravenous

MßCD:

Methyl-ß-cyclodextrin

SNAP-25:

Synaptic vesicle-associated protein with a mass of 25 kilodaltons

SV2:

Synaptic vesicle glycoprotein 2

TeNT:

Tetanus neurotoxin

TNFα:

Tumor necrosis factor-alpha

TTC:

Carboxyl terminal half of the heavy chain of tetanus toxin

VAMP-1-2:

Vesicle-associated membrane protein-1-2 or synaptobrevin-1 and -2

References

  • Albright AV, Shieh JT, Itoh T, Lee B, Pleasure D, O’Connor MJ. Microglia express CCR5, CXCR4, and CCR3, but of these, CCR5 is the principal coreceptor for human immunodeficiency virus type 1 dementia isolates. J Virol. 1999;73:205–13.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Backenson PB, Coleman JL, Benach JL. Borrelia burgdorferi shows specificity of binding to glycosphingolipids. Infect Immun. 1995;63:2811–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Banks WA, Freed EO, Wolf KM, Robinson SM, Franko M, Kumar VB. Transport of human immunodeficiency virus type 1 pseudoviruses across the blood-brain barrier: role of envelope proteins and adsorptive endocytosis. J Virol. 2001;75:4681–91.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bao H, Jin X, Li L, Lv F, Liu T. OX26 modified hyperbranched polyglycerol-conjugated poly(lactic-co-glycolic acid) nanoparticles: synthesis, characterization and evaluation of its brain delivery ability. J Mater Sci Mater Med. 2012;23:1891–901.

    Article  CAS  PubMed  Google Scholar 

  • Barrientos LG, O'Keefe BR, Bray M, Sanchez A, Gronenborn AM, Boyd MR. Cyanovirin-N binds to the viral surface glycoprotein, GP1,2 and inhibits infectivity of Ebola virus. Antiviral Res. 2003;58:47–56.

    Article  CAS  PubMed  Google Scholar 

  • Bercsenyi K, Giribaldi F, Schiavo G. The elusive compass of Clostridial neurotoxins: deciding when and where to go? In: Rummel A, Binz T, editors. Botulinum Neurotoxins, Curr Top Microbiol Immunol. 2013;364:91–113.

    Google Scholar 

  • Boyle MJ, Richards JS, Gilson PR, Chai W, Beeson JG. Interactions with heparin-like molecules during erythrocyte invasion by Plasmodium falciparum merozoites. Blood. 2010;115:4559–68.

    Article  CAS  PubMed  Google Scholar 

  • Brown DA, London E. Structure and function of sphongolipid- and cholesterol-rich membrane rafts. J Biol Chem. 2000;275:17221–4.

    Article  CAS  PubMed  Google Scholar 

  • Brudner M, Karpel M, Lear C, Chen L, Yantosca LM, Scully C, et al. Lectin-dependent enhancement of Ebola virus infection via soluble and transmembrane C-type lectin receptors. PLoS One. 2013;8:e60838. doi:10.1371/journal.pone.0060838. Epub 2013 Apr 2.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bullens RW, O'Hanlon GM, Wagner E, Molenaar PC, Furukawa K, Furukawa K, et al. Roles of complex gangliosides at the neuromuscular junction. Ann N Y Acad Sci. 2003;998:401–3.

    Article  CAS  PubMed  Google Scholar 

  • Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP. Lyme disease-a tick-borne spirochetosis? Science. 1982;216:1317–9.

    Article  CAS  PubMed  Google Scholar 

  • Calvo AC, Zaragoza P, Osta R. Gene therapy based on fragment C of tetanus toxin in ALS: a promising neuroprotective strategy for the bench to the bedside. Gene therapy—tools and potential applications. 2013; pp. 249–68. DOI: 10.5772/52896.

  • Chaddock J. Transforming the domain structure of botulinum neurotoxins into novel therapeutics. Curr Top Microbiol Immunol. 2013;364:287–306.

    PubMed  Google Scholar 

  • Champion E, André I, Moulis C, Boutet J, Descroix K, Morel S, et al. Design of alpha-transglucosidases of controlled specificity for programmed chemoenzymatic synthesis of antigenic oligosaccharides. J Am Chem Soc. 2009;131:7379–89.

    Article  CAS  PubMed  Google Scholar 

  • Chang YC, Stins MF, McCaffery MJ, Miller GF, Pare DR, Dam T, et al. Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Infect Immun. 2004;72:4985–95.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Corasaniti MT, Maccarrone M, Nistico R, Malorni W, Rotiroti D, Bagetta G. Exploitation of the HIV-1 coat glycoprotein, gp120, in neurodegenerative studies in vivo. J Neurochem. 2001;79:1–8.

    Article  CAS  PubMed  Google Scholar 

  • Cunningham MW. Streptococcus and rheumatic fever. Curr Opin Rheumatol. 2012;24:408–16.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cupelli K, Stehle T. Viral attachment strategies: the many faces of adenoviruses. Curr Opin Virol. 2011;1:84–91.

    Article  CAS  PubMed  Google Scholar 

  • Davis CW, Nguyen HY, Hanna SL, Sánchez MD, Doms RW, Pierson TC. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol. 2006;80:1290–301.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Denizot M, Neal JW, Gasque P. Encephalitis due to emerging viruses: CNS innate immunity and potential therapeutic targets. J Infect. 2012;65:1–16.

    Google Scholar 

  • Disson O, Lecuit M. Targeting of the central nervous system by Listeria monocytogenes. Virulence. 2012;3:213–21.

    Article  PubMed Central  PubMed  Google Scholar 

  • Dong M, Yeh F, Tepp WH, Dean C, Johnson EA, Janz R, et al. SV2 is the protein receptor for botulinum neurotoxin A. Science. 2006;312:592–6.

    Article  CAS  PubMed  Google Scholar 

  • Dong M, Tepp WH, Liu H, Johnson EA, Chapman ER. Mechanism of botulinum B and G entry into hippocampal neurons. J Cell Biol. 2007;179:1511–22.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dong M, Liu H, Tepp WH, Johnson EA, Janz R, Chapman ER. Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol Biol Cell. 2008;19:5226–37.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dover N, Barash JR, Hill KK, Xie G, Arnon SS. Molecular characterization of a novel botulinum neurotoxin type H gene. J Infect Dis. 2014;209:192–202.

    Google Scholar 

  • Fischer JR, LeBlanc KT, Leong JM. Fibronectin binding protein BBK32 of the Lyme disease spirochete promotes bacterial attachment to glycosaminoglycans. Infect Immun. 2006;74:435–41.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fuchs A, Lin TY, Beasley DW, Stover CM, Schwaeble WJ, Pierson TC, et al. Direct complement restriction of flavivirus infection requires glycan recognition by mannose-binding lectin. Cell Host Microbe. 2010;8:186–95.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fujii J, Kinoshita Y, Yamada Y, Yutsudo T, Kita T, Takeda T, et al. Neurotoxicity of intrathecal Shiga toxin 2 and protection by intrathecal injection of anti-Shiga toxin 2 antiserum in rabbits. Microb Pathog. 1998;25:139–46.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Monco JC, Fernandez-Villar B, Rogers RC, Szczepanski A, Wheeler CM, Benach JL. Borrelia burgdorferi and other related spirochetes bind to galactocerebroside. Neurology. 1992;42:1341–8.

    Article  CAS  PubMed  Google Scholar 

  • Gil C, Soler-Jover A, Blasi J, Aguilera J. Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes. Biochem Biophys Res Commun. 2005;329:117–24.

    Article  CAS  PubMed  Google Scholar 

  • Goldmann C, Petry H, Frye S, Ast O, Ebitsch S, Jentsch KD, et al. Molecular cloning and expression of major structural protein VP1 of the human polyomavirus JC virus: formation of virus-like particles useful for immunological and therapeutic studies. J Virol. 1999;73:4465–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Habermann E, Dreyer F. Clostridial neurotoxins: handling and action at the cellular and molecular level. Curr Top Microbiol Immunol. 1986;129:93–179.

    CAS  PubMed  Google Scholar 

  • Hallett M, Albanese A, Dressler D, Segal KR, Simpson DM, Truong D, et al. Evidence-based review and assessment of botulinum neurotoxin for the treatment of movement disorders. Toxicon. 2013;67:94–114.

    Article  CAS  PubMed  Google Scholar 

  • Halperin JJ, Shapiro ED, Logigian E, Belman AL, Dotevall L, Wormser GP, et al. Practice parameter: treatment of nervous system Lyme disease (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2007;69:91–102.

    Article  CAS  PubMed  Google Scholar 

  • Hamano S, Nakanishi Y, Nara T, Seki T, Ohtani T, Oishi T, et al. Neurological manifestations of hemorrhagic colitis in the outbreak of Escherichia coli O157:H7 infection in Japan. Acta Paediatr. 1993;82:454–8.

    Article  CAS  PubMed  Google Scholar 

  • Hanashima T, Miyake M, Yahiro K, Iwamaru Y, Ando A, Morinaga N, et al. Effect of Gb3 in lipid rafts in resistance to Shiga-like toxin of mutant Vero cells. Microb Pathog. 2008;45:124–33.

    Article  CAS  PubMed  Google Scholar 

  • Harouse JM, Bhat S, Spitalnik SL, Laughlin M, Stefano K, Silberberg DH, et al. Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide. Science. 1991;253:320–3.

    Article  CAS  PubMed  Google Scholar 

  • Harouse JM, Collman RG, González-Scarano F. Human immunodeficiency virus type 1 infection of SK-N-MC cells: domains of gp120 involved in entry into a CD4-negative, galactosyl ceramide/3′ sulfo-galactosyl ceramide-positive cell line. J Virol. 1995;69:7383–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Herreros J, Lalli G, Montecucco C, Schiavo G. Tetanus toxin fragment C binds to a protein present in neuronal cell lines and motoneurons. J Neurochem. 2000;74:1941–50.

    Article  CAS  PubMed  Google Scholar 

  • Horwacik I, KurciÅ„ski M, Bzowska M, Kowalczyk AK, Czaplicki D, KoliÅ„ski A, et al. Analysis and optimization of interactions between peptides mimicking the GD2 ganglioside and the monoclonal antibody 14G2a. Int J Mol Med. 2011;28:47–57.

    CAS  PubMed  Google Scholar 

  • Huang SH, Long M, Wu CH, Kwon-Chung KJ, Chang YC, Chi F, Lee S, Jong A. Invasion of Cryptococcus neoformans into human brain microvascular endothelial cells is mediated through the lipid rafts-endocytic pathway via the dual specificity tyrosine phosphorylation-regulated kinase 3 (DYRK3). J Biol Chem. 2011;286:34761–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jacquet A, Haumont M, Chellun D, Massaer M, Tufaro F, Bollen A, et al. The varicella zoster virus glycoprotein B (gB) plays a role in virus binding to cell surface heparan sulfate proteoglycans. Virus Res. 1998;53:197–207.

    Article  CAS  PubMed  Google Scholar 

  • Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, et al. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A. 2009;106:14063–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaneda K, Masuzawa T, Yasugami K, Suzuki T, Suzuki Y, Yanagihara Y. Glyco sphingolipid-binding protein of Borrelia burgdorferi sensu lato. Infect Immun. 1997;65:3180–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karalewitz AP, Fu Z, Baldwin MR, Kim JJ, Barbieri JT. Botulinum neurotoxin serotype C associates with dual ganglioside receptors to facilitate cell entry. J Biol Chem. 2012;287:40806–16.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim JH, Resende R, Wennekes T, Chen HM, Bance N, Buchini S, et al. Mechanism-based covalent neuraminidase inhibitors with broad-spectrum influenza antiviral activity. Science. 2013;340:71–5.

    Article  CAS  PubMed  Google Scholar 

  • Kirvan CA, Swedo SE, Heuser S, Cunningham MW. Mimicry and autoanti-body-mediated neuronal cell signaling in Sydenham chorea. Nat Med. 2003;9:914–20.

    Article  CAS  PubMed  Google Scholar 

  • Kitov PI, Sadowska JM, Mulvey G, Armstrong GD, Ling H, Pannu NS, et al. Shiga-like toxins are neutralized by tailored multivalent carbohydrate ligands. Nature. 2000;403:669–72.

    Article  CAS  PubMed  Google Scholar 

  • Komagome R, Sawa H, Suzuki T, Suzuki Y, Tanaka S, Atwood WJ, et al. Oligosaccharides as receptors for JC virus. J Virol. 2002;76:12992–3000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kurre P, Kiem HP, Morris J, Heyward S, Battini JL, Miller AD. Efficient transduction by an amphotropic retrovirus vector is dependent on high-level expression of the cell surface virus receptor. J Virol. 1999;73:495–500.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kwon SE, Chapman ER. Glycosylation is dispensable for sorting of synaptotagmin 1 but is critical fro targeting of SV2 and synaptophysin to recycling synaptic vesicles. J Biol Chem. 2012;287:35658–68.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lasala F, Arce E, Otero JR, Rojo J, Delgado R. Mannosyl glycodendritic structure inhibits DC-SIGN-mediated Ebola virus infection in cis and in trans. Antimicrob Agents Chemother. 2003;47:3970–2.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee RT, Lee YC. Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconj J. 2000;17:543–51.

    Article  CAS  PubMed  Google Scholar 

  • Lentz TB, Gray SJ, Samulski RJ. Viral vectors for gene delivery to the central nervous system. Neurobiol Dis. 2012;48:179–88.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ling H, Boodhoo A, Hazes B, Cummings MD, Armstrong GD, Brunton JL, et al. Structure of the shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry. 1998;37:1777–88.

    Article  CAS  PubMed  Google Scholar 

  • Maccarrone M, Navarra M, Catani V, Corasaniti MT, Bagetta G, Finazzi-Agrò A. Cholesterol-dependent modulation of the toxicity of HIV-1 coat protein gp120 in human neuroblastoma cells. J Neurochem. 2002;82:1444–52.

    Article  CAS  PubMed  Google Scholar 

  • Mahrhold S, Rummel A, Bigalke H, Davletov B, Binz T. The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 2006;580:2011–4.

    Article  CAS  PubMed  Google Scholar 

  • Meena AK, Khadilkar SV, Murthy JMK. Treatment guidelines for Guillain-Barre Syndrome. Ann Indian Acad Neurol. 2011;14(1):S73–81.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merritt EA, Zhang Z, Pickens JC, Ahn M, Hol WG, Fan E. Characterization and crystal structure of a high-affinity pentavalent receptor-binding inhibitor for cholera toxin and E coli heat-labile enterotoxin. J Am Chem Soc. 2002;124:8818–24.

    Article  CAS  PubMed  Google Scholar 

  • Michelow IC, Lear C, Scully C, Prugar LI, Longley CB, Yantosca LM, et al. High-dose mannose-binding lectin therapy for Ebola virus infection. Infect Dis. 2011;203:175–9.

    Article  CAS  Google Scholar 

  • Mochalova L, Kurova V, Shtyrya Y, Korchagina E, Gambaryan A, Belyanchikov I. Oligosaccharide specificity of H1N1 virus neuraminidases. Arch Virol. 2007;152:2047–57.

    Article  CAS  PubMed  Google Scholar 

  • Muthana S, Cao H, Chen X. Recent progress in chemical and chemoenzymatic synthesis of carbohydrates. Curr Opin Chem Biol. 2009;13:573–81.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Naesens R, Ronsyn M, Druwé P, Denis O, Ieven M, Jeurissen A. Central nervous system invasion by community-acquired meticillin-resistant Staphylococcus aureus. J Med Microbiol. 2009;58:1247–51.

    Article  PubMed  Google Scholar 

  • Neu U, Bauer J, Stehle T. Viruses and sialic acids: rules of engagement. Curr Opin Struct Biol. 2011;21:610–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ng V, Zanazzi G, Timpl R, Talts JF, Salzer JL, Brennan PJ, Rambukkana A. Role of the cell wall phenolic glycolipid-1 in the peripheral nerve predilection of Mycobacterium leprae. Cell. 2000;103:511–24.

    Article  CAS  PubMed  Google Scholar 

  • Nilsson EC, Storm RJ, Bauer J, Johansson SM, Lookene A, Angstrom J, et al. The GD1a glycan is a cellular receptor for adenoviruses causing epidemic keratoconjunctivitis. Nat Med. 2011;17:105–9.

    Article  CAS  PubMed  Google Scholar 

  • Pahud BA, Glaser CA, Dekker CL, Arvin AM, Schmid DS. Varicella zoster disease of the central nervous system: epidemiological, clinical, and laboratory features 10 years after the introduction of the varicella vaccine. J Infect Dis. 2011;203:316–23.

    Article  PubMed Central  PubMed  Google Scholar 

  • Parveen N, Leong JM. Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol. 2000;35:1220–34.

    Article  CAS  PubMed  Google Scholar 

  • Paton AW, Morona R, Paton JC. Bioengineered bugs expressing oligosaccharide receptor mimics: toxin-binding probiotics for treatment and prevention of enteric infections. Bioeng Bugs. 2010;1(3):172–7.

    Article  PubMed Central  PubMed  Google Scholar 

  • Peng L, Tepp WH, Johnson EA, Dong M. Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors. PLoS Pathog. 2011;7(3):e1002008.

    Google Scholar 

  • Peng CZ, Morris Jr JG, Rodriguez RL, Shukla AW, Tapia-Núñez J, Okun MS. Emerging opportunities for serotypes of botulinum neurotoxins. Toxins (Basel). 2012;4:1196–222.

    Article  Google Scholar 

  • Petro KA, Dyer MA, Yowler BC, Schengrund C-L. Disruption of lipid rafts enhances activity of botulinum neurotoxin serotype A. Toxicon. 2006;48:1035–45.

    Article  CAS  PubMed  Google Scholar 

  • Pshezhetsky AV, Hinek A. Where catabolism meets signalling: neuraminidase 1 as a modulator of cell receptors. Glycoconj J. 2011;28:441–52.

    Article  CAS  PubMed  Google Scholar 

  • Puri A, Hug P, Jernigan K, Barchi J, Kim HY, Hamilton J, et al. The neutral glycosphingolipid globotriaosylceramide promotes fusion mediated by a CD4-dependent CXCR4-utilizing HIV type 1 envelope glycoprotein. Proc Natl Acad Sci U S A. 1998;95:14435–40.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rambukkana A, Zanazzi G, Tapinos N, Salzer JL. Contact-dependent demyelination by Mycobacterium leprae in the absence of immune cells. Science. 2002;296:927–31.

    Article  CAS  PubMed  Google Scholar 

  • Ramos TN, Bullard DC, Darley MM, McDonald K, Crawford DF, Barnum SR. Experimental cerebral malaria develops independently of endothelial expression of intercellular adhesion molecule-1 (icam-1). J Biol Chem. 2013;288:10962–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rees JH, Soudain SE, Gregson NA, Hughes RAC. Campylobacter jejuni infection and Guillain–Barré syndrome. N Engl J Med. 1995;333:1374–9.

    Article  CAS  PubMed  Google Scholar 

  • Rich JR, Withers SG. A chemoenzymatic total synthesis of the neurogenic starfish ganglioside LLG-3 using an engineered and evolved synthase. Angew Chem Int Ed Engl. 2012;51:8640–3.

    Article  CAS  PubMed  Google Scholar 

  • Rosa Borges A, Wieczorek L, Johnson B, Benesi AJ, Brown BK, Kensinger RD, et al. Multivalent dendrimeric compounds containing carbohydrates expressed on immune cells inhibit infection by primary isolates of HIV-1. Virology. 2010;408:80–8.

    Article  CAS  PubMed  Google Scholar 

  • Rummel A, Hafner K, Mahrhold S, Darashchonak N, Holt M, Jahn R, et al. Botulinum neurotoxins C, E and F bind gangliosides via a conserved binding site prior to stinulation-dependent uptake with botulinum neurotoxin F utilizing the three isoforms of SV2 as a second receptor. J Neurochem. 2009;110:1942–54.

    Article  CAS  PubMed  Google Scholar 

  • Rustici M, Santucci A, Lozzi L, Petreni S, Spreafico A, Neri P. A monoclonal antibody to a synthetic fragment of rabies virus glycoprotein binds ligands of the nicotinic cholinergic receptor. J Mol Recognit. 1989;2:51–5.

    Article  CAS  PubMed  Google Scholar 

  • Schengrund CL, Ringler NJ. Binding of Vibrio cholera toxin and the heat-labile enterotoxin of Escherichia coli to GM1, derivatives of GM1, and nonlipid oligosaccharide polyvalent ligands. J Biol Chem. 1989;264:13233–7.

    CAS  PubMed  Google Scholar 

  • Simon O, Lacour A, Delval A, Beaume A, Vermersch P. Recurrent multiple cranial nerve palsy and anti-GD1a antibodies. Muscle Nerve. 2011;43:447–8.

    Article  PubMed  Google Scholar 

  • Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000;1:31–9.

    Article  CAS  PubMed  Google Scholar 

  • Singh BR. Introduction: biomedical and toxico-chemical aspects of botulinum neurotoxins. J Toxicol Toxin Rev. 1999;18:vii–x.

    Article  Google Scholar 

  • Stettner MR, Nance JA, Wright CA, Kinoshita Y, Kim WK, Morgello S. SMAD proteins of oligodendroglial cells regulate transcription of JC virus early and late genes coordinately with the Tat protein of human immunodeficiency virus type 1. J Gen Virol. 2009;90:2005–14.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stojanov K, Georgieva JV, Brinkhuis RP, van Hest JC, Rutjes FP, Dierckx RA, et al. In vivo biodistribution of prion- and GM1-targeted polymersomes following intravenous administration in mice. Mol Pharm. 2012;9:1620–7.

    Article  CAS  PubMed  Google Scholar 

  • Svennerholm L. Ganglioside designation. Adv Exp Med Biol. 1980;125:11.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Funata N, Ikuta F, Sato S. Neuronal apoptosis and inflammatory responses in the central nervous system of a rabbit treated with Shiga toxin-2. J Neuroinflammation. 2008;5:11. doi:10.1186/1742-2094-5-11.

    Article  PubMed Central  PubMed  Google Scholar 

  • Thomas RJ. Use of receptor mimicry as a possible therapeutic treatment for biothtreat agents. Bioeng Bugs. 2010;1:17–30.

    Article  PubMed Central  PubMed  Google Scholar 

  • Thompson JP, Schengrund CL. Oligosaccharide-derivatized dendrimers: defined multivalent inhibitors of the adherence of the cholera toxin B subunit and the heat labile enterotoxin of E. coli to GM1. Glycoconj J. 1997;14:837–45.

    Article  CAS  PubMed  Google Scholar 

  • Usuki S, Thompson SA, Rivner MH, Taguchi K, Shibata K, Ariga T, et al. Molecular mimicry: sensitization of Lewis rats with Campylobacter jejuni lipopolysaccharides induces formation of antibody toward GD3 ganglioside. J Neurosci Res. 2006;83:274–84.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Usuki S, Taguchi K, Gu YH, Thompson SA, Yu RK. Development of a novel therapy for Lipo-oligosaccharide-induced experimental neuritis: use of peptide glycomimics. J Neurochem. 2010;113:351–62.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Verma A, Brissette CA, Bowman A, Stevenson B. Borrelia burgdorferi BmpA is a lamininbinding protein. Infect Immun. 2009;77:4940–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yao J, Nowack A, Kensel-Hammes P, Gardner RG, Bajjalieh SM. Cotrafficking of SV2 and synaptotagmin at the synapse. J Neurosci. 2010;30:5569–78.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yowler BC, Schengrund CL. Botulinum neurotoxin A changes conformation upon binding to ganglioside GT1b. Biochemistry. 2004;43:9725–31.

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Gershon MD, Ambron R, Gabel C, Gershon AA. Infection of cells by varicella zoster virus: inhibition of viral entry by mannose 6-phosphate and heparin. Proc Natl Acad Sci U S A. 1995;92:3546–50.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Cara-Lynne Schengrund declares that she has no conflict of interest and that she has used no human subjects in work cited that was done in her laboratory.

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  1. Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA

    Cara-Lynne Schengrund

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  1. Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Georgia Regents University, Augusta, Georgia, USA

    Robert K. Yu

  2. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, College of Medicine, Hershey, Pennsylvania, USA

    Cara-Lynne Schengrund

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Schengrund, CL. (2014). Roles of Carbohydrates in the Interaction of Pathogens with Neural Cells. In: Yu, R., Schengrund, CL. (eds) Glycobiology of the Nervous System. Advances in Neurobiology, vol 9. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1154-7_18

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