Double anchorage to the membrane and intact inter-chain disulfide bond are required for the low pH induced entry of tetanus and botulinum neurotoxins into neurons

Cellular Microbiology - Tập 13 Số 11 - Trang 1731-1743 - 2011
Marco Pirazzini1, Ornella Rossetto1,2,3,4, Paolo Bolognese1, Clifford C. Shone5, Cesare Montecucco1,2,3,4
1Dipartimento di Scienze Biomediche and Istituto CNR di Neuroscienze, Università di Padova, Viale G. Colombo 3, 35131 Padova, Italy
2e-mail: [email protected]
3Tel. (+39) 049 827 6058
4Tel. (+39) 049 827 6077
5Health Protection Agency, Porton Down, Salisbury, Wiltshire SP4 OJG, UK

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Arndt, 2006, A structural perspective of the sequence variability within botulinum neurotoxin subtypes A1-A4, J Mol Biol, 362, 733, 10.1016/j.jmb.2006.07.040

Bas, 2008, Very fast prediction and rationalization of pka values for protein ligand complexes, Proteins, 73, 765, 10.1002/prot.22102

Beise, 1994, Pore formation by tetanus toxin, its chain and fragments in neuronal membranes and evaluation of the underlying motifs in the structure of the toxin molecule, Naunyn Schmiedebergs Arch Pharmacol, 349, 66, 10.1007/BF00178208

Binz, 2009, Cell entry strategy of clostridial neurotoxins, J Neurochem, 109, 1584, 10.1111/j.1471-4159.2009.06093.x

Blaustein, 1987, The N-terminal half of the heavy chain of botulinum type a neurotoxin forms channels in planar phospholipid bilayers, FEBS Lett, 226, 115, 10.1016/0014-5793(87)80562-8

Boquet, 1982, Tetanus toxin fragment forms channels in lipid vesicles at low pH, Proc Natl Acad Sci USA, 79, 7614, 10.1073/pnas.79.24.7614

Chai, 2006, Structural basis of cell surface receptor recognition by botulinum neurotoxin B, Nature, 444, 1096, 10.1038/nature05411

Chen, 2008, Molecular basis for tetanus toxin coreceptor interactions, Biochemistry, 47, 7179, 10.1021/bi800640y

Chen, 2009, Gangliosides as high affinity receptors for tetanus neurotoxin, J Biol Chem, 284, 26569, 10.1074/jbc.M109.027391

Collier, 2001, Understanding the mode of action of diphtheria toxin: a perspective on progress during the 20th century, Toxicon, 39, 1793, 10.1016/S0041-0101(01)00165-9

Davletov, 2005, Beyond botox: advantages and limitations of individual botulinum neurotoxins, Trends Neurosci, 28, 446, 10.1016/j.tins.2005.06.001

De Paiva, 1993, A role for the interchain disulfide or its participating thiols in the internalization of botulinum neurotoxin A revealed by a toxin derivative that binds to ecto-acceptors and inhibits transmitter release intracellularly, J Biol Chem, 268, 20838, 10.1016/S0021-9258(19)36861-9

Dong, 2006, SV2 is the protein receptor for botulinum neurotoxin A, Science, 312, 592, 10.1126/science.1123654

Dong, 2008, Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons, Mol Biol Cell, 19, 5226, 10.1091/mbc.E08-07-0765

Donovan, 1986, Ion-conducting channels produced by botulinum toxin in planar lipid membranes, Biochemistry, 25, 2872, 10.1021/bi00358a020

Draper, 1980, The entry of diphtheria toxin into the mammalian cell cytoplasm: evidence for lysosomal involvement, J Cell Biol, 87, 849, 10.1083/jcb.87.3.849

Eswaramoorthy, 2004, Role of metals in the biological activity of clostridium botulinum neurotoxins, Biochemistry, 43, 2209, 10.1021/bi035844k

Fischer, 2007a, Single molecule detection of intermediates during botulinum neurotoxin translocation across membranes, Proc Natl Acad Sci USA, 104, 10447, 10.1073/pnas.0700046104

Fischer, 2007b, Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes, J Biol Chem, 282, 29604, 10.1074/jbc.M703619200

Fischer, 2008, Botulinum neurotoxin devoid of receptor binding domain translocates active protease, PLoS Pathog, 4, e1000245, 10.1371/journal.ppat.1000245

Fotinou, 2001, The crystal structure of tetanus toxin HC fragment complexed with a synthetic gt1b analogue suggests cross-linking between ganglioside receptors and the toxin, J Biol Chem, 276, 32274, 10.1074/jbc.M103285200

Fu, 1999, Calcein permeability of liposomes mediated by type A botulinum neurotoxin and its light and heavy chains, J Protein Chem, 18, 701, 10.1023/A:1020614525534

Fu, 2002, Spectroscopic analysis of low pH and lipid-induced structural changes in type A botulinum neurotoxin relevant to membrane channel formation and translocation, Biophys Chem, 99, 17, 10.1016/S0301-4622(02)00135-7

Fu, 2009, Glycosylated SV2 and gangliosides as dual receptors for botulinum neurotoxin serotype f, Biochemistry, 48, 5631, 10.1021/bi9002138

van der Goot, 1993, Role of acidic lipids in the translocation and channel activity of colicins A and N in Escherichia coli cells, Eur J Biochem, 213, 217, 10.1111/j.1432-1033.1993.tb17751.x

Han, 2004, N-glycosylation is essential for vesicular targeting of synaptotagmin 1, Neuron, 41, 85, 10.1016/S0896-6273(03)00820-1

Hoch, 1985, Channels formed by botulinum, tetanus, and diphtheria toxins in planar lipid bilayers: relevance to translocation of proteins across membranes, Proc Natl Acad Sci USA, 82, 1692, 10.1073/pnas.82.6.1692

Jayaraman, 2005, Common binding site for disialyllactose and tri-peptide in c-fragment of tetanus neurotoxin, Proteins, 61, 288, 10.1002/prot.20595

Jin, 2006, Botulinum neurotoxin B recognizes its protein receptor with high affinity and specificity, Nature, 444, 1092, 10.1038/nature05387

Johnson, 2008, Botulism, Handb Clin Neurol, 91, 333, 10.1016/S0072-9752(07)01511-4

Karalewitz, 2010, Identification of a unique ganglioside binding loop within botulinum neurotoxins C and D-SA, Biochemistry, 49, 8117, 10.1021/bi100865f

Keller, 1999, Persistence of botulinum neurotoxin action in cultured spinal cord cells, FEBS Lett, 456, 137, 10.1016/S0014-5793(99)00948-5

Kistner, 1993, Disulfide formation in reduced tetanus toxin by thioredoxin: the pharmacological role of interchain covalent and noncovalent bonds, Toxicon, 31, 1423, 10.1016/0041-0101(93)90208-Z

Koriazova, 2003, Translocation of botulinum neurotoxin light chain protease through the heavy chain channel, Nat Struct Biol, 10, 13, 10.1038/nsb879

Kumaran, 2009, Domain organization in clostridium botulinum neurotoxin type E is unique: its implication in faster translocation, J Mol Biol, 386, 233, 10.1016/j.jmb.2008.12.027

Lacy, 1999, Sequence homology and structural analysis of the clostridial neurotoxins, J Mol Biol, 291, 1091, 10.1006/jmbi.1999.2945

Lacy, 1998, Crystal structure of botulinum neurotoxin type A and implications for toxicity, Nat Struct Biol, 5, 898, 10.1038/2338

Lalli, 1999, Functional characterisation of tetanus and botulinum neurotoxins binding domains, J Cell Sci, 112, 2715, 10.1242/jcs.112.16.2715

Li, 2005, Very fast empirical prediction and rationalization of protein pka values, Proteins, 61, 704, 10.1002/prot.20660

McNutt, 2011, Embryonic stem cell-derived neurons are a novel, highly sensitive tissue culture platform for botulinum research, Biochem Biophys Res Commun, 405, 85, 10.1016/j.bbrc.2010.12.132

Mahrhold, 2006, The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves, FEBS Lett, 580, 2011, 10.1016/j.febslet.2006.02.074

Menestrina, 1989, Interaction of tetanus toxin with lipid vesicles. Effects of pH, surface charge, and transmembrane potential on the kinetics of channel formation, Biophys J, 55, 393, 10.1016/S0006-3495(89)82833-4

Miesenböck, 1998, Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins, Nature, 394, 192, 10.1038/28190

Montal, 2009, Translocation of botulinum neurotoxin light chain protease by the heavy chain protein-conducting channel, Toxicon, 54, 565, 10.1016/j.toxicon.2008.11.018

Montal, 2010, Botulinum neurotoxin: a marvel of protein design, Annu Rev Biochem, 79, 591, 10.1146/annurev.biochem.051908.125345

Montecucco, 1986, How do tetanus and botulinum toxins bind to neuronal membranes?, Trends biochem sci, 11, 314, 10.1016/0968-0004(86)90282-3

Montecucco, 2005, Botulinal neurotoxins: revival of an old killer, Curr Opin Pharmacol, 5, 274, 10.1016/j.coph.2004.12.006

Montecucco, 1989, Effect of pH on the interaction of botulinum neurotoxins A, B and E with liposomes, Biochem J, 259, 47, 10.1042/bj2590047

Montecucco, 2004, Presynaptic receptor arrays for clostridial neurotoxins, Trends Microbiol, 12, 442, 10.1016/j.tim.2004.08.002

Moriishi, 1996, Mosaic structures of neurotoxins produced from clostridium botulinum types C and D organisms, Biochim Biophys Acta, 1307, 123, 10.1016/0167-4781(96)00006-1

Muraro, 2009, The N-terminal half of the receptor domain of botulinum neurotoxin A binds to microdomains of the plasma membrane, Biochem Biophys Res Commun, 380, 76, 10.1016/j.bbrc.2009.01.037

Nishiki, 1996, The high-affinity binding of clostridium botulinum type B neurotoxin to synaptotagmin II associated with gangliosides gt1b/gd1a, FEBS Lett, 378, 253, 10.1016/0014-5793(95)01471-3

Olsson, 2011, PROPKA3: consistent treatment of internal and surface residues in empirical pka predictions, J Chem Theory Comput, 7, 525, 10.1021/ct100578z

Peng, 2011, Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors, PLoS Pathog, 7, e1002008, 10.1371/journal.ppat.1002008

Perier, 2007, Concerted protonation of key histidines triggers membrane interaction of the diphtheria toxin t domain, J Biol Chem, 282, 24239, 10.1074/jbc.M703392200

Puhar, 2004, Comparison of the pH-induced conformational change of different clostridial neurotoxins, Biochem Biophys Res Commun, 319, 66, 10.1016/j.bbrc.2004.04.140

Rigoni, 2004, Snake presynaptic neurotoxins with phospholipase A2 activity induce punctate swellings of neurites and exocytosis of synaptic vesicles, J Cell Sci, 117, 3561, 10.1242/jcs.01218

Rodnin, 2010, Conformational switching of the diphtheria toxin t domain, J Mol Biol, 402, 1, 10.1016/j.jmb.2010.07.024

Rossetto, 2006, Presynaptic enzymatic neurotoxins, J Neurochem, 97, 1534, 10.1111/j.1471-4159.2006.03965.x

Rummel, 2003, Two carbohydrate binding sites in the H(Cc)-domain of tetanus neurotoxin are required for toxicity, J Mol Biol, 326, 835, 10.1016/S0022-2836(02)01403-1

Rummel, 2004a, The Hcc-domain of botulinum neurotoxins A and B exhibits a singular ganglioside binding site displaying serotype specific carbohydrate interaction, Mol Microbiol, 51, 631, 10.1046/j.1365-2958.2003.03872.x

Rummel, 2004b, Synaptotagmins I and II act as nerve cell receptors for botulinum neurotoxin G, J Biol Chem, 279, 30865, 10.1074/jbc.M403945200

Rummel, 2007, Identification of the protein receptor binding site of botulinum neurotoxins B and G proves the double-receptor concept, Proc Natl Acad Sci USA, 104, 359, 10.1073/pnas.0609713104

Rummel, 2009, Botulinum neurotoxins C, E and F bind gangliosides via a conserved binding site prior to stimulation-dependent uptake with botulinum neurotoxin F utilising the three isoforms of SV2 as second receptor, J Neurochem, 110, 1942, 10.1111/j.1471-4159.2009.06298.x

Sandberg, 1989, Studies on the intoxication pathway of tetanus toxin in the rat pheochromocytoma (PC12) cell line. Binding, internalization, and inhibition of acetylcholine release, J Biol Chem, 264, 5679, 10.1016/S0021-9258(18)83602-X

Sandvig, 1980, Diphtheria toxin entry into cells is facilitated by low pH, J Cell Biol, 87, 828, 10.1083/jcb.87.3.828

Sankaranarayanan, 2000, Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system, Nat Cell Biol, 2, 197, 10.1038/35008615

Schiavo, 1990, An intact interchain disulfide bond is required for the neurotoxicity of tetanus toxin, Infect Immun, 58, 4136, 10.1128/IAI.58.12.4136-4141.1990

Schiavo, 1991, On the role of polysialoglycosphingolipids as tetanus toxin receptors. A study with lipid monolayers, Eur J Biochem, 199, 705, 10.1111/j.1432-1033.1991.tb16174.x

Schiavo, 1994, Tetanus and botulinum neurotoxins are zinc proteases specific for components of the neuroexocytosis apparatus, Ann N Y Acad Sci, 710, 65, 10.1111/j.1749-6632.1994.tb26614.x

Sheridan, 1998, Gating and permeability of ion channels produced by botulinum toxin types A and E in PC12 cell membranes, Toxicon, 36, 703, 10.1016/S0041-0101(97)00131-1

Shi, 2009, TCEP treatment reduces proteolytic activity of BoNT/B in human neuronal SHSY-5Y cells, J Cell Biochem, 107, 1021, 10.1002/jcb.22205

Shone, 1995, Growth of clostridia and preparation of their neurotoxins, Curr Top Microbiol Immunol, 195, 143

Shone, 1987, A 50-kDa fragment from the NH2-terminus of the heavy subunit of clostridium botulinum type A neurotoxin forms channels in lipid vesicles, Eur J Biochem, 167, 175, 10.1111/j.1432-1033.1987.tb13320.x

Simpson, 1994, Inhibition of vacuolar adenosine triphosphatase antagonizes the effects of clostridial neurotoxins but not phospholipase A2 neurotoxins, J Pharmacol Exp Ther, 269, 256

Simpson, 2004, The role of the interchain disulfide bond in governing the pharmacological actions of botulinum toxin, J Pharmacol Exp Ther, 308, 857, 10.1124/jpet.103.058149

Stahl, 2007, Primary cultures of embryonic chicken neurons for sensitive cell-based assay of botulinum neurotoxin: implications for therapeutic discovery, J Biomol Screen, 12, 370, 10.1177/1087057106299163

Strotmeier, 2010, Botulinum neurotoxin serotype D attacks neurons via two carbohydrate-binding sites in a ganglioside-dependent manner, Biochem J, 431, 207, 10.1042/BJ20101042

Swaminathan, 2000, Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B, Nat Struct Biol, 7, 617, 10.1038/78005

Verderio, 1999, Internalization and proteolytic action of botulinum toxins in CNS neurons and astrocytes, J Neurochem, 73, 372, 10.1046/j.1471-4159.1999.0730372.x

Williamson, 1994, Bafilomycin A1 inhibits the action of tetanus toxin in spinal cord neurons in cell culture, J Neurochem, 63, 2342, 10.1046/j.1471-4159.1994.63062342.x

Yeh, 2010, SV2 mediates entry of tetanus neurotoxin into central neurons, PLoS Pathog, 6, e1001207, 10.1371/journal.ppat.1001207

Zhang, 2011, Crystal structure of the receptor binding domain of the botulinum C-D mosaic neurotoxin reveals potential roles of lysines 1118 and 1136 in membrane interactions, Biochem Biophys Res Commun, 404, 407, 10.1016/j.bbrc.2010.11.134