The elusive compass of clostridial neurotoxins: Deciding when and where to go?

Current Topics in Microbiology and Immunology

Volumn 364, Issue , 2013, Pages 91-113

  Bercsenyi, Kinga ^a   Giribaldi, Francesco ^b   Schiavo, Giampietro ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b Section of Pharmacology and Toxicology   (Italy)

Author keywords

Axonal transport; Botulinum neurotoxin; Endocytosis motor neurons; Tetanus toxin

Indexed keywords

BOTULINUM TOXIN; CLOSTRIDIAL NEUROTOXIN; NEUROTOXIN; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; TETANUS TOXIN; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; GANGLIOSIDE; NERVE GROWTH FACTOR;

ARTICLE; CELL SURFACE; ENDOCYTOSIS; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RETROGRADE NERVE FIBER TRANSPORT; SIGNAL TRANSDUCTION; ANIMAL; CELL MEMBRANE; CLOSTRIDIUM TETANI; METABOLISM; MOTONEURON; NERVE FIBER TRANSPORT; PROTEIN TERTIARY STRUCTURE; REVIEW; SYNAPSE VESICLE;

ANIMALS; AXONAL TRANSPORT; CELL MEMBRANE; CLOSTRIDIUM TETANI; ENDOCYTOSIS; GANGLIOSIDES; MOTOR NEURONS; NERVE GROWTH FACTORS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; SYNAPTIC VESICLES; TETANUS TOXIN;

EID: 84875813026     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-642-33570-9-5     Document Type: Article

References (126)

1. Antonucci F, Rossi C, Gianfranceschi L, Rossetto O, Caleo M (2008) Long-distance retrograde effects of botulinum neurotoxin A. J Neurosci 28:3689-3696
2. Baldwin MR, Barbieri JT (2007) Association of botulinum neurotoxin serotypes A and B with synaptic vesicle protein complexes. Biochemistry 46:3200-3210
3. Bearer EL, Reese TS (1999) Association of actin filaments with axonal microtubule tracts. J Neurocytol 28:85-98
4. Bigalke H, Muller H, Dreyer F (1986) Botulinum A neurotoxin unlike tetanus toxin acts via a neuraminidase sensitive structure. Toxicon 24:1065-1074
5. Bilsland LG, Sahai E, Kelly G, Golding M, Greensmith L, Schiavo G (2010) Deficits in axonal transport precede ALS symptoms in vivo. Proc Natl Acad Sci U S A 107:20523-20528
6. Black JD, Dolly JO (1986) Interaction of 125I-labeled botulinum neurotoxins with nerve terminals. II. Autoradiographic evidence for its uptake into motor nerves by acceptormediated endocytosis. J Cell Biol 103:535-544
7. Blasi J, Chapman ER, Link E, Binz T, Yamasaki S, De Camilli P, Südhof TC, Niemann H, Jahn R (1993a) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365:160-163
8. Blasi J, Chapman ER, Yamasaki S, Binz T, Niemann H, Jahn R (1993b) Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin. EMBO J 12:4821-4828
9. Blum FC, Chen C, Kroken AR, Barbieri JT (2012) Tetanus toxin and botulinum toxin a utilize unique mechanisms to enter neurons of the central nervous system. Infect Immun 80:1662-1669
10. Bocking T, Aguet F, Harrison SC, Kirchhausen T (2011) Single-molecule analysis of a molecular disassemblase reveals the mechanism of Hsc70-driven clathrin uncoating. Nat Struct Mol Biol 18:295-301
11. Bohnert S, Schiavo G (2005) Tetanus toxin is transported in a novel neuronal compartment characterized by a specialized pH regulation. J Biol Chem 280:42336-42344
12. Borchelt DR, Koliatsos VE, Guarnieri M, Pardo CA, Sisodia SS, Price DL (1994) Rapid anterograde axonal transport of the cellular prion glycoprotein in the peripheral and central nervous systems. J Biol Chem 269:14711-14714
13. Butowt R, von Bartheld CS (2003) Connecting the dots: trafficking of neurotrophins, lectins and diverse pathogens by binding to the neurotrophin receptor p75NTR. Eur J Neurosci 17:673-680
14. Caleo M, Schiavo G (2009) Central effects of tetanus and botulinum neurotoxins. Toxicon 54:593-599
15. Chen C, Baldwin MR, Barbieri JT (2008) Molecular basis for tetanus toxin coreceptor interactions. Biochemistry 47:7179-7186
16. Chen C, Fu Z, Kim JJ, Barbieri JT, Baldwin MR (2009) Gangliosides as high affinity receptors for tetanus neurotoxin. J Biol Chem 284:26569-26577
17. Costantin L, Bozzi Y, Richichi C, Viegi A, Antonucci F, Funicello M, Gobbi M, Mennini T, Rossetto O, Montecucco C, Maffei L, Vezzani A, Caleo M (2005) Antiepileptic effects of botulinum neurotoxin E. J Neurosci 25:1943-1951
18. Deinhardt K, Berninghausen O, Willison HJ, Hopkins CR, Schiavo G (2006a) Tetanus toxin is internalized by a sequential clathrin-dependent mechanism initiated within lipid microdomains and independent of epsin1. J Cell Biol 174:459-471
19. Deinhardt K, Salinas S, Verastegui C, Watson R, Worth D, Hanrahan S, Bucci C, Schiavo G (2006b) Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52:293-305
20. Della-Bianca V, Rossi F, Armato U, Dal-Pra I, Costantini C, Perini G, Politi V, Della Valle G (2001) Neurotrophin p75 receptor is involved in neuronal damage by prion peptide-(106-126). J Biol Chem 276:38929-38933
21. Dong M, Liu H, Tepp WH, Johnson EA, Janz R, Chapman ER (2008) Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol Biol Cell 5226-5237
22. Dong M, Richards DA, Goodnough MC, Tepp WH, Johnson EA, Chapman ER (2003) Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells. J Cell Biol 162:1293-1303
23. Dong M, Tepp WH, Liu H, Johnson EA, Chapman ER (2007) Mechanism of botulinum neurotoxin B and G entry into hippocampal neurons. J Cell Biol 179:1511-1522
24. Dong M, Yeh F, Tepp WH, Dean C, Johnson EA, Janz R, Chapman ER (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312:592-596
25. Encalada SE, Szpankowski L, Xia CH, Goldstein LS (2011) Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles. Cell 144:551-565
26. Ferguson SM, De Camilli P (2012) Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13:75-88
27. Fischer A, Montal M (2007) Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. J Biol Chem 282:29604-29611
28. Fischer A, Mushrush DJ, Lacy DB, Montal M (2008) Botulinum neurotoxin devoid of receptor binding domain translocates active protease. PLoS Pathog 4:e1000245
29. Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ, Evans PR, McMahon HT (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419:361-366
30. Fotinou C, Emsley P, Black I, Ando H, Ishida H, Kiso M, Sinha KA, Fairweather NF, Isaacs NW (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 276:32274-32281
31. Gil C, Chaib-Oukadour I, Aguilera J (2003) C-terminal fragment of tetanus toxin heavy chain activates Akt and MEK/ERK signalling pathways in a Trk receptor-dependent manner in cultured cortical neurons. Biochem J 373:613-620
32. Gil C, Chaib-Oukadour I, Blasi J, Aguilera J (2001) HC fragment (C-terminal portion of the heavy chain) of tetanus toxin activates protein kinase C isoforms and phosphoproteins involved in signal transduction. Biochem J 356:97-103
33. Gil C, Chaib-Oukadour I, Pelliccioni P, Aguilera J (2000) Activation of signal transduction pathways involving trkA, PLCgamma-1, PKC isoforms and ERK-1/2 by tetanus toxin. FEBS Lett 481:177-182
34. Greber UF, Way M (2006) A superhighway to virus infection. Cell 124:741-754
35. Habermann E, Dreyer F (1986) Clostridial neurotoxins: handling and action at the cellular and molecular level. Curr Top Microbiol Immunol 129:93-179
36. Hackett R, Kam PC (2007) Botulinum toxin: pharmacology and clinical developments: a literature review. Med Chem 3:333-345
37. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, Lalli G, Witherden AS, Hummerich H, Nicholson S, Morgan PJ, Oozageer R, Priestley JV, Averill S, King VR, Ball S, Peters J, Toda T, Yamamoto A, Hiraoka Y, Augustin M, Korthaus D, Wattler S, Wabnitz P, Dickneite C, Lampel S, Boehme F, Peraus G, Popp A, Rudelius M, Schlegel J, Fuchs H, Hrabe de Angelis M, Schiavo G, Shima DT, Russ AP, Stumm G, Martin JE, Fisher EM (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-812
38. Harper CB, Martin S, Nguyen TH, Daniels SJ, Lavidis NA, Popoff MR, Hadzic G, Mariana A, Chau N, McCluskey A, Robinson PJ, Meunier FA (2011) Dynamin inhibition blocks botulinum neurotoxin type A endocytosis in neurons and delays botulism. J Biol Chem 286:35966-35976
39. Haucke V (2005) Phosphoinositide regulation of clathrin-mediated endocytosis. Biochem Soc Trans 33:1285-1289
40. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, McMahon HT (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328:1281-1284
41. Herreros J, Lalli G, Montecucco C, Schiavo G (2000) Tetanus toxin fragment C binds to a protein present in neuronal cell lines and motoneurons. J Neurochem 74:1941-1950
42. Herreros J, Ng T, and Schiavo G (2001) Lipid rafts act as specialised domains for tetanus toxin binding and internalisation into neurons. Submitted
43. Hinrichsen L, Meyerholz A, Groos S, Ungewickell EJ (2006) Bending a membrane: how clathrin affects budding. Proc Natl Acad Sci U S A 103:8715-8720
44. Hirokawa N, Niwa S, Tanaka Y (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68:610-638
45. Hoeller D, Volarevic S, Dikic I (2005) Compartmentalization of growth factor receptor signalling. Curr Opin Cell Biol 17:107-111
46. Howe CL (2005) Modeling the signaling endosome hypothesis: why a drive to the nucleus is better than a (random) walk. Theor Biol Med Model 2:43
47. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, Collins BM, Honing S, Evans PR, Owen DJ (2010) A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141:1220-1229
48. Keller JE, Cai F, Neale EA (2004) Uptake of botulinum neurotoxin into cultured neurons. Biochemistry 43:526-532
49. Kitamura M, Igimi S, Furukawa K (2005) Different response of the knockout mice lacking bseries gangliosides against botulinum and tetanus toxins. Biochim Biophys Acta 1741:1-3
50. Kitamura M, Takamiya K, Aizawa S, Furukawa K (1999) Gangliosides are the binding substances in neural cells for tetanus and botulinum toxins in mice. Biochim Biophys Acta 1441:1-3
51. Koriazova LK, Montal M (2003) Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat Struct Biol 10:13-18
52. Kroken AR, Karalewitz AP, Fu Z, Baldwin MR, Kim JJ, Barbieri JT (2011) Unique ganglioside binding by botulinum neurotoxins C and D-SA. FEBS J 278:4486-4496
53. Lacy DB, Tepp W, Cohen AC, Das Gupta BR, Stevens RC (1998) Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat Struct Biol 5:898-902
54. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X (2003) Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100:9280-9285
55. Lalli G, Bohnert S, Deinhardt K, Verastegui C, Schiavo G (2003a) The journey of tetanus and botulinum neurotoxins in neurons. Trends Microbiol 11:431-437
56. Lalli G, Gschmeissner S, Schiavo G (2003b) Myosin Va and microtubule-based motors are required for fast axonal retrograde transport of tetanus toxin in motor neurons. J Cell Sci 116:4639-4650
57. Lalli G, Schiavo G (2002) Analysis of retrograde transport in motor neurons reveals common endocytic carriers for tetanus toxin and neurotrophin receptor p75NTR. J Cell Biol 156:233-239
58. Langford GM (2002) Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3:859-865
59. Lawrence GW, Ovsepian SV, Wang J, Aoki KR, Dolly JO (2012) Extravesicular intraneuronal migration of internalized botulinum neurotoxins without detectable inhibition of distal neurotransmission. Biochem J 441:443-452
60. Le Roy C, Wrana JL (2005) Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6:112-126
61. Mahrhold S, Rummel A, Bigalke H, Davletov B, Binz T (2006) The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett 580:2011-2014
62. Marxen P, Ahnert-Hilger G, Wellhöner HH, Bigalke H (1990) Tetanus antitoxin binds to intracellular tetanus toxin in permeabilized chromaffin cells without restoring Ca2 (+)-induced exocytosis. Toxicon 28:1077-1082
63. Marxen P, Bigalke H (1989) Tetanus toxin: inhibitory action in chromaffin cells is initiated by specified types of gangliosides and promoted in low ionic strength solution. Neurosci Lett 107:261-266
64. Matteoli M, Verderio C, Rossetto O, Iezzi N, Coco S, Schiavo G, Montecucco C (1996) Synaptic vesicle endocytosis mediates the entry of tetanus neurotoxin into hippocampal neurons. Proc Natl Acad Sci U S A 93:13310-13315
65. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrinmediated endocytosis. Nat Rev Mol Cell Biol 12:517-533
66. McMahon HT, Ushkaryov YA, Edelmann L, Link E, Binz T, Niemann H, Jahn R, Sudhof TC (1993) Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 364:346-349
67. Montal M (2010) Botulinum neurotoxin: a marvel of protein design. Annu Rev Biochem 79:591-617
68. Montecucco C (1986) How do tetanus and botulinum toxins bind to neuronal membranes? Trends Biochem Sci 11:315-317
69. Montecucco C, Schiavo G, Brunner J, Duflot E, Boquet P, Roa M (1986) Tetanus toxin is labeled with photoactivatable phospholipids at low pH. Biochemistry 25:919-924
70. Montecucco C, Schiavo G, Dasgupta BR (1989) Effect of pH on the interaction of botulinum neurotoxins A, B and E with liposomes. Biochem J 259:47-53
71. Munro P, Kojima H, Dupont JL, Bossu JL, Poulain B, Boquet P (2001) High sensitivity of mouse neuronal cells to tetanus toxin requires a GPI-anchored protein. Biochem Biophys Res Commun 289:623-629
72. Nishiki T, Kamata Y, Nemoto Y, Omori A, Ito T, Takahashi M, Kozaki S (1994) Identification of protein receptor for Clostridium botulinum type B neurotoxin in rat brain synaptosomes. J Biol Chem 269:10498-10503
73. Nishiki T, Tokuyama Y, Kamata Y, Nemoto Y, Yoshida A, Sato K, Sekiguchi M, Takahashi M, Kozaki S (1996a) The high-affinity binding of Clostridium botulinum type B neurotoxin to synaptotagmin II associated with gangliosides GT1b/GD1a. FEBS Lett 378:253-257
74. Nishiki T, Tokuyama Y, Kamata Y, Nemoto Y, Yoshida A, Sekiguchi M, Takahashi M, Kozaki S (1996b) Binding of botulinum type B neurotoxin to Chinese hamster ovary cells transfected with rat synaptotagmin II cDNA. Neurosci Lett 208:105-108
75. Ochanda JO, Syuto B, Ohishi I, Naiki M, Kubo S (1986) Binding of Clostridium botulinum neurotoxin to gangliosides. J Biochem 100:27-33
76. Ohka S, Sakai M, Bohnert S, Igarashi H, Deinhardt K, Schiavo G, Nomoto A (2009) Receptordependent and-independent axonal retrograde transport of poliovirus in motor neurons. J Virol 83:4995-5004
77. Peng L, Berntsson RP, Tepp WH, Pitkin RM, Johnson EA, Stenmark P, Dong M (2012) Botulinum neurotoxin D-C uses synaptotagmin I/II as receptors and human synaptotagmin II is not an effective receptor for type B, D-C, and G toxins. J Cell Sci 125(Pt 13):3233-3242
78. Peng L, Tepp WH, Johnson EA, Dong M (2011) Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors. PLoS Pathog 7:e1002008
79. Pirazzini M, Rossetto O, Bolognese P, Shone CC, Montecucco C (2011) 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. Cell Microbiol 13:1731-1743
80. Polley EH, Vick JA, Ciuchta HP, Fischetti DA, Macchitelli FJ, Montanarelli N (1965) Botulinum toxin, type A: effects on central nervous system. Science 147:1036-1037
81. Poon WW, Blurton-Jones M, Tu CH, Feinberg LM, Chabrier MA, Harris JW, Jeon NL, Cotman CW (2011) Beta-amyloid impairs axonal BDNF retrograde trafficking. Neurobiol Aging 32:821-833
82. Qualmann B, Koch D, Kessels MM (2011) Let's go bananas: revisiting the endocytic BAR code. EMBO J 30:3501-3515
83. Restani L, Antonucci F, Gianfranceschi L, Rossi C, Rossetto O, Caleo M (2011) Evidence for anterograde transport and transcytosis of botulinum neurotoxin A (BoNT/A). J Neurosci 31:15650-15659
84. Restani L, Giribaldi F, Manich M, Bercsenyi K, Menendez G, Rossetto O, Caleo M, and Schiavo G (2012a) Botulinum neurotoxins A and E undergo retrograde axonal transport in primary motor neurons. PLoS Pathog: in press
85. Restani L, Novelli E, Bottari D, Leone P, Barone I, Galli-Resta L, Strettoi E, Caleo M (2012b) Botulinum neurotoxin a impairs neurotransmission following retrograde transynaptic transport. Traffic 13:1083-1089
86. Rinaldi S, Brennan KM, Goodyear CS, O'Leary C, Schiavo G, Crocker PR, Willison HJ (2009) Analysis of lectin binding to glycolipid complexes using combinatorial glycoarrays. Glycobiology 19:789-796
87. Rishal I, Kam N, Perry RB, Shinder V, Fisher EM, Schiavo G, Fainzilber M (2012) A motor driven mechanism for cell length sensing. Cell Rep 1:608-616
88. Roux S, Saint Cloment C, Curie T, Girard E, Mena FJ, Barbier J, Osta R, Molgo J, Brulet P (2006) Brain-derived neurotrophic factor facilitates in vivo internalization of tetanus neurotoxin C-terminal fragment fusion proteins in mature mouse motor nerve terminals. Eur J Neurosci 24:1546-1554
89. Rummel A, Bade S, Alves J, Bigalke H, Binz T (2003) Two carbohydrate binding sites in the H (CC)-domain of tetanus neurotoxin are required for toxicity. J Mol Biol 326:835-847
90. Rummel A, Eichner T, Weil T, Karnath T, Gutcaits A, Mahrhold S, Sandhoff K, Proia RL, Acharya KR, Bigalke H, Binz T (2007) Identification of the protein receptor binding site of botulinum neurotoxins B and G proves the double-receptor concept. Proc Natl Acad Sci U S A 104:359-364
91. Rummel A, Hafner K, Mahrhold S, Darashchonak N, Holt M, Jahn R, Beermann S, Karnath T, Bigalke H, Binz T (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 110:1942-1954
92. Rummel A, Karnath T, Henke T, Bigalke H, Binz T (2004) Synaptotagmins I and II act as nerve cell receptors for botulinum neurotoxin G. J Biol Chem 279:30865-30870
93. Salinas S, Bilsland LG, Henaff D, Weston AE, Keriel A, Schiavo G, Kremer EJ (2009) CAR-associated vesicular transport of an adenovirus in motor neuron axons. PLoS Pathog 5:e1000442
94. Salinas S, Schiavo G, Kremer EJ (2010) A hitchhiker's guide to the nervous system: the complex journey of viruses and toxins. Nat Rev Microbiol 8:645-655
95. Schecterson LC, Bothwell M (2010) Neurotrophin receptors: old friends with new partners. Dev Neurobiol 70:332-338
96. Schengrund CL, Das Gupta BR, Ringler NJ (1991) Binding of botulinum and tetanus neurotoxins to ganglioside GT1b and derivatives thereof. J Neurochem 57:1024-1032
97. Schiavo G, Benfenati F, Poulain B, Rossetto O, Polverino de Laureto P, Das Gupta BR, Montecucco C (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359:832-835
98. Schiavo G, Ferrari G, Rossetto O, Montecucco C (1991) Tetanus toxin receptor. Specific crosslinking of tetanus toxin to a protein of NGF-differentiated PC 12 cells. FEBS Lett 290:227-230
99. Schiavo G, Matteoli M, Montecucco C (2000) Neurotoxins affecting neuroexocytosis. Physiol Rev 80:717-766
100. Schiavo G, Santucci A, Dasgupta BR, Mehta PP, Jontes J, Benfenati F, Wilson MC, Montecucco C (1993a) Botulinum neurotoxins serotypes A and E cleave SNAP-25 at distinct COOH-terminal peptide bonds. FEBS Lett 335:99-103
101. Schiavo G, Shone CC, Rossetto O, Alexander FC, Montecucco C (1993b) Botulinum neurotoxin serotype F is a zinc endopeptidase specific for VAMP/synaptobrevin. J Biol Chem 268:11516-11519
102. Schiavo G, van der Goot FG (2001) The bacterial toxin toolkit. Nat Rev Mol Cell Biol 2:530-537
103. Schmitt A, Dreyer F, John C (1981) At least three sequential steps are involved in the tetanus toxin-induced block of neuromuscular transmission. Naunyn Schmiedebergs Arch Pharmacol 317:326-330
104. Sieczkarski SB, Whittaker GR (2003) Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4:333-343
105. Simpson LL (1985) Pharmacological experiments on the binding and internalization of the 50, 000 dalton carboxyterminus of tetanus toxin at the cholinergic neuromuscular junction. J Pharmacol Exp Ther 234:100-105
106. Smith AE, Lilie H, Helenius A (2003) Ganglioside-dependent cell attachment and endocytosis of murine polyomavirus-like particles. FEBS Lett 555:199-203
107. Soo KY, Farg M, Atkin JD (2011) Molecular motor proteins and amyotrophic lateral sclerosis. Int J Mol Sci 12:9057-9082
108. Stiess M, Bradke F (2011) Neuronal transport: myosins pull the ER. Nat Cell Biol 13:10-11
109. Strotmeier J, Gu S, Jutzi S, Mahrhold S, Zhou J, Pich A, Eichner T, Bigalke H, Rummel A, Jin R, Binz T (2011) The biological activity of botulinum neurotoxin type C is dependent upon novel types of ganglioside binding sites. Mol Microbiol 81:143-156
110. Swaminathan S (2011) Molecular structures and functional relationships in clostridial neurotoxins. FEBS J 278:4467-4485
111. Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9:e1000604
112. Tsukamoto K, Kohda T, Mukamoto M, Takeuchi K, Ihara H, Saito M, Kozaki S (2005) Binding of Clostridium botulinum type C and D neurotoxins to ganglioside and phospholipid. Novel insights into the receptor for clostridial neurotoxins. J Biol Chem 280:35164-35171
113. Tsukamoto K, Kozai Y, Ihara H, Kohda T, Mukamoto M, Tsuji T, Kozaki S (2008) Identification of the receptor-binding sites in the carboxyl-terminal half of the heavy chain of botulinum neurotoxin types C and D. Microb Pathog 44:484-493
114. Tuffereau C, Schmidt K, Langevin C, Lafay F, Dechant G, Koltzenburg M (2007) The rabies virus glycoprotein receptor p75NTR is not essential for rabies virus infection. J Virol 81:13622-13630
115. Ugolini G (1995) Specificity of rabies virus as a transneuronal tracer of motor networks: transfer from hypoglossal motoneurons to connected second-order and higher order central nervous system cell groups. J Comp Neurol 356:457-480
116. Vale RD, Schnapp BJ, Reese TS, Sheetz MP (1985) Movement of organelles along filaments dissociated from the axoplasm of the squid giant axon. Cell 40:449-454
117. Verderio C, Coco S, Rossetto O, Montecucco C, Matteoli M (1999) Internalization and proteolytic action of botulinum toxins in CNS neurons and astrocytes. J Neurochem 73:372-379
118. Vidricaire G, Tremblay MJ (2005) Rab5 and Rab7, but not ARF6, govern the early events of HIV-1 infection in polarized human placental cells. J Immunol 175:6517-6530
119. Vonderheit A, Helenius A (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3:e233
120. Wiegand H, Erdmann G, Wellhöner HH (1976) 125I-labelled botulinum A neurotoxin: pharmacokinetics in cats after intramuscular injection. Naunyn-Schemiedeberg's Archives Pharmacoloy 292:161-165
121. Winckler B, Yap CC (2011) Endocytosis and endosomes at the crossroads of regulating trafficking of axon outgrowth-modifying receptors. Traffic 12:1099-1108
122. Yaar M, Zhai S, Pilch PF, Doyle SM, Eisenhauer PB, Fine RE, Gilchrest BA (1997) Binding of beta-amyloid to the p75 neurotrophin receptor induces apoptosis. A possible mechanism for Alzheimer's disease. J Clin Invest 100:2333-2340
123. Yamasaki S, Baumeister A, Binz T, Blasi J, Link E, Cornille F, Roques B, Fykse EM, Sudhof TC, Jahn R et al (1994) Cleavage of members of the synaptobrevin/VAMP family by types D and F botulinal neurotoxins and tetanus toxin. J Biol Chem 269:12764-12772
124. Yeh FL, Dong M, Yao J, Tepp WH, Lin G, Johnson EA, Chapman ER (2010) SV2 mediates entry of tetanus neurotoxin into central neurons. PLoS Pathog 6:e1001207
125. Yowler BC, Schengrund CL (2004) Glycosphingolipids-sweets for botulinum neurotoxin. Glycoconj J 21:287-293
126. Zhang Y, Varnum SM (2012) The receptor binding domain of botulinum neurotoxin serotype C binds phosphoinositides. Biochimie 94:920-923