Molecular components required for resting and stimulated endocytosis of botulinum neurotoxins by glutamatergic and peptidergic neurons

FASEB Journal

Volumn 27, Issue 8, 2013, Pages 3167-3180

  Meng, Jianghui ^a   Wang, Jiafu ^a   Lawrence, Gary W ^a   Dolly, J Oliver ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

Amphiphysin; AP2; Clathrin; Dynamin; Large dense core vesicles; Small clear synaptic vesicles

Indexed keywords

ADAPTOR PROTEIN; AMPHIPHYSIN; BOTULINUM TOXIN; CLATHRIN; DYNAMIN; SYNTHETIC DNA; ADAPTOR PROTEIN COMPLEX 2, ALPHA 2 SUBUNIT; ALPHA ADAPTIN; BOTULINUM TOXIN B; GLUTAMIC ACID; ISOPROTEIN; NERVE PROTEIN; NEUROTOXIN; PEPTIDE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; ENDOCYTOSIS; GENE EXPRESSION; GENETIC TRANSFECTION; GLUTAMATERGIC NERVE CELL; LARGE DENSE CORE VESICLE; MEMBRANE DEPOLARIZATION; MOLECULAR BIOLOGY; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SMALL CLEAR SYNAPTIC VESICLE; SYNAPSE VESICLE; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTATION; NERVE CELL; RNA INTERFERENCE; SECRETORY VESICLE; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE;

ADAPTOR PROTEIN COMPLEX 2; ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ANIMALS; BOTULINUM TOXINS; CELLS, CULTURED; CLATHRIN; DYNAMINS; ENDOCYTOSIS; GLUTAMIC ACID; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MUTATION; NERVE TISSUE PROTEINS; NEURONS; NEUROTOXINS; PEPTIDES; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SECRETORY VESICLES; SYNAPTIC VESICLES;

EID: 84881141444     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-228973     Document Type: Article

References (73)

1. Montal, M. (2010) Botulinum neurotoxin: a marvel of protein design. Annu. Rev. Biochem. 79, 591-617
2. Davletov, B., Bajohrs, M., and Binz, T. (2005) Beyond BOTOX: advantages and limitations of individual botulinum neurotoxins. Trends Neurosci. 28, 446-452
3. Dolly, J. O., Wang, J., Zurawski, T. H., and Meng, J. (2011) Novel therapeutics based on recombinant botulinum neurotoxins to normalize the release of transmitters and pain mediators. FEBS J. 278, 4454-4466
4. Dodick, D. W., Turkel, C. C., DeGryse, R. E., Aurora, S. K., Silberstein, S. D., Lipton, R. B., Diener, H. C., and Brin, M. F. (2010) OnabotulinumtoxinA for treatment of chronic migraine: pooled results from the double-blind, randomized, placebo-controlled phases of the PREEMPT clinical program. Headache 50, 921-936
5. Jackson, J. L., Kuriyama, A., and Hayashino, Y. (2012) Botulinum toxin A for prophylactic treatment of migraine and tension headaches in adults: a meta-analysis. JAMA 307, 1736-1745
6. Peng, L., Tepp, W. H., Johnson, E. A., and Dong, M. (2011) Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors. PLoS Pathog. 7, e1002008
7. Dong, M., Yeh, F., Tepp, W. H., Dean, C., Johnson, E. A., Janz, R., and Chapman, E. R. (2006) SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592-596
8. Mahrhold, S., Rummel, A., Bigalke, H., Davletov, B., and Binz, T. (2006) The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 580, 2011-2014
9. Dong, M., Liu, H., Tepp, W. H., Johnson, E. A., Janz, R., and Chapman, E. R. (2008) Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol. Biol. Cell 19, 5226-5237
10. Fu, Z., Chen, C., Barbieri, J. T., Kim, J. J., and Baldwin, M. R. (2009) Glycosylated SV2 and gangliosides as dual receptors for botulinum neurotoxin serotype F. Biochemistry 48, 5631-5641
11. Rummel, A., Hafner, K., Mahrhold, S., Darashchonak, N., Holt, M., Jahn, R., Beermann, S., Karnath, T., Bigalke, H., and Binz, T. (2009) Botulinum neurotoxins C, E and F bind gangliosides via a conserved binding site before stimulation-dependent uptake with botulinum neurotoxin F utilising the three isoforms of SV2 as second receptor. J. Neurochem. 110, 1942-1954
12. Rummel, A., Karnath, T., Henke, T., Bigalke, H., and Binz, T. (2004) Synaptotagmins I and II act as nerve cell receptors for botulinum neurotoxin G. J. Biol. Chem. 279, 30865-30870
13. Jin, R., Rummel, A., Binz, T., and Brunger, A. T. (2006) Botulinum neurotoxin B recognizes its protein receptor with high affinity and specificity. Nature 444, 1092-1095
14. Dong, M., Tepp, W. H., Liu, H., Johnson, E. A., and Chapman, E. R. (2007) Mechanism of botulinum neurotoxin B and G entry into hippocampal neurons. J. Cell Biol. 179, 1511-1522
15. Dong, M., Richards, D. A., Goodnough, M. C., Tepp, W. H., Johnson, E. A., and Chapman, E. R. (2003) Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells. J. Cell Biol. 162, 1293-1303
16. Dolly, J. O., Black, J., Williams, R. S., and Melling, J. (1984) Acceptors for botulinum beurotoxin reside on motor-nerve terminals and mediate its internalization. Nature 307, 457-460
17. Simpson, L. L. (1980) Kinetic studies on the interaction between botulinum toxin type A and the cholinergic neuromuscular junction. J. Pharmacol. Exp. Ther. 212, 16-21
18. Black, J. D., and Dolly, J. O. (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
19. Partoens, P., Slembrouck, D., Quatacker, J., Baudhuin, P., Courtoy, P. J., and De Potter, W. P. (1998) Retrieved constituents of large dense-cored vesicles and synaptic vesicles intermix in stimulation-induced early endosomes of noradrenergic neurons. J. Cell Sci. 111, 681-689
20. Fischer, A., Nakai, Y., Eubanks, L. M., Clancy, C. M., Tepp, W. H., Pellett, S., Dickerson, T. J., Johnson, E. A., Janda, K. D., and Montal, M. (2009) Bimodal modulation of the botulinum neurotoxin protein-conducting channel. Proc. Natl. Acad. Sci. U. S. A. 106, 1330-1335
21. Ferguson, S. M., and De Camilli, P. (2012) Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13, 75-88
22. Harper, C. B., Martin, S., Nguyen, T. H., Daniels, S. J., Lavidis, N. A., Popoff, M. R., Hadzic, G., Mariana, A., Chau, N., McCluskey, A., Robinson, P. J., and Meunier, F. A. (2011) Dynamin inhibition blocks botulinum neurotoxin type A endocytosis in neurons and delays botulism. J. Biol. Chem. 286, 35966-35976
23. Haucke, V., and De Camilli, P. (1999) AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285, 1268-1271
24. Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R., and Owen, D. J. (2002) Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523-535
25. Zhang, J. Z., Davletov, B. A., Sudhof, T. C., and Anderson, R. G. (1994) Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78, 751-760
26. Couesnon, A., Shimizu, T., and Popoff, M. R. (2009) Differential entry of botulinum neurotoxin A into neuronal and intestinal cells. Cell. Microbiol. 11, 289-308
27. Lichte, B., Veh, R. W., Meyer, H. E., and Kilimann, M. W. (1992) Amphiphysin, a novel protein associated with synaptic vesicles. EMBO J. 11, 2521-2530
28. Wigge, P., Kohler, K., Vallis, Y., Doyle, C. A., Owen, D., Hunt, S. P., and McMahon, H. T. (1997) Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol. Biol. Cell 8, 2003-2015
29. Wang, J., Meng, J., Lawrence, G. W., Zurawski, T. H., Sasse, A., Bodeker, M. O., Gilmore, M. A., Fernandez-Salas, E., Francis, J., Steward, L. E., Aoki, K. R., and Dolly, J. O. (2008) Novel chimeras of botulinum neurotoxins A and E unveil contributions from the binding, translocation, and protease domains to their functional characteristics. J. Biol. Chem. 283, 16993-17002
30. Wang, J., Zurawski, T. H., Meng, J., Lawrence, G., Olango, W. M., Finn, D. P., Wheeler, L., and Dolly, J. O. (2011) A dileucine in the protease of botulinum toxin A underlies its long-lived neuroparalysis: transfer of longevity to a novel potential therapeutic. J. Biol. Chem. 286, 6375-6385
31. Wang, J., Zurawski, T. H., Bodeker, M. O., Meng, J., Boddul, S., Aoki, K. R., and Dolly, J. O. (2012) Longer-acting and highly potent chimaeric inhibitors of excessive exocytosis created with domains from botulinum neurotoxin A and B. Biochem. J. 444, 59-67
32. Meng, J., Wang, J., Lawrence, G., and Dolly, J. O. (2007) Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential. J. Cell Sci. 120, 2864-2874
33. Meng, J., Ovsepian, S. V., Wang, J., Pickering, M., Sasse, A., Aoki, K. R., Lawrence, G. W., and Dolly, J. O. (2009) Activation of TRPV1 mediates calcitonin gene-related peptide release, which excites trigeminal sensory neurons and is attenuated by a retargeted botulinum toxin with anti-nociceptive potential. J. Neurosci. 29, 4981-4992
34. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., and Kirchhausen, T. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850
35. Doherty, G. J., and McMahon, H. T. (2009) Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902
36. Mayor, S., and Pagano, R. E. (2007) Pathways of clathrinindependent endocytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612
37. Von Kleist, L., Stahlschmidt, W., Bulut, H., Gromova, K., Puchkov, D., Robertson, M. J., MacGregor, K. A., Tomilin, N., Pechstein, A., Chau, N., Chircop, M., Sakoff, J., von Kries, J. P., Saenger, W., Krausslich, H. G., Shupliakov, O., Robinson, P. J., McCluskey, A., and Haucke, V. (2011) Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146, 471-484
38. Urrutia, R., Henley, J. R., Cook, T., and McNiven, M. A. (1997) The dynamins: redundant or distinct functions for an expanding family of related GTPases? Proc. Natl. Acad. Sci. U. S. A. 94, 377-384
39. Cao, H., Garcia, F., and McNiven, M. A. (1998) Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell. 9, 2595-2609
40. Yao, J., Kwon, S. E., Gaffaney, J. D., Dunning, F. M., and Chapman, E. R. (2011) Uncoupling the roles of synaptotagmin I during endo-and exocytosis of synaptic vesicles. Nat. Neurosci. 15, 243-249
41. Lowe, A. W., Madeddu, L., and Kelly, R. B. (1988) Endocrine secretory granules and neuronal synaptic vesicles have three integral membrane proteins in common. J. Cell Biol. 106, 51-59
42. Ferguson, S. M., Brasnjo, G., Hayashi, M., Wolfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L. W., Ariel, P., Paradise, S., O'Toole, E., Flavell, R., Cremona, O., Miesenbock, G., Ryan, T. A., and De Camilli, P. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316, 570-574
43. Matteoli, M., Takei, K., Perin, M. S., Sudhof, T. C., and De Camilli, P. (1992) Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol. 117, 849-861
44. Zhu, Y., Xu, J., and Heinemann, S. F. (2009) Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron 61, 397-411
45. Bauerfeind, R., Takei, K., and De Camilli, P. (1997) Amphiphysin I is associated with coated endocytic intermediates and undergoes stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 272, 30984-30992
46. Liu, J. P., Sim, A. T., and Robinson, P. J. (1994) Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265, 970-973
47. Soderberg, O., Gullberg, M., Jarvius, M., Ridderstrale, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000
48. Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., and Sanes, J. R. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51
49. Chai, Q., Arndt, J. W., Dong, M., Tepp, W. H., Johnson, E. A., Chapman, E. R., and Stevens, R. C. (2006) Structural basis of cell surface receptor recognition by botulinum neurotoxin B. Nature 444, 1096-1100
50. Restani, L., Giribaldi, F., Manich, M., Bercsenyi, K., Menendez, G., Rossetto, O., Caleo, M., and Schiavo, G. (2012) Botulinum neurotoxins A and E undergo retrograde axonal transport in primary motor neurons. PLoS Pathog. 8, e1003087
51. Black, J. D., and Dolly, J. O. (1986) Interaction of 125I-labeled botulinum neurotoxins with nerve terminals. I. Ultrastructural autoradiographic localization and quantitation of distinct membrane acceptors for types A and B on motor nerves. J. Cell Biol. 103, 521-534
52. Yowler, B. C., Kensinger, R. D., and Schengrund, C. L. (2002) Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J. Biol. Chem. 277, 32815-32819
53. Kirkham, M., and Parton, R. G. (2005) Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim. Biophys. Acta 1745, 273-286
54. Chung, C., Barylko, B., Leitz, J., Liu, X., and Kavalali, E. T. (2010) Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J. Neurosci. 30, 1363-1376
55. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S., and Parton, R. G. (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465-476
56. Hesse, S., Jahnke, M. T., Luecke, D., and Mauritz, K. H. (1995) Short-term electrical stimulation enhances the effectiveness of botulinum toxin in the treatment of lower limb spasticity in hemiparetic patients. Neurosci. Lett. 201, 37-40
57. Yiangou, Y., Anand, U., Otto, W. R., Sinisi, M., Fox, M., Birch, R., Foster, K. A., Mukerji, G., Akbar, A., Agarwal, S. K., and Anand, P. (2011) Increased levels of SV2A botulinum neurotoxin receptor in clinical sensory disorders and functional effects of botulinum toxins A and E in cultured human sensory neurons. J. Pain Res. 4, 347-355
58. Binz, T., and Rummel, A. (2009) Cell entry strategy of clostridial neurotoxins. J. Neurochem. 109, 1584-1595
59. Yao, J., Nowack, A., Kensel-Hammes, P., Gardner, R. G., and Bajjalieh, S. M. (2010) Cotrafficking of SV2 and synaptotagmin at the synapse. J. Neurosci. 30, 5569-5578
60. Kasprowicz, J., Kuenen, S., Miskiewicz, K., Habets, R. L., Smitz, L., and Verstreken, P. (2008) Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J. Cell Biol. 182, 1007-1016
61. Clayton, E. L., Anggono, V., Smillie, K. J., Chau, N., Robinson, P. J., and Cousin, M. A. (2009) The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J. Neurosci. 29, 7706-7717
62. Granseth, B., Odermatt, B., Royle, S. J., and Lagnado, L. (2006) Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773-786
63. Clayton, E. L., and Cousin, M. A. (2009) The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J. Neurochem. 111, 901-914
64. Clayton, E. L., Sue, N., Smillie, K. J., O'Leary, T., Bache, N., Cheung, G., Cole, A. R., Wyllie, D. J., Sutherland, C., Robinson, P. J., and Cousin, M. A. (2010) Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat. Neurosci. 13, 845-851
65. Voglmaier, S. M., Kam, K., Yang, H., Fortin, D. L., Hua, Z., Nicoll, R. A., and Edwards, R. H. (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51, 71-84
66. Newell-Litwa, K., Seong, E., Burmeister, M., and Faundez, V. (2007) Neuronal and non-neuronal functions of the AP-3 sorting machinery. J. Cell Sci. 120, 531-541
67. Cheung, G., and Cousin, M. A. (2012) Adaptor protein complexes 1 and 3 are essential for generation of synaptic vesicles from activity-dependent bulk endosomes. J. Neurosci. 32, 6014-6023
68. Tomizawa, K., Sunada, S., Lu, Y. F., Oda, Y., Kinuta, M., Ohshima, T., Saito, T., Wei, F. Y., Matsushita, M., Li, S. T., Tsutsui, K., Hisanaga, S., Mikoshiba, K., Takei, K., and Matsui, H. (2003) Cophosphorylation of amphiphysin I and dynamin I by Cdk5 regulates clathrin-mediated endocytosis of synaptic vesicles. J. Cell Biol. 163, 813-824
69. Allan, V. J., Thompson, H. M., and McNiven, M. A. (2002) Motoring around the Golgi. Nat. Cell Biol. 4, E236-242
70. Raimondi, A., Ferguson, S. M., Lou, X., Armbruster, M., Paradise, S., Giovedi, S., Messa, M., Kono, N., Takasaki, J., Cappello, V., O'Toole, E., Ryan, T. A., and De Camilli, P. (2011) Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70, 1100-1114
71. Deinhardt, K., Berninghausen, O., Willison, H. J., Hopkins, C. R., and Schiavo, G. (2006) Tetanus toxin is internalized by a sequential clathrin-dependent mechanism initiated within lipid microdomains and independent of epsi n1. J. Cell Biol. 174, 459-471
72. Artalejo, C. R., Elhamdani, A., and Palfrey, H. C. (2002) Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin-and dynamin-2-mediated slow endocytosis in chromaffin cells. Proc. Natl. Acad. Sci. U. S. A. 99, 6358-6363
73. Verhage, M., McMahon, H. T., Ghijsen, W. E., Boomsma, F., Scholten, G., Wiegant, V. M., and Nicholls, D. G. (1991) Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6, 517-524