Differential entry of botulinum neurotoxin a into neuronal and intestinal cells: An ultrastructural approach

Botulinum Journal

Volumn 1, Issue 4, 2010, Pages 375-392

  Couesnon, Aurélie ^a   Colasante, Cesare ^b,c   Molgó, Jordi ^c   Popoff, Michel R ^a  

^a INSTITUT PASTEUR   (France)

^b Universidad De Los Andes Facultad de Medicina   (Venezuela)

^c LABORATOIRE DE NEUROBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

Author keywords

BoNT; Botulinum neurotoxin; Botulism; Electron microscopy; Intestinal cell; Neuronal cell

Indexed keywords

BOTULINUM TOXIN A; CLATHRIN; DYNAMIN; INTERSECTIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ULTRASTRUCTURE; COATED VESICLE; CRYPT CELL; CYTOPLASM VESICLE; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; INTESTINE CELL; NERVE CELL;

EID: 79952855554     PISSN: 17547326     EISSN: 17547318     Source Type: Journal    
DOI: 10.1504/TBJ.2010.039113     Document Type: Article

References (54)

1. Ahsan, C.R., Hajnoczky, G., Maksymowych, A.B. and Simpson, L.L. (2005) 'Visualization of binding and transcytosis of botulinum toxin by human intestinal epithelial cells', J. Pharmacol. Exp. Ther., Vol. 315, pp.1028-1035. (Pubitemid 41635388)
2. Baldwin, M.R. and Barbieri, J.T. (2009) 'Association of botulinum neurotoxins with synaptic vesicle protein complexes', Toxicon., Vol. 54, pp.570-574.
3. Bens, M., Bogdanova, A., Cluzeaud, F., Miquerol, L., Kerneis, S., Kraehenbuhl, J.P., Kahn, A., Pringault, E. and Vandewalle, A. (1996) 'Transimmortalized mouse intestinal cells (M-Icc12) that maintain a crypt phenotype', Am. J. Physiol., Vol. 270, pp.C1666-C1674.
4. Bohnert, S. and Schiavo, G. (2005) 'Tetanus toxin is transported in a novel neuronal compartment characterized by a specialized pH regulation', J. Biol. Chem., Vol. 280, pp.42336-42344. (Pubitemid 43023205)
5. Bohnert, S., Deinhardt, K., Salinas, S. and Schiavo, G. (2006) 'Uptake and transport of clostridium neurotoxins', in Alouf, J.E. and Popoff, M.R. (Eds.): The Sourcebook of Comprehensive Bacterial Protein Toxins, 3rd ed., Elsevier Academic Press, Amsterdam, pp.390-408.
6. Brook, I. (2007) 'Infant botulism', J. Perinatol., Vol. 27, pp.175-180. (Pubitemid 46322649)
7. Brunger, A.T., Jin, R. and Breidenbach, M.A. (2008) 'Highly specific interactions between botulinum neurotoxins and synaptic vesicle proteins', Cell Mol. Life Sci., Vol. 65, pp.2296-2306.
8. Couesnon, A., Pereira, Y. and Popoff, M.R. (2008) 'Receptor-mediated transcytosis of botulinum neurotoxin A through intestinal cell monolayers', Cell. Microbiol., Vol. 10, pp.375-387.
9. Couesnon, A., Shimizu, T. and Popoff, M.R. (2009) 'Differential entry of botulinum neurotoxin A into neuronal and intestinal cells', Cell Microbiol., Vol. 11, pp.289-308.
10. 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., Vol. 162, pp.1293-1303. (Pubitemid 37210885)
11. 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, Vol. 312, pp.592-596.
12. Fernandez-Salas, E., Garay, P., Jacky, B., Dupuy, J., Wang, J., Nelson, J., Raymond, C.S. and Aoki, K.R. (2008) 'Identification of the fibroblast growth factor receptor Fgfr3 as a component of the receptor complex for botulinum neurotoxin type A', Toxicon, Vol. 51, Suppl. 1, p.3.
13. 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. USA, Vol. 106, pp.1330-1335.
14. Fujinaga, Y., Inoue, K., Watanabe, S., Yokota, K., Hirai, Y., Nagamachi, E. and Oguma, K. (1997) 'The haemagglutinin of Clostridium botulinum Type C progenitor toxin plays an essential role in binding of toxin to the epithelial cells of guinea pig intestine, leading to the efficient absorption of the toxin', Microbiol., Vol. 143, pp.3841-3847. (Pubitemid 28004616)
15. Fujinaga, Y., Matsumura, T., Jin, Y., Takegahara, Y. and Sugawara, Y. (2008) 'A novel function of botulinum toxin-associated proteins: Ha proteins disrupt intestinal epithelial barrier to increase toxin absorption', Toxicon, Vol. 54, No. 5, pp.583-586.
16. Herreros, J., Lalli, G., Montecucco, C. and Schiavo, G. (1999) 'Pathophysiological properties of clostridial neurotoxins', in Alouf, J.E. and Freer, J.H. (Eds.): The Comprehensive Sourcebook of Bacterial Protein Toxins, Academic Press, London, pp.202-228.
17. Hughson, E.J. and Hopkins, C.R. (1990) 'Endocytic pathways in polarized Caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces', J. Cell Biol., Vol. 110, pp.337-348.
18. Humeau, Y., Doussau, F., Grant, N.J. and Poulain, B. (2000) 'How botulinum and tetanus neurotoxins block neurotransmitter', Biochimie, Vol. 82, pp.427-446. (Pubitemid 30391899)
19. Jin, Y., Takegahara, Y., Sugawara, Y., Matsumura, T. and Fujinaga, Y. (2009) 'Disruption of the epithelial barrier by botulinum haemagglutinin (Ha) proteins - differences in cell tropism and the mechanism of action between Ha proteins of types A Or B, and Ha proteins of Type C', Microbiology, Vol. 155, pp.35-45.
20. Keller, J.E., Cai, F. and Neale, E.A. (2004) 'Uptake of botulinum neurotoxin into cultured neurons', Biochem., Vol. 43, pp.526-532. (Pubitemid 38082576)
21. Kitamura, M., Takamiya, K., Aizawa, S. and Furukawa, K. (1999) 'Gangliosides are the binding substances in neural cells for tetanus and botulinum toxins in mice', Biochem. Biophys. Acta, Vol. 1441, pp.1-3. (Pubitemid 29469431)
22. Klein, I.K., Predescu, D.N., Sharma, T., Knezevic, I., Malik, A.B. and Predescu, S. (2009) 'Intersectin-21 regulates caveola endocytosis secondary to Cdc42-mediated actin polymerization', J. Biol. Chem., Vol. 284, pp.25953-25961.
23. Kozaki, S., Kamata, Y., Watarai, S., Nishiki, T. and Mochida, S. (1998) 'Ganglioside Gt1b as a complementary receptor component for Clostridium botulinum neurotoxins', Microbiol. Pathol., Vol. 25, pp.91-99. (Pubitemid 28398979)
24. Kumari, S. and Mayor, S. (2008) 'Arf1 is directly involved in dynamin-independent endocytosis'. Nat. Cell Biol., Vol. 10, pp.30-41.
25. ntr', J. Cell Biol., Vol. 156, pp.233-239. (Pubitemid 34839905)
26. Lalli, G., Bohnert, S., Deinhardt, K., Verastegui, C. and Schiavo, G. (2003) 'The journey of tetanus and botulinum neurotoxins in neurons', Trends Microbiol., Vol. 11, pp.431-437. (Pubitemid 37101483)
27. Lamaze, C. and Johannes, L. (2006a) 'Intracellular trafficking of bacterial and plant protein toxins', in Alouf, J.E. and Popoff, M.R. (Eds.): The Sourcebook of Bacterial Protein Toxins, 3rd ed., Elsevier Academic Press, Amsterdam, pp.135-153.
28. Lamaze, C. and Johannes, L. (2006b) 'Intracellular trafficking of bacterial and plant toxins', in Alouf, J.E. and Popoff, M.R. (Eds.): The Comprehensive Sourcebook of Bacterial Protein Toxins, 3rd ed., Elsevier-Academic Press, Amsterdam, pp.135-153.
29. 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., Vol. 580, pp.2011-2014.
30. Maksymowych, A.B. and Simpson, L.I. (2004) 'Structural features of the botulinum neurotoxin molecule that govern binding and transcytosis across polarized human intestinal epithelial cells', J. Pharmacol. Exp. Ther., Vol. 210, pp.633-641. (Pubitemid 38988908)
31. Maksymowych, A.B. and Simpson, L.L. (1998) 'Binding and transcytosis of botulinum neurotoxin by polarized human carcinoma cells', J. Biol. Chem., Vol. 273, pp.21950-21957. (Pubitemid 28405374)
32. Maksymowych, A.B., Rienhard, M., Malizio, C.J., Goodnough, M.C., Johnson, E.A. and Simpson, L.L. (1999) 'Pure botulinum neurotoxin is absorbed from the stomach and small intestine and produces peripheral neuromuscular blockade', Infect. Immun., Vol. 67, pp.4708-4712. (Pubitemid 29400453)
33. Matsumura, T., Jin, Y., Kabumoto, Y., Takegahara, Y., Oguma, K., Lencer, W.I. and Fujinaga, Y. (2007) 'The Ha proteins of botulinum toxin disrupt intestinal epithelial intercellular junctions to increase toxin absorption', Cell Microbiol., Vol. 10, pp.355-364.
34. Matteoli, M., Verderio, C., Rossetto, O., Iezzi, N., Coco, S., Schiavo, G. and Montecucco, C. (1996) 'Synaptic vesicle endocytosis mediates the entry of tetanus neurotoxin into hippocampal neurons', Proc. Natl. Acad. Sci., USA, Vol. 93, pp.13310-13315. (Pubitemid 26382812)
35. Mayor, S. and Pagano, R.E. (2007) 'Pathways of clathrin-independent endocytosis', Nat. Rev. Mol. Cell Biol., Vol. 8, pp.603-612. (Pubitemid 47106613)
36. Meunier, F.A., Herreros, J., Schiavo, G., Poulain, B. and Molgo, J. (2002) 'Molecular mechanism of action of botulinal neurotoxins and the synaptic remodeling they induce in vivo at the skeletal neuromuscular junction', in Massaro, J. (Ed.): Handbook of Neurotoxicology, Humana Press, Totowa, NJ, pp.305-347.
37. Montecucco, C., Rossetto, O. and Schiavo, G. (2004) 'Presynaptic receptor arrays for clostridial neurotoxins', Trends Microbiol., Vol. 12, pp.442-446. (Pubitemid 39286121)
38. Nishikawa, A., Uotsu, N., Arimitsu, H., Lee, J.C., Miura, Y., Fujinaga, Y., Nakada, H., Watanabe, T., Ohyama, T., Sakano, Y. and Oguma, K. (2004) 'The receptor and transporter for internalization of Clostridium botulinum type C progenitor toxin into Ht-29 cells', Biochem. Biophys. Res. Commun., Vol. 319, pp.327-333. (Pubitemid 38725950)
39. Nishiki, T., Kamata, Y., Nemoto, Y., Omori, A., Ito, T., Takahashi, M. and Kozaki, S. (1994) 'Identification of protein receptor for Clostridium botulinum Type B neurotoxin in rat brain synaptosomes', J. Biol. Chem., Vol. 269, pp.10498-10503. (Pubitemid 24198248)
40. 1a', Febs Lett., Vol. 378, pp.253-257.
41. Park, J.B. and Simpson, L.L. (2003) 'Inhalation poisoning by botulinum toxin and inhalation vaccination with its heavy-chain component', Infect. Immun., Vol. 71, pp.1147-1154. (Pubitemid 36254295)
42. Poulain, B., Stiles, B.G., Popoff, M.R. and Molgo, J. (2006) 'Attack of the nervous system by clostridial toxins: physical findings, cellular and molecular actions', in Alouf, J.E. and Popoff, M.R. (Eds.): The Sourcebook of Bacterial Protein Toxins, 3rd ed., Academic Press, Amsterdam, Elsevier, pp.348-389.
43. Predescu, S.A., Predescu, D.N. and Malik, A.B. (2007) 'Molecular determinants of endothelial transcytosis and their role in endothelial permeability', Am. J. Physiol. Lung Cell Mol. Physiol., Vol. 293, pp.L823-L842. (Pubitemid 47572231)
44. Rummel, A., Karnath, T., Henke, T., Bigalke, H. and Binz, T. (2004a) 'Synaptotagmins I And Ii act as nerve cell receptors for botulinum neurotoxin G', J. Biol. Chem., Vol. 279, pp.30865-30870. (Pubitemid 38938022)
45. cc-domain of botulinum neurotoxins A and B exhibits a singular gangliosside binding site displaying serotype specific carbohydrate interaction', Mol. Microbiol., Vol. 51, pp.631-643. (Pubitemid 38233933)
46. Sabharanjak, S., Sharma, P., Parton, R.G. and Mayor, S. (2002) 'GPI-anchored proteins are delivered to recycling endosomes via a distinct Cdc42-regulated, clathrin-independent pinocytic pathway', Develop. Cell, Vol. 2, pp.411-423. (Pubitemid 34436571)
47. Schiavo, G., Matteoli, M. and Montecucco, C. (2000) 'Neurotoxins affecting neuroexocytosis', Physiol. Rev., Vol. 80, pp.717-766. (Pubitemid 30164948)
48. Sharma, D.K., Varma, R., Sarasij, R.C., Ira, Gousset, K., Krishnamoorthy, G., Rao, M. and Mayor, S. (2004) 'Nanoscale organization of multiple GPI-anchored proteins in living cell membranes', Cell, Vol. 116, pp.577-589. (Pubitemid 38264434)
49. Simpson, L.L., Coffield, J.A. and Bakry, N. (1994) 'Inhibition of vacuolar adenosine triphosphatase antagonizes the effects of clostridial neurotoxins but not phospholipase A2 neurotoxins', J. Pharmacol. Exp. Ther., Vol. 269, pp.256-262. (Pubitemid 24143262)
50. Sobel, J. (2005) 'Botulism', Clin. Infect. Dis., Vol. 41, pp.1167-1173. (Pubitemid 41429481)
51. Tacket, C.O. and Rogawski, M.A. (1989) 'Botulism', in Simpson, L.L. (Ed.): Botulinum Neurotoxin and Tetanus Toxin, Academic Press, San Diego, pp.351-378.
52. Tavallaie, M., Chenal, A., Gillet, D., Pereira, Y., Manich, M., Gibert, M., Raffestin, S., Popoff, M.R. and Marvaud, J.C. (2004) 'Interaction between the two subdomains of the C-terminal part of the botulinum neurotoxin A is essential for the generation of protective antibodies', Febs. Lett., Vol. 572, pp.299-306. (Pubitemid 39092553)
53. Uotsu, N., Nishikawa, A., Watanabe, T., Ohyama, T., Tonozuka, T., Sakano, Y. and Oguma, K. (2005) 'Cell internalization and traffic pathway of Clostridium Botulinum Type C neurotoxin in Ht-29 cells', Biochim. Biophys. Acta, Vol. 1763, pp.120-128. (Pubitemid 43208739)
54. Verderio, C., Grumelli, C., Raiteri, L., Coco, S., Paluzzi, S., Caccin, P., Rossetto, O., Bonanno, G., Montecucco, C. and Matteoli, M. (2007) 'Traffic of botulinum toxins A and E in excitatory and inhibitory neurons', Traffic, Vol. 8, pp.142-153. (Pubitemid 46100001)