Tetanus and tetanus neurotoxin: From peripheral uptake to central nervous tissue targets.
inhibitory interneurons
metalloprotease
retroaxonal transport
tetanus
tetanus neurotoxin
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
28
01
2021
received:
03
11
2020
accepted:
15
02
2021
pubmed:
26
2
2021
medline:
18
11
2021
entrez:
25
2
2021
Statut:
ppublish
Résumé
Tetanus is a deadly but preventable disease caused by a protein neurotoxin produced by Clostridium tetani. Spores of C. tetani may contaminate a necrotic wound and germinate into a vegetative bacterium that releases a toxin, termed tetanus neurotoxin (TeNT). TeNT enters the general circulation, binds to peripheral motor neurons and sensory neurons, and is transported retroaxonally to the spinal cord. It then enters inhibitory interneurons and blocks the release of glycine or GABA causing a spastic paralysis. This review attempts to correlate the metalloprotease activity of TeNT and its trafficking and localization into the vertebrate body to the nature and sequence of appearance of the symptoms of tetanus.
Substances chimiques
Neurotoxins
0
Tetanus Toxin
0
Tetanus Toxoid
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1244-1253Informations de copyright
© 2021 International Society for Neurochemistry.
Références
Ablett, J. J. L. (1956). Tetanus and the anaesthetist: A review of the symptomatology and the recent advances in treatment. British Journal of Anaesthesia, 28, 258-273. https://doi.org/10.1093/bja/28.6.258
Azarnia Tehran, D., Pirazzini, M., Leka, O., Mattarei, A., Lista, F., Binz, T., Rossetto, O., & Montecucco, C. (2017). Hsp90 is involved in the entry of clostridial neurotoxins into the cytosol of nerve terminals. Cellular Microbiology, 19, https://doi.org/10.1111/cmi.12647
Behring, E. V., & Kitasato, S. (1890). Ueber das Zustandekommen der Diphtherie-Immunität und der Tetanus-Immunität bei Thieren. Deutsche Medizinische Wochenschrift, 49, 1113-1114.
Bercsenyi, K., Giribaldi, F., & Schiavo, G. (2013). The elusive compass of clostridial neurotoxins: Deciding when and where to go? Current Topics in Microbiology and Immunology, 364, 91-113.
Bercsenyi, K., Schmieg, N., Bryson, J. B., Wallace, M., Caccin, P., Golding, M., Zanotti, G., Greensmith, L., Nischt, R., & Schiavo, G. (2014). Nidogens are therapeutic targets for the prevention of tetanus. Science, 346, 1118-1123. https://doi.org/10.1126/science.1258138
Betley, J. N., Wright, C. V., Kawaguchi, Y., Erdélyi, F., Szabó, G., Jessell, T. M., & Kaltschmidt, J. A. (2009). Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell, 139, 161-174. https://doi.org/10.1016/j.cell.2009.08.027
Binz, T., & Rummel, A. (2009). Cell entry strategy of clostridial neurotoxins. Journal of Neurochemistry, 109, 1584-1595. https://doi.org/10.1111/j.1471-4159.2009.06093.x
Brooks, V. B., Curtis, D. R., & Eccles, J. C. (1955). Mode of action of tetanus toxin. Nature, 175, 120-121. https://doi.org/10.1038/175120b0
Brooks, V. B., Curtis, D. R., & Eccles, J. C. (1957). The action of tetanus toxin on the inhibition of motoneurones. Journal of Physiology, 135, 655-672. https://doi.org/10.1113/jphysiol.1957.sp005737
Bruggemann, H., Baumer, S., Fricke, W. F., Wiezer, A., Liesegang, H., Decker, I., Herzberg, C., Martinez-Arias, R., Merkl, R., Henne, A., & Gottschalk, G. (2003). The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proceedings of the National Academy of Sciences of the United States of America, 100, 1316-1321. https://doi.org/10.1073/pnas.0335853100
Bruggemann, H., Brzuszkiewicz, E., Chapeton-Montes, D., Plourde, L., Speck, D., & Popoff, M. R. (2015). Genomics of Clostridium tetani. Research in Microbiology, 166, 326-331. https://doi.org/10.1016/j.resmic.2015.01.002
Carle, A., & Rattone, G. (1884). Studio sperimentale sull’eziologia del tetano (Experimental studies of the etiology of tetanus). Giorn. Accad. Med. Torino, 32, 174-179.
Chapeton-Montes, D., Plourde, L., Bouchier, C., Ma, L., Diancourt, L., Criscuolo, A., Popoff, M. R., & Brüggemann, H. (2019). The population structure of Clostridium tetani deduced from its pan-genome. Scientific Reports, 9, 11220., https://doi.org/10.1038/s41598-019-47551-4
Charlier, C. M., Debaisieux, S., Foret, C., Thouard, A., Schiavo, G., Gonzalez-Dunia, D., & Malnou, C. E. (2016). Neuronal retrograde transport of Borna disease virus occurs in signalling endosomes. Journal of General Virology, 97, 3215-3224.
Chen, C., Fu, Z., Kim, J. J., Barbieri, J. T., & Baldwin, M. R. (2009). Gangliosides as high affinity receptors for tetanus neurotoxin. Journal of Biological Chemistry, 284(39), 26569-26577
Chen, S., & Barbieri, J. T. (2008). Substrate recognition of VAMP-2 by botulinum neurotoxin B and tetanus neurotoxin. Journal of Biological Chemistry, 283, 21153-21159.
Cohen, J. E., Wang, R., Shen, R. F., Wu, W. W., & Keller, J. E. (2017). Comparative pathogenomics of Clostridium tetani. PLoS One, 12, e0182909.-https://doi.org/10.1371/journal.pone.0182909
Cook, T. M., Protheroe, R. T., & Handel, J. M. (2001). Tetanus: A review of the literature. British Journal of Anaesthesia, 87, 477-487. https://doi.org/10.1093/bja/87.3.477
Curtis, D. R., Game, C. J., Lodge, D., & McCulloch, R. M. (1976). A pharmacological study of Renshaw cell inhibition. Journal of Physiology, 258, 227-242. https://doi.org/10.1113/jphysiol.1976.sp011416
Deinhardt, K., Salinas, S., Verastegui, C., Watson, R., Worth, D., Hanrahan, S., Bucci, C., & Schiavo, G. (2006). Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron, 52, 293-305. https://doi.org/10.1016/j.neuron.2006.08.018
Deppe, J., Weisemann, J., Mahrhold, S., & Rummel, A. (2020). The 25 kDa HCN domain of clostridial neurotoxins is indispensable for their neurotoxicity. Toxins, 12, https://doi.org/10.3390/toxins12120743
Dong, M., Masuyer, G., & Stenmark, P. (2019). Botulinum and tetanus neurotoxins. Annual Review of Biochemistry, 88, 811-837. https://doi.org/10.1146/annurev-biochem-013118-111654
Egawa, G., Nakamizo, S., Natsuaki, Y., Doi, H., Miyachi, Y., & Kabashima, K. (2013). Intravital analysis of vacular permeability in mice using two-photon microscopy. Scientific Reports, 3, 1932.
Erdmann, G., Wiegand, H., & Wellhöner, H. H. (1975). Intraaxonal and extraaxonal transport of 125I-tetanus toxin in early local tetanus. Naunyn-Schmiedeberg's Archives of Pharmacology, 290, 357-373. https://doi.org/10.1007/BF00499949
Faber, K. (1890). Die Pathogenie des Tetanus [The pathogenesis of tetanus]. Berl. klin. Wochenschr, 27, 717-720.
Fischer, A., & Montal, M. (2007a). Single molecule detection of intermediates during botulinum translocation across membranes. Proceedings of the National Academy of Sciences of the United States of America, 104, 10447-10452.
Fischer, A., & Montal, M. (2007b). Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. Journal of Biological Chemistry, 282, 29604-29611. https://doi.org/10.1074/jbc.M703619200
Gluska, S., Zahavi, E. E., Chein, M., Gradus, T., Bauer, A., Finke, S., & Perlson, E. (2014). Rabies virus hijacks and accelerates the p75NTR retrograde axonal transport machinery. PLoS Path, 10(8), e1004348.-https://doi.org/10.1371/journal.ppat.1004348
Gonzales, Y., Tucker, R. D., & Frazee, B. (2014). View from the front lines: An emergency medicine perspective on clostridial infections in injection drug users. Anaerobe, 30, 108-115. https://doi.org/10.1016/j.anaerobe.2014.09.005
Goulding, M. (2009). Circuits controlling vertebrate locomotion: Moving in a new direction. Nature Reviews Neuroscience, 10, 507-518. https://doi.org/10.1038/nrn2608
Habermann, E., & Dimpfel, W. (1973). Distribution of 125I-tetanus toxin and 125I-toxoid in rats with generalized tetanus, as influenced by antitoxin. Naunyn-Schmiedeberg's Archives of Pharmacology, 276, 327-340. https://doi.org/10.1007/BF00499887
Hortnagl, H., Brucke, T. H., & Hackl, J. M. (1979). The involvement of the sympathetic nervous system in tetanus. Klin Wochen, 57, 383-389. https://doi.org/10.1007/BF01480476
Ikeda, K., & Bekkers, J. M. (2009). Counting the number of releasable synaptic vesicles in a presynaptic terminal. Proceedings of the National Academy of Sciences of the United States of America, 106, 2945-2950. https://doi.org/10.1073/pnas.0811017106
Jacobsson, G., Piehl, F., & Meister, B. (1998). VAMP-1 and VAMP-2 gene expression in rat spinal motoneurones: Differential regulation after neuronal injury. European Journal of Neuroscience, 10, 301-316. https://doi.org/10.1046/j.1460-9568.1998.00050.x
Johnson, E. A., & Montecucco, C. (2008). Botulism. Handbook of Clinical Neurology, 91, 333-368.
Kanda, K., & Takano, K. (1983). Effect of tetanus toxin on the excitatory and the inhibitory post-synaptic potentials in the cat motoneurone. Journal of Physiology, 335, 319-333. https://doi.org/10.1113/jphysiol.1983.sp014536
Kitasato, S. (1889). Ueber den Tetanus bacillus (On the tetanus bacillus). Z. Hyg. Infekt. Kr., 7, 225-233. https://doi.org/10.1007/BF02188336
Lalli, G., & Schiavo, G. (2002). Analysis of retrograde transport in motor neurons reveals common endocytic carriers for tetanus toxin and neurotrophin receptor p75NTR. Journal of Cell Biology, 156, 233-239. https://doi.org/10.1083/jcb.200106142
Leak, L. V. (1971). Studies on the permeability of lymphatic capillaries. Journal of Cell Biology, 50, 300-323. https://doi.org/10.1083/jcb.50.2.300
Mallick, I. H., & Winslet, M. C. (2004). A review of the epidemiology, pathogenesis and management of tetanus. International Journal of Surgery, 2, 109-112. https://doi.org/10.1016/S1743-9191(06)60056-3
Masuyer, G., Conrad, J., & Stenmark, P. (2017). The structure of the tetanus toxin reveals pH-mediated domain dynamics. EMBO Reports, 18, 1306-1317.
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. Proceedings of the National Academy of Sciences of the United States of America, 93, 13310-13315. https://doi.org/10.1073/pnas.93.23.13310
Meckler, R. L., Baron, R., & McLachlan, E. M. (1990). Selective uptake of C-fragment of tetanus toxin by sympathetic preganglionic nerve terminals. Neuroscience, 36, 823-829. https://doi.org/10.1016/0306-4522(90)90025-Y
Montal, M. (2017). Tetanus neurotoxin: Conformational plasticity as an adaptive strategy. EMBO Reports, 18, 1268-1270. https://doi.org/10.15252/embr.201744500
Montecucco, C. (1986). How do tetanus and botulinum toxins bind to neuronal membranes? Trends in Biochemical Sciences, 11, 314-317. https://doi.org/10.1016/0968-0004(86)90282-3
Montecucco, C., Rossetto, O., & Schiavo, G. (2004). Presynaptic receptor arrays for clostridial neurotoxins. Trends in Microbiology, 12, 442-446. https://doi.org/10.1016/j.tim.2004.08.002
Njuguna, H. N., Yusuf, N., Raza, A. A., Ahmed, B., & Tohme, R. A. (2020). Progress toward maternal and neonatal tetanus elimination - worldwide, 2000-2018. MMWR. Morbidity and Mortality Weekly Report, 69, 515-520. https://doi.org/10.15585/mmwr.mm6917a2
Ohka, S., & Nomoto, A. (2001). The molecular basis of poliovirus neurovirulence. Developmental Biology, 105, 51-58.
Paar, G. H., & Wellhöner, H. H. (1973). The action of tetanus toxin on preganglionic sympathetic reflex discharges. Naunyn-Schmiedeberg's Arch. Pharmacol, 276, 437-445.
Pantano, S., & Montecucco, C. (2014). The botulinum neurotoxins and the neuroexocytosis apparatus. Cellular and Molecular Life Sciences, 71, 793-811. https://doi.org/10.1007/s00018-013-1380-7
Pappas, G., Kiriaze, I. J., & Falagas, M. E. (2008). Insights into infectious disease in the era of Hippocrates. International Journal of Infectious Diseases, 12, 347-350. https://doi.org/10.1016/j.ijid.2007.11.003
Patarnello, T., Bargelloni, L., Rossetto, O., Schiavo, G., & Montecucco, C. (1993). Neurotransmission and secretion. Nature, 364, 581-582. https://doi.org/10.1038/364581b0
Phillips, L. A. (1967). A classification of tetanus. Lancet, 289, P1216-1217. https://doi.org/10.1016/S0140-6736(67)92858-9
Pirazzini, M., Azarnia Tehran, D., Leka, O., Zanetti, G., Rossetto, O., & Montecucco, C. (2016). On the translocation of botulinum and tetanus neurotoxins across the membrane of acidic intracellular compartments. Biochimica Et Biophysica Acta, 1858, 467-474. https://doi.org/10.1016/j.bbamem.2015.08.014
Pirazzini, M., Bordin, F., Rossetto, O., Shone, C. C., Binz, T., & Montecucco, C. (2013). The thioredoxin reductase-thioredoxin system is involved in the entry of tetanus and botulinum neurotoxins in the cytosol of nerve terminals. FEBS Letters, 587, 150-155. https://doi.org/10.1016/j.febslet.2012.11.007
Pirazzini, M., Rossetto, O., Eleopra, R., & Montecucco, C. (2017). Botulinum neurotoxins: Biology, pharmacology, and toxicology. Pharmacological Reviews, 69, 200-235. https://doi.org/10.1124/pr.116.012658
Proux-Gillardeaux, V., Rudge, R., & Galli, T. (2005). The tetanus neurotoxin-sensitive and insensitive routes to and from the plasma membrane: Fast and slow pathways? Traffic, 6, 366-373.
Ramírez-Jarquín, U. N., & Tapia, R. (2018). Excitatory and Inhibitory Neuronal Circuits in the Spinal Cord and Their Role in the Control of Motor Neuron Function and Degeneration. ACS Chem Neurosci, 9, 211-216. https://doi.org/10.1021/acschemneuro.7b00503
Rossetto, O., & Montecucco, C. (2019). Tables of toxicity of botulinum and tetanus neurotoxins. Toxins (Basel), 11, pii: E686. https://doi.org/10.3390/toxins11120686
Rummel, A. (2013). Double receptor anchorage of botulinum neurotoxins accounts for their exquisite neurospecificity. Current Topics in Microbiology and Immunology, 364, 61-90.
Rummel, A. (2017). Two feet on the membrane: Uptake of clostridial neurotoxins. Current Topics in Microbiology and Immunology, 406, 1-37.
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. Journal of Molecular Biology, 326, 835-847. https://doi.org/10.1016/S0022-2836(02)01403-1
Rybak, I. A., Dougherty, K. J., & Shevtsova, N. A. (2015) Organization of the mammalian locomotor CPG: Review of computational model and circuit architectures based on genetically identified spinal interneurons. Eneuro, 2(5). https://doi.org/10.1523/ENEURO.0069-15.2015
Salinas, S., Schiavo, G., & Kremer, E. J. (2010). A hitchhiker's guide to the nervous system: The complex journey of viruses and toxins. Nature Reviews Microbiology, 8, 645-655. https://doi.org/10.1038/nrmicro2395
Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B. R., & Montecucco, C. (1992). Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature, 359, 832-835. https://doi.org/10.1038/359832a0
Schiavo, G., Papini, E., Genna, G., & Montecucco, C. (1990). An intact interchain disulfide bond is required for the neurotoxicity of tetanus toxin. Infection and Immunity, 58, 4136-4141. https://doi.org/10.1128/IAI.58.12.4136-4141.1990
Schiavo, G., Poulain, B., Rossetto, O., Benfenati, F., Tauc, L., & Montecucco, C. (1992). b) Tetanus toxin is a zinc protein and its inhibition of neurotransmitter release depends on zinc. EMBO Journal, 11, 3577-3583.
Schmieg, N., Menendez, G., Schiavo, G., & Terenzio, M. (2014). Signalling endosomes in axonal transport: Travel updates on the molecular highways. Seminars in Cell and Developmental Biology, 27, 32-43.
Schwab, M. E. (1980). Axonal transport from the nerve ending to the nerve cell body: A pathway for trophic signals and neurotoxins. Bulletin Der Schweizerischen Akademie Der Medizinischen Wissenschaften, 36, 7-19.
Schwab, M. E., Suda, K., & Thoenen, H. (1979). Selective retrograde transsynaptic transfer of a protein, tetanus toxin, subsequent to its retrograde axonal transport. Journal of Cell Biology, 82, 798-810. https://doi.org/10.1083/jcb.82.3.798
Schwab, M. E., & Thoenen, H. (1976). Electron microscopic evidence for a transsynaptic migration of tetanus toxin in spinal cord motoneurons: An autoradiographic and morphometric study. Brain Research, 105, 213-227. https://doi.org/10.1016/0006-8993(76)90422-4
Schwab, M., & Thoenen, H. (1977). Selective trans-synaptic migration of tetanus toxin after retrograde axonal transport in peripheral sympathetic nerves: A comparison with nerve growth factor. Brain Research, 122, 459-474.
Shepard, G. (2004). The synaptic organization of the brain. Spinal cord: Ventral Horn (Vol. 3, pp. 79-123).Oxford University Press.
Sherrington, C. S. (1907). On reciprocal innervation of antagonistic muscles. Tenth note. Proceedings of the Royal Society, 79, 337-349.
Sikorra, S., Henke, T., Galli, T., & Binz, T. (2008). Substrate recognition mechanism of VAMP/synaptobrevin-cleaving clostridial neurotoxins. Journal of Biological Chemistry, 283, 21145-21152. https://doi.org/10.1074/jbc.M800610200
Sleigh, J. N., Vagnoni, A., Twelvetrees, A. E., & Schiavo, G. (2017). Methodological advances in imaging intravital axonal transport. F1000Research, 6, 200. https://doi.org/10.12688/f1000research.10433.1
Stöckel, K., Schwab, M., & Thoenen, H. (1975). Comparison between the retrograde axonal transport of nerve growth factor and tetanus toxin in motor, sensory and adrenergic neurons. Brain Research, 99, 1-16. https://doi.org/10.1016/0006-8993(75)90604-6
Stoeckel, K., Schwab, M., & Thoenen, H. (1977). Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin. Brain Research, 132, 273-285. https://doi.org/10.1016/0006-8993(77)90421-8
Surana, S., Tosolini, A. P., Meyer, I. F. G., Fellows, A. D., Novoselov, S. S., & Schiavo, G. (2018). The travel diaries of tetanus and botulinum neurotoxins. Toxicon, 147, 58-67. https://doi.org/10.1016/j.toxicon.2017.10.008
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S. A., Rammner, B., Gräter, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., … Jahn, R. (2006). Molecular anatomy of a trafficking organelle. Cell, 127, 831-846. https://doi.org/10.1016/j.cell.2006.10.030
Taylor, M. P., & Enquist, L. W. (2015). Axonal spread of neuroinvasive viral infections. Trends in Microbiology, 23, 283-288. https://doi.org/10.1016/j.tim.2015.01.002
Thwaites, C. L., Beeching, N. J., & Newton, C. R. (2015). Maternal and neonatal tetanus. Lancet, 385, 362-370. https://doi.org/10.1016/S0140-6736(14)60236-1
Thwaites, C. L., & Farrar, J. J. (2003). Preventing and treating tetanus. British Medical Journal, 326, 117-118.
Thwaites, C. L., Yen, L. M., Glover, C., Tuan, P. Q., Nga, N. T. N., Parry, J., Loan, H. T., Bethell, D., Day, N. P. J., White, N. J., Soni, N., & Farrar, J. J. (2006). Predicting the clinical outcome of tetanus: The tetanus severity score. Tropical Medicine and International Health, 11, 279-287. https://doi.org/10.1111/j.1365-3156.2006.01562.x
Tizzoni, G., & Cattani, G. (1889). Ricerche Batteriologiche Sul Tetano. Riforma Med., 5, 512-513.
Tizzoni, G., & Cattani, G. (1890). Uber das Tetanusgift (On tetanus toxin). Zentralbl. Bakt., 8, 69-73.
van Heyningen, W. E. (1974). Gangliosides as membrane receptors for tetanus toxin, cholera toxin and serotonin. Nature, 249, 415-417. https://doi.org/10.1038/249415a0
Verderio, C., Coco, S., Bacci, A., Rossetto, O., De Camilli, P., Montecucco, C., & Matteoli, M. (1999). Tetanus toxin blocks the exocytosis of synaptic vesicles clustered at synapses but not of synaptic vesicles in isolated axons. Journal of Neuroscience, 19, 6723-6732. https://doi.org/10.1523/JNEUROSCI.19-16-06723.1999
Windhorst, U. (1996). On the role of recurrent inhibitory feedback in motor control. Progress in Neurobiology, 49, 517-587. https://doi.org/10.1016/0301-0082(96)00023-8
Yeh, F. L., Dong, M., Yao, J., Tepp, W. H., Lin, G., Johnson, E. A., & Chapman, E. R. (2010). SV2 mediates entry of tetanus neurotoxin into central neurons. PLOS Path, 6, e1001207.-https://doi.org/10.1371/journal.ppat.1001207
Zuverink, M., Bluma, M., & Barbieri, J. T. (2020). Tetanus Toxin cis-loop Contributes to light-chain Translocation. mSphere, 5, e00244-e320.