Widespread Sequence Variations in VAMP1 across Vertebrates Suggest a Potential Selective Pressure from Botulinum Neurotoxins

PLoS Pathogens

Volumn 10, Issue 7, 2014, Pages

  Peng, Lisheng ^a   Adler, Michael ^b   Demogines, Ann ^c   Borrell, Andrew ^b   Liu, Huisheng ^d   Tao, Liang ^a   Tepp, William H ^e   Zhang, Su Chun ^d   Johnson, Eric A ^e   Sawyer, Sara L ^c   Dong, Min ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN; SYNAPTOBREVIN 1; VAMP1 PROTEIN, HUMAN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 1, MOUSE; VESICLE-ASSOCIATED MEMBRANE PROTEIN 1, RAT;

AMINO ACID SEQUENCE; ANIMAL; CHEMICALLY INDUCED; COMPARATIVE STUDY; DIAPHRAGM; GENETIC VARIABILITY; GENETICS; HUMAN; INNERVATION; MALE; METABOLISM; MOLECULAR GENETICS; MOTONEURON; MOUSE; PARESIS; PATHOLOGY; RAT; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT;

AMINO ACID SEQUENCE; ANIMALS; BOTULINUM TOXINS; DIAPHRAGM; GENETIC VARIATION; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; PARESIS; RATS; RATS, SPRAGUE-DAWLEY; SPECIES SPECIFICITY; VESICLE-ASSOCIATED MEMBRANE PROTEIN 1;

EID: 84905374103     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004177     Document Type: Article

References (35)

1. Schiavo G, Matteoli M, Montecucco C, (2000) Neurotoxins affecting neuroexocytosis. Physiol Rev 80: 717-766.
2. Montal M, (2010) Botulinum neurotoxin: a marvel of protein design. Annu Rev Biochem 79: 591-617.
3. Shapiro RL, Hatheway C, Swerdlow DL, (1998) Botulism in the United States: a clinical and epidemiologic review. Ann Intern Med 129: 221-228.
4. Collins MD, East AK, (1998) Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J Appl Microbiol 84: 5-17.
5. Dover N, Barash JR, Hill KK, Xie G, Arnon SS, (2013) Molecular characterization of a novel botulinum neurotoxin type H gene. J Infect Dis 209: 192-202.
6. Jahn R, Scheller RH, (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643.
7. Dolly JO, Black J, Williams RS, Melling J, (1984) Acceptors for botulinum neurotoxin reside on motor nerve terminals and mediate its internalization. Nature 307: 457-460.
8. Aguado F, Majo G, Ruiz-Montasell B, Llorens J, Marsal J, et al. (1999) Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 88: 437-446.
9. Meunier FA, Lisk G, Sesardic D, Dolly JO, (2003) Dynamics of motor nerve terminal remodeling unveiled using SNARE-cleaving botulinum toxins: the extent and duration are dictated by the sites of SNAP-25 truncation. Mol Cell Neurosci 22: 454-466.
10. Rozas JL, Gomez-Sanchez L, Mircheski J, Linares-Clemente P, Nieto-Gonzalez JL, et al. (2012) Motorneurons require cysteine string protein-alpha to maintain the readily releasable vesicular pool and synaptic vesicle recycling. Neuron 74: 151-165.
11. Li JY, Edelmann L, Jahn R, Dahlstrom A, (1996) Axonal transport and distribution of synaptobrevin I and II in the rat peripheral nervous system. J Neurosci 16: 137-147.
12. Liu Y, Sugiura Y, Lin W, (2011) The role of synaptobrevin1/VAMP1 in Ca2+-triggered neurotransmitter release at the mouse neuromuscular junction. J Physiol 589: 1603-1618.
13. Nystuen AM, Schwendinger JK, Sachs AJ, Yang AW, Haider NB, (2007) A null mutation in VAMP1/synaptobrevin is associated with neurological defects and prewean mortality in the lethal-wasting mouse mutant. Neurogenetics 8: 1-10.
14. Schiavo G, Benfenati F, Poulain B, Rossetto O, Polverino de Laureto P, et al. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359: 832-835.
15. Yamamoto H, Ida T, Tsutsuki H, Mori M, Matsumoto T, et al. (2012) Specificity of botulinum protease for human VAMP family proteins. Microbiol Immunol 56: 245-253.
16. Burgen AS, Dickens F, Zatman LJ, (1949) The action of botulinum toxin on the neuro-muscular junction. J Physiol 109: 10-24.
17. Coffield JA, Bakry N, Zhang RD, Carlson J, Gomella LG, et al. (1997) In vitro characterization of botulinum toxin types A, C and D action on human tissues: combined electrophysiologic, pharmacologic and molecular biologic approaches. J Pharmacol Exp Ther 280: 1489-1498.
18. Sobel J, (2005) Botulism. Clin Infect Dis 41: 1167-1173.
19. Eleopra R, Montecucco C, Devigili G, Lettieri C, Rinaldo S, et al. (2013) Botulinum neurotoxin serotype D is poorly effective in humans: an in vivo electrophysiological study. Clin Neurophysiol 124: 999-1004.
20. Peng L, Liu H, Ruan H, Tepp WH, Stoothoff WH, et al. (2013) Cytotoxicity of botulinum neurotoxins reveals a direct role of syntaxin 1 and SNAP-25 in neuron survival. Nat Commun 4: 1472.
21. Hu BY, Zhang SC, (2009) Differentiation of spinal motor neurons from pluripotent human stem cells. Nat Protoc 4: 1295-1304.
22. Pellizzari R, Mason S, Shone CC, Montecucco C, (1997) The interaction of synaptic vesicle-associated membrane protein/synaptobrevin with botulinum neurotoxins D and F. FEBS Lett 409: 339-342.
23. Yamasaki S, Baumeister A, Binz T, Blasi J, Link E, 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.
24. Nakamura K, Kohda T, Shibata Y, Tsukamoto K, Arimitsu H, et al. (2012) Unique biological activity of botulinum D/C mosaic neurotoxin in murine species. Infect Immun 80: 2886-2893.
25. Baumert M, Maycox PR, Navone F, De Camilli P, Jahn R, (1989) Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. Embo J 8: 379-384.
26. Sudhof TC, Baumert M, Perin MS, Jahn R, (1989) A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 2: 1475-1481.
27. Trimble WS, Gray TS, Elferink LA, Wilson MC, Scheller RH, (1990) Distinct patterns of expression of two VAMP genes within the rat brain. J Neurosci 10: 1380-1387.
28. Raptis A, Torrejon-Escribano B, Gomez de Aranda I, Blasi J, (2005) Distribution of synaptobrevin/VAMP 1 and 2 in rat brain. J Chem Neuroanat 30: 201-211.
29. Sutton RB, Fasshauer D, Jahn R, Brunger AT, (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353.
30. Fasshauer D, Sutton RB, Brunger AT, Jahn R, (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 95: 15781-15786.
31. Koo SJ, Markovic S, Puchkov D, Mahrenholz CC, Beceren-Braun F, et al. (2011) SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc Natl Acad Sci U S A 108: 13540-13545.
32. Miller SE, Sahlender DA, Graham SC, Honing S, Robinson MS, et al. (2011) The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147: 1118-1131.
33. Meng J, Wang J, Lawrence G, Dolly JO, (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.
34. 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.
35. Demogines A, Truong KA, Sawyer SL, (2012) Species-specific features of DARC, the primate receptor for Plasmodium vivax and Plasmodium knowlesi. Mol Biol Evol 29: 445-449.