Novel ganglioside-mediated entry of botulinum neurotoxin serotype D into neurons

Journal of Biological Chemistry

Volumn 286, Issue 30, 2011, Pages 26828-26837

  Kroken, Abby R ^a   Karalewitz, Andrew P A ^a   Fu, Zhuji ^a   Kim, Jung Ja P ^a   Barbieri, Joseph T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC RINGS; B-SERIES; BINDING LOOP; BINDING POCKETS; BOTULINUM NEUROTOXINS; IMMUNOPRECIPITATIONS; LOOP STRUCTURE; MEMBRANE DEPOLARIZATION; RECEPTOR-BINDING DOMAINS; SEROTYPES; STRUCTURAL STUDIES; SYNAPTIC VESICLE; SYNAPTOPHYSIN;

AMINO ACIDS;

BOTULINUM TOXIN; BOTULINUM TOXIN D; GANGLIOSIDE; GANGLIOSIDE GD 1B; GANGLIOSIDE GD2; GANGLIOSIDE GT1B; PHENYLALANINE; SYNAPTOBREVIN 2; SYNAPTOPHYSIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; IMMUNOPRECIPITATION; INTOXICATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; RECEPTOR BINDING; SEROTYPE; SYNAPSE VESICLE;

ANIMALS; BOTULINUM TOXINS; CELL LINE; GANGLIOSIDES; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PROTEIN STRUCTURE, SECONDARY; RATS;

EID: 79960680902     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.254086     Document Type: Article

References (59)

1. Gill, D. M. (1982) Microbiol. Rev. 46, 86-94
2. Arnon, S. S., Schechter, R., Inglesby, T. V., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., Fine, A. D., Hauer, J., Layton, M., Lillibridge, S., Osterholm, M. T., O'Toole, T., Parker, G., Perl, T. M., Russell, P. K., Swerdlow, D. L., and Tonat, K. (2001) JAMA 285, 1059-1070
3. Eleopra, R., Tugnoli, V., Rossetto, O., Montecucco, C., and De Grandis, D. (1997) Neurosci. Lett. 224, 91-94
4. Davletov, B., Bajohrs, M., and Binz, T. (2005) Trends Neurosci. 28, 446-452
5. Coffield, J. A., Bakry, N., Zhang, R. D., Carlson, J., Gomella, L. G., and Simpson, L. L. (1997) J. Pharmacol. Exp. Ther. 280, 1489-1498
6. Woodward, L. A., Arimitsu, H., Hirst, R., and Oguma, K. (2003) Infect. Immun. 71, 2941-2944
7. Lacy, D. B., Tepp, W., Cohen, A. C., DasGupta, B. R., and Stevens, R. C. (1998) Nat. Struct. Biol. 5, 898-902
8. Dong, M., Liu, H., Tepp, W. H., Johnson, E. A., Janz, R., and Chapman, E. R. (2008) Mol. Biol. Cell 19, 5226-5237
9. Ochanda, J. O., Syuto, B., Ohishi, I., Naiki, M., and Kubo, S. (1986) J. Biochem. 100, 27-33
10. Rummel, A., Mahrhold, S., Bigalke, H., and Binz, T. (2004) Mol. Microbiol. 51, 631-643
11. Dong, M., Yeh, F., Tepp, W. H., Dean, C., Johnson, E. A., Janz, R., and Chapman, E. R. (2006) Science 312, 592-596
12. Dong, M., Richards, D. A., Goodnough, M. C., Tepp, W. H., Johnson, E. A., and Chapman, E. R. (2003) J. Cell Biol. 162, 1293-1303
13. Fu, Z., Chen, C., Barbieri, J. T., Kim, J. J., and Baldwin, M. R. (2009) Biochemistry 48, 5631-5641
14. Koriazova, L. K., and Montal, M. (2003) Nat. Struct. Biol. 10, 13-18
15. Montecucco, C., and Schiavo, G. (1993) Trends Biochem. Sci. 18, 324-327
16. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino, de Laureto, P., DasGupta, B. R., and Montecucco, C. (1992) Nature 359, 832-835
17. Yamasaki, S., Baumeister, A., Binz, T., Blasi, J., Link, E., Cornille, F., Roques, B., Fykse, E. M., Südhof, T. C., and Jahn, R. (1994) J. Biol. Chem. 269, 12764-12772
18. Hill, K. K., Smith, T. J., Helma, C. H., Ticknor, L. O., Foley, B. T., Svensson, R. T., Brown, J. L., Johnson, E. A., Smith, L. A., Okinaka, R. T., Jackson, P. J., and Marks, J. D. (2007) J. Bacteriol. 189, 818-832
19. Rummel, A., Häfner, K., Mahrhold, S., Darashchonak, N., Holt, M., Jahn, R., Beermann, S., Karnath, T., Bigalke, H., and Binz, T. (2009) J. Neurochem. 110, 1942-1954
20. Dong, M., Tepp, W. H., Liu, H., Johnson, E. A., and Chapman, E. R. (2007) J. Cell Biol. 179, 1511-1522
21. Tsukamoto, K., Kohda, T., Mukamoto, M., Takeuchi, K., Ihara, H., Saito, M., and Kozaki, S. (2005) J. Biol. Chem. 280, 35164-35171
22. Simpson, L., and Rapport, M. (1971) J. Neurochem. 18, 1341-1343
23. Karalewitz, A. P., Kroken, A. R., Fu, Z., Baldwin, M. R., Kim, J. J., and Barbieri, J. T. (2010) Biochemistry 49, 8117-8126
24. Tsukamoto, K., Kozai, Y., Ihara, H., Kohda, T., Mukamoto, M., Tsuji, T., and Kozaki, S. (2008) Microb. Pathog. 44, 484-493
25. Strotmeier, J., Lee, K., Völker, A. K., Mahrhold, S., Zong, Y., Zeiser, J., Zhou, J., Pich, A., Bigalke, H., Binz, T., Rummel, A., and Jin, R. (2010) Biochem. J. 431, 207-216
26. Peng, L., Tepp, W. H., Johnson, E. A., and Dong, M. (2011) PLoS Pathog. 7, e1002008
27. Baldwin, M. R., Tepp, W. H., Przedpelski, A., Pier, C. L., Bradshaw, M., Johnson, E. A., and Barbieri, J. T. (2008) Infect. Immun. 76, 1314-1318
28. Manders, E. E. M., Verbeek, F. J., and Aten, J. A. (1993) J. Microsc. 169, 375-382
29. Li, Q., Lau, A., Morris, T. J., Guo, L., Fordyce, C. B., and Stanley, E. F. (2004) J. Neurosci. 24, 4070-4081
30. Baldwin, M. R., and Barbieri, J. T. (2007) Biochemistry 46, 3200-3210
31. Huttner, W. B., Schiebler, W., Greengard, P., and De Camilli, P. (1983) J. Cell Biol. 96, 1374-1388
32. McPherson, A. (1999) Crystallization of Biological Macromolecules, pp. 188-192, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
33. Minor, W., Tomchick, D., and Otwinowski, Z. (2000) Structure 8, R105-R110
34. CCP4 (1994) Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
35. Brunger, A. T. (2007) Nat. Protoc. 2, 2728-2733
36. Roussel, A., Inisan, A. G., Knoop-Mouthuy, A., and Cambillau, C. (1999) Turbo-Frodo, Version OpenGL:1, CNRS/Universitite, Marseille, France
37. Chai, Q., Arndt, J. W., Dong, M., Tepp, W. H., Johnson, E. A., Chapman, E. R., and Stevens, R. C. (2006) Nature 444, 1096-1100
38. Zenisek, D., Steyer, J. A., and Almers, W. (2000) Nature 406, 849-854
39. Chen, C., Fu, Z., Kim, J. J., Barbieri, J. T., and Baldwin, M. R. (2009) J. Biol. Chem. 284, 26569-26577
40. Yeh, F. L., Dong, M., Yao, J., Tepp, W. H., Lin, G., Johnson, E. A., and Chapman, E. R. (2010) PLoS Pathog. 6, e1001207
41. Pang, Z. P., and Südhof, T. C. (2010) Curr. Opin. Cell Biol. 22, 496-505
42. Hoopmann, P., Punge, A., Barysch, S. V., Westphal, V., Bückers, J., Opazo, F., Bethani, I., Lauterbach, M. A., Hell, S. W., and Rizzoli, S. O. (2010) Proc. Natl. Acad. Sci. U.S.A. 107, 19055-19060
43. Bennett, M. K., Calakos, N., Kreiner, T., and Scheller, R. H. (1992) J. Cell Biol. 116, 761-775
44. Lazzell, D. R., Belizaire, R., Thakur, P., Sherry, D. M., and Janz, R. (2004) J. Biol. Chem. 279, 52124-52131
45. Zhang, Y., Buchko, G. W., Qin, L., Robinson, H., and Varnum, S. M. (2010) Biochem. Biophys. Res. Commun. 401, 498-503
46. Lacy, D. B., and Stevens, R. C. (1999) J. Mol. Biol. 291, 1091-1104
47. Stenmark, P., Dupuy, J., Imamura, A., Kiso, M., and Stevens, R. C. (2008) PLoS Pathog. 4, e1000129
48. Cole, A. A., Dosemeci, A., and Reese, T. S. (2010) Biochem. J. 427, 535-540
49. Sheikh, K. A., Sun, J., Liu, Y., Kawai, H., Crawford, T. O., Proia, R. L., Griffin, J. W., and Schnaar, R. L. (1999) Proc. Natl. Acad. Sci. U.S.A. 96, 7532-7537
50. Takamiya, K., Yamamoto, A., Furukawa, K., Yamashiro, S., Shin, M., Okada, M., Fukumoto, S., Haraguchi, M., Takeda, N., Fujimura, K., Sakae, M., Kishikawa, M., Shiku, H., Furukawa, K., and Aizawa, S. (1996) Proc. Natl. Acad. Sci. U.S.A. 93, 10662-10667
51. Sugiura, Y., Furukawa, K., Tajima, O., Mii, S., Honda, T., and Furukawa, K. (2005) Neuroscience 135, 1167-1178
52. Yoshinaka, K., Kumanogoh, H., Nakamura, S., and Maekawa, S. (2004) Neurosci. Lett. 363, 168-172
53. Ando, S., Tanaka, Y., Waki, H., Kon, K., Iwamoto, M., and Fukui, F. (1998) Ann. N.Y. Acad. Sci. 845, 232-239
54. Mutch, S. A., Kensel-Hammes, P., Gadd, J. C., Fujimoto, B. S., Allen, R. W., Schiro, P. G., Lorenz, R. M., Kuyper, C. L., Kuo, J. S., Bajjalieh, S. M., and Chiu, D. T. (2011) J. Neurosci. 31, 1461-1470
55. 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., Heuser, J., Wieland, F., and Jahn, R. (2006) Cell 127, 831-846
56. Bonanomi, D., Benfenati, F., and Valtorta, F. (2006) Prog. Neurobiol. 80, 177-217
57. Keller, J. E., Cai, F., and Neale, E. A. (2004) Biochemistry 43, 526-532
58. Swaminathan, S., and Eswaramoorthy, S. (2000) Nat. Struct. Biol. 7, 693-699
59. Kumaran, D., Eswaramoorthy, S., Furey, W., Navaza, J., Sax, M., and Swaminathan, S. (2009) J. Mol. Biol. 386, 233-245