A new sialidase mechanism: Bacteriophage K1F endosialidase is an inverting glycosidase

Journal of Biological Chemistry

Volumn 284, Issue 26, 2009, Pages 17404-17410

  Morley, Thomas J ^a   Willis, Lisa M ^b   Whitfield, Chris ^b   Wakarchuk, Warren W ^c   Withers, Stephen G ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC RESIDUES; ACTIVE SITE; CATALYTIC MECHANISMS; CLEAVAGE SITES; E. COLI; GLYCOSIDASE; GLYCOSIDASES; NEW MECHANISMS; PH VALUE; POLYSIALIC ACID; PROTONATED; SIALIDASE; SIALIDASES; TRANS-SIALIDASES; WILD TYPES;

ACIDS; ESCHERICHIA COLI; HYDROLYSIS;

BACTERIOPHAGES;

ALANINE; ENDOSIALIDASE; GLUTAMIC ACID; GLYCOSIDASE; UNCLASSIFIED DRUG; VIRUS SIALIDASE;

ARTICLE; BACTERIOPHAGE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME MECHANISM; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT;

ANIMALS; BACTERIOPHAGES; BINDING SITES; CAMPYLOBACTER JEJUNI; CHROMATOGRAPHY, THIN LAYER; GLYCOPROTEINS; GLYCOSIDE HYDROLASES; GLYCOSIDES; HYDROLYSIS; MAGNETIC RESONANCE SPECTROSCOPY; MUTAGENESIS, SITE-DIRECTED; MUTATION; NEURAMINIDASE; SIALYLTRANSFERASES; SUBSTRATE SPECIFICITY; TRYPANOSOMA CRUZI;

ESCHERICHIA COLI;

EID: 67650516796     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M109.003970     Document Type: Article

References (88)

1. Schauer, R. (2000) Glycoconj. J. 17, 485-499
2. Franz, C. K., Rutishauser, U., and Rafuse, V. F. (2005) J. Neurosci. 25, 2081-2091
3. Fujimoto, I., Bruses, J. L., and Rutishauser, U. (2001) J. Biol. Chem. 276, 31745-31751
4. Vimr, E., and Lichtensteiger, C. (2002) Trends Microbiol. 10, 254-257
5. Schauer, R. (2004) Zoology 107, 49-64
6. Taylor, G. (1996) Curr. Opin. Struct. Biol. 6, 830-837
7. Cippola, L., Peri, F., and Airoldi, C. (2008) Curr. Med. Chem. Anti-Cancer Agents 8, 92-121
8. Angata, T., and Varki, A. (2002) Chem. Rev 102, 439-469
9. Breton, C., Snajdrová, L., Jeanneau, C., Koca, J., and Imberty, A. (2006) Glycobiology 16, 29R-37R
10. Newstead, S. L., Potter, J. A., Wilson, J. C., Xu, G., Chien, C. H., Watts, A. G., Withers, S. G., and Taylor, G. L. (2008) J. Biol. Chem. 283, 9080-9088
11. Kao, Y. H., Lerner, L., and Warner, T. G. (1997) Glycobiology 7, 559-563
12. Manzoni, M., Colombi, P., Papini, N., Rubaga, L., Tiso, N., Preti, A., Venerando, B., Tettamanti, G., Bresciani, R., Argenton, F., Borsani, G., and Monti, E. (2007) Biochem. J. 408, 395-406
13. Kobayashi, T., Ito, M., Ikeda, K., Tanaka, K., and Saito, M. (2000) J. Biochem. 127, 569-575
14. Troy, F. A., 2nd (1992) Glycobiology 2, 5-23
15. Stummeyer, K., Dickmanns, A., Mühlenhoff, M., Gerardy-Schahn, R., and Ficner, R. (2005) Nat. Struct. Mol. Biol. 12, 90-96
16. Mühlenhoff, M., Eckhardt, M., and Gerardy-Schahn, R. (1998) Curr. Opin. Struct. Biol. 8, 558-564
17. Drake, P. M., Nathan, J. K., Stock, C. M., Chang, P. V., Muench, M. O., Nakata, D., Reader, J. R., Gip, P., Golden, K. P., Weinhold, B., Gerardy-Schahn, R., Troy, F. A., 2nd, and Bertozzi, C. R. (2008) J. Immunol. 181, 6850-6858
18. Finne, J. (1982) J. Biol. Chem. 257, 1966-1970
19. Röckle, I., Seidenfaden, R., Weinhold, B., Mühlenhoff, M., Gerardy-Schahn, R., and Hildebrandt, H. (2008) Dev. Neurobiol. 68, 1170-1184
20. Galuska, S. P., Geyer, R., Gerardy-Schahn, R., Mühlenhoff, M., and Geyer, H. (2008) J. Biol. Chem. 283, 17-28
21. Hildebrandt, H., Mühlenhoff, M., Weinhold, B., and Gerardy-Schahn, R. (2007) J. Neurochem. 103, 56-64
22. Rutishauser, U. (1998) J. Cell. Biochem. 70, 304-312
23. Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M., and Sunshine, J. (1988) Science 240, 53-57
24. Acheson, A., Sunshine, J. L., and Rutishauser, U. (1991) J. Cell Biol. 114, 143-153
25. Muller, D., Djebbara-Hannas, Z., Jourdain, P., Vutskits, L., Durbec, P., Rougon, G., and Kiss, J. Z. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 4315-4320
26. Horstkorte, R., Mühlenhoff, M., Reutter, W., Nöhring, S., Zimmermann-Kordmann, M., and Gerardy-Schahn, R. (2004) Exp. Cell Res. 298, 268-274
27. Seidenfaden, R., Krauter, A., Schertzinger, F., Gerardy-Schahn, R., and Hildebrandt, H. (2003) Mol. Cell. Biol. 23, 5908-5918
28. Seidenfaden, R., Krauter, A., Schertzinger, F., Muhlenhoff, M., Gerardy-Schahn, R., and Hildebrandt, H. (2003) Eur. J. Cell Biol. 82, 48-49
29. Roth, J., Zuber, C., Wagner, P., Blaha, I., Bitter-Suermann, D., and Heitz, P. U. (1988) Am. J. Pathol. 133, 227-240
30. Moolenaar, C. E., Muller, E. J., Schol, D. J., Figdor, C. G., Bock, E., Bitter-Suermann, D., and Michalides, R. J. (1990) Cancer Res. 50, 1102-1106
31. Roth, J., Zuber, C., Wagner, P., Taatjes, D. J., Weisgerber, C., Heitz, P. U., Goridis, C., and Bittersuermann, D. (1988) Proc. Natl. Acad. Sci. U.S.A. 85, 2999-3003
32. Figarella-Branger, D. F., Durbec, P. L., and Rougon, G. N. (1990) Cancer Res. 50, 6364-6370
33. Adlam, C., Knights, J. M., Mugridge, A., Williams, J. M., and Lindon, J. C. (1987) FEMS Microbiol. Lett. 42, 23-25
34. Jennings, H. J., Roy, R., and Michon, F. (1985) J. Immunol. 134, 2651-2657
35. Bhattacharjee, A. K., Jennings, H. J., Kenny, C. P., Martin, A., and Smith, I. C. P. (1975) J. Biol. Chem. 250, 1926-1932
36. Jennings, H. J., Katzenellenbogen, E., Lugowski, C., Michon, F., Roy, R., and Kasper, D. L. (1984) Pure Appl. Chem. 56, 893-905
37. Devi, S. J., Schneerson, R., Egan, W., Vann, W. F., Robbins, J. B., and Shiloach, J. (1991) Infect. Immun. 59, 732-736
38. Gotschlich, E. C., Fraser, B. A., Nishimura, O., Robbins, J. B., and Liu, T. Y. (1981) J. Biol. Chem. 256, 8915-8921
39. Finne, J., Leinonen, M., and Mäkelä, P. H. (1983) Lancet 2, 355-357
40. Kim, K. S. (2003) Nat. Rev. Neurosci. 4, 376-385
41. Silver, R. P., Vann, W. F., and Aaronson, W. (1984) J. Bacteriol. 157, 568-575
42. Jann, K., and Jann, B. (1983) Prog. Allergy 33, 53-79
43. Orskov, I., Orskov, F., Jann, B., and Jann, K. (1977) Bacteriol. Rev. 41, 667-710
44. Leiman, P. G., Battisti, A. J., Bowman, V. D., Stummeyer, K., Mühlenhoff, M., Gerardy-Schahn, R., Scholl, D., and Molineux, I. J. (2007) J. Mol. Biol. 371, 836-849
45. Kaper, J. B., Nataro, J. P., and Mobley, H. L. T. (2004) Nat. Rev. Microbiol. 2, 123-140
46. Gross, R. J., Cheasty, T., and Rowe, B. (1977) J. Clin. Microbiol. 6, 548-550
47. Miyake, K., Muraki, T., Hattori, K., Machida, Y., Watanabe, M., Kawase, M., Yoshida, Y., and Iijima, S. (1997) J. Ferment. Bioeng. 84, 90-93
48. Jakobsson, E., Jokilammi, A., Aalto, J., Ollikka, P., Lehtonen, J. V., Hirvonen, H., and Finne, J. (2007) Biochem. J. 405, 465-472
49. Machida, Y., Hattori, K., Miyake, K., Kawase, Y., Kawase, M., and Iijima, S. (2000) J. Biosci. Bioeng. 90, 62-68
50. Machida, Y., Miyake, K., Hattori, K., Yamamoto, S., Kawase, M., and Iijima, S. (2000) FEMS Microbiol. Lett. 182, 333-337
51. Scholl, D., Rogers, S., Adhya, S., and Merril, C. R. (2001) J. Virol. 75, 2509-2515
52. Long, G. S., Bryant, J. M., Taylor, P. W., and Luzio, J. P. (1995) Biochem. J. 309, 543-550
53. Hallenbeck, P. C., Vimr, E. R., Yu, F., Bassler, B., and Troy, F. A. (1987) J. Biol. Chem. 262, 3553-3561
54. Engstler, M., Talhouk, J. W., Smith, R. E., and Schauer, R. (1997) Anal. Biochem. 250, 176-180
55. Chiu, C. P., Watts, A. G., Lairson, L. L., Gilbert, M., Lim, D., Wakarchuk, W. W., Withers, S. G., and Strynadka, N. C. (2004) Nat. Struct. Mol. Biol. 11, 163-170
56. Damager, I., Buchini, S., Amaya, M. F., Buschiazzo, A., Alzari, P., Frasch, A. C., Watts, A., and Withers, S. G. (2008) Biochemistry 47, 3507-3512
57. Petter, J. G., and Vimr, E. R. (1993) J. Bacteriol. 175, 4354-4363
58. Willis, L. M., Gilbert, M., Karwaski, M. F., Blanchard, M. C., and Wakarchuk, W. W. (2008) Glycobiology 18, 177-186
59. Joshi, M. D., Sidhu, G., Pot, I., Brayer, G. D., Withers, S. G., and McIntosh, L. P. (2000) J. Mol. Biol. 299, 255-279
60. Jolley, M. E., and Glaudemans, C. P. (1974) Carbohydr. Res. 33, 377-382
61. Henkel, E., Sollmann, C., and Henkel, R. (1983) Clin. Chem. 29, 1182-1182
62. Brayer, G. D., Sidhu, G., Maurus, R., Rydberg, E. H., Braun, C., Wang, Y., Nguyen, N. T., Overall, C. M., and Withers, S. G. (2000) Biochemistry 39, 4778-4791
63. Tull, D., and Withers, S. G. (1994) Biochemistry 33, 6363-6370
64. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Biochem. J. 321, 557-559
65. Kataoka, Y., Miyake, K., and Iijima, S. (2006) J. Biosci. Bioeng. 101, 198-201
66. Pelkonen, S., Pelkonen, J., and Finne, J. (1989) J. Virol. 63, 4409-4416
67. Schwarzer, D., Stummeyer, K., Haselhorst, T., Freiberger, F., Rode, B., Grove, M., Scheper, T., von Itzstein, M., Mühlenhoff, M., and Gerardy-Schahn, R. (2009) J. Biol. Chem. 284, 9465-9474
68. Wang, Q., Trimbur, D., Graham, R., Warren, R. A., and Withers, S. G. (1995) Biochemistry 34, 14554-14562
69. Ogura, H., Furuhata, K., Itoh, M., and Shitori, Y. (1986) Carb. Res. 158, 37-51
70. Watson, J. N., Dookhun, V., Borgford, T. J., and Bennet, A. J. (2003) Biochemistry 42, 12682-12690
71. Finne, J., and Mäkelä, P. H. (1985) J. Biol. Chem. 260, 1265-1270
72. Manzi, A. E., Higa, H. H., Diaz, S., and Varki, A. (1994) J. Biol. Chem. 269, 23617-23624
73. Schauer, R., and Kamerling, J. P. (eds) (1997) Glycoproteins II, pp. 243-372, Vol. 19B, Elsevier Science, New York, NY
74. Severi, E., Müller, A., Potts, J. R., Leech, A., Williamson, D., Wilson, K. S., and Thomas, G. H. (2008) J. Biol. Chem. 283, 4841-4849
75. Watson, J. N., Indurugalla, D., Cheng, L. L., Narine, A. A., and Bennet, A. J. (2006) Biochemistry 45, 13264-13275
76. Newstead, S., Watson, J. N., Knoll, T. L., Bennet, A. J., and Taylor, G. (2005) Biochemistry 44, 9117-9122
77. Hoffman, S., Sorkin, B. C., White, P. C., Brackenbury, R., Mailhammer, R., Rutishauser, U., Cunningham, B. A., and Edelman, G. M. (1982) J. Biol. Chem. 257, 7720-7729
78. Key, B., and Akeson, R. A. (1990) J. Cell Biol. 110, 1729-1743
79. Troy, F. A., and McCloskey, M. A. (1979) J. Biol. Chem. 254, 7377-7387
80. Evans, S. V., Sigurskjold, B. W., Jennings, H. J., Brisson, J. R., To, R., Tse, W. C., Altman, E., Frosch, M., Weisgerber, C., Kratzin, H. D., Klebert, S., Vaesen, M., Bittersuermann, D., Rose, D. R., Young, N. M., and Bundle, D. R. (1995) Biochemistry 34, 6737-6744
81. Jennings, H. J., Evans, S. V., Brisson, J. R., Bundle, D. R., Frosch, M., and Bittersuermann, D. (1993) Glycoconj. J. 10, 328-328
82. Brisson, J. R., Baumann, H., Imberty, A., Pérez, S., and Jennings, H. J. (1992) Biochemistry 31, 4996-5004
83. Michon, F., Brisson, J. R., and Jennings, H. J. (1987) Biochemistry 26, 8399-8405
84. Yamasaki, R., and Bacon, B. (1991) Biochemistry 30, 851-857
85. Haselhorst, T., Stummeyer, K., Mühlenhoff, M., Schaper, W., Gerardy-Schahn, R., and von Itzstein, M. (2006) ChemBioChem 7, 1875-1877
86. Ashwell, M., Guo, X. M., and Sinnott, M. L. (1992) J. Am. Chem. Soc. 114, 10158-10166
87. Namchuk, M. N., McCarter, J. D., Becalski, A., Andrews, T., and Withers, S. G. (2000) J. Am. Chem. Soc. 122, 1270-1277
88. Damude, H. G., Ferro, V., Withers, S. G., and Warren, R. A. J. (1996) Biochem. J. 315, 467-472