Selective translocation of the Bordetella pertussis adenylate cyclase toxin across the basolateral membranes of polarized epithelial cells

Journal of Biological Chemistry

Volumn 285, Issue 14, 2010, Pages 10662-10670

  Eby, Joshua C ^a   Ciesla, William P ^b,d   Hamman, Wendy ^b   Donato, Gina M ^a   Pickles, Raymond J ^c   Hewlett, Erik L ^a   Lencer, Wayne I ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d Primedoc of Richmond   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; BASOLATERAL MEMBRANES; CATALYTIC DOMAINS; CELL MONOLAYERS; EPITHELIAL CELLS; HIGHLY SENSITIVE; HOST CELLS; HUMAN AIRWAY; INTRACELLULAR CAMP; MAMMALIAN CELLS; MEMBRANE POTENTIALS; MEMBRANE RECEPTORS; MUCOSAL SURFACE; NANOMOLAR CONCENTRATION; PLASMA MEMBRANES; POST-TRANSLATIONAL ACYLATION; TOXIN BINDING;

CELL MEMBRANES; FETAL MONITORING; MAMMALS; MEMBRANES; MONOLAYERS; TOXICITY;

CELL CULTURE;

ADENYLATE CYCLASE TOXIN; CD11B ANTIGEN; CD18 ANTIGEN; CYCLIC AMP;

ACYLATION; ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; BORDETELLA PERTUSSIS; CELL POLARITY; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; INTOXICATION; MEMBRANE TRANSPORT; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL;

ACYLATION; ADENYLATE CYCLASE TOXIN; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD18; BIOLOGICAL TRANSPORT; BRONCHI; CELL MEMBRANE; CELL POLARITY; CELLS, CULTURED; CHLORIDES; CYCLIC AMP; ELECTROPHYSIOLOGY; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; KINETICS; MEMBRANE POTENTIALS; PROTEIN TRANSPORT; TRACHEA;

BORDETELLA PERTUSSIS; MAMMALIA;

EID: 77951235024     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M109.089219     Document Type: Article

References (67)

1. Wolff, J., and Cook, G. H. (1973) J. Biol. Chem. 248, 350-355
2. Goldhammer, A. R., Wolff, J., Hope Cook, G., Berkowitz, S. A., Klee, C. B., Manclark, C. R., and Hewlett, E. L. (1981) Eur. J. Biochem. 115, 605-609
3. Pearson, R. D., Symes, P., Conboy, M., Weiss, A. A., and Hewlett, E. L. (1987) J. Immunol. 139, 2749-2754
4. Hanski, E., and Farfel, Z. (1985) J. Biol. Chem. 260, 5526-5532
5. Gordon, V. M., Leppla, S. H., and Hewlett, E. L. (1988) Infect. Immun. 56, 1066-1069
6. Welch, R. A. (1991) Mol. Microbiol. 5, 521-528
7. Lally, E. T., Hill, R. B., Kieba, I. R., and Korostoff, J. (1999) Trends Microbiol. 7, 356-361
8. Vojtova-Vodolanova, J., Basler, M., Osicka, R., Knapp, O., Maier, E., Cerny, J., Benada, O., Benz, R., and Sebo, P. (2009) FASEB J. 23, 2831-2843
9. Weiss, A. A., Hewlett, E. L., Myers, G. A., and Falkow, S. (1983) Infect. Immun. 42, 33-41
10. Glaser, P., Sakamoto, H., Bellalou, J., Ullmann, A., and Danchin, A. (1988) EMBO J. 7, 3997-4004
11. Szabo, G., Gray, M. C., and Hewlett, E. L. (1994) J. Biol. Chem. 269, 22496-22499
12. Sakamoto, H., Bellalou, J., Sebo, P., and Ladant, D. (1992) J. Biol. Chem. 267, 13598-13602
13. Hewlett, E. L., Donato, G. M., and Gray, M. C. (2006) Mol. Microbiol. 59, 447-459
14. Basler, M., Masin, J., Osicka, R., and Sebo, P. (2006) Infect. Immun. 74, 2207-2214
15. Benz, R., Maier, E., Ladant, D., Ullmann, A., and Sebo, P. (1994) J. Biol. Chem. 269, 27231-27239
16. Gordon, V. M., Young, W. W., Jr., Lechler, S. M., Gray, M. C., Leppla, S. H., and Hewlett, E. L. (1989) J. Biol. Chem. 264, 14792-14796
17. Vojtová, J., Kofronová, O., Sebo, P., and Benada, O. (2006) Microsc. Res. Tech. 69, 119-129
18. Knapp, O., Maier, E., Masín, J., Sebo, P., and Benz, R. (2008) Biochim. Biophys. Acta 1778, 260-269
19. Guermonprez, P., Khelef, N., Blouin, E., Rieu, P., Ricciardi-Castagnoli, P., Guiso, N., Ladant, D., and Leclerc, C. (2001) J. Exp. Med. 193, 1035-1044
20. Confer, D. L., and Eaton, J. W. (1982) Science 217, 948-950
21. Barrett, K. E. (1997) Am. J. Physiol. 272, C1069-C1076
22. Lencer, W. I., Delp, C., Neutra, M. R., and Madara, J. L. (1992) J. Cell Biol. 117, 1197-1209
23. Dharmsathaphorn, K., and Madara, J. L. (1990) Methods Enzymol. 192, 354-389
24. Gray, M. C., Lee, S. J., Gray, L. S., Zaretzky, F. R., Otero, A. S., Szabo, G., and Hewlett, E. L. (2001) J. Bacteriol. 183, 5904-5910
25. Hewlett, E. L., Gray, M. C., Ehrmann, I. E., Maloney, N. J., Otero, A. S., Gray, L., Allietta, M., Szabo, G., Weiss, A. A., and Barry, E. M. (1993) J. Biol. Chem. 268, 7842-7848
26. Lee, S. J., Gray, M. C., Guo, L., Sebo, P., and Hewlett, E. L. (1999) Infect. Immun. 67, 2090-2095
27. Rufo, P. A., Merlin, D., Riegler, M., Ferguson-Maltzman, M. H., Dickinson, B. L., Brugnara, C., Alper, S. L., and Lencer, W. I. (1997) J. Clin. Invest. 100, 3111-3120
28. Pickles, R. J., McCarty, D., Matsui, H., Hart, P. J., Randell, S. H., and Boucher, R. C. (1998) J. Virol. 72, 6014-6023
29. Grubb, B. R., Pickles, R. J., Ye, H., Yankaskas, J. R., Vick, R. N., Engelhardt, J. F., Wilson, J. M., Johnson, L. G., and Boucher, R. C. (1994) Nature 371, 802-806
30. Ingalls, R. R., Arnaout, M. A., and Golenbock, D. T. (1997) J. Immunol. 159, 433-438
31. Gray, M. C., Ross, W., Kim, K., and Hewlett, E. L. (1999) Infect. Immun. 67, 4393-4399
32. Strohmeier, G. R., Reppert, S. M., Lencer, W. I., and Madara, J. L. (1995) J. Biol. Chem. 270, 2387-2394
33. Fiser, R., Masín, J., Basler, M., Krusek, J., Spulá ková, V., Konopásek, I., and Sebo, P. (2007) J. Biol. Chem. 282, 2808-2820
34. Schroeder, B. C., Waldegger, S., Fehr, S., Bleich, M., Warth, R., Greger, R., and Jentsch, T. J. (2000) Nature 403, 196-199
35. Clarke, L. L., Chinet, T., and Boucher, R. C. (1997) Am. J. Physiol. 272, L1084-L1091
36. Ma, T., Thiagarajah, J. R., Yang, H., Sonawane, N. D., Folli, C., Galietta, L. J., and Verkman, A. S. (2002) J. Clin. Invest. 110, 1651-1658
37. Osicka, R., Osicková, A., Basar, T., Guermonprez, P., Rojas, M., Leclerc, C., and Sebo, P. (2000) Infect. Immun. 68, 247-256
38. Bejerano, M., Nisan, I., Ludwig, A., Goebel, W., and Hanski, E. (1999) Mol. Microbiol. 31, 381-392
39. Gray, M., Szabo, G., Otero, A. S., Gray, L., and Hewlett, E. (1998) J. Biol. Chem. 273, 18260-18267
40. Deleted in proof
41. Otero, A. S., Yi, X. B., Gray, M. C., Szabo, G., and Hewlett, E. L. (1995) J. Biol. Chem. 270, 9695-9697
42. Karimova, G., Fayolle, C., Gmira, S., Ullmann, A., Leclerc, C., and Ladant, D. (1998) Proc. Natl. Acad. Sci. U.S.A. 95, 12532-12537
43. Basar, T., Havlícek, V., Bezousková, S., Hackett, M., and Sebo, P. (2001) J. Biol. Chem. 276, 348-354
44. Barry, E. M., Weiss, A. A., Ehrmann, I. E., Gray, M. C., Hewlett, E. L., and Goodwin, M. S. (1991) J. Bacteriol. 173, 720-726
45. El-Azami-El-Idrissi, M., Bauche, C., Loucka, J., Osicka, R., Sebo, P., Ladant, D., and Leclerc, C. (2003) J. Biol. Chem. 278, 38514-38521
46. Beauregard, K. E., Wimer-Mackin, S., Collier, R. J., and Lencer, W. I. (1999) Infect. Immun. 67, 3026-3030
47. Lisanti, M. P., Sargiacomo, M., Graeve, L., Saltiel, A. R., and Rodriguez-Boulan, E. (1988) Proc. Natl. Acad. Sci. U.S.A. 85, 9557-9561
48. Abrami, L., Fivaz, M., and van der Goot, F. G. (2000) Trends Microbiol. 8, 168-172
49. Gordon, V. M., Nelson, K. L., Buckley, J. T., Stevens, V. L., Tweten, R. K., Elwood, P. C., and Leppla, S. H. (1999) J. Biol. Chem. 274, 27274-27280
50. Abrami, L., Fivaz, M., Glauser, P. E., Sugimoto, N., Zurzolo, C., and van der Goot, F. G. (2003) Infect. Immun. 71, 739-746
51. Sonoda, N., Furuse, M., Sasaki, H., Yonemura, S., Katahira, J., Horiguchi, Y., and Tsukita, S. (1999) J. Cell Biol. 147, 195-204
52. Atapattu, D. N., and Czuprynski, C. J. (2007) Infect. Immun. 75, 4719-4727
53. Fong, K. P., Pacheco, C. M., Otis, L. L., Baranwal, S., Kieba, I. R., Harrison, G., Hersh, E. V., Boesze-Battaglia, K., and Lally, E. T. (2006) Cell Microbiol. 8, 1753-1767
54. Schuck, S., and Simons, K. (2004) J. Cell Sci. 117, 5955-5964
55. Ou, G., Baranov, V., Lundmark, E., Hammarström, S., and Hammarström, M. L. (2009) Scand. J. Immunol. 69, 150-161
56. Liévin-Le Moal, V., and Servin, A. L. (2006) Clin. Microbiol. Rev. 19, 315-337
57. Stonebraker, J. R., Wagner, D., Lefensty, R. W., Burns, K., Gendler, S. J., Bergelson, J. M., Boucher, R. C., O'Neal, W. K., and Pickles, R. J. (2004) J. Virol. 78, 13755-13768
58. Pickles, R. J., Fahrner, J. A., Petrella, J. M., Boucher, R. C., and Bergelson, J. M. (2000) J. Virol. 74, 6050-6057
59. Morova, J., Osicka, R., Masin, J., and Sebo, P. (2008) Proc. Natl. Acad. Sci. U.S.A. 105, 5355-5360
60. Mallory, F. B., and Hornor, A. A. (1912) J. Med. Res. 27, 115-124
61. Soane, M. C., Jackson, A., Maskell, D., Allen, A., Keig, P., Dewar, A., Dougan, G., and Wilson, R. (2000) Respir. Med. 94, 791-799
62. Tuomanen, E. I., and Hendley, J. O. (1983) J. Infect. Dis. 148, 125-130
63. Lovell, M. A., Miller, A. M., and Hendley, J. O. (1998) Arch. Pediatr. Adolesc. Med. 152, 925-926
64. Groathouse, N. A., Heinzen, R. A., and Boitano, S. (2003) Infect. Immun. 71, 7208-7210
65. Sawal, M., Cohen, M., Irazuzta, J. E., Kumar, R., Kirton, C., Brundler, M. A., Evans, C. A., Wilson, J. A., Raffeeq, P., Azaz, A., Rotta, A. T., Vora, A., Vohra, A., Abboud, P., Mirkin, L. D., Cooper, M., Dishop, M. K., Graf, J. M., Petros, A., and Klonin, H. (2009) Pediatr. Pulmonol. 44, 970-980
66. Paddock, C. D., Sanden, G. N., Cherry, J. D., Gal, A. A., Langston, C., Tatti, K. M., Wu, K. H., Goldsmith, C. S., Greer, P. W., Montague, J. L., Eliason, M. T., Holman, R. C., Guarner, J., Shieh, W. J., and Zaki, S. R. (2008) Clin. Infect. Dis. 47, 328-338
67. Bassinet, L., Fitting, C., Housset, B., Cavaillon, J. M., and Guiso, N. (2004) Infect. Immun. 72, 5530-5533