Chlamydia attachment to mammalian cells requires protein disulfide isomerase

Cellular Microbiology

Volumn 9, Issue 1, 2007, Pages 222-232

  Conant, Carolyn G ^a,b   Stephens, Richard S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXIN; PROTEIN DISULFIDE ISOMERASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL SURFACE; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; HOST CELL; HOST PATHOGEN INTERACTION; MAMMAL CELL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEOMICS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; CELL MEMBRANE; CHLAMYDIA TRACHOMATIS; CHO CELLS; CRICETINAE; CRICETULUS; DIPHTHERIA TOXIN; EPITHELIAL CELLS; MOLECULAR SEQUENCE DATA; PROTEIN DISULFIDE-ISOMERASE; PROTEOMICS;

CHLAMYDIA; MAMMALIA;

EID: 33845415066     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00783.x     Document Type: Article

References (53)

1. Abell, B.A., and Brown, D.T. (1993) Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface. J Virol 67: 5496-5501.
2. Barbouche, R., Miquelis, R., Jones, I.M., and Fenouillet, E. (2003) Protein-disulfide isomerase-mediated reduction of two disulfide bonds of HIV envelope glycoprotein 120 occurs post-CXCR4 binding and is required for fusion. J Biol Chem 278: 3131-3136.
3. Bavoil, P., Ohlin, A., and Schachter, J. (1984) Role of disulfide bonding in outer membrane structure and permeability in Chlamydia trachomatis. Infect Immun 44: 479-485.
4. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
5. Byrne, G.I. (1976) Requirements for ingestion of Chlamydia psittaci by mouse fibroblasts (L cells). Infect Immun 14: 645-651.
6. Carabeo, R.A., and Hackstadt, T. (2001) Isolation and characterization of a mutant Chinese hamster ovary cell line that is resistant to Chlamydia trachomatis infection at a novel step in the attachment process. Infect Immun 69: 5899-5904.
7. Chittum, H.S., Lane, W.S., Carlson, B.A., Roller, P.P., Lung, F.D., Lee, B.J., and Hatfield, D.L. (1998) Rabbit beta-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps. Biochemistry 37: 10866-10870.
8. Clifton, D.R., Fields, K.A., Grieshaber, S.S., Dooley, C.A., Fischer, E.R., Mead, D.J., et.al. (2004) A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc Natl Acad Sci USA 101: 10166-10171.
9. Couet, J., de Bernard, S., Loosfelt, H., Saunier, B., Milgrom, E., and Misrahi, M. (1996) Cell surface protein disulfide-isomerase is involved in the shedding of human thyrotropin receptor ectodomain. Biochemistry 35: 14800-14805.
10. Davis, C.H., Raulston, J.E., and Wyrick, P.B. (2002) Protein disulfide isomerase, a component of the estrogen receptor complex, is associated with Chlamydia trachomatis serovar E attached to human endometrial epithelial cells. Infect Immun 70: 3413-3418.
11. Eidels, L., Proia, R.L., and Hart, D.A. (1983) Membrane receptors for bacterial toxins. Microbiol Rev 47: 596-620.
12. Eng, J.K., McCormick, A.L., and Yates, J.R.I. (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5: 976-989.
13. Fenouillet, E., Barbouche, R., Courageot, J., and Miquelis, R. (2001) The catalytic activity of protein disulfide isomerase is involved in human immunodeficiency virus envelope-mediated membrane fusion after CD4 cell binding. J Infect Dis 183: 744-752.
14. Fudyk, T., Olinger, L., and Stephens, R.S. (2002) Selection of mutant cell lines resistant to infection by Chlamydia trachomatis and Chlamydia pneumoniae. Infect Immun 70: 6444-6447.
15. Fudyk, T., Olinger, L., and Stephens, R.S. (2006) Selection of mutant cell lines resistant to infection by Chlamydia spp. Infect Immun 74: 1996-1997.
16. Gallina, A., Hanley, T.M., Mandel, R., Trahey, M., Broder, C.C., Viglianti, G.A., and Ryser, H.J. (2002) Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J Biol Chem 277: 50579-50588.
17. Giannini, G., Rappuoli, R., and Ratti, G. (1984) The amino-acid sequence of two non-toxic mutants of diphtheria toxin: CRM45 and CRM197. Nucleic Acids Res 12: 4063-4069.
18. Guseva, N.V., Dessus-Babus, S.C., Whittimore, J.D., Moore, C.G., and Wyrick, P.B. (2005) Characterization of estrogen-responsive epithelial cell lines and their infectivity by genital Chlamydia trachomatis. Microbes Infect 7: 1469-1481.
19. Hackstadt, T. (1999) Cell biology. In Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. Stephens, R.S. (ed.). Washington, DC: American Society for Microbiology, pp. 101-138.
20. Hackstadt, T., Todd, W.J., and Caldwell, H.D. (1985) Disulfide-mediated interactions of the chlamydial major outer membrane protein: Role in the differentiation of chlamydiae? J Bacteriol 161: 25-31.
21. Hatch, T.P. (1996) Disulfide cross-linked envelope proteins: The functional equivalent of peptidoglycan in chlamydiae? J Bacteriol 178: 1-5.
22. Hatch, T.P., Allan, I., and Pearce, J.H. (1984) Structural and polypeptide differences between envelopes of infective and reproductive life cycle forms of Chlamydia spp. J Bacteriol 157: 13-20.
23. Hausman, R.E., and Moscona, A.A. (1975) Purification and characterization of the retina-specific cell-aggregating factor. Proc Natl Acad Sci USA 72: 916-920.
24. Higashiyama, S., Abraham, J.A., Miller, J., Fiddes, J.C., and Klagsbrun, M. (1991) A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251: 936-939.
25. Hotchkiss, K.A., Chesterman, C.N., and Hogg, P.J. (1996) Catalysis of disulfide isomerization in thrombospondin 1 by protein disulfide isomerase. Biochemistry 35: 9761-9767.
26. Huang, E.M., Detwiler, T.C., Milev, Y., and Essex, D.W. (1997) Thiol-disulfide isomerization in thrombospondin: Effects of conformation and protein disulfide isomerase. Blood 89: 3205-3212.
27. Jiang, X.M., Fitzgerald, M., Grant, C.M., and Hogg, P.J. (1999) Redox control of exofacial protein thiols/disulfides by protein disulfide isomerase. J Biol Chem 274: 2416-2423.
28. Kihlstrom, E., Majeed, M., Rozalska, B., and Wadstrom, T. (1992) Binding of Chlamydia trachomatis serovar L2 to collagen types I and IV, fibronectin, heparan sulfate, laminin and vitronectin. Zentralbl Bakteriol 277: 329-333.
29. Kleba, B., and Stephens, R.S. (2005) Bacteria-associated fibronectin does not enhance Chlamydia trachomatis infectivity in vitro. Microb Pathog 39: 53-55.
30. Kleba, B.J., Banta, E., Lindquist, E.A., and Stephens, R.S. (2002) Recruitment of mammalian cell fibronectin to the surface of Chlamydia trachomatis. Infect Immun 70: 3935-3938.
31. Koehler, J.E., Burgess, R.R., Thompson, N.E., and Stephens, R.S. (1990) Chlamydia trachomatis RNA polymerase major sigma subunit. Sequence and structural comparison of conserved and unique regions with Escherichia coli sigma 70 and Bacillus subtilis sigma 43. J Biol Chem 265: 13206-13214.
32. Krishna Rao, A.S., and Hausman, R.E. (1993) cDNA for R-cognin: Homology with a multifunctional protein. Proc Natl Acad Sci USA 90: 2950-2954.
33. Lamberg, A., Jauhiainen, M., Metso, J., Ehnholm, C., Shoulders, C., Scott, J., et.al. (1996) The role of protein disulfide isomerase in the microsomal triacylglycerol transfer protein does not reside in its isomerase activity. Biochem J 315 (Part 2): 533-536.
34. Lindquist, E.A., Marks, J.D., Kleba, B.J., and Stephens, R.S. (2002) Phage-display antibody detection of Chlamydia trachomatis -associated antigens. Microbiology 148: 443-451.
35. Markovic, I., Stantchev, T.S., Fields, K.H., Tiffany, L.J., Tomic, M., Weiss, C.D., et.al. (2003) Thiol/disulfide exchange is a pre-requisite for CXCR4-tropic HIV-1 envelope-mediated T-cell fusion during viral entry. Blood 103: 1586-1594.
36. Mekalanos, J.J., Collier, R.J., and Romig, W.R. (1979) Enzymatic activity of cholera toxin. II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition. J Biol Chem 254: 5855-5861.
37. Moss, J., Manganiello, V.C., and Vaughan, M. (1976) Hydrolysis of nicotinamide adenine dinucleotide by choleragen and its A protomer: possible role in the activation of adenylate cyclase. Proc Natl Acad Sci USA 73: 4424-4427.
38. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
39. Noiva, R. (1999) Protein disulfide isomerase: The multifunctional redox chaperone of the endoplasmic reticulum. Semin Cell Dev Biol 10: 481-493.
40. O'Farrell, P.H. (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021.
41. Ryser, H.J., Mandel, R., and Ghani, F. (1991) Cell surface sulfhydryls are required for the cytotoxicity of diphtheria toxin but not of ricin in Chinese hamster ovary cells. J Biol Chem 266: 18439-18442.
42. Ryser, H.J., Levy, E.M., Mandel, R., and DiSciullo, G.J. (1994) Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc Natl Acad Sci USA 91: 4559-4563.
43. Schachter, J. (1999) Infection and disease epidemiology. In Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. Stephens, R.S. (ed.). Washington, DC: American Society for Microbiology, pp. 139-169.
44. Stephens, R.S. (2003) The cellular paradigm of chlamydial pathogenesis. Trends Microbiol 11: 44-51.
45. Su, H., Raymond, L., Rockey, D.D., Fischer, E., Hackstadt, T., and Caldwell, H.D. (1996) A recombinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc Natl Acad Sci USA 93: 11143-11148.
46. Ting, L.M., Hsia, R.C., Haidaris, C.G., and Bavoil, P.M. (1995) Interaction of outer envelope proteins of Chlamydia psittaci GPIC with the HeLa cell surface. Infect Immun 63: 3600-3608.
47. Tsai, B., Rodighiero, C., Lencer, W.I., and Rapoport, T.A. (2001) Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104: 937-948.
48. Turano, C., Coppari, S., Altieri, F., and Ferraro, A. (2002) Proteins of the PDI family: Unpredicted non-ER locations and functions. J Cell Physiol 193: 154-163.
49. Vretou, E., Goswami, P.C., and Bose, S.K. (1989) Adherence of multiple serovars of Chlamydia trachomatis to a common receptor on HeLa and McCoy cells is mediated by thermolabile protein(s). J Gen Microbiol 135 (Part 12): 3229-3237.
50. Wehrl, W., Brinkmann, V., Jungblut, P.R., Meyer, T.F., and Szczepek, A.J. (2004) From the inside out -processing of the chlamydial autotransporter PmpD and its role in bacterial adhesion and activation of human host cells. Mol Microbiol 51: 319-334.
51. Wetterau, J.R., Combs, K.A., Spinner, S.N., and Joiner, B.J. (1990) Protein disulfide isomerase is a component of the microsomal triglyceride transfer protein complex. J Biol Chem 265: 9801-9807.
52. Zhang, J.P., and Stephens, R.S. (1992) Mechanism of C.trachomatis attachment to eukaryotic host cells. Cell 69: 861-869.
53. Zhang, Y.X., Watkins, N.G., Stewart, S., and Caldwell, H.D. (1987) The low-molecular-mass, cysteine-rich outer membrane protein of Chlamydia trachomatis possesses both biovar- and species-specific epitopes. Infect Immun 55: 2570-2573.