Infection of epithelial cells by pathogenic neisseriae reduces the levels of multiple lysosomal constituents

Infection and Immunity

Volumn 66, Issue 10, 1998, Pages 5001-5007

  Ayala, Patricia ^a   Lin, Lan ^b   Hopper, Sylvia ^a   Fukuda, Minoru ^c   So, Magdalene ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; BETA TUBULIN; GLYCOPROTEIN; LYSOSOME ENZYME; MEMBRANE PROTEIN;

ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; GONORRHEA; GRAM NEGATIVE INFECTION; HUMAN; HUMAN CELL; HYDROLYSIS; LYSOSOME; NEISSERIA GONORRHOEAE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL;

EID: 0031658088     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.66.10.5001-5007.1998     Document Type: Article

References (34)

1. Barriocanal, J. G., J. S. Bonifacino, L. Yuan, and I. V. Sandoval. 1986. Biosynthesis, glycosylation, movement through the Golgi system and transport to lysosomes by an N-linked carbohydrate independent mechanism of three lysosomal integral membrane proteins. J. Biol. Chem. 261:16755-16763.
2. Carlsson, S. R., J. Roth, F. Piller, and M. Fukuda. 1988. Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp1 and h-lamp2. Major sialoglycoproteins carrying polylactosaminoglycan. J. Biol. Chem. 263:18911-18919.
3. Cha, Y., S. M. Holland, and J. T. August. 1990. The cDNA sequence of mouse LAMP-2. J. Biol. Chem. 265:5008-5013.
4. Chen, J. W., G. L. Chen, M. P. D'Souza, T. L. Murphy, and J. T. August. 1986. Lysosomal membrane glycoproteins: properties of LAMP-1 and LAMP-2 Bioehem. Soc. Symp. 51:97-112.
5. Chen, J. W., T. L. Murphy, M. C . Willingham, I. Pastan, and J. T. August. 1985. Identification of two lysosomal membrane glycoproteins. J. Cell Biol. 101:85-95.
6. Frangione, B., and C. Wolfenstein-Todel. 1972. Partial duplication in the "hinge" region of IgA1 myeloma proteins. Proc. Natl. Acad. Sci. USA 69:3073-3676.
7. Fukuda, M. 1991. Lysosomal glycoproteins: structure, biosynthesis and intracellular trafficking. J. Biol. Chem. 266:21327-21330.
8. Fukuda, M., J. Viitala, J. Muttermon, and S. R. Carlsson. 1988. Cloning of cDNAs encoding human lysosomal membrane glycoproteins. h-lamp1 and h-lamp2. Comparison of their deduced amino acid sequences. J. Biol. Chem. 263:18920-18928.
9. Gottschalk, S., A. Waheed, P. Schmidt, P. Laidler, and K. von Figura. 1989. Sequential processing of lysosomal acid phosphatase by a cytoplasmic thiol proteinase and a lysosomal aspartyl proteinase. EMBO J. 8:3215-3219.
10. Hauck, C. R., and T. F. Meyer. 1997. The lysosomal/phagosomal membrane protein h-lamp-1 is a target of the IgA1 protease of Neisseria gonorrhoeae. FEBS Lett. 405:86-90.
11. Holtzman, E. 1989. Lysosomes. Coordinating ed., P. Siekewitz, Plenum Press, New York, N.Y.
12. Kornfeld, R., and S. Kornfeld. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664.
13. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
14. Lin, L., P. Ayala, J. Larson, M. Mulks, M. Fukuda, S. R. Carlsson, C. Enns, and M. So. 1997. The Neisseria type 2 IgA1 protease cleaves LAMP1 and promotes survival of bacteria within epithelial cells. Mol. Microbiol. 24:1083-1094.
15. McGee, Z., A. Johnson, and D. Taylor-Robinson. 1981. Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J. Infect. Dis. 143:413-422.
16. Merz, A., and M. So. Unpublished data.
17. Merz, A. J., D. B. Rifenberry, C. G. Arvidson, and M. So. 1996. Traversal of a polarized epithelium by pathogenic Neisseriae: facilitation by Type IV pili and maintenance of epithelial barrier function. Mol. Med. 2:745-754.
18. Metzelaar, M. J., P. L. Wijngaard, P. J. Peters, J. J. Sixma, H. C. N- ieuwenhuis, and H. C. Clevers. 1991. CD63 antigen, A novel lysosomal membrane glycoprotein. cloned by a screening procedure for intracellular antigens in eukaryotic cells. J. Biol. Chem. 266:3239-3245.
19. Mulks, M. H. 1985. Microbial IgA proteases. Coordinating ed., I. I. Holder. CRC Press, Boca Raton, Fla.
20. Mulks, M. H., and R. J. Shoberg. 1994. Bacterial immunoglubulin A1 proteases. Methods Enzymol. 235:543-554.
21. Nassif, X., J. Lowy, P. Stenberg, P. O'Gaora, A. Ganji, and M. So. 1993. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 8:719-725.
22. Plaut, A. G., J. V. Gilbert, M. S. Artenstein, and J. D. Capra. 1975. Neisseria gonorrhoeae and Neisseria meningitidis: extracellular enzyme cleaves human immunoglobulin A. Science 190:1103-1105.
23. Pohlmann, R., C. Krentler, B. Schmidt, W. Schroder, G. Lorkowski, G. Culley, G. Mersmann, C. Geier, A. Waheed, S. Gottschalk, K. H. Grzeschik, A. Hasilik, and F. von Figura. 1988. Human lysosomal acid phosphatases: cloning, expression and chromosomal assignment. EMBO J. 7:2343-2350.
24. Pohlner, J., R. Halter, K. Beyreuther, and T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458-460.
25. Pujol, C., E. Eugène, L. de Saint Martin, and X. Nassif. 1997. Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect. Immun. 65:4836-4842.
26. Shaw, J. H., and S. Falkow. 1988. Model for invasion of human tissue culture cells by Neisseria gonorrhoeae. Infect. Immun. 56:1625-1632.
27. Shoberg, R. J., and M. H. Mulks. 1991. Proteolysis of bacterial membrane proteins by Neisseria gonorrhoeae type 2 immunoglobulin A1 protease. Infect. Immun. 59:2535-2541.
28. Stephens, D. S. 1989. Gonococcal and meningococcal pathogenesis as defined by human cell, cell culture, and organ culture assays. Clin. Microbiol. Rev. 2:S104-S111.
29. Stephens, D. S., L. H. Hoffman, and Z. McGee. 1983. Interaction of Neisseria meningitidis with human nasopharyngeal mucosa: attachment and entry into columnar epithelial cells. J. Infect. Dis. 148:369-376.
30. Viitala, J., S. R. Carlson, P. D. Siebert, and M. Fukuda. 1988. Molecular cloning of cDNAs encoding lampA, a human lysosomal membrane glycoprotein with apparent Mr= 120,000. Proc. Natl. Acad. Sci. USA 85:3743-3747.
31. Waheed, A., S. Gottschalk, A. Hille, C. Krentler, R. Pohlmann, T. Braulke, H. Hauser, H. Geuze, and K. von Figura. 1988. Human lysosomal acid phosphatase is transported as a transmembrane protein to lysosomes in transfected baby hamster kidney cells. EMBO J. 7:2351-2358.
32. Weel, J. F., C. T. Hopman, and J. P. van Putten. 1991. Bacterial entry and intracellular processing of Neisseria gonorrhoeae in epithelial cells: immunomorphological evidence for alterations in the major outer membrane protein P.IB. J. Exp. Med. 174:705-715.
33. Williams, J. M., G. C. Chen, L. Zhu, and R. F. Rest. 1997. Using the yeast two-hybrid system to identify human epithelial cell proteins that bind gonococcal Opa proteins: intracellular gonococci bind pyruvate kinase via their Opa-proteins and require host pyruvate for growth. Mol. Microbiol. 27:171-186.
34. Zamboni, L., and C. Di Martino. 1967. Buffered picric acid paraformaldehyde: a new, rapid fixative for electron microscopy. J. Cell Biol. 35:148A.