Proteolytic pathways of activation and degradation of a bacterial phospholipase C during intracellular infection by Listeria monocytogenes

Journal of Cell Biology

Volumn 137, Issue 6, 1997, Pages 1381-1392

  Marquis, Hélène ^a,c   Goldfine, Howard ^a   Portnoy, Daniel A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; PHOSPHOLIPASE C;

ARTICLE; BACTERIAL VIRULENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME LOCALIZATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CYTOSOL; ENDOPEPTIDASES; ENZYME ACTIVATION; LISTERIA MONOCYTOGENES; METALLOENDOPEPTIDASES; MICE; PHOSPHATIDYLCHOLINES; PHOSPHOLIPASE C; SPHINGOMYELINS; SUBCELLULAR FRACTIONS; VIRULENCE;

EID: 0030955705     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.6.1381     Document Type: Article

References (61)

1. Bernardini, M.L., J. Mounier, H. d'Hauteville, M. Coquis-Rondon, and P.J. Sansonetti. 1989. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra-and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. USA. 86:3867-3871.
2. Berón, W., C. Alvarez-Dominguez, L. Mayorga, and P.D. Stahl. 1995. Membrane trafficking along the phagocytic pathway. Trends Cell Biol. 5:100-104.
3. Biclecki, J., P. Youngman, P. Connelly, and D.A. Portnoy. 1990. Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature (Lond.). 345:175-176.
4. Bishop, D.K., and D.J. Hinrichs. 1987. Adoptive transfer of immunity to Listeria monocytogenes: the influence of in vitro stimulation on lymphocyte subset requirements. J. Immunol. 139:2005-2009.
5. Bohley, P., and P.O. Seglen. 1992. Proteases and proteolysis in the lysosome. Experientia (Basel). 48:151-157.
6. Brundage, R.A., G.A. Smith, A. Camilli, J.A. Theriot, and D.A. Portnoy. 1993. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc. Natl. Acad. Sci. USA. 90:11890-11894.
7. Camilli, A., L.G. Tilney, and D.A. Portnoy. 1993. Dual roles of plcA in Lisieria monocytogenes pathogenesis. Mol. Microbiol 8:143-157.
8. 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.
9. Clague, M.J., S. Urbé, F. Aniento, and J. Gruenberg. 1994. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269:21-24.
10. Conte, M.P., G. Petrone, C. Longhi, P. Valenti, R. Morelli, F. Superti, and L. Seganti. 1996. The effects of inhibitors of vacuolar acidification on the release of Listeria monocytogenes from phagosomes of Caco-2 cells. J. Med. Microbiol. 44:418-424.
11. Cossart, P., and J. Mengaud. 1989. Listeria monocytogenes. A model system for the molecular study of intracellular parasitism. Mol. Biol. Med. 6:463-474.
12. Cossart, P., M.F. Vicente, J. Mengaud, F. Baquero, J.C. Perez-Diaz, and P. Berchc. 1989. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect. Immun. 57:3629-3636.
13. Crawford, C., R.W. Mason, P. Wikstrom, and E. Shaw. 1988. The design of peptidyldiazomethane inhibitors to distinguish between the cysteine proteinases calpain II, cathepsin L and cathepsin B. Biochem. J. 253:751-758.
14. Cudmore, S., P. Cossart, G. Griffiths, and M. Way. 1995. Actin-based motility of vaccinia virus. Nature (Lond.). 378:636-638.
15. Dabiri, G.A., J.M. Sanger, D.A. Portnoy, and F.S. Southwick. 1990. Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc. Natl. Acad. Sci. USA. 87:6068-6072.
16. Desjardins, M., L.A. Huber, R.G. Parton, and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124:677-688.
17. Domann, E., M. Leimeister-Wächter, W. Goebel, and T. Chakraborty. 1991. Molecular cloning, sequencing, and identification of a metalloprotease gene from Listeria monocytogenes that is species specific and physically linked to the listeriolysin gene. Infect. Immun. 59:65-72.
18. Domann, E., J. Wehland, M. Ronde, S. Pistor, M. Hartl, W. Goebel, M. Leimeister-Wächter, M. Wuenscher, and T. Chakraborty. 1992. A novel bacterial virulence gene in Liberia monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO (Eur. Mol. Biol. Organ.) J. 11:1981-1990.
19. Gaillard, J.-L., P. Berche, and P. Sansonetti. 1986. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Liberia monocytogenes. Infect. Immun. 52:50-55.
20. Gaillard, J.-L., P. Berche, J. Mounier, S. Richard, and P. Sansonetti. 1987. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect. Immun. 55:2822-2829.
21. Geoffroy, C., J.-L. Gaillard, J.E. Alouf, and P. Berche. 1987. Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Infect. Immun. 55:1641-1646.
22. Geoffroy, C., J. Raveneau, J.-L. Beretti, A. Lecroisey, J.-A. Vazquez-Boland, J.E. Alouf, and P. Berche. 1991. Purification and characterization of an extracellular 29-kilodalton phospholipase C from Listeria monocytogenes. Infect. Immun. 59:2382-2388.
23. Goldfine, H., N.C. Johnston, and C. Knob. 1993. Nonspecific phospholipase C of Listeria monocytogenes: activity on phospholipids in Triton X-100-mixed micelles and in biological membranes. J. Bacteriol. 175:4298-4306.
24. Gruenberg, J., and F.R. Maxfield. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
25. Hase, C.C., and R.A. Finkelstein. 1993. Bacterial extracellular zinc-containing metalloproteases. Microbiol. Rev. 57:823-837.
26. Havell, E.A. 1986. Synthesis and secretion of interferon by murine fibroblasts in response to intracellular Listeria monocytogenes. Infect. Immun. 54:787-792.
27. Heinzen, R.A., S.F. Haves, M.G. Peacock, and T. Hackstadt. 1993. Directional actin polymerization associated with spotted fever group Rickettsia infection of Vero cells. Infect. Immun. 61:1926-1935.
28. Jones, S., K. Preiter, and D.A. Portnoy. 1996. Conversion of an extracellular cytolysin into a phagosome-specific lysin which supports the growth of an intracellular pathogen. Mol. Microbiol. 21:1219-1225.
29. Kathariou, S., P. Metz, H. Hof, and W. Goebel. 1987. Tn916-induced mutations in the hemolvsin determinant affecting virulence of Listeria monocytogenes. J. Bacteriol. 169:1291-1297.
30. Kathariou, S., L. Pine, V. George, G.M. Carlone, and B.P. Holloway. 1990. Nonhemolvtic Listeria monocytogenes mutants that are also noninvasive for mammalian cells in culture: evidence for coordinate regulation of virulence. Infect. Immun. 58:3988-3995.
31. 2. Biochem. Biophys. Res. Commun. 101: 454-458.
32. Kocks, C., E. Gouin, M. Tabouret, P. Berche, H. Ohayon, and P. Cossart. 1992. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell. 68:521-531.
33. Kuhn, M., S. Kathariou, and W. Goebel. 1988. Hemolysin supports survival but not entry of the intracellular bacterium Listeria monocytogenes. Infect. Immun. 56:79-82.
34. Leary, R., D. Larsen, H. Watanabe, and E. Shaw. 1977. Diazomethyl ketone substrate derivatives as active-site directed inhibitors of thiol proteases. Pa-pain. Biochemistry. 16:5857-5861.
35. Lewis, V., S.A. Green, M. Marsh, P. Vihko, A. Helenius, and I. Mellman. 1985. Glycoproteins of the lysosomal membrane. J. Cell Biol. 100:1839-1847.
36. Marquis, H., V. Doshi, and D.A. Portnoy. 1995. The broad-range phospholipase C and a metalloprotease mediate listeriolysin O-independent escape of Listeria monocytogenes from a primary vacuole in human epithelial cells. Infect. Immun. 63:4531-4534.
37. Mengaud, J., C. Geoffroy, and P. Cossart. 1991. Identification of a new operon involved in Listeria monocytogenes virulence: its first gene encodes a protein homologous to bacterial metalloproteases. Infect. Immun. 59:1043-1049.
38. Michel, E., K.A. Reich, R. Favier, P. Berche, and P. Cossart. 1990. Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol. Microbiol. 4:2167-2178.
39. Mounier, J., A. Ryter, M. Coquis-Rondon, and P.J. Sansonetti. 1990. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect. Immun. 58:1048-1058.
40. Niebuhr, K., T. Chakraborty, P. Köllner, and J. Wehland. 1993. Production of monoclonal antibodies to the phosphatidylcholine-specific phospholipase C of Listeria monocytogenes, a virulence factor lor this species. Med. Microbiol. Lett. 2:9-16.
41. North, R.J. 1970. Suppression of cell-mediated immunity to infection by an antimitotic drug. J. Exp. Med. 132:535-545.
42. Olmsted, J.B. 1981. Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples. J. Biol. Chem. 256:11955-11957.
43. Pitt, A., L.S. Mayorga, P.D. Stahl, and A.L. Schwartz. 1992. Alterations in the protein composition of maturing phagosomes. J. Clin. Invest. 90:1978-1983.
44. Portnoy, D.A., P.S. Jacks, and D.J. Hinrichs. 1988. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 167:1459-1471.
45. Portnoy, D.A., T. Chakraborty, W. Goebel, and P. Cossart. 1992. Molecular determinants of Listeria monocytogenes pathogenesis. Infect. Immun. 60:1263-1267.
46. Poyart, C., E. Abachin, I. Razafimanantsoa, and P. Berche. 1993. The zinc metalloprotease of Listeria monocytogenes is required for maturation of phosphatidylcholine phospholipase C: direct evidence obtained by gene complementation. Infect. Immun. 61:1576-1580.
47. Raveneau, J., C. Geoffroy, J.-L. Beretti, J.-L. Gaillard, J.E. Alouf, and P. Berche. 1992. Reduced virulence of a Listeria monocytogenes phospholipase-deficient mutant obtained by transposon insertion into the zinc metalloprotease gene. Infect. Immun. 60:916-921.
48. Rock, K.L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A.L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 78:761-771.
49. Rosen, H., S. Gordon, and R.J. North. 1989. Exacerbation of murine listeriosis by a monoclonal antibody specific for the type 3 complement receptor of myelomonocytic cells. J. Exp. Med. 170:27-37.
50. Smith, G.A., H. Marquis, S. Jones, N.C. Johnston, D.A. Portnoy, and H. Goldfine. 1995. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect. Immun. 63:4231-4237.
51. Smith, K., and P. Youngman. 1992. Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie (Paris). 74:705-711.
52. Sun, A.N., A. Camilli, and D.A. Portnoy. 1990. Isolation of Listeria monocytogenes small-plaque mutants defective for intracelluiar growth and cell-to-cell spread. Infect. Immun. 58:3770-3778.
53. Teysseire, N., C. Chiche-Portiche, and D. Raoult. 1992. Intracellular movements of Rickettsia conorii and R. typhi based on actin polymerization. Res. Microbiol. 143:821-829.
54. Theriot, J.A., T.J. Mitchison, L.G. Tilney, and D.A. Portnoy. 1992. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature (Lond.). 357:257-260.
55. Tilney, L.G., and D.A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite. Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
56. van Weert, A.W.M., K.W. Dunn, H.J. Geuze, F.R. Maxfield, and W. Stoorvogel. 1995. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 130:821-834.
57. Vazquez-Boland, J.-A., C. Kocks, S. Dramsi, H. Ohayon, C. Geoffroy, J. Mengaud, and P. Cossart. 1992. Nucleotide sequence of the lecithinase operon of Liberia monocyogenes and possible role of lecithinase in cell-to-cell spread. Infect. Immun. 60:219-230.
58. Villanueva, M.S., A.J.A.M. Sijts, and E.G. Pamer. 1995. Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells. J. Immunol. 155:5227-5233.
59. Vinitsky, A., C. Michaud, J.C. Powers, and M. Orlowski. 1992. Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex. Biochemistry. 31:9421-9428.
60. Wilcox, D., and R.W. Mason. 1992. Inhibition of cysteine proteinases in lysosomes and whole cells. Biochem. J. 285:495-502.
61. +-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 266:17707-17712.