Biological characterization of Chlamydia trachomatis plasticity zone MACPF domain family protein CT153

Infection and Immunity

Volumn 78, Issue 6, 2010, Pages 2691-2699

  Taylor, Lacey D ^a   Nelson, David E ^b   Dorward, David W ^a   Whitmire, William M ^a   Caldwell, Harlan D ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COMPLEMENT MEMBRANE ATTACK COMPLEX; CT153 PROTEIN; PERFORIN; PHOSPHOLIPASE D; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GROWTH; CELL FRACTIONATION; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS;

BACTERIAL PROTEINS; CELL FRACTIONATION; CELL MEMBRANE; CHLAMYDIA TRACHOMATIS; CYTOSOL; HUMANS; HYDROLYSIS; INCLUSION BODIES; VIRULENCE FACTORS;

EID: 77952734617     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01455-09     Document Type: Article

References (60)

1. Azuma, Y., H. Hirakawa, A. Yamashita, Y. Cai, M. A. Rahman, H. Suzuki, S. Mitaku, H. Toh, S. Goto, T. Murakami, K. Sugi, H. Hayashi, H. Fukushi, M. Hattori, S. Kuhara, and M. Shirai. 2006. Genome sequence of the cat pathogen, Chlamydophila felis. DNA Res. 13:15-23.
2. Bannantine, J. P., R. S. Griffiths, W. Viratyosin, W. J. Brown, and D. D. Rockey. 2000. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell. Microbiol. 2:35-47.
3. Beatty, W. L. 2006. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J. Cell Sci. 119:350-359.
4. Beatty, W. L., G. I. Byrne, and R. P. Morrison. 1993. Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc. Natl. Acad. Sci. U. S. A. 90:3998-4002.
5. Beatty, W. L., R. P. Morrison, and G. I. Byrne. 1994. Immunoelectron-microscopic quantitation of differential levels of chlamydial proteins in a cell culture model of persistent Chlamydia trachomatis infection. Infect. Immun. 62:4059-4062.
6. Belland, R. J., M. A. Scidmore, D. D. Crane, D. M. Hogan, W. Whitmire, G. McClarty, and H. D. Caldwell. 2001. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc. Natl. Acad. Sci. U. S. A. 98:13984-13989.
7. Belland, R. J., G. Zhong, D. D. Crane, D. Hogan, D. Sturdevant, J. Sharma, W. L. Beatty, and H. D. Caldwell. 2003. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. U. S. A. 100:8478-8483.
8. Caldwell, H. D., J. Kromhout, and J. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31:1161-1176.
9. Caldwell, H. D., C. C. Kuo, and G. E. Kenny. 1975. Antigenic analysis of chlamydiae by two-dimensional immunoelectrophoresis. I. Antigenic heterogeneity between C. trachomatis and C. psittaci. J. Immunol. 115:963-968.
10. Caldwell, H. D., H. Wood, D. Crane, R. Bailey, R. B. Jones, D. Mabey, I. Maclean, Z. Mohammed, R. Peeling, C. Roshick, J. Schachter, A. W. Solomon, W. E. Stamm, R. J. Suchland, L. Taylor, S. K. West, T. C. Quinn, R. J. Belland, and G. McClarty. 2003. Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J. Clin. Invest. 111:1757-1769.
11. Carabeo, R. A., D. J. Mead, and T. Hackstadt. 2003. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc. Natl. Acad. Sci. U. S. A. 100:6771-6776.
12. Carlson, J. H., S. Hughes, D. Hogan, G. Cieplak, D. E. Sturdevant, G. McClarty, H. D. Caldwell, and R. J. Belland. 2004. Polymorphisms in the Chlamydia trachomatis cytotoxin locus associated with ocular and genital isolates. Infect. Immun. 72:7063-7072.
13. Carlson, J. H., S. F. Porcella, G. McClarty, and H. D. Caldwell. 2005. Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect. Immun. 73:6407-6418.
14. Cocchiaro, J. L., Y. Kumar, E. R. Fischer, T. Hackstadt, and R. H. Valdivia. 2008. Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc. Natl. Acad. Sci. U. S. A. 105:9379-9384.
15. Cossart, P., M. F. Vicente, J. Mengaud, F. Baquero, J. C. Perez-Diaz, and P. Berche. 1989. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect. Immun. 57:3629-3636.
16. Dong, F., J. Sharma, Y. Xiao, Y. Zhong, and G. Zhong. 2004. Intramolecular dimerization is required for the chlamydia-secreted protease CPAF to degrade host transcriptional factors. Infect. Immun. 72:3869-3875.
17. Ellis, R. J., and S. M. van der Vies. 1991. Molecular chaperones. Annu. Rev. Biochem. 60:321-347.
18. Fan, T., H. Lu, H. Hu, L. Shi, G. A. McClarty, D. M. Nance, A. H. Greenberg, and G. Zhong. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187:487-496.
19. 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. (Pubitemid 17084156)
20. Giddings, K. S., A. E. Johnson, and R. K. Tweten. 2003. Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins. Proc. Natl. Acad. Sci. U. S. A. 100:11315-11320.
21. Hackstadt, T., D. D. Rockey, R. A. Heinzen, and M. A. Scidmore. 1996. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 15:964-977.
22. Hadders, M. A., D. X. Beringer, and P. Gros. 2007. Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317:1552-1554.
23. Hadding, U., and H. J. Muller-Eberhard. 1969. The ninth component of human complement: isolation, description and mode of action. Immunology 16:719-735.
24. Hatch, G. M., and G. McClarty. 1998. Phospholipid composition of purified Chlamydia trachomatis mimics that of the eucaryotic host cell. Infect. Immun. 66:3727-3735.
25. Heuer, D., A. R. Lipinski, N. Machuy, A. Karlas, A. Wehrens, F. Siedler, V. Brinkmann, and T. F. Meyer. 2009. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457:731-735.
26. Ishino, T., Y. Chinzei, and M. Yuda. 2005. A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell. Microbiol. 7:199-208.
27. Kadota, K., T. Ishino, T. Matsuyama, Y. Chinzei, and M. Yuda. 2004. Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc. Natl. Acad. Sci. U. S. A. 101:16310-16315.
28. Kafsack, B. F., J. D. Pena, I. Coppens, S. Ravindran, J. C. Boothroyd, and V. B. Carruthers. 2009. Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323:530-533.
29. Kalman, S., W. Mitchell, R. Marathe, C. Lammel, J. Fan, R. W. Hyman, L. Olinger, J. Grimwood, R. W. Davis, and R. S. Stephens. 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21:385-389.
30. Kari, L., W. M. Whitmire, J. H. Carlson, D. D. Crane, N. Reveneau, D. E. Nelson, D. C. Mabey, R. L. Bailey, M. J. Holland, G. McClarty, and H. D. Caldwell. 2008. Pathogenic diversity among Chlamydia trachomatis ocular strains in nonhuman primates is affected by subtle genomic variations. J. Infect. Dis. 197:449-456.
31. Kleba, B., and R. S. Stephens. 2008. Chlamydial effector proteins localized to the host cell cytoplasmic compartment. Infect. Immun. 76:4842-4850.
32. Kumar, Y., J. Cocchiaro, and R. H. Valdivia. 2006. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr. Biol. 16: 1646-1651.
33. Madden, J. C., N. Ruiz, and M. Caparon. 2001. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in Grampositive bacteria. Cell 104:143-152.
34. McClarty, G., H. D. Caldwell, and D. E. Nelson. 2007. Chlamydial interferon gamma immune evasion influences infection tropism. Curr. Opin. Microbiol. 10:47-51.
35. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143-190.
36. Nagamune, H., C. Ohnishi, A. Katsuura, K. Fushitani, R. A. Whiley, A. Tsuji, and Y. Matsuda. 1996. Intermedilysin, a novel cytotoxin specific for human cells secreted by Streptococcus intermedius UNS46 isolated from a human liver abscess. Infect. Immun. 64:3093-3100.
37. Nelson, D. E., D. D. Crane, L. D. Taylor, D. W. Dorward, M. M. Goheen, and H. D. Caldwell. 2006. Inhibition of chlamydiae by primary alcohols correlates with the strain-specific complement of plasticity zone phospholipase D genes. Infect. Immun. 74:73-80.
38. Nelson, D. E., L. D. Taylor, J. G. Shannon, W. M. Whitmire, D. D. Crane, G. McClarty, H. Su, L. Kari, and H. D. Caldwell. 2007. Phenotypic rescue of Chlamydia trachomatis growth in IFN-gamma treated mouse cells by irradiated Chlamydia muridarum. Cell. Microbiol. 9:2289-2298.
39. Nelson, D. E., D. P. Virok, H. Wood, C. Roshick, R. M. Johnson, W. M. Whitmire, D. D. Crane, O. Steele-Mortimer, L. Kari, G. McClarty, and H. D. Caldwell. 2005. Chlamydial IFN-gamma immune evasion is linked to host infection tropism. Proc. Natl. Acad. Sci. U. S. A. 102:10658-10663.
40. Peitsch, M. C., P. Amiguet, R. Guy, J. Brunner, J. V. Maizel, Jr., and J. Tschopp. 1990. Localization and molecular modelling of the membrane-inserted domain of the ninth component of human complement and perforin. Mol. Immunol. 27:589-602.
41. Ponting, C. P. 1999. Chlamydial homologues of the MACPF (MAC/perforin) domain. Curr. Biol. 9:R911-R913.
42. Ponting, C. P., and I. D. Kerr. 1996. A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues. Protein Sci. 5:914-922.
43. Raulston, J. E. 1997. Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect. Immun. 65:4539-4547.
44. Read, T. D., R. C. Brunham, C. Shen, S. R. Gill, J. F. Heidelberg, O. White, E. K. Hickey, J. Peterson, T. Utterback, K. Berry, S. Bass, K. Linher, J. Weidman, H. Khouri, B. Craven, C. Bowman, R. Dodson, M. Gwinn, W. Nelson, R. DeBoy, J. Kolonay, G. McClarty, S. L. Salzberg, J. Eisen, and C. M. Fraser. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397-1406.
45. Read, T. D., G. S. Myers, R. C. Brunham, W. C. Nelson, I. T. Paulsen, J. Heidelberg, E. Holtzapple, H. Khouri, N. B. Federova, H. A. Carty, L. A. Umayam, D. H. Haft, J. Peterson, M. J. Beanan, O. White, S. L. Salzberg, R. C. Hsia, G. McClarty, R. G. Rank, P. M. Bavoil, and C. M. Fraser. 2003. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res. 31:2134-2147.
46. Robertson, D. K., L. Gu, R. K. Rowe, and W. L. Beatty. 2009. Inclusion biogenesis and reactivation of persistent Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog. 5:e1000664.
47. Rosado, C. J., A. M. Buckle, R. H. Law, R. E. Butcher, W. T. Kan, C. H. Bird, K. Ung, K. A. Browne, K. Baran, T. A. Bashtannyk-Puhalovich, N. G. Faux, W. Wong, C. J. Porter, R. N. Pike, A. M. Ellisdon, M. C. Pearce, S. P. Bottomley, J. Emsley, A. I. Smith, J. Rossjohn, E. L. Hartland, I. Voskoboinik, J. A. Trapani, P. I. Bird, M. A. Dunstone, and J. C. Whisstock. 2007. A common fold mediates vertebrate defense and bacterial attack. Science 317: 1548-1551.
48. Rosado, C. J., S. Kondos, T. E. Bull, M. J. Kuiper, R. H. Law, A. M. Buckle, I. Voskoboinik, P. I. Bird, J. A. Trapani, J. C. Whisstock, and M. A. Dunstone. 2008. The MACPF/CDC family of pore-forming toxins. Cell. Microbiol. 10:1765-1774.
49. Sakurai, N., J. Kaneko, Y. Kamio, and T. Tomita. 2004. Cloning, expression, and pore-forming properties of mature and precursor forms of pleurotolysin, a sphingomyelin-specific two-component cytolysin from the edible mushroom Pleurotus ostreatus. Biochim. Biophys. Acta 1679:65-73.
50. Shirai, M., H. Hirakawa, M. Kimoto, M. Tabuchi, F. Kishi, K. Ouchi, T. Shiba, K. Ishii, M. Hattori, S. Kuhara, and T. Nakazawa. 2000. Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA. Nucleic Acids Res. 28:2311-2314.
51. 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.
52. Stephens, R. S., S. Kalman, C. Lammel, J. Fan, R. Marathe, L. Aravind, W. Mitchell, L. Olinger, R. L. Tatusov, Q. Zhao, E. V. Koonin, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
53. Swanson, K. A., L. D. Taylor, S. D. Frank, G. L. Sturdevant, E. R. Fischer, J. H. Carlson, W. M. Whitmire, and H. D. Caldwell. 2009. Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure. Infect. Immun. 77:508-516.
54. Tamura, A., A. Matsumoto, G. P. Manire, and N. Higashi. 1971. Electron microscopic observations on the structure of the envelopes of mature elementary bodies and developmental reticulate forms of Chlamydia psittaci. J. Bacteriol. 105:355-360.
55. Thomson, N. R., M. T. Holden, C. Carder, N. Lennard, S. J. Lockey, P. Marsh, P. Skipp, C. D. O'Connor, I. Goodhead, H. Norbertzcak, B. Harris, D. Ormond, R. Rance, M. A. Quail, J. Parkhill, R. S. Stephens, and I. N. Clarke. 2008. Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18:161-171.
56. Thomson, N. R., C. Yeats, K. Bell, M. T. Holden, S. D. Bentley, M. Living-stone, A. M. Cerdeno-Tarraga, B. Harris, J. Doggett, D. Ormond, K. Mungall, K. Clarke, T. Feltwell, Z. Hance, M. Sanders, M. A. Quail, C. Price, B. G. Barrell, J. Parkhill, and D. Longbottom. 2005. The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res. 15:629-640.
57. Tweten, R. K. 2005. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 73:6199-6209.
58. Uellner, R., M. J. Zvelebil, J. Hopkins, J. Jones, L. K. MacDougall, B. P. Morgan, E. Podack, M. D. Waterfield, and G. M. Griffiths. 1997. Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J. 16:7287-7296.
59. Wylie, J. L., G. M. Hatch, and G. McClarty. 1997. Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J. Bacteriol. 179:7233-7242.
60. Zhong, G., P. Fan, H. Ji, F. Dong, and Y. Huang. 2001. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J. Exp. Med. 193:935-942.