Reassessing the role of the secreted protease CPAF in Chlamydia trachomatis infection through genetic approaches

Pathogens and Disease

Volumn 71, Issue 3, 2014, Pages 336-351

  Snavely, Emily A ^a   Kokes, Marcela ^a   Dunn, Joe Dan ^a   Saka, Hector A ^a,c   Nguyen, Bidong D ^a   Bastidas, Robert J ^a   Mccafferty, Dewey G ^a,b   Valdivia, Raphael H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Chlamydia mutants; Live cell imaging; Pathogenesis; Proteolysis

Indexed keywords

CHLAMYDIAL PROTEASE LIKE ACTIVITY FACTOR; ENZYME PRECURSOR; GLYCOGEN; HYDROLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LAMIN ASSOCIATED PROTEIN 1; SERINE PROTEINASE; STAUROSPORINE; SYNAPSIN I; UNCLASSIFIED DRUG; VIMENTIN; BACTERIAL PROTEIN; MUTANT PROTEIN; PEPTIDE HYDROLASE; VIRULENCE FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL VIABILITY; CELL LYSATE; CELL MEMBRANE; CHEMICAL MUTAGENESIS; CHLAMYDIASIS; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVITY; ENZYME RELEASE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC MANIPULATION; GENOTYPE; GOLGI COMPLEX; HELA CELL LINE; HOST CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; INTERMEDIATE FILAMENT; LOSS OF FUNCTION MUTATION; MEMBRANE PERMEABILITY; NONHUMAN; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; REINFECTION; VERO CELL LINE; ANIMAL; CHLAMYDIA TRACHOMATIS; CHLOROCEBUS AETHIOPS; DEFICIENCY; ENZYMOLOGY; EPITHELIUM CELL; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY;

ANIMALS; BACTERIAL PROTEINS; CERCOPITHECUS AETHIOPS; CHLAMYDIA TRACHOMATIS; EPITHELIAL CELLS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MUTANT PROTEINS; PEPTIDE HYDROLASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; VERO CELLS; VIRULENCE FACTORS;

EID: 84904867513     PISSN: None     EISSN: 2049632X     Source Type: Journal    
DOI: 10.1111/2049-632X.12179     Document Type: Article

References (46)

1. Bednar MM, Jorgensen I, Valdivia RH & McCafferty DG (2011) Chlamydia protease-like activity factor (CPAF): characterization of proteolysis activity in vitro and development of a nanomolar affinity CPAF zymogen-derived inhibitor. Biochemistry 50: 7441-7443.
2. Belland R, Ojcius DM & Byrne GI (2004) Chlamydia. Nature reviews. Microbiology 2: 530-531.
3. Brown HM, Knowlton AE & Grieshaber SS (2012) Chlamydial infection induces host cytokinesis failure at abscission. Cell Microbiol 14: 1554-1567.
4. Byrne GI & Ojcius DM (2004) Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat Rev Microbiol 2: 802-808.
5. Chen D, Lei L, Lu C, Flores R, DeLisa MP, Roberts TC, Romesberg FE & Zhong G (2010) Secretion of the chlamydial virulence factor CPAF requires the Sec-dependent pathway. Microbiology 156: 3031-3040.
6. Chen AL, Johnson KA, Lee JK, Sutterlin C & Tan M (2012) CPAF: a Chlamydial protease in search of an authentic substrate. PLoS Pathog 8: e1002842.
7. Christian JG, Vier J, Paschen SA & Hacker G (2010a) Cleavage of the NF-{kappa}B-family protein p65/RelA by the chlamydial protease chlamydial protease-like activity factor (CPAF) impairs pro-inflammatory signalling in cells Infected with Chlamydiae. J Biol Chem 285: 41320-41327.
8. Christian J, Vier J, Paschen SA & Hacker G (2010b) Cleavage of the NF-kappaB family protein p65/RelA by the chlamydial protease-like activity factor (CPAF) impairs proinflammatory signaling in cells infected with Chlamydiae. J Biol Chem 285: 41320-41327.
9. Christian JG, Heymann J, Paschen SA, Vier J, Schauenburg L, Rupp J, Meyer TF, Häcker G & Heuer D (2011) Targeting of a chlamydial protease impedes intracellular bacterial growth. PLoS Pathog 7: e1002283.
10. Conrad T, Yang Z, Ojcius D & Zhong G (2013) A path forward for the chlamydial virulence factor CPAF. Microbes Infect 15: 1026-1032.
11. Darville T & Hiltke TJ (2010) Pathogenesis of genital tract disease due to Chlamydia trachomatis. J Infect Dis 201(suppl 2): S114-S125.
12. Dong F, Su H, Huang Y, Zhong Y & Zhong G (2004a) Cleavage of host keratin 8 by a Chlamydia-secreted protease. Infect Immun 72: 3863-3868.
13. Dong F, Pirbhai M, Zhong Y & Zhong G (2004b) Cleavage-dependent activation of a chlamydia-secreted protease. Mol Microbiol 52: 1487-1494.
14. Fan T, Lu H, Hu H, Shi L, McClarty GA, Nance DM, Greenberg AH & Zhong G (1998) Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med 187: 487-496.
15. Fischer SF, Vier J, Kirschnek S, Klos A, Hess S, Ying S & Häcker G (2004) Chlamydia inhibit host cell apoptosis by degradation of proapoptotic BH3-only proteins. J Exp Med 200: 905-916.
16. Giles DK & Wyrick PB (2008) Trafficking of chlamydial antigens to the endoplasmic reticulum of infected epithelial cells. Microbes Infect 10: 1494-1503.
17. Giles DK, Whittimore JD, LaRue RW, Raulston JE & Wyrick PB (2006) Ultrastructural analysis of chlamydial antigen-containing vesicles everting from the Chlamydia trachomatis inclusion. Microbes Infect 8: 1579-1591.
18. Goodchild RE & Dauer WT (2005) The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J Cell Biol 168: 855-862.
19. Heuer D, Rejman Lipinski A, Machuy N, Karlas A, Wehrens A, Siedler F, Brinkmann V & Meyer TF (2009) Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457: 731-735.
20. Hou S, Lei L, Yang Z, Qi M, Liu Q & Zhong G (2013) Chlamydia trachomatis outer membrane complex protein B (OmcB) is processed by the protease CPAF. J Bacteriol 195: 951-957.
21. Hu VH, Harding-Esch E. M., Burton M. J., Bailey R. L., Kadimpeul J. & Mabey D. C. (2010) Epidemiology and control of trachoma: systematic review. Trop Med Int Health 15: 673-691.
22. Hybiske K & Stephens RS (2007) Mechanisms of host cell exit by the intracellular bacterium Chlamydia. P Natl Acad Sci USA 104: 11430-11435.
23. Jorgensen I, Bednar MM, Amin V, Davis BK, Ting JP, McCafferty DG & Valdivia RH (2011) The Chlamydia protease CPAF regulates host and bacterial proteins to maintain pathogen vacuole integrity and promote virulence. Cell Host Microbe 10: 21-32.
24. Kari L, Goheen MM, Randall LB et al. (2011) Generation of targeted Chlamydia trachomatis null mutants. P Natl Acad Sci USA 108: 7189-7193.
25. Kawana K, Quayle AJ, Ficarra M et al. (2007) CD1d degradation in Chlamydia trachomatis-infected epithelial cells is the result of both cellular and chlamydial proteasomal activity. J Biol Chem 282: 7368-7375.
26. Kumar Y & Valdivia RH (2008) Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4: 159-169.
27. Murthy AK, Guentzel MN, Zhong G & Arulanandam BP (2009) Chlamydial protease-like activity factor-insights into immunity and vaccine development. J Reprod Immunol 83: 179-184.
28. Murthy AK, Li W, Guentzel MN, Zhong G & Arulanandam BP (2011) Vaccination with the defined chlamydial secreted protein CPAF induces robust protection against female infertility following repeated genital chlamydial challenge. Vaccine 29: 2519-2522.
29. Nguyen BD & Valdivia RH (2012) Virulence determinants in the obligate intracellular pathogen Chlamydia trachomatis revealed by forward genetic approaches. P Natl Acad Sci USA 109: 1263-1268.
30. Nguyen BD & Valdivia RH (2013) Forward genetic approaches in Chlamydia trachomatis. J Vis Exp e50636.
31. Paschen SA, Christian JG, Vier J, Schmidt F, Walch A, Ojcius DM & Häcker G (2008) Cytopathicity of Chlamydia is largely reproduced by expression of a single chlamydial protease. J Cell Biol 182: 117-127.
32. Pirbhai M, Dong F, Zhong Y, Pan KZ & Zhong G (2006) The secreted protease factor CPAF is responsible for degrading pro-apoptotic BH3-only proteins in Chlamydia trachomatis-infected cells. J Biol Chem 281: 31495-31501.
33. Qi M, Gong S, Lei L, Liu Q & Zhong G (2011) A Chlamydia trachomatis OmcB C-terminal fragment is released into the host cell cytoplasm and is immunogenic in humans. Infect Immun 79: 2193-2203.
34. Saka HA, Thompson JW, Chen YS, Kumar Y, Dubois LG, Moseley MA & Valdivia RH (2011) Quantitative proteomics reveals metabolic and pathogenic properties of Chlamydia trachomatis developmental forms. Mol Microbiol 82: 1185-1203.
35. Sandkvist M (2001) Type II secretion and pathogenesis. Infect Immun 69: 3523-3535.
36. Sharma M & Rudel T (2009) Apoptosis resistance in Chlamydia-infected cells: a fate worse than death? FEMS Immunol Med Microbiol 55: 154-161.
37. Shaw AC, Vandahl BB, Larsen MR, Roepstorff P, Gevaert K, Vandekerckhove J, Christiansen G & Birkelund S (2002) Characterization of a secreted Chlamydia protease. Cell Microbiol 4: 411-424.
38. Stokes GV (1973) Formation and destruction of internal membranes in L cells infected with Chlamydia psittaci. Infect Immun 7: 173-177.
39. Sun J, Kintner J & Schoborg RV (2008) The host adherens junction molecule nectin-1 is downregulated in Chlamydia trachomatis-infected genital epithelial cells. Microbiology 154: 1290-1299.
40. Valdivia RH (2008) Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr Opin Microbiol 11: 53-59.
41. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR & Clarke IN (2011) Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLoS Pathog 7: e1002258.
42. Yu H, Schwarzer K, Forster M, Kniemeyer O, Forsbach-Birk V, Straube E & Rödel J (2010) Role of high-mobility group box 1 protein and poly(ADP-ribose) polymerase 1 degradation in Chlamydia trachomatis-induced cytopathicity. Infect Immun 78: 3288-3297.
43. Zhong G (2009) Killing me softly: chlamydial use of proteolysis for evading host defenses. Trends Microbiol 17: 467-474.
44. Zhong G (2011) Chlamydia trachomatis secretion of proteases for manipulating host signaling pathways. Front Microbiol 2: 14.
45. Zhong G, Liu L, Fan T, Fan P & Ji H (2000) Degradation of transcription factor RFX5 during the inhibition of both constitutive and interferon gamma-inducible major histocompatibility complex class I expression in chlamydia-infected cells. J Exp Med 191: 1525-1534.
46. Zhong G, Fan P, Ji H, Dong F & Huang Y (2001) Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J Exp Med 193: 935-942.