Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal

Current Opinion in Microbiology

Volumn 12, Issue 1, 2009, Pages 81-87

  Betts, Helen J ^a   Wolf, Katerina ^a   Fields, Kenneth A ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEINS; CHLAMYDIA; CYTOPLASM; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE TRANSPORT PROTEINS; VIRULENCE FACTORS;

CHLAMYDIA; CHLAMYDIAE;

EID: 59849092485     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2008.11.009     Document Type: Review

References (50)

1. Kuo C.C., Jackson L.A., Campbell L.A., and Grayston J.T. Chlamydia pneumoniae (TWAR). Clin Microbiol Rev 8 (1995) 451-461
2. Schachter J. Overview of human diseases. In: Barron A.L. (Ed). Microbiology of Chlamydia (1988), CRC Press, Inc. 153-165
3. Horn M. Chlamydiae as symbionts in eukaryotes. Annu Rev Microbiol 62 (2008) 113-131
4. Horn M., Collingro A., Schmitz-Esser S., Beier C.L., Purkhold U., Fartmann B., Brandt P., Nyakatura G.J., Droege M., Frishman D., et al. Illuminating the evolutionary history of chlamydiae. Science 304 (2002) 728-730
5. Valdivia R.H. Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr Opin Microbiol 11 (2008) 53-59
6. Byrne G.I., and Moulder J.W. Parasite-specified phagocytosis of Chlamydia psittaci and Chlamydia trachomatis by L and HeLa cells. Infect Immun 19 (1978) 598-606
7. Chen J.C., Zhang J.P., and Stephens R.S. Structural requirements of heparin binding to Chlamydia trachomatis. J Biol Chem 271 (1996) 11134-11140
8. Wuppermann F.N., Hegemann J.H., and Jantos C.A. Heparan sulfate-like glycosaminoglycan is a cellular receptor for Chlamydia pneumoniae. J Infect Dis 184 (2001) 181-187
9. Zhang D. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell 69 (1992) 861-869
10. Campbell S., Richmond S.J., and Yates P.S. The effect of Chlamydia trachomatis infection on the host cell cytoskeleton and membrane compartments. J Gen Microbiol 135 (1989) 2379-2386
11. Carabeo R., Grieshaber S., Fischer E., and Hackstadt T. Chlamydia trachomatis induces remodeling of the actin cytoskeleton during attachment and entry into HeLa cells. Infect Immun 70 (2002) 3793-3803
12. Dautry-Varsat A., Subtil A., and Hackstadt T. Recent insights into the mechanisms of Chlamydia entry. Cell Microbiol (2005) 7
13. Carabeo R.A., Grieshaber S.S., Hasenkrug A., Dooley C.A., and Hackstadt T. requirement for the Rac GTPase in Chlamydia trachomatis invasion of non-phagocytic cells. Traffic 5 (2004) 418-425
14. Carabeo R.A., Dooley C.A., Grieshaber S.S., and hackstadt T. Rac interacts with Abi-1 and WAVE2 to promote an Arp2/3-dependent actin recruitment during chlamydial invasion. Cell Microbiol 9 (2007) 2278-2288
15. •].
16. Clifton D.R., Fields K.A., Grieshaber S.S., Dooley C.A., Fischer E.R., Mead D.J., Carabeo R.A., and Hackstadt T. A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc Natl Acad Sci U S A 101 (2004) 10166-10171
17. Jewett T.J., Fischer E.R., Mead D.J., and Hackstadt T. Chlamydial TARP is a bacterial nucleator of actin. PNAS 103 (2006) 15599-15604
18. Jewett T.J., Dooley C.A., Mead D.J., and Hackstadt T. Chlamydia trachomatis tarp is phosphorylated by src family tyrosine kinases. Biochem Biophys Res Comm 371 (2008) 339-344
19. ••]. siRNA-mediated depletion of these GEFs resulted in diminished chlamydial infectivity.
20. Clifton D.R., Dooley C.A., Grieshaber S.S., Carabeo R.A., Fields K.A., and Hackstadt T. Tyrosine phosphorylation of the chlamydial effector protein Tarp is species specific and not required for recruitment of actin. Infect Immun 73 (2005) 3860-3868
21. Subtil A., Wyplosz B., Balana M.E., and Dautry-Varsat A. Analysis of Chlamydia caviae entry sites and involvement of Cdc42 and Rac activity. J Cell Sci 117 (2004) 3923-3933
22. Heinzen R.A., and Hackstadt T. The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecular-weight compounds. Infect Immun 65 (1997) 1088-1094
23. Rockey D.D., Scidmore M.A., Bannantine J.P., and Brown W.J. Proteins in the chlamydial inclusion membrane. Microbes Infect 4 (2002) 333-340
24. Fields K.A., and Hackstadt T. The chlamydial inclusion: escape from the endocytic pathway. Annu Rev Cell Dev Biol 14 (2002) 14
25. Heinzen R.A., Scidmore M.A., Rockey D.D., and Hackstadt T. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun 64 (1996) 796-809
26. Beatty W.L. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J Cell Sci 119 (2006) 350-359
27. Cocchiaro J.L., Kumar Y., Fischer E.R., Hackstadt T., and Valdivia R.H. Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. PNAS 105 (2008) 9379-9384
28. Rzomp K.A., Scholtes L.D., Briggs B.J., Whittaker G.R., and Sidmore M.A. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 71 (2003) 5855-5870
29. Rzomp K.A., Moorhead A.R., and Scidmore M.A. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 74 (2006) 5362-5373
30. Cortes C., Rzomp K.A., Tvinnereim A., Scidmore M.A., and Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 75 (2007) 5586-5596
31. Hackstadt T., Scidmore-Carlson M.A., and Dooley C.A. Chlamydia trachomatis inclusion membrane protein required for intracellular development. Mol Biol Cell 10 Suppl. S (1999) 182A
32. Moorhead A.R., Rzomp K.A., and Scidmore M.A. The Rab6 effector Bicaudal D1 associates with Chlamydia trachomatis inclusions in a biovar-specific manner. Infect Immun 75 (2007) 781-791
33. Delevoye C., Nigles M., Dehoux P., Paumet F., Perrinet S., Dautry-Varsat A., and Subtil A. SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 4 (2008) e1000022. The authors document the ability of SNARE proteins Vamp3, Vamp7, and Vamp8 to associate with chlamydial inclusions. IncA and other Incs are shown to contain SNARE-like motifs. IncA is shown to bind these SNAREs and evidence is presented indicating that SNARE recruitment is dependent on IncA.
34. Dekevoye C., Nilges M., Dautry-Varsat A., and Subtil A. Conservation of the biochemical properties of IncA from Chlamydia trachomatis and Chlamydia caviae: oligomerization of IncA mediates interaction between facing membranes. J Biol Chem. 279 (2004) 46896-46906
35. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82 (2002) 373-428
36. Misaghi S., Balsara Z.R., Catic A., Spooner E., Ploegh H.L., and Starnbach M.N. Chlamydia trachomatis-derived deubiquitinating enzymes in mammalian cells during infection. Mol Microbiol 61 (2006) 142-150
37. Le Negrate G., Krieg A., Faustin M.L., Godzik A., Krajewski S., and Reed J.C. ChlaDub1 of Chlamydia trachomatis suppresses NF-kappaB activation and inhibits IkappaBalpha ubiquitination and degradation. Cell Microbiol 10 (2008) 1879-1892. Ectopic expression studies using C. trachomatis ChlaDub1 revealed the ability of this protein to interfere with NF-kB activation stimulated by proinflammatory stimuli including TNFα, IL-1β, or TLR4 signaling. This activity was shown to correlate with ChlaDub1 binding to IκBα leading to decreased ubiquitination and degradation of IκBα. This activity was specific since ubiquitination of neither TRAF 2 nor TRAF 6 was affected.
38. Lad S.P., Li J., Correia J., Pan Q., Gadwal S., Ulevitch R.J., and Li E. Cleavage of p65/RelA of the NF-κB pathway by Chlamydia. PNAS 104 (2007) 2933-2938
39. Lad S.P., Yang G., Scott D.A., Wang G., Nair P., Mathison J., Reddy V.S., and Li E. Chlamydial CT441 is a PDZ domain-containing tail-specific protease that interferes with the NF-κB pathway of immune response. J Bacteriol 189 (2007) 6619-6625. This study addresses the mechanism by which chlamydial infection induces degradation of RelA. Ectopic expression studies were used to show that the predicted tail-specific protease CT441, but not CPAF, was capable of mediating RelA degradation. Importantly, this activity was detectible in human but not murine cells.
40. Hayden M.S., West A.P., and Ghosh S. NF-kappaB and the immune response. Oncogene 25 (2006) 6758-6780
41. Belland R.J., Scidmore M.A., Crane D.D., Hogan D.M., Whitmire W., McClarty G., and Caldwell H.D. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc Natl Acad Sci U S A 98 (2001) 13984-13989
42. Scidmore M.A.T.H. Mammalian 14-3-3 beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol Microbiol 39 (2001) 1638-1650
43. Jorgensen I., and Valdivia R.H. Pmp-like proteins Pls1 and Pls2 are secreted into the lumen of the Chlamydia trachomatis inclusion. Infect Immun 76 (2008) 3940-3950
44. Kiselev A.O., Stamm W.E., Yates J.R., and Lampe M. Expression, processing, and localization of PmpD of Chlamydia trachomatis serovar L2 during the chlamydial developmental cycle. PLoS ONE 2 (2007) e568
45. Swanson K.A., Taylor L.D., Frank S.D., Sturdevant G.L., Fischer E.R., Carlson J.H., Whitmire W.M., and Caldwell H.D. Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure. Infect Immun 77 (2008) 508-516
46. Wehrl W., Brinkmann V., Jungblut P.R., Meyer T.F., and Szczepek A.J. 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 (2004) 319-334
47. Kumar Y., Cocchiaro J.L., and Valdivia R.H. The Obligate Intracellular Pathogen Chlamydia trachomatis. Targets Host Lipid Droplets Curr Biol 16 (2006) 1646-1651
48. Chellas-Gery B., Linton C.L., and Fields K.A. Human GCIP interacts with CT847, a novel Chlamydia trachomatis type III secretion substrate, and is degraded in a tissue-culture infection model. Cell Microbiol 9 (2007) 2417-2430
49. Stenner-Liewen F., Liewen H., Zapata J., Pawlowski K., Godzik A., and Reed J. CADD, a Chlamydia protein that interacts with death receptors. J Biol Chem 277 (2002) 9633-9636
50. Wolf K, Plano GV, adn Fields KA: CP0236 is a C. pneumoniae-specific Inc which impairs IL-17 signaling via interaction with human Act1. 6th Meeting of the European Society for Chlamydia research [Abstract O57]. 2008. Aarhus, DK.