Chlamydia trachomatis Inclusion Membrane Protein CT228 Recruits Elements of the Myosin Phosphatase Pathway to Regulate Release Mechanisms

Cell Reports

Volumn 3, Issue 6, 2013, Pages 1921-1931

  Lutter, ErikaI ^a   Barger, AlexandraC ^a   Nair, Vinod ^a   Hackstadt, Ted ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CT228 PROTEIN; MYOSIN IIA; MYOSIN IIB; MYOSIN LIGHT CHAIN 2; MYOSIN LIGHT CHAIN KINASE; MYOSIN PHOSPHATASE 1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; CARBOXY TERMINAL SEQUENCE; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; DOWN REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; CHLAMYDIA TRACHOMATIS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PHOSPHORYLATION;

CHLAMYDIA TRACHOMATIS;

EID: 84879795143     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.04.027     Document Type: Article

References (55)

1. Amano M., Ito M., Kimura K., Fukata Y., Chihara K., Nakano T., Matsuura Y., Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J.Biol. Chem. 1996, 271:20246-20249.
2. Bannantine J.P., Griffiths R.S., Viratyosin W., Brown W.J., Rockey D.D. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell. Microbiol. 2000, 2:35-47.
3. Belland R.J., Zhong G., Crane D.D., Hogan D., Sturdevant D., Sharma J., Beatty W.L., Caldwell H.D. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. USA 2003, 100:8478-8483.
4. Birukov K.G., Csortos C., Marzilli L., Dudek S., Ma S.F., Bresnick A.R., Verin A.D., Cotter R.J., Garcia J.G. Differential regulation of alternatively spliced endothelial cell myosin light chain kinase isoforms by p60(Src). J.Biol. Chem. 2001, 276:8567-8573.
5. Bishai E.A., Sidhu G.S., Li W., Dhillon J., Bohil A.B., Cheney R.E., Hartwig J.H., Southwick F.S. Myosin-X facilitates Shigella-induced membrane protrusions and cell-to-cell spread. Cell. Microbiol. 2013, 15:353-367.
6. Burton M.J., Mabey D.C. The global burden of trachoma: a review. PLoS Negl. Trop. Dis. 2009, 3:e460.
7. Caldwell H.D., Kromhout J., Schachter J. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 1981, 31:1161-1176.
8. Carabeo R.A., Mead D.J., Hackstadt T. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc. Natl. Acad. Sci. USA 2003, 100:6771-6776.
9. Chin E., Kirker K., Zuck M., James G., Hybiske K. Actin recruitment to the Chlamydia inclusion is spatiotemporally regulated by a mechanism that requires host and bacterial factors. PLoS ONE 2012, 7:e46949.
10. Clausen J.D., Christiansen G., Holst H.U., Birkelund S. Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol. Microbiol. 1997, 25:441-449.
11. Dehoux P., Flores R., Dauga C., Zhong G., Subtil A. Multi-genome identification and characterization of chlamydiae-specific type III secretion substrates: the Inc proteins. BMC Genomics 2011, 12:109.
12. Derré I., Swiss R., Agaisse H. The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER-Chlamydia inclusion membrane contact sites. PLoS Pathog. 2011, 7:e1002092.
13. Feng J., Ito M., Ichikawa K., Isaka N., Nishikawa M., Hartshorne D.J., Nakano T. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J.Biol. Chem. 1999, 274:37385-37390.
14. Friedrich N., Hagedorn M., Soldati-Favre D., Soldati T. Prison break: pathogens' strategies to egress from host cells. Microbiol. Mol. Biol. Rev. 2012, 76:707-720.
15. Grieshaber S., Grieshaber N., Hackstadt T. Chlamydia trachomatis uses host cell dynein to traffic to the microtube organizing center in a p50 dynamitin independent process. J.Cell Biol. 2003, 116:3793-3802.
16. Grieshaber S.S., Grieshaber N.A., Miller N., Hackstadt T. Chlamydia trachomatis causes centrosomal defects resulting in chromosomal segregation abnormalities. Traffic 2006, 7:940-949.
17. Hackstadt T., Rockey D.D., Heinzen R.A., Scidmore M.A. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 1996, 15:964-977.
18. Hackstadt T., Fischer E.R., Scidmore M.A., Rockey D.D., Heinzen R.A. Origins and functions of the chlamydial inclusion. Trends Microbiol. 1997, 5:288-293.
19. Hackstadt T., Scidmore-Carlson M.A., Shaw E.I., Fischer E.R. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell. Microbiol. 1999, 1:119-130.
20. Haystead T.A. ZIP kinase, a key regulator of myosin protein phosphatase 1. Cell. Signal. 2005, 17:1313-1322.
21. Higashi N. Electron microscopic studies on the mode of reproduction of trachoma virus and psittacosis virus in cell cultures. Exp. Mol. Pathol. 1965, 76:24-39.
22. Hybiske K., Stephens R.S. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl. Acad. Sci. USA 2007, 104:11430-11435.
23. Hybiske K., Stephens R.S. Exit strategies of intracellular pathogens. Nat. Rev. Microbiol. 2008, 6:99-110.
24. Kawano Y., Fukata Y., Oshiro N., Amano M., Nakamura T., Ito M., Matsumura F., Inagaki M., Kaibuchi K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase invivo. J.Cell Biol. 1999, 147:1023-1038.
25. Kiss E., Murányi A., Csortos C., Gergely P., Ito M., Hartshorne D.J., Erdodi F. Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochem. J. 2002, 365:79-87.
26. Kumar Y., Valdivia R.H. Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 2008, 4:159-169.
27. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J.Mol. Biol. 1982, 157:105-132.
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
29. Li Z., Chen C., Chen D., Wu Y., Zhong Y., Zhong G. Characterization of fifty putative inclusion membrane proteins encoded in the Chlamydia trachomatis genome. Infect. Immun. 2008, 76:2746-2757.
30. Lutter E.I., Martens C., Hackstadt T. Evolution and conservation of predicted inclusion membrane proteins in chlamydiae. Comp. Funct. Genomics 2012, 2012:362104.
31. Manjarrez-Hernandez H.A., Baldwin T.J., Williams P.H., Haigh R., Knutton S., Aitken A. Phosphorylation of myosin light chain at distinct sites and its association with the cytoskeleton during enteropathogenic Escherichia coli infection. Infect. Immun. 1996, 64:2368-2370.
32. Mital J., Hackstadt T. Diverse requirements for Src-family tyrosine kinases distinguish chlamydial species. mBio. 2011, 2. e00031-11.
33. Mital J., Miller N.J., Fischer E.R., Hackstadt T. Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network. Cell. Microbiol. 2010, 12:1235-1249.
34. Mott A., Lenormand G., Costales J., Fredberg J.J., Burleigh B.A. Modulation of host cell mechanics by Trypanosoma cruzi. J.Cell. Physiol. 2009, 218:315-322.
35. Moulder J.W. Interaction of chlamydiae and host cells invitro. Microbiol. Rev. 1991, 55:143-190.
36. Philpott D.J., McKay D.M., Mak W., Perdue M.H., Sherman P.M. Signal transduction pathways involved in enterohemorrhagic Escherichia coli-induced alterations in T84 epithelial permeability. Infect. Immun. 1998, 66:1680-1687.
37. Rathman M., de Lanerolle P., Ohayon H., Gounon P., Sansonetti P. Myosin light chain kinase plays an essential role in S.flexneri dissemination. J.Cell Sci. 2000, 113:3375-3386.
38. Rockey D.D., Grosenbach D., Hruby D.E., Peacock M.G., Heinzen R.A., Hackstadt T. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol. Microbiol. 1997, 24:217-228.
39. Rzomp K.A., Moorhead A.R., Scidmore M.A. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect. Immun. 2006, 74:5362-5373.
40. Santangelo P.J., Bao G. Dynamics of filamentous viral RNPs prior to egress. Nucleic Acids Res. 2007, 35:3602-3611.
41. Savkovic S.D., Koutsouris A., Hecht G. PKC zeta participates in activation of inflammatory response induced by enteropathogenic E.coli. Am. J. Physiol. Cell Physiol. 2003, 285:C512-C521.
42. Schachter J. Infection and disease epidemiology. Chlamydia: Intracellular Biology, Pathogenesis, and Immunity 1999, 139-169. ASM Press, Washington, DC. R.S. Stephens (Ed.).
43. Scidmore M.A., Hackstadt T. Mammalian 14-3-3beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol. Microbiol. 2001, 39:1638-1650.
44. Scidmore M.A., Rockey D.D., Fischer E.R., Heinzen R.A., Hackstadt T. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect. Immun. 1996, 64:5366-5372.
45. Scidmore-Carlson M.A., Shaw E.I., Dooley C.A., Fischer E.R., Hackstadt T. Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol. Microbiol. 1999, 33:753-765.
46. Seth-Smith H.M., Harris S.R., Persson K., Marsh P., Barron A., Bignell A., Bjartling C., Clark L., Cutcliffe L.T., Lambden P.R., et al. Co-evolution of genomes and plasmids within Chlamydia trachomatis and the emergence in Sweden of a new variant strain. BMC Genomics 2009, 10:239.
47. Shaw E.I., Dooley C.A., Fischer E.R., Scidmore M.A., Fields K.A., Hackstadt T. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol. Microbiol. 2000, 37:913-925.
48. Sousa S., Cabanes D., El-Amraoui A., Petit C., Lecuit M., Cossart P. Unconventional myosin VIIa and vezatin, two proteins crucial for Listeria entry into epithelial cells. J.Cell Sci. 2004, 117:2121-2130.
49. Todd W.J., Caldwell H.D. The interaction of Chlamydia trachomatis with host cells: ultrastructural studies of the mechanism of release of a biovar II strain from HeLa 229 cells. J.Infect. Dis. 1985, 151:1037-1044.
50. Toh H., Miura K., Shirai M., Hattori M. In silico inference of inclusion membrane protein family in obligate intracellular parasites chlamydiae. DNA Res. 2003, 10:9-17.
51. Tóth A., Kiss E., Gergely P., Walsh M.P., Hartshorne D.J., Erdödi F. Phosphorylation of MYPT1 by protein kinase C attenuates interaction with PP1 catalytic subunit and the 20kDa light chain of myosin. FEBS Lett. 2000, 484:113-117.
52. van Leeuwen H., Elliott G., O'Hare P. Evidence of a role for nonmuscle myosin II in herpes simplex virus type 1 egress. J.Virol. 2002, 76:3471-3481.
53. Wasylnka J.A., Bakowski M.A., Szeto J., Ohlson M.B., Trimble W.S., Miller S.I., Brumell J.H. Role for myosin II in regulating positioning of Salmonella-containing vacuoles and intracellular replication. Infect. Immun. 2008, 76:2722-2735.
54. Xing J., Birukova A.A. ANP attenuates inflammatory signaling and Rho pathway of lung endothelial permeability induced by LPS and TNFalpha. Microvasc. Res. 2010, 79:56-62.
55. Yuhan R., Koutsouris A., Savkovic S.D., Hecht G. Enteropathogenic Escherichia coli-induced myosin light chain phosphorylation alters intestinal epithelial permeability. Gastroenterology 1997, 113:1873-1882.