Role for the Src family kinase Fyn in sphingolipid acquisition by chlamydiae

Infection and Immunity

Volumn 79, Issue 11, 2011, Pages 4559-4568

  Mital, Jeffrey ^a   Hackstadt, Ted ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE FYN; SMALL INTERFERING RNA; SPHINGOMYELIN;

ARTICLE; CELL INCLUSION; CELL LEVEL; CHLAMYDIA TRACHOMATIS; CHLAMYDOPHILA; CHLAMYDOPHILA CAVIAE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SCREENING;

BIOLOGICAL TRANSPORT; CHLAMYDIA TRACHOMATIS; CHLAMYDOPHILA; GENE SILENCING; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPID METABOLISM; PROTO-ONCOGENE PROTEINS C-FYN; RNA, SMALL INTERFERING; SPHINGOMYELINS;

EID: 80855134661     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05692-11     Document Type: Article

References (66)

1. Andreev, J., et al. 1999. Identification of a new Pyk2 target protein with Arf-GAP activity. Mol. Cell. Biol. 19:2338-2350.
2. Baba, A., et al. 2009. Fyn tyrosine kinase regulates the surface expression of glycosylphosphatidylinositol-linked ephrin via the modulation of sphingomyelin metabolism. J. Biol. Chem. 284:9206-9214.
3. Bache, K. G., C. Raiborg, A. Mehlum, and H. Stenmark. 2003. STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278:12513-12521.
4. 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.
5. 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.
6. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
7. Bokoch, G. M., et al. 1998. A GTPase-independent mechanism of p21-activated kinase activation. Regulation by sphingosine and other biologically active lipids. J. Biol. Chem. 273:8137-8144.
8. Boleti, H., A. Benmerah, D. M. Ojcius, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Chlamydia infection of epithelial cells expressing dynamin and Eps15 mutants: clathrin-independent entry into cells and dynamin-dependent productive growth. J. Cell Sci. 112:1487-1496.
9. Brumell, J. H., and M. A. Scidmore. 2007. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 71:636-652.
10. 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.
11. Capmany, A., and M. T. Damiani. 2010. Chlamydia trachomatis intercepts Golgi-derived sphingolipids through a Rab14-mediated transport required for bacterial development and replication. PLoS One 5:e14084.
12. 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.
13. Cocchiaro, J., Y. Kumar, E. R. Fischer, T. Hackstadt, and R. H. Valdivia. 2008. Cytoplasmic lipid droplets are translocatedd into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc. Natl. Acad. Sci. U. S. A. 105:9379-9384.
14. de Heuvel, E., et al. 1997. Identification of the major synaptojanin-binding proteins in brain. J. Biol. Chem. 272:8710-8716.
15. Derre, I., R. Swiss, and H. Agaisse. 2011. The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER-Chlamydia inclusion membrane contact sites. PLoS Pathog. 7:e1002092.
16. Elwell, C. A., A. Ceesay, J. H. Kim, D. Kalman, and J. N. Engel. 2008. RNA interference screen identifies Abl kinase and PDGFR signaling in Chlamydia trachomatis entry. PLoS Pathog. 4:e1000021.
17. Fields, K. A., and T. Hackstadt. 2002. The chlamydial inclusion: escape from the endocytic pathway. Annu. Rev. Cell Dev. Biol. 18:221-245.
18. 2+ sensor synaptotagmin VII to lysosomes. J. Cell Biol. 191:599-613.
19. Gold, E. S., et al. 2000. Amphiphysin IIm, a novel amphiphysin II isoform, is required for macrophage phagocytosis. Immunity 12:285-292.
20. Gold, E. S., et al. 2004. Amphiphysin IIm is required for survival of Chlamydia pneumoniae in macrophages. J. Exp. Med. 200:581-586.
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. Hackstadt, T., M. A. Scidmore, and D. D. Rockey. 1995. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. U. S. A. 92:4877-4881.
23. Hatch, G. M., and G. McClarty. 1998. Cardiolipin remodeling in eukaryotic cells infected with Chlamydia trachomatis is linked to elevated mitochondrial metabolism. Biochem. Biophys. Res. Commun. 243:356-360.
24. Heinzen, R. A., M. A. Scidmore, D. D. Rockey, and T. Hackstadt. 1996. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect. Immun. 64:796-809.
25. Heuer, D., et al. 2009. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457:731-735.
26. Hybiske, K., and R. S. Stephens. 2007. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl. Acad. Sci. U. S. A. 104:11430-11435.
27. Jewett, T. J., C. A. Dooley, D. J. Mead, and T. Hackstadt. 2008. Chlamydia trachomatis tarp is phosphorylated by src family tyrosine kinases. Biochem. Biophys. Res. Commun. 371:339-344.
28. Johannes, L., et al. 1996. Evidence for a functional link between Rab3 and the SNARE complex. J. Cell Sci. 109:2875-2884.
29. Kumar, Y., J. Cocchiaro, and R. H. Valdivia. 2006. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr. Biol. 16: 1646-1651.
30. Kumar, Y., and R. H. Valdivia. 2008. Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4:159-169.
31. Lipinski, A. R., et al. 2009. Rab6 and Rab11 regulate Chlamydia trachomatis development and Golgin-84-dependent Golgi fragmentation. PLoS Pathog. 5:1-12.
32. Lipsky, N. G., and R. E. Pagano. 1985. Intracellular translocation of fluorescent sphingolipids in cultured fibroblasts: endogenously synthesized sphingomyelin and glucocerebroside analogues pass through the Golgi apparatus en route to the plasma membrane. J. Cell Biol. 100:27-34.
33. Lipsky, N. G., and R. E. Pagano. 1985. A vital stain for the Golgi apparatus. Science 228:745-747.
34. Mehlitz, A., S. Banhart, S. Hess, M. Selbach, and T. F. Meyer. 2008. Complex kinase requirements for Chlamydia trachomatis Tarp phosphorylation. FEMS Microbiol. Lett. 289:233-240.
35. Mital, J., and T. Hackstadt. 2011. Diverse requirements for Src-family tyrosine kinases distinguish chlamydial species. mBio 2:e00031-11.
36. Mital, J., N. J. Miller, E. R. Fischer, and T. Hackstadt. 2010. Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network. Cell. Microbiol. 12:1235-1249.
37. Moore, E. R., E. R. Fischer, D. J. Mead, and T. Hackstadt. 2008. The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9:2130-2140.
38. Moorhead, A. M., J. Y. Jung, A. Smirnov, S. Kaufer, and M. A. Scidmore. 2010. Multiple host proteins that function in phosphatidylinositol-4-phosphate metabolism are recruited to the chlamydial inclusion. Infect. Immun. 78:1990-2007.
39. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143-190.
40. 2+-induced endocytosis by recruitment of AP2 and clathrin. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1549-G1558.
41. Ouellette, S. P., and R. A. Carabeo. 2010. A functional slow recycling pathway of transferrin is required for growth of chlamydia. Front. Microbiol. 1:112.
42. Peretti, D., N. Dahan, E. Shimoni, K. Hirschberg, and S. Lev. 2008. Coordinated lipid transfer between the endoplasmic reticulum and the Golgi complex requires the VAP proteins and is essential for Golgi-mediated transport. Mol. Biol. Cell 19:3871-3884.
43. Perin, M. S., V. A. Fried, D. K. Stone, X. S. Xie, and T. C. Sudhof. 1991. Structure of the 116-kDa polypeptide of the clathrin-coated vesicle/synaptic vesicle proton pump. J. Biol. Chem. 266:3877-3881.
44. Puri, V., et al. 2001. Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol. 154:535-547.
45. Raiborg, C., et al. 2002. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4:394-398.
46. Ramjaun, A. R., K. D. Micheva, I. Bouchelet, and P. S. McPherson. 1997. Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J. Biol. Chem. 272:16700-16706.
47. Ren, G., P. Vajjhala, J. S. Lee, B. Winsor, and A. L. Munn. 2006. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70:37-120.
48. Robertson, D. K., L. Gu, R. K. Rowe, and W. L. Beatty. 2009. Inclusion biogenesis and reactivation of persistant Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog. 5:e1000664.
49. Rockey, D. D., E. R. Fischer, and T. Hackstadt. 1996. Temporal analysis of the developing Chlamydia psittaci inclusion by use of fluorescence and electron microscopy. Infect. Immun. 64:4269-4278.
50. Rockey, D. D., M. A. Scidmore, J. P. Bannantine, and W. J. Brown. 2002. Proteins in the chlamydial inclusion membrane. Microbes Infect. 4:333-340.
51. Rzomp, K. A., L. D. Scholtes, B. J. Briggs, G. R. Whittaker, and M. A. Scidmore. 2003. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect. Immun. 71: 5855-5870.
52. Schachter, J. 1999. Infection and disease epidemiology, p. 139-169. In R. S. Stephens (ed.), Chlamydia: intracellular biology, pathogenesis, and immunity. ASM Press, Washington, DC.
53. Scidmore, M. A., D. D. Rockey, E. R. Fischer, R. A. Heinzen, and T. Hackstadt. 1996. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect. Immun. 64:5366-5372.
54. Shivshankar, P., L. Lei, J. Wang, and G. Zhong. 2008. Rottlerin inhibits chlamydial intracellular growth and blocks chlamydial acquisition of sphingolipids from host cells. Appl. Environ. Microbiol. 74:1243-1249.
55. Soltoff, S. P. 2007. Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta. Trends Pharmacol. Sci. 28:453-458.
56. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513-525.
57. 2+-regulated exocytosis and SNARE function. Trends Endocrinol. Metab. 16:81-83.
58. Su, H., et al. 2004. Activation of RAf/MEK/ERK/cPLA2 signaling pathway is essential for chlamydial acquisition of host glycerophospholipids. J. Biol. Chem. 279:9409-9416.
59. Takei, K., V. I. Slepnev, V. Haucke, and P. De Camilli. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33-39.
60. Thalmann, J., et al. 2010. Actin re-organization induced by Chlamydia trachomatis serovar D-evidence for a critical role of the effector protein CT166 targeting Rac. PLoS One 5:e9887.
61. Vadlamudi, R. K., et al. 2004. Dynein light chain 1, a p21-activated kinase 1-interacting substrate, promotes cancerous phenotypes. Cancer Cell 5:575-585.
62. van Ooij, C., et al. 2000. Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis. Cell. Microbiol. 2:627-637.
63. Verbeke, P., et al. 2006. Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog. 2:e45.
64. Weller, S. G., et al. 2010. Src kinase regulates the integrity and function of the Golgi apparatus via activation of dynamin 2. Proc. Natl. Acad. Sci. U. S. A. 107:5863-5868.
65. Wolf, K., and T. Hackstadt. 2001. Sphingomyelin trafficking in Chlamydia pneumoniae-infected cells. Cell. Microbiol. 3:145-152.
66. Wubbolts, R., et al. 1999. Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J. Cell Sci. 112(Pt. 6):785-795.