Flotillin-1 (reggie-2) contributes to Chlamydia pneumoniae growth and is associated with bacterial inclusion

Infection and Immunity

Volumn 80, Issue 3, 2012, Pages 1072-1078

  Korhonen, Juha T ^a,b   Puolakkainen, Mirja ^c   Häivälä, Reetta ^c   Penttilä, Tuula ^d   Haveri, Anu ^d   Markkula, Eveliina ^c   Lahesmaa, Riitta ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b Drug Discovery Graduate School   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

FLOTILLIN 1;

ARTICLE; BACTERIAL CELL; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIUM ADHERENCE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CHLAMYDOPHILA PNEUMONIAE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE;

BACTERIAL LOAD; BACTERIAL PROTEINS; CELL LINE; CHLAMYDOPHILA PNEUMONIAE; ENDOCYTOSIS; EPITHELIAL CELLS; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; INCLUSION BODIES; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; PHOSPHOPROTEINS; RNA INTERFERENCE;

EID: 84857663223     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05528-11     Document Type: Article

References (61)

1. Airaksinen U, et al. 2003. Production of Chlamydia pneumoniae proteins in Bacillus subtilis and their use in characterizing immune responses in the experimental infection model. Clin. Diagn. Lab. Immunol. 10:367-375.
2. Ait-Slimane T, Galmes R, Trugnan G, Maurice M. 2009. Basolateral internalization of GPI-anchored proteins occurs via a clathrinindependent flotillin-dependent pathway in polarized hepatic cells. Mol. Biol. Cell 20:3792-3800.
3. Babuke T, et al. 2009. Hetero-oligomerization of reggie-1/flotillin-2 and reggie-2/flotillin-1 is required for their endocytosis. Cell. Signal. 21:1287-1297.
4. Babuke T, Tikkanen R. 2007. Dissecting the molecular function of reggie/ flotillin proteins. Eur. J. Cell Biol. 86:525-532.
5. Beatty WL. 2006. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J. Cell Sci. 119:350-359.
6. Beatty WL. 2008. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect. Immun. 76:2872-2881.
7. Bickel PE, et al. 1997. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272:13793-13802.
8. Bobryshev YV, Killingsworth MC, Tran D, Lord R. 2008. Amalgamation of Chlamydia pneumoniae inclusions with lipid droplets in foam cells in human atherosclerotic plaque. Virchows Arch. 453:69-77.
9. Browman DT, Hoegg MB, Robbins SM. 2007. The SPFH domaincontaining proteins: more than lipid raft markers. Trends Cell Biol. 17:394-402.
10. Browman DT, Resek ME, Zajchowski LD, Robbins SM. 2006. Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER. J. Cell Sci. 119:3149-3160.
11. Caldwell HD, Kromhout J, Schachter J. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31:1161-1176.
12. Campbell LA, Kuo CC. 2004. Chlamydia pneumoniae-an infectious risk factor for atherosclerosis? Nat. Rev. Microbiol. 2:23-32.
13. Carabeo RA, Mead DJ, Hackstadt T. 2003. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc. Natl. Acad. Sci. U. S. A. 100:6771-6776.
14. Chu HG, Weeks SK, Gilligan DM, Rockey DD. 2008. Host alphaadducin is redistributed and localized to the inclusion membrane in chlamydia-and chlamydophila-infected cells. Microbiology 154:3848-3855.
15. Cles LD, Stamm WE. 1990. Use of HL cells for improved isolation and passage of Chlamydia pneumoniae. J. Clin. Microbiol. 28:938-940.
16. Cocchiaro JL, Kumar Y, Fischer ER, Hackstadt T, Valdivia RH. 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.
17. Dermine JF, et al. 2001. Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J. Biol. Chem. 276:18507-18512.
18. Ekman MR, et al. 1993. An epidemic of infections due to Chlamydia pneumoniae in military conscripts. Clin. Infect. Dis. 17:420-425.
19. Fields KA, Hackstadt T. 2000. Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol. Microbiol. 38:1048-1060.
20. Fields KA, Hackstadt T. 2002. The chlamydial inclusion: escape from the endocytic pathway. Annu. Rev. Cell Dev. Biol. 18:221-245.
21. Frick M, et al. 2007. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr. Biol. 17:1151-1156.
22. Glebov OO, Bright NA, Nichols BJ. 2006. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat. Cell Biol. 8:46-54.
23. Hackstadt T, Rockey DD, Heinzen RA, Scidmore MA. 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.
24. Hackstadt T, Scidmore MA, Rockey DD. 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.
25. Hackstadt T, Scidmore-Carlson MA, Shaw EI, Fischer ER. 1999. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell. Microbiol. 1:119-130.
26. Hasegawa A, Sogo LF, Tan M, Sutterlin C. 2009. Host complement regulatory protein CD59 is transported to the chlamydial inclusion by a Golgi apparatus-independent pathway. Infect. Immun. 77:1285-1292.
27. Howe D, Heinzen RA. 2006. Coxiella burnetii inhabits a cholesterol-rich vacuole and influences cellular cholesterol metabolism. Cell. Microbiol. 8:496-507.
28. Kokubo H, et al. 2003. Ultrastructural localization of flotillin-1 to cholesterol-rich membrane microdomains, rafts, in rat brain tissue. Brain Res. 965:83-90.
29. Kumar Y, Cocchiaro J, Valdivia RH. 2006. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr. Biol. 16:1646-1651.
30. Kuo CC, Grayston JT. 1990. A sensitive cell line, HL cells, for isolation and propagation of Chlamydia pneumoniae strain TWAR. J. Infect. Dis. 162:755-758.
31. Kuo CC, Jackson LA, Campbell LA, Grayston JT. 1995. Chlamydia pneumoniae (TWAR). Clin. Microbiol. Rev. 8:451-461.
32. Langhorst MF, Reuter A, Stuermer CA. 2005. Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell. Mol. Life Sci. 62:2228-2240.
33. Langui D, et al. 2004. Subcellular topography of neuronal Abeta peptide in APPxPS1 transgenic mice. Am. J. Pathol. 165:1465-1477.
34. Lee BY, et al. 2010. The Mycobacterium bovis bacille Calmette-Guerin phagosome proteome. Mol. Cell. Proteomics 9:32-53.
35. Lichtenberg D, Goni FM, Heerklotz H. 2005. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 30:430-436.
36. Liu J, Deyoung SM, Zhang M, Dold LH, Saltiel AR. 2005. The stomatin/ prohibitin/flotillin/HflK/C domain of flotillin-1 contains distinct sequences that direct plasma membrane localization and protein interactions in 3T3-L1 adipocytes. J. Biol. Chem. 280:16125-16134.
37. Liu P, et al. 2004. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279:3787-3792.
38. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
39. Ludwig A, et al. 2010. Flotillin microdomains interact with the cortical cytoskeleton to control uropod formation and neutrophil recruitment. J. Cell Biol. 191:771-781.
40. Mannonen L, Kamping E, Penttila T, Puolakkainen M. 2004. IFNgamma induced persistent Chlamydia pneumoniae infection in HL and Mono Mac 6 cells: characterization by real-time quantitative PCR and culture. Microb. Pathog. 36:41-50.
41. Mital J, Miller NJ, Fischer ER, Hackstadt T. 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.
42. Moore ER, Mead DJ, Dooley CA, Sager J, Hackstadt T. 2011. The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157:830-838.
43. Moorhead AM, Jung JY, Smirnov A, Kaufer S, Scidmore MA. 2010. Multiple host proteins that function in phosphatidylinositol-4-phosphate metabolism are recruited to the chlamydial inclusion. Infect. Immun. 78:1990-2007.
44. Mori S, et al. 2003. PACSIN3 binds ADAM12/meltrin alpha and upregulates ectodomain shedding of heparin-binding epidermal growth factor-like growth factor. J. Biol. Chem. 278:46029-46034.
45. Morrow IC, Parton RG. 2005. Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6:725-740.
46. Murphy SC, et al. 2004. Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood 103:1920-1928.
47. O'Connell CM, Ionova IA, Quayle AJ, Visintin A, Ingalls RR. 2006. Localization of TLR2 and MyD88 to Chlamydia trachomatis inclusions. Evidence for signaling by intracellular TLR2 during infection with an obligate intracellular pathogen. J. Biol. Chem. 281:1652-1659.
48. Rajendran L, Le Lay S, Illges H. 2007. Raft association and lipid droplet targeting of flotillins are independent of caveolin. Biol. Chem. 388:307-314.
49. Riento K, Frick M, Schafer I, Nichols BJ. 2009. Endocytosis of flotillin-1 and flotillin-2 is regulated by Fyn kinase. J. Cell Sci. 122:912-918.
50. Robertson DK, Gu L, Rowe RK, Beatty WL. 2009. Inclusion biogenesis and reactivation of persistent Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog. 5:e1000664.
51. Rzomp KA, Scholtes LD, Briggs BJ, Whittaker GR, Scidmore MA. 2003. Rab GTPases are recruited to chlamydial inclusions in both a speciesdependent and species-independent manner. Infect. Immun. 71:5855-5870.
52. Santamaria A, et al. 2005. PTOV1 enables the nuclear translocation and mitogenic activity of flotillin-1, a major protein of lipid rafts. Mol. Cell. Biol. 25:1900-1911.
53. Scidmore MA, Fischer ER, Hackstadt T. 2003. Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect. Immun. 71:973-984.
54. Scidmore MA, Hackstadt T. 2001. Mammalian 14-3-3beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol. Microbiol. 39:1638-1650.
55. Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569-572.
56. Simons K, Ikonen E. 2000. How cells handle cholesterol. Science 290:1721-1726.
57. Solis GP, et al. 2007. Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains. Biochem. J. 403:313-322.
58. Stuermer CA. 2011. Reggie/flotillin and the targeted delivery of cargo. J. Neurochem. 116:708-713.
59. Stuermer CA, et al. 2001. Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and-2. Mol. Biol. Cell 12:3031-3045.
60. Subtil A, Parsot C, Dautry-Varsat A. 2001. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol. Microbiol. 39:792-800.
61. Vassilieva EV, Ivanov AI, Nusrat A. 2009. Flotillin-1 stabilizes caveolin-1 in intestinal epithelial cells. Biochem. Biophys. Res. Commun. 379:460-465.