Golgi fragmentation and sphingomyelin transport to Chlamydia trachomatis during penicillin-induced persistence do not depend on the cytosolic presence of the chlamydial protease CPAF

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Dille, Stephanie ^a   Herbst, Katharina ^a   Volceanov, Larisa ^a   Nölke, Thilo ^b   Kretz, Oliver ^b   Häcker, Georg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CERAMIDE; CPAF PROTEIN; PENG; PENICILLIN G; SPHINGOMYELIN; UNCLASSIFIED DRUG; PENICILLIN DERIVATIVE; PROTEINASE;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CELLULAR PARAMETERS; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; CYTOSOL; EMBRYO; ENZYME LOCALIZATION; ENZYME RELEASE; EXPERIMENTAL INFECTION; FIBROBLAST; FLUORESCENCE; GOLGI COMPLEX; GOLGI FRAGMENTATION; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IN VITRO STUDY; MOUSE; NONHUMAN; OVIDUCT; PERSISTENT INFECTION; PHOSPHOLIPID TRANSFER; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; CELL CULTURE; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL LINE; CELLS, CULTURED; CERAMIDES; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; ENDOPEPTIDASES; GOLGI APPARATUS; HELA CELLS; HUMANS; MICE; PENICILLINS; SPHINGOMYELINS;

EID: 84904906405     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103220     Document Type: Article

References (42)

1. Gerbase AC, Rowley JT, Mertens TE (1998) Global epidemiology of sexually transmitted diseases. Lancet 351 Suppl 3: 2-4. (Pubitemid 128643727)
2. Belland R, Ojcius DM, Byrne GI (2004) Chlamydia. Nat Rev Microbiol 2: 530-531.
3. Haider S, Wagner M, Schmid MC, Sixt BS, Christian JG, et al. (2010) Raman microspectroscopy reveals long-term extracellular activity of Chlamydiae. Mol Microbiol 77: 687-700.
4. Wylie JL, Hatch GM, McClarty G (1997) Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J Bacteriol 179: 7233-7242. (Pubitemid 27509958)
5. Hatch GM, McClarty G (1998) Phospholipid composition of purified Chlamydia trachomatis mimics that of the eucaryotic host cell. Infect Immun 66: 3727-3735. (Pubitemid 28347830)
6. 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. (Pubitemid 36666655)
7. van Ooij C, Kalman L, van I, Nishijima M, Hanada K, et al. (2000) Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis. Cell Microbiol 2: 627-637.
8. 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.
9. Elwell CA, Engel JN (2012) Lipid acquisition by intracellular Chlamydiae. Cell Microbiol 14: 1010-1018.
10. Scidmore MA, Fischer ER, Hackstadt T (1996) Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J Cell Biol 134: 363-374. (Pubitemid 26250705)
11. 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. (Pubitemid 26077824)
12. Heuer D, Lipinski AR, Machuy N, Karlas A, Wehrens A, et al. (2009) Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457: 731-735.
13. 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.
14. Snavely EA, Kokes M, Dunn JD, Saka HA, Nguyen BD, et al. (2014) Reassessing the role of the secreted protease CPAF in Chlamydia trachomatis infection through genetic approaches. Pathog Dis.
15. Christian JG, Heymann J, Paschen SA, Vier J, Schauenburg L, et al. (2011) Targeting of a chlamydial protease impedes intracellular bacterial growth. PLoS Pathog 7: e1002283.
16. Zhong G (2009) Killing me softly: chlamydial use of proteolysis for evading host defenses. Trends Microbiol 17: 467-474.
17. Wyrick PB (2010) Chlamydia trachomatis persistence in vitro: an overview. J Infect Dis 201 Suppl 2: S88-95.
18. Beatty WL, Morrison RP, Byrne GI (1994) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58: 686-699.
19. Weber A, Kirejczyk Z, Potthoff S, Ploner C, Hacker G (2009) Endogenous Noxa Determines the Strong Proapoptotic Synergism of the BH3-Mimetic ABT-737 with Chemotherapeutic Agents in Human Melanoma Cells. Transl Oncol 2: 73-83.
20. Johnson RM (2004) Murine oviduct epithelial cell cytokine responses to Chlamydia muridarum infection include interleukin-12-p70 secretion. Infect Immun 72: 3951-3960.
21. Skilton RJ, Cutcliffen LT, Barlow D, Wang Y, Salim O, et al. (2009) Penicillin induced persistence in Chlamydia trachomatis: high quality time lapse video analysis of the developmental cycle. PLoS One 4: e7723.
22. Christian J, Vier J, Paschen SA, Hacker G (2010) Cleavage of the NF-{kappa}B 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.
23. Watzele G, Berger EG (1990) Near identity of HeLa cell galactosyltransferase with the human placental enzyme. Nucleic Acids Res 18: 7174.
24. Lisauskas T, Matula P, Claas C, Reusing S, Wiemann S, et al. (2012) Live-cell assays to identify regulators of ER-to-Golgi trafficking. Traffic 13: 416-432.
25. Derre I, Swiss R, Agaisse H (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.
26. Elwell CA, Jiang S, Kim JH, Lee A, Wittmann T, et al. (2011) Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog 7: e1002198.
27. Chen D, Lei L, Lu C, Flores R, DeLisa MP, et al. (2010) Secretion of the chlamydial virulence factor CPAF requires the Sec-dependent pathway. Microbiology 156: 3031-3040.
28. Heuer D, Brinkmann V, Meyer TF, Szczepek AJ (2003) Expression and translocation of chlamydial protease during acute and persistent infection of the epithelial HEp-2 cells with Chlamydophila (Chlamydia) pneumoniae. Cell Microbiol 5: 315-322. (Pubitemid 37009909)
29. Wang J, Frohlich KM, Buckner L, Quayle AJ, Luo M, et al. (2011) Altered protein secretion of Chlamydia trachomatis in persistently infected human endocervical epithelial cells. Microbiology 157: 2759-2771.
30. Nguyen BD, Valdivia RH (2012) Virulence determinants in the obligate intracellular pathogen Chlamydia trachomatis revealed by forward genetic approaches. Proc Natl Acad Sci U S A 109: 1263-1268.
31. Lucocq JM, Warren G (1987) Fragmentation and partitioning of the Golgi apparatus during mitosis in HeLa cells. EMBO J 6: 3239-3246.
32. Acharya U, Mallabiabarrena A, Acharya JK, Malhotra V (1998) Signaling via mitogen-activated protein kinase kinase (MEK1) is required for Golgi fragmentation during mitosis. Cell 92: 183-192. (Pubitemid 28073042)
33. Welch WJ, Suhan JP (1985) Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol 101: 1198-1211. (Pubitemid 16203736)
34. Lee JE, Patel K, Almodovar S, Tuder RM, Flores SC, et al. (2011) Dependence of Golgi apparatus integrity on nitric oxide in vascular cells: implications in pulmonary arterial hypertension. Am J Physiol Heart Circ Physiol 300: H1141-1158.
35. Gonatas NK, Stieber A, Gonatas JO (2006) Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci 246: 21-30. (Pubitemid 43815336)
36. Diao A, Rahman D, Pappin DJ, Lucocq J, Lowe M (2003) The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J Cell Biol 160: 201-212. (Pubitemid 36254954)
37. Echeverry N, Bachmann D, Ke F, Strasser A, Simon HU, et al. (2013) Intracellular localization of the BCL-2 family member BOK and functional implications. Cell Death Differ 20: 785-799.
38. Zhou Z, Mogensen MM, Powell PP, Curry S, Wileman T (2013) Foot-and-mouth disease virus 3C protease induces fragmentation of the Golgi compartment and blocks intra-Golgi transport. J Virol 87: 11721-11729.
39. Machner MP, Isberg RR (2006) Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 11: 47-56. (Pubitemid 43960806)
40. Mounier J, Boncompain G, Senerovic L, Lagache T, Chretien F, et al. (2012) Shigella effector IpaB-induced cholesterol relocation disrupts the Golgi complex and recycling network to inhibit host cell secretion. Cell Host Microbe 12: 381-389.
41. Romano JD, Sonda S, Bergbower E, Smith ME, Coppens I (2013) Toxoplasma gondii salvages sphingolipids from the host Golgi through the rerouting of selected Rab vesicles to the parasitophorous vacuole. Mol Biol Cell 24: 1974-1995.
42. Dumoux M, Le Gall SM, Habbeddine M, Delarbre C, Hayward RD, et al. (2013) Penicillin kills Chlamydia following the fusion of bacteria with lysosomes and prevents genital inflammatory lesions in C. muridarum-infected mice. PLoS One 8: e83511.