Dynamin-mediated lipid acquisition is essential for Chlamydia trachomatis development

Molecular Microbiology

Volumn 94, Issue 1, 2014, Pages 186-201

  Gurumurthy, Rajendra Kumar ^a   Chumduri, Cindrilla ^a   Karlas, Alexander ^a   Kimmig, Sonja ^a   Gonzalez, Erik ^a   Machuy, Nikolaus ^a   Rudel, Thomas ^b   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; LENTIVIRUS VECTOR; LIPID; SHORT HAIRPIN RNA; DNM2 PROTEIN, HUMAN; DYNAMIN I;

ARTICLE; BACTERIAL GROWTH; BACTERIAL REPRODUCTION; BACTERIAL SURVIVAL; CELL CYCLE PHASE; CELL INCLUSION; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; GOLGI COMPLEX; HEK293 CELL LINE; HELA CELL LINE; HOST CELL; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR BACTERIUM; LIPID TRANSPORT; MITOSIS; NONHUMAN; PRIORITY JOURNAL; CHLAMYDIASIS; CYTOLOGY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; MICROBIOLOGY;

CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; DYNAMIN I; DYNAMINS; GOLGI APPARATUS; HUMANS; LIPID METABOLISM;

EID: 84907853391     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12751     Document Type: Article

References (41)

1. 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.
2. Beatty, W.L. (2008) Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 76: 2872-2881.
3. Boleti, H., Benmerah, A., Ojcius, D.M., Cerf-Bensussan, N., and Dautry-Varsat, A. (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 (Part 10): 1487-1496.
4. Brunham, R.C., and Rey-Ladino, J. (2005) Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol 5: 149-161.
5. Carabeo, R.A., Mead, D.J., and Hackstadt, T. (2003) Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci USA 100: 6771-6776.
6. Chen, A.L., Johnson, K.A., Lee, J.K., Sutterlin, C., and Tan, M. (2012) CPAF: a Chlamydial protease in search of an authentic substrate. PLoS Pathog 8: e1002842.
7. Christian, J.G., Heymann, J., Paschen, S.A., Vier, J., Schauenburg, L., Rupp, J., etal. (2011) Targeting of a chlamydial protease impedes intracellular bacterial growth. PLoS Pathog 7: e1002283.
8. Cocchiaro, J.L., Kumar, Y., Fischer, E.R., Hackstadt, T., and Valdivia, R.H. (2008) Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci USA 105: 9379-9384.
9. Colanzi, A., and Corda, D. (2007) Mitosis controls the Golgi and the Golgi controls mitosis. Curr Opin Cell Biol 19: 386-393.
10. Colanzi, A., Suetterlin, C., and Malhotra, V. (2003) Cell-cycle-specific Golgi fragmentation: how and why? Curr Opin Cell Biol 15: 462-467.
11. De Matteis, M.A., and Luini, A. (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9: 273-284.
12. Derre, I., Pypaert, M., Dautry-Varsat, A., and Agaisse, H. (2007) RNAi screen in Drosophila cells reveals the involvement of the Tom complex in Chlamydia infection. PLoS Pathog 3: 1446-1458.
13. Dietmaier, W., Fabry, S., and Schmitt, R. (1993) DISEC-TRISEC: di- and trinucleotide-sticky-end cloning of PCR-amplified DNA. Nucleic Acids Res 21: 3603-3604.
14. Elwell, C.A., Ceesay, A., Kim, J.H., Kalman, D., and Engel, J.N. (2008) RNA interference screen identifies Abl kinase and PDGFR signaling in Chlamydia trachomatis entry. PLoS Pathog 4: e1000021.
15. Gold, E.S., Underhill, D.M., Morrissette, N.S., Guo, J., McNiven, M.A., and Aderem, A. (1999) Dynamin 2 is required for phagocytosis in macrophages. J Exp Med 190: 1849-1856.
16. Gurumurthy, R.K., Maurer, A.P., Machuy, N., Hess, S., Pleissner, K.P., Schuchhardt, J., etal. (2010) A loss-of-function screen reveals Ras- and Raf-independent MEK-ERK signaling during Chlamydia trachomatis infection. Sci Signal 3: ra21.
17. Gussmann, J., Al-Younes, H.M., Braun, P.R., Brinkmann, V., and Meyer, T.F. (2008) Long-term effects of natural amino acids on infection with Chlamydia trachomatis. Microb Pathog 44: 438-447.
18. Hackstadt, T., Scidmore, M.A., and Rockey, D.D. (1995) Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc Natl Acad Sci USA 92: 4877-4881.
19. Hackstadt, T., Rockey, D.D., Heinzen, R.A., and Scidmore, M.A. (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.
20. Henley, J.R., Krueger, E.W., Oswald, B.J., and McNiven, M.A. (1998) Dynamin-mediated internalization of caveolae. J Cell Biol 141: 85-99.
21. Heuer, D., Rejman Lipinski, A., Machuy, N., Karlas, A., Wehrens, A., Siedler, F., etal. (2009) Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457: 731-735.
22. Hybiske, K., and Stephens, R.S. (2007) Mechanisms of Chlamydia trachomatis entry into nonphagocytic cells. Infect Immun 75: 3925-3934.
23. Jain, A., Shroff, S.G., Janicki, J.S., Reddy, H.K., and Weber, K.T. (1991) Relation between mixed venous oxygen saturation and cardiac index. Nonlinearity and normalization for oxygen uptake and hemoglobin. Chest 99: 1403-1409.
24. Jones, S.M., Howell, K.E., Henley, J.R., Cao, H., and McNiven, M.A. (1998) Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279: 573-577.
25. Kumar, Y., Cocchiaro, J., and Valdivia, R.H. (2006) The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr Biol 16: 1646-1651.
26. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., and Kirchhausen, T. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850.
27. McNiven, M.A., and Thompson, H.M. (2006) Vesicle formation at the plasma membrane and trans-Golgi network: the same but different. Science 313: 1591-1594.
28. McNiven, M.A., Cao, H., Pitts, K.R., and Yoon, Y. (2000) The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem Sci 25: 115-120.
29. Malo, N., Hanley, J.A., Cerquozzi, S., Pelletier, J., and Nadon, R. (2006) Statistical practice in high-throughput screening data analysis. Nat Biotechnol 24: 167-175.
30. Moulder, J.W. (1991) Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55: 143-190.
31. Naldini, L., Blomer, U., Gage, F.H., Trono, D., and Verma, I.M. (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci USA 93: 11382-11388.
32. Nishi, T., and Forgac, M. (2002) The vacuolar (H+)-ATPases - nature's most versatile proton pumps. Nat Rev Mol Cell Biol 3: 94-103.
33. Oh, P., McIntosh, D.P., and Schnitzer, J.E. (1998) Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141: 101-114.
34. Rejman Lipinski, A., Heymann, J., Meissner, C., Karlas, A., Brinkmann, V., Meyer, T.F., and Heuer, D. (2009) Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation. PLoS Pathog 5: e1000615.
35. Robertson, D.K., Gu, L., Rowe, R.K., and Beatty, W.L. (2009) Inclusion biogenesis and reactivation of persistent Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog 5: e1000664.
36. Sandvig, K., and van Deurs, B. (1994) Endocytosis without clathrin. Trends Cell Biol 4: 275-277.
37. Weller, S.G., Capitani, M., Cao, H., Micaroni, M., Luini, A., Sallese, M., and McNiven, M.A. (2010) Src kinase regulates the integrity and function of the Golgi apparatus via activation of dynamin 2. Proc Natl Acad Sci USA 107: 5863-5868.
38. Wiedemann, N., Frazier, A.E., and Pfanner, N. (2004) The protein import machinery of mitochondria. J Biol Chem 279: 14473-14476.
39. Wiznerowicz, M., and Trono, D. (2003) Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 77: 8957-8961.
40. Wright, H.R., Turner, A., and Taylor, H.R. (2008) Trachoma. Lancet 371: 1945-1954.
41. Zufferey, R., Nagy, D., Mandel, R.J., Naldini, L., and Trono, D. (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15: 871-875.