Acquisition of nutrients by Chlamydiae: unique challenges of living in an intracellular compartment

Current Opinion in Microbiology

Volumn 13, Issue 1, 2010, Pages 4-10

  Saka, Hector Alex ^a   Valdivia, Raphael H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAB PROTEIN; SNARE PROTEIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELL VACUOLE; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDOPHILA PNEUMONIAE; CYTOPLASM; EUKARYOTIC CELL; GOLGI COMPLEX; HOST PATHOGEN INTERACTION; MEMBRANE VESICLE; NONHUMAN; NUTRIENT; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

CHLAMYDIA; CHLAMYDIA INFECTIONS; EUKARYOTIC CELLS; HUMANS; VACUOLES;

CHLAMYDIAE; EUKARYOTA;

EID: 75249089782     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2009.11.002     Document Type: Article

References (72)

1. Horn M., Collingro A., Schmitz-Esser S., Beier C.L., Purkhold U., Fartmann B., Brandt P., Nyakatura G.J., Droege M., Frishman D., et al. Illuminating the evolutionary history of chlamydiae. Science 304 (2004) 728-730
2. Bebear C., and de Barbeyrac B. Genital Chlamydia trachomatis infections. Clin Microbiol Infect 15 (2009) 4-10
3. Blasi F., Tarsia P., and Aliberti S. Chlamydophila pneumoniae. Clin Microbiol Infect 15 (2009) 29-35
4. Beeckman D.S., and Vanrompay D.C. Zoonotic Chlamydophila psittaci infections from a clinical perspective. Clin Microbiol Infect 15 (2009) 11-17
5. Stephens R.S., Myers G., Eppinger M., and Bavoil P.M. Divergence without difference: phylogenetics and taxonomy of Chlamydia resolved. FEMS Immunol Med Microbiol 55 (2009) 115-119
6. Schachter J. Chlamydia: intracellular biology, pathogenesis and immunity. In: Stephens R.S. (Ed). Infection and Disease Epidemiology. (1999), A.S.M. 139-169
7. Valdivia R.H. Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr Opin Microbiol 11 (2008) 53-59
8. Kalman S., Mitchell W., Marathe R., Lammel C., Fan J., Hyman R.W., Olinger L., Grimwood J., Davis R.W., and Stephens R.S. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat Genet 21 (1999) 385-389
9. Moran N.A. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108 (2002) 583-586
10. Stephens R.S., Kalman S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R.L., Zhao Q., et al. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282 (1998) 754-759
11. Read T.D., Myers G.S., Brunham R.C., Nelson W.C., Paulsen I.T., Heidelberg J., Holtzapple E., Khouri H., Federova N.B., Carty H.A., et al. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res 31 (2003) 2134-2147
12. Read T.D., Brunham R.C., Shen C., Gill S.R., Heidelberg J.F., White O., Hickey E.K., Peterson J., Utterback T., Berry K., et al. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 28 (2000) 1397-1406
13. Moulder J.W. Interaction of Chlamydiae and host cells in vitro. Microbiol Rev 55 (1991) 143-190
14. McClarty G., and Fan H. Purine metabolism by intracellular Chlamydia psittaci. J Bacteriol 175 (1993) 4662-4669
15. McClarty G., and Qin B. Pyrimidine metabolism by intracellular Chlamydia psittaci. J Bacteriol 175 (1993) 4652-4661
16. McClarty G. Chlamydiae and the biochemistry of intracellular parasitism. Trends Microbiol 2 (1994) 157-164
17. Wylie J.L., Hatch G.M., and McClarty G. Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J Bacteriol 179 (1997) 7233-7242
18. Cocchiaro J.L., and Valdivia R.H. New insights into Chlamydia intracellular survival mechanisms. Cell Microbiol 11 (2009) 1571-1578
19. Zalkin H., and Nygaard P. Biosynthesis of purine nucleotides. In: Neidhardt F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella: Cellular and Molecular Biology. edn 2 (1996), A.S.M. 561-579
20. Neuhard J., and Kelln R.A. Biosynthesis and conversion of pyrimidines. In: Neidhardt F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella: Cellular and Molecular Biology. edn 2 (1996), A.S.M. 580-599
21. Tipples G., and McClarty G. The obligate intracellular bacterium Chlamydia trachomatis is auxotrophic for three of the four ribonucleoside triphosphates. Mol Microbiol 8 (1993) 1105-1114
22. Wylie J.L., Berry J.D., and McClarty G. Chlamydia trachomatis CTP synthetase: molecular characterization and developmental regulation of expression. Mol Microbiol 22 (1996) 631-642
23. + transporter in an intracellular bacterial symbiont related to Chlamydiae. Nature 432 (2004) 622-625
24. Linka N., Hurka H., Lang B.F., Burger G., Winkler H.H., Stamme C., Urbany C., Seil I., Kusch J., and Neuhaus H.E. Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306 (2003) 27-35
25. Winkler H.H., and Neuhaus H.E. Non-mitochondrial ATP transport. Trends Biochem Sci 24 (1999) 64-68
26. Tjaden J., Winkler H.H., Schwoppe C., Van der Laan M., Mohlmann T., and Neuhaus H.E. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J Bacteriol 181 (1999) 1196-1202
27. Trentmann O., Horn M., van Scheltinga A.C., Neuhaus H.E., and Haferkamp I. Enlightening energy parasitism by analysis of an ATP/ADP transporter from chlamydiae. PLoS Biol 5 (2007) e231. In this study, a detailed biochemical analysis of an ATP/ADP transporter (PamNTT1), from Protochlamydia amoebophila (UWE25) was performed. This paper contains the first successful purification and functional reconstitution of a bacterial nucleotide transporter and provides the functional basis of how an obligate intracellular parasite exploits the energy pool of its host cell.
28. Schmitz-Esser S., Linka N., Collingro A., Beier C.L., Neuhaus H.E., Wagner M., and Horn M. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J Bacteriol 186 (2004) 683-691
29. Haferkamp I., Schmitz-Esser S., Wagner M., Neigel N., Horn M., and Neuhaus H.E. Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol Microbiol 60 (2006) 1534-1545
30. Heizer Jr. E.M., Raiford D.W., Raymer M.L., Doom T.E., Miller R.V., and Krane D.E. Amino acid cost and codon-usage biases in 6 prokaryotic genomes: a whole-genome analysis. Mol Biol Evol 23 (2006) 1670-1680
31. Braun P.R., Al-Younes H., Gussmann J., Klein J., Schneider E., and Meyer T.F. Competitive inhibition of amino acid uptake suppresses chlamydial growth: involvement of the chlamydial amino acid transporter BrnQ. J Bacteriol 190 (2008) 1822-1830
32. Rottenberg M.E., Gigliotti-Rothfuchs A., and Wigzell H. The role of IFN-gamma in the outcome of chlamydial infection. Curr Opin Immunol 14 (2002) 444-451
33. Fehlner-Gardiner C., Roshick C., Carlson J.H., Hughes S., Belland R.J., Caldwell H.D., and McClarty G. Molecular basis defining human Chlamydia trachomatis tissue tropism. A possible role for tryptophan synthase. J Biol Chem 277 (2002) 26893-26903
34. McClarty G., Caldwell H.D., and Nelson D.E. Chlamydial interferon gamma immune evasion influences infection tropism. Curr Opin Microbiol 10 (2007) 47-51
35. Caldwell H.D., Wood H., Crane D., Bailey R., Jones R.B., Mabey D., Maclean I., Mohammed Z., Peeling R., Roshick C., et al. Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J Clin Invest 111 (2003) 1757-1769
36. Heinzen R.A., and Hackstadt T. The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecular-weight compounds. Infect Immun 65 (1997) 1088-1094
37. Taraska T., Ward D.M., Ajioka R.S., Wyrick P.B., Davis-Kaplan S.R., Davis C.H., and Kaplan J. The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect Immun 64 (1996) 3713-3727
38. Heinzen R.A., Scidmore M.A., Rockey D.D., and Hackstadt T. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun 64 (1996) 796-809
39. Scidmore M.A., Fischer E.R., and Hackstadt T. Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect Immun 71 (2003) 973-984
40. Moore E.R., Fischer E.R., Mead D.J., and Hackstadt T. The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9 (2008) 2130-2140. In this paper, the authors developed a polarized epithelial cell model to study how Chlamydia affects vectoral trafficking of lipids and proteins to the inclusion. C2BBe1 polarized colonic cells were infected with C. trachomatis and the traffic of ceramide and its metabolic derivatives, glucosylceramide and sphingomyelin, was evaluated. Results support that, as apposed to glucosylceramide, sphingomyelin was retained in the chlamydial inclusion and incorporated into elementary bodies. This retention of sphingomyelin correlated with a disruption of basolateral trafficking.
41. van Ooij C., Apodaca G., and Engel J. Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect Immun 65 (1997) 758-766
42. Wolf K., and Hackstadt T. Sphingomyelin trafficking in Chlamydia pneumoniae-infected cells. Cell Microbiol 3 (2001) 145-152
43. Hackstadt T., Rockey D.D., Heinzen R.A., and 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 15 (1996) 964-977
44. Rockey D.D., Fischer E.R., and Hackstadt T. Temporal analysis of the developing Chlamydia psittaci inclusion by use of fluorescence and electron microscopy. Infect Immun 64 (1996) 4269-4278
45. Su H., McClarty G., Dong F., Hatch G.M., Pan Z.K., and Zhong G. Activation of Raf/MEK/ERK/cPLA2 signaling pathway is essential for chlamydial acquisition of host glycerophospholipids. J Biol Chem 279 (2004) 9409-9416
46. Rzomp K.A., Scholtes L.D., Briggs B.J., Whittaker G.R., and Scidmore M.A. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 71 (2003) 5855-5870
47. Rzomp K.A., Moorhead A.R., and Scidmore M.A. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 74 (2006) 5362-5373
48. Cortes C., Rzomp K.A., Tvinnereim A., Scidmore M.A., and Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 75 (2007) 5586-5596
49. Delevoye C., Nilges M., Dehoux P., Paumet F., Perrinet S., Dautry-Varsat A., and Subtil A. SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 4 (2008) e1000022. The authors show that host SNARE proteins Vamp3, Vamp7, and Vamp8 are recruited to the immediate vicinity of the inclusion membrane and that chlamydial inclusion membrane protein IncA has a dominant role in this recruitment. SNARE-like motifs were found in the inclusion membrane proteins IncA and CT813 from Chlamydia trachomatis and these two proteins were shown to bind SNAREs. Moreover, SNARE-like motif present in IncA was shown to be required for IncA-SNARE binding.
50. Paumet F., Wesolowski J., Garcia-Diaz A., Delevoye C., Aulner N., Shuman H.A., Subtil A., and Rothman J.E. Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS One 4 (2009) e7375. In this paper, the investigators assess how different bacteria can influence eukaryotic membrane fusion. The results show that both, IncA from Chlamydia trachomatis and IcmG/DotF from Legionella pneuomphila, can inhibit the endocytic SNARE machinery. The inhibitory function was found to reside in the SNARE-like motifs present in these bacterial proteins.
51. Beatty W.L. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J Cell Sci 119 (2006) 350-359
52. Beatty W.L. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 76 (2008) 2872-2881
53. Heuer D., Lipinski A.R., Machuy N., Karlas A., Wehrens A., Siedler F., Brinkmann V., and Meyer T.F. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457 (2009) 731-735. This study shows that in Chlamydia-infected cells, the Golgi apparatus is fragmented into ministacks and recruited to the parasitopherous vacuole. Golgi fragmentation was associated with host caspases and calpains-mediated processing of the Golgi protein golgin-84. This phenomenon was required for lipid acquisition and replication of C. trachomatis.
54. Lipinski A.R., Heymann J., Meissner C., Karlas A., Brinkmann V., Meyer T.F., and Heuer D. Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation. PLoS Pathog 5 (2009) e1000615. By using RNA interference, these investigators show that depletion of Rab6 or Rab11, negatively impacted Chlamydia trachomatis replication. These Rab proteins were found to be required for Chlamydia-induced Golgi-fragmentation downstream of golgin-84 processing. Moreover, knocking down of Rab6 and Rab11 blocked sphingolipid transport to the chlamydial inclusion.
55. Kumar Y., Cocchiaro J., and Valdivia R.H. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr Biol 16 (2006) 1646-1651
56. Cocchiaro J.L., Kumar Y., Fischer E.R., Hackstadt T., and Valdivia R.H. Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A 105 (2008) 9379-9384. By means of live cell, confocal and electron microscopy, this paper provides evidence showing that host cell lipid droplets are recruited around and translocated int the chlamydial inclusion. The fact that intact organelles can be translocated into the inclusion demonstrate that besides vesicle fusion, another means of nutrients delivery into the inclusion lumen can occur.
57. •] describe genome wide RNAi screens in Drosophila S2 cells for host factors required for chlamydial replication. This study reveals a role for mitochondria for efficient C. caviae infection.
58. van Ooij C., Kalman L., van I., Nishijima M., Hanada K., Mostov K., and Engel J.N. Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis. Cell Microbiol 2 (2000) 627-637
59. Carabeo R.A., Mead D.J., and Hackstadt T. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci U S A 100 (2003) 6771-6776
60. Hackstadt T., Scidmore M.A., and Rockey D.D. 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 (1995) 4877-4881
61. •] describe genome wide RNAi screens in Drosophila S2 cells for host factors required for chlamydial replication. This study reveals a role for c-Abl in chlamydial entry.
62. Hasegawa A., Sogo L.F., Tan M., and Sutterlin C. Host complement regulatory protein CD59 is transported to the chlamydial inclusion by a Golgi apparatus-independent pathway. Infect Immun 77 (2009) 1285-1292
63. De Matteis M.A., and Luini A. Exiting the Golgi complex. Nat Rev Mol Cell Biol 9 (2008) 273-284
64. Stenmark H. RabGTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10 (2009) 513-525
65. Sudhof T.C., and Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 323 (2009) 474-477
66. Li Z., Chen C., Chen D., Wu Y., Zhong Y., and Zhong G. Characterization of fifty putative inclusion membrane proteins encoded in the Chlamydia trachomatis genome. Infect Immun 76 (2008) 2746-2757
67. Hatch G.M., and McClarty G. Phospholipid composition of purified Chlamydia trachomatis mimics that of the eucaryotic host cell. Infect Immun 66 (1998) 3727-3735
68. Fader C.M., and Colombo M.I. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16 (2009) 70-78
69. Russell M.R., Nickerson D.P., and Odorizzi G. Molecular mechanisms of late endosome morphology, identity and sorting. Curr Opin Cell Biol 18 (2006) 422-428
70. Guo Y., Cordes K.R., Farese Jr. R.V., and Walther T.C. Lipid droplets at a glance. J Cell Sci 122 (2009) 749-752
71. Walther T.C., and Farese Jr. R.V. The life of lipid droplets. Biochim Biophys Acta 1791 (2009) 459-466
72. Robertson D.K., Gu L., Rowe R.K., and Beatty W.L. Inclusion biogenesis and reactivation of persistent chlamydia trachomatis requires host cell Sphingolipid Biosynthesis. PLoS Pathog 5 (2009) e1000664