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Make It a Sweet Home: Responses of to the Challenges of an Intravacuolar Lifestyle

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  • Authors: Sébastien Triboulet1, Agathe Subtil2
  • Editors: Pascale Cossart3, Craig R. Roy4, Philippe Sansonetti5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institut Pasteur, Cell Biology of Microbial Infection, 75015 Paris, France; 2: Institut Pasteur, Cell Biology of Microbial Infection, 75015 Paris, France; 3: Institut Pasteur, Paris, France; 4: Yale University School of Medicine, New Haven, Connecticut; 5: Institut Pasteur, Paris, France
  • Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0005-2019
  • Received 21 March 2018 Accepted 18 January 2019 Published 08 March 2019
  • Agathe Subtil, [email protected]
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  • Abstract:

    Intravacuolar development has been adopted by several bacteria that grow inside a host cell. Remaining in a vacuole, as opposed to breaching the cytosol, protects the bacteria from some aspects of the cytosolic innate host defense and allows them to build an environment perfectly adapted to their needs. However, this raises new challenges: the host resources are separated from the bacteria by a lipid bilayer that is nonpermeable to most nutrients. In addition, the area of this lipid bilayer needs to expand to accommodate bacterial multiplication. This requires building material and energy that are not directly invested in bacterial growth. This article describes the strategies acquired by the obligate intracellular pathogen to circumvent the difficulties raised by an intravacuolar lifestyle. We start with an overview of the origin and composition of the vacuolar membrane. Acquisition of host resources is largely, although not exclusively, mediated by interactions with membranous compartments of the eukaryotic cell, and we describe how the inclusion modifies the architecture of the cell and distribution of the neighboring compartments. The second part of this review describes the four mechanisms characterized so far by which the bacteria acquire resources from the host: (i) transport/diffusion across the vacuole membrane, (ii) fusion of this membrane with host compartments, (iii) direct transfer of lipids at membrane contact sites, and (iv) engulfment by the vacuole membrane of large cytoplasmic entities.

  • Citation: Triboulet S, Subtil A. 2019. Make It a Sweet Home: Responses of to the Challenges of an Intravacuolar Lifestyle. Microbiol Spectrum 7(2):BAI-0005-2019. doi:10.1128/microbiolspec.BAI-0005-2019.

References

1. 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 USA 92:4877–4881 http://dx.doi.org/10.1073/pnas.92.11.4877. [PubMed]
2. Moore ER, Fischer ER, Mead DJ, Hackstadt T. 2008. The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9:2130–2140 http://dx.doi.org/10.1111/j.1600-0854.2008.00828.x. [PubMed]
3. Carabeo RA, Mead DJ, Hackstadt T. 2003. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci USA 100:6771–6776 http://dx.doi.org/10.1073/pnas.1131289100. [PubMed]
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 http://dx.doi.org/10.1128/jb.179.23.7233-7242.1997. [PubMed]
5. Yao J, Dodson VJ, Frank MW, Rock CO. 2015. Chlamydia trachomatis scavenges host fatty acids for phospholipid synthesis via an acyl-acyl carrier protein synthetase. J Biol Chem 290:22163–22173 http://dx.doi.org/10.1074/jbc.M115.671008. [PubMed]
6. Yao J, Cherian PT, Frank MW, Rock CO. 2015. Chlamydia trachomatis relies on autonomous phospholipid synthesis for membrane biogenesis. J Biol Chem 290:18874–18888 http://dx.doi.org/10.1074/jbc.M115.657148. [PubMed]
7. Taraska T, Ward DM, Ajioka RS, Wyrick PB, Davis-Kaplan SR, Davis CH, Kaplan J. 1996. The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect Immun 64:3713–3727. [PubMed]
8. Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T. 1996. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun 64:796–809. [PubMed]
9. 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 http://dx.doi.org/10.1128/IAI.71.2.973-984.2003. [PubMed]
10. Aeberhard L, Banhart S, Fischer M, Jehmlich N, Rose L, Koch S, Laue M, Renard BY, Schmidt F, Heuer D. 2015. The proteome of the isolated Chlamydia trachomatis containing vacuole reveals a complex trafficking platform enriched for retromer components. PLoS Pathog 11:e1004883 http://dx.doi.org/10.1371/journal.ppat.1004883. [PubMed]
11. Dehoux P, Flores R, Dauga C, Zhong G, Subtil A. 2011. Multi-genome identification and characterization of chlamydiae-specific type III secretion substrates: the Inc proteins. BMC Genomics 12:109 http://dx.doi.org/10.1186/1471-2164-12-109. [PubMed]
12. 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 http://dx.doi.org/10.1046/j.1365-2958.2001.02272.x. [PubMed]
13. Galán JE, Lara-Tejero M, Marlovits TC, Wagner S. 2014. Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68:415–438 http://dx.doi.org/10.1146/annurev-micro-092412-155725. [PubMed]
14. Bannantine JP, Griffiths RS, Viratyosin W, Brown WJ, Rockey DD. 2000. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell Microbiol 2:35–47 http://dx.doi.org/10.1046/j.1462-5822.2000.00029.x. [PubMed]
15. Lutter EI, Martens C, Hackstadt T. 2012. Evolution and conservation of predicted inclusion membrane proteins in chlamydiae. Comp Funct Genomics 2012:362104 http://dx.doi.org/10.1155/2012/362104. [PubMed]
16. Weber MM, Bauler LD, Lam J, Hackstadt T. 2015. Expression and localization of predicted inclusion membrane proteins in Chlamydia trachomatis. Infect Immun 83:4710–4718 http://dx.doi.org/10.1128/IAI.01075-15. [PubMed]
17. Shaw EI, Dooley CA, Fischer ER, Scidmore MA, Fields KA, Hackstadt T. 2000. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol Microbiol 37:913–925 http://dx.doi.org/10.1046/j.1365-2958.2000.02057.x. [PubMed]
18. Mital J, Miller NJ, Dorward DW, Dooley CA, Hackstadt T. 2013. Role for chlamydial inclusion membrane proteins in inclusion membrane structure and biogenesis. PLoS One 8:e63426 http://dx.doi.org/10.1371/journal.pone.0063426. [PubMed]
19. Gauliard E, Ouellette SP, Rueden KJ, Ladant D. 2015. Characterization of interactions between inclusion membrane proteins from Chlamydia trachomatis. Front Cell Infect Microbiol 5:13 http://dx.doi.org/10.3389/fcimb.2015.00013. [PubMed]
20. Grieshaber SS, Grieshaber NA, Hackstadt T. 2003. Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process. J Cell Sci 116:3793–3802 http://dx.doi.org/10.1242/jcs.00695. [PubMed]
21. Kumar Y, Valdivia RH. 2008. Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4:159–169 http://dx.doi.org/10.1016/j.chom.2008.05.018. [PubMed]
22. Volceanov L, Herbst K, Biniossek M, Schilling O, Haller D, Nölke T, Subbarayal P, Rudel T, Zieger B, Häcker G. 2014. Septins arrange F-actin-containing fibers on the Chlamydia trachomatis inclusion and are required for normal release of the inclusion by extrusion. mBio 5:e01802-14 http://dx.doi.org/10.1128/mBio.01802-14. [PubMed]
23. Al-Zeer MA, Al-Younes HM, Kerr M, Abu-Lubad M, Gonzalez E, Brinkmann V, Meyer TF. 2014. Chlamydia trachomatis remodels stable microtubules to coordinate Golgi stack recruitment to the chlamydial inclusion surface. Mol Microbiol 94:1285–1297 http://dx.doi.org/10.1111/mmi.12829. [PubMed]
24. Kokes M, Dunn JD, Granek JA, Nguyen BD, Barker JR, Valdivia RH, Bastidas RJ. 2015. Integrating chemical mutagenesis and whole-genome sequencing as a platform for forward and reverse genetic analysis of Chlamydia. Cell Host Microbe 17:716–725 http://dx.doi.org/10.1016/j.chom.2015.03.014. [PubMed]
25. Wesolowski J, Weber MM, Nawrotek A, Dooley CA, Calderon M, St Croix CM, Hackstadt T, Cherfils J, Paumet F. 2017. Chlamydia hijacks ARF GTPases to coordinate microtubule posttranslational modifications and Golgi complex positioning. mBio 8:e02280-16 http://dx.doi.org/10.1128/mBio.02280-16. [PubMed]
26. Dumoux M, Menny A, Delacour D, Hayward RD. 2015. A Chlamydia effector recruits CEP170 to reprogram host microtubule organization. J Cell Sci 128:3420–3434 http://dx.doi.org/10.1242/jcs.169318. [PubMed]
27. Gurumurthy RK, Chumduri C, Karlas A, Kimmig S, Gonzalez E, Machuy N, Rudel T, Meyer TF. 2014. Dynamin-mediated lipid acquisition is essential for Chlamydia trachomatis development. Mol Microbiol 94:186–201 http://dx.doi.org/10.1111/mmi.12751. [PubMed]
28. Scidmore MA, Fischer ER, Hackstadt T. 1996. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J Cell Biol 134:363–374 http://dx.doi.org/10.1083/jcb.134.2.363. [PubMed]
29. Derré 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 http://dx.doi.org/10.1371/journal.ppat.1002092. [PubMed]
30. Phillips MJ, Voeltz GK. 2016. Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol 17:69–82 http://dx.doi.org/10.1038/nrm.2015.8. [PubMed]
31. Derré I. 2015. Chlamydiae interaction with the endoplasmic reticulum: contact, function and consequences. Cell Microbiol 17:959–966 http://dx.doi.org/10.1111/cmi.12455. [PubMed]
32. Stanhope R, Flora E, Bayne C, Derré I. 2017. IncV, a FFAT motif-containing Chlamydia protein, tethers the endoplasmic reticulum to the pathogen-containing vacuole. Proc Natl Acad Sci USA 114:12039–12044 http://dx.doi.org/10.1073/pnas.1709060114. [PubMed]
33. Dumoux M, Clare DK, Saibil HR, Hayward RD. 2012. Chlamydiae assemble a pathogen synapse to hijack the host endoplasmic reticulum. Traffic 13:1612–1627 http://dx.doi.org/10.1111/tra.12002. [PubMed]
34. Kokes M, Valdivia RH. 2015. Differential translocation of host cellular materials into the Chlamydia trachomatis inclusion lumen during chemical fixation. PLoS One 10:e0139153 http://dx.doi.org/10.1371/journal.pone.0139153. [PubMed]
35. Kurihara Y, Itoh R, Shimizu A, Walenna NF, Chou B, Ishii K, Soejima T, Fujikane A, Hiromatsu K. 2019. Chlamydia trachomatis targets mitochondrial dynamics to promote intracellular survival and proliferation. Cell Microbiol 21:e12962 http://dx.doi.org/10.1111/cmi.12962. [PubMed]
36. Chowdhury SR, Reimer A, Sharan M, Kozjak-Pavlovic V, Eulalio A, Prusty BK, Fraunholz M, Karunakaran K, Rudel T. 2017. Chlamydia preserves the mitochondrial network necessary for replication via microRNA-dependent inhibition of fission. J Cell Biol 216:1071–1089 http://dx.doi.org/10.1083/jcb.201608063. [PubMed]
37. Larson CL, Heinzen RA. 2017. High-content imaging reveals expansion of the endosomal compartment during Coxiella burnetii parasitophorous vacuole maturation. Front Cell Infect Microbiol 7:48 http://dx.doi.org/10.3389/fcimb.2017.00048. [PubMed]
38. Heinzen RA, Hackstadt T. 1997. The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecular-weight compounds. Infect Immun 65:1088–1094. [PubMed]
39. Grieshaber S, Swanson JA, Hackstadt T. 2002. Determination of the physical environment within the Chlamydia trachomatis inclusion using ion-selective ratiometric probes. Cell Microbiol 4:273–283 http://dx.doi.org/10.1046/j.1462-5822.2002.00191.x. [PubMed]
40. Senerovic L, Tsunoda SP, Goosmann C, Brinkmann V, Zychlinsky A, Meissner F, Kolbe M. 2012. Spontaneous formation of IpaB ion channels in host cell membranes reveals how Shigella induces pyroptosis in macrophages. Cell Death Dis 3:e384 http://dx.doi.org/10.1038/cddis.2012.124. [PubMed]
41. Dortet L, Lombardi C, Cretin F, Dessen A, Filloux A. 2018. Pore-forming activity of the Pseudomonas aeruginosa type III secretion system translocon alters the host epigenome. Nat Microbiol 3:378–386 http://dx.doi.org/10.1038/s41564-018-0109-7. [PubMed]
42. Chellas-Géry B, Wolf K, Tisoncik J, Hackstadt T, Fields KA. 2011. Biochemical and localization analyses of putative type III secretion translocator proteins CopB and CopB2 of Chlamydia trachomatis reveal significant distinctions. Infect Immun 79:3036–3045 http://dx.doi.org/10.1128/IAI.00159-11. [PubMed]
43. Fisher DJ, Fernández RE, Adams NE, Maurelli AT. 2012. Uptake of biotin by Chlamydia spp. through the use of a bacterial transporter (BioY) and a host-cell transporter (SMVT). PLoS One 7:e46052 http://dx.doi.org/10.1371/journal.pone.0046052. [PubMed]
44. Cox JV, Naher N, Abdelrahman YM, Belland RJ. 2012. Host HDL biogenesis machinery is recruited to the inclusion of Chlamydia trachomatis-infected cells and regulates chlamydial growth. Cell Microbiol 14:1497–1512 http://dx.doi.org/10.1111/j.1462-5822.2012.01823.x. [PubMed]
45. Cox JV, Abdelrahman YM, Peters J, Naher N, Belland RJ. 2016. Chlamydia trachomatis utilizes the mammalian CLA1 lipid transporter to acquire host phosphatidylcholine essential for growth. Cell Microbiol 18:305–318 http://dx.doi.org/10.1111/cmi.12523. [PubMed]
46. Gehre L, Gorgette O, Perrinet S, Prevost MC, Ducatez M, Giebel AM, Nelson DE, Ball SG, Subtil A. 2016. Sequestration of host metabolism by an intracellular pathogen. eLife 5:e12552 http://dx.doi.org/10.7554/eLife.12552. [PubMed]
47. 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 http://dx.doi.org/10.1002/j.1460-2075.1996.tb00433.x. [PubMed]
48. Elwell C, Mirrashidi K, Engel J. 2016. Chlamydia cell biology and pathogenesis. Nat Rev Microbiol 14:385–400 http://dx.doi.org/10.1038/nrmicro.2016.30. [PubMed]
49. Damiani MT, Gambarte Tudela J, Capmany A. 2014. Targeting eukaryotic Rab proteins: a smart strategy for chlamydial survival and replication. Cell Microbiol 16:1329–1338 http://dx.doi.org/10.1111/cmi.12325. [PubMed]
50. Delevoye C, Nilges M, Dehoux P, Paumet F, Perrinet S, Dautry-Varsat A, Subtil A. 2008. SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 4:e1000022 http://dx.doi.org/10.1371/journal.ppat.1000022. [PubMed]
51. Paumet F, Wesolowski J, Garcia-Diaz A, Delevoye C, Aulner N, Shuman HA, Subtil A, Rothman JE. 2009. Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS One 4:e7375 http://dx.doi.org/10.1371/journal.pone.0007375. [PubMed]
52. Mirrashidi KM, Elwell CA, Verschueren E, Johnson JR, Frando A, Von Dollen J, Rosenberg O, Gulbahce N, Jang G, Johnson T, Jäger S, Gopalakrishnan AM, Sherry J, Dunn JD, Olive A, Penn B, Shales M, Cox JS, Starnbach MN, Derre I, Valdivia R, Krogan NJ, Engel J. 2015. Global mapping of the Inc-human interactome reveals that retromer restricts Chlamydia infection. Cell Host Microbe 18:109–121 http://dx.doi.org/10.1016/j.chom.2015.06.004. [PubMed]
53. Pokrovskaya ID, Szwedo JW, Goodwin A, Lupashina TV, Nagarajan UM, Lupashin VV. 2012. Chlamydia trachomatis hijacks intra-Golgi COG complex-dependent vesicle trafficking pathway. Cell Microbiol 14:656–668 http://dx.doi.org/10.1111/j.1462-5822.2012.01747.x. [PubMed]
54. Vromman F, Perrinet S, Gehre L, Subtil A. 2016. The DUF582 proteins of Chlamydia trachomatis bind to components of the ESCRT machinery, which is dispensable for bacterial growth in vitro. Front Cell Infect Microbiol 6:123 http://dx.doi.org/10.3389/fcimb.2016.00123. [PubMed]
55. Giles DK, Wyrick PB. 2008. Trafficking of chlamydial antigens to the endoplasmic reticulum of infected epithelial cells. Microbes Infect 10:1494–1503 http://dx.doi.org/10.1016/j.micinf.2008.09.001. [PubMed]
56. Elwell CA, Jiang S, Kim JH, Lee A, Wittmann T, Hanada K, Melancon P, Engel JN. 2011. Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog 7:e1002198 CORRECTION PLoS Pathog 9:10.1371/annotation/f8e7c7e3-c347-4243-9146-db77900cb90c http://dx.doi.org/10.1371/journal.ppat.1002198.
57. 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 USA 105:9379–9384 http://dx.doi.org/10.1073/pnas.0712241105. [PubMed]
58. Saka HA, Thompson JW, Chen YS, Dubois LG, Haas JT, Moseley A, Valdivia RH. 2015. Chlamydia trachomatis infection leads to defined alterations to the lipid droplet proteome in epithelial cells. PLoS One 10:e0124630 http://dx.doi.org/10.1371/journal.pone.0124630. [PubMed]
59. Soupene E, Wang D, Kuypers FA. 2015. Remodeling of host phosphatidylcholine by Chlamydia acyltransferase is regulated by acyl-CoA binding protein ACBD6 associated with lipid droplets. MicrobiologyOpen 4:235–251 http://dx.doi.org/10.1002/mbo3.234. [PubMed]
60. Recuero-Checa MA, Sharma M, Lau C, Watkins PA, Gaydos CA, Dean D. 2016. Chlamydia trachomatis growth and development requires the activity of host long-chain acyl-CoA synthetases (ACSLs). Sci Rep 6:23148 http://dx.doi.org/10.1038/srep23148. [PubMed]
61. Boncompain G, Müller C, Meas-Yedid V, Schmitt-Kopplin P, Lazarow PB, Subtil A. 2014. The intracellular bacteria Chlamydia hijack peroxisomes and utilize their enzymatic capacity to produce bacteria-specific phospholipids. PLoS One 9:e86196 http://dx.doi.org/10.1371/journal.pone.0086196. [PubMed]
62. Nguyen PH, Lutter EI, Hackstadt T. 2018. Chlamydia trachomatis inclusion membrane protein MrcA interacts with the inositol 1,4,5-trisphosphate receptor type 3 (ITPR3) to regulate extrusion formation. PLoS Pathog 14:e1006911 http://dx.doi.org/10.1371/journal.ppat.1006911. [PubMed]
63. Verbeke P, Welter-Stahl L, Ying S, Hansen J, Häcker G, Darville T, Ojcius DM. 2006. Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog 2:e45 http://dx.doi.org/10.1371/journal.ppat.0020045. [PubMed]
64. Gurumurthy RK, Mäurer AP, Machuy N, Hess S, Pleissner KP, Schuchhardt J, Rudel T, Meyer TF. 2010. A loss-of-function screen reveals Ras- and Raf-independent MEK-ERK signaling during Chlamydia trachomatis infection. Sci Signal 3:ra21 http://dx.doi.org/10.1126/scisignal.2000651. [PubMed]
65. Suchland RJ, Rockey DD, Bannantine JP, Stamm WE. 2000. Isolates of Chlamydia trachomatis that occupy nonfusogenic inclusions lack IncA, a protein localized to the inclusion membrane. Infect Immun 68:360–367 http://dx.doi.org/10.1128/IAI.68.1.360-367.2000. [PubMed]
66. Belland RJ, Zhong G, Crane DD, Hogan D, Sturdevant D, Sharma J, Beatty WL, Caldwell HD. 2003. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc Natl Acad Sci USA 100:8478–8483 http://dx.doi.org/10.1073/pnas.1331135100. [PubMed]
67. Lutter EI, Barger AC, Nair V, Hackstadt T. 2013. Chlamydia trachomatis inclusion membrane protein CT228 recruits elements of the myosin phosphatase pathway to regulate release mechanisms. Cell Reports 3:1921–1931 http://dx.doi.org/10.1016/j.celrep.2013.04.027. [PubMed]
68. Sixt BS, Bastidas RJ, Finethy R, Baxter RM, Carpenter VK, Kroemer G, Coers J, Valdivia RH. 2016. The Chlamydia trachomatis inclusion membrane protein CpoS counteracts STING-mediated cellular surveillance and suicide programs. Cell Host Microbe 21:113–121 10.1016/j.chom.2016.12.002:1-34.
69. Weber MM, Lam JL, Dooley CA, Noriea NF, Hansen BT, Hoyt FH, Carmody AB, Sturdevant GL, Hackstadt T. 2017. Absence of specific Chlamydia trachomatis inclusion membrane proteins triggers premature inclusion membrane lysis and host cell death. Cell Reports 19:1406–1417 http://dx.doi.org/10.1016/j.celrep.2017.04.058. [PubMed]
70. Almeida F, Luís MP, Pereira IS, Pais SV, Mota LJ. 2018. The human centrosomal protein CCDC146 binds Chlamydia trachomatis inclusion membrane protein CT288 and is recruited to the periphery of the Chlamydia-containing vacuole. Front Cell Infect Microbiol 8:254 http://dx.doi.org/10.3389/fcimb.2018.00254. [PubMed]
71. Mital J, Lutter EI, Barger AC, Dooley CA, Hackstadt T. 2015. Chlamydia trachomatis inclusion membrane protein CT850 interacts with the dynein light chain DYNLT1 (Tctex1). Biochem Biophys Res Commun 462:165–170 http://dx.doi.org/10.1016/j.bbrc.2015.04.116. [PubMed]
72. 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 http://dx.doi.org/10.1111/j.1462-5822.2010.01465.x. [PubMed]
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/content/journal/microbiolspec/10.1128/microbiolspec.BAI-0005-2019
2019-03-08
2019-10-18

Abstract:

Intravacuolar development has been adopted by several bacteria that grow inside a host cell. Remaining in a vacuole, as opposed to breaching the cytosol, protects the bacteria from some aspects of the cytosolic innate host defense and allows them to build an environment perfectly adapted to their needs. However, this raises new challenges: the host resources are separated from the bacteria by a lipid bilayer that is nonpermeable to most nutrients. In addition, the area of this lipid bilayer needs to expand to accommodate bacterial multiplication. This requires building material and energy that are not directly invested in bacterial growth. This article describes the strategies acquired by the obligate intracellular pathogen to circumvent the difficulties raised by an intravacuolar lifestyle. We start with an overview of the origin and composition of the vacuolar membrane. Acquisition of host resources is largely, although not exclusively, mediated by interactions with membranous compartments of the eukaryotic cell, and we describe how the inclusion modifies the architecture of the cell and distribution of the neighboring compartments. The second part of this review describes the four mechanisms characterized so far by which the bacteria acquire resources from the host: (i) transport/diffusion across the vacuole membrane, (ii) fusion of this membrane with host compartments, (iii) direct transfer of lipids at membrane contact sites, and (iv) engulfment by the vacuole membrane of large cytoplasmic entities.

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Figures

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FIGURE 1

Cells infected with for 24 h (top left) and 48 h (top right). The bacteria were stably transformed to express the green fluorescent protein and appear in green; the inclusion lumen was labeled in red with an antibody against one Inc protein. DNA was stained in blue. Distortion of the nucleus due to the growth of the inclusion is already visible 24 hours postinfection. Infected cells are often multinucleated, as shown in the 48-hour infection example here, due to a failure to proceed through cytokinesis. Bar, 10 μm. Chlamydiae undergo a biphasic developmental cycle. The infectious form, called the elementary body (EB), is not replicative. Once internalized, it differentiates into a reticulate body (RB). RBs multiply several times in the inclusion before differentiating into EBs. Differentiation is not synchronous, and mature inclusions contain both EBs and RBs. The electron micrograph (bottom) shows part of a mature inclusion, with bacteria in contact with the inclusion membrane. The EBs can be distinguished from the RBs by their smaller size and their condensed chromatin.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0005-2019
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Image of FIGURE 2
FIGURE 2

Pathways for the import of molecules in the membrane and lumen of the inclusion. This schematic view of an inclusion depicts reticulate bodies and elementary bodies in light and dark gray, respectively. The four boxes show enlargements of the different suspected mechanisms for material import in the inclusion, with the purple arrow pointing to the direction of transport. (1) Channel proteins have not been identified yet, but the type 3 translocon proteins CopB and -B2 are attractive candidates for cation transport. Specific transport proteins have been observed at the inclusion membrane, and some of their substrates are listed as examples. (2) Fusion with host compartments is required to import host integral membrane proteins, and several host and Inc proteins have been implicated in the regulation of this process. However, the exact nature of the donor compartment(s) which fuses with the inclusion membrane is not known. (3) The endoplasmic reticulum makes close contacts with the inclusion membrane, and by co-opting a dedicated host machinery, the bacteria induce direct transfer of ceramide to the inclusion membrane. (4) Whether the engulfment of lipid droplets (LD), peroxisomes (P), and glycogen (G) proceeds via the same pathway, with inward invagination and scission of the inclusion membrane, remains to be determined.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0005-2019
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Tables

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TABLE 1

Identified Inc-host interactions

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0005-2019

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