A novel co-infection model with Toxoplasma and Chlamydia trachomatis highlights the importance of host cell manipulation for nutrient scavenging

Cellular Microbiology

Volumn 15, Issue 4, 2013, Pages 619-646

  Romano, Julia D ^a   de Beaumont, Catherine ^a   Carrasco, Jose A ^b   Ehrenman, Karen ^a   Bavoil, Patrik M ^b   Coppens, Isabelle ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM; CELL LEVEL; CELL MANIPULATION; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; NONHUMAN; NUTRIENT; ORGANELLE SHAPE; PARASITE; PHENOTYPE; PRIORITY JOURNAL; SCAVENGING SYSTEM; TOXOPLASMA; CELL CULTURE; FOOD; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; ORGANISMAL INTERACTION; PHYSIOLOGICAL STRESS;

BACTERIA (MICROORGANISMS); CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDOPHILA PSITTACI; MAMMALIA; TOXOPLASMA;

CELLS, CULTURED; CHLAMYDIA TRACHOMATIS; FOOD; HUMANS; MICROBIAL INTERACTIONS; STRESS, PHYSIOLOGICAL; TOXOPLASMA;

EID: 84874953682     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12060     Document Type: Article

References (77)

1. Baczynska, A., Birkelund, S., and Christiansen, G. (2006) Chlamydia trachomatis and genital mycoplasmas in the co-infection model - in vitro study. In Proceedings of the Eleventh International Symposium on Human Chlamydial Infections. Chernesky, M., Caldwell, H., Christiansen, G., Clarke, I.N., Kaltenboeck, B., Knirsch, C., etal. (eds). San Francisco, CA: International Chlamydia Symposium, pp. 225-228.
2. 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.
3. Beatty, W.L. (2008) Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 76: 2872-2881.
4. Beatty, W.L., Morrison, R.P., and Byrne, G.I. (1994) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58: 686-699.
5. Beeckman, D.S., and Vanrompay, D.C. (2010) Biology and intracellular pathogenesis of high or low virulent Chlamydophila psittaci strains in chicken macrophages. Vet Microbiol 141: 342-353.
6. Binet, R., and Maurelli, A.T. (2005) Fitness cost due to mutations in the 16S rRNA associated with spectinomycin resistance in Chlamydia psittaci 6BC. Antimicrob Agents Chemother 49: 4455-4464.
7. Black, C.M., Bermudez, L.E., Young, L.S., and Remington, J.S. (1990) Co-infection of macrophages modulates interferon gamma and tumor necrosis factor-induced activation against intracellular pathogens. J Exp Med 172: 977-980.
8. Borel, N., Dumrese, C., Ziegler, U., Schifferli, A., Kaiser, C., and Pospischil, A. (2010) Mixed infections with Chlamydia and porcine epidemic diarrhea virus - a new in vitro model of chlamydial persistence. BMC Microbiol 10: 201-210.
9. Byrne, G.I., and Moulder, J.W. (1978) Parasite-specified phagocytosis of Chlamydia psittaci and Chlamydia trachomatis by L and HeLa cells. Infect Immun 19: 598-606.
10. Byrne, G.I., Ouellette, S.P., Wang, Z., Rao, J.P., Lu, L., Beatty, W.L., and Hudson, A.P. (2001) Chlamydia pneumoniae expresses genes required for DNA replication but not cytokinesis during persistent infection of HEp-2 cells. Infect Immun 69: 5423-5429.
11. Caldwell, H.D., Wood, H., Crane, D., Bailey, R., Jones, R.B., Mabey, D., etal. (2003) Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J. Clin Investig 111: 1757-1769.
12. Capmany, A., and Damiani, M.T. (2010) Chlamydia trachomatis intercepts Golgi-derived sphingolipids through a Rab14-mediated transport required for bacterial development and replication. PLoS ONE 5: e14084.
13. 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.
14. Carrasco, J.A., Tan, C., Rank, R.G., Hsia, R.C., and Bavoil, P.M. (2011) Altered developmental expression of polymorphic membrane proteins in penicillin-stressed Chlamydia trachomatis. Cell Microbiol 13: 1014-1025.
15. Casadevall, A. (2008) Evolution of intracellular pathogens. Annu Rev Microbiol 62: 19-33.
16. de Chastellier, C., Thibon, M., and Rabinovitch, M. (1999) Construction of chimeric phagosomes that shelter Mycobacterium avium and Coxiella burnetii (phase II) in doubly infected mouse macrophages: an ultrastructural study. Eur J Cell Biol 78: 580-592.
17. Clausen, J.D., Christiansen, G., Holst, H.U., and Birkelund, S. (1997) Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol Microbiol 25: 441-449.
18. Cocchiaro, J.L., and Valdivia, R.H. (2009) New insights into Chlamydia intracellular survival mechanisms. Cell Microbiol 11: 1571-1578.
19. 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.
20. Coles, A.M., Reynolds, D.J., Harper, A., Devitt, A., and Pearce, J.H. (1993) Low-nutrient induction of abnormal chlamydial development: a novel component of chlamydial pathogenesis? FEMS Microbiol Lett 106: 193-200.
21. Coppens, I., and Joiner, K.A. (2003) Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol Biol Cell 14: 3804-3820.
22. Coppens, I., Sinai, A.P., and Joiner, K.A. (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149: 167-180.
23. Coppens, I., Dunn, J.D., Romano, J.D., Pypaert, M., Zhang, H., Boothroyd, J.C., and Joiner, K.A. (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125: 261-274.
24. Crane, D.D., Carlson, J.H., Fischer, E.R., Bavoil, P., Hsia, R.C., Tan, C., etal. (2006) Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc Natl Acad Sci USA 103: 1894-1899.
25. Crawford, M.J., Thomsen-Zieger, N., Ray, M., Schachtner, J., Roos, D.S., and Seeber, F. (2006) Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J 25: 3214-3222.
26. Dautry-Varsat, A., Subtil, A., and Hackstadt, T. (2005) Recent insights into the mechanisms of Chlamydia entry. Cell Microbiol 7: 1714-1722.
27. Derouin, F., and Chastang, C. (1989) In vitro effects of folate inhibitors on Toxoplasma gondii. Antimicrob Agents Chemother 33: 1753-1759.
28. Derré, I., Swiss, R., and 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.
29. Elwell, C.A., and Engel, J.N. (2012) Lipid acquisition by intracellular Chlamydiae. Cell Microbiol 14: 1010-1018.
30. Escalante-Ochoa, C., Ducatelle, R., and Haesebrouck, F. (1998) The intracellular life of Chlamydia psittaci: how do the bacteria interact with the host cell? FEMS Microbiol Rev 22: 65-78.
31. Ferreira da Silva Mda, F., Barbosa, H.S., Gross, U., and Lüder, C.G. (2008) Stress-related and spontaneous stage differentiation of Toxoplasma gondii. Mol Biosyst 4: 824-834.
32. Fields, K.A., and Hackstadt, T. (2002) The chlamydial inclusion: escape from the endocytic pathway. Annu Rev Cell Dev Biol 18: 221-245.
33. Fraser-Liggett, C.M. (2005) Insights on biology and evolution from microbial genome sequencing. Genome Res 15: 1603-1610.
34. Grieshaber, S.S., Grieshaber, N.A., and 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.
35. Hackstadt, T., Scidmore, M., and Rockey, 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.
36. 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.
37. Hatch, T.P., Al-Hossainy, E., and Silverman, J.A. (1982) Adenine nucleotide and lysine transport in Chlamydia psittaci. J Bacteriol 150: 662-670.
38. Heuer, D., Rejman Lipinski, A., Machuy, N., Karlas, A., Wehren, A., Siedler, F., etal. (2009) Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457: 731-735.
39. Johnson, K.A., Tan, M., and Sütterlin, C. (2009) Centrosome abnormalities during a Chlamydia trachomatis infection are caused by dysregulation of the normal duplication pathway. Cell Microbiol 11: 1064-1073.
40. Kokab, A., Jennings, R., Eley, A., Pacey, A.A., and Cross, N.A. (2010) Analysis of modulated gene expression in a model of Interferon-γ-induced persistence of Chlamydia trachomatis in HEp-2 cells. Microb Pathog 49: 217-225.
41. Kumar, Y., and Valdivia, R.H. (2009) Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5: 593-601.
42. Laliberté, J., and Carruthers, V.B. (2008) Host cell manipulation by the human pathogen Toxoplasma gondii. Cell Mol Life Sci 65: 1900-1915.
43. Lambden, P.R., Pickett, M.A., and Clarke, I.N. (2006) The effect of penicillin on Chlamydia trachomatis DNA replication. Microbiology 152: 2573-2578.
44. Luft, B.F., and Remington, J.S. (1992) Toxoplasma encephalitis in AIDS. Clin Infect Dis 15: 211-222.
45. Matsumoto, A., and Manire, G.P. (1970) Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J Bacteriol 101: 278-285.
46. Meirelles, M.N., and De Souza, W. (1983) Interaction of lysosomes with endocytic vacuoles in macrophages simultaneously infected with Trypanosoma cruzi and Toxoplasma gondii. J Submicrosc Cytol 15: 889-896.
47. de Melo, E.J., and de Souza, W. (1996) Pathway of C6-NBD-Ceramide on the host cell infected with Toxoplasma gondii. Cell Struct Funct 21: 47-52.
48. Mercier, C., Dubremetz, J.F., Rauscher, B., Lecordier, L., Sibley, L.D., and Cesbron-Delauw, M.F. (2002) Biogenesis of nanotubular network in Toxoplasma parasitophorous vacuole induced by parasite proteins. Mol Biol Cell 13: 2397-2409.
49. Moulder, J.W., Levy, N.J., and Schulman, L.P. (1980) Persistent infection of mouse fibroblasts (L cells) with Chlamydia psittaci: evidence for a cryptic chlamydial form. Infect Immun 30: 874-883.
50. Poumay, Y., and Ronveaux-Dupal, M.F. (1985) Rapid preparative isolation of concentrated low-density lipoproteins and of lipoprotein-deficient serum using vertical rotor gradient ultracentrifugation. J Lipid Res 26: 1476-1480.
51. Rabinovitch, M., and Veras, P.S. (1996) Cohabitation of Leishmania amazonensis and Coxiella burnetii. Trends Microbiol 4: 158-161.
52. Ramaswamy, A.V., and Maurelli, A.T. (2010) Chlamydia trachomatis serovar L2 can utilize exogenous lipoic acid through the action of the lipoic acid ligase LplA1. J Bacteriol 192: 6172-6181.
53. Raulston, J.E. (1997) Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect Immun 65: 4539-4547.
54. 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.
55. Rockey, D.D., and Matsumoto, A. (2000) The chlamydial developmental cycle. In Prokaryotic Development. Brun, Y.V., and Shimkets, L.J. (eds). Washington DC: ASM Press, pp. 403-425.
56. Romano, J.D., Bano, N., and Coppens, I. (2008) New host nuclear functions are not required for the modifications of the parasitophorous vacuole of Toxoplasma. Cell Microbiol 10: 465-476.
57. Roos, D.S., Donald, R.G., Morrissette, N.S., and Moulton, A.L. (1994) Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45: 27-63.
58. Saka, H.A., and Valdivia, R.H. (2010) Acquisition of nutrients by Chlamydiae: unique challenges of living in an intracellular compartment. Curr Opin Microbiol 13: 4-10.
59. Schachter, J. (1999) Infection and disease epidemiology. In Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. Stephens, R.S. (ed.). Washington DC: ASM Press, pp. 139-169.
60. Schramm, N., and Wyrick, P.B. (1995) Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect Immun 63: 324-332.
61. Scidmore, M.A., Fischer, E.R., and Hackstadt, T. (2003) Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect Immun 71: 973-984.
62. Sibley, L.D. (2003) Toxoplasma gondii: perfecting an intracellular life style. Traffic 4: 581-586.
63. Sibley, L.D., Messina, M., and Niesman, I.R. (1994) Stable DNA transformation in the obligate intracellular parasite Toxoplasma gondii by complementation of tryptophan auxotrophy. Proc Natl Acad Sci USA 91: 5508-5512.
64. Sibley, L.D., Niesman, I.R., Parmley, S.F., and Cesbron-Delauw, M.F. (1995) Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J Cell Sci 108: 1669-1677.
65. Sinai, A.P., Paul, S., Rabinovitch, M., Kaplan, G., and Joiner, K.A. (2000) Coinfection of fibroblasts with Coxiella burnetti and Toxoplasma gondii: to each their own. Microbes Infect 2: 727-736.
66. Skilton, R.J., Cutcliffen, L.T., Barlow, D., Wang, Y., Salim, O., Lambden, P.R., and Clarke, I.N. (2009) Penicillin induced persistence in Chlamydia trachomatis: high quality time lapse video analysis of the developmental cycle. PLoS ONE 4: e7723.
67. Spano, F., Ricci, I., Di Cristina, M., Possenti, A., Tinti, M., Dendouga, N., etal. (2002) The SAG5 locus of Toxoplasma gondii encodes three novel proteins belonging to the SAG1 family of surface antigens. Int J Parasitol 32: 121-131.
68. Sweeney, K.R., Morrissette, N.S., LaChapelle, S., and Blader, I.J. (2010) Host cell invasion by Toxoplasma gondii is temporally regulated by the host microtubule cytoskeleton. Eukaryot Cell 9: 1680-1689.
69. Tan, C., Hsia, R.C., Shou, H., Carrasco, J.A., Rank, R.G., and Bavoil, P.M. (2010) Variable expression of surface-exposed polymorphic membrane proteins in in vitro-grown Chlamydia trachomatis. Cell Microbiol 12: 174-187.
70. Thompson, C.C., and Carabeo, R.A. (2011) An optimal method of iron starvation of the obligate intracellular pathogen, Chlamydia trachomatis. Front Microbiol 2: 1-10.
71. Tischler, M.E., Desautels, M., and Goldberg, A.L. (1982) Does leucine, leucyl-tRNA, or some metabolite of leucine regulate protein synthesis and degradation in skeletal and cardiac muscle? J Biol Chem 257: 1613-1621.
72. Vanover, J., Sun, J., Deka, S., Kintner, J., Duffourc, M.M., and Schoborg, R.V. (2008) Herpes simplex virus co-infection-induced Chlamydia trachomatis persistence is not mediated by any known persistence inducer or anti-chlamydial pathway. Microbiology 154: 971-978.
73. Volpon, L., and Lancelin, J. (2000) Solution NMR structures of the polyene macrolide antibiotic filipin III. FEBS Lett 478: 137-140.
74. Walker, M.E., Hjort, E.E., Smith, S.S., Tripathi, A., Hornick, J.E., Hinchcliffe, E.H., etal. (2008) Toxoplasma gondii actively remodels the microtubule network in host cells. Microbes Infect 10: 1440-1449.
75. Wilson, D.P., Mathews, S., Wan, C., Pettitt, A.N., and McElwain, D.L. (2004) Use of a quantitative gene expression assay based on micro-array techniques and a mathematical model for the investigation of chlamydial generation time. Bull Math Biol 66: 523-537.
76. Wyrick, P.B. (2010) Chlamydia trachomatis persistence in vitro: an overview. J Infect Dis 201: S88-S95.
77. Zhang, Y.X., Shi, Y., Zhou, M., and Petsko, G.A. (1994) Cloning, sequencing, and expression in Escherichia coli of the gene encoding a 45-kilodalton protein, elongation factor Tu, from Chlamydia trachomatis serovar F. J Bacteriol 176: 1184-1187.