Chapter 5 : Cell Biology

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Cell Biology, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818203/9781555811556_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555818203/9781555811556_Chap05-2.gif


Chlamydiae are extremely successful pathogens of humans and animals. The chlamydial developmental cycle may be considered superficially analogous to bacterial sporulation in that it consists of an environmentally stable cell type, called the elementary body (EB), and a functionally and morphologically distinct vegetative cell type, termed the reticulate body (RB). Electrostatic interactions play an important role in at least the initial stages of infection. Attachment is dependent upon cations to neutralize the net negative surface charge of both host and parasite. Several chlamydial components have been proposed at one time or another to function as adhesins. A number of EB surface components have been proposed as potential ligands mediating attachment to host cells. Currently, heparan sulfate-like proteoglycans are considered one of the more promising candidates mediating at least an initial electrostatic interaction between the EB and the host cell surface. The general implication is that chlamydiae, like many other intracellular pathogens, similarly stimulate signal transduction pathways, including tyrosine phosphorylation of host proteins involved in rearrangements of the actin skeleton to promote entry. This chapter talks about intracellular development. Intracellular parasites have evolved diverse strategies for evasion of host cellular defense mechanisms associated with adaptations for survival in distinct intracellular compartments. The chapter discusses effects of the host cell. It is essential that chlamydiae maintain the integrity of the host cell for the duration of their intracellular growth because they are obligate intracellular parasites.

Citation: Hackstadt T. 1999. Cell Biology, p 101-138. In Stephens R (ed), Chlamydia. ASM Press, Washington, DC. doi: 10.1128/9781555818203.ch5
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

The developmental cycle. Infection is initiated by EBs. Immediately after endocytosis, EBs are found within tightly associated membrane vesicles (0 Hr). Within a few hours, EBs differentiate into the larger, metabolically active RBs (2 Hr). As the chlamydiae multiply, the inclusion increases in size to accommodate the multiplying bacteria. RBs are typically observed juxtaposed to the inclusion membrane (18 Hr). As the infection progresses, increasing numbers of chlamydiae are observed unattached in the interior of the inclusion (36 Hr). These unattached organisms are, for the most part, EBs and intermediate developmental forms. EBs accumulate within the inclusion even as RBs, still associated with the inclusion membrane, continue to multiply until the cell lyses at 40 to 48 h postinfection. Reprinted from with permission.

Citation: Hackstadt T. 1999. Cell Biology, p 101-138. In Stephens R (ed), Chlamydia. ASM Press, Washington, DC. doi: 10.1128/9781555818203.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Models of the vesicular interactions of the chlamydial inclusion before (early inclusion) (A) and after (mature inclusion) (B) modification of the host's response as a result of chlamydial polypeptide synthesis. Endocytosed EBs are internalized into a vesicle that displays minimal interaction with the endocytic pathway and is very restricted in its fusion with lysosomes. No interaction with vesicles delivering sphingomyelin or ceramide is initiated. EBs prevented from modifying the vesicle by inhibitors of chlamydial transcription or translation remain within this vesicle and are eventually degraded within lysosomes. By 2 h postinfection, in a process that requires early protein synthesis, actively transforms the properties of the nascent inclusion. Once these modifications have occurred, the inclusion is believed to exhibit the properties of a mature inclusion. Plasma membrane markers, fluid-phase markers, markers for early (transferrin and transferring receptor) and late (cation-independent mannose-6-phosphate receptor) endosomes, or lysosomes (acid phosphatase, cathepsin D, lysosomal glycoproteins, or the vacuolar H-ATPase) are not associated with the chlamydial inclusion. Instead, the chlamydial inclusion fuses with a subset of sphingomyelin-containing vesicles in transit to the plasma membrane. Fusion of these vesicles exposes the sphingomyelin on the luminal surface of the inclusion membrane from which it is adsorbed by the chlamydiae and incorporated into their cell walls.

Citation: Hackstadt T. 1999. Cell Biology, p 101-138. In Stephens R (ed), Chlamydia. ASM Press, Washington, DC. doi: 10.1128/9781555818203.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Alexander, J. J. 1968. Separation of protein synthesis in meningopneumonitis agent from that in L cells by differential susceptibility to cycloheximide. J. Bacteriol 95:327332.
2. Allan, I.,, and J. H. Pearce. 1987. Association of Chlamydia trachomatis with mammalian and cultured insect cells lacking putative chlamydial receptors. Microb. Pathog. 2:6370.
3. Allen, J. E.,, M. C. Cerrone,, P. R. Beatty,, and R. S. Stephens. 1990. Cysteine-rich outer membrane proteins of Chlamydia trachomatis display compensatory sequence changes between biovariants. Mol. Microbiol. 4:15431550.
4. Banks, J.,, B. Eddie,, J. Schachter,, and K. F. Meyer. 1970. Plaque formation by Chlamydia in L cells. Infect. Immun. 1:259262.
5. Bannantine, J. P.,, D. D. Rockey,, and T. Hackstadt. 1998. Tandem genes of Chlamydia psittaci that encode proteins localized to the inclusion membrane. Mol. Microbiol. 28:10171026.
6. Barnewall, R. E.,, Y. Rikihisa,, and E. H. Lee. 1997. Ehrlichia chaffeensis inclusions are early endosomes which selectively accumulate transferrin receptor. Infect. Immun. 65:14551461.
7. Barry, C. E., III,, T. J. Brickman,, and T. Hackstadt. 1993. Hcl-mediated effects on DNA structure: a potential regulator of chlamydial development. Mol. Microbiol. 9:273283.
8. Barry, C. E., III,, S. F. Hayes,, and T. Hackstadt 1992. Nucleoid condensation in Escherichia coli that express a chlamydial histone homolog. Science 256:377379.
9. Baseman, J. B.,, and E. C. Hayes. 1980. Molecular characterization of receptor binding proteins and immunogens of virulent Treponema pallidum. J. Exp. Med. 151:573586.
10. Batteiger, B. E.,, W. J. Newhall V,, and R. B. Jones. 1985. Differences in outer membrane proteins of the lymphogranuloma venereum and trachoma biovars of Chlamydia trachomatis. Infect. Immun. 50:488494.
11. Bavoil, P.,, A. Ohlin,, and J. Schachter. 1984. Role of disulfide bonding in outer membrane structure and permeability in Chlamydia trachomatis. Infect. Immun. 44:479485.
12. Bavoil, P. M.,, and R. C. Hsia. 1998. Type HI secretion in Chlamydia: a case of deja vu? Mol. Microbiol. 28:859862.
13. Becker, Y.,, E. Hochberg,, and Z. Zakay-Rones. 1969. Interaction of trachoma elementary bodies with host cells. Isr. J. Med. Sci. 5:121124.
14. Birkelund, S.,, H. Johnsen,, and G. Christiansen. 1994. Chlamydia trachomatis serovar L2 induces protein tyrosine phosphorylation during uptake by HeLa cells. Infect. Immun. 62:49004908.
15. Birkelund, S.,, K. Knudsen,, A. Madsen,, E. Falk,, P. Mygind,, and G. Christiansen,. 1998. Differential expression of Chlamydia pneumoniae Omp4 and Omp5 after infection of C57-black mice, p. 275282. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, R. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
16. Blyth, W. A.,, and J. Taverne. 1974. Cultivation of TRIC agents: a comparison between the use of BHK-21 and irradiated McCoy cells. J. Hyg. 72:121128.
17. Bose, S. K.,, and P. C. Goswami. 1986. Host modification of the adherence properties of Chlamydia trachomatis. J. Gen. Microbiol. 132:16311639.
18. Bose, S. K.,, and H. Liebhaber. 1979. Deoxyribonucleic acid synthesis, cell cycle progression, and division of Chlamydia-infected HeLa 229 cells. Infect. Immun. 24:953957.
19. Bose, S. K.,, and R. G. Paul. 1982. Purification of Chlamydia trachomatis lymphogranuloma venereum elementary bodies and their interaction with HeLa cells. J. Gen. Microbiol. 128:13711379.
20. Bose, S. K.,, G. B. Smith,, and R. G. Paul. 1983. Influence of lectins, hexoses, and neuraminidase on the association of purified elementary bodies of Chlamydia trachomatis UW-31 with HeLa cells. Infect. Immun. 40:10601067.
21. Brickman, T. J.,, C. E. Barry HI,, and T. Hackstadt. 1993. Molecular cloning and expression of hctB encoding a strain-variant chlamydial histone-like protein with DNA-binding activity. J. Bacteriol. 175:42744281.
22. Burgoyne, R. D.,, and M. J. Clague. 1994. Annexins in the endocytic pathway. Trends Biochem. Sci. 19:231232.
23. Byrne, G. I. 1976. Requirements for ingestion of Chlamydia psittaci by mouse fibroblasts (L cells). Infect. Immun. 14:645651.
24. Byrne, G. I. 1978. Kinetics of phagocytosis of Chlamydia psittaci by mouse fibroblasts (L cells): separation of the attachment and ingestion stages. Infect. Immun. 19:607612.
25. Byrne, G. I.,, and J. W. Moulder. 1978. Parasite-specified phagocytosis of Chlamydia psittaci and Chlamydia trachomatis by L and HeLa cells. Infect. Immun. 19:598606.
26. Caldwell, H. D.,, J. Kromhout,, and J. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31:11611176.
27. Caldwell, H. D.,, and J. Schachter. 1982. Antigenic analysis of the major outer membrane protein of Chlamydia spp. Infect. Immun. 35:10241031.
28. Cevenini, R.,, M. Donati,, E. Brocchi,, F. De Simone,, and M. La Placa. 1991. Partial characterization of an 89-kDa highly immunoreactive protein from Chlamydia psittaci A/22 causing ovine abortion. FEMS Microbiol Lett. 81:111116.
29. Chen, J. C.,, and R. S. Stephens. 1997. Chlamydia trachomatis glycosaminoglycan-dependent and independent attachment to eukaryotic cells. Microb. Pathog. 22:2330.
30. Chen, J. C.-R.,, J. P. Zhang,, and R. S. Stephens. 1996. Structural requirements of heparin binding to Chlamydia trachomatis. J. Biol. Chem. 271:1113411140.
31. Chi, E. Y.,, C.-C. Kuo,, and J. T. Grayston. 1987. Unique ultrastructure in the elementary body of Chlamydia sp. strain TWAR. J. Bacteriol. 169:37573763.
32. Christiansen, G.,, L. B. Pedersen,, J. E. Koehler,, A. G. Lundemose,, and S. Birkelund. 1993. Interaction between the Chlamydia trachomatis histone HI-like protein (Hc1) and DNA. J. Bacteriol. 175:17851795.
33. Clausen, J. D.,, G. Christiansen,, H. U. Hoist,, and S. Birkelund. 1997. Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol. Microbiol. 25:441449.
34. Clemens, D. L. 1996. Characterization of the Mycobacterium tuberculosis phagosome. Trends Microbiol. 4:113118.
35. Collett, B. A.,, W. J. Newhall V,, R. A. Jersild, Jr.,, and R. B. Jones. 1989. Detection of surface-exposed epitopes on Chlamydia trachomatis by immune electron microscopy. J. Gen. Microbiol. 135:8594.
36. Creutz, C. E. 1992. The annexins and exocytosis. Science 258:924931.
37. Croy, T. R.,, C.-C. Kuo,, and S.-P. Wang. 1975. Comparative susceptibility of eleven mammalian cell lines to infection with trachoma organisms. J. Clin. Microbiol. 1:434439.
38. Davis, C. H.,, and P. B. Wyrick. 1997. Differences in the association of Chlamydia trachomatis serovar E and serovar L2 with epithelial cells in vitro may reflect biological differences in vivo. Infect. Immun. 65:29142924.
39. Dehio, C.,, M.-C. Prevost,, and P. J. Sansonetti. 1995. Invasion of epithelial cells by Shigella flexneri induces tyrosine phosphorylation of cortactin by a pp60c-src-mediated signalling pathway. EMBO J. 14:24712482.
40. Desai, S. A.,, D. J. Krogstad,, and E. W. McClesky. 1993. A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362:643646.
41. Eissenberg, L. G.,, and P. B. Wyrick. 1981. Inhibition of phagolysosome fusion is localized to Chlamydia psittaci-XaAzn vacuoles. Infect. Immun. 32:889896.
42. Eissenberg, L. G.,, P. B. Wyrick,, C. H. Davis,, and J. W. Rumpp. 1983. Chlamydia psittaci elementary body envelopes: ingestion and inhibition of phagolysosome fusion. Infect. Immun. 40:741751.
43. Everett, K. D.,, A. A. Andersen,, M. Plaunt,, and T. P. Hatch. 1991. Cloning and sequence analysis of the major outer membrane protein gene of Chlamydia psittaci 6BC. Infect. Immun. 59:28532855.
44. Falkow, S.,, R. R. Isberg,, and D. A. Portnoy. 1992. The interaction of bacteria with mammalian cells. Annu. Rev. Cell Biol. 8:333363.
45. Fan, T.,, H. Lu,, H. Hu,, L. Shi,, G. McClarty,, D. Nance,, A. Greenberg,, and G. Zhong. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187:487496.
46. Fawaz, F. S.,, C. van Ooij,, E. Homola,, S. C. Mutka,, and J. N. Engel. 1997. Infection with Chlamydia trachomatis alters the tyrosine phosphorylation and/or localization of several host cell proteins including cortactin. Infect. Immun. 65:53015308.
47. Finlay, B. B.,, and P. Cossart. 1997. Exploitation of mammalian host cell functions by bacterial pathogens. Science 276:718725.
48. Friis, R. R. 1972. Interaction of L cells and Chlamydia psittaci: entry of the parasite and host responses to its development. J. Bacteriol. 110:706721.
49. Furness, G.,, D. M. Graham,, and P. Reeve. 1960. The titration of trachoma and inclusion blennorrhoea viruses in cell cultures. J. Gen. Microbiol. 23:613619.
50. Garcia-del Portillo, F.,, and B. B. Finlay. 1995. The varied lifestyles of intracellular pathogens within eukaryotic vacuolar compartments. Trends Microbiol. 3:373380.
51. Gennis, R. B. 1989. Biomembranes: Molecular Structure and Function. Springer-Verlag KG, Berlin, Germany.
52. Gill, S. D.,, and R. B. Stewart. 1970. Respiration of L cells infected with Chlamydia psittaci. Can. J. Microbiol. 16:10331039.
53. Grimwood, J.,, W. P. Mitchell,, and R. S. Stephens,. 1998. Phylogenetic analysis of a multigene family conserved between Chlamydia trachomatis and Chlamydia pneumoniae, p. 263266. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, P. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
54. Gutierrez-Martin, C. B.,, R. Hsia,, R. Hellio,, R. M. Bavoil,, and A. Dautry-Varsat. 1997. Heparin-mediated inhibition of Chlamydia psittaci adherence to HeLa cells. Microb. Pathog. 22:4757.
55. Hackstadt, T. 1986. Identification and properties of chlamydial polypeptides that bind eukaryotic cell surface components. J. Bacteriol. 165:1320.
56. Hackstadt, T. 1998. The diverse habitats of obligate intracellular parasites. Curr. Opin. Microbiol. 1: 8287.
57. Hackstadt, T., W, Baehr, and Y. Yuan. 1991. Chlamydia trachomatis developmental^ regulated protein is homologous to eukaryotic histone H1. Proc. Natl. Acad. Sci. USA 88:39373941.
58. Hackstadt, T.,, and H. D. Caldwell. 1985. Effect of proteolytic cleavage of surface-exposed proteins on infectivity of Chlamydia trachomatis. Infect. Immun. 48:546551.
59. Hackstadt, T.,, E. R. Fischer,, M. A. Scidmore,, D. D. Rockey,, and R. A. Heinzen. 1997. Origins and functions of the chlamydial inclusion. Trends Microbiol. 5:288293.
60. Hackstadt, T.,, D. D. Rockey,, R. A. Heinzen,, and M. A. Scidmore. 1996. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 15:964977.
61. Hackstadt, T.,, M. A. Scidmore,, and D. D. Rockey. 1995. Lipid metabolism in Chlamydia trachomatis infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. USA 92:48774881.
62. Hackstadt, T.,, M. Scidmore-Carlson,, and E. Fischer,. 1998. Rapid dissociation of the Chlamydia trachomatis inclusion from endocytic compartments, p. 127130. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, R. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
63. Hackstadt, T.,, W. J. Todd,, and H. D. Caldwell. 1985. Disulfide-mediated interactions of the chlamydial major outer membrane protein: role in the differentiation of chlamydiae. J. Bacteriol. 161:2531.
64. Hackstadt, T.,, and J. C. Williams. 1981. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc. Natl. Acad. Sci. USA 78:32403244.
65. Hatch, G. M.,, and G. McClarty. 1998. Cardiolipin remodeling in eukaryotic cells infected with Chlamydia trachomatis is linked to elevated mitochondrial metabolism. Biochem. Biophys. Res. Commun. 243:356360.
66. Hatch, T. P. 1975a. Competition between Chlamydia psittaci and L cells for host isoleucine pools: a limiting factor in chlamydial multiplication. Infect. Immun. 12:211220.
67. Hatch, T. P. 1975b. Utilization of L-cell nucleoside triphosphates by Chlamydia psittaci for ribonucleic acid synthesis. J. Bacteriol. 122:393400.
68. Hatch, T. P.,, E. Al-Hossainy,, and J. A. Silverman. 1982. Adenine nucleotide and lysine transport in Chlamydia psittaci. J. Bacteriol. 150:662670.
69. Hatch, T. P.,, I. Allan,, and J. H. Pearce. 1984. Structural and polypeptide differences between envelopes of infective and reproductive life cycle forms of Chlamydia spp. J. Bacteriol. 157:1320.
70. Hatch, T. P.,, M. Miceli,, and J. A. Silverman. 1985. Synthesis of protein in host-free reticulate bodies of Chlamydia psittaci and Chlamydia trachomatis. J. Bacteriol. 162:938942.
71. Hatch, T. P.,, M. Miceli,, and J. E. Sublett. 1986. Synthesis of disulfide-bonded outer membrane proteins during the developmental cycle of Chlamydia psittaci and Chlamydia trachomatis. J. Bacteriol. 165:379385.
72. Hatch, T. P.,, D. W. Vance, Jr.,, and E. Al-Hossainy. 1981. Attachment of Chlamydia psittaci to formaldehyde-fixed and unfixed L cells. J. Gen. Microbiol. 125:273283.
73. Heinzen, R. A.,, and T. Hackstadt. 1997. The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low molecular weight compounds. Infect. Immun. 65:10881094.
74. Heinzen, R. A.,, M. A. Scidmore,, D. D. Rockey,, and T. Hackstadt. 1996. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect. Immun. 64:796809.
75. Higashi, N. 1955. Electron microscopic studies on the mode of reproduction of trachoma virus and psittacosis virus in cell cultures. Exp. Mol. Pathol. 4:2439.
76. Hodinka, R. L.,, C. H. Davis,, J. Choong,, and P. B. Wyrick. 1988. Ultrastructural study of endocytosis of Chlamydia trachomatis by McCoy cells. Infect. Immun. 56:14561463.
77. Hodinka, R. L.,, and P. B. Wyrick. 1986. Ultrastructural study of mode of entry of Chlamydia psittaci into L-929 cells. Infect. Immun. 54:855863.
78. Hsia, R. C.,, Y. Pannekoek,, E. Ingerowski,, and P. M. Bavoil. 1997. Type III secretion genes identify a putative virulence locus of Chlamydia. Mol. Microbiol. 25:351359.
79. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379433.
80. Jackson, R. L.,, S. J. Busch,, and A. D. Cardin. 1991. Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev. 71:481539.
81. Joiner, K. A.,, S. A. Fuhrman,, H. M. Miettinen,, L. H. Kasper,, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249:641646.
82. Joseph, T. D.,, and S. K. Bose. 1991a. Further characterization of an outer membrane protein of Chlamydia trachomatis with cytadherence properties. FEMS Microbiol. Lett. 84:167172.
83. Joseph, T. D.,, and S. K. Bose. 1991b. A heat-labile protein of Chlamydia trachomatis binds to HeLa cells and inhibits the adherence of chlamydiae. Proc. Natl. Acad. Sci. USA 88:40544058.
84. Klausner, R. D.,, J. G. Donaldson,, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:10711080.
85. Koval, M.,, and R. E. Pagano. 1991. Intracellular transport and metabolism of sphingomyelin. Biochim. Biophys. Acta 1082:113125.
86. Kraaipoel, R. J.,, and A. M. van Duin. 1979. Isoelectric focusing of Chlamydia trachomatis. Infect. Immun. 26:775778.
87. Krause, D. C.,, and J. B. Baseman. 1982. Mycoplasma pneumoniae proteins that selectively bind to host cells. Infect. Immun. 37:382386.
88. Krivan, H. C.,, B. Nilsson,, C. A. Lingwood,, and H. Ryu. 1991. Chlamydia trachomatis and Chlamydia pneumoniae bind specifically to phosphatidylethanolamine in HeLa cells and to GALNACbetal-4GALbetal-4GLC sequences found in asialo-gml and asialo-gm2. Biochem. Biophys. Res. Commun. 175:10821089.
89. Kubo, A.,, and R. Stephens,. 1998. Temporal differences in transcription of type III secretion genes during the Chlamydia trachomatis developmental cycle, p. 539542. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, P. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
90. Kubori, T.,, Y. Matsushima,, D. Nakamura,, J. Uralil,, M. Lara-Tejero,, A. Sukhan,, J. E. Galan,, and S. I. Aizawa. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602605.
91. Kuo, C.,, N. Takahashi,, A. F. Swanson,, Y. Ozeki,, and S. Hakomori. 1996. An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J. Clin. Invest. 98:28132818.
92. Kuo, C.-C.,, E. Y. Chi,, and J. T. Grayston. 1988. Ultrastructural study of entry of Chlamydia strain TWAR into HeLa cells. Infect. Immun. 56:16681672.
93. Kuo, C.-C.,, and J. T. Grayston. 1976. Interaction of Chlamydia trachomatis organisms and HeLa 229 cells. Infect. Immun. 13:11031109.
94. Kuo, C.-C.,, S.-P. Wang,, and J. T. Grayston. 1972. Differentiation of TRIC and LGV organisms based on enhancement of infectivity by DEAE-dextran in cell culture. J. Infect. Dis. 125:313317.
95. Kuo, C-C.,, S.-P. Wang,, and J. T. Grayston. 1973. Effect of polycations, polyanions, and neuraminidase on the infectivity of trachoma-inclusion conjunctivitis and lymphogranuloma venereum organisms in HeLa cells: sialic acid residues as possible receptors for trachoma-inclusion conjunctivitis. Infect. Immun. 8:7479.
96. Lawn, A. M.,, W. A. Blyth,, and J. Taverne. 1973. Interactions of TRIC agents with macrophages and BHK-21 cells observed by electron microscopy. J. Hyg. 71:515532.
97. Lechner, J.,, and F. Wieland. 1989. Structure and biosynthesis of prokaryotic glycoproteins. Annu. Rev. Biochem. 58:173194.
98. Lee, C. K. 1981. Interaction between a trachoma strain of Chlamydia trachomatis and mouse fibroblasts (McCoy cells) in the absence of centrifugation. Infect. Immun. 31:584591.
99. Levy, N. J. 1979. Wheat germ agglutinin blockage of chlamydial attachment sites: antagonism by N-acetyl-D-glucosamine. Infect. Immun. 25:946953.
100. Levy, N. J.,, and J. W. Moulder. 1982. Attachment of cell walls of Chlamydia psittaci to mouse fibroblasts (L cells). Infect. Immun. 37:10591065.
101. Lindquist, E.,, and R. Stephens,. 1998. Transcriptional activity of a sequence variable protein family in Chlamydia trachomatis, p. 259262. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, P. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
102. Lipsky, N. G.,, and R. E. Pagano. 1985a. Intracellular translocation of fluorescent sphingolipids in cultured fibroblasts: endogenously synthesized sphingomyelin and glucocerebroside analogues pass through the Golgi apparatus en route to the plasma membrane. J. Cell Biol. 100:2734.
103. Lipsky, N. G.,, and R. E. Pagano. 1985b. A vital stain for the Golgi apparatus. Science 228:745747.
104. Longbottom, D.,, J. Findlay,, E. Vretou,, and S. M. Dunbar. 1998a. Immunoelectron microscopic localisation of the OMP90 family on the outer membrane surface of Chlamydia psittaci. FEMS Microbiol. Lett. 164:111117.
105. Longbottom, D.,, M. Russell,, S. M. Dunbar,, G. E. Jones,, and A. J. Herring. 1998b. Molecular cloning and characterization of the genes coding for the highly immunogenic cluster of 90-kilodalton envelope proteins from the Chlamydia psittaci subtype that causes abortion in sheep. Infect. Immun. 66:13171324.
106. Lundemose, A. G.,, S. Birkelund,, P. M. Larsen,, S. J. Fey,, and G. Christiansen. 1990. Characterization and identification of early proteins in Chlamydia trachomatis serovar L2 by two-dimensional gel electrophoresis. Infect. Immun. 58:24782486.
107. Majeed, M.,, J. D. Ernst,, K. E. Magnusson,, E. Kihlstrom,, and O. Stendahl. 1994. Selective translocation of annexins during intracellular redistribution of Chlamydia trachomatis in HeLa and McCoy cells. Infect. Immun. 62:126134.
108. Majeed, M.,, M. Gustafsson,, E. Kihlstrom,, and O. Stendahl. 1993. Roles of Ca2+ and F-actin in intracellular aggregation of Chlamydia trachomatis in eukaryotic cells. Infect. Immun. 61:14061414.
109. Majeed, M.,, and E. Kihlstrom. 1991. Mobilization of F-actin and clathrin during redistribution of Chlamydia trachomatis to an intracellular site in eukaryotic cells. Infect. Immun. 59:44654472.
110. Matsumoto, A. 1981. Isolation and electron microscopic observations of intracytoplasmic inclusions containing Chlamydia psittaci. J. Bacteriol. 145:605612.
111. Matsumoto, A., 1988. Structural characteristics of chlamydial bodies, p. 2145. In A. L. Barron (ed.), Microbiology of Chlamydia. CRC Press, Boca Raton, Fla.
112. Matsumoto, A.,, I. Bessho,, K. Uchira,, and T. Suda. 1991. Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J. Electron Microsc. 40:356363.
113. Matsumoto, A.,, H. Izutsu,, N. Miyashita,, and M. Ohuchi. 1998. Plaque formation by and plaque cloning of Chlamydia trachomatis biovar trachoma. J. Clin. Microbiol. 36:30133019.
114. McBride, T.,, and E. Wilde III,. 1990. Intracellular translocation of Chlamydia trachomatis, p. 3639. In W. R. Bowie,, H. D. Caldwell,, R. P. Jones,, P.-A. Mardh,, G. L. Ridgway,, J. Schachter,, W. E. Stamm,, and M. E. Ward (ed.), Chlamydial Infections. Cambridge University Press, Cambridge, United Kingdom.
115. McClarty, G. 1994. Chlamydiae and the biochemistry of intracellular parasitism. Microbiology 2:157164.
116. McClarty, G.,, and G. Tipples. 1991. In situ studies on incorporation of nucleic acid precursors into Chlamydia trachomatis DNA. J. Bacteriol. 173:49224931.
117. Misumi, Y.,, A. Miki,, A. Takatsuki,, G. Tamura,, and Y. Ikehara. 1986. Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 261:1139811403.
118. Moulder, J. W. 1970. Glucose metabolism of L cells before and after infection with Chlamydia psittaci. J. Bacteriol. 104:11891196.
119. Moulder, J. W. 1974. Intracellular parasitism: life in an extreme environment. J. Infect. Dis. 130:300306.
120. Moulder, J. W. 1985. Comparative biology of intracellular parasitism. Microbiol. Rev. 49:298337.
121. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143190.
122. Moulder, J. W.,, T. P. Hatch,, G. I. Byrne,, and K. R. Kellogg. 1976. Immediate toxicity of high multiplicities of Chlamydia psittaci for mouse fibroblasts (L cells). Infect. Immun. 14:277289.
123. Mukkada, A. J.,, J. C. Meade,, T. A. Glaser,, and P. F. Bonventre. 1985. Enhanced metabolism of Leishmania donovani amastigotes at acid pH: an adaptation for intracellular growth. Science 229: 10991101.
124. Murray, A.,, and M. E. Ward. 1984. Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: the role of calmodulin. J. Gen. Microbiol. 130:193201.
125. Newhall, W. J. V.,, and R. B. Jones. 1983. Disulfide-linked oligomers of the major outer membrane protein of chlamydiae. J. Bacteriol. 154:9981001.
126. Nichols, B. A.,, P. Y. Setzer,, F. Pang,, and C. R. Dawson. 1985. New view of the surface projections of Chlamydia trachomatis. J. Bacteriol. 164:344349.
127. Ojcius, D. M.,, H. Degani,, J. Mispelter,, and A. Dautry-Varsat. 1998. Enhancement of ATP levels and glucose metabolism during an infection by Chlamydia. NMR studies of living cells. J. Biol. Chem. 273:70527058.
128. Ojcius, D. M.,, R. Hellio,, and A. Dautry-Varsat. 1997. Distribution of endosomal, lysosomal, and major histocompatibility complex markers in a monocytic cell line infected with Chlamydia psittaci. Infect. Immun. 65:24372442.
129. Pagano, R. E.,, and K. J. Longmuir. 1985. Phosphorylation, transbilayer movement, and facilitated intracellular transport of diacylglycerol are involved in the uptake of a fluorescent analog of phosphatide acid by cultured fibroblasts. J. Biol. Chem. 260:19091916.
130. Pagano, R. E.,, M. A. Sepanski,, and O. C. Martin. 1989. Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy. J. Cell Biol. 109:20672079.
131. Perara, E.,, D. Ganem,, and J. N. Engel. 1992. A developmentally regulated chlamydial gene with apparent homology to eukaryotic histone HI. Proc. Natl. Acad. Sci. USA 89:21252129.
132. Perara, E.,, T. S. Yen,, and D. Ganem. 1990. Growth of Chlamydia trachomatis in enucleated cells. Infect. Immun. 58:38163818.
133. Peterson, E. M.,, and L. M. de la Maza. 1988. Chlamydia parasitism: ultrastructural characterization of the interaction between the chlamydial cell envelope and the host cell. J. Bacteriol. 170:13891392.
134. Pfeffer, S. R.,, and J. E. Rothman. 1987. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu. Rev. Biochem. 56:829852.
135. Plaunt, M. R.,, and T. P. Hatch. 1988. Protein synthesis early in the developmental cycle of Chlamydia psittaci. Infect. Immun. 56:30213025.
136. Prain, C. J.,, and J. H. Pearce. 1989. Ultrastructural studies on the intracellular fate of Chlamydia psittaci (strain guinea pig inclusion conjunctivitis) and Chlamydia trachomatis (strain lymphogranuloma venereum 434): modulation of intracellular events and relationship with endocytic mechanism. J. Gen. Microbiol. 135:21072123.
137. Raulston, J. E. 1997. Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect. Immun. 65:45394547.
138. Raulston, J. E.,, C. H. Davis,, T. R. Paul,, and P. B. Wyrick,. 1998. Heat shock protein 70 kDa and the chlamydial envelope: an entry-level position, p. 8386. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, P. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
139. Raulston, J. E.,, C. H. Davis,, D. H. Schmiel,, M. W. Morgan,, and P. B. Wyrick. 1993. Molecular characterization and outer membrane association of a Chlamydia trachomatis protein related to the Hsp70 family of proteins. J. Biol. Chem. 268:2313923147.
140. Reynolds, D. J.,, and J. H. Pearce. 1990. Characterization of the cytochalasin D-resistant (pinocytic) mechanisms of endocytosis utilized by chlamydiae. Infect. Immun. 58:32083216.
141. Ridderhof, J. C.,, and R. C. Barnes. 1989. Fusion of inclusions following superinfection of HeLa cells by two serovars of Chlamydia trachomatis. Infect. Immun. 57:31893193.
142. Rockey, D. D.,, D. Grosenbach,, D. E. Hruby,, M. G. Peacock,, R. A. Heinzen,, and T. Hackstadt. 1997. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol. Microbiol. 24:217228.
143. Rockey, D. D.,, R. A. Heinzen,, and T. Hackstadt. 1995. Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized to the inclusion membrane of infected cells. Mol. Microbiol. 15:617626.
144. Rockey, D. D.,, and J. L. Rosquist. 1994. Protein antigens of Chlamydia psittaci present in infected cells but not detected in the infectious elementary body. Infect. Immun. 62:106112.
145. Rosenwald, A. G.,, and R. E. Pagano. 1993. Intracellular transport of ceramide and its metabolites at the Golgi complex: insights from short-chain analogs. Adv. Lipid Res. 26:101118.
146. Rostand, K. S.,, and J. D. Esko. 1997. Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65:18.
147. Russell, D. G. 1996. Mycobacterium and Leishmanial stowaways in the endosomal network. Trends Cell Biol. 5:125128.
148. Schechter, E. M. 1966. Synthesis of nucleic acid and protein in L cells infected with the agent of meningopneumonitis. J. Bacteriol. 91:20692080.
149. Schmiel, D. H.,, S. T. Knight,, J. E. Raulston,, J. Choong,, C. H. Davis,, and P. B. Wyrick. 1991. Recombinant Escherichia coli clones expressing Chlamydia trachomatis gene products attach to human endometrial epithelial cells. Infect. Immun. 59:40014012.
150. Schramm, N.,, C. R. Bagnell,, and P. B. Wyrick. 1996. Vesicles containing Chlamydia trachomatis serovar L2 remain above pH 6 within HEC-1B cells. Infect. Immun. 64:12081214.
151. Schramm, N.,, and P. B. Wyrick. 1995. Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect. Immun. 63:324332.
152. Schwab, J. C.,, C. J. M. Beckers,, and K. A. Joiner. 1994. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc. Natl. Acad. Sci. USA 91:509513.
153. Schwarzmann, G.,, and K. Sandhoff. 1990. Metabolism and intracellular transport of glycosphingolipids. Biochemistry 29:1086510871.
154. Scidmore, M. A.,, E. R. Fischer,, and T. Hackstadt. 1996a. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J. Cell Biol. 134:363374.
155. Scidmore, M. A.,, and T. Hackstadt. 1995. Ability of Chlamydia trachomatis to obtain iron from transferrin, abstr. D-161, p. 277. In Abstracts of the 95th General Meeting of the American Society for Microbiology 1995. American Society for Microbiology, Washington, D.C..
156. Scidmore, M. A.,, D. D. Rockey,, E. R. Fischer,, R. A. Heinzen,, and T. Hackstadt. 1996b. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect. Immun. 64:53665372.
157. Scidmore-Carlson, M.,, E. I. Shaw,, C. A. Dooley,, and T. Hackstadt 1998,. Identification and characterization of putative Chlamydia trachomatis inclusion membrane proteins, p. 103106. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, P. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
158. Shainkin-Kestenbaum, R.,, Y. Winikoff,, R. Kol,, C. Chaimovitz,, and I. Sarov. 1989. Inhibition of growth of Chlamydia trachomatis by the calcium antagonist verapamil. J. Gen. Microbiol. 135:16191623.
159. Sinai, A. P.,, and K. A. Joiner. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51:415462.
160. Sinai, A. P.,, P. Webster,, and K. A. Joiner. 1997. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J. Cell Sci. 110:21172128.
161. Small, P. L., C. L. Ramakrishnan,, and S. Falkow. 1994. Remodeling schemes of intracellular pathogens. Science 263:637639.
162. Sneddon, J. M.,, and W. M. Wenman. 1985. The effect of ions on the adhesion and internalization of Chlamydia trachomatis by HeLa cells. Can. J. Microbiol. 31:371374.
163. Soderlund, G.,, and E. Kihlstrom. 1982. Physicochemical surface properties of elementary bodies from different serotypes of Chlamydia trachomatis and their interaction with mouse fibroblasts. Infect. Immun. 36:893899.
164. Soderlund, G.,, and E. Kihlstrom. 1983a. Attachment and internalization of a Chlamydia trachomatis lymphogranuloma venereum strain by McCoy cells: kinetics of infectivity and effect of lectins and carbohydrates. Infect. Immun. 42:930935.
165. Soderlund, G.,, and E. Kihlstrom. 1983b. Effect of methylamine and monodansylcadaverine on the susceptibility of McCoy cells to Chlamydia trachomatis infection. Infect. Immun. 40:534541.
166. Spears, P.,, and J. Storz. 1979. Biotyping of Chlamydia psittaci based on inclusion morphology and response to diethylaminoethyl-dextran and cycloheximide. Infect. Immun. 24:224232.
167. Stephens, R. S. 1993. Challenge of Chlamydia research. Infect. Agents Dis. 1:279293.
168. Stephens, R. S. 1994. Molecular mimicry and Chlamydia trachomatis infection of eukaryotic cells. Trends Microbiol. 2:99101.
169. Stephens, R. S.,, S. Kalman,, C. Lammel,, J. Fan,, R. Marathe,, L. Aravind,, W. Mitchell,, L. Olinger,, R. L. Tatusov,, Q. Zhao,, E. V. Koonin,, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754759.
170. Struyve, M.,, M. Moons,, and J. Tommassen. 1991. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218:141148.
171. Sturgill-Koszycki, S.,, U. E. Schaible,, and D. G. Russell. 1996. Mycobacterium-contaimng phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J. 15:69606968.
172. Su, H.,, and H. D. Caldwell. 1998. Sulfated polysaccharides and a synthetic sulfated polymer are potent inhibitors of Chlamydia trachomatis infectivity in vitro but lack protective efficacy in an in vivo murine model of chlamydial genital tract infection. Infect. Immun. 66:12581260.
173. Su, H.,, L. Raymond,, D. D. Rockey,, E. Fischer,, T. Hackstadt,, and H. D. Caldwell. 1996. A recombinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc. Natl. Acad. Sci. USA 93:1114311148.
174. Su, H.,, G. J. Spangrude,, and H. D. Caldwell. 1991. Expression of Fc gammaRHI on HeLa 229 cells: possible effect on in vitro neutralization of Chlamydia trachomatis. Infect. Immun. 59:38113814.
175. Su, H.,, N. G. Watkins,, Y.-X. Zhang,, and H. D. Caldwell. 1990. Chlamydia trachomatis-host cell interactions: role of the chlamydial major outer membrane protein as an adhesin. Infect. Immun. 58: 10171025.
176. Su, H.,, Y.-X. Zhang,, O. Barrera,, N. G. Watkins,, and H. D. Caldwell. 1988. Differential effect of trypsin on infectivity of Chlamydia trachomatis: loss of infectivity requires cleavage of major outer membrane protein variable domains II and IV. Infect. Immun. 56:20942100.
177. Swanson, A. F.,, and C.-C. Kuo. 1990. Identification of lectin-binding proteins in Chlamydia species. Infect. Immun. 58:502507.
178. Swanson, A. F.,, and C.-C. Kuo. 1991. Evidence that the major outer membrane protein of Chlamydia trachomatis is glycosylated. Infect. Immun. 59:21202125.
179. Swanson, A. F.,, and C.-C. Kuo. 1994a. The 32-kDa glycoprotein of Chlamydia trachomatis is an acidic protein that may be involved in the attachment process. FEMS Microbiol. Lett. 123:113118.
180. Swanson, A. F.,, and C-C. Kuo. 1994b. Binding of the glycan of the major outer membrane protein of Chlamydia trachomatis to HeLa cells. Infect. Immun. 62:2428.
181. Swanson, A. F.,, and C.-C. Kuo. 1996. The 18 kDa lectin-binding protein of Chlamydia trachomatis is different from the 18-kDa histone-like protein. FEMS Microbiol. Lett. 137:189192.
182. Tao, S.,, R. Kaul,, and W. M. Wenman. 1991. Identification and nucleotide sequence of a developmentally regulated gene encoding a eukaryotic histone HI-like protein from Chlamydia trachomatis. J. Bacteriol. 173:28182822.
183. Taraska, T.,, D. M. Ward,, R. S. Ajioka,, P. B. Wyrick,, S. R. Davis-Kaplan,, C. H. Davis,, and J. Kaplan. 1996. The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect. Immun. 64:37133727.
184. Ting, L.-M.,, R.-C. Hsia,, C. G. Haidaris,, and P. M. Bavoil. 1995. Interaction of outer envelope proteins of Chlamydia psittaci GPIC with the HeLa cell surface. Infect. Immun. 63:36003608.
185. Tipples, G.,, and G. McClarty. 1993. The obligate intracellular bacterium Chlamydia trachomatis is auxotrophic for three of the four ribonucleoside triphosphates. Mol. Microbiol. 8:11051114.
186. Todd, W. J.,, and H. D. Caldwell. 1985. The interaction of Chlamydia trachomatis with host cells: ultrastructural studies of the mechanism of release of a biovar II strain from HeLa 229 cells. J. Infect. Dis. 151:10371044.
187. van Meer, G.,, E. H. K. Stelzer,, R. W. Wijnaendts-van Resandt,, and K. Simons. 1987. Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells. J. Cell Biol. 105:16231635.
188. van Ooij, C.,, G. Apodaca,, and J. Engel. 1997. Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect. Immun. 65:758766.
189. van Ooij, C.,, S. van Ijzendoorn,, M. Nishijima,, K. Hanada,, K. Mostov,, and J. Engel,. 1998. Acquisition of host-derived sphingolipids are essential for the intracellular growth of Chlamydia trachomatis, p. 9194. In R. S. Stephens,, G. I. Byrne,, G. Christiansen,, I. N. Clarke,, J. T. Grayston,, R. G. Rank,, G. L. Ridgway,, R. Saikku,, J. Schachter,, and W. E. Stamm (ed.), Chlamydial Infections. Proceedings of the Ninth International Symposium on Human Chlamydial Infection. International Chlamydia Symposium, San Francisco, Calif..
190. Vretou, E.,, P. C. Goswami,, and S. K. Bose. 1989. Adherence of multiple serovars of Chlamydia trachomatis to a common receptor on HeLa and McCoy cells is mediated by thermolabile protein(s). J. Gen. Microbiol. 135:32293237.
191. Wagar, E. A.,, and R. S. Stephens. 1988. Developmental-form-specific DNA-binding proteins in Chlamydia spp. Infect. Immun. 56:16781684.
192. Ward, M. E.,, and A. Murray. 1984. Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: mechanisms of endocytosis. J. Gen. Microbiol. 130:17651780.
193. Ward, M. E.,, and H. S. Salari. 1980. Modulation of Chlamydia trachomatis infection by cyclic nucleotides and prostaglandins. FEMS Microbiol. Lett. 7:141143.
194. Ward, M. E.,, and H. Salari. 1982. Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: modulation by cyclic nucleotides, prostaglandins and calcium. J. Gen. Microbiol. 128:639650.
195. Watson, M. W.,, P. R. Lambden,, M. E. Ward,, and I. N. Clarke. 1989. Chlamydia trachomatis 60 kDa cysteine rich outer membrane protein: sequence homology between trachoma and LGV biovars. FEMS Microbiol Lett. 65:293298.
196. Wenman, W. M.,, and R. U. Meuser. 1986. Chlamydia trachomatis elementary bodies possess proteins which bind to eukaryotic cell membranes. J. Bacteriol. 165:602607.
197. Willingham, M. C.,, J. A. Hanover,, R. B. Dickson,, and I. Pastan. 1984. Morphologic characterization of the pathway of transferrin endocytosis and recycling in human KB cells. Proc. Natl. Acad. Sci. USA 81:175179.
198. Wylie, J. L.,, G. M. Hatch,, and G. McClarty. 1997. Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J. Bacteriol. 179:72337242.
199. Wyrick, P. B.,, and E. A. Brownridge. 1978. Growth of Chlamydia psittaci in macrophages. Infect. Immun. 19:10541060.
200. Wyrick, P. B.,, J. Choong,, C. H. Davis,, S. T. Knight,, M. O. Royal,, A. S. Maslow,, and C. R. Bagnell. 1989. Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect. Immun. 57:23782389.
201. Yong, E. C.,, E. Y. Chi,, and C.-C. Kuo. 1987. Differential antimicrobial activity of human mononuclear phagocytes against the human biovars of Chlamydia trachomatis. J. Immunol. 139:12971302.
202. Zeichner, S. L. 1983. Isolation and characterization of macrophage phagosomes containing infectious and heat-inactivated Chlamydia psittaci: two phagosomes with different intracellular behaviors. Infect. Immun. 40:956966.
203. Zhang, J. P.,, and R. S. Stephens. 1992. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell 69:861869.
204. Zhu, Z.,, M. D. Gershon,, R. Ambron,, C. Gabel,, and A. A. Gershon. 1995. Infection of cells by varicella zoster virus: inhibition of viral entry by mannose 6-phosphate and heparin. Proc. Natl. Acad. Sci. USA 92:35463550.
205. Zychlinsky, A.,, and P. J. Sansonetti. 1997. Apoptosis as a proinflammatory event: what can we learn from bacteria-induced cell death? Trends Microbiol. 5:201204.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error