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Chapter 20 : The Chlamydial Developmental Cycle

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Abstract:

This chapter describes an account of what was learned by the earliest and possibly most astute chlamydiologists, and then describes current molecular and cellular biology approaches that have expanded upon these early observations. Collectively, the chapter provides a picture of the developmental cycle, a process common to all chlamydial species but unique among prokaryotes. The central core of the developmental cycle is the alternating and complementary nature of the distinct developmental forms. Elementary bodies (EBs) are small coccoid electron-dense structures. The electron-dense center is bound by inner and outer membranes that have lipid compositions more similar to that of the infected host cell mitochondria than to those of other bacteria. Experiments with truncated Hc1 proteins localized the DNA binding domain to the region that had identity with H1 and showed that the amino-terminal region of the protein likely had an alternate function. The activation and subsequent multiplication of RBs leads to an accumulation of these developmental forms within the young and "middle-aged" inclusions. The recent completion of the genome sequence as well as the anticipated availability of genetic transformation techniques will likely speed up these investigations, leading to a thorough understanding of the developmental cycle.

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 1
FIGURE 1

Line drawing of a generalized chlamydial developmental cycle. Infection begins when an infectious but metabolically inactive EB comes in contact with a host cell (A) and is endocytosed (B). The phago-cytic vacuole (the inclusion) migrates toward the Golgi apparatus, and the EB differentiates into the noninfectious but metabolically active RB (C). RB division ensues, and the inclusion increases in size (D). Reticulate bodies then begin to reorganize back into EBs, and the inclusion grows until it occupies the entire cytoplasm of the infected cell (E). The inclusion lyses, the host cell lyses, and EBs are freed to infect another cell. While there are differences in this cycle among the different chlamydial strains and species, the general process is similar. N, nucleus.

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 2
FIGURE 2

Electron micrographs of the sequential changes from attachment of EBs to host cells through the division of RBs. These micrographs show Cal 10 infecting L929 cells. (A and B) 30 min p.i. Electrostatic and receptor-mediated adhesions between the EB and the cell can be observed. (C) 60 min p.i. Note the nucleoid structure and the apparent fusion of a tiny vesicle to the phagocyte. (D) 100 min p.i. Two developmental forms can be observed: a typical EB very soon after phagocytosis (top) and another located in the deeper cytoplasm. Note the larger size and apparent reorganization of the nucleoid. The images in panels C and D also represent the sequential change from the EB to intermediate body—a structure that is found both at the beginning and the end of the cycle. (E and F) 6 h p.i. The conversion from EBs to RBs is complete. At this point inclusions will be found in the region of the Golgi apparatus. Note the larger size of the RB in panel F. This may represent growth prior to the initial division process. (G) 8 h p.i. Note the RB constriction prior to binary fission and the fine comb-like structure on the right side of the RB. (H and I) 10 h p.i. Terminal stages of first division. Mitochondria can be seen in the vicinity of the inclusion, but not associated with the inclusion membrane. Magnification of all micrographs, X 60,000; bar in panel I = 1 μm.

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 3
FIGURE 3

Electron micrographs of the later stages of inclusion development in both C. and (A to C) Cal 10-infected L929 cells cultured at 37°C. (A) 18 h p.i.; (B) 24 h p.i.; (C) 34 h p.i. In each panel, note the relative numbers of RBs and EBs and the association between the inclusion and host cell mitochondria. (D to F) C. TW-183 in HEp-2 cells, cultured at 37°C. (D) 18 h p.i.; (E) 24 h p.i.; (F) 34 h p.i. Note the apparent lack of mitochondria! association, the more spherical nature of the inclusion, and the slight compression of the host nuclei. The inclusions in panels A, D, and E contain exclusively RBs, while the remaining panels show the asynchronous nature of the later inclusions. Bars = 1 μm.

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 4
FIGURE 4

Effects of detergents and reducing agents on the integrity of EB and RB developmental forms. In both panels the arrows point to the 60-kDa EnvB (Omp2) and the 12-kDa EnvA (Omp3) proteins, and the arrowhead points to the 40-kDa MOMP band. (A) Sodium dodecyl sulfate-polyacrylamide gel electro-phoresis (SDS-PAGE) profiles of insoluble residues of EBs and RBs after extraction with detergents plus or minus 2-mercaptoethanol (2-ME). Purified developmental forms were treated with the extracting agent and subjected to high-speed centrifugation. The material in the pellets was then prepared for standard PAGE. Lanes: 1, EB extracted with phosphate-buffered saline (PBS); 2, EBs extracted with Sarkosyl; 3, EBs extracted with SDS; 4, EBs extracted with SDS plus 2-ME; 5, RBs extracted with PBS; 6, RBs extracted with Sarkosyl; 7, RBs extracted with SDS; 8, RBs extracted with SDS plus 2-ME. Note the absence of detectable EnvA and EnvB in the RB preparations but the abundance of MOMP in both EBs and FU3s. (B) A similar experiment with EBs cultured in the presence of either [S]cysteine or [S]methionine. Purified EBs were then extracted with either PBS (lanes 1 and 2) or SDS (lanes 3 and 4). Insoluble material was collected by centrifugation and prepared for standard PAGE. The resulting gel was dried and exposed to film. The samples in lanes 1 and 3 represent EB labeled with [S]cysteine. The samples in lanes 2 and 4 represent EB labeled with [S]methionine. Note the distinction between detectable SDS-insoluble EB proteins under the two labeling conditions. (Data reproduced from , with permission of the authors and ASM.)

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 5
FIGURE 5

Morphologies of highly purified EBs fixed differently prior to thin sectioning. (A) EBs were doubly fixed with glutaraldehyde and OsO and embedded in Epon. Thin sections were doubly stained with uranylacetate and lead citrate solutions. Note the lack of visible surface projections. (B) EBs were fixed with glutaraldehyde and treated with tannic acid. The sections were examined without subsequent staining with uranylacetate and lead citrate. While the internal structures are not visible, the regular nature of the surface projections is clearly demonstrated. (C) Purified EBs were fixed with glutaraldehyde and treated with ruthenium red. Thin sections were then stained with uranyl acetate and lead citrate. Note that the surface projections are located only on the EB surface opposite the nucleoid structure. Magnifications of all micrographs, X 90,000. Bar (panel C) = 0.1 μm.

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 6
FIGURE 6

Freeze-etch micrographs of the external surfaces of chlamydial inclusions. (A) C. Cal 10 inclusion 16 h p.i. Note the surface projections enlarged in the inset (X76,000). (B) Similar micrograph of Cal 10 at 18 h p.i. Magnification, X 30,000. Bars = 1 μm (full-scale images) and 0.1 μm (inset).

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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Image of FIGURE 7
FIGURE 7

Aberrant RB forms produced during culture of L2/434/Bu in the presence of penicillin G (128 μg/ml). (A) Thin section of penicillin-treated, infected cells fixed 24 h p.i. Note the extremely large and vacuolated single RB within a spacious inclusion and the extra folds of membrane adjacent to the RB. (B) A higher magnification of the region of contact between the RB and the inclusion membrane (indicated by an arrow in panel A). Note the connections between the inclusion membrane and RB at the point of contact. (C) Freeze-etch preparation of a similar inclusion. Note the surface projections extending through the surface of the inclusion (arrowhead), as seen in Fig. 6 with normal inclusions. The effect of penicillin on is very similar to that seen with other chlamydiae.

Citation: Rockey D, Matsumoto A. 2000. The Chlamydial Developmental Cycle, p 403-425. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch20
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References

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1. Allan, I.,, T. P. Hatch,, and J. H. Pearce. 1985. Influence of cysteine deprivation on chlamydial differentiation from reproductive to infective life-cycle forms. J. Gen. Microbiol. 131: 3171 3177.
2. Baehr, W.,, Y.-X. Zhang,, T. Joseph,, H. Su,, F. E. Nano,, K. D. E. Everett,, and H. D. Caldwell. 1988. Mapping antigenic domains expressed by Chlamydia trachomatis major outer membrane protein genes. Proc. Nail. Acad. Sci. USA 85: 4000 4004.
3. Baghian, A.,, K. Kousoulas,, R. Truax,, and J. Storz. 1996. Specific antigens of Chlamydiapecorutn and their homologues in C. psittaci and C. trachomatis. Am.J. Vet. Res. 57: 1720 1725.
4. Bannantine, J. P.,, M. J. Parnell,, H. D. Caldwell,, and D. D. Rockey,. 1998a. Use of a primate model system for identification of Chlamydia trachomatis proteins recognized in the context of infection, p. 99 102. In R. S. Stephens et al. (ed.), Chlamydial Infections. International Chlamydia Symposium, San Francisco, Calif.
5. Bannantine, J. P.,, D. D. Rockey,, and T. Hackstadt. 1998b. Tandem genes of Chlamydia psittaci that encode proteins localized to the inclusion membrane. Mol. Microbiol. 28: 1017 1026.
6. Barry, C. E. III,, S. F. Hayes,, and T. Hackstadt. 1992. Nucleoid condensation in Escherichia coli that express a chlamydial histone homolog. Science 256: 377 379.
7. Barry, C. E. Ill,, T. J. Brickman,, and T. Hackstadt. 1993. Hc1-mediated effects on DNA structure: a potential regulator of chlamydial development. Mol. Miaobiol. 9: 273 283.
8. Baumann, M.,, L. Brade,, E. Fasske,, and H. Brade. 1992. Staining of surface antigens of Chlamydia trachomatis L2 in tissue culture. Infect. Immun. 60: 4433 4438.
9. Bavoil, P.,, and R. Hsia. 1998. Type III secretion in Chlamydia: a case of deja vu? Mol. Microbiol. 28: 860 862.
10. Bavoil, P.,, A. Ohlin, andj. Schachter. 1984. Role of disulfide bonding in outer membrane structure and permeability in Chlamydia trachomatis. Infect. Immun. 44: 479 485.
11. Bavoil, P.,, R. C. Hsia,, and R. G. Rank. 1996. Prospects for a vaccine against chlamydial genital disease. I. Microbiology and pathogenesis. Bull. Inst. Pasteur 94: 5 54.
12. Beatty, W. L.,, G. I. Byrne,, and R. P. Morrison. 1993. Morphologic and antigenic characterization of interferon-gamma mediated persistent Chlamydia trachomatis infection in vitro. Proc. Natl. Acad. Sci. USA 90: 3998 4002.
13. Beatty, W. L.,, G. I. Byrne,, and R. P. Morrison. 1994. Repeated and persistent infection with Chlamydia and the development of chronic inflammation and disease. Trends Microbiol. 2: 94 98.
14. Beatty, W. L.,, R. P. Morrison,, and G. I. Byrne. 1995. Reactivation of persistent Chlamydia trachomatis infection in cell culture. Infect. Immun. 63: 199 205.
15. Bedson, S. P. 1932. The nature of the elementary bodies in psittacosis. J. Exp. Pathol. 13: 65 72.
16. Bedson, S. P. 1933. Observations of the developmental forms of psittacosis virus. J. Exp. Pathol. 14: 267 277.
17. Bedson, S. P.,, and J. O. W. Bland. 1934. The developmental forms of psittacosis virus. J. Exp. Pathol. 15: 243 247.
18. Brade, H.,, L. Brade,, and F. E. Nano. 1987. Chemical and serological investigations on the genus-specific lipopolysaccharide epitope of Chlamydia. Proc. Natl. Acad. Sci. USA 84: 2508 2512.
19. Brickman, T. J.,, I. Barry,, and T. Hackstadt. 1993. Molecular cloning and expression ofhctB encoding a strain-variant chlamydial histone-like protein with DNA-binding activity. J. Bacteriol. 175: 4274 4281.
20. Caldwell, H. D.,, and P. J. Hitchcock. 1984. Monoclonal antibody against a genus-specific antigen of Chlamydia species: location of the epitope on chlamydial lipopolysaccharide. Infect. Immun. 44: 306 314.
21. Caldwell, H. D.,, and L. J. Perry. 1982. Neutralization of Chlamydia trachomatis infectivity with antibodies to the major outer membrane protein. Infect. Immun. 38: 745 754.
22. Caldwell, H. D.,, J. Kromhout, andj. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia tra-chomatis. Infect. Immun. 31: 1161 1176.
23. Cevenini, R.,, M. Donati,, E. Brocchi,, F. De Si-mone,, and M. La Placa. 1991. Partial characterization of an 89-kDa highly immunoreactive protein from Chlamydia psittaci A/22 causing ovine abortion. FEMS Mkrobiol. Lett. 81: 111 116.
24. Collier, L. H. 1962. Growth characteristics of inclusion blennorrhea virus in cell cultures. Ann. N. Y. Acad. Sci. 98: 42 49.
25. Everett, K. D. E.,, and T. P. Hatch. 1995. Architecture of the cell envelope of Chlamydia psittaci 6BC. J. Bacteriol. 177: 877 882.
26. Everett, K. D. E.,, D. M. Desiderio,, and T. P. Hatch. 1994. Characterization of lipoprotein EnvA in Chlamydia psittaci 6BC. J. Bacteriol. 176: 6082 6087.
27. Fox, A.,, J. C. Rogers,, J. Gilbart,, S. Morgan,, C. H. Davis,, S. Knight,, and P. B. Wyrick. 1990. Muramic acid is not detectable in Chlamydia psittaci or Chlamydia trachomatis by gas chromatography-mass spectrometry. Infect. Immun. 58: 835 837.
28. Girardi, A. J.,, E. G. Allen,, and M. M. Sigel. 1952. Studies on the psittacosis-lymphogranuloma group. II. A non-infectious phase in virus development following adsorption to host tissue. J. Exp. Med. 96: 233 246.
29. Gordon, M. H. 1930. Virus studies concerning the etiology of psittacosis. Lancet 218: 1174 1177.
30. Grayston, J. T. 1992. Infections caused by Chlamydia pneumoniae strain TWAR. Gin. Infect. Dis. 15: 757 761.
31. Gregory, W. W.,, M. Gardner,, G. I. Byrne,, and J. W. Moulder. 1979. Arrays of hemispheric surface projections on Chlamydia psittaci and Chlamydia trachomatis observed by scanning electron microscopy. J. Bacteriol. 138: 241 244.
32. Grimwood, J.,, W. Mitchell,, and R. S. Stephens,. 1998. Phylogenetic analysis of a multigene family conserved between Chlamydia trachomatis and Chlamydia pneumoniae, p. 263 266. In R. S. Stephens et. al. (ed.), Chlamydial Infections. International Chlamydia Symposium, San Francisco, Calif.
33. Hackstadt, T. 1986. Identification and properties of chlamydial polypeptides that bind eucaryotic cell surface components. J. Bacteriol. 165: 13 20.
34. Hackstadt, T.,, W. Baehr,, and Y. Yuan. 1991. Chlamydia trachomatis developmentally regulated protein is homologous to eukaryotic histone HI. Proc. Natl. Acad. Sci. USA 88: 3937 3941.
35. Hackstadt, T.,, T. J. Brickman,, C. E. Barry, III, and J. D. Sager. 1993. Diversity in the Chlamydia trachomatis histone homolog Hc2. Gene 132: 137 141.
36. Hackstadt, T.,, M. A. Scidmore,, and D. D. Rockey. 1995. Lipid metabolism in Chlamydia trachomatis infected cells: directed trafficking of Golgiderived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. USA 92: 4877 4881.
37. Hackstadt, T.,, D. D. Rockey,, R. A. Heinzen,, and M. A. Scidmore. 1996. Chlamydia trachomatis interrupts an exocytic pathway to acquire endoge-nously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBOJ. 15: 964 977.
38. Hackstadt, T.,, E. R. Fischer,, M. A. Scidmore,, D. D. Rockey,, and R. A. Heinzen. 1997. Origins and functions of the chlamydial inclusion. Trends Mkrobiol. 5: 288 293.
39. Hatch, T.,, and D. Rockey. Unpublished data.
40. Hatch, T. P.,, D. W. Vance Jr.,, and E. Al-Hos-sainy. 1981. Identification of a major envelope protein in Chlamydiad spp. J. Bacteriol. 146: 426 429.
41. 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: 13 20.
42. 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: 379 385.
43. 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: 796 809.
44. Hsia, R.,, Y. Pannekoek,, E. Ingerowski,, and P. M. Bavoil. 1997. Type III secretion genes identify a putative virulence locus of Chlamydia. Mol. Mkrobiol. 25: 351 359.
45. Karimi, S. T.,, R. H. Schloemer,, and C. E. Wilde III. 1989. Accumulation of chlamydial lipopolysac-charide antigen in the plasma membranes of infected cells. Infect. Immun. 57: 1780 1785.
46. Kaul, R.,, and W. M. Wenman. 1986. Cyclic AMP inhibits developmental regulation of Chlamydia trachomatis. J. Bacteriol. 168: 722 727.
47. Kaul, R.,, A. Hoang,, P. Yau,, E. M. Bradbury,, and W. M. Wenman. 1997. The chlamydial EUO gene encodes a histone HI-specific protease. J. Bacteriol. 179: 5928 5934.
48. Knudsen, K.,, A. S. Madsen,, P. Mygind,, G. Christiansen,, and S. Birkelund,. 1998. Surface localized proteins of Chlamydia pneumoniae, p. 267 270. In R. S. Stephens et al. (ed.), Chlamydial Infections. International Chlamydia Symposium, San Francisco, Calif.
49. Krumwiede, C.,, M. McGrath,, and C. Old-enbusch. 1930. The etiology of the disease psittacosis. Science 71: 262 263.
50. Kubori, T.,, Y. Matsushima,, D. Nakamura,, J. Ur-alil,, M. Lara-Tejero,, A. Sukhan,, J. E. Galan,, and S. Aizawa. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602 605.
51. Kuo, C. -C.,, J. T. Grayston,, L. A. Campbell,, Y. A. Goo,, R. W. Wissler,, and E. P. Benditt. 1995. Chlamydia pneumoniae (TWAR) in coronary arteries of young adults (15-34 years old). Proc. Natl. Acad. Set. USA 92: 6911 6914.
52. Lambden, P. R.,, J. S. Everson,, M. E. Ward,, and I. N. Clarke. 1990. Sulfur-rich proteins of Chlamydia trachomatis: developmentally regulated transcription of polycistronic mRNA from tandem promoters. Gene 87: 105 112.
53. Longbottom, D.,, M. Russel,, G. E. Jones,, A. Lainson,, and A. J. Herring. 1996. Identification of a multigene family coding for the 90 kDa proteins of the ovine abortion subtype of Chlamydia psittaci. FEMS Microbiol. Lett. 142: 277 281.
54. Longbottom, D.,, M. Russell,, S. M. Dunbar,, G. E. Jones,, and A. J. Herring. 1998. 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. Inject. Immun. 66: 1317 1324.
55. Louis, C.,, G. Nicolas,, F. Eb,, J.-F. Lefebvre,, and J. Orfila. 1980. Modifications of the envelope of Chlamydia psittaci during its developmental cycle: freeze-fracture study of complementary replicas. J. Bacteriol. 141: 868 875.
56. 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: 2478 2486.
57. Mardh, P.-A. 1992. Natural history of genital and allied chlamydial infections. Curr. Opin. Infect. Dis. 5: 12 17.
58. Matsumoto, A. 1973. Fine structures of cell envelopes of Chlamydia organisms as revealed by freeze-etching and negative staining techniques. J. Bacteriol. 116: 1355 1363.
59. Matsumoto, A. 1982a. Electron microscopic observations of surface projections on Chlamydia psittaci reticulate bodies. J. Bacteriol. 150: 358 364.
60. Matsumoto, A. 1982b. Surface projections of Chlamydia psittaci elementary bodies as revealed by freeze-deep-etching. J. Bacteriol. 151: 1040 1042.
61. Matsumoto, A.,, E. Fujiwara,, and N. Higashi. 1976. Observations of the surface projections of infectious small cells of Chlamydia psittaci in thin sections. J. Electron Microsc. 25: 169 170.
62. McClarty, G. 1994. Chlamydiae and the biochemistry of intracellular parasitism. Microbiology 2: 157 164.
63. Moulder, J. M. 1964. The Psittacosis Group as Bacteria. John Wiley and Sons, New York, N.Y.
64. Moulder, J. W. 1991. Interaction of Chlamydiae and host cells in vitro. Microbiol. Rev. 55: 143 190.
65. Moulder, J. W. 1993. Why is Chlamydia sensitive to penicillin in the absence of peptidoglycan? Infect. Agents Dis. 2: 87 99.
66. Moulder, J. W.,, D. L. Novosel,, and J. E. Officer. 1963. Inhibition of the growth of agents of the psittacosis group by D-cycloserine and its specific reversal by D-alanine. J. Bacteriol. 85: 707 711.
67. Nano, F. E.,, and H. D. Caldwell. 1985. Expression of the chlamydial genus-specific lipopolysaccharide epitope in Escherichia coli. Science 228: 742 744.
68. Newhall, W. J.,, and R. B. Jones. 1983. Disulfide-linked oligomers of the major outer membrane protein of chlamydiae. J. Bacteriol. 154: 998 1001.
69. 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: 344 349.
70. Nurminen, M.,, M. Leinonen,, P. Saikku,, and P. H. Makela. 1983. The genus-specific antigen of Chlamydia: resemblance to the lipopolysaccharide of enteric bacteria. Science 220: 1279 1281.
71. Pagano, R. E.,, O. C. Martin,, H. C. Kang,, and R. P. Haugland. 1991. A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor J. CellBiol. 113: 1267 1279.
72. Page, L. A. 1966. Revision of the Family Chlamyd-iaceae Rake (Rickettsiales): unification of the psit-tacosis-lymphogranuloma venereum-trachoma group of organisms in the genus Chlamydia Jones, Rake and Steams. Int. J. Syst. Bacteriol. 16: 223 252.
73. Pedersen, L. B.,, S. Birkelund,, and G. Christiansen. 1996a. Purification of recombinant Chlamydia trachomatis Hl-like protein Hc2, and comparative functional analysis of Hc2 and Hc1. Mol. Microbiol. 20: 295 311.
74. Pedersen, L. B.,, S. Birkelund,, A. Holm,, S. Oster-gaard,, and G. Christiansen. 1996b. The 18-ki-lodalton Chlamydia trachomatis histone Hl-like protein (Hc1) contains a potential N-terminal dimerization site and a C-terminal nucleic acid-binding domain. J. Bacteriol. 178: 994 1002.
75. Perara, E.,, D. Ganem, andj. N. Engel. 1992. A developmentally regulated chlamydial gene with apparent homology to eukaryotic histone HI. Proc. Natl. Acad. Set. USA 89: 2125 2129.
76. Plaunt, M. R.,, and T. P. Hatch. 1988. Protein synthesis early in the developmental cycle of Chlamydia psittaci. Infect. Immun. 56: 3021 3025.
77. Remacha, M.,, R. Kaul,, R. Sherburne,, and W. M. Wenman. 1996. Functional domains of chlamydial Hl-like protein. Biochem. J. 315: 481 486.
78. 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: 106 112.
79. 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. Miaobiol. 15: 617 626.
80. 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. Miaobiol. 24: 217 228.
81. Schachter, J. 1978. Chlamydial infections. N. Engl. J. Med. 298: 428 434.
82. Schachter, J.,, and C. R. Dawson. 1990. The epidemiology of trachoma predicts more blindness in the future. Scand.J. Infect. Dis. 69: 55 62.
83. Scidmore, M. A.,, D. D. Rockey,, E. R. Fischer,, R. A. Heinzen,, and T. Hackstadt. 1996. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect. Immun. 64: 5366 5372.
84. Scidmore-Carlson, M. A.,, E. I. Shaw,, C. A. Dooley,, E. R. Fischer,, and T. Hackstadt. 1999. Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol. Microbiol. 33: 753 765.
85. Shemer, Y.,, and I. Sarov. 1985. Inhibition of growth of Chlamydia trachomatis by human gamma interferon. Infect. Immun. 48: 592 596.
86. Shemer-Avni, Y.,, D. Wallach,, and I. Sarov. 1988. Inhibition of Chlamydia trachomatis growth by re-combinant tumor necrosis factor. Infect. Immun. 56: 2503 2506.
87. Stephens, R. S.,, G. Mullenbach,, R. Sanchez-Pes-cador,, and N. Agabian. 1986. Sequence analysis of the major outer membrane protein gene from Chlamydia trachomatis serovar L2. J. Bacteriol. 168: 1277 1282.
88. Stephens, R. S.,, R. Sanchez-Pescador,, E. A. Wagar,, C. Inouye,, and M. S. Urdea. 1987. Diversity of Chlamydia trachomatis major outer membrane protein genes. J. Bacteriol 169: 3879 3885.
89. Stephens, R. S.,, S. Kalman,, C. Lammel,, J. Fan,, R. Maratha,, L. Aravind,, W. Mitchell,, L. Olinger,, R. L. Tatusov,, Q. Zhao,, E. U. Kooning,, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754 759.
90. Su, H.,, and H. D. Caldwell. 1991. In vitro neutralization of Chlamydia trachomatis by monovalent Fab antibody specific to the major outer membrane protein. Infect. Immun. 59: 2843 2845.
91. 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: 1017 1025.
92. Su, H.,, L. Raymond,, D. D. Rockey,, E. Fischer,, T. Hackstadt,, and H. D. Caldwell. 1996. A re-combinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc. Natl. Acad. Set. USA 93: 11143 11148.
93. Tamura, A.,, A. Ma tsumo to,, and N. Higashi. 1967. Purification and chemical composition of reticulate bodies of the meningopneumonitis organisms. J. Bacteriol. 93: 2003 2008.
94. Thygeson, P. 1962. Trachoma virus: historical background and review of isolates. Ann. N. Y. Acad. Sci. 98: 6 13.
95. 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: 3600 3608.
96. Todd, W. J.,, and H. D. Caldwell. 1985. The interaction of Chlamydia trachomatis with host cells: ultra-structural studies of the mechanism of release of a biovar II strain from HeLa 229 cells. J. Infect. Dis. 151: 1037 1044.
97. University of California, Berkeley. 1999. Chlamydia Genome Project Database. [Online.] http: //chlamydia-www.berkeley.edu:4231/.
98. Wagar, E. A.,, and R. S. Stephens. 1988. Development-form-specific DNA-binding proteins in Chlamydia spp. Infect. Immun. 56: 1678 1684.
99. Washington, A. E.,, R. E. Johnson,, and L. L. Sanders Jr.. 1987. Chlamydia trachomatis infections in the United States: what are they costing us? JAMA 257: 2070 2072.
100. Watson, M. W.,, I. N. Clarke,, J. S. Everson,, and P. R. Lambden. 1995. The CrP operon of Chlamydia psittaci and Chlamydia pneumoniae. Microbiology 141: 2489 2497.
101. Weiss, E. 1950. The effect of antibiotics on agents of the psittacosis-lymphogranuloma group. I. The effect of penicillin. J. Infect. Dis. 87: 249 263.
102. Wichlan, D. G.,, and T. P. Hatch. 1993. Identification of an early-stage gene of Chlamydia psittaci. J. Bacteriol. 175: 2936 2942.
103. 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: 7233 7242.
104. Wyllie, S.,, R. H. Ashley,, D. Longbottom,, and A. J. Herring. 1998. The major outer membrane protein of Chlamydia psittaci functions as a porin-like ion channel. Infect. Immun. 66: 5202 5207.
105. Yuan, Y.,, Y.-X. Zhang,, N. G. Watkins,, and H. D. Caldwell. 1989. Nucleotide and deduced amino acid sequences for the four variable domains of the major outer membrane proteins of the 15 Chlamydia trachomatis serovars. Inject. Immun. 57: 1040 1049.
106. Zhang, L.,, A. L. Douglas,, and T. P. Hatch. 1998. Characterization of a Chlamydia psittaci DNA binding protein (EUO) synthesized during the early and middle phases of the developmental cycle. Infect. Immun. 66: 1167 1173.
107. Zhang, Y.-X.,, S. J. Stewart,, and H. D. Caldwell. 1989. Protective monoclonal antibodies to Chlamydia trachomatis serovar- and serogroup-specific major outer membrane protein determinants. Infect. Immun. 57: 636 638.

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