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. 1997 Jul;65(7):2914–2924. doi: 10.1128/iai.65.7.2914-2924.1997

Differences in the association of Chlamydia trachomatis serovar E and serovar L2 with epithelial cells in vitro may reflect biological differences in vivo.

C H Davis 1, P B Wyrick 1
PMCID: PMC175409  PMID: 9199467

Abstract

Chlamydia trachomatis serovar E is one of the most common bacterial sexually transmitted pathogens. Since it is an obligate intracellular bacterium, efficient colonization of genital mucosal epithelial cells is crucial to the infectious process. Serovar E elementary bodies (EB) metabolically radiolabeled with 35S-Cys-Met and harvested from microcarrier bead cultures, which significantly improves the infectious EB-to-particle ratio, provided a more accurate picture of the parameters of attachment of EB to human endometrial epithelial cells (HEC-1B) than did less infectious 14C-EB harvested from flask cultures. Binding of serovar E EB was (i) equivalent at 35 and 4 degrees C, (ii) decreased by preexposure of EB to heat or the topical microbicide C31G, (iii) comparable among common eukaryotic cell lines (HeLa, McCoy), and (iv) significantly increased to the apical surfaces of polarized cells versus nonpolarized cells. In parallel experiments with C. trachomatis serovar L2, serovar E attachment was not affected by heparin or heparan sulfate whereas these glucosaminoglycans dramatically reduced serovar L2 attachment. These data were confirmed by competitive inhibition of serovar E binding and infectivity by excess unlabeled live and UV-inactivated serovar E EB but not by excess serovar L2 EB. The noninvasive serovar E strains in the lumen of the genital tract enter and exit the apical domains of target columnar epithelial cells to spread canalicularly in an ascending fashion from the lower to the upper genital tract. In contrast, the invasive serovar L2 strains are primarily submucosal pathogens and likely use the glucosaminoglycans concentrated in the extracellular matrix to colonize the basolateral domains of mucosal epithelia to perpetuate the infectious process.

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Selected References

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  1. Boutin E. L., Sanderson R. D., Bernfield M., Cunha G. R. Epithelial-mesenchymal interactions in uterus and vagina alter the expression of the cell surface proteoglycan, syndecan. Dev Biol. 1991 Nov;148(1):63–74. doi: 10.1016/0012-1606(91)90317-v. [DOI] [PubMed] [Google Scholar]
  2. Chen J. C., Stephens R. S. Trachoma and LGV biovars of Chlamydia trachomatis share the same glycosaminoglycan-dependent mechanism for infection of eukaryotic cells. Mol Microbiol. 1994 Feb;11(3):501–507. doi: 10.1111/j.1365-2958.1994.tb00331.x. [DOI] [PubMed] [Google Scholar]
  3. Chen J. C., Zhang J. P., Stephens R. S. Structural requirements of heparin binding to Chlamydia trachomatis. J Biol Chem. 1996 May 10;271(19):11134–11140. [PubMed] [Google Scholar]
  4. Chen T., Belland R. J., Wilson J., Swanson J. Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J Exp Med. 1995 Aug 1;182(2):511–517. doi: 10.1084/jem.182.2.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Eissenberg L. G., Wyrick P. B., Davis C. H., Rumpp J. W. Chlamydia psittaci elementary body envelopes: ingestion and inhibition of phagolysosome fusion. Infect Immun. 1983 May;40(2):741–751. doi: 10.1128/iai.40.2.741-751.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hackstadt T., Rockey D. D., Heinzen R. A., Scidmore M. A. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 1996 Mar 1;15(5):964–977. [PMC free article] [PubMed] [Google Scholar]
  7. Hackstadt T., Scidmore M. A., Rockey D. D. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc Natl Acad Sci U S A. 1995 May 23;92(11):4877–4881. doi: 10.1073/pnas.92.11.4877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hodinka R. L., Davis C. H., Choong J., Wyrick P. B. Ultrastructural study of endocytosis of Chlamydia trachomatis by McCoy cells. Infect Immun. 1988 Jun;56(6):1456–1463. doi: 10.1128/iai.56.6.1456-1463.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Lee C. K. Interaction between a trachoma strain of Chlamydia trachomatis and mouse fibroblasts (McCoy cells) in the absence of centrifugation. Infect Immun. 1981 Feb;31(2):584–591. doi: 10.1128/iai.31.2.584-591.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Newhall W. J., Batteiger B., Jones R. B. Analysis of the human serological response to proteins of Chlamydia trachomatis. Infect Immun. 1982 Dec;38(3):1181–1189. doi: 10.1128/iai.38.3.1181-1189.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Peeling R. W., Brunham R. C. Neutralization of Chlamydia trachomatis: kinetics and stoichiometry. Infect Immun. 1991 Aug;59(8):2624–2630. doi: 10.1128/iai.59.8.2624-2630.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Rostand K. S., Esko J. D. Microbial adherence to and invasion through proteoglycans. Infect Immun. 1997 Jan;65(1):1–8. doi: 10.1128/iai.65.1.1-8.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Schlessinger J., Lax I., Lemmon M. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell. 1995 Nov 3;83(3):357–360. doi: 10.1016/0092-8674(95)90112-4. [DOI] [PubMed] [Google Scholar]
  14. Schramm N., Wyrick P. B. Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect Immun. 1995 Jan;63(1):324–332. doi: 10.1128/iai.63.1.324-332.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Scidmore M. A., Rockey D. D., Fischer E. R., Heinzen R. A., Hackstadt T. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect Immun. 1996 Dec;64(12):5366–5372. doi: 10.1128/iai.64.12.5366-5372.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Su H., Raymond L., Rockey D. D., Fischer E., Hackstadt T., Caldwell H. D. A recombinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11143–11148. doi: 10.1073/pnas.93.20.11143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Su H., Watkins N. G., Zhang Y. X., Caldwell H. D. Chlamydia trachomatis-host cell interactions: role of the chlamydial major outer membrane protein as an adhesin. Infect Immun. 1990 Apr;58(4):1017–1025. doi: 10.1128/iai.58.4.1017-1025.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tam J. E., Knight S. T., Davis C. H., Wyrick P. B. Eukaryotic cells grown on microcarrier beads offer a cost-efficient way to propagate Chlamydia trachomatis. Biotechniques. 1992 Sep;13(3):374–378. [PubMed] [Google Scholar]
  19. Taraska T., Ward D. M., Ajioka R. S., Wyrick P. B., Davis-Kaplan S. R., Davis C. H., Kaplan J. The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect Immun. 1996 Sep;64(9):3713–3727. doi: 10.1128/iai.64.9.3713-3727.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Thompson K. A., Malamud D., Storey B. T. Assessment of the anti-microbial agent C31G as a spermicide: comparison with nonoxynol-9. Contraception. 1996 May;53(5):313–318. [PubMed] [Google Scholar]
  21. Ting L. M., Hsia R. C., Haidaris C. G., Bavoil P. M. Interaction of outer envelope proteins of Chlamydia psittaci GPIC with the HeLa cell surface. Infect Immun. 1995 Sep;63(9):3600–3608. doi: 10.1128/iai.63.9.3600-3608.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Vretou E., Goswami P. C., Bose S. K. 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. 1989 Dec;135(12):3229–3237. doi: 10.1099/00221287-135-12-3229. [DOI] [PubMed] [Google Scholar]
  23. Wyrick P. B., Choong J., Davis C. H., Knight S. T., Royal M. O., Maslow A. S., Bagnell C. R. Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect Immun. 1989 Aug;57(8):2378–2389. doi: 10.1128/iai.57.8.2378-2389.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wyrick P. B., Davis C. H., Knight S. T., Choong J., Raulston J. E., Schramm N. An in vitro human epithelial cell culture system for studying the pathogenesis of Chlamydia trachomatis. Sex Transm Dis. 1993 Sep-Oct;20(5):248–256. doi: 10.1097/00007435-199309000-00002. [DOI] [PubMed] [Google Scholar]
  25. Wyrick P. B., Gerbig D. G., Jr, Knight S. T., Raulston J. E. Accelerated development of genital Chlamydia trachomatis serovar E in McCoy cells grown on microcarrier beads. Microb Pathog. 1996 Jan;20(1):31–40. doi: 10.1006/mpat.1996.0003. [DOI] [PubMed] [Google Scholar]
  26. Zaretzky F. R., Pearce-Pratt R., Phillips D. M. Sulfated polyanions block Chlamydia trachomatis infection of cervix-derived human epithelia. Infect Immun. 1995 Sep;63(9):3520–3526. doi: 10.1128/iai.63.9.3520-3526.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Zhang J. P., Stephens R. S. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell. 1992 May 29;69(5):861–869. doi: 10.1016/0092-8674(92)90296-o. [DOI] [PubMed] [Google Scholar]
  28. van Putten J. P., Paul S. M. Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 1995 May 15;14(10):2144–2154. doi: 10.1002/j.1460-2075.1995.tb07208.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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