Journal of Reproductive Immunology
Volume 84, Issue 2 , Pages 145-153 , March 2010

Characterization of the invasive and inflammatory traits of oral Campylobacter rectus in a murine model of fetoplacental growth restriction and in trophoblast cultures

  • R.M. Arce

      Affiliations

    • Center for Oral and Systemic Diseases, NC Oral Health Institute, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Authors equally contributed to this report.
    • ,
  • P.I. Diaz

      Affiliations

    • Department of Periodontology, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Authors equally contributed to this report.
    • Current affiliation: Division of Periodontology, Department of Oral Health and Diagnostic Sciences, School of Dental Medicine, The University of Connecticut Health Center, Farmington, CT, USA.
    • ,
  • S.P. Barros

      Affiliations

    • Center for Oral and Systemic Diseases, NC Oral Health Institute, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Department of Periodontology, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • ,
  • P. Galloway

      Affiliations

    • Center for Oral and Systemic Diseases, NC Oral Health Institute, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • ,
  • Y. Bobetsis

      Affiliations

    • Center for Oral and Systemic Diseases, NC Oral Health Institute, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Department of Periodontology, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Current affiliation: Department of Periodontology, School of Dentistry, University of Athens, Athens, Greece.
    • ,
  • D. Threadgill

      Affiliations

    • Department of Genetics, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Current affiliation: Department of Microbiology, North Carolina State University, Raleigh, NC, USA.
    • ,
  • S. Offenbacher

      Affiliations

    • Center for Oral and Systemic Diseases, NC Oral Health Institute, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Department of Periodontology, School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
    • Corresponding Author InformationCorresponding author at: NC Oral Health Institute, School of Dentistry, University of North Carolina at Chapel Hill, 79 T.W. Alexander Drive, 4301 Research Commons, Research Triangle Park, NC 27709, USA. Tel.: +1 919 425 3596; fax: +1 919 425 3532.

Received 3 September 2009 ,Revised 27 October 2009 ,Accepted 23 November 2009.

References 

  1. Abrahams VM, Bole-Aldo P, Kim YM, Straszewski-Chavez SL, Chaiworapongsa T, Romero R, et al. Divergent trophoblast responses to bacterial products mediated by TLRs. J. Immunol. 2004;173(7):4286–4296
  2. Allos BM. Campylobacter jejuni infections: update on emerging issues and trends. Clin. Infect. Dis. 2001;32(8):1201–1206
  3. Arce RM, Barros SP, Wacker B, Peters B, Moss K, Offenbacher S. Increased TLR4 expression in murine placentas after oral infection with periodontal pathogens. Placenta. 2009;30(2):156–162
  4. Bacon DJ, Alm RA, Burr DH, Hu L, Kopecko DJ, Ewing CP, et al. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 2000;68(8):4384–4390
  5. Bakardjiev AI, Theriot JA, Portnoy DA. Listeria monocytogenes traffics from maternal organs to the placenta and back. PLoS Pathog. 2006;2(6):e66
  6. Biswas D, Niwa H, Itoh K. Infection with Campylobacter jejuni induces tyrosine-phosphorylated proteins into INT-407 cells. Microbiol. Immunol. 2004;48(4):221–228
  7. Bobetsis YA, Barros SP, Lin DM, Weidman JR, Dolinoy DC, Jirtle RL, et al. Bacterial infection promotes DNA hypermethylation. J. Dent. Res. 2007;86(2):169–174
  8. Bowen JA, Hunt JS. Expression of cell adhesion molecules in murine placentas and a placental cell line. Biol. Reprod. 1999;60(2):428–434
  9. Chen ML, Ge Z, Fox JG, Schauer DB. Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infect. Immun. 2006;74(12):6581–6589
  10. Fields JA, Thompson SA. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J. Bacteriol. 2008;190(9):3411–3416
  11. Friis LM, Pin C, Pearson BM, Wells JM. In vitro cell culture methods for investigating Campylobacter invasion mechanisms. J. Microbiol. Methods. 2005;61(2):145–160
  12. Gomez R, Romero R, Edwin SS, David C. Pathogenesis of preterm labor and preterm premature rupture of membranes associated with intraamniotic infection. Infect. Dis. Clin. North Am. 1997;11(1):135–176
  13. Hanel I, Muller J, Muller W, Schulze F. Correlation between invasion of Caco-2 eukaryotic cells and colonization ability in the chick gut in Campylobacter jejuni. Vet. Microbiol. 2004;101(2):75–82
  14. Ihara H, Miura T, Kato T, Ishihara K, Nakagawa T, Yamada S, et al. Detection of Campylobacter rectus in periodontitis sites by monoclonal antibodies. J. Periodont. Res. 2003;38(1):64–72
  15. Kalischuk LD, Inglis GD, Buret AG. Strain-dependent induction of epithelial cell oncosis by Campylobacter jejuni is correlated with invasion ability and is independent of cytolethal distending toxin. Microbiology. 2007;153(Pt 9):2952–2963
  16. Krause-Gruszczynska M, Rohde M, Hartig R, Genth H, Schmidt G, Keo T, et al. Role of the small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni. Cell Microbiol. 2007;9(10):2431–2444
  17. LaGier MJ, Threadgill DS. Identification of novel genes in the oral pathogen Campylobacter rectus. Oral Microbiol. Immunol. 2008;23(5):406–412
  18. Levy O. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat. Rev. Immunol. 2007;7(5):379–390
  19. Li L, Michel R, Cohen J, Decarlo A, Kozarov E. Intracellular survival and vascular cell-to-cell transmission of Porphyromonas gingivalis. BMC Microbiol. 2008;8:26
  20. Madianos PN, Lieff S, Murtha AP, Boggess KA, Auten RL, Beck JD, et al. Maternal periodontitis and prematurity. Part II. Maternal infection and fetal exposure. Ann. Periodontol. 2001;6(1):175–182
  21. Medina E, Goldmann O, Toppel AW, Chhatwal GS. Survival of Streptococcus pyogenes within host phagocytic cells: a pathogenic mechanism for persistence and systemic invasion. J. Infect. Dis. 2003;187(4):597–603
  22. Mor G. Inflammation and pregnancy: the role of toll-like receptors in trophoblast-immune interaction. Ann. N. Y. Acad. Sci. 2008;1127:121–128
  23. O'Sullivan AM, Dore CJ, Coid CR. Campylobacters and impaired fetal development in mice. J. Med. Microbiol. 1988;25(1):7–12
  24. Offenbacher S, Riche EL, Barros SP, Bobetsis YA, Lin D, Beck JD. Effects of maternal Campylobacter rectus infection on murine placenta, fetal and neonatal survival, and brain development. J. Periodontol. 2005;76(11 Suppl.):2133–2143
  25. Okuda K, Kigure T, Yamada S, Kaneko T, Ishihara K, Miura T, et al. Role for the S-layer of Campylobacter rectus ATCC33238 in complement mediated killing and phagocytic killing by leukocytes from guinea pig and human peripheral blood. Oral Dis. 1997;3(2):113–120
  26. Pattillo RA, Gey GO. The establishment of a cell line of human hormone-synthesizing trophoblastic cells in vitro. Cancer Res. 1968;28(7):1231–1236
  27. Rinella ES, Eversley CD, Carroll IM, Andrus JM, Threadgill DW, Threadgill DS. Human epithelial-specific response to pathogenic Campylobacter jejuni. FEMS Microbiol. Lett. 2006;262(2):236–243
  28. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J. Biol. Chem. 2003;278(16):14112–14120
  29. Sharma RK. Mouse trophoblastic cell lines. I. Relationship between invasive potential and TGF-beta 1. In Vivo. 1998;12(5):431–440
  30. Simor AE, Karmali MA, Jadavji T, Roscoe M. Abortion and perinatal sepsis associated with campylobacter infection. Rev. Infect. Dis. 1986;8(3):397–402
  31. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 1998;25(2):134–144
  32. Tanner A, Maiden MF, Macuch PJ, Murray LL, Kent RL. Microbiota of health, gingivitis, and initial periodontitis. J. Clin. Periodontol. 1998;25(2):85–98
  33. van Alphen LB, Bleumink-Pluym NM, Rochat KD, van Balkom BW, Wosten MM, van Putten JP. Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell Microbiol. 2008;10(1):53–66
  34. Wang B, Kraig E, Kolodrubetz D. Use of defined mutants to assess the role of the Campylobacter rectus S-layer in bacterium-epithelial cell interactions. Infect. Immun. 2000;68(3):1465–1473
  35. Wine E, Chan VL, Sherman PM. Campylobacter jejuni mediated disruption of polarized epithelial monolayers is cell-type specific, time dependent, and correlates with bacterial invasion. Pediatr. Res. 2008;64(6):599–604
  36. Wong SN, Tam AY, Yuen KY. Campylobacter infection in the neonate: case report and review of the literature. Pediatr. Infect. Dis. J. 1990;9(9):665–669
  37. Yeo A, Smith MA, Lin D, Riche EL, Moore A, Elter J, et al. Campylobacter rectus mediates growth restriction in pregnant mice. J. Periodontol. 2005;76(4):551–557
  38. Yokoyama M, Hinode D, Masuda K, Yoshioka M, Grenier D. Effect of female sex hormones on Campylobacter rectus and human gingival fibroblasts. Oral Microbiol. Immunol. 2005;20(4):239–243
  39. Yokoyama M, Hinode D, Yoshioka M, Fukui M, Tanabe S, Grenier D, et al. Relationship between Campylobacter rectus and periodontal status during pregnancy. Oral Microbiol. Immunol. 2008;23(1):55–59

PII: S0165-0378(09)00553-1

doi: 10.1016/j.jri.2009.11.003

Journal of Reproductive Immunology
Volume 84, Issue 2 , Pages 145-153 , March 2010

Article Tools

* Image Usage & Resolution