TREM-2 binds to lipooligosaccharides of Neisseria gonorrhoeae and is expressed on reproductive tract epithelial cells

Mucosal Immunology

Volumn 1, Issue 3, 2008, Pages 229-238

  Quan, D N ^a   Cooper, M D ^b   Potter, J L ^b   Roberts, M H ^b   Cheng, H ^a   Jarvis, G A ^a,c  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; LIPID A; LIPOOLIGOSACCHARIDE; MEMBRANE RECEPTOR; OPACITY PROTEIN; OUTER MEMBRANE PROTEIN; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; CELL ACTIVATION; CELL ASSAY; CELL LINEAGE; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEACYLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; GENETIC TRANSFECTION; GENITAL SYSTEM; HELA CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; UROGENITAL SYSTEM; UTERINE TUBE; WESTERN BLOTTING;

EID: 42149188248     PISSN: 19330219     EISSN: None     Source Type: Journal    
DOI: 10.1038/mi.2008.1     Document Type: Article

References (53)

1. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance. US Department of Health and Human Services, Public Health Service (2005).
2. Paavonen, J. Pelvic inflammatory disease. From diagnosis to prevention. Dermatol. Clin. 16, 747-756 (1998).
3. Cohen, M.S. et al. Reduction of concentration of HIV-1 in semen after treatment of urethritis: Implications for prevention of sexual transmission of HIV-1. Lancet 349, 1868-1873 (1997).
4. Chesson, H.W. & Pinkerton, S.D. Sexually transmitted diseases and the increased risk for HIV transmission: Implications for cost-effectiveness analyses of sexually transmitted disease prevention interventions. J. Acquir. Immune. Defic. Syndr. 24, 48-56 (2000).
5. Mabey, D. Interactions between HIV infection and other sexually transmitted diseases. Trop. Med. Int. Health 5, A32-A36 (2000).
6. Farley, T.A., Cohen, D.A., Wu, S.Y. & Besch, C.L. The value of screening for sexually transmitted diseases in an HIV clinic. J. Acquir. Immune. Defic. Syndr. 33, 642-648 (2003).
7. Pridmore, A.C. et al. Activation of toll-like receptor 2 (TLR2) and TLR4/MD2 by Neissería is independent of capsule and lipooligosaccharide (LOS) sialylation but varies widely among LOS from different strains. Infect. Immun. 71, 3901-3908 (2003).
8. Massari, P. et al. Cutting edge: Immune stimulation by neisserial porins is toll-like receptor 2 and MyD88 dependent. J. Immunol. 168, 1533-1537 (2002).
9. Fisette, P.L., Ram, S., Andersen, J.M., Guo, W. & Ingalls, R.R. The lip lipoprotein from Neisseria gonorrhoeae stimulates cytokine release and NF-κB activation in epithelial cells in a Toll-like receptor 2-dependent manner. J. Biol. Chem. 278, 46252-46260 (2003).
10. Fichorova, R.N., Desai, P.J., Gibson, F.C. III & Genco, C.A. Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect. Immun. 69, 5840-5848 (2001).
11. Naumann, M., Wessler, S., Bartsch, C., Wieland, B. & Meyer, T.F. Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor κB and activator protein 1 and the induction of inflammatory cytokines. J. Exp. Med. 186, 247-258 (1997).
12. Jarvis, G.A., Li, J. & Swanson, K.V. Invasion of human mucosal epithelial cells by Neisseria gonorrhoeae upregulates expression of intercellular adhesion molecule 1 (ICAM-1). Infect. Immun. 67, 1149-1156 (1999).
13. Ramsey, K.H. et al. Inflammatory cytokines produced in response to experimental human gonorrhea. J. Infect. Dis. 172, 186-191 (1995).
14. McGee, Z.A. et al. Gonococcal infection of human fallopian tube mucosa in organ culture: Relationship of mucosal tissue TNF-α concentration to sloughing of ciliated cells. Sex Transm. Dis. 26, 160-165 (1999).
15. Kahler, C.M. & Stephens, D.S. Genetic basis for biosynthesis, structure, and function of meningococcal lipooligosaccharide (endotoxin . Crit. Rev. Microbiol. 24, 281-334 (1998).
16. Griffiss, J.M. et al. Physical heterogeneity of neisserial lipooligosaccharides reflects oligosaccharides that differ in apparent molecular weight, chemical composition, and antigenic expression. Infect. Immun. 55, 1792-1800 (1987).
17. Takayama, K. et al. Characterization of a structural series of lipid A obtained from the lipopolysaccharides of Neisseria gonorrhoeae. Combined laser desorption and fast atom bombardment mass spectral analysis of high performance liquid chromatography-purified dimethyl derivatives. J. Biol. Chem. 261, 10624-10631 (1986).
18. Erwin, A.L., Mandrell, R.E. & Munford, R.S. Enzymatically deacylated Neisseria lipopolysaccharide (LPS) inhibits murine splenocyte mitogenesis induced by LPS. Infect. Immun. 59, 1881-1887 (1991).
19. Roth, R.I., Yamasaki, R., Mandrell, R.E. & Griffiss, J.M. Ability of gonococcal and meningococcal lipooligosaccharides to clot Limulus amebocyte lysate. Infect. Immun. 60, 762-767 (1992).
20. Colonna, M. TREMs in the immune system and beyond. Nat. Rev. Immunol. 3, 445-453 (2003).
21. Bouchon, A., Dietrich, J. & Colonna, M. Cutting edge: Inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J. Immunol. 164, 4991-4995 (2000).
22. Bouchon, A., Hernandez-Munain, C., Cella, M. & Colonna, M. A DAP12-mediated pathway regulates expression of CC chemokine receptor 7 and maturation of human dendritic cells. J. Exp. Med. 194, 1111-1122 (2001).
23. Daws, M.R., Lanier, L.L., Seaman, W.E. & Ryan, J.C. Cloning and characterization of a novel mouse myeloid DAP12-associated receptor family. Eur. J. Immunol. 31, 783-791 (2001).
24. Bouchon, A., Facchetti, F., Weigand, M.A. & Colonna, M. TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 410, 1103-1107 (2001).
25. Daws, M. R. et al. Pattern recognition by TREM-2: Binding of anionic ligands. J. Immunol. 171, 594-599 (2003).
26. Chung, D.H., Seaman, W.E. & Daws, M.R. Characterization of TREM-3, an activating receptor on mouse macrophages: Definition of a family of single Ig domain receptors on mouse chromosome 17. Eur. J. Immunol. 32, 59-66 (2002).
27. Fichorova, R.N., Cronin, A.O., Lien, E., Anderson, D.J. & Ingalls, R.R. Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of toll-like receptor 4-mediated signaling. J. Immunol. 168, 2424-2432 (2002).
28. Cooper, M.D., McGee, Z.A., Mulks, M.H., Koorney, J.M. & Hindman, T.L. Attachment to and invasion of human fallopian tube mucosa by an IgA1 protease-deficient mutant of Neisseria gonorrhoeae and its wild-type parent. J. Infect. Dis. 150, 737-744 (1984).
29. Allcock, R.J., Barrow, A.D., Forbes, S., Beck, S. & Trowsdale, J. The human TREM gene cluster at 6p21.1 encodes both activating and inhibitory single IgV domain receptors and includes NKp44. Eur. J. Immunol. 33, 567-577 (2003).
30. Thomas, C.J. et al. Evidence of a trimolecular complex involving LPS, LPS binding protein and soluble CD14 as an effector of LPS response. FEBS Lett. 531, 184-188 (2002).
31. Levels, J.H. et al. Lipopolysaccharide is transferred from high-density to low-density lipoproteins by lipopolysaccharide-binding protein and phospholipid transfer protein. Infect. Immun. 73 2321-2326 (2005).
32. John, C.M. et al. Galectin-3 binds lactosaminylated lipooligosaccharides from Neisseria gonorrhoeae and is selectively expressed by mucosal epithelial cells that are infected. Cell Microbiol. 4, 649-662 (2002).
33. Begum, N.A. et al. Mycobacteidum bovis BCG cell wall-specific differentially expressed genes identified by differential display and cDNA subtraction in human macrophages. Infect. Immun. 72, 937-948 (2004).
34. Zhang, P. et al. DC-SIGN(CD209) recognition of Neisseria gronorrhoeae is circumvented by lipooligosaccharide vadation. J. Leukoc. Biol. 79, 731-738 (2006).
35. Harvey, H.A., Jennings, M.P., Campbell, C.A., Williams, R. & Apicella, M.A. Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: The role of the asiatoglycoprotein receptor. Mol. Microbiol. 42, 659-672 (2001).
36. Porat, N., Apicella, M.A. & Blake, M.S. A lipooligosaccharide-binding site on HepG2 cells similar to the gonococcal opacity-associated surface protein Opa. Infect. Immun. 63, 2164-2172 (1995).
37. Virji, M., Watt, S.M., Barker, S., Makepeace, K. & Doyonnas, R. The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol. Microbiol. 22, 929-939 (1996).
38. Estabrook, M.M., Jack, D. L., Klein, N.J. & Jarvis, G.A. Mannose-binding lectin binds to two major outer membrane proteins, opacity protein and porin, of Neisseria meningitidis. J. Immunol. 172, 3784-3792 (2004).
39. Bouchon, A., Hernandez-Munain, C., Cella, M. & Colonna, M. A DAP12-mediated pathway regulates expression of CC chemokine receptor 7 and maturation of human dendritic cells. J. Exp. Med. 194, 1111-1122 (2001).
40. Zhang, J. et al. Neisseria gonorrhoeae enhances infection of dendritic cells by HIV type 1. J. Immunol. 174, 7995-8002 (2005).
41. Pater, M.M. & Pater, A. Human papillomavirus types 16 and 18 sequences in carcinoma cell lines of the cervix. Virology 145, 313-318 (1985).
42. Fichorova, R.N., Rheinwald, J.G. & Anderson, D.J. Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol. Reprod. 57, 847-855 (1997).
43. Hamerman, J.A. et al. Cutting edge: Inhibition of TLR and FcR responses in macrophages by triggedrig receptor expressed on myeloid cells (TREM)-2 and DAP12. J. Immunol. 177, 2051-2055 (2006).
44. Hedges, S.R., Sibley, D.A., Mayo, M.S., Hook, E.W. III & Russell, M.W. Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: Effects of concomitant infections. J. Infect. Dis. 178, 742-751 (1998).
45. Swanson, K.V. & Griffiss, J.M. Separation and identification of neisserial lipooligosaccharide oligosaccharides using high-performance anion-exchange chromatography with pulsed amperometric detection. Carbohydr. Res. 341, 388-396 (2006).
46. Zollinger, W.D., Mandrell, R.E., Griffiss, J.M., Altieri, P. & Berman, S. Complex of meningococcal group B polysaccharide and type 2 outer membrane protein immunogenic in man. J. Clin. Invest. 63, 836-848 (1979).
47. Apicella, M.A., Griffiss, J. M. & Schneider, H. Isolation and characterization of lipopolysaccharides, lipooligosaccharides, and lipid A. Methods Enzymol. 235, 242-252 (1994).
48. John, C.M., Schneider, H. & Griffiss, J.M. Neisseria gonorrhoeae that infect men have lipooligosaccharides with terminal N acetyllactosamine repeats. J. Biol. Chem. 274, 1017-1025 (1999).
49. Griffiss, J. M., Lammel, C.J., Wang, J., Dekker, N.P. & Brooks, G.F. Neisseria gonorrhoeae coordinately uses Pili and Opa to activate HEC-1-B cell microvilli, which causes engulfment of the gonococci. Infect. Immun. 67, 3469-3480 (1999).
50. Estabrook, M.M., Griffiss, J.M. Jarvis, G.A. Sialylation of Neisseria meningitidis lipooligosaccharide inhibits serum bactericidal activity by masking lacto-N-neotetraose. Infect. Immun. 65, 4436-4444 (1997).
51. Takamatsu, D. et al. Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein lbα. Mol. Microbiol. 58, 380-392 (2005).
52. Sanderson, S. & Shastri, N. LacZ inducible, antigen/MHC-specific T cell hybrids. Int. Immunol. 6, 369-376 (1994).
53. Cooper, M.D., Rapp, J., Jeffery-Wiseman, C., Barnes, R.C. & Stephens, D.S. Chlamydia trachomatis infection of human fallopian tube organ cultures. J. Gen. Microbiol. 136, 1109-1115 (1990).