The innate immune system is activated by stimulation of vaginal epithelial cells with Staphylococcus aureus and toxic shock syndrome toxin 1

Infection and Immunity

Volumn 73, Issue 4, 2005, Pages 2164-2174

  Peterson, Marnie L ^a   Ault, Kevin ^b   Kremer, Mary J ^c   Klingelhutz, Aloysius J ^b   Davis, Catherine C ^d   Squier, Christopher A ^c   Schlievert, Patrick M ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d PROCTER AND GAMBLE COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; EXOTOXIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MELANOMA GROWTH STIMULATORY ACTIVITY FACTOR; MELANOMA GROWTH STIMULATORY ACTIVITY FACTOR BETA; MELANOMA GROWTH STIMULATORY ACTIVITY FACTOR GAMMA; TOXIC SHOCK SYNDROME TOXIN 1; UNCLASSIFIED DRUG; BACTERIAL TOXIN; CHEMOKINE; CYTOKINE; ENTEROTOXIN; ENTEROTOXIN F, STAPHYLOCOCCAL; KERATIN; SUPERANTIGEN;

ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA MICROARRAY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; INNATE IMMUNITY; LYMPHOCYTE TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION, SYNTHESIS AND MODIFICATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; STAPHYLOCOCCUS AUREUS; TOXIN ANALYSIS; UPREGULATION; VAGINA EPITHELIUM; VAGINA MUCOSA; ANIMAL; BACTERIUM ADHERENCE; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOGENICITY; SWINE; VAGINA;

ANIMALS; BACTERIAL ADHESION; BACTERIAL TOXINS; CELL LINE; CHEMOKINES; CYTOKINES; ENTEROTOXINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, NATURAL; KERATINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STAPHYLOCOCCUS AUREUS; SUPERANTIGENS; SWINE; VAGINA;

EID: 16244381104     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.4.2164-2174.2005     Document Type: Article

References (64)

1. Abbas, A. K., K. M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature 383:787-793.
2. Albanesi, C., A. Cavani, and G. Girolomoni. 1998. Interferon-gamma- stimulated human keratinocytes express the genes necessary for the production of peptide-loaded MHC class II molecules. J. Investig. Dermatol. 110:138-142.
3. Albanesi, C., C. Scarponi, S. Sebastiani, A. Cavani, M. Federici, S. Sozzani, and G. Girolomoni. 2001. A cytokine-to-chemokine axis between T lymphocytes and keratinocytes can favor Th1 cell accumulation in chronic inflammatory skin diseases. J. Leukoc. Biol. 70:617-623.
4. Anderson, D. J., J. A. Politch, L. D. Tucker, R. Fichorova, F. Haimovici, R. E. Tuomala, and K. H. Mayer. 1998. Quantitation of mediators of inflammation and immunity in genital tract secretions and their relevance to HIV type 1 transtnission. AIDS Res. Hum. Retrovir. 14(Suppl. 1):S43-S49.
5. Arad, G., R. Levy, D. Hillman, and R. Kaempfer. 2000. Superantigen antagonist protects against lethal shock and defines a new domain for T-cell activation. Nat. Med. 6:414-421.
6. Baggiolini, M. 1998. Chemokines and leukocyte traffic. Nature 392:565-568.
7. Banerjee, G., A. Damodaran, N. Devi, K. Dharmalingam, and G. Raman. 2004. Role of keratinocytes in antigen presentation and polarization of human T lymphocytes. Scand. J. Immunol. 59:385-394.
8. Bergdoll, M. S., B. A. Crass, R. F. Reiser, R. N. Robbins, and J. P. Davis. 1981. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet 1:1017-1021.
9. Beutler, B., K. Hoebe, X. Du, and R. J. Ulevitch. 2003. How we detect microbes and respond to them: the Toll-like receptors and their transducers. J. Leukoc. Biol. 74:479-485.
10. Blomster-Hautamaa, D. A., and P. M. Schlievert. 1988. Preparation of toxic shock syndrome toxin-1. Methods Enzymol. 165:37-43.
11. Centers for Disease Control and Prevention. 1999. Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus-Minnesota and North Dakota, 1997-1999. JAMA 282:1123-1125.
12. Charbonnier, A. S., N. Kohrgruber, E. Kriehuber, G. Stingl, A. Rot, and D. Maurer. 1999. Macrophage inflammatory protein 3alpha is involved in the constitutive trafficking of epidermal langerhans cells. J. Exp. Med. 190:1755-1768.
13. Davis, C. C., M. J. Kremer, P. M. Schlievert, and C. A. Squier. 2003. Penetration of toxic shock syndrome toxin-1 across porcine vaginal mucosa ex vivo: permeability characteristics, toxin distribution, and tissue damage. Am. J. Obstet. Gynecol. 189:1785-1791.
14. Davis, J. P., P. J. Chesney, P. J. Wand, and M. LaVenture. 1980. Toxic-shock syndrome: epidemiologic features, recurrence, risk factors, and prevention. N. Engl. J. Med. 303:1429-1435.
15. Dieu-Nosjean, M. C., C. Massacrier, B. Homey, B. Vanbervliet, J. J. Pin, A. Vicari, S. Lebecque, C. Dezutter-Dambuyant, D. Schmitt, A. Zlotnik, and C. Caux. 2000. Macrophage inflammatory protein Salpha is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 192:705-718.
16. Dinges, M. M., P. M. Orwin, and P. M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13:16-34.
17. Fey, P. D., B. Said-Salim, M. E. Rupp, S. H. Hinrichs, D. J. Boxrud, C. C. Davis, B. N. Kreiswirth, and P. M. Schlievert. 2003. Comparative molecular analysis of community- or hospital-acquired methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 47:196-203.
18. Fichorova, R. N., and D. J. Anderson. 1999. Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol. Reprod. 60:508-514.
19. Fichorova, R. N., A. O. Cronin, E. Lien, D. J. Anderson, and R. R. Ingalls. 2002. Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of toll-like receptor 4-mediated signaling. J. Immunol. 168:2424-2432.
20. Fichorova, R. N., P. J. Desai, F. C. Gibson III, and C. A. Genco. 2001. Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect. Immun. 69:5840-5848.
21. Fichorova, R. N., L. D. Tucker, and D. J. Anderson. 2001. The molecular basis of nonoxynol-9-induced vaginal inflammation and its possible relevance to human immunodeficiency virus type 1 transmission. J. Infect. Dis. 184:418-428.
22. Fields, B. A., E. L. Malchiodi, H. Li, X. Ysern, C. V. Stauffacher, P. M. Schlievert, K. Karjalainen, and R. A. Mariuzza. 1996. Crystal structure of a T-cell receptor beta-chain complexed with a superantigen, Nature 384:188-192.
23. Gromme, M., and J. Neetjes. 2002. Antigen degradation or presentation by MHC class I molecules via classical and non-classical pathways. Mol. Immunol. 39:181-202.
24. Gromme, M., F. G. Uytdehaag, H. Janssen, J. Calafat, R. S. van Binnendijk, M. J. Kenter, A. Tulp, D. Verwoerd, and J. Neefjes. 1999. Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. USA 96:10326-10331.
25. Haibert, C. L., G. W. Deniers, and D. A. Galloway. 1992. The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells. J. Virol. 66:2125-2134.
26. Harris, T. O., D. Grossman, J. W. Kappler, P. Marrack, R. R. Rich, and M. J. Betley. 1993. Lack of complete correlation between emetic and T-cell-stimulatory activities of staphylococcal enterotoxins. Infect. Immun. 61:3175-3183.
27. Hasseus, B., M. Jontell, G. Bergenholtz, and U. I. Dahlgren. 2004. T-cell costimulatory capacity of oral and skin epithelial cells in vitro: presence of suppressive activity in supernatants from skin epithelial cell cultures. Eur. J. Oral Sci. 112:48-54.
28. Homey, B., A. Muller, and A. Zlotnik. 2002. Chemokines: agents for the immunotherapy of cancer? Nat. Rev. Immunol. 2:175-184.
29. Kass, E. H., M. I. Kendrick, Y. C. Tsai, and J. Parsonnet. 1987. Interaction of magnesium ion, oxygen tension, and temperature in the production of toxic-shock-syndrome toxin-1 by Staphylococcus aureus. J. Infect. Dis. 155:812-815.
30. Kiyono, T., S. A. Foster, J. I. Koop, J. K. McDougall, D. A. Galloway, and A. J. Klingelhutz. 1998. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396:84-88.
31. Kushnarjov, V. M., M. S. Bergdoll, H. S. MacDonald, J. Vellinga, and R. Reiser. 1984. Study of staphylococcal toxic shock syndrome toxin in human epithelial cell culture. J. Infect. Dis. 150:535-545.
32. Kushnaryov, V. M., H. S. MacDonald, R. Reiser, and M. S. Bergdoll. 1984. Staphylococcal toxic shock toxin specifically binds to cultured human epithelial cells and is rapidly internalized. Infect. Immun. 45:566-571.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227:680-685.
34. Larkin, S. M., D. N. Williams, M. T. Osterholm, R. W. Tofte, and Z. Posalaky. 1982. Toxic shock syndrome: clinical, laboratory, and pathologic findings in nine fatal cases. Ann. Intern. Med. 96:858-864.
35. Li, H., A. Liera, E. L. Malchiodi, and R. A. Mariuzza. 1999. The structural basis of T cell activation by superantigens. Annu. Rev. Immunol. 17:435-466.
36. Li, H., A. Liera, D. Tsuchiya, L. Leder, X. Ysern, P. M. Schlievert, K. Karjalainen, and R. A. Mariuzza. 1998. Three-dimensional structure of the complex between a T cell receptor beta chain and the superantigen staphylococcal enterotoxin B. Immunity 9:807-816.
37. Li, Y., H. Li, N. Dimasi, J. K. McCormick, R. Martin, P. Schuck, P. M. Schlievert, and R. A. Mariuzza. 2001. Crystal structure of a superantigen bound to the high-affinity, zinc-dependent site on MHC class II. Immunity 14:93-104.
38. Luther, S. A., and J. G. Cyster. 2001. Chemokines as regulators of T cell differentiation. Nat. Immunol. 2:102-107.
39. Marrack, P., and J. Kappler. 1990. The staphylococcal enterotoxins and their relatives. Science 248:705-711.
40. McCormick, J. K., and P. M. Schlievert. 2000. Toxins and superantigens of group A streptococci, p. 43-52. in V. A. Fischetti, R. P. Novick, J. J. Ferretti, D. A. Portnoy, and J. I. Rood (ed.). Gram-positive pathogens. ASM Press, Washington, D.C.
41. McCormick, J. K., T. J. Tripp, A. S. Liera, E. J. Sundberg, M. M. Dinges, R. A. Mariuzza, and P. M. Schlievert. 2003. Functional analysis of the TCR binding domain of toxic shock syndrome toxin-1 predicts further diversity in MHC class II/superantigen/TCR ternary complexes. J. Immunol. 171:1385-1392.
42. McCormick, J. K., J. M. Yanvood, and P. M. Schlievert. 2001. Toxic shock syndrome and bacterial superantigens: an update. Annu. Rev. Microbiol. 55:77-104.
43. Murray, D. L., C. A. Earhart, D. T. Mitchell, D. H. Ohlendorf, R. P. Novick, and P. M. Schlievert. 1996. Localization of biologically important regions on toxic shock syndrome toxin 1. Infect. Immun. 64:371-374.
44. Murray, D. L., G. S. Prasad, C. A. Earhart, B. A. Leonard, B. N. Kreiswirth, R. P. Novick, D. H. Ohlendorf, and P. M. Schlievert. 1994. Immunobiologic and biochemical properties of mutants of toxic shock syndrome toxin-1. J. Immunol. 152:87-95.
45. Musser, J. M., P. M. Schlievert, A. W. Chow, P. Ewan, B. N. Kreiswirth, V. T. Rosdahl, A. S. Naidu, W. Witte, and R. K. Selander. 1990. A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome. Proc. Natl. Acad. Sci. USA 87:225-229.
46. Osterholm, M. T., J. P. Davis, R. W. Gibson, J. S. Mandel, L. A. Wintermeyer, C. M. Helms, J. C. Forfang, J. Rondeau, and J. M. Vergeront. 1982. Tri-state toxic-state syndrome study. I. Epidemiologic findings. J. Infect. Dis. 145:431-440.
47. Rajan, N., D. L. Pruden, H. Kaznari, Q. Cao, B. E. Anderson, J. L. Duncan, and A. J. Schaeffer. 2000. Characterization of an immortalized human vaginal epithelial cell line. J. Urol. 163:616-622.
48. Reingold, A. L., N. T. Hargrett, B. B. Dan, K. N. Shands, B. Y. Strickland, and C. V. Broome. 1982. Nonmenstrual toxic shock syndrome: a review of 130 cases. Ann. Intern. Med. 96:871-874.
49. Rogge, L. 2002. A genomic view of helper T cell subsets. Ann. N. Y. Acad. Sci. 975:57-67.
50. Rollins, B. J. 1997. Chemokines. Blood 90:909-928.
51. Romagnani, S. 1994. Lymphokine production by human T cells in disease states. Annu. Rev. Immunol. 12:227-257.
52. Schlievert, P. M. 1996. Effect of Merocel vaginal sponge on growth of Staphylococcus aureus and production of toxic shock syndrome-associated toxins. J. Am. Coll. Surg. 183:19-24.
53. Schlievert, P. M., and D. A. Blomster. 1983. Production of staphylococcal pyrogenic exotoxin type C: influence of physical and chemical factors. J. Infect. Dis. 147:236-242.
54. Schlievert, P. M., L. M. Jablonski, M. Roggiani, I. Sadler, S. Callantine, D. T. Mitchell, D. H. Ohlendorf, and G. A. Bohach. 2000. Pyrogenic toxin superantigen site specificity in toxic shock syndrome and food poisoning in animals. Infect. Immun. 68:3630-3634.
55. Schlievert, P. M., M. T. Osterholm, J. A. Kelly, and R. D. Nishimura. 1982. Toxin and enzyme characterization of Staphylococcus aureus isolates from patients with and without toxic shock syndrome. Ann. Intern. Med. 96:937-940.
56. Schlievert, P. M., K. N. Shands, B. B. Dan, G. P. Schmid, and R. D. Nishimura. 1981. Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic-shock syndrome. J. Infect. Dis. 143:509-516.
57. Schmuth, M., S. Neyer, C. Rainer, A. Grassegger, P. Fritsch, N. Romani, and C. Heufler. 2002. Expression of the C-C chemokine MIP-3 alpha/CCL20 in human epidermis with impaired permeability barrier function. Exp. Dermatol. 11:135-142.
58. Shands, K. N., G. P. Schmid, B. B. Dan, D. Blum, R. J. Guidotti, N. T. Hargrett, R. L. Anderson, D. L. Hill, C. V. Broome, J. D. Band, and D. W. Fraser. 1980. Toxic-shock syndrome in menstruating women: association with tampon use and Staphylococcus aureus and clinical features in 52 cases. N. Engl. J. Med. 303:1436-1442.
59. Shehin, S. E., M. B. Jones, A. E. Hochwalt, F. C. Sarbaugh, and S. Nunn. 2003. Clinical safety-in-use study of a new tampon design. Infect. Dis. Obstet. Gynecol. 11:89-99.
60. Shupp, J. W., M. Jett, and C. H. Pontzer. 2002. Identification of a transcytosis epitope on staphylococcal enterotoxins. Infect. Immun. 70:2178-2186.
61. Thompson, I. O., P. van der Bijl, C. W. van Wyk, and A. D. van Eyk. 2001. A comparative light-microscopic, electron-microscopic and chemical study of human vaginal and buccal epithelium. Arch. Oral Biol. 46:1091-1098.
62. von Aulock, S., S. Morath, L. Hareng, S. Knapp, K. P. van Kessel, J. A. van Stryp, and T. Hartung. 2003. Lipoteichoic acid from Staphylococcus aureus is a potent stimulus for neutrophil recruitment. Immunobiology 208:413-422.
63. Yarwood, J. M., J. K. McCorraick, M. L. Paustian, V. Kapur, and P. M. Schlievert. 2002. Repression of the Staphylococcus aureus accessory gene regulator in serum and in vivo. J. Bacteriol. 184:1095-1101.
64. Yarwood, J. M., and P. M. Schlievert. 2000. Oxygen and carbon dioxide regulation of toxic shock syndrome toxin 1 production by Staphylococcus aureus MN8. J. Clin. Microbiol. 38:1797-1803.