Toll-like receptors in female reproductive tract and their menstrual cycle dependent expression

Journal of Reproductive Immunology

Volumn 77, Issue 1, 2008, Pages 7-13

  Aflatoonian, Reza ^a   Fazeli, Alireza ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Female reproductive tract; Menstrual cycle; Sex hormones; Toll like receptors

Indexed keywords

GRANULOCYTE CHEMOTACTIC PROTEIN 2; INTERLEUKIN 6; INTERLEUKIN 8; SEX HORMONE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9;

ARTICLE; ENDOMETRIUM; FEMALE GENITAL SYSTEM; HUMAN; INNATE IMMUNITY; MENSTRUAL CYCLE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; UTERINE ENDOCERVIX;

ANIMALS; FEMALE; GENITALIA, FEMALE; GONADAL STEROID HORMONES; HUMANS; IMMUNITY, NATURAL; MENSTRUAL CYCLE; PREGNANCY; RNA, MESSENGER; TOLL-LIKE RECEPTORS;

EID: 38349016581     PISSN: 01650378     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jri.2007.03.014     Document Type: Article

References (69)

1. Abrahams V.M., Bole-Aldo P., Kim Y.M., Straszewski-Chavez S.L., Chaiworapongsa T., Romero R., and Mor G. Divergent trophoblast responses to bacterial products mediated by TLRs. J. Immunol. 173 (2004) 4286-4296
2. Abrahams V.M., and Mor G. Toll-like receptors and their role in the trophoblast. Placenta 26 (2005) 540-547
3. Abrahams V.M., Schaefer T.M., Fahey J.V., Visintin I., Wright J.A., Aldo P.B., Romero R., Wira C.R., and Mor G. Expression and secretion of antiviral factors by trophoblast cells following stimulation by the TLR-3 agonist, poly(I:C). Hum. Reprod. 21 (2006) 2432-2439
4. Abrahams V.M., Visintin I., Aldo P.B., Guller S., Romero R., and Mor G. A role for TLRs in the regulation of immune cell migration by first trimester trophoblast cells. J. Immunol. 175 (2005) 8096-8104
5. Aflatoonian R., Tuckerman E., Elliott S.L., Bruce C., Aflatoonian A., Li T.C., and Fazeli A. Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum. Reprod. 22 (2007) 586-593
6. Akashi S., Nagai Y., Ogata H., Oikawa M., Fukase K., Kusumoto S., Kawasaki K., Nishijima M., Hayashi S., Kimoto M., et al. Human MD-2 confers on mouse Toll-like receptor 4 species-specific lipopolysaccharide recognition. Int. Immunol. 13 (2001) 1595-1599
7. Akira S., Takeda K., and Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2 (2001) 675-680
8. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001) 732-738
9. Andersen J.M., Al-Khairy D., and Ingalls R.R. Innate immunity at the mucosal surface: role of toll-like receptor 3 and toll-like receptor 9 in cervical epithelial cell responses to microbial pathogens. Biol. Reprod. 74 (2006) 824-831
10. Anderson K.V., Bokla L., and Nusslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product. Cell 42 (1985) 791-798
11. Anderson K.V., Jurgens G., and Nusslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42 (1985) 779-789
12. Arechavaleta-Velasco F., Koi H., Strauss III J.F., and Parry S. Viral infection of the trophoblast: time to take a serious look at its role in abnormal implantation and placentation?. J. Reprod. Immunol. 55 (2002) 113-121
13. Belvin M.P., and Anderson K.V. A conserved signaling pathway: the Drosophila toll-dorsal pathway. Annu. Rev. Cell. Dev. Biol. 12 (1996) 393-416
14. Chuang T., and Ulevitch R.J. Identification of hTLR10: a novel human Toll-like receptor preferentially expressed in immune cells. Biochim. Biophys. Acta 1518 (2001) 157-161
15. Chuang T.H., and Ulevitch R.J. Cloning and characterization of a sub-family of human toll-like receptors: hTLR7, hTLR8 and hTLR9. Eur. Cytokine Netw. 11 (2000) 372-378
16. Elovitz M.A., Wang Z., Chien E.K., Rychlik D.F., and Phillippe M. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and Toll-like receptor-4. Am. J. Pathol. 163 (2003) 2103-2111
17. Fazeli A., Bruce C., and Anumba D.O. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum. Reprod. 20 (2005) 1372-1378
18. Fichorova R.N., Cronin A.O., Lien E., Anderson D.J., and 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 (2002) 2424-2432
19. Flacher V., Bouschbacher M., Verronese E., Massacrier C., Sisirak V., Berthier-Vergnes O., de Saint-Vis B., Caux C., Dezutter-Dambuyant C., Lebecque S., et al. Human langerhans cells express a specific TLR profile and differentially respond to viruses and gram-positive bacteria. J. Immunol. 177 (2006) 7959-7967
20. Givan A.L., White H.D., Stern J.E., Colby E., Gosselin E.J., Guyre P.M., and Wira C.R. Flow cytometric analysis of leukocytes in the human female reproductive tract: comparison of fallopian tube, uterus, cervix and vagina. Am. J. Reprod. Immunol. 38 (1997) 350-359
21. Grossman C.J. Interactions between the gonadal steroids and the immune system. Science 227 (1985) 257-261
22. Hasan U., Chaffois C., Gaillard C., Saulnier V., Merck E., Tancredi S., Guiet C., Briere F., Vlach J., Lebecque S., et al. Human TLR10 is a functional receptor, expressed by B cells and plasmacytoid dendritic cells, which activates gene transcription through MyD88. J. Immunol. 174 (2005) 2942-2950
23. Hayashi F., Smith K.D., Ozinsky A., Hawn T.R., Yi E.C., Goodlett D.R., Eng J.K., Akira S., Underhill D.M., and Aderem A. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410 (2001) 1099-1103
24. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., et al. Toll-like receptor recognizes bacterial DNA. Nature 408 (2000) 740-745
25. Hirata T., Osuga Y., Hirota Y., Koga K., Yoshino O., Harada M., Morimoto C., Yano T., Nishii O., Tsutsumi O., et al. Evidence for the presence of toll-like receptor 4 system in the human endometrium. J. Clin. Endocrinol. Metab. 90 (2005) 548-556
26. Holmlund U., Cebers G., Dahlfors A.R., Sandstedt B., Bremme K., Ekstrom E.S., and Scheynius A. Expression and regulation of the pattern recognition receptors Toll-like receptor-2 and Toll-like receptor-4 in the human placenta. Immunology 107 (2002) 145-151
27. Hsu C.D., and Witter F.R. Urogenital infection in preeclampsia. Int. J. Gynaecol. Obstet. 49 (1995) 271-275
28. Hunt J.S. Immunologically relevant cells in the uterus. Biol. Reprod. 50 (1994) 461-466
29. Itoh H., Nasu K., Nishida M., Matsumoto H., Yuge A., and Narahara H. Human oviductal stromal fibroblasts, but not oviductal epithelial cells, express Toll-like receptor 4: the site-specific mucosal immunity of the human fallopian tube against bacterial infection. Am. J. Reprod. Immunol. 56 (2006) 91-101
30. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 20 (2002) 197-216
31. Jorgenson R.L., Young S.L., Lesmeister M.J., Lyddon T.D., and Misfeldt M.L. Human endometrial epithelial cells cyclically express Toll-like receptor 3 (TLR3) and exhibit TLR3-dependent responses to dsRNA. Hum. Immunol. 66 (2005) 469-482
32. Jurk M., Heil F., Vollmer J., Schetter C., Krieg A.M., Wagner H., Lipford G., and Bauer S. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat. Immunol. 3 (2002) 499
33. Kariko K., Ni H., Capodici J., Lamphier M., and Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J. Biol. Chem. 279 (2004) 12542-12550
34. Kumazaki K., Nakayama M., Yanagihara I., Suehara N., and Wada Y. Immunohistochemical distribution of Toll-like receptor 4 in term and preterm human placentas from normal and complicated pregnancy including chorioamnionitis. Hum. Pathol. 35 (2004) 47-54
35. Lamont R.F. Infection in the prediction and antibiotics in the prevention of spontaneous preterm labour and preterm birth. Br. J. Obstet. Gynaecol. 110 Suppl. 20 (2003) 71-75
36. Lesmeister M.J., Jorgenson R.L., Young S.L., and Misfeldt M.L. 17Beta-estradiol suppresses TLR3-induced cytokine and chemokine production in endometrial epithelial cells. Reprod. Biol. Endocrinol. 3 (2005) 74
37. Medzhitov R., and Janeway Jr. C. The Toll receptor family and microbial recognition. Trends Microbiol. 8 (2000) 452-456
38. Medzhitov R., and Janeway Jr. C.A. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9 (1997) 4-9
39. Medzhitov R., and Janeway Jr. C.A. Decoding the patterns of self and nonself by the innate immune system. Science 296 (2002) 298-300
40. Nagai Y., Akashi S., Nagafuku M., Ogata M., Iwakura Y., Akira S., Kitamura T., Kosugi A., Kimoto M., and Miyake K. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3 (2002) 667-672
41. Nakao Y., Funami K., Kikkawa S., Taniguchi M., Nishiguchi M., Fukumori Y., Seya T., and Matsumoto M. Surface-expressed TLR6 participates in the recognition of diacylated lipopeptide and peptidoglycan in human cells. J. Immunol. 174 (2005) 1566-1573
42. Nasu K., Itoh H., Yuge A., Nishida M., and Narahara H. Human oviductal epithelial cells express Toll-like receptor 3 and respond to double-stranded RNA: fallopian tube-specific mucosal immunity against viral infection. Hum. Reprod. 22 (2007) 356-361
43. Nurkkala M., Nordstrom I., Telemo E., and Eriksson K. MHC expression and chemokine production in the murine vagina following intra-vaginal administration of ligands to Toll-like receptors 3, 7 and 9. J. Reprod. Immunol. 73 (2007) 148-157
44. Ozinsky A., Underhill D.M., Fontenot J.D., Hajjar A.M., Smith K.D., Wilson C.B., Schroeder L., and Aderem A. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 13766-13771
45. Pasare C., and Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Microbes Infect. 6 (2004) 1382-1387
46. Pioli P.A., Amiel E., Schaefer T.M., Connolly J.E., Wira C.R., and Guyre P.M. Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract. Infect. Immun. 72 (2004) 5799-5806
47. Pivarcsi A., Nagy I., Koreck A., Kis K., Kenderessy-Szabo A., Szell M., Dobozy A., and Kemeny L. Microbial compounds induce the expression of pro-inflammatory cytokines, chemokines and human beta-defensin-2 in vaginal epithelial cells. Microbes Infect. 7 (2005) 1117-1127
48. Rock F.L., Hardiman G., Timans J.C., Kastelein R.A., and Bazan J.F. A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 588-593
49. Schaefer T.M., Desouza K., Fahey J.V., Beagley K.W., and Wira C.R. Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 112 (2004) 428-436
50. Schaefer T.M., Fahey J.V., Wright J.A., and Wira C.R. Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J. Immunol. 174 (2005) 992-1002
51. Schwandner R., Dziarski R., Wesche H., Rothe M., and Kirschning C.J. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J. Biol. Chem. 274 (1999) 17406-17409
52. Soboll G., Schaefer T.M., and Wira C.R. Effect of toll-like receptor (TLR) agonists on TLR and microbicide expression in uterine and vaginal tissues of the mouse. Am. J. Reprod. Immunol. 55 (2006) 434-446
53. Soboll G., Shen L., and Wira C.R. Expression of Toll-like receptors (TLR) and responsiveness to TLR agonists by polarized mouse uterine epithelial cells in culture. Biol. Reprod. 75 (2006) 131-139
54. Spornitz U.M. The functional morphology of the human endometrium and decidua. Adv. Anat. Embryol. Cell. Biol. 124 (1992) 1-99
55. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int. Immunol. 17 (2005) 1-14
56. Takeda K., Kaisho T., and Akira S. Toll-like receptors. Annu. Rev. Immunol. 21 (2003) 335-376
57. Takeuchi O., Sato S., Horiuchi T., Hoshino K., Takeda K., Dong Z., Modlin R.L., and Akira S. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169 (2002) 10-14
58. Underhill D.M., Ozinsky A., Smith K.D., and Aderem A. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 14459-14463
59. Varner M.W., and Esplin M.S. Current understanding of genetic factors in preterm birth. Br. J. Obstet. Gynecol. 112 Suppl. 1 (2005) 28-31
60. von Dadelszen P., Magee L.A., Krajden M., Alasaly K., Popovska V., Devarakonda R.M., Money D.M., Patrick D.M., and Brunham R.C. Levels of antibodies against cytomegalovirus and Chlamydophila pneumoniae are increased in early onset pre-eclampsia. Br. J. Obstet. Gynecol. 110 (2003) 725-730
61. Wetzler L.M. The role of Toll-like receptor 2 in microbial disease and immunity. Vaccine 21 Suppl. 2 (2003) S55-S60
62. Wira C.R., Fahey J.V., Sentman C.L., Pioli P.A., and Shen L. Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol. Rev. 206 (2005) 306-335
63. Wira C.R., Grant-Tschudy K.S., and Crane-Godreau M.A. Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am. J. Reprod. Immunol. 53 (2005) 65-76
64. Yarovinsky F., and Sher A. Toll-like receptor recognition of Toxoplasma gondii. Int. J. Parasitol. 36 (2006) 255-259
65. Yarovinsky F., Zhang D., Andersen J.F., Bannenberg G.L., Serhan C.N., Hayden M.S., Hieny S., Sutterwala F.S., Flavell R.A., Ghosh S., et al. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308 (2005) 1626-1629
66. Yeaman G.R., Guyre P.M., Fanger M.W., Collins J.E., White H.D., Rathbun W., Orndorff K.A., Gonzalez J., Stern J.E., and Wira C.R. Unique CD8+ T cell-rich lymphoid aggregates in human uterine endometrium. J. Leukoc. Biol. 61 (1997) 427-435
67. Young S.L., Lyddon T.D., Jorgenson R.L., and Misfeldt M.L. Expression of Toll-like receptors in human endometrial epithelial cells and cell lines. Am. J. Reprod. Immunol. 52 (2004) 67-73
68. Zarember K.A., and Godowski P.J. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol. 168 (2002) 554-561
69. Zhang D., Zhang G., Hayden M.S., Greenblatt M.B., Bussey C., Flavell R.A., and Ghosh S. A Toll-like receptor that prevents infection by uropathogenic bacteria. Science 303 (2004) 1522-1526