Innate immunity in the female reproductive tract: Role of sex hormones in regulating uterine epithelial cell protection against pathogens

Current Women's Health Reviews

Volumn 4, Issue 2, 2008, Pages 102-117

  Ochiel, Daniel O ^a   Fahey, John V ^a   Ghosh, Mimi ^a   Haddad, Severina N ^a   Wira, Charles R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Antigen presenting cells; EGF receptor; HIV; Insulin Like Growth Factor I; Macrophage Chemotactic Factor; Toll Like Receptors

Indexed keywords

CHEMOKINE; CYTOKINE; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; IMMUNOGLOBULIN; KERATINOCYTE GROWTH FACTOR; MICROBICIDE; SCATTER FACTOR; SEX HORMONE; SOMATOMEDIN C; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; CELL FUNCTION; CELL PROTECTION; ENDOMETRIUM CELL; FEMALE GENITAL SYSTEM; FERTILIZATION; HORMONAL REGULATION; HORMONE ACTION; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; MUCOSAL IMMUNITY; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; REPRODUCTIVE HEALTH; REVIEW; SEXUALLY TRANSMITTED DISEASE; SURVIVAL; TIGHT JUNCTION; UTERUS FUNCTION; WOMEN'S HEALTH;

EID: 47749117663     PISSN: 15734048     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340408784246395     Document Type: Review

References (226)

1. UNAIDS 2007. AIDS epidemic update JUNPoHAUaWHOW, Geneva, Switzerland 2007.
2. Padian N, van der Straten A, Ramjee G, et al. Diaphragm and lubricant gel for prevention of HIV acquisition in southern African women: a randomised controlled trial. Lancet 2007; 370: 251-61.
3. Cohen J. AIDS research. Promising AIDS vaccine's failure leaves field reeling. Science 2007; 318: 28-29.
4. Cohen J. Promising prevention interventions perform poorly in trials. Science 2007; 317: 440.
5. Editorial team. Phase III anti-HIV microbicide trial in Africa and India stopped as preliminary results show gel may increase risk of infection. Euro Surveill 2007; 12: E070208.6.
6. Honey K. Microbicide trial screeches to a halt. J Clin Invest 2007; 117: 1116.
7. Piot P. UNAIDS Executive Director. San Francisco Chronicle (May 9, 2007) 2007.
8. Ogra P, Yamanaka T, Losonsky GA. Local immunologic defenses in the genital tract. In: Fleicher N, ed. Reproductive Immunology. New York: Alan R. Liss, Inc. 1981; pp. 381-94.
9. Fahey JV, Wira CR. Effect of menstrual status on antibacterial activity and secretory leukocyte protease inhibitor production by human uterine epithelial cells in culture. J Infect Dis 2002; 185: 1606-13.
10. Wira CR, Fahey JV, Schaefer TM, et al. Innate and adaptive immunity in the human female reproductive tract: influence of the menstrual cycle and menopause on the mucosal immune system in the uterus. In: Glasser S, Aplin J, Giudice L, Tabibzadeh S, eds. The Endometrium 2007; pp. 491-521.
11. Wira CR, Richardson J, Prabhala R. Endocrine regulation of mucosal immunity: effect of sex hormones and cytokines on the afferent and efferent arms of the immune system in the female reproductive tract. In: Ogra PL, Mestecky J, Lamm ME, et al., eds. Handbook of Mucosal Immunology. New York: Academic Press. 1994; pp. 705-18.
12. Kutteh WH, Mestecky J, Wira CR. Mucosal immune system in the human female reproductive tract. In: Mestecky J LM, Strober W, Bienenstock J, McGhee JR and Mayer L, eds. Mucosal Immunology. 3rd Edition ed. Burlington, MA: Elselvier Academic Press. 2005; pp. 1631-46.
13. Wira CR, Crane-Godreau MA, Grant-Tschudy KS. Endocrine regulation of mucosal immune system in the female reproductive tract. In: Mestecky J, Lamm M, Strober W, et al., eds. Mucosal Immunology. Burlington, MA: Elselvier Academic Press 2005; pp. 1661-78.
14. Godfrey RWA. Human airway epithelial tight junctions. Microscopy Res Tech 1997; 38: 488-99.
15. Simons K, Wandinger-Ness A. Polarized sorting in epithelia. Cell 1990; 62: 207-10.
16. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol 2006; 22: 207-35.
17. Matter K, Aijaz S, Tsapara A, et al. Mammalian tight junctions in the regulation of epithelial differentiation and proliferation. Curr Opin Cell Biol 2005; 17: 453-8.
18. Planchon S, Fiocchi C, Takafuji V, et al. Transforming growth factor-beta1 preserves epithelial barrier function: identification of receptors, biochemical intermediates and cytokine antagonists. J Cell Physiol 1999; 181: 55-66.
19. Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001; 2: 285-93.
20. Crane-Godreau MA, Wira CR. CCL20/macrophage inflammatory protein 3alpha and tumor necrosis factor alpha production by primary uterine epithelial cells in response to treatment with lipopolysaccharide or Pam3Cys. Infect Immun 2005; 73: 476-84.
21. Fahey JV, Prabhala RH, Guyre PM, et al. Antigen-presenting cells in the human female reproductive tract: analysis of antigen presentation in pre- and post-menopausal women. Am J Reprod Immunol 1999; 42: 49-57.
22. Grant KS, Wira CR. Effect of mouse uterine stromal cells on epithelial cell transepithelial resistance (TER) and TNFalpha and TGFbeta release in culture. Biol Reprod 2003; 69: 1091-8.
23. Kaushic C, Wira CR. IgA and Reproductive Tract Immunity. In: Kaetzel C, ed. Mucosal Immune Defense: Immunoglobulin A. New York: Kluwer Academic/ Plenum Publisher. 2008; pp. 291-320.
24. Gruber CJ, Tschugguel W, Schneeberger C, et al. Production and actions of estrogens. N Engl J Med 2002; 346: 340-52.
25. Grant-Tschudy KS, Wira CR. Paracrine mediators of mouse uterine epithelial cell transepithelial resistance in culture. J Reprod Immunol 2005; 67: 1-12.
26. Grant-Tschudy KS, Wira CR. Hepatocyte growth factor regulation of uterine epithelial cell transepithelial resistance and tumor necrosis factor {alpha} release in culture. Biol Reprod 2004; 72: 814-21.
27. Groten T, Pierce AA, Huen AC, et al. 17 beta-estradiol transiently disrupts adherens junctions in endothelial cells. FASEB J 2005; 19: 1368-70.
28. Phillips ML, Schultz BD. Steroids modulate transepithelial resistance and Na+ absortion across cultured porcine vas deferens epithelia. Biol Reprod 2002; 66: 1016-23.
29. Schaefer TM, Desouza K, Fahey JV, et al. Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 2004; 112: 428-36.
30. Schaefer TM, Fahey JV, Wright JA, et al. Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J Immunol 2005; 174: 992-1002.
31. Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 2004; 127: 224-38.
32. Yi X, Wang Y, Yu FS. Corneal epithelial fight junctions and their response to lipopolysaccharide challenge. Invest Ophthalmol Vis Sci 2000; 41: 4093-100.
33. Zech JC, Pouvreau I, Cotinet A, et al. Effect of cytokines and nitric oxide on tight junctions in cultured rat retinal pigment epithelium. Invest Ophthalmol Vis Sci 1998; 39: 1600-8.
34. Chen J, Tsang LL, Ho LS, et al. Modulation of human enteric epithelial barrier and ion transport function by Peyer's patch lymphocytes. World J Gastroenterol 2004; 10: 1594-9.
35. Lorenzo-Zuniga V, Rodriguez-Ortigosa CM, Bartoli R, et al. Insulin-like growth factor-I improves intestinal barrier function in cirrhotic rats. Gut 2006; 55: 1306-12.
36. Lytton SD, Fischer W, Nagel W, et al. Production of ammonium by Helicobacter pylori mediates occludin processing and disruption of tight junctions in Caco-2 cells. Microbiology 2005; 151: 3267-76.
37. Terres AM, Pajares JM, Hopkins AM, et al. Helicobacter pylori disrupts epithelial barrier function in a process inhibited by protein kinase C activators. Infect Immun 1998; 66: 2943-50.
38. Ciarlet M, Crawford SE, Estes MK. Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acid-independent rotavirus strains. J Virol 2001; 75: 11834-50.
39. Tafazoli F, Magnusson KE, Zheng L. Disruption of epithetial barrier integrity by Salmonella enterica serovar typhimurium requires geranylgeranylated proteins. Infect Immun 2003; 71: 872-81.
40. Muza-Moons MM, Koutsouris A, Hecht G. Disruption of cell polarity by enteropathogenic Escherichia coli enables basolateral membrane proteins to migrate apically and to potentiate physiological consequences. Infect Immun 2003; 71: 7069-78.
41. Chakravortty D, Kumar KS. Modulation of barrier function of small intestinal epithelial cells by lamina propria fibroblasts in response to lipopolysaccharide: possible role in TNFalpha in inducing barrier dysfunction. Microbiol Immunol 1999; 43: 527-33.
42. Czerucka D, Dahan S, Mograbi B, et al. Saccharomyces boulardii preserves the barrier function and modulates the signal transduction pathway induced in enteropathogenic Escherichia coli-infected T84 cells. Infect Immun 2000; 68: 5998-6004.
43. Resta-Lenert S, Barrett KE. Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 2006; 130: 731-46.
44. Fichorova RN, Zbou F, Ratnam V, et al. Anti-human immunodeficiency virus type 1 microbicide cellulose acetate 1,2-benzenedicarboxylate in a human in vitro model of vaginal inflammation. Antimicrob Agents Chemother 2005; 49: 323-35.
45. Dezzutti CS, James VN, Ramos A, et al. In vitro comparison of topical microbicides for prevention of human immunodeficiency virus type 1 transmission. Antimicrob Agents Chemother 2004; 48: 3834-44.
46. Maher S, McClean S. Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem Pharmacol 2006; 71: 1289-98.
47. Marinaro M, Fasano A, De Magistris MT. Zonula occludens toxin acts as an adjuvant through different mucosal routes and induces protective immune responses. Infect Immun 2003; 71: 1897-902.
48. Cooke PS, Buchanan DL, Kurita T, et al. Role of stromal-epithelial interactions in hormonal responses of the uterus. In: Glasser SR, Aplin JD, Giudice LC, Tabibzadeh S, eds. The Endometrium. New York: Taylor & Francis. 2002; pp. 151-66.
49. Cunha GR. Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Mullerian ducts and urogenital sinus during development of the uterus and vagina in mice. J Exp Zool 1976; 196: 361-70.
50. Cunha GR, Young P. Role of stroma in oestrogen-induced epithelial proliferation. Epithelial Cell Biol 1992; 1: 18-31.
51. Cooke PS, Buchanan DL, Young P, et al. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci U S A 1997; 94: 6535-40.
52. Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mot Endocrinol 2003; 17: 309-17.
53. Shupnik MA. Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene 2004; 23: 7979-89.
54. Carpenter G, Cohen S. Epidermal growth factor. J Biol Chem 1990; 265: 7709-12.
55. Imai T, Kurachi H, Adachi K, et al. Changes in epidermal growth factor receptor and the levels of its figands during menstrual cycle in human endometrium. Biol Reprod 1995; 52: 928-38.
56. Moller B, Rasmussen C, Lindblom B, et al. Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometriurn during the menstrual cycle. Mol Hum Reprod 2001; 7: 65-72.
57. Ejskjaer K, Sorensen BS, Poulsen SS, et al. Expression of the epidermal growth factor system in human endometrium during the menstrual cycle. Mot Hum Reprod 2005; 11: 543-51.
58. Lee AV, Cui X, Oesterreich S. Cross-talk among estrogen receptor, epidermal growth factor, and insulin-like growth factor signaling in breast cancer. Clin Cancer Res 2001; 7: 4429s-35s; discussion 11s-12s.
59. Murphy LJ, Ghahary A. Uterine insulin-like growth factor-1: regulation of expression and its role in estrogen-induced uterine proliferation. Endocr Rev 1990; 11: 443-53.
60. Woelfle J, Chia DJ, Massart-Schlesinger MB, et al. Molecular physiology, pathology, and regulation of the growth hormone/insulin-like growth factor-I system. Pediatr Nephrol 2005; 20: 295-302.
61. Rutanen EM. Insulin-like growth factors in endometrial function. Gynecol Endocrinol 1998; 12: 399-406.
62. Moyano P, Rotwein P. Mini-review: estrogen action in the uterus and insulin-like growth factor-L Growth Horm IGF Res 2004; 14: 431-5.
63. Pollack AL, Runyan RB, Mostov KE. Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev Biol 1998; 204: 64-79.
64. Murakami S, Miyamoto Y, Fujiwara C, et al. Expression and action of hepatocyte growth factor in bovine endometrial stromal and epithelial cells in vitro. Mot Reprod Dev 2001; 60: 472-80.
65. Pollack AL, Apodaca G, Mostov KE. Hepatocyte growth factor induces MDCK cell morphogenesis without causing loss of tight junction functional integrity. Am J Physiol Cell Pbysiol 2004; 286: C482-94.
66. Nasu K, Sugano T, Matsui N, et al. Expression of hepatocyte growth factor in cultured human endometrial stromal cells is induced through a protein kinase C-dependent pathway. Biol Reprod 1999; 60: 1183-7.
67. Yang XM, Park M. Expression of the hepatocyte growth factor/scatter factor receptor tyrosine kinase is localized to epithelia in the adult mouse. Lab Invest 1995; 73: 483-91.
68. Chen C, Spencer TE, Bazer FW. Expression of hepatocyte growth factor and its receptor c-met in the ovine uterus. Biol Reprod 2000; 62: 1844-50.
69. Khan KN, Masuzaki H, Fujishita A, et al. Immunoexpression of hepatocyte growth factor and c-Met receptor in the eutopic endometrium predicts the activity of ectopic endometrium. Fertil Steril 2003; 79: 173-81.
70. Zhang HZ, Bennett JM, Smith KT, et al. Estrogen mediates mammary epithelial cell proliferation in serum-free culture indirectly via mammary stroma-derived hepatocyte growth factor. Endocrinology 2002; 143: 3427-34.
71. Imagawa W, Pedchenko VK, Helber J, et al. Hormone/growth factor interactions mediating epithelial/stromal communication in mammary gland development and carcinogenesis. J Steroid Biochem Mol Biol 2002; 80: 213-30.
72. Negami AI, Sasaki H, Kawakami Y, et al. Serum human hepatocyte growth factor in human menstrual cycle and pregnancy: a novel serum marker of regeneration and reconstruction of human endometrium. Horm Res 1995; 44 (Suppl 2): 42-6.
73. Rubin JS, Osada H, Finch PW, et al. Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci USA 1989; 86: 802-6.
74. Finch PW, Rubin JS, Miki T, et al. Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 1989; 245: 752-5.
75. Hom YK, Young P, Thomson AA, et al. Keratinocyte growth factor injected into female mouse neonates stimulates uterine and vaginal epithelial growth. Endocrinology 1998; 139: 3772-9.
76. Miki T, Bottaro DP, Fleming TP, et al. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci USA 1992; 89: 246-50.
77. Bottaro DP, Rubin JS, Ron D, et al. Characterization of the receptor for keratinocyte growth factor. Evidence for multiple fibroblast growth factor receptors. J Biol Chem 1990; 265: 12767-70.
78. Pedchenko VK, Imagawa W. Estrogen treatment in vivo increases keratinocyte growth factor expression in the marnmary gland. J Endocrinol 2000; 165: 39-49.
79. Pekonen F, Nyman T, Rutanen EM. Differential expression of keratinocyte growth factor and its receptor in the human uterus. Mol Cell Endocrinol 1993; 95: 43-9.
80. Siegfried S, Pekonen F, Nyman T, et al. Expression of mRNA for keratinocyte growth factor and its receptor in human endometrium. Acta Obstet Gynecol Scand 1995; 74: 410-4.
81. Koji T, Chedid M, Rubin JS, et al. Progesterone-dependent expression of keratinocyte growth factor mRNA in stromal cells of the primate endometrium: keratinocyte growth factor as a progestomedin. J Cell Biol 1994; 125: 393-401.
82. Pedchenko VK, Imagawa WT. Mammogenic hormones differentially modulate keratinocyte growth factor (KGF)-induced proliferation and KGF receptor expression in cultured mouse mammary gland epithelium. Endocrinology 1998; 139: 2519-26.
83. Imagawa W, Pedchenko VK. In vivo inhibition of keratinocyte growth factor receptor expression by estrogen and antagonism by progesterone in the mouse mammary gland. J Endocrinol 2001; 171: 319-27.
84. Li Y, Rinehart CA. Regulation of keratinocyte growth factor expression in human endometrium: implications for hormonal carcinogenesis. Mot Carcinog 1998; 23: 217-25.
85. Siegfried S, Pekonen F, Nyman T, et al. Distinct patterns of expression of keratiriocyte growth factor and its receptor in endometrial carcinoma. Cancer 1997; 79: 1166-71.
86. Taniguchi F, Harada T, Sakamoto Y, et al. Activation of mitogen-activated protein kinase pathway by kCTatinocyte growth factor or fibroblast growth factor-10 promotes cell proliferation in human endometrial carcinoma cells. J Clin Endocrinol Metab 2003; 88: 773-80.
87. Zang XP, Pento JT. Keratinocyte growth factoT-induced motility of breast cancer cells. Clin Exp Metastasis 2001; 18: 573-80.
88. Tamaru N, Hishikawa Y, Ejima K, et al. Estrogen receptor-associated expression of keratinocyte growth factor and its possible role in the inhibition of apoptosis in human breast cancer. Lab Invest 2004; 84: 1460-71.
89. Hishikawa Y, Tamaru N, Ejima K, et al. Expression of keratinocyte growth factor and its receptor in human breast cancer: its inhibitory role in the induction of apoptosis possibly through the over-expression of Bcl-2. Arch Histol Cytol 2004; 67: 455-64.
90. Yang D, Chen Q, Hoover DM, et al. Many chemokines including CCL20/ MIP-3alpha display antimicrobial activity. J Leukoc Biol 2003; 74: 448-55.
91. Perez-Canadillas JM, Zaballos A, Gutierrez J, et al. NMR solution structure of murine CCL20/MIP-3 alpha, a chemokine that specifically chemoattracts immature dendritic cells and lymphocytes through its highly specific interaction with the beta-chemokine receptor CCR6. J Biol Chem 2001; 276: 28372-9.
92. Taniguchi F, Harada, T, Yoshida S, et al. Paracrine effects of bFGF and KGF on the process of mouse blastocyst implantation. Mol Reprod Dev 1998; 50: 54-62.
93. Slayden OD, Rubin JS, Lacey DL, et al. Effects of keratinocyte growth factor in the endometrium of Thesus macaques during the luteal-follicular transition. J Clin Endocrinol Metab 2000; 85: 275-85.
94. Matsui H, Taga M, Kurogi K, et al. Gene expressions of keratinocyte growth factor and its receptor in the human endometrium/ decidua and chorionic villi. Endocr J 1997; 44: 867-71.
95. Mascia F, Mariani V, Girolomoni G, et al. Blockade of the EGF receptor induces a deranged chemokine expression in keratinocytes leading to enhanced skin inflammation. Am J Pathol 2003; 163: 303-12.
96. Mikami F, Gu H, Jono H, et al. Epidermal growth factor receptor acts as a negative regulator for bacterium nontypeable Haemophilus influenzae-induced Toll-like receptor 2 expression via an Src-dependent p38 mitogen-activated protein kinase signaling pathway. J Biol Chem 2005; 280: 36185-94.
97. Huang W, Rothe MJ, Grant-Kels JM. The burning mouth syndrome. J Am Acad Dermatol 1996; 34: 91-8.
98. Congote LF. Monitoring insulin-like growth factors in HIV infection and AIDS. Clin Chim Acta 2005; 361: 30-53.
99. Wira CR, Rossoll RM. Antigen-presenting cells in the female reproductive tract: influence of sex hormones on antigen presentation in the vagina. Immunology 1995; 84: 505-8.
100. Pudney J, Quayle AJ, Anderson DJ. Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation zone. Biol Reprod 2005; 73: 1253-63.
101. Fahey JV, Wallace PK, Johnson K, et al. Antigen presentation by human uterine epithelial cells to autologous T cells. Am J Reprod Immunol 2006; 5 5: 1-11.
102. Wallace PK, Yeaman GR, Johnson K, et al. MHC class II expression and antigen presentation by human endometrial cells. J Steroid Biochem Mol Biol 2001; 76: 203-11.
103. Wira CR, Rossoll RM, Young RC. Polarized uterine epithelial cells preferentially present antigen at the basolateral surface: Role of stromal cells in regulating Class II mediated epithelial cell antigen presentation. J Immunol 2005; 175: 1795-804.
104. Trombetta ES, Mellman I. Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 2005; 23: 975-1028.
105. Iezzi G, Karjalainen K, Lanzavecrhia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 1998; 8: 89-95.
106. Iezzi G, Scotet E, Scheidegger D, et al. The interplay between the duration of TCR and cytokine signaling determines T cell polarization. Eur J Immunol 1999; 29: 4092-101.
107. Kroczek RA, Mages HW, Hutloff A. Emerging paradigms of T-cell co-stimulation. Curr Opin Immunol 2004; 16: 321-7.
108. Edelstam GA, Lundkvist OE, Klareskog L, et al. Cyclic variation of major histocompatibility complex class II antigen expression in the human fallopian tube epithelium. Fertil Steril 1992; 57: 1225-9.
109. Bjercke S, Brandtzaeg P. Glandualr distribution of immunolglobulins, J chain, secretory component and HLA-DR in the human endometrium throughout the menstrual cycle. Hum Reprod 1993; 8: 1420-25.
110. Ljunggren G, Anderson DJ. Cytokine induced modulation of MBC class I and class II molecules on human cervical epithelial cells. J Reprod Immunol 1998; 38: 123-38.
111. Sallinen K, Verajankorva E, Pollanen P. Expression of antigens involved in the presentation of lipid antigens and induction of clonal anergy in the female reproductive tract. J Reprod Immunol 2000; 46: 91-101.
112. Wira CR, Rossoll RM, Kaushic C. Antigen-presenting cells in the female reproductive tract: influence of estradiol on antigen presentation by vaginal cells. Endocrinology 2000; 141: 2877-85.
113. Petroff MG, Chen L, Phillips TA, et al. B7 family molecules are favorably positioned at the human maternal-fetal interface. Biol Reprod 2003; 68: 1496-504.
114. Petroff MG, Chen L, Phillips TA, et al. B7 family molecules: novel immunomodulators at the maternal-fetal interface. Placenta 2002; 23 (Suppl A): S95-101.
115. Prabhala RH, Wira CR. Sex hormone and IL-6 regulation of antigen presentation in the female reproductive tract mucosal tissues. J Inummol 1995; 155: 5566-73.
116. Wira CR, Fahey JV, White HD, et al. The mucosal immune system in the human female reproductive tract: influence of Stage of the Menstrual Cycle and Menopause on Mucosal immunity in the uterus. In: Glasser S, Aplin J, Giudice L, Tabibzadch S, eds. The Endometrium. London: Taylor & Francis. 2002; pp. 371-404.
117. Wira CR, Fahey JV, Abrahams VM, et al. Influence of stage of the reproductive cycle and estradiol on thymus cell antigen presentation. J Steroid Biochem Mol Biol 2003; 84: 79-87.
118. Woof JM, Mestecky J. Mucosal immunoglobulins. Immumol Rev 2005; 206: 64-82.
119. Russell MW, Mestecky J. Humoral immune responses to microbial infections in the genital tract. Microbes Infect 2002; 4: 667-77.
120. Parr MB, Parr EL. Immunoglobulins in the female genital tract. In: Bronson RD, Alexander NJ, Anderson DJ, Branch DW, Kuteh WH, eds. Reproductive Immunology. Cambridge, Massachusetts: Blackwell Science. 1996; pp. 275-308.
121. Mestecky J, Moro I, Kerr MA, et al. Mucosal Immunoglobulins. In: Mestecky J LM, Strober W, Bienenstock J, McGhee JR Mayer L, ed. Mucosal Immunology. Burlington, MA: Elselvier Academic Press. 2005; pp. 153-81.
122. Brandtzaeg P. Role of secretory antibodies in defence against infections. Int J Med Microbiol 2003; 293: 3-15.
123. Tourville DR, Ogra S, Lippes J, et al. The human female reproductive tract: immunohistochemical localization of gA, gG, gM, secretory piece and lactoferrin. Am J Obstet Gynecol 1970; 108: 1102-08.
124. Rebello R, Green F, Fox H. A study of secretory immune system of the female reproductive tract. Br J Obstet Gynecol 1975; 82: 812-16.
125. Kutteh WH, Hatch KD, Blackwell RE, et al. Secretory immune system of the female reproductive tract: I. Immunoglobulin and secretory component-containing cells. Obstet Gynecol 1988; 71: 56-60.
126. Vaerman J, Ferin J. Local immunological response in vagina, cervix and endometrium. Acta Endocrinol Suppl (Copenh) 1975; 194: 281-305.
127. Brandtzaeg P. Mucosal immunity in the female genital tract. J Reprod Immunol 1997; 36: 23-50.
128. Mestecky J, Moldoveanu Z, Russell MW. Immunologic uniqueness of the genital tract: challenge for vaccine development. Am J Reprod Immunol 2005; 53: 208-14.
129. Wira CR, Sullivan DA. Estradiol and progesterone regulation of IgA, IgG and secretory component in cervico-vaginal secretions of the rat. Biol Reprod 1985; 32: 90-95.
130. Sullivan DA, Underdown BJ, Wira CR. Steroid hormone regulation of free secretory component in the rat uterus. Immunology 1983; 49: 379-86.
131. Sullivan DA, Richardson GS, MacLaughlin DT, et al. Variations in the levels of secretory component in human uterine fluid during the menstrual cycle. J Steroid Biochem 1984; 20: 509-13.
132. Tauber PF, Wettich W, Nohlen M, et al. Diffusible proteins of the mucosa of the human cervix, uterus, and fallopian tubes: distribution and variations during the menstrual cycle. Am J Obstet Gynecol 1985; 15: 1115-25.
133. Schumacher GFB. Humoral immune factors in the female reproductive tract and their changes during the cycle. In: Dinsda D, Schumacher G, eds. Immunological Aspects of Infertility and Fertility Control. North Holland, New York: Elsevier. 1980; pp. 93-141.
134. Gravlee LC. Jet irrigation method for the diagnosis of endometrial carcinoma. Obstet Gynecol 1969; 34: 168-72.
135. Sylvan PE, MacLaughlin DT, Richardson GS, et al. Human uterine fluid proteins associated with secretory phase endometrium: progesterone-induced proteins? Biol Reprod 1981; 24: 423-29.
136. Waldmann R, Cruz J, Rowe D. Immunoglobulin levels to Candida albicans in human cervicovaginal secretions. Clin Exp Immunol 1971; 9: 427-34.
137. Woof JM, Kerr MA. The function of immunoglobulin A in immunity. J Pathol 2006; 208: 270-82.
138. Burns JW, Siadat-Pajouh M, Krishnaney AA, et al. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science 1996; 272: 104-7.
139. Michetti P, Mahan MJ, Slauch JM, et al. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect Immun 1992; 60: 1786-92.
140. Mazanec MB, Kaetzel CS, Lamm ME, et al. Intracellular neutralization of virus by immunoglobulin A antibodies. Proc Natl Acad Sci USA 1992; 89: 6901-5.
141. Mazanec MB, Kaetzel CS, Lamm ME, et al. Intracellular neutralization of Sendai and influenza viruses by IgA monoclonal antibodies. Adv Exp Med Biol 1995; 371 A: 651-4.
142. Huang YT, Wright A, Gao X, et al. Intraepithelial cell neutralization of HIV-1 replication by IgA. J Immunol 2005; 174: 4828-35.
143. Nardelli-Haefliger DJ, Wirthner D, Schiller J, et al. Specific antibody levels at the cervix during the menstrual cycle of women vaccinated with human papillomaviras 16 virus-like particles. J Nat Cancer Inst 2003; 95: 1128-37.
144. Dominguez F, Pellicer A, Simon C. Paracrine dialogue in implantation. Mol Cell Endocrinol 2002; 186: 175-81.
145. Tabibzadeh S. The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 1996; 2: 77-92.
146. Tabibzadeh S. Evidence of T-cell activation and potential cytokine action in human endometrium. J Clin Endocrinol Metab 1990; 71: 645-49.
147. Kayisli UA, Mahutte NG, Arici A. Uterine chemokines in reproductive physiology and pathology. Am J Reprod Immunol 2002; 47: 213-21.
148. Critchley HO, Kelly RW, Brenner RM, et al. The endocrinology of menstruation-a role for the immune system. Clin Endocrinol (Oxf) 2001; 55: 701-10.
149. Yeaman GF, Howell AL, Weldon S, et al. Human immunodeficiency virus receptor and coreceptor expression on human uterine epithelial cells: regulation of expression during the menstrual cycle and implications for human immunodeficiency virus infection. Immunology 2003; 109: 137-46.
150. Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001; 2: 361-7.
151. Goepfert AR, Goldenberg RL, Andrews WW, et al. The Preterm Prediction Study: association between cervical interleukin 6 concentration and spontaneous preterm birth. Am J Obstet Gynecol 2001; 184: 483-8.
152. Jacobsson B, Holst RM, Wennerholm UB, et al. Monocyte chemotactic protein-1 in cervical and amniotic fluid: relationship to microbial invasion of the amniotic cavity, intra-amniotic inflammation, and preterm delivery. Am J Obstet Gynecol 2003; 189: 1161-7.
153. Matsuda Y, Kouno S, Nakano H. Effects of antibiotic treatment on the concentrations of interleukin-6 and interleukin-8 in cervicovaginal fluid. Fetal Diagn Ther 2002; 17: 228-32.
154. Tanaka Y, Narahara H, Takai N, et al. Interleukin-1 beta and interleukin-8 in cervicovaginal fluid during pregnancy. Am J Obstet Gynecol 1998; 179: 644-9.
155. Simhan HN, Caritis SN, Krohn MA, et al. Decreased cervical proinflammatory cytokines permit subsequent upper genital tract infection during pregnancy. Am J Obstet Gynecol 2003; 189: 560-7.
156. Romero R, Chaiworapongsa T, Kuivaniemi H, et al. Bacterial vaginosis, the inflammatory response and the risk of preterm birth: a role for genetic epidemiology in the prevention of preterm birth. Am J Obstet Gynecol 2004; 190: 1509-19.
157. Baggiolini M. Activation and recruitment of neutrophil leukocytes. Clin Exp Immunol 1995; 101 (Suppl 1): 5-6.
158. Yoshimura T, Leonard EJ. Human monocyte chemoattractant protein-1: structure and function. Cytokines 1992; 4: 131-52.
159. Shen L, Fahey JV, Hussey SB, et al. Synergy between IL-8 and GM-CSF in reproductive tract epithelial cell secretions promotes enhanced neutrophil chemotaxis. Cell Immunol 2004; 230: 23-32.
160. Meter RA, Wira CR, Fahey JV. Secretion of monocyte chemotactic protein-1 by human uterine epithelium directs monocyte migration in culture. Fertil Steril 2005; 84: 191-201.
161. Allen SJ, Crown SE, Handel TM. Chemokine: receptor structure, interactions, and antagonism. Annu Rev Immunol 2007; 25: 787-820.
162. Yang D, Chertov O, Bykovskaia SN, et al. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell, CCR6. Science 1999; 286: 525-8.
163. Niyonsaba F, Ogawa H, Nagaoka I. Human beta-defensin-2 functions as a chemotactic agent for tumour necrosis factor-alpha-treated human neutrophils. Immunology 2004; 111: 273-81.
164. Wira CF, Grant-Tschudy KS, Crane-Godreau MA. Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. AJRI 2005; 53: 65-76.
165. Hoover DM, Boulegue C, Yang D, et al. The structure of human macrophage inflammatory protein-3alpha/CCL20. Linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J Biol Chem 2002; 277: 37647-54.
166. Chabalgoity JA, Baz A, Rial A, et al. The relevance of cytokines for development of protective immunity and rational design of vaccines. Cytokine Growth Factor Rev 2007; 18: 195-207.
167. Toka FN, Rouse BT. Mucosal application of plasmid-encoded IL-15 sustains a highly protective anti-Herpes simplex virus immunity. J Leukoc Biol 2005; 78: 178-86.
168. Toka FN, Gierynska M, Rouse BT. Codelivery of CCR7 ligands as molecular adjuvants enhances the protective immune response against herpes simplex virus type 1. J Vitol 2003; 77: 12742-52.
169. Toka FN, Pack CD, Rouse BT. Molecular adjuvants for mucosal immunity. Immunol Rev 2004; 199: 100-12.
170. Tsuji T, Hamajima K, Fukushima J, et al. Enhancement of cell-mediated immunity against HIV-1 induced by coinnoculation of plasmid-encoded HIV-1 antigen with plasmid expressing IL-12. J Immunol 1997; 158:4008-13.
171. Fahey JV, Schaefer TM, Channon JY, et al. Secretion of cytokines and chemokines by polarized human epithelial cells from the female reproductive tract. Hum Reprod 2005; 20: 1439-46.
172. Wira CR, Fahey JV. The innate immune system: gatekeeper to the female reproductive tract. Immunology 2004; 111: 13-5.
173. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
174. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol 2003; 21: 335-76.
175. Underhill DM. Toll-like receptors and microbes take aim at each other. Curr Opin Immunol 2004; 16: 483-7.
176. Kopp E, Medzhitov R. Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 2003; 15: 396-401.
177. Meylan E, Tschopp J, Karin M. Intracellular pattern recognition receptors in the host response. Nature 2006; 442: 39-44.
178. Kanneganti TD, Lamkanfi M, Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007; 27: 549-59.
179. Underhill DM. Collaboration between the innate immune receptors dectin-1, TLRs, and Nods. Immunol Rev 2007; 219: 75-87.
180. Pioli PA, Amiel E, Schaefer TM, et al. Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract. Infect Immun 2004; 72: 5799-806.
181. Fazeli A, Bruce C, Anumba DO. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum Reprod 2005; 20: 1372-8.
182. Itoh H, Nasu K, Nishida M, et al. 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 2006; 56: 91-101.
183. Nasu K, Itoh H, Yuge A, et al. 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 2007; 22: 356-61.
184. Hirata T, Osuga Y, Hirota Y, et al. Evidence for the presence of toll-like receptor 4 system in the human endometrium. J Clin Endocrinol Metab 2005; 90: 548-56.
185. Larsen B, Monif GR. Understanding the bacterial flora of the female genital tract. Clin Infect Dis 2001; 32: e69-77.
186. Young SL, Lyddon TD, Jorgenson RL, et al. Expression of Toll-like receptors in human endometrial epithelial cells and cell lines. Am J Reprod Immunol 2004; 52: 67-73.
187. Ghosh M, Schaefer TM, Fahey JV, et al. Antiviral responses of human Fallopian tube epithelial cells to toll-like receptor 3 agonist poly(I:C). Fertil Steril 2007: [Epubahead of Print].
188. Eriksson M, Meadows SK, Basu S, et al. TLRs mediate IFN-gamma production by human uterine NK cells in endometrium. J Immunol 2006; 176: 6219-24.
189. Shen L, Smith JM, Shen Z, et al. Inhibition of human neutrophil degranulation by transforming growth factor-beta1. Clin Exp Immunol 2007; 149: 155-61.
190. Aflatoonian R, Tuckerman E, Elliott SL, et al. Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum Reprod 2007; 22: 586-93.
191. Hirata T, Osuga Y, Hamasaki K, et al. Expression of toll-like receptors 2, 3, 4, and 9 genes in the human endometrium, during the menstrual cycle. J Reprod Immunol 2007; 74: 53-60.
192. Yao XD, Fernandez S, Kelly MM, et al. Expression of Toll-like receptors in murine vaginal epithelium is affected by the estrous cycle and stromal cells. J Reprod Immunol 2007; 75: 106-19.
193. Ishii KJ, Akira S. Toll or toll-ftee adjuvant path toward the optimal vaccine development. J Clin Immunol 2007; 27: 363-71.
194. Mata-Haro V, Cekic C, Martin M, et al. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007; 316: 1628-32.
195. West MA, Wallin RP, Matthews SP, et al. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 2004; 305: 1153-7.
196. Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 2006; 440: 808-12.
197. Blander JM. Coupling Toll-like receptor signaling with phagocytosis: potentiation of antigen presentation. Trends Immunol 2007; 28: 19-25.
198. King AE, Critchley HO, Kelly RW. Innate immune defenses in the human endometrium. Reprod Biol Endocrinol 2003; 1: 116-23.
199. Yang D, Chertov O, Oppenheim JJ. Participation of mammalian defensins and cathelicidins in anti-microbial immunity: receptors and activities of human defensins and cathelicidin (LL-37). J Leukoc Biol 2001; 69: 691-7.
200. Williams SE, Brown TI, Roghanian A, et al. SLPI and clafin: one glove, many fingers. Clin Sci (Lond) 2006; 110: 21-35.
201. Weinberg A, Quinones-Mateu ME, Lederman MM. Role of human beta-defensins in HIV infection. Adv Dent Res 2006; 19: 42-8.
202. Shugars DC. Endogenous mucosal antiviral factors of the oral cavity. 3 Infect Dis 1999; 179 (Suppl 3): S431-5.
203. Capobianchi MR. Induction of lymphomonocyte activation by HIV-1 glycoprotein gp120. Possible role in AIDS pathogenesis. J Biol Regul Homeost Agents 1996; 10: 83-91.
204. Garzino-Demo A. Chemokines and defensins as HIV suppressive factors: an evolving story. Curr Pharm. Des 2007; 13: 163-72.
205. Porter E, Yang H, Yavagal S, et al. Distinct defensin profiles in Neisseria gonorrhocae and Chlamydia trachomatis urethritis reveal novel epithelial cell-neutrophil interactions. Infect Immun 2005; 73: 4823-33.
206. Feng Z, Jiang B, Chandra J, et al. Human beta-defensins: differential activity against candidal species and regulation by Candida albicans. J Dent Res 2005; 84: 445-50.
207. John M, Keller MJ, Fam EH, et al. Cervicovaginal secretions contribute to innate resistance to herpes simplex virus infection. J Infect Dis 2005; 192: 1731-40.
208. Garzino-Demo A, DeVico AL, Gallo RC. Chemokine receptors and chemokines in HIV infection. J Clin Immunol 1998; 18: 243-55.
209. Cummins JE, Christensen L, Lennox JL, et al. Mucosal innate immune factors in the female genital tract are associated with vaginal HIV-1 shedding independent of plasma viral load. AIDS Res Hum Retroviruses 2006; 22: 788-95.
210. Oberley RE, Goss KL, Ault KA, et al. Surfactant protein D is present in the human female reproductive tract and inhibits Chlamydia trachomatis infection. Mol Hum Reprod 2004; 10: 861-70.
211. Logdberg L, Wester L. Immunocalins: a lipocalin subfamily that modulates immune and inflammatory responses. Biochim Biophys Acta 2000; 1482: 284-97.
212. Ganz T. Antimicrobial polypeptides. J Leukoc Biol 2004; 75: 34-8.
213. Cole AM, Liao HI, Stuchlik O, et al. Cationic polypeptides are required for antibacterial activity of human airway fluid. J Imummol 2002; 169: 6985-91.
214. Fluckinger M, Haas H, Merschak P, et al. Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob Agents Chemother 2004; 48: 3367-72.
215. King AE, Critchley HO, Sallenave JK et al. Elafin in human endometrium: an antiprotease and antimicrobial molecule expressed during menstruation. J Clin Endocrinol Metab 2003; 88: 4426-31.
216. Moutsopoulos NM, Greenwell-Wild T, Wahl SM. Differential mucosal susceptibility in HIV-1 transmission and infection. Adv Dent Res 2006; 19: 52-6.
217. Stemstraesser L, Tippler B, Mertens J, et al. Inhibition of early steps in the lentiviral replication cycle by cathelicidin host defense peptides. Retrovirology 2005; 2: 2.
218. Le Bon A, Tough DF. Links between innate and adaptive immunity via type 1 interferon. Curr Opin Immunol 2002; 14: 432-6.
219. Deonarain R, Alcami A, Alexiou M, et al. Impaired antiviral response and alpha/beta interferon induction in mice lacking beta interferon. J Virol 2000; 74: 3404-9.
220. Hallero, Kochs G, Weber F. Interferon, Mx, and viral countermeasures. Cytokine Growth Factor Rev 2007; 18: 425-33.
221. Garcia MA, Meurs EF, Esteban M. The dsRNA protein kinase PKR: virus and cell control. Biochimie 2007; 89: 799-811.
222. Holmes RK, Malim MH, Bishop KN. APOBEC-mediated viral restriction: not simply editing? Trends Biochem Sci 2007; 32: 118-28.
223. Keller M, Guzman E, Hazrati E, et al. PRO 2000 elicits a decline in genital tract immune mediators without compromising intrinsic antimicrobial activity. AIDS 2007; 21: 467-76.
224. Martin HL, Jr., Nyange PM, Richardson BA, et al. Hormonal contraception, sexually transmitted diseases, and risk of heterosexual transmission of human immunodeficiency virus type 1. J Infect Dis 1998; 178: 1053-9.
225. Smith SM, Mefford M, Sodora D, et al. Topical estrogen protects against SIV vaginal transmission without evidence of systemic effect. Aids 2004; 18: 1637-43.
226. Lederman MM, Veazey RS, Offord R, et al. Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science 2004; 306: 485-7.