Influence of the murine oestrous cycle on the induction of mucosal immunity

American Journal of Reproductive Immunology

Volumn 50, Issue 5, 2003, Pages 369-379

  Gockel, Christine M ^a   Bao, Shisan ^b   Holland, Michael K ^c   Beagley, Kenneth W ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b University of Sydney   (Australia)

^c Pest Animal Control Cooperative Research Centre   (Australia)

Author keywords

Cholera toxin; Mucosal immunization; Oestrous cycle

Indexed keywords

ANTIBODY; CHOLERA TOXIN; ESTRADIOL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; SEX HORMONE; TETANUS TOXOID;

ADOLESCENT; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ARTICLE; CAUDA EQUINA; CELLULAR IMMUNITY; CONTROLLED STUDY; DIESTRUS; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTRUS; ESTRUS CYCLE; FECES ANALYSIS; FECES COMPOSITION; FECES LEVEL; FEMALE; FEMALE GENITAL SYSTEM; HUMORAL IMMUNITY; IMMUNITY; IMMUNIZATION; LUMBAR SPINE; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MOUSE; MUCOSA; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; T LYMPHOCYTE ACTIVATION;

ADMINISTRATION, CUTANEOUS; ADMINISTRATION, INTRANASAL; ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES; CELL DIVISION; CHOLERA TOXIN; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESTROUS CYCLE; FECES; FEMALE; GENITALIA, FEMALE; IMMUNITY, MUCOSAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MUCOUS MEMBRANE; MUCUS; SALIVA; T-LYMPHOCYTES; TETANUS TOXOID; VACCINATION;

EID: 0142043157     PISSN: 87558920     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0897.2003.00097.x     Document Type: Article

References (52)

1. Prabhala RH, Wira CR: Influence of estrous cycle and estradiol on mitogenic responses of splenic T- and B-lymphocytes. Adv Exp Med Biol 1995; 371A:379-381.
2. Rachman F, Casimiri V, Psychoyos A, Bernard O. Immunoglobulins in the mouse uterus during the oestrous cycle. J Reprod Fertil 1983; 69: 17-21.
3. Richardson JM, Wira CR: Uterine stromal cell suppression of pIgR production by uterine epithelial cells in vitro: A mechanism for regulation of pIgR production. J Reprod Immunol 1997; 33:95-112.
4. White HD, Crassi KM, Givan AL, Stern JE, Gonzalez JL, Memoli VA, Green WR, Wira CR. CD3+ CD8+ CTL activity within the human female reproductive tract: Influence of stage of the menstrual cycle and menopause. J Immunol 1997; 158:3017-3027.
5. Wira C, Kaushic C: Mucosal immunity in the female reproductive tract: Effect of sex hormones on immune recognition and responses. In Mucosal Vaccines: New Trends in Immunization, H Kiyono, PL Ogra, JR McGhee (eds). New York, Academic Press, 1996, pp 375-388.
6. Wira CR, Sandoe CP: Hormonal regulation of immunoglobulins: Influence of estradiol on immunoglobulins A and G in the rat uterus. Endocrinology 1980; 106:1020-1026.
7. Wira CR, Sandoe CP: Origin of IgA and IgG antibodies in the female reproductive tract: Regulation of the genital response by estradiol. Adv Exp Med Biol 1987; 216A:403-412.
8. Gockel CM, Bao S, Beagley KW: Transcutaneous immunization induces mucosal and systemic immunity: A potent method for targeting immunity to the female reproductive tract. Mol Immunol 2000; 37:537-544.
9. Kaushic C, Frauendorf E, Rossoll RM, Richardson JM, Wira CR. Influence of the estrous cycle on the presence and distribution of immune cells in the rat reproductive tract. Am J Reprod Immunol 1998; 39:209-216.
10. Anderson DJ: The importance of mucosal immunology to problems in human reproduction. J Reprod Immunol 1996; 31:3-19.
11. Haimovici F, Takahashi K, Anderson DJ: Antifertility effects of antisperm cell-mediated immunity in mice. J Reprod Immunol 1992; 22:281-298.
12. Han Y, Morrison RP, Cutler JE: A vaccine and monoclonal antibodies that enhance mouse resistance to Candida albicans vaginal infection. Infect Immun 1998; 66:5771-5776.
13. Johansson EL, Rask C, Fredriksson M, Eriksson K, Czerkinsky C, Holmgren J. Antibodies and antibody-secreting cells in the female genital tract after vaginal or intranasal immunization with cholera toxin B subunit or conjugates. Infect Immun 1998; 66:514-520.
14. Livingston JB, Lu S, Robinson H, Anderson DJ. Immunization of the female genital tract with a DNA-based vaccine. Infect Immun 1998; 66:322-329.
15. Menge AC et al. Immune response of the female rat genital tract after oral and local immunization with Keyhole Limpet Hemocyanin conjugated to the cholera toxin B subunit. Infect Immun 1993; 61:2162-2171.
16. Rosenthal KL, Gallichan WS: Challenges for vaccination against sexually-transmitted diseases: Induction and long-term maintenance of mucosal immune responses in the female genital tract. Semin Immunol 1997; 9:303-314.
17. Wu HY, Abdu S, Stinson D, Russell MW. Generation of female genital tract antibody responses by local or central (common) mucosal immunization. Infect Immun 2000; 68:5539-5545.
18. Bebo BF Jr, Schuster JC, Vandenbark AA, Offner H: Androgens alter the cytokine profile and reduce encephalitogenicity of myelin-reactive T cells. J Immunol 1999; 162:35-40.
19. Kim S, Liva SM, Dalal MA, Verity MA, Voskuhl RR. Estriol ameliorates autoimmune demyelinating disease: Implications for multiple sclerosis. Neurology 1999; 52:1230-1238.
20. Screpanti I, Meco D, Morrone S, Gulino A, Mathieson BJ, Frati L. In vivo modulation of the distribution of thymocyte subsets: Effects of estrogen on the expression of different T cell receptor V beta gene families in CD4-, CD8- thymocytes. Cell Immunol 1991; 134:414-426.
21. Tornwall J, Carey AB, Fox RI, Fox HS. Estrogen in autoimmunity: Expression of estrogen receptors in thymic and autoimmune T cells. J Gend Specif Med 1999; 2:33-40.
22. Mor G, Sapi E, Abrahams VM, Rutherford T, Song J, Hao XY, Muzaffar S, Kohen F. Interaction of the estrogen receptors with the Fas ligand promoter in human monocytes. J Immunol 2003; 170:114-122.
23. Benten WP, Stephan C, Lieberherr M, Wunderlich F. Estradiol signaling via sequestrable surface receptors. Endocrinology 2001; 142:1669-1677.
24. Vegeto E, Bonincontro C, Pollio G, Sala A, Viappiani S, Nardi F, Brusadelli A, Viviani B, Ciana P, Maggi A. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J Neurosci 2001; 21:1809-1818.
25. Vickers AE, Lucier GW: Estrogen receptor levels and occupancy in hepatic sinusoidal endothelial and Kupffer cells are enhanced by initiation with diethylnitrosamine and promotion with 17alpha-ethinylestradiol in rats. Carcinogenesis 1996; 17:1235-1242.
26. Giron-Gonzalez JA, Moral FJ, Elvira J, Garcia-Gil D, Guerrero F, Gavilan I, Escobar L. Consistent production of a higher TH1:TH2 cytokine ratio by stimulated T cells in men compared with women. Eur J Endocrinol 2000; 143: 31-36.
27. Laskarin G, Strbo N, Sotosek V, Rukavina D, Faust Z, Szekeres-Bartho J, Podack ER. Progesterone directly and indirectly affects perforin expression in cytolytic cells. Am J Reprod Immunol (Copenhagen) 1999; 42:312-320.
28. Yang JH, Chen CD, Wu MY, Chao KH, Yang YS, Ho HN. Hormone replacement therapy reverses the decrease in natural killer cytotoxicity but does not reverse the decreases in the T-cell subpopulation or interferon-gamma production in postmenopausal women. Fertil Steril 2000; 74:261-267.
29. Arici A, Senturk LM, Seli E, Bahtiyar MO, Kim G. Regulation of monocyte chemotactic protein-1 expression in human endometrial stromal cells by estrogen and progesterone. Biol Reprod 1999; 61:85-90.
30. Penny LA, Armstrong DG, Baxter G, Hogg C, Kindahl H, Bramley T, Watson ED, Webb R. Expression of monocyte chemoattractant protein-1 in the bovine corpus luteum around the time of natural luteolysis. Biol Reprod 1998; 59:1464-1469.
31. Sonoda Y, Mukaida N, Wang JB, Shimada-Hiratsuka M, Naito M, Kasahara T, Harada A, Inoue M, Matsushima K. Physiologic regulation of postovulatory neutrophil migration into vagina in mice by a C-X-C chemokine(s). J Immunol 1998; 160:6159-6165.
32. Wira CR, Kaushic C, Richardson J: Role of sex hormones and cytokines in regulating the mucosal immune system in the female reproductive tract. In Mucosal Immunology, Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR (eds). San Diego, Academic Press, 1999, pp 1449-1461.
33. Wira CR, Sullivan DA: Estradiol and progesterone regulation of immunoglobulin A and G and secretory component in cervicovaginal secretions of the rat. Biol Reprod 1985; 32:90-95.
34. Wira CR, Sandoe CP: Specific IgA and IgG antibodies in the secretions of the female reproductive tract: Effects of immunization and estradiol on expression of this response in vivo. J Immunol 1987; 138:4159-4164.
35. McAnulty PA, Morton DB: The immune response of the genital tract of the female rabbit following systemic and local immunization. J Clin Lab Immunol 1978; 1:255-260.
36. Belec L, Tevi-Benissan C, Lu XS, Prazuck T, Pillot J. Local synthesis of IgG antibodies to HIV within the female and male genital tracts during asymptomatic and pre-AIDS stages of HIV infection. AIDS Res Hum Retroviruses 1995; 11:719-729.
37. Berneman A, Belec L, Fischetti VA, Bouvet JP. The specificity patterns of human immunoglobulin G antibodies in serum differ from those in autologous secretions. Infect Immun 1998; 66:4163-4168.
38. Nardelli-Haefliger D, Roden R, Balmelli C, Potts A, Schiller J, De Grandi P. Mucosal but not parenteral immunization with purified human papillomavirus type 16 virus-like particles induces neutralizing titers of antibodies throughout the estrous cycle of mice. J Virol 1999; 73:9609-9613.
39. Glenn GM, Scharton-Kersten T, Vassell R, Mallett CP, Hale TL, Alving CR. Transcutaneous immunization with cholera toxin protects mice against lethal mucosal toxin challenge. J Immunol 1998; 161:3211-3214.
40. Carter PB, Collins FM: The route of enteric infection in normal mice. J Exp Med 1974; 139:1189-1203.
41. Kaushic C, Frauendorf E, Wira CR: Polymeric immunoglobulin A receptor in the rodent female reproductive tract: Influence of estradiol in the vagina and differential expression of messenger ribonucleic acid during estrous cycle. Biol Reprod 1997; 57:958-966.
42. Yellayi S, Teuscher C, Woods JA, Welsh Jr. TH, Tung KS, Nakai M, Rosenfeld CS, Lubahn DB, Cooke PS. Normal development of thymus in male and female mice requires estrogen/estrogen receptor-alpha signaling pathway. Endocrine 2000; 12:207-213.
43. Okasha SA, Ryu S, Do Y, McKallip RJ, Nagarkatti M, Nagarkatti PS. Evidence for estradiol-induced apoptosis and dysregulated T cell maturation in the thymus. Toxicology 2001; 163:49-62.
44. 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; 141:2877-2885.
45. Mestecky J: The common mucosal immune system and current strategies for induction of immune responses in external secretions. J Clin Immunol 1987; 7:265-276.
46. Wu HY, Russell MW: Nasal lymphoid tissue, intranasal immunization, and compartmentalization of the common mucosal immune system. Immunol Res 1997; 16:187-201.
47. Penny LA: Monocyte chemoattractant protein 1 in luteolysis. Rev Reprod 2000; 5:63-66.
48. Petrovska M, Dimitrov DG, Michael SD: Quantitative changes in macrophage distribution in normal mouse ovary over the course of the estrous cycle examined with an image analysis system. Am J Reprod Immunol 1996; 36:175-183.
49. Yeaman GR, Guyre PM, Fanger MW, Collins JE, White HD, Rathbun W, Orndorff KA, Gonzalez J, Stern JE, Wira CR. Unique CD8+ T cell-rich lymphoid aggregates in human uterine endometrium. J Leukoc Biol 1997; 61:427-435.
50. Campbell JJ, Haraldsen G, Pan J, Rottman J, Qin S, Ponath P, Andrew DP, Warnke R, Ruffing N, Kassam N, Wu L, Butcher EC. The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 1999; 400:776-780.
51. Kunkel EJ, Campbell JJ, Haraldsen G, Pan J, Boisvert J, Roberts AI, Ebert EC, Vierra MA, Goodman SB, Genovese MC, Wardlaw AJ, Greenberg HB, Parker CM, Butcher EC, Andrew DP, Agace WW. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: Epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med 2000; 192:761-768.
52. Rossi DL, Hurst SD, Xu Y, Wang W, Menon S, Coffman RL, Zlotnik A. Lungkine, a novel CXC chemokine, specifically expressed by lung bronchoepithelial cells. J Immunol 1999; 162:5490-5497.