Immunological responses to semen in the female genital tract

Theriogenology

Volumn 70, Issue 8, 2008, Pages 1174-1181

  Schuberth, H J ^a   Taylor, U ^b   Zerbe, H ^c   Waberski, D ^a   Hunter, R ^a   Rath, D ^b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b Bundesforschungsanstalt fü Landwirtschaft   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Immune response; Reproduction; Seminal fluid; Uterus

Indexed keywords

ANIMAL; ARTICLE; FEMALE; FEMALE GENITAL SYSTEM; HUMAN; IMMUNOLOGY; MALE; RODENT; SPERM; SPERM PRESERVATION; SWINE;

ANIMALS; FEMALE; GENITALIA, FEMALE; HUMANS; MALE; RODENTIA; SEMEN; SEMEN PRESERVATION; SWINE;

EID: 55849105911     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2008.07.020     Document Type: Article

References (64)

1. Robertson S.A. Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res 322 (2005) 43-52
2. Robertson S.A. Seminal fluid signaling in the female reproductive tract: lessons from rodents and pigs. J Anim Sci 85 (2007) E36-44
3. Waberski D., Claassen R., Hahn T., Jungblut P.W., Parvizi N., Kallweit E., et al. LH profile and advancement of ovulation after transcervical infusion of seminal plasma at different stages of oestrus in gilts. J Reprod Fertil 109 (1997) 29-34
4. Waberski D., Sudhoff H., Hahn T., Jungblut P.W., Kallweit E., Calvete J.J., et al. Advanced ovulation in gilts by the intrauterine application of a low molecular mass pronase-sensitive fraction of boar seminal plasma. J Reprod Fertil 105 (1995) 247-252
5. Espey L.L. Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol Reprod 50 (1994) 233-238
6. O'Leary S., Robertson S.A., and Armstrong D.T. The influence of seminal plasma on ovarian function in pigs-a novel inflammatory mechanism?. J Reprod Immunol 57 (2002) 225-238
7. Waberski D., Dohring A., Ardon F., Ritter N., Zerbe H., Schuberth H.J., et al. Physiological routes from intra-uterine seminal contents to advancement of ovulation. Acta Vet Scand 48 (2006) 13
8. O'Leary S., Jasper M.J., Warnes G.M., Armstrong D.T., and Robertson S.A. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction 128 (2004) 237-247
9. Brannstrom M., Bonello N., Wang L.J., and Norman R.J. Effects of tumour necrosis factor alpha (TNF alpha) on ovulation in the rat ovary. Reprod Fertil Dev 7 (1995) 67-73
10. Einer-Jensen N., and Hunter R. Counter-current transfer in reproductive biology. Reproduction 129 (2005) 9-18
11. Bischof R.J., Brandon M.R., and Lee C.S. Studies on the distribution of immune cells in the uteri of prepubertal and cycling gilts. J Reprod Immunol 26 (1994) 111-129
12. Kaeoket K., Persson E., and Dalin A.M. The sow endometrium at different stages of the oestrous cycle: studies on morphological changes and infiltration by cells of the immune system. Anim Reprod Sci 65 (2001) 95-114
13. Rodriguez-Martinez H., Nicander L., Viring S., Einarsson S., and Larsson K. Ultrastructure of the uterotubal junction in preovulatory pigs. Anat Histol Embryol 19 (1990) 16-36
14. Matthijs A., Engel B., and Woelders H. Neutrophil recruitment and phagocytosis of boar spermatozoa after artificial insemination of sows, and the effects of inseminate volume, sperm dose and specific additives in the extender. Reproduction 125 (2003) 357-367
15. Rozeboom K.J., Troedsson M.H., and Crabo B.G. Characterization of uterine leukocyte infiltration in gilts after artificial insemination. J Reprod Fertil 114 (1998) 195-199
16. Rozeboom K.J., Troedsson M.H., Molitor T.W., and Crabo B.G. The effect of spermatozoa and seminal plasma on leukocyte migration into the uterus of gilts. J Anim Sci 77 (1999) 2201-2206
17. Robertson S.A., Mau V.J., Tremellen K.P., and Seamark R.F. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil 107 (1996) 265-277
18. Pandya I.J., and Cohen J. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril 43 (1985) 417-421
19. Robertson S.A., O'Connell A.C., Hudson S.N., and Seamark R.F. Granulocyte-macrophage colony-stimulating factor (GM-CSF) targets myeloid leukocytes in the uterus during the post-mating inflammatory response in mice. J Reprod Immunol 46 (2000) 131-154
20. Lovell J.W., and Getty R. Fate of semen in the uterus of the sow: histologic study of endometrium during the 27 h after natural service. Am J Vet Res 29 (1968) 609-625
21. Gutsche S., von Wolff M., Strowitzki T., and Thaler C.J. Seminal plasma induces mRNA expression of IL-1beta, IL-6 and LIF in endometrial epithelial cells in vitro. Mol Hum Reprod 9 (2003) 785-791
22. Gorgens A., Leibold W., Klug E., Schuberth H.J., Martinsson G., and Zerbe H. Inseminate components are modulating the chemotactic activity of uterine polymorphonuclear granulocytes (PMN) of mares. Anim Reprod Sci 89 (2005) 308-310
23. McMaster M.T., Newton R.C., Dey S.K., and Andrews G.K. Activation and distribution of inflammatory cells in the mouse uterus during the preimplantation period. J Immunol 148 (1992) 1699-1705
24. Katila T. Onset and duration of uterine inflammatory response of mares after insemination with fresh semen. Biol Reprod Mono 1 (1995) 515-517
25. Bischof R.J., Lee C.S., Brandon M.R., and Meeusen E. Inflammatory response in the pig uterus induced by seminal plasma. J Reprod Immunol 26 (1994) 131-146
26. Rubtsov Y.P., and Rudensky A.Y. TGFbeta signalling in control of T-cell-mediated self-reactivity. Nat Rev Immunol 7 (2007) 443-453
27. Tremellen K.P., Seamark R.F., and Robertson S.A. Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod 58 (1998) 1217-1225
28. Rozeboom K.J., Rocha-Chavez G., and Troedsson M.H. Inhibition of neutrophil chemotaxis by pig seminal plasma in vitro: a potential method for modulating post-breeding inflammation in sows. Reproduction 121 (2001) 567-572
29. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., et al. Neutrophil extracellular traps kill bacteria. Science 303 (2004) 1532-1535
30. Alghamdi A.S., and Foster D.N. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol Reprod 73 (2005) 1174-1181
31. Gorgens A., Leibold W., Klug E., Schuberth H.J., Martinsson, and Zerbe H. Influence of repeated artificial insemination (IS) on functional properties of uterine neutrophils of mares. Anim Reprod Sci 89 (2005) 258-261
32. Troedsson M.H., Scott M.A., and Liu I.K. Comparative treatment of mares susceptible to chronic uterine infection. Am J Vet Res 56 (1995) 468-472
33. Vogelpoel F.R., and Verhoef J. Activation of polymorphonuclear leukocytes by spermatozoa. Arch Androl 14 (1985) 123-131
34. Kotilainen T., Huhtinen M., and Katila T. Sperm-induced leukocytosis in the equine uterus. Theriogenology 41 (1994) 629-636
35. Eisenbach M. Why are sperm cells phagocytosed by leukocytes in the female genital tract?. Med Hypotheses 60 (2003) 590-592
36. Tomlinson M.J., White A., Barratt C.L., Bolton A.E., and Cooke I.D. The removal of morphologically abnormal sperm forms by phagocytes: a positive role for seminal leukocytes?. Hum Reprod 7 (1992) 517-522
37. Binks S., and Pockley A.G. Modulation of leukocyte phagocytic and oxidative burst responses by human seminal plasma. Immunol Invest 28 (1999) 353-364
38. Galdiero F., Tufano M.A., De Martino L., Capasso C., Porta R., Ravagnan G., et al. Inhibition of macrophage phagocytic activity by SV-IV, a major protein secreted from the rat seminal vesicle epithelium. J Reprod Immunol 16 (1989) 269-284
39. Gilbert R.O., and Fales M.H. The effect of bovine seminal plasma on the function and integrity of bovine neutrophils. Theriogenology 46 (1996) 649-658
40. Bennouna S., Bliss S.K., Curiel T.J., and Denkers E.Y. Cross-talk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J Immunol 171 (2003) 6052-6058
41. Chertov O., Ueda H., Xu L.L., Tani K., Murphy W.J., Wang J.M., et al. Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J Exp Med 186 (1997) 739-747
42. van Gisbergen K.P., Sanchez-Hernandez M., Geijtenbeek T.B., and van Kooyk Y. Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 201 (2005) 1281-1292
43. Saez F., Motta C., Boucher D., and Grizard G. Prostasomes inhibit the NADPH oxidase activity of human neutrophils. Mol Hum Reprod 6 (2000) 883-891
44. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6 (2006) 173-182
45. Blanco A.M., Palaoro L., Ahedo M.I., Palamas M., and Zanchetti F. Phagocytosis of ejaculated spermatozoa. Acta Cytol 36 (1992) 251-258
46. Matthijs A., Harkema W., Engel B., and Woelders H. In vitro phagocytosis of boar spermatozoa by neutrophils from peripheral blood of sows. J Reprod Fertil 120 (2000) 265-273
47. Strzemienski P.J. Effect of bovine seminal plasma on neutrophil phagocytosis of bull spermatozoa. J Reprod Fertil 87 (1989) 519-528
48. Troedsson M.H., Desvousges A., Alghamdi A.S., Dahms B., Dow C.A., Hayna J., et al. Components in seminal plasma regulating sperm transport and elimination. Anim Reprod Sci 89 (2005) 171-186
49. Vazquez J.M., Martinez E.A., Roca J., Gil M.A., Parrilla I., Cuello C., et al. Improving the efficiency of sperm technologies in pigs: the value of deep intrauterine insemination. Theriogenology 63 (2005) 536-547
50. Taylor U., Rath D., Zerbe H., and Schuberth H.J. Interaction of intact porcine spermatozoa with epithelial cells and neutrophilic granulocytes during uterine passage. Reprod Domest Anim 43 (2008) 166-175
51. Green C.E., Bredl J., Holt W.V., Watson P.F., and Fazeli A. Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro. Reproduction 122 (2001) 305-315
52. Ofek I., and Sharon N. Lectinophagocytosis: a molecular mechanism of recognition between cell surface sugars and lectins in the phagocytosis of bacteria. Infect Immun 56 (1988) 539-547
53. Topfer-Petersen E., Wagner A., Friedrich J., Petrunkina A., Ekhlasi-Hundrieser M., Waberski D., et al. Function of the mammalian oviductal sperm reservoir. J Exp Zool 292 (2002) 210-215
54. Wagner A., Ekhlasi-Hundrieser M., Hettel C., Petrunkina A., Waberski D., Nimtz M., et al. Carbohydrate-based interactions of oviductal sperm reservoir formation-studies in the pig. Mol Reprod Dev 61 (2002) 249-257
55. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6 (2006) 295-307
56. Zhang Q., Collins V., Chakrabarty K., Rose J.C., and Wu W.X. Regulation of the prostaglandin enzymatic system by estradiol and progesterone in nonpregnant sheep cervix. Reproduction 133 (2007) 1027-1034
57. Liu W., and Kelly K.A. Prostaglandin E2 modulates dendritic cell function during chlamydial genital infection. Immunology 123 (2008) 290-303
58. Par G., Geli J., Kozma N., Varga P., and Szekeres-Bartho J. Progesterone regulates IL12 expression in pregnancy lymphocytes by inhibiting phospholipase A2. Am J Reprod Immunol 49 (2003) 1-5
59. Robertson S.A., O'Leary S., and Armstrong D.T. Influence of semen on inflammatory modulators of embryo implantation. Soc Reprod Fertil Suppl 62 (2006) 231-245
60. Moffett A., and Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol 6 (2006) 584-594
61. Aplin J.D. Endometrial extracellular matrix. In: Glasser J.A.S.R., Guidice L.C., and Tabibzadeh S. (Eds). The endometrium (2002), Taylor and Francis, London 294-307
62. Curry Jr. T.E., and Osteen K.G. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24 (2003) 428-465
63. Das S.K., Yano S., Wang J., Edwards D.R., Nagase H., and Dey S.K. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse uterus during the peri-implantation period. Dev Genet 21 (1997) 44-54
64. Sunderkotter C., Steinbrink K., Goebeler M., Bhardwaj R., and Sorg C. Macrophages and angiogenesis. J Leukoc Biol 55 (1994) 410-422