Spermatozoa and seminal plasma induce a greater inflammatory response in the ovine uterus at oestrus than dioestrus

Reproduction, Fertility and Development

Volumn 21, Issue 7, 2009, Pages 817-826

  Scott, Jennifer L ^a   Ketheesan, Natkunam ^a   Summers, Phillip M ^a  

^a JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 8;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL INSEMINATION; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIESTRUS; ENDOMETRIUM CELL; EOSINOPHIL; ESTRUS; FEMALE; INFLAMMATION; MACROPHAGE; MALE; MAST CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN SECRETION; SEMINAL PLASMA; SPERM; SPERMATOZOON; UTERUS;

ANIMALS; ANTI-BACTERIAL AGENTS; DIESTRUS; EOSINOPHILS; ESTRUS; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INFLAMMATION; INSEMINATION, ARTIFICIAL; INTERLEUKIN-8; MACROPHAGES; MALE; MAST CELLS; NEUTROPHIL INFILTRATION; SEMEN; SHEEP; SPERMATOZOA; UTERUS;

OVIS;

EID: 69249129094     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09012     Document Type: Article

References (80)

1. Arici, A., Seli, E., Senturk, L. M., Gutierrez, L., Oral, E., and Taylor, H. S. (1998). Interleukin-8 in the human endometrium. J. Clin. Endocrinol. Metab. 83, 1783-1787. doi:10.1210/JC.83.5.1783
2. Assreuy, A. M. S., Calvete, J. J., Alencar, N. M. N., Cavada, B. S., Rocha-Filho, D. R., Melo, S. C., Cunha, F. Q., and Ribeiro, R. A. (2002). Spermadhesin PSP-I/PSP-II heterodimer and its isolated subunits induced neutrophil migration into the peritoneal cavity of rats. Biol. Reprod. 67, 1796-1803. doi:10.1095/BIOLREPROD.102.007013
3. Barratt, C. L. R., Bolton, A. E., and Cooke, I. D. (1990). Functional significance of white blood cells in the male and female reproductive tract. Hum. Reprod. 5, 639-648.
4. Bischof, R. J., Brandon, M. R., and Lee, C.-S. (1994a). Studies on the distribution of immune cells in the uteri of prepubertal and cycling gilts. J. Reprod. Immunol. 26, 111-129. doi:10.1016/0165-0378(94)90035-3
5. Bischof, R. J., Lee, C.-S., Brandon, M. R., and Meeusen, E. (1994b). Inflammatory response in the pig uterus induced by seminal plasma. J. Reprod. Immunol. 26, 131-146. doi:10.1016/0165-0378(94)90036-1
6. Bonatz, G., Hansmann, M.-L., Buchholz, F., Mettler, L., Radzun, H. J., and Semm, K. (1992). Macrophage- and lymphocyte-subtypes in the endometrium during different phases of the ovarian cycle. Int. J. Gynaecol. Obstet. 37, 29-36. doi:10.1016/0020-7292(92)90974-N
7. Bowen, J. A., and Burghardt, R. C. (2000). Cellular mechanisms of implantation in domestic farm animals. Cell. Dev. Biol. 11, 93-104.
8. Bytautiene, E.,Vedernikov,Y. P., Saade, G. R., Romero, R., and Garfield,R.E. (2004). Degranulation of uterine mast cell modifies contractility of isolated myometrium from pregnant women. Am. J. Obstet. Gynecol. 191, 1705-1710. doi:10.1016/J.AJOG.2004.04.008
9. Cassatella, M. A. (1995). The production of cytokines by polymorphonuclear neutrophils. Immunol. Today 16, 21-26. doi:10.1016/0167-5699(95)80066-2
10. Clark, R. A., and Klebanoff, S. J. (1976). Generation of a neutrophil chemotactic agent by spermatozoa: role of complement and regulation by seminal plasma factors. J. Immunol. 117, 1378-1386.
11. Conover, W. J., and Iman, R. L. (1981). Rank transformations as a bridge between parametric and non-parametric statistics.Am. Stat. 35, 124-129. doi:10.2307/2683975
12. Corbeil, L. B., Campero, C. M., Rhyan, J. C., Anderson, M. L., Gershwin, L. J., Agnew, D. W., Munson, L., and Bon Durant, R. H. (2005). Uterine mast cells and immunoglobulin-E antibody responses during clearance of Tritrichomonas foetus. Vet. Pathol. 42, 282-290. doi:10.1354/VP.42-3-282
13. Daimon, E., and Wada, Y. (2005). Role of neutrophils in matrix metalloproteinase activity in the preimplantation mouse uterus. Biol. Reprod. 73, 163-171. doi:10.1095/BIOLREPROD.104.038539
14. De, M., and Wood, G. W. (1990). Influence of oestrogen and progesterone on macrophage distribution in the mouse uterus. J. Endocrinol. 126, 417-424. doi:10.1677/JOE.0.1260417
15. De, M., Choudhuri, R., andWood,G.W. (1991). Determination of the number and distribution of macrophages, lymphocytes, and granulocytes in the mouse uterus from mating through implantation. J. Leukoc. Biol. 50, 252-262.
16. De, S. K., McMaster,M.T., andAndrews, G. K. (1990). Endotoxin induction of murine metallothionein gene expression. J. Biol. Chem. 265, 15 267-15 274.
17. DeLoia, J. A., Stewart-Akers, A. M., Brekosky, J., and Kubik, C. J. (2002). Effects of exogenous estrogen on uterine leukocyte recruitment. Fertil. Steril. 77, 548-554. doi:10.1016/S0015-0282(01)03062-X
18. Evans, G., and Maxwell,W. M. C. (1987) 'Salamon'sArtificial Insemination of Sheep and Goats.' (Butterworths: Sydney.)
19. First, N. L., Short, R. E., Peters, J. B., and Stratman, F.W. (1968). Transport and loss of boar spermatozoa in the reproductive tract of the sow. J. Anim. Sci. 27, 1037-1040.
20. Frayne, J., and Stokes, C. R. (1994). MHC class II positive cells and T cells in the equine endometrium throughout the oestrous cycle.Vet. Immunol. Immunopathol. 41, 55-72. doi:10.1016/0165-2427(94)90057-4
21. Garfield, R. E., Bytautiene, E., Vedernikov, Y. P., Marshall, J. S., and Romero, R. (2000). Modulation of rat uterine contractility by mast cells and their mediators. Am. J. Obstet. Gynecol. 183, 118-125.
22. Glynn, D. J., and Robertson, S. A. (2005). LPS introduced at mating induces KC production in the murine uterus during early pregnancy. Reprod. Fertil. Dev. 17, 121. [Abstract]
23. Graham, J. K. (1994). Effect of seminal plasma on the motility of epididymal and ejaculated spermatozoa of the ram and bull during the cryopreservation process. Theriogenology 41, 1151-1162. doi:10.1016/S0093-691X(05)80037-8
24. Gutsche, S., vonWolfe, M., Strowitzki, T., and Thaler, C. J. (2003). Seminal plasma induces mRNA expression of IL-1beta, IL-6 and LIF in endometrial epithelial cells in vitro. Mol. Hum. Reprod. 9, 785-791. doi:10.1093/MOLEHR/GAG095
25. Howe,G.R. (1967). Leucocytic response to spermatozoa in ligated segments of the rabbit vagina, uterus and oviduct. J. Reprod. Fertil. 13, 563-566. doi:10.1530/JRF.0.0130563
26. Kaeoket, K., Dalin, A.-M., Magnusson, U., and Persson, E. (2001). The sow endometrium at different stages of the oestrous cycle: immunohistochemical study on the distribution of SWC3-expressing cells (granulocytes, monocytes and macrophages). J.Vet. Med.A Physiol. Pathol. Clin. Med. 48, 507-511. doi:10.1046/J.1439-0442.2001.00363.X
27. Kaeoket, K., Persson, E., and Dalin, A.-M. (2002). Corrigendum to "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. 73, 89-107. doi:10.1016/S0378-4320(02)00126-4
28. Kaushic, C., Frauendorf, E., Rossoll, R. M., Richardson, J. M., and Wira, C. R. (1998). Influence of the estrous cycle on the presence and distribution of immune cells in the rat reproductive tract. Am. J. Reprod. Immunol. 39, 209-216.
29. Kotilainen, T., Huhtinen, M., and Katila, T. (1994). Sperm-induced leukocytosis in the equine uterus. Theriogenology 41, 629-636. doi:10.1016/0093-691X(94)90173-G
30. Lovell, J. W., and Getty, R. (1968). Fate of semen in the uterus of the sow: histologic study of endometrium during the 27 hours after natural service. Am. J. Vet. Res. 29, 609-625.
31. Mackler, A. M., Ducsay, T. C., Ducsay, C. A., and Yellon, S. M. (2003). Effect of endotoxin and macrophage-related cytokines on the contractile activity of the gravid murine uterus. Biol. Reprod. 69, 1165-1169. doi:10.1095/BIOLREPROD.103.015586
32. Mahajan, S. C., and Menge, A. C. (1967). Influence of reproductive phase on the inflammatory response and rate of sperm removal in the uterus and oviduct of the cow. Am. J. Vet. Res. 28, 1037-1041.
33. Martal, J., Chêne, N., Camous, S., Huynh, L., Lantier, F., Hermier, P., L'Haridon, R., Charpigny, G., Charlier, M., and Chaouat, G. (1997). Recent developments and potentialities for reducing embryo mortality in ruminants: the role of IFN-tau and other cytokines in early pregnancy. Reprod. Fertil. Dev. 9, 355-380. doi:10.1071/R96083
34. Matthijs, A., Engel, B., and Woelders, H. (2003). Neutrophil recruitment and phagocytosis of boar spermatozoa after artificial insemination of sows, and the effects of inseminate volume, spermdose and specific additives in the extender. Reproduction 125, 357-367. doi:10.1530/REP.0.1250357
35. Mattner, P. E. (1968). The distribution of spermatozoa and leukocytes in the female genital tract in goats and cattle. J. Reprod. Fertil. 17, 253-261. doi:10.1530/JRF.0.0170253
36. Mattner, P. E. (1969). Differential leukocyte responses to spermatozoa in the cervix and the uterus in ewes. J. Reprod. Fertil. 18, 297-303. doi:10.1530/JRF.0.0180297
37. McDonald, L. E., Black,W. G., McNutt, S. H., and Casida, L. E. (1952). The response of the rabbit uterus to instillation of semen at different phases of the estrous cycle. Am. J. Vet. Res. 13, 419-424.
38. McGuire, W. J., Imakawa, K., Tamura, K., Meka, C. S. R., and Christenson, R. K. (2002). Regulation of endometrial granulocyte macrophage-colony stimulating factor (GM-CSF) in the ewe. Domest. Anim. Endocrinol. 23, 383-396. doi:10.1016/S0739-7240(02)00181-9
39. McMaster, M. T., Newton, R. C., Dey, S. K., and Andrews, G. K. (1992). Activation and distribution of inflammatory cells in the mouse uterus during the preimplantation period. J. Immunol. 148, 1699-1705.
40. Mellor, A. L., and Munn, D. H. (2000). Immunology at the maternalfetal interface: lessons for T cell tolerance and suppression. Annu. Rev. Immunol. 18, 367-391. doi:10.1146/ANNUREV.IMMUNOL.18.1.367
41. Mitchell, S. E., Robinson, J. J., King, M. E., McKelvey, W. A. C., and Williams, L. M. (2002). Interleukin 8 in the cervix of non-pregnant ewes. Reproduction 124, 409-416. doi:10.1530/REP.0.1240409
42. O'Leary, S., Armstrong, D. T., and Robertson, S. A. (2002). Presence of immune modulating molecules in boar seminal plasma. Reprod. Fertil. Dev. 14, 67. [Abstract]
43. O'Leary, S., Jasper, M. J., Warnes, G. M., Armstrong, D. T., and Robertson, S. A. (2004). Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction 128, 237-247. doi:10.1530/REP.1.00160
44. Palter, S. F., Mulayim, N., Senturk, L., and Arici, A. (2001). Interleukin-8 in the human fallopian tube. J. Clin. Endocrinol. Metab. 86, 2660-2667. doi:10.1210/JC.86.6.2660
45. Pandya, I. J., and Cohen, J. (1985). The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil. Steril. 43, 417-421.
46. Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171-1180. doi:10.1095/BIOLREPROD38.5.1171
47. Phillips, D. M., and Mahler, S. (1977). Leukocyte emigration and migration in the vagina following mating in the rabbit. Anat. Rec. 189, 45-59. doi:10.1002/AR.1091890104
48. Robertson, S. A. (2002). Finding solutions: semen and maternal immune tolerance. Reprod. Fertil. Dev. 14, 60. [Abstract]
49. Robertson, S. A. (2005). Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res. 322, 43-52. doi:10.1007/S00441-005-1127-3
50. Robertson, S.A., and Seamark, R. F. (1990). Granulocyte macrophage colony stimulating factor (GM-CSF) in the murine reproductive tract: stimulation by seminal factors. Reprod. Fertil. Dev. 2, 359-368. doi:10.1071/RD9900359
51. Robertson, S. A., and Sharkey, D. J. (2001). The role of semen in the induction of maternal immune tolerance to pregnancy. Semin. Immunol. 13, 243-254.
52. Robertson, S. A., Mayrhofer, G., and Seamark, R. F. (1992). Uterine epithelial cells synthesize granulocyte-macrophage colony-stimulating factor and interleukin-6 in pregnant and nonpregnant mice. Biol. Reprod. 46, 1069-1079. doi:10.1095/BIOLREPROD46.6.1069
53. Robertson, S. A., Mau, V. J., Tremellen, K. P., and Seamark, R. (1996a). Role of high-molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J. Reprod. Fertil. 107, 265-277. doi:10.1530/JRF.0.1070265
54. Robertson, S. A., Mayrhofer, G., and Seamark, R. F. (1996b). Ovarian steroid hormones regulate granulocyte-macrophage colony-stimulating factor synthesis by uterine epithelial cells in the mouse. Biol. Reprod. 54, 183-196. doi:10.1095/BIOLREPROD54.1.183
55. Robertson, S. A., Mau, V. J., Hudson, S. N., and Tremellen, K. P. (1997). Cytokine-leukocyte networks and the establishment of pregnancy. Am. J. Reprod. Immunol. 37, 438-442.
56. Robertson, S. A., Allanson, M., and Mau, V. J. (1998). Molecular regulation of uterine leukocyte recruitment during early pregnancy in the mouse. Placenta 11 (Suppl. 1), 101-119. doi:10.1016/S0143-4004(98)80009- X
57. Robertson, S. A., Roberts, C. T., Farr, K. L., Dunn, A. R., and Seamark, R. F. (1999). Fertility impairment in granulocyte-macrophage colony stimulating factor-deficient mice. Biol. Reprod. 60, 251-261. doi:10.1095/BIOLREPROD60.2.251
58. Ross, R., and Klebanoff, S. J. (1966). The eosinophilic leukocyte. J. Exp. Med. 124, 653-660. doi:10.1084/JEM.124.4.653
59. Rozeboom, K. J.,Troedsson, M. H.T.,Molitor,T.W., and Crabo,B. G. (1999). The effect of spermatozoa and seminal plasma on leukocyte migration into the uterus of gilts. J. Anim. Sci. 77, 2201-2206.
60. Rozeboom, K. J., Troedsson, M. H. T., Hodson, H. H., Shurson, G. C., and Crabo, B. G. (2000). The importance of seminal plasma on the fertility of subsequent artificial inseminations in swine. J. Anim. Sci. 78, 443-448.
61. Rozeboom, K. J., Rocha-Chavez, G., and Troedsson, M. H. T. (2001). Inhibition of neutrophil chemotaxis by pig seminal plasma in vitro: a potential method for modulating post-breeding inflammation in sows. Reproduction 121, 567-572. doi:10.1530/REP.0.1210567
62. Sanford, T. R., De, M., and Wood, G. W. (1992). Expression of colonystimulating factors and inflammatory cytokines in the uterus of CD1 mice during Days 1 to 3 of pregnancy. J. Reprod. Fertil. 94, 213-220. doi:10.1530/JRF.0.0940213
63. Scott, J. L., Ketheesan, N., and Summers, P. M. (2006a). Leukocyte population changes in the reproductive tract of the ewe in response to insemination. Reprod. Fertil. Dev. 18, 627-634. doi:10.1071/RD05165
64. Scott, J. L., Ketheesan, N., and Summers, P. M. (2006b). Presence of TGFbeta but not IL-8 or GM-CSF in ram seminal plasma. In 'Proceedings of the 37th Annual Conference for the Society of Reproductive Biology, Gold Coast, Queensland'. p. 49. [Abstract 205]
65. Scott, J. L., Ketheesan, N., and Summers, P. M. (2007). Granulocytemacrophage colony-stimulating factor and interleukin-8 in the reproductive tract of ewes following oestrus and mating. Reprod. Fertil. Dev. 19, 585-593. doi:10.1071/RD06137
66. Sharkey, D. J., and Robertson, S. A. (2004). Seminal plasma TGF-beta activates pro-inflammatory cytokine synthesis in human cervical epithelial cells. Reprod. Fertil. Dev. 16, 229. [Abstract]
67. Sharkey, D. J., Tremellen, K. P., Dekker, G. A., and Robertson, S. A. (2002). Seminal cytokine concentration and human reproductive outcome. Reprod. Fertil. Dev. 14, 81. [Abstract]
68. Sjöblom, C. S., Roberts, C. T., Wikland, M., and Robertson, S. A. (2005). Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology 146, 2142-2153. doi:10.1210/EN.2004- 1260
69. Spencer, T. E., Johnson, G. A., Bazer, F. W., and Burghardt, R. C. (2004). Implantation mechanisms: insights from the sheep. Reproduction 128, 657-668. doi:10.1530/REP.1.00398
70. Starkey, P. M., Clover, L. M., and Rees, M. C. P. (1991). Variation during the menstrual cycle of immune cell populations in the human endometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 39, 203-207. doi:10.1016/0028-2243(91)90058-S
71. Summerfield, N. J., andWatson, E. D. (1998). Endometrial macrophage populations in genitally normal mares at oestrus and dioestrus and in mares susceptible to endometritis. Equine Vet. J. 30, 79-81.
72. Thompson, L.A., Barratt, C. L. R., Bolton,A. E., and Cooke, I.D. (1992).The leukocytic reaction of the human uterine cervix.Am. J. Reprod. Immunol. 28, 85-89.
73. Tibbetts, T. A., Conneely, O. M., and O'Malley, B.W. (1999). Progesterone via its receptor antagonizes the pro-inflammatory activity of estrogen in the mouse uterus. Biol. Reprod. 60, 1158-1165. doi:10.1095/ BIOLREPROD60.5.1158
74. Tremellen, K. P., Seamark, R. F., and Robertson, S. A. (1998). Seminal transforming growth factor beta-1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol. Reprod. 58, 1217-1225. doi:10.1095/ BIOLREPROD58.5.1217
75. Troedsson, M. H. T., Liu, I. K. M., and Crabo, B. G. (1998). Sperm transport and survival in the mare: a review. Theriogenology 50, 807-818.
76. Troedsson, M. H.T., Loset, K.,Alghamdi,A. M., Dahms,B., and Crabo,B. G. (2001). Interaction between equine semen and the endometrium: the inflammatory response to semen. Anim. Reprod. Sci. 68, 273-278. doi:10.1016/S0378-4320(01)00164-6
77. Tyler, K. R. (1977). Histological changes in the cervix of rabbits after coitus. J. Reprod. Fertil. 49, 341-345. doi:10.1530/JRF.0.0490341
78. Watari, M.,Watari, H., Fujimoto, T.,Yamada, H., Nishihira, J., Strauss, J. F., and Fujimoto, S. (2003). Lipopolysaccharide induces interleukin-8 production by human cervical smooth muscle cells. J. Soc. Gynecol. Investig. 10, 110-117. doi:10.1016/S1071-5576(02)00219-8
79. Wuyts, A., Proost, P., and Van Damme, J. (1998). Interleukin-8 and other CXC Chemokines. In 'The Cytokine Handbook'. (Ed. A. Thomson.) pp. 271-311. (Academic Press: London.)
80. Yeaman, G. R., Collins, J. E., Currie, J. K., Guyre, P. M., Wira, C. R., and Fanger, M. W. (1998). IFN-gamma is produced by polymorphonuclear neutrophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils. J. Immunol. 160, 5145-5153.