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Seminal Plasma in Early Murine and Human Pregnancy to.g.atÌ The immunoregulatory role of seminal plasma in early murine and human pregnancy Kelton Paul Tremellen MB, BS (Hons.) Department of Obstetrics and Gynaecology, University of Adelaide, Adelaide, Australia A thesis submitted to the University of Adelaide in fulfilment of the requirements for admission to the degree of Doctor of Philosophy December 1998 The desire of lqnowledge, like the thirst of riches, increases ever with the acquisition of it. Laurence Steme 17r3-r768 Abstract In mice, as in other mammals, deposition of semen in the female reproductive tract provokes local molecular and cellular changes that resemble an inflammatory response. The studies described in this thesis were initiated to investigate two aspects of the post-mating inflammatory cascade. Firstly, the molecular nature of the interaction between semen and cells within the female reproductive tract was cha¡acterised. Secondly, the physiological role that the post-mating inflammatory response plays in establishment of an immunological environment conducive to the accommodation of the semi-allogenic concepfus was evaluated. Previous studies have implicated cytokines produced by the murine uterine epithelium in regulating changes in tafficking and phenotype of endometrial leukocytes after mating. Of particular importance is the cytokine granulocyte- macrophage colony-stimulating factor (GM-CSF), the synthesis of which is up- regulated at least 2O-fold in response to proteinaceous factors in semen originating from the seminal vesicle gland. Fractionation of seminal vesicle gland secretions by size exclusion chromatography identified two moieties which could trigger the release of GM-CSF; an unidentified 650 kDa protein and the cytokine transforming growth factor beta-one (TGFBT). Since TGFBr had not previously been identified within murine seminal plasma, the TGFp, content of various male accessory sex glands (seminal vesicle, prostate, coagulating gland) was assessed. This revealed that seminal vesicle secretions contributed more than 90o/oto the TGFpI content of seminal plasma, consistent with the observation that secretions from this gland, but not other accessory sex glands, were able to initiate an increase in uterine epithelial cell GM-CSF production in vitro. Seminal vesicle-derived TGFp, was found to be secreted predominantly in the latent form. However, the murine uterus does appear to have the capacity to release bioactive TGFpr from seminal plasma, since within an hour of mating, the majority of uterine luminal TGFP' is present in the bioactive form. TGFPT, TGFP, and activin, all members of the TGFP superfamily, were noted to increase uterine epithelial cell GM-CSF ouþut in vitro. TGFBr and TGFpt exhibited similar potency, with activin showing only weak GM-CSF stimulating activity. Neutralisation of TGFB, bioactivity resulted in a75o/o decline in seminal vesicle GM-CSF stimulating activity, thereby implicating TGFpr as the dominant agent responsible for triggering the post-mating inflammatory response in the mouse. Fr¡rthermore, intrauterine injection of rTGFp, was observed to increase uterine epithelial cell GM-CSF production, and result in cellular changes that were comparable to those seen following natural mating. At the onset of these studies, little was known of the nafltre, location and molecular biology of the post-coital inflammatory response in women. In an attempt to determine if mechanistic parallels existed between mice and women, the effect on GM-CSF ouþut of addition of rTGFp, and semen to human endometrial and cervical keratinocyte cultures was determined. Both whole semen and rTGFpt significantly increased the release of GM-CSF and chemotactic activþ (assessed by an invitro leukocyte migration assay) from human cervical keratinocyte cultures. Conversely, only a small increase in ouþut of GM-CSF from endometrial cells was observed following rTGFp, treatment. This response may be less physiologically important than the cervical response, since in the human, ejaculation occurs at the level of the cervix, with seminal plasma not coming into direct contact with the endometrium. The second main aim of these studies was to explore interactions between the post-mating inflammatory response and maternal immune reactions to paternal antigens in semen. This was prompted by reports that semen exposure could induce maternal hlpo-responsiveness in cell-mediated immunity to paternal antigens. Delayed type hypersensitivity and complement-fixing anti-sperm IgG2b responses were significantly reduced in mice that received intrauterine inoculations of epididymal sperm in the presence of rTGFp,, compared with mice that received sperm alone, and were comparable to values obtained from mice inoculated naturally by mating. This data suggests that TGFp and /or other factors within seminal plasma may act to inhibit the Th1 compartment of the female immune response to seminal antigens. In addition, female mice were immunised with sperm or sperm plus TTGFBt prior to mating, to determine if deviation of the immune response to paternal antigens could alter pregnancy outcome. Immurrisation of females resulted in a small reduction in litter size, but fetal and placental weights were increased in the group immunised with sperm plus rTGFB,. Taken together, these observations suggest that seminal TGFPr may have a role in promoting successful pregnancy through initiating matemal immune "tolerance" to patemal antigens prior to implantation of the conceptus. ll Finally, the role of semen exposure in human reproduction w¿rs investigated by measwing the effect of intercowse on pregnancy outcome in women r:ndergoing in vitro fertllisation (fVF) with thawed embryo fransfer. No significant difference in pregnancy success was obsen¡ed between women who were exposed to semen around the time of embryo transfer compared to those women who abstained. Together, these studies identiff seminal TGFPr as an important triggering agent in both the human and murine post-mating inflammatory response. Fr¡rthermore, the cytokine environment provided by seminal TGFp', perhaps in conjunction with other seminal factors such as prostaglandin E, may promote successful pregnancy by initiating matemal "tolerance" to patemal antigens present within the ejaculate. The generation of a permissive immunological environment, prior to the trophoblast making contact with the maternal immune system at implantation, may favour the growth and development of the semi-allogenic conceptus. lu Acknowledgments This study was made possible with the support and resources provided to me through the Department of Obstetrics and Gynaecology at the University of Adelaide. I am deeply indebted to Professor Jeffrey Robinson for encouraging me to consider a career in clinical research. I am extremely grateful to Dr Sarah Robertson and Dr Robert Seamark for helping guide me down this path of scientific endeavour. Dr Robertson, my principal supervisor, provided an excellent role model on how to perform "excellent science". For this I am eternally grateful. I would also like to express my appreciation to Mr Don Bigham for his assistance with computing during the preparation of this thesis and Dr Leon Bignold for allowing me access to his chemotaxis laboratory. Thanks also go to Mrs Vicki Mau for performing the RT-PCR work described in this thesis. Professors Norman and Kerin provided assistance with the design of the human IVF trial, for which I am very grateful. I am also indebted to the nursing staff at the University of Adelaide's reproductive medicine program, especially Paula Scanlon, Margaret Hall and Helen Alvino, for helping recruit patients for the fVF intercourse trial. I would also like to thank all the patients who agreed to be involved in the trial, as well as those who consented to donating uterine tissue samples. Finally I would like to express my gratitude to my wife Katherine for her unwavering enthusiasm, encouragement and patience during the course of this study. Publications arising from these studies 1. Robertson SA, Mau VJ, Tremellen KP, Seamark RF. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J. Reprod. Fertl. 1996; 107:265-277. 2. Robertson SA, Mau VJ, Hudson SA, Tremellen KP. Cytokine-leukocyte networks and the establishment of pregnancy. Am. J. Reprod. Immmol. 1997;37:438-442. 3. Tremellen KP, Seamark RF, Robertson SA. Seminal transforming growth factor B, stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitrnent in the mr¡rine uterus. Biol. Reprod. 1998; 58:1217- 1,225. 4. Tremellen KP, Robertson SA. Seminal priming in successful mammalian pregnancy. Proceedings of the VII International Conference of Reproductive Immunology. New Delhi, India, 27ú40t^ October 1998. Patent 1. Treatment and diagnosis of infertility using TGFp or activin. InternationalpublicationnumberV/O 93/39021. Published 11ù Septer¡rber 1998 vl Short communications 1. Tremellen I(P, Robertson SA. Isolation of seminal vesicle proteins responsible for the initiation of the post-mating inflammatory response. Proceedings of the South Australian branch of the Australian Society for Medical Research. 31" May 1996. Awa¡ded the Ansett Ausfralia award for best oral presentation by a new investigator. 2. Tremellen I(P, Robertson SA. Potential role for transforming growth factor beta in modulating the maternal immune response during early murine pregnancy. 35* National Scientific Conference, The Australian
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