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BY Robert L. Gendron Department of Physiology Mcgill University

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BY Robert L. Gendron Department of Physiology Mcgill University c TBB IKMONOBIOLOGY OF FETAL RBSORPTIOR IR MICB BY Robert L. Gendron Department of Physiology McGill University Montreal, Quebec July, 1991 A thesis submitted to the Faculty of Graduate studies and Research in partial fulfillment of the requirements for the degree of Doctor of Philosophy c R.L. Gendron, 1991 c al c ABSTRACT Ph. D. Robert L. Gendron Physiology Human pregnancy failure is traumatic. Allogeneic concepti can be considered as grafts due to the presence of potentially foreign paternal antigens expressed in fetal tissue. Current thought on spontaneous pregnancy loss is centred around the role of the maternal immune response against the fetal tissues. However, the cellular immune events which mediate spontaneous fetal loss are at present only partially characterized. This thesis contributes to the knowledge of these events by addressing the role of non-specific immune reactions in fetal resorption in the mouse. Utilizing immunohistochemistry, we demonstrated that a large increase in the numbers of natural killer (NK) cells infiltrating the decidual-ectoplacental cone junction during days 6-9 of gestation precedes fetal resorption (occurring at a frequency of 25-30%) in CBA/J X DBA/2 concepti. The NK-modulatory treatments polyinosynic cytidilic acid (POLY I:C) and anti-asialo GMl (aAGMl), which alter the spontaneous resorption frequency, also alter the frequency of NK-infiltrated c a2 concepti. From these studies we concluded that NK cells may be important cellular effectors of fetal resorption. Since eicosanoids are thought to be instrumental in NK regulation and feto-maternal immunobiology, we focused on arachidonic acid metabolites in characterizing the compounds regulating fetoplacenatal NK activity. Individual fetoplacental units from normal and CBA/J X DBA/2 pregnancies were analysed for NK regulatory activity at stages corresponding to the increase in NK cell number. Using silica column extraction and testing for NK activity modulation in vitro, we found that CBA/J X DBA/2 fetoplacental units were deficient in a lipophilic NK inhibitory factor that was expressed at peak levels on days 7-8 in normal fetoplacental units. The deficiency in NK suppression correlated with NK infiltration and with resorption frequency in CBA/J X DBA/2 concepti. These results demonstrated that CBA/J X DBA/2 fetoplacental units may be inherently predisposed to NK-mediated fetal resorption. In a subsequent paper, we addressed the phenotype and functional significance of the NK inhibitory factor(s) in normal versus resorption-prone pregnancies. By using silica column extraction and specific radioimmunoassay in individual fetoplacental units, we 0 a3 c found that CBA/J X DBA/2 concepti were deficient in the production of the lipoxygenase metabolite leukotriene B4 (LTB4). Furthermore, we demonstrated that LTB4 may be functionally important in averting NK mediated fetal resorption. Supplementation in vitro of fetoplacental extracts from resorption-prone fetoplacental units with exogenous LTB4 resulted in the restoration of the extract's NK suppressive capacity. These results demonstrated that LTB4 may be important in averting NK­ mediated fetal resorption. In order to more fully characterize the role of non-specific immune reactions in fetal resorption, we utilized lipopolysaccharide (LPS) in an attempt to trigger activated macrophages in the fetoplacental unit. We demonstrated an extreme sensitivity to very low concentrations of LPS in early pregnancy. LPS-induced fetal resorption was associated with the intra-uterine production of tumor necrosis factor alpha (TNF-a). In the course of our analysis of the sites of fetoplacental TNF-a production, we found that a novel form of TNF-a with a molecular weight of 50 kilodaltons is expressed in the developing vertebrate nervous system. These findings suggest that TNF-a may play a plieotrophic role in both fetal development and resorption. The results presented 0 a4 in this thesis provide an in-depth analysis of some of the functional deficiencies and immunological events predisposing allogeneic pregnancies to spontaneous fetal loss. The major focus is in providing examples of how non-major histocompatibility complex (MHC)-specific immune reactions can determine fetal survival. c c RESUME PhD Robert L. Gendron Physiologie Chez l'homme, l'infecondite est une condition traumatique. Le foetus exprime des antigenes paterneles, et peut done etre considere comme un greffon. Tout laisse penser, en fait, que l'avortement spontane origine d'une reponse immunitaire de la mere encers son foetus. Cette these analyse les consequences de l'immunite non-specifiques sur le taux d'avortement spontane chez la souris, et les correle au evenements cellulaires et biochemiques observe. Utilisant les techniques d'immunolcalisation sur coups de tissue, nous avons demontre un grand nombre de cellules de type natural killer (NK) infiltrant la jonction du cone decidua-placentaire lors de croissements entre les souches de souris CBA/J X DBA/2. Les cellules NK apparaissent entre la 6 ieme et la 9 ieme journee de grossesse et precede la resorption des foetus (frequence de 20-30%). La modulation des cellules NK durant la grossesse avec l'agent POLY I:C ou des anticorps anti-asoalo GMl altere la frequence d'avortement spontane, et le nombre d'unite placentaire infiltre de cellules NK. Nous concluons de cette etude que les cellules NK jouent un rOle important dans l'avortement spontane. Les eicosanoides sont associes a la modulation de l'activite NK et de fa~on generate a l'immunobiologie de la grossesse. Nous avons done etudie le rOle des metabolites de l'acide arachidonique sur l'activite NK a l'interface foetoplacentaire tors de grossesses normales ou resultant du croissement CBA/J X DBA/2. Nous avons prepare des extraits d'unite foetoplacentaires et purifie les compose lipophiliques par chromatographie sur silice. Par la suite, ces composes furent analyse in-vitro pour leurs effects sur l'activite NK. Nous avons observe qu'un facteur lipophilique present auxjours 8-8 des unites foetoplacentaires normales 0 est absent des extraits CBA/J X DBA/2. Ces resultats demontrent que les unite foetoplacentaires CBA/J X DBA/2 possedent probablement un default primaire les c predisposant a l'activite NK et ultimement a la resorption des foetus. Une analyse subsequente a permit de definir le phenotype et !importance biologique du compose lipophilique pour le succes de la grossesse. La substance fut identifie par chromatografie sur silice et par dosage radio-immunologique comme un metabolite de la lipoxygenase, le leukotriene B4 (LTB4). L'addition du L TB4 aux extraits foetoplacentaires CBA/J X DBA/2 permet de contr6le ractivite NK in-vitro. Ces travaux suggerent que I'absence du L TB4 represente une anomalie biochemique probablement responsable du taux eleve d'avortement spontane chez le croissement CBA/J X DBA/2. Pour mieux definir les mechanismes immunologiques non-specifiques en cause dans le rejet du foetus, nous avons etudie la contibution des macrophages. Le lipopolysaccharide (LPS) fut utilise pour activer les macrophages. Nous avons demontre que le LPS a faible dose pertube fortement la viabilite de la grossesse. L'effect du LPS sur la resorption du foetus est associe a la production intra-uterine de TNF-a. Aussi, nous avons observe qu'un forme nouvelle de TNF-a ayant un poids moleculaire de 50 Kilodaltons est presente dans le systeme nerveux foetus. En conclusion, cette these apporte une meilleure connaissance des anomalies biochemiques susceptible d'initier l'avortement spontane, et contribue a definir la participation des processus immunitaires non-specifiques a la destruction du foetus. as c ACDOWLBDGBHBN'l'S I extend my sincere gratitude to my research supervisors, Or. M.G. Baines and Dr. R. Farookhi for their support, guidance, encouragement and cooperation. I thank the faculty members with whom I have collaborated, in particular, Dr. o.w. Blaschuk, Dr. w.s. Lapp, and Dr. w.s. Powell. I thank the student and staff members of the Physiology Department for contributing to my scientific and instructional development. I thank the members of the McGill Centre for the Study of Reproduction for support and intellectual guidance. A very warm thanks to the students and staff of the Microbiology & Immunology Department for providing scientific assistance in addition to making me really feel like "one of the gang". All of the above has made my stay a truly memorable and enjoyable experience. Among the many people I wish to thank are Ginette Berube, Richard Boismenu, Josee Brisbois, Feng Cai, sung Cha, Paul Carrier, Cosimo Oemitri, Ralph Diorio, Alain Ouclos, Francine Gravelle, Sylvie Gravel, Alan Lazarus, Ben Lee, Ursula McGuinness and Fred Nestel. A very special thanks to Emilia Anteka, Shelly Feran, Lori Haughn, Marina Pascali, Stev Thomas 0 a6 and Nicolai Van Oers. Finally, I thank my parents, brothers and grandmother for their continued support and endless encouragement. 0 a7 c CLAIM OF CONTRIBUTIOR TO LITERATURE 1. Demonstration that spontaneous fetal resorption in mice is preceded by early NK infiltration at the decidual-ectoplacental cone area. 2. Characterization and time course analysis of the expression of a lipophilic NK regulatory activity in normal mouse fetoplacental units. Partial abrogation of the activity by ASA suggested the involvement of a cyclooxygenase metabolite. 3. Identification of a deficiency of fetoplacental lipophilic NK suppressive activity in the CBA/J X DBA/2 conceptus which correlates with NK infiltration and fetal resorption. Phenotype analysis of the lipophilic NK regulatory fetoplacental extract by radioimmunoassay showed that CBA/J X DBA/2 concepti were deficient in the production of the lipoxyqenase metabolites LTB4 but not the cyclooxygenase metabolite PGE2. 4. Increased fetal viability was observed in CBA/J X DBA/2 second matings. These second matings showed LTB4 and PGE2 concentrations that more closely resembled those observed in normal pregnacies, suggesting that the uterus may retain the memory of 0 as c a "priming" event even from a non-compatible male.
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