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MORPHOLOGICAL, CELLULAR, and MOLECULAR EFFECTS of BISPHENOL a (BPA) and BISPHENOL ALTERNATIVES in the MOUSE MAMMARY GLAND Deirdr

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MORPHOLOGICAL, CELLULAR, and MOLECULAR EFFECTS of BISPHENOL a (BPA) and BISPHENOL ALTERNATIVES in the MOUSE MAMMARY GLAND Deirdr MORPHOLOGICAL, CELLULAR, AND MOLECULAR EFFECTS OF BISPHENOL A (BPA) AND BISPHENOL ALTERNATIVES IN THE MOUSE MAMMARY GLAND Deirdre K. Tucker A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Curriculum of Toxicology in the School of Medicine. Chapel Hill 2017 Approved by: William Coleman Suzanne Fenton Charles Perou Lola Reid John Rogers ©2017 Deirdre K. Tucker ALL RIGHTS RESERVED ii ABSTRACT Deirdre K. Tucker: Morphological, cellular, and molecular effects of bisphenol A (BPA) and bisphenol alternatives in the mouse mammary gland (Under the direction of Suzanne E. Fenton) Bisphenol A (BPA) is an industrial chemical used in manufacturing of epoxy resins and polycarbonate plastics that are in many consumer products, including canned foods, plastic bottles, and water supply pipes, thus increasing human exposure. The effects of early life exposure to BPA have been extensively documented in several tissues of multiple species. Animal studies have been critical in identifying morphological and transcriptional changes in the mammary gland, at human relevant BPA exposures (≤0.05 µg/kg bw/d). These studies have prompted increasing public concerns surrounding the use of BPA in consumer products and have warranted the implementation of alternative analogues, including the fluorinated and sulfonated derivatives, BPAF and BPS. Estrogenicity screenings of these analogues have revealed either enhanced or comparable properties to BPA, indicating their endocrine potential which may impact the mammary gland. This research investigates the potential effects of early life exposure to the bisphenol analogues, BPAF, BPS, and BPA on pubertal development and adult mammary gland alterations, as well as cellular and molecular pathways that are associated with these changes. Disposition studies were performed in pregnant CD-1 dams exposed once to BPA (50 mg/kg), BPAF (5 mg/kg), or BPS (5 mg/kg) to confirm transplacental transfer and to determine serum and urinary pharmacokinetics. This information was used to establish a proper dosing iii schedule for future developmental exposures. Dams had similar serum, urinary and fecal half- lives that were all ≤ 8 hr for all analogues. Urinary recovery was greatest for BPS whereas BPAF recovery was greater in the feces. All chemicals were confirmed to cross the placenta. Pregnant mice were then exposed to BPA (0.5-50 mg/kg) or BPAF and BPS (0.05-5 mg/kg) during the fetal period when rudimentary mammary placodes are forming (GD 10-17). Pubertal mammary glands from offspring exposed to every chemical exhibited accelerated development that included increased terminal end buds, branching density and longitudinal growth. The incidence of inflammation and proliferative epithelial lesions significantly increased in adult glands and produced adenocarcinomas at less than 12 mos. in chemically treated groups, with the highest occurrence in BPAF 5 mg/kg and BPS 0.5 mg/kg. Mammary transplants from digested FACS sorted mammary glands (PND 19-56) prenatally exposed to these two chemicals/concentrations revealed that neither BPAF nor BPS increased mammary repopulating unit frequency, changed expression of stem cell maintenance and differentiation genes, or altered total epithelial cell counts from pubertal mammary glands even though morphological changes at these time-points suggested that they would. Genome-wide analysis and RT-PCR validation of RNA from pubertal mammary glands revealed BPAF altered immune pathways, whereas BPS altered circadian rhythm and mitochondrial dysfunction pathways. Many gene changes occurred during early puberty (PND 20) and others continued into late puberty (PND 55). Neither chemical altered genes associated with apoptosis or from the nuclear receptor estrogen family except Errg (BPAF), but they did cause changes in Evi5 and Tsc22d1, two genes that are influential in epithelial cancers and adenocarcinomas. Together these data suggest that prenatal exposure to BPAF and BPS can morphologically alter the pubertal mammary gland in ways that persist into adulthood and encourage neoplasia formation. iv DEDICATION To my family who has been very instrumental in my success as a woman, mother, and scientist. v ACKNOWLEDGEMENTS I would like to extend a heartfelt thank you to my committee members Dr. William Coleman, Dr. Lola Reid, Dr. Charles Perou and Dr. John Rogers for providing their support and extensive knowledge that has certainly helped to shape this project. I would also like to thank the members of the Fenton lab, both past and present members for being such great team players. I am very thankful to have been able to receive great knowledge and feedback from you all and thank you for letting me share everything that I have learned. This project would not have been completed were it not for the many collaborators and Core facilities that I was privileged to have access to during my tenure at the NIEHS. Thank you to Maria Sifre and Page Meyers for the assistance with the flow cytometry and mammary gland transplants, respectively. Thank you to Fred Lih at the NIEHS and Drs. Antonia Calafat and Xiaoyun Ye from CDC who helped to run the samples from my disposition study. Additionally, I would like to thank Dr. Schantel Bouknight for her assistance with histo-pathological diagnoses and Grace Kissling for her statistical expertise. Thank you to Drs. Kevin Gerrish and Keith Shockley who were instrumental in helping me with my microarray experiments and data analysis. Lastly, I am extremely grateful to the NIEHS Histology core laboratory and Julie Foley for her collaborations on my project. I don’t think I could have made it this far without the help of some very awesome women. Dr. Bayse thank you so much for helping me find my passion for Toxicology. vi Furthermore, thank you Dr. Suzanne Fenton for your incredible mentorship and friendship. Thank you for pushing me even when I didn’t want to be pushed. Lastly, I would like to thank all my family and friends especially my grandmother, Irene Hadley, and my mother Shirley Ingram. I would not be the woman that I am today had it not been for these two wonderful women. Also, I am so very grateful for the two most important men in my life. Thank you, Reggie, for being such a wonderful and supportive husband throughout out this journey. You were there from day one, and I can’t tell you how much I appreciate you. To my wonderful son, Sean, thank you for continuing to be mommy’s greatest inspiration. I will always strive to be the best person I can because of you. vii TABLE OF CONTENTS LIST OF TABLES ………………………………………………………………………......…...ix LIST OF FIGURES………………………………………………………...…………………….xi LIST OF ABBREVIATIONS…………………………………………………………………...xiv CHAPTER: Introduction…………………………………………...……………..........................1 CHAPTER 2: Disposition and early developmental effects of bisphenol analogues in CD-1 mice……………...…………………..………………………59 CHAPTER 3: Precocious development, ductal hyperplasia, and mammary tumors in CD-1 mice following prenatal exposure to bisphenol analogues………….......95 CHAPTER 4: Isolation and characterization of mammary stem cells following prenatal bisphenol analogue exposures in CD-1 mice………...………………………….153 CHAPTER 5: Effects of prenatal exposure to BPAF and BPS on peri-pubertal mammary gland gene expression in CD-1 mice……………………………...…193 CHAPTER 6: Conclusions and Future Perspectives…………………………………………...239 APPENDIX I: Preparation of high quality hematoxylin and eosin-stained sections from rodent mammary gland whole mounts for histopathologic review……….257 APPENDIX II: The mammary gland is a sensitive pubertal target in CD-1 and C57Bl/6 mice following perinatal perfluorooctanoic acid (PFOA) exposure…………..271 APPENDIX III: Premature animal deaths…………………………………………………..….310 viii LIST OF TABLES Table 2.1 - Toxicokinetic parameters of BPA, BPAF, and BPS in maternal serum, urine, feces and amniotic fluid………………………………………………………80 Table 2.2 - Total bisphenol serum concentrations in female and male offspring following a single in utero exposure on GD16……………………………………...81 Table 2.3 - PND 1 pup weights and litter outcomes following BP analogue in utero exposure………………………………………………………………….…82 Table 3.1 - Taqman gene primer list used for mammary gland samples………….…………....124 Table 3.2 - Days spent in estrus, diestrus and proestrus following in utero exposure to BPA, BPAF, and BPS (PND 63-83)…….………………………………….....…125 Table 3.3 - Qualitative pubertal mammary gland development scores of female offspring exposed in utero to BPA, BPAF, and BPS………………………...…..…126 Table 3.4 - Mammary gland diagnosis by time of death following prenatal exposure to BPA, BPAF, or BPS………………………………………………………….…127 Table 3.5: Proliferative epithelial lesions and tumors following prenatal exposure to BPA, BPAF, or BPS……………………………………………………...……..….128 Table 3.6 - Lesion Incidences…………………………………………………….………..129-130 Table 3.7 - Combined Incidences (p-values) ...………………………………………………...131 Table 4.1 - Flow Cytometry Antibodies Needed for Cell Fraction Sorting…………………….177 Table 4.2 - MaSC-Related Gene Primer List………………………………………………...…178 Table 4.3 - Mouse Strain Comparison of MRU Frequency in Controls………………………..179 Table 4.4 - MRU frequency following transplants of isolated MaSC from bisphenol analogue exposed mammary tissue………………………………….….180 Table 5-1 - Gene primer list…………………………………………………………………….216 Table 5.2 - Top 10 up and down regulated gene expression changes in mammary following
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