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Estrogen Status Alters Tissue Distribution and Metabolism Of THE EFFECT OF ESTROGEN STATUS ON SELENIUM METABOLISM IN FEMALE RATS DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Xiaodong Zhou, M.S. ***** The Ohio State University 2007 Dissertation Committee: Approved by Dr. Anne M. Smith, Advisor Dr. Mark L. Failla Dr. Steven K. Clinton Advisor Dr. Charles L. Brooks The Ohio State University Nutrition Graduate Program ABSTRACT An association between male and female sex hormones and selenium (Se) status has been reported in animals and humans. These relationships may be important in the regulation of selenium metabolism and relative to the possible use of selenium as an adjunct for treatment of hormone-related diseases such as breast cancer. Insights about impact of estrogen on distribution and metabolism of selenium in multiple tissues are limited. The purpose of the first part of this study was to examine the effect of estrogen status on the absorption, tissue distribution and metabolism of orally administered 75Se-selenite. Female Sprague Dawley (SD) rats were bilaterally ovariectomized and implanted with either a placebo pellet (OVX, n=16) or pellet with estradiol (OVX+E2, n=16) at 7 weeks of age. At 12 weeks of age, 60 µCi (43 ng total) of 75Se as selenite was orally administered to each rat. Blood and organs were collected 1, 3, 6, and 24h after dosing (4 rats/group at each time). Although apparent absorption of 75Se was independent of estrogen status, hormone associated differences of 75Se levels (P<0.05) were noted in plasma, RBC, liver, heart, kidney, spleen, brain, and thymus at certain times. For ii example, total 75Se in liver was greater in OVX than in OVX+E2 rats after 1 hour (13.1% vs.3.9% of total dose). However, OVX+E2 group had greater 75Se in liver than OVX group (18.0% vs. 10.9%) after 6h. The relative distribution of 75Se between cytosol and membrane fractions in organs was independent of estrogen status. Also the relative distribution of 75Se among the selenoproteins in cytosol of the organs was not influenced by estrogen status. However, plasma selenoprotein P (SelP) in OVX+E2 group contained a greater percentage of administered 75Se at 3, 6 and 24h after gavage compared to OVX group (P<0.05). 75Se in plasma glutathione peroxidase (GPx) also was greater in OVX+E2 compared to OVX group at 24 h (P<0.05). The second aim was to investigate the effect of estrogen status on selenium status in blood and tissues and explore whether hepatic levels of SelP mRNA and GPx1 mRNA were affected by estrogen status. SD female rats (7 weeks of age) were bilaterally ovariectomized and implanted with either a placebo pellet (OVX, n=6) or pellet with estradiol (OVX+E2, n=6). A second set of SD female rats also were sham-operated and implanted with a placebo pellet (Sham, n=24; 6 rats in each 4-day estrous cycle). Blood and tissues were collected at 12 weeks of age. Estrogen significantly increased selenium status as measured by selenium concentration and GPx activity in plasma, liver, and brain. Selenium concentration in RBC was also increased by estrogen treatment. Selenium status in kidney and heart was independent of estrogen treatment. Real-time RT-PCR iii analysis demonstrated that both hepatic SelP and GPx1 mRNA were significantly increased by estrogen treatment (P<0.05). In conclusion, these results suggest that estrogen status affects distribution of ingested selenium in tissue- and time-dependent manners. Expression of hepatic SelP and GPx was regulated by estrogen at both mRNA and protein levels. As SelP has been shown to function as a selenium transporter, estrogen regulation of SelP may play an important role in whole body metabolism of selenium. iv Dedicated to my wife, Wenyi v ACKNOWLEDGMENTS During my Ph.D. journey at The Ohio State University, there has been so much support and encouragement without which this dissertation could not have been possible. I would like to express my sincere gratitude to my advisor, Dr. Anne Smith. Her intellectual ideas, guidance, and research expertise was a tremendous help throughout my dissertation research. Especially, I am grateful for her patience and encouragement that helped me through each difficulty during my study. I wish to thank Dr. Mark Failla. His insightful advice and continuous intellectual challenge have been key in facilitating my growth as a researcher. I sincerely appreciate my committee members, Dr. Steven Clinton and Dr. Charles Brooks for sharing their time and research expertise with me over the years, and for their valuable advice on my dissertation research. I wish to thank Dr. Zhontang Yu and Dr. Mark Morrison for the incredible opportunity to work in the molecular microbiology lab to conduct the real-time RT-PCR analysis. Thanks to Dr. Jing Chen for training me on the molecular biology techniques, to Dr. Valerie Bergdall for the training on estrus cycle determination in rats and valuable advice on animal handling, to Dr. Michael Darby for helping me set up the gamma vi counter, to Dr. John Bruno for his kindness to let me use his microscope and dissection equipment at Townshend Hall, to Jodi Griffith for her help on animal tissue collection, to Dr. Maureen Geraghty for her encouragement and friendship, and to Jeanne McGuire for the help on radioactive materials handling. My special gratitude goes to Dr. Kristina Hill, and Dr. Raymond Burk at the Vanderbilt University, for their assistance on plasma selenoprotein P measurement, and insights on selenium research over the years. I am grateful to the financial support from OARDC for my dissertation research. I wish to express my appreciation to the Department of Chemistry, who granted me the highly competitive teaching assistantship during my final stage of the Ph.D. study. Lastly, I would like to especially thank my wife, Wenyi and my parents, for their love, faith, and expectation. I would not have reached this point without their consistent support. vii VITA January 21, 1971……………………Born Mianyang, Sichuan Province, China 1995…………………………………Bachelor of Medicine, West China University of Medical Sciences, China 1998…………………………………M.S., Human Nutrition, West China University of Medical Sciences, China 1998-2001…………………………..Clinical Dietitian and lecturer, First University Hospital, West China University of Medical Sciences, China 2001-2006…………………………..Graduate Research and Teaching Associate, Department of Human Nutrition, The Ohio State University 2006-present…………………………Graduate Teaching Associate, Department of Chemistry, The Ohio State University PUBLICATIONS 1． Zhou, X., Smith, A.M., and Failla, M.L. Estrogen Status Alters Tissue Distribution of Oral Dose of 75Se-Selenite and Liver mRNA Levels of SelP and GPx. FASEB J 2007; 21 (5): A717 (Abstract). 2． Zhou, X., Huang, C., Hong, J.,Yao, S., and Zhang, J. A Nested case-control Study on Riboflavin Levels in Blood and Urine and the Risk of Lung Cancer. Journal of Hygiene Research 2003; 32 (6):597-598, 601. viii 3． Mao, S., Li, J., Zhou, X., Yuan, H., and Yang Z. Enternal Nutrition Support for the Postoperative Patients with Larynx Tumor. Chinese Journal of Clinical Nutrition 2002; 10 (2): 93-95. 4． Zhang, J., Zhou, X., Huang, C., Yao, S., Chang, S., Qiao, Y., and Taylor, P. Reproducibility and Validity of a Food Frequency Questionnaire among Male Miners. Modern Preventive Medicine 1999; 26 (2): 198-199, 226. 5． Zhou, X., Zhang. J., Huang. C., Yao. S., Taylor, P., and Qiao, Y.. A Case-Control Study of Vitamins and Lung Cancer Risk. Acta Nutrimenta Sinica 1999; 21 (4): 470-473. 6． Zhou, X., Huang. C., Yu. Q., and Lin. Y. The Effects of Malva Crispa Powder on Immune Function in Normal Mice. Modern Preventive Medicine 1998; 25 (3): 311-313. FIELDS OF STUDY Major Field: The Ohio State University Nutrition Program ix TABLE OF CONTENTS Page Abstract…………………………………………………………………………………....ii Dedication………………………………………………………………………………....v Acknowledgments.. ..…………………………………………………………………….vi Vita……………………………………………………………………………………...viii Table of contents………………………………………………………………………….x List of tables…………………………………………………………………………….xiii List of figures……………………………………………………………………………xiv Chapters: 1 Introduction……………………………………………………………………….…1 2 Literature review…………………………………………………………………......8 2.1 General information of selenium…...……………………………………………8 2.2 Selenoproteins……………………………………………………………………9 2.2.1 Brief introduction of known selenoproteins…………………………….9 2.2.2 Glutathione peroxidase………………………………………………...12 2.2.3 Selenoprotein P………………………………………………………...19 2.3 Selenium metabolism…………………………………………………………...32 2.3.1 Absorption……………………………………………………………...33 2.3.2 Transport……………………………………………………………….37 2.3.3 Tissue distribution……………………………………………………...38 2.3.4 Metabolic pathways……………………………………………………41 2.3.5 Selenium incorporation into selenoproteins……………………………44 2.3.6 Excretion……………………………………………………………….46 2.3.7 Selenium metabolism models………………………………………….52 2.4 Requirements of selenium………………………………………………………59 2.5 Selenium deficiency…………………………………………………………….62 2.5.1 Keshan disease…………………………………………………………62 2.5.2 Kaschin-Beck disease………………………………………………….65 2.5.3 Selenium deficiency in New Zealand and Finland…………………….65 2.6 Selenium toxicity……………………………………………………………….66 x 2.7 Selenium and hormone-related cancers………………………………………...68 2.7.1 Selenium and breast cancer…………………………………………….69 2.7.2 Selenium and prostate cancer……………………………………….….73 2.8 Estrogen receptors in estrogen action…………………………………………..80 2.8.1 Estrogens……………………………………………………………….80 2.8.2 Estrogen receptor………………………………………………………82
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