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Arabidopsis Response to the Carcinogen Benzo[A]Pyrene

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Arabidopsis Response to the Carcinogen Benzo[A]Pyrene ARABIDOPSIS RESPONSE TO THE CARCINOGEN BENZO[A]PYRENE A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAW AIT IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN TROPICAL PLANT AND SOE. SCIENCES DECEMBER 2008 By Beth Irikura Dissertation Committee: Robert Pauli, Chairperson Henrik Albert Paul Moore Ming-Li Wang Paul Patek We certify that we have read this dissertation and that, in our opinion, it is satisfactory in scope and quality as a dissertation for the degree of Doctor of Philosophy in Tropical Plant and Soil Sciences. DISSERTATION COMMITTEE Chairperson 11 ©Copyright by Beth Irikxira 2008 All Rights Reserved 111 ACKNOWLEDGEMENTS I am fortunate to have been able to design a project that has held my interest throughout. Funding was provided in part by ARCS Foundation awards and a U.S. Dept, of Education GAANN Fellowship in Interdisciplinary Biotechnology. I’d like to acknowledge the people and situations that made this research possible. First, I thank my father for demonstrating a profound love of science, while encouraging his children to explore all other conceivable options. My mother’s death by lung cancer at the age of 54 interrupted my college education, too late to stop me from getting a BA in English literature, but so early that it forced me to reevaluate priorities. My mother also pioneered in our family, showing that an artist could teach science. The last photo of my mother is from late 1983. She’s dressed up as a chicken, and she’s laughing. I like to think she was trying to signal the connection between avian sarcoma virus and cancer, which provided the first molecular understanding of cancer processes. At the time, that connection was just beginning to be deciphered, and public understanding was at the level of thinking maybe you shouldn’t eat too much chicken. It’s hard to explain how I came to work with BaP, a chemical that very likely contributed to my mother’s death. My first project measured BaP interactions with monoclonal antibodies that had been produced by inducing cancers in mice. Yet without that initial work, it’s unlikely that I would have proposed this project. The ensuing years allowed me to develop as a scientist, and more importantly allowed the field to make major progress that I could later use. The situations and people that have impeded my progress (data not shown) have left some lasting scars, but the delay has meant that many exciting advances have been made in the meantime, which give my data a richer and more meaningful context. Without time served, this dissertation would be (even) more like an interpretive dance. Heartfelt thanks to my current advisor and committee members for their participation, insight, and support. Research is only possible through the sacrifices of people wiser and more patient than us. It is impossible and possibly impolitic to thank everyone who has helped, encouraged, or inspired me, but I am enormously grateful to all the people I’ve had the pleasure to work for and with. You know who you are; please accept my thanks. I thank my family for being beautiful, patient and there. To Kawai, Dasmin, Jonah, Joe, Kaimanu, Chase, Pele, Marley, Azzie and Ka‘eo: I’m sorry for working so much, I love you, go to college. Finally, this is for Aike, who was always there. IV ABSTRACT This project investigates the effects of the carcinogenic environmental pollutant benzo[a]pyrene (BaP) on the model plant, Arabidopsis thaliana ecotype Columbia. Previous research has demonstrated phytodegradation of BaP, in the presence and absence of microorganisms. BaP and its metabolites have been detected in plant tissues, but the parent compound is only found in parts-per-billion quantities in most plants.' Increases in plant biomass and lifespan have been observed after growth in BaP, raising questions about how plants are able to benefit from a compound that is detrimental to most other eukaryotes. Since plants share many of the same molecules used by animals in response to BaP (e.g. cytochrome P450, peroxidases, laccases, glutathione, glycosylases and aminotransferases), it has been assumed that they employ similar mechanisms to degrade BaP. Until now, investigations of these mechanisms were limited by methodological constraints. In this study, we applied genetic and genomic tools to determine specific gene expression responses to BaP in Arabidopsis. Particular attention was paid to the mechanisms by which BaP tolerance was achieved in the plant. Much research has shown functional equivalence between homologous genes in plants and animals, hence the results of this study may have applications in biomedical research on molecular mechanisms of BaP effects in mammals. TABLE OF CONTENTS page Acknowledgements.................................................................................................................. iv Abstract...................................................................................................................................... v Table of Contents..................................................................................................................... vi List of Tables.......................................................................................................................... xii List of Figures........................................................................................................................ xiii List of Abbreviations..............................................................................................................xv Chapter 1. Introduction........................................................................................................ 1 Chapter 2. Background and Literature Review 2.1 Benzo[a]pyrene as a model carcinogen 2.1.1 PAHsandBaP....................................................................................................3 2.1.2 Benzo[a]pyrene metabolism............................................................................. 3 2.1.3 BPDE in cancer...................................................................................................4 2.1.4 BaP quinones, hydroxy-BaP, and oxidative metabolites................................4 2.1.5 BaP as an endocrine dismptor..........................................................................5 2.1.6 BaP alters gene expression in multiple, interacting pathways...................... 6 2.2 Phytoremediation 2.2.1 Plants can remediate BaP..................................................................................7 2.2.2 Routes of exposure.......................................................................................... 10 2.2.3 Selection of plant..............................................................................................12 2.3 Expression Analysis 2.3.1 Microarrays...................................................................................................... 13 vi 2.3.2 Quantitative RT-PCR.......................................................................................14 2.3.3 Expression profiling.........................................................................................15 2.3.4 Bioinformatics.................................................................................................. 16 2.3.5 Gene expression profiling identifies additional genes and pathways 18 2.4 Related plant research 2.4.1 Plant response to PAH and other xenobiotics................................................19 2.4.2 Agrobacterium-indMCQd tamors—a plant cancer model?........................... 21 2.5 Cross-kingdom comparisons................................................................................... 22 Chapter 3. Hypotheses and Objectives 3.1 Hypotheses.................................................................................................................26 3.2 Objectives..................................................................................................................26 Chapter 4. Plant Uptake of BaP and Observable Changes 4.1 Introduction................................................................................................................27 4.2 Methods 4.2.1 Growth conditions and phenotypic measurements........................................ 28 4.2.2 Microscopic evidence of BaP effects............................................................. 30 4.2.3 HPLC to detect reduction of BaP in agar.......................................................30 4.2.4 Comet assay to measure DNA damage after root exposure to BaP..............30 4.3 Results 4.3.1 Phenotypic changes in Arabidopsis following exposure to BaP................ 32 4.3.2 Microscopic evidence of BaP effects............................................................33 4.3.3 HPLC to detect reduction of BaP in planted agar......................................... 34 4.3.4 DNA damage detected by the comet assay....................................................34 vii 4.4 Discussion.................................................................................................................43 Chapter 5. BaP Alters Gene Expression of Plants Grown in BaP for 4 Weeks 5.1 Introduction................................................................................................................ 48 5.2 Methods 5.2.1 Plant growth conditions in agar.....................................................................51 5.2.2 Affymetrix ATHl GeneChip analysis of agar-grown plants....................... 51 5.2.3 qRT-PCR of plants
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