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Converse-Dissertation-2018 Copyright by Aubrey Koch Converse 2018 The Dissertation Committee for Aubrey Koch Converse Certifies that this is the approved version of the following Dissertation: Functions and signaling mechanisms of the membrane androgen receptor ZIP9 in Atlantic croaker (Micropogonias undulatus) and zebrafish (Danio rerio) ovaries Committee: _____________________________ Peter Thomas, Supervisor _____________________________ Deana Erdner _____________________________ Andrew Esbaugh _____________________________ John Richburg Functions and signaling mechanisms of the membrane androgen receptor ZIP9 in Atlantic croaker (Micropogonias undulatus) and zebrafish (Danio rerio) ovaries by Aubrey Koch Converse Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin December 2018 Dedication I dedicate this work to my father Jeff Koch and daughter Chloe Converse, I love you both with all my heart. Acknowledgements First and foremost, I need to thank my advisor Peter Thomas, who has provided immeasurable support in the completion of this work. My research and writing skills have considerably improved under his guidance. Thank you to my committee, Deana Erdner, Andrew Esbaugh, and John Richburg, for their guidance and feedback on this work over the years. To my lab members, Yefei Pang, Jing Dong, and Md. Saydur Rahman, thank you for your patience in teaching me the protocols and skills that were essential in to research. To my dear friend Susan Lawson, I could not have completed this work without your dedicated care to our wet lab and fish, and I would not have stayed sane without your company and friendship. To past labmates and visitors, Wenxian Tan, Kathryn Ondricek, Joseph Aizen, Hakan Berg, Maria Camilletti, Amanda Fitzgerald, Luca Castelnovo, and Chenan Zhang, thank you all in your support in this undertaking. Thank you Bob Dickey and all of the staff at UTMSI, everyone’s dedication to the institute after Hurricane Harvey allowed for our research to continue. To my family, thank you for your support and patience over the many years, I’m am so sincerely appreciative. And finally, thank you to everyone I have met at UTMSI for truly enriching my life. v Abstract Functions and signaling mechanisms of the membrane androgen receptor ZIP9 in Atlantic croaker (Micropogonias undulatus) and zebrafish (Danio rerio) ovaries Aubrey Koch Converse, Ph.D. The University of Texas at Austin, 2018 Supervisor: Peter Thomas The overall goal of this research was to further characterize and verify the role of ZIP9 in mediating androgen-induced apoptosis of teleost granulosa/theca (G/T) cell co-culture. In addition, a global ZIP9 knockout zebrafish model was used to infer other roles of the receptor in the ovary, in vivo. While ZIP9 was first identified and found to mediate apoptosis of croaker G/T cells, little was known on the signaling mechanism mediated by the receptor. Therefore, stimulatory G protein alpha subunit-mediated signaling, MAP kinase (MAPK) activity, and the role of extracellular zinc were investigated in ZIP9- mediated apoptosis of croaker G/T cells. Additionally, the role of ZIP9 in mediation of testosterone-induced anti-apoptotic response observed in croaker G/T cells from fish outside of the reproductive peak was examined. To determine if ZIP9 mediates androgen- induced apoptosis in G/T cells of other teleosts, a zebrafish primary G/T culture system was used to examine androgen-mediated events. Finally, a global ZIP9 knockout zebrafish vi strain was developed to examine the effects of global ZIP9 knockout on female reproduction. The ZIP9-mediated apoptotic pathway in croaker G/T cells was found to require stimulatory G protein signaling and MAPK activity. Additionally, extracellular zinc is essential for the induction of ZIP9-mediated apoptosis in this model, and downstream responses to these signaling cascades include increased mRNA expression of pro-apoptotic protein members and caspase 3 activity. Pro- and anti-apoptotic effects of testosterone on croaker G/T cells was confirmed, and both responses were found to be mediated by ZIP9 in an ovarian follicle stage-dependent manner. ZIP9 activation of stimulatory and inhibitory G proteins elicits the pro- and anti-apoptotic responses, respectively. In pooled zebrafish G/T cells, testosterone treatment results in an increased incidence of apoptosis, caspase 3 activity, upregulation of pro-apoptotic protein member mRNA, and a rapid rise in intracellular free zinc. This testosterone-mediated response was attributed to ZIP9 activity, thus, ZIP9 mediates apoptosis through a similar mechanism in zebrafish G/T cells as observed in croaker. Finally, examination of ZIP9 global knockout zebrafish demonstrated that ZIP9 mutation results in reduced fecundity and abnormal egg phenotypes, even though no abnormalities in ovarian morphology were apparent through histological examination. vii Table of Contents List of Tables .......................................................................................................................x List of Figures .................................................................................................................... xi Chapter 1: Introduction .......................................................................................................1 Chapter 2: Membrane androgen receptor ZIP9 induces croaker ovarian cell apoptosis via stimulatory G protein alpha subunit and MAP kinase signaling .............................8 Abstract .......................................................................................................................8 Introduction .................................................................................................................9 Materials and Methods..............................................................................................13 Results .......................................................................................................................18 Discussion .................................................................................................................22 Figures ......................................................................................................................29 Supplemental Data ....................................................................................................39 Chapter 3: The membrane androgen receptor ZIP9-mediates pro- and anti-apoptotic responses in Atlantic croaker ovarian follicle cells by activating Gi and Gs in a follicle stage-dependent manner ..................................................................................42 Abstract .....................................................................................................................42 Introduction ...............................................................................................................43 Materials and Methods..............................................................................................47 Results .......................................................................................................................53 Discussion .................................................................................................................57 Figures ......................................................................................................................64 Supplemental data .....................................................................................................73 viii Chapter 4: Evidence that ZIP9 regulates both G/T cell apoptosis and oocyte activation in the zebrafish ovary ..................................................................................74 Abstract .....................................................................................................................74 Introduction ...............................................................................................................75 Materials and Methods..............................................................................................77 Results .......................................................................................................................85 Discussion .................................................................................................................90 Figures ......................................................................................................................98 Supplemental Data ..................................................................................................108 Chapter 5: Summary and Conclusions ............................................................................110 References ........................................................................................................................113 ix List of Tables Table 2.1: List of antibodies used in Chapter 2. …...…………………………………....39 Table 2.2: Sequence of primers (5’-3’) used for qPCR experiments (Chapter 2). ............39 Table 3.1: Sequence of primers (5’-3’) used for qPCR experiments (Chapter 3). ............73 Table 4.1: Sequence of primers (5’-3’) used for qPCR experiments (Chapter 4). ..........108 Table 4.2: Oligonucleotide sequences used in gRNA generation and stop codon cassette. .......................................................................................................108 Table 4.3: Primers
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