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The Physicochemical Properties and Cellular Toxicity Of THE PHYSICOCHEMICAL PROPERTIES AND CELLULAR TOXICITY OF VARIABLY SYNTHESIZED ZINC OXIDE NANOPARTICLES By Catherine Binns Anders A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biomolecular Sciences Boise State University December 2017 ©2017 Catherine Binns Anders ALL RIGHTS RESERVED BOISE STATE UNIVERSITY GRADUATE COLLEGE DEFENSE COMMITTEE AND FINAL READING APPROVALS of the dissertation submitted by Catherine Binns Anders Dissertation Title: The Physicochemical Properties and Cellular Toxicity of Variably Synthesized Zinc Oxide Nanoparticles Date of Final Oral Examination: 08 December 2017 The following individuals read and discussed the dissertation submitted by student Catherine Binns Anders, and they evaluated her presentation and response to questions during the oral examination. They found the student passed the oral examination. Denise G. Wingett, Ph.D. Chair, Supervisory Committee Daniel Fologea, Ph.D. Member, Supervisory Committee Matthew L. Ferguson, Ph.D. Member, Supervisory Committee Dmitri Tenne, Ph.D. Member, Supervisory Committee Sam Lohse, Ph.D. External Examiner The final reading approval of the dissertation was granted by Denise G. Wingett, Ph.D., Chair, Supervisory Committee. The dissertation was approved by the Graduate College. DEDICATION I dedicate this in memory of Dr. Alex Punnoose. You were an incredible mentor, a gifted scientist, and an uncommonly kind and genuine person. The world is a better place because of you. vi ACKNOWLEGEMENTS This endeavor would never have been possible without the support of a multitude of people. First, I would like to thank Dr. Denise Wingett for her unending support and for being the best mentor a student could ever ask for. Many thanks to my committee members, Dr. Daniel Fologea, Dr. Matt Ferguson and Dr. Dmitri Tenne, for their support and assistance. A special thanks to Josh Eixenberger and Jordan Chess for brainstorming and troubleshooting sessions, help with countless experiments, and hours of laughter. To John Rasmussen, Mahdu Kongara and Rebecca Hermann for all your help and answers to my never-ending stream of questions. Finally, I am forever grateful for the unconditional love and support of my family and friends. I wish I could thank you all personally but there will never be enough words. Know that I love you all deeply. Duane, you are my husband, father of my children, best friend, and my soul mate. You make my life work. Helen, your faith in me has often been my strength; thank you for reminding me daily of God’s presence in my life. Susannah, you truly are the sunshine and music in my life. Thank you for your infectious smile and joyful spirit. Clayton, you remind me that perseverance is worth it. Thank you for your goofiness, utter nonsense, and for believing in me. Brent, you will always be my doodle and quiet science guy. Thank you for loving science as much as I do, our long walks and thoughtful conversations. Beth, you are my rock – I love you sis! Finally, to Beth Gee and Cheri Lamb, I really don’t know what I would have done without either of you. Thanks for the late-night conversations, endless laughs and unwavering friendship. v ABSTRACT Nanotechnology has grown exponentially since its inception in the early 1970’s. Since then, bionanotechnological devices and treatment options have significantly improved disease treatments and patient outcomes; however, this rapid growth in consumer related products has also prompted concern. Zinc oxide nanoparticles (nZnO), known for their inherent toxicity and prevalent global use in consumer products and medical applications, have received much of this attention. Significant research efforts have focused on both toxicity remediation through material property modification and the exploitation of these same factors to create potential cancer therapeutics. There is general agreement that the physicochemical properties of nZnO strongly contribute to NP-induced toxicity; however, inconsistencies in the material property characterization methods employed, and an understanding of how those properties influence cytotoxicity in mammalian cells has led to discrepancies in the literature. Additionally, more research is needed to connect the material properties of nZnO to downstream cellular responses. Here, a panel of variably synthesized nZnO was utilized to thoroughly investigate the material properties of the particles as they relate to cytotoxicity, oxidative stress, and transcriptome changes in different mammalian cell types. The goals of this study are three-fold: i) reduce NP agglomeration and sedimentation tendencies within complex media and achieve dispersion stability, ii) define which material property interactions have the greatest potential to affect cellular toxicity, and to iii) examine the preferential toxicity of nZnO towards Jurkat leukemic cells through genetic expression studies. vi Chapter 2 highlights the importance of dispersion stability and the effect of fetal bovine serum (FBS) proteins on the dispersion stability, dosimetry and NP-induced cytotoxicity of nZnO in suspension and adherent in vitro cell culture models. The presence of surface adsorbed proteins from the FBS on the nZnO decreased agglomeration and sedimentation potential. Furthermore, FBS-stabilized nZnO dispersions resulted in toxicity increases in suspension cells when compared to unstable dispersions; however, toxicity was decreased in adherent cell models with stable dispersions. These observations indicate that improved dispersion stability leads to increased NP bioavailability for suspension cells and reduced NP sedimentation onto adherent cell layers resulting in more accurate in vitro toxicity assessments. In Chapter 3, we utilized an expanded panel of nZnO synthesized through wet chemical and high temperature methods, followed by thorough characterization to examine the importance of material property changes in NP-induced toxicity. We found our diverse set of nZnO displayed significant differences in surface reactivity, dissolution potential and cytotoxicity towards cancerous and primary T cells. Additionally, principal component analysis (PCA) suggested that the synthesis procedure conferred unique material properties, and can be a determinant of cellular cytotoxicity. Furthermore, we showed that attributing NP-induced toxicity to one specific material property is shortsighted and that complex interactions between these properties needs to be considered. Finally, Chapter 4 introduces future work dedicated to investigating transcriptome changes in cancerous and primary T cells exposed to nZnO. Both cell types demonstrated significant up- and down-regulation of genes in a dose-dependent manner. Many significant differentially expressed genes (SDEGs) corresponded to proteins involved in vii the sequestration and transport of ionic zinc confirming the importance of nZnO in the cytotoxic response. Additional analysis will focus on the importance of specific SDEGs involved in the regulation of oxidative stress pathways, cellular metabolism, inflammation, T cell activation, and protein misfolding in the NP-induced toxicity mechanism. viii TABLE OF CONTENTS DEDICATION ................................................................................................................... vi ACKNOWLEGEMENTS ....................................................................................................v ABSTRACT ....................................................................................................................... vi LIST OF TABLES .............................................................................................................xv LIST OF FIGURES ......................................................................................................... xvi LIST OF ABBREVIATIONS ........................................................................................ xxvi CHAPTER 1 INTRODUCTION ...................................................................................1 Zinc Oxide Nanoparticles - Cancer Therapeutic or Environmental Health Crisis? .1 nZnO Material Synthesis .........................................................................................2 Electronic Structure and Surface Reactivity ............................................................5 Intrinsic Surface Defects and Photocatalytic Activity .................................5 Zeta Potential ...............................................................................................8 Agglomeration Behavior ........................................................................................10 Colloidal Stability ......................................................................................10 Strategies to Achieve Dispersion Stability ................................................12 Dissolution Potential ..............................................................................................14 Inherent Toxicity of nZnO .....................................................................................16 ix Surface Property Contributions to nZnO Toxicity and Oxidative Stress ..16 Dissolution Contributions to nZnO Toxicity and Oxidative Stress ...........17 Cellular Regulation of and Response to Zinc and nZnO .......................................20 Maintaining Zinc Homeostasis ..................................................................20 Metallothioneins and Zinc Transporters ....................................................21
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