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Speciation, Metabolism, Toxicity, and Protein-Binding of Different Arsenic Species in Human Cells" (2014)

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Speciation, Metabolism, Toxicity, and Protein-Binding of Different Arsenic Species in Human Cells Florida International University FIU Digital Commons FIU Electronic Theses and Dissertations University Graduate School 3-24-2014 Speciation, Metabolism, Toxicity, and Protein- binding of Different Arsenic Species in Human Cells Szabina A. Stice Florida International University, [email protected] DOI: 10.25148/etd.FI14040844 Follow this and additional works at: https://digitalcommons.fiu.edu/etd Part of the Analytical Chemistry Commons, Medicinal-Pharmaceutical Chemistry Commons, and the Toxicology Commons Recommended Citation Stice, Szabina A., "Speciation, Metabolism, Toxicity, and Protein-binding of Different Arsenic Species in Human Cells" (2014). FIU Electronic Theses and Dissertations. 1203. https://digitalcommons.fiu.edu/etd/1203 This work is brought to you for free and open access by the University Graduate School at FIU Digital Commons. It has been accepted for inclusion in FIU Electronic Theses and Dissertations by an authorized administrator of FIU Digital Commons. For more information, please contact [email protected]. FLORIDA INTERNATIONAL UNIVERSITY Miami, Florida SPECIATION, METABOLISM, TOXICITY, AND PROTEIN-BINDING OF DIFFERENT ARSENIC SPECIES IN HUMAN CELLS A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY in CHEMISTRY by Szabina Stice 2014 To: Dean Kenneth G. Furton College of Arts and Sciences This dissertation, written by Szabina Stice, and entitled Speciation, Metabolism, Toxicity, and Protein-binding of Different Arsenic Species in Human Cells, having been approved in respect to style and intellectual content, is referred to you for judgment. We have read this dissertation and recommend that it be approved. _______________________________________ Joong Ho Moon _______________________________________ Yuan Liu _______________________________________ Barry Rosen _______________________________________ Lawrence Boise _______________________________________ Yong Cai, Major Professor Date of Defense: March 24, 2014 The dissertation of Szabina Stice is approved. _______________________________________ Dean Kenneth G. Furton College of Arts and Sciences _______________________________________ Dean Lakshmi N. Reddi University Graduate School Florida International University, 2014 ii ACKNOWLEDGMENTS I would like to thank the Florida International University Minority Biomedical Research Support Research Initiative for Scientific Enhancement (FIU MBRS RISE) program, Dr Charles Bigger, Dr Robert Lickliter, and the MBRS staff for their support. I would like to thank my advisor, Dr Yong Cai for his guidance, continuous support, and patience throughout my PhD studies. I am very grateful for all the scientific discussions and guidance I have received from Guangliang Liu, PhD. I would also like to thank him for the countless hours he patiently helped me to figure out and fix the problems I had with the analytical instrumentation. I would like to thank Shannon Matulis, PhD for all her help with the cancer cells and Dr Boise, Dr Liu, Dr Moon, and Dr Rosen for their help, guidance, and participation in my committee. I would also like to thank my family and all the other people who helped and supported me at Florida International University throughout my studies including but not limited to Dr Lichter, Dr McCord, Dr O’Shea, Dr Kavallieratos, and Dr Mebel. A part of chapter 3 was accepted for publication in the journal of Chemical Research in Toxicology. Adapted with permission from Yehiayan, L., Stice, S., Liu, G., Matulis, S., Boise, L., & Cai, Y. (2014). Dimethylarsinothioyl glutathione as a metabolite in human multiple myeloma cell lines upon exposure to Darinaparsin. Chemical Research in Toxicology. Copyright (2014) American Chemical Society. iii ABSTRACT OF THE DISSERTATION SPECIATION, METABOLISM, TOXICITY, AND PROTEIN-BINDING OF DIFFERENT ARSENIC SPECIES IN HUMAN CELLS by Szabina Stice Florida International University, 2014 Miami, Florida Professor Yong Cai, Major Professor Despite of its known toxicity and potential to cause cancer, arsenic has been proven to be a very important tool for the treatment of various refractory neoplasms. One of the promising arsenic-containing chemotherapeutic agents in clinical trials is Darinaparsin (dimethylarsinous glutathione, DMAIII(GS)). In order to understand its toxicity and therapeutic efficacy, the metabolism of Darinaparsin in human cancer cells was evaluated. With the aim of detecting all potential intermediates and final products of the biotransformation of Darinaparsin and other arsenicals, an analytical method employing high performance liquid chromatography inductively coupled mass spectrometry (HPLC- ICP-MS) was developed. This method was shown to be capable of separating and detecting fourteen human arsenic metabolites in one chromatographic run. The developed analytical technique was used to evaluate the metabolism of Darinaparsin in human cancer cells. The major metabolites of Darinaparsin were identified as dimethylarsinic acid (DMAV), DMAIII(GS), and dimethylarsinothioyl glutathione (DMMTAV(GS)). Moreover, the method was employed to study the conditions and mechanisms of formation of thiol-containing arsenic metabolites from DMAIII(GS) and DMAV as the iv mechanisms of formation of these important As species were unknown. The arsenic sulfur compounds studied included but were not limited to the newly discovered human arsenic metabolite DMMTAV(GS) and the unusually highly toxic dimethylmonothioarsinic acid (DMMTAV). It was found that these species may form from hydrogen sulfide produced in enzymatic reactions or by utilizing the sulfur present in protein persulfides. Possible pathways of thiolated arsenical formation were proposed and supporting data for their existence provided. In addition to known mechanism of arsenic toxicity such as protein-binding and reactive oxygen formation, it was proposed that the utilization of thiols from protein persulfides during the formation of thiolated arsenicals may be an additional mechanism of toxicity. The toxicities of DMAV(GS), DMMTAV, and DMMTAV(GS) were evaluated in cancer cells, and the ability of these cells to take the compounds up were compared. When assessing the toxicity by exposing multiple myeloma cells to arsenicals externally, DMMTAV(GS) was much less toxic than DMAIII(GS) and DMMTAV, probably as a result of its very limited uptake (less than 10% and 16% of DMAIII(GS) and DMMTAV respectively). v TABLE OF CONTENTS CHAPTER PAGE CHAPTER 1 Introduction....................................................................................................1 1.1 Arsenic in the Environment and its Effects on Human Health ............................. 2 1.2 Arsenic in Medicine ............................................................................................ 12 1.3 Arsenic Biotransformation .................................................................................. 23 1.4 Arsenic Speciation in Biological Systems ........................................................... 31 CHAPTER 2 Problem Statement, Objectives, Hypotheses ...............................................36 2.1 Problem Statement .............................................................................................. 37 2.2 Objectives ............................................................................................................ 38 2.3 Hypotheses .......................................................................................................... 39 CHAPTER 3 Dimethylarsinothioyl Glutathione as a Metabolite in Human Multiple Myeloma Cell Lines upon Exposure to Darinaparsin: Formation, Toxicity, and Cellular Uptake ...............................................................................................................41 3.1 Graphical Abstract ............................................................................................... 42 3.2 Abstract ............................................................................................................... 42 3.3 Introduction ......................................................................................................... 43 3.4 Experimental Procedures ..................................................................................... 46 3.5 Results ................................................................................................................. 52 3.6 Discussion ........................................................................................................... 57 CHAPTER 4 Simultaneous Determination of Multiple Human Arsenic Metabolites Employing High Performance Liquid Chromatograph Inductively Coupled Plasma Mass Spectrometer .............................................................................................................63 4.1 Graphical Abstract ............................................................................................... 64 4.2 Abstract ............................................................................................................... 64 4.3 Introduction ......................................................................................................... 65 4.4 Materials and Methods ........................................................................................ 69 4.5 Results and Discussion ........................................................................................ 76 4.6 Conclusions ......................................................................................................... 95
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