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Le Michelle 2017December Ph INVESTIGATING THE GENERATION OF BIOPHOTONS INDUCED BY LOW-DOSE BETA-IRRADIATION AND THEIR ROLE IN THE RADIATION-INDUCED BYSTANDER EFFECT INVESTIGATING THE GENERATION OF BIOPHOTONS INDUCED BY LOW-DOSE BETA-IRRADIATION AND THEIR ROLE IN THE RADIATION-INDUCED BYSTANDER EFFECT By MICHELLE LE, B.MRSc. A Thesis Submitted to the School of Graduate Studies in Partial Fulfilment of the Requirements for the Degree Doctor of Philosophy McMaster University © Copyright by Michelle Le, 2017 DOCTOR OF PHILOSOPHY (2017) McMaster University Radiation Sciences (Radiation Biology) Hamilton, Ontario TITLE: Investigating the Generation of Biophotons Induced by Low-Dose Beta- Irradiation and their Role in the Radiation-Induced Bystander Effect AUTHOR: Michelle Le, B.MRSc. (McMaster University) CO-SUPERVISORS: Dr. Fiona McNeill, Dr. Carmel Mothersill NUMBER OF PAGES: xv, 191 i Abstract The communication of information between irradiated and non-irradiated by- stander cell populations and the subsequent expression of radiation-like responses in the non-irradiated population, formally referred to as the radiation-induced by- stander effect, is a very well established phenomenon in the study of radiobiology. Intercellular communication of bystander signals is known to occur via the exchange of soluble factors through biological fluids and via the transfer of molecules between adjacent cells via gap-junctions. Both of these communication methods require some degree of physical contact between biological entities. However, observations made in the literature demonstrating the induction of radiation effects in optically-coupled, yet chemically-separated organisms raises the hypothesis that alternative radiation bystander communication mechanisms may exist that have not yet been explored. Following the detection of significant photon emission from human keratinocyte cells exposed to ionizing beta (β)-radiation by Ahmad in 2013, the involvement of an electromagnetic bystander signal was proposed. While not yet established in the field of radiobiology, intercellular communication via electromagnetic signalling is widely studied in the field of biophotonics. The emission of electromagnetic radiation from biological material, called biophoton emission, and the subsequent communication of effects using those signals has been characterized both spontaneously and as a result of perturbation by various stressors. This thesis therefore aimed to investigate intercellular communication via electromagnetic signalling stimulated by low-dose ionizing radiation to identify a possible convergence between the fields of biophoton communication and radiation-induced bystander effects. The characterization of biophoton emission from human cell cultures was accom- plished using a single photon counting photomultiplier tube. The results revealed that biophoton emission is exacerbated by external stimulation (β-radiation), it possesses a dependence upon the activity of radiation delivered, the density of the irradiated cell culture, and cell viability. These results suggest that biophoton emission is governed by physical transitions between excited and ground states and may further be modulated by metabolic processes. An effect of β-radiation-induced biophoton emission upon non-irradiated bystander cells was identified and manifested as a reduction in cell survival. The modulatory iii effects observed following the application of photomodulating agents to the bystander cultures support ultraviolet electromagnetic radiation as a responsible factor in the communication of bystander signals. Observation of photon emission across the entire ultraviolet, visible and infrared spectra lead to the suggestion that ultraviolet wavelengths are only a portion of the signal responsible for eliciting bystander responses and that coherent interaction of multiple wavelengths is probable in the intercellular exchange of information. The possibility of a link between biophoton bystander signalling and soluble- factor mediated bystander effects was investigated next by isolating exosomes from biophoton-exposed bystander cultures. Positive bystander responses were exhibited by secondary reporter cells incubated with the exosomes isolated from the biophoton- exposed bystander cultures, thereby suggesting that biophoton signalling is a possible form of biological redundancy where it acts as an intermediary to trigger soluble factor release and further reinforce intercellular communication. Finally, the effect of β-radiation-induced biophoton signals upon mitochondrial activity was assessed and revealed the capacity for biophotons to downregulate Complex I and ATP synthase activity. The demonstrated effect of biophotons upon mitochondria elucidates a candidate mechanism worthy of further exploration to determine how biophotons may trigger responses in bystander cells. Overall, this thesis elucidates an additional mechanism for intercellular communi- cation between biological systems perturbed by low doses of ionizing radiation, in the form of an electromagnetic signal. This work contributes to the current perspective on biophoton bystander signalling as a potential source of biological redundancy, facilitat- ing a means of intercellular communication when optical coupling but not chemical contact is available in a given system. iv Dedication Mom and Dad, I dedicate this thesis to you. The hardships you endured during your journey to Canada, the example of hard work you have always demonstrated, and the immense support you’ve given me are the reasons for any success I have been fortunate to experience. I couldn’t have made it here without you. v Acknowledgements This thesis would not have been possible without all of the people who were there to provide guidance, encouragement, and constant support over the past years. Firstly, I would like to express immense gratitude to my supervisors, Dr. Carmel Mothersill and Dr. Fiona McNeill. Carmel, thank you for your guidance, support and for providing a safe environment within which to learn and grow. Further, your dedication to your work absolutely astounds me and I hope that one day I will find a career that I enjoy as much as it is clear that you love and genuinely enjoy yours. Fiona, thank you for taking a chance on me as an undergraduate student trying to find her path. The research opportunity you provided me sparked an interest for scientific inquiry that I otherwise would not have had the opportunity to explore. I have learned so much as a result of your mentoring and cannot express how much I appreciate the support you have given me throughout my undergraduate and graduate career. I would also like to extend gratitude to my committee members, Dr. Colin Seymour and Dr. Andrew Rainbow. Your suggestions for experimental design and critical feedback for work conducted have been integral in shaping the investigations in this thesis. Without your direction, I do not believe we would have considered many of the aspects that we had. Sincerest thank you is due to Dr. Brandi Lee MacDonald for granting me the opportunity to learn and be a part of your PhD thesis as an undergraduate student. To Dr. Syed Bilal Ahmad, thank you for passing on your detector to me & educating me regarding its operation. Dr. Andrea Armstrong (McMaster Nuclear Reactor), thank you for kindly allowing me to use your lab space while also producing radioisotopes for our project. Glenn McClung (McMaster Health Physics Department), you were integral in aiding during the process of seeking approval for our tritium radioactivity permit. Thank you to Eric Johnston for fixing the PMT detector and helping with optimization of the settings for its use. You were also always happy to help me change the CO2 cylinders in our lab and for that I am greatly appreciative. Thank you to Dr. Marta Princz (Biointerfaces Institute) for your ongoing help in the Biointerfaces lab, to Zhilin Peng (CANS Facility) for the taking time out of your schedule to help with the acquisition of SEM micrographs free of charge, to Scott McMaster (McMaster Accelerator Labs) for your help machining holders for our open Yttrium-90 source, to Dr. Kevin Diamond (Juravinski Cancer Centre) for allowing us to borrow and subsequently keep your spectrometer for far too long without any complaints regarding its return, to Ramya Kumareswaran and Dr. Robert Bristow (University Health Network, University of Toronto) for welcoming me into your lab without any reservations and teaching me how to perform western blots, and of course to Alice Pidruczny (McMaster Nuclear Reactor) - thank you for meeting me every week outside of the high level lab to fill our liquid nitrogen tank. I had such anxiety over our cells dying if a week was missed but you were always reliably there to ensure that wasn’t the case - even over the Winter break! Thank you to these individuals and to those I may have forgotten to mention here, without whom this project could not have been possible. I appreciate the generosity you have shown me with your time, your patience and your genuine kindness. vi I would like to extend a special thank you to Dave Tucker (McMaster Health Physics Department). Taking your Operational Health Physics course has inspired the pursuit of a career in radiation protection. I am deeply grateful for your belief in me and for providing me with the opportunity to explore this career interest. Thank you to all of my labmates, both former and present. Christine Hanu and Cristian Fernandez- Palomo, thank you for welcoming me so warmly into the lab and for being a
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