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Trpa1) Activity by Cdk5 MODULATION OF TRANSIENT RECEPTOR POTENTIAL CATION CHANNEL, SUBFAMILY A, MEMBER 1 (TRPA1) ACTIVITY BY CDK5 A dissertation submitted to Kent State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Michael A. Sulak December 2011 Dissertation written by Michael A. Sulak B.S., Cleveland State University, 2002 Ph.D., Kent State University, 2011 Approved by _________________, Chair, Doctoral Dissertation Committee Dr. Derek S. Damron _________________, Member, Doctoral Dissertation Committee Dr. Robert V. Dorman _________________, Member, Doctoral Dissertation Committee Dr. Ernest J. Freeman _________________, Member, Doctoral Dissertation Committee Dr. Ian N. Bratz _________________, Graduate Faculty Representative Dr. Bansidhar Datta Accepted by _________________, Director, School of Biomedical Sciences Dr. Robert V. Dorman _________________, Dean, College of Arts and Sciences Dr. John R. D. Stalvey ii TABLE OF CONTENTS LIST OF FIGURES ............................................................................................... iv LIST OF TABLES ............................................................................................... vi DEDICATION ...................................................................................................... vii ACKNOWLEDGEMENTS .................................................................................. viii CHAPTER 1: Introduction .................................................................................. 1 Hypothesis and Project Rationale ................................................................. 24 Specific Aims ................................................................................................ 25 CHAPTER 2: Materials and Methods .............................................................. 26 Experimental Protocols ................................................................................ 35 CHAPTER 3: Results ........................................................................................ 39 CHAPTER 4: Discussion .................................................................................. 57 References ........................................................................................................ 68 iii LIST OF FIGURES Figure 1. TRP superfamily tree. ........................................................................... 8 Figure 2. TRPA1 reactive cysteines. ................................................................. 11 Figure 3. Various TRPA1 agonist structures...................................................... 12 Figure 4. Inflammatory soup cartoon. ................................................................ 14 Figure 5. TRPA1 domain cartoon. ..................................................................... 17 Figure 6. Cdk5/activator structure figure. ........................................................... 18 Figure 7. Serine 448 sequence alignment. ........................................................ 21 Figure 8. DRG Neuron photo. ............................................................................ 22 Figure 9. GFP/RFP transfection photo. ............................................................. 31 2+ Figure 10. Cdk5 inhibition attenuates TRPA1 agonist-induced rise in [Ca ]i in DRG neurons. .............................................................................................. 41 2+ Figure 11. Control trace illustrating TRPA1 agonist-induced rise in [Ca ]i in the absence of inhibition. ................................................................................ 42 Figure 12. Cdk5 inhibition does not attenuate TRPA1 agonist-induced rise in 2+ [Ca ]i in transfected HEK 293 cells, which lack Cdk5 activity...................... 43 Figure 13. Summarized data illustrating TRPA1 response attenuation by Cdk5 inhibition. ............................................................................................. 44 Figure 14. Trace illustrating reversible TRPA1 inhibition by roscovitine. ........... 46 Figure 15. Reversible inhibition summarized data. ............................................ 47 iv Figure 16. Roscovitine dose-dependently inhibits TRPA1 responses. .............. 49 Figure 17. Phosphoserine western blot. ............................................................ 51 Figure 18. Phosphoserine western blot summarized data. ................................ 52 Figure 19. Serine 448 kinase assay. ................................................................. 54 Figure 20. TRPA1 peptide kinase assay inhibitor effects................................... 56 v LIST OF TABLES Table 1. Nocisensors (and other thermosensitive TRPs) ..................................... 5 Table 2. Partial list of TRPA1 agonists. ............................................................. 13 vi DEDICATION For Mom vii ACKNOWLEDGEMENTS I would like to thank my advisor, Dr. Derek Damron, for providing the research environment and tools necessary to complete this dissertation, and for allowing me the freedom to pursue a project of my own genesis. I thank my committee members, Dr. Robert Dorman, Dr. Ernest Freeman and Dr. Ian Bratz, along with Graduate Faculty Representative, Dr. Bansidhar Datta, for playing their essential roles in the dissertation process. I thank my labmates, Bethany Prudner, Ryo Yuge and Hongyu Zhang for friendship and support over the years. A special thanks goes out to Erin Kellams, for preparing many of the DRGs necessary to complete this project. viii CHAPTER 1 Introduction In order to survive and thrive in a hostile environment, organisms require the capacity to detect and respond appropriately when potentially-harmful, tissue- damaging agents are encountered. The task of detecting such noxious mechanical, thermal and chemical stimuli is performed by a specialized class of sensory neurons of the peripheral nervous system (PNS) known as nociceptors (Sherrington, 1906; Burgess & Perl, 1967). When activated by interaction with a potentially damaging agent (such as a hot coffee cup), nociceptors respond by producing an action potential – sending an electrical signal to inform the central nervous system (CNS) that all is not well. The unpleasant sensation which results, pain, provides the perceiver with an extremely potent and compelling behavioral cue for avoidance of interactions detrimental to their health and well- being. Pain‟s importance as a guardian of bodily integrity is perhaps best illustrated by those rare cases where it‟s completely absent – in individuals suffering from neural disorders known as hereditary sensory and autonomic neuropathies (HSANs), which render them unable to sense pain (Axelrod & Gold-von Simson, 2007). An example of one such neuropathy is congenital insensitivity to pain with anhydrosis (CIPA, a.k.a., HSAN IV), a disorder characterized by patients‟ complete lack of small-diameter sensory neurons. As this type of neuron is 1 2 associated with both nociception and innervation of the sweat glands, CIPA‟s hallmark symptoms – the inability to either sense pain or produce sweat (often leading to potentially fatal hyperpyrexia), are easily explained, physiologically. Individuals afflicted with this rare and incurable condition frequently suffer burns, broken bones, self-mutilation and other serious injuries (leading to greatly shortened lifespans), as the „pain alarm‟ warning/informing of tissue damage is permanently off-line (Nagasako, Oaklander, & Dworkin, 2003; Axelrod & Gold- von Simson, 2007). While such disorders underline the value of pain and the perils of painlessness, at the other extreme can be found patients suffering from chronic pain syndromes – in these ailments, too much pain, rather than too little is the problem, as pain persists beyond its beneficial role as an acute warning device, and instead becomes a terrible burden in its own right. This type of chronic pain, in marked contrast to the rare, „pain-free‟ sensory neuropathies, is far from uncommon, but instead afflicts tens of millions of Americans each year and is a leading cause of disability. Also in contrast to hereditary neuropathies, which involve neuronal loss or failure to develop and are therefore incurable, clinical pain syndromes are amenable to therapeutic intervention, offering help and hope to the afflicted, and placing a tangible goal in the sights of biomedical and pharmaceutical researchers seeking to improve the status quo. Relief from unnecessary suffering is the therapeutic goal in treatment of pain, but extant pharmaceuticals (NSAIDs and opioids), for all their positive attributes, still have significant shortcomings, leaving a considerable burden of suffering non-palliated. A promising strategy to help fill this „palliation gap‟ is to 3 scour known pain-related pathways in the hope of identifying novel molecular targets for rationally-designed therapeutics (Patapoutian, Tate, & Woolf, 2009). To this end, advancing our understanding of the mechanisms of nociception at the subcellular, molecular level of detail is required. Just as man-made thermometers and pressure gauges measure temperature and mechanical force, and reactive dyes are capable of detecting oxidizing agents and pH change, there must exist analogous elements within nociceptive neurons possessing the capacity to interact with each nociceptive stimulus and subsequently produce reliable, functional responses – enabling these elements to act as stimulus detectors, or nocisensors. What are these nocisensors – the functional molecular
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