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Effects of Tumor Necrosis Factor-Alpha on Dorsal Vagal

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Effects of Tumor Necrosis Factor-Alpha on Dorsal Vagal EFFECTS OF TUMOR NECROSIS FACTOR-ALPHA ON DORSAL VAGAL COMPLEX NEURONS THAT EXERT REFLEX CONTROL OF THE GASTROINTESTINAL TRACT DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Gregory S. Emch, B. S. ***** The Ohio State University 2002 Dissertation Committee: Approved by: Richard C. Rogers, Advisor __________ Georgia A. Bishop Advisor Susan P. Travers Neuroscience ABSTRACT The results of the experiments presented in this thesis have shown that injection of tumor necrosis factor-alpha (TNF) into the dorsal vagal complex [DVC; made up of the area postrema (AP), the sensory nucleus of the solitary tract (NST), and the dorsal motor nucleus of the vagus (DMN)] has mixed results on neuronal activity in this medullary brainstem area. In the NST, microinjection of TNF causes a significant and dose-dependent increase in neuronal firing rate (FR) as compared to injection of saline controls. Subsequently, some NST neurons exhibit a potentiated response to afferent stimulation following pre-exposure of the neurons to TNF. Conversely, microinjection of TNF significantly inhibits the FR of most neurons in the DMN. Immunohistochemical studies show that the protein product of the proto-oncogene c-Fos (a marker of neuronal activation) is increased in response to systemic administration of lipopolysaccharide (LPS; bacterial cell coat component that induces endogenous production of TNF) in the DVC. Additionally, protein expression is independent of the integrity of the vagus nerve(s). That is, surgical section of the vagi does not inhibit the increase in number of c-Fos labeled neurons. Direct injection of TNF into the ii NST causes a significant elevation of Fos-labeled neurons, and protein expression is dependent on glutamate neurotransmission since glutamate receptor antagonists abolish any significant increase in Fos-positive neurons evoked by injection of TNF alone. Therefore, it was concluded that tumor necrosis factor-alpha causes gastrointestinal stasis by removing cholinergic excitation to the stomach. TNF alters vago-vagal reflexes by acting directly on neurons at the level of the dorsal vagal complex in the medullary brainstem. iii ACKNOWLEDGMENTS I would like to express my gratitude to Dr. Richard Rogers, my advisor of more than 4 years. He was interested in my progress on a daily basis, both in the lab and in my classes. Rick gave me excellent training in surgical techniques as well as in writing techniques. He also allowed me to work at my own pace and was very excited about my data. I am forever thankful to him for his excellent mentoring. I would also like to thank Dr. Gerlinda Hermann, my other mentor in the laboratory. Gerlinda was also very excited about my day-to-day work and was also an excellent teacher. Gerlinda was the best editor a student could ask for when submitting manuscripts for publication. Gerlinda was also a very good friend and was always there to give advice on any problem, whether it was academic or personal. Thank you to the other members of my dissertation committee, Dr. Georgia Bishop and Dr. Susan Travers. I appreciate your time spent in reviewing my dissertation and for administering my oral defense. Also, thanks to Georgia for serving as my official advisor for the final months of my graduate school experience. iv VITA Born: 11-24-74, Youngstown, OH 1997 – Present Ohio State University College of Medicine, Columbus, OH Graduate Student 1999 – 2001 Ohio State University Neuroscience Department Pre-doctoral Fellow 1993 – 1996 Youngstown State University Honors Program, Youngstown, OH Biology/Chemistry, BS, Cum Laude PUBLICATIONS Emch, GS, Hermann, GE, Rogers, RC. TNF-a induces c-Fos generation in the nucleus of the solitary tract that is blocked by NBQX and MK-801. Soc for Neurosci Abs. 634.9, 2001. Rogers, RC, Hermann, GE, Emch, GS, Travagli, RA, and Browning, KN. TNF-alpha acts directly on circuit elements in the dorsal vagal complex to control gastric motility. Brain Gut Odyssey Meeting, 2001. Rogers, RC, Emch, GS, and Hermann, GE. Central effects of TNF on dorsal vagal complex neurons. Euro Winter Brain Conference Abs. 86, 2001 Emch, GS, Hermann, GE, and Rogers, RC. Tumor necrosis factor-alpha: Effects on identified neurons of the dorsal vagal complex. Soc Neurosci Abs. 674.14, 1999. Emch, GS, Hermann, GE, and Rogers, RC. TNF activates gastric vago-vagal reflex NST neurons and potentiates their responsiveness to vagal afferent input. AGA Annual Meeting. Abs. 100130, 1999. Emch GS, Hermann, GE, and Rogers, RC. TNF-a inhibits physiologically identified dorsal motor nucleus neurons in vivo. Brain Res, Submitted. v Emch GS, Hermann, GE, and Rogers, RC. TNF-a induced c-Fos generation in the nucleus of the solitary tract is blocked by NBQX and MK-801. Am J Physiol 281: R1394-R1400, 2001. Hermann, GE, Emch, GS, Tovar, CA, and Rogers, RC. c-Fos generation in the dorsal vagal complex following systemic endotoxin is not dependent on the vagus nerve. Am J Physiol 280: R289-R299, 2001. Emch, GS, Hermann, GE, and Rogers, RC. TNF-a activates solitary nucleus neurons responsive to gastric distention. Am J Physiol 279: G582-G586, 2000. FIELDS OF STUDY Major Field: Neuroscience - Neurophysiology - Immunocytochemistry - Pharmacology vi TABLE OF CONTENTS Page: Abstract……………………………………………………………………………..ii Acknowledgments…………………………………………………………………iv Vita………………………………………………………………………………….v List of Figures……………………………………………………………………..xii Chapter 1: Introduction…………………………………………………………..1 Illness Response…………………………………………………………………..2 Tumor necrosis factor-alpha………………………………………………………3 Vago-vagal reflex control of digestion……………………………………………5 Afferent limb………………………………………………………………..5 NST………………………………………………………………………….6 DMN…………………………………………………………………………8 Nucleus ambiguous………………………………………………………..9 Chemical specificity of afferent connections to the DVC………………9 Examples of vago-vagal reflexes…………………………………………9 Modulation by central pathways………………………………………….10 Modulation by peripheral factors…………………………………………11 vii TNF and the DVC………………………………………………………………….13 TNF signal transduction…………………………………………………………..14 Cellular production of TNF………………………………………………………..16 TNF effects on glia………………………………………………………………...17 TNF effects on neurons…………………………………………………………...18 Central vs. peripheral activation by cytokines…………………………………..19 Hypothesis………………………………………………………………………….20 CHAPTER 2: TNF activates solitary nucleus neurons responsive to gastric distention……………………………………………………………………………21 Introduction…………………………………………………………………………21 Methods…………………………………………………………………………….24 Chemicals………………………………………………………………….24 Electrode construction…………………………………………………….24 Data collection……………………………………………………………..25 Gastric stimulation…………………………………………………………25 Surgical preparations……………………………………………………...26 Experimental design……………………………………………………….26 Statistical analysis…………………………………………………………28 Results………………………………………………………………………………28 Dose dependency of NST firing on TNF………………………………...29 Potentiation of NST response to gastric stimulation…………………...31 Discussion………………………………………………………………………….31 viii CHAPTER 3: TNF inhibits physiologically identified dorsal motor nucleus neurons in vivo…………………………………………………………………….36 Introduction……………………………………………………………… Methods…………………………………………………………………………….38 Chemicals………………………………………………………………….38 Pipette construction……………………………………………………….38 Data Collection…………………………………………………………….39 Gastric stimulation…………………………………………………………39 Surgical Preparations……………………………………………………..40 Experimental Design………………………………………………………40 Statistical Analysis…………………………………………………………42 Results………………………………………………………………………………42 Discussion………………………………………………………………………….45 CHAPTER 4: c-Fos generation in the dorsal vagal complex after systemic endotoxin is not dependent on the vagus nerve………………………………..47 Introduction…………………………………………………………………………47 Methods…………………………………………………………………………….52 Chemicals…………………………………………………………………..52 Experimental Design………………………………………………………53 Animals……………………………………………………………………..54 Surgical Preparations……………………………………………………..54 ix Histological processing for c-Fos protein………………………………..56 Counting c-Fos nuclei in the dorsal medulla……………………………57 TNF assay………………………………………………………………….57 Analysis…………………………………………………………………….58 Experiment 1: Intact Vagi / Inactin (thiobutabarbitol) anesthesia…….59 Experiment 2: Left Cervical Vagotomy…………………………………..60 Experiment 3: Bilateral Cervical Vagotomy……………………………..60 Plasma TNF levels………………………………………………………...61 Results………………………………………………………………………………61 Experiment 1: c-Fos labeling in the NST, DMN, and Area Postrema in the vagus-intact, Inactin anesthetized rat……………………………………………61 Experiment 2: Effects of LPS on c-Fos labeling in the NST, DMN, and Area Postrema in rats with left cervical vagotomy……………………………………64 Experiment 3: Effects of LPS on c-Fos labeling in the NST, DMN, and Area Postrema in rats with bilateral cervical vagotomy……………………………..67 Plasma TNF levels……………………………………………………………….70 Discussion…………………………………………………………………………72 CHAPTER 5: TNF induced c-Fos generation in the nucleus of the solitary tract is blocked by NBQX and MK-801………………………………………..76 Introduction……………………………………………………………………….76 Methods…………………………………………………………………………..80 Animals……………………………………………………………………80 Chemicals…………………………………………………………………80 x Surgical Preparation……………………………………………………..82 Experimental Design…………………………………………………….83 Histological processing…………………………………………………..84 Counting c-Fos labeled cells…………………………………………….85 Analysis…………………………………………………………………….86 Results………………………………………………………………………………86
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