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Inflammatory Regulation of Hypothalamic Neurons In INFLAMMATORY REGULATION OF HYPOTHALAMIC NEURONS < I IN SICKNESS BEHAVIOR by Aaron J. Grossberg A DISSERTATION > Presented to the Neuroscience Graduate Program and the Oregon Health & Science University School of Medicine in partial fulfillment of the requirements for the degree of Doctor of Philosophy April 201 1 School of Medicine Oregon Health & Science University CERTIFICATE OF APPROVa This is to certify that the Ph.D. dissertation of AARON GROSSBERG has been amroved on Anril 29- 20 1 1 Member fnd w,Gary Westbrook, MD - ~ember, usa ah Smith, PhD -- . LI- - Member, ha*, ~m~ - " / Member, &tl%&#arnes, TABLE OF CONTENTS Page CERTIFICATE OF APPROVAL TABLE OF CONTENTS LlST OF FIGURES LlST OF ABBREVIATIONS X ACKNOWLEDGEMENTS xv ABSTRACT xvii Chapter I.Introduction 1. Sickness Behavior Is An Adaptive Response to Disease 1.I. Fever 1.2. Anorexia in Acute Illness 1.3. Cachexia of Chronic Disease 1.4. Therapeutic Approaches to Cachexia 1.5. Defining Cachexia , 2. lnflammation Coordinates the Behavioral Response to Illness 2.1. Sickness Behavior is Associated with lnflammation 2.2. Peripheral lnflammation and Muscle Wasting 2.3. Central lnflammation 3. Hypothalamic Involvement in Cachexia 3.1. The Hypothalamus and Brainstem Respond to lnflammation P '/ I i /& i I f I I I 3.2. The Role of Central Melanocortins in Cachexia 11 1 ~ 1 ~l 3.3. Neuropeptide Y in Cachexia 14 4. Neurohumoral Link 4.1. The Hypothalamus Responds to Circulating Signals of Energy Status 4.2. Transmission of Signals Across the Blood brain Barrier 4.3. The Vagus Communicates Inflammation Into the CNS 5. Interaction of Cytokines with the Central Melanocortin System 5.1. IL-1P Regulates the Central Melanocortin System 5.2. LIF Chronically Suppresses Feeding 6. Sickness-induced lethargy and inactivity 7. Central regulation of arousal 7.1. Anatomy of the.Ascending Arousal System 7.2. VLPO Neurons Promote Sleep 7.3. Regulation of SleepNVake Consolidation and Transitions 7.4 Circadian Regulation of Arousal 7.5. Homeostatic Regulation of Arousal 7.6. Allostatic Regulation of Arousal 8. The Orexin System 42 8.1. Orexin Peptides and Receptors 1 42 8.2. Orexins and Narcolepsy 43 8.3. Neurotransmitters Regulating Orexin Neuron Activity 45 8.4. Orexins Stabilize Wakefulness 45 8.5. Orexins Promote Arousal in Response to Depleted Energy 47 I Status 8.6. Orexins Associate Stress and Arousal 52 8.7. Orexins, Reward, and Addiction 8.8. Orexin Regulation of Feeding and Metabolism 1 8.9. Orexins and Depression 8.10. Functional Dichotomy in Orexin Neurons 8.1 1. Orexins Are Allostatic Regulators of Arousal 9. lnflammation and Arousal 9.1. Sleep 58 9.2. Inflammatory Regulation of the VLPO and Basal Forebrain 59 9.3. Dopaminergic Neurons Exhibit Biphasic Responses to 61 lnflammation 9.4. Cytokines Suppress Serotonin Neuron Activity 62 9.5. Inflammation Dissociates Noradrenergic Tone from Arousal 63 Behavior 9.6. TMN Histaminergic Neurons Are Inhibited by Inflammation, 64 9.7. Effects of Inflammation on the LHA and Orexin Neurons 65 Hypothesis and Specific Aims 67 Chapter 2. Manuscript #I:Arcuate nucleus proopiomelanocortin '68 neurons mediate the acute anorectic actions of leukemia inhibitory factor via gp130 , 1. ABSTRACT 2. INTRODUCTION 3. MATERIALS AND METHODS 4. RESULTS 4.1 Induction of hypothalamic LIF mRNA expression following i.p LPS and i.c.v. IL-lp administration h f 4.2 lntracerebroventricular LIF induces anorexia associated 84 with increased ARC POMC neuron activity I 4.3 LIF-R is expressed by POMC neurons in the ARC 85 4.4 LIF increases a-MSH release from ARC POMC neurons 86 I 4.5 Generation of mice lacking gp130 in POMC-expressing cells 86 4.6 ~omc~re-~~l3d'~~~~~hypothalami do not increase a-MSH 87 release in response to LIF I 4.7 ~omc~re-gp130~~~~~mice display a diminished anorectic response to LIF 5. DISCUSSION Chapter 3. Manuscript #2: inflammation-induced lethargy is mediated by suppression of orexin neuron activity 1. ABSTRACT 2. INTRODUCTION 3. MATERIALS AND METHODS 4. RESULTS 4.1 LPS-induced inhibition of home cage LMA is associated with suppressed dark phase Ox signaling 4.2 Central (i.c.v.) OxA replacement prevents the onset of LPS- induced lethargy 4.3 LPS blocks FAA and Ox neuron activity in food-entrained rats 4.4 Central IL-1P blocks FAA and Ox neuron activity in food- entrained rats 4.5 Ox neurons are not direct targets for inflammatory signaling 4.6 LPS-induced lethargy is not melanocortin dependent IV 4.7 LHA neurotensin (Nts) neurons are activated during LPS- 132 I induced inflammation 5. DISCUSSION Chapter 4. Summary and Conclusions 152 1. LIF suppresses food intake by directly activating ARC 153 POMC neurons 1.1 . The Role of LIF in Cachexia 154 I.2 LIF Regulation of the Central Melanocortin System 156 1.3 The Central Melanocortin System and Locomotor Activity 159 2. Orexin Neurons Mediate Inflammation Induced Lethargy 160 2.1 Perifornical Orexin Neurons Are Inflammation Sensitive 160 2.2 Locomotor Activity and Feeding Are Independently 163 Regulated by lnflammation 2.3 Inflammation, Orexin, and Sleep 164 2.4 Therapeutic Potential of Orexin Agonists 164 3. Summary 168 References 170 -. Appendix 21 8 1 Appendix A: Supplemental Figures Referred to in Main Text 21 9 2. Appendix B: Studies Exploring the Effects of Chronic Central - LIF Administration 3. Appendix C: Studies Investigating the Mechanisms of Tumor- lnduced Cachexia - $ ,, v LIST OF FIGURES Chapter 'I Introduction Figure I LPS induces IL-IP expression in the hypothalamus and brainstem. 10 Figure 2 Induction of c-fos mRNA in hypothalamus and brainstem following intravenous IL-IP administration. 12 Figure 3 MC4-RKO mice are resistant to LPS-induced cachexia and illness 16 behavior. Figure 4 Model for the role of the central melanocorfin system in the 22 production of cachexia during disease. Figure 5 POMC and AgRP neurons in the ARC express IL-IRI. 26 Figure 6 Diagram showing projections of ascending arousal system and 34 > reciprocal inhibitory projections from VLPO. Figure 7 Schematic diagram of flip-flop switch model of sleep-wake regulation. Figure 8 Interactions between orexin neurons and other brain regions implicated in the regulation of arousal. Chapter 2 Arcuate nucleus proopiomelanocortin neurons mediate the acute anorectic actions of leukemia inhibitory factor via gp130 i, Figure 9 Hypothalamic LIF expression in response to LPS and IL-1P. Figure 10 Hypothalamic CNTF and IL-6 expression in response to LPS and IL- lp. Figure 11 Effects of central LIF on food intake in wild type mice. Figure 12 LIF activates POMC neurons in the hypothalamus. Figure 13 LIF does not activate brainstem POMC neurons. Figure 14 Expression of LIF-R in the hypothalamus. Figure 15 LIF stimulates a-MSH release from murine hypothalamic explants. Figure 16 Diagram of PomcCre-gp 136'0X/f10x mouse genetics. Figure 17 Metabolic phenotype of PomcCre-gp136'0X~f10Xmice. Figure 18 LIF-induced pSTAT3 IR in WT and gp136~~~~~~POMC neurons. Figure 19 gp13@0X'10xmice are resistant to both LIF-induced a-MSH 107 release and anorexia. ~ Figure 20 Hypothalamic LIF expression induced by chronic central LIF 108 I administration. Chapter 3 Inflammation-induced lethargy is mediated by suppression of orexin neuron activity Figure 21 LPS -induced inhibition of home cage LMA is associated with 138 reduced vespertine activation of Ox neurons and reduced dark phase accumulation of OxA in the CSF. Figure 22 LPS does not alter Ox mRNA expression. 139 Figure 23 OxA dose-response in aCSF- and LPS-treated rats. 140 Figure 24 Central OxA replacement prevents and reverses LPS- 141 induced lethargy. Figure 25 Continuous central OxA administration ameliorates LPS- 142 induced lethargy throughout the active phase. vii Figure 26 Effects of food entrainment on circadian LMA and i inflammatory response to LPS. I I Figure 27 Central OxA administration restores FAA in FR rats treated with 144 i.p. LPS or i.c. v. IL- IP. Figure 28 Ox neurons are not direct targets for inflammatory signaling. LPS- 146 induced lethargy is not dependent on central IL- I or PG signaling. I '1 Figure 29 Inhibition of prostaglandin synthesis blocks LPS induction of 147 fever but does not affect LMA. I Figure 30 LPS-induced lethargy is not melanocortin-dependent. Figure 31 LPS inhibition of orexin neuron activity is not dependent on central opioid signaling. ~ Figure 32 LPS treatment induces cFos IR in LHA NTS neurons while suppressing vespertine activation of Ox neurons in NTS-cre/GFP mice. Figure 33 Tumor-induced inflammation inhibits home cage LMA and reduces Ox mRNA expression in the medial hypothalamus. Chapter 4 Summary and Conclusions Figure 34 Schematic diagram depicting the hypothesized mechanisms by which hypothalamic inflammation induces sickness- associated anorexia and lethargy. Appendix Figure 35 LIF-R mRNA expression in brainstem and by ARC AgRP viii neurons in rat, Figure 36 qRT-PCR examination of cytokine and neuropeptide mRNA in hypothalamic homogenates from FR v. ad-lib rats after LPS treatment. Figure 37 LIF mRNA expression throughout forebrain I h after LPS administration. Figure 38 ~omc~re-gpl30~~~~~~mice show a normal anorectic response to LPS-induced systemic inflammation. Figure 39 Retrograde tract tracing in rats from DR to LHAIPFA. Figure 40 The effects of twice daily i,c. v, LIF bolus injection on feeding behavior and hypothalamic gene expression in C57BU6J mice. Figure 41 The effects of chronic i.c. v. LIF infusion on feeding behavior, body weight, and hypothalamic gene expression in C57B46J ( and MC4R-KO mice. Figure 42 Intra-3V administration of a LIF-expressing lentivirus failed to induce anorexia, loss of body weight or pSTAT3 IR in the ARC of WT mice. Figure 43 AgRP reverses MCA sarcoma induced anorexia and lean body wasting.
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