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The Regulation of Food Intake, Body Fat Stores and Energy Balance in The 6. G. <so THE REGULATION OF FOOD INTAKE, BODY F.AT STORES AI{D ENERGY BALANCE IN THE MARSUPIAL SMINTHOPSIS CRASSICAUDATA A Thesis submitted by Perdita Jane lfope For the Degree of Doctor of Philosophy Department of Medicine University of Adelaide January 2000 TABLE OF CONTENTS Thesis Summary. 1 Statement of Originality 9 Dedication 10 Acknowledgments. 11 Publications Arising from This Thesis. 15 Other Publications. .. .. t7 Conference Presentations. ... 18 CHAPTER 1: THE REGULATION OF BODY WEIGHT 20 1.1 Introduction. .... I.2 The 'Set-Point' Theory of Body Weight. 2l 1.2.1 The ooncept of a 'set-point' for body weight 2I 1.2.2 Body weight 'set-points' of obese in<lividuals 23 L2.3 Does a body weight 'set-point' exist in growing m¿mmals? 23 1.2.4 The 'unsettling mythology of set-points'. 25 1.3 The Lipostatic Hypothesis..... 26 1.3.1 Evidence zuppofiing the lipostatic hl,pothesis.. 27 t.4 Nutrient Partitioning, Macronutrient Metabolism, and Diet Composition 32 L.4.1 Substrate oxidation. 32 1.4.2 Metrbolism of maoronutrients. 35 1.5 Leptin, the ob Gene and the Regulation of Body Weight.. ... 38 1.5.1 Rodent studies. 39 1.5.2 The leptin reoeptor.. 43 1.5.3 Interaction of leptin with other neurotransmitters involved in energy balance. 44 1.5.4 Leptin resistance...... 47 1.5.5 Leptin and the neuroendocrine response to starvation........ 48 1.6 The Regulation of Energy Intake. 49 1.6.1 The peripheral control of appetite. .... 50 1.6.2 The central control of appetite. .. 52 I.6.3 Neurotransmitters that may decrease food intake. .. 56 1.6.4 Neurotransmitters that may increase food intake.... 69 1.6.5 Gonadal steroids and the regulation of food intake.. 76 I.6.6 Other neurotransmitters. .. 76 T.6.7 Sþals arising from adipose tissue. 77 I I.7 The Regulation of Energy Expenditure.... 78 1.7.1 Basal metabolic rate. 78 1.7.2 Physical activity...... 79 l. 7.3 Non-shivering thermoge,lresis. 79 L7 .4 Diet-induced thermogenesis. 8ó I.7.5 Tmpact ofthermogenesis on the regulation of body composition. 88 1.7.6 Conolusion 89 CHAPTER 2: RELEVANCE OF A MARST]PIAL MODEL FOR STUDMS RELATING TO THE REGIILATION OF BODY FAT STORES, APPETTTE, AND EI\ERGY EXPEI\DTTURE 2.1 Summary 90 2.2 The Evolution and Taxonomy of Marsupials. 9I 2.3 The Regulation ofAppetite and Energy Balance in Marsupials. 94 2.3.I Appetite regulation in marsupials.... 94 2.3.2 Thermogenesis in marsupials 96 2.4 Sminthopsis crassicaudata (the fat-tailed ûrnnart) 101 2.4.1 Classification, distribution, habitat and morphological variation. .. .. 101 2.4.2 Diet and food intake. t04 2.4.3 Aotivity. t07 2.4.4 Reproduction... 108 2.4.5 Caudal fat storage in S. crassicaudøta, 109 2.4.6 Thermoregulation in S. crassicaudatø. tr4 2.5 Overall Aims of the Study.... 115 CHAPTER 3: GENERAL MATERIALS AND METIIODS 3.1 Animals and Housing. 118 3.1.1 Animals. 118 3.1.2 Housing.. 118 3.1.3 Variation in day lengfh. 119 3.2 Diets. r20 3.2.1 Standard laboratory diet... r20 3.2.2 Mealworms. r20 3.2.3 Wúer t20 ü J.J Measurements.. ... 12L 3.3.1 Tailwidth. L2l 3.3.2 Enetgy intake (food intake)..... 12T 3.3.3 Body temperature...... t2r 3.3.4 Metabolic parameters t22 3.4 Blood Sampling. t23 3.4.I Blood glucose concentration 124 3.4.2 Plasma free fatty acid concentration.. 124 3.4.3 Plasma cortisol conce,lrtration....... 124 3.5 Drug Preparation and Administration.... t25 3.5.1 Leptin. 125 3.5.2 2-deoxy-D-glucose and insulin 125 3.5.3 Mercaptoacetate. t25 3.5.4 Opioid peptide antagonists 125 3.5.5 Gastrointestinal peptides.. .. ...... 126 3.5.6 Urooortin, corticotrophin releasing factor and antalarmin 126 3.6 Surgery. t27 3.6.1 Tail removal.... r28 3.6.2 Ovariectomy.... r28 3.7 Characterisation of Adipose Tissue. r29 3.7.I Analysis of fat content using a triglyceride assay. t29 3.7 .2 Electron microscopy. t29 3.7 .3 Biochemical analysis of interscapular adipose tissue. .. 130 3.8 Laboratory Techniques. 131 3.8.1 RNA extractions and agarose gel electrophoresis. .. 131 3.8.2 Probes.. L32 t'P 3.8.3 Northerr blotting using labeled DNA probes. 133 3.8.4 Northem blotting using DIG labelled oligonucleotides.... .. t34 3.8.5 Quantitation of ge,ne expression following Northem blotting 135 3.9 StatisticalAnalysis. 135 4: FEEDING PATTERNS IN CHAPTER ^S. CRASSICAUDATA: EFFECTS OF GENDE$ PHOTOPERIOD AND FASTING 4.1 Summary 136 4.2 Introduction. 137 ll1 4.3 Materials and Methods. .... t40 4.3.I Experimental animals and diets.. 140 4.3.2 Experimental protocols. 140 4.3.3 Statistical analyses. t42 4.4 Results.. r42 4.4.L Study 1: Circadian food intake 142 4.4.2 Study 2: Food intake immediateþ after the onset ofthe dark phase r42 4.4.3 Study 3: Effect offood deprivation r43 4.4.4 Study 4: Effect of a 24 hour fast on blood glucose and plasma free fatty acids. r44 4.5 Discussion 151 CHAPTER 5: CIIARACTERISATION OF TAIL FAT IN S. CRASS ICAUDATAZ EFFECT OF LIPECTOMY AND DIET 5.1 Summary 156 5.2 Introduction. t57 5.3 Materials and Methods.... ... 160 5.3.1 Experimental animals and diets.. 160 5.3.2 Experimental protocols.... ... .... 160 s.3.3 Statistical analyses. 162 5.4 Results t62 5.4.1 Characterisation of tail fat r62 5.4.2 F;trect of lipectomy on body weight, energy intake and tail fat stores. r62 5.4.3 Effect of a high calorie diet on energy intake, body weight, and tail fat stores. r64 5.5 Discussion 172 CHAPTER 6: CLOI\ING OF LEPTIN cDNA ANI) ASSIGNMENT TO THE LONG ARM OF CHROMOSONE 5IN S. CRASSICAUDATA 6.I Summary r75 6.2 Introduction. 176 ry 6.3 Materials and Methods. r78 6.3.1 Cloning of S. crsssicaudøta leptin. 178 6.3.2 Leptin sequence anaþsis. 179 6.3.3 Southem and Northem blotting. L79 6.3.4 Chromosomal localisation of ,S. crassicaudnta leptin cDNA..... 181 6.4 Results. t82 6.4.r Isolation and sequence of S. crassicaudnta leptn oDNA' . ... t82 6.4.2 Comparative anaþsis of S. crassicaudøta leptin protein..... 183 6.4.3 Phylogenetic analyses. 183 6.4.4 Expression of S. crassicaudata leptin. 183 6.4.5 Chromosomal localisation of S. crassicaudata leptin oDNA. 184 6.5 Discussion. 192 CHAPTER 7: THE EFFECT OF DIET ON THT'RESPONSE TO LEPTIN IN S. CRASSICAUDATA 7.1 Summary 197 7.2 Introduction 198 7.3 Materials and Methods 200 7.3.1 E4perimental animals, diets and drugs... 200 7.3.2 Metabolic parameters 200 t.J.t Experimental protocols. 200 7.3.4 Statistical analyses. 202 7.4 Results. 202 7.4.1 Study 1: Effect of leptin on body weight and tail width in relation to diet. 202 7.4.2 Sfidy 2: Effect of leptin on blood glucose concentratron in relation to diet. 207 7.5 Dscussion. 215 CHAPTER 8: GLUCOPRTVATION IN,S. CRASSICAUDATA AI\[D ITS EFFECTS ON APPETITE 8.1 Summary.... 222 8.2 Introduotion. 223 v 8.3 Materials and Methods 225 8.3.1 Experimental animals, diet and drugs.. 225 8.3.2 Experimental protocols. .. 226 8.3.3 Statistical anaþses. 227 8.4 Results 228 8.4.1 Study 1: Effect of insulin and 2-DG on blood glucose concentrations. 228 8.4.2 Study 2: Effect of insulin-induced h¡poglycaemia and2-DG on food intake...... 228 8.4.3 Study 3: Effect ofinsulin-induoed h¡poglycaemia and 2-DG on food intake in reqponse to photoperiod.. 229 8.4.4 Study 4: Effect of 2-DG on food intake in reqponse to a prefened food.. ..... 229 8.5 Discussion. 235 CHAPTER 9: FATTY ACIDS AND FOOD INTAKE IN S. CRASSICAUDATA 9.1 Summary 239 9.2 Introduction 240 9.3 Materials and Methods..... 243 9.3.1 Experiment¿l animals, diet and drugs... 243 9.3.2 Experimental protocols. .. 243 9.3.3 Statistical analyses. 244 9.4 Rezults. 244 9.4.1 Study 1: Effect of mercaptoacetate on plasma free fatty acid levels. 244 9.4.2 Sfidy 2: Effect ofmercaptoacetate on food intake during the light and dark phase. 245 9.5 Discussion 248 CHAPTER 10: PERIPITF',RAL ADMII\¡-ISTRATION OF CORTICOTROPHIN RELEASING FACTOR AND UROCORTIN: EFFECTS ON FOOI) Al\[D THE IIPA AXIS IN INTAI(E ^S. CRASSICAUDATA 10.1 Summary. .. 253 vr I0.2 Introduction 255 10.3 Materials and Methods.... 258 l0.3.1Experiment¿l animals, diet and drugs. 258 10.3.2 Metabolic variables, blood sampling, plasma oortisol measurement 258 10.3.3 Experimental protocols. .. 259 10. 3. 4 Statistical analyses. 260 10.4 Results 26r 10.4.1 Study 1: Effects of UCN, CRF and ANT on e,nergy intake.. 261 ll.4.2Study 2: Effects ofAl.IT on feedi.g following UCN or CRF administration 262 10.4.3 Study 3: Effects of CRF and UCN on VOz and RQ. 263 L0.4.4 Study 4: Effects of UCN and CRF on plasma cortisol........ 263 10.5 Discussion. 27t CHAPTER 11: FOOD INTAI(E AND FOOD CHOICE IN,S. CRASSICAUDATAZ THE ROLE OF THT ENDOGENOUS OPIOD PEPTIDES 11.1 Summary 277 IL.2 Introduction 278 11.3 Materials and Methods 280 11.3.1 Experimental animals, diets and drugs.. ... 280 I 1. 3. 2 Experimental protocols. 28t I 1. 3. 3 Statistical analyses. 282 Ll.4 Res,ults.
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