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Aus Dem Institut Für Humanernährung Und Lebensmittelkunde Der Christian-Albrechts-Universität Zu Kiel

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Aus Dem Institut Für Humanernährung Und Lebensmittelkunde Der Christian-Albrechts-Universität Zu Kiel Aus dem Institut für Humanernährung und Lebensmittelkunde der Christian-Albrechts-Universität zu Kiel Sex differences in Caenorhabditis elegans in body composition, lipid storage and gene expression under ad libitum and dietary restriction conditions Dissertation zur Erlangung des Doktorgrades der Agrar- und Ernährungswissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel vorgelegt von M.Sc. oec. troph. Claudia Miersch aus Bergen auf Rügen Kiel, 2012 Dekanin: Prof. Dr. Rainer Horn 1. Berichterstatter: Prof. Dr. Frank Döring 2. Berichterstatter: Prof. Dr. Gerald Rimbach Tag der mündlichen Prüfung: 12.07.2012 Gedruckt mit Genehmigung der Agrar- und Ernährungswissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel Wenn einer sucht, dann geschieht es leicht, dass sein Auge nur noch das Ding sieht, das er sucht, dass er nichts zu finden, nichts in sich einzulassen vermag, weil er immer nur an das Gesuchte denkt, weil er vom Ziel besessen ist. Suchen heißt: ein Ziel haben. Finden aber heißt: frei sein, offen stehen, kein Ziel haben. (Hermann Hesse) TABLE OF CONTENTS TABLE OF CONTENTS Preface I-X Table of contents I List of figures II List of tables IV Abbreviations V Abstract VII Zusammenfassung IX 1 Introduction 1-8 1.1 Caenorhabditis elegans as a model organism 1 1.2 Sex differences in C. elegans 2 1.3 Dietary restriction in C. elegans 4 1.4 Influence of paternal nutrition on offspring phenotype 7 1.5 Aims of the study 8 2 Material and Methods 9-13 3 Results 14-55 3.1 Analysis of sex differences in C. elegans 14 3.2 Response of males and hermaphrodites to dietary restriction 34 3.3 Influence of paternal dietary restriction on progeny fat content 52 4 Discussion 56-68 4.1 Sex differences under ad libitum conditions in body 56 proportions, RNA content, carbohydrate metabolism and gene expression of C-type lectins 4.2 Influence of dietary restriction on fat storage, lipid 62 metabolism, developmental growth and reproduction in males and hermaphrodites 4.3 Influence of paternal dietary restriction on progeny fat content 66 4.4 Conclusion 67 5 References 69-81 6 Appendix 82-117 6.1 Supporting information 82 6.2 Acknowledgments 114 I LIST OF FIGURES LIST OF FIGURES figure no. title page figure 1. Life cycle of C. elegans from egg to adulthood. 1 figure 2. Anatomy of C. elegans males (A) and hermaphrodites (B). 3 figure 3. Morphology (A) and flow cytometry-based separation (B) of 15 adult males and hermaphrodites in different C. elegans male mutants. figure 4. Relationship between time of flight (TOF) and body length (A) 16 and extinction (EXT) and body volume (B). figure 5. Flow cytometry-based parameters of body proportions of him-8 17 GFP males and hermaphrodites at different developmental stages. figure 6. Body length (A) and body volume (B) of adult males and 18 hermaphrodites in different C. elegans male mutants. figure 7. Body composition of males and hermaphrodites at different 19 developmental stages. figure 8. Glucose and trehalose content of males and hermaphrodites at 21 different developmental stages. figure 9. Total RNA content of young adult and adult him-8 GFP males 22 and hermaphrodites. figure 10. Number of differentially expressed genes between him-8 GFP 24 males and hermaphrodites. figure 11. Differential expression of C-type lectins between him-8 GFP 30 males and hermaphrodites at young adulthood (66 h) and adulthood (76 h). figure 12. Changes of body proportions under DR (OD 1.5) in males and 35 hermaphrodites at different developmental stages. figure 13. Changes of protein and total RNA content under DR (OD1.5) 37 in him-8 GFP males and hermaphrodites at different developmental stages. figure 14. Changes of body composition under DR (OD1.5) in him-8 38 GFP males and hermaphrodites at different developmental stages. figure 15. Lipid droplets under ad libitum (top) and DR (OD 1.5, bottom) 39 II LIST OF FIGURES conditions in him-8 males (A) and hermaphrodites (B). figure 16. Lipid droplets under ad libitum (top) and DR (OD 1.5, bottom) 40 conditions in him-5 males (A) and hermaphrodites (B). figure 17. Lipid droplets under two DR (OD 1.5 and OD 0.7) conditions in 41 fog-2 males (A) and females (B). figure 18. Changes of glucose and trehalose content under DR (OD 1.5) 42 in him-8 GFP males and hermaphrodites at different developmental stages. figure 19. Functional annotation clustering of DR regulated genes from 44 him-8 GFP worms at young adult (66 h) stage. figure 20. Functional annotation clustering of DR regulated genes from 46 him-8 GFP worms at adult (76 h) stage. figure 21. Differential expression of sperm-associated genes under DR 49 (OD 1.5) in him-8 GFP males and hermaphrodites. figure 22. Temporal gene expression drift of major sperm protein (msp) 50 genes under DR (OD 1.5) in him-8 GFP hermaphrodites (top) and males (bottom). figure 23. Temporal gene expression drift of sperm-associated genes 51 under DR (OD 1.5) in him-8 GFP hermaphrodites (grey) and males (black). figure 24. Experimental design to study the effects of paternal DR 52 on the F1 generation. figure 25. Influence of different DR conditions on P0 male body 53 proportions. figure 26. Influence of different paternal DR conditions on progeny body 54 proportions. figure 27. Influence of different paternal DR conditions on progeny fat 55 content (A) and relative fat content (B). figure 28. Conversion of glucose in males and hermaphrodites. 59 III LIST OF TABLES LIST OF TABLES table no. title page table 1. Male-specific genes. 25 table 2. Hermaphrodite-specific genes. 28 table 3. Sex differences in the gene expression of carbohydrate 32 metabolic genes. table 4. Number of DR-regulated genes in both sexes at both 43 developmental stages. table 5. Summary of sex differences under ad libitum and DR conditions 56 in C. elegans. Supporting information table S1 Calculation of dietary restriction ranking. 82 table S2 Body composition of males and hermaphrodites at different 83 developmental stages in different male mutants. table S3 Glucose and trehalose content of males and hermaphrodites 84 at different developmental stages in different male mutants. table S4 The entire list of male-specific genes. 85 table S5 The entire list of hermaphrodite-specific genes. 92 table S6 Body composition of him-8 GFP males and hermaphrodites 98 under ad libitum and DR at different developmental stages. table S7 Glucose and trehalose content of him-8 GFP males and 99 hermaphrodites under ad libitum and DR at different developmental stages. table S8 Overlapping genes between both sexes and both 100 developmental stages. table S9 Expression level and DR to ad libitum ratio of sperm- 108 associated genes in both sexes at young adult (66 h) stage. table S10 Expression level and DR to ad libitum ratio of sperm- 111 associated genes in both sexes at adult (76 h) stage. IV ABBREVIATIONS ABBREVIATIONS acbp Acyl-Coenzyme A binding protein age ageing alteration AMPK 5’ adenosine monophosphate-activated protein kinase ANOVA analysis of variance ATP andenosine-5’-triphosphate AU arbitrary unit BCA bicinchoninic acid ceh C. elegans homeobox C. elegans Caenorhabditis elegans CGC Caenorhabditis Genetics Center cht chitinase clec C-type lectin cyp cytochrome P450 family daf abnormal dauer formation DAVID Database for Annotation, Visualization and Integrated Discovery dhs dehydrogenases, short chain D. melanogaster Drosophila melanogaster dpy dumpy (shorter than wild type) DR dietary restriction eat eating (abnormal pharyngeal pumping) EXT extinction flh FLYWCH zinc finger transcription factor homolog fog feminization of germline FOX forkhead box GFP green fluorescence protein gob gut obstructed or defective gsp GLC7 (yeast Glc Seven) like phosphatase gsy glycogen synthase hif (hypoxia inducible factor) homologa him high incidence of males hsf heat shock factor KEGG Kyoto Encyclopedia of Genes and Genomes let lethal lipl lipase like lsy laterally symmetric (defective in lateral symmetry) mab male abnormal maoc MAO-C-like dehydratase domain msp major sperm protein mtl metallothionein mxl max-like protein NAD+ nicotinamide adenine dinucleotide NGM Nematode Growth Medium nhr nuclear hormone receptor nlp neuropeptide-like protein NMR Nuclear Magnetic Resonance nmur neuromedin U receptor V ABBREVIATIONS Nrf nuclear respiratory factor pes patterned expression site pha defective phaynx development pkd polycystic kidney disease (related) pmt phosphoethanolamine methyltransferase PMT photomultiplier RNA ribonucleic acid rRNA ribosomal RNA sams S-adenosyl methionine synthetase scl SCP-like extracellular protein SD standard deviation sdz SKN-1 dependent zygotic transcript skn Skinhead spe defective spermatogenesis ssp sperm-specific family class P ssq sperm-specific family class Q sss sperm-specific family class S sst sperm-specific transcript tbx T-box family TOF time of flight TOR target of rapamycin tps trehalose 6-phosphate synthase ugt UDP-glucoronosyltransferase ztf zinc finger putative transcription factor family VI ABSTRACT ABSTRACT The nematode Caenorhabditis elegans (C. elegans) contains two sexes, males and hermaphrodites, which are highly dimorphic in anatomy, nervous system and behavior. However, the physiology of males in comparison to hermaphrodites under normal feeding conditions and in the context of dietary restriction (DR) is largely unexplored. Here, body proportions and composition, certain aspects of carbohydrate metabolism, fat storage and gene expression of males and hermaphrodites were analyzed under ad libitum and DR conditions. Furthermore, males were used to determine the influence of different paternal DR regimes on F1 progeny fat content. In this study male-enriched mutant stains were used, one with a sex-specific GFP signal, led to a large number of males being separated from hermaphrodites by flow- cytometry. Analysis of sex differences under ad libitum conditions unraveled that the fat-to-fat- free mass as well as the body volume adjusted fat mass was similar between the sexes, although the body size was over 50 % lower in adult males than in age- matched hermaphrodites.
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