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The Teleost Taar Family of Olfactory Receptors

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The Teleost Taar Family of Olfactory Receptors The teleost taar family of olfactory receptors: From rapidly evolving receptor genes to ligand-induced behavior Inaugural-Dissertation zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultät der Universität zu Köln vorgelegt von Ashiq Hussain aus Jampur, Pakistan Köln 2010 1 Berichterstatter: Prof. Dr. Sigrun I. Korsching Prof. Dr. Jens C. Brüning Tag der mündlichen Prüfung: 23 November, 2010 2 ERKLÄRUNG Ich versichere, dass ich die von mir vorgelegte Dissertation selbstständig angefertigt, die benutzten Quellen und Hilfsmittel vollständig angegeben und die Stellen in der Arbeit - einschließlich Tabellen, Karten und Abbildungen -, die anderen Werken im Wortlaut oder dem Sinn nach entnommen sind, in jedem Einzelfall als Entlehnung kenntlich gemacht habe; dass diese Dissertation noch keiner anderen Fakultät oder Universität zur Prüfung vorgelegen hat; dass sie - abgesehen von den unten angegebenen Teilpublikationen – noch nicht veröffentlicht worden ist, sowie dass ich eine solche Veröffentlichung vor Abschluss des Promotionsverfahrens nicht vornehmen werde. Die Bestimmungen dieser Promotionsordnung sind mir bekannt. Die von mir vorgelegte Dissertation ist von Prof. Dr. Sigrun. I. Korsching betreut worden. Köln, den 04. Nov, 2010 Teilpublikationen: Hussain, A., Saraiva, L.R., Korsching, S.I. (2009)c Positive Darwinian selection and the birth of an olfactory receptor clade in teleosts. Proc. Natl. Acad. Sci. USA. 106(11):4313- 4318 Faculty of 1000 Biology: evaluations for Hussain A et al. Proc Natl Acad Sci U S A 2009 Mar 17,106 (11):4313-8 3 To my parents 4 I. Acknowledgement This study was conducted in the system neurobiology laboratory of Prof. Dr. Sigrun I. Korsching at the Institute for Genetics, University of Cologne, Germany. This research was supported by the generous grant from the International Graduate School of Genetics and Functional Genomics (IGSGFG) at the Institute for Genetics. Foremost, I pay my sincere gratitude to Prof. Dr. Sigrun I. Korsching for being a great mentor. I am very thankful to her for the support, advices and trust she bestowed on me. I learnt from her the meanings of patience, coordination, candidness and how to tackle daily life of a science laboratory. I am very contented that I had the opportunity to spend ~4 years in learning, from culture to science, at her laboratory. I will extend my acknowledgement to Prof. Dr. Jens C. Brüning and to Prof. Dr. Matthias Hammerschmidt for accepting to be in my thesis committee, for their interest in my research work, and for kindly serving as my thesis referees. I greatly appreciate Dr. Stephen D. Liberles at Harvard Medical School for our successful collaboration and for inviting me to work in his lab for the identification of ligands for Trace Amine-associated Receptors (TAARs). I am also very thankful to David Ferrero, who reproduced the TAAR ligands results and did the HPLC analysis, Jamie K. Lemon for her help regarding methodological aspects of ligands identification assays, and Wayne Korzan for his technical advices in establishing the behavioral assay. Many thanks to Prof. Ansgar Büschges and Dr. Matthias Gruhn for providing room for establishing behavior assay facility and for their technical help in WINANALYZE motion tracking software. I was humbled and honored for being accepted in the class of 2006 of graduate school. My family has a special bond of love and respect for Germany. I am the 3rd generation of my family to serve and study in Germany and I am obliged to this country for providing me the opportunity to learn and to the German people for being so civil and supportive. Many thanks are to Dr Isabell Witt, Brigitte Wilcken-Bergmann, Cathy Joergens and Joanna Majczak for their support in all walks of life at graduate school. I was fortunate to have cooperative and ambitious lab fellows like Dr. Luis R. Saraiva, Dr. Yuichiro Oka and Dr YenYen Kewan to whom I indebt a great deal of valuable feedback and collaborations. Sincere thanks to Mehmet Saltürk for taking care of all lab equipments, fish room, computers and experimental material supplies. I am in lack of words to thank my father who envision for the education of his children and migrated to a big city for this sole purpose. I am greatly thankful to him for financially and morally supporting me in my life. A great deal of thanks to my mother for taking care of the family, for staying awake with us during exams nights and for her all great sacrifices that she made with my father for their children´s education. Very special thanks to my wife Sofia Lyngemark Hussain for being a loving, supportive, caring and understanding life companion. I am thankful to her for understanding and accepting me to work in lab during weekends, for moral support in stressful experimental times (c-Fos and behavioral assays), for staying by herself while I attended international conferences and for all great things that she did for me. Thank you. 5 This page was intentionally left blank. 6 II. TABLE OF CONTENTS I. ACKNOWLEDGEMENT ................................................................................................... 5 II. TABLE OF CONTENTS .................................................................................................. 7 III. LIST OF FIGURES ....................................................................................................... 12 IV. LIST OF TABLES......................................................................................................... 13 V. LIST OF SUPPLEMENTARY TABLES ......................................................................... 13 VI. ABSTRACT .................................................................................................................. 14 ZUSAMMENFASSUNG .................................................................................................... 16 CHAPTER 1 ...................................................................................................................... 18 VII. INTRODUCTION ........................................................................................................ 19 1. OLFACTORY SYSTEM ................................................................................................. 19 1.1. Mammalian olfactory system ...................................................................................... 20 1.2. Zebrafish olfactory system ......................................................................................... 22 1.3. OLFACTORY SENSORY NEURON (OSNS) ............................................................. 24 1.3.1. Ciliated olfactory sensory neurons .......................................................................... 24 1.3.2. Microvillous olfactory sensory neurons ................................................................... 25 1.3.3. Crypt sensory neurons ............................................................................................ 25 1.4. OLFACTORY RECEPTOR GENE FAMILY REPERTOIRE ....................................... 26 1.4.1. Odorant receptor family (OR) .................................................................................. 28 1.4.2. Trace amine-associated receptor family (TAAR) .................................................... 30 1.4.3. Vomeronasal receptors family type1 (V1R) ............................................................. 32 7 1.4.4. Vomeronasal receptors family type2 (V2R) ............................................................. 34 1.4.5. Formyl peptide receptor family (FPR) ..................................................................... 35 1.5. OLFACTORY SIGNALING TRANSDUCTION ........................................................... 35 1.6. LIGANDS FOR OLFACTORY RECEPTORS ............................................................. 38 1.7. FISH BEHAVIOR........................................................................................................ 39 1.8. ZEBRAFISH AS A MODEL ORGANISM .................................................................... 41 CHAPTER 2 ...................................................................................................................... 44 VIII. RESULTS .................................................................................................................. 45 1. PHYLOGENOMICS, SELECTION PRESSURE, INTRON DYNAMICS AND CELLULAR EXPRESSION OF TAARS ................................................................................................ 45 1.1. TAAR genes encompass monophyletic origin distinct from aminergic GPCRs ......... 45 1.2. Rapid evolution of TAAR gene as a recurrent species-specific expansions in teleost46 1.3. TAAR genes are an evolutionary young family .......................................................... 50 1.4. TAAR family is characterized by distinctive consensus motifs, despite the overall heterogeneity. ................................................................................................................... 52 1.5. Genomic arrangement of teleost TAAR genes pinpoints the evolutionary origin of class III. ............................................................................................................................. 54 1.6. Gene duplication rate and gene divergence are much higher in teleost compared with mammalian species, suggesting a teleost- restricted rapid evolution of taar genes. ........ 55 1.7. Strong local positive selection in teleost taar genes is masked by global negative selection. ..........................................................................................................................
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