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Development of a Genetic Multicolor Cell Labeling Approach for Neural Development of a genetic multicolor cell labeling approach for neural circuit analysis in Drosophila Dafni Hadjieconomou January 2013 Division of Molecular Neurobiology MRC National Institute for Medical Research The Ridgeway Mill Hill, London NW7 1AA U.K. Department of Cell and Developmental Biology University College London A thesis submitted to the University College London for the degree of Doctor of Philosophy Declaration of authenticity This work has been completed in the laboratory of Iris Salecker, in the Division of Molecular Neurobiology at the MRC National Institute for Medical Research. I, Dafni Hadjieconomou, declare that the work presented in this thesis is the result of my own independent work. Any collaborative work or data provided by others have been indicated at respective chapters. Chapters 3 and 5 include data generated and kindly provided by Shay Rotkopf and Iris Salecker as indicated. 2 Acknowledgements I would like to express my utmost gratitude to my supervisor, Iris Salecker, for her valuable guidance and support throughout the entire course of this PhD. Working with you taught me to work with determination and channel my enthusiasm in a productive manner. Thank you for sharing your passion for science and for introducing me to the colourful world of Drosophilists. Finally, I must particularly express my appreciation for you being very understanding when times were difficult, and for your trust in my successful achieving. Many thanks to my thesis committee, Alex Gould, James Briscoe and Vassilis Pachnis for their quidance during this the course of this PhD. I am greatly thankful to all my colleagues and friends in the lab. Holger Apitz, Katarina Timofeev, Carole Chotard, Willy Joly, Justine Oyallon, Lauren Ferreira, Emily Richardson, Benjamin Richier, Frederico Rodrigues and Nana Shimosako. I particularly like to thank Willy Joly for being my teacher in molecular biology techniques and such a fun person to work with. In addition, special thanks to Cyrille Alexandre for all help and fruitful discussions with molecular biology issues that have been raised during the course of this project. Thanks to the fly community of the NIMR as well as the MNB division. This goes to all past and present members of the Gould, Vincent, Gullemot and Pachnis labs, for providing feedback and technical help and a fantastic working atmosphere. Special, thanks to the CIAL facility and specifically to Donald Bell. My special thanks go to Holger for being a colleague, a flatmate and a true friend. Your help has been the catalyst for my thesis to progress and eventually close it’s cycle. My immense gratitude to Katarina, my PhD buddy for sharing this unique experience with me step by step. Thanks to Myrto Denaxa, you have been the sunshine in the rainy days of work or life. You sheltered me in your house in difficult times, and you were always there to joke and help. Thank you for your friendship. Thanks to Angeliki Achimastou for being such a generous and patient friend. Thanks Philippos and Maria, Nikos and Gitta for making me laugh out loud. Thanks to Thomas Brantzos for undertaking the adventure of a scientific life with, me and even though it has been a rocky path remained by my side. Thanks to Toby Coleman for skipping all the holidays I couldn't make and for always showing me the silver lining of things in life. Most importantly, thanks to my family. This thesis, I dedicate to you Maria, Andreas and Sophia who make me who I am. Thanks to my parents for supporting my decisions all the way, even if that meant my long absence from our common life. I love you and have no words to express my gratitude towards you. Thanks to my sister, Sofia, that completes and inspires me. You show me how to live the life to its silly and serious moments! 3 Abstract The assembly of functional neural circuits during development is pivotal for the ability of the brain to generate complex behaviors. To facilitate the analysis of the underlying molecular mechanisms in Drosophila, we have developed a genetic multicolor cell labeling approach called Flybow (FB), which is based on the vertebrate Brainbow-2 system. FB relies on the stochastic expression of membrane tethered fluorescent proteins (FPs). FP encoding sequences were arranged in pairs within one or two cassettes each flanked by recombination sites. Recombination mediated by an inducible modified Flp/FRT system results in both excisions and inversions of the flanked cassettes providing temporal control of FP expression. Moreover, FB employs the GAL4/UAS system and hence can be used to investigate distinct cell populations in the tissue of interest. We have generated three FB variants. FB1.0 consists of one cassette driving expression of either mCherry or V5-tagged Cerulean. FB1.1 contains a second cassette with opposing enhanced green fluorescent protein (EGFP) and mCitrine cDNAs leading to stochastic expression of four FPs. Finally, FB2.0 contains an additional excisable cassette flanked by classical FRT sites to refine transgene expression in specific cell types, in which Gal4 and Flp activities overlap. The FB approach was validated by investigating neural circuit assembly and connectivity in the visual system. FB makes it possible to visualize dendritic and axonal arborizations of different neuron subtypes and the morphology of glial cells with single cell resolution in one sample. Using live and fixed embryonic tissue, we could show that FB is suitable for studies of this early developmental stage. Additionally, we demonstrated that the approach can be used in non-neural tissues. Finally, combining the mosaic analysis with a repressible cell marker (MARCM) and FB approaches, we demonstrate that our technique is compatible with available Drosophila tools for genetic dissection of neural circuit formation. 4 Table of contents Title 1 Declaration 2 Acknowledgements 3 Abstract 4 Table of contents 5 List of figures and tables 8 Abbreviations 10 Chapter 1 – Introduction 13 1.1 Cells in the nervous system entwine to form complex network 14 1.1.1 Lessons from history 14 1.1.2 Wiring diagrams can be used to decode the complexity of neural network 16 functions 1.1.3 The concept of the “connectome” 18 1.1.4 Generation of network components during development 20 1.1.5 Netrins guide axons by both attraction and repulsion 24 1.1.6 The Robo/Slit system prevents ipsilateral axons from crossing and 27 commissural axons from re-crossing the midline 1.1.7 Ephrin and Semaphorin guidance system provide repulsive guidance cues 29 in the midline 1.2 The visual system of Drosophila as a model to study neural circuit formation 31 1.2.1 Visual systems comprise good models for circuit studies 31 1.2.2 Anatomy of the fly visual system 32 1.2.3 Visual information is processed in parallel pathways within the 33 medulla neuropil 1.2.4 Cell diversity in the Drosophila visual system 34 1.2.5 Subtypes of neurons in the fly visual system are generated using 35 distinct mechanisms 1.2.6 Different glia subtypes are found within the Drosophila optic lobes 36 1.2.7 Neurons and glia are implicated in neural network assembly of Drosophila 38 optic lobes 1.2.8 Molecular and other mechanisms involved in network formation 39 1.3 Approaches to understand the connectivity and development of neural circuits 39 1.3.1 Genetic approaches to manipulate genes in circuits in Drosophila 40 1.3.2 Genetic markers allow neuron labeling within a network in Drosophila 42 1.3.3 Advanced genetic strategies combined with imaging approaches to study 45 connectivity 1.3.4 Randomized multicolor cell labelling 46 1.4 Aims of the work undertaken to complete this thesis 48 Chapter 2 - Materials and Methods 49 2.1 Genetics 50 2.1.1 Fly Stocks 50 2.1.2 Transgenesis using the attP/attB system 53 2.1.3 Clone induction 54 2.2 Molecular biology 55 2.2.1 Standard PCR 55 2.2.2 Gel electrophoresis 56 2.2.3 PCR on bacterial colonies 56 2.2.4 Annealing oligonucleotides 57 2.2.5 PCR and gel band purification 57 2.2.6 DNA quantification 58 2.2.7 DNA modifications 58 2.2.7a Restriction endonuclease digestion of DNA 58 2.2.7b DNA ligation 58 5 2.2.7c DNA dephosphorylation 58 2.2.8 Molecular cloning 58 2.2.9 Protein expression in bacteria 59 2.2.10 Western blot analysis 59 2.2.11 Transient transfection of S2 cells 60 2.2.11a Culture conditions 60 2.2.11b Fixation of cells 61 2.2.12 Immunohistochemistry 61 2.3 Image acquisition and analysis 62 2.3.1 Confocal microscopy 62 2.3.2 Channel separation and image processing 63 2.4 Quantifications 64 Chapter 3 - Building “Flybow” 65 3.1 Introduction 66 3.2 Adapting the tool for Drosophila 66 3.3 Choosing a modified FLP/FRT system 67 3.4 General features of Flybow variants – an overview 69 3.5 The cloning strategy 71 3.5.1 Building the modified vectors 71 3.5.2 Building the basic modules 73 3.6 Expression of individual membrane-tethered fluorescent proteins in bacteria 77 3.7 Pilot transgenesis using UAS-cd8-mCherry 79 3.8 Assembling Flybow variants 80 3.9 Generation of Flybow transgenic lines 85 3.10 Discussion 85 3.10.1 Transfer to a Fly “bow”- Advantages and limitations 85 Employing the power of fly genetics 86 Switching to a new DNA recombination system 86 3.10.2 Generating complex, yet adjustable DNA constructs 87 Switching to a different membrane tag 88 Chapter 4 - FB1.0 in vivo-Putting the approach to the test 89 4.1 Introduction 90 4.2 Expression of mFlp5 leads to inversion of FB1.0 cassette 90 4.3 Suboptimal fluorescence levels of Cerulean 92 4.4 Discussion 93 4.4.1 Establishing inversions as an alternative
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