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Analysis of Murine Homeobox Genes Anthony Graham ANALYSIS OF MURINE HOMEOBOX GENES ANTHONY GRAHAM Thesis for the Degree of Doctor of Philosophy Division of Eukaryotic Molecular Genetics National In s titu te fo r Medical Research The Ridgeway, M ill H ill London NW7 1AA Univeristy College London Gower Street London WC1E 6BT November, 1989 ProQuest Number: 10611102 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest 10611102 Published by ProQuest LLC(2017). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLC. ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106- 1346 This thesis is dedicated to my mother and father. i i The work in this thesis is original except where stated. The sequences used for comparisons in Chapter 3 were not determined by the author but were either from publications from other laboratories or from other members of the laboratory. Anthony Graham: ABSTRACT The work in this thesis is consistent with , and strengthens, suggestions that murine homeobox genes play a role in the establishment of regional specification. It is shown that there is a correlation between the physical order of members of the Hox 2 cluster and their order of expression along the rostrocaudal axis, such that each more 3' gene is expressed more rostrally. Such a correlation has been previously shown for the Drosophila homeotic genes o f the ANT-C and BX-C, where i t was clear that these genes were involved in the establishment of regional identity along the rostrocaudal axis. It has also been demonstrated that the relationship between the murine and Drosophila clusters extends further than aspects of their expression patterns. Sequence comparisons suggest that the murine Hox clusters and the Drosophila homeobox clusters arose from a common ancestral cluster that existed prior to the divergence between the protostomes and thejdeuterostomes, jheref0re the corresponding utilisation of ordered region specific expression of members of homeobox clusters in flie s and mice together with their conservation would suggest that these genes are involved in the establishment of rostrocaudal regional specification in these organisms, and by inference in all other higher metazoans. I t is also demonstrated that the Hox 2 genes show s p a tia lly and temporally dynamic patterns of expression in the transverse plane of the developing central nervous system. Since a ll of the Hox 2 genes e xh ib it similar expression patterns it is fe lt they are reflecting events during ontogeny of the spinal cord. The observed patterns correlate with the timing and location of the b irth of the major classes of neurons. I t is suggested that the Hox 2 genes are conferring rostrocaudal positional information on each class of newly born neurons. These genes also e xh ib it a s trik in g dorsal restriction in their expression within the developing spinal cord which does not appear to correlate with morphology and eventually breaks down. ACKNOWLEDGEMENTS Firstly, I would like to thank my external supervisor Dr. Robb Krumlauf for all of his excellent help, encouragement and guidance during the course of this work. I also thank Dr. David Latchman (University College, London) for efficiently fu lfillin g his role as my University supervisor. This research was carried out at the National Institute for Medical Research and was supported by the MRC. I wish to acknowledge the assistance provided by the NIMR photography section. I also thank many of the past and present members of NIMR, particularly o f the laboratories of Molecular Embryology and Embryogenesis, fo r a ll of their help and friendship. Particular thanks to a few gurus - Jonathan Cooke, / Peter Holland, Malcolm Maden and DennisSummerbell who have been an invaluable source of information and discussion . Jeremy Green and Peter Vize have been wonderful proof readers, spotting many a ridiculous mistake, and who have also come up with more than a few smart ideas. Extra thanks go to Nancy Papalopulu, my long suffering lab mate and friend, who has helped immensely throughout the period of this work both technically and intellectually and without whom I don't know what I would have done. I also wish to thank Pal Njolstad ,the zebrafish man, who has generously supplied much unpublished information. Cheers Big Man, by the way - Sheila, Kathleen, Gerard, P h ilip , Brian ,Carol and Dan and not to forget Sandy for many an interesting biological discussion. Finally thanks to mum and dad for everything for the past many years. iv CONTENTS Page No. T itle Page i Dedication ii Abstract iii Acknowledgements iv Contents v List of Figures x Abbreviations xiii References 110 Chapter One : Introduction 1 1.1 Regional specification. 1 1.2 A summary of mouse embryogenesis. 3 1.2.1 Pre-implantation development. 4 1.2.2 Gastrulation and the generation of the body plan. 5 1.3 Strategies towards a molecular understanding of murine development. 9 1.4 Regional specification in Drosophila embryogenesis. 11 1.4.1 The genetics of anteroposterior specification. 11 1.4.2 The genetics of dorsoventral specification. 14 1.4.3 Neurogenesis. 15 1.5 The homeobox. 16 Chapter Two : Material and Methods 19 v 2.1 Buffers and stock solutions. 19 2.2 Bacterial media and antibiotics. 22 2.3 Animals. 22 2.4 Cloning and DNA methods. 22 2.4.1 Bacterial strain. 22 2.4.2 The production of cells competent for transformation. 23 2.4.3 Bacterial transformation. 23 2.4.4 Standard DNA methods. 23 2.4.5 Restriction digests. 24 2.4.6 Agarose gel electrophoresis. 24 2.4.7 Isolation of DNA fragments from gels. 24 2.4.8 Sub-cloning and ligations. 24 2.4.9 Isolation of plasmid DNA- mini prep. 25 2.4.10 Isolation of plasmid DNA- maxi prep. 25 2.4.11 Southern b lo t. 26 2.4.12 Colony screen. 26 2.5 RNA methods. 27 2.5.1 In vitro transcription. 27 2.5.2 Agarose formaldehyde gels. 28 2.5.3 Northern blot. 28 2.5.4 In situ hybridisation. 28 2.6 Sequence comparisons. 30 2.6.1 Sequences used fo r comparisons. 30 2.7 The Hox 3.1 probe 31 Chapter Three: The murine and Drosophila clusters are evolutionary related. 32 3.1 Introduction. 32 3.2 The mouse Hox clusters are related, possibly by duplication. 35 vi 3.3 S im ila ritie s between mouse Hox complexes and those of other vertebrates. 38 3.4 The mouse and Drosophila homeobox gene complexes have common features of organisation. 39 3.5 A common ancestor fo r the mouse and Drosophila homeobox gene complexes. 41 Chapter 4 : Expression of Hox 2 genes along the rostrocaudal axis of the mouse embryo. 45 4.1 General features of murine homeobox gene expression. 45 4.2 Relationship between the clustering of homeoboxes and their expression. 48 4.3 The Hox 2 probes used in in situ hybridisation. 50 4.4 Ordered expression of Hox 2 genes in the central nervous system (CNS). 51 4.5 Correlation between gene order and expression is also evident in other ectodermal derivatives. 56 4.6 Ordered differential expression of Hox 2 genes in mesodermal derivatives. 60 4.7 Discussion: Position of genes within a cluster reflect domains of expression along the rostrocaudal axis for both mouse and Drosophila. 65 4.7.1 Ordered expression in ectoderm. 65 4.7.2 Hox 2 gene expression in the hindbrain and rhombomeres. 66 4.7.3 Hox 2 gene expression in the mesoderm. 68 4.7.4 The anterior boundaries in mesoderm and ectoderm are not coincident. 70 4.7.5 Correlation between gene order and expression is a general aspect of homeobox clusters. 70 vi i Chapter Five : Dynamic Hox 2 gene expression during development of the central nervous system. 72 5.1 Introduction 72 5.2 Hox 2 genes are dorsally restricted at 12.5 days 73 5.3 Hox 2 genes are expressed uniformly across the nerve cord at 10.5 days. 79 5.4 Strong lateral expression of Hox 2 genes at 11.5 days. 79 5.5 Expression of Hox 2 genes reappears ve n tra lly at 14.5 days. 83 5.6 Hox 3.1 is expressed in stripes. 83 5.7 Discussion 86 5.7.1 Hox 2 gene expression correlates with the time and place of the birth of the major classes of spinal neurons. 87 5.7.2 The Hox 2 genes and Hox 3.1 must be responding to d iffe re n t signals. 88 5.7.3 Re-expression ve n tra lly and the sharp dorsal demarcation in the expression patterns. 89 Chapter Six : General discussion 92 6.1 Positions of genes in a cluster reflect domains of expression in the rostrocaudal axis for both mouse and Drosophila. 92 6.2 Evolution of homeobox gene clusters and the evolution of the body plan. 93 6.3 Relationships between the expression patterns of genes 95 from related murine Hox clusters. 6.4 Hox 2 gene expression and the vertebrate head. 96 vi i i 6.5 Hox genes are involved in the interpretation of regional 97 cues. 6.6 Differences between Drosophila and mouse development that 97 could preclude the use of identical genetic mechanisms.
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