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A NOVEL GAIN of FUNCTION of the <I>IRX1</I> and <I>IRX2</I> GENES DISRUPTS AXIS ELONGATION in the ARAUCA

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A NOVEL GAIN of FUNCTION of the <I>IRX1</I> and <I>IRX2</I> GENES DISRUPTS AXIS ELONGATION in the ARAUCA Clemson University TigerPrints All Dissertations Dissertations 8-2013 A NOVEL GAIN OF FUNCTION OF THE IRX1 AND IRX2 GENES DISRUPTS AXIS ELONGATION IN THE ARAUCANA RUMPLESS CHICKEN Nowlan Freese Clemson University, [email protected] Follow this and additional works at: https://tigerprints.clemson.edu/all_dissertations Part of the Developmental Biology Commons Recommended Citation Freese, Nowlan, "A NOVEL GAIN OF FUNCTION OF THE IRX1 AND IRX2 GENES DISRUPTS AXIS ELONGATION IN THE ARAUCANA RUMPLESS CHICKEN" (2013). All Dissertations. 1198. https://tigerprints.clemson.edu/all_dissertations/1198 This Dissertation is brought to you for free and open access by the Dissertations at TigerPrints. It has been accepted for inclusion in All Dissertations by an authorized administrator of TigerPrints. For more information, please contact [email protected]. A NOVEL GAIN OF FUNCTION OF THE IRX1 AND IRX2 GENES DISRUPTS AXIS ELONGATION IN THE ARAUCANA RUMPLESS CHICKEN A Thesis Presented to the Graduate School of Clemson University In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Biological Sciences by Nowlan Hale Freese August 2013 Accepted by: Dr. Susan C. Chapman, Committee Chair Dr. Lesly A. Temesvari Dr. Matthew W. Turnbull Dr. Leigh Anne Clark Dr. Lisa J. Bain ABSTRACT Caudal dysplasia describes a range of developmental disorders that affect normal development of the lumbar spinal column, sacrum and pelvis. An important goal of the congenital malformation field is to identify the genetic mechanisms leading to caudal deformities. To identify the genetic cause(s) and subsequent molecular mechanisms I turned to an animal model, the rumpless Araucana chicken breed. Araucana fail to form vertebrae beyond the level of the hips. I performed a genome wide association study to identify candidate genomic regions associated with the rumpless phenotype, compared to tailed Araucana. A candidate region of chromosome 2 containing just two genes, IRX1 and IRX2, was identified. In situ hybridization analysis showed that a gain-of-function mutation resulted in both genes being misexpressed at the onset of secondary neurulation in the caudal organizer progenitor population. The caudal progenitor population has a bipotential fate, contributing cells to both mesoderm and neural lineages. This finding is significant because it is the first identified instance of a gain-of-function mutation resulting in axial truncation. The main question that arises from this novel finding is what is the functional mechanism leading to axial truncation? Possibilities include: the effect on the balance of cell fates within the progenitor population, on proliferation and apoptosis, on cell ingression, and the effect on molecular signaling within caudal tissues. Whereas none of these is ii mutually exclusive, I wanted to identify the single molecular event that triggers the cascade of downstream changes that results in axial truncation. I functionally examined each potential to determine the sequence of events in affected Araucana embryos. Based on the results of this study, I propose a model of development where initial misexpression of the two proneural Iroquois gene family members directs the bipotential progenitor population toward the neural lineage. This results in premature reduction of the progenitor population due to 1) the withdrawal of neuralized cells from the cell cycle, 2) reduced ingression of new progenitor cells via the ventral ectodermal ridge 3) reduced proliferation rates resulting in a failure to extend the axis that then results in 4) early termination of axial elongation and widespread apoptosis. In conclusion, I have identified a novel genetic basis for axial truncation that sheds light on the molecular mechanisms operating during secondary neurulation and axial elongation. iii DEDICATION I dedicate this to Robert, Betsy, Warren, Caroline, and Daniella Freese. My accomplishments would not have been made, nor would they have carried the same weight, without the support of those I love. iv ACKNOWLEDGMENTS I would like to thank Dr. Susan C. Chapman for not only her help and guidance over the past 5 years, but her belief in my ability to succeed. It is immeasurable how much I have learned, gained and grown over the course of my Ph.D. Thank you. I would also like to thank everyone on my committee (Dr. Turnbull, Dr. Temesvari, Dr. Bain and Dr. Clark). Each has provided me with a unique perspective on my own work, which has been invaluable over the years. I am extremely grateful for the help of all of my lab members over the past 5 years. You have made my every day brighter. v TABLE OF CONTENTS Page TITLE PAGE .................................................................................................................... i ABSTRACT ..................................................................................................................... ii DEDICATION ................................................................................................................ iv ACKNOWLEDGMENTS ............................................................................................... v LIST OF TABLES ........................................................................................................ viii LIST OF FIGURES ........................................................................................................ ix CHAPTER I. INTRODUCTION ......................................................................................... 1 Morphological processes involved in axis elongation ............................. 1 Morphogenesis of the caudal embryonic axis occurs during posterior axis elongation ......................................................... 4 Differences between primary versus secondary body formation ............................................................................................ 8 Bipotential fate model ............................................................................ 14 Signaling and cell cycling processes involved in axis elongation ......................................................................................... 17 Determination front ................................................................................ 17 Molecular oscillator (clock) is responsible for the timing of somite formation .......................................................................... 21 Termination of axis elongation and somitogenesis ................................ 22 Pathologies involving axis elongation and patterning ........................... 26 Origin and breed characteristics of the Araucana chicken ..................... 29 Identifying candidate region(s) associated with a phenotype ......................................................................................... 32 References .............................................................................................. 37 II. GENOME-WIDE ASSOCIATION MAPPING AND IDENTIFICATION OF CANDIDATE GENES FOR THE RUMPLESS AND EAR-TUFTED TRAITS OF THE ARAUCANA CHICKEN ............... 44 Abstract .................................................................................................. 45 Introduction ............................................................................................ 46 vi Results .................................................................................................... 49 Discussion .............................................................................................. 51 Materials and Methods ........................................................................... 54 Acknowledgements ................................................................................ 55 References .............................................................................................. 56 Figures.................................................................................................... 59 III. A NOVEL GAIN OF FUNCTION OF THE IRX1 AND IRX2 GENES DISRUPTS AXIS ELONGATION IN THE ARAUCANA RUMPLESS CHICKEN ........................................ 63 Abstract .................................................................................................. 64 Introduction ............................................................................................ 65 Materials and Methods ........................................................................... 69 Results .................................................................................................... 74 Discussion .............................................................................................. 87 Acknowledgements ................................................................................ 96 References .............................................................................................. 97 Figures.................................................................................................. 104 Tables ................................................................................................... 122 IV. DISCUSSION ............................................................................................ 123 Analysis of genes in the rumpless haplotype ....................................... 123 iroquois 1 and iroquois 2 homologues ................................................. 124 Bipotential fate choice of the tail progenitor population ..................... 128 Changes in migration and proliferation ............................................... 130 Maintenance of
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