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Evolution of Vertebrate Cartilage Development

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Evolution of Vertebrate Cartilage Development EVOLUTION OF VERTEBRATE CARTILAGE DEVELOPMENT By GUANGJUN ZHANG A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2007 1 © 2007 GuangJun Zhang 2 To my wife, Li Lei, who provided constant support from China to the US, and to my parents for their encouragement to pursue my goals and dreams. 3 ACKNOWLEDGMENTS I greatly acknowledge the help and support of my advisor, Marty Cohn, who introduced me to a new field, evolution and development, and expanded my ways of thinking about scientific questions. I especially thank him for his patience and tolerance during the whole study period. I really feel privileged to be able to work with Marty. I am also grateful to my supervisory committee (Mike Miyamoto, Brian Harfe, Paul Oh and Steve Phelps) for inspiring discussions and constant support. I especially acknowledge Mike for the time that he spent helping me to conduct the phylogenetic studies. Without his help, I would not have gotten this far on the molecular analysis. I would like to thank James Albert for his great help when I first got into the program. I also want to thank Rob Robins and Griffin Sheehy for the help to adapt myself to Gainesville daily life. I would also thanks Renata Freitas for technical help and stimulating discussion, and Ashley Seifert for manuscript reading. Many thanks go to Larry Page, Rob Robins, Simone Shuster, Ben Olaivar, Gordon Weddle, Gretchen Walker, Nick Holland and Linda Holland for assistance with specimen collection. I would also thank Phyllis Luvalle, Keith Choe, Kelley Hyndman, Justin Havird and David Evans for sharing materials and equipment. Lastly I thank my wife Li Lei for her understanding and unselfish support. I also thank my parents for their encouragement and continuous support. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................4 LIST OF FIGURES .........................................................................................................................8 ABSTRACT...................................................................................................................................10 CHAPTER 1 GENERAL INTRODUCTION..............................................................................................12 Vertebrate Cartilage Structures...............................................................................................12 Tetrapods .........................................................................................................................12 Teleosts............................................................................................................................13 Chondrichthyans..............................................................................................................14 Agnathans........................................................................................................................14 Invertebrates ....................................................................................................................15 Compositions of Vertebrate Cartilage Matrix ........................................................................16 Collagens .........................................................................................................................16 Proteoglycans ..................................................................................................................17 Evolutionary History of Cartilage ..........................................................................................18 Vertebrate Skeletal Development...........................................................................................21 Embryonic Origins and Mesenchymal Condensation .....................................................21 Skeletal Cell Lineage Determination...............................................................................22 Chondrogenesis ...............................................................................................................25 Non-hypertrophic chondrocyte differentiation and proliferation.............................26 Chondrocyte proliferation and hypertrophy.............................................................27 Blood vessel invasion and osteoclast development..................................................35 Complexity of Skeletal Development, Secondary Cartilage and Influences of Epigenetic Factors........................................................................................................36 Summary.................................................................................................................................37 2 LAMPREY TYPE II COLLAGEN AND SOX9 REVEAL AN ANCIENT ORIGIN OF THE VERTEBRATE COLLAGENOUS SKEELTON .........................................................43 Introduction.............................................................................................................................43 Materials and Methods ...........................................................................................................45 Gene Cloning and Sequence Analyses............................................................................45 In Situ Hybridization .......................................................................................................47 Immunohistochemistry....................................................................................................48 Results.....................................................................................................................................48 Lampreys have Two Col2a1 Orthologues.......................................................................48 Col2a1a and Col2a1b are Expressed during Lamprey Chondrogenesis.........................48 Adult Lamprey Cartilage Contains COL2A1 Protein .....................................................50 Upstream of Col2a1: a Lamprey Orthologue of Sox9.....................................................50 5 Sox9 Expression Co-Localizes with Col2a1a and Cola1b in the Developing Skeleton........................................................................................................................51 Discussion...............................................................................................................................51 Molecular Evolution of Lamprey Collagens ...................................................................52 Evolution of Collagen-Based Cartilage...........................................................................53 3 HAGFISH AND LANCELET FIBRILLAR COLLAGENS REVEAL THAT TYPE II COLLAGEN-BASED CARTILAGE EVOLVED IN STEM VERTEBRATES...................64 Introduction.............................................................................................................................64 Materials and Methods ...........................................................................................................65 Animals............................................................................................................................65 Gene Cloning...................................................................................................................65 Sequence Analysis and Molecular Phylogenetics ...........................................................65 Histology, Immunohistochemistry and In Situ Hybridization.........................................67 Results.....................................................................................................................................67 Identification of Col2a1 in Hagfishes .............................................................................67 COL2A1 Localizes to Hagfish Soft Cartilage.................................................................68 AmphiColA is Expressed in the Lancelet Notochord and Neural Tube...........................70 Discussion...............................................................................................................................71 COL2A1-Based Cartilage is a Shared Character of Crown-group Vertebrates ..............71 Did vertebrate Chondrocytes Evolve from the Notochord?............................................72 Clade A fibrillar Collagen Duplication Facilitated Evolution of the Vertebrate Skeleton........................................................................................................................72 4 MOLECULAR IDENTIFICATION OF A SCLEROTOME IN LAMPREYS AND SHARKS: IMPLICATIONS FOR THE ORGIN OF THE VERTEBRAL COLUMN .........81 Introduction.............................................................................................................................81 Materials and Methods ...........................................................................................................84 Fish Embryos...................................................................................................................84 Gene Cloning and Phylogenetic Analysis .......................................................................85 In Situ Hybridization and Cryosections...........................................................................86 Results.....................................................................................................................................87 Isolation and Analysis of Lamprey and
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