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Origins of Animal Cell Adhesion University of Denver Digital Commons @ DU Electronic Theses and Dissertations Graduate Studies 1-1-2018 Origins of Animal Cell Adhesion Jennyfer Mora Mitchell University of Denver Follow this and additional works at: https://digitalcommons.du.edu/etd Part of the Cell Biology Commons, Developmental Biology Commons, Other Ecology and Evolutionary Biology Commons, and the Zoology Commons Recommended Citation Mitchell, Jennyfer Mora, "Origins of Animal Cell Adhesion" (2018). Electronic Theses and Dissertations. 1422. https://digitalcommons.du.edu/etd/1422 This Dissertation is brought to you for free and open access by the Graduate Studies at Digital Commons @ DU. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of Digital Commons @ DU. For more information, please contact [email protected],[email protected]. ORIGINS OF ANIMAL CELL ADHESION __________ A Dissertation Presented to the Faculty of Natural Science and Mathematics University of Denver __________ In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy __________ by Jennyfer Mora Mitchell June 2018 Advisor: Scott A. Nichols, PhD. ©Copyright by Jennyfer Mora Mitchell, 2018 All Rights Reserved Author: Jennyfer Mora Mitchell Title: ORIGINS OF ANIMAL CELL ADHESION Advisor: Scott A. Nichols, PhD. Degree Date: June 2018 Abstract A fundamental requirement for multicellularity is cell adhesion. This includes mechanisms by which cells adhere to each other and to their secreted extracellular matrix (ECM). Two well characterized adhesion complexes in animals include: 1) adherens junctions (AJs), which are involved in cell-cell adhesion and composed of cadherin receptors, p120-, α- and β-catenin, and 2) focal adhesions (FAs), which are involved in cell-ECM adhesion and include proteins such as integrins, vinculin, paxillin, talin and focal adhesion kinase (FAK). The molecular components of AJs are widely conserved in animals, and largely absent in non-animals. In contrast, the molecular components of FAs have more ancient origins and can be traced to the last common ancestor of Holozoa. The wide distribution of these structures in animals suggests that they evolved early, possibly coincident with multicellularity. However, a challenge to this perspective is that previous studies of sponges – a divergent animal lineage – indicated that their tissues are organized primarily by an alternative, sponge- specific cell adhesion complex called the ‘aggregation factor’. But, a recent study in Ephydatia muelleri places the AJ protein β-catenin at AJ-like structures in cell- i cell contacts, and at FA-like structures in the cell-ECM interface. This led us to further examine the focal adhesion proteins vinculin, focal adhesion kinase and integrin in sponges. Our data show that vinculin localizes to both cell-cell and cell-ECM contacts has biochemical and structural properties similar to vertebrate vinculin. These data provide compelling evidence that sponge tissues are indeed organized like epithelia in other animals and support that AJ- and FA-like structures extend to the earliest periods of animal evolution. However, the colocalization of FA-proteins with β-catenin at these structures indicates a fundamental difference between the organization and molecular composition of cell junctions in sponge tissues compared to bilaterian epithelia. This interpretation was functionally examined through pharmacological perturbation of FAK to test for cell-adhesion and cell-migration phenotypes. ii Acknowledgements My most sincere acknowledgments to my advisor Dr Scott Nichols for his instruction, intellectual advice, financial, academic and personal support. Special thanks to our collaborators in Stanford University, Dr Weis, Dr Nelson, Dr Miller, Dr Pokutta, and Dr Lowe, and from the University of California-Santa Cruz, Betsy Steele for allowing us to collect O. pearsei tissues. Many thanks to Dr Knowles and Dr Moon for their instruction and advice on TIRF microscopy, writing and career advising. To Catherine Durso, who advised me on statistical analysis. To Jeff Colgren, for his unconditional support, intellectual advice and effective conversations about the scientific endeavor. To my dissertation committee for their valuable suggestions and support to improve my dissertation. To all the current and former Nichols lab members but specially Shaleigh Smith, Lindsey Ray and Austin Armstrong, also from the Latham, Margittai and multiple Biology labs. The kindest thanks to my career mentors from the University of Denver: Anthea J. Roenn, Dr Sasaki, Dr Hoffmann, Dr Murphy, Dr Morris, Dr Hurtt and from the Richmond University, Dr April and Dr Malcom Hill. As well as many other colleagues that I encountered throughout these years whose names I can’t fit in this page but whose encouragement and example was paramount to complete this degree and to continue doing science and pursue a life in the academia. To the best partner in the business of life, Crheston Mitchell. iii Table of Contents Chapter One: A brief History of Animal Cell Adhesion ............................................... 1 Adhesion molecules in the animal stem-lineage and their precursors ........ 1 Functional evidence of cell adhesion proteins in non-bilaterian animals .... 7 Chapter Two: Molecular Characterization of Cell Junctions in the Freshwater Sponge Ephydatia muelleri ........................................................................................... 13 INTRODUCTION ................................................................................................ 13 METHODS........................................................................................................... 17 Protein Searches and Analysis ............................................................ 17 Molecular Phylogenetics for vinculin family proteins ........................ 18 Live Materials .......................................................................................... 19 Em Vcl, Em FAK and Em ITGB Antibody Production and Western Blot Analysis ............................................................................................ 19 Immunostaining of Ephydatia muelleri juveniles ............................... 23 Quantification of Focal Adhesions in E. muelleri Juveniles ............. 24 Co-IP and Mass Spectrometry ............................................................. 25 Pharmacological inhibition of FAK ....................................................... 27 RESULTS ............................................................................................................ 29 Vinculin-family proteins encoded by the Ephydatia transcriptome . 29 Antibody validations and detection of endogenous binding partners ................................................................................................................... 32 Em Vcl, Em FAK and Em ITGB localize to Focal Adhesion-like structures in the substrate-attachment epithelium ............................ 36 Em Vcl localize to adherens junction-like structures in the attachment epithelium, and in the apical endopinacoderm ............. 44 Collective and individual cell migration in E. muelleri might be governed by different mechanisms ..................................................... 50 DISCUSSION ...................................................................................................... 54 References ...................................................................................................................... 60 Appendix A ...................................................................................................................... 69 Supplemental Figures for Chapter 2 ............................................................... 69 Appendix B ...................................................................................................................... 86 Supplemental Tables for Chapter 2 ................................................................ 86 Appendix C ...................................................................................................................... 93 Antibody validation for Ephydatia muelleri ‘uncharacterized’ vinculin related protein and α-catenin............................................................................ 93 METHODS............................................................................................... 93 RESULS................................................................................................... 99 Appendix D .................................................................................................................... 106 iv Preliminary characterization of the roles of Salpingoeca rosetta vinculin homolog ............................................................................................................. 106 INTRODUCTION .................................................................................. 106 METHODS............................................................................................. 108 RESULTS .............................................................................................. 113 Appendix E .................................................................................................................... 123 Antibody validation and immunostaining for Oscarella pearsei vinculin homolog ............................................................................................................. 123 INTRODUCTION .................................................................................
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