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Schmidtea Mediterranea Thesis Open Research Online The Open University’s repository of research publications and other research outputs Epidermis and Re-epithelialization in Schmidtea mediterranea Thesis How to cite: Gumbrys, Aurimas (2017). Epidermis and Re-epithelialization in Schmidtea mediterranea. PhD thesis The Open University. For guidance on citations see FAQs. c 2016 The Author https://creativecommons.org/licenses/by-nc-nd/4.0/ Version: Version of Record Link(s) to article on publisher’s website: http://dx.doi.org/doi:10.21954/ou.ro.0000c71c Copyright and Moral Rights for the articles on this site are retained by the individual authors and/or other copyright owners. For more information on Open Research Online’s data policy on reuse of materials please consult the policies page. oro.open.ac.uk Epidermis and re-epithelialization in Schmidtea mediterranea Aurimas Gumbrys, B.Sc., M.Sc. A thesis submitted in fulfillment of the requirements of the Open University for the Degree of Doctor of Philosophy The Stowers Institute for Medical Research Kansas City, USA an Affiliated Research Center of the Open University, UK 31 Decemer 2016 Abstract Epidermal layer is crucial for organism’s survival as its ability to close the wound is essential for tissue recovery. Planarian epidermis enables animal recovery and survival after virtually any body part amputation. Nevertheless, neither the epidermis nor the mechanisms endowing such a remarkable wound healing capacity is described in detail in planarians. Our work introduces live imaging methodology, which allows following epidermal cells and their response to tissue damage or tissue loss for extended time (hours) and in high resolution. Using our methods, we followed planarian cells live for the first time and in conjunction with electron microscopy analysis we described epidermal cell behaviors during tissue maintenance, response to tissue damage and tissue loss. Our data provides comprehensive description of cellular wound response, wound closure as well as preexisting tissue contribution to tissue restoration. In addition, we performed epidermal expression profile analysis to identify the candidate list of epidermally expressed genes to depict the machinery endowing these epidermal cell behaviors. In the pilot functional (RNAi) screen an array of transcription factors with a tissue maintenance phenotypes were identified. Our work established tools for subsequent functional studies of other epidermal expressed genes and paved the way to dissect the mechanisms of the epidermis’ maintenance and efficient wound healing in planarians. iii Joriui ir Agnei, Brangiausiem mano v Acknowledgements It is ten years since I first entered into a research lab. Five laboratories, four countries and two continents later I am getting ready to finish my studies. It has been a journey through which I was privileged to meet countless inspiring people. Although I will not be able to mention them all, I want to express my gratitude to those who made the most profound influence to my recent personal and professional development. I want to start by thanking my mentor Alejandro Sánchez Alvarado. Meeting him allowed me to discover what is the most important in science – the great joy of exploration. I am thankful to Alejandro for opportunity to join the lab I loved as well as for helping me to find courage to overcome challenges I did not think I was capable to solve. I am grateful to my wife, Agne, with whom I shared this journey from the very beginning. No achievement would mean much if I could not share it with her. She is the best partner and friend and no journey is too long if we travel together. I thank my son Joris for all the beautiful emotions he brought to my life. I am thankful to Sarah Elliott, Kim Tu, Erin Davies, Alessandro Rossi, Li-Chun Chen, Kai Lei and Carrie Adler for all the emotional support they provided. I also want to thank my parents, family and friends I left back in Lithuania. Not being able to see each other was a sacrifice, but they supported me throughout the way. I also want to thank all of my new friends in Kansas City. They made this city feel like home and I cherish moments we shared together. I want to thank my thesis committee members Robb Krumlauf, Matt Gibson and Tatjana Piotrowski, who guided me throughout the project. I want to thank all past and current colleagues for opportunity to learn from them. Thank you, Sarah Elliott, An Zeng, Hanh Vu, Christopher Arnold, Alessandro Rossi, Longhua Guo, Li-Chun Cheng, Carrie Adler, Stephanie Nowotarski, Beth Duncan, Kim Tu, Erin Davies, Kai Lei, Shasha Zhang, Carlos Guerrero, Eric Ross, Wei Wang and others for their insight at my lab meetings. I am thanking Leanne Wiedemann for organizing my graduate studies, Stephanie Nowotarski, Sarah Elliott, Kim Tu, Erin Davies, Hugo Parker, Nishal Patel and Mark Mattingly for helping me to improve my writing skills. I want to thank Melainia McClain and Rhonda Ross for assisting electron microscopy work, Chris Seidel and Stowers molecular biology core for genomic analysis, Jeff Lange for PDMS device fabrication, library staff as well as all the other Stowers Institute members whose work and expertise contributed to this project. vii Table of Contents Abstract ..................................................................................................................................... iii Acknowledgements ......................................................................................................................... vii Table of Contents .............................................................................................................................. ix Table of Figures ............................................................................................................................. xiii Table of Tables ................................................................................................................................. xv Chapter 1 Introduction ...................................................................................................................... 1 1.1 Epidermis – ectodermal epithelia ...................................................................................... 1 1.2 Wound healing across Metazoa ........................................................................................ 2 Cellular wound healing – miniature model for damage repair .................................................. 4 Tissue damage repair across phylogeny: model systems and their adaptations ........................ 5 Wound healing in Cnidarians ..................................................................................................... 6 Wound healing in Ecdysozoa...................................................................................................... 7 The Nematode roundworm Caenorhabditis elegans .............................................................................. 7 The fruitfly Drosophila melanogaster ................................................................................................... 8 Wound healing in vertebrates ................................................................................................... 10 Discussion ................................................................................................................................ 14 1.3 Regeneration ................................................................................................................... 18 1.4 Epidermal role in regeneration ........................................................................................ 19 1.5 Planarians as a model for Lophotrochozoan wound healing ........................................... 20 The intact planarian epidermis ................................................................................................ 20 Epidermal homeostasis ....................................................................................................................... 23 Wound closure .......................................................................................................................... 25 Epidermal regeneration ........................................................................................................... 27 Discussion ................................................................................................................................ 28 Chapter 2 Characterization of S. mediterranea epidermis .......................................................... 31 2.1 General morphology of S. mediterranea epidermis ........................................................ 31 2.2 Response to tissue loss in S. mediterranea ...................................................................... 34 Cellular response to tissue loss (electron microscopy) ............................................................ 35 Wound closure dynamics visualized by SEM............................................................................ 35 ix Wound closure and epidermal regeneration visualized by TEM .............................................. 38 Epidermal tissue reorganization during blastema growth visualized by TEM ......................... 42 Epidermal tissue regeneration visualized by TEM ................................................................... 44 Summary 45 Chapter 3 Live imaging methodology development ...................................................................... 47 3.1 Animal immobilization ..................................................................................................
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