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Hair Follicle Transplantation: Implications for Cell Migration and Wound Healing

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Hair Follicle Transplantation: Implications for Cell Migration and Wound Healing Hair Follicle Transplantation: Implications for Cell Migration and Wound Healing Azar Asgari (MD) Submitted in total fulfilment of the requirements for the degree of Doctor of Philosophy Sep 2016 Department of Medicine The University Of Melbourne and O’Brien Institute 2 Abstract Chronic wounds are a major problem in the health care system. The increasing incidence of obesity and diabetes and longer life expectancy are adding to the burden. Treatment options are currently limited indicating needs for new treatment modalities. Impaired innate healing response is the main characteristic of chronic wounds. In recent years, there has been a focus on stem cell therapy and tissue engineering as an alternative treatment for chronic wounds to replace the damaged tissue with cells that possess a normal injury response. The hair follicle’s continuous cycling and their response to trauma stimulation, indicate a strong regenerative potential. It has been shown that hair follicles participate in wound re-epithelialization and respond to skin injury by promoting skin innervation and vascularization. This dissertation explores the potential of hair follicle transplantation to enhance wound healing. It was hypothesized that hair follicle transplantation can promote healing in skin wounds. Whole hair follicle were isolated and re-established in the wound site where they preserved their structure and function. This approach exploits the normal endogenous function of hair follicle cells to enhance skin wound healing. First, a vibrissae follicle transplantation technique was established and optimised in nude mice. Using donor follicles from GFP transgenic mice made it possible to investigate cell trafficking from transplanted follicles during epidermal and dermal repair. Transplanted vibrissae follicles integrated normally into the host epithelium and ninety percent of grafted vibrissae produced a hair shaft. The GFP labelled cells were confined to the transplanted hair follicles and were not found in the interfollicular epidermis. It was then possible to identify migrating hair follicle cells from recipient inter-follicular epidermis in lineage tracing wound experiments. Healing responses were then compared in excisional wounds with and without adjacent transplanted follicles. My findings re-confirmed that hair follicle cells participated in i wound re-epithelialisation. Neighbouring transplanted follicles accelerated wound closure. Wounds adjacent to transplanted follicles also showed four times higher nerve density in the granulation tissue than the wounds without adjacent follicular transplants. There was no significant difference in capillary density and macrophage density in wounds with and without hair transplants. I also conducted a preliminary investigation of incisional wounds perpendicular or parallel to transplanted follicles, to compare hair follicle cell migration from damaged and intact hair follicles. In these experiments, intact hair follicles participated only in the epidermal component of wound healing and cells migrated from transplanted hair follicles to the healing dermis only when the hair follicles were cross-sectioned. The results of this dissertation indicated that re-epithelialization and promotion of innervation were possible mechanisms by which transplanted follicles contributed to wound healing. These findings lay the foundations for using follicular transplantation to promote healing in chronic or neuropathic wounds and peripheral nerve injuries. In addition, damage to hair follicles may be a starting signal for migration and participation of hair follicle cells in the repair of dermis, which may subsequently influence the healing outcome. ii Declaration This is to certify that i. The thesis comprises only my original work towards the Doctor of Philosophy, ii. Due acknowledgment has been made in the text to all other material used; iii. The thesis is less than 100,000 words in length, exclusive of tables and bibliographies. Azar Asgari iii iv Acknowledgements Without the support of many this project would have never come to fruition. Foremost, I would like to express my sincere gratitude to my supervisors, Prof. Rodney Sinclair, Dr. Nicholas Rufaut, Prof. Wayne Morrison, Dr. Rodney Dilley and Ass/Prof. Lesley Jones. I would like to thank my primary supervisor, Prof. Rodney Sinclair for the continuous support of my Ph.D study. His dedication to his work, his immense knowledge and his great research mind has inspired me to strive throughout my Ph.D. I would like to give a heartfelt special thanks to Dr Nicholas Rafaut. Thank you for the intellectual support and discussions, for being patient, motivating and encouraging, and for helping me during the challenging times throughout this journey. I am grateful to Prof. Wayne Morrison, for his time and efforts in supervising me, great mentorship and his intellectual input. I would like to thank Ass/Prof. Rodney Dilley for his guidance and encouragement. I am also thankful to Ass/Prof. Lesley Jones for discussions, and for teaching me the micro-dissection of hair follicle dermal papilla at the beginning of this journey. Although the project changed toward a new direction, learning the fine and dedicated technique of micro-dissection and cell culture taught me the discipline and delicacy needed for laboratory work. I would like to thank staff and students at O’Brien institute and the Department of Dermatology who have provided me with insight and inspiration for this work. I am thankful to my colleagues at the O’Brien Institute, namely Dr. Zerina Lokmic, Effie Keramidaris, Yi-wen Gerrand, Dr. Caroline Taylor, Priya Simakumaran, Jennifer Knowlson, Tiffany Tran, and my fellow postgraduate students Anusha Yazdabadi, , Niloufar Torkamani, and Sholeh Boodhun for their friendship, support and discussions. Special thanks to Jason Palmer and Xiao Lian Han for their great patience and technical assistance with my histology works. v I am thankful to Dr Russel Knudsen for teaching me the hair transplant technique and special thanks to Mr. Mutimer and Dr Ross Farhadieh for the access to hair follicle samples. As the majority of my work consisted of in vivo experiments, it would not have been as successful without the time, patience and professional assistance of Sue McKay, Liliana Pepe, Anna Deftereos and Amanda Rixon of the Experimental Medical and Surgical Unit (EMSU). I am grateful for their kindness, assistance and friendship throughout these past few years. I would also like to thank Dr. Maree Faux from Eliza Hall Institute of Medical Research for the access to GFP transgenic mice. I thank friends who kept me going throughout the years. Special thanks to Ben, Roshana and Alison for their editorial support. Big thanks to my family, my parents, for their unconditional love and support, to my daughters Roshana and Ava, for giving me the strength to complete this marathon. Finally, but most importantly, thank you, Majid, for encouragement, for infinite patience and for always supporting me in every possible way. vi Table of Contents ABSTRACT I DECLARATION III ACKNOWLEDGEMENTS V TABLE OF CONTENTS VII LIST OF PUBLICATIONS AND PRESENTATIONS XI GRANTS AND SCHOLARSHIPS XII LIST OF FIGURES XIII LIST OF TABLES XV ABBREVIATIONS XVI MEASUREMENT AND STATISTICAL SYMBOLS XVI CHAPTER 1 GENERAL INTRODUCTION AND REVIEW 1 1.1 PROBLEM STATEMENT 1 1.2 SKIN ANATOMY AND DEVELOPMENT 4 1.2.1 SKIN ANATOMY 4 1.2.2 SKIN DEVELOPMENT 16 1.3 HAIR FOLLICLE ANATOMY, PHYSIOLOGY AND DEVELOPMENT 21 1.3.1 HAIR FOLLICLE ANATOMY 22 1.3.2 HAIR FIBRE TYPES 29 1.3.3 DEVELOPMENT OF FOLLICULAR UNIT 31 1.3.4 HAIR FOLLICLE DEVELOPMENT 33 1.3.5 HAIR CYCLE 36 1.3.6 CHANGES IN SKIN VASCULARITY AND INNERVATION DURING THE HAIR CYCLE 41 1.4 HAIR FOLLICLE AS A SENSORY ORGAN 43 1.4.1 HAIR FOLLICLE INNERVATION 43 1.4.2 REGULATORY EFFECT OF FOLLICULAR NERVE ON HAIR BIOLOGY 47 1.4.3 NEUROTROPHIC EFFECT OF HAIR FOLLICLE ON PERIPHERAL NERVES 47 1.5 CUTANEOUS STEM CELLS 49 1.5.1 SLOW CYCLING ‘LABEL RETAINING’ STEM CELLS 49 1.5.2 INTERFOLLICULAR STEM CELLS 50 1.5.3 HAIR FOLLICLE EPITHELIAL STEM CELLS 53 1.5.4 HAIR FOLLICLE EPIDERMAL CELLS IN WOUND HEALING 58 1.5.5 HAIR FOLLICLE DERMAL STEM CELLS 61 1.5.6 HAIR FOLLICLE DERMAL CELLS IN WOUND HEALING 64 1.5.7 CELL TRAFFICKING IN HAIR FOLLICLE STEM CELL NICHE 67 1.5.8 HAIR FOLLICLE MELANOCYTE STEM CELLS 68 1.5.9 NEURAL CREST STEM CELLS 69 1.6 WOUND HEALING 72 1.6.1 ACUTE WOUND HEALING 72 1.6.2 CHRONIC WOUND 90 1.6.3 CHRONIC WOUND TREATMENT 97 1.6.4 RODENT WOUND HEALING 104 vii 1.7 HAIR FOLLICLE STEM CELLS AND REGENERATIVE MEDICINE 106 1.7.1 METHODS FOR ISOLATING HAIR FOLLICLE AND HAIR FOLLICLE CELLS 108 1.7.2 HAIR INDUCTION AND RESTORING HAIR GROWTH 109 1.7.3 MULTI-POTENTIAL STEM CELLS 110 1.7.4 SKIN REGENERATION AND WOUND HEALING 112 1.7.5 NERVE REGENERATION AND REPAIR 114 1.7.6 SMOOTH MUSCLE DIFFERENTIATION AND VASCULAR TISSUE ENGINEERING 114 1.7.7 REPROGRAMING HAIR FOLLICLE CELLS 115 1.8 NORMAL PHYSIOLOGIC RESPONSE OF HAIR FOLLICLE TO SKIN WOUNDS 116 1.9 HYPOTHESIS 118 1.10 AIMS, SCOPE AND METHODOLOGY 119 CHAPTER 2 GENERAL MATERIALS AND METHODS 121 2.1 ANIMALS 121 2.1.1 GFP MICE 121 2.2 ASEPTIC TECHNIQUE AND ANAESTHESIA METHODS 122 2.3 BONE MARROW HARVESTING 122 2.4 FLUORESCENCE-ACTIVATED CELL SORTING 123 2.5 HISTOLOGY TISSUE PREPARATION 123 2.5.1 PARAFFIN EMBEDDED TISSUE 123 2.5.2 FROZEN TISSUE PREPARATION 124 2.6 HISTOCHEMICAL STAINING 124 2.7 IMMUNOHISTOCHEMISTRY 126 CHAPTER 3 HAIR FOLLICLE TRANSPLANTATION IN NUDE MICE 135 3.1 INTRODUCTION 135 3.1.1 NUDE MICE 137 3.1.2 HAIR FOLLICLE
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