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The Potential of Amniotic Fluid Stem Cells in Prenatal Gene and Cell Therapy

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The Potential of Amniotic Fluid Stem Cells in Prenatal Gene and Cell Therapy The potential of amniotic fluid stem cells in prenatal gene and cell therapy Sheng-Wen Steven Shaw University College London 2013 A thesis submitted for the degree of Doctor of Philosophy ! 1! Declaration ! ! I, Sheng-Wen Steven Shaw, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. ! 2! Abstract Amniotic fluid stem (AFS) cells can be expanded without feeder layers and can differentiate into mesenchymal and haematopoietic lineages. Long term engraftment has been difficult to achieve after prenatal stem cell transplantation mainly because of allogeneic rejection. Autologous cells could be obtained from amniotic fluid (AF) with minimal risk. My thesis aims to define the potential of human, sheep and mouse AFS cells as an autologous stem cell source for prenatal cell/gene therapy. Using pregnant sheep, I explored using AF mesenchymal stem cells (AFMSCs) and CD34+ cells for autologous in utero therapy. AF was collected under ultrasound- guided amniocentesis in early gestation. Those cells were transduced with enhanced green-fluorescent-protein (GFP) using lentivirus vector. After expansion, transduced AFMSCs were injected into peritoneal cavity of each donor fetal sheep. Widespread transgenic GFP expression was detected in fetal tissue. For looking into haematopoietic potential, I transplanted autologous fresh and frozen CD34+AFS, and bone marrow cells into immunocompromised mice. Sheep CD34+AFS cells formed colonies, and were positive for CD45, but negative for CD14/CD31/CD4/ CD58. Flow cytometric analysis at 3 months showed GFP positive cells in all haematopoietic organs. To prove congenic transplantation is better than allogeneic, I collected AF from YFP+/C57BL/6 mice at E13. CKit+/Lin- cells were injected into peritoneal cavity of every mouse fetus. Peripheral blood engraftment was significantly higher in mice transplanted with congenic, versus allogeneic cells, as was liver and spleen engraftment. Finally, looking ahead to clinical translation, human AF cells could be cultured, transduced, sorted and expanded in vitro by using conditional medium in adherent plates. Xenogeneic transplantation of human Ckit+ AFS cells into fetal mice also showed minimal engraftment in peripheral blood. ! 3! In conclusion, AF derived stem cells are an important source of autologous cells that could have prenatal therapeutic value in cell or cell-based gene therapy in the future. ! 4! Table of contents Declaration .................................................................................................................... 2 Abstract ......................................................................................................................... 3 Table of contents .......................................................................................................... 5 List of Figures ............................................................................................................. 11 List of Tables .............................................................................................................. 16 Publications ................................................................................................................ 18 Acknowledgements .................................................................................................... 19 Selective Abbreviations ............................................................................................. 21 Chapter 1: Introduction ............................................................................................ 24 1.1 The burden of congenital disease ................................................................... 24 1.2 Advantages of prenatal over postnatal therapy for severe life-threatening early onset congenital disease .................................................................................. 25 1.3 Gene therapy ................................................................................................... 26 1.3.1 Vectors for gene therapy .......................................................................... 26 1.3.2 Lentivirus vectors .................................................................................... 28 1.3.3 In utero gene therapy ............................................................................... 29 1.3.4 Translating fetal gene therapy into the clinic .......................................... 30 1.4 Stem cells ........................................................................................................ 30 1.4.1 Stem cells from the fetal liver .................................................................. 31 1.4.2 Stem cells from the placenta .................................................................... 32 1.4.3 Cord blood stem cells .............................................................................. 32 1.4.4 Stem cells derived from amniotic fluid ................................................... 33 1.4.5 CKit+ amniotic fluid stem (AFS) cells .................................................... 34 1.4.6 Amniotic fluid mesenchymal stem cells (AFMSC) ................................ 38 1.5 Autologous, allogeneic and xenogeneic stem cell transplantation ................. 39 1.6 In utero stem cell transplantation .................................................................... 40 1.6.1 Preclinical experiments on in utero stem cell transplantation ................. 40 1.6.2 IUSCT in humans .................................................................................... 41 1.7 Development of the human fetal immune system .......................................... 42 1.8 Clinical applications of post-natal haematopoietic stem cell transplantation and gene transfer ...................................................................................................... 42 1.9 Animal models ................................................................................................ 43 1.9.1 Gestation length ....................................................................................... 44 1.9.2 Maternal fetal cell trafficking .................................................................. 44 1.9.3 Open or ultrasound guided delivery of stem cells to the fetus ................ 45 1.9.4 Route of administration ........................................................................... 46 1.9.5 The development of the immune system in animals ............................... 46 1.10 The concept and clinical applications of amniotic fluid stem cells in prenatal and postnatal autologous transplantation ................................................................. 48 1.11 Clinical applications of amniotic fluid stem cells: Postnatal tissue repair ... 49 1.12 Study aims .................................................................................................... 53 Chapter 2: Material and Methods ............................................................................ 55 2.1 Sheep experiments .......................................................................................... 55 2.1.1 Generation of time mated sheep .............................................................. 55 2.1.2 Sheep anaesthesia and preparation for surgery ........................................ 56 ! 5! 2.1.3 Collection of amniotic fluid at necropsy ................................................. 58 2.1.4 Amniocentesis in sheep ........................................................................... 58 2.1.5 Ultrasound-guided in utero reinjection of transduced amniotic fluid stem cells 59 2.1.6 Follow up after amniocentesis or ultrasound guided reinjection of transduced amniotic fluid stem cells .................................................................... 60 2.1.7 Postmortem examination of sheep and lambs ......................................... 61 2.2 Sheep stem cell culture ................................................................................... 62 2.2.1 Ex vivo expansion of sheep amniotic fluid mesenchymal stem cells ...... 62 2.2.2 Differentiation and characterization of sheep amniotic fluid mesenchymal stem cells ....................................................................................... 63 2.2.3 Isolation and culturing of sheep CD34+ amniotic fluid cells and adult bone marrow cells ................................................................................................ 63 2.3 Mouse experiments ......................................................................................... 65 2.3.1 Generation of pregnant mice and surgical procedures ............................ 65 2.3.2 Experimental mice used ........................................................................... 67 2.3.3 Xenotransplantation to adult NOD-SCID gamma mice using sheep cells 69 2.3.4 Follow up after in utero transplantation and neonatal care ..................... 69 2.3.5 Blood sampling of alive mice .................................................................. 70 2.3.6 Postmortem examination of mice ............................................................ 70 2.4 Mouse stem cell culture .................................................................................. 71 2.4.1 Collection of mouse amniotic fluid and isolation of Ckit+/Lin- AFS cells 71 2.4.2 Culturing and viral transduction of the Ckit+/Lin- AFS cells ................. 72 2.5 Human amniotic fluid collection ...................................................................
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