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The Role of Primary Cilia in Skeletal Muscle

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The Role of Primary Cilia in Skeletal Muscle TECHNISCHE UNIVERSITÄT MÜNCHEN Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt The role of primary cilia in skeletal muscle Lisann Heyner Vollständiger Abdruck der von der Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt der Technischen Universität München zur Erlangung des akademischen Grades Doktors der Naturwissenschaften genehmigten Dissertation. Vorsitzende: Prof. Dr. Nina H. Uhlenhaut Prüfer der Dissertation: 1. Prof. Dr. Martin Hrabé de Angelis 2. Prof. Dr. Gunnar Schotta Die Dissertation wurde am 17.10.2019 bei der Technischen Universität München eingereicht und durch die Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt am 05.05.2020 angenommen. Table of Contents Table of Contents 1 List of Abbreviations ..................................................................................................... 1 2 Abstract ........................................................................................................................ 6 3 Zusammenfassung ....................................................................................................... 7 4 Introduction .................................................................................................................. 8 4.1 Diabetes mellitus and glucose homeostasis ............................................................ 8 4.2 Glucose metabolism and skeletal muscle ................................................................ 9 4.3 Primary cilia are signaling hubs of the cell ..............................................................10 4.4 Ciliopathies ............................................................................................................14 4.5 Myopathies: skeletal muscle atrophy and dystrophy ...............................................17 4.6 Skeletal muscle regeneration .................................................................................21 4.7 Actin remodeling and endocytosis ..........................................................................26 4.8 Aim of the thesis .....................................................................................................29 5 Results ........................................................................................................................30 5.1 Muscle phenotype of the Bbs4 mouse model .........................................................30 5.1.1 Bbs4-/- mice showed decreased skeletal muscle strength ................................31 5.1.2 Generation of an inducible, muscle-specific Ift88 knock-out mouse line ..........33 5.1.3 Ciliary impairment does not induce intramuscular fat accumulation .................37 5.1.4 Bbs4-/- skeletal muscle does not exhibit changes in fiber type composition, atrophy or dystrophy ......................................................................................................39 5.2 Differential gene expression in Bbs4-/- and Bbs4+/+ mice .........................................42 5.2.1 Characterization of Bbs4-/- Soleus based on RNA-Seq candidate genes .........43 5.2.2 Characterization of Bbs4-/- EDL based on RNA-Seq candidate genes .............46 5.3 Ift88 knock-down myoblasts show reduced differentiation efficiency ......................52 5.3.1 Characterization of shIft88-expressing C2C12 myoblasts................................52 5.3.2 Altered Rac1 and Cdc42 activity in Ift88-depleted C2C12 myoblasts ..............54 5.3.3 Increased Notch1 signaling in Ift88-knockdown C2C12 myoblasts ..................57 5.3.4 Differentiation and MyoD expression of C2C12 myoblasts ..............................58 5.3.5 Fusion and differentiation index of Ift88-depleted myoblasts ...........................59 5.3.6 Confirmation of Hh signaling regulation in differentiating myoblasts ................61 6 Discussion ...................................................................................................................63 6.1 The role of ciliary proteins in skeletal muscle..........................................................63 6.1.1 Lean mass and grip strength in Bbs4-/- mice ....................................................63 6.1.2 Fat mass and obesity in Bbs4-/- mice ...............................................................65 6.1.3 Genotype/phenotype correlations of Bbs4-/- mutations ....................................67 6.1.4 Postnatal body size in mouse and human Bbs4-/- ............................................68 Table of Contents 6.2 Ift88 knock-down effects myoblast cell cycle ..........................................................69 6.3 Implication of ciliary impairment on actin remodeling in skeletal muscle .................70 6.4 Primary cilia involvement in myoblast function ........................................................70 6.4.1 Primary cilia involvement in myoblast Notch signaling .....................................70 6.4.2 Primary cilia involvement in myoblast differentiation ........................................72 6.5 Gene editing as a potential treatment of muscle mass loss in ciliopathies ..............76 7 Material and Methods ..................................................................................................78 7.1 Material ..................................................................................................................78 7.1.1 Equipment .......................................................................................................78 7.1.2 Consumables, size standards and serum ........................................................79 7.1.3 Kits and Mastermix ..........................................................................................81 7.1.4 Chemicals .......................................................................................................81 7.1.5 Buffers and solutions .......................................................................................83 7.1.6 Solutions for cell culture ..................................................................................84 7.1.7 Enzymes and inhibitors ...................................................................................85 7.1.8 Antibodies .......................................................................................................85 7.1.9 TaqMan primer ................................................................................................86 7.1.10 Cell line and culture medium ...........................................................................87 7.1.11 Mouse lines .....................................................................................................87 7.2 Methods .................................................................................................................87 7.2.1 Ethical approval ...............................................................................................87 7.2.2 Genotyping of mouse lines ..............................................................................88 7.2.3 Mouse line phenotyping ..................................................................................89 7.2.4 Tissue dissection .............................................................................................90 7.2.5 Cell culture ......................................................................................................90 7.2.6 RNA biochemistry ...........................................................................................93 7.2.7 Protein biochemistry ........................................................................................94 7.2.8 Immunostaining ...............................................................................................95 7.2.9 Statistics ..........................................................................................................97 8 List of Figures and Tables ...........................................................................................98 8.1 List of Schematics ..................................................................................................98 8.2 List of Figures .........................................................................................................98 8.3 List of Tables ..........................................................................................................99 9 References ................................................................................................................ 100 10 Acknowledgements ................................................................................................... 120 11 Attachment: Scientific paper manuscript .................................................................... 121 List of Abbreviations 1 List of Abbreviations µg microgram µl microliter AAV adeno-associated virus Aph1b anterior pharynx defective 1 homolog B APS ammonium persulfate Arl13b ADP ribosylation factor like GTPase 13B Arp2/3 actin-related protein 2/3 ATP adenosine triphosphate Bbs Bardet-Biedl Syndrome BLOC-1 biogenesis of lysosome-related organelles complex-1 BSA bovine serum albumin BW body weight Cdc42 cell division cycle 42 cDNA complementary DNA CME clathrin-mediated endocytosis Cre cyclization recombination CSL CBF1, suppressor of hairless, Lag-1 d day DAPI 4′,6-Diamidin-2-phenylindol DGC dystrophin-glycoprotein complex Dll4 delta like canonical Notch ligand 4 DMD Duchenne Muscular Dystrophy DMEM Dulbecco's modified Eagle's medium DNA deoxyribonucleic acid DPBS Dulbecco's phosphate-buffered
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