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The Huntingtin CAG Repeats As 'Fine-Tuning Knob' for Protein

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The Huntingtin CAG Repeats As 'Fine-Tuning Knob' for Protein UNIVERSITÀ DEGLI STUDI DI MILANO PhD Course in Molecular and Cellular Biology XXX Cycle The huntingtin CAG repeats as ‘fine-tuning knob’ for protein neural function Raffaele Iennaco PhD Thesis Scientific tutor: Elena Cattaneo Academic year: 2016-2017 SSD: BIO/14 Thesis performed at University of Milan, Department of Biosciences Laboratory of Stem Cell Biology and Pharmacology of Neurodegenerative Diseases Directed by Prof. Elena Cattaneo INDEX ABSTRACT .................................................................................................................................................... 6 1. INTRODUCTION ..................................................................................................................................... 7 1.1 HTT structure and function ....................................................................................................................... 8 1.1.1 HTT gene evolution ................................................................................................................................................... 8 1.1.2 HTT expression and distribution ...................................................................................................................... 11 1.1.3 HTT structure ............................................................................................................................................................ 12 1.1.4 HTT PTMs, proteolysis, and interactors ........................................................................................................ 14 1.1.4 HTT functions ............................................................................................................................................................ 17 HTT in development ........................................................................................................................................................................ 17 HTT regulates tissue maintenance and cell morphology ................................................................................................ 19 HTT in cell survival .......................................................................................................................................................................... 20 1.2 CAG trinucleotide repeats ........................................................................................................................ 22 1.2.1 Simple sequence repeats and their biological meaning .......................................................................... 22 1.2.2 HTT CAG repeats variability in human population ................................................................................... 24 1.3 ESCs: Cell-based platform to study HTT functions ........................................................................... 26 1.3.1 Embryonic Stem Cells (ESCs) ............................................................................................................................. 26 1.3.2 From ESCs to neurons: neural differentiation protocols ........................................................................ 30 1.3.3 Neural rosette formation as in vitro model for neurogenesis .............................................................. 32 2. AIM ........................................................................................................................................................... 35 3. METHODS .............................................................................................................................................. 37 4. RESULTS ................................................................................................................................................. 43 4.1 HTT rosette formation potential is confined to its N-terminal portion ................................... 44 4.2 Generation of cell lines stably expressing mutated versions of the CAG tract ....................... 44 4.3 PolyQ stretch deletion causes defects in rosette formation ......................................................... 47 4.4 PolyQ stretch increases rosette formation in a length-dependent manner ........................... 48 4.5 Interruption of polyQ tract purity reduces in vitro neurulation ................................................ 49 4.6 Pathological HTT polyQ tract impairs neurulation ......................................................................... 50 4.7 PolyQ domain is not involved in the antiapoptotic function of HTT ......................................... 51 4.8 Automatization of rosette assay for high-content analysis .......................................................... 54 4.8.1 Optimization of neural differentiation protocol procedures ................................................................ 54 4.8.2 Automatization of image acquisition and rosette quantification ....................................................... 56 4.8.3 Evaluation of rosette phenotype by automated method ........................................................................ 58 5. DISCUSSION AND CONCLUSIONS .................................................................................................... 61 6. REFERENCES ......................................................................................................................................... 64 5 ABSTRACT Introduction. Huntingtin gene (HTT) encodes for a high molecular weight protein (HTT) that is essential during gastrulation and in forebrain formation. The N-terminal region of the protein has been recently associated to in vitro pro-neurulation activity. This region includes a peculiar CAG repeat stretch whose expansion results in an inherited neurodegenerative disorder named Huntington’s disease (HD). The disease itself, its penetrance and age of onset are dependent on the length of CAG stretch that encodes for a polyglutamine (polyQ) tract. Evolutionary studies showed that this polyQ tract appeared for the first time in echinoderms, then increased in length during deuterostome evolution in parallel to the emergence of progressively more complex nervous systems. Despite these indications, the functional significance of the polyQ variability in normal HTT remains to be explored. Aim. Here we investigate whether the polyQ tract in HTT is biologically active during early neurogenesis. In particular, as a tool to study in vitro neurogenesis, we adopted the rosette assay, an in vitro assay that measures the ability of ES cell-derived neural progenitors to form radial arrangements of columnar cells (named neural rosettes) that mimic neural tube formation in vivo. Additionally, we worked on designing a novel automated method for faster and unbiased quantifications of the rosette phenotype. Methods. We produced a mouse embryonic stem (mES) cell-based platform for complementation assays with HTT N-terminal portion bearing different polyQ repeats, their deletion and substitutions (0Q, 2Q, 4Q, 7Q, 15Q, 128Q, Q3Q(CAA)Q3, and Q3PQ3). The newly generated cells were exposed to a neural induction protocol to assess their rosette formation potential. Results. We report that the pro-neurulation activity, but not the antiapoptotic function, of HTT is impaired by the sole polyQ domain deletion from the N-terminal portion of HTT. Moreover, the CAG tract length affects rosette formation potential in a linear fashion. Conversely, either a pathological CAG expansion or a CAG interruption causes loss of HTT N-terminal pro-neurulation activity. Finally, to further characterize this phenotype in an unbiased and quantitative way, we developed and tested a novel automated system, based on high-content imaging approach that allowed us to pinpoint this trait with unparalleled precision and efficiency. Conclusions. Overall, these results demonstrate that HTT ability to promote rosette formation is linked to a persistent and uninterrupted CAG tract, while HTT antiapoptotic activity lays outside HTT polyQ domain. 6 1. INTRODUCTION 7 Introduction Huntingtin (HTT) is a high molecular weight protein (348kDa) that is encoded by the Huntingtin gene (HTT); also known as IT-15 and maps on chromosome 4. While the human HTT protein (NCBI RefSeq: NP_002102) is 3144 amino acids long, the mouse protein (NP_034544) contains 3120 amino acids. When excluding the differences in their polyglutamine (polyQ) tract and proline-rich domain (PRD), the human and mouse proteins are 91% identical and 95% similar (Ehrnhoefer et al., 2009). An expansion of the CAG repeats (CAGs) within the coding region of the HTT results in an elongated stretch of glutamine (Q) in the HTT N-terminus that causes an inherited autosomal dominant neurodegenerative disorder named Huntington’s disease, HD (HD Collaborative Research Group, 1993). In the non-HD population the CAG triplet is repeated between 9 and 35 times, while an expansion above 36 repeats results in the development of the disease. Rare carriers of 36 to 39 CAGs show a lower penetrance and later onset of the disease compared to those with 40 or more CAGs (McNeil et al., 1997; Quarrell et al., 2007). The neuropathology of HD results in a massive brain neurodegeneration characterized by the prevalent dysfunction and loss of specific neurons (efferent medium spiny neurons) in the striatum of the basal ganglia, which is the principal responsible for the typical HD symptoms (Reiner et al., 1988). However, corticostriatal projection neurons are also particularly affected and a more widespread degeneration of the brain (including
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