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Institute
- Graduate School of Life Sciences (807) (remove)
Sonstige beteiligte Institutionen
- Helmholtz Institute for RNA-based Infection Research (HIRI) (8)
- Rudolf Virchow Center for Integrative and Translational Bioimaging, University of Würzburg (2)
- Universitätsklinikum Münster (2)
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- Biomedical Center Munich, Department of Physiological Chemistry, Ludwig-Maximilians-Universität München (1)
- CAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - the development agency of the Brazilian Federal Government (1)
- Carl-Ludwig-Institut für Physiologie, Universität Leipzig (1)
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Acceleration is a central aim of clinical and technical research in magnetic resonance imaging (MRI) today, with the potential to increase robustness, accessibility and patient comfort, reduce cost, and enable entirely new kinds of examinations. A key component in this endeavor is image reconstruction, as most modern approaches build on advanced signal and image processing. Here, deep learning (DL)-based methods have recently shown considerable potential, with numerous publications demonstrating benefits for MRI reconstruction. However, these methods often come at the cost of an increased risk for subtle yet critical errors. Therefore, the aim of this thesis is to advance DL-based MRI reconstruction, while ensuring high quality and fidelity with measured data. A network architecture specifically suited for this purpose is the variational network (VN). To investigate the benefits these can bring to non-Cartesian cardiac imaging, the first part presents an application of VNs, which were specifically adapted to the reconstruction of accelerated spiral acquisitions. The proposed method is compared to a segmented exam, a U-Net and a compressed sensing (CS) model using qualitative and quantitative measures. While the U-Net performed poorly, the VN as well as the CS reconstruction showed good output quality. In functional cardiac imaging, the proposed real-time method with VN reconstruction substantially accelerates examinations over the gold-standard, from over 10 to just 1 minute. Clinical parameters agreed on average.
Generally in MRI reconstruction, the assessment of image quality is complex, in particular for modern non-linear methods. Therefore, advanced techniques for precise evaluation of quality were subsequently demonstrated.
With two distinct methods, resolution and amplification or suppression of noise are quantified locally in each pixel of a reconstruction. Using these, local maps of resolution and noise in parallel imaging (GRAPPA), CS, U-Net and VN reconstructions were determined for MR images of the brain. In the tested images, GRAPPA delivers uniform and ideal resolution, but amplifies noise noticeably. The other methods adapt their behavior to image structure, where different levels of local blurring were observed at edges compared to homogeneous areas, and noise was suppressed except at edges. Overall, VNs were found to combine a number of advantageous properties, including a good trade-off between resolution and noise, fast reconstruction times, and high overall image quality and fidelity of the produced output. Therefore, this network architecture seems highly promising for MRI reconstruction.
Articular cartilage defects represent one of the most challenging clinical problem for orthopedic surgeons and cartilage damage after trauma can result in debilitating joint pain, functional impairment and in the long-term development of osteoarthritis. The lateral cartilage-cartilage integration is crucial for the long-term success and to prevent further tissue degeneration. Tissue adhesives and sealants are becoming increasingly more popular and can be a beneficial approach in fostering tissue integration, particularly in tissues like cartilage where alternative techniques, such as suturing, would instead introduce further damage. However, adhesive materials still require optimization regarding the maximization of adhesion strength on the one hand and long-term tissue integration on the other hand. In vitro models can be a valuable support in the investigation of potential candidates and their functional mechanisms. For the conducted experiments within this work, an in vitro disc/ring model obtained from porcine articular cartilage tissue was established. In addition to qualitative evaluation of regeneration, this model facilitates the implementation of biomechanical tests to quantify cartilage integration strength. Construct harvesting for histology and other evaluation methods could be standardized and is ethically less questionable compared to in vivo testing. The opportunity of cell culture technique application for the in vitro model allowed a better understanding of cartilage integration processes.
Tissue bonding requires chemical or physical interaction of the adhesive material and the substrate. Adhesive hydrogels can bind to the defect interface and simultaneously fill the gap of irregularly shaped defect voids. Fibrin gels are derived from the physiological blood-clot formation and are clinically applied for wound closure. Within this work, comparisons of different fibrin glue formulations with the commercial BioGlue® were assessed, which highlighted the need for good biocompatibility when applied on cartilage tissue in order to achieve satisfying long-term integration. Fibrin gel formulations can be adapted with regard to their long-term stability and when applied on cartilage disc/ring constructs improved integrative repair is observable. The kinetic of repairing processes was investigated in fibrin-treated cartilage composites as part of this work. After three days in vitro cultivation, deposited extracellular matrix (ECM) was obvious at the glued interface that increased further over time. Interfacial cell invasion from the surrounding native cartilage was detected from day ten of tissue culture. The ECM formation relies on molecular factors, e.g., as was shown representatively for ascorbic acid, and contributes to increasing integration strengths over time. The experiments performed with fibrin revealed that the treatment with a biocompatible adhesive that allows cartilage neosynthesis favors lateral cartilage integration in the long term. However, fibrin has limited immediate bonding strength, which is disadvantageous for use on articular cartilage that is subject to high mechanical stress. The continuing aim of this thesis was to further develop adhesive mechanisms and new adhesive hydrogels that retain the positive properties of fibrin but have an increased immediate bonding strength.
Two different photochemical approaches with the advantage of on-demand bonding were tested. Such treatment potentially eases the application for the professional user. First, an UV light induced crosslinking mechanism was transferred to fibrin glue to provide additional bonding strength. For this, the cartilage surface was functionalized with highly reactive light-sensitive diazirine groups, which allowed additional covalent bonds to the fibrin matrix and thus increased the adhesive strength. However, the disadvantages of this approach were the multi-step bonding reactions, the need for enzymatic pretreatment of the cartilage, expensive reagents, potential UV-light damage, and potential toxicity hazards. Due to the mentioned disadvantages, no further experiments, including long-term culture, were carried out. A second photosensitive approach focused on blue light induced crosslinking of fibrinogen (RuFib) via a photoinitiator molecule instead of using thrombin as a crosslinking mediator like in normal fibrin glue. The used ruthenium complex allowed inter- and intramolecular dityrosine binding of fibrinogen molecules. The advantage of this method is a one-step curing of fibrinogen via visible light that further achieved higher adhesive strengths than fibrin. In contrast to diazirine functionalization of cartilage, the ruthenium complex is of less toxicological concern. However, after in vitro cultivation of the disc/ring constructs, there was a decrease in integration strength. Compared to fibrin, a reduced cartilage synthesis was observed at the defect. It is also disadvantageous that a direct adjustment of the adhesive can only be made via protein concentration, since fibrinogen is a natural protein that has a fixed number of tyrosine binding sites without chemical modification.
An additional cartilage adhesive was developed that is based on a mussel-inspired adhesive mechanism in which reactivity to a variety of substrates is enabled via free DOPA amino acids. DOPA-based adhesion is known to function in moist environments, a major advantage for application on water-rich cartilage tissue surrounded by synovial liquid. Reactive DOPA groups were synthetically attached to a polymer, here POx, to allow easy chemical modifiability, e.g. insertion of hydrolyzable ester motifs for tunable degradation. The possibility of preparing an adhesive hybrid hydrogel of POx in combination with fibrinogen led to good cell compatibility as was similarly observed with fibrin, but with increased immediate adhesive strength. Degradation could be adjusted by the amount of ester linkages on the POx and a direct influence of degradation rates on the development of integration in the in vitro model could be shown.
Hydrogels are well suited to fill defect gaps and immediate integration can be achieved via adhesive properties. The results obtained show that for the success of long-term integration, a good ability of the adhesive to take up synthesized ECM components and cells to enable regeneration is required. The degradation kinetics of the adhesive must match the remodeling process to avoid intermediate loss of integration power and to allow long-term firm adhesion to the native tissue.
Hydrogels are not only important as adhesives for smaller lesions, but also for filling large defect volumes and populating them with cells to produce tissue engineered cartilage. Many different hydrogel types suitable for cartilage synthesis are reported in the literature. A long-term stable fibrin formulation was tested in this work not only as an adhesive but also as a bulk hydrogel construct. Agarose is also a material widely used in cartilage tissue engineering that has shown good cartilage neosynthesis and was included in integration assessment. In addition, a synthetic hyaluronic acid-based hydrogel (HA SH/P(AGE/G)) was used. The disc/ring construct was adapted for such experiments and the inner lumen of the cartilage ring was filled with the respective hydrogel. In contrast to agarose, fibrin and HA-SH/P(AGE/G) gels have a crosslink mechanism that led to immediate bonding upon contact with cartilage during curing. The enhanced cartilage neosynthesis in agarose compared to the other hydrogel types resulted in improved integration during in vitro culture. This shows that for the long-term success of a treatment, remodeling of the hydrogel into functional cartilage tissue is a very high priority. In order to successfully treat larger cartilage defects with hydrogels, new materials with these properties in combination with chemical modifiability and a direct adhesion mechanism are one of the most promising approaches.
In the initiation phase of acute graft-versus-host disease (aGvHD), CD4+ T cells are activated by hematopoietic antigen presenting cells in secondary lymphoid organs whereas in effector phase by non-hematopoietic cells in the small intestine. We hypothesized that alloreactive CD4+ T cells primarily home to the secondary lymphoid organs subsequent to allogeneic hematopoietic cell transplantation in the initiation phase of aGvHD and are activated by the non-hematopoietic lymph node stromal cells via MHC class II. To test this hypothesis, we employed CD4+ T cell-dependent major mismatch aGvHD mouse model to study this correlation.
Upon analyzing the early events following allo-HCT with bioluminescence imaging, flow cytometry and whole-mount light sheet fluorescence microscopy, we found that allogeneic T cells exclusively home to the spleen, lymph nodes and the Peyer’s patches and not to the intestinal lamina propria in the initiation phase of aGvHD. Utilizing mice devoid of partial or complete hematopoietic antigen presentation we could show allogeneic CD4+ T cells activation in the lymphoid organs of MHCIIΔCD11c and MHCIIΔ BM chimeric mice early after allo-HCT. MHCIIΔ BM chimeras failure of thymic negative selection and developing tissue wasting disease upon syn-HCT deemed them unsuitable to study non-hematopoietic antigen presentation in aGvHD. To overcome this challenge, we generated MHCIIΔVav1 mice that lack MHC class II expression on all hematopoietic cells. MHCIIΔVav1 mice were susceptible to aGvHD and LNSCs from these animals activated allogeneic CD4+ T cells in mixed lymphocyte reaction. Likewise, mesenteric lymph nodes from CD11c.DTR mice surgically transplanted into a MHCIIΔ mouse could activate CD4+ T cells in vivo, clearly demonstrating LNSCs as non-hematopoietic APCs of the lymphoid organs.
We specifically target lymph node stromal cell subsets via the Cre/loxP system, we employed single cell RNA sequencing and selected Ccl19 and VE-Cadherin to specifically target the fibroblastic reticular cells and endothelial cells of the lymph nodes respectively. In MHCIIΔCcl19 mice, alloreactive CD4+ T cells activation was discreetly reduced in the initiation phase of aGvHD whereas absence of MHCII on fibroblastic reticular cells resulted in hyper-activation of allogeneic CD4+ T cells leading to poor survival. This phenotype was modulated by the regulatory T cells that were able to rescue H2-Ab1fl mice but not the MHCIIΔCcl19 subsequent to GvHD.
Knock-out of MHCII on endothelial cells MHCIIΔVE Cadherin, resulted only in modest reduction of CD4+ T cells activation in the initiation phase of GvHD, conversely MHCIIΔVE Cadherin mice showed a protective phenotype compared against littermates H2-Ab1fl mice in long-term survival. Furthermore, to pin-point endothelial cells MHCII antigen presentation we generated MHCIIΔVE Cadherin ΔVav1 animals devoid of antigen presentation in both endothelial and hematopoietic compartments. LNSCs from MHCIIΔVE Cadherin ΔVav1 were unable to activate alloreactive CD4+ T cells in mixed lymphocyte reaction.
Altogether, we demonstrate for the first time that MHC class II on the lymph node stromal cells plays a crucial role in the modulation of allogeneic CD4+ T cells in the initiation and later in the effector phase of graft-versus-host-disease.
In the face of threat, animals react with a defensive reaction to avoid or reduce harm. This defensive reaction encompasses apart from behavioral changes also physiological, analgetic, and endocrine adaptations. Nonetheless, most animal studies on fear and anxiety are based on behavioral observations only, disregarding other aspects of the defensive reaction, or integrating their inter-related dynamics only insufficiently. The first part of this thesis aimed in characterizing patterned associations of behavioral and physiological responses, termed integrated defensive states. Analyzing cardiac and behavioral responses in mice undergoing multiple fear and anxiety paradigms revealed a complex and dynamic interaction of those readouts on both, short and long timescales. Microstates, stereotypical combinations of i.e. freezing and decelerating heart rates, are short-lasting and were, in turn, shown to be influenced by slow acting macrostate changes. One of those higher order macrostates, called `rigidity`, was defined as a latent process that constrains the range of momentary displayed heart rate values. Furthermore, integrated defensive states were found to be highly dependent on the cue and the context the animals are confronted with. Importantly, same behavioral observations, i.e. freezing, were associated with distinct cardiac responses, highlighting the importance of multivariate analysis of integrated defensive states. Defensive states are orchestrated by the brain, which has evolved evolutionary conserved survival circuits. A central brain area of these circuits is the periaqueductal gray (PAG) in the midbrain. It plays a pivotal role in mediating defensive states, as it receives signals about external and internal information from multiple brain regions and sends information to both, higher order brain areas as well as to the brainstem ultimately causing the execution of threat responses. In the second part of this thesis, different neuronal circuit elements in the PAG were optically manipulated in order to gain mechanistic insight into the defense network in the brain underlying the previously delineated cardio-behavioral defensive states. Optical activation of glutamatergic PAG neurons evoked heterogeneous, light-intensity dependent responses. However, a further molecular restriction of the glutamatergic neuronal population targeting only Chx10+ neurons, led to a cardio-behavioral state that resembled spontaneous freezing-bradycardia bouts.
In summary, this thesis presents a multivariate description of defensive states, which includes the complex interaction of cardiac and behavioral responses on different timescales and, furthermore, functionally dissects different excitatory and inhibitory PAG circuit elements mediating these defensive states.
The emergence of human induced pluripotent stem cells (iPSCs) and the rise of the clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) gene editing technology innovated the research platform for scientists based on living human pluripotent cells. The revolutionary combination of both Nobel Prize-honored techniques enables direct disease modeling especially for research focused on genetic diseases. To allow the study on mutation-associated pathomechanisms, we established robust human in vitro systems of three inherited cardiomyopathies: arrhythmogenic cardiomyopathy (ACM), dilated cardiomyopathy with juvenile cataract (DCMJC) and dilated cardiomyopathy with ataxia (DCMA).
Sendai virus vectors encoding OCT3/4, SOX2, KLF4, and c-MYC were used to reprogram human healthy control or mutation-bearing dermal fibroblasts from patients to an embryonic state thereby allowing the robust and efficient generation of in total five transgene-free iPSC lines. The nucleofection-mediated CRISPR/Cas9 plasmid delivery in healthy control iPSCs enabled precise and efficient genome editing by mutating the respective disease genes to create isogenic mutant control iPSCs. Here, a PKP2 knock-out and a DSG2 knock-out iPSC line were established to serve as a model of ACM. Moreover, a DNAJC19 C-terminal truncated variant (DNAJC19tv) was established to mimic a splice acceptor site mutation in DNAJC19 of two patients with the potential of recapitulating DCMA-associated phenotypes. In total eight self-generated iPSC lines were assessed matching internationally defined quality control criteria. The cells retained their ability to differentiate into cells of all three germ layers in vitro and maintained a stable karyotype. All iPSC lines exhibited a typical stem cell-like morphology as well as expression of characteristic pluripotency markers with high population purities, thus validating the further usage of all iPSC lines in in vitro systems of ACM, DCMA and DCMJC.
Furthermore, cardiac-specific disease mechanisms underlying DCMA were investigated using in vitro generated iPSC-derived cardiomyocytes (iPSC-CMs). DCMA is an autosomal recessive disorder characterized by life threatening early onset cardiomyopathy associated with a metabolic syndrome. Causal mutations were identified in the DNAJC19 gene encoding an inner mitochondrial membrane (IMM) protein with a presumed function in mitochondrial biogenesis and cardiolipin (CL) remodeling. In total, two DCMA patient-derived iPSC lines (DCMAP1, DCMAP2) of siblings with discordant cardiac phenotypes, a third isogenic mutant control iPSC line (DNAJC19tv) as well as two control lines (NC6M and NC47F) were directed towards the cardiovascular lineage upon response to extracellular specification cues. The monolayer cardiac differentiation approach was successfully adapted for all five iPSC lines and optimized towards ventricular subtype identity, higher population purities and enhanced maturity states to fulfill all DCMA-specific requirements prior to phenotypic investigations. To provide a solid basis for the study of DCMA, the combination of lactate-based metabolic enrichment, magnetic-activated cell sorting, mattress-based cultivation and prolonged cultivation time was performed in an approach-dependent manner. The application of the designated strategies was sufficient to ensure adult-like characteristics, which included at least 60-day-old iPSC-CMs. Therefore, the novel human DCMA platform was established to enable the study of the pathogenesis underlying DCMA with respect to structural, morphological and functional changes.
The disease-associated protein, DNAJC19, is constituent of the TIM23 import machinery and can directly interact with PHB2, a component of the membrane bound hetero-oligomeric prohibitin ring complexes that are crucial for phospholipid and protein clustering in the IMM. DNAJC19 mutations were predicted to cause a loss of the DnaJ interaction domain, which was confirmed by loss of full-length DNAJC19 protein in all mutant cell lines. The subcellular investigation of DNAJC19 demonstrated a nuclear restriction in mutant iPSC-CMs. The loss of DNAJC19 co-localization with mitochondrial structures was accompanied by enhanced fragmentation, an overall reduction of mitochondrial mass and smaller cardiomyocytes. Ultrastructural analysis yielded decreased mitochondria sizes and abnormal cristae providing a link to defects in mitochondrial biogenesis and CL remodeling. Preliminary data on CL profiles revealed longer acyl chains and a more unsaturated acyl chain composition highlighting abnormities in the phospholipid maturation in DCMA.
However, the assessment of mitochondrial function in iPSCs and dermal fibroblasts revealed an overall higher oxygen consumption that was even more enhanced in iPSC-CMs when comparing all three mutants to healthy controls. Excess oxygen consumption rates indicated a higher electron transport chain (ETC) activity to meet cellular ATP demands that probably result from proton leakage or the decoupling of the ETC complexes provoked by abnormal CL embedding in the IMM.
Moreover, in particular iPSC-CMs presented increased extracellular acidification rates that indicated a shift towards the utilization of other substrates than fatty acids, such as glucose, pyruvate or glutamine. The examination of metabolic features via double radioactive tracer uptakes (18F-FDG, 125I-BMIPP) displayed significantly decreased fatty acid uptake in all mutants that was accompanied by increased glucose uptake in one patient cell line only, underlining a highly dynamic preference of substrates between mutant iPSC-CMs.
To connect molecular changes directly to physiological processes, insights on calcium kinetics, contractility and arrhythmic potential were assessed and unraveled significantly increased beating frequencies, elevated diastolic calcium concentrations and a shared trend towards reduced cell shortenings in all mutant cell lines basally and upon isoproterenol stimulation. Extended speed of recovery was seen in all mutant iPSC-CMs but most striking in one patient-derived iPSC-CM model, that additionally showed significantly prolonged relaxation times. The investigations of calcium transient shapes pointed towards enhanced arrhythmic features in mutant cells comprised by both the occurrence of DADs/EADs and fibrillation-like events with discordant preferences.
Taken together, new insights into a novel in vitro model system of DCMA were gained to study a genetically determined cardiomyopathy in a patient-specific manner upon incorporation of an isogenic mutant control. Based on our results, we suggest that loss of full-length DNAJC19 impedes PHB2-complex stabilization within the IMM, thus hindering PHB-rings from building IMM-specific phospholipid clusters. These clusters are essential to enable normal CL remodeling during cristae morphogenesis. Disturbed cristae and mitochondrial fragmentation were observed and refer to an essential role of DNAJC19 in mitochondrial morphogenesis and biogenesis. Alterations in mitochondrial morphology are generally linked to reduced ATP yields and aberrant reactive oxygen species production thereby having fundamental downstream effects on the cardiomyocytes` functionality. DCMA-associated cellular dysfunctions were in particular manifested in excess oxygen consumption, altered substrate utilization and abnormal calcium kinetics. The summarized data highlight the usage of human iPSC-derived CMs as a powerful tool to recapitulate DCMA-associated phenotypes that offers an unique potential to identify therapeutic strategies in order to reverse the pathological process and to pave the way towards clinical applications for a personalized therapy of DCMA in the future.
Motor neuron diseases (MNDs) encompass a variety of clinically and genetically heterogeneous disorders, which lead to the degeneration of motor neurons (MNs) and impaired motor functions. MNs coordinate and control movement by transmitting their signal to a target muscle cell. The synaptic endings of the MN axon and the contact site of the muscle cell thereby form the presynaptic and postsynaptic structures of the neuromuscular junction (NMJ). In MNDs, synaptic dysfunction and synapse elimination precede MN loss suggesting that the NMJ is an early target in the pathophysiological cascade leading to MN death. In this study, we established new experimental strategies to analyze human MNDs by patient derived induced pluripotent stem cells (iPSCs) and investigated pathophysiological mechanisms in two different MNDs.
To study human MNDs, specialized cell culture systems that enable the connection of MNs to their target muscle cells are required to allow the formation of NMJs. In the first part of this study, we established and validated a human neuromuscular co-culture system consisting of iPSC derived MNs and 3D skeletal muscle tissue derived from myoblasts. We generated 3D muscle tissue by culturing primary myoblasts in a defined extracellular matrix in self-microfabricated silicone dishes that support the 3D tissue formation. Subsequently, iPSCs from healthy donors and iPSCs from patients with the progressive MND Amyotrophic Lateral Sclerosis (ALS) were differentiated into MNs and used for 3D neuromuscular co-cultures. Using a combination of immunohistochemistry, calcium imaging, and pharmacological stimulations, we characterized and confirmed the functionality of the 3D muscle tissue and the 3D neuromuscular co-cultures. Finally, we applied this system as an in vitro model to study the pathophysiology of ALS and found a decrease in neuromuscular coupling, muscle contraction, and axonal outgrowth in co-cultures with MNs harboring ALS-linked superoxide dismutase 1 (SOD1) mutation. In summary, this co-culture system presents a human model for MNDs that can recapitulate aspects of ALS pathophysiology.
In the second part of this study, we identified an impaired unconventional protein secretion (UPS) of Sod1 as pathological mechanisms in Pleckstrin homology domain-containing family G member 5 (Plekhg5)-associated MND. Sod1 is a leaderless cytosolic protein which is secreted in an autophagy-dependent manner. We found that Plekhg5 depletion in primary MNs and NSC34 cells leads to an impaired secretion of wildtype Sod1, indicating that Plekhg5 drives the UPS of Sod1 in vitro. By interfering with different steps during the biogenesis of autophagosomes, we could show that Plekhg5-regulated Sod1 secretion is determined by autophagy. To analyze our findings in a clinically more relevant model we utilized human iPSC MNs from healthy donors and ALS patients with SOD1 mutations. We observed reduced SOD1 secretion in ALS MNs which coincides with reduced protein expression of PLEKHG5 compared to healthy and isogenic control MNs. To confirm this correlation, we depleted PLEKHG5 in control MNs and found reduced extracellular SOD1 levels, implying that SOD1 secretion depends on PLEKHG5. In summary, we found that Plekh5 regulates the UPS of Sod1 in mouse and human MNs and that Sod1 secretion occurs in an autophagy dependent manner. Our data shows an unreported mechanistic link between two MND-associated proteins.
The variant surface glycoprotein (VSG) of African trypanosomes plays an essential role in protecting the parasites from host immune factors. These trypanosomes undergo antigenic variation resulting in the expression of a single VSG isoform out of a repertoire of around 2000 genes. The molecular mechanism central to the expression and regulation of the VSG is however not fully understood.
Gene expression in trypanosomes is unusual due to the absence of typical RNA polymerase II promoters and the polycistronic transcription of genes. The regulation of gene expression is therefore mainly post-transcriptional. Regulatory sequences, mostly present in the 3´ UTRs, often serve as key elements in the modulation of the levels of individual mRNAs. In T. brucei VSG genes, a 100 % conserved 16mer motif within the 3´ UTR has been shown to modulate the stability of VSG transcripts and hence their expression. As a stability-associated sequence element, the absence of nucleotide substitutions in the motif is however unusual. It was therefore hypothesised that the motif is involved in other essential roles/processes besides stability of the VSG transcripts.
In this study, it was demonstrated that the 100 % conservation of the 16mer motif is not essential for cell viability or for the maintenance of functional VSG protein levels. It was further shown that the intact motif in the active VSG 3´ UTR is neither required to promote VSG silencing during switching nor is it needed during differentiation from bloodstream forms to procyclic forms. Crosstalk between the VSG and procyclin genes during differentiation to the insect vector stage is also unaffected in cells with a mutated 16mer motif. Ectopic overexpression of a second VSG however requires the intact motif to trigger silencing and exchange of the active VSG, suggesting a role for the motif in transcriptional VSG switching. The 16mer motif therefore plays a dual role in VSG in situ switching and stability of VSG transcripts. The additional role of the 16mer in the essential process of antigenic variation appears to be the driving force for the 100 % conservation of this RNA motif.
A screen aimed at identifying candidate RNA-binding proteins interacting with the 16mer motif, led to the identification of a DExD/H box protein, Hel66. Although the protein did not appear to have a direct link to the 16mer regulation of VSG expression, the DExD/H family of proteins are important players in the process of ribosome biogenesis. This process is relatively understudied in trypanosomes and so this candidate was singled out for detailed characterisation, given that the 16mer story had reached a natural end point. Ribosome biogenesis is a major cellular process in eukaryotes involving ribosomal RNA, ribosomal proteins and several non-ribosomal trans-acting protein factors. The DExD/H box proteins are the most important trans-acting protein factors involved in the biosynthesis of ribosomes. Several DExD/H box proteins have been directly implicated in this process in yeast. In trypanosomes, very few of this family of proteins have been characterised and therefore little is known about the specific roles they play in RNA metabolism. Here, it was shown that Hel66 is involved in rRNA processing during ribosome biogenesis. Hel66 localises to the nucleolus and depleting the protein led to a severe growth defect. Loss of the protein also resulted in a reduced rate of global translation and accumulation of rRNA processing intermediates of both the small and large ribosomal subunits. Hel66 is therefore an essential nucleolar DExD/H protein involved in rRNA processing during ribosome biogenesis. As very few protein factors involved in the processing of rRNAs have been described in trypanosomes, this finding represents an important platform for future investigation of this topic.
Cardiovascular disease is one of the leading causes of death worldwide and, so far, echocardiography, nuclear cardiology, and catheterization are the gold standard techniques used for its detection. Cardiac magnetic resonance (CMR) can replace the invasive imaging modalities and provide a "one-stop shop" characterization of the cardiovascular system by measuring myocardial tissue structure, function and perfusion of the heart, as well as anatomy of and flow in the coronary arteries. In contrast to standard clinical magnetic resonance imaging (MRI) scanners, which are often operated at a field strength of 1.5 or 3 Tesla (T), a higher resolution and subsequent cardiac parameter quantification could potentially be achieved at ultra-high field, i.e., 7 T and above.
Unique insights into the pathophysiology of the heart are expected from ultra-high field MRI, which offers enhanced image quality in combination with novel contrast mechanisms, but suffers from spatio-temporal B0 magnetic field variations. Due to the resulting spatial misregistration and intra-voxel dephasing, these B0-field inhomogeneities generate a variety of undesired image artifacts, e.g., artificial image deformation. The resulting macroscopic field gradients lead to signal loss, because the effective transverse relaxation time T2* is shortened. This affects the accuracy of T2* measurements, which are essential for myocardial tissue characterization. When steady state free precession-based pulse sequences are employed for image acquisition, certain off-resonance frequencies cause signal voids. These banding artifacts complicate the proper marking of the myocardium and, subsequently, systematic errors in cardiac function measurements are inevitable. Clinical MR scanners are equipped with basic shim systems to correct for occurring B0-field inhomogeneities and resulting image artifacts, however, these are not sufficient for the advanced measurement techniques employed for ultra-high field MRI of the heart.
Therefore, this work focused on the development of advanced B0 shimming strategies for CMR imaging applications to correct the spatio-temporal B0 field variations present in the human heart at 7 T. A novel cardiac phase-specific shimming (CPSS) technique was set up, which featured a triggered B0 map acquisition, anatomy-matched selection of the shim-region-of-interest (SROI), and calibration-based B0 field modeling. The influence of technical limitations on the overall spherical harmonics (SH) shim was analyzed. Moreover, benefits as well as pitfalls of dynamic shimming were debated in this study. An advanced B0 shimming strategy was set up and applied in vivo, which was the first implementation of a heart-specific shimming approach in human UHF MRI at the time.
The spatial B0-field patterns which were measured in the heart throughout this study contained localized spots of strong inhomogeneities. They fluctuated over the cardiac cycle in both size and strength, and were ideally addressed using anatomy-matched SROIs. Creating a correcting magnetic field with one shim coil, however, generated eddy currents in the surrounding conducting structures and a resulting additional, unintended magnetic field. Taking these shim-to-shim interactions into account via calibration, it was demonstrated for the first time that the non-standard 3rd-order SH terms enhanced B0-field homogeneity in the human heart. However, they were attended by challenges for the shim system hardware employed in the presented work, which was indicated by the currents required to generate the optimal 3rd-order SH terms exceeding the dynamic range of the corresponding shim coils. To facilitate dynamic shimming updated over the cardiac cycle for cine imaging, the benefit of adjusting the oscillating CPSS currents was found to be vital. The first in vivo application of the novel advanced B0 shimming strategy mostly matched the simulations.
The presented technical developments are a basic requirement to quantitative and functional CMR imaging of the human heart at 7 T. They pave the way for numerous clinical studies about cardiac diseases, and continuative research on dedicated cardiac B0 shimming, e.g., adapted passive shimming and multi-coil technologies.
The reprogramming of metabolic pathways is a hallmark of cancer: Tumour cells are dependent on the supply with metabolites and building blocks to fulfil their increased need as highly proliferating cells. Especially de novo synthesis pathways are upregulated when the cells of the growing tumours are not able to satisfy the required metabolic levels by uptake from the environment.
De novo synthesis pathways are often under the control of master transcription factors which regulate the gene expression of enzymes involved in the synthesis process. The master regulators for de novo fatty acid synthesis and cholesterogenesis are sterol regulatory element-binding proteins (SREBPs). While SREBP1 preferably controls the expression of enzymes involved in fatty acid synthesis, SREBP2 regulates the transcription of the enzymes of the mevalonate pathway and downstream processes namely cholesterol, isoprenoids and building blocks for ubiquinone synthesis.
SREBP activity is tightly regulated at different levels: The post-translational modification by ubiquitination decreases the stability of active SREBPs. The attachment of K48-linked ubiquitin chains marks the transcription factors for the proteasomal degradation. In tumour cells, high levels of active SREBPs are essential for the upregulation of the respective metabolic pathways. The increased stability and activity of SREBPs were investigated in this thesis.
SREBPs are ubiquitinated by the E3 ligase Fbw7 which leads to the subsequential proteolysis of the transcription factors. The work conducted in this thesis identified the counteracting deubiquitination enzyme USP28 which removes the ubiquitin chains from SREBPs and prevents their proteasomal degradation.
It further revealed that the stabilization of SREBP2 by USP28 plays an important role in the context of squamous cancers. Increased USP28 levels are associated with a poor survival in patients with squamous tumour subtypes. It was shown that reduced USP28 levels in cell lines and in vivo result in a decrease of SREBP2 activity and downregulation of the mevalonate pathway. This manipulation led to reduced proliferation and tumour growth.
A direct comparison of adenocarcinomas and squamous cell carcinomas in lung cancer patients revealed an upregulation of USP28 as well as SREBP2 and its target genes. Targeting the USP28-SREBP2 regulatory axis in squamous cell lines by inhibitors also reduced cell viability and proliferation.
In conclusion, this study reports evidence for the importance of the mevalonate pathway regulated by the USP28-SREBP2 axis in tumour initiation and progression of squamous cancer. The combinatorial inhibitor treatment of USP28 and HMGCR, the rate limiting enzyme of the mevalonate pathway, by statins opens the possibility for a targeted therapeutic treatment of squamous cancer patients.
Within this thesis, three main approaches for the assessment and investigation of altered hemodynamics like wall shear stress, oscillatory shear index and the arterial pulse wave velocity in atherosclerosis development and progression were conducted:
1. The establishment of a fast method for the simultaneous assessment of 3D WSS and PWV in the complete murine aortic arch via high-resolution 4D-flow MRI
2. The utilization of serial in vivo measurements in atherosclerotic mouse models using high-resolution 4D-flow MRI, which were divided into studies describing altered hemodynamics in late and early atherosclerosis
3. The development of tissue-engineered artery models for the controllable application and variation of hemodynamic and biologic parameters, divided in native artery models and biofabricated artery models, aiming for the investigation of the relationship between atherogenesis and hemodynamics
Chapter 2 describes the establishment of a method for the simultaneous measurement of 3D WSS and PWV in the murine aortic arch at, using ultra high-field MRI at 17.6T [16], based on the previously published method for fast, self-navigated wall shear stress measurements in the murine aortic arch using radial 4D-phase contrast MRI at 17.6 T [4]. This work is based on the collective work of Dr. Patrick Winter, who developed the method and the author of this thesis, Kristina Andelovic, who performed the experiments and statistical analyses. As the method described in this chapter is basis for the following in vivo studies and undividable into the sub-parts of the contributors without losing important information, this chapter was not split into the single parts to provide fundamental information about the measurement and analysis methods and therefore better understandability for the following studies. The main challenge in this chapter was to overcome the issue of the need for a high spatial resolution to determine the velocity gradients at the vascular wall for the WSS quantification and a high temporal resolution for the assessment of the PWV without prolonging the acquisition time due to the need for two separate measurements. Moreover, for a full coverage of the hemodynamics in the murine aortic arch, a 3D measurement is needed, which was achieved by utilization of retrospective navigation and radial trajectories, enabling a highly flexible reconstruction framework to either reconstruct images at lower spatial resolution and higher frame rates for the acquisition of the PWV or higher spatial resolution and lower frame rates for the acquisition of the 3D WSS in a reasonable measurement time of only 35 minutes. This enabled the in vivo assessment of all relevant hemodynamic parameters related to atherosclerosis development and progression in one experimental session. This method was validated in healthy wild type and atherosclerotic Apoe-/- mice, indicating no differences in robustness between pathological and healthy mice.
The heterogeneous distribution of plaque development and arterial stiffening in atherosclerosis [10, 12], however, points out the importance of local PWV measurements. Therefore, future studies should focus on the 3D acquisition of the local PWV in the murine aortic arch based on the presented method, in order to enable spatially resolved correlations of local arterial stiffness with other hemodynamic parameters and plaque composition.
In Chapter 3, the previously established methods were used for the investigation of changing aortic hemodynamics during ageing and atherosclerosis in healthy wild type and atherosclerotic Apoe-/- mice using the previously established methods [4, 16] based on high-resolution 4D-flow MRI. In this work, serial measurements of healthy and atherosclerotic mice were conducted to track all changes in hemodynamics in the complete aortic arch over time. Moreover, spatially resolved 2D projection maps of WSS and OSI of the complete aortic arch were generated. This important feature allowed for the pixel-wise statistical analysis of inter- and intragroup hemodynamic changes over time and most importantly – at a glance. The study revealed converse differences of local hemodynamic profiles in healthy WT and atherosclerotic Apoe−/− mice, with decreasing longWSS and increasing OSI, while showing constant PWV in healthy mice and increasing longWSS and decreasing OSI, while showing increased PWV in diseased mice. Moreover, spatially resolved correlations between WSS, PWV, plaque and vessel wall characteristics were enabled, giving detailed insights into coherences between hemodynamics and plaque composition. Here, the circWSS was identified as a potential marker of plaque size and composition in advanced atherosclerosis. Moreover, correlations with PWV values identified the maximum radStrain could serve as a potential marker for vascular elasticity. This study demonstrated the feasibility and utility of high-resolution 4D flow MRI to spatially resolve, visualize and analyze statistical differences in all relevant hemodynamic parameters over time and between healthy and diseased mice, which could significantly improve our understanding of plaque progression towards vulnerability. In future studies the relation of vascular elasticity and radial strain should be further investigated and validated with local PWV measurements and CFD.
Moreover, the 2D histological datasets were not reflecting the 3D properties and regional characteristics of the atherosclerotic plaques. Therefore, future studies will include 3D plaque volume and composition analysis like morphological measurements with MRI or light-sheet microscopy to further improve the analysis of the relationship between hemodynamics and atherosclerosis.
Chapter 4 aimed at the description and investigation of hemodynamics in early stages of atherosclerosis. Moreover, this study included measurements of hemodynamics at baseline levels in healthy WT and atherosclerotic mouse models. Due to the lack of hemodynamic-related studies in Ldlr-/- mice, which are the most used mouse models in atherosclerosis research together with the Apoe-/- mouse model, this model was included in this study to describe changing hemodynamics in the aortic arch at baseline levels and during early atherosclerosis development and progression for the first time. In this study, distinct differences in aortic geometries of these mouse models at baseline levels were described for the first time, which result in significantly different flow- and WSS profiles in the Ldlr-/- mouse model. Further basal characterization of different parameters revealed only characteristic differences in lipid profiles, proving that the geometry is highly influencing the local WSS in these models. Most interestingly, calculation of the atherogenic index of plasma revealed a significantly higher risk in Ldlr-/- mice with ongoing atherosclerosis development, but significantly greater plaque areas in the aortic arch of Apoe-/- mice. Due to the given basal WSS and OSI profile in these two mouse models – two parameters highly influencing plaque development and progression – there is evidence that the regional plaque development differs between these mouse models during very early atherogenesis.
Therefore, future studies should focus on the spatiotemporal evaluation of plaque development and composition in the three defined aortic regions using morphological measurements with MRI or 3D histological analyses like LSFM. Moreover, this study offers an excellent basis for future studies incorporating CFD simulations, analyzing the different measured parameter combinations (e.g., aortic geometry of the Ldlr-/- mouse with the lipid profile of the Apoe-/- mouse), simulating the resulting plaque development and composition. This could help to understand the complex interplay between altered hemodynamics, serum lipids and atherosclerosis and significantly improve our basic understanding of key factors initiating atherosclerosis development.
Chapter 5 describes the establishment of a tissue-engineered artery model, which is based on native, decellularized porcine carotid artery scaffolds, cultured in a MRI-suitable bioreactor-system [23] for the investigation of hemodynamic-related atherosclerosis development in a controllable manner, using the previously established methods for WSS and PWV assessment [4, 16]. This in vitro artery model aimed for the reduction of animal experiments, while simultaneously offering a simplified, but completely controllable physical and biological environment. For this, a very fast and gentle decellularization protocol was established in a first step, which resulted in porcine carotid artery scaffolds showing complete acellularity while maintaining the extracellular matrix composition, overall ultrastructure and mechanical strength of native arteries. Moreover, a good cellular adhesion and proliferation was achieved, which was evaluated with isolated human blood outgrowth endothelial cells. Most importantly, an MRI-suitable artery chamber was designed for the simultaneous cultivation and assessment of high-resolution 4D hemodynamics in the described artery models. Using high-resolution 4D-flow MRI, the bioreactor system was proven to be suitable to quantify the volume flow, the two components of the WSS and the radStrain as well as the PWV in artery models, with obtained values being comparable to values found in literature for in vivo measurements. Moreover, the identification of first atherosclerotic processes like intimal thickening is achievable by three-dimensional assessment of the vessel wall morphology in the in vitro models. However, one limitation is the lack of a medial smooth muscle cell layer due to the dense ECM. Here, the utilization of the laser-cutting technology for the generation of holes and / or pits on a microscale, eventually enabling seeding of the media with SMCs showed promising results in a first try and should be further investigated in future studies. Therefore, the proposed artery model possesses all relevant components for the extension to an atherosclerosis model which may pave the way towards a significant improvement of our understanding of the key mechanisms in atherogenesis.
Chapter 6 describes the development of an easy-to-prepare, low cost and fully customizable artery model based on biomaterials. Here, thermoresponsive sacrificial scaffolds, processed with the technique of MEW were used for the creation of variable, biomimetic shapes to mimic the geometric properties of the aortic arch, consisting of both, bifurcations and curvatures. After embedding the sacrificial scaffold into a gelatin-hydrogel containing SMCs, it was crosslinked with bacterial transglutaminase before dissolution and flushing of the sacrificial scaffold. The hereby generated channel was subsequently seeded with ECs, resulting in an easy-to-prepare, fast and low-cost artery model. In contrast to the native artery model, this model is therefore more variable in size and shape and offers the possibility to include smooth muscle cells from the beginning. Moreover, a custom-built and highly adaptable perfusion chamber was designed specifically for the scaffold structure, which enabled a one-step creation and simultaneously offering the possibility for dynamic cultivation of the artery models, making it an excellent basis for the development of in vitro disease test systems for e.g., flow-related atherosclerosis research. Due to time constraints, the extension to an atherosclerosis model could not be achieved within the scope of this thesis. Therefore, future studies will focus on the development and validation of an in vitro atherosclerosis model based on the proposed bi- and three-layered artery models.
In conclusion, this thesis paved the way for a fast acquisition and detailed analyses of changing hemodynamics during atherosclerosis development and progression, including spatially resolved analyses of all relevant hemodynamic parameters over time and in between different groups. Moreover, to reduce animal experiments, while gaining control over various parameters influencing atherosclerosis development, promising artery models were established, which have the potential to serve as a new platform for basic atherosclerosis research.