Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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GPCR-bigrams : Enigmatic signaling components in oomycetes
Hoogen, Johan van den; Govers, Francine - \ 2018
PLoS Pathogens 14 (2018)7. - ISSN 1553-7366
Dissecting cellular signaling in Phytophthora
Hoogen, Johan van den - \ 2018
University. Promotor(en): Francine Govers. - Wageningen : Wageningen University - ISBN 9789463438667 - 141
The G-protein γ subunit of Phytophthora infestans is involved in sporangial development
Hoogen, Johan van den; Verbeek-de Kruif, Natalie ; Govers, Francine - \ 2018
Fungal Genetics and Biology 116 (2018). - ISSN 1087-1845 - p. 73 - 82.
G-protein subunit - GPCR - Oomycetes - Phytophthora - Signaling

The oomycete Phytophthora infestans is a notorious plant pathogen with potato and tomato as its primary hosts. Previous research showed that the heterotrimeric G-protein subunits Gα and Gβ have a role in zoospore motility and virulence, and sporangial development, respectively. Here, we present analyses of the gene encoding a Gγ subunit in P. infestans, Pigpg1. The overall similarity of PiGPG1 with non-oomycete Gγ subunits is low, with only the most conserved amino acids maintained, but similarity with its homologs in other oomycetes is high. Pigpg1 is expressed in all life stages and shows a similar expression profile as the gene encoding the Gβ subunit, Pigpb1. To elucidate its function, transformants were generated in which Pigpg1 is silenced or overexpressed and their phenotypes were analyzed. Pigpg1-silenced lines produce less sporangia, which are malformed. Altogether, the results show that PiGPG1 is crucial for proper sporangia development and zoosporogenesis. PiGPG1 is a functional Gγ, and likely forms a dimer with PiGPB1 that mediates signaling.

Phytophthora infestans enzymes and their role in the interaction with its hosts
Schoina, Charikleia - \ 2018
University. Promotor(en): Francine Govers; Klaas Bouwmeester. - Wageningen : Wageningen University - ISBN 9789463432870 - 198
Feeding the 10 billion: sustainabele future proteins
Govers, Coen ; Wichers, Harry - \ 2018
Reduction of obesity and related diseases by targeted nutritional treatment
Henquet, M.G.L. ; Boer, V.C.J. de; Keijer, J. ; Wichers, H.J. ; Govers, C.C.F.M. ; Bastiaan-Net, S. ; Bergervoet, J.H.W. ; Griensven, L.J.L.D. van - \ 2018
With 2.3 billion overweight and 700 million obese adults worldwide in 2015 (WHO), obesity and consequently diabetes type II are among the biggest global health problems. Even though dietary and lifestyle changes may eventually reduce obesity for some individuals, new safe and more efficacious drugs are required for successful weight reduction and treatment of type 2 diabetes in a large proportion of obese individuals. It has been shown that various G-protein coupled receptors (GPCRs) expressed in various tissues such as liver, muscle, pancreatic islets, immune cells and the central nervous system are involved. GPCRs are important targets for food components. The members of this large family of membrane proteins are involved in virtually every physiological process. This study will focus on the interaction between food ligands and GPCRs.
Genome-wide characterization of Phytophthora infestans metabolism : a systems biology approach
Rodenburg, Y.A. ; Seidl, M.F. ; Ridder, D. de; Govers, F. - \ 2018
Molecular Plant Pathology 19 (2018)6. - ISSN 1464-6722 - p. 1403 - 1413.
Genome-scale metabolic models (GEMs) provide a functional view of the complex network of biochemical reactions in the living cell. Initially mainly applied to reconstruct the metabolism of model organisms, the availability of increasingly sophisticated reconstruction methods and more extensive biochemical databases now make it possible to reconstruct GEMs for less well-characterized organisms, and have the potential to unravel the
metabolism in pathogen–host systems. Here, we present a GEM for the oomycete plant pathogen Phytophthora infestans as a first step towards an integrative model with its host. We predict the biochemical reactions in different cellular compartments and investigate the gene–protein–reaction associations in this model to obtain an impression of the biochemical capabilities of
P. infestans . Furthermore, we generate life stage-specific models to place the transcriptomic changes of the genes encoding metabolic enzymes into a functional context. In sporangia and zoospores, there is an overall down-regulation, most strikingly reflected in the fatty acid biosynthesis pathway. To investigate the robustness of the GEM, we simulate gene deletions to predict which enzymes are essential for in vitro growth. This model is an
essential first step towards an understanding of P. infestans and its interactions with plants as a system, which will help to formulate new hypotheses on infection mechanisms and disease prevention.
The ancient link between G-protein-coupled receptors and C-terminal phospholipid kinase domains
Hoogen, D.J. van den; Meijer, Harold J.G. ; Seidl, Michael F. ; Govers, Francine - \ 2018
MBio 9 (2018)1. - ISSN 2161-2129
Cell signaling - G-protein-coupled receptors - Oomycetes - Phospholipid-mediated signaling - Phytophthora
Sensing external signals and transducing these into intracellular responses requires a molecular signaling system that is crucial for every living organism. Two important eukaryotic signal transduction pathways that are often interlinked are G-protein signaling and phospholipid signaling. Heterotrimeric G-protein subunits activated by G-protein-coupled receptors (GPCRs) are typical stimulators of phospholipid signaling enzymes such as phosphatidylinositol phosphate kinases (PIPKs) or phospholipase C (PLC). However, a direct connection between the two pathways likely exists in oomycetes and slime molds, as they possess a unique class of GPCRs that have a PIPK as an accessory domain. In principle, these so-called GPCR-PIPKs have the capacity of perceiving an external signal (via the GPCR domain) that, via PIPK, directly activates downstream phospholipid signaling. Here we reveal the sporadic occurrence of GPCR-PIPKs in all eukaryotic supergroups, except for plants. Notably, all species having GPCR-PIPKs are unicellular microorganisms that favor aquatic environments. Phylogenetic analysis revealed that GPCR-PIPKs are likely ancestral to eukaryotes and significantly expanded in the last common ancestor of oomycetes. In addition to GPCR-PIPKs, we identified five hitherto-unknown classes of GPCRs with accessory domains, four of which are universal players in signal transduction. Similarly to GPCR-PIPKs, this enables a direct coupling between extracellular sensing and downstream signaling. Overall, our findings point to an ancestral signaling system in eukaryotes where GPCR-mediated sensing is directly linked to downstream responses. IMPORTANCE G-protein-coupled receptors (GPCRs) are central sensors that activate eukaryotic signaling and are the primary targets of human drugs. In this report, we provide evidence for the widespread though limited presence of a novel class of GPCRs in a variety of unicellular eukaryotes. These include free-living organisms and organisms that are pathogenic for plants, animals, and humans. The novel GPCRs have a C-terminal phospholipid kinase domain, pointing to a direct link between sensing external signals via GPCRs and downstream intracellular phospholipid signaling. Genes encoding these receptors were likely present in the last common eukaryotic ancestor and were lost during the evolution of higher eukaryotes. We further describe five other types of GPCRs with a catalytic accessory domain, the so-called GPCR-bigrams, four of which may potentially have a role in signaling. These findings shed new light onto signal transduction in microorganisms and provide evidence for alternative eukaryotic signaling pathways.
The Effect of Tomatine on Gene Expression and Cell Monolayer Integrity in Caco-2
Arena, Mattia ; Govers, C.C.F.M. ; Lotti, Concetta ; Ricciardi, Luigi ; Wichers, H.J. ; Mes, J.J. - \ 2018
Molecules 23 (2018)3. - ISSN 1420-3049
More understanding of the risk-benefit effect of the glycoalkaloid tomatine is required to be able to estimate the role it might play in our diet. In this work, we focused on effects towards intestinal epithelial cells based on a Caco-2 model in order to analyze the influence on the cell monolayer integrity and on the expression levels of genes involved in cholesterol/sterol biosynthesis (LDLR), lipid metabolism (NR2F2), glucose and amino acid uptake (SGLT1, PAT1), cell cycle (PCNA, CDKN1A), apoptosis (CASP-3, BMF, KLF6), tight junctions (CLDN4, OCLN2) and cytokine-mediated signaling (IL-8, IL1β, TSLP, TNF-α). Furthermore, since the bioactivity of the compound might vary in the presence of a food matrix and following digestion, the influence of both pure tomatine and in vitro digested tomatine with and without tomato fruit matrix was studied. The obtained results suggested that concentrations <20 µg/mL of tomatine, either undigested or in vitro digested, do not compromise the viability of Caco-2 cells and stimulate cytokine expression. This effect of tomatine, in vitro digested tomatine or in vitro digested tomatine with tomato matrix differs slightly, probably due to variations of bioactivity or bioavailability of the tomatine. The results lead to the hypothesis that tomatine acts as hormetic compound that can induce beneficial or risk toxic effects whether used in low or high dose.
RXLR effector diversity in Phytophthora infestans isolates determines recognition by potato resistance proteins; the case study AVR1 and R1
Du, Y. ; Weide, R. ; Zhao, Z. ; Msimuko, P. ; Govers, F. ; Bouwmeester, K. - \ 2018
Studies in Mycology 89 (2018). - ISSN 0166-0616 - p. 85 - 93.
Effector variation - Effector-triggered immunity (ETI) - Host defence - Late blight disease - Nucleotide-binding and leucine-rich repeat (NLR) protein - Potato resistance
Late blight disease caused by the plant pathogenic oomycete pathogen Phytophthora infestans is one of the most limiting factors in potato production. P. infestans is able to overcome introgressed late blight resistance by adaptation of effector genes. AVR1 is an RXLR effector that triggers immune responses when recognized by the potato resistance protein R1. P. infestans isolates avirulent on R1 plants were found to have AVR1 variants that are recognized by R1. Virulent isolates though, lack AVR1 but do contain a close homologue of AVR1, named A-L, of which all variants escape recognition by R1. Co-expression of AVR1 and R1 in Nicotiana benthamiana results in a hypersensitive response (HR). In contrast, HR is not activated when A-L is co-expressed with R1. AVR1 and A-L are highly similar in structure. They share two W motifs and one Y motif in the C-terminal part but differ in the T-region, a 38 amino acid extension at the carboxyl-terminal tail of AVR1 lacking in A-L. To pinpoint what determines R1-mediated recognition of AVR1 we tested elicitor activity of AVR1 and A-L chimeric and deletion constructs by co-expression with R1. The T-region is important as it enables R1-mediated recognition of A-L, not only when fused to A-L but also via trans-complementation. Yet, AVR1 lacking the T-region is still active as an elicitor of HR, but this activity is lost when certain motifs are swapped with A-L. These data show that A-L circumvents R1 recognition not only because it lacks the T-region, but also because of differences in the conserved C-terminal effector motifs.
Review of the health effects of berries and their phytochemicals on the digestive and immune systems
Govers, Coen ; Kasikci, Muzeyyen Berkel ; Sluis, Addie A. van der; Mes, Jurriaan J. - \ 2018
Nutrition Reviews 76 (2018)1. - ISSN 0029-6643 - p. 29 - 46.
Berry - Digestive system - Immune system - In vivo - Phytochemicals
Berries are generally considered beneficial to health. This health-promoting potential has mainly been ascribed to berries' phytochemical and vitamin content, and little attention has been paid to the potential benefits of berries for the digestive tract, despite this being the first point of contact. In vivo studies that described the health effects of berries on individual parts of the digestive tract (ie, the mouth, esophagus, stomach, small and large intestine, microbiome, and immune system) were reviewed. Immune effects were included because a large part of the immune system is located in the intestine. Beneficial health effects were mainly observed for whole berry extracts, not individual berry components. These effects ranged from support of the immune system and beneficial microbiota to reduction in the number and size of premalignant and malignant lesions. These results demonstrate the potency of berries and suggest berries can serve as a strong adjuvant to established treatments or therapies for a variety of gastrointestinal and immune-related illnesses.
Solanaceous exocyst subunits are involved in immunity to diverse plant pathogens
Du, Yu ; Overdijk, Elysa J.R. ; Berg, Jeroen A. ; Govers, Francine ; Bouwmeester, Klaas - \ 2018
Journal of Experimental Botany 69 (2018)3. - ISSN 0022-0957 - p. 655 - 666.
Basal defence - exocyst complex - exocytosis - gene silencing - phylogenetic analysis - plant resistance - Solanaceous plants - vesicle trafficking
The exocyst, a multiprotein complex consisting of eight subunits, plays an essential role in many biological processes by mediating secretion of post-Golgi-derived vesicles towards the plasma membrane. In recent years, roles for plant exocyst subunits in pathogen defence have been uncovered, largely based on studies in the model plant Arabidopsis. Only a few studies have been undertaken to assign the role of exocyst subunits in plant defence in other plants species, including crops. In this study, predicted protein sequences from exocyst subunits were retrieved by mining databases from the Solanaceous plants Nicotiana benthamiana, tomato, and potato. Subsequently, their evolutionary relationship with Arabidopsis exocyst subunits was analysed. Gene silencing in N. benthamiana showed that several exocyst subunits are required for proper plant defence against the (hemi-)biotrophic plant pathogens Phytophthora infestans and Pseudomonas syringae. In contrast, some exocyst subunits seem to act as susceptibility factors for the necrotrophic pathogen Botrytis cinerea. Furthermore, the majority of the exocyst subunits were found to be involved in callose deposition, suggesting that they play a role in basal plant defence. This study provides insight into the evolution of exocyst subunits in Solanaceous plants and is the first to show their role in immunity against multiple unrelated pathogens.
Food-Derived β-glucans: Polarization towards M1-like macrophages
Graaff, Priscilla de; Laar, Amar van; Tomassen, M.M.M. ; Berrevoets, C. ; Debets, R. ; Govers, C.C.F.M. - \ 2017
Effectievere afweer tegen kanker met voedingsvezels?
Govers, Coen - \ 2017

Onderzoeker van de week: Coen Govers

Seagrass leaf element content : A global overview
Vonk, J.A. ; Smulders, Fee O.H. ; Christianen, Marjolijn J.A. ; Govers, Laura L. - \ 2017
Marine Pollution Bulletin (2017). - ISSN 0025-326X
Environmental adaptation - Evolutionary history - Micronutrients - Plant physiology - Seagrass - Successional stage
Knowledge on the role of seagrass leaf elements and in particular micronutrients and their ranges is limited. We present a global database, consisting of 1126 unique leaf values for ten elements, obtained from literature and unpublished data, spanning 25 different seagrass species from 28 countries. The overall order of average element values in seagrass leaves was Na. >. K. >. Ca. >. Mg. >. S. >. Fe. >. Al. >. Si. >. Mn. >. Zn. Although we observed differences in leaf element content between seagrass families, high intraspecific variation indicated that leaf element content was more strongly determined by environmental factors than by evolutionary history. Early successional species had high leaf Al and Fe content. In addition, seagrass leaf element content also showed correlations with macronutrients (N and P), indicating that productivity also depends on other elements. Expected genomes of additional seagrass species in combination with experiments manipulating (micro)nutrients and environmental drivers might enable us to unravel the importance of various elements to sustain productive and flourishing meadows.
Bomen en plantenverdelgers
Govers, F. - \ 2017
In: Schimmels Stichting Biowetenschappen en Maatschappij (Cahier Biowetenschappen en Maatschappij 4) - ISBN 9789073196889 - p. 29 - 32.
Een plaag voor de landbouw
Govers, F. - \ 2017
In: Schimmels Stichting Biowetenschappen en Maatschappij (Cahier Biowetenschappen en Maatschappij 4) - ISBN 9789073196889 - p. 50 - 55.
Water-soluble polysaccharide extracts from the oyster culinary-medicinal mushroom pleurotus ostreatus (Agaricomycetes) with HMGCR inhibitory activity
Gil-Ramírez, Alicia ; Smiderle, Fhernanda R. ; Morales, Diego ; Govers, Coen ; Synytsya, Andriy ; Wichers, Harry J. ; Iacomini, Marcello ; Soler-Rivas, Cristina - \ 2017
International Journal of Medicinal Mushrooms 19 (2017)10. - ISSN 1521-9437 - p. 879 - 892.
Caco2 - Cholesterol - HMGCR - Medicinal mushrooms - Pleurotus ostreatus - Polysaccharides - β-glucans
Water extracts from Pleurotus ostreatus containing no statins showed 3-hydroxy-3-methyl-glutaryl CoA reductase (HMGCR) inhibitory activity (in vitro) that might be due to specific water-soluble polysaccharides (WSPs); when isolated and deproteinized, increasing concentrations of the WSP extract induced higher inhibition. The WSP extract contained mainly β-glucans, mannogalactans, and glycogen (e.g., α-glucans), although derivatives or fragments with lower molecular weights (between 14 and 3.5 kDa) were present and were able to induce the inhibitory activity. The extract contained more β-(1→3)-glucans than β-(1→3),(1→6)-glucans, and they partially survived digestion and managed to pass through Caco2 cell monolayers to the lower compartment after in vitro digestion and transport experiments. The WSP might also modulate Caco2 membrane integrity.
Blood–brain barrier transport and neuroprotective potential of blackberry-digested polyphenols : an in vitro study
Figueira, Inês ; Tavares, Lucélia ; Jardim, Carolina ; Costa, Inês ; Terrasso, Ana P. ; Almeida, Andreia F. ; Govers, Coen ; Mes, Jurriaan J. ; Gardner, Rui ; Becker, Jörg D. ; McDougall, Gordon J. ; Stewart, Derek ; Filipe, Augusto ; Kim, Kwang S. ; Brites, Dora ; Brito, Catarina ; Brito, M.A. ; Santos, Cláudia N. - \ 2017
European Journal of Nutrition (2017). - ISSN 1436-6207 - p. 1 - 18.
Blackberry - Brain endothelial cells - In vitro digestion - Microarrays - Neuronal cells
Purpose: Epidemiological and intervention studies have attempted to link the health effects of a diet rich in fruits and vegetables with the consumption of polyphenols and their impact in neurodegenerative diseases. Studies have shown that polyphenols can cross the intestinal barrier and reach concentrations in the bloodstream able to exert effects in vivo. However, the effective uptake of polyphenols into the brain is still regarded with some reservations. Here we describe a combination of approaches to examine the putative transport of blackberry-digested polyphenols (BDP) across the blood–brain barrier (BBB) and ultimate evaluation of their neuroprotective effects. Methods: BDP was obtained by in vitro digestion of blackberry extract and BDP major aglycones (hBDP) were obtained by enzymatic hydrolysis. Chemical characterization and BBB transport of extracts were evaluated by LC–MSn. BBB transport and cytoprotection of both extracts was assessed in HBMEC monolayers. Neuroprotective potential of BDP was assessed in NT2-derived 3D co-cultures of neurons and astrocytes and in primary mouse cerebellar granule cells. BDP-modulated genes were evaluated by microarray analysis. Results: Components from BDP and hBDP were shown to be transported across the BBB. Physiologically relevant concentrations of both extracts were cytoprotective at endothelial level and BDP was neuroprotective in primary neurons and in an advanced 3D cell model. The major canonical pathways involved in the neuroprotective effect of BDP were unveiled, including mTOR signaling and the unfolded protein response pathway. Genes such as ASNS and ATF5 emerged as novel BDP-modulated targets. Conclusions: BBB transport of BDP and hBDP components reinforces the health benefits of a diet rich in polyphenols in neurodegenerative disorders. Our results suggest some novel pathways and genes that may be involved in the neuroprotective mechanism of the BDP polyphenol components.
Non-digestible polysaccharides to support the intestinal immune barrier: in vitro models to unravel molecular mechanisms
Tang, Yongfu - \ 2017
University. Promotor(en): Harry Wichers, co-promotor(en): Jurriaan Mes; Coen Govers. - Wageningen : Wageningen University - ISBN 9789463437134 - 166
polysaccharides - health - immunomodulatory properties - homeostasis - intestinal diseases - human nutrition research - polysacchariden - gezondheid - immunomodulerende eigenschappen - homeostase - darmziekten - voedingsonderzoek bij de mens

Non-digestible polysaccharides (NDPs) are considered as important ingredients to support health. Among these health effects, immunomodulatory effects raised interests in the past decade. The intestine is the primary organ that interact with NDPs. The intestinal epithelial cells (IECs) form a dynamic physical barrier and together with associated immune cells determine for a large part our immune homeostasis. Studying the direct interaction between NDPs and intestinal and immune cells could help us to uncover the mechanism by which NDPs exert immunomodulatory effects and how NDPs can differ in this activity. In this thesis, we investigated the immunomodulatory effects of NDPs through interaction with intestinal immune cells using in vitro methods in order to characterise the NDPs and preselect NDPs with differential activity for further in vivo evaluations.

The intestinal immune barrier is formed by various IECs and immune cells, which are introduced and their specific functions discussed in Chapter 1. NDPs could interact directly with both IECs and immune cells that sample in or from the lumen. The majority of IECs are enterocytes and most relevant immune cells responsible for sampling in the lumen have been characterised as macrophages, which leads us to focus on these cell types by in vitro approaches. In addition, basic information on NDPs and current status on health effects of NDPs both in vitro and in vivo are discussed.

In Chapter 2, the direct response of IEC to NDPs stimulation was investigated. IECs form the largest surface of the body that, with a crucial role as barrier also, perform a role in signalling towards immune cells. We used 21-day transwell cultured Caco-2 to resemble the small intestinal enterocytes that form largest part of this intestinal layer. We first characterized the chemical composition of five NDPs which revealed different mono sugar composition, linkages of backbone and side chains and a wide range of MW (from 17 KDa to 2100 KDa). The NDPs could reduce translocation of FITC-Dextran of 4 kDa across the epithelial layer, potentially through physical interference. Gene expression analysis indicated the induction of unique gene expression characteristics in Caco-2 cells upon exposure to different NDPs. An arabinoxylan preparation from wheat and a lentinan-containing extract from shiitake mushrooms showed upregulation of gene expression of the NF-κB family and chemokines CCL20 and CXCL10. Besides these immune related changes by some NDPs, we also observed changes in receptor expression (like TLR2, CD14 and GPCRs) and other pathways, amongst which the cholesterol biosynthesis pathway.

Macrophages, as the resident population of immune cells penetrating between or associating with close contact with the IECs, are generally classified as inflammatory (M1) or as tolerant (M2) macrophages. In Chapter 3, we set up a macrophage differentiation method based on primary blood cells and selected and validated M1 and M2 specific gene expression markers. Next, we analysed the effect when macrophages are exposed to NDPs and compared the resulting macrophages with M1 and M2 macrophages. Based on M1 and M2 markers we identified an alternative subset that we named MNDP. This MNDP was further studied by microarray analysis and revealed a commonly modulated set of genes, involved in migration, metabolic processes, cell cycle, and inflammatory immune function.

In Chapter 4, we further functionally characterize these MNDP in comparison to M1 and M2 macrophages based on a set of functional assays. NDP-treated macrophages showed no IDO activity and showed an inhibited antigen uptake and processing capacity compared to M1 and M2 macrophages. Also their phagocytic capacity was reduced compared to both M1 and M2 macrophages. Furthermore, the alternative expression pattern for NDP-treated macrophages, as demonstrated by gene expression, was confirmed by protein measurements. The signature mix of the chemokines CCL1, CCL5, CCL20, CCL24, CXCL8, and IL1β secreted by MNDP, and in particular when macrophages were treated with Naxus, was shown to induce a recruitment of monocytes.

As macrophage plasticity could be essential for intestinal immune homeostasis, resolving activity of inflammatory responses upon a challenge is important. Besides, redirecting differentiation and function of tolerant macrophages can also be beneficial to the intestinal immune status. In Chapter 5, we analysed plasticity of M1 and M2 macrophages to NDPs exposure. Macrophage plasticity was demonstrated as M1 and M2 could be skewed to an alternative subset indicated by a dedicated set of gene expression markers, selected to characterize M1, M2 and MNDP macrophages. In addition, phagocytosis and antigen processing capacity of both M1 and M2 were decreased by the NDP Naxus. Besides, Naxus could change the secretion of cytokines by macrophages that previously were differentiated towards M1 and M2. For M2, this resulted in an increase of recruitment of monocytes by M2 macrophages.

In Chapter 6, we discussed the important findings in each chapter of this thesis together with current literature, and gave a general perspective on this research line focussing on the immunomodulating activity of NDPs and the direction for future research. We suggested NDPs in terms of Naxus as candidate for guiding investigations in ex vivo and in vivo studies for immunomodulation of intestinal disease.

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