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Tessa Gryp
Nephrology Division, Ghent University Hospital and Ghent University, 9000 Ghent, Belgium

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Journal article
Published: 01 June 2020 in Kidney International
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Chronic kidney disease (CKD) is characterized by accumulation of protein-bound uremic toxins such as p-cresyl sulfate, p-cresyl glucuronide, indoxyl sulfate and indole-3-acetic acid, which originate in the gut. Intestinal bacteria metabolize aromatic amino acids into p-cresol and indole, (further conjugated in the colon mucosa and liver) and indole-3-acetic acid. Here we measured fecal, plasma and urine metabolite concentrations; the contribution of gut bacterial generation to plasma protein-bound uremic toxins accumulation; and influx into the gut of circulating protein-bound uremic toxins at different stages of CKD. Feces, blood and urine were collected from 14 control individuals and 141 patients with CKD. Solutes were quantified by ultra-high performance liquid chromatography. To assess the rate of bacterial generation of p-cresol, indole and indole-3-acetic acid, fecal samples were cultured ex vivo. With CKD progression, an increase in protein-bound uremic toxins levels was observed in plasma, whereas the levels of these toxins and their precursors remained the same in feces and urine. Anaerobic culture of fecal samples showed no difference in ex vivo p-cresol, indole and indole-3-acetic acid generation. Therefore, differences in plasma protein-bound uremic toxins levels between different CKD stages cannot be explained by differences in bacterial generation rates in the gut, suggesting retention due to impaired kidney function as the main contributor to their increased plasma levels. Thus, as fractional clearance decreased with the progression of CKD, tubular clearance appeared to be more affected than the glomerular filtration rate, and there was no net increase in protein-bound uremic toxins influx into the gut lumen with increased plasma levels.

ACS Style

Tessa Gryp; Kim De Paepe; Raymond Vanholder; Frederiek-Maarten Kerckhof; Wim Van Biesen; Tom Van de Wiele; Francis Verbeke; Marijn Speeckaert; Marie Joossens; Marie Madeleine Couttenye; Mario Vaneechoutte; Griet Glorieux. Gut microbiota generation of protein-bound uremic toxins and related metabolites is not altered at different stages of chronic kidney disease. Kidney International 2020, 97, 1230 -1242.

AMA Style

Tessa Gryp, Kim De Paepe, Raymond Vanholder, Frederiek-Maarten Kerckhof, Wim Van Biesen, Tom Van de Wiele, Francis Verbeke, Marijn Speeckaert, Marie Joossens, Marie Madeleine Couttenye, Mario Vaneechoutte, Griet Glorieux. Gut microbiota generation of protein-bound uremic toxins and related metabolites is not altered at different stages of chronic kidney disease. Kidney International. 2020; 97 (6):1230-1242.

Chicago/Turabian Style

Tessa Gryp; Kim De Paepe; Raymond Vanholder; Frederiek-Maarten Kerckhof; Wim Van Biesen; Tom Van de Wiele; Francis Verbeke; Marijn Speeckaert; Marie Joossens; Marie Madeleine Couttenye; Mario Vaneechoutte; Griet Glorieux. 2020. "Gut microbiota generation of protein-bound uremic toxins and related metabolites is not altered at different stages of chronic kidney disease." Kidney International 97, no. 6: 1230-1242.

Review
Published: 11 April 2020 in Toxins
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Several of the uremic toxins, which are difficult to remove by dialysis, originate from the gut bacterial metabolism. This opens opportunities for novel targets trying to decrease circulating levels of these toxins and their pathophysiological effects. The current review focuses on immunomodulatory effects of these toxins both at their side of origin and in the circulation. In the gut end products of the bacterial metabolism such as p-cresol, trimethylamine and H2S affect the intestinal barrier structure and function while in the circulation the related uremic toxins stimulate cells of the immune system. Both conditions contribute to the pro-inflammatory status of patients with chronic kidney disease (CKD). Generation and/or absorption of these toxin precursors could be targeted to decrease plasma levels of their respective uremic toxins and to reduce micro-inflammation in CKD.

ACS Style

Griet Glorieux; Tessa Gryp; Alessandra Perna. Gut-Derived Metabolites and Their Role in Immune Dysfunction in Chronic Kidney Disease. Toxins 2020, 12, 245 .

AMA Style

Griet Glorieux, Tessa Gryp, Alessandra Perna. Gut-Derived Metabolites and Their Role in Immune Dysfunction in Chronic Kidney Disease. Toxins. 2020; 12 (4):245.

Chicago/Turabian Style

Griet Glorieux; Tessa Gryp; Alessandra Perna. 2020. "Gut-Derived Metabolites and Their Role in Immune Dysfunction in Chronic Kidney Disease." Toxins 12, no. 4: 245.

Journal article
Published: 14 March 2020 in International Journal of Molecular Sciences
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In chronic kidney disease (CKD), impaired kidney function results in accumulation of uremic toxins, which exert deleterious biological effects and contribute to inflammation and cardiovascular morbidity and mortality. Protein-bound uremic toxins (PBUTs), such as p-cresyl sulfate, indoxyl sulfate and indole-3-acetic acid, originate from phenolic and indolic compounds, which are end products of gut bacterial metabolization of aromatic amino acids (AAA). This study investigates gut microbial composition at different CKD stages by isolating, identifying and quantifying PBUT precursor-generating bacteria. Fecal DNA extracts from 14 controls and 138 CKD patients were used to quantify total bacterial number and 11 bacterial taxa with qPCR. Moreover, isolated bacteria from CKD 1 and CKD 5 fecal samples were cultured in broth medium supplemented with AAA under aerobic and anaerobic conditions, and classified as PBUT precursor-generators based on their generation capacity of phenolic and indolic compounds, measured with U(H)PLC. In total, 148 different fecal bacterial species were isolated, of which 92 were PBUT precursor-generators. These bacterial species can be a potential target for reducing PBUT plasma levels in CKD. qPCR indicated lower abundance of short chain fatty acid-generating bacteria, Bifidobacterium spp. and Streptococcus spp., and higher Enterobacteriaceae and E. coli with impaired kidney function, confirming an altered gut microbial composition in CKD.

ACS Style

Tessa Gryp; Geert R.B. Huys; Marie Joossens; Wim Van Biesen; Griet Glorieux; Mario Vaneechoutte. Isolation and Quantification of Uremic Toxin Precursor-Generating Gut Bacteria in Chronic Kidney Disease Patients. International Journal of Molecular Sciences 2020, 21, 1986 .

AMA Style

Tessa Gryp, Geert R.B. Huys, Marie Joossens, Wim Van Biesen, Griet Glorieux, Mario Vaneechoutte. Isolation and Quantification of Uremic Toxin Precursor-Generating Gut Bacteria in Chronic Kidney Disease Patients. International Journal of Molecular Sciences. 2020; 21 (6):1986.

Chicago/Turabian Style

Tessa Gryp; Geert R.B. Huys; Marie Joossens; Wim Van Biesen; Griet Glorieux; Mario Vaneechoutte. 2020. "Isolation and Quantification of Uremic Toxin Precursor-Generating Gut Bacteria in Chronic Kidney Disease Patients." International Journal of Molecular Sciences 21, no. 6: 1986.

Research article
Published: 21 February 2020 in PLOS ONE
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RNA quality and quantity are important factors for ensuring the accuracy of gene expression analysis and other RNA-based downstream applications. Thus far, only a limited number of methodological studies have compared sample storage and RNA extraction procedures for human cells. We compared three commercially available RNA extraction kits, i.e., (NucliSENS) easyMAG, RNeasy (Mini Kit) and RiboPure (RNA Purification Kit–blood). In addition, additional conditions, such as storage medium and storage temperature of human peripheral blood mononuclear cells were evaluated, i.e., 4 °C for RNAlater or -80 °C for QIAzol and for the respective cognate lysis buffers; easyMAG, RNeasy or RiboPure. RNA was extracted from aliquots that had been stored for one day (Run 1) or 83 days (Run 2). After DNase treatment, quantity and quality of RNA were assessed by means of a NanoDrop spectrophotometer, 2100 Bioanalyzer and RT-qPCR for the ACTB reference gene. We observed that high-quality RNA can be obtained using RNeasy and RiboPure, regardless of the storage medium, whereas samples stored in RNAlater resulted in the least amount of RNA extracted. In addition, RiboPure combined with storage of samples in its cognate lysis buffer yielded twice as much RNA as all other procedures. These results were supported by RT-qPCR and by the reproducibility observed for two independent extraction runs.

ACS Style

Antonio Rodríguez; Hans Duyvejonck; Jonas D. Van Belleghem; Tessa Gryp; Leen Van Simaey; Stefan Vermeulen; Els Van Mechelen; Mario Vaneechoutte. Comparison of procedures for RNA-extraction from peripheral blood mononuclear cells. PLOS ONE 2020, 15, e0229423 .

AMA Style

Antonio Rodríguez, Hans Duyvejonck, Jonas D. Van Belleghem, Tessa Gryp, Leen Van Simaey, Stefan Vermeulen, Els Van Mechelen, Mario Vaneechoutte. Comparison of procedures for RNA-extraction from peripheral blood mononuclear cells. PLOS ONE. 2020; 15 (2):e0229423.

Chicago/Turabian Style

Antonio Rodríguez; Hans Duyvejonck; Jonas D. Van Belleghem; Tessa Gryp; Leen Van Simaey; Stefan Vermeulen; Els Van Mechelen; Mario Vaneechoutte. 2020. "Comparison of procedures for RNA-extraction from peripheral blood mononuclear cells." PLOS ONE 15, no. 2: e0229423.

Original article
Published: 08 February 2020 in Journal of Applied Microbiology
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Aim To determine the most effective DNA extraction method for bacteria in fecal samples. Materials and Results This study assessed five commercial methods, i.e. NucliSens easyMag, QIAamp DNA Stool Mini kit, PureLink Microbiome DNA purification kit, QIAamp PowerFecal DNA kit, and RNeasy PowerMicrobiome kit, of which the latter has been optimized for DNA extraction. The DNA quantity and quality were determined using Nanodrop, Qubit and qPCR. The PowerMicrobiome kit recovered the highest DNA concentration, whereby this kit also recovered the highest gene copy number of Gram‐positives, Gram‐negatives and total bacteria. Furthermore, the PowerMicrobiome kit in combination with mechanical pre‐treatment (bead beating) and with combined enzymatic and mechanical pre‐treatment (proteinase K+mutanolysin+bead beating) was more effective than without pre‐treatment. Conclusion From the five DNA extraction methods that were compared, the PowerMicrobiome kit, preceded by bead beating, which is standard included, was found to be the most effective DNA extraction method for bacteria in fecal samples. Significance and impact of the study The quantity and quality of DNA extracted from human fecal samples is a first important step to optimize molecular methods. Here we have shown that the PowerMicrobiome kit is an effective DNA extraction method for bacterial cells in fecal samples for downstream qPCR purpose.

ACS Style

Tessa Gryp; Griet Glorieux; Marie Joossens; Mario Vaneechoutte. Comparison of five assays for DNA extraction from bacterial cells in human faecal samples. Journal of Applied Microbiology 2020, 129, 378 -388.

AMA Style

Tessa Gryp, Griet Glorieux, Marie Joossens, Mario Vaneechoutte. Comparison of five assays for DNA extraction from bacterial cells in human faecal samples. Journal of Applied Microbiology. 2020; 129 (2):378-388.

Chicago/Turabian Style

Tessa Gryp; Griet Glorieux; Marie Joossens; Mario Vaneechoutte. 2020. "Comparison of five assays for DNA extraction from bacterial cells in human faecal samples." Journal of Applied Microbiology 129, no. 2: 378-388.

Journal article
Published: 25 September 2019 in Scientific Reports
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To determine phage titers accurately, reproducibly and in a non-laborious and cost-effective manner, we describe the development of a qPCR platform for molecular quantification of five phages present in bacteriophage cocktail 2 (BFC2). We compared the performance of this molecular approach, with regard to quantification and reproducibility, with the standard culture-based double agar overlay method (DAO). We demonstrated that quantification of each of the five phages in BFC2 was possible by means of qPCR, without prior DNA extraction, but yields were significantly higher in comparison to DAO. Although DAO is assumed to provide an indication of the number of infective phage particles, whereas qPCR only provides information on the number of phage genomes, the difference in yield (qPCR/DAO ratio) was observed to be phage-dependent and appeared rather constant for all phages when analyzing different (freshly prepared) stocks of these phages. While DAO is necessary to determine sensitivity of clinical strains against phages in clinical applications, qPCR might be a valid alternative for rapid and reproducible quantification of freshly prepared stocks, after initial establishment of a correction factor towards DAO.

ACS Style

Hans Duyvejonck; Maya Merabishvili; Jean-Paul Pirnay; Daniel De Vos; Gilbert Verbeken; Jonas Van Belleghem; Tessa Gryp; Julie De Leenheer; Kelly Van Der Borght; Leen Van Simaey; Stefan Vermeulen; Els Van Mechelen; Mario Vaneechoutte. Development of a qPCR platform for quantification of the five bacteriophages within bacteriophage cocktail 2 (BFC2). Scientific Reports 2019, 9, 1 -10.

AMA Style

Hans Duyvejonck, Maya Merabishvili, Jean-Paul Pirnay, Daniel De Vos, Gilbert Verbeken, Jonas Van Belleghem, Tessa Gryp, Julie De Leenheer, Kelly Van Der Borght, Leen Van Simaey, Stefan Vermeulen, Els Van Mechelen, Mario Vaneechoutte. Development of a qPCR platform for quantification of the five bacteriophages within bacteriophage cocktail 2 (BFC2). Scientific Reports. 2019; 9 (1):1-10.

Chicago/Turabian Style

Hans Duyvejonck; Maya Merabishvili; Jean-Paul Pirnay; Daniel De Vos; Gilbert Verbeken; Jonas Van Belleghem; Tessa Gryp; Julie De Leenheer; Kelly Van Der Borght; Leen Van Simaey; Stefan Vermeulen; Els Van Mechelen; Mario Vaneechoutte. 2019. "Development of a qPCR platform for quantification of the five bacteriophages within bacteriophage cocktail 2 (BFC2)." Scientific Reports 9, no. 1: 1-10.

Postscript
Published: 07 November 2018 in Gut
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In the recent paper by Chu and colleagues,1 the potential role of microbiota-related metabolites in the progression of non-alcoholic fatty liver disease is discussed. This topic has been studied in the context of chronic kidney disease (CKD), characterised by changes in gut microbiota composition,2 accumulation of microbiota-derived metabolites,3 interruption of intestinal barrier function and chronic inflammation.4 In line with this, we focused, in a cohort of 17 patients with end-stage kidney disease (ESKD), on the role of gut microbiota in the generation of precursors of specific uraemic toxins which are associated with negative outcomes in these patients.5 By collecting multiple samples over time, assessment of variability within and between patients in relation to disease progress and clinical variables was possible. Faecal and serum samples were collected at eight time-points over a 4-month period (online supplementary table 1). Uraemic metabolites and microbial profiling were determined by HPLC and 16S rRNA amplicon sequencing, respectively (see Supplementary data). Variation in microbial profiles of patients with ESKD was compared with that of 1106 subjects from a population-based cohort, the Flemish Gut Flora Project (FGFP),6 which have a similar genetic and environmental background as well as to a subset of age-matched controls of comparable health status (n=32). ### Supplementary data [gutjnl-2018-317561-SP1.pdf] In this longitudinal study, within-patient analyses showed that variations in peripheral levels of p -cresyl conjugates (the composite of p -cresyl sulfate (pCS)/glucuronide (pCG); p C), indoxyl sulfate (IxS), indole acetic acid and …

ACS Style

Marie Joossens; Karoline Faust; Tessa Gryp; Anh Thi Loan Nguyen; Jun Wang; Sunny Eloot; Eva Schepers; Annemieke Dhondt; Anneleen Pletinck; Sara Vieira-Silva; Gwen Falony; Mario Vaneechoutte; Raymond Vanholder; Wim Van Biesen; Geert Roger Bertrand Huys; Jeroen Raes; Griet Glorieux. Gut microbiota dynamics and uraemic toxins: one size does not fit all. Gut 2018, 68, 2257.1 -2260.

AMA Style

Marie Joossens, Karoline Faust, Tessa Gryp, Anh Thi Loan Nguyen, Jun Wang, Sunny Eloot, Eva Schepers, Annemieke Dhondt, Anneleen Pletinck, Sara Vieira-Silva, Gwen Falony, Mario Vaneechoutte, Raymond Vanholder, Wim Van Biesen, Geert Roger Bertrand Huys, Jeroen Raes, Griet Glorieux. Gut microbiota dynamics and uraemic toxins: one size does not fit all. Gut. 2018; 68 (12):2257.1-2260.

Chicago/Turabian Style

Marie Joossens; Karoline Faust; Tessa Gryp; Anh Thi Loan Nguyen; Jun Wang; Sunny Eloot; Eva Schepers; Annemieke Dhondt; Anneleen Pletinck; Sara Vieira-Silva; Gwen Falony; Mario Vaneechoutte; Raymond Vanholder; Wim Van Biesen; Geert Roger Bertrand Huys; Jeroen Raes; Griet Glorieux. 2018. "Gut microbiota dynamics and uraemic toxins: one size does not fit all." Gut 68, no. 12: 2257.1-2260.

Review
Published: 12 April 2017 in Nephrology Dialysis Transplantation
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Urea, a marker of uraemic retention in chronic kidney disease (CKD) and of adequacy of intradialytic solute removal, has traditionally been considered to be biologically inert. However, a number of recent experimental data suggest that urea is toxic at concentrations representative for CKD. First of all, at least five studies indicate that urea itself induces molecular changes related to insulin resistance, free radical production, apoptosis and disruption of the protective intestinal barrier. Second, urea is at the origin of the generation of cyanate, ammonia and carbamylated compounds, which as such all have been linked to biological changes. Especially carbamylation has been held responsible for post-translational protein modifications that are involved in atherogenesis and other functional changes. In observational clinical studies, these carbamylated compounds were associated with cardiovascular and overall morbidity and mortality. These findings shed new light on the validity of Kt/Vurea as a marker of dialysis adequacy. Yet, also the views that the kinetics of urea are not representative of the kinetics of several other uraemic retention solutes, and that urea cannot be held responsible for all complex metabolic and clinical changes responsible for the uraemic syndrome, still remain valid. Future efforts to improve the outcome of patients with CKD might be directed at further improving removal of solutes implied in the uraemic syndrome, including but not restricted to urea, also taking into account the impact of the intestine and (residual) renal function on solute concentration.

ACS Style

Raymond Vanholder; Tessa Gryp; Griet Glorieux. Urea and chronic kidney disease: the comeback of the century? (in uraemia research). Nephrology Dialysis Transplantation 2017, 33, 4 -12.

AMA Style

Raymond Vanholder, Tessa Gryp, Griet Glorieux. Urea and chronic kidney disease: the comeback of the century? (in uraemia research). Nephrology Dialysis Transplantation. 2017; 33 (1):4-12.

Chicago/Turabian Style

Raymond Vanholder; Tessa Gryp; Griet Glorieux. 2017. "Urea and chronic kidney disease: the comeback of the century? (in uraemia research)." Nephrology Dialysis Transplantation 33, no. 1: 4-12.

Review
Published: 29 January 2017 in Toxins
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If chronic kidney disease (CKD) is associated with an impairment of kidney function, several uremic solutes are retained. Some of these exert toxic effects, which are called uremic toxins. p-Cresyl sulfate (pCS) is a prototype protein-bound uremic toxin to which many biological and biochemical (toxic) effects have been attributed. In addition, increased levels of pCS have been associated with worsening outcomes in CKD patients. pCS finds its origin in the intestine where gut bacteria metabolize aromatic amino acids, such as tyrosine and phenylalanine, leading to phenolic end products, of which pCS is one of the components. In this review we summarize the biological effects of pCS and its metabolic origin in the intestine. It appears that, according to in vitro studies, the intestinal bacteria generating phenolic compounds mainly belong to the families Bacteroidaceae, Bifidobacteriaceae, Clostridiaceae, Enterobacteriaceae, Enterococcaceae, Eubacteriaceae, Fusobacteriaceae, Lachnospiraceae, Lactobacillaceae, Porphyromonadaceae, Staphylococcaceae, Ruminococcaceae, and Veillonellaceae. Since pCS remains difficult to remove by dialysis, the gut microbiota could be a future target to decrease pCS levels and its toxicity, even at earlier stages of CKD, aiming at slowing down the progression of the disease and decreasing the cardiovascular burden.

ACS Style

Tessa Gryp; Raymond Vanholder; Mario Vaneechoutte; Griet Glorieux. p-Cresyl Sulfate. Toxins 2017, 9, 52 .

AMA Style

Tessa Gryp, Raymond Vanholder, Mario Vaneechoutte, Griet Glorieux. p-Cresyl Sulfate. Toxins. 2017; 9 (2):52.

Chicago/Turabian Style

Tessa Gryp; Raymond Vanholder; Mario Vaneechoutte; Griet Glorieux. 2017. "p-Cresyl Sulfate." Toxins 9, no. 2: 52.