Publications by authors named "Hasan Ufuk Celebioglu"

12 Publications

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Effects of potential synbiotic interaction between Lactobacillus rhamnosus GG and salicylic acid on human colon and prostate cancer cells.

Arch Microbiol 2021 Apr 23;203(3):1221-1229. Epub 2021 Feb 23.

Department of Biotechnology, Faculty of Science, Bartin University, Bartin, Turkey.

Salicylic acid, widely distributed in the whole plant kingdom, is a benzoic acid derivative acting as a signal substance in plants, but could be related to differences in cancer incidence, as many herbs and spices contain high amounts. Lactobacillus rhamnosus GG (LGG) is one of the best-known lactic acid bacteria that has been studied for over 30 years. Probiotic and/or commensal bacteria of the human microbiota are known to respond to diet constituents. Therefore, the present study aims at investigating the possible effects of salicylic acid on the probiotic properties of LGG, and in vitro cytotoxic effects of combination of salicylic acid and LGG on human colon and prostate cancer cells. Salicylic acid significantly (p < 0.05) increased co-aggregation of LGG with E. coli (~ twofold) and anti-oxidant properties. Furthermore, it also induced the cytotoxic effects of LGG against human colon cancer cells. These results suggest that interaction of LGG with salicylic acid can exert more probiotic properties.
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http://dx.doi.org/10.1007/s00203-021-02200-1DOI Listing
April 2021

Metal contained Phthalocyanines with 3,4-Dimethoxyphenethoxy substituents: their anticancer, antibacterial activities and their inhibitory effects on some metabolic enzymes with molecular docking studies.

J Biomol Struct Dyn 2020 Nov 24:1-12. Epub 2020 Nov 24.

Department of Chemistry, Faculty of Science, Ataturk University, Erzurum, Turkey.

The compounds (-) used in this study were re-synthesized in accordance with our previous study. The inhibitory effect of the complexes on some metabolic enzymes was examined and it was demonstrated that the enzymes inhibited by ligands and their complex molecules at micromolar level. The best Ki value for α-glycosidase enzyme was absorved 1.01±0.08 µM for compound . The biological activity of ligand and metal complexes against enzymes was compared with molecular docking method. The enzymes used against ligand and metal complexes respectively: Achethylcholinesterase for ID 4M0E (AChE), butyrylcholinesterase for ID 5NN0 (BChE), α-glycosidase for ID 1XSI (α-Gly). ADME analysis was performed to examine the drug properties of the compounds (-). Besides, the anticancer properties of the complexes were studied. The doses of all compounds caused significant reductions in MCF-7 cell viability. The and compounds administered to PC-3 cells exhibited a more pronounced cytotoxic effect than the other two compounds ( and ). Furthermore, antibacterial activities of these compounds against and were examined.Communicated by Ramaswamy H. Sarma.
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http://dx.doi.org/10.1080/07391102.2020.1844051DOI Listing
November 2020

Cytotoxic effects, carbonic anhydrase isoenzymes, α-glycosidase and acetylcholinesterase inhibitory properties, and molecular docking studies of heteroatom-containing sulfonyl hydrazone derivatives.

J Biomol Struct Dyn 2020 Jul 21:1-12. Epub 2020 Jul 21.

Department of Chemistry, Faculty of Sciences, Ataturk University, Erzurum, Turkey.

Today, interest in studies on the search for new drugs to be used in diseases such as cancer, cardiovascular diseases, neurodegenerative diseases and diabetes, as well as prevention of microbial inflammation is increasing day by day. Emerging biological and pharmacological effects of sulfonyl hydrazone derivative compounds reveal their importance. In the present study, heteroatom-containing sulfonyl hydrazone derivatives have been studied for their anticancer and antimicrobial properties, as well as their effects on enzymes that could play roles in Alzheimer's dissease and diabetes. High doses of the tested compounds significantly decreased the cell viabilities of breast cancer (MCF-7) and prostate cancer (PC-3) cell lines. Furthermore, all compounds possessed antimicrobial activities against very common bacteria and . These compounds were good inhibitors of the α-glycosidase, human carbonic anhydrase I and II isoforms and acetylcholinesterase enzyme with values in the range of 1.14 ± 0.14-3.63 ± 0.26 nM for α-glycosidase, 66.05 ± 9.21-125.45 ± 11.54 nM for hCA I, 89.14 ± 10.43-170.22 ± 26.05 nM for hCA II and 754.03 ± 73.22-943.92 ± 58.15 nM for AChE, respectively. Molecular docking method was used to theoretically compare biological activities of sulfonyl hydrazone derivatives against enzymes. The theoretical results were compared with the experimental results. Thus, these compounds have strong biological activities.Communicated by Ramaswamy H. Sarma.
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http://dx.doi.org/10.1080/07391102.2020.1792345DOI Listing
July 2020

Determination of anticancer properties and inhibitory effects of some metabolic enzymes including acetylcholinesterase, butyrylcholinesterase, alpha-glycosidase of some compounds with molecular docking study.

J Biomol Struct Dyn 2021 Jul 4;39(10):3693-3702. Epub 2020 Jun 4.

Department of Chemistry, Faculty of Science, Ataturk University, Erzurum, Turkey.

Inhibitory effect of the complexes on some metabolic enzyme demonstrated that the enzymes inhibited by ligand and it's complex molecules at the micromolar level. The best inhibition effect for α-glycosidase (α-Gly) enzyme against cobalt complex with Ki value of 3.77 ± 0.58 µM. For achethylcholinesterase (AChE) and butyrylcholinesterase (BChE) enzymes against SM-Co complex, Ki values of 74.23 ± 5.02 µM and 101.21 ± 12.84 µM Ki were observed, respectively. Molecular docking studies were performed to compare the biological activities of ligands and ligand complexes against enzymes whose names are AChE for ID 4M0E, BChE for ID 5NN0, α-Gly for ID 1XSI respectively. Also, anticancer properties of the complexes studied. The doses of all compounds caused significant reductions in MCF-7 cell viability. Zr compound showed the best cytotoxic activity against the MCF-7 cell. SM ligand administered to PC-3 cells exhibited a more pronounced cytotoxic effect than the SM-Co and Zr compounds.Communicated by Ramaswamy H. Sarma.
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http://dx.doi.org/10.1080/07391102.2020.1768901DOI Listing
July 2021

Dietary Nutrients, Proteomes, and Adhesion of Probiotic Lactobacilli to Mucin and Host Epithelial Cells.

Microorganisms 2018 Aug 21;6(3). Epub 2018 Aug 21.

Department of Biotechnology and Biomedicine, Technical University of Denmark, DK-2800 Kgs Lyngby, Denmark.

The key role of diet and environment in human health receives increasing attention. Thus functional foods, probiotics, prebiotics, and synbiotics with beneficial effects on health and ability to prevent diseases are in focus. The efficacy of probiotic bacteria has been connected with their adherence to the host epithelium and residence in the gut. Several in vitro techniques are available for analyzing bacterial interactions with mucin and intestinal cells, simulating adhesion to the host in vivo. Proteomics has monitored and identified proteins of probiotic bacteria showing differential abundance elicited in vitro by exposure to food components, including potential prebiotics (e.g., certain carbohydrates, and plant polyphenols). While adhesion of probiotic bacteria influenced by various environmental factors relevant to the gastrointestinal tract has been measured previously, this was rarely correlated with changes in the bacterial proteome induced by dietary nutrients. The present mini-review deals with effects of selected emerging prebiotics, food components and ingredients on the adhesion of probiotic lactobacilli to mucin and gut epithelial cells and concomitant abundancy changes of specific bacterial proteins. Applying this in vitro synbiotics-like approach enabled identification of moonlighting and other surface-located proteins of NCFM that are possibly associated with the adhesive mechanism.
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http://dx.doi.org/10.3390/microorganisms6030090DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6163540PMC
August 2018

Plant Polyphenols Stimulate Adhesion to Intestinal Mucosa and Induce Proteome Changes in the Probiotic Lactobacillus acidophilus NCFM.

Mol Nutr Food Res 2018 02 12;62(4). Epub 2018 Jan 12.

Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark.

Scope: Plant phenolics, known to exert beneficial effects on human health, were supplemented to cultures of the probiotic bacterium Lactobacillus acidophilus NCFM (NCFM) to assess their effect on its adhesive capacity and the abundancy of individual proteins.

Methods And Results: The presence of resveratrol and ferulic acid during bacterial growth stimulated adhesion of NCFM to mucin and human intestinal HT-29 cells, while tannic acid improved adhesion only to HT-29 cells and caffeic acid had very modest effect overall. Some dosage dependence was found for the four phenolics supplemented at 100, 250, and 500 μg mL to the cultures. Notably, 500 μg mL ferulic acid only stimulated adhesion to mucin. Analyses of differential whole-cell as well as surface proteomes revealed relative abundancy changes for a total of 27 and 22 NCFM proteins, respectively. These changes include enzymes acting in metabolic pathways, such as glycolysis, nucleotide metabolism, and stress response, as well as known moonlighting or surface-associated proteins.

Conclusion: The five plant phenolics found in various foods stimulate the adhesive capacity of NCFM in diverse ways and elicit relative abundancy changes of specific proteins, providing molecular level insight into the mechanism of the putative beneficial effects of the polyphenols.
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http://dx.doi.org/10.1002/mnfr.201700638DOI Listing
February 2018

Data regarding the growth of NCFM on different carbohydrates and recombinant production of elongation factor G and pyruvate kinase.

Data Brief 2017 Oct 14;14:118-122. Epub 2017 Jul 14.

Enzyme and Protein Chemistry, Department of Biotechnology and Biomedicine, Technical University of Denmark, Denmark.

The present study describes the growth of the very well-known probiotic bacterium NCFM on different carbohydrates. Furthermore, recombinant production of putative moonlighting proteins elongation factor G and pyruvate kinase from this bacterium is described. For further and detailed interpretation of the data presented here, please see the research article "Mucin- and carbohydrate-stimulated adhesion and subproteome changes of the probiotic bacterium NCFM" (Celebioglu et al., 2017) [1].
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http://dx.doi.org/10.1016/j.dib.2017.07.021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5567391PMC
October 2017

Mucin- and carbohydrate-stimulated adhesion and subproteome changes of the probiotic bacterium Lactobacillus acidophilus NCFM.

J Proteomics 2017 06 19;163:102-110. Epub 2017 May 19.

Enzyme and Protein Chemistry, Department of Biotechnology and Biomedicine, Technical University of Denmark, Elektrovej, Building 375, DK-2800 Kgs. Lyngby, Denmark. Electronic address:

Adhesion to intestinal mucosa is a crucial property for probiotic bacteria. Adhesion is thought to increase host-bacterial interactions, thus potentially enabling health benefits to the host. Molecular events connected with adhesion and surface proteome changes were investigated for the probiotic Lactobacillus acidophilus NCFM cultured with established or emerging prebiotic carbohydrates as carbon source and in the presence of mucin, the glycoprotein of the epithelial mucus layer. Variation in adhesion to HT29-cells and mucin was associated with carbon source and mucin-induced subproteome abundancy differences. Specifically, while growth on fructooligosaccharides (FOS) only stimulated adhesion to intestinal HT-29 cells, cellobiose and polydextrose in addition increased adhesion to mucin. Adhesion to HT-29 cells increased by about 2-fold for bacteria grown on mucin-supplemented glucose. Comparative 2DE-MS surface proteome analysis showed different proteins in energy metabolism appearing on the surface, suggesting they exert moonlighting functions. Mucin-supplemented bacteria had relative abundance of pyruvate kinase and fructose-bisphosphate aldolase increased by about 2-fold while six spots with 3.2-2.1 fold reduced relative abundance comprised elongation factor G, phosphoglycerate kinase, BipAEFTU family GTP-binding protein, ribonucleoside triphosphate reductase, adenylosuccinate synthetase, 30S ribosomal protein S1, and manganese-dependent inorganic pyrophosphatase. Surface proteome of cellobiose- compared to glucose-grown L. acidophilus NCFM had phosphate starvation inducible protein stress-related, thermostable pullulanase, and elongation factor G increasing 4.4-2.4 fold, while GAPDH, elongation factor Ts, and pyruvate kinase were reduced by 2.0-1.5 fold in relative abundance. Addition of recombinant L. acidophilus NCFM elongation factor G and pyruvate kinase to a coated mucin layer significantly suppressed subsequent adhesion of the bacterium.

Biological Significance: Human diet is important for intestinal health and food components, especially non-digestible carbohydrates can beneficially modify the microbiota. In the present study, effects of emerging and established prebiotic carbohydrates on the probiotic potential of Lactobacillus acidophilus NCFM were investigated by testing adhesion to a mucin layer and intestinal cells, and comparing this with changes in abundancy of surface proteins thought to be important for host interactions. Increased adhesion was observed following culturing of the bacterium with fructooligosaccharides, cellobiose or polydextrose, as well as mucin-supplemented glucose as carbon source. Enhanced adhesion ability can prolong bacterial residence in GIT yielding positive health effects. Higher relative abundance of certain surface proteins under various conditions (i.e. grown on cellobiose or mucin-supplemented glucose) suggested involvement of these proteins in adhesion, as confirmed by competition in case of two recombinantly produced moonlighting proteins. Combination of Lactobacillus acidophilus NCFM with different carbohydrates revealed potential bacterial determinants of synbiotic interactions, including stimulation of adhesion.
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http://dx.doi.org/10.1016/j.jprot.2017.05.015DOI Listing
June 2017

An Extracellular Cell-Attached Pullulanase Confers Branched α-Glucan Utilization in Human Gut Lactobacillus acidophilus.

Appl Environ Microbiol 2017 06 31;83(12). Epub 2017 May 31.

Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs. Lyngby, Denmark

Of the few predicted extracellular glycan-active enzymes, glycoside hydrolase family 13 subfamily 14 (GH13_14) pullulanases are the most common in human gut lactobacilli. These enzymes share a unique modular organization, not observed in other bacteria, featuring a catalytic module, two starch binding modules, a domain of unknown function, and a C-terminal surface layer association protein (SLAP) domain. Here, we explore the specificity of a representative of this group of pullulanases, Pul13_14 (Pul13_14), and its role in branched α-glucan metabolism in the well-characterized NCFM, which is widely used as a probiotic. Growth experiments with NCFM on starch-derived branched substrates revealed a preference for α-glucans with short branches of about two to three glucosyl moieties over amylopectin with longer branches. Cell-attached debranching activity was measurable in the presence of α-glucans but was repressed by glucose. The debranching activity is conferred exclusively by Pul13_14 and is abolished in a mutant strain lacking a functional Pul13_14 gene. Hydrolysis kinetics of recombinant Pul13_14 confirmed the preference for short-branched α-glucan oligomers consistent with the growth data. Curiously, this enzyme displayed the highest catalytic efficiency and the lowest reported for a pullulanase. Inhibition kinetics revealed mixed inhibition by β-cyclodextrin, suggesting the presence of additional glucan binding sites besides the active site of the enzyme, which may contribute to the unprecedented substrate affinity. The enzyme also displays high thermostability and higher activity in the acidic pH range, reflecting adaptation to the physiologically challenging conditions in the human gut. Starch is one of the most abundant glycans in the human diet. Branched α-1,6-glucans in dietary starch and glycogen are nondegradable by human enzymes and constitute a metabolic resource for the gut microbiota. The role of health-beneficial lactobacilli prevalent in the human small intestine in starch metabolism remains unexplored in contrast to colonic bacterial residents. This study highlights the pivotal role of debranching enzymes in the breakdown of starchy branched α-glucan oligomers (α-limit dextrins) by human gut lactobacilli exemplified by NCFM, which is one of the best-characterized strains used as probiotics. Our data bring novel insight into the metabolic preference of for α-glucans with short α-1,6-branches. The unprecedented affinity of the debranching enzyme that confers growth on these substrates reflects its adaptation to the nutrient-competitive gut ecological niche and constitutes a potential advantage in cross-feeding from human and bacterial dietary starch metabolism.
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http://dx.doi.org/10.1128/AEM.00402-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5452828PMC
June 2017

Exo- and surface proteomes of the probiotic bacterium Lactobacillus acidophilus NCFM.

Proteomics 2017 Jun;17(11)

Enzyme and Protein Chemistry, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs. Lyngby, Denmark.

Lactobacillus acidophilus NCFM is a well-known probiotic bacterium extensively studied for its beneficial health effects. Exoproteome (proteins exported into culture medium) and surface proteome (proteins attached to S-layer) of this probiotic were identified by using 2DE followed by MALDI TOF MS to find proteins potentially involved in bacteria-host interactions. The exo- and surface proteomes included 43 and 39 different proteins from 72 and 49 successfully identified spots, respectively. Twenty-two proteins were shared between the two proteomes; both contained the major surface layer protein that participates in host interaction as well as several well-known and putative moonlighting proteins. The exoproteome contained nine classically-secreted (containing a signal sequence) and ten nonclassically-secreted proteins, while the surface proteome contained four classically-secreted and eight nonclassically secreted proteins. Identification of exo- and surface proteomes contributes describing potential protein-mediated probiotic-host interactions.
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http://dx.doi.org/10.1002/pmic.201700019DOI Listing
June 2017

Comparative proteomics of oxidative stress response of Lactobacillus acidophilus NCFM reveals effects on DNA repair and cysteine de novo synthesis.

Proteomics 2017 03;17(5)

Department of Life Sciences and Systems Biology, Università di Torino, Torino, Italy.

Probiotic cultures encounter oxidative conditions during manufacturing, yet protein abundance changes induced by such stress have not been characterized for some of the most common probiotics and starters. This comparative proteomics investigation focuses on the response by Lactobacillus acidophilus NCFM to H O simulating an oxidative environment. Bacterial growth was monitored by BioScreen and batch cultures were harvested at exponential phase for protein profiling of stress responses by 2D gel based comparative proteomics. Proteins identified in 19 of 21 spots changing in abundance due to H O were typically related to carbohydrate and energy metabolism, cysteine biosynthesis, and stress. In particular, increased cysteine synthase activity may accumulate a cysteine pool relevant for protein stability, enzyme catalysis, and the disulfide-reducing pathway. The stress response further included elevated abundance of biomolecules reducing damage such as enzymes from DNA repair pathways and metabolic enzymes with active site cysteine residues. By contrast, a protein-refolding chaperone showed reduced abundance, possibly reflecting severe oxidative protein destruction that was not overcome by refolding. The proteome analysis provides novel insight into resistance mechanisms in lactic acid bacteria against reactive oxygen species and constitutes a valuable starting point for improving industrial processes, food design, or strain engineering preserving microorganism viability.
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http://dx.doi.org/10.1002/pmic.201600178DOI Listing
March 2017

Differential proteome and cellular adhesion analyses of the probiotic bacterium Lactobacillus acidophilus NCFM grown on raffinose - an emerging prebiotic.

Proteomics 2016 05 13;16(9):1361-75. Epub 2016 Apr 13.

Enzyme and Protein Chemistry, Department of Systems Biology, Technical University of Denmark, Elektrovej, Lyngby, Denmark.

Whole cell and surface proteomes were analyzed together with adhesive properties of the probiotic bacterium Lactobacillus acidophilus NCFM (NCFM) grown on the emerging prebiotic raffinose, exemplifying a synbiotic. Adhesion of NCFM to mucin and intestinal HT-29 cells increased three-fold after culture with raffinose versus glucose, as also visualized by scanning electron microscopy. Comparative proteomics using 2D-DIGE showed 43 unique proteins to change in relative abundance in whole cell lysates from NCFM grown on raffinose compared to glucose. Furthermore, 14 unique proteins in 18 spots of the surface subproteome underwent changes identified by differential 2DE, including elongation factor G, thermostable pullulanase, and phosphate starvation inducible stress-related protein increasing in a range of +2.1 - +4.7 fold. By contrast five known moonlighting proteins decreased in relative abundance by up to -2.4 fold. Enzymes involved in raffinose catabolism were elevated in the whole cell proteome; α-galactosidase (+13.9 fold); sucrose phosphorylase (+5.4 fold) together with metabolic enzymes from the Leloir pathway for galactose utilization and the glycolysis; β-galactosidase (+5.7 fold); galactose (+2.9/+3.1 fold) and fructose (+2.8 fold) kinases. The insights at the molecular and cellular levels contributed to the understanding of the interplay of a synbiotic composed of NCFM and raffinose with the host.
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http://dx.doi.org/10.1002/pmic.201500212DOI Listing
May 2016