Startseite Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
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Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage

  • Margareta Marusakova , Boris Dudik , Katarina Hadova , Zuzana Kmecova , Eva Kralova , Peter Krenek , Andrea Bilkova und Jan Klimas EMAIL logo
Veröffentlicht/Copyright: 27. Juni 2022
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 17 Heft 1

Abstract

Overweight and obesity have been linked with increased intake of sugar-sweetened beverages. On the other hand, physical activity has been known to lead to weight loss. Therefore, we hypothesized that exercise might influence the Lactobacillus population in fecal microbiota as their changed abundance is often associated with shifts in the physical activity and diet. In our experiment, Wistar rats were allocated into groups with normal feed or added sugar-sweetened beverages with or without access to a running wheel. Interestingly, only a combination of physical activity and sweetened beverage intake was associated with a significant increase in fecal lactobacilli abundance, suggesting a connection between exercise and a rise in lactobacilli abundance. Moreover, physical activity has improved weight-related parameters and led to increased plasma and mRNA adiponectin levels. Ghrelin and leptin plasma levels were unaltered. Taken together, our results demonstrate that effect of physical activity on adiposity even during unhealthy feeding patterns is accompanied by increased lactobacilli abundance in the fecal microbiota population.

Keywords: overweight; sweetened beverage; physical activity; fecal Lactobacillus abundance; adiponectin

1 Introduction

Consumption of fructose and/or sucrose via ingestion of sugar-sweetened beverages has increased significantly in the last decades, and this overconsumption has been linked with dyslipidemia, obesity, and diabetes epidemic [1]. Low doses of fructose in the diet are metabolized by the small intestine, but at high doses, fructose is metabolized and digested directly by the liver and microbiota, causing fatty liver and obesity [2]. In addition, it has been shown to affect lipid metabolism by increasing plasma triglycerides (TAG) and fasting plasma free fatty acids [3]. Multiple studies suggest a relation between fructose consumption and the onset of obesity and dyslipidemia [4] and often nonalcoholic fatty liver disease [5]. Importantly, sweetened cola beverages’ intake in rodents has been used as an experimental model for studying metabolic syndrome-related features by stimulating the human unhealthy feeding pattern [6,7].

While it is clear that an imbalance between energy intake and energy expenditure leads to body weight gain, it has not been fully explained yet which factor of these two has been more markedly promoting the obesity epidemic [8]. A longitudinal study tracking voluntary exercise in free time and body weight increase in children reported that higher physical activity levels predicted lower adiposity during growth [9]. Similar studies in animals demonstrated that spontaneous physical activity also significantly attenuates adiposity gain [10]. Exercise has a strong positive effect on weight loss in general and insulin sensitization, blood pressure normalization, and overall cardiovascular health [11].

It is well established that the amount and nutrient content of ingested food can affect the microbial composition of the gut; obesity has been linked with modified bacterial diversity as an effect of both high fat and high sugar diets [12]. More recently, an experimental study has indicated that physical activity could alter the gut microbiota in high fat diet-induced obese mice [13], and also, several clinical studies suggested that exercise could play an important role in modifying microbial composition in obese and diabetic individuals [14,15]. Particularly, a varied abundance of the fecal microbiota populations of bacteria from the genus Lactobacillus is often associated with changes in physical activity and diet [16]. Although lactobacilli represent only <1% of the total bacterial population in the gut [17], their altered abundance has been related to various metabolic disorders, including type 1 and type 2 diabetes mellitus [18,19]. Relevant to our study, there are conflicting reports on the association of intestinal lactobacilli abundance with obesity in humans [20,21]. Because lactobacilli appear to be associated with both weight increase and weight loss [22], these findings may reflect discrepancies in the lactobacilli properties induced by species and strain differences [23]. Probiotic supplementation of lactobacilli is often associated with a positive influence on a whole-body metabolism by affecting energy balance and inflammation [24], as well as on performance in athletes [25,26], but this effect is also known to be strain specific.

The aim of this study is to investigate the effect of sweetened beverage intake on the overall metabolic state. We hypothesized that physical activity, even during unhealthy feeding represented by sugar-sweetened beverages intake, may attenuate weight gain and obesity-related features in young rats by improving overall metabolic state due to increased energy output and by affecting microbiota composition. We also aim to demonstrate the role of microbiota in obesity prevention in connection with physical exercise.

2 Materials and methods

2.1 Animal model

Four-week-old male Wistar rats (obtained from a breeding station Dobra Voda, Institute of Experimental Pharmacology & Toxicology, Centre of Experimental Medicine, Slovak Academy of Sciences) were randomly allocated into the following groups: animals drinking tap water (CON, n = 10) and animals drinking sweetened cola beverage (Coca-Cola Original®) (SSB, n = 10) ad libitum, which were further divided into subgroups with access to physical activity [control group drinking water and exercising = SPA (n = 10) and group drinking sugar-sweetened beverage and exercising = SSB + SPA (n = 10)]. Animals in these subgroups had a running wheel available in their individual cages to allow for spontaneous physical activity. To measure the covered distance, the wheels were equipped with a magnet and a sensor, and upon their passage, the distance was continuously recorded. Randomization into all groups was performed so that the bodyweight would not differ at the beginning of the experiment, and animals were co-housed in groups of 2–3 animals.

Animals had free access to water or decarbonized sweetened cola beverage (according to the manufacturer, 100 mL of this beverage contains 27 g sugars, mainly high fructose corn syrup), were fed a normal chow diet, and the experimental period lasted 6 months. Weight gain and food and liquid intake were recorded weekly. Total caloric intake was calculated as a sum of ingested liquids and solid food for 24 h in a metabolic cage, where individual animals were placed at the end of the experiment. Then, TAG levels and random and fasting glycemia in capillary blood were measured using a commercially available analyzer (Accutrend, Roche, Switzerland). Animals were sacrificed by exsanguination in full anesthesia induced by tribromethanol (dose 13 mL/kg in the form of Avertin solution, Sigma-Aldrich, Germany).

  1. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals, has been conformed to the Guide for the Care and Use of Laboratory Animals (8th edition, National Academies Press) and to the Guide for the Care and Use of Laboratory Animals published in the Collection of Laws of the Slovak Republic, and was approved by the Ethics Committee of the Faculty of Pharmacy, Comenius University and by the State Veterinary and Food Administration of the Slovak Republic.

2.2 Origin and cultivation of bacterial strain

Lactobacillus reuteri CCM 3625 was purchased from the Czech Collection of Microorganisms (Brno, Czech Republic). The bacterial strain was cultivated in MRS broth (VWR, USA) at 37°C in anaerobic conditions for 18 h.

2.3 DNA isolation from fecal samples

Fecal samples harvested on the day of sacrifice individually from each animal were frozen immediately and stored at −80°C until further analysis. Total genomic DNA from feces was isolated by FastDNATM Kit for Feces (mpbio, USA) according to manufacturer’s instructions. The quality and concentration of isolated DNA were verified by spectrophotometry on Epoch microplate spectrophotometer (Biotek, USA), and samples were stored at −20°C until qPCR analysis.

2.4 Relative abundance of target bacteria in feces analyzed by qPCR

To quantify the relative abundance of bacteria of genus Lactobacillus in feces, qPCR using specific primers for genus Lactobacillus (LAC) and universal bacterial primers (UNI) designed on the basis of 16S rRNA gene sequences (Table 1) was conducted. Expressions of studied genes were quantified by qPCR using thermocycler QuantStudioTM 3 (Applied Biosystems, Thermo Fisher Scientific, USA) using HOT FIREPol EvaGreen qPCR mix Plus (Solis, BioDyne, Estonia). The PCR program consisted of initial denaturation at 95°C for 15 min, followed by 40 cycles of 95°C for 15 s, 60°C for 30 s, and 72°C for 30 s. All experiments were conducted in triplicates along with no template control. PCR products were evaluated by melting curve analysis and gel electrophoresis to confirm specific amplification. Amplification efficiency of primers was determined by making serial dilutions of reference bacterial DNA (L. reuteri CCM 3625), calculating a linear regression based on the Ct data points, and inferring the efficiency from the slope of the line. qPCR was performed as described above with six 10-fold dilutions of L. reuteri CCM 3625 genomic DNA (extracted from 109 CFU using the above-mentioned kit) for both primer pairs. The Ct values obtained from each sample were transformed into a percentage with the equation:

X = ( Eff . UNI ) Ct UNI ( Eff . LAC ) Ct LAC × 100 .

Table 1

Primer sequences for bacterial studies and rat tissue qPCR

Target gene Primer sequence (5′  → 3′) qPCR efficiency (%) Reference
Universal bacterial group F-TCCTACGGGAGGCAGCAGT 96.20 [41]
R-GGACTACCAGGGTATCTAATCCTGTT
Lactobacillus genus F-GAGGCAGCAGTAGGGAATCTTC 99.26 [42]
R-GGCCAGTTACTACCTCTATCCTTCTTC
B2m F-ATGGAGCTCTGAATCATCTGG NA This study
R-AGAAGATGGTGTGCTCATTGC
Actb F-CCGCGAGTACAACCTTGTTG NA This study
R-GCAGCGATATCGTCATCCA
TNF F-AACTTCGGGGTGATCGGTCCCA NA This study
R-TACGACGTGGGCTACGGGCTT
Lep F-AGACCCCAGCGAGGAAAATG NA This study
R-TACCGACTGCGTGTGTGAAA
GLUT4 F-GACCCGCCCTTTGCACACCA NA This study
R-TCACTCGCTGCTGGGGGGT
Adiponectin F-GGGAGACGCAGGTGTTCTTG NA This study
R-CCTACGCTGAATGCTGAGTGA

Eff. UNI is the calculated efficiency of the universal primers (2 = 100% and 1 = 0%) and Eff. LAC refers to the efficiency of the primers for the genus Lactobacillus. The Cts are the threshold cycles registered by the thermocycler. Resolving this formula, X represents the percentage of 16S rRNA taxon-specific copy numbers existing in a sample [27].

2.5 RNA isolation and qPCR analysis of adipose tissue

Samples of white adipose tissue were dissected and stored at −80°C until RNA isolation with Tri-Reagent® (Sigma-Aldrich, USA). Afterward, a transcription into cDNA was performed (High capacity cDNA Reverse Transcription Kit with RNAse inhibitor, Applied Biosystems, USA). Complementary DNA was then used for qPCR analysis (StepOne Plus System, Applied Biosystems) using SYBR Select Master Mix (Applied Biosystems) under the following conditions: denaturation at 95°C, annealing at 60°C, and extension at 72°C for 40 cycles. B2-microglobulin (B2m) and beta-actin (Actb) were used as references. We used sequences of primers shown in Table 1. PCR efficiency was calculated by LinReg, the exact percentage is not reported for specific genes. Relative quantification of mRNA expression in the qPCR reaction was calculated by the 2ΔΔCt method.

2.6 Plasma concentrations of adiponectin, insulin, and ghrelin

To measure and analyze adiponectin (as an adipose tissue-related indicator of metabolic changes), insulin (as a pancreas-related indicator of metabolic changes), and ghrelin (as a gastrointestinal tract-related indicator of appetite), commercially available kits for ELISA were used (Rat Ghrelin ELISA Kit, Elabscience, USA; Rat Adiponectin ELISA Kit, Abcam, UK; and Rat Insulin ELISA Kit, Mercodia, Sweden, respectively).

2.7 Statistical analysis

Results are shown as an average of the whole group ± SEM. Statistical analyses were performed using GraphPad software via one-way analysis of variance with the Bonferroni post hoc test. For Lactobacillus studies, Kruskal–Wallis test with Dunn´s multiple comparison test was used. p values <0.05 were considered statistically significant.

3 Results

3.1 Percentage abundance of genus Lactobacillus in stool samples

We observed a significantly higher abundance of genus Lactobacillus in feces of the group drinking sweetened beverage while performing physical activity (SSB + SPA, 1.05% of total bacterial population in stool, n = 8) vs sedentary group drinking sweetened beverage (SSB, 0.44% of total bacteria, n = 9; p < 0.05) (Figure 1). Unhealthy feeding (SSB) or physical activity (SPA) alone did not affect the population of lactobacilli.

Figure 1 Relative abundance of genus Lactobacillus in feces of rats. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Results shown as average ± SEM. n = 8–10 per group; *p < 0.01 vs SSB, $ p < 0.01 vs SPA.
Figure 1

Relative abundance of genus Lactobacillus in feces of rats. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Results shown as average ± SEM. n = 8–10 per group; *p < 0.01 vs SSB, $ p < 0.01 vs SPA.

3.2 Effect of physical activity on weight gain and overweight-related features

Long-term consumption of sweetened cola beverages led to only an insignificant increase in body weight in young rats (Table 2; Figure 2). On the other hand, voluntary physical activity suppressed a body weight increase in both the sweetened beverage drinking group (SSB + SPA) and the control group (SPA) during 6 months duration of the experiment. Sweetened cola beverage intake increased by 41%, although non-significant, in retroperitoneal white adipose tissue mass and non-significant increase in TAG plasma concentration by 20% in the sugar-sweetened beverage drinking group. On the other hand, physical activity significantly reduced weight gain, white adipose tissue mass, and plasma TAG levels both in control and sugar-sweetened beverage drinking rats (Table 2). Following cola beverage feeding, random as well as fasting glycemia remained stable, suggesting effective compensatory mechanisms in young rats. This was in line with only slightly increased (by 16%, Figure 3) insulin plasma levels in sedentary animals. Physical activity did not influence glycemia-related features after sugar-sweetened beverage intake but led to decreased fasting glycemia levels (by 18%, p < 0.05).

Table 2

Effect of SPA on body weight and weight gain related parameters

CON SSB SSB + SPA SPA
Final body weight (BW) (g) 574.5 ± 12.4 615.6 ± 29.4 534.8 ± 16.8* 513.4 ± 15.5#
BW increase (%) 491.9 ± 23.0 514.6 ± 27.9 443.1 ± 31.5* 413.6 ± 37.9#
WAT weight (g) 6.4 ± 0.3 9.0 ± 1.4 5.4 ± 0.6*$ 3.9 ± 0.4#
Liver weight (g) 17.0 ± 0.6 21.5 ± 1.5 18.2 ± 0.7* 16.2 ± 0.9
Plasma TAG concentration (mmol/L) 2.5 ± 0.2 3.0 ± 0.5 1.9 ± 0.2* 1.5 ± 0.1#
Fasting glycemia (mmol/L) 6.59 ± 0.24 6.30 ± 0.26 5.81 ± 0.29 5.40 ± 0.38#
Random glycemia (mmol/L) 6.84 ± 0.21 6.77 ± 0.64 6.84 ± 0.43 7.07 ± 0.32

CON, control group; SSB, group drinking sugar sweetened beverage; SSB + SPA, group drinking sugar sweetened beverage concomitant to spontaneous physical activity; SPA, group performing spontaneous physical activity; WAT, white adipose tissue; TAG, triglycerides; AUC, area under the curve in oral glucose tolerance test. Number of animals = 10 per group, average ± SEM, *p < 0.05 vs SSB, # p < 0.05 vs CON, $ p < 0.05 vs SPA.

Figure 2 Effect of SPA on fluids and pellets intake and diuresis at the end of follow-up in control and cola SBP drinking rats and on the long-term body weight gain during follow-up and daily average distance ran. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Average ± SEM. n = 10 per group, n = 6–7 in daily distance run figure; # p < 0.01 vs CON, $ p < 0.01 vs SPA.
Figure 2

Effect of SPA on fluids and pellets intake and diuresis at the end of follow-up in control and cola SBP drinking rats and on the long-term body weight gain during follow-up and daily average distance ran. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Average ± SEM. n = 10 per group, n = 6–7 in daily distance run figure; # p < 0.01 vs CON, $ p < 0.01 vs SPA.

Figure 3 Effect of SPA on insulin, adiponectin, and ghrelin levels in plasma of controls and cola SSB drinking rats. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Average ± SEM. n = 8 per group; *p < 0.05 vs SSB, # p < 0.05 vs CON.
Figure 3

Effect of SPA on insulin, adiponectin, and ghrelin levels in plasma of controls and cola SSB drinking rats. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Average ± SEM. n = 8 per group; *p < 0.05 vs SSB, # p < 0.05 vs CON.

3.3 Effect of physical activity on energy intake

Cola beverage drinking rats significantly increased their liquid intake (by approximately 200%, p < 0.05) but compensated for this supply of fluid-based sugars by a significant reduction of pellets intake (by approximately 31%, p < 0.05). This was observed independently of exercise or sedentary settings. Interestingly, compensatory reduction of chow intake resulted in similar energy intake per 24 h in all rat groups (Figure 2).

3.4 Effect of physical activity on inflammatory mediators in plasma and white adipose tissue

In contrast to insulin and ghrelin, which remained stable under all studied conditions, plasma levels of adiponectin were significantly elevated in both activity groups (Figure 3), which possibly mirrors the decreased proportion of adipose tissue in active rats when compared to sedentary controls. Interestingly, mRNA levels of adiponectin in white adipose tissue were significantly increased only in the group drinking sugar-sweetened beverage while performing physical activity (SSB + SPA) (Figure 4).

Figure 4 Effect of SPA on relative mRNA expression of TNF, Lep, and GLUT4 in white adipose tissue (WAT) of control and cola drinking rats. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Average ± SEM. n = 10 per group; *p < 0.05 vs SSB.
Figure 4

Effect of SPA on relative mRNA expression of TNF, Lep, and GLUT4 in white adipose tissue (WAT) of control and cola drinking rats. CON = control group, SSB = group drinking sugar sweetened beverage, SSB + SPA = group drinking sugar sweetened beverage concomitant to spontaneous physical activity, SPA = group performing spontaneous physical activity. Average ± SEM. n = 10 per group; *p < 0.05 vs SSB.

Exclusively, the glucose transporter type 4 (GLUT4) expression was elevated in white adipose tissue of rats drinking sugar-sweetened beverages while performing physical activity (Figure 4), suggesting a better insulin-related glucose utilization in fat tissue following activity in rats drinking cola beverage. Other indicators of altered activity of adipose tissue, metabolic [leptin (Lep)], or inflammatory [tumor necrosis factor (TNF)] indicators remained unaltered, suggesting that although the proportion of adipose tissue in the whole body increased, its function remained in a normal, probably healthy mode.

4 Discussion

In this study, we investigated whether physical activity influences weight gain and related biochemical and molecular indicators in settings of chronic unhealthy feeding. The main finding was the influence of exercise on fecal lactobacilli abundance in rats during a long-term administration of sweetened cola beverage in early adulthood.

Physical activity per se was insufficient to alter lactobacilli abundance in our study. This is in contrast to a study in mice, where voluntary wheel running was found to alter gut microbiota composition by increasing the number of Lactobacillus spp. compared to sedentary mice [22] and also to the current view that physical (in)activity can lead to a gut microbiota change [28]. On the other hand, also in humans, a causal relationship between exercise and gut microbiota composition has not been yet fully established and is thought to be directly linked with dietary adjustments [29]. Thus, it is conceivable that a combination of exercise with diet is required for microbiota change.

In line with this hypothesis, we documented a rise of lactobacilli in the group drinking sugar-sweetened beverages while performing physical activity. It has been previously observed in similar animal experiments that fecal samples of obese rats were enriched with Lactobacillus spp., specifically after exercise [16]. In general, numerous strains of lactobacilli may positively influence not only gastrointestinal health but also performance in athletes [25,26]. However, the mechanism by which microbiota affects exercise and vice versa has not been supported by substantial evidence. Alteration of gut motility is one mechanism by which exercise may influence the microbiome [30]. Exercise can also reduce intestinal blood flow [31], which could potentially lead to reduced absorption of fructose from the gut, thus increasing the availability of the sugars to the microbes. It has been recently reported that dietary fructose is converted by the microbiome into short-chain fatty acids, such as acetate [2], and acetate is most likely to be an important energy source in the skeletal muscle, especially during endurance exercise [32]. Taken together, this would suggest that exercise could lead to increased production of acetate from dietary fructose, which would potentially, in turn, further increase exercise endurance.

Interestingly, in our experiment, rats drinking sugar-sweetened beverages did not exhibit increased exercise performance compared to rats performing physical activity without access to such drink (rather non-significantly decreased). From our perspective, the lack of enhanced performance in the exercising group while having access to cola-sweetened beverages is somewhat unexpected, but it is suggestive that the compensatory reduction of feed may influence effective energy production. Another explanation may simply lie in the fact that sugar-sweetened beverage drinking rats, though exercising, still had significantly larger adipose tissue mass compared to control exercising animals, which could be limiting the activity.

As mentioned above, when comparing a total caloric intake by calculating the sum of energy from liquid and food ingested, we discovered that decreased food intake in both sweetened beverage drinking groups contributed to total energy intake comparable to the control group. This remained similar also under increased energy expenditure conditions in exercising animals. Indeed, one of the typical phenomena observed in animal experiments with sugar-sweetened beverage administration is the compensatory reduction of feeding [33]. It is thought to be a result of drinking large volumes of high caloric drinks, such as cola, which provides excess caloric intake [34], or could be connected to a high content of caffeine in cola beverages, which is known for its direct appetite suppressing effect [35,36]. Nevertheless, in spite of unchanged total caloric intake, favoring the high fructose intake may directly enhance body adiposity and microbiota composition.

We have observed an increase in adiponectin plasma levels in both exercising groups. However, only a combination of exercise and sweetened beverage intake also exhibited an increase in mRNA levels of adiponectin in white adipose tissue. Adiponectin is a circulating protein with a role in metabolism regulation and inflammation and is produced by more tissues, including the white adipose tissue and skeletal muscle [37]. Even though lower adiponectin levels are often observed in obese [38] and diabetic populations [39], exercise can restore plasma adiponectin concentration. This is metabolically relevant due to adiponectin’s insulin-sensitizing, anti-inflammatory, and antioxidant properties [38]. Similar to our results, it was previously reported that endurance training leads to increased adiponectin mRNA levels in mice fed a high-fat diet [40]. Our results suggest that exercise can improve adiponectin plasma concentration within both normal as well as unhealthy feeding. In the case of sugar-sweetened beverage intake, this effect is apparently related to alterations in the white adipose tissue.

There are certain limitations in our study that need to be considered. We measured only the white adipose tissue mRNA expressions, while methods determining protein levels would provide more detailed information. The gut motility, as well as plasma acetate concentration, was not monitored. Although not the aim of this study, changes in other bacterial genus may provide a deeper understanding of interactions between microbiota and exercise.

5 Conclusion

Our results demonstrate that spontaneous physical activity leads to the prevention of weight gain and improvement of lipid-related features of obesity and increases the plasma levels of adiponectin. It can also be concluded that spontaneous physical activity in young rats drinking sweetened cola is accompanied by increased abundance of lactobacilli in the fecal microbiota population. This suggests that lactobacilli may require an additional source of energy in the form of sugars present in the sugar-sweetened beverage used in this experiment: gut microbiota is known to metabolize fructose into short-chain fatty acids, which can serve as a source of energy for a skeletal muscle. This proposes a research area of interest – can lactobacilli in connection with exercise be directly involved in obesity prevention?

Acknowledgments

The authors gratefully acknowledge the help with critical reading of this manuscript from Dr. Hana Kinova Sepova and excellent technical assistance of Ms. Elena Vilemova.

  1. Funding information: This work was supported by grant from the Ministry of Education, Science, Research and Sport of the Slovak Republic VEGA 1/0195/20, by Comenius University Grant UK/101/2018 and Faculty of Pharmacy Grant FaFUK/31/2019.

  2. Conflict of interest: Authors state no conflicts of interest.

  3. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2021-12-21
Revised: 2022-03-28
Accepted: 2022-04-07
Published Online: 2022-06-27

© 2022 Margareta Marusakova et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
  3. The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
  4. Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
  5. LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
  6. Association study of CLDN14 variations in patients with kidney stones
  7. Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
  8. Regulation of miR-30b in cancer development, apoptosis, and drug resistance
  9. Informatic analysis of the pulmonary microecology in non-cystic fibrosis bronchiectasis at three different stages
  10. Swimming attenuates tumor growth in CT-26 tumor-bearing mice and suppresses angiogenesis by mediating the HIF-1α/VEGFA pathway
  11. Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
  12. Functional conservation and divergence in plant-specific GRF gene family revealed by sequences and expression analysis
  13. Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
  14. Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
  15. Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
  16. Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
  17. Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
  18. Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
  19. Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
  20. Nutrition intervention in the management of novel coronavirus pneumonia patients
  21. circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
  22. Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
  23. Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
  24. Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
  25. Comparison of axon extension: PTFE versus PLA formed by a 3D printer
  26. Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
  27. A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
  28. Study on the mechanism of inhibiting patulin production by fengycin
  29. SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
  30. Relationship between blood clots and COVID-19 vaccines: A literature review
  31. Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
  32. Bioinformatics network analyses of growth differentiation factor 11
  33. NR4A1 inhibits the epithelial–mesenchymal transition of hepatic stellate cells: Involvement of TGF-β–Smad2/3/4–ZEB signaling
  34. Expression of Zeb1 in the differentiation of mouse embryonic stem cell
  35. Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
  36. Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
  37. Assessment of the anesthetic effect of modified pentothal sodium solution on Sprague-Dawley rats
  38. Genetic susceptibility to high myopia in Han Chinese population
  39. Potential biomarkers and molecular mechanisms in preeclampsia progression
  40. Silencing circular RNA-friend leukemia virus integration 1 restrained malignancy of CC cells and oxaliplatin resistance by disturbing dyskeratosis congenita 1
  41. Endostar plus pembrolizumab combined with a platinum-based dual chemotherapy regime for advanced pulmonary large-cell neuroendocrine carcinoma as a first-line treatment: A case report
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  43. Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
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  46. Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
  47. MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
  48. Study of hsa_circRNA_000121 and hsa_circRNA_004183 in papillary thyroid microcarcinoma
  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
  51. Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
  54. Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
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  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
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  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
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  64. Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
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  68. Bacteriospermia – A formidable player in male subfertility
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  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
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https://doi.org/10.1515/biol-2022-0070
Schlagwörter für diesen Artikel
overweight; sweetened beverage; physical activity; fecal Lactobacillus abundance; adiponectin
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
  3. The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
  4. Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
  5. LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
  6. Association study of CLDN14 variations in patients with kidney stones
  7. Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
  8. Regulation of miR-30b in cancer development, apoptosis, and drug resistance
  9. Informatic analysis of the pulmonary microecology in non-cystic fibrosis bronchiectasis at three different stages
  10. Swimming attenuates tumor growth in CT-26 tumor-bearing mice and suppresses angiogenesis by mediating the HIF-1α/VEGFA pathway
  11. Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
  12. Functional conservation and divergence in plant-specific GRF gene family revealed by sequences and expression analysis
  13. Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
  14. Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
  15. Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
  16. Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
  17. Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
  18. Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
  19. Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
  20. Nutrition intervention in the management of novel coronavirus pneumonia patients
  21. circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
  22. Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
  23. Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
  24. Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
  25. Comparison of axon extension: PTFE versus PLA formed by a 3D printer
  26. Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
  27. A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
  28. Study on the mechanism of inhibiting patulin production by fengycin
  29. SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
  30. Relationship between blood clots and COVID-19 vaccines: A literature review
  31. Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
  32. Bioinformatics network analyses of growth differentiation factor 11
  33. NR4A1 inhibits the epithelial–mesenchymal transition of hepatic stellate cells: Involvement of TGF-β–Smad2/3/4–ZEB signaling
  34. Expression of Zeb1 in the differentiation of mouse embryonic stem cell
  35. Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
  36. Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
  37. Assessment of the anesthetic effect of modified pentothal sodium solution on Sprague-Dawley rats
  38. Genetic susceptibility to high myopia in Han Chinese population
  39. Potential biomarkers and molecular mechanisms in preeclampsia progression
  40. Silencing circular RNA-friend leukemia virus integration 1 restrained malignancy of CC cells and oxaliplatin resistance by disturbing dyskeratosis congenita 1
  41. Endostar plus pembrolizumab combined with a platinum-based dual chemotherapy regime for advanced pulmonary large-cell neuroendocrine carcinoma as a first-line treatment: A case report
  42. The significance of PAK4 in signaling and clinicopathology: A review
  43. Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
  44. Characterization of rabbit polyclonal antibody against camel recombinant nanobodies
  45. Active legumain promotes invasion and migration of neuroblastoma by regulating epithelial-mesenchymal transition
  46. Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
  47. MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
  48. Study of hsa_circRNA_000121 and hsa_circRNA_004183 in papillary thyroid microcarcinoma
  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
  51. Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
  54. Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
  55. Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
  57. β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
  58. Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
  59. BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
  60. Mucormycosis co-infection in COVID-19 patients: An update
  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
  63. Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
  64. Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
  65. Nasopharyngeal tuberculosis: A case report
  66. Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
  67. Aberrant pulmonary immune response of obese mice to periodontal infection
  68. Bacteriospermia – A formidable player in male subfertility
  69. In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
  70. Effects of KCa channels on biological behavior of trophoblasts
  71. Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
  72. Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
  73. Prognostic signature related to the immune environment of oral squamous cell carcinoma
  74. Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
  75. Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
  76. Role of MMP-2 and CD147 in kidney fibrosis
  77. Geometric basis of action potential of skeletal muscle cells and neurons
  78. Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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Heruntergeladen am 9.10.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0070/html
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