Abstract
Background
Obesity is a public health problem that increases the risk of type 2 diabetes, coronary heart disease, and cancer, and is associated with increased mortality. These comorbidities are thought to develop due to hyperinsulinemia, chronic inflammation, and reactive oxygen species. Recently, the effect of epigenetic factors on the development of obesity and comorbidities is emphasized.
Aim
In this study, the relationship between lncRNA-p5549 and associated TDG gene expressions with obesity, metabolic-inflammatory status and bariatric surgery was investigated.
Methods
33 patients between the ages of 18 and 65 who underwent LSG operation participated in our study. In addition, 33 healthy volunteers between the ages of 18–65, who were compatible with these patients in terms of age and gender, were included in the study. Demographic characteristics and routine biochemical assays of the patients were recorded. For expression analyses, RNA was isolated from the serum.
Results
Increased lncRNA and TDG gene expression in obese individuals has decreased to the level of healthy control after bariatric surgery.
Conclusion
The decrease in TDG gene expression associated with LncRNA-p5549 and DNA repair after surgery suggests that bariatric surgery reduces DNA damage.
Supplementary Information
The online version contains supplementary material available at 10.1186/s13098-025-01809-2.
Keywords: Obesity, Bariatric surgery, LncRNA, DNA repair
Introduction
The primary goals of treatment in obesity are to improve obesity-related comorbid conditions and quality of life, and to reduce the risk of developing obesity-related complications. Obesity treatment always begins with lifestyle changes and continues with pharmacotherapy or bariatric surgery, depending on the BMI risk category [1].
Non-coding RNAs (ncRNA) have emerged as relevant transcriptional factors in physiological and pathophysiological situations; therefore, gene silencing with their use can be used as a therapeutic strategy [2]. LncRNAs are defined as RNA molecules with more than 200 nucleotides present in a large number in the genome. LncRNAs form a new class of RNAs that regulate gene expression; they are involved in regulating the expression of several genes of related cellular functions. They are also involved in post-transcriptional regulation as well as chromatin remodeling [3].
Few studies have investigated the modulation of lncRNA expression after bariatric surgery, and most of these have been performed in animal models. Investigation of altered expressions related to metabolism and endocrine regulation requires further research to identify potential therapeutic targets for obesity [4].
There are 11 identified DNA glycosylases in mammalian cells. DNA glycosylases recognize bases that are not suitable. It removes by hydrolysis of the N-glycosidic bond between deoxyribose sugar and base. Each recognizes a defined group of DNA lesions [5]. Although DNA glycosylases have different structures and substrate selectivity, they have a common mechanism of action.
Thymine DNA glycosylase (TDG) is also one of the DNA glycosylases that initiates the BER DNA repair pathway. TDG removes fragments of the thymine from G/T mismatches. With lower activity, this enzyme also clears the thymine from C/T and T/T mismatches. TDG can also remove uracil and 5-bromouracil from mispairings with guanine [6].
Most of the evidence suggests that lncRNA expression may regulate the expression of neighboring mRNAs and have high correlations of expressions with them [7]. Accordingly, a study has shown that lncRNA-p5549 is associated with thymine-DNA glycosylase (TDG) by bioinformatic analyses [4].
Previous studies have shown that increased BMI is associated with higher DNA damage, but data on weight loss and possible reduction of DNA damage are insufficient so far. This may be due to the fact that effective weight loss is very difficult to achieve and maintain in human study groups and / or that reduction of DNA damage occurs only after major weight loss or can only be detected in people with very high BMI. Therefore, it has been suggested that surgical intervention is the most effective option that can show that DNA repair capacity increases [8, 9].
In a study by Sun et al.(2016), it was observed that the expression of circulating lncRNA-p5549, lncRNA-p21015, and lncRNA-p19461 was down-regulated in obese individuals compared to healthy controls. In this study, it was also predicted bioinformatically that lncRNAs and co-expressed mRNAs play a role in the response to DNA damage. lncRNA-p5549 has been associated with thymine-DNA glycosylase (TDG), which is involved in DNA repair, DNA demethylation and transcriptional regulation [4].
With this study, we aim to isolate total RNA from blood samples taken from obesity patients before and after obesity surgery and from healthy individuals, and to investigate the expression of lncRNA-p5549 and the related TDG gene. Our goal is to compare these three groups in terms of DNA repair.
Materials and methods
33 patients between the ages of 18 and 65 who underwent LSG operation between March 2022 and September 2022 at Pamukkale University General Surgery Clinic participated in our study. In addition, 33 healthy volunteers between the ages of 18–65, who were compatible with these patients in terms of age and gender, were included in the study.
Demographic characteristics of the patients (age, gender, height (cm), weight (kg), BMI (kg/m2), waist circumference (cm), body fat composition (Tanita MC 580 body analyzer)) were recorded. Routine assays (fasting glucose, fasting insulin, c-peptide, HOMA-IR, triglyceride, total cholesterol, HDL, LDL, CRP) showing the metabolic table were recorded. All patients underwent laparoscopic sleeve gastrectomy surgery. No intraoperative and postoperative complications were detected. Height (cm), weight (kg), body fat composition, waist circumference (cm) were measured and BMI (kg/m2) was recorded in the outpatient clinic controls of the patients at the postoperative 3rd month. Routine analyses showing the postoperative metabolic table were recorded.
In addition to the patient group, anthropometric measurements including body mass index (BMI, kg/m²), waist circumference (cm), and body fat percentage (%) were also obtained from the healthy control group using the Tanita MC 580 body composition analyzer. These values were recorded at a single time point.
Venous blood samples were taken from healthy volunteers and patients (separately in the preoperative and 3rd month controls) through the arm, 5-10 cc in 1 Yellow Lid Vacuum Plastic Gel Tube. Blood samples were obtained after overnight fasting. Serum was obtained by centrifuging the blood samples at + 4 °C at 2500 rpm for 10 min. Serums obtained until the completion of the study samples were stored at -80 °C.
Serum RNA isolation
RNA isolation from serum samples was performed according to the relevant kit protocol using Total RNA Purification Kit (Norgen).
cDNA synthesis
For expression analysis, cDNA conversion was performed in accordance with the relevant kit protocol (Biorad).
Expression analysis
real-Time PCR was performed in accordance with the kit protocol for lncRNA-p5549, 18s RNA, TDG and GAPDH-specific primer and SYBR Green master mix (Biorad).
Statistical analysis
Data were analyzed using SPSS package program. Continuous variables were given as mean ± standard deviation and categorical variables as numbers and percentages. In addition, the relationships between continuous variables were examined by Spearman or Pearson correlation analysis, and the differences between categorical variables were examined by Chi-square analysis. PCR data were quantified with a computer program using the ΔΔCT method. Volcano Plot analyses, which are available in the web-based “RT² Profiler™ PCR Array Data Analysis” program, were used. The comparison of the groups was statistically evaluated with the “Student t-test” analysis in the “RT² Profiler™ PCR Array Data Analysis” program.
Results
Anthropometric and metabolic characteristics of patients
33 patients between the ages of 18 and 65 who underwent LSG surgery between March 2022 and September 2022 participated in our study. In addition, 33 healthy volunteers between the ages of 18–65, who were compatible with these patients in terms of age and gender, were included in the study. The mean age of the patients included in our study was 36 ± 13, and the mean age of healthy volunteers was 34 ± 10 (p:0.774). Of the 66 patients included in the study, 35 were female (53%) and 31 were male (47%). There was no significant difference between the groups in terms of gender distribution (p:0.722).
T2D was present in 4 (12%) of the patient group.
Anthropometric and metabolic characteristics of the participants are summarized in the Table 1.
Table 1.
Anthropometric and metabolic characteristics of the participants
| Healthy Control (n:33) | Obesity Patients (n:33) | Postoperative 3rd month (n:33) | p value | |
|---|---|---|---|---|
| Age | 36 ± 13 | 34 ± 10 | - | 0,774 |
| Gender (woman/man) | 18/15 | 17/16 | - | 0,722 |
| BMI (kg/m2) | 22.0 ± 2.0 | 44,07 ± 6,64 | 35,39 ± 5,64 | 0,000 |
| Waist circumference (cm) |
75.0 ± 6.0 (female) 85.0 ± 7.0 (male) |
136,00 ± 25,54 | 110,54 ± 19,39 | 0,001 |
| Body fat percentage (%) |
26.0 ± 5.0 (female) 16.0 ± 4.0 (male) |
45,59 ± 4,76 | 38,91 ± 5,71 | 0,000 |
| Fasting glucose (mg/dL) | 88,91 ± 7,94 | 104,31 ± 32,00 | 92,72 ± 20,95 | 0,060 |
| Fasting insulin (µmol/mL) | 7,14 ± 3,12 | 21,10 ± 10,90 | 8,93 ± 4,66 | 0,000 |
| Fasting C-peptide (ng/dL) | 2,34 ± 1,85 | 3,35 ± 1.25 | 2,50 ± 0,89 | 0,016 |
| HOMA-IR | 1,60 ± 0,75 | 5,64 ± 3,00 | 2,04 ± 1,20 | 0,000 |
| Total cholesterol (mg/dL) | 166,58 ± 40,44 | 184,40 ± 34,74 | 183,72 ± 34,24 | 0,180 |
| Fasting triglyceride (mg/dL) | 110,87 ± 50,02 | 134,45 ± 61,92 | 102,27 ± 39,61 | 0,105 |
| HDL cholesterol (mg/dL) | 46,87 ± 14,73 | 47,68 ± 10,82 | 49,04 ± 13,23 | 0,852 |
| LDL cholesterol (mg/dL) | 97,54 ± 35,08 | 109,86 ± 35,22 | 116,13 ± 28,18 | 0,158 |
| CRP (mg/dL) | 4,94 ± 4,58 | 8,10 ± 8,15 | 3,60 ± 4,25 | 0,039 |
When the 3 groups were compared in terms of the changes of other biochemical variables, no significant difference was found.
Expression analyses
TDG was expressed up to 2.16 times in obesity patients compared to healthy participants. (p:0.151)
TDG showed 1.63 times increased expression in the postoperative clinical controls of the patients compared to the healthy participants. (p:0.247)
lncRNA was expressed up to 2.78 times in obesity patients compared to healthy participants. (p:0.03)
LncRNA showed 1.54 times increased expression in the postoperative clinical controls of the patients compared to the healthy participants (p:0.323).
Expression results are summarized in Fig. 1.
Fig. 1.
The lncRNA-p5549 and TDG expression analyse results in preoperative and postoperative patients
| Preoperative | p | Postoperative | p | |
|---|---|---|---|---|
| TDG | 2.16 | 0,039 | 1.54 | 0,297 |
| lncRNA-p5549 | 2.78 | 0,151 | 1.63 | 0,247 |
Correlations of patient variables and expression analyses
A positive correlation was found between TDG and lncRNA-p5549 according to Pearson correlation (0.391) (p:0.001).
Significant positive correlations were found between BMI and waist circumference (0.915, p:0.000), body fat percentage (0.818, p:0.000), CRP (0.523, p:0.000), fasting insulin (0.468, p:0.001), HOMA-IR (0.531, p:0.000), and C-peptide (0.314, p:0.038) according to Pearson correlation.
A negative correlation was obtained between BMI and LDL cholesterol according to Pearson correlation (-0.373) (p:0.013).
Significant positive correlations were found between waist circumference and body fat percentage (0.668, p:0.000), CRP (0.394, p:0.008), C-peptide (0.438, p:0.003), fasting insulin (0.564, p:0.000), and HOMA-IR (0.593, p:0.000) according to Pearson correlation.
Negative correlations were obtained between waist circumference and total cholesterol (-0.321) (p:0.034), and LDL cholesterol (-0.371) (p:0.013) according to Pearson correlation.
Significant positive correlations were found between body fat percentage and CRP (0.501, p:0.001), fasting glucose (0.305, p:0.044), and HOMA-IR (0.380, p:0.011) according to Pearson correlation.
A negative correlation was obtained between body fat percentage and LDL cholesterol according to Pearson correlation (0.389) (p:0.009).
A positive correlation was obtained between fasting insulin and triglyceride according to Pearson correlation (0.482) (p:0.000).
A negative correlation was obtained between fasting insulin and HDL cholesterol according to Pearson correlation (-0.267) (p:0.028).
Significant positive correlations were found between C-peptide and triglycerides (0.390, p:0.001) and HOMA-IR (0.557, p:0.000) according to Pearson correlation.
Significant correlations were found between C-peptide and HDL cholesterol (-0.283, p:0.019), HOMA-IR and triglycerides (0.515, p:0.000), HOMA-IR and HDL cholesterol (-0.294, p:0.015), and triglycerides and HDL cholesterol (-0.336, p:0.005) according to Pearson correlation.
These results suggest that bariatric surgery not only contributes to metabolic improvement but may also reduce DNA damage, as reflected by the downregulation of TDG and lncRNA-p5549 expression postoperatively. This highlights the potential role of these markers in monitoring epigenetic recovery following metabolic surgery.
Discussion
In recent years, studies have increasingly focused on epigenetics due to the growing evidence linking environmental factors with a heightened susceptibility to obesity and its comorbidities [10]. These studies propose epigenetic modifications as early prognostic markers for conditions such as obesity and offer a framework for designing personalized prevention and treatment strategies based on individual metabolic risk [11].
There are multiple reports indicating differential expression of lncRNAs between obese and non-obese populations. For instance, Sun et al. observed decreased expression of three lncRNAs (lncRNA-p5549, lncRNA-p21015, and lncRNA-p19461) in obese individuals, and noted an upregulation of lncRNA-p19461 following a 12-week dietary intervention [4]. Most studies investigating changes in lncRNA expression following weight loss interventions are based on animal models. In one such study, duodeno-jejunal bypass surgery led to the upregulation of 232 and downregulation of 69 lncRNAs in mice, several of which were linked to inflammation and insulin pathways and proposed as biomarkers for therapeutic response to bariatric surgery [19].
Although the effects of bariatric surgery on metabolic and clinical outcomes have been well established, its impact on DNA damage and repair pathways remains largely unexplored. In this study, we examined the expression of DNA repair-related lncRNA-p5549 and its associated gene TDG in obese patients undergoing sleeve gastrectomy, comparing the results to those from healthy controls.
The mean BMI in our patients decreased significantly—from 44.07 ± 6.64 to 35.39 ± 5.64—within just three months, with a mean weight loss of 19.65%. This is consistent with previous studies demonstrating postoperative improvements in metabolic parameters and oxidative stress, such as the one reporting a reduction from a BMI of 46.22 ± 5.33 preoperatively to 37.1 ± 5 after three months and 31.2 ± 5 after one year [13].
Consistent with known associations, BMI in our study was positively correlated with waist circumference and body fat percentage, and inversely correlated with LDL cholesterol. CRP levels in the postoperative group were found to approach those of healthy controls. These observations suggest that reduced adiposity leads to a lower inflammatory burden. Previous studies have reported that CRP correlates with insulin resistance, and some experimental data support the hypothesis that CRP itself may contribute to this resistance [16, 17]. Notably, one study reported changes in CRP and insulin resistance following gastric bypass surgery that were independent of body weight reduction [18].
In our study, lncRNA-p5549 expression was 2.78-fold higher in obese individuals compared to controls, and decreased postoperatively. This contrasts with the findings by Sun et al., where lncRNA-p5549 was downregulated in obese patients and did not significantly change after a three-month low-carbohydrate diet [4]. The mean BMI and waist circumference of participants in Sun’s study were considerably lower than those in our cohort, and the mean weight loss was just 8%, compared to nearly 20% in our group. Our patients also exhibited higher HOMA-IR and CRP levels, suggesting a more pronounced inflammatory and metabolic disturbance.
These differences may explain the contrasting expression patterns of lncRNA-p5549 and underscore the influence of BMI, adiposity, and systemic inflammation on gene regulation. Sun et al. also reported a negative correlation between plasma lncRNA-p5549 levels and BMI, waist circumference, and fasting insulin, which may further reflect population-specific variations in inflammatory profiles and gene expression dynamics.
Moreover, although Sun et al. demonstrated higher expression of lncRNA-p5549 in adipose tissue compared to plasma, they did not observe a correlation with BMI in adipose samples. In our study, no correlation was detected between plasma lncRNA-p5549 expression and BMI, waist circumference, body fat percentage, fasting glucose, fasting insulin, triglycerides, HOMA-IR, or CRP. These findings support the notion that lncRNA expression may be modulated by multifactorial influences such as age, sex, ethnicity, comorbid conditions, and environmental exposures.
Importantly, we investigated TDG expression as a novel marker of DNA repair. In obese individuals, TDG expression was elevated by 2.16-fold relative to healthy controls, and subsequently decreased after surgery. These results suggest that bariatric surgery may reduce DNA damage, potentially by lowering inflammation and reactive oxygen species, thereby diminishing the cellular need for DNA repair.
The relationship between lncRNA-p5549 and TDG was initially proposed through bioinformatics analyses in the study by Sun et al. [4]. Our results provide clinical evidence supporting this interaction and highlight the potential regulatory axis of lncRNA-p5549 and TDG in the context of obesity-related DNA damage.
In addition to DNA repair mechanisms, recent studies highlight the importance of intracellular signaling pathways in the regulation of postoperative metabolic recovery. In particular, the TFF3/PI3K/Akt pathway has emerged as a key player in energy metabolism and insulin sensitivity restoration following bariatric surgery. Combining lncRNA-mediated epigenetic regulation analysis with pathway-specific interventions, such as TFF3 activation, may open new avenues for treating obesity-related comorbidities. Such integrated approaches could strengthen the therapeutic potential of epigenetic biomarkers and improve personalized treatment strategies for metabolic diseases [20].
Future research should include functional validation studies, such as lncRNA-p5549 gene silencing or overexpression, to elucidate the direct regulatory relationship between lncRNA-p5549 and TDG. These approaches will provide mechanistic insights and strengthen the evidence base for understanding how lncRNA-mediated pathways contribute to DNA damage repair and inflammation resolution in obesity.
Conclusion
In this study investigating DNA repair-related lncRNA-p5549 and associated TDG gene expressions that can prove weight loss and reduced DNA damage in preoperative and postoperative blood samples of patients scheduled for sleeve gastrectomy compared to healthy controls, the expression of both genes increased significantly and decreased postoperatively in the obesity group. It was confirmed in our study that the expressions of these two genes associated with database analyses were correlated.
Accordingly, it can be suggested that the increased DNA repair activity in obese patients decreases postoperatively, so DNA damage may have decreased.
The investigation of molecular and epigenetic mechanisms that are thought to underlie postoperative metabolic and inflammatory recovery in obesity patients continues to require new scientific contributions.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Author contributions
B.E.R and S.Y wrote the main manuscript text, E.D.Y and M.R.A collected samples and B.E.R, S.Ş and İ. A. did the experiments. All authors reviewed the manuscript.
Funding
This study was supported by Pamukkale University Scientific Research Projects Coordination Unit’s decision dated 21-07-2022 and numbered 2022TIPF023.
Data availability
No datasets were generated or analysed during the current study.
Declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Footnotes
Publisher’s note
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Contributor Information
Sevda Yilmaz, Email: s.yilmaz@pau.edu.tr.
Buket Er Urganci, Email: aber@pau.edu.tr.
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Associated Data
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Supplementary Materials
Data Availability Statement
No datasets were generated or analysed during the current study.