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Association of vitamin D status & miRNA-155 levels with disease severity in patients with dengue
For correspondence: Prof Silvio Urcuqui-Inchima, Grupo Inmunovirología, Facultad de Medicina, Universidad de Antioquia, 500 10, Antioquia, Colombia e-mail: silvio.urcuqui@udea.edu.co
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Received: ,
Accepted: ,
Abstract
Background & objectives
The clinical manifestation of dengue results from a complex and finely balanced interaction between the dengue virus (DENV) and the host immune responses, particularly excessive inflammation driven by pro-inflammatory cytokines. Vitamin D is an essential modulator of antiviral innate immunity, capable of reducing cytokine production and viral replication in vitamin D3-differentiated monocyte-derived macrophages (D3-MDM). It also downregulates inflammatory miRNAs, including miRNA-155. This study aimed to investigate serum levels of 25-hydroxyvitamin D [25(OH)D], cytokine production, and the expression of microRNA-155 (miRNA-155) in patients with dengue.
Methods
Serum samples were collected from 98 dengue-positive patients categorised as dengue without warning signs, dengue with warning signs, or severe dengue, along with 10 healthy individuals as controls. Clinical and laboratory data were also analysed.
Results
Serum 25(OH)D levels were significantly higher in dengue without warning as compared to other two categories. Although dengue with warning signs patients exhibited higher 25(OH)D levels than those with severe dengue, both groups showed a significant reduction compared to healthy controls. In contrast, miRNA-155 expression was highest in the severe dengue group, followed by dengue with warning signs, dengue without warning signs, and controls. A significant negative correlation was observed between serum 25(OH)D levels and miRNA-155 expression. Lower 25(OH)D concentrations were associated with elevated TNF-α, IL-6, and IFN-γ levels, particularly in patients with warning signs and severe dengue.
Interpretation & conclusions
These findings suggest a relationship between vitamin D status, miRNA-155 expression, and immune activation during dengue infection. The inverse correlation between 25(OH)D and miRNA-155 highlights their potential as disease severity and progression biomarkers in patients infected by dengue virus.
Keywords
Biomarker
cytokines
dengue virus
inflammation
microRNA
vitamin D
Dengue virus infections are classified into dengue without warning signs, with warning signs, and severe dengue1. Predicting disease progression remains challenging since non-severe cases may evolve into severe dengue. Identifying predictive markers is crucial for avoiding unnecessary hospitalisations and providing timely care for at-risk patients.
The mechanisms leading from dengue without warning signs to severe dengue are not fully understood, but a pro-inflammatory cytokine profile is believed to play a critical role. Cytokines, initially produced by monocytes, macrophages, and endothelial cells, and subsequently by T cells, are detectable in the serum of patients. Their excessive presence contributes to vascular leakage and endothelial damage, hallmarks of severe dengue. Beyond its role in calcium-phosphate metabolism, vitamin D [25(OH)D] has demonstrated immunomodulatory and antiviral effects in several viral infections, including dengue2-5. Given the cytokine imbalance in dengue, vitamin D may help control inflammation and reduce the severity of dengue6. While its antiviral mechanism remains unclear, vitamin D restricts dengue viral replication and regulates the innate immune response. Puerta-Guardo et al7 showed 1,25(OH)2D reduced DENV infection and proinflammatory cytokine production in Huh-7 and U937 cells. Our group previously found that vitamin D3-differentiated monocyte-derived macrophages (D3-MDMs) reduced dengue virus-2 (DENV-2) infection and inflammation by downregulating the mannose receptor8. Furthermore, high-dose vitamin D lowered the susceptibility of MDMs and monocyte-derived dendritic cells to DENV-2 and reducedpro-inflammatorycytokineproduction9-10.
MicroRNAs (miRNAs) are small, non-coding RNA molecules that regulate gene expression at the post-transcriptional level. They are key immune response regulators and influence DENV replication and host cell susceptibility11-15. Recent studies show that vitamin D modulates immune-related miRNAs, especially miRNA-15516,17. Arboleda et al18 reported that vitamin D downregulated miRNA-155 in DENV-infected D3-MDMs, increasing SOCS-1 expression, a negative regulator of TLR4 signaling4. This pathway may affect DENV outcomes, supporting the need to evaluate serum 25(OH)VD and miRNA-155 levels concerning disease severity. This study aimed to compare serum 25(OH)VD, miRNA-155, and proinflammatory cytokines in dengue patients by disease severity.
Materials & Methodology
This study was undertaken by the department of Microbiology and Parasitology, Faculty of Medicine, University of Antioquia, and Center of Biomedical Research, Faculty of Health Sciences, Quindío, Colombia. The study was conducted in accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committee of the University of Antioquia-SIU, Colombia. All study participants provided written informed consent after a clear explanation of the procedure. Venous blood samples were collected from all dengue patients and healthy individuals (HI) enrolled in the study.
Dengue patients and controls
One hundred and fifty individuals suspected of dengue infection were seen in the Molecular Immunology Group at the Faculty of Health Sciences, University of Quindío, during the study period (October 2014 to December 2015). They sought medical care at first-, second-, and third-level healthcare institutions in the Department of Quindío (Colombia), between October 2015 and February 2016. For these patients, complete blood count results at admission and follow up were considered as recorded in their clinical history and presenting symptoms. A physician evaluated individuals with dengue-like symptoms, administered a symptom questionnaire, and obtained informed consent. Individuals aged 4 and 76 yr were included. Exclusion criteria comprised individuals with autoimmune diseases, comorbidities, cancer, severe malnutrition, pregnancy, or those who did not sign the informed consent. Dengue classification was determined according to World Health Organization criteria. As a control group, 10 healthy individuals undergoing routine physical check-ups were recruited, and their negative status for DENV, HBV, HCV, and HIV-1 was confirmed through routine serological testing.
Dengue diagnostic tests
Laboratory confirmation of DENV infection was performed by detecting the NS1 antigen and DENV-specific IgM and IgG antibodies using the dengue NS1 antigen kit (Bio-Rad Laboratories, Marnes-la-Coquette, France), following the manufacturer’s instructions. For further confirmation, a dengue IgMELISA assay (Vircell Microbiologists, Granada, Spain)) was performed on samples that tested negative for NS1. All serum samples were separated, aliquoted, and stored at −80°C after routine diagnostic testing until further evaluation in this study.
Quantification of serum 25(OH)D level
Vitamin D status was assessed in dengue patients and controls by measuring serum 25(OH)D concentrations using an enzyme-linked fluorescent assay (ELFA, VIDAS ® 25 OH Vitamin D TOTAL, (bioMérieux S.A., Marcy-l’Étoile, France), following the manufacturer’s instructions.
RNA extraction
RNA was extracted from the same serum pools using the mirVanaTM miRNA isolation kit (Invitrogen, USA), following the manufacturer’s instructions. The purity and concentration of total RNA were assessed by measuring the absorbance ratio at 260/280 nm using the Epoch Spectrophotometer (Biotek, USA). All preparation and handling procedures were conducted under RNase-free conditions. Total RNA was stored at -70°C until used. Serum 18S rRNA was used as a constitutive gene for data normalisation.
cDNA synthesis and quantification of miRNA-155 using RT-qPCR
MicroRNA cDNA was synthesized from 10 ng/μL of total RNA using specific miRNA stem-loop primers and TaqMan MicroRNA reverse transcription kit (ThermoFisher Scientific, USA) following the manufacturer’s instructions. The cDNA was stored at -20°C. To quantify the miRNA-155 levels, RT-qPCR was performed in a 15 μL reaction using TaqManTM assays (Thermo Fisher Scientific, USA) on a Bio-Rad CFX PCR system under the following cycle conditions: 95°C for 10 min followed by 40 cycles of 95°C for 15 sec and 60°C for 1 min. miRNA-155 levels were normalized to 18S rRNA and control serum and calculated using the comparative Ct (2-∆∆Ct) method19, where Ct represents the cycle threshold. All PCR reactions were duplicated, and miRNA-155 data from serum samples were validated through two independent experiments.
Cytokines production
Serum levels of TNF-α, IL-6, and IFN-γ were quantified in the serum of dengue patients and healthy individuals using an ELISA kit (BD Biosciences, San Jose, CA), according to the manufacturer’s recommendations. All samples were analysed in duplicate to ensure accuracy and reproducibility.
Statistical analysis
Statistical analysis was performed using GraphPad Prism 5 (GraphPad Software Inc., San Diego, CA, USA). Cytokine levels among healthy individuals and various severity categories of patients with dengue were compared using the Kruskal-Wallis test with Dunn’s post-hoc test. The correlation between miRNA-155 and 25(OH)VD was assessed by linear regression. P< 0.05 was considered significant.
Results
Demographic and clinical characteristics of patients
This study included 150 clinically suspected dengue patients with acute febrile syndrome who attended a hospital in Armenia. Of these, 98 samples were confirmed as dengue-positive (either by dengue IgM antibody, DENV-NS1, or both) and were included in the study, as they met all laboratory test requirements. Ten healthy individuals were included as a control group. Table presents the demographic characteristics, including age and sex, along with clinical data for each dengue patient group. There were no significant differences in gender distribution among the groups. None of the patients received vitamin D supplementation before or during the study.
| Clinical features | Dengue without warning signs (n=28) |
Dengue with warning signs (n=53) |
Severe dengue (n=17) |
|---|---|---|---|
| Age, yr [mean (SD)] | 30 (±15) | 33 (±18) | 51 (±23) |
| Fever | 12 (43%) | 24 (45%) | 11 (65%) |
| Vomiting | 6 | 16 | 6 |
| Jaundice | 0 | 0 | 3 |
| Eye pain | 10 | 20 | 8 |
| Arthralgia | 5 | 14 | 7 |
| Rash | 6 | 13 | 4 |
| Diarrhoea | 7 | 17 | 5 |
| Epistaxis | 1 | 8 | 0 |
| Pulmonary oedema | 0 | 19 | 4 |
| Abdominal pain | 7 | 22 | 11 |
| Headache | 11 | 9 | 3 |
| Petechiae | 2 | 0 | 8 |
| Altered consciousness | 0 | 0 | 5 |
| Hepatomegaly | 0 | 1 | 3 |
| Splenomegaly | 0 | 20 | 6 |
| Myalgia | 8 | 19 | 0 |
SD, standard deviation
Serum levels of TNF-α, IL-6, and IFN-γ in dengue patients
During the acute febrile phase of infection, patients with dengue exhibited significantly elevated serum TNF-α levels compared to controls (Fig. 1A). IL-6 levels were significantly higher in patients with severe dengue, compared to the rest. Patients with dengue with warning signs showed significantly higher IL-6 levels than those without warning signs and controls (Fig. 1B). Patients with severe dengue exhibited significantly higher IFN-γ levels compared to those without warning signs. Patients with warning signs had substantially higher IFN-γ levels than those without warning signs and healthy controls (Fig. 1C).
- Serum cytokine levels in dengue patients and healthy individuals. The concentrations of (A) TNF-α, (B) IL-6, and (C) IFN-γ were analysed in the serum of DwoWS, DwWS, SD, and HI. Cytokines were measured using an ELISA test. Statistical analysis was performed using the Kruskal–Wallis test. P*< 0.05; **< 0.01; ***< 0.001 were considered significant difference. DwoWS, dengue without warning signs; DwWS, dengue with warning signs; SD, severe dengue; HI, healthy individuals.
Serum 25(OH)VD andmiRNA-155 levels
As shown in figure 2A, serum 25(OH)D levels were significantly lower in dengue patients compared to the control group. Highest 25(OH)D levels were observed in controls (44±8 ng/mL), followed by dengue without sign (33±7 ng/mL) and dengue with warning sign (25±6. ng/mL). Lowest levels were found in patients with severe dengue (20±5 ng/mL) patients without warning signs exhibited significantly higher 25(OH)D levels than those with warning signs and severe dengue. Individuals with warning signs had significantly higher 25(OH)D levels compared to severe dengue (Fig. 2A). Serum 25(OH)D level were lowest in severe dengue.
- Levels of 25(OH)VD and microRNA-155 expression in the serum of dengue patients and healthy individuals. (A) Serum 25(OH)VD levels and (B) microRNA-155 expression are shown for the study cohort divided into groups. (C) Correlation analysis between serum microRNA-155 expression and 25(OH)VD levels in patients infected with DENV. Data were analysed using linear regression. r = Pearson correlation coefficient; R2 = Coefficient of determination.
Serum miRNA-155 levels increased in a severity-dependent manner (Fig. 2B), being highest in severe dengue (15 ± 1 ng/mL) followed by dengue with warning signs (13± 1 ng/mL), dengue without warning signs (10 ± 1ng/mL) and controls (6 ± 3 ng/mL). Patients with severe dengue exhibited significantly elevated levels of miRNA-155 as compared to other categories (Fig. 2B). Patients with warning signs had substantially higher miRNA-155 levels than less severe categories and controls. The results suggest that miRNA-155 may play a crucial role in dengue pathogenesis due to its significant impact on inflammatory response. Furthermore, as previously reported18, vitamin D may mediate the downregulation of microRNA-155 in dengue patients, which appears to be closely associated with dengue disease progression.
Serum 25(OH)VD and microRNA-155 levels correlate negatively with dengue severity
Figure 2C reveals an inverse correlation between serum 25(OH)VD and miRNA-155 levels (r=-0.5; P<0.0001), indicating that vitamin D downregulates microRNA-155 expression.
Discussion
This study assessed serum cytokines, 25(OH)D levels, and miRNA-155 expression in dengue patients across severity groups. TNF-α levels were significantly higher in patients with dengue than in healthy individuals. Elevated TNF-α has been linked to vascular leakage and severe outcomes in Brazil, Tahiti, and French Polynesia. IL-6, secreted by T cells, macrophages, and NK cells, was significantly increased only in severe dengue. IL-6 promotes the release of IL-8, VEGF, and MCP-1, while reducing E-cadherin, contributing to endothelial permeability and plasma leakage20. We also observed increased IFN-γ levels in severe dengue. The increased concentrations of IFN-γ detected in individuals with dengue may indicate a heightened inflammatory response, which could contribute to the progression of the disease and be associated with less favourable clinical outcomes. Therefore, controlled cytokine secretion is essential to prevent disease progression21. Previously, we reported that vitamin D3-differentiated MDMs reduced DENV infection and modulated cytokine responses8. Vitamin D regulates cytokines via NF-κB modulation and VDR-dependent gene expression22.
Our current findings expand upon these observations. Serum 25(OH)D levels were significantly lower in patients with severe dengue and those with warning signs. Low vitamin D concentrations were associated with elevated levels of IL-6, IFN-γ, and TNF-α, particularly in these patients. These results align with Ahmed et al23, who showed that vitamin D suppresses cytokine storms in SARS-CoV-2 infection.
Unlike tissue miRNAs, circulating miRNA-155 has not been extensively studied in dengue. In previous work, we found that miRNA-155 was upregulated following DENV-2 infection but downregulated in D3-MDMs188. Here, our results showed an elevated expression of miRNA-155 in the serum samples obtained from severe dengue and those with warning signs, compared to those without warning signs and controls. This finding is of particular relevance given that endothelial dysfunction mediated by pro-inflammatory factors characterizes severe dengue.
The observed inverse relationship between vitamin D status and miRNA-155 expression implies that vitamin D deficiency may disrupt the regulation of miRNA-155, potentially amplifying pro-inflammatory response and exacerbating disease progression. Considering the immunomodulatory roles of vitamin D, its deficiency could compromise both antiviral defences and anti-inflammatory mechanisms, whereas heightened miRNA-155 levels may sustain inflammatory signalling and promote endothelial dysfunction. These results suggest that miRNA-155 is a critical contributor to dengue pathogenesis. The link between vitamin D status and miRNA-155 regulation has been previously documented. Chen et al24 demonstrated that activation of vitamin D receptor pathway attenuates inflammation through modulation of miRNA-155-SOCS1 axis. In accordance with these findings, our data suggest that elevated miR‐155 expression in patients with severe forms of dengue may downregulate SOCS1, thereby enhancing IFN‐γ production. This, in turn, may further induce miRNA-155 expression, establishing a self-reinforcing loop that contributes to sustained inflammation and disease severity. Thus, the immunomodulatory action of vitamin D during DENV infection may involve the suppression of miR-155, leading to tighter regulation of inflammatory response and potentially reducing the risk of progression to severe dengue. This is especially significant considering that miR-155 is a powerful modulator of immune and inflammatory pathways. Vitamin D status could thus represent a complementary biomarker in the clinical assessment of dengue, potentially aiding in differentiating between mild, moderate, and severe manifestations of the disease.
It has been demonstrated that vitamin D can suppress the expression of miR-155-5p which is also recognised as a key modulator of antiviral immunity. Experimental studies have demonstrated that miRNA-155 overexpression can confer protection in murine models of DENV and West Nile Virus infection by lowering viral load and enhancing IFN-mediated responses24-26. Su et al24 reported that miR-155 may exert a protective effect against DENV by promoting an IFN-dependent antiviral mechanism. Supporting this notion, a study in a resistant Thai population also identified elevated miR-155 expression as a potential contributor to host resistance27. While these findings suggested that miRNA-155 modulation could be a promising therapeutic approach, the divergent outcomes reported across studies underscore the need for further investigation to delineate its precise role in DENV infection. In conclusion, our findings revealed a gradient of serum vitamin D levels corresponding to dengue severity and thus could serve as a useful diagnostic biomarker to support early risk assessment and guide clinical decision-making in dengue cases. This hypothesis aligns with prior in vitro studies demonstrating that monocyte-derived macrophages and dendritic cells from vitamin D-supplemented healthy donors show reduced susceptibility to DENV infection9,28.
Although this study provides important and valuable insights into the role of vitamin D and miRNA-155 in the pathogenesis of dengue patients, several limitations should be acknowledged and considered. One notable constraint is the limited number of healthy controls, which may reduce the robustness and generalizability of the comparative analysis. Further, our investigation was limited to the measurement of three proinflammatory cytokines in serum, excluding key anti-inflammatory markers such as IL-10 and TGF-β. The inclusion of these mediators could have contributed to a more nuanced understanding of the immune regulatory milieu in dengue infection.
To conclude, our results demonstrated that reduced serum vitamin D levels correlated with heightened proinflammatory cytokine production and increased miRNA-155 expression in patients with severe forms of dengue. These findings suggest a potential antiviral and immunomodulatory role for vitamin D during DENV infection, which the suppression of microRNA-155 expression may mediate. This dual action, restraining excessive inflammation while supporting antiviral defences, highlights the protective potential of vitamin D in dengue pathogenesis. As such, both vitamin D and miRNA-155 represent promising molecular targets for the development of future therapeutic strategies aimed at mitigating immune dysregulation and limiting viral replication.
Financial support & sponsorship
This study was financially supported by Colciencias/MinCiencias (grant No. 111556933443) and Universidad de Antioquia-CODI.
Conflicts of Interest
None.
Use of Artificial Intelligence (AI)-Assisted Technology for manuscript preparation
The authors confirm that there was no use of AI-assisted technology for assisting in the writing of the manuscript and no images were manipulated using AI.
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