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Dysregulated expression of microRNAs in aqueous humor from intraocular tuberculosis patients

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Abstract

Background

Systemic Mycobacterium tuberculosis (Mtb) infection alters microRNA’s expression that controls cellular processes and modulates host defense mechanisms. However, the role of miRNAs in intraocular tuberculosis (IOTB) remains unknown. Therefore, this study aims to identify dysregulated miRNAs in the aqueous humor (AH) of patients with IOTB.

Methods

AH from intraocular tuberculosis patients (n = 2) and cataract controls (n = 2) were used for small RNA deep sequencing using HiSeq Illumina sequencing platform. Differentially expressed miRNAs and their targets were identified by the bioinformatics approach, and their regulatory functions were predicted by pathway enrichment analysis. The expression of selected miRNAs and their binding targets were further validated by real-time quantitative PCR (RT-qPCR).

Results

In total, we identified 56 differentially expressed miRNAs in the AH of intraocular tuberculosis (IOTB) patients compared to controls. We selected four significantly dysregulated miRNAs (miR-423-5p, miR-328-3p, miR-21-5p, and miR-16-5p) based on the RT-qPCR validation and predicted their gene targets. We developed a miRNA-targets regulatory network by combining pathways of interest and genes associated with TB. We identified that these four miRNAs might play an important role in IOTB pathogenesis via tuberculosis-associated pathways; PI3K-Akt signaling, autophagy and MAPK pathway.

Conclusions

For the first time, this study identifies the dysregulation of four miRNAs in the AH of IOTB patients using the ultra-low input small-RNA sequencing approach. Further target prediction and validation identify the role of these miRNAs in tuberculosis pathogenesis via tuberculosis-related pathways. This study identifies miRNAs as potentially ideal biomarkers in the aqueous humor of IOTB patients.

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Fig. 1
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Data availability

All data generated during this study are included in this article and its additional files.

Abbreviations

AH:

Aqueous humor

Mtb :

Mycobacterium tuberculosis

IOTB:

Intraocular tuberculosis

PCR:

Polymerase chain reaction

miRNA:

MicroRNA

TB:

Tuberculosis

HIV:

Human immunodeficiency virus

LTB:

Latent tuberculosis

NGS:

Next generation sequencing

OTB:

Ocular tuberculosis

PTB:

Pulmonary tuberculosis

DNA:

Deoxyribonucleic acid

CAT:

Cataract

RNA:

Ribonucleic acid

STAR:

Spliced transcripts alignment to a reference

DAVID:

Database for annotation, visualization, and integrated discovery

FDR:

False discovery rate

P-value:

Calculated probability

KEGG:

Kyoto encyclopedia of genes and genomes

cDNA:

Complementary DNA

SRA:

Sequence read archive

ATT:

Anti-tuberculosis therapy

DE:

Differential expression

TST:

Tuberculin skin test

CT:

Computerized tomography

MAPK9:

Mitogen-activated protein kinase 9

VPS33A:

Vacuolar protein sorting-associated protein 33A

IL-1B:

Interleukin 1 beta

CREB1:

Cyclic AMP-responsive element-binding protein 1

CTSD:

Catepsin D

CEBPB:

CCAAT/enhancer-binding protein beta

RAB5B:

Ras-related protein Rab-5B

SRC:

Proto-oncogene tyrosine-protein kinase Src

APAF1:

Apoptotic protease- activating factor 1

IRAK2:

Interleukin-1 receptor-associated kinase-like 2

MRC2:

Mannose receptor, C type 2

CD209:

DC-SIGN

ATP6VOD1:

V-ATPase

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Acknowledgements

The authors thank the Uvea Clinic, Aravind Eye Hospital, Madurai, India, for the IOTB samples, and Dr. Madhu Shekar, Aravind Eye Hospital, for cataract control samples. We also thank Department of Biotechnology (DBT), India for funding support and Indian Council of Medical Research (ICMR), India for Senior Research Fellowship.

Funding

Department of Biotechnology, India (No: BT/PR20733/MED/29/1075/2016), Senior Research Fellow -Indian Council of Medical Research (ICMR), India (Sanction letter No. 2019-4013/Gen-BMS dt.30.09.2019).

Author information

Authors and Affiliations

  1. Department of Microbiology and Bioinformatics, Aravind Medical Research Foundation, 1, Anna Nagar, Madurai, Tamil Nadu, 625 020, India

    Swathi Chadalawada, Kandasamy Kathirvel & Bharanidharan Devarajan

  2. Biomedical Sciences, Madurai Kamaraj University, Madurai, India

    Swathi Chadalawada

  3. Department of Microbiology, Aravind Eye Hospital, Madurai, India

    Prajna Lalitha

  4. Uveitis Service, Aravind Eye Hospital, Madurai, India

    S. R. Rathinam

  5. School of Chemical and Biotechnology, SASTRA Deemed to be University, Thanjavur, India

    Kandasamy Kathirvel

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  1. Swathi Chadalawada
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  2. Kandasamy Kathirvel
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  3. Prajna Lalitha
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  4. S. R. Rathinam
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  5. Bharanidharan Devarajan
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Contributions

SC: Data curation, Formal analysis, Writing- Original draft preparation KK: NGS data analysis, Reviewing PL: Reviewing and Editing RS: Resources, Investigation, Reviewing and Editing BD: Conceptualization, Methodology, Writing- Reviewing and Editing.

Corresponding author

Correspondence to Bharanidharan Devarajan.

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Conflict of interest

All the authors declared that they have no conflict of interest.

Ethical approval

This study was approved by the Institutional Ethics Committee of Aravind Eye Hospital, Madurai, Tamil Nadu, India (IRB2017007BAS).

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Supplementary Information

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11033_2021_6846_MOESM1_ESM.tif

Supplementary file1 (TIF 204 kb). Additional file 1: Supplementary Figure S1. The expression analysis of selected thirteen miRNAs in aqueous humor of IOTB patients (N=7) and Cataract controls (N=7) using RT-qPCR. Median values are showed in horizontal lines using a Mann-Whitney test. *P<0.05, ** P<0.01, *** P<0.001

11033_2021_6846_MOESM2_ESM.tif

Supplementary file2 (TIF 372 kb). Additional file 2: Supplementary Figure S2. The expression analysis of selected miRNA’s targets genes in aqueous humor of IOTB patients (N=5) and Cataract controls (N=6) using RT-qPCR. Median values are shown by horizontal lines using a Mann-Whitney test. *P<0.05, ** P<0.01

11033_2021_6846_MOESM3_ESM.docx

Supplementary file3 (DOCX 16 kb). Additional file 3: Supplementary Table S1. Patient details of Intraocular tuberculosis and Cataract controls

Supplementary file4 (DOCX 43 kb). Additional file 4: Supplementary Table S2. List of primers used for RT-qPCR analysis

11033_2021_6846_MOESM5_ESM.docx

Supplementary file5 (DOCX 13 kb). Additional file 5: Supplementary Table S3. Summary statistics of small-RNA deep sequencing of two IOTB and cataract controls

Supplementary file6 (XLSX 28 kb). Additional file 6: Supplementary Table S4: List of MiRNAs detected in NGS data

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Chadalawada, S., Kathirvel, K., Lalitha, P. et al. Dysregulated expression of microRNAs in aqueous humor from intraocular tuberculosis patients. Mol Biol Rep 49, 97–107 (2022). https://doi.org/10.1007/s11033-021-06846-4

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