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Overexpression of Synoviolin and miR-125a-5p, miR-19b-3p in peripheral blood of rheumatoid arthritis patients after treatment with conventional DMARDs and methylprednisolone

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Abstract

Purpose

SYVN1 is an endoplasmic reticulum (ER)-resident E3 ubiquitin ligase that has an essential function along with SEL1L in rheumatoid arthritis (RA) pathogenesis. This study aimed to investigate the changes in the expression of peripheral blood ncRNAs and SYVN1-SEL1L affected by DMARDs treatment.

Methods

Twenty-five newly diagnosed RA patients were randomly assigned to receive conventional DMARDs (csDMARDs) and methylprednisolone for six months. The peripheral blood gene expression of SYVN1 and SEL1L and possible regulatory axes, NEAT1, miR-125a-5p, and miR-19b-3p, were evaluated before and after qRT-PCR. We also compared differences between the patients and healthy controls (HCs), and statistical analyses were performed to determine the correlation between ncRNAs with SYVN1-SEL1L and the clinical parameters of RA.

Results

Expression of NEAT1 (P = 0.0001), miR-19b-3p (P = 0.007), miR-125a-5p (P = 0.005), and SYVN1 (P = 0.036) was significantly increased in newly diagnosed patients compared to HCs; also, miR-125a-5p, miR-19b-3p, and SYVN1 were significantly overexpressed after treatment (P = 0.001, P = 0.001, and P = 0.005, respectively). NEAT1 was positively correlated with SYVN1, and miR-125a-5p had a negative correlation with anti-cyclic citrullinated peptides. The ROC curve analysis showed the potential role of selected ncRNAs in RA pathogenesis.

Conclusion

The results indicate the ineffectiveness of the csDMARDs in reducing SYVN1 expression. The difference in expression of ncRNAs might be useful markers for monitoring disease activity and determining therapeutic responses in RA patients.

Key Points

• The expression of NEAT1 is significantly upregulated in RA patients compared to HC subjects.

• miR-19b-3p, miR-125a-5p, and SYVN1 are significantly upregulated in RA patients compared to HC subjects.

• The expression of miR-19b-3p and miR-125a-5p is significantly increased in RA patients after treatment with DMARDs and methylprednisolone.

• NEAT1 is positively correlated with SYVN1.

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Data availability

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

ACR:

American College Of Rheumatology

AICD:

Activation-Induced Cell Death

AUC:

Area Under The Curve

DMARDs:

Disease-Modifying Antirheumatic Drugs

EDTA:

Ethylenediaminetetraacetic Acid

ERAD:

ER-Associated Degradation

ESR:

Erythrocyte Sedimentation Rate

EULAR:

European League Against Rheumatism

HCQ:

Hydroxychloroquine

LncRNA:

Long Non-Coding RNA

miRNA:

MicroRNA

mPRED:

Methylprednisolone

MTX:

Methotrexate

ncRNA:

Non-Coding RNA

NEAT1:

Nuclear Paraspeckle Assembly Transcript 1

ROC:

Receiver Operating Characteristic

SYVN1:

Synoviolin1

UPR:

Unfolded Protein Response

WBC:

White Blood Cells

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Acknowledgements

We thank all the patients and medical staff who generously contributed to this study.

Funding

This research has been supported by grants from Kermanshah University of Medical Sciences (KUMS); Grant No. (4000650).

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Authors and Affiliations

  1. Student Research Committee, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Negin Karamali

  2. Department of Immunology, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Negin Karamali

  3. Department of Immunology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

    Zahra Mahmoudi

  4. Medical Biology Research Center, Health Technology Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Seyed Askar Roghani

  5. Clinical Research Development Center, Imam Reza Hospital, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Seyed Askar Roghani, Shirin Assar, Mehran Pournazari & Parviz Soufivand

  6. Department of Immunology, School of Medicine, Kermanshah University of Medical Sciences, Daneshgah Street, Shahid Shiroudi Boulevard, Kermanshah, 6714869914, Iran

    Ali Gorgin Karaji & Alireza Rezaiemanesh

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Contributions

N.K. conceived the study and wrote the manuscript. S.A. and P.S. contributed to sample preparation. S.A.R. and Z.M. took the lead in writing the manuscript. A.G.K and M.P. contributed to the interpretation of the results. A.R. critically revised the manuscript and provided the final approval. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Alireza Rezaiemanesh.

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Ethical statement

The study was performed with the support of the Ethics Committee of the Kermanshah University of medical sciences (IR.KUMS.MED.REC.1400.051) and all methods were performed in accordance with relevant guidelines and regulations. Informed consent was obtained from all patients participating in the study.

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Karamali, N., Mahmoudi, Z., Roghani, S.A. et al. Overexpression of Synoviolin and miR-125a-5p, miR-19b-3p in peripheral blood of rheumatoid arthritis patients after treatment with conventional DMARDs and methylprednisolone. Clin Rheumatol 43, 147–157 (2024). https://doi.org/10.1007/s10067-023-06808-0

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