Immune Regulation and ECM-Related Pathway Enrichment Reveal ATP2A3 as a Prognostic Biomarker for Nonspecific Orbital Inflammation: An Integrated Machine Learning and Mendelian Randomization Analysis

Mediators Inflamm. 2025 Jun 13:2025:7061507. doi: 10.1155/mi/7061507. eCollection 2025.

Abstract

Background: Nonspecific orbital inflammation (NSOI) is a heterogeneous inflammatory disorder of the orbit with an unclear etiology. ATP2A3, a key regulator of calcium homeostasis in the endoplasmic reticulum (ER), may play a pivotal role in NSOI pathogenesis. Its potential as a diagnostic biomarker merits thorough investigation. Methods: Differentially expressed genes (DEGs) common to two GEO datasets (GSE58331 and GSE105149) were intersected with immune-related genes from the ImmPort database, yielding 89 candidates. ATP2A3 was prioritized using machine learning (ML) approaches, including LASSO, support vector machine (SVM)-RFE, and weighted gene coexpression network analysis (WGCNA). Functional enrichment was assessed using GSEA and GSVA based on genes co-expressed with ATP2A3. Immune microenvironment characteristics were evaluated using CIBERSORT and ESTIMATE. Expression of ATP2A3 was validated in GSE105149. Results: Fifteen hub genes were identified, with ATP2A3 strongly linked to immune-related pathways. Genes positively correlated with ATP2A3 were enriched in sensory perception and extracellular matrix (ECM) organization. Immune infiltration analysis revealed a positive association between ATP2A3 expression and memory B cells, M2 macrophages, resting mast cells, monocytes, and regulatory T cells (Tregs), while naive B cells and plasma cells were negatively associated. ATP2A3 exhibited significant diagnostic potential for distinguishing NSOI. Conclusions: In the context of NSOI, we identify ATP2A3 as a novel contributor to immune-driven pathogenesis. Its significant dysregulation in NSOI tissues relative to healthy controls underscores its potential as a prognostic marker within the inflammatory microenvironment.

Keywords: ATP2A3; Lasso regression; Mendelian randomization; autoimmune inflammatory disorder; nonspecific orbital inflammation (NSOI).

MeSH terms

  • Biomarkers / metabolism
  • Extracellular Matrix* / metabolism
  • Gene Expression Profiling
  • Gene Regulatory Networks
  • Humans
  • Inflammation* / genetics
  • Inflammation* / immunology
  • Inflammation* / metabolism
  • Machine Learning*
  • Prognosis
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases* / genetics
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases* / metabolism

Substances

  • Biomarkers
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases