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Gamma-ray irradiation differentially modulates PD-1 and CTLA-4 expression and tumour growth in parental and acquired radioresistant EMT6 mouse models

Nur Fatihah Ronny Sham 1 ORCID logo
Syed Baharom Syed Ahmad Fuad 2 ORCID logo
Muhammad Khalis Abdul Karim 3
Nora Julianna Osman 4 ORCID logo
Suraya Othman 4 ORCID logo
Nurhaslina Hasan 5 ORCID logo
Wan Nor I'zzah Wan Mohamad Zain 6 ORCID logo
Harissa Husainy Hasbullah 7 ORCID logo
Narimah Abdul Hamid Hasani 6 ORCID logo
Mohammad Johari Ibahim 6, * ORCID logo
  1. Centre for Graduate Studies, University of Cyberjaya, 63000 Cyberjaya, Malaysia
  2. Department of Anatomy, Faculty of Medicine, Universiti Teknologi MARA, Jalan Hospital, 47000 Sungai Buloh, Selangor, Malaysia
  3. Department of Physics, Faculty of Science, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia
  4. Department of Surgery, Hospital Al-Sultan Abdullah, Universiti Teknologi MARA, 42300 Bandar Puncak Alam, Selangor, Malaysia
  5. Centre of Preclinical Science Studies, Faculty of Dentistry, Universiti Teknologi MARA, 47000 Sungai Buloh, Selangor, Malaysia
  6. Department of Biochemistry & Molecular Medicine, Faculty of Medicine, Universiti Teknologi MARA, Jalan Hospital, 47000 Sungai Buloh, Selangor, Malaysia
  7. Oncologist, Hospital Pakar Pusrawi, Jalan Tun Razak, Titiwangsa, 50400 Kuala Lumpur, Malaysia
Correspondence to: Mohammad Johari Ibahim, Department of Biochemistry & Molecular Medicine, Faculty of Medicine, Universiti Teknologi MARA, Jalan Hospital, 47000 Sungai Buloh, Selangor, Malaysia. ORCID: https://orcid.org/0000-0003-3826-7360. Email: mji@uitm.edu.my.
Volume & Issue: Vol. 13 No. 1 (2026) | Page No.: 8141-8152 | DOI: 10.15419/g5ywny29
Published: 2026-01-31

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This article is published with open access by BioMedPress. This article is distributed under the terms of the Creative Commons Attribution License (CC-BY 4.0) which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited. 

Abstract

Background: Immune checkpoint proteins such as PD-1 and CTLA-4 play pivotal roles in tumour immune evasion. Our previous in vitro studies demonstrated upregulation of Pdcd1 and Ctla4 mRNA in the acquired radioresistant murine breast cancer cell line EMT6RR_MJI. This study aimed to evaluate their gene expression in vivo and assess the impact of gamma-ray irradiation on tumour progression.

Methods: Two in vivo experiments were conducted using a mouse xenograft model subcutaneously implanted with either parental EMT6 or EMT6RR_MJI mammary carcinoma cells. In Experiment 1, levels of Pdcd1, Cd274, and Ctla4 mRNA were quantified by real-time PCR from tumours relative to control groups in both models. Mice in both control and treated groups were sacrificed on day 19 post-inoculation (5 days post-irradiation for treated groups), and tumour origin was validated by determining the expression of epithelial marker E-cadherin (Cdh1) and mesenchymal marker N-cadherin (Cdh2). In Experiment 2, tumour volume was measured weekly to assess treatment response relative to controls. Mice were sacrificed if they lost ≥10% of their body weight or showed signs of stress or ulceration.

Results: Pdcd1 expression was significantly higher in EMT6RR_MJI tumours compared to parental EMT6 tumours (p<0.0001), with no significant difference observed for Ctla4. Gamma-ray irradiation reduced Pdcd1 expression in EMT6RR_MJI tumours (p<0.01) but not in EMT6. Conversely, Ctla4 expression increased significantly in irradiated EMT6 tumours (p<0.01) but remained unchanged in EMT6RR_MJI. Tumour growth was markedly faster in EMT6 tumours than in EMT6RR_MJI tumours from week 2 onward (p<0.0001). Irradiation significantly reduced tumour volume in EMT6 tumours at weeks 3 (p<0.01), 4, and 5 (p<0.001), while EMT6RR_MJI tumours showed no reduction.

Conclusion: Gamma-ray irradiation differentially modulated Pdcd1 and Ctla4 expression in radioresistant (EMT6RR_MJI) and parental (EMT6) tumour models. The absence of tumour reduction in EMT6RR_MJI tumours suggests inherent radioresistance. These findings provide preliminary insights into the link between immune checkpoint regulation and radiation response in breast cancer.

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