Jindal Udita, Mamgain Mukesh, Nath Uttam Kumar, Sharma Isha, Pant Bhaskar, Sharma Ankita, Gupta Archita, Rahman Khaliqur, Yadav Sunil, Singh Manish Pratap, Mishra Shaktiprasad, Chaturvedi Chandra Praksah, Courty Jose, Singh Navin, Gupta Seema, Kumar Sanjeev, Verma Shailendra Prasad, Mallick Saumyaranjan, Gogia Ajay, Raghav Sunil, Sarkar Jayanta, Srivastava Kinshuk Raj, Datta Dipak, Jain Neeraj
Division of Cancer Biology, CSIR-Central Drug Research Institute, Lucknow, Uttar Pradesh, 226031, India.
Academy of Scientific and Innovative Research, Ghaziabad, Uttar Pradesh, 201002, India.
Leukemia. 2024 Oct;38(10):2196-2209. doi: 10.1038/s41375-024-02344-1. Epub 2024 Jul 13.
The interaction between stromal and tumor cells in tumor microenvironment is a crucial factor in Mantle cell lymphoma (MCL) progression and therapy resistance. We have identified a long non-coding RNA, CERS6-AS1, upregulated in MCL and associated with poor overall survival. CERS6-AS1 expression was elevated in primary MCL within stromal microenvironment and in a subset of MCL cells adhered to stromal layer. These stromal-adhered MCL-subsets exhibited cancer stem cell signatures than suspension counterparts. Mechanistically, we found that downregulating CERS6-AS1 in MCL reduced Fibroblast Growth Factor Receptor-1 (FGFR1), expression attributed to loss of its interaction with RNA-binding protein nucleolin. In addition, using in-silico approach, we have discovered a direct interaction between nucleolin and 5'UTR of FGFR1, thereby regulating FGFR1 transcript stability. We discovered a positive association of CERS6-AS1 with cancer stem cell signatures, and Wnt signaling. Building on these, we explored potential therapeutic strategies where combining nucleolin-targeting agent with FGFR1 inhibition significantly contributed to reversing cancer stem cell signatures and abrogated primary MCL cell growth on stromal layer. These findings provide mechanistic insights into regulatory network involving CERS6-AS1, nucleolin, and FGFR1 axis-associated crosstalk between tumor cells and stromal cell interaction and highlights therapeutic potential of targeting a non-coding RNA in MCL.
肿瘤微环境中基质细胞与肿瘤细胞之间的相互作用是套细胞淋巴瘤(MCL)进展和治疗耐药的关键因素。我们鉴定出一种长链非编码RNA,即CERS6-AS1,其在MCL中上调且与总体生存率低相关。CERS6-AS1在基质微环境中的原发性MCL以及粘附于基质层的一部分MCL细胞中表达升高。这些粘附于基质的MCL亚群比悬浮对应物表现出癌症干细胞特征。从机制上讲,我们发现下调MCL中的CERS6-AS1会降低成纤维细胞生长因子受体-1(FGFR1)的表达,这归因于其与RNA结合蛋白核仁素相互作用的丧失。此外,通过计算机模拟方法,我们发现核仁素与FGFR1的5'UTR之间存在直接相互作用,从而调节FGFR1转录本的稳定性。我们发现CERS6-AS1与癌症干细胞特征和Wnt信号传导呈正相关。基于这些发现,我们探索了潜在的治疗策略,即联合使用核仁素靶向剂与FGFR1抑制剂可显著有助于逆转癌症干细胞特征并消除原发性MCL细胞在基质层上的生长。这些发现为涉及CERS6-AS1、核仁素和FGFR1轴的调控网络提供了机制性见解,揭示了肿瘤细胞与基质细胞相互作用之间的串扰,并突出了靶向MCL中非编码RNA的治疗潜力。