Hsa-miR-23a-5p: A Potential Prognostic Biomarker in Diffuse Large B-cell Lymphoma
-
Yunfei Zhao
,
Anna Su
,
Rui Bai
,
Gulimire Adili
,
Laxin Sabitjan
,
Xun Li
Abstract
This study aimed to identify a novel microRNA (miRNA)-related circulating biomarker that is easily accessible for clinical use and can dynamically monitor the biological characteristics of diffuse large B-cell lymphoma (DLBCL).
We analyzed miRNA expression profiles in DLBCL from the Gene Expression Omnibus (GEO) (GSE171272 and GSE173080) and The Cancer Genome Atlas (TCGA). The immune microenvironment and immune-related gene differences associated with hsa-miR-23a-5p were assessed through the single-sample gene set enrichment analysis and CIBERSORT. Gene set enrichment analysis identified expression trends related to hsa-miR-23a-5p. The 50% inhibitory concentration of chemotherapy agents was estimated for hsa-miR-23a-5p. Potential miRNA targets were identified using TargetScan, miRWalk, and RNA22, and validated with miRTarBase, DIANA-TarBase, and NPInter. Gene functions and associated pathways were analyzed through Gene Ontology and the Kyoto Encyclopedia of Genes and Genomes. Protein-Protein Interaction networks were built using Cytoscape. SNRPD1-related analysis was conducted using TCGA and GEO data.
Hsa-miR-23a-5p was significantly overexpressed in the tumor tissues and serum exosomes of patients with DLBCL. The expression levels of hsa-miR-23a-5p were associated with distinct prognostic outcomes, immune landscapes, chemoresistance, and biological processes, serving as potential risk factors. The target gene SNRPD1 was an independent prognostic factor significantly associated with patient survival.
This study identifies hsa-miR-23a-5p and its target SNRPD1 as potential prognostic factors for DLBCL. Specifically, the overexpression of hsa-miR-23a-5p in serum exosomes of patients with DLBCL suggests that it could serve as a convenient, non-invasive biomarker for clinical evaluation of DLBCL. However, further research and validation are necessary to confirm these findings.
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53. Ganesan S, Palani HK, Lakshmanan V, et al. Stromal cells downregulate miR-23a-5p to activate protective autophagy in acute myeloid leukemia. Cell Death Dis. 2019;10(10):736.
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55. Squadrito ML, Baer C, Burdet F, et al. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 2014;8(5):1432-1446.
56. Huang X, Shen Y, Liu M, et al. Quantitative proteomics reveals that miR-155 regulates the PI3K-AKT pathway in diffuse large B-cell lymphoma. Am J Pathol. 2012;181(1):26-33.
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2. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403(6769):503-11.
3. Schmitz R, Wright GW, Huang DW, et al. Genetics and pathogenesis of diffuse large B-cell lymphoma. N Engl J Med. 2018;378(15):1396-407.
4. Bea S, Zettl A, Wright G, et al. Diffuse large B-cell lymphoma subgroups have distinct genetic profiles that influence tumor biology and improve gene-expression-based survival prediction. Blood. 2005;106(9):3183-90.
5. Chapuy B, Stewart C, Dunford AJ, et al. Molecular subtypes of diffuse large B cell lymphoma are associated with distinct pathogenic mechanisms and outcomes. Nat Med. 2018;24(5):679-90.
6. Tilly H, Morschhauser F, Sehn LH, et al. Polatuzumab vedotin in previously untreated diffuse large B-cell lymphoma. N Engl J Med. 2022;386(4):351-63.
7. Meyer PN, Fu K, Greiner TC, et al. Immunohistochemical methods for predicting cell of origin and survival in patients with diffuse large B-cell lymphoma treated with rituximab. J Clin Oncol. 2011;29(2):200-7.
8. National Cancer Institute. Diffuse Large B-Cell Lymphoma-Cancer Stat Facts. SEER. Accessed April 24, 2024.https://seer.cancer.gov/statfacts/html/dlbcl.html
9. Bouroumeau A, Bussot L, Bonnefoix T, et al. c-MYC and p53 expression highlight starry-sky pattern as a favourable prognostic feature in R-CHOP-treated diffuse large B-cell lymphoma. J Pathol Clin Res. 2021;7(6):604-15.
10. Vodicka P, Klener P, Trneny M. Diffuse large B-cell lymphoma (DLBCL): early patient management and emerging treatment options. Onco Targets Ther. 2022;15:1481-501.
11. Jiang S, Qin Y, Jiang H, et al. Molecular profiling of Chinese R-CHOP treated DLBCL patients: identifying a high-risk subgroup. Int J Cancer. 2020;147(9):2611-20.
12. Lim KG, Sumera A, Burud IAS, Venkateswaran SP. Diffuse large B-cell lymphoma research in Malaysia: a review. Malays J Pathol. 2023;45(1):1-10.
13. Morin RD, Assouline S, Alcaide M, et al. Genetic landscapes of relapsed and refractory diffuse large B-cell lymphomas. Clin Cancer Res. 2016;22(9):2290-300.
14. Shimkus G, Nonaka T. Molecular classification and therapeutics in diffuse large B-cell lymphoma. Front Mol Biosci. 2023;10:1124360.
15. Zhang J, Gu Y, Chen B. Drug-resistance mechanism and new targeted drugs and treatments of relapse and refractory DLBCL. Cancer Manag Res. 2023;15:245-55.
16. Wight JC, Chong G, Grigg AP, Hawkes EA. Prognostication of diffuse large B-cell lymphoma in the molecular era: moving beyond the IPI. Blood Rev. 2018;32(5):400-15.
17. Lee YS, Dutta A. MicroRNAs in cancer. Annu Rev Pathol. 2009;4:199-227.
18. Chen Y, Stallings RL. Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer Res. 2007;67(3):976-83.
19. Scott GK, Goga A, Bhaumik D, et al. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem. 2007;282(2):1479-86.
20. Kosaka N, Yoshioka Y, Fujita Y, Ochiya T. Versatile roles of extracellular vesicles in cancer. J Clin Invest. 2016;126(4):1163-72.
21. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183(3):1161-72.
22. Huang X, Yuan T, Tschannen M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013;14:319.
23. Li C, Zhou T, Chen J, et al. The role of exosomal miRNAs in cancer. J Transl Med. 2022;20(1):6.
24. Cao D, Cao X, Jiang Y, et al. Circulating exosomal microRNAs as diagnostic and prognostic biomarkers in patients with diffuse large B-cell lymphoma. Hematol Oncol. 2022;40(2):172-80.
25. Jiao L, Liu Y, Yu XY, et al. Ribosome biogenesis in disease: new players and therapeutic targets. Signal Transduct Target Ther. 2023;8(1):15.
26. Gaviraghi M, Vivori C, Tonon G. How cancer exploits ribosomal RNA biogenesis: a journey beyond the boundaries of rRNA transcription. Cells. 2019;8(9):1069.
27. Elhamamsy AR, Metge BJ, Alsheikh HA, et al. Ribosome biogenesis: a central player in cancer metastasis and therapeutic resistance. Cancer Res. 2022;82(13):2344-53.
28. Hwang SP, Denicourt C. The impact of ribosome biogenesis in cancer: from proliferation to metastasis. NAR Cancer. 2024;6(2):zcae017.
29. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 2010;11(9):597-610.
30. Manier S, Liu CJ, Avet-Loiseau H, et al. Prognostic role of circulating exosomal miRNAs in multiple myeloma. Blood. 2017;129(17):2429-36.
31. van Eijndhoven MA, Zijlstra JM, Groenewegen NJ, et al. Plasma vesicle miRNAs for therapy response monitoring in Hodgkin lymphoma patients. JCI Insight. 2016;1(19):e89631.
32. Lai X, Wang M, McElyea SD, et al. A microRNA signature in circulating exosomes is superior to exosomal glypican-1 levels for diagnosing pancreatic cancer. Cancer Lett. 2017;393:86-93.
33. Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523(7559):177-82.
34. Siravegna G, Marsoni S, Siena S, Bardelli A. Integrating liquid biopsies into the management of cancer. Nat Rev Clin Oncol. 2017;14(9):531-48.
35. Cohen SJ, Punt CJ, Iannotti N, et al. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol. 2008;26(19):3213-21.
36. Krebs MG, Sloane R, Priest L, et al. Evaluation and prognostic significance of circulating tumor cells in patients with non-small-cell lung cancer. J Clin Oncol. 2011;29(12):1556-63.
37. Cai X, Janku F, Zhan Q, Fan JB. Accessing genetic information with liquid biopsies. Trends Genet. 2015;31(10):564-75.
38. Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329-35.
39. Yu W, Hurley J, Roberts D, et al. Exosome-based liquid biopsies in cancer: opportunities and challenges. Ann Oncol. 2021;32(4):466-77.
40. Voss G, Edsjö A, Bjartell A, Ceder Y. Quantification of microRNA editing using two-tailed RT-qPCR for improved biomarker discovery. RNA. 2021;27(11):1412-24.
41. Ekiz Kanik F, Celebi I, Sevenler D, et al. Attomolar sensitivity microRNA detection using real-time digital microarrays. Sci Rep. 2022;12(1):16220.
42. Benesova S, Kubista M, Valihrach L. Small RNA-sequencing: approaches and considerations for miRNA analysis. Diagnostics (Basel). 2021;11(6):1069.
43. Ergin S, Kherad N, Alagoz M. RNA sequencing and its applications in cancer and rare diseases. Mol Biol Rep. 2022;49(3):2325-33.
44. Yaylak B, Akgül B. Experimental microRNA detection methods. Methods Mol Biol. 2022;2257:33-55.
45. Paulsen IW, Bzorek M, Olsen J, et al. A novel approach for microRNA in situ hybridization using locked nucleic acid probes. Sci Rep. 2021;11(1):4504.
46. Cirillo PDR, Margiotti K, Mesoraca A, Giorlandino C. Quantification of circulating microRNAs by droplet digital PCR for cancer detection. BMC Res Notes. 2020;13(1):351.
47. Low SS, Ji D, Chai WS, et al. Recent progress in nanomaterials modified electrochemical biosensors for the detection of microRNA. Micromachines (Basel). 2021;12(11):1359.
48. Li Y, Quan J, Pan X, et al. Suppressing cell growth and inducing apoptosis by inhibiting miR 23a 5p in human bladder cancer. Mol Med Rep. 2018;18(6):5256-60.
49. Xu L, Li L, Li J, et al. Overexpression of miR-1260b in non-small cell lung cancer is associated with lymph node metastasis. Aging Dis. 2015;6(6):478-85.
50. Ma Y, Shan Z, Ma J, et al. Validation of downregulated microRNAs during osteoclast formation and osteoporosis progression. Mol Med Rep. 2016;13(3):2273-80.
51. Caserta S, Kern F, Cohen J, et al. Circulating plasma microRNAs can differentiate human sepsis and systemic inflammatory response syndrome (SIRS). Sci Rep. 2016;6:28006.
52. Zhao Y, Liu J, Xiong Z, et al. Exosome-derived miR-23a-5p inhibits HCC proliferation and angiogenesis by regulating PRDX2 expression: miR-23a-5p/PRDX2 axis in HCC progression. Heliyon. 2024;10(1):e23168.
53. Ganesan S, Palani HK, Lakshmanan V, et al. Stromal cells downregulate miR-23a-5p to activate protective autophagy in acute myeloid leukemia. Cell Death Dis. 2019;10(10):736.
54. Niwa Y, Yamada S, Sonohara F, et al. Identification of a serum-based miRNA signature for response of esophageal squamous cell carcinoma to neoadjuvant chemotherapy. J Transl Med. 2019;17(1):1.
55. Squadrito ML, Baer C, Burdet F, et al. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 2014;8(5):1432-1446.
56. Huang X, Shen Y, Liu M, et al. Quantitative proteomics reveals that miR-155 regulates the PI3K-AKT pathway in diffuse large B-cell lymphoma. Am J Pathol. 2012;181(1):26-33.
57. Liu K, Du J, Ruan L. MicroRNA-21 regulates the viability and apoptosis of diffuse large B-cell lymphoma cells by upregulating B cell lymphoma-2. Exp Ther Med. 2017;14(5):4489-96.
58. Fan Q, Meng X, Liang H, et al. miR-10a inhibits cell proliferation and promotes cell apoptosis by targeting BCL6 in diffuse large B-cell lymphoma. Protein Cell. 2016;7(12):899-912.
59. Huang F, Jin Y, Wei Y. MicroRNA-187 induces diffuse large B-cell lymphoma cell apoptosis via targeting BCL6. Oncol Lett. 2016;11(4):2845-50.
60. Jia YJ, Liu ZB, Wang WG, et al. HDAC6 regulates microRNA-27b that suppresses proliferation, promotes apoptosis and target MET in diffuse large B-cell lymphoma. Leukemia. 2018;32(3):703-11.
61. Song G, Song G, Ni H, et al. Deregulated expression of miR-224 and its target gene: CD59 predicts outcome of diffuse large B-cell lymphoma patients treated with R-CHOP. Curr Cancer Drug Targets. 2014;14(7):659-70.
62. Farina FM, Inguscio A, Kunderfranco P, et al. MicroRNA-26a/cyclin-dependent kinase 5 axis controls proliferation, apoptosis and in vivo tumor growth of diffuse large B-cell lymphoma cell lines. Cell Death Dis. 2017;8(6):e2890.
63. Wu X, Wang F, Li Y, et al. Evaluation of latent membrane protein 1 and microRNA-155 for the prognostic prediction of diffuse large B cell lymphoma. Oncol Lett. 2018;15(6):9725-34.
64. Zhong H, Xu L, Zhong JH, et al. Clinical and prognostic significance of miR-155 and miR-146a expression levels in formalin-fixed/paraffin-embedded tissue of patients with diffuse large B-cell lymphoma. Exp Ther Med. 2012;3(5):763-70.
65. Berglund M, Hedström G, Amini RM, et al. High expression of microRNA-200c predicts poor clinical outcome in diffuse large B-cell lymphoma. Oncol Rep. 2013;29(2):720-4.
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| Files | ||
| Issue | Articles in Press | |
| Section | Original Article(s) | |
| Keywords | ||
| Diffuse large B‐cell lymphoma Exosome MicroRNA Prognosis | ||
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How to Cite
1.
Zhao Y, Su A, Bai R, Adili G, Sabitjan L, Li X. Hsa-miR-23a-5p: A Potential Prognostic Biomarker in Diffuse Large B-cell Lymphoma. Iran J Allergy Asthma Immunol. 2026;:1-19.
