MicroRNA-mediated Metabolic Regulation of Immune Cells in Cancer: an Updated Review

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2024 Jul 15

PMID 39007129

Authors

Sepideh Chowdary Khameneh

Sara Razi

Ramin Lashanizadegan

Sanaz Akbari

Masoud Sayaf

Karimeh Haghani

Salar Bakhtiyari

Affiliations

Soon will be listed here.

Abstract

The study of immunometabolism, which examines how immune cells regulate their metabolism to maintain optimal performance, has become an important area of focus in cancer immunology. Recent advancements in this field have highlighted the intricate connection between metabolism and immune cell function, emphasizing the need for further research. MicroRNAs (miRNAs) have gained attention for their ability to post-transcriptionally regulate gene expression and impact various biological processes, including immune function and cancer progression. While the role of miRNAs in immunometabolism is still being explored, recent studies have demonstrated their significant influence on the metabolic activity of immune cells, such as macrophages, T cells, B cells, and dendritic cells, particularly in cancer contexts. Disrupted immune cell metabolism is a hallmark of cancer progression, and miRNAs have been linked to this process. Understanding the precise impact of miRNAs on immune cell metabolism in cancer is essential for the development of immunotherapeutic approaches. Targeting miRNAs may hold potential for creating groundbreaking cancer immunotherapies to reshape the tumor environment and improve treatment outcomes. In summary, the recognition of miRNAs as key regulators of immune cell metabolism across various cancers offers promising potential for refining cancer immunotherapies. Further investigation into how miRNAs affect immune cell metabolism could identify novel therapeutic targets and lead to the development of innovative cancer immunotherapies.

References

Orso F, Quirico L, Dettori D, Coppo R, Virga F, Ferreira L . Role of miRNAs in tumor and endothelial cell interactions during tumor progression. Semin Cancer Biol. 2019; 60:214-224. DOI: 10.1016/j.semcancer.2019.07.024. View

Hanahan D, Weinberg R . Hallmarks of cancer: the next generation. Cell. 2011; 144(5):646-74. DOI: 10.1016/j.cell.2011.02.013. View

Zhao E, Maj T, Kryczek I, Li W, Wu K, Zhao L . Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction. Nat Immunol. 2015; 17(1):95-103. PMC: 4684796. DOI: 10.1038/ni.3313. View

Ganeshan K, Chawla A . Metabolic regulation of immune responses. Annu Rev Immunol. 2014; 32:609-34. PMC: 5800786. DOI: 10.1146/annurev-immunol-032713-120236. View

Buck M, OSullivan D, Geltink R, Curtis J, Chang C, Sanin D . Mitochondrial Dynamics Controls T Cell Fate through Metabolic Programming. Cell. 2016; 166(1):63-76. PMC: 4974356. DOI: 10.1016/j.cell.2016.05.035. View

Tomczak K, Czerwinska P, Wiznerowicz M . The Cancer Genome Atlas (TCGA): an immeasurable source of knowledge. Contemp Oncol (Pozn). 2015; 19(1A):A68-77. PMC: 4322527. DOI: 10.5114/wo.2014.47136. View

Katoh M . Cardio-miRNAs and onco-miRNAs: circulating miRNA-based diagnostics for non-cancerous and cancerous diseases. Front Cell Dev Biol. 2014; 2:61. PMC: 4207049. DOI: 10.3389/fcell.2014.00061. View

Zhou M, Niu C, Jia L, He H . The value of MGMT promote methylation and IDH-1 mutation on diagnosis of pseudoprogression in patients with high-grade glioma: A meta-analysis. Medicine (Baltimore). 2019; 98(50):e18194. PMC: 6922590. DOI: 10.1097/MD.0000000000018194. View

Xing Y, Wang Z, Lu Z, Xia J, Xie Z, Jiao M . MicroRNAs: immune modulators in cancer immunotherapy. Immunother Adv. 2022; 1(1):ltab006. PMC: 9327120. DOI: 10.1093/immadv/ltab006. View

10.

He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S . The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A. 2005; 102(52):19075-80. PMC: 1323209. DOI: 10.1073/pnas.0509603102. View

11.

Zhu Z, Luo L, Xiang Q, Wang J, Liu Y, Deng Y . MiRNA-671-5p Promotes prostate cancer development and metastasis by targeting NFIA/CRYAB axis. Cell Death Dis. 2020; 11(11):949. PMC: 7642259. DOI: 10.1038/s41419-020-03138-w. View

12.

Zhang T, Zhang Z, Li F, Ping Y, Qin G, Zhang C . miR-143 Regulates Memory T Cell Differentiation by Reprogramming T Cell Metabolism. J Immunol. 2018; 201(7):2165-2175. DOI: 10.4049/jimmunol.1800230. View

13.

Liu Z, Smith K, Khong H, Huang J, Ahn E, Zhou M . miR-125b regulates differentiation and metabolic reprogramming of T cell acute lymphoblastic leukemia by directly targeting A20. Oncotarget. 2016; 7(48):78667-78679. PMC: 5346668. DOI: 10.18632/oncotarget.12018. View

14.

Sugiura A, Rathmell J . Metabolic Barriers to T Cell Function in Tumors. J Immunol. 2018; 200(2):400-407. PMC: 5777533. DOI: 10.4049/jimmunol.1701041. View

15.

Ma E, Poffenberger M, Wong A, Jones R . The role of AMPK in T cell metabolism and function. Curr Opin Immunol. 2017; 46:45-52. DOI: 10.1016/j.coi.2017.04.004. View

16.

Gulino R, Forte S, Parenti R, Memeo L, Gulisano M . MicroRNA and pediatric tumors: Future perspectives. Acta Histochem. 2015; 117(4-5):339-54. DOI: 10.1016/j.acthis.2015.02.007. View

17.

Wang S, Wu J, Ren J, Vlantis A, Li M, Liu S . MicroRNA-125b Interacts with Foxp3 to Induce Autophagy in Thyroid Cancer. Mol Ther. 2018; 26(9):2295-2303. PMC: 6127503. DOI: 10.1016/j.ymthe.2018.06.015. View

18.

Chapman N, Boothby M, Chi H . Metabolic coordination of T cell quiescence and activation. Nat Rev Immunol. 2019; 20(1):55-70. DOI: 10.1038/s41577-019-0203-y. View

19.

Iorio M, Ferracin M, Liu C, Veronese A, Spizzo R, Sabbioni S . MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005; 65(16):7065-70. DOI: 10.1158/0008-5472.CAN-05-1783. View

20.

Ji Y, Wrzesinski C, Yu Z, Hu J, Gautam S, Hawk N . miR-155 augments CD8+ T-cell antitumor activity in lymphoreplete hosts by enhancing responsiveness to homeostatic γc cytokines. Proc Natl Acad Sci U S A. 2014; 112(2):476-81. PMC: 4299215. DOI: 10.1073/pnas.1422916112. View