m6A甲基化修饰调控肿瘤免疫的研究进展

doi:10.3969/j.issn.1674-8115.2024.01.016

摘要/Abstract

摘要：

N⁶-甲基腺苷（N⁶-methyladenosine，m⁶A）是一种调控真核细胞基因表达最常见的修饰方式，影响RNA的剪接、降解、稳定性以及蛋白翻译等过程。研究表明m⁶A甲基化修饰与肿瘤发生发展密切相关，在肿瘤免疫应答的相关过程中也发挥着重要的调控作用。m⁶A修饰参与调节免疫细胞的分化、成熟过程以及相关的抗肿瘤免疫反应。在肿瘤微环境中，m⁶A修饰也可影响免疫细胞的募集、活化和极化等，从而促进或抑制肿瘤细胞的增殖与转移，起到重塑肿瘤免疫微环境的重要作用。近年来肿瘤的免疫治疗逐渐应用于临床，如免疫检查点抑制剂治疗、过继性细胞免疫治疗等，都取得了较好的临床效果。通过靶向m⁶A修饰来干预机体免疫系统，如通过小分子抑制剂靶向失调的m⁶A调控因子、诱导免疫细胞重编程等，可提高抗肿瘤免疫反应，加强免疫细胞对肿瘤细胞的识别和杀伤能力。m⁶A修饰是肿瘤免疫治疗的一个新方向，具有潜在的临床应用价值。该文围绕m⁶A甲基化修饰对免疫细胞及肿瘤免疫应答的调控作用进行综述，探讨其免疫治疗的新思路。

关键词: m⁶A甲基化, 肿瘤免疫, 免疫治疗

Abstract:

N⁶-methyladenosine (m⁶A) is the most prevalent modification that regulates gene expression in eukaryotes. It regulates splicing, degradation, stability, and translation of RNA. Numerous studies have demonstrated the close association between m⁶A methylation and tumor development, highlighting its crucial role in regulating tumor immune response. The m⁶A modification actively participates in governing immune cell differentiation and maturation as well as modulating anti-tumor immune responses. Within the tumor microenvironment, m⁶A modification can also impact the recruitment, activation, and polarization of immune cells, thereby either promoting or inhibiting tumor cell proliferation and metastasis. Consequently, it plays a pivotal role in reshaping the tumor immune microenvironment. In recent years, immunotherapy for tumors has been increasingly applied to clinical practice with notable success achieved through approaches such as immune checkpoint inhibitor therapy and adoptive cell immunotherapy. Targeting m⁶A modifications to interfere with the immune system, such as targeting dysregulated m⁶A regulators through small molecule inhibitors and inducing immune cell reprogramming, can improve anti-tumor immune response and strengthen immune cells′ ability to recognize and kill tumor cells. The m⁶A modification represents a novel avenue for potential clinical application within tumor immunotherapy. This review provides a comprehensive summary of the regulatory impact of m⁶A methylation modification on immune cells in the context of cancer, while also delving into novel targets for tumor immunotherapy.

Key words: m⁶A methylation, tumor immunity, immunotherapy

中图分类号:

R730.51

周海霞, 张靖. m⁶A甲基化修饰调控肿瘤免疫的研究进展[J]. 上海交通大学学报（医学版）, 2024, 44(1): 137-144.

ZHOU Haixia, ZHANG Jing. Research progress of m⁶A methylation modification in regulating tumor immunity[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2024, 44(1): 137-144.

图/表 3

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Immune cell	m⁶A regulator	Type	Related factor	Function	Reference
DC	METTL3	Writer	CD40, CD80 and Tirap	Positively correlates with DC maturation and function in promoting T-cell activation	[11]
	YTHDF1	Reader	Lysosomal proteases	Negatively correlates with cross-presentation of engulfed tumour neoantigens	[13]
	YTHDF2	Reader	lnc-Dpf3	Positively correlates with DC migration	[12]
NK	METTL3	Writer	SHP-2	Positively correlates antitumor immunity of NK cells	[15]
NK	YTHDF2	Reader	Tardb	Positively correlates with NK cell antitumor activity as well as NK cell homeostasis and maturation	[16]
TAM	METTL3	Writer	STAT1, STAT3	Positively correlates with M1 macrophage polarization	[20-21]
TAM	YTHDF2	Reader	STAT1	Negatively correlates with macrophage reprogramming and antitumor immunity	[22]
Monocyte	METTL3	Writer	PGC-1α	Positively correlates with monocyte differentiation into different types of macrophages	[25]
Neutrophil	WTAP	Writer	ENO1	Positively correlates with tumor glycolysis mediated by C5aR1-positive neutrophils	[27]
Neutrophil	FTO	Eraser	ZEB1	Positively correlates with senescent neutrophils-mediated chemoresistance in breast cancer	[28]
MDSC	METTL3	Writer	BHLHE41	Positively correlates with MDSC migration	[30]
MDSC	YTHDF1	Reader	EZH2	Positively correlates with MDSC recruitment and activation	[31]
γδ T cell	METTL3	Writer	STAT1	Positively correlates with equilibrate γδ T1 and γδ T17 cells	[34]
γδ T cell	ALKBH5	Eraser	Jagged1/Notch2	Negatively correlates with proliferation and differentiation of γδ T cell precursors	[33]
Mast cell	METTL3	Writer	IL-13	Negatively correlates with inflammatory responses of mast cells	[38]

Immune cell	m⁶A regulator	Type	Related factor	Function	Reference
DC	METTL3	Writer	CD40, CD80 and Tirap	Positively correlates with DC maturation and function in promoting T-cell activation	[11]
	YTHDF1	Reader	Lysosomal proteases	Negatively correlates with cross-presentation of engulfed tumour neoantigens	[13]
	YTHDF2	Reader	lnc-Dpf3	Positively correlates with DC migration	[12]
NK	METTL3	Writer	SHP-2	Positively correlates antitumor immunity of NK cells	[15]
NK	YTHDF2	Reader	Tardb	Positively correlates with NK cell antitumor activity as well as NK cell homeostasis and maturation	[16]
TAM	METTL3	Writer	STAT1, STAT3	Positively correlates with M1 macrophage polarization	[20-21]
TAM	YTHDF2	Reader	STAT1	Negatively correlates with macrophage reprogramming and antitumor immunity	[22]
Monocyte	METTL3	Writer	PGC-1α	Positively correlates with monocyte differentiation into different types of macrophages	[25]
Neutrophil	WTAP	Writer	ENO1	Positively correlates with tumor glycolysis mediated by C5aR1-positive neutrophils	[27]
Neutrophil	FTO	Eraser	ZEB1	Positively correlates with senescent neutrophils-mediated chemoresistance in breast cancer	[28]
MDSC	METTL3	Writer	BHLHE41	Positively correlates with MDSC migration	[30]
MDSC	YTHDF1	Reader	EZH2	Positively correlates with MDSC recruitment and activation	[31]
γδ T cell	METTL3	Writer	STAT1	Positively correlates with equilibrate γδ T1 and γδ T17 cells	[34]
γδ T cell	ALKBH5	Eraser	Jagged1/Notch2	Negatively correlates with proliferation and differentiation of γδ T cell precursors	[33]
Mast cell	METTL3	Writer	IL-13	Negatively correlates with inflammatory responses of mast cells	[38]

Immune cell	m⁶A regulator	Type	Related factor	Function	Reference
CD4⁺T cell	METTL3	Writer	SOCS	Positively correlates with proliferation and differentiation of T cells	[42]
CD4⁺T cell	ALKBH5	Eraser	IFN-γ, CXCL2	Positively correlates with Th1 cell activation	[43]
Treg cell	METTL3	Writer	SOCS	Positively correlates with sustaining Treg suppressive functions	[45]
Treg cell	METTL14	Writer	RORγt	Positively correlates with Tregs differentiation	[44]
CD8⁺T cell	METTL3	Writer	circIGF2BP3	Negatively correlates with CD8⁺T cell responses and facilitates tumor immune	[48]
	METTL14	Writer	Ebi3	Negatively correlates with dysfunctional CD8⁺T cell levels in patients with colorectal cancer	[46]
	YTHDF1/2	Reader	unkown	Positively correlates with tumor-infiltrating lymphocytes, including CD8⁺T cells	[47]
	FTO	Eraser	c-Jun, JunB, and C/EBPβ	Positively correlates with glycolytic metabolism of tumor cells; negatively correlates with CD8⁺T cell responses	[49]
B cell	METTL14	Writer	Lax1, Tipe2	Positively correlates with B cell maturation	[52]
B cell	FTO	Eraser	HSF1	Positively correlates with tumor-promoting and pro-metastatic in multiple myeloma	[53]

Immune cell	m⁶A regulator	Type	Related factor	Function	Reference
CD4⁺T cell	METTL3	Writer	SOCS	Positively correlates with proliferation and differentiation of T cells	[42]
CD4⁺T cell	ALKBH5	Eraser	IFN-γ, CXCL2	Positively correlates with Th1 cell activation	[43]
Treg cell	METTL3	Writer	SOCS	Positively correlates with sustaining Treg suppressive functions	[45]
Treg cell	METTL14	Writer	RORγt	Positively correlates with Tregs differentiation	[44]
CD8⁺T cell	METTL3	Writer	circIGF2BP3	Negatively correlates with CD8⁺T cell responses and facilitates tumor immune	[48]
	METTL14	Writer	Ebi3	Negatively correlates with dysfunctional CD8⁺T cell levels in patients with colorectal cancer	[46]
	YTHDF1/2	Reader	unkown	Positively correlates with tumor-infiltrating lymphocytes, including CD8⁺T cells	[47]
	FTO	Eraser	c-Jun, JunB, and C/EBPβ	Positively correlates with glycolytic metabolism of tumor cells; negatively correlates with CD8⁺T cell responses	[49]
B cell	METTL14	Writer	Lax1, Tipe2	Positively correlates with B cell maturation	[52]
B cell	FTO	Eraser	HSF1	Positively correlates with tumor-promoting and pro-metastatic in multiple myeloma	[53]

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[15]	刘洁，仇晓春. 乳腺肿瘤干细胞研究热点及趋势分析[J]. 上海交通大学学报(医学版), 2020, 40(7): 881-888.

m⁶A甲基化修饰调控肿瘤免疫的研究进展

Research progress of m⁶A methylation modification in regulating tumor immunity

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