Research progress of m6A methylation modification in regulating tumor immunity

doi:10.3969/j.issn.1674-8115.2024.01.016

Abstract

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

CLC Number:

R730.51

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.

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References 58

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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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Research progress of m⁶A methylation modification in regulating tumor immunity

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