长链非编码RNA GASAL1靶向EIF2AK2调控食管鳞癌恶性表型的机制研究

doi:10.3969/j.issn.1006-5725.2026.13.007

Abstract

Abstract:

Objective To investigate the functional role and underlying mechanism of long non-coding RNA GASAL1 and its interaction with eukaryotic translation initiation factor 2 alpha kinase 2 （EIF2AK2） in esophageal squamous cell carcinoma （ESCC）. Methods LncRNA GASAL1 expression in ESCC tissues and cell lines was quantified using quantitative real-time PCR （qRT-PCR） and validated by fluorescence in situ hybridization （FISH）. Clinical correlations were assessed using patient clinicopathological data. Subcellular localization was determined via RNA-FISH and nucleocytoplasmic fractionation. Cell viability， proliferation， migration， and invasion were evaluated using CCK-8， colony formation， wound healing， and Transwell assays， respectively. RNA immunoprecipitation （RIP） followed by western blotting was used to verify the direct interaction between GASAL1 and EIF2AK2. RNA-protein colocalization was visualized by combined FISH and immunofluorescence staining. Rescue experiments were performed to determine whether EIF2AK2 mediates the oncogenic effects of GASAL1. Results GASAL1 was significantly upregulated in ESCC tissues and cell lines compared to controls. Elevated GASAL1 expression positively correlated with lymph node metastasis and advanced clinical stage. Both GASAL1 and EIF2AK2 were predominantly localized in the cytoplasm. Functionally， GASAL1 knockdown significantly impaired ESCC cell viability， proliferation， migration， and invasion. RNA pull-down coupled with mass spectrometry identified EIF2AK2 as a direct binding partner， which was subsequently validated by RIP assays. Rescue experiments revealed that EIF2AK2 knockdown recapitulated the tumor-suppressive effects of GASAL1 silencing， whereas GASAL1 overexpression rescued the malignant phenotypes inhibited by EIF2AK2 depletion. Conclusions GASAL1 is upregulated in ESCC and correlates with aggressive clinicopathological features， suggesting its potential as a prognostic biomarker. Mechanistically， cytoplasmic GASAL1 promotes ESCC progression by interacting with EIF2AK2 to enhance tumor cell proliferation， migration， and invasion. The GASAL1/EIF2AK2 axis represents a promising therapeutic target for ESCC management.

Key words: esophageal squamous cell carcinoma, LncRNA GASAL1, EIF2AK2, proliferation, migration, invasion

CLC Number:

R735.1

Zhenya MA,Yanlei GE,Junqing GAN,Ye JIN,Xuan ZHENG,Guogui SUN. Mechanism study of long non-coding RNA GASAL1 targeting EIF2AK2 to regulate malignant phenotype in esophageal squamous cell carcinoma[J]. The Journal of Practical Medicine, 2026, 42(13): 2317-2330.

Figures/Tables 20

Tab.1

Fig.1

Tab.2

Tab.3

Expression of GASAL1 in ESCC tissues and its association with clinicopathological features"

临床病理特征	例数	GASAL1表达水平		$χ 2$ 值	P值
临床病理特征	例数	低表达（n = 40）	高表达（n = 40）	$χ 2$ 值	P值
性别				2.143	0.143
男	56	25	31
女	24	15	9
年龄				1.528	0.216
≤ 60岁	33	19	14
60岁	46	20	26
肿瘤最大径^#				3.337	0.068
5 cm	44	26	18
≥ 5 cm	34	13	21
淋巴结转移				4.053	0.044
无	41	25	16
有	39	15	24
临床分期^#				7.204	0.007
Ⅰ期 + Ⅱ期	19	15	4
Ⅲ期 + Ⅳ期	28	11	17

Tab.3

Tab.4

Fig.2

Fig.3

Tab.5

Tab.6

Tab.7

Fig.4

Tab.8

Tab.9

Fig.5

Tab.10

Tab.11

Tab.12

Tab.13

Tab.14

Fig.6

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名称	引物序列（5′→3′）
GASAL1	上游引物：GCCTTGCCACTCCTCACTCA
	下游引物：CTCCTTGGTAACCGATGTCATT
EIF2AK2	上游引物：TCTGACTACCTGTCCTCTGGTTC
	下游引物：CTGCTGAGAAGTCACCTTCAGAT
GAPDH	上游引物：ACCCACTCCTCCACCTTTGA
	下游引物：CCACCCTGTTGCTGTAGCCA
U6	上游引物：CTCGCTTCGGCAGCACA
	下游引物：AACGCTTCACGAATTTGCGT

细胞	GASAL1表达水平	t值	P值
HEEC	1.00 ± 0.00
KYSE-410	1.42 ± 0.11	6.78	0.003
TE-1	3.55 ± 0.41	10.82	0.001
TE-10	1.85 ± 0.08	18.80	0.001

组别	GAPDH	U6	GASAL1
TE-1
细胞质	0.87 ± 0.01	0.27 ± 0.02	0.61 ± 0.01
细胞核	0.13 ± 0.01	0.73 ± 0.02	0.39 ± 0.01
TE-10
细胞质	1.00 ± 0.00	0.22 ± 0.04	0.77 ± 0.02
细胞核	0.00 ± 0.00	0.76 ± 0.04	0.23 ± 0.02

细胞	组别	GASAL1表达水平	t值	P值
TE-1	si-NC	1.00 ± 0.00
	si-GASAL1-1	0.26 ± 0.00	440.20	0.001
	si-GASAL1-2	0.31 ± 0.02	47.81	0.001
	si-GASAL1-3	0.39 ± 0.02	39.82	0.001
TE-10	si-NC	1.00 ± 0.00
	si-GASAL1-1	0.27 ± 0.04	29.62	0.001
	si-GASAL1-2	0.37 ± 0.10	11.08	0.001
	si-GASAL1-3	0.27 ± 0.06	23.16	0.001

组别	吸光度值（450 nm）				细胞克隆数
组别	24 h	48 h	72 h	96 h	细胞克隆数
TE-1
si-NC	0.24 ± 0.01	0.66 ± 0.01	1.20 ± 0.02	1.73 ± 0.07	431.00 ± 27.07
si-GASAL1	0.15 ± 0.01	0.35 ± 0.02	0.82 ± 0.07	1.21 ± 0.05	220.30 ± 45.50
t值	8.413	23.39	6.872	8.829	6.892
P值	0.001	0.001	0.002	0.001	0.002
TE-10
si-NC	0.23 ± 0.02	0.54 ± 0.02	1.12 ± 0.04	1.52 ± 0.03	525.30 ± 20.40
si-GASAL1	0.16 ± 0.01	0.38 ± 0.01	0.82 ± 0.04	1.13 ± 0.04	277.70 ± 5.67
t值	5.325	11.850	8.510	11.850	20.250
P值	0.006	0.001	0.001	0.001	0.001

Mechanism study of long non-coding RNA GASAL1 targeting EIF2AK2 to regulate malignant phenotype in esophageal squamous cell carcinoma

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组别	细胞迁移率/%	细胞侵袭数量/个
TE-1
si-NC	68.68 ± 0.99	888.70 ± 15.63
si-GASAL1	46.19 ± 0.37	349.70 ± 40.38
t值	30.08	21.56
P值	0.001	0.001
TE-10
si-NC	51.27 ± 0.73	668.70 ± 14.01
si-GASAL1	31.05 ± 1.18	321.00 ± 55.43
t值	20.60	10.53
P值	0.001	0.001

编号	总分	肽段覆盖度	基因名	种属	高置信度肽段
1	85.96	36.54	MTCL1	人	54
3	77.26	34.98	MTCL2	人	46
4	75.96	43.25	DHX36	人	58
10	60.71	74.69	YBX1	人	76
13	51.18	31.38	PRPF4B	人	34
14	50.15	52.45	EIF2AK2	人	48
17	47.2	27.57	HNRNPUL1	人	51
18	45.97	16.85	SNRNP200	人	24
22	44.65	29.67	EIF5B	人	29

细胞	组别	GASAL1表达水平	t值	P值
TE-1	IP组	29.49 ± 3.03	16.31	0.001
	IgG组	1.00 ± 0.00	16.31	0.001
TE-10	IP组	31.05 ± 2.85	18.26	0.001
	IgG组	1.00 ± 0.00	18.26	0.001

细胞	EIF2AK2表达水平	t值	P值
HEEC	1.01 ± 0.00
TE-1	3.51 ± 1.09	3.98	0.016
TE-10	8.36 ± 1.24	10.29	0.001

细胞	组别	GASAL1表达水平	t值	P值
TE-1	GASAL1-plasmid-NC	1.00 ± 0.00	21.45	0.001
	GASAL1-plasmid	61.00 ± 4.84	21.45	0.001
TE-10	GASAL1-plasmid-NC	1.00 ± 0.00	26.38	0.001
	GASAL1-plasmid	52.20 ± 3.36	26.38	0.001

细胞	组别	细胞迁移率/%	细胞侵袭数量/个
TE-1	GASAL1 plasmid+si-EIF2AK2	58.04 ± 0.23^*#	352.33 ± 34.41^*#
	GASAL1 plasmid+si-NC	78.64 ± 0.05^#	752.00 ± 54.55^#
	GASAL1 plasmid-NC+si-EIF2AK2	35.67 ± 0.54^*	162.33 ± 9.84^*
	GASAL1 plasmid-NC+si-NC	54.45 ± 0.10^*#	322.67 ± 31.48^*#
	F值	6918.00	95.84
	P值	0.000	0.000
TE-10	GASAL1 plasmid+si-EIF2AK2	61.79 ± 0.34^*#	406.67 ± 39.88^*#
	GASAL1 plasmid+si-NC	72.11 ± 0.70^#	627.00 ± 25.31^#
	GASAL1 plasmid-NC+si-EIF2AK2	36.09 ± 1.88^*	140.33 ± 25.04^*
	GASAL1 plasmid-NC+si-NC	54.59 ± 1.66^*#	325.33 ± 19.22^*#
	F值	267.94	100.84
	P值	0.000	0.000

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细胞	组别	吸光度值（450nm）				细胞克隆数
细胞	组别	24 h	48 h	72 h	96 h	细胞克隆数
TE-1	GASAL1 plasmid+si-EIF2AK2	0.21 ± 0.01^*#	0.36 ± 0.01^*#	0.62 ± 0.00^*#	1.05 ± 0.03^*#	119.33 ± 12.04^*#
	GASAL1 plasmid+si-NC	0.34 ± 0.01^#	0.45 ± 0.00^#	0.86 ± 0.06^#	1.35 ± 0.04^#	289.67 ± 20.43^#
	GASAL1 plasmid-NC+si-EIF2AK2	0.11 ± 0.02^*	0.25 ± 0.00^*	0.40 ± 0.05^*	0.64 ± 0.04^*	47.33 ± 2.05^*
	GASAL1 plasmid-NC+si-NC	0.22 ± 0.02^*#	0.34 ± 0.02^*#	0.57 ± 0.00^*#	0.97 ± 0.02^*#	111.33 ± 8.58^*#
	F值	73.602	128.300	53.316	138.46	134.210
	P值	0.000	0.000	0.000	0.000	0.000
TE-10	GASAL1 plasmid+si-EIF2AK2	015 ± 0.02^*#	0.38 ± 0.02^*#	0.85 ± 0.03^*#	1.23 ± 0.03^*#	158.00 ± 8.60^*#
	GASAL1 plasmid+si-NC	0.22 ± 0.03^#	0.66 ± 0.06^#	1.12 ± 0.04^#	1.55 ± 0.04^#	252.67 ± 37.61^#
	GASAL1 plasmid-NC+si-EIF2AK2	0.09 ± 0.01^*	0.26 ± 0.01^*	0.59 ± 0.06^*	0.81 ± 0.02^*	52.33 ± 19.77^*
	GASAL1 plasmid-NC+si-NC	0.14 ± 0.01^*#	0.33 ± 0.04^*#	0.83 ± 0.01^*#	1.14 ± 0.05^*#	157.33 ± 33.77^*#
	F值	17.563	43.592	65.289	24.676	17.747
	P值	0.001	0.000	0.000	0.000	0.001