The EEF1AKMT3/MAP2K7/TP53 axis suppresses tumor invasiveness and metastasis in gastric cancer

The importance of methylation in the tumorigenic responses of nonhistone proteins, such as TP53, PTEN, RB1, AKT, and STAT3, has been emphasized in numerous studies. In parallel, the corresponding nonhistone protein methyltransferases have been acknowledged in the pathophysiology of cancer. Thus, thi...

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Veröffentlicht in:Cancer letters 2022-09, Vol.544, p.215803-215803, Article 215803
Hauptverfasser: Hong, Yo Han, Aziz, Nur, Park, Jae Gwang, Lee, Dagyeong, Kim, Jin Kyeong, Kim, Seung A., Choi, Wooram, Lee, Chae Young, Lee, Hwa Pyoung, Huyen Trang, Ha Thi, Kim, Han Gyung, Jeon, Young-Jun, Kim, Bokyoung, Kim, Younghoon, Kim, Kyung-Hee, Yoo, Byong Chul, Han, Jeung-Whan, Parameswaran, Narayana, Kim, Ji Hye, Hur, Hoon, Cho, Jae Youl
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container_issue
container_start_page 215803
container_title Cancer letters
container_volume 544
creator Hong, Yo Han
Aziz, Nur
Park, Jae Gwang
Lee, Dagyeong
Kim, Jin Kyeong
Kim, Seung A.
Choi, Wooram
Lee, Chae Young
Lee, Hwa Pyoung
Huyen Trang, Ha Thi
Kim, Han Gyung
Jeon, Young-Jun
Kim, Bokyoung
Kim, Younghoon
Kim, Kyung-Hee
Yoo, Byong Chul
Han, Jeung-Whan
Parameswaran, Narayana
Kim, Ji Hye
Hur, Hoon
Cho, Jae Youl
description The importance of methylation in the tumorigenic responses of nonhistone proteins, such as TP53, PTEN, RB1, AKT, and STAT3, has been emphasized in numerous studies. In parallel, the corresponding nonhistone protein methyltransferases have been acknowledged in the pathophysiology of cancer. Thus, this study aimed to explore the pathological role of a nonhistone methyltransferase in gastric cancer (GC), identify nonhistone substrate protein, and understand the underlying mechanism. Interestingly, among the 24 methyltransferases and methyltransferase family 16 (MTF16) proteins, EEF1AKMT3 (METTL21B) expression was prominently lower in GC tissues than in normal adjacent tissues and was associated with a worse prognosis. In addition, EEF1AKMT3-knockdown induced gastric tumor invasiveness and migration. Through gain and loss-of-function studies, mass spectrometry analysis, RNA-seq, and phospho-antibody array, we identified EEF1AKMT3 as a novel tumor-suppressive methyltransferase that catalyzes the monomethylation of MAP2K7 (MKK7) at K296, thereby decreasing the phosphorylation, ubiquitination, and degradation of TP53. Furthermore, EEF1AKMT3, p-MAP2K7, and TP53 protein levels were positively correlated in GC tissues. Collectively, our results delineate the tumor-suppressive function of the EEF1AKMT3/MAP2K7/TP53 signaling axis and suggest the dysregulation of the signaling axis as potential targeted therapy in GC. •EEF1AKMT3 was identified as gastric tumor suppressor using in vitro and in vivo model.•As a novel EEF1AKMT3 substrate, MAP2K7 was found to be methylated at K296.•Methylated MAP2K7 was revealed to promote TP53 protein stability,.•Experimental data showed that a molecular complex composed of EEF1AKMT3, MAP2K7, and TP53 acts as a tumor suppressor axis and highlights therapeutic exploitability in gastric cancer.
doi_str_mv 10.1016/j.canlet.2022.215803
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In parallel, the corresponding nonhistone protein methyltransferases have been acknowledged in the pathophysiology of cancer. Thus, this study aimed to explore the pathological role of a nonhistone methyltransferase in gastric cancer (GC), identify nonhistone substrate protein, and understand the underlying mechanism. Interestingly, among the 24 methyltransferases and methyltransferase family 16 (MTF16) proteins, EEF1AKMT3 (METTL21B) expression was prominently lower in GC tissues than in normal adjacent tissues and was associated with a worse prognosis. In addition, EEF1AKMT3-knockdown induced gastric tumor invasiveness and migration. Through gain and loss-of-function studies, mass spectrometry analysis, RNA-seq, and phospho-antibody array, we identified EEF1AKMT3 as a novel tumor-suppressive methyltransferase that catalyzes the monomethylation of MAP2K7 (MKK7) at K296, thereby decreasing the phosphorylation, ubiquitination, and degradation of TP53. Furthermore, EEF1AKMT3, p-MAP2K7, and TP53 protein levels were positively correlated in GC tissues. Collectively, our results delineate the tumor-suppressive function of the EEF1AKMT3/MAP2K7/TP53 signaling axis and suggest the dysregulation of the signaling axis as potential targeted therapy in GC. •EEF1AKMT3 was identified as gastric tumor suppressor using in vitro and in vivo model.•As a novel EEF1AKMT3 substrate, MAP2K7 was found to be methylated at K296.•Methylated MAP2K7 was revealed to promote TP53 protein stability,.•Experimental data showed that a molecular complex composed of EEF1AKMT3, MAP2K7, and TP53 acts as a tumor suppressor axis and highlights therapeutic exploitability in gastric cancer.</description><identifier>ISSN: 0304-3835</identifier><identifier>EISSN: 1872-7980</identifier><identifier>DOI: 10.1016/j.canlet.2022.215803</identifier><language>eng</language><publisher>Clare: Elsevier B.V</publisher><subject>AKT protein ; Antibodies ; Cell culture ; Cloning ; EEF1AKMT3 ; Gastric cancer ; Gastric tumor ; Gene expression ; Invasiveness ; MAP2K7 ; Mass spectroscopy ; Medical prognosis ; Medical research ; Metastases ; Metastasis ; Methylation ; Methyltransferase ; Mutagenesis ; Nonhistone proteins ; p53 Protein ; Phosphorylation ; Pore size ; Protein methylation ; Proteins ; PTEN protein ; Software ; Stat3 protein ; TP53 ; Tumor suppressor ; Tumorigenesis ; Tumors ; Ubiquitination</subject><ispartof>Cancer letters, 2022-09, Vol.544, p.215803-215803, Article 215803</ispartof><rights>2022 Elsevier B.V.</rights><rights>2022. 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Aziz, Nur ; Park, Jae Gwang ; Lee, Dagyeong ; Kim, Jin Kyeong ; Kim, Seung A. ; Choi, Wooram ; Lee, Chae Young ; Lee, Hwa Pyoung ; Huyen Trang, Ha Thi ; Kim, Han Gyung ; Jeon, Young-Jun ; Kim, Bokyoung ; Kim, Younghoon ; Kim, Kyung-Hee ; Yoo, Byong Chul ; Han, Jeung-Whan ; Parameswaran, Narayana ; Kim, Ji Hye ; Hur, Hoon ; Cho, Jae Youl</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c367t-c04da2b57b7d67d3331b21a432a226dd4dd8f1164827f148556b20a17134f4793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>AKT protein</topic><topic>Antibodies</topic><topic>Cell culture</topic><topic>Cloning</topic><topic>EEF1AKMT3</topic><topic>Gastric cancer</topic><topic>Gastric tumor</topic><topic>Gene expression</topic><topic>Invasiveness</topic><topic>MAP2K7</topic><topic>Mass spectroscopy</topic><topic>Medical prognosis</topic><topic>Medical research</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Methylation</topic><topic>Methyltransferase</topic><topic>Mutagenesis</topic><topic>Nonhistone proteins</topic><topic>p53 Protein</topic><topic>Phosphorylation</topic><topic>Pore size</topic><topic>Protein methylation</topic><topic>Proteins</topic><topic>PTEN protein</topic><topic>Software</topic><topic>Stat3 protein</topic><topic>TP53</topic><topic>Tumor suppressor</topic><topic>Tumorigenesis</topic><topic>Tumors</topic><topic>Ubiquitination</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hong, Yo Han</creatorcontrib><creatorcontrib>Aziz, Nur</creatorcontrib><creatorcontrib>Park, Jae Gwang</creatorcontrib><creatorcontrib>Lee, Dagyeong</creatorcontrib><creatorcontrib>Kim, Jin Kyeong</creatorcontrib><creatorcontrib>Kim, Seung A.</creatorcontrib><creatorcontrib>Choi, Wooram</creatorcontrib><creatorcontrib>Lee, Chae Young</creatorcontrib><creatorcontrib>Lee, Hwa Pyoung</creatorcontrib><creatorcontrib>Huyen Trang, Ha Thi</creatorcontrib><creatorcontrib>Kim, Han Gyung</creatorcontrib><creatorcontrib>Jeon, Young-Jun</creatorcontrib><creatorcontrib>Kim, Bokyoung</creatorcontrib><creatorcontrib>Kim, Younghoon</creatorcontrib><creatorcontrib>Kim, Kyung-Hee</creatorcontrib><creatorcontrib>Yoo, Byong Chul</creatorcontrib><creatorcontrib>Han, Jeung-Whan</creatorcontrib><creatorcontrib>Parameswaran, Narayana</creatorcontrib><creatorcontrib>Kim, Ji Hye</creatorcontrib><creatorcontrib>Hur, Hoon</creatorcontrib><creatorcontrib>Cho, Jae Youl</creatorcontrib><collection>CrossRef</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health &amp; 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In parallel, the corresponding nonhistone protein methyltransferases have been acknowledged in the pathophysiology of cancer. Thus, this study aimed to explore the pathological role of a nonhistone methyltransferase in gastric cancer (GC), identify nonhistone substrate protein, and understand the underlying mechanism. Interestingly, among the 24 methyltransferases and methyltransferase family 16 (MTF16) proteins, EEF1AKMT3 (METTL21B) expression was prominently lower in GC tissues than in normal adjacent tissues and was associated with a worse prognosis. In addition, EEF1AKMT3-knockdown induced gastric tumor invasiveness and migration. Through gain and loss-of-function studies, mass spectrometry analysis, RNA-seq, and phospho-antibody array, we identified EEF1AKMT3 as a novel tumor-suppressive methyltransferase that catalyzes the monomethylation of MAP2K7 (MKK7) at K296, thereby decreasing the phosphorylation, ubiquitination, and degradation of TP53. Furthermore, EEF1AKMT3, p-MAP2K7, and TP53 protein levels were positively correlated in GC tissues. Collectively, our results delineate the tumor-suppressive function of the EEF1AKMT3/MAP2K7/TP53 signaling axis and suggest the dysregulation of the signaling axis as potential targeted therapy in GC. •EEF1AKMT3 was identified as gastric tumor suppressor using in vitro and in vivo model.•As a novel EEF1AKMT3 substrate, MAP2K7 was found to be methylated at K296.•Methylated MAP2K7 was revealed to promote TP53 protein stability,.•Experimental data showed that a molecular complex composed of EEF1AKMT3, MAP2K7, and TP53 acts as a tumor suppressor axis and highlights therapeutic exploitability in gastric cancer.</abstract><cop>Clare</cop><pub>Elsevier B.V</pub><doi>10.1016/j.canlet.2022.215803</doi><tpages>1</tpages></addata></record>
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subjects AKT protein
Antibodies
Cell culture
Cloning
EEF1AKMT3
Gastric cancer
Gastric tumor
Gene expression
Invasiveness
MAP2K7
Mass spectroscopy
Medical prognosis
Medical research
Metastases
Metastasis
Methylation
Methyltransferase
Mutagenesis
Nonhistone proteins
p53 Protein
Phosphorylation
Pore size
Protein methylation
Proteins
PTEN protein
Software
Stat3 protein
TP53
Tumor suppressor
Tumorigenesis
Tumors
Ubiquitination
title The EEF1AKMT3/MAP2K7/TP53 axis suppresses tumor invasiveness and metastasis in gastric cancer
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