CST1 inhibits ferroptosis and promotes gastric cancer metastasis by regulating GPX4 protein stability via OTUB1

Metastasis is an important factor contributing to poor prognosis in patients with gastric cancer; yet, the molecular mechanism leading to this cell behavior is still not well understood. In this study, we explored the role of cysteine protease inhibitor SN (Cystatin SN, CST1) in promoting gastric ca...

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Vydané v:	Oncogene Ročník 42; číslo 2; s. 83 - 98
Hlavní autori:	Li, Dongbao, Wang, Yuhong, Dong, Chao, Chen, Tao, Dong, Anqi, Ren, Jiayu, Li, Weikang, Shu, Gege, Yang, Jiaoyang, Shen, Wenhao, Qin, Lei, Hu, Lin, Zhou, Jin
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	London Nature Publishing Group UK 05.01.2023 Nature Publishing Group
Predmet:	13 13/51 13/89 38 631/67/1504/1829 692/53/2422 82 82/1 82/58 82/80 Animals Apoptosis Ascites Cell Biology Cell Line, Tumor Cystatins Cysteine proteinase Ferroptosis Ferroptosis - genetics Gastric cancer Human Genetics Immunoprecipitation Internal Medicine Mass spectroscopy Medicine Medicine & Public Health Mesenchyme Metastases Metastasis Mice Mice, Nude Oncology Peripheral blood Prognosis Proteinase inhibitors Proteins Reactive oxygen species Risk factors Salivary Cystatins - metabolism Stomach Neoplasms - pathology Therapeutic targets Transcriptomes Ubiquitination
ISSN:	0950-9232, 1476-5594, 1476-5594
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Abstract	Metastasis is an important factor contributing to poor prognosis in patients with gastric cancer; yet, the molecular mechanism leading to this cell behavior is still not well understood. In this study, we explored the role of cysteine protease inhibitor SN (Cystatin SN, CST1) in promoting gastric cancer metastasis. We hypothesized that CST1 could regulate gastric cancer progression by regulating GPX4 and ferroptosis. Whole transcriptome sequencing suggested that the expression of CST1 was significantly increased in metastatic cancer, and high CST1 expression was correlated with a worse prognosis. Our data further confirmed that the overexpression of CST1 may significantly promote the migration and invasion of gastric cancer cells in vitro and enhance liver, lung, and peritoneal metastasis of gastric cancer in nude mice. Meanwhile, high expression of CST1 promoted the epithelial-mesenchymal transition (EMT) of gastric cancer cells. Mechanistically, a co-immunoprecipitation experiment combined with mass spectrometry analysis confirmed that CST1 could interact with GPX4, a key protein regulating ferroptosis. CST1 relieves GPX4 ubiquitination modification by recruiting OTUB1, improving GPX4 protein stability and reducing intracellular reactive oxygen species (ROS), thereby inhibiting ferroptosis and, in turn, promoting gastric cancer metastasis. Moreover, clinical data suggested that CST1 is significantly increased in peripheral blood and ascites of gastric cancer patients with metastasis; multivariate Cox regression model analysis showed that CST1 was an independent risk factor for the prognosis of gastric cancer patients. Overall, our results elucidated a critical pathway through which high CST1 expression protects gastric cancer cells from undergoing ferroptosis, thus promoting its progression and metastasis. CST1 may be used as a new oncological marker and potential therapeutic target for gastric cancer metastasis.
AbstractList	Metastasis is an important factor contributing to poor prognosis in patients with gastric cancer; yet, the molecular mechanism leading to this cell behavior is still not well understood. In this study, we explored the role of cysteine protease inhibitor SN (Cystatin SN, CST1) in promoting gastric cancer metastasis. We hypothesized that CST1 could regulate gastric cancer progression by regulating GPX4 and ferroptosis. Whole transcriptome sequencing suggested that the expression of CST1 was significantly increased in metastatic cancer, and high CST1 expression was correlated with a worse prognosis. Our data further confirmed that the overexpression of CST1 may significantly promote the migration and invasion of gastric cancer cells in vitro and enhance liver, lung, and peritoneal metastasis of gastric cancer in nude mice. Meanwhile, high expression of CST1 promoted the epithelial-mesenchymal transition (EMT) of gastric cancer cells. Mechanistically, a co-immunoprecipitation experiment combined with mass spectrometry analysis confirmed that CST1 could interact with GPX4, a key protein regulating ferroptosis. CST1 relieves GPX4 ubiquitination modification by recruiting OTUB1, improving GPX4 protein stability and reducing intracellular reactive oxygen species (ROS), thereby inhibiting ferroptosis and, in turn, promoting gastric cancer metastasis. Moreover, clinical data suggested that CST1 is significantly increased in peripheral blood and ascites of gastric cancer patients with metastasis; multivariate Cox regression model analysis showed that CST1 was an independent risk factor for the prognosis of gastric cancer patients. Overall, our results elucidated a critical pathway through which high CST1 expression protects gastric cancer cells from undergoing ferroptosis, thus promoting its progression and metastasis. CST1 may be used as a new oncological marker and potential therapeutic target for gastric cancer metastasis. Metastasis is an important factor contributing to poor prognosis in patients with gastric cancer; yet, the molecular mechanism leading to this cell behavior is still not well understood. In this study, we explored the role of cysteine protease inhibitor SN (Cystatin SN, CST1) in promoting gastric cancer metastasis. We hypothesized that CST1 could regulate gastric cancer progression by regulating GPX4 and ferroptosis. Whole transcriptome sequencing suggested that the expression of CST1 was significantly increased in metastatic cancer, and high CST1 expression was correlated with a worse prognosis. Our data further confirmed that the overexpression of CST1 may significantly promote the migration and invasion of gastric cancer cells in vitro and enhance liver, lung, and peritoneal metastasis of gastric cancer in nude mice. Meanwhile, high expression of CST1 promoted the epithelial-mesenchymal transition (EMT) of gastric cancer cells. Mechanistically, a co-immunoprecipitation experiment combined with mass spectrometry analysis confirmed that CST1 could interact with GPX4, a key protein regulating ferroptosis. CST1 relieves GPX4 ubiquitination modification by recruiting OTUB1, improving GPX4 protein stability and reducing intracellular reactive oxygen species (ROS), thereby inhibiting ferroptosis and, in turn, promoting gastric cancer metastasis. Moreover, clinical data suggested that CST1 is significantly increased in peripheral blood and ascites of gastric cancer patients with metastasis; multivariate Cox regression model analysis showed that CST1 was an independent risk factor for the prognosis of gastric cancer patients. Overall, our results elucidated a critical pathway through which high CST1 expression protects gastric cancer cells from undergoing ferroptosis, thus promoting its progression and metastasis. CST1 may be used as a new oncological marker and potential therapeutic target for gastric cancer metastasis.Metastasis is an important factor contributing to poor prognosis in patients with gastric cancer; yet, the molecular mechanism leading to this cell behavior is still not well understood. In this study, we explored the role of cysteine protease inhibitor SN (Cystatin SN, CST1) in promoting gastric cancer metastasis. We hypothesized that CST1 could regulate gastric cancer progression by regulating GPX4 and ferroptosis. Whole transcriptome sequencing suggested that the expression of CST1 was significantly increased in metastatic cancer, and high CST1 expression was correlated with a worse prognosis. Our data further confirmed that the overexpression of CST1 may significantly promote the migration and invasion of gastric cancer cells in vitro and enhance liver, lung, and peritoneal metastasis of gastric cancer in nude mice. Meanwhile, high expression of CST1 promoted the epithelial-mesenchymal transition (EMT) of gastric cancer cells. Mechanistically, a co-immunoprecipitation experiment combined with mass spectrometry analysis confirmed that CST1 could interact with GPX4, a key protein regulating ferroptosis. CST1 relieves GPX4 ubiquitination modification by recruiting OTUB1, improving GPX4 protein stability and reducing intracellular reactive oxygen species (ROS), thereby inhibiting ferroptosis and, in turn, promoting gastric cancer metastasis. Moreover, clinical data suggested that CST1 is significantly increased in peripheral blood and ascites of gastric cancer patients with metastasis; multivariate Cox regression model analysis showed that CST1 was an independent risk factor for the prognosis of gastric cancer patients. Overall, our results elucidated a critical pathway through which high CST1 expression protects gastric cancer cells from undergoing ferroptosis, thus promoting its progression and metastasis. CST1 may be used as a new oncological marker and potential therapeutic target for gastric cancer metastasis.
Author	Dong, Chao Yang, Jiaoyang Li, Dongbao Li, Weikang Wang, Yuhong Chen, Tao Shu, Gege Hu, Lin Dong, Anqi Ren, Jiayu Qin, Lei Zhou, Jin Shen, Wenhao
Author_xml	– sequence: 1 givenname: Dongbao orcidid: 0000-0002-2905-9079 surname: Li fullname: Li, Dongbao organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 2 givenname: Yuhong surname: Wang fullname: Wang, Yuhong organization: Department of Pathology, The First Affiliated Hospital of Soochow University – sequence: 3 givenname: Chao surname: Dong fullname: Dong, Chao organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 4 givenname: Tao surname: Chen fullname: Chen, Tao organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 5 givenname: Anqi orcidid: 0000-0001-8503-4071 surname: Dong fullname: Dong, Anqi organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 6 givenname: Jiayu surname: Ren fullname: Ren, Jiayu organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 7 givenname: Weikang surname: Li fullname: Li, Weikang organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 8 givenname: Gege surname: Shu fullname: Shu, Gege organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 9 givenname: Jiaoyang surname: Yang fullname: Yang, Jiaoyang organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 10 givenname: Wenhao surname: Shen fullname: Shen, Wenhao organization: State Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection and School for Radiological and Interdisciplinary Sciences (RADX), Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions, Soochow University – sequence: 11 givenname: Lei orcidid: 0000-0003-3323-3989 surname: Qin fullname: Qin, Lei email: qinlei@suda.edu.cn organization: Department of General Surgery, The First Affiliated Hospital of Soochow University – sequence: 12 givenname: Lin orcidid: 0000-0001-8986-3918 surname: Hu fullname: Hu, Lin email: hulin@suda.edu.cn organization: State Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection and School for Radiological and Interdisciplinary Sciences (RADX), Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions, Soochow University – sequence: 13 givenname: Jin orcidid: 0000-0002-6829-6149 surname: Zhou fullname: Zhou, Jin email: zhoujinsuda@suda.edu.cn organization: Department of General Surgery, The First Affiliated Hospital of Soochow University
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Snippet	Metastasis is an important factor contributing to poor prognosis in patients with gastric cancer; yet, the molecular mechanism leading to this cell behavior is...
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SubjectTerms	13 13/51 13/89 38 631/67/1504/1829 692/53/2422 82 82/1 82/58 82/80 Animals Apoptosis Ascites Cell Biology Cell Line, Tumor Cystatins Cysteine proteinase Ferroptosis Ferroptosis - genetics Gastric cancer Human Genetics Immunoprecipitation Internal Medicine Mass spectroscopy Medicine Medicine & Public Health Mesenchyme Metastases Metastasis Mice Mice, Nude Oncology Peripheral blood Prognosis Proteinase inhibitors Proteins Reactive oxygen species Risk factors Salivary Cystatins - metabolism Stomach Neoplasms - pathology Therapeutic targets Transcriptomes Ubiquitination
Title	CST1 inhibits ferroptosis and promotes gastric cancer metastasis by regulating GPX4 protein stability via OTUB1
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