TIP60 is required for tumorigenesis in non‐small cell lung cancer

Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer re...

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Published inCancer science Vol. 114; no. 6; pp. 2400 - 2413
Main Authors Shibahara, Daisuke, Akanuma, Naoki, Kobayashi, Ikei S., Heo, Eunyoung, Ando, Mariko, Fujii, Masanori, Jiang, Feng, Prin, P. Nicholas, Pan, Gilbert, Wong, Kwok‐Kin, Costa, Daniel B., Bararia, Deepak, Tenen, Daniel G., Watanabe, Hideo, Kobayashi, Susumu S.
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.06.2023
John Wiley and Sons Inc
Subjects
Acetyltransferase
Animals
Antitumor activity
artemisinin
Cancer therapies
Carcinogenesis - genetics
Carcinoma, Non-Small-Cell Lung - genetics
Cell adhesion & migration
Cell culture
Cell growth
Cell migration
Cell Transformation, Neoplastic - genetics
Cloning
Comparative analysis
Datasets
Epigenetics
Experiments
Histone Acetyltransferases - genetics
Histone Acetyltransferases - metabolism
Histones
Homeostasis
Humans
Hypotheses
KAT5
Kinases
Lung cancer
Lung Neoplasms - genetics
Mice
Mutation
Non-small cell lung carcinoma
Original
Prostate
Proteins
Sarcoma
Small cell lung carcinoma
TGM5
TIP60
Transcription activation
Tumor cell lines
Tumorigenesis
Wound healing
artemisinin
lung cancer
KAT5
TGM5
TIP60
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Abstract Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non‐small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung‐specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA‐seq and ChIP‐seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo. In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo. Taken together, suppression of TIP60 activity shows tumor‐specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer. Genetic and pharmacological inhibition of TIP60 attenuates tumorigenesis in non‐small cell lung cancer, implicating that targeting TIP60 could be a novel approach for lung cancer treatment.
AbstractList Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non-small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung-specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA-seq and ChIP-seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo. In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo. Taken together, suppression of TIP60 activity shows tumor-specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer.Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non-small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung-specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA-seq and ChIP-seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo. In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo. Taken together, suppression of TIP60 activity shows tumor-specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer.
Abstract Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non‐small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung‐specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA‐seq and ChIP‐seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo . In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo . Taken together, suppression of TIP60 activity shows tumor‐specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer.
Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non‐small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung‐specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA‐seq and ChIP‐seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo. In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo. Taken together, suppression of TIP60 activity shows tumor‐specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer. Genetic and pharmacological inhibition of TIP60 attenuates tumorigenesis in non‐small cell lung cancer, implicating that targeting TIP60 could be a novel approach for lung cancer treatment.
Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non-small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung-specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA-seq and ChIP-seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo. In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo. Taken together, suppression of TIP60 activity shows tumor-specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer.
Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K) acetyltransferases 5 (TIP60, also known as KAT5) is reportedly implicated in cancer development and maintenance, although its function in lung cancer remains controversial. Here we demonstrate that TIP60 knockdown in non‐small cell lung cancer cell lines decreased tumor cell growth, migration, and invasion. Furthermore, analysis of a mouse lung cancer model with lung‐specific conditional Tip60 knockout revealed suppressed tumor formation relative to controls, but no apparent effects on normal lung homeostasis. RNA‐seq and ChIP‐seq analyses of inducible TIP60 knockdown H1975 cells relative to controls revealed transglutaminase enzyme (TGM5) as downstream of TIP60. Investigation of a connectivity map database identified several candidate compounds that decrease TIP60 mRNA, one that suppressed tumor growth in cell culture and in vivo . In addition, TH1834, a TIP60 acetyltransferase inhibitor, showed comparable antitumor effects in cell culture and in vivo . Taken together, suppression of TIP60 activity shows tumor‐specific efficacy against lung cancer, with no overt effect on normal tissues. Our work suggests that targeting TIP60 could be a promising approach to treating lung cancer. Genetic and pharmacological inhibition of TIP60 attenuates tumorigenesis in non‐small cell lung cancer, implicating that targeting TIP60 could be a novel approach for lung cancer treatment.
Author Akanuma, Naoki
Jiang, Feng
Heo, Eunyoung
Kobayashi, Ikei S.
Watanabe, Hideo
Shibahara, Daisuke
Bararia, Deepak
Costa, Daniel B.
Ando, Mariko
Tenen, Daniel G.
Pan, Gilbert
Prin, P. Nicholas
Wong, Kwok‐Kin
Fujii, Masanori
Kobayashi, Susumu S.
AuthorAffiliation 5 Perlmutter Cancer Center NYU Langone Medical Center New York New York USA
1 Department of Medicine, Beth Israel Deaconess Medical Center Harvard Medical School Boston Massachusetts USA
4 Division of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Department of Genetics and Genomic Sciences Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai New York New York USA
8 Division of Translational Genomics, Exploratory Oncology Research and Clinical Trial Center National Cancer Center Kashiwa Japan
3 Department of Internal Medicine SMG‐SNU Boramae Medical Center Seoul South Korea
2 Department of Pathology University of California San Francisco San Francisco California USA
7 Cancer Science Institute of Singapore National University of Singapore Singapore Singapore
6 Harvard Stem Cell Institute, Harvard Medical School Boston Massachusetts USA
AuthorAffiliation_xml – name: 2 Department of Pathology University of California San Francisco San Francisco California USA
– name: 5 Perlmutter Cancer Center NYU Langone Medical Center New York New York USA
– name: 6 Harvard Stem Cell Institute, Harvard Medical School Boston Massachusetts USA
– name: 3 Department of Internal Medicine SMG‐SNU Boramae Medical Center Seoul South Korea
– name: 7 Cancer Science Institute of Singapore National University of Singapore Singapore Singapore
– name: 4 Division of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Department of Genetics and Genomic Sciences Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai New York New York USA
– name: 1 Department of Medicine, Beth Israel Deaconess Medical Center Harvard Medical School Boston Massachusetts USA
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Keywords artemisinin
lung cancer
KAT5
TGM5
TIP60
Language English
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2023 The Authors. Cancer Science published by John Wiley & Sons Australia, Ltd on behalf of Japanese Cancer Association.
This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
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Notes Daisuke Shibahara and Naoki Akanuma contributed equally to this work.
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Snippet Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K)...
Abstract Histone modifications play crucial roles in transcriptional activation, and aberrant epigenetic changes are associated with oncogenesis. Lysine (K)...
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SubjectTerms Acetyltransferase
Animals
Antitumor activity
artemisinin
Cancer therapies
Carcinogenesis - genetics
Carcinoma, Non-Small-Cell Lung - genetics
Cell adhesion & migration
Cell culture
Cell growth
Cell migration
Cell Transformation, Neoplastic - genetics
Cloning
Comparative analysis
Datasets
Epigenetics
Experiments
Histone Acetyltransferases - genetics
Histone Acetyltransferases - metabolism
Histones
Homeostasis
Humans
Hypotheses
KAT5
Kinases
Lung cancer
Lung Neoplasms - genetics
Mice
Mutation
Non-small cell lung carcinoma
Original
Prostate
Proteins
Sarcoma
Small cell lung carcinoma
TGM5
TIP60
Transcription activation
Tumor cell lines
Tumorigenesis
Wound healing
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Title TIP60 is required for tumorigenesis in non‐small cell lung cancer
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fcas.15785
https://www.ncbi.nlm.nih.gov/pubmed/36916958
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https://pubmed.ncbi.nlm.nih.gov/PMC10236639
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