Truncated PPM1D impairs stem cell response to genotoxic stress and promotes growth of APC-deficient tumors in the mouse colon

Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gai...

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Published inCell death & disease Vol. 10; no. 11; pp. 818 - 15
Main Authors Burocziova, Monika, Burdova, Kamila, Martinikova, Andra S., Kasparek, Petr, Kleiblova, Petra, Danielsen, Stine A., Borecka, Marianna, Jenikova, Gabriela, Janečková, Lucie, Pavel, Jozef, Zemankova, Petra, Schneiderova, Michaela, Schwarzova, Lucie, Ticha, Ivana, Sun, Xiao-Feng, Jiraskova, Katerina, Liska, Vaclav, Vodickova, Ludmila, Vodicka, Pavel, Sedlacek, Radislav, Kleibl, Zdenek, Lothe, Ragnhild A., Korinek, Vladimír, Macurek, Libor
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 28.10.2019
Springer Nature B.V
Subjects
13
13/1
13/100
13/106
13/31
13/51
38/23
5-Fluorouracil
631/67/70
631/80/641/2187
64
64/60
82/29
Adenomatous polyposis coli
Adenomatous Polyposis Coli Protein - genetics
Animals
Antibodies
Biochemistry
Biomedical and Life Sciences
Carcinogenesis - drug effects
Cell activation
Cell Biology
Cell Culture
Cell cycle
Cell Cycle Checkpoints - genetics
Cell proliferation
Cell Proliferation - drug effects
Chemotherapy
Chromatin
Chromatin - drug effects
Colonic Neoplasms - drug therapy
Colonic Neoplasms - genetics
Colonic Neoplasms - pathology
Colorectal cancer
Colorectal carcinoma
Deoxyribonucleic acid
DNA
DNA damage
DNA Damage - drug effects
DNA repair
DNA Repair - drug effects
Exons - genetics
Fluorouracil - pharmacology
Gene Expression Regulation, Neoplastic - drug effects
Genotoxicity
Humans
Immunology
Life Sciences
Magnesium
Mice
Mutation
Mutation - genetics
Organoids
p53 Protein
Protein phosphatase
Protein Phosphatase 2C - genetics
Stem cell transplantation
Stem cells
Tumor suppressor genes
Tumor Suppressor Protein p53 - genetics
Tumorigenesis
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Abstract Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1D T allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1D T resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apc min mice and diminished survival. Moreover, tumor organoids derived from colon of the Apc min Ppm1d T/+ mice were less sensitive to 5-fluorouracil when compared to Apc min Ppm1d +/+ and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.
AbstractList Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1D(T) allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1D(T) resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apc(min) mice and diminished survival. Moreover, tumor organoids derived from colon of the Apc(min)Ppm1d(T/+) mice were less sensitive to 5-fluorouracil when compared to Apc(min)Ppm1d(+/+)and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.
Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1DT allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1DT resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apcmin mice and diminished survival. Moreover, tumor organoids derived from colon of the ApcminPpm1dT/+ mice were less sensitive to 5-fluorouracil when compared to ApcminPpm1d+/+and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1DT allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1DT resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apcmin mice and diminished survival. Moreover, tumor organoids derived from colon of the ApcminPpm1dT/+ mice were less sensitive to 5-fluorouracil when compared to ApcminPpm1d+/+and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.
Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1D allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1D resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apc mice and diminished survival. Moreover, tumor organoids derived from colon of the Apc Ppm1d mice were less sensitive to 5-fluorouracil when compared to Apc Ppm1d and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.
Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1DT allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1DT resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apcmin mice and diminished survival. Moreover, tumor organoids derived from colon of the ApcminPpm1dT/+ mice were less sensitive to 5-fluorouracil when compared to ApcminPpm1d+/+and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.
Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and other targets at chromatin. Mutations in the exon 6 of the PPM1D result in production of a highly stable, C-terminally truncated PPM1D. These gain-of-function PPM1D mutations are present in various human cancers but their role in tumorigenesis remains unresolved. Here we show that truncated PPM1D impairs activation of the cell cycle checkpoints in human non-transformed RPE cells and allows proliferation in the presence of DNA damage. Next, we developed a mouse model by introducing a truncating mutation in the PPM1D locus and tested contribution of the oncogenic PPM1D T allele to colon tumorigenesis. We found that p53 pathway was suppressed in colon stem cells harboring PPM1D T resulting in proliferation advantage under genotoxic stress condition. In addition, truncated PPM1D promoted tumor growth in the colon in Apc min mice and diminished survival. Moreover, tumor organoids derived from colon of the Apc min Ppm1d T/+ mice were less sensitive to 5-fluorouracil when compared to Apc min Ppm1d +/+ and the sensitivity to 5-fluorouracil was restored by inhibition of PPM1D. Finally, we screened colorectal cancer patients and identified recurrent somatic PPM1D mutations in a fraction of colon adenocarcinomas that are p53 proficient and show defects in mismatch DNA repair. In summary, we provide the first in vivo evidence that truncated PPM1D can promote tumor growth and modulate sensitivity to chemotherapy.
ArticleNumber 818
Author Danielsen, Stine A.
Vodicka, Pavel
Kasparek, Petr
Liska, Vaclav
Vodickova, Ludmila
Ticha, Ivana
Jenikova, Gabriela
Schwarzova, Lucie
Borecka, Marianna
Burdova, Kamila
Kleiblova, Petra
Pavel, Jozef
Zemankova, Petra
Jiraskova, Katerina
Macurek, Libor
Sedlacek, Radislav
Burocziova, Monika
Martinikova, Andra S.
Schneiderova, Michaela
Sun, Xiao-Feng
Korinek, Vladimír
Kleibl, Zdenek
Lothe, Ragnhild A.
Janečková, Lucie
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Snippet Protein phosphatase magnesium-dependent 1 delta (PPM1D) terminates cell response to genotoxic stress by negatively regulating the tumor suppressor p53 and...
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Adenomatous polyposis coli
Adenomatous Polyposis Coli Protein - genetics
Animals
Antibodies
Biochemistry
Biomedical and Life Sciences
Carcinogenesis - drug effects
Cell activation
Cell Biology
Cell Culture
Cell cycle
Cell Cycle Checkpoints - genetics
Cell proliferation
Cell Proliferation - drug effects
Chemotherapy
Chromatin
Chromatin - drug effects
Colonic Neoplasms - drug therapy
Colonic Neoplasms - genetics
Colonic Neoplasms - pathology
Colorectal cancer
Colorectal carcinoma
Deoxyribonucleic acid
DNA
DNA damage
DNA Damage - drug effects
DNA repair
DNA Repair - drug effects
Exons - genetics
Fluorouracil - pharmacology
Gene Expression Regulation, Neoplastic - drug effects
Genotoxicity
Humans
Immunology
Life Sciences
Magnesium
Mice
Mutation
Mutation - genetics
Organoids
p53 Protein
Protein phosphatase
Protein Phosphatase 2C - genetics
Stem cell transplantation
Stem cells
Tumor suppressor genes
Tumor Suppressor Protein p53 - genetics
Tumorigenesis
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Title Truncated PPM1D impairs stem cell response to genotoxic stress and promotes growth of APC-deficient tumors in the mouse colon
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Volume 10
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