Radiation Resistance in KRAS-Mutated Lung Cancer Is Enabled by Stem-like Properties Mediated by an Osteopontin–EGFR Pathway

Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here, we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized b...

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Published inCancer research (Chicago, Ill.) Vol. 77; no. 8; pp. 2018 - 2028
Main Authors Wang, Meng, Han, Jing, Marcar, Lynnette, Black, Josh, Liu, Qi, Li, Xiangyong, Nagulapalli, Kshithija, Sequist, Lecia V., Mak, Raymond H., Benes, Cyril H., Hong, Theodore S., Gurtner, Kristin, Krause, Mechthild, Baumann, Michael, Kang, Jing X., Whetstine, Johnathan R., Willers, Henning
Format Journal Article
LanguageEnglish
Published United States American Association for Cancer Research, Inc 15.04.2017
Subjects
A549 Cells
Animals
Cancer therapies
Carcinoma, Non-Small-Cell Lung - genetics
Carcinoma, Non-Small-Cell Lung - metabolism
Carcinoma, Non-Small-Cell Lung - pathology
Carcinoma, Non-Small-Cell Lung - radiotherapy
Chromatin
DNA damage
Epidermal growth factor receptors
Female
Genotype & phenotype
Heterografts
Humans
Invasiveness
K-Ras protein
Lung cancer
Lung Neoplasms - genetics
Lung Neoplasms - metabolism
Lung Neoplasms - pathology
Lung Neoplasms - radiotherapy
Lungs
Male
Mice
Mice, Nude
Mitosis
Mutation
Neoplastic Stem Cells - metabolism
Neoplastic Stem Cells - pathology
Neoplastic Stem Cells - radiation effects
Osteopontin
Osteopontin - biosynthesis
Osteopontin - genetics
Osteopontin - metabolism
p53 Protein
Proto-Oncogene Proteins p21(ras) - genetics
Proto-Oncogene Proteins p21(ras) - metabolism
Radiation Tolerance - genetics
Receptor, Epidermal Growth Factor - metabolism
Signal Transduction
Treatment resistance
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Abstract Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here, we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized by mitosis-like condensed chromatin (MLCC), high CD133 expression, invasive potential, and tumor-initiating properties. Mechanistic investigations defined a pathway involving osteopontin and the EGFR in promoting this phenotype. Osteopontin/EGFR–dependent MLCC protected cells against radiation-induced DNA double-strand breaks and repressed putative negative regulators of stem-like properties, such as CRMP1 and BIM. The MLCC-positive phenotype defined a subset of KRAS-mutated lung cancers that were enriched for co-occurring genomic alterations in TP53 and CDKN2A. Our results illuminate the basis for the radiation resistance of KRAS-mutated lung cancers, with possible implications for prognostic and therapeutic strategies. Cancer Res; 77(8); 2018–28. ©2017 AACR.
AbstractList Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized by mitosis-like condensed chromatin (MLCC), high CD133 expression, invasive potential, and tumor-initiating properties. Mechanistic investigations defined a pathway involving osteopontin and the EGFR in promoting this phenotype. Osteopontin/EGFR-dependent MLCC protected cells against radiation-induced DNA double-strand breaks and repressed putative negative regulators of stem-like properties such as CRMP1 and BIM. The MLCC-positive phenotype defined a subset of KRAS-mutated lung cancers that were enriched for co-occurring genomic alterations in TP53 and CDKN2A. Our results illuminate the basis for the radiation resistance of KRAS-mutated lung cancers with possible implications for prognostic and therapeutic strategies.
In elucidating mechanisms that link the stem-like phenotype of KRAS-mutated lung cancer cells to radiation resistance, this study identifies potential therapeutic targets to overcome this resistance.Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here, we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized by mitosis-like condensed chromatin (MLCC), high CD133 expression, invasive potential, and tumor-initiating properties. Mechanistic investigations defined a pathway involving osteopontin and the EGFR in promoting this phenotype. Osteopontin/EGFR–dependent MLCC protected cells against radiation-induced DNA double-strand breaks and repressed putative negative regulators of stem-like properties, such as CRMP1 and BIM. The MLCC-positive phenotype defined a subset of KRAS-mutated lung cancers that were enriched for co-occurring genomic alterations in TP53 and CDKN2A. Our results illuminate the basis for the radiation resistance of KRAS-mutated lung cancers, with possible implications for prognostic and therapeutic strategies. Cancer Res; 77(8); 2018–28. ©2017 AACR.
Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here, we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized by mitosis-like condensed chromatin (MLCC), high CD133 expression, invasive potential, and tumor-initiating properties. Mechanistic investigations defined a pathway involving osteopontin and the EGFR in promoting this phenotype. Osteopontin/EGFR-dependent MLCC protected cells against radiation-induced DNA double-strand breaks and repressed putative negative regulators of stem-like properties, such as CRMP1 and BIM. The MLCC-positive phenotype defined a subset of KRAS-mutated lung cancers that were enriched for co-occurring genomic alterations in TP53 and CDKN2A. Our results illuminate the basis for the radiation resistance of KRAS-mutated lung cancers, with possible implications for prognostic and therapeutic strategies. Cancer Res; 77(8); 2018-28. ©2017 AACR.
In elucidating mechanisms that link the stem-like phenotype of KRAS-mutated lung cancer cells to radiation resistance, this study identifies potential therapeutic targets to overcome this resistance. Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here, we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized by mitosis-like condensed chromatin (MLCC), high CD133 expression, invasive potential, and tumor-initiating properties. Mechanistic investigations defined a pathway involving osteopontin and the EGFR in promoting this phenotype. Osteopontin/EGFR-dependent MLCC protected cells against radiation-induced DNA double-strand breaks and repressed putative negative regulators of stem-like properties, such as CRMP1 and BIM. The MLCC-positive phenotype defined a subset of KRAS-mutated lung cancers that were enriched for co-occurring genomic alterations in TP53 and CDKN2A. Our results illuminate the basis for the radiation resistance of KRAS-mutated lung cancers, with possible implications for prognostic and therapeutic strategies. Cancer Res; 77(8); 2018-28. [copy2017 AACR.
Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to radiation therapy is poorly understood. Here, we describe a radiation resistance phenotype conferred by a stem-like subpopulation characterized by mitosis-like condensed chromatin (MLCC), high CD133 expression, invasive potential, and tumor-initiating properties. Mechanistic investigations defined a pathway involving osteopontin and the EGFR in promoting this phenotype. Osteopontin/EGFR-dependent MLCC protected cells against radiation-induced DNA double-strand breaks and repressed putative negative regulators of stem-like properties, such as CRMP1 and BIM. The MLCC-positive phenotype defined a subset of KRAS-mutated lung cancers that were enriched for co-occurring genomic alterations in TP53 and CDKN2A. Our results illuminate the basis for the radiation resistance of KRAS-mutated lung cancers, with possible implications for prognostic and therapeutic strategies. .
Author Willers, Henning
Black, Josh
Krause, Mechthild
Baumann, Michael
Whetstine, Johnathan R.
Wang, Meng
Gurtner, Kristin
Liu, Qi
Li, Xiangyong
Marcar, Lynnette
Mak, Raymond H.
Benes, Cyril H.
Nagulapalli, Kshithija
Kang, Jing X.
Han, Jing
Sequist, Lecia V.
Hong, Theodore S.
AuthorAffiliation 8 Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts
5 Laboratory for Lipid Medicine and Technology, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts
6 Center for Computational Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts
2 Jinan Municipal Center for Disease Control and Prevention, Shandong, China
4 Center for Cancer Research, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts
7 Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
3 University of Colorado School of Medicine, Aurora, Colorado
1 Department of Radiation Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
9 Department of Radiation Oncology, Medical Faculty and University Hospital Carl Gustav Carus, Technische Universität Dresden; OncoRay National Center for Radiation Research in Oncology; Medical Facul
AuthorAffiliation_xml – name: 7 Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
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Snippet Lung cancers with activating KRAS mutations are characterized by treatment resistance and poor prognosis. In particular, the basis for their resistance to...
In elucidating mechanisms that link the stem-like phenotype of KRAS-mutated lung cancer cells to radiation resistance, this study identifies potential...
SourceID pubmedcentral
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StartPage 2018
SubjectTerms A549 Cells
Animals
Cancer therapies
Carcinoma, Non-Small-Cell Lung - genetics
Carcinoma, Non-Small-Cell Lung - metabolism
Carcinoma, Non-Small-Cell Lung - pathology
Carcinoma, Non-Small-Cell Lung - radiotherapy
Chromatin
DNA damage
Epidermal growth factor receptors
Female
Genotype & phenotype
Heterografts
Humans
Invasiveness
K-Ras protein
Lung cancer
Lung Neoplasms - genetics
Lung Neoplasms - metabolism
Lung Neoplasms - pathology
Lung Neoplasms - radiotherapy
Lungs
Male
Mice
Mice, Nude
Mitosis
Mutation
Neoplastic Stem Cells - metabolism
Neoplastic Stem Cells - pathology
Neoplastic Stem Cells - radiation effects
Osteopontin
Osteopontin - biosynthesis
Osteopontin - genetics
Osteopontin - metabolism
p53 Protein
Proto-Oncogene Proteins p21(ras) - genetics
Proto-Oncogene Proteins p21(ras) - metabolism
Radiation Tolerance - genetics
Receptor, Epidermal Growth Factor - metabolism
Signal Transduction
Treatment resistance
Title Radiation Resistance in KRAS-Mutated Lung Cancer Is Enabled by Stem-like Properties Mediated by an Osteopontin–EGFR Pathway
URI https://www.ncbi.nlm.nih.gov/pubmed/28202526
https://www.proquest.com/docview/1983364301
https://www.proquest.com/docview/1869074310
https://www.proquest.com/docview/1897390754
https://pubmed.ncbi.nlm.nih.gov/PMC5445902
Volume 77
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