Mosaic Analysis with Double Markers Reveals Tumor Cell of Origin in Glioma

Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity. Thus, an ideal approach to identify the cell of origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Her...

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Published in	Cell Vol. 146; no. 2; pp. 209 - 221
Main Authors	Liu, Chong, Sage, Jonathan C., Miller, Michael R., Verhaak, Roel G.W., Hippenmeyer, Simon, Vogel, Hannes, Foreman, Oded, Bronson, Roderick T., Nishiyama, Akiko, Luo, Liqun, Zong, Hui
Format	Journal Article
Language	English
Published	United States Elsevier Inc 22.07.2011
Subjects	Animal models Animals Astrocytes - pathology Biomarkers Brain Neoplasms - embryology Brain Neoplasms - genetics Brain Neoplasms - pathology Brain tumors Gene expression Genes, p53 Glial stem cells Glioma Glioma - embryology Glioma - genetics Glioma - pathology Malignancy Mice Molecular Sequence Data Mosaicism Mosaics Mutation neoplasm cells neoplasms Neoplastic Stem Cells - pathology Neural stem cells Neural Stem Cells - pathology Neurofibromin 1 - genetics Neurons - pathology Oligodendroglia - pathology p53 protein stem cells transcriptome Tumor cells Tumors
Online Access	Get full text
ISSN	0092-8674 1097-4172 1097-4172
DOI	10.1016/j.cell.2011.06.014

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Abstract	Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity. Thus, an ideal approach to identify the cell of origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Here, we use mosaic analysis with double markers (MADM) in mice to model gliomagenesis by initiating concurrent p53/Nf1 mutations sporadically in neural stem cells (NSCs). Surprisingly, MADM-based lineage tracing revealed significant aberrant growth prior to malignancy only in oligodendrocyte precursor cells (OPCs), but not in any other NSC-derived lineages or NSCs themselves. Upon tumor formation, phenotypic and transcriptome analyses of tumor cells revealed salient OPC features. Finally, introducing the same p53/Nf1 mutations directly into OPCs consistently led to gliomagenesis. Our findings suggest OPCs as the cell of origin in this model, even when initial mutations occur in NSCs, and highlight the importance of analyzing premalignant stages to identify the cancer cell of origin. [Display omitted] ► Modeling human glioma using mosaic analysis with double markers (MADM) ► Tracking lineage-specific aberrant growth at pretransformation stages ► Oligodendrocyte precursor cells (OPCs) are a cell of origin for glioma ► Cancer cell of mutation and cell of origin are distinct
AbstractList	Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity. Thus, an ideal approach to identify the cell of origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Here, we use mosaic analysis with double markers (MADM) in mice to model gliomagenesis by initiating concurrent p53/Nf1 mutations sporadically in neural stem cells (NSCs). Surprisingly, MADM-based lineage tracing revealed significant aberrant growth prior to malignancy only in oligodendrocyte precursor cells (OPCs), but not in any other NSC-derived lineages or NSCs themselves. Upon tumor formation, phenotypic and transcriptome analyses of tumor cells revealed salient OPC features. Finally, introducing the same p53/Nf1 mutations directly into OPCs consistently led to gliomagenesis. Our findings suggest OPCs as the cell of origin in this model, even when initial mutations occur in NSCs, and highlight the importance of analyzing premalignant stages to identify the cancer cell of origin. Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity. Thus, an ideal approach to identify the cell of origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Here, we use mosaic analysis with double markers (MADM) in mice to model gliomagenesis by initiating concurrent p53/Nf1 mutations sporadically in neural stem cells (NSCs). Surprisingly, MADM-based lineage tracing revealed significant aberrant growth prior to malignancy only in oligodendrocyte precursor cells (OPCs), but not in any other NSC-derived lineages or NSCs themselves. Upon tumor formation, phenotypic and transcriptome analyses of tumor cells revealed salient OPC features. Finally, introducing the same p53/Nf1 mutations directly into OPCs consistently led to gliomagenesis. Our findings suggest OPCs as the cell of origin in this model, even when initial mutations occur in NSCs, and highlight the importance of analyzing premalignant stages to identify the cancer cell of origin.Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity. Thus, an ideal approach to identify the cell of origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Here, we use mosaic analysis with double markers (MADM) in mice to model gliomagenesis by initiating concurrent p53/Nf1 mutations sporadically in neural stem cells (NSCs). Surprisingly, MADM-based lineage tracing revealed significant aberrant growth prior to malignancy only in oligodendrocyte precursor cells (OPCs), but not in any other NSC-derived lineages or NSCs themselves. Upon tumor formation, phenotypic and transcriptome analyses of tumor cells revealed salient OPC features. Finally, introducing the same p53/Nf1 mutations directly into OPCs consistently led to gliomagenesis. Our findings suggest OPCs as the cell of origin in this model, even when initial mutations occur in NSCs, and highlight the importance of analyzing premalignant stages to identify the cancer cell of origin. Cancer cell-of-origin is difficult to identify by analyzing cells within terminal-stage tumors, whose identity could be concealed by the acquired plasticity. Thus an ideal approach to identify the cell-of-origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Here we use Mosaic Analysis with Double Markers (MADM) in mice to model gliomagenesis by initiating concurrent p53/Nf1 mutations sporadically in neural stem cells (NSCs). Surprisingly, MADM-based lineage tracing revealed significant aberrant growth prior to malignancy only in oligodendrocyte precursor cells (OPCs), but not in any other NSC-derived lineages or NSCs themselves. Upon tumor formation, phenotypic and transcriptome analyses of tumor cells revealed salient OPC features. Finally, introducing the same p53/Nf1 mutations directly into OPCs consistently led to gliomagenesis. Our findings suggest OPCs as the cell-of-origin in this model even when initial mutations occur in NSCs, and highlight the importance of analyzing pre-malignant stages to identify the cancer cell-of-origin. Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity. Thus, an ideal approach to identify the cell of origin is to analyze proliferative abnormalities in distinct lineages prior to malignancy. Here, we use mosaic analysis with double markers (MADM) in mice to model gliomagenesis by initiating concurrent p53/Nf1 mutations sporadically in neural stem cells (NSCs). Surprisingly, MADM-based lineage tracing revealed significant aberrant growth prior to malignancy only in oligodendrocyte precursor cells (OPCs), but not in any other NSC-derived lineages or NSCs themselves. Upon tumor formation, phenotypic and transcriptome analyses of tumor cells revealed salient OPC features. Finally, introducing the same p53/Nf1 mutations directly into OPCs consistently led to gliomagenesis. Our findings suggest OPCs as the cell of origin in this model, even when initial mutations occur in NSCs, and highlight the importance of analyzing premalignant stages to identify the cancer cell of origin. [Display omitted] ► Modeling human glioma using mosaic analysis with double markers (MADM) ► Tracking lineage-specific aberrant growth at pretransformation stages ► Oligodendrocyte precursor cells (OPCs) are a cell of origin for glioma ► Cancer cell of mutation and cell of origin are distinct
Author	Liu, Chong Hippenmeyer, Simon Nishiyama, Akiko Luo, Liqun Zong, Hui Verhaak, Roel G.W. Vogel, Hannes Foreman, Oded Bronson, Roderick T. Sage, Jonathan C. Miller, Michael R.
AuthorAffiliation	3 HHMI and Department of Biology, Stanford University, Stanford, CA94305 2 Department of Bioinformatics and Computational Biology, MD Anderson Cancer Center, Houston, TX 77030 4 Neuropathology, Stanford University School of Medicine, Stanford, CA94305 5 The Jackson Laboratory, Sacramento, CA95838 7 Department of Physiology and Neurobiology, University of Connecticut, Storrs, CT06269 1 Institute of Molecular Biology, University of Oregon, Eugene, OR97403 6 Department of Biomedical Sciences, Tufts Cummings School of Veterinary Medicine, North Grafton, MA01536
AuthorAffiliation_xml	– name: 3 HHMI and Department of Biology, Stanford University, Stanford, CA94305 – name: 5 The Jackson Laboratory, Sacramento, CA95838 – name: 6 Department of Biomedical Sciences, Tufts Cummings School of Veterinary Medicine, North Grafton, MA01536 – name: 4 Neuropathology, Stanford University School of Medicine, Stanford, CA94305 – name: 1 Institute of Molecular Biology, University of Oregon, Eugene, OR97403 – name: 2 Department of Bioinformatics and Computational Biology, MD Anderson Cancer Center, Houston, TX 77030 – name: 7 Department of Physiology and Neurobiology, University of Connecticut, Storrs, CT06269
Author_xml	– sequence: 1 givenname: Chong surname: Liu fullname: Liu, Chong organization: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403, USA – sequence: 2 givenname: Jonathan C. surname: Sage fullname: Sage, Jonathan C. organization: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403, USA – sequence: 3 givenname: Michael R. surname: Miller fullname: Miller, Michael R. organization: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403, USA – sequence: 4 givenname: Roel G.W. surname: Verhaak fullname: Verhaak, Roel G.W. organization: Department of Bioinformatics and Computational Biology, MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 5 givenname: Simon surname: Hippenmeyer fullname: Hippenmeyer, Simon organization: HHMI and Department of Biology, Stanford University, Stanford, CA 94305, USA – sequence: 6 givenname: Hannes surname: Vogel fullname: Vogel, Hannes organization: Department of Neuropathology, School of Medicine, Stanford University, Stanford, CA 94305, USA – sequence: 7 givenname: Oded surname: Foreman fullname: Foreman, Oded organization: The Jackson Laboratory, Sacramento, CA 95838, USA – sequence: 8 givenname: Roderick T. surname: Bronson fullname: Bronson, Roderick T. organization: Department of Biomedical Sciences, Tufts Cummings School of Veterinary Medicine, North Grafton, MA 01536, USA – sequence: 9 givenname: Akiko surname: Nishiyama fullname: Nishiyama, Akiko organization: Department of Physiology and Neurobiology, University of Connecticut, Storrs, CT 06269, USA – sequence: 10 givenname: Liqun surname: Luo fullname: Luo, Liqun organization: HHMI and Department of Biology, Stanford University, Stanford, CA 94305, USA – sequence: 11 givenname: Hui surname: Zong fullname: Zong, Hui email: hzong@uoregon.edu organization: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21737130$$D View this record in MEDLINE/PubMed
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Snippet	Cancer cell of origin is difficult to identify by analyzing cells within terminal stage tumors, whose identity could be concealed by the acquired plasticity.... Cancer cell-of-origin is difficult to identify by analyzing cells within terminal-stage tumors, whose identity could be concealed by the acquired plasticity....
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SubjectTerms	Animal models Animals Astrocytes - pathology Biomarkers Brain Neoplasms - embryology Brain Neoplasms - genetics Brain Neoplasms - pathology Brain tumors Gene expression Genes, p53 Glial stem cells Glioma Glioma - embryology Glioma - genetics Glioma - pathology Malignancy Mice Molecular Sequence Data Mosaicism Mosaics Mutation neoplasm cells neoplasms Neoplastic Stem Cells - pathology Neural stem cells Neural Stem Cells - pathology Neurofibromin 1 - genetics Neurons - pathology Oligodendroglia - pathology p53 protein stem cells transcriptome Tumor cells Tumors
Title	Mosaic Analysis with Double Markers Reveals Tumor Cell of Origin in Glioma
URI	https://dx.doi.org/10.1016/j.cell.2011.06.014 https://www.ncbi.nlm.nih.gov/pubmed/21737130 https://www.proquest.com/docview/1093442595 https://www.proquest.com/docview/2000037883 https://www.proquest.com/docview/879101951 https://pubmed.ncbi.nlm.nih.gov/PMC3143261
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