Cited by 131Protein Kinase Regulation and GTPase SignalingProtein Tyrosine PhosphatasesDevelopmental Biology and Gene Regulation

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Sprouty-2 regulates oncogenic K-ras in lung development and tumorigenesis

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Shaw, Alice T., Meissner, Alexander, Dowdle, James A., Crowley, Denise, Magendantz, Margaret, Ouyang, Chensi, Parisi, Tiziana, Rajagopal, Jayaraj, Blank, Leah J., Bronson, Roderick T., Stone, James R., Tuveson, David A., Jaenisch, Rudolf, Jacks, Tyler·2007·Genes & Development

DOI 10.1101/gad.1526207PMC PMC1820943

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Abstract

Somatic activation of Ras occurs frequently in human cancers, including one-third of lung cancers. Activating Ras mutations also occur in the germline, leading to complex developmental syndromes. The precise mechanism by which Ras activation results in human disease is uncertain. Here we describe the phenotype of a mouse engineered to harbor a germline oncogenic K-ras G12D mutation. This mouse exhibits early embryonic lethality due to a placental trophoblast defect. Reconstitution with a wild-type placenta rescues the early lethality, but mutant embryos still succumb to cardiovascular and hematopoietic defects. In addition, mutant embryos demonstrate a profound defect in lung branching morphogenesis associated with striking up-regulation of the Ras/mitogen-activated protein kinase (MAPK) antagonist Sprouty-2 and abnormal localization of MAPK activity within the lung epithelium. This defect can be significantly suppressed by lentiviral short hairpin RNA (shRNA)-mediated knockdown of Sprouty-2 in vivo. Furthermore, in the context of K-ras G12D -mediated lung tumorigenesis, Sprouty-2 is also up-regulated and functions as a tumor suppressor to limit tumor number and overall tumor burden. These findings indicate that in the lung, Sprouty-2 plays a critical role in the regulation of oncogenic K-ras, and implicate counter-regulatory mechanisms in the pathogenesis of Ras-based disease.

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Authors: Shaw, A. T., Meissner, A., Dowdle, J. A., Crowley, D., Magendantz, M., Ouyang, C., Parisi, T., Rajagopal, J., Blank, L. J., Bronson, R. T., Stone, J. R., Tuveson, D. A., Jaenisch, R., & Jacks, T.
Affiliations: Harvard University (US)
Whitehead Institute for Biomedical Research (US)
Massachusetts Institute of Technology (US)
Howard Hughes Medical Institute (US)
Tufts University (US)
Corresponding author: Jacks, Tyler
ORCID: Shaw, Alice T.
Meissner, Alexander
Dowdle, James A.
Ouyang, Chensi
Rajagopal, Jayaraj
Blank, Leah J.
Bronson, Roderick T.
Stone, James R.
Tuveson, David A.
Jaenisch, Rudolf
Jacks, Tyler
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2007-03-15
Volume: 21
Issue: 6
Pages: 694-707
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.1526207
PMC: PMC1820943
OpenAlex: W2102049157
Cited by: 131
References: 49
Citations by year: 2026: 1 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 5 · 2018: 3 · 2017: 3 · 2016: 9 · 2015: 11 · 2014: 6 · 2013: 9 · 2012: 7
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Genes & Development (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Funders: Howard Hughes Medical Institute (P30-CA14051)
Damon Runyon Cancer Research Foundation
National Cancer Institute (5K08CA111634-2, 5-U01-CA84306-06, CA14051, U01CA084306, K08CA111634, P30CA014051, P30-CA-14051)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Tyrosine Phosphatases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: Sprouty2, KRAS G12D, lung development, lung carcinogenesis, lung branching morphogenesis, MAPK signaling, tumor suppressor, embryonic lethality, cardiovascular defects, hematopoietic defects
MeSH terms: Animals, Base Sequence, Female, Humans, Lung, Lung Neoplasms, Membrane Proteins, Mice, Transgenic, Pregnancy, Genes, ras, RNA, Gene Expression Regulation, Neoplastic, Protein Serine-Threonine Kinases, Germ-Line Mutation, Mice, Knockout, Gene Expression Regulation, Developmental, MAP Kinase Signaling System, Embryo Loss, Intracellular Signaling Peptides and Proteins, Adaptor Proteins, Signal Transducing, Mice

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Sprouty-2 regulates oncogenic K-ras in lung development and tumorigenesis

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