Cited by 2,311Autophagy in Disease and TherapyCancer-related Molecular PathwaysUbiquitin and proteasome pathways

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Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene

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Qu, Xueping, Yu, Jie, Bhagat, Govind, Furuya, Norihiko, Hibshoosh, Hanina, Troxel, Andrea, Rosen, Jeffrey, Eskelinen, Eeva-Liisa, Mizushima, Noboru, Ohsumi, Yoshinori, Cattoretti, Giorgio, Levine, Beth·2003·Journal of Clinical Investigation

DOI 10.1172/jci20039PMC PMC297002

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Abstract

Malignant cells often display defects in autophagy, an evolutionarily conserved pathway for degrading long-lived proteins and cytoplasmic organelles. However, as yet, there is no genetic evidence for a role of autophagy genes in tumor suppression. The beclin 1 autophagy gene is monoallelically deleted in 40-75% of cases of human sporadic breast, ovarian, and prostate cancer. Therefore, we used a targeted mutant mouse model to test the hypothesis that monoallelic deletion of beclin 1 promotes tumorigenesis. Here we show that heterozygous disruption of beclin 1 increases the frequency of spontaneous malignancies and accelerates the development of hepatitis B virus-induced premalignant lesions. Molecular analyses of tumors in beclin 1 heterozygous mice show that the remaining wild-type allele is neither mutated nor silenced. Furthermore, beclin 1 heterozygous disruption results in increased cellular proliferation and reduced autophagy in vivo. These findings demonstrate that beclin 1 is a haplo-insufficient tumor-suppressor gene and provide genetic evidence that autophagy is a novel mechanism of cell-growth control and tumor suppression. Thus, mutation of beclin 1 or other autophagy genes may contribute to the pathogenesis of human cancers.

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Authors: Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.-L., Mizushima, N., Ohsumi, Y., Cattoretti, G., & Levine, B.
Affiliations: Columbia University (US)
Baylor College of Medicine (US)
National Institute for Basic Biology (JP)
Corresponding author: Levine, Beth
ORCID: Qu, Xueping
Yu, Jie
Bhagat, Govind
Furuya, Norihiko
Hibshoosh, Hanina
Troxel, Andrea
Rosen, Jeffrey
Eskelinen, Eeva-Liisa
Mizushima, Noboru
Ohsumi, Yoshinori
Cattoretti, Giorgio
Levine, Beth
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2003-12-15
Volume: 112
Issue: 12
Pages: 1809-1820
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci20039
PMC: PMC297002
OpenAlex: W2115886998
Cited by: 2,311
References: 71
Citations by year: 2026: 46 · 2025: 55 · 2024: 75 · 2023: 85 · 2022: 110 · 2021: 142 · 2020: 122 · 2019: 125 · 2018: 123 · 2017: 122 · 2016: 125 · 2015: 144 · 2014: 154 · 2013: 179 · 2012: 130
FWCI: 21.62
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
Funders: National Institutes of Health (5r01ai044157-03, CA16303)
National Cancer Institute (R01 CA84254, R01CA016303, R01 CA16303, R01CA084254)
National Institute of Allergy and Infectious Diseases (R01 AI44157)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Keywords: Beclin-1, autophagy, tumor suppression, haploinsufficiency, hepatitis B virus, precancerous lesions, cell proliferation, monoallelic deletion, carcinogenesis
MeSH terms: Beclin-1, Alleles, Animals, Autophagy, Cell Division, Cell Transformation, Neoplastic, Female, Genotype, Hepatitis B virus, Heterozygote, Male, Membrane Proteins, Mice, Inbred C57BL, Mice, Mutant Strains, Mice, Transgenic, Microscopy, Fluorescence, Models, Genetic, Mutation, Neoplasms, Proteins, Recombination, Genetic, Thymus Gland, Time Factors, Blotting, Southern, DNA Primers, Mice, Knockout, Cell Line, Tumor, Apoptosis Regulatory Proteins, Mice

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Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene

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