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

The DOI matches its Crossref record; 71 of the 71 references it cites were found in a registry or an index.

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

Open access

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

Open this paper in CoChat — free account Open PDF

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1172/jci20039

Cites

71 of 71 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Mutation and cancer: statistical study of retinoblastoma
Knudson, A. G. (1971) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.68.4.820 · Cited by 7,612
LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., & Yoshimori, T. (2000) · The EMBO Journal · doi:10.1093/emboj/19.21.5720 · Cited by 6,605
Self-citation
Induction of the Vitamin D Receptor Attenuates Autophagy Dysfunction-Mediated Cell Death Following Traumatic Brain Injury
Cui, C., Cui, J., Jin, F., Cui, Y., Li, R., Jiang, X., Tian, Y., Wang, R. C., Jiang, P., & Gao, J. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479571 · Cited by 5,214
Autophagy as a Regulated Pathway of Cellular Degradation
Klionsky, D. J., & Emr, S. D. (2000) · Science · doi:10.1126/science.290.5497.1717 · Cited by 3,630
Induction of autophagy and inhibition of tumorigenesis by beclin 1
Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., & Levine, B. (1999) · Nature · doi:10.1038/45257 · Cited by 3,347
Self-citation
Stereological Principles for Morphometry in Electron Microscopic Cytology
Weibel, E. R. (1969) · International review of cytology · doi:10.1016/s0074-7696(08)61637-x · Cited by 1,932
Isolation and characterization of autophagy‐defective mutants of Saccharomyces cerevisiae
Tsukada, M., & Ohsumi, Y. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80398-e · Cited by 1,837
Self-citation
Tor, a Phosphatidylinositol Kinase Homologue, Controls Autophagy in Yeast
Noda, T., & Ohsumi, Y. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.7.3963 · Cited by 1,303
Self-citation
Autophagy Genes Are Essential for Dauer Development and Life-Span Extension in C. elegans
Meléndez, A., Tallóczy, Z., Seaman, M., Eskelinen, E.-L., Hall, D. H., & Levine, B. (2003) · Science · doi:10.1126/science.1087782 · Cited by 1,270
Self-citation
Distinct Classes of Phosphatidylinositol 3′-Kinases Are Involved in Signaling Pathways That Control Macroautophagy in HT-29 Cells
Petiot, A., Ogier‐Denis, É., Blommaart, E. F. C., Meijer, A. J., & Codogno, P. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.2.992 · Cited by 1,168

Show all 71 references

Research works printed but not linked: 11

Russell, 1990, Oncogene., 5, 1581
Eccles, 1992, Oncogene., 7, 2069
Cliby, 1993, Cancer Res., 53, 2393
Tangir, 1996, Oncogene., 12, 735
Futreal, 1992, Cancer Res., 52, 2624
Saito, 1993, Cancer Res., 53, 3382
Gao, 1995, Cancer Res., 55, 1002
Liang, 2001, Cancer Res., 61, 3443
Huang, 2002, Curr. Opin. Investig. Drugs., 3, 295
Elit, 2002, Curr. Opin. Investig. Drugs., 3, 1249
Ogier-Denis, 2003, Biochim. Biophys. Acta., 1603, 113

Sorted by citations

Items 801–900 of 1,003

Suppression of lung metastases by the CD26/DPP4 inhibitor Vildagliptin in mice
Jang, J., Baerts, L., Waumans, Y., Meester, I. D., Yamada, Y., Limani, P., Bazo, I. G., Weder, W., & Jungraithmayr, W. (2015) · Clinical & Experimental Metastasis · doi:10.1007/s10585-015-9736-z · Cited by 70
Autophagy inhibition contributes to radiation sensitization of esophageal squamous carcinoma cells
Chen, Y. S., Song, H., Lü, Y., Li, X., Chen, T., Zhang, Y., Xue, J. X., Liu, H., Kan, B., Yang, G., et al. (2010) · Diseases of the Esophagus · doi:10.1111/j.1442-2050.2010.01156.x · Cited by 70
Elevated p62/SQSTM1 determines the fate of autophagy-deficient neural stem cells by increasing superoxide
Wang, C., Chen, S., Yeo, S., Karsli-Uzunbas, G., White, E., Mizushima, N., Virgin, H. W., & Guan, J.-L. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201507023 · Cited by 69
Self-citation
The Role of Autophagy in Liver Cancer: Crosstalk in Signaling Pathways and Potential Therapeutic Targets
Cui, J., Shen, H., & Lim, L. H. K. (2020) · Pharmaceuticals · doi:10.3390/ph13120432 · Cited by 72
Isoginkgetin, a potential CDK6 inhibitor, suppresses SLC2A1/GLUT1 enhancer activity to induce AMPK-ULK1-mediated cytotoxic autophagy in hepatocellular carcinoma
Yao, J., Tang, S., Shi, C., Lin, Y., Ge, L., Chen, Q., Ou, B., Liu, D., Miao, Y., Xie, Q., et al. (2022) · Autophagy · doi:10.1080/15548627.2022.2119353 · Cited by 69
Transcription Factor EB Is Selectively Reduced in the Nuclear Fractions of Alzheimer’s and Amyotrophic Lateral Sclerosis Brains
Wang, H., Wang, R., Xu, S., & Lakshmana, M. K. (2016) · Neuroscience Journal · doi:10.1155/2016/4732837 · Cited by 69
Autophagy- An emerging target for melanoma therapy
Ndoye, A., & Weeraratna, A. T. (2016) · F1000Research · doi:10.12688/f1000research.8347.1 · Cited by 73
The role of HBV-induced autophagy in HBV replication and HBV related-HCC
Xie, M., Yang, Z., Liu, Y., & Zheng, M. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.04.051 · Cited by 69
Molecular Mechanisms of Autophagy in Cancer Development, Progression, and Therapy
Vitto, V. A. M., Bianchin, S., Zolondick, A. A., Pellielo, G., Rimessi, A., Chianese, D., Yang, H., Carbone, M., Pinton, P., Giorgi, C., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10071596 · Cited by 73
Interplay of CD36, autophagy, and lipid metabolism: insights into cancer progression
Yang, Y., Liu, X., Yang, D., Li, L., Li, S., Lu, S., & Li, N. (2024) · Metabolism · doi:10.1016/j.metabol.2024.155905 · Cited by 68
Autophagy Shapes Inflammation
Fésüs, L., Demény, M. Á., & Petrovski, G. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3485 · Cited by 69
Cardiomyocyte autophagy and cancer chemotherapy
Li, D. ‘., & Hill, J. A. (2013) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.11.007 · Cited by 69
Genes for Plant Autophagy: Functions and Interactions
Kim, S.-H., Kwon, C., Lee, J., & Chung, T. (2012) · Molecules and Cells · doi:10.1007/s10059-012-0098-y · Cited by 72
Genetics and Biology of Pancreatic Ductal Adenocarcinoma
Dunne, R. F., & Hezel, A. F. (2015) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2015.04.003 · Cited by 68
Signaling and other functions of lipids in autophagy: a review
Soto-Avellaneda, A., & Morrison, B. E. (2020) · Lipids in Health and Disease · doi:10.1186/s12944-020-01389-2 · Cited by 71
Regulation of Autophagy by Glycolysis in Cancer
Chu, Y., Chang, Y., Lü, W., Sheng, X., Wang, S., Xu, H., & Ma, J. (2020) · Cancer Management and Research · doi:10.2147/cmar.s279672 · Cited by 68
Quinacrine promotes autophagic cell death and chemosensitivity in ovarian cancer and attenuates tumor growth
Khurana, A., Roy, D., Kalogera, E., Mondal, S., Wen, X., He, X., Dowdy, S. C., & Shridhar, V. (2015) · Oncotarget · doi:10.18632/oncotarget.5632 · Cited by 67
Autophagy Pathway Is Required for IL-6 Induced Neuroendocrine Differentiation and Chemoresistance of Prostate Cancer LNCaP Cells
Chang, P., Wang, T., Chang, Y.-T., Chu, C.-Y., Lee, C.-L., Hsu, H.-W., Zhou, T.-A., Wu, Z., Kim, R. H., Desai, S. J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088556 · Cited by 67
ABHD5 interacts with BECN1 to regulate autophagy and tumorigenesis of colon cancer independent of PNPLA2
Peng, Y., Miao, H., Wu, S., Yang, W., Zhang, Y., Xie, G., Xie, X., Li, J., Shi, C., Ye, L., et al. (2016) · Autophagy · doi:10.1080/15548627.2016.1217380 · Cited by 67
The Emerging Roles of Autophagy in Human Diseases
Lei, Y., & Klionsky, D. J. (2021) · Biomedicines · doi:10.3390/biomedicines9111651 · Cited by 68
The mTOR–lysosome axis at the centre of ageing
Carosi, J. M., Fourrier, C., Bensalem, J., & Sargeant, T. J. (2021) · FEBS Open Bio · doi:10.1002/2211-5463.13347 · Cited by 70
Chemotherapy Resistance: Role of Mitochondrial and Autophagic Components
Bahar, E., Han, S., Kim, J., & Yoon, H. (2022) · Cancers · doi:10.3390/cancers14061462 · Cited by 67
Autophagic Degradation of Mitochondria in White Adipose Tissue Differentiation
Goldman, S. J., Zhang, Y., & Jin, S. V. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3777 · Cited by 68
Autophagy: a targetable linchpin of cancer cell metabolism
Leone, R. D., & Amaravadi, R. K. (2013) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2013.01.008 · Cited by 68
Autophagy in Dementias
Kragh, C. L., Ubhi, K. K., Wyss‐Coray, T., & Masliah, E. (2011) · Brain Pathology · doi:10.1111/j.1750-3639.2011.00545.x · Cited by 66
Histone deacetylase inhibitor potentiated the ability of MTOR inhibitor to induce autophagic cell death in Burkitt leukemia/lymphoma
Dong, L., Cheng, S., Zheng, Z., Wang, L., Shen, Y., Shen, Z. X., Chen, S., & Zhao, W. L. (2013) · Journal of Hematology & Oncology · doi:10.1186/1756-8722-6-53 · Cited by 66
Autophagy in blood cancers: biological role and therapeutic implications
Nencioni, A., Cea, M., Montecucco, F., Longo, V. D., Patrone, F., Carella, A. M., Holyoake, T. L., & Helgason, G. V. (2013) · Haematologica · doi:10.3324/haematol.2012.079061 · Cited by 67
BRAF associated autophagy exploitation: BRAF and autophagy inhibitors synergise to efficiently overcome resistance of BRAF mutant colorectal cancer cells
Goulielmaki, M., Koustas, E., Moysidou, E., Vlassi, M., Sasazuki, T., Shirasawa, S., Zografos, G., Oikonomou, E., & Pintzas, A. (2016) · Oncotarget · doi:10.18632/oncotarget.6942 · Cited by 67
mTORC1-independent autophagy regulates receptor tyrosine kinase phosphorylation in colorectal cancer cells via an mTORC2-mediated mechanism
Lampada, A., O’Prey, J., Szabadkai, G., Ryan, K. M., Hochhauser, D., & Salomoni, P. (2017) · Cell Death and Differentiation · doi:10.1038/cdd.2017.41 · Cited by 66
Pro-survival autophagy: An emerging candidate of tumor progression through maintaining hallmarks of cancer
Das, C. K., Banerjee, I., & Mandal, M. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.08.020 · Cited by 70
Regulation and repurposing of nutrient sensing and autophagy in innate immunity
Sanchez‐Garrido, J., & Shenoy, A. R. (2020) · Autophagy · doi:10.1080/15548627.2020.1783119 · Cited by 67
The Emerging Roles of Autophagy-Related MicroRNAs in Cancer
Shan, C., Chen, X., Cai, H., Hao, X., Li, J., Zhang, Y., Gao, J., Zhou, Z., Li, X., Liu, C., et al. (2020) · International Journal of Biological Sciences · doi:10.7150/ijbs.50773 · Cited by 66
Impaired autophagy and delayed autophagic clearance of transforming growth factor β-induced protein (TGFBI) in granular corneal dystrophy type 2
Choi, S., Kim, B.-Y., Dadakhujaev, S., Oh, J.-Y., Kim, T., Kim, J. Y., & Kim, E. K. (2012) · Autophagy · doi:10.4161/auto.22067 · Cited by 65
Decreased Expression of Beclin 1 Correlates Closely with Bcl-xL Expression and Poor Prognosis of Ovarian Carcinoma
Lin, H., Qiu, H., Zeng, F., Rao, H., Yang, G.-F., Kung, H., Zhu, X., Zeng, Y.-X., Cai, M.-Y., & Xie, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060516 · Cited by 67
Autophagy inhibition suppresses the tumorigenic potential of cancer stem cell enriched side population in bladder cancer
Ojha, R., Jha, V., Singh, S. K., & Bhattacharyya, S. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.07.007 · Cited by 68
Autophagy as a Possible Underlying Mechanism of Nanomaterial Toxicity
Cohignac, V., Landry, M., Boczkowski, J., & Lanone, S. (2014) · Nanomaterials · doi:10.3390/nano4030548 · Cited by 70
DHA-induced stress response in human colon cancer cells – Focus on oxidative stress and autophagy
Pettersen, K., Monsen, V. T., Pettersen, C. H. H., Overland, H. B., Pettersen, G. K., Samdal, H., Tesfahun, A. N., Lundemo, A. G., Bjørkøy, G., & Schønberg, S. A. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.11.018 · Cited by 68
Polypyrimidine tract-binding protein 1-mediated down-regulation of ATG10 facilitates metastasis of colorectal cancer cells
Jo, Y. K., Roh, S. A., Lee, H., Park, N. Y., Choi, E. S., Oh, J., Park, S. J., Shin, J. H., Suh, Y., Lee, E. K., et al. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.11.002 · Cited by 66
Immunolocalization of beclin 1, a bcl-2-binding, autophagy-related protein, in the human ovary: possible relation to life span of corpus luteum
Gaytán, M., Morales, C., Sánchez‐Criado, J. E., & Gaytán, F. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0531-2 · Cited by 65
Selective Types of Autophagy
Reggiori, F., Komatsu, M., Finley, K. D., & Simonsen, A. (2012) · International Journal of Cell Biology · doi:10.1155/2012/156272 · Cited by 68
Detection of WIPI1 mRNA as an indicator of autophagosome formation
Tsuyuki, S., Takabayashi, M., Kawazu, M., Kudo, K., Watanabe, A., Nagata, Y., Kusama, Y., & Yoshida, K. (2014) · Autophagy · doi:10.4161/auto.27419 · Cited by 65
Comprehensive autophagy evaluation in cardiac disease models
Kaludercic, N., Maiuri, M. C., Kaushik, S., Fernández, Á. F., de Bruijn, J., Castoldi, F., Chen, Y., Ito, J., Mukai, R., Murakawa, T., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvz233 · Cited by 64
Telomeres and Cancer: Resolving the Paradox
Nassour, J., Schmidt, T. T., & Karlseder, J. (2021) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-050420-023410 · Cited by 70
Cross talk between autophagy and oncogenic signaling pathways and implications for cancer therapy
Zada, S., Hwang, J. S., Ahmed, M., Lai, T. H., Pham, T. M., Elashkar, O., & Kim, D. R. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188565 · Cited by 65
Ammonia: A Diffusible Factor Released by Proliferating Cells That Induces Autophagy
Mariño, G., & Kroemer, G. (2010) · Science Signaling · doi:10.1126/scisignal.3124pe19 · Cited by 66
The miR-290-295 cluster suppresses autophagic cell death of melanoma cells
Chen, Y., Liersch, R., & Detmar, M. J. (2012) · Scientific Reports · doi:10.1038/srep00808 · Cited by 65
Beclin 1, an autophagy-related gene, augments apoptosis in U87 glioblastoma cells
HUANG, X., QI, Q., Hua, X., Li, X., Zhang, W., Sun, H. Y., Li, S., Wang, X., & Li, B. (2014) · Oncology Reports · doi:10.3892/or.2014.3015 · Cited by 64
Pharmacological Modulation of Autophagy During Cardiac Stress
Sciarretta, S., Zhai, P., Volpe, M., & Sadoshima, J. (2012) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0b013e3182575f61 · Cited by 65
New Potential Pharmacological Functions of Chinese Herbal Medicines via Regulation of Autophagy
Law, B. Y. K., Mok, S. W. F., Wu, A., Lam, C. W. K., Yu, M., & Wong, V. K. W. (2016) · Molecules · doi:10.3390/molecules21030359 · Cited by 65
Autophagy: A Potential Therapeutic Target for Reversing Sepsis-Induced Immunosuppression
Ren, C., Zhang, H., Wu, T., & Yao, Y.-M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01832 · Cited by 64
S100A4 promotes lung tumor development through β-catenin pathway-mediated autophagy inhibition
Hou, S., Tian, T., Qi, D., Sun, K., Yuan, Q., Wang, Z., Qin, Z., Wu, Z., Chen, Z., & Zhang, J. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0319-1 · Cited by 67
Knockdown ATG4C inhibits gliomas progression and promotes temozolomide chemosensitivity by suppressing autophagic flux
Wen, Z., Zeng, W., Chen, Y., He, L., Wang, J., Cheng, Q., Yu, J., Zhou, H., Liu, Z.-Z., Xiao, J., et al. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-019-1287-8 · Cited by 64
Self-citation
Adaptive response of resistant cancer cells to chemotherapy
Chern, Y., & Tai, I. T. (2020) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0005 · Cited by 67
Anticancer Properties of PPARα‐Effects on Cellular Metabolism and Inflammation
Grabacka, M., & Reiss, K. (2008) · PPAR Research · doi:10.1155/2008/930705 · Cited by 66
Therapeutic targeting of the USP2-E2F4 axis inhibits autophagic machinery essential for zinc homeostasis in cancer progression
Xiao, W., Wang, J., Wang, X., Cai, S., Guo, Y., Ye, L., Li, D., Hu, A., Jin, S., Yuan, B., et al. (2022) · Autophagy · doi:10.1080/15548627.2022.2044651 · Cited by 66
Chapter 16 Novel Methods for Measuring Cardiac Autophagy In Vivo
Perry, C. N., Kyoi, S., Hariharan, N., Takagi, H., Sadoshima, J., & Gottlieb, R. A. (2009) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(08)04016-0 · Cited by 64
Analysis of a lung defect in autophagy-deficient mouse strains
Cheong, H., Wu, J., Gonzales, L. K., Guttentag, S. H., Thompson, C. B., & Lindsten, T. (2013) · Autophagy · doi:10.4161/auto.26505 · Cited by 64
Non-enzymatic post-translational protein modifications and proteostasis network deregulation in carcinogenesis
Trougakos, I. P., Sesti, F., Tsakiri, E. N., & Gorgoulis, V. G. (2013) · Journal of Proteomics · doi:10.1016/j.jprot.2013.02.024 · Cited by 63
Analysis of DRAM-related proteins reveals evolutionarily conserved and divergent roles in the control of autophagy
O’Prey, J., Skommer, J., Wilkinson, S., & Ryan, K. M. (2009) · Cell Cycle · doi:10.4161/cc.8.14.9050 · Cited by 63
Cryptotanshinone induces G1 cell cycle arrest and autophagic cell death by activating the AMP-activated protein kinase signal pathway in HepG2 hepatoma
Park, I.-J., Yang, W. K., Nam, S., Hong, J., Yang, K. R., Kim, J., Kim, S. S., Choe, W., Kang, I., & Ha, J. (2013) · APOPTOSIS · doi:10.1007/s10495-013-0929-0 · Cited by 65
The involvement of cell death and survival in neural tube defects: a distinct role for apoptosis and autophagy?
Cecconi, F., Piacentini, M., & Fimia, G. M. (2008) · Cell Death and Differentiation · doi:10.1038/cdd.2008.64 · Cited by 63
Autophagy Enhanced by Microtubule- and Mitochondrion-Associated MAP1S Suppresses Genome Instability and Hepatocarcinogenesis
Xie, R., Wang, F., McKeehan, W. L., & Liu, L. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-2170 · Cited by 66
Gene of the month: BECN1
Sahni, S., Merlot, A. M., Krishan, S., Jansson, P. J., & Richardson, D. R. (2014) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2014-202356 · Cited by 65
Therapeutic Implications of Autophagy Inducers in Immunological Disorders, Infection, and Cancer
Byun, S., Lee, E., & Lee, K. W. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18091959 · Cited by 64
Intensified Beclin-1 Mediated by Low Expression of Mir-30a-5p Promotes Chemoresistance in Human Small Cell Lung Cancer
Yang, X., Bai, F., Xu, Y., Chen, Y., & Chen, L. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000481754 · Cited by 63
Programmed cell death in cardiac myocytes: strategies to maximize post-ischemic salvage
Mani, K. M. (2008) · Heart Failure Reviews · doi:10.1007/s10741-007-9073-7 · Cited by 64
Stat3 inhibits Beclin 1 expression through recruitment of HDAC3 in nonsmall cell lung cancer cells
Miao, L.-J., Huang, F.-X., Sun, Z.-T., Zhang, R.-X., Huang, S.-F., & Wang, J. (2014) · Tumor Biology · doi:10.1007/s13277-014-1961-6 · Cited by 62
Autophagy Function and Dysfunction: Potential Drugs as Anti-Cancer Therapy
Cuomo, F., Altucci, L., & Cobellis, G. (2019) · Cancers · doi:10.3390/cancers11101465 · Cited by 64
Punicalagin in Cancer Prevention—Via Signaling Pathways Targeting
Berdowska, I., Matusiewicz, M., & Fecka, I. (2021) · Nutrients · doi:10.3390/nu13082733 · Cited by 62
Novel Insights into Autophagy and Prostate Cancer: A Comprehensive Review
Loizzo, D., Pandolfo, S. D., Rogers, D. E., Cerrato, C., di Meo, N. A., Riccardo Autorino, B., Mirone, V. G., Ferro, M., Porta, C., Stella, A., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073826 · Cited by 62
Autophagy is required for G 1 /G 0 quiescence in response to nitrogen starvation in Saccharomyces cerevisiae
An, Z., Tassa, A., Thomas, C., Zhong, R. M., Xiao, G., Fotedar, R., Tu, B. P., Klionsky, D. J., & Levine, B. (2014) · Autophagy · doi:10.4161/auto.32122 · Cited by 62
Self-citation
Beta-asarone attenuates ischemia–reperfusion-induced autophagy in rat brains via modulating JNK, p-JNK, Bcl-2 and Beclin 1
Liu, L., Fang, Y., Xue, Z., He, Y., Fang, R., & Li, L. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.01.016 · Cited by 62
Impact of cellular autophagy on viruses: Insights from hepatitis B virus and human retroviruses
Tang, S.-W., Ducroux, A., Jeang, K., & Neuveut, C. (2012) · Journal of Biomedical Science · doi:10.1186/1423-0127-19-92 · Cited by 63
γ-Tocotrienol-induced autophagy in malignant mammary cancer cells
Tiwari, R. V., Parajuli, P., & Sylvester, P. W. (2013) · Experimental Biology and Medicine · doi:10.1177/1535370213511022 · Cited by 62
Beclin 1-Vps34 complex architecture: Understanding the nuts and bolts of therapeutic targets
Morris, D. H., Yip, C. K., Shi, Y., Chait, B. T., & Wang, Q. J. (2015) · Frontiers in Biology · doi:10.1007/s11515-015-1374-y · Cited by 66
How Autophagy Shapes the Tumor Microenvironment in Ovarian Cancer
Ferraresi, A., Girone, C., Esposito, A., Vidoni, C., Vallino, L., Secomandi, E., Dhanasekaran, D. N., & Isidoro, C. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.599915 · Cited by 62
The role of apoptosis in cancer cell survival and therapeutic outcome
Kim, R., Emi, M., & Tanabe, K. (2006) · Cancer Biology & Therapy · doi:10.4161/cbt.5.11.3456 · Cited by 62
Autophagy in cancer: a complex relationship
Wilde, L. R., Tanson, K., Curry, J., & Martinez‐Outschoorn, U. (2018) · Biochemical Journal · doi:10.1042/bcj20170847 · Cited by 62
MnSOD Upregulation Induces Autophagic Programmed Cell Death in Senescent Keratinocytes
Deruy, E., Gosselin, K., Vercamer, C., Martien, S., Bouali, F., Slomianny, C., Bertout, J., Bernard, D., Pourtier, A., & Abbadie, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012712 · Cited by 67
Autophagy function and its relationship to pathology, clinical applications, drug metabolism and toxicity
Petibone, D. M., Majeed, W., & Casciano, D. A. (2016) · Journal of Applied Toxicology · doi:10.1002/jat.3393 · Cited by 63
Beclin-1 and hypoxia-inducible factor-1α genes expression: Potential biomarkers in acute leukemia patients
Radwan, S. M., Hamdy, N. Μ., Hegab, H. M. A.-A., & EL-Mesallamy, H. O. (2016) · Cancer Biomarkers · doi:10.3233/cbm-160603 · Cited by 60
Activation Mechanisms of the VPS34 Complexes
Ohashi, Y. (2021) · Cells · doi:10.3390/cells10113124 · Cited by 62
Is Autophagy Always a Barrier to Cisplatin Therapy?
Xu, J., & Gewirtz, D. A. (2022) · Biomolecules · doi:10.3390/biom12030463 · Cited by 60
The Interaction Between Autophagy and JAK/STAT3 Signaling Pathway in Tumors
Xu, J., Zhang, J., Mao, Q., Wu, J., & Wang, Y. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.880359 · Cited by 62
Autophagy, a major adaptation pathway shaping cancer cell death and anticancer immunity responses following photodynamic therapy
Garg, A. D., Maes, H., Romano, E., & Agostinis, P. (2015) · Photochemical & Photobiological Sciences · doi:10.1039/c4pp00466c · Cited by 61
Autophagy is involved in anticancer effects of matrine on SGC-7901 human gastric cancer cells
Li, Y. (2011) · Oncology Reports · doi:10.3892/or.2011.1277 · Cited by 60
Downregulation of autophagy by Bcl-2 promotes MCF7 breast cancer cell growth independent of its inhibition of apoptosis
Oh, S., Xiaofei, E., Ni, D., Pirooz, S. D., Lee, J.-Y., Lee, D., Zhao, Z., Lee, S., Lee, H. M., Ku, B., et al. (2010) · Cell Death and Differentiation · doi:10.1038/cdd.2010.116 · Cited by 60
New insights into autophagy in hepatocellular carcinoma: mechanisms and therapeutic strategies.
Yang, S., Yang, L., Li, X., Li, B., Li, Y., Zhang, X., Ma, Y., Peng, X., Jin, H., & Li, H. (2019) · PubMed Central · Cited by 60
Cancer-Associated Fibroblast-Derived IL-6 Determines Unfavorable Prognosis in Cholangiocarcinoma by Affecting Autophagy-Associated Chemoresponse
Thongchot, S., Vidoni, C., Ferraresi, A., Loilome, W., Khuntikeo, N., Sa-Ngiamwibool, P., Titapun, A., Isidoro, C., & Namwat, N. (2021) · Cancers · doi:10.3390/cancers13092134 · Cited by 59
Liver autophagy: physiology and pathology
Komatsu, M. (2012) · The Journal of Biochemistry · doi:10.1093/jb/mvs059 · Cited by 61
Beclin 1 Biology and its Role in Heart Disease
Zhu, H., & He, L. (2015) · Current Cardiology Reviews · doi:10.2174/1573403x10666141106104606 · Cited by 61
Effectors of mTOR-autophagy pathway: targeting cancer, affecting the skeleton
Chagin, A. S. (2016) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2016.02.004 · Cited by 59
Mechanisms of autophagy and relevant small-molecule compounds for targeted cancer therapy
Zhang, J. C., Wang, G., Zhou, Y., Chen, Y., Ouyang, L., & Liu, B. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2759-2 · Cited by 59
RAS-related GTPases DIRAS1 and DIRAS2 induce autophagic cancer cell death and are required for autophagy in murine ovarian cancer cells
Sutton, M. N., Yang, H., Huang, G. Y., Fu, C., Pontikos, M. A., Wang, Y., Mao, W., Pang, L., Yang, M., Liu, J., et al. (2018) · Autophagy · doi:10.1080/15548627.2018.1427022 · Cited by 59
17β-Estradiol on the Expression of G-Protein Coupled Estrogen Receptor (GPER/GPR30) Mitophagy, and the PI3K/Akt Signaling Pathway in ATDC5 Chondrocytes In Vitro
Fan, D., Yang, X., Li, Y., & Guo, L. (2018) · Medical Science Monitor · doi:10.12659/msm.909365 · Cited by 59
Ginsenoside metabolite compound K induces apoptosis and autophagy in non-small cell lung cancer cells via AMPK–mTOR and JNK pathways
Li, C., Dong, Y., Wang, L., Xu, G., Yang, Q., Tang, X., Qiao, Y., & Cong, Z. (2018) · Biochemistry and Cell Biology · doi:10.1139/bcb-2018-0226 · Cited by 59
Targeting Autophagy to Treat Cancer: Challenges and Opportunities
Lim, J., & Murthy, A. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.590344 · Cited by 61
Inhibition of autophagy enhances the effects of the AKT inhibitor MK‐2206 when combined with paclitaxel and carboplatin in BRAF wild‐type melanoma
Rebecca, V. W., Massaro, R. R., Fedorenko, I. V., Sondak, V. K., Anderson, A. R. A., Kim, E., Amaravadi, R. K., Maria‐Engler, S. S., Messina, J. L., Gibney, G. T., et al. (2014) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.12227 · Cited by 58
“Following the inhibition of mTORC1, the cytoplasmic autophagy machinery is recruited onto phospholipid membranes derived from the endoplasmic reticulum (ER) and the golgi apparatus leading to the formation of autophagosomes, which then mature with the aid of ATG5 and LC3 (Rabinowitz and White, 2010).”
BackgroundInfluential
Danger matrix molecules orchestrate CD14/CD44 signaling in cancer development
Roedig, H., Damiescu, R., Zeng-Brouwers, J., Kutija, I., Trebicka, J., Wygrecka, M., & Schaefer, L. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.07.026 · Cited by 58
Targeting mTOR for Anti-Aging and Anti-Cancer Therapy
Fu, W., & Wu, G. (2023) · Molecules · doi:10.3390/molecules28073157 · Cited by 62

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks