Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy
Open accessAbstract
Autophagy plays an important role in cellular quality control and is responsible for removing protein aggregates and dysfunctional organelles. Bnip3 is an atypical BH3-only protein that is known to cause mitochondrial dysfunction and cell death. Interestingly, Bnip3 can also protect against cell death by inducing mitochondrial autophagy. The mechanism for this process, however, remains poorly understood. Bnip3 contains a C-terminal transmembrane domain that is essential for homodimerization and proapoptotic function. In this study, we show that homodimerization of Bnip3 is also a requirement for induction of autophagy. Several Bnip3 mutants that do not interfere with its mitochondrial localization but disrupt homodimerization failed to induce autophagy in cells. In addition, we discovered that endogenous Bnip3 is localized to both mitochondria and the endoplasmic reticulum (ER). To investigate the effects of Bnip3 at mitochondria or the ER on autophagy, Bnip3 was targeted specifically to each organelle by substituting the Bnip3 transmembrane domain with that of Acta or cytochrome b(5). We found that Bnip3 enhanced autophagy in cells from both sites. We also discovered that Bnip3 induced removal of both ER (ERphagy) and mitochondria (mitophagy) via autophagy. The clearance of these organelles was mediated in part via binding of Bnip3 to LC3 on the autophagosome. Although ablation of the Bnip3-LC3 interaction by mutating the LC3 binding site did not impair the prodeath activity of Bnip3, it significantly reduced both mitophagy and ERphagy. Our data indicate that Bnip3 regulates the apoptotic balance as an autophagy receptor that induces removal of both mitochondria and ER.
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Mitophagy can also occur through Parkin-independent pathways.
“Mitophagy can also occur through Parkin-independent pathways.”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [138]
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1 retracted
Mitochondrial Autophagy Is an HIF-1-dependent Adaptive Metabolic Response to Hypoxia
Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., & Semenza, G. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800102200 · Cited by 1,601 · see citing works
RetractedPankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J.-A., Outzen, H., Øvervatn, A., Bjørkøy, G., & Johansen, T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702824200 · Cited by 4,578 · see citing works
Levine, B., & Klionsky, D. J. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00099-1 · Cited by 3,671 · see citing works
The Beclin 1 network regulates autophagy and apoptosis
Kang, R., Zeh, H. J., Lotze, M. T., & Tang, D. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.191 · Cited by 2,485 · see citing works
Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.
Komatsu, M., Waguri, S., Koike, M., Sou, Y.-S., Ueno, T., Hara, T., Mizushima, N., Iwata, J.-I., Ezaki, J., Murata, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.035 · Cited by 2,124 · see citing works
Selective degradation of mitochondria by mitophagy
Kim, I., Rodriguez-Enriquez, S., & Lemasters, J. J. (2007) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2007.03.034 · Cited by 1,558 · see citing works
The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress
Nakai, A., Yamaguchi, O., Takeda, T., Higuchi, Y., Hikoso, S., Taniike, M., Omiya, S., Mizote, I., Matsumura, Y., Asahi, M., et al. (2007) · Nature Medicine · doi:10.1038/nm1574 · Cited by 1,520 · see citing works
Bellot, G., Garcia-Medina, R., Gounon, P., Chiche, J., Roux, D., Pouysségur, J., & Mazure, N. M. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00166-09 · Cited by 1,501 · see citing works
LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation
Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y., & Yoshimori, T. (2004) · Journal of Cell Science · doi:10.1242/jcs.01131 · Cited by 1,394 · see citing works
BAX and BAK Regulation of Endoplasmic Reticulum Ca 2+ : A Control Point for Apoptosis
Scorrano, L., Oakes, S. A., Opferman, J. T., Cheng, E. H. Y., Sorcinelli, M. D., Pozzan, T., & Korsmeyer, S. J. (2003) · Science · doi:10.1126/science.1081208 · Cited by 1,387 · see citing works
Yoshimori, T., Yamamoto, A., Moriyama, Y., Futai, M., & Tashiro, Y. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)47429-2 · Cited by 1,334 · see citing works
Nix is a selective autophagy receptor for mitochondrial clearance
Novak, I., Kirkin, V., McEwan, D. G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Löhr, F., Popovic, D., Occhipinti, A., et al. (2010) · The EMBO Reports · doi:10.1038/embor.2009.256 · Cited by 1,309 · see citing works
A Role for NBR1 in Autophagosomal Degradation of Ubiquitinated Substrates
Kirkin, V., Lamark, T., Sou, Y., Bjørkøy, G., Nunn, J. A. L., Bruun, J., Shvets, E., McEwan, D. G., Clausen, T. H., Wild, P. S., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.01.020 · Cited by 1,158 · see citing works
NIX is required for programmed mitochondrial clearance during reticulocyte maturation
Schweers, R. L., Zhang, J., Randall, M. S., Loyd, M. R., Li, W., Dorsey, F. C., Kundu, M., Opferman, J. T., Cleveland, J. L., Miller, J. L., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708818104 · Cited by 939 · see citing works
Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice
Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E.-L., Hartmann, D., Lüllmann-Rauch, R., Janssen, P. M. L., Blanz, J., von Figura, K., & Saftig, P. (2000) · Nature · doi:10.1038/35022595 · Cited by 925 · see citing works
Velde, C. V., Cizeau, J., Dubik, D., Alimonti, J. B., Brown, T., Israels, S. J., Hakem, R., & Greenberg, A. H. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.15.5454-5468.2000 · Cited by 619 · see citing works
Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy
Hamacher-Brady, A., Brady, N. R., Logue, S. E., Sayen, M. R., Jinno, M., Kirshenbaum, L. A., Gottlieb, R. A., & Gustafsson, Å. B. (2007) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4401936 · Cited by 609 · see citing works
Self-citationBcl-2 decreases the free Ca 2+ concentration within the endoplasmic reticulum
Foyouzi-Youssefi, R., Arnaudeau, S., Borner, C., Kelley, W. L., Tschopp, J., Lew, D. P., Demaurex, N., & Krause, K. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.11.5723 · Cited by 432 · see citing works
Kanzawa, T., Zhang, L., Xiao, L., Germano, I. M., Kondo, Y., & Kondo, S. (2004) · Oncogene · doi:10.1038/sj.onc.1208095 · Cited by 407 · see citing works
Lee, Y., Lee, H.-Y., Hanna, R. A., & Gustafsson, Å. B. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00368.2011 · Cited by 398 · see citing works
Self-citationER-Phagy: Selective Autophagy of the Endoplasmic Reticulum
Bernales, S., Schuck, S., & Walter, P. (2007) · Autophagy · doi:10.4161/auto.3930 · Cited by 357 · see citing works
Azad, M. B., Chen, Y., Henson, E. S., Cizeau, J., McMillan‐Ward, E., Israels, S. J., & Gibson, S. B. (2008) · Autophagy · doi:10.4161/auto.5278 · Cited by 355 · see citing works
Ray, R., Chen, G., Velde, C. V., Cizeau, J., Park, J. H., Reed, J. C., Gietz, R. D., & Greenberg, A. H. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.2.1439 · Cited by 349 · see citing works
The E1B 19K/Bcl-2–binding Protein Nip3 is a Dimeric Mitochondrial Protein that Activates Apoptosis
Chen, G., Ray, R., Dubik, D., Shi, L. F., Cizeau, J., Bleackley, R. C., Saxena, S. P., Gietz, R. D., & Greenberg, A. H. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.12.1975 · Cited by 332 · see citing works
Regula, K. M., Ens, K., & Kirshenbaum, L. A. (2002) · Circulation Research · doi:10.1161/01.res.0000029232.42227.16 · Cited by 318 · see citing works
Regulation of autophagy by the inositol trisphosphate receptor
Criollo, A., Maiuri, M. C., Tasdemir, E., Vitale, I., Fiebig, A. A., Andrews, D. W., Molgó, J., Dı́az, J., Lavandero, S., Harper, F., et al. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402099 · Cited by 305 · see citing works
Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L)
Fan, W., Nassiri, A., & Zhong, Q. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016472108 · Cited by 285 · see citing works
Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover
Rikka, S., Quinsay, M. N., Thomas, R. L., Kubli, D. A., Zhang, X., Murphy, A. N., & Gustafsson, Å. B. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.146 · Cited by 277 · see citing works
Self-citationNix directly binds to GABARAP: A possible crosstalk between apoptosis and autophagy
Schwarten, M., Mohrluder, J., Ma, P., Stoldt, M., Thielmann, Y., Stangler, T., Hersch, N., Hoffmann, B., Merkel, R., & Willbold, D. (2009) · Autophagy · doi:10.4161/auto.5.5.8494 · Cited by 247 · see citing works
Quinsay, M. N., Thomas, R. L., Lee, Y., & Gustafsson, Å. B. (2010) · Autophagy · doi:10.4161/auto.6.7.13005 · Cited by 239 · see citing works
Self-citationSilencing of the Hypoxia-Inducible Cell Death Protein BNIP3 in Pancreatic Cancer
Okami, J., Simeone, D. M., & Logsdon, C. D. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0089 · Cited by 238 · see citing works
Erkan, M., Kleeff, J. H., Esposito, I., Giese, T., Ketterer, K., Büchler, M. W., Giese, N. A., & Frieß, H. (2005) · Oncogene · doi:10.1038/sj.onc.1208642 · Cited by 216 · see citing works
Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak
Kubli, D. A., Ycaza, J. E., & Gustafsson, Å. B. (2007) · Biochemical Journal · doi:10.1042/bj20070319 · Cited by 208 · see citing works
Self-citationKubli, D. A., Quinsay, M. N., Huang, C., Lee, Y., & Gustafsson, Å. B. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00552.2008 · Cited by 187 · see citing works
Self-citationAberrant Methylation and Silencing of theBNIP3Gene in Colorectal and Gastric Cancer
Murai, M., Toyota, M., Suzuki, H., Satoh, A., Sasaki, Y., Akino, K., Ueno, M., Takahashi, F., Kusano, M., Mita, H., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.1021.11.3 · Cited by 168 · see citing works
Starvation Triggers the Delivery of the Endoplasmic Reticulum to the Vacuole via Autophagy in Yeast
Hamasaki, M., Noda, T., Baba, M., & Ohsumi, Y. (2004) · Traffic · doi:10.1111/j.1600-0854.2004.00245.x · Cited by 167 · see citing works
Endoplasmic reticulum–mitochondria crosstalk in NIX-mediated murine cell death
Diwan, A., Matkovich, S. J., Yuan, Q., Zhao, W. H., Yatani, A., Brown, J. H., Molkentin, J. D., Kranias, E. G., & Dorn, G. W. (2008) · Journal of Clinical Investigation · doi:10.1172/jci36445 · Cited by 139 · see citing works
Enhancing lysosome biogenesis attenuates BNIP3-induced cardiomyocyte death
Ma, X., Godar, R. J., Liu, H., & Diwan, A. (2012) · Autophagy · doi:10.4161/auto.18658 · Cited by 138 · see citing works
Bocharov, E. V., Pustovalova, Y. E., Pavlov, K. V., Volynsky, P. E., Goncharuk, M. V., Ermolyuk, Y. S., Karpunin, D. V., Schulga, A. A., Kirpichnikov, M. P., Efremov, R. G., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701745200 · Cited by 128 · see citing works
Sulistijo, E. S., Jaszewski, T. M., & MacKenzie, K. R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308429200 · Cited by 100 · see citing works
Autophagy in organelle homeostasis: Peroxisome turnover
Monastyrska, I., & Klionsky, D. J. (2006) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2006.08.004 · Cited by 95 · see citing works
Gao, W., Kang, J. H., Liao, Y., Ding, W.-X., Gambotto, A. A., Watkins, S. C., Liu, Y.-J., Stolz, D. B., & Yin, X.-M. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.054197 · Cited by 94 · see citing works
BNIP3 Upregulation and EndoG Translocation in Delayed Neuronal Death in Stroke and in Hypoxia
Zhang, Z., Yang, X., Zhang, S., Ma, X., & Kong, J. (2007) · Stroke · doi:10.1161/strokeaha.106.475129 · Cited by 93 · see citing works
BNip3 and signal-specific programmed death in the heart
Webster, K. A., Graham, R. M., & Bishopric, N. H. (2004) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.11.007 · Cited by 92 · see citing works
Zhang, L., Li, L., Liu, H., Borowitz, J. L., & Isom, G. E. (2009) · The FASEB Journal · doi:10.1096/fj.08-124354 · Cited by 65 · see citing works
Jian, B., Yang, S., Chen, D., Zou, L., Chatham, J. C., Chaudry, I. H., & Raju, R. P. (2010) · Molecular Medicine · doi:10.2119/molmed.2010.00195 · Cited by 33 · see citing works
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Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Self-citationKlionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Mitophagy and Quality Control Mechanisms in Mitochondrial Maintenance
Pickles, S., Vigié, P., & Youle, R. J. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.004 · Cited by 2,081 · see citing works
Mechanisms regulating skeletal muscle growth and atrophy
Schiaffino, S., Dyar, K. A., Ciciliot, S., Blaauw, B., & Sandri, M. (2013) · The FEBS Journal · doi:10.1111/febs.12253 · Cited by 1,492 · see citing works
Cellular and molecular mechanisms of muscle atrophy
Bonaldo, P., & Sandri, M. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.010389 · Cited by 1,284 · see citing works
Chu, C. T., Ji, J., Dagda, R. K., Jiang, J. F., Tyurina, Y. Y., Kapralov, A. A., Tyurin, V. A., Yanamala, N., Shrivastava, I. H., Mohammadyani, D., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2837 · Cited by 1,083 · see citing works
Protein breakdown in muscle wasting: Role of autophagy-lysosome and ubiquitin-proteasome
Sandri, M. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.04.023 · Cited by 689 · see citing works
Kubli, D. A., Zhang, X., Lee, Y., Hanna, R. A., Quinsay, M. N., Nguyen, C. K., Jimenez, R., Petrosyan, S., Murphy, A. N., & Gustafsson, Å. B. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.411363 · Cited by 476 · see citing works
Self-citationMitochondrial quality control and muscle mass maintenance.
Romanello, V., & Sandri, M. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2015.00422 · Cited by 434 · see citing works
Mechanisms of Selective Autophagy
Lamark, T., & Johansen, T. (2021) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-120219-035530 · Cited by 429 · see citing works
Receptor-mediated mitophagy in yeast and mammalian systems
Liu, L., Sakakibara, K., Chen, Q., & Okamoto, K. (2014) · Cell Research · doi:10.1038/cr.2014.75 · Cited by 421 · see citing works
Diverse Cellular Roles of Autophagy
Morishita, H., & Mizushima, N. (2019) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100818-125300 · Cited by 376 · see citing works
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Webster, J. M., Kempen, L. J. A. P., Hardy, R. S., & Langen, R. C. J. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.597675 · Cited by 372 · see citing works
Mitophagy: An Emerging Role in Aging and Age-Associated Diseases
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Polletta, L., Vernucci, E., Carnevale, I., Arcangeli, T., Rotili, D., Palmerio, S., Steegborn, C., Nowak, T., Schutkowski, M., Pellegrini, L., et al. (2015) · Autophagy · doi:10.1080/15548627.2015.1009778 · Cited by 350 · see citing works
Potential function for the Huntingtin protein as a scaffold for selective autophagy
Ochaba, J., Lukacsovich, T., Csikos, G., Zheng, S., Margulis, J., Salazar, L., Mao, K., Lau, A. L., Yeung, S. Y., Humbert, S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420103111 · Cited by 308 · see citing works
Mitochondrial degradation: Mitophagy and beyond
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Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging
Leduc-Gaudet, J.-P., Hussain, S. N. A., Barreiro, E., & Gouspillou, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158179 · Cited by 268 · see citing works
Vasheghani, F., Zhang, Y., Li, Y.-H., Blati, M., Fahmi, H., Lussier, B., Roughley, P., Lagares, D., Endisha, H., Saffar, B., et al. (2015) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2014-205743 · Cited by 221 · see citing works
Hypoxia and Selective Autophagy in Cancer Development and Therapy
Daskalaki, I., Gkikas, I., & Tavernarakis, N. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00104 · Cited by 188 · see citing works
Li, W., Zhang, X., Zhuang, H., Chen, H.-G., Chen, Y., Tian, W., Wu, W., Li, Y., Wang, S., Zhang, L., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.537050 · Cited by 145 · see citing works
Lu, X., Altshuler-Keylin, S., Wang, Q., Chen, Y., Henrique Sponton, C., Ikeda, K., Maretich, P., Yoneshiro, T., & Kajimura, S. (2018) · Science Signaling · doi:10.1126/scisignal.aap8526 · Cited by 143 · see citing works
Strategies Used by Bacteria to Grow in Macrophages
Mitchell*, G., Chen*, C., & Portnoy, D. A. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.mchd-0012-2015 · Cited by 137 · see citing works
Ju, J.-S., Jeon, S.-I., Park, J.-Y., Lee, J.-Y., Lee, S.-C., Cho, K.-J., & Jeong, J.-M. (2016) · The Journal of Physiological Sciences · doi:10.1007/s12576-016-0440-9 · Cited by 125 · see citing works
Inhibition of BMI1 induces autophagy-mediated necroptosis
Dey, A., Mustafi, S. B., Saha, S., Kumar Dhar Dwivedi, S., Mukherjee, P., & Bhattacharya, R. (2016) · Autophagy · doi:10.1080/15548627.2016.1147670 · Cited by 97 · see citing works
Kubli, D. A., Cortez, M. Q., Moyzis, A. G., Najor, R. H., Lee, Y., & Gustafsson, Å. B. (2015) · PLOS ONE · doi:10.1371/journal.pone.0130707 · Cited by 102 · see citing works
Self-citationImpaired Mitophagy Plays a Role in Denervation of Neuromuscular Junctions in ALS Mice
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Toward understanding genomic instability, mitochondrial dysfunction and aging
Fakouri, N. B., Hou, Y., Demarest, T. G., Christiansen, L. S., Okur, M. N., Mohanty, J. G., Croteau, D. L., & Bohr, V. A. (2019) · The FEBS Journal · doi:10.1111/febs.14663 · Cited by 77 · see citing works
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Conway, O., Akpinar, H. A., Rogov, V. V., & Kirkin, V. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.10.013 · Cited by 75 · see citing works
Vrahnas, C., Blank, M., Dite, T. A., Tatarczuch, L., Ansari, N., Crimeen-Irwin, B., Nguyen, H., Forwood, M. R., Hu, Y., Ikegame, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11373-9 · Cited by 70 · see citing works
Cilenti, L., Ambivero, C. T., Ward, N., Alnemri, E. S., Germain, D., & Zervos, A. S. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.03.027 · Cited by 70 · see citing works
HIF1α-dependent mitophagy facilitates cardiomyoblast differentiation
Zhao, J.-F., Rodger, C. E., Allen, G. F. G., Weidlich, S., & Ganley, I. G. (2020) · Cell Stress · doi:10.15698/cst2020.05.220 · Cited by 61 · see citing works
The lifecycle of skeletal muscle mitochondria in obesity
Pileggi, C. A., Parmar, G., & Harper, M. (2021) · Obesity Reviews · doi:10.1111/obr.13164 · Cited by 61 · see citing works
Wiederstein, J. L., Nolte, H., Günther, S., Piller, T., Baraldo, M., Kostin, S., Bloch, W., Schindler, N., Sandri, M., Blaauw, B., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.136 · Cited by 52 · see citing works
Qin, X., Wang, R., Xu, H., Tu, L., Chen, H., Li, H., Liu, N., Wang, J., Li, S., Yin, F., et al. (2022) · Autophagy · doi:10.1080/15548627.2021.2022360 · Cited by 55 · see citing works
Castets, P., Frank, S., Sinnreich, M., & Rüegg, M. A. (2016) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-160153 · Cited by 49 · see citing works
Liu, C., Ma, J., Zhang, J., Zhao, H., Zhu, Y., Qi, J., Liu, L., Zhu, L., Jiang, Y., Tang, G., et al. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00505 · Cited by 34 · see citing works
Roles of HIF1α- and HIF2α-regulated BNIP3 in hypoxia-induced injury of neurons
Zhu, L., Qi, B., & Hou, D. (2019) · Pathology - Research and Practice · doi:10.1016/j.prp.2019.01.022 · Cited by 20 · see citing works
The pivotal role of dysregulated autophagy in the progression of non-alcoholic fatty liver disease
Shen, Q., Yang, M., Wang, S., Chen, X., Chen, S., Zhang, R., Xiong, Z., & Leng, Y. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1374644 · Cited by 15 · see citing works
AlphaFold2 SLiM screen for LC3-LIR interactions in autophagy
Stuke, J. F. M., & Hummer, G. (2025) · Autophagy · doi:10.1080/15548627.2025.2493999 · Cited by 8 · see citing works
- Authors
- Hanna, R. A., Quinsay, M. N., Orogo, A. M., Giang, K., Rikka, S., & Gustafsson, Å. B.
- Affiliations
- University of California San Diego (US)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 287
- Issue
- 23
- Pages
- 19094-19104
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3365942
- OpenAlex
- W2122556106
- Cited by
- 762
- References
- 46
- Citations by year
- 2026: 54 · 2025: 54 · 2024: 60 · 2023: 60 · 2022: 77 · 2021: 79 · 2020: 71 · 2019: 45 · 2018: 48 · 2017: 42 · 2016: 44 · 2015: 49 · 2014: 40 · 2013: 30 · 2012: 9
- FWCI
- 30.54
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL101217, R01HL087023)
- National Institute of General Medical Sciences (T32GM007752)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- BNIP3, LC3, autophagy, mitophagy, endoplasmic reticulum, mitochondria, BH3-only proteins, protein homodimerization, autophagy receptors, autophagosomes, transmembrane domain
- MeSH terms
- Autophagy, Endoplasmic Reticulum, HeLa Cells, Humans, Membrane Proteins, Microtubule-Associated Proteins, Mitochondria, Mutation, Proto-Oncogene Proteins, Apoptosis, Protein Structure, Tertiary
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 ›
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