The DOI matches its Crossref record; 35 of the 35 references it cites were found in a registry or an index.
Nix is a selective autophagy receptor for mitochondrial clearance
Open accessAbstract
Autophagy is the cellular homeostatic pathway that delivers large cytosolic materials for degradation in the lysosome. Recent evidence indicates that autophagy mediates selective removal of protein aggregates, organelles and microbes in cells. Yet, the specificity in targeting a particular substrate to the autophagy pathway remains poorly understood. Here, we show that the mitochondrial protein Nix is a selective autophagy receptor by binding to LC3/GABARAP proteins, ubiquitin-like modifiers that are required for the growth of autophagosomal membranes. In cultured cells, Nix recruits GABARAP-L1 to damaged mitochondria through its amino-terminal LC3-interacting region. Furthermore, ablation of the Nix:LC3/GABARAP interaction retards mitochondrial clearance in maturing murine reticulocytes. Thus, Nix functions as an autophagy receptor, which mediates mitochondrial clearance after mitochondrial damage and during erythrocyte differentiation.
Overview
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
Cites
Statistics
Verification
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?
In the citing paper
“Mitophagy can also occur through Parkin-independent pathways.”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [140]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Pankiv, 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
Parkin is recruited selectively to impaired mitochondria and promotes their autophagy
Narendra, D., Tanaka, A., Suen, D.-F., & Youle, R. J. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200809125 · Cited by 4,026
Autophagosome formation: core machinery and adaptations
Xie, Z., & Klionsky, D. J. (2007) · Nature Cell Biology · doi:10.1038/ncb1007-1102 · Cited by 2,237
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
Dynamics and diversity in autophagy mechanisms: lessons from yeast
Nakatogawa, H., Suzuki, K., Kamada, Y., & Ohsumi, Y. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2708 · Cited by 1,761
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
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
A Role for Ubiquitin in Selective Autophagy
Kirkin, V., McEwan, D. G., Novak, I., & Đikić, I. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.04.026 · Cited by 1,268
Essential role for Nix in autophagic maturation of erythroid cells
Sandoval, H., Thiagarajan, P., Dasgupta, S. K., Schumacher, A., Prchal, J. T., Chen, M., & Wang, J. (2008) · Nature · doi:10.1038/nature07006 · Cited by 1,185
A Role for NBR1 in Autophagosomal Degradation of Ubiquitinated Substrates
Kirkin, V., Lamark, T., Sou, Y.-S., Bjørkøy, G., Nunn, J. L., Bruun, J.-A., Shvets, E., McEwan, D. G., Clausen, T. H., Wild, P., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.01.020 · Cited by 1,065
Flagged first, then by citations
Cited by
Sorted by citations
Items 101–200 of 1,000
Hamacher‐Brady, A., & Brady, N. R. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2087-8 · Cited by 410
“The LC3 family includes LC3A, LC3B, LC3B2, and LC3C, and the GABARAP family includes GABARAP, GABARAP-L1, GABARAP-L2/ GATE-16, and GABARAP-L3.”
BackgroundInfluentialAutophagy in acute kidney injury
Kaushal, G. P., & Shah, S. V. (2016) · Kidney International · doi:10.1016/j.kint.2015.11.021 · Cited by 389
The crosstalk between ferroptosis and mitochondrial dynamic regulatory networks
Li, J., Jia, Y., Ding, Y.-X., Bai, J., Cao, F., & Li, F. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.83348 · Cited by 417
PINK1/Parkin-mediated mitophagy in neurodegenerative diseases
Li, J., Yang, D., Li, Z., Zhao, M., Wang, D., Sun, Z., Wen, P., Dai, Y., Gou, F., Ji, Y., et al. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101817 · Cited by 406
Zhou, J., Wang, J., Cheng, Y., Chi, Y., Fan, B., Yu, J., & Chen, Z. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003196 · Cited by 379
“In addition, Nix acts as an adaptor for autophagy of mitochondria (mitophagy) during erythrocyte differentiation [7].”
BackgroundThe emerging, multifaceted role of mitophagy in cancer and cancer therapeutics
Panigrahi, D. P., Praharaj, P. P., Bhol, C. S., Mahapatra, K. K., Patra, S., Behera, B. P., Mishra, S. R., & Bhutia, S. K. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.07.015 · Cited by 379
Chen, M., Meng, Q., Qin, Y., Liang, P., Tan, P., He, L., Zhou, Y., Chen, Y., Huang, J., Wang, R., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.08.025 · Cited by 367
The role of mitochondria in aging
Jang, J. Y., Blum, A., Liu, J., & Finkel, T. (2018) · Journal of Clinical Investigation · doi:10.1172/jci120842 · Cited by 358
“In the reticulocyte, there is evidence that NIX might play this role (77).”
van der Veen, A. G., & Ploegh, H. L. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-093010-153308 · Cited by 381
Mitophagy: An Emerging Role in Aging and Age-Associated Diseases
Chen, G., Kroemer, G., & Kepp, O. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00200 · Cited by 359
Autophagy in Antimicrobial Immunity
Gomes, L. C., & Dikic, I. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.009 · Cited by 350
“Analogous to aggrephagy (Kirkin et al., 2009a) or mitophagy (Novak et al., 2010), xenophagy utilizes autophagy receptors that bind both a molecular tag (for instance, ubiquitin chains) attached to the cargo and the autophagy modifier LC3 or GABARAP to selectively bring the cargo to the…”
BackgroundNoda, N. N., & Inagaki, F. (2015) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-060414-034248 · Cited by 363
Svenning, S., Lamark, T., Krause, K., & Johansen, T. (2011) · Autophagy · doi:10.4161/auto.7.9.16389 · Cited by 368
Mitochondrial Quality Control and Disease: Insights into Ischemia-Reperfusion Injury
Anzell, A. R., Maizy, R., Przyklenk, K., & Sanderson, T. H. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0503-9 · Cited by 359
From Erythroblasts to Mature Red Blood Cells: Organelle Clearance in Mammals
Moras, M., Lefevre, S. D., & Ostuni, M. A. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.01076 · Cited by 364
“This protein is upregulated during erythropoiesis and induces mitochondrial membrane depolarization and membrane conjugated LC3 recruitment to the mitochondria (Aerbajinai et al., 2003; Novak et al., 2010).”
BackgroundHale, A. N., Ledbetter, D., Gawriluk, T. R., & Rucker, E. B. (2013) · Autophagy · doi:10.4161/auto.24273 · Cited by 343
Programmed mitophagy is essential for the glycolytic switch during cell differentiation
Esteban‐Martínez, L., Sierra‐Filardi, E., McGreal, R., Salazar‐Roa, M., Mariño, G., Seco, E., Durand, S., Enot, D. P., Graña‐Castro, O., Malumbres, M., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201695916 · Cited by 344
“During programmed mitophagy, NIX is mainly regulated at the transcriptional level and acts as a mitophagy receptor, mediating autophagic sequestration of mitochondria by interacting with LC3 via its LIR domain (Novak et al , 2010).”
von Muhlinen, N., Akutsu, M., Ravenhill, B. J., Foeglein, Á., Bloor, S., Rutherford, T. J., Freund, S. M. V., Komander, D., & Randow, F. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.08.024 · Cited by 332
“Intriguingly, the mitophagy adaptor Nix, binds LC3A but not LC3B (LC3C was not tested) (Novak et al., 2010).”
Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates
Korac, J., Schaeffer, V., Kovacevic, I., Clement, A. M., Jungblut, B., Behl, C., Terzic, J., & Dikic, I. (2013) · Journal of Cell Science · doi:10.1242/jcs.114926 · Cited by 336
“, 2010), defective mitochondria (Novak et al., 2010) and bacteria Salmonella enterica (Thurston”
BackgroundProtecting the mitochondrial powerhouse
Scheibye‐Knudsen, M., Fang, E. F., Croteau, D. L., Wilson, D. M., & Bohr, V. A. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.11.002 · Cited by 337
“This process is believed to be initiated through increased expression of the promitophagic factor NIX (BNIP3L) [92].”
BackgroundMitophagy defects arising from BNip3 loss promote mammary tumor progression to metastasis
Chourasia, A. H., Tracy, K., Frankenberger, C. A., Boland, M. L., Sharifi, M. N., Drake, L. E., Sachleben, J. R., Asara, J. M., Locasale, J. W., Karczmar, G. S., et al. (2015) · EMBO Reports · doi:10.15252/embr.201540759 · Cited by 344
“Also, it is possible that while mitophagy is reduced in BNip3 null tumors, it is not completely inhibited and that other mitophagy regulators, such as NIX or Parkin [53,54], partially compensate for BNIP3 loss.”
Ubiquitin signaling and autophagy
Grumati, P., & Đikić, I. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.tm117.000117 · Cited by 336
“Conversely, FUNDC1, BNIP3, andNIX are specific autophagy receptors, which lead to Ub-independentmitophagy (63, 64).”
BackgroundLewy Body-like α-Synuclein Aggregates Resist Degradation and Impair Macroautophagy
Tanik, S. A., Schultheiss, C. E., Volpicelli-Daley, L. A., Brunden, K. R., & Lee, V. M. Y. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.457408 · Cited by 326
“An impairment of autophagosome clearance is likely to be detrimental, as removal of both unwanted and damaged proteins and defective organelles such as mitochondria (69, 70) is vital for cells.”
BackgroundMolecular Mechanisms of Mitochondrial Autophagy/Mitophagy in the Heart
Saito, T., & Sadoshima, J. (2015) · Circulation Research · doi:10.1161/circresaha.116.303790 · Cited by 329
“Mutation of the LIR of Nix/Bnip3L results in a partial reduction of mitochondrial autophagy in reticulocytes.(54)”
The pharmacological regulation of cellular mitophagy
Georgakopoulos, N., Wells, G., & Campanella, M. (2017) · Nature Chemical Biology · doi:10.1038/nchembio.2287 · Cited by 330
Mitochondrial autophagy: Origins, significance, and role of BNIP3 and NIX
Ney, P. A. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.02.022 · Cited by 328
Khandia, R., Dadar, M., Munjal, A. K., Dhama, K., Karthik, K., Tiwari, R., Yatoo, M. I., Iqbal, H. M. N., Singh, K. P., Joshi, S. K., et al. (2019) · Cells · doi:10.3390/cells8070674 · Cited by 337
“The mitochondrial outer membrane protein, Atg32, is a receptor for selective autophagy [126] that is not conserved in mammalian species; instead, FUNDC1 and BNIP3, BNIP3L/NIX, and SQSTM1/p62 act as mitophagy receptors, and are dependent upon hypoxia, erythrocyte maturation, and damage-induced mitophagy, respectively […”
BackgroundLi, F., Chung, T., & Vierstra, R. D. (2014) · The Plant Cell · doi:10.1105/tpc.113.120014 · Cited by 312
“As examples, yeast ATG11 interacts with the mitophagy receptor ATG32 to remove aberrant or superfluous mitochondria when nutrients become limiting (Kanki et al., 2009; Okamoto et al., 2009), whereas mice missing FIP200 hyperaccumulate mitochondria damaged by depolarization (Liang et al., 2010).”
BNIP3- and BNIP3L-Mediated Mitophagy Promotes the Generation of Natural Killer Cell Memory
O’Sullivan, T. E., Johnson, L. R., Kang, H. H., & Sun, J. C.-Y. (2015) · Immunity · doi:10.1016/j.immuni.2015.07.012 · Cited by 311
“…that BNIP3 and BNIP3L can serve directly as ‘‘mitophagy receptors’’ through binding their conserved LC3-interacting region (LIR) to LC3b present on autophagosomes (Hanna et al., 2012; Novak et al., 2010; Zhu et al., 2013) to mediate recruitment of autophagosomes to dysfunctional mitochondria.”
The multiple roles of autophagy in cancer
Rosenfeldt, M. T., & Ryan, K. M. (2011) · Carcinogenesis · doi:10.1093/carcin/bgr031 · Cited by 311
Alpha-synuclein and Protein Degradation Systems: a Reciprocal Relationship
Xilouri, M., Brekk, O. R., & Stefanis, L. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8341-2 · Cited by 310
“Moreover, several other proteins (“autophagy receptors”) linking the autophagic machinery to its substrates have been identified [30–33] reinforcing the idea that macroautophagy can be a rather selective process.”
Rogov, V. V., SUZUKI, H., Marinković, M., Lang, V., Kato, R., Kawasaki, M., Buljubašić, M., Šprung, M., Rogova, N. Y., Wakatsuki, S., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-01258-6 · Cited by 310
Mitochondrial dysfunction in neurodegenerative diseases and the potential countermeasure
Wang, Y., Xu, E., Musich, P. R., & Lin, F. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13116 · Cited by 298
Mitochondrial E3 ligase MARCH5 regulates FUNDC1 to fine‐tune hypoxic mitophagy
Chen, Z., Liu, L., Cheng, Q., Li, Y., Wu, H., Zhang, W., Wang, Y., Sehgal, S. A., Siraj, S., Wang, X., et al. (2017) · EMBO Reports · doi:10.15252/embr.201643309 · Cited by 299
Mitochondrial shape changes: orchestrating cell pathophysiology
Campello, S., & Scorrano, L. (2010) · EMBO Reports · doi:10.1038/embor.2010.115 · Cited by 307
“…in which it has been tested; (ii) cristae remodelling was originally identified (and is still studied) by using an in vitro system in which caspases are absent, ruling out a role for any postmitochondrial pathway; and (iii) differences in the experimental conditions and in the way that…”
Backgroundp62 and NDP52 Proteins Target Intracytosolic Shigella and Listeria to Different Autophagy Pathways
Mostowy, S., Sancho-Shimizu, V., Hamon, M. A., Simeone, R., Brosch, R., Johansen, T., & Cossart, P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.223610 · Cited by 294
Zhu, J., Wang, K. Z. Q., & Chu, C. T. (2013) · Autophagy · doi:10.4161/auto.24135 · Cited by 303
Ferritinophagy/ferroptosis: Iron‐related newcomers in human diseases
Tang, M., Chen, Z., Wu, D., & Chen, L. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26954 · Cited by 292
Crosstalk between mitochondrial biogenesis and mitophagy to maintain mitochondrial homeostasis
Liu, L., Li, Y., Chen, G., & Chen, Q. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00975-7 · Cited by 322
“This association was shown to be required for the clearance of mitochondria during erythrocyte development [152].”
BackgroundThe Cvt pathway as a model for selective autophagy
Lynch-Day, M. A., & Klionsky, D. J. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.02.013 · Cited by 329
“NBR1 is involved in the clearance of ubiquitinated aggregates [89], whereas Nix plays a role in the selective clearance of mitochondria by autophagy (mitophagy) during reticulocyte maturation [90,91].”
BackgroundSkeletal muscle mitochondrial remodeling in exercise and diseases
Gan, Z., Fu, T., Kelly, D. P., & Vega, R. B. (2018) · Cell Research · doi:10.1038/s41422-018-0078-7 · Cited by 297
ATG8 Family Proteins Act as Scaffolds for Assembly of the ULK Complex
Alemu, E. A., Lamark, T., Torgersen, K. M., Birgisdottir, Å. B., Larsen, K. B., Jain, A., Olsvik, H. L., Øvervatn, A., Kirkin, V., & Johansen, T. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.378109 · Cited by 303
“p62 (16), NBR1 (19), AtNBR1 (43), ATG4B (44), TP53INP1 and TP53INP2/DOR (45), FYCO1 (21), Dvl2 (46), NIX (47), FUNDC1 (48), Calreticulin (49), clathrin heavy”
HUWE1 E3 ligase promotes PINK1/PARKIN-independent mitophagy by regulating AMBRA1 activation via IKKα
Rita, A. D., Peschiaroli, A., D’Acunzo, P., Strobbe, D., Hu, Z., Gruber, J., Nygaard, M. M., Lambrughi, M., Melino, G., Papaleo, E., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05722-3 · Cited by 286
Parkin and mitophagy in cancer
Bernardini, J. P., Lazarou, M., & Dewson, G. (2016) · Oncogene · doi:10.1038/onc.2016.302 · Cited by 291
Role and Mechanisms of Mitophagy in Liver Diseases
Ma, X., McKeen, T., Zhang, J., & Ding, W. (2020) · Cells · doi:10.3390/cells9040837 · Cited by 288
Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle
Drake, J. C., Wilson, R. J., & Yan, Z. (2016) · The FASEB Journal · doi:10.1096/fj.15-276337 · Cited by 263
“BNIP3 and Nix localize to the OMM where they may interact with MAP1LC3 for the docking of the autophagosome (99).”
BackgroundBnip3 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
“was recently reported to interact directly with the autophagy proteins LC3 and GABARAP.(23) To investigate whether Bnip3 also interacts with LC3, we performed co-immunoprecipitation experiments of Bnip3 and LC3.”
BNIP3 Interacting with LC3 Triggers Excessive Mitophagy in Delayed Neuronal Death in Stroke
Shi, R., Zhu, S., Li, V., Gibson, S. B., Xu, X., & Kong, J. (2014) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12325 · Cited by 282
“To date, multiple lines of evidence supports the essential role of NIX in developmental removal of mitochondria during erythrocyte maturation [47,48], but other functions of NIX-mediated mitophagy are still unknown.”
BackgroundDynamic regulation of macroautophagy by distinctive ubiquitin-like proteins
Klionsky, D. J., & Schulman, B. A. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2787 · Cited by 284
BNIP3L/NIX-mediated mitophagy protects against ischemic brain injury independent of PARK2
Yuan, Y., Zheng, Y., Zhang, X., Chen, Y., Wu, X., Wu, J., Shen, Z., Jiang, L., Wang, L., Yang, W. Y., et al. (2017) · Autophagy · doi:10.1080/15548627.2017.1357792 · Cited by 283
“autophagosomes, to mitochondria by directly binding with Atg8 family proteins.(20) BNIP3L may coordinate with PARK2”
BackgroundLethal Cardiomyopathy in Mice Lacking Transferrin Receptor in the Heart
Xu, W., Barrientos, T., Mao, L., Rockman, H. A., Sauve, A. A., & Andrews, N. C. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.023 · Cited by 280
“Autophagy-related proteins LC3-II, p62, Fundc1, Nix, Ulk-1 and Cisd2, showed no significant differences (Fig 6C–”
BackgroundInfluentialSelf and Nonself: How Autophagy Targets Mitochondria and Bacteria
Randow, F., & Youle, R. J. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.03.012 · Cited by 281
“Although Nix was found to have a consensus LC3 interaction region (LIR) motif that binds to both LC3 and GABARAP (Novak et al., 2010), suggesting it functions to recruit mitochondria into isolation membranes/phagophores, in vivo experiments indicate additional unknown functions for Nix during…”
InfluentialWurzer, B., Zaffagnini, G., Fracchiolla, D., Turco, E., Abert, C., Romanov, J., & Martens, S. (2015) · eLife · doi:10.7554/elife.08941 · Cited by 290
“…Komatsu et al., 2007; Pankiv et al., 2007; Szeto et al., 2006), damaged mitochondria (Geisler et al., 2010; Kanki et al., 2009; Narendra et al., 2008; Novak et al., 2010; Okamoto et al., 2009), intracellular pathogens (Gutierrez et al., 2004; Nakagawa et al., 2004; Thurston et al., 2009; Yoshikawa…”
BackgroundRole of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle
Vainshtein, A., Tryon, L. D., Pauly, M., & Hood, D. A. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00380.2014 · Cited by 273
“Mitochondrial targeting can occur via mitophagy-specific receptors such as Bcl-2/adenovirus E1B 19-kDa interacting protein 3-like (Nix/Bnip3) (14, 26, 30) or by ubiquitination of mitochondrial outer membrane proteins by E3 ligases such as Parkin and Mul1 (4, 21, 25).”
BackgroundMitochondrial quality control in health and in Parkinson’s disease
Eldeeb, M. A., Thomas, R. A., Ragheb, M. A., Fallahi, A., & Fon, E. A. (2022) · Physiological Reviews · doi:10.1152/physrev.00041.2021 · Cited by 281
Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic reticulum stress
Deegan, S., Saveljeva, S., Gorman, A. M., & Samali, A. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1173-4 · Cited by 280
“Nix has only been shown to be involved in the selective removal of mitochondria, most prominently shown during reticulocyte differentiation [88, 89].”
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
Pex3‐anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae
Motley, A. M., Nuttall, J. M., & Hettema, E. H. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.151 · Cited by 275
“Likewise, in mammalian cells, known autophagy receptors bind to Atg8-family orthologues via conserved LIRs (LC3-interacting region), and these interactions are essential for function (Kirkin et al , 2009; Novak et al , 2010; Wild et al , 2011).”
Mitophagy in Alzheimer’s Disease and Other Age-Related Neurodegenerative Diseases
Cai, Q., & Jeong, Y. Y. (2020) · Cells · doi:10.3390/cells9010150 · Cited by 270
“NIX/BNIP3L contains an LIR motif at the amino-terminal that binds to LC3 on phagophore or isolation membranes, and is transcriptionally upregulated during erythrocyte differentiation [58].”
BackgroundHallmarks of Aging: An Autophagic Perspective
Barbosa, M. C., Grosso, R. A., & Fader, C. M. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00790 · Cited by 275
“These proteins contain a LC3 interacting region (LIR), which allows the recognition of elements to be engulfed by the phagophore and eliminated in an autophagic manner (18, 19).”
BackgroundAutophagy and organelle homeostasis in cancer
Miller, D. R., & Thorburn, A. M. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.02.010 · Cited by 271
Autophagy and A lpha‐ S ynuclein: R elevance to P arkinson's D isease and R elated S ynucleopathies
Xilouri, M., Brekk, O. R., & Stefanis, L. (2016) · Movement Disorders · doi:10.1002/mds.26477 · Cited by 280
Rheb Regulates Mitophagy Induced by Mitochondrial Energetic Status
Melser, S., Chatelain, É. H., Lavie, J., Mahfouf, W., José, C., Obre, É., Goorden, S. M. I., Priault, M., Elgersma, Y., Rezvani, H. R., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.03.014 · Cited by 270
“This mechanism involves the outer mitochondrial membrane receptor Nix (or Bnip3l) and autophagosome-associated protein LC3 (Novak et al., 2010).”
BackgroundMitochondrial Dysfunction in Alzheimer’s Disease and the Rationale for Bioenergetics Based Therapies
Onyango, I. G., Dennis, J., & Khan, S. M. (2016) · Aging and Disease · doi:10.14336/ad.2015.1007 · Cited by 260
“Nat Cell Biol, 14: 177–185 [54] Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, et al.”
BackgroundWei, H., Liu, L., & Chen, Q. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.03.013 · Cited by 266
“Studies using NIX-/- mice revealed that NIX is involved in the process of reticulocytes maturation [14, 59, 61, 62].”
BackgroundInfluentialMitophagy in Cancer: A Tale of Adaptation
Vara‐Pérez, M., Felipe‐Abrio, B., & Agostinis, P. (2019) · Cells · doi:10.3390/cells8050493 · Cited by 264
Mitochondrial morphology in mitophagy and macroautophagy
Gomes, L. C., & Scorrano, L. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.02.012 · Cited by 259
“LIR domain of NIX [56].”
BackgroundInfluentialThe LC3 interactome at a glance
Wild, P. S., McEwan, D. G., & Đikić, I. (2013) · Journal of Cell Science · doi:10.1242/jcs.140426 · Cited by 263
“and FUNDC1 in mammals) are outer mitochondrial membrane proteins that are already placed and primed for autophagic clearance of mitochondria (Hanna et al., 2012; Kanki et al., 2009; Liu et al., 2012; Novak et al., 2010; Okamoto et al., 2009).”
BackgroundRegulation of PRKN-independent mitophagy
Terešak, P., Lapão, A., Subic, N., Boya, P., Elazar, Z., & Simonsen, A. (2021) · Autophagy · doi:10.1080/15548627.2021.1888244 · Cited by 256
“HIF1A regulates the transcription of hundreds of genes in response to hypoxia, including the mitophagy receptors BNIP3 and BNIP3L [42].”
BackgroundInfluentialMitochondrial dysfunction and mitophagy: the beginning and end to diabetic nephropathy?
Higgins, G. C., & Coughlan, M. T. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12503 · Cited by 257
“, 2010), Nix (Bnip3L) (Novak et al., 2010), Bnip3 (Hanna et al.”
BackgroundInfluentialMitophagy and mitochondrial integrity in cardiac ischemia-reperfusion injury
Yang, M., Linn, B. S., Zhang, Y., & Ren, J. T. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.05.007 · Cited by 253
Orphan nuclear receptor TR3 acts in autophagic cell death via mitochondrial signaling pathway
Wang, W.-J., Wang, Y., Chen, H., Xing, Y.-Z., Li, F.-W., Zhang, Q., Zhou, B., Zhang, H., Zhang, J., Bian, X., et al. (2013) · Nature Chemical Biology · doi:10.1038/nchembio.1406 · Cited by 253
Mitophagy in tumorigenesis and metastasis
Poole, L. P., & Macleod, K. F. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03774-1 · Cited by 257
Selective degradation of p62 by autophagy
Ichimura, Y., & Komatsu, M. (2010) · Seminars in Immunopathology · doi:10.1007/s00281-010-0220-1 · Cited by 250
“Furthermore, the Atg32 and Nix/Bnip3L involved in selective degradation of the mitochondria through autophagy (mitophagy) also contain WxxL-like motifs to interact with Atg8, LC3, and GABA(A) receptor-associated protein, respectively [26–29].”
BackgroundMitochondrial dysfunction and mitophagy defect triggered by heterozygous GBA mutations
Li, H., Ham, A., Ma, T. C., Kuo, S., Kanter, E., Kim, D., Ko, H. S., Quan, Y., Sardi, S. P., Li, A., et al. (2018) · Autophagy · doi:10.1080/15548627.2018.1509818 · Cited by 251
Tian, Y., Chang, J. C., Fan, E. Y., Flajolet, M., & Greengard, P. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315110110 · Cited by 233
Mehrbod, P., Ande, S. R., Alizadeh, J., Rahimizadeh, S., Shariati, A., Malek, H., Hashemi, M. M., Glover, K. K. M., Sher, A. A., Coombs, K. M., et al. (2019) · Virulence · doi:10.1080/21505594.2019.1605803 · Cited by 246
The Role of Mitophagy in Innate Immunity
Gkikas, I., Palikaras, K., & Tavernarakis, N. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01283 · Cited by 248
“NIX has been shown to mediate mitochondrial turnover during reticulocytes’ maturation (56).”
BackgroundQuinsay, M. N., Thomas, R. L., Lee, Y., & Gustafsson, Å. B. (2010) · Autophagy · doi:10.4161/auto.6.7.13005 · Cited by 244
Identification of an Autophagy Defect in Smokers’ Alveolar Macrophages
Monick, M. M., Powers, L. S., Walters, K., Lovan, N., Zhang, M., Gerke, A., Hansdottir, S., & Hunninghake, G. W. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001603 · Cited by 214
“Nix forms a complex with LC3 and GABARAP-L1 that mediates mitochondrial clearance (55).”
BackgroundExercise Training-Induced Regulation of Mitochondrial Quality
Yan, Z., Lira, V. A., & Greene, N. P. (2012) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3182575599 · Cited by 244
“Other proteins that have been implicated in mitophagy are mitochondrially localized BNIP3 (Bcl-2 and 19 kd interacting protein 37) and BNIP3-like protein (BNIP3L) (30,40).”
BackgroundWhen autophagy meets cancer through p62/SQSTM1.
Puissant, A., Fenouille, N., & Auberger, P. (2012) · Europe PMC (PubMed Central) · Cited by 236
The Spectrum of Achalasia: Lessons From Studies of Pathophysiology and High-Resolution Manometry
Kahrilas, P. J., & Boeckxstaens, G. E. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.08.038 · Cited by 236
Wu, H., Wang, Y., Li, W., Chen, H., Du, L., Liu, D., Wang, X., Xu, T., Liu, L., & Chen, Q. (2019) · Autophagy · doi:10.1080/15548627.2019.1596482 · Cited by 235
“These include BNIP3L/NIX [13], BNIP3 [14], BCL2L13 [15], PHB2 [16], and FKBP8 [17] in mammalian cells, as well as Atg32 [18,19] in yeast.”
AMPK Activation Stimulates Autophagy and Ameliorates Muscular Dystrophy in the mdx Mouse Diaphragm
Pauly, M., Daussin, F., Burelle, Y., Li, T., Godin, R., Fauconnier, J., Koechlin-Ramonatxo, C., Hugon, G., Lacampagne, A., Coisy-Quivy, M., et al. (2012) · The American Journal of Pathology · doi:10.1016/j.ajpath.2012.04.004 · Cited by 225
“In addition, we observed increased expression of Bnip3, a mitochondrial BH3-only protein of the Bcl-2 family, which recruits the autophagy proteins LC3-II and Gabarap to mitochondria.(41) Bnip3 has also been strongly implicated in the process of mitophagy, and inhibition of Bnip3 impedes autophagosome formation in ske…”
BackgroundAutophagy in health and disease. 5. Mitophagy as a way of life
Gottlieb, R. A., & Carreira, R. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00097.2010 · Cited by 230
Evolving and Expanding the Roles of Mitophagy as a Homeostatic and Pathogenic Process
Gustafsson, Å. B., & Dorn, G. W. (2018) · Physiological Reviews · doi:10.1152/physrev.00005.2018 · Cited by 235
Autophagy Signaling Through Reactive Oxygen Species
Huang, J., Lam, G. Y., & Brumell, J. H. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3554 · Cited by 228
“…mammalian mitochondria-localized protein Nix [also known as Bcl2 = E1B 19 kDa-interacting protein 3 (BNIP3)-like protein (BNIP3L)] was recently shown to be a receptor on mitochondria, mediating mammalian mitophagy through interaction with LC3 via the N-terminal LC3 inter-acting region (111).”
Reggiori, F., & Molinari, M. (2022) · Physiological Reviews · doi:10.1152/physrev.00038.2021 · Cited by 232
Regulation of lipid droplets by autophagy
Dong, H., & Czaja, M. J. (2011) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2011.02.003 · Cited by 197
“Nix binds proteins required for autophagosome membrane formation [33], presumably recruiting the components necessary to assemble an autophagosome around mitochondria.”
Mitophagy and Parkinson's disease: The PINK1–parkin link
Deas, E., Wood, N. W., & Plun‐Favreau, H. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.08.007 · Cited by 230
No Parkin Zone: Mitophagy without Parkin
Villa, E., Marchetti, S., & Ricci, J. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.07.004 · Cited by 229
BNIP3L/NIX-mediated mitophagy: molecular mechanisms and implications for human disease
Li, Y., Zheng, W., Lu, Y., Zheng, Y., Pan, L., Wu, X., Yuan, Y., Shen, Z., Ma, S., Zhang, X., et al. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-04469-y · Cited by 246
“BNIP3L has been accepted as a mitophagy receptor that binds to Atg8 proteins [9].”
BackgroundInfluentialContribution of Impaired Mitochondrial Autophagy to Cardiac Aging
Dutta, D., Calvani, R., Bernabei, R., Leeuwenburgh, C., & Marzetti, E. (2012) · Circulation Research · doi:10.1161/circresaha.111.246108 · Cited by 224
Organellophagy: Eliminating cellular building blocks via selective autophagy
Okamoto, K. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201402054 · Cited by 225
“actions of receptor proteins with Atg8/LC3 and Atg11/Atg17 (Farré et al., 2008, 2013; Novak et al., 2010; Aoki et al., 2011; Kondo-Okamoto et al., 2012; Liu et al., 2012; Kanki et al., 2013; Zhu et al., 2013).”
InfluentialAlterations in Mitochondrial Quality Control in Alzheimer’s Disease
Cai, Q., & Tammineni, P. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00024 · Cited by 226
Mechanisms of selective autophagy and mitophagy: Implications for neurodegenerative diseases
Chu, C. T. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.07.015 · Cited by 218
Mitochondrial Pruning by Nix and BNip3: An Essential Function for Cardiac-Expressed Death Factors
Dorn, G. W. (2010) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-010-9174-x · Cited by 215
“A nearly concurrent report identified the Nix-GABARAP interaction in a yeast two-hybrid screen using the autophagy factor Atg8 as bait [44].”
AMPK–mTOR Signaling and Cellular Adaptations in Hypoxia
Chun, Y., & Kim, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189765 · Cited by 237
A guide to the regulation of selective autophagy receptors
Gubaš, A., & Đikić, I. (2021) · FEBS Journal · doi:10.1111/febs.15824 · Cited by 229
Metadata
- Authors
- Novak, I., Kirkin, V., McEwan, D. G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Löhr, F., Popovic, D., Occhipinti, A., Reichert, A. S., Terzic, J., Dötsch, V., Ney, P. A., & Dikic, I.
- Affiliations
- Mediterranean Institute for Life Sciences (HR)
- Goethe University Frankfurt (DE)
- St. Jude Children's Research Hospital (US)
- ORCID
- Venue
- The EMBO Reports
- Published
- 2009-12-11
- Volume
- 11
- Issue
- 1
- Pages
- 45-51
- ISSN
- 1469-221X (ISSN-L)
- 1469-3178
- PMC
- PMC2816619
- OpenAlex
- W2127440157
- Cited by
- 1,309
- References
- 35
- Citations by year
- 2026: 63 · 2025: 77 · 2024: 79 · 2023: 72 · 2022: 81 · 2021: 106 · 2020: 96 · 2019: 86 · 2018: 77 · 2017: 74 · 2016: 85 · 2015: 72 · 2014: 77 · 2013: 63 · 2012: 90
- FWCI
- 44.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- EMBO Reports (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft ((EXC 115).)
- Terry Fox Foundation
- National Institutes of Health (CA21765))
- National Cancer Institute (P 30CA 21765, P30CA021765)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK074519, R21DK074519)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- Nix, selective autophagy, mitophagy, autophagy receptors, LC3, GABARAP, LC3-interacting region, mitochondrial clearance, mitochondrial damage, reticulocytes, erythroid differentiation, ubiquitin-like proteins
- MeSH terms
- Autophagy-Related Protein 8 Family, Amino Acid Sequence, Animals, Autophagy, Binding Sites, Cells, Cultured, Chlorocebus aethiops, Humans, Membrane Proteins, Microtubule-Associated Proteins, Mitochondria, Molecular Sequence Data, Protein Binding, Proto-Oncogene Proteins, Receptors, GABA-A, Reticulocytes, Substrate Specificity, Blotting, Western, COS Cells, Amino Acid Motifs, Mitochondrial Proteins, Tumor Suppressor Proteins, Saccharomyces cerevisiae Proteins, Ubiquitin-Protein Ligases, 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
