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
Cited by
Sorted by citations
Items 401–500 of 1,000
Mitochondrial Protein Quality Control Mechanisms
Jadiya, P., & Tomar, D. (2020) · Genes · doi:10.3390/genes11050563 · Cited by 93
Ossareh‐Nazari, B., Niño, C. A., Bengtson, M. H., Lee, J.-W., Joazeiro, C. A. P., & Dargemont, C. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201308139 · Cited by 97
“Cargoes of selective autophagy pathways are recognized by specific receptors that simultaneously bind to autophagosomeassociated proteins, such as the ubiquitin-like protein Atg8 (LC3 in mammalian cells; Shintani et al., 2002; Novak et al., 2010; Suzuki et al., 2010; Motley et al., 2012).”
Mitophagy in carcinogenesis, drug resistance and anticancer therapeutics
Guan, Y., Wang, Y., Li, B., Shen, K., Li, Q., Ni, Y.-Y., & Huang, L. H. (2021) · Cancer Cell International · doi:10.1186/s12935-021-02065-w · Cited by 97
“The interaction between BNIP3L and GABARAP1/LC3A leads to depolarized mitochondrial clearance upon reticulocyte maturation [22, 28, 29].”
Bloemberg, D., & Quadrilatero, J. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00261.2018 · Cited by 100
Entrenching role of cell cycle checkpoints and autophagy for maintenance of genomic integrity
Anand, S. K., Sharma, A., Singh, N., & Kakkar, P. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.102748 · Cited by 92
Autophagy machinery in the context of mammalian mitophagy
Yoshii, S. R., & Mizushima, N. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.01.013 · Cited by 96
Cheng, M., Liu, L., Lao, Y., Liao, W., Liao, M., Luo, X., Wu, J., Xie, W., Zhang, Y., & Xu, N. (2016) · Oncotarget · doi:10.18632/oncotarget.9786 · Cited by 92
“com/oncotarget Recent studies have identified specific regulators of mitophagy including PINK1/Parkin and mitophagy receptors in mammalian systems [10-14].”
BackgroundBenefit of Oleuropein Aglycone for Alzheimer’s Disease by Promoting Autophagy
Cordero, J. G., García‐Escudero, R., Ávila, J., Gargini, R., & García‐Escudero, V. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/5010741 · Cited by 95
“Additionally, BNIP3L is a mitochondrial membrane protein containing a LC3-interacting region motif involved in the targeted clearance of damaged mitochondria [17].”
BackgroundMitophagy in the Pathogenesis of Liver Diseases
Ke, P. (2020) · Cells · doi:10.3390/cells9040831 · Cited by 91
“In mammals, the BCL2 family protein BNIP3L/Nix was demonstrated to function in mitochondrial turnover by interacting with ATG8/LC3 family proteins during erythrocyte maturation [222,276,277,325,326].”
BackgroundKeeping the immune system in check: a role for mitophagy
Lazarou, M. (2014) · Immunology and Cell Biology · doi:10.1038/icb.2014.75 · Cited by 92
AMBRA1 regulates mitophagy by interacting with ATAD3A and promoting PINK1 stability
Rienzo, M. D., Romagnoli, A., Ciccosanti, F., Refolo, G., Consalvi, V., Arena, G., Valente, E. M., Piacentini, M., & Fimia, G. M. (2021) · Autophagy · doi:10.1080/15548627.2021.1997052 · Cited by 92
The fate of damaged mitochondrial DNA in the cell
Liao, S., Chen, L., Song, Z., & He, H. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2022.119233 · Cited by 97
Mitochondrial homeostasis in adipose tissue remodeling
Altshuler-Keylin, S., & Kajimura, S. (2017) · Science Signaling · doi:10.1126/scisignal.aai9248 · Cited by 93
“NIX mediates mitophagy in a ubiquitin-independent manner, and blocking the direct interaction between NIX and LC3 leads to accumulation of mitochondria in maturing erythrocytes (19).”
The role of mitochondrial DNA damage in the development of atherosclerosis
Yu, E., & Bennett, M. R. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.06.011 · Cited by 92
Autophagy inDrosophila: From Historical Studies to Current Knowledge
Mulakkal, N. C., Nagy, P., Takáts, S., Tusco, R., Juhász, G., & Nezis, I. P. (2014) · BioMed Research International · doi:10.1155/2014/273473 · Cited by 93
“Atg8/LC3 was observed to interact with mitochondrial membrane proteins via its LIR motif, such as the yeast Atg32 [252] and the mammalian NIP3-like protein NIX [253, 254].”
BackgroundMechanisms, pathophysiological roles and methods for analyzing mitophagy – recent insights
Williams, J. A. R., & Ding, W. (2017) · Biological Chemistry · doi:10.1515/hsz-2017-0228 · Cited by 92
“Bnip3 and Nix both have an LIR and interact with the autophagosome membrane protein LC3 (Novak et al., 2010; Novak and Dikic, 2011; Hanna et al., 2012).”
BackgroundPlant Selective Autophagy—Still an Uncharted Territory With a Lot of Hidden Gems
Stephani, M., & Dagdas, Y. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.028 · Cited by 86
Human Atg8-cardiolipin interactions in mitophagy: Specific properties of LC3B, GABARAPL2 and GABARAP
Antón, Z., Landajuela, A., Hervás, J. H., Montes, L. R., Hernández‐Tiedra, S., Velasco, G., Goñi, F. M., & Alonso, A. (2016) · Autophagy · doi:10.1080/15548627.2016.1240856 · Cited by 94
“In mammals, the ubiquitin-binding receptor SQSTM1 (sequestosome 1) is thought to act in the same way as Atg11(39) and during erythrocyte differentiation mitochondrial resident BNIP3L (BCL2 interacting protein 3 like) functions as a mitophagy receptor at least in part by binding to LC3 orthologs.(40)”
BackgroundAutophagy in adipose tissue biology
Zhang, Y., Zeng, X., & Jin, S. V. (2012) · Pharmacological Research · doi:10.1016/j.phrs.2012.09.004 · Cited by 92
Autophagy in Skeletal Muscle Homeostasis and in Muscular Dystrophies
Grumati, P., & Bonaldo, P. (2012) · Cells · doi:10.3390/cells1030325 · Cited by 96
Mitophagy in the pathogenesis and management of disease
Wang, Q., Sun, Y., Li, T. Y., & Auwerx, J. (2026) · Cell Research · doi:10.1038/s41422-025-01203-7 · Cited by 103
“104 For example, BNIP3 mediates mitophagy under hypoxia, 99,102 whereas NIX is essential for mitochondrial elimination during reticulocyte maturation, 100 erythroid cell maturation, 101 and retinal ganglion cell differentiation.”
FBXL4 suppresses mitophagy by restricting the accumulation of NIX and BNIP3 mitophagy receptors
Nguyen, G., Kozul, K., Cui, Y., Townsend, B., Gosavi, P., Ooi, S. S., Marzio, A., Carrodus, N. L., Zuryn, S., Pagano, M., et al. (2023) · The EMBO Journal · doi:10.15252/embj.2022112767 · Cited by 89
“4 Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Lohr F, Popovic D, 629 Occhipinti A et al (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO 630 Rep 11: 45-51 631 Onishi M, Yamano K, Sato M, Matsuda N, Okamoto K (2021) Molecular mechanisms and 632 physiological functi…”
InfluentialReceptor protein complexes are in control of autophagy
Mijaljica, D., Nazarko, T. Y., Brumell, J. H., Huang, W., Komatsu, M., Prescott, M., Simonsen, A., Yamamoto, A., Zhang, H., Klionsky, D. J., et al. (2012) · Autophagy · doi:10.4161/auto.21332 · Cited by 87
Jatana, N., Ascher, D. B., Pires, D. E. V., Gokhale, R. S., & Thukral, L. (2019) · Autophagy · doi:10.1080/15548627.2019.1606636 · Cited by 79
“The importance of these residues has been established by mutagenesis experiments whereby alanine mutant of F52 and Y49 abrogates LC3 binding to SQSTM1/p62 [36], GABARAP binding to NBR1 [26] and BNIP3L/Nix (BCL2 interacting protein 3 like) [21], respectively.”
BackgroundMitophagy in the retina: Viewing mitochondrial homeostasis through a new lens
Jiménez‐Loygorri, J. I., Benítez‐Fernández, R., Viedma-Poyatos, Á., Zapata‐Muñoz, J., Villarejo‐Zori, B., Gómez‐Sintes, R., & Boya, P. (2023) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2023.101205 · Cited by 84
“Long-chain CE generated by the enzyme CERS1 (C18-ceramide) accumulates preferentially in the OMM and can also interact directly with LC3B, triggering mitophagy (Teresak et al., 2022).”
InfluentialZhao, P., Yin, S., Qiu, Y., Sun, C., & Yu, H. (2025) · Molecular Cancer · doi:10.1186/s12943-024-02217-2 · Cited by 102
Hammerling, B. C., & Gustafsson, Å. B. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.07.013 · Cited by 86
“Although they are both known to induce mitochondrial dysfunction and cell death, they can also direct mitochondria to autophagosomes by directly binding to LC3 or gamma-aminobutyric acid receptor-associated protein (GABARAP) on the autophagosome [57], [58] and [59].”
Yamaguchi, O., Murakawa, T., Nishida, K., & Otsu, K. (2016) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2016.03.010 · Cited by 86
“NIX is highly induced during the late phase of erythrocyte maturation and is involved in the elimination of mitochondria from reticulocytes; this process is essential for red blood cell maturaion [63].”
Qi, N., Shi, Y., Zhang, R., Zhu, W., Yuan, B., Li, X., Wang, C., Zhang, X., & Hou, F. (2017) · Nature Communications · doi:10.1038/ncomms15676 · Cited by 84
Pgc-1α overexpression Via local transfection attenuates mitophagy pathway in muscle disuse atrophy
Kang, C., & Ji, L. L. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.12.032 · Cited by 83
Mitochondrial dismissal in mammals, from protein degradation to mitophagy
Campello, S., Strappazzon, F., & Cecconi, F. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.11.010 · Cited by 88
Habisov, S., Huber, J., Ichimura, Y., Akutsu, M., Rogova, N. Y., Loehr, F., McEwan, D. G., Johansen, T., Đikić, I., Dötsch, V., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.715474 · Cited by 78
“Interestingly, LIR/UFIM preferentially binds GABARAPs, similar to the LIRs found in NBR1 (14), NIX/BNIP3L (42), KBTBD6/7 (20), ATG13, and ULK1 (19), and ALFY (43).”
BackgroundMitochondrial quality control: The role of mitophagy in aging
Shi, R., Guberman, M., & Kirshenbaum, L. A. (2017) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2017.11.008 · Cited by 87
“It is worth mentioning, that Nix-mediated mitophagy likely plays an important physiological role in most circumstances such as culling excess mitochondria during cardiac hypertrophy [75,119], excessive activation of Nix may similarly promote cell death like Bnip3 [45,125].”
BackgroundInfluentialWeil, R., Laplantine, E., Curic, S., & Génin, P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01243 · Cited by 83
“NIX was also shown to promote clearance of damaged mitochondria after cell treatment with mitophagy inducers, although mutation of its LIR domain has only a partial effect in vivo (83).”
BackgroundMitofusins: Disease Gatekeepers and Hubs in Mitochondrial Quality Control by E3 Ligases
Escobar‐Henriques, M., & Joaquim, M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00517 · Cited by 85
SAMM50 acts with p62 in piecemeal basal- and OXPHOS-induced mitophagy of SAM and MICOS components
Abudu, Y. P., Shrestha, B. K., Zhang, W., Palara, A., Brenne, H. B., Larsen, K. B., Wolfson, D. L., Dumitriu, G., Øie, C. I., Ahluwalia, B. S., et al. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202009092 · Cited by 79
Shi, P., Wei, Y., Zhang, J. Y., Gál, J., & Zhu, H. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100366 · Cited by 82
“cytes [139].”
Molecular machinery of macroautophagy and its deregulation in diseases
Wong, A. S. L., Cheung, Z. H., & Ip, N. Y. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.07.005 · Cited by 95
“Additional proteins such as Nix [87,88] are required for mitophagy of damaged mitochondria, but the mechanisms involved remain unclear.”
BackgroundInfluentialMitochondrial dynamics: orchestrating the journey to advanced age
Biala, A. K., Dhingra, R., & Kirshenbaum, L. A. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.04.015 · Cited by 82
“tophagy has been reported to be critical for preventing age induced cardiomyopathy [103,104].”
BackgroundConnecting mitochondrial dynamics and life-or-death events via Bcl-2 family proteins
Aouacheria, A., Baghdiguian, S., Lamb, H. M., Huska, J. D., Pineda, F. J., & Hardwick, J. M. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.04.009 · Cited by 81
“…including functioning as regulatory molecules (e.g. Bcl-2-Beclin1 inhibitory interaction) (Pattingre et al., 2005) and as mitophagypromoting mitochondrial receptors (e.g. Bnip3, Bnip3L/Nix, and Bcl2L13/Bcl-Rambo) (Hanna et al., 2012; Murakawa et al., 2015; Novak et al., 2010; Zhu et al., 2013).”
The autophagy conundrum in cancer: influence of tumorigenic metabolic reprogramming
Eng, C. H., & Abraham, R. T. (2011) · Oncogene · doi:10.1038/onc.2011.220 · Cited by 83
Mitophagy and Innate Immunity in Infection.
Cho, D., Kim, J. K., & Jo, E. (2020) · Europe PMC (PubMed Central) · doi:10.14348/molcells.2020.2329 · Cited by 85
“BCL2-interacting protein 3 (BNIP3) and its homolog BNIP3-like (BNIP3L/NIX) can also induce mitophagy in Parkin-deficient cells (Ney, 2015; Novak et al., 2010; Quinsay et al., 2010).”
BackgroundMitochondrial Dysfunction in Age‐Related Metabolic Disorders
Natarajan, V., Chawla, R., Mah, T. K. L., Vivekanandan, R., Tan, S., Sato, P. Y., & Mallilankaraman, K. B. (2020) · PROTEOMICS · doi:10.1002/pmic.201800404 · Cited by 83
An updated review of autophagy in ischemic stroke: From mechanisms to therapies
Wang, X., Fang, Y., Huang, Q., Xu, P., Lenahan, C., Lü, J., Zheng, J., Dong, X., Shao, A., & Zhang, J. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113684 · Cited by 80
BNIP3 and Nix: Atypical regulators of cell fate
Field, J. T., & Gordon, J. W. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2022.119325 · Cited by 84
Autophagy in Toxicology: Cause or Consequence?
Orrenius, S., Kaminskyy, V. O., & Zhivotovsky, B. (2012) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-011112-140210 · Cited by 81
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
A time to reap, a time to sow: Mitophagy and biogenesis in cardiac pathophysiology
Andres, A. M., Stotland, A., Queliconi, B. B., & Gottlieb, R. A. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.10.003 · Cited by 78
“These proteins insert into the OMM and facilitate engulfment by the autophagosome through a LIR domain that can interact with LC3 isoforms including gamma-aminobutyric acid receptor-associated protein (GABARAP) and GABARAP-like 1 (GABARAPL1) [49, 50].”
BackgroundMeasuring Autophagy in Stressed Cells
Sharifi, M. N., Mowers, E. E., Drake, L. E., & Macleod, K. F. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2522-3_10 · Cited by 80
“Alternatively, LC3 interactions have been detected using protein cross-linking methods and yeast twohybrid screening [35].”
MethodMitochondrial quality control in AMD: does mitophagy play a pivotal role?
Hyttinen, J. M. T., Viiri, J., Kaarniranta, K., & Błasiak, J. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2843-7 · Cited by 82
Receptor Proteins in Selective Autophagy
Behrends, C., & Fulda, S. (2012) · International Journal of Cell Biology · doi:10.1155/2012/673290 · Cited by 79
“Nix functions as a mitophagy receptor in mammalian cells that mediates selective clearance of mitochondria [45].”
BackgroundThe Role of Mitophagy in Regulating Cell Death
Li, S., Zhang, J., Liu, C., Wang, Q., Yan, J., Hui, L., Jia, Q., Shan, H., Tao, L., & Zhang, M. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/6617256 · Cited by 76
“Like BNIP3, NIX also has key domains that can directly bind to Atg8/LC3 in the family-LIR domain as a receptor for autophagy machinery [64].”
BackgroundMechanism governing heme synthesis reveals a GATA factor/heme circuit that controls differentiation
Tanimura, N., Miller, E. C., Igarashi, K., Yang, D. T., Burstyn, J. N., Dewey, C. N., & Bresnick, E. H. (2015) · EMBO Reports · doi:10.15252/embr.201541465 · Cited by 79
Role of Autophagy in COPD Skeletal Muscle Dysfunction
Hussain, S. N. A., & Sandri, M. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00893.2012 · Cited by 77
“Recent studies have demonstrated that both BNIP3 and BNIP3L induce removal of mitochondria via autophagy and that this process is independent of changes in PTP opening; it is accomplished through direct binding of LC3B, which is followed by recruitment of growing autophagosomes to the mitochondria (28, 51).”
Selective Autophagy Receptors in Neuronal Health and Disease
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
Brennan, L., McGreal, R., Logan, C. M., Cvekl, A., Menko, A. S., & Kantorow, M. (2018) · Experimental Eye Research · doi:10.1016/j.exer.2018.06.003 · Cited by 75
“Previous work has determined that BNIP3L has weak affinity for LC3B but a much higher affinity for its homologues GABARAPL1 and GATE16 (Novak et al., 2010) suggesting that these proteins may participate in the BNIP3L-mediated elimination of lens fiber cell mitochondria, ER Fig.”
InfluentialMitochondrial Quality Control: Role in Cardiac Models of Lethal Ischemia-Reperfusion Injury
Kulek, A. R., Anzell, A. R., Wider, J. M., Sanderson, T. H., & Przyklenk, K. (2020) · Cells · doi:10.3390/cells9010214 · Cited by 78
The role of autophagy in cancer: from molecular mechanism to therapeutic window
Jalali, P., Shahmoradi, A., Samii, A., Mazloomnejad, R., Hatamnejad, M. R., Saeed, A., Namdar, A., & Salehi, Z. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1528230 · Cited by 89
Autophagy and mitophagy in the myocardium: therapeutic potential and concerns
Jimenez, R. E., Kubli, D. A., & Gustafsson, Å. B. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12477 · Cited by 77
“The resulting mature LC3-II resides on the autophagosome membrane and interacts with specific adapter proteins or receptors that are present on the cargo to be degraded (Geisler et al., 2010; Novak et al., 2010).”
BackgroundInfluentialAmadoro, G., Corsetti, V., Florenzano, F., Atlante, A., Bobba, A., Nicolin, V., Nori, S. L., & Calissano, P. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00018 · Cited by 77
Autophagy—from molecular mechanisms to clinical relevance
Lippai, M., & Szatmári, Z. (2016) · Cell Biology and Toxicology · doi:10.1007/s10565-016-9374-5 · Cited by 80
Xiang, G., Yang, L., Long, Q., Chen, K., Tang, H., Wu, Y., Liu, Z., Zhou, Y., Qi, J., Zheng, L., et al. (2017) · Autophagy · doi:10.1080/15548627.2017.1338545 · Cited by 77
Mitophagy and Mitochondrial Dysfunction in Cancer
Macleod, K. F. (2019) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030419-033405 · Cited by 76
Abnormal Mitochondrial Quality Control in Neurodegenerative Diseases
Yan, X., Wang, B., Hu, Y., Wang, S., & Zhang, X. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00138 · Cited by 74
Mitochondria: Insights into Crucial Features to Overcome Cancer Chemoresistance
Genovese, I., Carinci, M., Modesti, L., Aguiari, G., Pinton, P., & Giorgi, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094770 · Cited by 77
Mitochondria Autophagy in Yeast
Kanki, T., Klionsky, D. J., & Okamoto, K. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3762 · Cited by 77
“sequence that is identified as a yeast Atg8 and mammalian LC3 binding motif (62, 63).”
The Multifaceted Roles of Autophagy in Tumors—Implications for Breast Cancer
Debnath, J. (2011) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-011-9223-3 · Cited by 78
“The other major pathway implicated in mitophagy involves the two related BH3 family proteins, BNIP3 and NIX/BNIP3L, which promote mitochondrial clearance during reticulocyte development [78,95,97], and during hypoxia [81,104,114,115].”
Mitophagy in maintaining skeletal muscle mitochondrial proteostasis and metabolic health with ageing
Drake, J. C., & Yan, Z. (2017) · The Journal of Physiology · doi:10.1113/jp274337 · Cited by 76
“Importantly, expression of the BH3-only family protein Bnip3 (or the analogous, Nix), which plays a role in recognizing damaged mitochondria by facilitating docking of autophagosomes through binding to Lc3 (Novak et al. 2010), increases with both acute exercise and exercise training in mouse skeletal muscle (Jamart et…”
BackgroundInfluentialRahman, F. A., & Quadrilatero, J. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03807-9 · Cited by 77
Li, C., Duckney, P. J., Zhang, T., Fu, Y., Li, X., Kroon, J., Jaeger, G. D., Cheng, Y., Hussey, P. J., & Wang, P. (2022) · Nature Communications · doi:10.1038/s41467-022-33402-w · Cited by 78
Autophagy receptors in developmental clearance of mitochondria
Novak, I., & Đikić, I. (2011) · Autophagy · doi:10.4161/auto.7.3.14509 · Cited by 75
“We have recently described Nix (also named Bnip3L) as mammalian mitophagy receptor important for selective removal of damaged mitochondria as well as complete removal of mitochondria during reticulocyte maturation.(6) Nix-deficient mice develop anemia and severe reticulocytosis caused by inefficient loss of mitochondr…”
BackgroundMitochondrial quality control in the diabetic heart
Liang, Q., & Kobayashi, S. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.12.025 · Cited by 75
Mitophagy and DNA damage signaling in human aging
Babbar, M., Basu, S., Yang, B., Croteau, D. L., & Bohr, V. A. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111207 · Cited by 77
Role of Mitophagy in Cardiovascular Disease
Yang, Y., Li, T., Li, Z., Liu, N., Yan, Y., & Liu, B. (2020) · Aging and Disease · doi:10.14336/ad.2019.0518 · Cited by 74
“The Nterminal extends into the cytoplasm and is linked to LC3related molecules[51-53].”
BackgroundChen, Y.-Y., Wang, W., Che, L., Lan, Y., Zhang, L., Zhan, D.-L., Huang, Z., Lin, Z., & Lin, Y. (2020) · Cancers · doi:10.3390/cancers12030655 · Cited by 79
“Interestingly, the expression of HIF-1α target gene BNIP3L has been reported to cause mitochondrial dysfunction and cell death in breast tumors [15,16].”
BackgroundThe functions of Atg8-family proteins in autophagy and cancer: linked or unrelated?
Jacquet, M., Boyer‐Guittaut, M., Fraîchard, A., & Despouy, G. (2020) · Autophagy · doi:10.1080/15548627.2020.1749367 · Cited by 72
A brief overview of BNIP3L/NIX receptor‐mediated mitophagy
Marinković, M., & Novak, I. (2021) · FEBS Open Bio · doi:10.1002/2211-5463.13307 · Cited by 78
Galizzi, G., & Carlo, M. D. (2022) · Biology · doi:10.3390/biology11060943 · Cited by 77
Mitophagy Contributes to the Pathogenesis of Inflammatory Diseases
Zhao, Y., Huang, S., Liu, J., Wu, X., Zhou, S., Dai, K., & Kou, Y. (2018) · Inflammation · doi:10.1007/s10753-018-0835-2 · Cited by 74
TBK1 (TANK-binding kinase 1)-mediated regulation of autophagy in health and disease
Herhaus, L. (2021) · Matrix Biology · doi:10.1016/j.matbio.2021.01.004 · Cited by 71
Mitochondrial dynamics in cancer stem cells
Sessions, D. T., & Kashatus, D. F. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03773-2 · Cited by 75
NIX initiates mitochondrial fragmentation via DRP1 to drive epidermal differentiation
Simpson, C. L., Tokito, M. K., Uppala, R., Sarkar, M. K., Gudjonsson, J. E., & Holzbaur, E. L. F. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108689 · Cited by 74
“, 2018); these control removal of mitochondria from highly differentiated cells, such as erythrocytes (Diwan et al., 2007; Novak et al., 2010; Schweers et al., 2007).”
BackgroundPatergnani, S., Missiroli, S., Morciano, G., Perrone, M., Mantovani, C. M., Anania, G., Fiorica, F., Pinton, P., & Giorgi, C. (2021) · Cancers · doi:10.3390/cancers13225622 · Cited by 77
“However, the molecular mechanisms at the basis of mitophagy started to be unveiled in the early 2000s when it was demonstrated that, during the differentiative process, red blood cells [46–48] eliminate their mitochondria by a mechanism orchestrated by the OMM resident NIP3-like protein X (NIX/BNIP3L), which, thanks t…”
BackgroundThe Multifaceted Roles of Autophagy in Flavivirus-Host Interactions
Ke, P. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19123940 · Cited by 78
“In addition to the PINK1/Parkin-mediated mitophagy pathway, several outer mitochondrial membrane proteins, such as FUN14 domain-containing 1 (FUNDC1), BCL2/adenovirus E1B 19 kDa protein-interacting protein 3 (BNIP3), BCL2/adenovirus E1B 19 kDa protein-interacting protein 3-like (BNIP3L) and yeast ATG32, have been show…”
BackgroundJin, X., Zhu, L., Lu, S., Li, C., Bai, M., Xu, E., Shen, J.-D., & Li, Y. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175435 · Cited by 73
Jiang, B., Zhou, X., Yang, T., Wang, L., Feng, L., Wang, Z., Xu, J., Jing, W., Wang, T., Su, H., et al. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1088575 · Cited by 73
“The lack of NIX promotes the accumulation of injured mitochondria in cells, which leads to increase the apoptosis and developmental defects, but the signaling cascade of NIX-mediated mitochondrial autophagy is still unclear (32, 33).”
BackgroundMitochondrial responsibility in ageing process: innocent, suspect or guilty
López‐Lluch, G., Santos‐Ocaña, C., Sánchez-Alcázar, J. A., Fernández‐Ayala, D. J. M., Asencio, C., Rodríguez‐Aguilera, J. C., & Navas, P. (2015) · Biogerontology · doi:10.1007/s10522-015-9585-9 · Cited by 72
Fregno, I., & Molinari, M. (2018) · F1000Research · doi:10.12688/f1000research.13968.1 · Cited by 70
Vo, M. T., Smith, B. J., Nicholas, J., & Choi, Y. B. (2019) · Nature Communications · doi:10.1038/s41467-019-11164-2 · Cited by 70
Regulation of Innate Immune Responses by Autophagy: A Goldmine for Viruses
Pradel, B., Robert-Hebmann, V., & Espert, L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.578038 · Cited by 71
“In addition, there are other proteins involved in selective autophagy, such as NIP3 like protein X (NIX) in mitophagy (34).”
BackgroundBao, F., Zhou, L., Zhou, R., Huang, Q., Chen, J., Zeng, S., Wu, Y., Yang, L., Qian, S., Wang, M., et al. (2022) · Science Advances · doi:10.1126/sciadv.abk2376 · Cited by 70
ORP8 acts as a lipophagy receptor to mediate lipid droplet turnover
Pu, M., Zheng, W., Zhang, H., Wan, W., Peng, C., Chen, X., Liu, X., Xu, Z., Zhou, T., Sun, Q., et al. (2022) · Protein & Cell · doi:10.1093/procel/pwac063 · Cited by 76
“So far, many such receptors have been found to guide the encapsulation of mitochondria (Novak et al., 2010; Liu et al., 2012; Wei et al., 2017), endoplasmic reticulum (ER) (Khaminets et al.”
BackgroundTraditional Chinese medicine and mitophagy: A novel approach for cardiovascular disease management
Wang, J., Zou, J., Shi, Y., Zeng, N., Guo, D., Wang, H., Zhao, C., Luan, F., Zhang, X., & Sun, J. (2024) · Phytomedicine · doi:10.1016/j.phymed.2024.155472 · Cited by 75
Tan, S., Sun, Y., Li, S., Wu, H., & Ding, Y. (2025) · Bone Research · doi:10.1038/s41413-025-00460-x · Cited by 81
“68 Knocking down proliferator-activated receptor-γ coactivator-1 α (PGC-1 α ) can activate mitophagy by promoting the expression of BNIP3.”
InfluentialProteotoxicity: An underappreciated pathology in cardiac disease
Sandri, M., & Robbins, J. M. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.12.015 · Cited by 73
“Bnip3 and Bnip3L are BH3-only proteins localized at the outer membrane of the mitochondria after cellular stress, and reportedly bind directly to LC3, thereby recruiting the autophagosome to damaged mitochondria [71, 72] [71, 72].”
BackgroundEffects of NIX‐mediated mitophagy on ox‐LDL‐induced macrophage pyroptosis in atherosclerosis
Peng, X., Chen, H., Li, Y., Huang, D., Huang, B., & Sun, D. (2020) · Cell Biology International · doi:10.1002/cbin.11343 · Cited by 73
“NIX inhibits the activation of caspase‐1 and the maturation of IL‐1β induced by ox‐LDL in macrophages ox‐LDLs have been previously shown to trigger caspase‐1 activation and expression of proinflammatory cytokines, such as IL‐1β and IL‐18 inmacrophages (Novak et al., 2010).”
BackgroundInfluentialPINK1-dependent mitophagy is driven by the UPS and can occur independently of LC3 conversion
Rakovic, A., Ziegler, J., Mårtensson, C. U., Prasuhn, J., Shurkewitsch, K., König, P., Paulson, H. L., & Klein, C. (2019) · Cell Death & Differentiation · doi:10.1038/s41418-018-0219-z · Cited by 69
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, J., Abeliovich, H., Acevedo‐Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Kölner Universitäts PublikationsServer (Universität zu Köln) · doi:10.5167/uzh-131237 · Cited by 69
Research progress on the pharmacological effects of berberine targeting mitochondria
Fang, X., Wu, H., Wei, J., Miao, R., Zhang, Y., & Tian, J. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.982145 · Cited by 75
“NIX and BNIP3 can directly bind to LC3 through their BH3 domains to induce mitophagy (41, 42).”
BackgroundRole of mitochondria in pathogenesis and therapy of renal fibrosis
Zhao, X., Li, Y., Yu, J., Teng, H., Wu, S., Wang, Y., Zhou, H., & Li, F. (2024) · Metabolism · doi:10.1016/j.metabol.2024.155913 · Cited by 71
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
