Cited by 1,309Autophagy in Disease and TherapyUbiquitin and proteasome pathwaysCalcium signaling and nucleotide metabolism

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Nix is a selective autophagy receptor for mitochondrial clearance

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Novak, Ivana, Kirkin, Vladimir, McEwan, David G, Zhang, Ji, Wild, Philipp, Rozenknop, Alexis, Rogov, Vladimir, Löhr, Frank, Popovic, Doris, Occhipinti, Angelo, Reichert, Andreas S, Terzic, Janos, Dötsch, Volker, Ney, Paul A, Dikic, Ivan·2010·The EMBO Reports

DOI 10.1038/embor.2009.256PMC PMC2816619

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Abstract

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.

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Background
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Background
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Background
Mitophagy in human astrocytes treated with the antiretroviral drug Efavirenz: Lack of evidence or evidence of the lack
Arroyo, O., Gruevska, A., Víctor, V. M., González‐Polo, R. A., Yakhine-Diop, S. M. S., Fuentes, J. M., Esplugues, J. V., Blas‐García, A., & Apostolova, N. (2019) · Antiviral Research · doi:10.1016/j.antiviral.2019.04.015 · Cited by 11
Differential interaction between DARC and SDF-1 on erythrocytes and their precursors
Klei, T. R. L., Aglialoro, F., Mul, E. P. J., Tol, S., Ligthart, P. C., Seignette, I. M., Geissler, J., van den Akker, E., & van Bruggen, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-52186-6 · Cited by 10
Macroautophagy and Cell Responses Related to Mitochondrial Dysfunction, Lipid Metabolism and Unconventional Secretion of Proteins
Demine, S., Michel, S., Vannuvel, K., Wanet, A., Renard, P., & Arnould, T. (2012) · Cells · doi:10.3390/cells1020168 · Cited by 11
“As Atg32 (a yeast protein sharing UBA and LIR domains with the Nix protein), Nix may trigger phagophore elongation by interacting with LC3 by its LIR (LC3-interacting region) domain [47].”
Background
Mitochondria in Health and Disease
Meiliana, A., Dewi, N. M., & Wijaya, A. (2019) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v11i1.779 · Cited by 13
Mitophagy in yeast: known unknowns and unknown unknowns
Abeliovich, H. (2023) · Biochemical Journal · doi:10.1042/bcj20230279 · Cited by 11
From homeostasis to defense: Exploring the role of selective autophagy in innate immunity and viral infections
Huang, M., Zhang, W., Yang, Y., Shao, W., Wang, J., Cao, W., Zhu, Z., Yang, F., & Zheng, H. (2024) · Clinical Immunology · doi:10.1016/j.clim.2024.110169 · Cited by 9
Phospholipid Supply for Autophagosome Biogenesis
Isola, D., & Elazar, Z. (2024) · Journal of Molecular Biology · doi:10.1016/j.jmb.2024.168691 · Cited by 9
Prospective Intervention Strategies Between Skeletal Muscle Health and Mitochondrial Changes During Aging
Zhang, X., Liao, S., Huang, L., & Wang, J. (2024) · Advanced Biology · doi:10.1002/adbi.202400235 · Cited by 11
Mitochondrial Quality Control Orchestrates the Symphony of B Cells and Plays Critical Roles in B Cell‐Related Diseases
Li, W., Cai, P., Xu, Y., Tian, W., Jing, L., Lv, Q., Zhao, Y., Wang, H., & Shao, Q. (2024) · Journal of Immunology Research · doi:10.1155/2024/5577506 · Cited by 9
Selective autophagy: a therapeutic target for healthy aging?
Manastireanu, D. M., Salazar, N. A., Bejarano, E., & Nieto-Torres, J. L. (2024) · Aging advances. · doi:10.4103/agingadv.agingadv-d-24-00002 · Cited by 10
TFAM and Mitochondrial Protection in Diabetic Kidney Disease
Yu, S., Lü, X., Li, C., Han, Z., Li, Y., Zhang, X., & Guo, D. (2024) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s487815 · Cited by 10
Stressful situations: Molecular insights on mitochondrial quality control pathways
Romanelli, S., & Trempe, J. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110483 · Cited by 11
“NIX (also known as BNIP3L) and BNIP3 are receptors located on the OMM, where they bind to LC3 on the autophagosome, facilitating mitophagy (124, 125).”
Mitochondrial echoes in the bloodstream: decoding ccf-mtDNA for the early detection and prognosis of hepatocellular carcinoma
Chu, Y., Chen, W., Lin, W.-R., Lai, M. W., & Yeh, C. (2025) · Cell & Bioscience · doi:10.1186/s13578-025-01456-0 · Cited by 11
“Figure illustrated using BioRender engagement with ATG8 family proteins [33–42].”
Autophagy at the synapse, an early site of dysfunction in neurodegeneration
Jasutkar, H. G., & Yamamoto, A. (2023) · Current Opinion in Physiology · doi:10.1016/j.cophys.2023.100631 · Cited by 9
Mitophagy and spermatogenesis: Role and mechanisms
Rotimi, D. E., Iyobhebhe, M. E., Oluwayemi, E. T., Evbuomwan, I. O., Asaleye, R. M., Ojo, O. A., & Adeyemı, O. S. (2024) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2024.101698 · Cited by 11
“Among these proteins, BNIP3 and NIX interact with LC3 through their BH3 domains, which further promote mitophagy [21 – 23].”
Background
Dimorphic effect of TFE3 in determining mitochondrial and lysosomal content in muscle following denervation
Oliveira, A. N., Memme, J. M., Wong, J., & Hood, D. A. (2024) · Skeletal Muscle · doi:10.1186/s13395-024-00339-1 · Cited by 10
“A variety of mitophagic signaling pathways have been described, which all culminate in engulfment by the autophagosome and trafficking to the lysosome [24, 27–29].”
Background
Flow Cytometer Monitoring of Bnip3- and Bnip3L/Nix-Dependent Mitophagy
Šprung, M., Đikić, I., & Novak, I. (2017) · Methods in molecular biology · doi:10.1007/7651_2017_14 · Cited by 9
Detection of Iron Depletion- and Hypoxia-Induced Mitophagy in Mammalian Cells
Yamashita, S., & Kanki, T. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7831-1_18 · Cited by 9
Use of Peptide Arrays for Identification and Characterization of LIR Motifs
Rasmussen, M. S., Birgisdottir, Å. B., & Johansen, T. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-8873-0_8 · Cited by 7
Adaptation of Proteasomes and Lysosomes to Cellular Environments
Mebratu, Y. A., Negasi, Z. H., Dutta, S., Rojas, J., & Tesfaigzi, Y. (2020) · Cells · doi:10.3390/cells9102221 · Cited by 9
“Upon induced expression or activation by hypoxia, these receptors localize to OMM and through their LIR motifs directly induce both formation of autophagosomes and mitophagy [73,74].”
Background
Cellular and Mitochondrial Quality Control Mechanisms in Maintaining Homeostasis in Aging
Langeh, U., Kumar, V., Kumar, A., Kumar, P., Singh, C., & Singh, A. (2022) · Rejuvenation Research · doi:10.1089/rej.2022.0027 · Cited by 9
“57,58 Lipid-mediated mitophagy Lipids are also reported to be helpful to act as a signal to remove damaged mitochondria.”
Functional implications of mitochondrial reactive oxygen species generated by oncogenic viruses
Choi, Y. B., & Harhaj, E. W. (2014) · Frontiers in Biology · doi:10.1007/s11515-014-1332-0 · Cited by 11
“The BH3-only protein (BOP) NIX plays an important role as a mitophagy receptor in maturing murine reticulocytes by recruiting Atg8 family members LC3 and GABARAP to damaged mitochondria (Novak et al., 2010).”
Regulation of Autophagy by Protein Phosphorylation
Stork, B., Alers, S., Antje, S., & Wesselborg, S. (2012) · InTech eBooks · doi:10.5772/48502 · Cited by 8
“Examples are the mitochondrial protein NIX, which is a selective autophagy receptor for mitochondrial clearance, or Tecpr1, which binds Atg5 and WIPI-2 [184-186].”
Background
Methods for Mitochondria and Mitophagy Flux Analyses in Stem Cells of Resting and Regenerating Skeletal Muscle
García‐Prat, L., Martínez‐Vicente, M., & Muñoz‐Cánoves, P. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3810-0_16 · Cited by 9
Deregulated Expression of Mitochondrial Proteins Mfn2 and Bcnl3L in Placentae from Sheep Somatic Cell Nuclear Transfer (SCNT) Conceptuses
Czernik, M., Toschi, P., Zacchini, F., Iuso, D., & Ptak, G. (2017) · PLoS ONE · doi:10.1371/journal.pone.0169579 · Cited by 9
“Low expression of Nix negatively affects incorporation of damaged mitochondria into autophagosomes [36,37], resulting in abnormal cellular function.”
Background
Regulation of the Stress-Activated Degradation of Mitochondrial Respiratory Complexes in Yeast
Timón‐Gómez, A., Sanfeliu-Redondo, D., Pascual‐Ahuir, A., & Proft, M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00106 · Cited by 11
“These mechanisms involve outer mitochondrial mitophagy receptors such as Nix or FUNDC1, which are essential for mitophagic pathways induced during erythroid cell maturation (Sandoval et al., 2008; Novak et al., 2010) or by hypoxia (Liu et al., 2012; Wu et al., 2014), respectively.”
Background
Autophagy, Oxidative Stress, and Redox Regulation
Ma, J., Yang, L., Ren, J. T., & Yang, J. Z. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805253-2.00020-1 · Cited by 10
New insights into AtNBR1 as a selective autophagy cargo receptor in Arabidopsis
Lin, Y., Guo, R., Ji, C., Zhou, J. M., & Jiang, L. (2020) · Plant Signaling & Behavior · doi:10.1080/15592324.2020.1839226 · Cited by 9
Role of mitophagy in spinal cord ischemia-reperfusion injury
Duan, Y., Yang, F., Zhang, Y., Zhang, M., Shi, Y., Lang, Y., Sun, H., Wang, X., Jin, H., & Kang, X. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00668 · Cited by 8
The African swine fever virus p22 inhibits the JAK-STAT signaling pathway by promoting the TAX1BP1-mediated degradation of the type I interferon receptor
Ren, H., Wang, Y., Li, L., Shi, L.-F., Ma, Y., Fan, J.-H., Pan, X.-Y., Shao, H.-C., Zhang, Y., Han, S., et al. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1013319 · Cited by 11
“For instance, the autophagy receptor NIX interacts with LC3 via its LC3-interacting region (LIR) to induce mitophagy [57,58].”
PPA1 promotes oxidative phosphorylation and malignant progression of colorectal cancer under glucose restriction via AMPK/ULK1/FUNDC1-mediated mitophagy
Chen, Y., Deng, Q., Chen, Z., Yang, L., Li, X., & Fu, Z. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02816-y · Cited by 8
New perspective on neurodegenerative diseases: Focusing on the interaction between autophagy and oxidative stress and targeted strategies
Jin, J., Cen, Q., Wang, H., Xin, Y., Feng, J., Cui, Y., Li, J., You, Z., Jing, F., Yu, Y., et al. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107283 · Cited by 12
A novel modelling mechanism of PAEL receptor and GABARAPL2 interaction involved in Parkinson’s disease
Dutta, P., Dargahi, L., O’Connell, K. E., Bolia, A., Özkan, B., Sailer, A. W., & Dev, K. K. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.02.055 · Cited by 8
Selective Autophagy Regulates Innate Immunity Through Cargo Receptor Network
Wu, Y., & Cui, J. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-0606-2_9 · Cited by 9
β-arrestin1 inhibits hypoxic injury-induced autophagy in human pulmonary artery endothelial cells via the Akt/mTOR signaling pathway
Ning, H., Deng, J., Chen, F., Liu, Y., Kong, D., Shan, L., Zhang, Z., & Hu, T. (2020) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2020.105791 · Cited by 9
The molecular mechanisms and intervention strategies of mitophagy in cardiorenal syndrome
Yao, M., Liu, Y., Sun, M., Qin, S., Xin, W., Guan, X., Zhang, B., He, T., & Huang, Y. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1008517 · Cited by 8
Minimal adaptation of the molecular regulators of mitochondrial dynamics in response to unilateral limb immobilisation and retraining in middle-aged men
Pileggi, C. A., Hedges, C. P., D’Souza, R. F., Durainayagam, B. R., Zeng, N., Figueiredo, V. C., Hickey, A. J., Mitchell, C. J., & Cameron‐Smith, D. (2022) · European Journal of Applied Physiology · doi:10.1007/s00421-022-05107-x · Cited by 9
“Bcl-2 and adenovirus E1B 19 kDa-interacting protein 3 (BNIP3) and Bnip3-like (NIX) are receptor proteins that contain LC3 interacting regions (LIRs) on the outer mitochondrial membrane which can facilitate the encapsulation of mitochondria into autophagosomes through direct interactions with LC3BII (Novak et al. 2010;…”
Background
PACSIN2as a modulator of autophagy and mercaptopurine cytotoxicity: mechanisms in lymphoid and intestinal cells
Zudeh, G., Franca, R., Lucafò, M., Bonten, E. J., Bramuzzo, M., Sgarra, R., Lagatolla, C., Franzin, M., Evans, W. E., Decorti, G., et al. (2023) · Life Science Alliance · doi:10.26508/lsa.202201610 · Cited by 8
Role of TFEB and TFE3 in mediating lysosomal and mitochondrial adaptations to contractile activity in skeletal muscle myotubes
Oliveira, A. N., Tamura, Y., Memme, J. M., & Hood, D. A. (2023) · Mitochondrial Communications · doi:10.1016/j.mitoco.2023.10.001 · Cited by 8
Mechanisms of mitochondrial reorganization
Maruyama, T., Hama, Y., & Noda, N. N. (2023) · The Journal of Biochemistry · doi:10.1093/jb/mvad098 · Cited by 7

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: Novak, Ivana
Kirkin, Vladimir
McEwan, David G
Zhang, Ji
Wild, Philipp
Rogov, Vladimir
Löhr, Frank
Popovic, Doris
Reichert, Andreas S
Dötsch, Volker
Venue: The EMBO Reports
Publisher: Springer Science and Business Media LLC
Published: 2009-12-11
Volume: 11
Issue: 1
Pages: 45-51
ISSN: 1469-221X (ISSN-L)
1469-3178
DOI: 10.1038/embor.2009.256
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
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
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

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Nix is a selective autophagy receptor for mitochondrial clearance

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