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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.
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“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]
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“…under certain physiological conditions, such as hypoxia, mitophagy can also be initiated via mitophagy receptors, including NIX, BNIP3, FUNDC1, Bcl2L13, Prohibitin 2, and FKBP8 (Zhang & Ney, 2009; Novak et al, 2010; Liu et al, 2012; Murakawa et al, 2015; Bhujabal et al, 2017; Wei et al, 2017).”
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“These include Bcl-2/adenovirus E1B 19 kDa-interacting protein 3 (BNIP3) [177]; BNIP3-like protein (BNIP3L/NIX) [178]; UN14 domain-containing 1 (FUNDC1) [179]; B-cell lymphoma 2-like protein 13 (Bcl2-L-13) [180]; FK506-binding protein 8 (FKBP8) [181]; prohibitin-2 (PHB-2) [182]; and cardiolipin…”
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Wu, H., & Chen, Q. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6204 · Cited by 119
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BackgroundMitophagy for cardioprotection
Titus, A. S., Sung, E., Zablocki, D., & Sadoshima, J. (2023) · Basic Research in Cardiology · doi:10.1007/s00395-023-01009-x · Cited by 128
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Stotland, A. B., & Gottlieb, R. A. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.12.041 · Cited by 123
“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) [60,61].”
BackgroundAutophagy and Mammalian Viruses
Paul, P., & Münz, C. (2016) · Advances in virus research · doi:10.1016/bs.aivir.2016.02.002 · Cited by 119
“Not surprisingly, alternative mechanisms have been described involving the autophagy receptors NIX, BNIP3 and FUNDC1 (Liu et al., 2012;Novak et al., 2010;Quinsay et al., 2010).”
BackgroundCytoplasmic DAXX drives SQSTM1/p62 phase condensation to activate Nrf2-mediated stress response
Yang, Y., Willis, T. L., Button, R. W., Strang, C. J., Fu, Y., Wen, X., Grayson, P. R. C., Evans, T., Sipthorpe, R. J., Roberts, S. L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11671-2 · Cited by 115
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“dria (NIX) [43], as well as for ubiquitinated protein aggregates (p62 and NBR1, described below) [44–46].”
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Iriondo, M. N., Etxaniz, A., Varela, Y. R., Ballesteros, U., Hervás, J. H., Montes, L. R., Goñi, F. M., & Alonso, A. (2022) · Autophagy · doi:10.1080/15548627.2022.2062111 · Cited by 118
“(B) Sequence alignment of the human orthologs of Atg8 obtained with Clustal W. LC3A (Q9GZQ8), LC3B (Q9GZQ8), LC3C (Q9BXW4), GABARAP (O95166), GABARAPL1 (Q9H0R8) and GABARAPL2 (P60520).”
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GABARAPL1 (GEC1) associates with autophagic vesicles
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A short linear motif in BNIP3L (NIX) mediates mitochondrial clearance in reticulocytes
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“NIX was recently identified as mitophagy receptor in mammalian cells (Novak et al. 2010).”
BackgroundYamaguchi, M., Noda, N. N., Nakatogawa, H., Kumeta, H., Ohsumi, Y., & Inagaki, F. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.113670 · Cited by 110
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“Mammalian NIX (NIP3-like protein X), Bnip3, FUNDC1 and yeast Atg32 localize to the mitochondrial outer membrane, where they are anchored by transmembrane domains and mediate selective clearance of mitochondria through LIR-dependent interaction with ATG8 family proteins [11–15] (Figure 2).”
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Meng, Y., Qiu, L., Zeng, X., Hu, X., Zhang, Y., Wan, X., Mao, X., Wu, J., Xu, Y., Xiong, Q., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01253-y · Cited by 116
“Additionally, growing evidence indicates that FUN14 domain-containing protein 1 (FUNDC1) could be a mitophagy receptor controlled by phosphorylation by ULK1 on S17,(58) and NIX serves as a selective autophagy receptor that facilitates the recruitment of LC3/GABARAP for mitochondrial clearance.(59) Our results indicate…”
BackgroundThe Interrelation between Reactive Oxygen Species and Autophagy in Neurological Disorders
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Qian, L., Nasab, E. M., Athari, S. M., & Athari, S. S. (2022) · Journal of Investigative Medicine · doi:10.1136/jim-2021-002098 · Cited by 117
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“A trio of kinases, specifically PINK1, TBK1, and ULK1, orchestrate three feedback amplification circuits governing mitophagy [61].”
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Božić, M., van den Bekerom, L., Milne, B. A., Goodman, N., Roberston, L., Prescott, A. R., Macartney, T., Dawe, N., & McEwan, D. G. (2020) · EMBO Reports · doi:10.15252/embr.201948412 · Cited by 112
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“In that context, NIX may function as a mitochondrial receptor for autophagy by interacting with LC3 [20].”
BackgroundUbiquitin and Receptor-Dependent Mitophagy Pathways and Their Implication in Neurodegeneration
Fritsch, L. E., Moore, M. E., Sarraf, S. A., & Pickrell, A. M. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.10.015 · Cited by 106
“cyanide m-chlorophenylhydrazone (CCCP), the NIX and LC3 interaction increased, indicating a possible mechanism for mitophagy regulation [135].”
BackgroundRegulation and function of mitophagy in development and cancer
Lu, H., Li, G., Liu, L., Feng, L., Wang, X., & Jin, H. (2013) · Autophagy · doi:10.4161/auto.26550 · Cited by 107
“Indeed, BNIP3L has been verified as a mitophagy receptor in mammalian cells.(80) It is anchored at the OMM and contains a WXXL motif near its N terminus facing the cytosol, which binds to the mammalian homolog of Atg8, LC3, and the LC3 homolog GABARAP.”
BackgroundInfluentialAutophagy facilitates organelle clearance during differentiation of human erythroblasts
Betin, V. M. S., Singleton, B. K., Parsons, S. F., Anstee, D. J., & Lane, J. D. (2013) · Autophagy · doi:10.4161/auto.24172 · Cited by 109
Precision autophagy directed by receptor regulators – emerging examples within the TRIM family
Kimura, T., Mandell, M. A., & Deretic, V. P. (2016) · Journal of Cell Science · doi:10.1242/jcs.163758 · Cited by 106
“During reticulocyte development, Nix (also known as BNIP3L) appears to be the receptor for mitophagy (Sandoval et al., 2008; Schwarten et al., 2009; Novak et al., 2010).”
BackgroundHow to get rid of mitochondria: crosstalk and regulation of multiple mitophagy pathways
Zimmermann, M., & Reichert, A. S. (2017) · Biological Chemistry · doi:10.1515/hsz-2017-0206 · Cited by 104
Praharaj, P. P., Naik, P. P., Panigrahi, D. P., Bhol, C. S., Mahapatra, K. K., Patra, S., Sethi, G., & Bhutia, S. K. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2990-x · Cited by 104
Ordureau, A., Kraus, F., Zhang, J., An, H., Park, S., Ahfeldt, T., Paulo, J. A., & Harper, J. W. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.10.001 · Cited by 104
Proteolytic control of mitochondrial function and morphogenesis
Anand, R., Langer, T., & Baker, M. J. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.06.025 · Cited by 113
Autophagy and polyglutamine diseases
Jiménez-Sánchez, M., Thomson, F., Zavodszky, E., & Rubinsztein, D. C. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.08.013 · Cited by 105
“In higher eukaryotes, a similar cargo receptor function for mitophagy has been attributed to Nix/Bni3L (Schweers et al., 2007; Sandoval et al., 2008; Novak et al., 2010).”
MacVicar, T., & Lane, J. D. (2014) · Journal of Cell Science · doi:10.1242/jcs.144337 · Cited by 108
“This correlated with a dramatic stimulation of basal autophagy and required Nix/BNIP3L, as well as recruitment of the small GTPase Rheb to the OMM (Melser et al., 2013).”
BackgroundQuality Control in Neurons: Mitophagy and Other Selective Autophagy Mechanisms
Evans, C. S., & Holzbaur, E. L. F. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.031 · Cited by 109
“Structurally, NIX/BNIP3L is anchored to the OMM via a C-terminal transmembrane domain and interacts with multiple mATG8s, such as LC3 and GABA type A receptor-associated protein (GABARAP), through a N-terminus LIR domain [22, 104].”
BackgroundMa, Z., Bai, J., Jiang, C., Zhu, H., Liu, D., Pan, M., Wang, X., Pi, J., Jiang, P., & Liu, X. (2022) · Autophagy · doi:10.1080/15548627.2022.2139921 · Cited by 104
“Also, recent studies have uncovered autophagy as a selective degradation system when delivering substrates, such as damaged organelles or aggregated proteins, to autophagosomes for lysosomal degradation via cargo receptors, including SQSTM1/p62 (sequestosome 1), NBR1 (NBR1 autophagy cargo receptor), OPTN (optineurin),…”
BackgroundRole of autophagy, SQSTM1, SH3GLB1, and TRIM63 in the turnover of nicotinic acetylcholine receptors
Khan, M. M., Strack, S., Wild, F., Hanashima, A., Gasch, A., Brohm, K., Reischl, M., Carnio, S., Labeit, D., Sandri, M., et al. (2013) · Autophagy · doi:10.4161/auto.26841 · Cited by 106
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
Inhibition of Autophagy by a Small Molecule through Covalent Modification of the LC3 Protein
Fan, S., Yue, L., Wan, W., Zhang, Y., Zhang, B., Otomo, C., Li, Q., Lin, T., Hu, J., Xu, P., et al. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202109464 · Cited by 101
Autophagy in neuronal cells: general principles and physiological and pathological functions
Daμμe, M., Suntio, T., Säftig, P., & Eskelinen, E. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1361-4 · Cited by 109
“BNIP3L and FUNDC1 are integral membrane proteins of the mitochondrial outer membrane and interact with LC3 in order to mediate hypoxia-induced mitophagy [132, 169].”
Structural basis for phosphorylation-triggered autophagic clearance of Salmonella
Rogov, V. V., SUZUKI, H., Fiškin, E., Wild, P. S., Kniss, A., Rozenknop, A., Kato, R., Kawasaki, M., McEwan, D. G., Löhr, F., et al. (2013) · Biochemical Journal · doi:10.1042/bj20121907 · Cited by 101
Characterization of the Interaction of GABARAPL-1 with the LIR Motif of NBR1
Rozenknop, A., Rogov, V. V., Rogova, N. Y., Löhr, F., Güntert, P., Đikić, I., & Dötsch, V. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.05.003 · Cited by 102
“To investigate whether a higher number of negatively charged amino acids could compensate for the substitutionof tryptophanwith tyrosine,we extended the stretch of negatively charged amino acids directly N-terminal to Y732 in NBR1.”
BackgroundMethodInfluentialThe complex interplay between autophagy, apoptosis, and necrotic signals promotes T‐cell homeostasis
Walsh, C. M., & Edinger, A. L. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00919.x · Cited by 99
“to recruit LC3 to mitochondria causing their targeting to autophagosomes, similar to how p62 functions in the clearance of ubiquitinated protein aggregates (32, 77).”
BackgroundMitophagy in yeast: Molecular mechanisms and physiological role
Kanki, T., Furukawa, K., & Yamashita, S. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.01.005 · Cited by 108
Tang, F., Wang, B., Li, N., Wu, Y., Jia, J., Suo, T., Chen, Q., Liu, Y., & Tang, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024367 · Cited by 99
“NIX was proposed as a counterpart of Atg32 in higher organisms because it binds LC3/GABARAP and mediates mitochondrial clearance in murine reticulocytes[71,72].”
BackgroundModulating Mitophagy in Mitochondrial Disease
Dombi, E., Mortiboys, H., & Poulton, J. (2017) · Current Medicinal Chemistry · doi:10.2174/0929867324666170616101741 · Cited by 100
Ribosome Abundance Control Via the Ubiquitin–Proteasome System and Autophagy
An, H., & Harper, J. W. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.001 · Cited by 104
“For example, mitochondria are removed through a form of selective autophagy involving specific autophagy receptors on the mitochondrial outer membrane [50-52].”
BackgroundAutophagic pathways in Parkinson disease and related disorders
Xilouri, M., & Stefanis, L. (2011) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399411001803 · Cited by 100
“Immunology 10, 1215-1221 28 Novak, I. et al. (2010) Nix is a selective autophagy”
BackgroundWohlgemuth, S. E., Calvani, R., & Marzetti, E. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.03.007 · Cited by 97
“Interestingly, NIX not only controls Parkin translocation to mitochondria [86], but also possesses a LC3/GABARAP-interacting region that recruits autophagosomal membranes to mitochondria via LC3-binding [88].”
BackgroundMolecular signaling toward mitophagy and its physiological significance
Feng, D., Liu, L., Zhu, Y., & Chen, Q. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.03.034 · Cited by 99
“Several mitophagy receptors have been reported, including ATG32 in yeast [1,2], NIX/BNIP3L [3], BNIP3 [4], and the newly identified fun14 domain-containing protein 1 (FUNDC1) in mammalian cells [5].”
BackgroundInfluentialMitochondrial Metabolism in Acute Kidney Injury
Clark, A. J., & Parikh, S. M. (2020) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2020.01.002 · Cited by 97
BNIP3L/NIX regulates both mitophagy and pexophagy
Wilhelm, L. P., Zapata‐Muñoz, J., Villarejo‐Zori, B., Pellegrin, S., Freire, C. M., Toye, A. M., Boya, P., & Ganley, I. G. (2022) · The EMBO Journal · doi:10.15252/embj.2022111115 · Cited by 98
“Both mitochondria and peroxisomes were found in LC3-positive structures, but rarely were all three colocalised together (see white arrowhead in Fig 5A).”
BackgroundInfluentialDuan, W., Li, Y.-F., Liu, F., Deng, J., Wu, Y., Yuan, W., Tsoi, B., Chen, J., Wang, Q., Cai, S., et al. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.03.022 · Cited by 95
Sensing, signaling and surviving mitochondrial stress
Eckl, E.-M., Ziegemann, O., Krumwiede, L., Fessler, E., & Jae, L. T. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03887-7 · Cited by 93
“These receptors include Bcl2 like protein 13 (BCL2L13) [284], a mammalian homolog of the yeast mitophagy receptor Atg32, FK506 binding protein 8 (FKBP8) [285], FUN14 domain containing 1 (FUNDC1) [286], BH3-only Bcl-2 family protein (BNIP3) [287] and its homolog Nip3-like protein (NIX/BNIP3L) [288], nucleotide-binding…”
BackgroundBnip3 as a Dual Regulator of Mitochondrial Turnover and Cell Death in the Myocardium
Gustafsson, Å. B. (2011) · Pediatric Cardiology · doi:10.1007/s00246-010-9876-5 · Cited by 101
“separate investigations recently reported that Nix interacts with the autophagy proteins LC3 and GABARAP [35, 42].”
BackgroundKirkin, V., & Đikić, I. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.10.004 · Cited by 95
What to Eat: Evidence for Selective Autophagy in PlantsF
Floyd, B. E., Morriss, S. C., MacIntosh, G. C., & Bassham, D. C. (2012) · Journal of Integrative Plant Biology · doi:10.1111/j.1744-7909.2012.01178.x · Cited by 95
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
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