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Newly born peroxisomes are a hybrid of mitochondrial and ER-derived pre-peroxisomes
Abstract
Peroxisomes function together with mitochondria in a number of essential biochemical pathways, from bile acid synthesis to fatty acid oxidation. Peroxisomes grow and divide from pre-existing organelles, but can also emerge de novo in the cell. The physiological regulation of de novo peroxisome biogenesis remains unclear, and it is thought that peroxisomes emerge from the endoplasmic reticulum in both mammalian and yeast cells. However, in contrast to the yeast system, a number of integral peroxisomal membrane proteins are imported into mitochondria in mammalian cells in the absence of peroxisomes, including Pex3, Pex12, Pex13, Pex14, Pex26, PMP34 and ALDP. Overall, the mitochondrial localization of peroxisomal membrane proteins in mammalian cells has largely been considered a mis-targeting artefact in which de novo biogenesis occurs exclusively from endoplasmic reticulum-targeted peroxins. Here, in following the generation of new peroxisomes within human patient fibroblasts lacking peroxisomes, we show that the essential import receptors Pex3 and Pex14 target mitochondria, where they are selectively released into vesicular pre-peroxisomal structures. Maturation of pre-peroxisomes containing Pex3 and Pex14 requires fusion with endoplasmic reticulum-derived vesicles carrying Pex16, thereby providing full import competence. These findings demonstrate the hybrid nature of newly born peroxisomes, expanding their functional links to mitochondria.
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“Peroxisomes have recently been shown to have a shared mitochondrial and endoplasmic reticulum (ER) origin, further linking the function of mitochondria and peroxisomes (Sugiura et al., 2017).”
From NAD+ in Brain Aging and Neurodegenerative Disorders (2019) · cites this paper as Sugiura et al., 2017
In the citing paper
“In de novo synthesis, mature peroxisomes are built incrementally, with the first step a budding of pre-peroxisomal vesicles bearing complementary proteins of the early import machinery, PEX16 and PEX3, from membranes of the endoplasmic reticulum and mitochondria, respectively (Schrader and Pellegrini, 2017; Sugiura et al., 2017). Heterotypic fusion of PEX3- and PEX16-bearing vesicles establish a”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Sugiura et al., 2017
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Connecting 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
“Thus Bak is yet another factor shared between peroxisomes and mitochondria (Sugiura et al., 2017).”
Mitochondrial Quality Control Mechanisms and the PHB (Prohibitin) Complex
Hernando‐Rodríguez, B., & Artal‐Sanz, M. (2018) · Cells · doi:10.3390/cells7120238 · Cited by 90
Peroxisomes control mitochondrial dynamics and the mitochondrion-dependent apoptosis pathway
Tanaka, H., Okazaki, T., Aoyama-Ishiwatari, S., Yokota, M., Koike, M., Okada, Y., Fujiki, Y., & Gotoh, Y. (2019) · Journal of Cell Science · doi:10.1242/jcs.224766 · Cited by 84
Lee, C., Nam, J. S., Lee, C. G., Park, M., Yoo, C., Rhee, H., Seo, J. K., & Kwon, T. (2021) · Nature Communications · doi:10.1038/s41467-020-20210-3 · Cited by 82
Peroxisomal ACBD4 interacts with VAPB and promotes ER-peroxisome associations
Costello, J. L., Castro, I. G., Schrader, T. A., Islinger, M., & Schrader, M. (2017) · Cell Cycle · doi:10.1080/15384101.2017.1314422 · Cited by 79
Xiao, J., Luo, J., Hu, A., Xiao, T., Li, M., Kong, Z., Jiang, L., Zhou, Z.-M., Liao, Y.-C., Xie, C., et al. (2019) · Science China Life Sciences · doi:10.1007/s11427-019-9569-9 · Cited by 80
Dysregulation of organelle membrane contact sites in neurological diseases
Kim, S., Coukos, R., Gao, F., & Krainc, D. (2022) · Neuron · doi:10.1016/j.neuron.2022.04.020 · Cited by 82
Mitochondrial-Derived Vesicles: The Good, the Bad, and the Ugly
Picca, A., Guerra, F., Calvani, R., Coelho‐Júnior, H. J., Landi, F., Bucci, C., & Marzetti, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241813835 · Cited by 81
“Their heterogeneity is reflected by the multiple processes in which they are involved, including mitochondrial fission, biogenesis of peroxisomes, resistance to oxidative stress and infections, and innate immunity signaling [11,28–31].”
One ring to bring them all and in the darkness bind them: The trafficking of heme without deliverers
Chambers, I. G., Willoughby, M. M., Hamza, I., & Reddi, A. R. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118881 · Cited by 77
VPS13D promotes peroxisome biogenesis
Baldwin, H. A., Wang, C., Kanfer, G., Shah, H. V., Velayos‐Baeza, A., Dulovic‐Mahlow, M., Brüggemann, N., Anding, A. L., Baehrecke, E. H., Maric, D., et al. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202001188 · Cited by 67
“In the absence of peroxisomes, several PEX proteins, such as PEX3, PEX12, PEX13, PEX26, and PEX14, mislocalize to mitochondria (Sugiura et al., 2017).”
InfluentialA PEX 5 missense allele preferentially disrupts PTS 1 cargo import into Arabidopsis peroxisomes
Patel, K. J., Kao, Y., Llinas, R. J., & Bartel, B. (2019) · Plant Direct · doi:10.1002/pld3.128 · Cited by 70
Ubiquitin ligase MARCH5 localizes to peroxisomes to regulate pexophagy
Zheng, J., Chen, X., Liu, Q., Zhong, G., & Zhuang, M. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202103156 · Cited by 68
Sensing the Stress: A Role for the UPRmt and UPRam in the Quality Control of Mitochondria
Callegari, S., & Dennerlein, S. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00031 · Cited by 58
“…the ER (Kornmann et al., 2009; Elbaz-Alon et al., 2015; Lewis et al., 2016; Cohen et al., 2017), but mitochondria are also in constant exchange with other organelles such as lysosomes (Raimundo, 2014; Diogo et al., 2017), lipid droplets (Nguyen et al., 2017), and peroxisomes (Sugiura et al., 2017).”
Peroxisomal dysfunction in neurodegenerative diseases
Jo, D. S., & Cho, D. (2019) · Archives of Pharmacal Research · doi:10.1007/s12272-019-01131-2 · Cited by 66
How oxygen gave rise to eukaryotic sex
Hörandl, E., & Speijer, D. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2706 · Cited by 63
The peroxisomal AAA-ATPase Pex1/Pex6 unfolds substrates by processive threading
Gardner, B. M., Castanzo, D. T., Chowdhury, S., Stjepanović, G., Stefely, M. S., Hurley, J. H., Lander, G. C., & Martin, A. (2018) · Nature Communications · doi:10.1038/s41467-017-02474-4 · Cited by 63
Peroxisomal Metabolite and Cofactor Transport in Humans
Chornyi, S., IJlst, L., van Roermund, C. W. T., Wanders, R. J. A., & Waterham, H. R. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.613892 · Cited by 64
Peroxisomal Stress Response and Inter-Organelle Communication in Cellular Homeostasis and Aging
Kim, J., & Bai, H. (2022) · Antioxidants · doi:10.3390/antiox11020192 · Cited by 64
“Furthermore, the same group recently demonstrated that MDVs fused with ER-derived pre-peroxisomes to form mature functional peroxisomes [18].”
BackgroundRole of PEX5 ubiquitination in maintaining peroxisome dynamics and homeostasis
Wang, W., & Subramani, S. E. (2017) · Cell Cycle · doi:10.1080/15384101.2017.1376149 · Cited by 59
“in mammalian cells shows that mature peroxisomes are formed through a hybrid of mitochondria- and ER- derived vesicles.(28)”
BackgroundThe Interplay between Antiviral Signalling and Carcinogenesis in Human Papillomavirus Infections
Ferreira, A., Ramalho, A. C., Marques, M., & Ribeiro, D. (2020) · Cancers · doi:10.3390/cancers12030646 · Cited by 60
“E7 was also reported to decrease the DNA binding activity of NF-κB and to reduce nuclear translocation and acetylation of the p65 subunit of NF-κB [82,116,117].”
BackgroundThe biochemical basis of mitochondrial dysfunction in Zellweger Spectrum Disorder
Nuebel, E., Morgan, J. T., Fogarty, S., Winter, J. M., Lettlová, S., Berg, J. A., Chen, Y.-C., Kidwell, C. U., Maschek, J. A., Clowers, K. J., et al. (2021) · EMBO Reports · doi:10.15252/embr.202051991 · Cited by 59
“Mitochondria not only share and complement peroxisomal roles in lipid metabolism and reactive oxygen species defense, but have also been shown to participate in peroxisome biogenesis in conjunction with the endoplasmic reticulum (ER) (Schrader & Yoon, 2007; Sugiura et al , 2017).”
Emerging roles of peroxisomes in viral infections
Ferreira, A., Marques, M., Ramos, B., Kagan, J. C., & Ribeiro, D. (2021) · Trends in Cell Biology · doi:10.1016/j.tcb.2021.09.010 · Cited by 55
Mitochondrial-derived vesicles: Gatekeepers of mitochondrial response to oxidative stress
Peng, T., Xie, Y., Sheng, H., Wang, C., Lian, Y., & Xie, N. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.06.233 · Cited by 57
Endosymbiotic selective pressure at the origin of eukaryotic cell biology
Raval, P. K., Garg, S. G., & Gould, S. B. (2022) · eLife · doi:10.7554/elife.81033 · Cited by 60
“De novo biosynthesis of peroxisomes involves MDVs with integrated Pex3 and Pex14 that fuse with ER- derived vesicles containing Pex16 (Sugiura et al., 2017), and the compartment for beta- oxidation appears absent in species lacking respiring mitochondria (Le et al., 2020).”
InfluentialParkin‐mediated ubiquitylation redistributes MITOL/March5 from mitochondria to peroxisomes
Koyano, F., Yamano, K., Kosako, H., Kimura, Y., Kimura, M., Fujiki, Y., Tanaka, K., & Matsuda, N. (2019) · EMBO Reports · doi:10.15252/embr.201947728 · Cited by 56
Prefused lysosomes cluster on autophagosomes regulated by VAMP8
Chen, Q., Hao, M., Wang, L., Li, L., Chen, Y., Shao, X., Tian, Z., Pfuetzner, R. A., Zhong, Q., Brünger, A. T., et al. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-04243-0 · Cited by 58
The MFN1 and MFN2 mitofusins promote clustering between mitochondria and peroxisomes
Huo, Y., Sun, W., Shi, T., Gao, S., & Zhuang, M. (2022) · Communications Biology · doi:10.1038/s42003-022-03377-x · Cited by 59
“The chosen human outer mitochondrial membrane protein Tom20 (full length) was genetically fused with N terminus of Venus fluorescent protein (1-154), the transmembrane fragment of peroxisomal membrane protein PEX26 (237-305) was genetically fused with the C terminus of Venus fluorescent protein (155-238).”
MethodDaily mitochondrial dynamics in cone photoreceptors
Giarmarco, M. M., Brock, D. C., Robbings, B. M., Cleghorn, W. M., Tsantilas, K. A., Kuch, K. C., Ge, W., Rutter, K. M., Parker, E. D., Hurley, J. B., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2007827117 · Cited by 57
“We did not investigate their composition, but they resemble osmiophilic structures observed in and around mitochondria of other cells, proposed to have roles in lipid metabolism (figure 8 (97, 98), and peroxisome synthesis (99).”
Archaeal Histone Contributions to the Origin of Eukaryotes
Brunk, C. F., & Martin, W. F. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.04.002 · Cited by 55
Peroxisome Plasticity at the Virus–Host Interface
Cook, K. C., Moreno, J. A., Beltran, P. M. J., & Cristea, I. M. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.06.006 · Cited by 55
Mitochondrial adventures at the organelle society
Diogo, C. V., Yambire, K. F., Fernández-Mosquera, L., Fonseca, T. B., & Raimundo, N. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.04.124 · Cited by 55
Nury, T., Sghaier, R., Zarrouk, A., Ménétrier, F., Uzun, T., Leoni, V., Caccia, C., Meddeb, W., Namsi, A., Sassi, K., et al. (2018) · Biochimie · doi:10.1016/j.biochi.2018.07.009 · Cited by 54
A PEROXO-Tag Enables Rapid Isolation of Peroxisomes from Human Cells
Ray, G. J., Boydston, E. A., Shortt, E., Wyant, G. A., Lourido, S., Chen, W. W., & Sabatini, D. M. (2020) · iScience · doi:10.1016/j.isci.2020.101109 · Cited by 49
“This mitochondrial signal is potentially a result of native mitochondrial-peroxisomal contacts (23), transfer of mitochondrial material to peroxisomes via mitochondrial-derived vesicles (24, 25), and/or the contribution of mitochondria to the de novo synthesized pool of peroxisomes (26).”
BackgroundBülow, M. H., Wingen, C., Senyilmaz, D., Gosejacob, D., Sociale, M., Bauer, R., Schulze, H., Sandhoff, K., Teleman, A. A., Hoch, M., et al. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-08-0535 · Cited by 52
“Third, increased free fatty acid levels can harm mitochondria for a number of reasons, among them their effect on membrane permeability with mitochondrial swelling as a possible result (Sultan and Sokolove, 2001; Schönfeld and Reiser, 2013).”
Background
Metadata
- Authors
- Sugiura, A., Mattie, S., Prudent, J., & McBride, H. M.
- Affiliations
- Montreal Neurological Institute and Hospital (CA)
- Corresponding author
- McBride, Heidi M.
- Venue
- Nature
- Published
- 2017-02-01
- Volume
- 542
- Issue
- 7640
- Pages
- 251-254
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2585343016
- Cited by
- 386
- References
- 38
- Citations by year
- 2026: 26 · 2025: 25 · 2024: 26 · 2023: 42 · 2022: 47 · 2021: 46 · 2020: 42 · 2019: 44 · 2018: 53 · 2017: 34
- FWCI
- 25.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- peroxisome biogenesis, PEX3, PEX14, PEX16, PEX12, PEX13, ALDP, peroxisomal membrane proteins, mitochondrial targeting, endoplasmic reticulum
- MeSH terms
- Peroxins, Bacterial Proteins, Organelle Biogenesis, Cell Line, Endoplasmic Reticulum, Fibroblasts, Humans, Intracellular Membranes, Lipoproteins, Luminescent Proteins, Membrane Proteins, Mitochondria, Repressor Proteins, Zellweger Syndrome, Peroxisomes, Protein Transport
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