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Metabolic Interplay between Peroxisomes and Other Subcellular Organelles Including Mitochondria and the Endoplasmic Reticulum
Open accessAbstract
Peroxisomes are unique subcellular organelles which play an indispensable role in several key metabolic pathways which include: (1.) etherphospholipid biosynthesis; (2.) fatty acid beta-oxidation; (3.) bile acid synthesis; (4.) docosahexaenoic acid (DHA) synthesis; (5.) fatty acid alpha-oxidation; (6.) glyoxylate metabolism; (7.) amino acid degradation, and (8.) ROS/RNS metabolism. The importance of peroxisomes for human health and development is exemplified by the existence of a large number of inborn errors of peroxisome metabolism in which there is an impairment in one or more of the metabolic functions of peroxisomes. Although the clinical signs and symptoms of affected patients differ depending upon the enzyme which is deficient and the extent of the deficiency, the disorders involved are usually (very) severe diseases with neurological dysfunction and early death in many of them. With respect to the role of peroxisomes in metabolism it is clear that peroxisomes are dependent on the functional interplay with other subcellular organelles to sustain their role in metabolism. Indeed, whereas mitochondria can oxidize fatty acids all the way to CO2 and H2O, peroxisomes are only able to chain-shorten fatty acids and the end products of peroxisomal beta-oxidation need to be shuttled to mitochondria for full oxidation to CO2 and H2O. Furthermore, NADH is generated during beta-oxidation in peroxisomes and beta-oxidation can only continue if peroxisomes are equipped with a mechanism to reoxidize NADH back to NAD(+), which is now known to be mediated by specific NAD(H)-redox shuttles. In this paper we describe the current state of knowledge about the functional interplay between peroxisomes and other subcellular compartments notably the mitochondria and endoplasmic reticulum for each of the metabolic pathways in which peroxisomes are involved.
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“All of these metabolites must be transferred into mitochondria for full β-oxidation into CO2 and H2O because peroxisomes lack a Krebs’ cycle [162].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [162]
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“Peroxisomes are oxidative organelles present in all tissues and organisms [83, 84, 102, 103] and are involved in several anabolic and catabolic reactions, including the following: the degradation of long- and very long-chain fatty acids (LCFA, VLCFA (C ≥ 22:0), respectively) by α- or β-oxidation and hydrogen peroxide…”
BackgroundInfluentialCellular Compartmentation and the Redox/Nonredox Functions of NAD +
Kulkarni, C. A., & Brookes, P. S. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2018.7722 · Cited by 68
“We focus on the cytosolic, mitochondrial, and nuclear compartments, since these are the most studied, with NAD(H) in other compartments such as endoplasmic reticulum (ER) or peroxisomes being beyond the scope of this review [see (166) for review].”
BackgroundHuman milk microbiota associated with early colonization of the neonatal gut in Mexican newborns
Corona-Cervantes, K., García‐González, I., Villalobos-Flores, L. E., Hernández-Quiroz, F., Piña-Escobedo, A., Hoyo‐Vadillo, C., Rangel-Calvillo, M. N., & Garcı́a-Mena, J. (2020) · PeerJ · doi:10.7717/peerj.9205 · Cited by 62
Regulating peroxisome–ER contacts via the ACBD5-VAPB tether by FFAT motif phosphorylation and GSK3β
Kors, S., Hacker, C., Bolton, C., Maier, R., Reimann, L., Kitchener, E. J. A., Warscheid, B., Costello, J. L., & Schrader, M. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202003143 · Cited by 62
Kuna, R. S., Kumar, A., Gálvez, H., Wessendorf-Rodriguez, K. A., Green, C. R., McGregor, G. H., Cordes, T., Shaw, R. J., Svensson, R. U., & Metallo, C. M. (2023) · Science Advances · doi:10.1126/sciadv.adf0138 · Cited by 63
Achar, P. N., Quyen, P. T. T., Adukwu, E. C., Sharma, A., Msimanga, H. Z., Nagaraja, H., & Sreenivasa, M. Y. (2020) · Journal of Fungi · doi:10.3390/jof6040383 · Cited by 63
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
“Peroxisomes are the major site for both the production and degradation of hydrogen peroxide (H2O2) due to their high content of peroxisomal oxidases and antioxidant enzymes, such as catalase.”
BackgroundInfluentialKumar, V., Singh, D. D., Lakhawat, S. S., Yasmeen, N., Pandey, A., & Singla, R. K. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/6852276 · Cited by 64
“)e obese individual tends to depend upon glucose oxidation more than fatty acid oxidation revealing that mitochondrial fatty acid oxidation is compromised [67].”
BackgroundRole of Fatty Acids β-Oxidation in the Metabolic Interactions Between Organs
Panov, A. V., Mayorov, V., & Dikalov, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252312740 · Cited by 63
“Phytanic acid initially activates phytanyl CoA; then, phytanyl CoA hydroxylase ( α -hydroxylase), encoded by the PHYH gene, introduces a hydroxyl group to the alpha carbon [48].”
Lipids, lysosomes and mitochondria: insights into Lewy body formation from rare monogenic disorders
Erskine, D., Koss, D. J., Korolchuk, V. I., Outeiro, T. F., Attems, J., & McKeith, I. G. (2021) · Acta Neuropathologica · doi:10.1007/s00401-021-02266-7 · Cited by 58
“For example, there is considerable evidence of mitochondrial respiratory chain dysfunction in LBD, but relatively little is known about peroxisomal function, despite their role in degrading very long chain fatty acids for mitochondrial β-oxidation and scavenging ROS placing them at a potentially pivotal juncture betwe…”
BackgroundHelf, M. J., Fox, B. W., Artyukhin, A. B., Zhang, Y. K., & Schroeder, F. C. (2022) · Nature Communications · doi:10.1038/s41467-022-28391-9 · Cited by 59
Chronic acidosis rewires cancer cell metabolism through PPARα signaling
Rolver, M. G., Holland, L. K. K., Ponniah, M., Prasad, N. S., Yao, J., Schnipper, J., Kramer, S. H., Elingaard-Larsen, L. O., Pedraz‐Cuesta, E., Liu, B., et al. (2022) · International Journal of Cancer · doi:10.1002/ijc.34404 · Cited by 58
“34 Accord-ingly, a striking number of peroxisomal genes were upregulated in AA cells, including Peroxisomal biogenesis factor 5 (PEX5), PEX11A, other PEX isoforms, and acyl-coenzyme A oxidase 1 (ACOX1), the main enzyme responsible for peroxisomal oxidation of VLCFAs 34 (Figures 3A and S6 and Tables S1 and S2).”
BackgroundInfluentialChirumbolo, S., & Bjørklund, G. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18010165 · Cited by 55
“Furthermore, a metabolic interplay exists between peroxisomes and other intracellular organelles, whereby peroxisomes are involved in the ROS/RNS metabolism [60].”
BackgroundThe translational regulator FMRP controls lipid and glucose metabolism in mice and humans
Leboucher, A., Pisani, D. F., Martinez-Gili, L., Chilloux, J., Bermudez-Martin, P., Van Dijck, A., Ganief, T., Macek, B., Becker, J. A. J., Le Merrer, J., et al. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.01.002 · Cited by 56
“Furthermore, overabundance of the FA transporter Abcd3 and of the aldehyde dehydrogenase Aldh3a2 could also be indicative of increased peroxisomal b-oxidation of lipids [53].”
BackgroundFarrugia, M. A., & Puglielli, L. (2018) · Journal of Cell Science · doi:10.1242/jcs.221747 · Cited by 52
“, 2001), the peroxisome (Wanders et al., 2015), the nucleus”
Che, X., Brydges, C. R., Yu, Y., Price, A., Joshi, S., Roy, A., Lee, B., Barupal, D. K., Cheng, A., Palmer, D. M., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23147906 · Cited by 52
“Peroxisomal β-oxidation of very long-chain fatty acids leads to their breakdown into short-chain products that serve as substrates for mitochondrial β-oxidation [34].”
BackgroundNury, 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
Bülow, 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
“…measured as the amount of oxygen consumption (in the presence of palmitoyl-CoA substrate, the necessary TCA cycle intermediates, and ADP, i.e., state 3 respiration) that is sensitive to etomoxir, a standard carnitine palmitoyl transferase (CPT-I) inhibitor (Kuznetsov et al., 2008; Xu et al., 2012).”
BackgroundPI5P4Ks drive metabolic homeostasis through peroxisome-mitochondria interplay
Ravi, A., Palamiuc, L., Loughran, R. M., Triscott, J., Arora, G. K., Kumar, A., Tieu, V., Pauli, C., Reist, M., Lew, R. J., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.04.019 · Cited by 53
Ghareghani, M., Scavo, L., Jand, Y., Farhadi, N., Sadeghi, H., Ghanbari, A., Mondello, S., Arnoult, D., Gharaghani, S., & Zibara, K. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00147 · Cited by 48
“Indeed, FAs are converted to acetyl-carnitine which is then exported to cytosol where it can be converted to acetyl-CoA, to be used again as a substrate in FA and cholesterol synthesis (Wanders et al., 2015).”
BackgroundMolecular insights into peroxisome homeostasis and peroxisome biogenesis disorders
Fujiki, Y., Okumoto, K., Honsho, M., & Abe, Y. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2022.119330 · Cited by 47
Intracellular to Interorgan Mitochondrial Communication in Striated Muscle in Health and Disease
Boardman, N. T., Trani, G., Scalabrin, M., Romanello, V., & Wüst, R. C. I. (2023) · Endocrine Reviews · doi:10.1210/endrev/bnad004 · Cited by 51
Coconut-sourced MCT oil: its potential health benefits beyond traditional coconut oil
Ďúranová, H., Kuželová, L., Fialková, V., Šimora, V., Kováčiková, E., Joanidis, P., Borotová, P., Straka, D., Hoskin, R. T., Moncada, M. L., et al. (2024) · Phytochemistry Reviews · doi:10.1007/s11101-024-09969-1 · Cited by 62
“However, these subcellular organelles depend on cooperation with mitochondria, as they receive the end products of peroxisomal b - oxidation for complete degradation to CO 2 and H 2 O (Wanders et al. 2016).”
Peroxisomes: role in cellular ageing and age related disorders
Deori, N. M., Kale, A., Maurya, P. K., & Nagotu, S. (2018) · Biogerontology · doi:10.1007/s10522-018-9761-9 · Cited by 47
Dysregulated Provision of Oxidisable Substrates to the Mitochondria in ME/CFS Lymphoblasts
Missailidis, D., Sanislav, O., Allan, C. Y., Smith, P. K., Annesley, S. J., & Fisher, P. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042046 · Cited by 46
“Acyl-CoA oxidase 1 (ACOX1) is the enzyme which first initiates VLCFA β-oxidation inside the peroxisome and is the rate-controlling enzyme of this process [50].”
BackgroundInfluentialDirect androgen receptor control of sexually dimorphic gene expression in the mammalian kidney
Xiong, L., Liu, J., Han, S. Y., Koppitch, K. A., Guo, J., Rommelfanger, M. K., Miao, Z., Gao, F., Hallgrímsdóttir, I. B., Pachter, L. S., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.08.010 · Cited by 45
Fatty Liver Due to Increased de novo Lipogenesis: Alterations in the Hepatic Peroxisomal Proteome
Knebel, B., Fahlbusch, P., Dille, M. A., Wahlers, N., Hartwig, S., Jacob, S., Kettel, U., Schiller, M., Herebıan, D., Koellmer, C., et al. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00248 · Cited by 44
“It is well known that mitochondria have a central role in lipid-degrading, but the metabolic function of peroxisomes is also becoming more important in order to counteract lipid accumulation in hepatocytes during metabolic stress (Unger et al., 2010; Fransen et al., 2012; Wanders, 2013; Knebel et al., 2015, 2018a; Wan…”
BackgroundEaston, Z. J. W., & Regnault, T. R. H. (2020) · Nutrients · doi:10.3390/nu12103031 · Cited by 49
“In brief, peroxisomal beta-oxidation shortens long-chain FA species into acetyl-CoA and short-chain acyl-CoAs such as octanoyl-CoA which can then be exported into the mitochondria for complete oxidation [99,101].”
BackgroundStay in touch with the endoplasmic reticulum
Sun, S., Gan, Z., Jia, M., Jiang, Q., Li, S., Wang, H., Li, W., Wang, Y., Bian, X., Zhao, Y. G., et al. (2024) · Science China Life Sciences · doi:10.1007/s11427-023-2443-9 · Cited by 45
“In addition, ROS signaling has been observed in the ER, mitochondria, and peroxisome, with these three organelles forming the intriguing “ redox triangle ” (Wanders et al., 2016), an entity that is evidently contact-dependent.”
BackgroundRuiz, M., Cuillerier, A., Daneault, C., Deschênes, S., Frayne, I. R., Bouchard, B., Forest, A., Legault, J. T., Vaz, F. M., Rioux, J. D., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.123231 · Cited by 46
“…obtained in the nutrient-uptake challenge condition. with a very-long-chain (VLCFAs; >20 C), which cannot be oxidized by mitochondria, or with an odd chain, generated from dietary phytanic acid metabolism (18), and (ii) C24 BAs conjugated with glycine (glyco-BA) or taurine (tauro-BA) (19, 26).”
BackgroundMethodInfluentialStaying in Healthy Contact: How Peroxisomes Interact with Other Cell Organelles
Sargsyan, Y., & Thoms, S. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.09.012 · Cited by 47
Wright, Z. J., & Bartel, B. (2020) · Nature Communications · doi:10.1038/s41467-020-20099-y · Cited by 43
Biochemistry, Fatty Acid Oxidation
Talley, J. T., & Mohiuddin, S. S. (2021) · StatPearls · Cited by 42
Genome‐wide characterization of Phytophthora infestans metabolism: a systems biology approach
Rodenburg, S. Y. A., Seidl, M. F., de Ridder, D., & Govers, F. (2017) · Molecular Plant Pathology · doi:10.1111/mpp.12623 · Cited by 37
“There is an extensive exchange of metabolites between subcellular compartments (Wanders et al., 2016).”
Multi-localized Proteins: The Peroxisome-Mitochondria Connection
Costello, J. L., Passmore, J. B., Islinger, M., & Schrader, M. (2018) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-981-13-2233-4_17 · Cited by 39
Kingsmore, K. M., Bachali, P., Catalina, M. D., Daamen, A. R., Heuer, S. E., Robl, R. D., Grammer, A. C., & Lipsky, P. E. (2021) · Scientific Reports · doi:10.1038/s41598-021-93034-w · Cited by 40
Determinants of Peroxisome Membrane Dynamics
Carmichael, R. E., & Schrader, M. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.834411 · Cited by 39
Passmore, J. B., Pinho, S., Gómez-Lázaro, M., & Schrader, M. (2017) · Histochemistry and Cell Biology · doi:10.1007/s00418-017-1577-1 · Cited by 38
L-Carnitine in Drosophila: A Review
Carillo, M. R., Bertapelle, C., Scialò, F., Siervo, M., Spagnuolo, G., Simeone, M., Peluso, G., & Digilio, F. A. (2020) · Antioxidants · doi:10.3390/antiox9121310 · Cited by 37
Metadata
- Authors
- Wanders, R. J. A., Waterham, H. R., & Ferdinandusse, S.
- Affiliations
- Amsterdam UMC Location University of Amsterdam (NL)
- Corresponding author
- Wanders, Ronald J. A.
- Venue
- Frontiers in Cell and Developmental Biology
- Publisher
- Frontiers Media SA
- Published
- 2016-01-28
- Volume
- 3
- Pages
- 83-83
- ISSN
- 2296-634X (ISSN-L)
- PMC
- PMC4729952
- OpenAlex
- W2262335045
- Cited by
- 366
- References
- 88
- Citations by year
- 2026: 25 · 2025: 36 · 2024: 43 · 2023: 31 · 2022: 56 · 2021: 39 · 2020: 50 · 2019: 30 · 2018: 29 · 2017: 24 · 2016: 2
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cell and Developmental Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (acceptedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- European Commission (316723)
- Hersenstichting (F2012(1)-102)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Keywords
- peroxisomes, fatty acid beta-oxidation, NADH reoxidation, bile acid synthesis, glyoxylate metabolism, amino acid catabolism
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