A paREDOX in the control of cholesterol biosynthesis: Does the NADPH sensor and E3 ubiquitin ligase MARCHF6 protect mammalian cells during oxidative stress by controlling sterol biosynthesis?

التفاصيل البيبلوغرافية
العنوان:	A paREDOX in the control of cholesterol biosynthesis: Does the NADPH sensor and E3 ubiquitin ligase MARCHF6 protect mammalian cells during oxidative stress by controlling sterol biosynthesis?
المؤلفون:	Fenton NM; School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia., Qian L; School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia., Paine EG; School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia., Sharpe LJ; School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia., Brown AJ; School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
المصدر:	BioEssays : news and reviews in molecular, cellular and developmental biology [Bioessays] 2024 Jul; Vol. 46 (7), pp. e2400073. Date of Electronic Publication: 2024 May 17.
نوع المنشور:	Journal Article; Review
اللغة:	English
بيانات الدورية:	Publisher: Wiley Country of Publication: United States NLM ID: 8510851 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1521-1878 (Electronic) Linking ISSN: 02659247 NLM ISO Abbreviation: Bioessays Subsets: MEDLINE
أسماء مطبوعة:	Publication: <2005->: Hoboken, N.J. : Wiley Original Publication: Cambridge, UK : Published for the ICSU Press by Cambridge University Press, c1984-
مواضيع طبية MeSH:	Oxidative Stress* , NADP/metabolism , Cholesterol/biosynthesis , Cholesterol/metabolism , Ubiquitin-Protein Ligases/metabolism , Ubiquitin-Protein Ligases*/genetics, Humans ; Animals ; Membrane Proteins/metabolism ; Membrane Proteins/genetics ; Oxidation-Reduction ; Sterols/metabolism ; Sterols/biosynthesis
مستخلص:	Sterols and the reductant nicotinamide adenine dinucleotide phosphate (NADPH), essential for eukaryotic life, arose because of, and as an adaptation to, rising levels of molecular oxygen (O 2 ). Hence, the NADPH and O 2 -intensive process of sterol biosynthesis is inextricably linked to redox status. In mammals, cholesterol biosynthesis is exquisitely regulated post-translationally by multiple E3 ubiquitin ligases, with membrane associated Really Interesting New Gene (RING) C 3 HC 4 finger 6 (MARCHF6) degrading at least six enzymes in the pathway. Intriguingly, all these MARCHF6-dependent enzymes require NADPH. Moreover, MARCHF6 is activated by NADPH, although what this means for control of cholesterol synthesis is unclear. Indeed, this presents a paradox for how NADPH regulates this vital pathway, since NADPH is a cofactor in cholesterol biosynthesis and yet, low levels of NADPH should spare cholesterol biosynthesis enzymes targeted by MARCHF6 by reducing its activity. We speculate MARCHF6 helps mammalian cells adapt to oxidative stress (signified by low NADPH levels) by reducing degradation of cholesterogenic enzymes, thereby maintaining synthesis of protective cholesterol. (© 2024 The Authors. BioEssays published by Wiley Periodicals LLC.)
References:	Ouweneel, A. B., Thomas, M. J., & Sorci‐Thomas, M. G. (2020). The ins and outs of lipid rafts: Functions in intracellular cholesterol homeostasis, microparticles, and cell membranes. Journal of Lipid Research, 61(5), 676–686. https://doi.org/10.1194/jlr.TR119000383. Miller, W. L., & Auchus, R. J. (2011). The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocrine Reviews, 32(1), 81–151. https://doi.org/10.1210/er.2010‐0013. Russell, D. W. (2009). Fifty years of advances in bile acid synthesis and metabolism. Journal of Lipid Research, 50, S120–S125. https://doi.org/10.1194/jlr.R800026‐JLR200. Prabhu, A. V., Luu, W., Sharpe, L. J., & Brown, A. J. (2016). Cholesterol‐mediated degradation of 7‐dehydrocholesterol reductase switches the balance from cholesterol to vitamin D synthesis. Journal of Biological Chemistry, 291(16), 8363–8373. https://doi.org/10.1074/jbc.M115.699546. Brown, A. J., Coates, H. W., & Sharpe, L. J. (2021). Cholesterol synthesis. In N. D. Ridgway, & R. S. McLeod (Eds.), Biochemistry of lipids, lipoproteins and membranes (7th ed., pp. 317–355). Elsevier. https://doi.org/10.1016/B978‐0‐12‐824048‐9.00005‐5. Sharpe, L. J., Coates, H. W., & Brown, A. J. (2020). Post‐translational control of the long and winding road to cholesterol. Journal of Biological Chemistry, 295(51), 17549–17559. https://doi.org/10.1074/jbc.REV120.010723. Horton, J. D., Goldstein, J. L., & Brown, M. S. (2002). SREBPs: Activators of the complete program of cholesterol and fatty acid synthesis in the liver. The Journal of Clinical Investigation, 109(9), 1125–1131. https://doi.org/10.1172/JCI15593. Scott, N. A., Sharpe, L. J., & Brown, A. J. (2021). The E3 ubiquitin ligase MARCHF6 as a metabolic integrator in cholesterol synthesis and beyond. Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids, 1866(1), 158837. https://doi.org/10.1016/j.bbalip.2020.158837. Mao, C., & Gan, B. (2022). Navigating ferroptosis via an NADPH sensor. Nature Cell Biology, 24(8), 1186–1187. https://doi.org/10.1038/s41556‐022‐00963‐3. Bloch, K. (1964, December 11). The biological synthesis of cholesterol [Nobel Lecture]. https://www.nobelprize.org/prizes/medicine/1964/bloch/lecture/. Bloch, K. (1994). Blondes in venetian paintings, the nine‐banded armadillo, and other essays in biochemistry. Yale University Press. Brown, A. J., & Galea, A. M. (2010). Cholesterol as an evolutionary response to living with oxygen. Evolution: International Journal of Organic Evolution, 64(7), 2179–2183. https://doi.org/10.1111/j.1558‐5646.2010.01011.x. Xu, F., Rychnovsky, S. D., Belani, J. D., Hobbs, H. H., Cohen, J. C., & Rawson, R. B. (2005). Dual roles for cholesterol in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 102(41), 14551–14556. https://doi.org/10.1073/pnas.0503590102. Zhang, X., Barraza, K. M., & Beauchamp, J. L. (2018). Cholesterol provides nonsacrificial protection of membrane lipids from chemical damage at air–water interface. Proceedings of the National Academy of Sciences of the United States of America, 115(13), 3255–3260. https://doi.org/10.1073/pnas.1722323115. Galea, A. M., & Brown, A. J. (2009). Special relationship between sterols and oxygen: Were sterols an adaptation to aerobic life? Free Radical Biology and Medicine, 47(6), 880–889. https://doi.org/10.1016/j.freeradbiomed.2009.06.027. Giudetti, A. M., Damiano, F., Gnoni, G. V., & Siculella, L. (2013). Low level of hydrogen peroxide induces lipid synthesis in BRL‐3A cells through a CAP‐independent SREBP‐1a activation. The International Journal of Biochemistry, & Cell Biology, 45(7), 1419–1426. https://doi.org/10.1016/j.biocel.2013.04.004. Pedroso, N., Matias, A. C., Cyrne, L., Antunes, F., Borges, C., Malhó, R., de Almeida, R. F. M., Herrero, E., & Marinho, H. S. (2009). Modulation of plasma membrane lipid profile and microdomains by H2O2 in Saccharomyces cerevisiae. Free Radical Biology, & Medicine, 46(2), 289–298. https://doi.org/10.1016/j.freeradbiomed.2008.10.039. Jové, M., Mota‐Martorell, N., Obis, È., Sol, J., Martín‐Garí, M., Ferrer, I., Portero‐Otín, M., & Pamplona, R. (2023). Lipid adaptations against oxidative challenge in the healthy adult human brain. Antioxidants (Basel, Switzerland), 12(1), 177. https://doi.org/10.3390/antiox12010177. Zuniga‐Hertz, J. P., & Patel, H. H. (2019). The evolution of cholesterol‐rich membrane in oxygen adaption: The respiratory system as a model. Frontiers in Physiology, 10, 1340. https://doi.org/10.3389/fphys.2019.01340. Cui, S., & Ye, J. (2024). 7‐Dehydrocholesterol: A sterol shield against an iron sword. Molecular Cell, 84(7), 1183–1185. https://doi.org/10.1016/j.molcel.2024.03.003. Spaans, S. K., Weusthuis, R. A., van der Oost, J., & Kengen, S. W. M. (2015). NADPH‐generating systems in bacteria and archaea. Frontiers in Microbiology, 6, 742. https://doi.org/10.3389/fmicb.2015.00742. Schröder, K. (2020). NADPH oxidases: Current aspects and tools. Redox Biology, 34, 101512. https://doi.org/10.1016/j.redox.2020.101512. Gould, S. B., Garg, S. G., Handrich, M., Nelson‐Sathi, S., Gruenheit, N., Tielens, A. G. M., & Martin, W. F. (2019). Adaptation to life on land at high O(2) via transition from ferredoxin‐to NADH‐dependent redox balance. Proceedings. Biological Sciences, 286(1909), 20191491. https://doi.org/10.1098/rspb.2019.1491. Kreft, S. G., Wang, L., & Hochstrasser, M. (2006). Membrane topology of the yeast endoplasmic reticulum‐localized ubiquitin ligase Doa10 and comparison with its human ortholog TEB4 (MARCH‐VI). Journal of Biological Chemistry, 281(8), 4646–4653. https://doi.org/10.1074/jbc.M512215200. Zattas, D., Berk, J. M., Kreft, S. G., & Hochstrasser, M. (2016). A conserved C‐terminal element in the yeast Doa10 and human MARCH6 ubiquitin ligases required for selective substrate degradation. Journal of Biological Chemistry, 291(23), 12105–12118. https://doi.org/10.1074/jbc.M116.726877. Botsch, J. J., Junker, R., Sorgenfrei, M., Ogger, P. P., Stier, L., von Gronau, S., Murray, P. J., Seeger, M. A., Schulman, B. A., & Bräuning, B. (2024). Doa10/MARCH6 architecture interconnects E3 ligase activity with lipid‐binding transmembrane channel to regulate SQLE. Nature Communications, 15(1), 410. https://doi.org/10.1038/s41467‐023‐44670‐5. Wu, K., Itskanov, S., Lynch, D. L., Chen, Y., Turner, A., Gumbart, J. C., & Park, E. (2024). Substrate recognition mechanism of the endoplasmic reticulum‐associated ubiquitin ligase Doa10. Nature Communications, 15(1), 2182. https://doi.org/10.1038/s41467‐024‐46409‐2. Lin, H., Li, S., & Shu, H.‐B. (2019). The membrane‐associated MARCH E3 ligase family: Emerging roles in immune regulation. Frontiers in Immunology, 10, 1751. https://doi.org/10.3389/fimmu.2019.01751. Fenton, N. M., Qian, L., Scott, N. A., Paine, E. G., Sharpe, L. J., & Brown, A. J. (2024). SC5D is the sixth enzyme in cholesterol biosynthesis targeted by the E3 ubiquitin ligase MARCHF6. Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids, 1869(4), 159482. https://doi.org/10.1016/j.bbalip.2024.159482. Qian, L., Scott, N. A., Capell‐Hattam, I. M., Draper, E. A., Fenton, N. M., Luu, W., Sharpe, L. J., & Brown, A. J. (2023). Cholesterol synthesis enzyme SC4MOL is fine‐tuned by sterols and targeted for degradation by the E3 ligase MARCHF6. Journal of Lipid Research, 64(5), 100362. https://doi.org/10.1016/j.jlr.2023.100362. Scott, N. A., Sharpe, L. J., Capell‐Hattam, I. M., Gullo, S. J., Luu, W., & Brown, A. J. (2020). The cholesterol synthesis enzyme lanosterol 14α‐demethylase is post‐translationally regulated by the E3 ubiquitin ligase MARCH6. Biochemical Journal, 477(2), 541–555. https://doi.org/10.1042/BCJ20190647. Zelcer, N., Sharpe, L. J., Loregger, A., Kristiana, I., Cook, E. C. L., Phan, L., Stevenson, J., & Brown, A. J. (2014). The E3 ubiquitin ligase MARCH6 degrades squalene monooxygenase and affects 3‐hydroxy‐3‐methyl‐glutaryl coenzyme A reductase and the cholesterol synthesis pathway. Molecular and Cellular Biology, 34(7), 1262–1270. https://doi.org/10.1128/MCB.01140‐13. Sharpe, L. J., Howe, V., Scott, N. A., Luu, W., Phan, L., Berk, J. M., Hochstrasser, M., & Brown, A. J. (2019). Cholesterol increases protein levels of the E3 ligase MARCH6 and thereby stimulates protein degradation. Journal of Biological Chemistry, 294(7), 2436–2448. https://doi.org/10.1074/jbc.RA118.005069. Foresti, O., Ruggiano, A., Hannibal‐Bach, H. K., Ejsing, C. S., & Carvalho, P. (2013). Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. eLife, 2, e00953. https://doi.org/10.7554/eLife.00953. Nguyen, K. T., Mun, S. H., Yang, J., Lee, J., Seok, O. H., Kim, E., Kim, D., An, S. Y., Seo, D. Y., Suh, J. Y., Lee, Y., & Hwang, C. S. (2022). The MARCHF6 E3 ubiquitin ligase acts as an NADPH sensor for the regulation of ferroptosis. Nature Cell Biology, 24(8), 1239–1251. https://doi.org/10.1038/s41556‐022‐00973‐1. Xie, Y., Hou, W., Song, X., Yu, Y., Huang, J., Sun, X., Kang, R., & Tang, D. (2016). Ferroptosis: Process and function. Cell Death & Differentiation, 23(3), 369–379. https://doi.org/10.1038/cdd.2015.158. Dickson, A. S., Pauzaite, T., Arnaiz, E., Ortmann, B. M., West, J. A., Volkmar, N., Martinelli, A. W., Li, Z., Wit, N., Vitkup, D., Kaser, A., Lehner, P. J., & Nathan, J. A. (2023). A HIF independent oxygen‐sensitive pathway for controlling cholesterol synthesis. Nature Communications, 14(1), 4816. https://doi.org/10.1038/s41467‐023‐40541‐1. Coates, H. W., Capell‐Hattam, I. M., Olzomer, E. M., Du, X., Farrell, R., Yang, H., Byrne, F. L., & Brown, A. J. (2023). Hypoxia truncates and constitutively activates the key cholesterol synthesis enzyme squalene monooxygenase. eLife, 12, e82843. https://doi.org/10.7554/eLife.82843. Draper, S. W. (1978). The Penrose triangle and a family of related figures. Perception, 7(3), 283–296. Furuta, E., Pai, S. K., Zhan, R., Bandyopadhyay, S., Watabe, M., Mo, Y. Y., Hirota, S., Hosobe, S., Tsukada, T., Miura, K., Kamada, S., Saito, K., Iiizumi, M., Liu, W., Ericsson, J., & Watabe, K. (2008). Fatty acid synthase gene is up‐regulated by hypoxia via activation of Akt and sterol regulatory element binding protein‐1. Cancer Research, 68(4), 1003–1011. https://doi.org/10.1158/0008‐5472.CAN‐07‐2489. Nguyen, A. D., McDonald, J. G., Bruick, R. K., & DeBose‐Boyd, R. A. (2007). Hypoxia stimulates degradation of 3‐hydroxy‐3‐methylglutaryl‐coenzyme A reductase through accumulation of lanosterol and hypoxia‐inducible factor‐mediated induction of insigs. The Journal of Biological Chemistry, 282(37), 27436–27446. https://doi.org/10.1074/jbc.M704976200. Sies, H. (2020). Oxidative stress: Concept and some practical aspects. Antioxidants, 9(9), 852. https://doi.org/10.3390/antiox9090852. Krycer, J. R., Phan, L., & Brown, A. J. (2012). A key regulator of cholesterol homoeostasis, SREBP‐2, can be targeted in prostate cancer cells with natural products. Biochemical Journal, 446(2), 191–201. https://doi.org/10.1042/BJ20120545. Weng, L., Tang, W. S., Wang, X., Gong, Y., Liu, C., Hong, N. N., Tao, Y., Li, K. Z., Liu, S. N., Jiang, W., Li, Y., Yao, K., Chen, L., Huang, H., Zhao, Y. Z., Hu, Z. P., Lu, Y., Ye, H., Du, X., …, & Zhao, T. J. (2024). Surplus fatty acid synthesis increases oxidative stress in adipocytes and induces lipodystrophy. Nature Communications, 15(1), 133. https://doi.org/10.1038/s41467‐023‐44393‐7. Haggarty, P., Shetty, P., Thangam, S., Kumar, S., Kurpad, A., Ashton, J., Milne, E., & Earl, C. (2000). Free and esterified fatty acid and cholesterol synthesis in adult malesand its effect on the doubly‐labelled water method. British Journal of Nutrition, 83(3), 227–234. Cambridge Core. https://doi.org/10.1017/S0007114500000295. Yoshioka, H., Coates, H. W., Chua, N. K., Hashimoto, Y., Brown, A. J., & Ohgane, K. (2020). A key mammalian cholesterol synthesis enzyme, squalene monooxygenase, is allosterically stabilized by its substrate. Proceedings of the National Academy of Sciences of the United States of America, 117(13), 7150–7158. https://doi.org/10.1073/pnas.1915923117. Gill, S., Stevenson, J., Kristiana, I., & Brown, A. J. (2011). Cholesterol‐dependent degradation of squalene monooxygenase, a control point in cholesterol synthesis beyond HMG‐CoA reductase. Cell Metabolism, 13(3), 260–273. https://doi.org/10.1016/j.cmet.2011.01.015. Larsson, P., Engqvist, H., Biermann, J., Werner Rönnerman, E., Forssell‐Aronsson, E., Kovács, A., Karlsson, P., Helou, K., & Parris, T. Z. (2020). Optimization of cell viability assays to improve replicability and reproducibility of cancer drug sensitivity screens. Scientific Reports, 10(1), 5798. https://doi.org/10.1038/s41598‐020‐62848‐5. Mullarky, E., & Cantley, L. C. (2015). Diverting glycolysis to combat oxidative stress. In K. Nakao, N. Minato, & S. Uemoto (Eds.), Innovative medicine (pp. 3–23). Springer Japan. Hu, J., Liu, N., Song, D., Steer, C. J., Zheng, G., & Song, G. (2023). A positive feedback between cholesterol synthesis and the pentose phosphate pathway rather than glycolysis promotes hepatocellular carcinoma. Oncogene, 42(39), 2892–2904. https://doi.org/10.1038/s41388‐023‐02757‐9.
معلومات مُعتمدة:	DP170101178 Australian Research Council Discovery Project; Australian Government Research Training Program Scholarship
فهرسة مساهمة:	Keywords: E3 ubiquitin ligase; MARCHF6; NADPH; cholesterol; fatty acids; oxidative stress; oxygen
المشرفين على المادة:	53-59-8 (NADP) 97C5T2UQ7J (Cholesterol) EC 2.3.2.27 (Ubiquitin-Protein Ligases) 0 (Membrane Proteins) EC 2.3.2.27 (MARCHF6 protein, human) 0 (Sterols)
تواريخ الأحداث:	Date Created: 20240517 Date Completed: 20240626 Latest Revision: 20240628
رمز التحديث:	20240628
DOI:	10.1002/bies.202400073
PMID:	38760877
قاعدة البيانات:	MEDLINE

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تدمد:	1521-1878
DOI:	10.1002/bies.202400073