61
Views
5
CrossRef citations to date
0
Altmetric
Research Article

Yeast Mpo1 Is a Novel Dioxygenase That Catalyzes the α-Oxidation of a 2-Hydroxy Fatty Acid in an Fe2+-Dependent Manner

, , , & ORCID Icon
Article: e00428-18 | Received 27 Aug 2018, Accepted 02 Dec 2018, Published online: 03 Mar 2023

REFERENCES

  • Kihara A, Mitsutake S, Mizutani Y, Igarashi Y. 2007. Metabolism and biological functions of two phosphorylated sphingolipids, sphingosine 1-phosphate and ceramide 1-phosphate. Prog Lipid Res 46:126–144. https://doi.org/10.1016/j.plipres.2007.03.001.
  • Kulkarni AA, Weiss AA, Iyer SS. 2010. Glycan-based high-affinity ligands for toxins and pathogen receptors. Med Res Rev 30:327–393. https://doi.org/10.1002/med.20196.
  • Pontier SM, Schweisguth F. 2012. Glycosphingolipids in signaling and development: from liposomes to model organisms. Dev Dyn 241:92–106. https://doi.org/10.1002/dvdy.22766.
  • Schmitt S, Castelvetri LC, Simons M. 2015. Metabolism and functions of lipids in myelin. Biochim Biophys Acta 1851:999–1005. https://doi.org/10.1016/j.bbalip.2014.12.016.
  • Kihara A. 2016. Synthesis and degradation pathways, functions, and pathology of ceramides and epidermal acylceramides. Prog Lipid Res 63:50–69. https://doi.org/10.1016/j.plipres.2016.04.001.
  • Pruett ST, Bushnev A, Hagedorn K, Adiga M, Haynes CA, Sullards MC, Liotta DC, Merrill AH, Jr. 2008. Biodiversity of sphingoid bases (“sphingosines”) and related amino alcohols. J Lipid Res 49:1621–1639. https://doi.org/10.1194/jlr.R800012-JLR200.
  • Dickson RC, Sumanasekera C, Lester RL. 2006. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45:447–465. https://doi.org/10.1016/j.plipres.2006.03.004.
  • Nakahara K, Ohkuni A, Kitamura T, Abe K, Naganuma T, Ohno Y, Zoeller RA, Kihara A. 2012. The Sjögren-Larsson syndrome gene encodes a hexadecenal dehydrogenase of the sphingosine 1-phosphate degradation pathway. Mol Cell 46:461–471. https://doi.org/10.1016/j.molcel.2012.04.033.
  • Kihara A. 2014. Sphingosine 1-phosphate is a key metabolite linking sphingolipids to glycerophospholipids. Biochim Biophys Acta 1841:766–772. https://doi.org/10.1016/j.bbalip.2013.08.014.
  • Saba JD, Nara F, Bielawska A, Garrett S, Hannun YA. 1997. The BST1 gene of Saccharomyces cerevisiae is the sphingosine-1-phosphate lyase. J Biol Chem 272:26087–26090.
  • Nagiec MM, Skrzypek M, Nagiec EE, Lester RL, Dickson RC. 1998. The LCB4 (YOR171c) and LCB5 (YLR260w) genes of Saccharomyces encode sphingoid long chain base kinases. J Biol Chem 273:19437–19442.
  • Kohama T, Olivera A, Edsall L, Nagiec MM, Dickson R, Spiegel S. 1998. Molecular cloning and functional characterization of murine sphingosine kinase. J Biol Chem 273:23722–23728.
  • Zhou J, Saba JD. 1998. Identification of the first mammalian sphingosine phosphate lyase gene and its functional expression in yeast. Biochem Biophys Res Commun 242:502–507. https://doi.org/10.1006/bbrc.1997.7993.
  • Liu H, Sugiura M, Nava VE, Edsall LC, Kono K, Poulton S, Milstien S, Kohama T, Spiegel S. 2000. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J Biol Chem 275:19513–19520. https://doi.org/10.1074/jbc.M002759200.
  • Ohkuni A, Ohno Y, Kihara A. 2013. Identification of acyl-CoA synthetases involved in the mammalian sphingosine 1-phosphate metabolic pathway. Biochem Biophys Res Commun 442:195–201. https://doi.org/10.1016/j.bbrc.2013.11.036.
  • Rizzo WB. 2007. Sjögren-Larsson syndrome: molecular genetics and biochemical pathogenesis of fatty aldehyde dehydrogenase deficiency. Mol. Genet Metab 90:1–9. https://doi.org/10.1016/j.ymgme.2006.08.006.
  • Atkinson D, Nikodinovic Glumac J, Asselbergh B, Ermanoska B, Blocquel D, Steiner R, Estrada-Cuzcano A, Peeters K, Ooms T, De Vriendt E, Yang XL, Hornemann T, Milic Rasic V, Jordanova A. 2017. Sphingosine 1-phosphate lyase deficiency causes Charcot-Marie-Tooth neuropathy. Neurology 88:533–542. https://doi.org/10.1212/WNL.0000000000003595.
  • Janecke AR, Xu R, Steichen-Gersdorf E, Waldegger S, Entenmann A, Giner T, Krainer I, Huber LA, Hess MW, Frishberg Y, Barash H, Tzur S, Schreyer-Shafir N, Sukenik-Halevy R, Zehavi T, Raas-Rothschild A, Mao C, Müller T. 2017. Deficiency of the sphingosine-1-phosphate lyase SGPL1 is associated with congenital nephrotic syndrome and congenital adrenal calcifications. Hum Mutat 38:365–372. https://doi.org/10.1002/humu.23192.
  • Lovric S, Goncalves S, Gee HY, Oskouian B, Srinivas H, Choi W-I, Shril S, Ashraf S, Tan W, Rao J, Airik M, Schapiro D, Braun DA, Sadowski CE, Widmeier E, Jobst-Schwan T, Schmidt JM, Girik V, Capitani G, Suh JH, Lachaussée N, Arrondel C, Patat J, Gribouval O, Furlano M, Boyer O, Schmitt A, Vuiblet V, Hashmi S, Wilcken R, Bernier FP, Innes AM, Parboosingh JS, Lamont RE, Midgley JP, Wright N, Majewski J, Zenker M, Schaefer F, Kuss N, Greil J, Giese T, Schwarz K, Catheline V, Schanze D, Franke I, Sznajer Y, Truant AS, Adams B, Désir J, et al. 2017. Mutations in sphingosine-1-phosphate lyase cause nephrosis with ichthyosis and adrenal insufficiency. J Clin Invest 127:912–928. https://doi.org/10.1172/JCI89626.
  • Prasad R, Hadjidemetriou I, Maharaj A, Meimaridou E, Buonocore F, Saleem M, Hurcombe J, Bierzynska A, Barbagelata E, Bergada I, Cassinelli H, Das U, Krone R, Hacihamdioglu B, Sari E, Yesilkaya E, Storr HL, Clemente M, Fernandez-Cancio M, Camats N, Ram N, Achermann JC, Van Veldhoven PP, Guasti L, Braslavsky D, Guran T, Metherell LA. 2017. Sphingosine-1-phosphate lyase mutations cause primary adrenal insufficiency and steroid-resistant nephrotic syndrome. J Clin Invest 127:942–953. https://doi.org/10.1172/JCI90171.
  • Kondo N, Ohno Y, Yamagata M, Obara T, Seki N, Kitamura T, Naganuma T, Kihara A. 2014. Identification of the phytosphingosine metabolic pathway leading to odd-numbered fatty acids. Nat Commun 5:5338. https://doi.org/10.1038/ncomms6338.
  • Foulon V, Sniekers M, Huysmans E, Asselberghs S, Mahieu V, Mannaerts GP, Van Veldhoven PP, Casteels M. 2005. Breakdown of 2-hydroxylated straight chain fatty acids via peroxisomal 2-hydroxyphytanoyl-CoA lyase: a revised pathway for the α-oxidation of straight chain fatty acids. J Biol Chem 280:9802–9812. https://doi.org/10.1074/jbc.M413362200.
  • Kitamura T, Seki N, Kihara A. 2017. The phytosphingosine degradation pathway includes novel fatty acid α-oxidation reactions in the endoplasmic reticulum. Proc Natl Acad Sci U S A 114:E2616–E2623. https://doi.org/10.1073/pnas.1700138114.
  • Ikeda M, Kihara A, Igarashi Y. 2004. Sphingosine-1-phosphate lyase SPL is an endoplasmic reticulum-resident, integral membrane protein with the pyridoxal 5'-phosphate binding domain exposed to the cytosol. Biochem Biophys Res Commun 325:338–343. https://doi.org/10.1016/j.bbrc.2004.10.036.
  • Ashibe B, Hirai T, Higashi K, Sekimizu K, Motojima K. 2007. Dual subcellular localization in the endoplasmic reticulum and peroxisomes and a vital role in protecting against oxidative stress of fatty aldehyde dehydrogenase are achieved by alternative splicing. J Biol Chem 282:20763–20773. https://doi.org/10.1074/jbc.M611853200.
  • Nozawa A, Tozawa Y. 2014. Modifications of wheat germ cell-free system for functional proteomics of plant membrane proteins. Methods Mol Biol 1072:259–272. https://doi.org/10.1007/978-1-62703-631-3_19.
  • Arimitsu E, Ogasawara T, Takeda H, Sawasaki T, Ikeda Y, Hiasa Y, Maeyama K. 2014. The ligand binding ability of dopamine D1 receptors synthesized using a wheat germ cell-free protein synthesis system with liposomes. Eur J Pharmacol 745:117–122. https://doi.org/10.1016/j.ejphar.2014.10.011.
  • Takemori N, Takemori A, Matsuoka K, Morishita R, Matsushita N, Aoshima M, Takeda H, Sawasaki T, Endo Y, Higashiyama S. 2015. High-throughput synthesis of stable isotope-labeled transmembrane proteins for targeted transmembrane proteomics using a wheat germ cell-free protein synthesis system. Mol Biosyst 11:361–365. https://doi.org/10.1039/C4MB00556B.
  • Ohno Y, Kamiyama N, Nakamichi S, Kihara A. 2017. Formation of the skin barrier lipid ω-O-acylceramide by the ichthyosis gene PNPLA1. Nat Commun 8:14610. https://doi.org/10.1038/ncomms6338.
  • Yamahara R, Ogo S, Masuda H, Watanabe Y. 2002. (Catecholato)iron(III) complexes: structural and functional models for the catechol-bound iron(III) form of catechol dioxygenases. J Inorg Biochem 88:284–294.
  • Siddiq A, Aminova LR, Ratan RR. 2007. Hypoxia inducible factor prolyl 4-hydroxylase enzymes: center stage in the battle against hypoxia, metabolic compromise and oxidative stress. Neurochem Res 32:931–946. https://doi.org/10.1007/s11064-006-9268-7.
  • Nebert DW, Wikvall K, Miller WL. 2013. Human cytochromes P450 in health and disease. Philos Trans R Soc Lond B Biol Sci 368:20120431. https://doi.org/10.1098/rstb.2012.0431.
  • McMurry JE, Begley TP. 2015. Amino acid metabolism, p 245–332. In McMurry JE, Begley TP (ed), The organic chemistry of biological pathways, 2nd ed. Roberts and Company Publishers, Greenwood Village, CO.
  • Piña F, Yagisawa F, Obara K, Gregerson JD, Kihara A, Niwa M. 2018. Sphingolipids activate the endoplasmic reticulum stress surveillance pathway. J Cell Biol 217:495–505. https://doi.org/10.1083/jcb.201708068.
  • Grevengoed TJ, Klett EL, Coleman RA. 2014. Acyl-CoA metabolism and partitioning. Annu Rev Nutr 34:1–30. https://doi.org/10.1146/annurev-nutr-071813-105541.
  • Kitamura T, Naganuma T, Abe K, Nakahara K, Ohno Y, Kihara A. 2013. Substrate specificity, plasma membrane localization, and lipid modification of the aldehyde dehydrogenase ALDH3B1. Biochim Biophys Acta 1831:1395–1401. https://doi.org/10.1016/j.bbalip.2013.05.007.
  • Kitamura T, Takagi S, Naganuma T, Kihara A. 2015. Mouse aldehyde dehydrogenase ALDH3B2 is localized to lipid droplets via two C-terminal tryptophan residues and lipid modification. Biochem J 465:79–87. https://doi.org/10.1042/BJ20140624.
  • Naganuma T, Takagi S, Kanetake T, Kitamura T, Hattori S, Miyakawa T, Sassa T, Kihara A. 2016. Disruption of the Sjögren-Larsson syndrome gene Aldh3a2 in mice increases keratinocyte growth and retards skin barrier recovery. J Biol Chem 291:11676–11688. https://doi.org/10.1074/jbc.M116.714030.
  • Kanetake T, Sassa T, Nojiri K, Sawai M, Hattori S, Miyakawa T, Kitamura T, Kihara A. 7 August 2018. Neural symptoms in a gene knockout mouse model of Sjögren-Larsson syndrome are associated with a decrease in 2-hydroxygalactosylceramide. FASEB J https://doi.org/10.1096/fj.201800291R.
  • Wakashima T, Abe K, Kihara A. 2014. Dual functions of the trans-2-enoyl-CoA reductase TER in the sphingosine 1-phosphate metabolic pathway and in fatty acid elongation. J Biol Chem 289:24736–24748. https://doi.org/10.1074/jbc.M114.571869.
  • Jenkins B, West JA, Koulman A. 2015. A review of odd-chain fatty acid metabolism and the role of pentadecanoic acid (C15:0) and heptadecanoic acid (C17:0) in health and disease. Molecules 20:2425–2444. https://doi.org/10.3390/molecules20022425.
  • Michaelson LV, Napier JA, Molino D, Faure JD. 2016. Plant sphingolipids: their importance in cellular organization and adaption. Biochim Biophys Acta 1861:1329–1335. https://doi.org/10.1016/j.bbalip.2016.04.003.
  • Singh A, Del Poeta M. 2016. Sphingolipidomics: an important mechanistic tool for studying fungal pathogens. Front Microbiol 7:501. https://doi.org/10.3389/fmicb.2016.00501.
  • Olsen I, Jantzen E. 2001. Sphingolipids in bacteria and fungi. Anaerobe 7:103–112. https://doi.org/10.1006/anae.2001.0376.
  • Geiger O, González-Silva N, López-Lara IM, Sohlenkamp C. 2010. Amino acid-containing membrane lipids in bacteria. Prog Lipid Res 49:46–60. https://doi.org/10.1016/j.plipres.2009.08.002.
  • Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115–132. https://doi.org/10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2.
  • Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, Pai C, Rebischung C, Revuelta JL, Riles L, Roberts CJ, Ross-MacDonald P, Scherens B, Snyder M, Sookhai-Mahadeo S, Storms RK, Veronneau S, Voet M, Volckaert G, Ward TR, Wysocki R, Yen GS, Yu K, Zimmermann K, Philippsen P, Johnston M, Davis RW. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901–906.
  • Narita T, Naganuma T, Sase Y, Kihara A. 2016. Long-chain bases of sphingolipids are transported into cells via the acyl-CoA synthetases. Sci Rep 6:25469. https://doi.org/10.1038/srep25469.
  • Kihara A, Kurotsu F, Sano T, Iwaki S, Igarashi Y. 2005. Long-chain base kinase Lcb4 is anchored to the membrane through its palmitoylation by Akr1. Mol Cell Biol 25:9189–9197. https://doi.org/10.1128/MCB.25.21.9189-9197.2005.
  • Ohno Y, Suto S, Yamanaka M, Mizutani Y, Mitsutake S, Igarashi Y, Sassa T, Kihara A. 2010. ELOVL1 production of C24 acyl-CoAs is linked to C24 sphingolipid synthesis. Proc Natl Acad Sci U S A 107:18439–18444. https://doi.org/10.1073/pnas.1005572107.
  • Ohno Y, Nakamichi S, Ohkuni A, Kamiyama N, Naoe A, Tsujimura H, Yokose U, Sugiura K, Ishikawa J, Akiyama M, Kihara A. 2015. Essential role of the cytochrome P450 CYP4F22 in the production of acylceramide, the key lipid for skin permeability barrier formation. Proc Natl Acad Sci U S A 112:7707–7712. https://doi.org/10.1073/pnas.1503491112.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.