Biological Importance of Complex Sphingolipids and Their Structural Diversity in Budding Yeast

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 Nov 27

PMID 39596489

Authors

Motohiro Tani

Affiliations

Soon will be listed here.

Abstract

Complex sphingolipids are components of eukaryotic biomembranes and are involved in various physiological functions. In addition, their synthetic intermediates and metabolites, such as ceramide, sphingoid long-chain base, and sphingoid long-chain base 1-phosphate, play important roles as signaling molecules that regulate intracellular signal transduction systems. Complex sphingolipids have a large number of structural variations, and this structural diversity is considered an important molecular basis for their various physiological functions. The budding yeast has simpler structural variations in complex sphingolipids compared to mammals and is, therefore, a useful model organism for elucidating the physiological significance of this structural diversity. In this review, we focus on the structure and function of complex sphingolipids in and summarize the response mechanisms of to metabolic abnormalities in complex sphingolipids.

References

Clay L, Caudron F, Denoth-Lippuner A, Boettcher B, Buvelot Frei S, Snapp E . A sphingolipid-dependent diffusion barrier confines ER stress to the yeast mother cell. Elife. 2014; 3:e01883. PMC: 4009826. DOI: 10.7554/eLife.01883. View

Schafer J, Korner C, Esch B, Limar S, Parey K, Walter S . Structure of the ceramide-bound SPOTS complex. Nat Commun. 2023; 14(1):6196. PMC: 10550967. DOI: 10.1038/s41467-023-41747-z. View

Tani M, Kihara A, Igarashi Y . Rescue of cell growth by sphingosine with disruption of lipid microdomain formation in Saccharomyces cerevisiae deficient in sphingolipid biosynthesis. Biochem J. 2005; 394(Pt 1):237-42. PMC: 1386021. DOI: 10.1042/BJ20051354. View

Yamashita T, Hashiramoto A, Haluzik M, Mizukami H, Beck S, Norton A . Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc Natl Acad Sci U S A. 2003; 100(6):3445-9. PMC: 152312. DOI: 10.1073/pnas.0635898100. View

Toume M, Tani M . Yeast lacking the amphiphysin family protein Rvs167 is sensitive to disruptions in sphingolipid levels. FEBS J. 2016; 283(15):2911-28. DOI: 10.1111/febs.13783. View

Merrill Jr A . Sphingolipid and glycosphingolipid metabolic pathways in the era of sphingolipidomics. Chem Rev. 2011; 111(10):6387-422. PMC: 3191729. DOI: 10.1021/cr2002917. View

Sakata K, Hashii K, Yoshizawa K, Tahara Y, Yae K, Tsuda R . Coordinated regulation of TORC2 signaling by MCC/eisosome-associated proteins, Pil1 and tetraspan membrane proteins during the stress response. Mol Microbiol. 2022; 117(5):1227-1244. DOI: 10.1111/mmi.14903. View

Kihara A, Igarashi Y . Identification and characterization of a Saccharomyces cerevisiae gene, RSB1, involved in sphingoid long-chain base release. J Biol Chem. 2002; 277(33):30048-54. DOI: 10.1074/jbc.M203385200. View

Toda T, Urita A, Koga A, Takayama C, Tani M . ROS-mediated synthetic growth defect caused by impaired metabolism of sphingolipids and phosphatidylserine in budding yeast. Biosci Biotechnol Biochem. 2020; 84(12):2529-2532. DOI: 10.1080/09168451.2020.1810539. View

10.

Nakano M, Hanashima S, Hara T, Kabayama K, Asahina Y, Hojo H . FRET detects lateral interaction between transmembrane domain of EGF receptor and ganglioside GM3 in lipid bilayers. Biochim Biophys Acta Biomembr. 2021; 1863(8):183623. DOI: 10.1016/j.bbamem.2021.183623. View

11.

Heidler S, Radding J . The AUR1 gene in Saccharomyces cerevisiae encodes dominant resistance to the antifungal agent aureobasidin A (LY295337). Antimicrob Agents Chemother. 1995; 39(12):2765-9. PMC: 163026. DOI: 10.1128/AAC.39.12.2765. View

12.

Dickson R, Sumanasekera C, Lester R . Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res. 2006; 45(6):447-65. DOI: 10.1016/j.plipres.2006.03.004. View

13.

Nakahara K, Ohkuni A, Kitamura T, Abe K, Naganuma T, Ohno Y . The Sjögren-Larsson syndrome gene encodes a hexadecenal dehydrogenase of the sphingosine 1-phosphate degradation pathway. Mol Cell. 2012; 46(4):461-71. DOI: 10.1016/j.molcel.2012.04.033. View

14.

Otsu M, Toume M, Yamaguchi Y, Tani M . Proper regulation of inositolphosphorylceramide levels is required for acquirement of low pH resistance in budding yeast. Sci Rep. 2020; 10(1):10792. PMC: 7329899. DOI: 10.1038/s41598-020-67734-8. View

15.

Ogawa A, Endo M, Yoshioka H, Tsuruo T, Takesako K, Kato I . Role of ABC transporters in aureobasidin A resistance. Antimicrob Agents Chemother. 1998; 42(4):755-61. PMC: 105537. DOI: 10.1128/AAC.42.4.755. View

16.

Urita A, Ishibashi Y, Kawaguchi R, Yanase Y, Tani M . Crosstalk between protein kinase A and the HOG pathway under impaired biosynthesis of complex sphingolipids in budding yeast. FEBS J. 2021; 289(3):766-786. DOI: 10.1111/febs.16188. View

17.

Fan Y, Shi F, Liu J, Dong J, Bui H, Peake D . Selective reduction in the sphingomyelin content of atherogenic lipoproteins inhibits their retention in murine aortas and the subsequent development of atherosclerosis. Arterioscler Thromb Vasc Biol. 2010; 30(11):2114-20. PMC: 3426833. DOI: 10.1161/ATVBAHA.110.213363. View

18.

Coetzee T, Fujita N, Dupree J, Shi R, Blight A, Suzuki K . Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell. 1996; 86(2):209-19. DOI: 10.1016/s0092-8674(00)80093-8. View

19.

Yamagata M, Obara K, Kihara A . Unperverted synthesis of complex sphingolipids is essential for cell survival under nitrogen starvation. Genes Cells. 2013; 18(8):650-9. DOI: 10.1111/gtc.12062. View

20.

Mao C, Xu R, Bielawska A, Szulc Z, Obeid L . Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide. J Biol Chem. 2000; 275(40):31369-78. DOI: 10.1074/jbc.M003683200. View