The protein kinase Sch9 is a key regulator of sphingolipid metabolism in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 25, Issue 1, 2014, Pages 196-211

  Swinnen, Erwin ^a   Wilms, Tobias ^a   Idkowiak Baldys, Jolanta ^b   Smets, Bart ^a   De Snijder, Pepijn ^a   Accardo, Sabina ^a   Ghillebert, Ruben ^a   Thevissen, Karin ^a   Cammue, Bruno ^a   De Vos, Dirk ^a   Bielawski, Jacek ^b   Hannun, Yusuf A ^b   Winderickx, Joris ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUREOBASIDIN A; CERAMIDASE; CERAMIDE; INOSITOL; PHOSPHATE; PHOSPHOLIPASE C; SACCHAROMYCES CEREVISIAE PROTEIN; SPHINGOLIPID; THERMOZYMOCIDIN;

ARTICLE; FEEDBACK SYSTEM; IN VIVO STUDY; LIPID HYDROLYSIS; LIPID METABOLISM; LONGEVITY; NONHUMAN; NUTRIENT AVAILABILITY; OBSERVATIONAL STUDY; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ANTIFUNGAL AGENTS; CERAMIDES; DEPSIPEPTIDES; DRUG RESISTANCE, FUNGAL; FATTY ACIDS, MONOUNSATURATED; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPHINGOLIPIDS; SPHINGOSINE; TRANSCRIPTION, GENETIC; TYPE C PHOSPHOLIPASES;

EID: 84891772327     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-06-0340     Document Type: Article

References (80)

1. Aerts AM, Francois IE, Bammens L, Cammue BP, Smets B, Winderickx J, Accardo S, De Vos DE, Thevissen K (2006).Level of M(IP)2C sphingolipid affects plant defensin sensitivity, oxidative stress resistance and chronological life-span in yeast. FEBS Lett 580, 1903-1907.
2. Almeida T et al. (2008). Isc1p plays a key role in hydrogen peroxide resistance and chronological lifespan through modulation of iron levels and apoptosis. Mol Biol Cell 19, 865-876.
3. Barbosa AD, Osorio H, Sims KJ, Almeida T, Alves M, Bielawski J, Amorim MA, Moradas-Ferreira P, Hannun YA, Costa V (2011). Role for Sit4p-dependent mitochondrial dysfunction in mediating the shortened chronological lifespan and oxidative stress sensitivity of Isc1p-deficient cells. Mol Microbiol 81, 515-527.
4. Bikman BT, Summers SA (2011). Ceramides as modulators of cellular and whole-body metabolism. J Clin Invest 121, 4222-4230.
5. Birbes H, El Bawab S, Hannun YA, Obeid LM (2001). Selective hydrolysis of a mitochondrial pool of sphingomyelin induces apoptosis. FASEB J 15, 2669-2679.
6. Bligh EG, Dyer WJ (1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911-917.
7. 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.
8. Breslow DK, Collins SR, Bodenmiller B, Aebersold R, Simons K, Shevchenko A, Ejsing CS, Weissman JS (2010). Orm family proteins mediate sphingolipid homeostasis. Nature 463, 1048-1053.
9. Breslow DK, Weissman JS (2010). Membranes in balance: mechanisms of sphingolipid homeostasis. Mol Cell 40, 267-279.
10. Carmona-Gutierrez D et al. (2011). Ceramide triggers metacaspase- independent mitochondrial cell death in yeast. Cell Cycle 10, 3973-3978.
11. Chipuk JE, McStay GP, Bharti A, Kuwana T, Clarke CJ, Siskind LJ, Obeid LM, Green DR (2012). Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis. Cell 148, 988-1000.
12. Chung N, Mao C, Heitman J, Hannun YA, Obeid LM (2001). Phytosphingosine as a specific inhibitor of growth and nutrient import in Saccharomyces cerevisiae. J Biol Chem 276, 35614-35621.
13. Cowart LA, Shotwell M, Worley ML, Richards AJ, Montefusco DJ, Hannun YA, Lu X (2010). Revealing a signaling role of phytosphingosine-1-phosphate in yeast. Mol Syst Biol 6, 349.
14. Crauwels M, Donaton MC, Pernambuco MB, Winderickx J, de Winde JH, Thevelein JM (1997). The Sch9 protein kinase in the yeast Saccharomyces cerevisiae controls cAPK activity and is required for nitrogen activation of the fermentable-growth-medium-induced (FGM) pathway. Microbiology 143, 2627-2637.
15. Di Paola M, Cocco T, Lorusso M (2000). Ceramide interaction with the respiratory chain of heart mitochondria. Biochemistry 39, 6660-6668.
16. Dickson RC (2008). Thematic review series: sphingolipids. New insights into sphingolipid metabolism and function in budding yeast. J Lipid Res 49, 909-921.
17. Dickson RC (2010). Roles for sphingolipids in Saccharomyces cerevisiae. Adv Exp Med Biol 688, 217-231.
18. Dickson RC, Sumanasekera C, Lester RL (2006). Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45, 447-465.
19. Ella KM, Qi C, Dolan JW, Thompson RP, Meier KE (1997). Characterization of a sphingomyelinase activity in Saccharomyces cerevisiae. Arch Biochem Biophys 340, 101-110.
20. Fabrizio P, Pozza F, Pletcher SD, Gendron CM, Longo VD (2001). Regulation of longevity and stress resistance by Sch9 in yeast. Science 292, 288-290.
21. Funato K, Vallee B, Riezman H (2002). Biosynthesis and trafficking of sphingolipids in the yeast Saccharomyces cerevisiae. Biochemistry 41, 15105-15114.
22. Garcia-Ruiz C, Colell A, Mari M, Morales A, Fernandez-Checa JC (1997). Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J Biol Chem 272, 11369-11377.
23. Gudz TI, Tserng KY, Hoppel CL (1997).Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J Biol Chem 272, 24154-24158.
24. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S (2006). Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758, 2016-2026.
25. Han S, Lone MA, Schneiter R, Chang A (2010). Orm1 and Orm2 are conserved endoplasmic reticulum membrane proteins regulating lipid homeostasis and protein quality control. Proc Natl Acad Sci USA 107, 5851-5856.
26. Hannun YA, Obeid LM (2011). Many ceramides. J Biol Chem 286, 27855-27862.
27. Heidler SA, Radding JA (1995). The AUR1 gene in Saccharomyces cerevisiae encodes dominant resistance to the antifungal agent aureobasidin A (LY295337). Antimicrob Agents Chemother 39, 2765-2769.
28. Huang X, Liu J, Dickson RC (2012). Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet 8, e1002493.
29. ajiwara K, Muneoka T, Watanabe Y, Karashima T, Kitagaki H, Funato K (2012). Perturbation of sphingolipid metabolism induces endoplasmic reticulum stress-mediated mitochondrial apoptosis in budding yeast. Mol Microbiol 86, 1246-1261.
30. 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.
31. Kim S, Fyrst H, Saba J (2000). Accumulation of phosphorylated sphingoid long chain bases results in cell growth inhibition in Saccharomyces cerevisiae. Genetics 156, 1519-1529.
32. Kitagaki H, Cowart LA, Matmati N, Montefusco D, Gandy J, de Avalos SV, Novgorodov SA, Zheng J, Obeid LM, Hannun YA (2009). ISC1-dependent metabolic adaptation reveals an indispensable role for mitochondria in induction of nuclear genes during the diauxic shift in Saccharomyces cerevisiae. J Biol Chem 284, 10818-10830.
33. Kitagaki H, Cowart LA, Matmati N, Vaena de Avalos S, Novgorodov SA, Zeidan YH, Bielawski J, Obeid LM, Hannun YA (2007). Isc1 regulates sphingolipid metabolism in yeast mitochondria. Biochim Biophys Acta 1768, 2849-2861.
34. Klose C, Surma MA, Gerl MJ, Meyenhofer F, Shevchenko A, Simons K (2012). Flexibility of a eukaryotic lipidome-insights from yeast lipidomics. PLoS One 7, e35063.
35. Kobayashi SD, Nagiec MM (2003). Ceramide/long-chain base phosphate rheostat in Saccharomyces cerevisiae: regulation of ceramide synthesis by Elo3p and Cka2p. Eukaryot Cell 2, 284-294.
36. Lavoie H, Whiteway M (2008). Increased respiration in the sch9Delta mutant is required for increasing chronological life span but not replicative life span. Eukaryot Cell 7, 1127-1135.
37. Lester RL, Withers BR, Schultz MA, Dickson RC (2013). Iron, glucose and intrinsic factors alter sphingolipid composition as yeast cells enter stationary phase. Biochim Biophys Acta 1831, 726-736.
38. Levade T, Malagarie-Cazenave S, Gouaze V, Segui B, Tardy C, Betito S, Andrieu-Abadie N, Cuvillier O (2002). Ceramide in apoptosis: a revisited role. Neurochem Res 27, 601-607.
39. Liu J, Huang X, Withers BR, Blalock E, Liu K, Dickson RC (2013). Reducing sphingolipid synthesis orchestrates global changes to extend yeast lifespan. Aging Cell 12, 833-841.
40. Liu K, Zhang X, Lester RL, Dickson RC (2005). The sphingoid long chain base phytosphingosine activates AGC-type protein kinases in Saccharomyces cerevisiae including Ypk1, Ypk2, and Sch9. J Biol Chem 280, 22679-22687.
41. Liu M, Huang C, Polu SR, Schneiter R, Chang A (2012). Regulation of sphingolipid synthesis through Orm1 and Orm2 in yeast. J Cell Sci 125, 2428-2435.
42. Matmati N, Hannun YA (2008). Thematic review series: sphingolipids. ISC1 (inositol phosphosphingolipid-phospholipase C), the yeast homologue of neutral sphingomyelinases. J Lipid Res 49, 922-928.
43. Matmati N, Metelli A, Tripathi K, Yan S, Mohanty BK, Hannun YA (2013). Identification of C18:1-phytoceramide as the candidate lipid mediator for hydroxyurea resistance in yeast. J Biol Chem 288, 17272-17284.
44. McCourt PC, Morgan JM, Nickels JTJr (2009). Stress-induced ceramide-activated protein phosphatase can compensate for loss of amphiphysin-like activity in Saccharomyces cerevisiae and functions to reinitiate endocytosis. J Biol Chem 284, 11930-11941.
45. Miyake Y, Kozutsumi Y, Nakamura S, Fujita T, Kawasaki T (1995). Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem Biophys Res Commun 211, 396-403.
46. Nagiec MM, Nagiec EE, Baltisberger JA, Wells GB, Lester RL, Dickson RC (1997). Sphingolipid synthesis as a target for antifungal drugs. Complementation of the inositol phosphorylceramide synthase defect in a mutant strain of Saccharomyces cerevisiae by the AUR1 gene. J Biol Chem 272, 9809-9817.
47. Nickels JT, Broach JR (1996). A ceramide-activated protein phosphatase mediates ceramide-induced G1 arrest of Saccharomyces cerevisiae. Genes Dev 10, 382-394.
48. Okamoto M, Yoko-o T, Umemura M, Nakayama K, Jigami Y (2006). Glycosylphosphatidylinositol-anchored proteins are required for the transport of detergent-resistant microdomain-associated membrane proteins Tat2p and Fur4p. J Biol Chem 281, 4013-4023.
49. Olivera A, Kohama T, Edsall L, Nava V, Cuvillier O, Poulton S, Spiegel S (1999). Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J Cell Biol 147, 545-558.
50. Pan Y, Schroeder EA, Ocampo A, Barrientos A, Shadel GS (2011). Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab 13, 668-678.
51. Pan Y, Shadel GS (2009). Extension of chronological life span by reduced TOR signaling requires down-regulation of Sch9p and involves increased mitochondrial OXPHOS complex density. Aging (Albany NY) 1, 131-145.
52. Pascual-Ahuir A, Proft M (2007). Control of stress-regulated gene expression and longevity by the Sch9 protein kinase. Cell Cycle 6, 2445-2447.
53. Pedruzzi I, Dubouloz F, Cameroni E, Wanke V, Roosen J, Winderickx J, De Virgilio C (2003). TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell 12, 1607-1613.
54. Rego A, Costa M, Chaves SR, Matmati N, Pereira H, Sousa MJ, Moradas-Ferreira P, Hannun YA, Costa V, Corte-Real M (2012). Modulation of mitochondrial outer membrane permeabilization and apoptosis by ceramide metabolism. PLoS One 7, e48571.
55. Roelants FM, Breslow DK, Muir A, Weissman JS, Thorner J (2011). Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 108, 19222-19227.
56. Roelants FM, Torrance PD, Thorner J (2004). Differential roles of PDK1-and PDK2-phosphorylation sites in the yeast AGC kinases Ypk1, Pkc1 and Sch9. Microbiology 150, 3289-3304.
57. Roosen J, Engelen K, Marchal K, Mathys J, Griffioen G, Cameroni E, Thevelein JM, De Virgilio C, De Moor B, Winderickx J (2005). PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol Microbiol 55, 862-880.
58. Saddoughi SA, Song P, Ogretmen B (2008). Roles of bioactive sphingolipids in cancer biology and therapeutics. Subcell Biochem 49, 413-440.
59. Sawai H, Okamoto Y, Luberto C, Mao C, Bielawska A, Domae N, Hannun YA (2000). Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J Biol Chem 275, 39793-39798.
60. Serrano R, Ruiz A, Bernal D, Chambers JR, Arino J (2002). The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling. Mol Microbiol 46, 1319-1333.
61. Shimobayashi M, Oppliger W, Moes S, Jeno P, Hall MN (2013). TORC1-regulated protein kinase Npr1 phosphorylates Orm to stimulate complex sphingolipid synthesis. Mol Biol Cell 24, 870-881.
62. Sims KJ, Spassieva SD, Voit EO, Obeid LM (2004). Yeast sphingolipid metabolism: clues and connections. Biochem Cell Biol 82, 45-61.
63. Siskind LJ (2005). Mitochondrial ceramide and the induction of apoptosis. J Bioenerg Biomembr 37, 143-153.
64. Siskind LJ, Kolesnick RN, Colombini M (2002). Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins. J Biol Chem 277, 26796-26803.
65. Skrzypek MS, Nagiec MM, Lester RL, Dickson RC (1998). Inhibition of amino acid transport by sphingoid long chain bases in Saccharomyces cerevisiae. J Biol Chem 273, 2829-2834.
66. Smets B, De Snijder P, Engelen K, Joossens E, Ghillebert R, Thevissen K, Marchal K, Winderickx J (2008). Genome-wide expression analysis reveals TORC1-dependent and-independent functions of Sch9. FEMS Yeast Res 8, 1276-1288.
67. Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, Winderickx J (2010). Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae. Curr Genet 56, 1-32.
68. Stock SD, Hama H, Radding JA, Young DA, Takemoto JY (2000). Syringomycin E inhibition of Saccharomyces cerevisiae: requirement for biosynthesis of sphingolipids with very-long-chain fatty acids and mannose-and phosphoinositol-containing head groups. Antimicrob Agents Chemother 44, 1174-1180.
69. Sun Y, Miao Y, Yamane Y, Zhang C, Shokat KM, Takematsu H, Kozutsumi Y, Drubin DG (2012). Orm protein phosphoregulation mediates transient sphingolipid biosynthesis response to heat stress via the Pkh-Ypk and Cdc55-PP2A pathways. Mol Biol Cell 23, 2388-2398.
70. Sun Y, Taniguchi R, Tanoue D, Yamaji T, Takematsu H, Mori K, Fujita T, Kawasaki T, Kozutsumi Y (2000). Sli2 (Ypk1), a homologue of mammalian protein kinase SGK, is a downstream kinase in the sphingolipid-mediated signaling pathway of yeast. Mol Cell Biol 20, 4411-4419.
71. Swinnen E, Rosseels J, Winderickx J (2005). The minimum domain of Pho81 is not sufficient to control the Pho85-Rim15 effector branch involved in phosphate starvation-induced stress responses. Curr Genet 48, 18-33.
72. Thevissen K, Yen WL, Carmona-Gutierrez D, Idkowiak-Baldys J, Aerts AM, Francois IE, Madeo F, Klionsky DJ, Hannun YA, Cammue BP (2010). Skn1 and Ipt1 negatively regulate autophagy in Saccharomyces cerevisiae. FEMS Microbiol Lett 303, 163-168.
73. Toda T, Cameron S, Sass P, Wigler M (1988). SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits. Genes Dev 2, 517-527.
74. Urban J et al. (2007). Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell 26, 663-674.
75. Vaena de Avalos S, Okamoto Y, Hannun YA (2004). Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J Biol Chem 279, 11537-11545.
76. Vaena de Avalos S, Su X, Zhang M, Okamoto Y, Dowhan W, Hannun YA (2005). The phosphatidylglycerol/cardiolipin biosynthetic pathway is required for the activation of inositol phosphosphingolipid phospholipase C, Isc1p, during growth of Saccharomyces cerevisiae. J Biol Chem 280, 7170-7177.
77. Van Brocklyn JR, Williams JB (2012). The control of the balance between ceramide and sphingosine-1-phosphate by sphingosine kinase: oxidative stress and the seesaw of cell survival and death. Comp Biochem Physiol B Biochem Mol Biol 163, 26-36.
78. Voordeckers K, Kimpe M, Haesendonckx S, Louwet W, Versele M, Thevelein JM (2011). Yeast 3-phosphoinositide-dependent protein kinase-1 (PDK1) orthologs Pkh1-3 differentially regulate phosphorylation of protein kinase A (PKA) and the protein kinase B (PKB)/S6K ortholog Sch9. J Biol Chem 286, 22017-22027.
79. Wei M, Fabrizio P, Madia F, Hu J, Ge H, Li LM, Longo VD (2009). Tor1/Sch9-regulated carbon source substitution is as effective as calorie restriction in life span extension. PLoS Genet 5, e1000467.
80. Yorimitsu T, Zaman S, Broach JR, Klionsky DJ (2007). Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol Biol Cell 18, 4180-4189.