Distinct signaling roles of ceramide species in yeast revealed through systematic perturbation and systems biology analyses

Science Signaling

Volumn 6, Issue 299, 2013, Pages

  Montefusco, David J ^a   Chen, Lujia ^b   Matmati, Nabil ^a,c   Lu, Songjian ^b   Newcomb, Benjamin ^a,c   Cooper, Gregory F ^b   Hannun, Yusuf A ^a,c   Lu, Xinghua ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDASE; CERAMIDE; MYRISTIC ACID; PALMITIC ACID; SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID; ALKALINE DIHYDROCERAMIDASE, S CEREVISIAE; AMIDASE; DIHYDROCERAMIDE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTOME;

ARTICLE; BIOSYNTHESIS; CORRELATION COEFFICIENT; FUNGAL STRAIN; FUNGUS CULTURE; GENOMICS; GENOTYPE; HEAT STRESS; HYDROXYLATION; IRON TRANSPORT; LIPID METABOLISM; LIPIDOMICS; MASS SPECTROMETRY; MICROARRAY ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; SYSTEMS BIOLOGY; TRANSCRIPTOMICS; WILD TYPE; YEAST CELL; CHEMICAL STRUCTURE; CHEMISTRY; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; HEAT; METABOLISM; METHODOLOGY; MUTATION; PHYSIOLOGICAL STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMIDOHYDROLASES; CERAMIDASES; CERAMIDES; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION, FUNGAL; GENE ONTOLOGY; HOT TEMPERATURE; LIPID METABOLISM; MOLECULAR STRUCTURE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; STRESS, PHYSIOLOGICAL; SYSTEMS BIOLOGY; TRANSCRIPTOME;

EID: 84887214282     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004515     Document Type: Article

References (45)

1. Y. A. Hannun, L. M. Obeid, Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150 (2008).
2. T. Kolter, A view on sphingolipids and disease. Chem. Phys. Lipids 164, 590-606 (2011).
3. Y. A. Hannun, L. M. Obeid, Many ceramides. J. Biol. Chem. 286, 27855-27862 (2011).
4. T. D. Mullen, S. Spassieva, R. W. Jenkins, K. Kitatani, J. Bielawski, Y. A. Hannun, L. M. Obeid, Selective knockdown of ceramide synthases reveals complex interregulation of sphingolipid metabolism. J. Lipid Res. 52, 68-77 (2011).
5. S. D. Spassieva, M. Rahmaniyan, J. Bielawski, C. J. Clarke, J. M. Kraveka, L. M. Obeid, Cell density-dependent reduction of dihydroceramide desaturase activity in neuroblastoma cells. J. Lipid Res. 53, 918-928 (2012).
6. L. A. Cowart, M. Shotwell, M. L. Worley, A. J. Richards, D. J. Montefusco, Y. A. Hannun, X. Lu, Revealing a signaling role of phytosphingosine-1-phosphate in yeast. Mol. Syst. Biol. 6, 349 (2010).
7. G. B. Wells, R. C. Dickson, R. L. Lester, Heat-induced elevation of ceramide in Saccharomyces cerevisiae via de novo synthesis. J. Biol. Chem. 273, 7235-7243 (1998).
8. L. A. Cowart, Y. A. Hannun, Selective substrate supply in the regulation of yeast de novo sphingolipid synthesis. J. Biol. Chem. 282, 12330-12340 (2007).
9. L. A. Cowart, Y. Okamoto, F. R. Pinto, J. L. Gandy, J. S. Almeida, Y. A. Hannun, Roles for sphingolipid biosynthesis in mediation of specific programs of the heat stress response determined through gene expression profiling. J. Biol. Chem. 278, 30328-30338 (2003).
10. G. M. Jenkins, Y. A. Hannun, Role for de novo sphingoid base biosynthesis in the heat-induced transient cell cycle arrest of Saccharomyces cerevisiae. J. Biol. Chem. 276, 8574-8581 (2001).
11. N. Matmati, H. Kitagaki, D. Montefusco, B. K. Mohanty, Y. A. Hannun, Hydroxyurea sensitivity reveals a role for ISC1 in the regulation of G2/M. J. Biol. Chem. 284, 8241-8246 (2009).
12. L. A. Cowart, J. L. Gandy, B. Tholanikunnel, Y. A. Hannun, Sphingolipids mediate formation of mRNA processing bodies during the heat-stress response of Saccharomyces cerevisiae. Biochem. J. 431, 31-38 (2010).
13. G. G. Guenther, E. R. Peralta, K. R. Rosales, S. Y. Wong, L. J. Siskind, A. L. Edinger, Ceramide starves cells to death by downregulating nutrient transporter proteins. Proc. Natl. Acad. Sci. U.S.A. 105, 17402-17407 (2008).
14. L. A. Cowart, Y. Okamoto, X. Lu, Y. A. Hannun, Distinct roles for de novo versus hydrolytic pathways of sphingolipid biosynthesis in Saccharomyces cerevisiae. Biochem. J. 393, 733-740 (2006).
15. J. Petschnigg, H. Wolinski, D. Kolb, G. n. Zellnig, C. F. Kurat, K. Natter, S. D. Kohlwein, Good fat, essential cellular requirements for triacylglycerol synthesis to maintain membrane homeostasis in yeast. J. Biol. Chem. 284, 30981-30993 (2009).
16. D. A. Toke, C. E. Martin, Isolation and characterization of a gene affecting fatty acid elongation in Saccharomyces cerevisiae. J. Biol. Chem. 271, 18413-18422 (1996).
17. W. Al-Feel, J.C. DeMar,S. J.Wakil, A Saccharomyces cerevisiae mutant strain defective in acetyl-CoA carboxylase arrests at the G2/M phase of the cell cycle. Proc. Natl. Acad. Sci. U.S.A. 100, 3095-3100 (2003).
18. N. Matmati, A. Metelli, K. Tripathi, S. Yan, B. K. Mohanty, Y. A. Hannun, Identification of c18:1-phytoceramide as the candidate lipid mediator for hydroxyurea resistance in yeast. J. Biol. Chem. 288, 17272-17284 (2013).
19. S. Monti, P. Tamayo, J. Mesirov, T. Golub, Consensus clustering: A resampling-based method for class discovery and visualization of gene expression microarray data. Mach. Learn. 52, 91-118 (2003).
20. T. I. Simpson, J. D. Armstrong, A. P. Jarman, Merged consensus clustering to assess and improve class discovery with microarray data. BMC Bioinformatics 11, 590 (2010).
21. C. J. Mousley, K. Tyeryar, K. E. Ile, G. Schaaf, R. L. Brost, C. Boone, X. Guan, M. R.Wenk, V. A. Bankaitis, Trans-Golgi network and endosome dynamics connect ceramide homeostasis with regulation of the unfolded protein response and TOR signaling in yeast. Mol. Biol. Cell 19, 4785-4803 (2008).
22. R. C. Dickson, C. Sumanasekera, R. L. Lester, Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid Res. 45, 447-465 (2006).
23. D. J. Klionsky, H. Abeliovich, P. Agostinis, D. K. Agrawal, G. Aliev, D. S. Askew, M. Baba, E. H. Baehrecke, B. A. Bahr, A. Ballabio, B. A. Bamber, D. C. Bassham, E. Bergamini, X. Bi, M. Biard-Piechaczyk, J. S. Blum, D. E. Bredesen, J. L. Brodsky, J. H. Brumell, U. T. Brunk, W. Bursch, N. Camougrand, E. Cebollero, F. Cecconi, Y. Chen, L. S. Chin, A. Choi, C. T. Chu, J. Chung, P. G. Clarke, R. S. Clark, S. G. Clarke, C. Clavé, J. L. Cleveland, P. Codogno, M. I. Colombo, A. Coto-Montes, J. M. Cregg, A. M. Cuervo, J. Debnath, F. Demarchi, P. B. Dennis, P. A. Dennis, V. Deretic, R. J. Devenish, F. Di Sano, J. F. Dice, M. Difiglia, S. Dinesh-Kumar, C. W. Distelhorst, M. Djavaheri-Mergny, F. C. Dorsey, W. Dröge, M. Dron, W. A. Dunn Jr., M. Duszenko, N. T. Eissa, Z. Elazar, A. Esclatine, E. L. Eskelinen, L. Fésüs, K. D. Finley, J. M. Fuentes, J. Fueyo, K. Fujisaki, B. Galliot, F. B. Gao, D. A. Gewirtz, S. B. Gibson, A. Gohla, A. L. Goldberg, R. Gonzalez, C. González- Estévez, S. Gorski, R. A. Gottlieb, D. Häussinger, Y. W. He, K. Heidenreich, J. A. Hill, M. Høyer-Hansen, X. Hu, W. P. Huang, A. Iwasaki, M. Jäättelä, W. T. Jackson, X. Jiang, S. Jin, T. Johansen, J. U. Jung, M. Kadowaki, C. Kang, A. Kelekar, D. H. Kessel, J. A. Kiel, H. P. Kim, A. Kimchi, T. J. Kinsella, K. Kiselyov, K. Kitamoto, E. Knecht, M. Komatsu, E. Kominami, S. Kondo, A. L. Kovács, G. Kroemer, C. Y. Kuan, R. Kumar, M. Kundu, J. Landry, M. Laporte,W. Le, H. Y. Lei, M. J. Lenardo, B. Levine, A. Lieberman, K. L. Lim, F. C. Lin, W. Liou, L. F. Liu, G. Lopez-Berestein, C. López-Otín, B. Lu, K. F. Macleod, W. Malorni, W. Martinet, K. Matsuoka, J. Mautner, A. J. Meijer, A. Meléndez, P. Michels, G. Miotto, W. P. Mistiaen, N. Mizushima, B. Mograbi, I. Monastyrska, M. N. Moore, P. I. Moreira, Y. Moriyasu, T. Motyl, C. Münz, L. O. Murphy, N. I. Naqvi, T. P. Neufeld, I. Nishino, R. A. Nixon, T. Noda, B. Nürnberg, M. Ogawa, N. L. Oleinick, L. J. Olsen, B. Ozpolat, S. Paglin, G. E. Palmer, I. Papassideri, M. Parkes, D. H. Perlmutter, G. Perry, M. Piacentini, R. Pinkas-Kramarski, M. Prescott, T. Proikas-Cezanne, N. Raben, A. Rami, F. Reggiori, B. Rohrer, D. C. Rubinsztein, K. M. Ryan, J. Sadoshima, H. Sakagami, Y. Sakai, M. Sandri, C. Sasakawa, M. Sass, C. Schneider, P. O. Seglen, O. Seleverstov, J. Settleman, J. J. Shacka, I. M. Shapiro, A. Sibirny, E. C. Silva-Zacarin, H. U. Simon, C. Simone, A. Simonsen, M. A. Smith, K. Spanel-Borowski, V. Srinivas, M. Steeves, H. Stenmark, P. E. Stromhaug, C. S. Subauste, S. Sugimoto, D. Sulzer, T. Suzuki, M. S. Swanson, I. Tabas, F. Takeshita, N. J. Talbot, Z. Tallóczy, K. Tanaka, K. Tanaka, I. Tanida, G. S. Taylor, J. P. Taylor, A. Terman, G. Tettamanti, C. B. Thompson, M. Thumm, A. M. Tolkovsky, S. A. Tooze, R. Truant, L. V. Tumanovska, Y. Uchiyama, T. Ueno, N. L. Uzcátegui, I. van der Klei, E. C. Vaquero, T. Vellai, M. W. Vogel, H. G. Wang, P.Webster, J.W.Wiley, Z. Xi, G. Xiao, J. Yahalom, J. M. Yang, G. Yap, X. M. Yin, T. Yoshimori, L. Yu, Z. Yue, M. Yuzaki, O. Zabirnyk, X. Zheng, X. Zhu, R. L. Deter, Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175 (2008).
24. M. Liu, C. Huang, S. R. Polu, R. Schneiter, A. Chang, Regulation of sphingolipid synthesis via Orm1 and Orm2 in yeast. J. Cell Sci. 125, 2428-2435 (2012).
25. D. N. Reshef, Y. A. Reshef, H. K. Finucane, S. R. Grossman, G. McVean, P. J. Turnbaugh, E. S. Lander, M. Mitzenmacher, P. C. Sabeti, Detecting novel associations in large data sets. Science 334, 1518-1524 (2011).
26. J. Storey, The positive false discovery rate: A Bayesian interpretation and the q-value. Ann. Statist. 31, 2013-2035 (2003).
27. P. Good, Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses (Springer, Berlin, 1994).
28. J. Friedman, T. Hastie, R. Tibshirani, Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1-22 (2010).
29. V. Chen, X. Lu, Conceptualization of molecular findings by mining gene annotations. BMC Proc., in press.
30. C. Mao, R. Xu, A. Bielawska, L. M. Obeid, Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity. J. Biol. Chem. 275, 6876-6884 (2000).
31. M. Sambade, M. Alba, A. M. Smardon, R. W. West, P. M. Kane, A genomic screen for yeast vacuolar membrane ATPase mutants. Genetics 170, 1539-1551 (2005).
32. G. Giaever, A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Véronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. André, A. P. Arkin, A. Astromoff, M. El-Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Güldener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kötter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M.Voet, G. Volckaert,C.Y.Wang, T.R.Ward, J.Wilhelmy, E.A.Winzeler,Y.Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, M. Johnston, Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391 (2002).
33. N. Mira, M. Teixeira, I. Sá-Correia, Adaptative response and tolerance to weak acid stress in Saccharomyces cerevisiae: A genome-wide view. OMICS 14, 525-540 (2010).
34. P. Motshwene, R. Karreman, G. Kgari, W. Brandt, G. Lindsey, LEA (late embryonic abundant)-like protein Hsp 12 (heat-shock protein 12) is present in the cell wall and enhances the barotolerance of the yeast Saccharomyces cerevisiae. Biochem. J. 377, 769-774 (2004).
35. R. J. Karreman, G. G. Lindsey, Modulation of Congo-red-induced aberrations in the yeast Saccharomyces cerevisiae by the general stress response protein Hsp12p. Can. J. Microbiol. 53, 1203-1210 (2007).
36. S. Li, S. Dean, Z. Li, J. Horecka, R. J. Deschenes, J. S. Fassler, The eukaryotic twocomponent histidine kinase Sln1p regulates OCH1 via the transcription factor, Skn7p. Mol. Biol. Cell 13, 412-424 (2002).
37. K. Brombacher, B. B. Fischer, K. Rüfenacht, R. I. L. Eggen, The role of Yap1p and Skn7p-mediated oxidative stress response in the defence of Saccharomyces cerevisiae against singlet oxygen. Yeast 23, 741-750 (2006).
38. C. Glymour, G. Cooper, Computation, Causation, and Discovery (MIT Press, Cambridge, MA, 1999).
39. M. A. Collart, S. Oliviero, Preparation of yeast RNA, in Current Protocols in Molecular Biology (John Wiley & Sons Inc., New York, 1993), pp. 13.12.1-13.12.5.
40. D. J. Montefusco, B. Newcomb, J. L. Gandy, S. E. Brice, N. Matmati, L. A. Cowart, Y. A. Hannun, Sphingoid bases and the serine catabolic enzyme CHA1 define a novel feedforward/feedback mechanism in the response to serine availability. J. Biol. Chem. 287, 9280-9289 (2012).
41. J. Bielawski, Z. M. Szulc, Y. A. Hannun, A. Bielawska, Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39, 82-91 (2006).
42. F. M. Ausubel, Short Protocols in Molecular Biology: A Compendium of Methods from Current Protocols in Molecular Biology (Wiley, New York, 2002).
43. H. Kitagaki, L. A. Cowart, N. Matmati, D. Montefusco, J. Gandy, S. V. de Avalos, S. A. Novgorodov, J. Zheng, L. M. Obeid, Y. A. Hannun, 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 (2009).
44. M. Ashburner, C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, G. Sherlock, Gene Ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29 (2000).
45. B. Muller, A. J. Richards, B. Jin, X. Lu, GOGrapher: A Python library for GO graph representation and analysis. BMC Res. Notes 2, 122 (2009).