The yeast Magmas ortholog Pam16 has an essential function in fermentative growth that involves sphingolipid metabolism

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Short, Mary K ^a   Hallett, Joshua P ^a   Tar, Krisztina ^a   Dange, Thomas ^a   Schmidt, Marion ^a   Moir, Robyn ^a   Willis, Ian M ^a   Jubinsky, Paul T ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; C18 ALPHA HYDROXY PHYTOCERAMIDE; CERAMIDE DERIVATIVE; GLUCOSE; GLYCEROL; MAGMA PROTEIN; MITOCHONDRIAL PROTEIN; OLEIC ACID; PROTEIN PAM16; SPHINGOLIPID; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; FEN1 GENE; FERMENTATION; FUNGUS GROWTH; G1 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; GENE FUNCTION; GENE INTERACTION; GENE MUTATION; GROWTH INHIBITION; IPT1 GENE; ISC1 GENE; LIPID METABOLISM; MITOCHONDRION; NONHUMAN; ORTHOLOGY; PEROXISOME; PLEIOTROPY; SKN1 GENE; SUPPRESSOR GENE; SUR4 GENE; TEMPERATURE SENSITIVITY;

ACETYLTRANSFERASES; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; FERMENTATION; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPHINGOLIPIDS; TEMPERATURE;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84863659982     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039428     Document Type: Article

References (93)

1. Jubinsky PT, Messer A, Bender J, Morris RE, Ciraolo GM, et al. (2001) Identification and characterization of Magmas, a novel mitochondria-associated protein involved in granulocyte-macrophage colony-stimulating factor signal transduction. Exp Hematol 29: 1392-1402.
2. Peng J, Huang CH, Short MK, Jubinsky PT, (2005) Magmas gene structure and evolution. In Silico Biol 5: 251-263.
3. Becker S, Gehrsitz A, Bork P, Buchner S, Buchner E, (2001) The black-pearl gene of Drosophila defines a novel conserved protein family and is required for larval growth and survival. Gene 262: 15-22.
4. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
5. Gonczy P, Echeverri C, Oegema K, Coulson A, Jones SJ, et al. (2000) Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408: 331-336.
6. Jubinsky PT, Short MK, Mutema G, Witte DP, (2003) Developmental expression of Magmas in murine tissues and its co-expression with the GM-CSF receptor. J Histochem Cytochem 51: 585-596.
7. Jubinsky PT, Short MK, Mutema G, Morris RE, Ciraolo GM, et al. (2005) Magmas expression in neoplastic human prostate. J Mol Histol 36: 69-75.
8. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, et al. (2007) Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 13: 3207-3214.
9. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, et al. (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347: 1999-2009.
10. Kawano T, Sugawara S, Hosono M, Tatsuta T, Nitta K, (2008) Alteration of gene expression induced by Silurus asotus lectin in Burkitt's lymphoma cells. Biol Pharm Bull 31: 998-1002.
11. Tagliati F, Gentilin E, Buratto M, Mole D, degli Uberti EC, et al. (2010) Magmas, a gene newly identified as overexpressed in human and mouse ACTH-secreting pituitary adenomas, protects pituitary cells from apoptotic stimuli. Endocrinology 151: 4635-4642.
12. Elsner S, Simian D, Iosefson O, Marom M, Azem A, (2009) The mitochondrial protein translocation motor: Structural conservation between the human and yeast Tim14/Pam18-Tim16/Pam16 co-chaperones. Int J Mol Sci 10: 2041-2053.
13. Sinha D, Joshi N, Chittoor B, Samji P, D'Silva P, (2010) Role of Magmas in protein transport and human mitochondria biogenesis. Hum Mol Genet 19: 1248-1262.
14. Frazier AE, Dudek J, Guiard B, Voos W, Li Y, et al. (2004) Pam16 has an essential role in the mitochondrial protein import motor. Nat Struct Mol Biol 11: 226-233.
15. Kozany C, Mokranjac D, Sichting M, Neupert W, Hell K, (2004) The J domain-related cochaperone Tim16 is a constituent of the mitochondrial TIM23 preprotein translocase. Nat Struct Mol Biol 11: 234-241.
16. D'Silva PR, Schilke B, Walter W, Craig EA, (2005) Role of Pam16′s degenerate J domain in protein import across the mitochondrial inner membrane. Proc Natl Acad Sci U S A 102: 12419-12424.
17. Hutu DP, Guiard B, Chacinska A, Becker D, Pfanner N, et al. (2008) Mitochondrial protein import motor: differential role of Tim44 in the recruitment of Pam17 and J-complex to the presequence translocase. Mol Biol Cell 19: 2642-2649.
18. Pais JE, Schilke B, Craig EA, (2011) Reevaluation of the role of the Pam18:Pam16 interaction in translocation of proteins by the mitochondrial Hsp70-based import motor. Mol Biol Cell 22: 4740-4749.
19. Li Y, Dudek J, Guiard B, Pfanner N, Rehling P, et al. (2004) The presequence translocase-associated protein import motor of mitochondria. Pam16 functions in an antagonistic manner to Pam18. J Biol Chem 279: 38047-38054.
20. Mokranjac D, Berg A, Adam A, Neupert W, Hell K, (2007) Association of the Tim14.Tim16 subcomplex with the TIM23 translocase is crucial for function of the mitochondrial protein import motor. J Biol Chem 282: 18037-18045.
21. 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.
22. Oh CS, Toke DA, Mandala S, Martin CE, (1997) ELO2 and ELO3, homologues of the Saccharomyces cerevisiae ELO1 gene, function in fatty acid elongation and are required for sphingolipid formation. J Biol Chem 272: 17376-17384.
23. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, et al. (2012) Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res 40: D700-705.
24. Wiedemann N, van der Laan M, Hutu DP, Rehling P, Pfanner N, (2007) Sorting switch of mitochondrial presequence translocase involves coupling of motor module to respiratory chain. J Cell Biol 179: 1115-1122.
25. Barrell D, Dimmer E, Huntley RP, Binns D, O'Donovan C, et al. (2009) The GOA database in 2009-an integrated Gene Ontology Annotation resource. Nucleic Acids Res 37: D396-403.
26. Hiltunen JK, Schonauer MS, Autio KJ, Mittelmeier TM, Kastaniotis AJ, et al. (2009) Mitochondrial fatty acid synthesis type II: more than just fatty acids. J Biol Chem 284: 9011-9015.
27. Schonauer MS, Kastaniotis AJ, Hiltunen JK, Dieckmann CL, (2008) Intersection of RNA processing and the type II fatty acid synthesis pathway in yeast mitochondria. Mol Cell Biol 28: 6646-6657.
28. Schonauer MS, Kastaniotis AJ, Kursu VA, Hiltunen JK, Dieckmann CL, (2009) Lipoic acid synthesis and attachment in yeast mitochondria. J Biol Chem 284: 23234-23242.
29. Jiang F, Ryan MT, Schlame M, Zhao M, Gu Z, et al. (2000) Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J Biol Chem 275: 22387-22394.
30. Chen S, Tarsio M, Kane PM, Greenberg ML, (2008) Cardiolipin mediates cross-talk between mitochondria and the vacuole. Mol Biol Cell 19: 5047-5058.
31. Tamura Y, Endo T, Iijima M, Sesaki H, (2009) Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J Cell Biol 185: 1029-1045.
32. Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, et al. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278: 52873-52880.
33. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, et al. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581-592.
34. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, et al. (2005) Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605.
35. de Nadal E, Zapater M, Alepuz PM, Sumoy L, Mas G, et al. (2004) The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 427: 370-374.
36. Sertil O, Vemula A, Salmon SL, Morse RH, Lowry CV, (2007) Direct role for the Rpd3 complex in transcriptional induction of the anaerobic DAN/TIR genes in yeast. Mol Cell Biol 27: 2037-2047.
37. Chan NC, Lithgow T, (2008) The peripheral membrane subunits of the SAM complex function codependently in mitochondrial outer membrane biogenesis. Mol Biol Cell 19: 126-136.
38. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, et al. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325: 477-481.
39. Young JC, Hoogenraad NJ, Hartl FU, (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112: 41-50.
40. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, et al. (2000) Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19: 2444-2451.
41. Tatsuta T, Model K, Langer T, (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16: 248-259.
42. Leonhard K, Stiegler A, Neupert W, Langer T, (1999) Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature 398: 348-351.
43. Dunn CD, Lee MS, Spencer FA, Jensen RE, (2006) A genomewide screen for petite-negative yeast strains yields a new subunit of the i-AAA protease complex. Mol Biol Cell 17: 213-226.
44. van der Laan M, Chacinska A, Lind M, Perschil I, Sickmann A, et al. (2005) Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol Cell Biol 25: 7449-7458.
45. Vizeacoumar FJ, Torres-Guzman JC, Bouard D, Aitchison JD, Rachubinski RA, (2004) Pex30p, Pex31p, and Pex32p form a family of peroxisomal integral membrane proteins regulating peroxisome size and number in Saccharomyces cerevisiae. Mol Biol Cell 15: 665-677.
46. Vizeacoumar FJ, Torres-Guzman JC, Tam YY, Aitchison JD, Rachubinski RA, (2003) YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size, and distribution in Saccharomyces cerevisiae. J Cell Biol 161: 321-332.
47. Dickson RC, (2010) Roles for sphingolipids in Saccharomyces cerevisiae. Adv Exp Med Biol 688: 217-231.
48. Sawai H, Okamoto Y, Luberto C, Mao C, Bielawska A, et al. (2000) Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J Biol Chem 275: 39793-39798.
49. Kitagaki H, Cowart LA, Matmati N, Montefusco D, Gandy J, et al. (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.
50. Kitagaki H, Cowart LA, Matmati N, Vaena de Avalos S, Novgorodov SA, et al. (2007) Isc1 regulates sphingolipid metabolism in yeast mitochondria. Biochim Biophys Acta 1768: 2849-2861.
51. Dickson RC, Nagiec EE, Wells GB, Nagiec MM, Lester RL, (1997) Synthesis of mannose-(inositol-P)2-ceramide, the major sphingolipid in Saccharomyces cerevisiae, requires the IPT1 (YDR072c) gene. J Biol Chem 272: 29620-29625.
52. Thevissen K, Idkowiak-Baldys J, Im YJ, Takemoto J, Francois IE, et al. (2005) SKN1, a novel plant defensin-sensitivity gene in Saccharomyces cerevisiae, is implicated in sphingolipid biosynthesis. FEBS Lett 579: 1973-1977.
53. Thevissen K, Yen WL, Carmona-Gutierrez D, Idkowiak-Baldys J, Aerts AM, et al. (2010) Skn1 and Ipt1 negatively regulate autophagy in Saccharomyces cerevisiae. FEMS Microbiol Lett 303: 163-168.
54. Zaman S, Lippman SI, Zhao X, Broach JR, (2008) How Saccharomyces responds to nutrients. Annu Rev Genet 42: 27-81.
55. Busti S, Coccetti P, Alberghina L, Vanoni M, (2010) Glucose signaling-mediated coordination of cell growth and cell cycle in Saccharomyces cerevisiae. Sensors (Basel) 10: 6195-6240.
56. Dickson RC, (2008) Thematic review series: sphingolipids. New insights into sphingolipid metabolism and function in budding yeast. J Lipid Res 49: 909-921.
57. Delgado A, Casas J, Llebaria A, Abad JL, Fabrias G, (2006) Inhibitors of sphingolipid metabolism enzymes. Biochim Biophys Acta 1758: 1957-1977.
58. Westermann B, Neupert W, (2000) Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16: 1421-1427.
59. Saleem RA, Long-O'Donnell R, Dilworth DJ, Armstrong AM, Jamakhandi AP, et al. (2010) Genome-wide analysis of effectors of peroxisome biogenesis. PLoS One 5: e11953.
60. Saleem RA, Rogers RS, Ratushny AV, Dilworth DJ, Shannon PT, et al. (2010) Integrated phosphoproteomics analysis of a signaling network governing nutrient response and peroxisome induction. Mol Cell Proteomics 9: 2076-2088.
61. Einerhand AW, Voorn-Brouwer TM, Erdmann R, Kunau WH, Tabak HF, (1991) Regulation of transcription of the gene coding for peroxisomal 3-oxoacyl-CoA thiolase of Saccharomyces cerevisiae. Eur J Biochem 200: 113-122.
62. Vaena de Avalos S, Su X, Zhang M, Okamoto Y, Dowhan W, et al. (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.
63. Gault CR, Obeid LM, Hannun YA, (2010) An overview of sphingolipid metabolism: from synthesis to breakdown. Adv Exp Med Biol 688: 1-23.
64. 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.
65. Hannun YA, Obeid LM, (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150.
66. Roy S, Short MK, Stanley ER, Jubinsky PT, (2012) Essential Role of Drosophila black-pearl is Mediated by its Effects on Mitochondrial Respiration. FASEB J.
67. Perkins GA, Renken CW, van der Klei IJ, Ellisman MH, Neupert W, et al. (2001) Electron tomography of mitochondria after the arrest of protein import associated with Tom19 depletion. Eur J Cell Biol 80: 139-150.
68. Gaspar ML, Jesch SA, Viswanatha R, Antosh AL, Brown WJ, et al. (2008) A block in endoplasmic reticulum-to-Golgi trafficking inhibits phospholipid synthesis and induces neutral lipid accumulation. J Biol Chem 283: 25735-25751.
69. Schuck S, Prinz WA, Thorn KS, Voss C, Walter P, (2009) Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 187: 525-536.
70. Bleve G, Di Sansebastiano GP, Grieco F, (2011) Over-expression of functional Saccharomyces cerevisiae GUP1, induces proliferation of intracellular membranes containing ER and Golgi resident proteins. Biochim Biophys Acta 1808: 733-744.
71. Shechtman CF, Henneberry AL, Seimon TA, Tinkelenberg AH, Wilcox LJ, et al. (2011) Loss of subcellular lipid transport due to ARV1 deficiency disrupts organelle homeostasis and activates the unfolded protein response. J Biol Chem.
72. Hiltunen JK, Mursula AM, Rottensteiner H, Wierenga RK, Kastaniotis AJ, et al. (2003) The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 27: 35-64.
73. Guan XL, Souza CM, Pichler H, Dewhurst G, Schaad O, et al. (2009) Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol Biol Cell 20: 2083-2095.
74. Sims KJ, Spassieva SD, Voit EO, Obeid LM, (2004) Yeast sphingolipid metabolism: clues and connections. Biochem Cell Biol 82: 45-61.
75. Plesofsky NS, Levery SB, Castle SA, Brambl R, (2008) Stress-induced cell death is mediated by ceramide synthesis in Neurospora crassa. Eukaryot Cell 7: 2147-2159.
76. Haak D, Gable K, Beeler T, Dunn T, (1997) Hydroxylation of Saccharomyces cerevisiae ceramides requires Sur2p and Scs7p. J Biol Chem 272: 29704-29710.
77. 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.
78. Wu BX, Clarke CJ, Matmati N, Montefusco D, Bartke N, et al. (2011) Identification of novel anionic phospholipid binding domains in neutral sphingomyelinase 2 with selective binding preference. J Biol Chem 286: 22362-22371.
79. Claypool SM, (2009) Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim Biophys Acta 1788: 2059-2068.
80. Joshi AS, Zhou J, Gohil VM, Chen S, Greenberg ML, (2009) Cellular functions of cardiolipin in yeast. Biochim Biophys Acta 1793: 212-218.
81. Jubinsky PT, Short MK, Ghanem M, Das BC, (2011) Design, synthesis, and biological activity of novel Magmas inhibitors. Bioorg Med Chem Lett 21: 3479-3482.
82. Scatena R, (2012) Mitochondria and cancer: a growing role in apoptosis, cancer cell metabolism and dedifferentiation. Adv Exp Med Biol 942: 287-308.
83. Ward PS, Thompson CB, (2012) Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 21: 297-308.
84. Fox TD, Folley LS, Mulero JJ, McMullin TW, Thorsness PE, et al. (1991) Analysis and manipulation of yeast mitochondrial genes. Methods Enzymol 194: 149-165.
85. Thomas BJ, Rothstein R, (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56: 619-630.
86. Boeke JD, Trueheart J, Natsoulis G, Fink GR, (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 154: 164-175.
87. Tong AH, Boone C, (2007) High-Throughput Construction and systematic synthetic lethal screening in saccharomyces cerevisae. Methods in Microbiology 36: 369-386.
88. Tong AH, Lesage G, Bader GD, Ding H, Xu H, et al. (2004) Global mapping of the yeast genetic interaction network. Science 303: 808-813.
89. Tong AH, Boone C, (2006) Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313: 171-192.
90. Piper PW, Curran B, Davies MW, Lockheart A, Reid G, (1986) Transcription of the phosphoglycerate kinase gene of Saccharomyces cerevisiae increases when fermentative cultures are stressed by heat-shock. Eur J Biochem 161: 525-531.
91. Bielawski J, Szulc ZM, Hannun YA, Bielawska A, (2006) Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39: 82-91.
92. Vaden DL, Gohil VM, Gu Z, Greenberg ML, (2005) Separation of yeast phospholipids using one-dimensional thin-layer chromatography. Anal Biochem 338: 162-164.
93. Breitkreutz BJ, Stark C, Tyers M, (2003) Osprey: a network visualization system. Genome Biol 4: R22.