Yarrowia lipolytica AAL genes are involved in peroxisomal fatty acid activation

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 7, 2016, Pages 555-565

  Dulermo, Rémi ^a   Gamboa Meléndez, Heber ^a   Ledesma Amaro, Rodrigo ^a   Thevenieau, France ^b   Nicaud, Jean Marc ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b SOFIPROTEOL   (France)

Author keywords

FAA1; Fatty acid activation; Fatty acyl CoA synthetases; Peroxisome; Yarrowia

Indexed keywords

ADENOSINE TRIPHOSPHATE; FATTY ACID; LONG CHAIN FATTY ACID COENZYME A LIGASE; OLEIC ACID; SHORT CHAIN FATTY ACID; ADENINE NUCLEOTIDE TRANSLOCASE; CELL RECEPTOR; COENZYME A LIGASE; FAT DROPLET; FUNGAL PROTEIN; ISOENZYME; PEROXISOME-TARGETING SIGNAL 1 RECEPTOR;

AAL GENE; ANT1 GENE; ARTICLE; CYTOPLASM; ENZYME SPECIFICITY; FAA1 GENE; FATTY ACID OXIDATION; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE OVEREXPRESSION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; UPREGULATION; YARROWIA LIPOLYTICA; AMINO ACID SEQUENCE; CHEMISTRY; DEFICIENCY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYLOGENY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL; YARROWIA;

ADENINE NUCLEOTIDE TRANSLOCATOR 1; AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; COENZYME A LIGASES; FATTY ACIDS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; ISOENZYMES; LIPID DROPLETS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PEROXISOMES; PHYLOGENY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; YARROWIA;

EID: 84964324550     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.04.002     Document Type: Article

References (55)

1. A.M. Anterola, and N.G. Lewis Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity Phytochemistry 61 2002 221 294
2. C. de Azevedo Souza, S.S. Kim, S. Koch, L. Kienow, K. Schneider, S.M. McKim, G.W. Haughn, E. Kombrink, and C.J. Douglas A novel fatty acyl-CoA synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis Plant Cell 21 2009 507 525
3. G. Barth, and C. Gaillardin Yarrowia lipolytica K. Wolf, Non Conventional Yeasts in Biotechnology Vol. 1 1996 Springer Berlin, Germany 313 388
4. A. Beopoulos, Z. Mrozova, F. Thevenieau, M.T. Le Dall, I. Hapala, S. Papanikolaou, T. Chardot, and J.M. Nicaud Control of lipid accumulation in the yeast Yarrowia lipolytica Appl. Environ. Microbiol. 74 2008 7779 7789
5. A. Beopoulos, J.M. Nicaud, and C. Gaillardin An overview of lipid metabolism in yeasts and its impact on biotechnological processes Appl. Microbiol. Biotechnol. 90 2011 1193 1206
6. M.A. van den Berg, P. de Jong-Gubbels, C.J. Kortland, J.P. van Dijken, J.T. Pronk, and H.Y. Steensma The two acetyl-coenzyme A synthetases of Saccharomyces cerevisiae differ with respect to kinetic properties and transcriptional regulation J. Biol. Chem. 271 1996 28953 28959
7. P.N. Black, and C.C. DiRusso Yeast acyl-CoA synthetases at the crossroads of fatty acid metabolism and regulation Biochim. Biophys. Acta 1771 2007 286 298
8. C.A. Boulton, and C. Ratledge ATP: citrate lyase - the regulatory enzyme for lipid biosynthesis in Lipomyces starkeyi? Microbiology 127 1981 423 426
9. J. Browse, P.J. McCourt, and C.R. Somerville Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue Anal. Biochem. 152 1986 141 145
10. F. Corpet Multiple sequence alignment with hierarchical clustering Nucleic Acids Res. 16 1988 10881 10890
11. M.A. Costa, D.L. Bedgar, S.G. Moinuddin, K.W. Kim, C.L. Cardenas, F.C. Cochrane, J.M. Shockey, G.L. Helms, Y. Amakura, H. Takahashi, J.K. Milhollan, L.B. Davin, J. Browse, and N.G. Lewis Characterization in vitro and in vivo of the putative multigene 4-coumarate:CoA ligase network in Arabidopsis: syringyl lignin and sinapate/sinapyl alcohol derivative formation Phytochemistry 66 2005 2072 2091
12. R. Dulermo, H. Gamboa-Meléndez, T. Dulermo, F. Thevenieau, and J.M. Nicaud The fatty acid transport protein Fat1p is involved in the export of fatty acids from lipid bodies in Yarrowia lipolytica FEMS Yeast Res. 14 2014 883 896
13. R. Dulermo, H. Gamboa-Meléndez, R. Ledesma-Amaro, F. Thévenieau, and J.M. Nicaud Unraveling fatty acid transport and activation mechanisms in Yarrowia lipolytica BBA Lipids 15 2015 1202 1217
14. R. Dulermo, H. Gamboa-Meléndez, S. Michely, F. Thevenieau, C. Neuvéglise, and J.M. Nicaud The evolution of Jen3 proteins and their role in dicarboxylic acid transport in Yarrowia Microbiol. Open 4 2015 100 120
15. R. Dulermo, T. Dulermo, H. Gamboa-Meléndez, F. Thevenieau, and J.M. Nicaud Role of Pex11p in lipid homeostasis in Yarrowia lipolytica, Eukaryot Cell 14 2015 511 525
16. T. Dulermo, Z. Lazar, R. Dulermo, M. Rakicka, R. Haddouche, and J.M. Nicaud Analysis of ATP-citrate lyase and malic enzyme mutants of Yarrowia lipolytica points out the importance of mannitol metabolism in fatty acid synthesis Biochim. Biophys. Acta 1851 2015 1107 1117
17. R.J. Duronio, L.J. Knoll, and J.I. Gordon Isolation of a Saccharomyces cerevisiae long chain fatty acyl:CoA synthetase gene (FAA1) and assessment of its role in protein N-myristoylation J. Cell Biol. 117 1992 515 529
18. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797
19. P. Fickers, M.T. Le Dall, C. Gaillardin, P. Thonart, and J.M. Nicaud New disruption cassettes for rapid gene disruption and marker rescue in the yeast Yarrowia lipolytica J. Microbiol. Methods 55 2003 727 737
20. F. Gabriel, I. Accoceberry, J.J. Bessoule, B. Salin, M. Lucas-Guérin, S. Manon, K. Dementhon, and T. Noël A Fox2-dependent fatty acid ß-oxidation pathway coexists both in peroxisomes and mitochondria of the ascomycete yeast Candida lusitaniae PLoS One 9 2014 e114531
21. E.H. Hettema, C.W. van Roermund, B. Distel, M. van den Berg, C. Vilela, C. Rodrigues-Pousada, R.J. Wanders, and H.F. Tabak The ABC transporter proteins Pat1 and Pat2 are required for import of long-chain fatty acids into peroxisomes of Saccharomyces cerevisiae EMBO J. 15 1996 3813 3822
22. R. Haddouche, S. Delessert, J. Sabirova, C. Neuvéglise, Y. Poirier, and J.M. Nicaud Roles of multiple acyl-CoA oxidases in the routing of carbon flow towards β-oxidation and polyhydroxyalkanoate biosynthesis in Yarrowia lipolytica FEMS Yeast Res. 10 2010 917 927
23. Y. Hu, Y. Gai, L. Yin, X. Wang, C. Feng, L. Feng, D. Li, X.N. Jiang, and D.C. Wang Crystal structures of a Populus tomentosa 4-coumarate:CoA ligase shed light on its enzymatic mechanisms Plant Cell 22 2010 3093 3104
24. D.R. Johnson, L.J. Knoll, N. Rowley, and J.I. Gordon Genetic analysis of the role of Saccharomyces cerevisiae acyl-CoA synthetase genes in regulating protein N-myristoylation J. Biol. Chem. 269 1994 18037 18046
25. D.R. Johnson, L.J. Knoll, D.E. Levin, and J.I. Gordon Saccharomyces cerevisiae contains four fatty acid activation (FAA) genes: an assessment of their role in regulating protein N-myristoylation and cellular lipid metabolism J. Cell Biol. 127 1994 751 762
26. P. Kabran, T. Rossignol, C. Gaillardin, J.M. Nicaud, and C. Neuvéglise Alternative splicing regulates targeting of malate dehydrogenase in Yarrowia lipolytica DNA Res. 19 2012 231 244
27. L. Kienow, K. Schneider, M. Bartsch, H.P. Stuible, H. Weng, O. Miersch, C. Wasternack, and E. Kombrink Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana J. Exp. Bot. 59 2008 403 419
28. L.J. Knoll, D.R. Johnson, and J.I. Gordon Complementation of Saccharomyces cerevisiae strains containing fatty acid activation gene (FAA) deletions with a mammalian acyl-CoA synthetase J. Biol. Chem. 270 1995 10861 10867
29. A.J. Koo, H.S. Chung, Y. Kobayashi, and G.A. Howe Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis J. Biol. Chem. 281 2006 33511 33520
30. M.T. Le Dall, J.M. Nicaud, and C. Gaillardin Multiple-copy integration in the yeast Yarrowia lipolytica Curr. Genet. 26 1994 38 44
31. M.H. Liang, and J.G. Jiang Advancing oleaginous microorganisms to produce lipid via metabolic engineering technology Prog. Lipid Res. 52 2013 395 408
32. A. Marchler-Bauer, J.B. Anderson, M.K. Derbyshire, C. DeWeese-Scott, N.R. Gonzales, M. Gwadz, L. Hao, S. He, D.I. Hurwitz, J.D. Jackson, Z. Ke, D. Krylov, C.J. Lanczycki, C.A. Liebert, C. Liu, F. Lu, S. Lu, G.H. Marchler, M. Mullokandov, J.S. Song, N. Thanki, R.A. Yamashita, J.J. Yin, D. Zhang, and S.H. Bryant CDD: a conserved domain database for interactive domain family analysis Nucleic Acids Res. 35 2007 D237 D240
33. K. Mlícková, E. Roux, K. Athenstaedt, S. d'Andrea, G. Daum, T. Chardot, and J.M. Nicaud Lipid accumulation, lipid body formation, and acyl coenzyme A oxidases of the yeast Yarrowia lipolytica Appl. Environ. Microbiol. 70 2004 3918 3924
34. N. Morin, X. Calcas, H. Devillers, P. Durrens, D.J. Sherman, J.M. Nicaud, and C. Neuvéglise Draft genome sequence of Rhodosporidium toruloides CECT1137, an oleaginous yeast of biotechnological interest Genome Announc. 2 2014 14 e00641
35. K. Natter, P. Leitner, A. Faschinger, H. Wolinski, S. McCraith, S. Fields, and S.D. Kohlwein The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy Mol. Cell. Proteomics 4 2005 662 672
36. Y. Oba, M. Ojika, and S. Inouye Firefly luciferase is a bifunctional enzyme: ATP-dependent monooxygenase and a long chain fatty acyl-CoA synthetase FEBS Lett. 540 2003 251 254
37. Y. Oba, M. Ojika, and S. Inouye Characterization of CG6178 gene product with high sequence similarity to firefly luciferase in Drosophila melanogaster Gene 329 2004 137 145
38. Y. Oba, M. Furuhashi, and S. Inouye Identification of a functional luciferase gene in the non-luminous diurnal firefly, Lucidina biplagiata Insect Mol. Biol. 19 2010 737 743
39. A. Querol, E. Barrio, T. Huerta, and D. Ramón Molecular monitoring of wine fermentations conducted by active dry yeast strains Appl. Environ. Microbiol. 58 1992 2948 2953
40. C. Ratledge Regulation of lipid accumulation in oleaginous micro-organisms Biochem. Soc. Trans. 30 2002 1047 1050
41. C.W. van Roermund, R. Drissen, M. van Den Berg, L. Ijlst, E.H. Hettema, H.F. Tabak, H.R. Waterham, and R.J. Wanders Identification of a peroxisomal ATP carrier required for medium-chain fatty acid β-oxidation and normal peroxisome proliferation in Saccharomyces cerevisiae Mol. Cell. Biol. 21 2001 4321 4329
42. C.W. van Roermund, L. Ijlst, W. Majczak, H.R. Waterham, H. Folkerts, R.J. Wanders, and K.J. Hellingwerf Peroxisomal fatty acid uptake mechanism in Saccharomyces cerevisiae J. Biol. Chem. 287 2012 20144 20153
43. J. Sambrook, T. Maniatis, and E.F. Fritsch Molecular Cloning: A Laboratory Manual second ed. 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York
44. K. Schneider, K. Hövel, K. Witzel, B. Hamberger, D. Schomburg, E. Kombrink, and H.P. Stuible The substrate specificity-determining amino acid code of 4-coumarate:CoA ligase Proc. Natl. Acad. Sci. U. S. A. 100 2003 8601 8606
45. K. Schneider, L. Kienow, E. Schmelzer, T. Colby, M. Bartsch, O. Miersch, C. Wasternack, E. Kombrink, and H.P. Stuible A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid J. Biol. Chem. 280 2005 13962 13972
46. K. Shashi, A.K. Bachhawat, and R. Joseph ATP:citrate lyase of Rhodotorula gracilis: purification and properties Biochim. Biophys. Acta 1033 1990 23 30
47. J.M. Shockey, M.S. Fulda, and J. Browse Arabidopsis contains a large superfamily of acyl-activating enzymes; phylogenetic and biochemical analysis reveals a new class of acyl-coenzyme A synthetases Plant Physiol. 132 2003 1065 1076
48. J. Shockey, and J. Browse Genome-level and biochemical diversity of the acyl-activating enzyme superfamily in plants Plant J. 66 2011 143 160
49. H.P. Stuible, and E. Kombrink Identification of the substrate specificity-conferring amino acid residues of 4-coumarate:coenzyme A ligase allows the rational design of mutant enzymes with new catalytic properties J. Biol. Chem. 276 2001 26893 26897
50. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: molecular evolutionary genetics analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729
51. Tenagy, J.S. Park, R. Iwama, S. Kobayashi, A. Ohta, H. Horiuchi, and R. Fukuda Involvement of acyl-CoA synthetase genes in n-alkane assimilation and fatty acid utilization in yeast Yarrowia lipolytica FEMS Yeast Res. 15 2015 (Epub 2015 May 27)
52. J. Wang, B. Zhang, and S. Chen Oleaginous yeast Yarrowia lipolytica mutants with a disrupted fatty acyl-CoA synthetase gene accumulate saturated fatty acid Process Biochem. 46 2011 1436 1441
53. P.A. Watkins, D. Maiguel, Z. Jia, and J. Pevsner Evidence for 26 distinct acyl-coenzyme A synthetase genes in the human genome J. Lipid Res. 48 2007 2736 2750
54. X. Xu, P. Gopalacharyulu, T. Seppänen-Laakso, A.L. Ruskeepää, C.C. Aye, B.P. Carson, S. Mora, M. Orešič, and A.A. Teleman Insulin signaling regulates fatty acid catabolism at the level of CoA activation PLoS Genet. 8 2012 e1002478
55. Z. Zou, F. Tong, N.J. Faergeman, C. Børsting, P.N. Black, and C.C. DiRusso Vectorial acylation in Saccharomyces cerevisiae. Fat1p and fatty acyl-CoA synthetase are interacting components of a fatty acid import complex J. Biol. Chem. 278 2003 16414 16422