New insights into the peroxisomal protein inventory: Acyl-CoA oxidases and -dehydrogenases are an ancient feature of peroxisomes

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 1, 2015, Pages 111-125

  Camões, Fátima ^a   Islinger, Markus ^a,c   Guimarães, Sofia C ^a,b   Kilaru, Sreedhar ^b   Schuster, Martin ^b   Godinho, Luis F ^a   Steinberg, Gero ^b   Schrader, Michael ^a,b  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Fatty acid beta oxidation; Filamentous fungus; Mitochondria; Organelle biogenesis; Peroxisome; Ustilago maydis

Indexed keywords

ACYL COENZYME A DEHYDROGENASE; ACYL COENZYME A OXIDASE; COMPLEMENTARY DNA; FATTY ACID; OLEIC ACID;

ARTICLE; BIOINFORMATICS; CELL CULTURE; CELL FRACTIONATION; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; FATTY ACID OXIDATION; GENETIC TRANSFECTION; LIPID HOMEOSTASIS; MAMMAL CELL; MITOCHONDRION; NONHUMAN; PEROXISOMAL TARGETING SIGNAL; PEROXISOME; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; USTILAGO MAYDIS; FUNGUS; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; USTILAGO;

ACYL-COA DEHYDROGENASES; ACYL-COA OXIDASE; FATTY ACIDS; FUNGI; HUMANS; OXIDATION-REDUCTION; PEROXISOMES; USTILAGO;

EID: 84908296422     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.10.005     Document Type: Article

References (72)

1. Islinger M., Cardoso M.J., Schrader M. Be different-the diversity of peroxisomes in the animal kingdom. Biochim. Biophys. Acta 2010, 1803:881-897.
2. Wanders R.J., Waterham H.R. Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 2006, 75:295-332.
3. Waterham H.R., Ebberink M.S. Genetics and molecular basis of human peroxisome biogenesis disorders. Biochim. Biophys. Acta 2012, 1822:1430-1441.
4. Nordgren M., Fransen M. Peroxisomal metabolism and oxidative stress. Biochimie 2014, 98:56-62.
5. Islinger M., Grille S., Fahimi H.D., Schrader M. The peroxisome: an update on mysteries. Histochem. Cell Biol. 2012, 137:547-574.
6. Dixit E., Boulant S., Zhang Y., Lee A.S., Odendall C., Shum B., Hacohen N., Chen Z.J., Whelan S.P., Fransen M., Nibert M.L., Superti-Furga G., Kagan J.C. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 2010, 141:668-681.
7. Camoes F., Bonekamp N.A., Delille H.K., Schrader M. Organelle dynamics and dysfunction: a closer link between peroxisomes and mitochondria. J. Inherit. Metab. Dis. 2009, 32:163-180.
8. Schrader M. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 2006, 1763:531-541.
9. Schrader M., Yoon Y. Mitochondria and peroxisomes: are the 'big brother' and the 'little sister' closer than assumed?. BioEssays 2007, 29:1105-1114.
10. Schrader M., Grille S., Fahimi H.D., Islinger M. Peroxisome interactions and cross-talk with other subcellular compartments in animal cells. Subcell. Biochem. 2013, 69:1-22.
11. Poirier Y., Antonenkov V.D., Glumoff T., Hiltunen J.K. Peroxisomal beta-oxidation-a metabolic pathway with multiple functions. Biochim. Biophys. Acta 2006, 1763:1413-1426.
12. Ivashchenko O., Van Veldhoven P.P., Brees C., Ho Y.S., Terlecky S.R., Fransen M. Intraperoxisomal redox balance in mammalian cells: oxidative stress and interorganellar cross-talk. Mol. Biol. Cell 2011, 22:1440-1451.
13. Wang B., Van Veldhoven P.P., Brees C., Rubio N., Nordgren M., Apanasets O., Kunze M., Baes M., Agostinis P., Fransen M. Mitochondria are targets for peroxisome-derived oxidative stress in cultured mammalian cells. Free Radic. Biol. Med. 2013, 65:882-894.
14. Delille H.K., Schrader M. Targeting of hFis1 to peroxisomes is mediated by Pex19p. J. Biol. Chem. 2008, 283:31107-31115.
15. Schrader M., Bonekamp N.A., Islinger M. Fission and proliferation of peroxisomes. Biochim. Biophys. Acta 2012, 1822:1343-1357.
16. Neuspiel M., Schauss A.C., Braschi E., Zunino R., Rippstein P., Rachubinski R.A., Andrade-Navarro M.A., McBride H.M. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 2008, 18:102-108.
17. Steinberg G., Perez-Martin J. Ustilago maydis, a new fungal model system for cell biology. Trends Cell Biol. 2008, 18:61-67.
18. Munsterkotter M., Steinberg G. The fungus Ustilago maydis and humans share disease-related proteins that are not found in Saccharomyces cerevisiae. BMC Genomics 2007, 8:473.
19. Neuberger G., Maurer-Stroh S., Eisenhaber B., Hartig A., Eisenhaber F. Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J. Mol. Biol. 2003, 328:567-579.
20. Schluter A., Real-Chicharro A., Gabaldon T., Sanchez-Jimenez F., Pujol A. PeroxisomeDB 2.0: an integrative view of the global peroxisomal metabolome. Nucleic Acids Res. 2010, 38:D800-D805.
21. Claros M.G., Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 1996, 241:779-786.
22. Small I., Peeters N., Legeai F., Lurin C. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 2004, 4:1581-1590.
23. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
24. Schluter A., Fourcade S., Domenech-Estevez E., Gabaldon T., Huerta-Cepas J., Berthommier G., Ripp R., Wanders R.J., Poch O., Pujol A. PeroxisomeDB: a database for the peroxisomal proteome, functional genomics and disease. Nucleic Acids Res. 2007, 35:D815-D822.
25. Kiel J.A., Veenhuis M., van der Klei I.J. PEX genes in fungal genomes: common, rare or redundant. Traffic 2006, 7:1291-1303.
26. Steinberg G., Schuster M. The dynamic fungal cell. Fung Biol Rev 2011, 25:14-37.
27. Tang X., Halleck M.S., Schlegel R.A., Williamson P. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 1996, 272:1495-1497.
28. Raymond C.K., Pownder T.A., Sexson S.L. General method for plasmid construction using homologous recombination. BioTechniques 1999, 26:134-138. (140-131).
29. Schuster M., Kilaru S., Ashwin P., Lin C., Severs N.J., Steinberg G. Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track. EMBO J. 2011, 30:652-664.
30. Hollyday R. Ustilago maydis. Handbook of Genetics 1974, vol. 1:575-595. K. R.C. (Ed.).
31. Schmitt M.E., Brown T.A., Trumpower B.L. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 1990, 18:3091-3092.
32. Islinger M., Luers G.H., Li K.W., Loos M., Volkl A. Rat liver peroxisomes after fibrate treatment. A survey using quantitative mass spectrometry. J. Biol. Chem. 2007, 282:23055-23069.
33. Koch A., Schneider G., Luers G.H., Schrader M. Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J. Cell Sci. 2004, 117:3995-4006.
34. Bonekamp N.A., Islinger M., Lazaro M.G., Schrader M. Cytochemical detection of peroxisomes and mitochondria. Methods Mol. Biol. 2013, 931:467-482.
35. Islinger M., Weber G. Free flow isoelectric focusing: a method for the separation of both hydrophilic and hydrophobic proteins of rat liver peroxisomes. Methods Mol. Biol. 2008, 432:199-215.
36. Shen Y.Q., Lang B.F., Burger G. Diversity and dispersal of a ubiquitous protein family: acyl-CoA dehydrogenases. Nucleic Acids Res. 2009, 37:5619-5631.
37. Shen Y.Q., Burger G. Plasticity of a key metabolic pathway in fungi. Funct. Integr. Genom. 2009, 9:145-151.
38. Kikuchi M., Hatano N., Yokota S., Shimozawa N., Imanaka T., Taniguchi H. Proteomic analysis of rat liver peroxisome: presence of peroxisome-specific isozyme of Lon protease. J. Biol. Chem. 2004, 279:421-428.
39. Wiese S., Gronemeyer T., Ofman R., Kunze M., Grou C.P., Almeida J.A., Eisenacher M., Stephan C., Hayen H., Schollenberger L., Korosec T., Waterham H.R., Schliebs W., Erdmann R., Berger J., Meyer H.E., Just W., Azevedo J.E., Wanders R.J., Warscheid B. Proteomics characterization of mouse kidney peroxisomes by tandem mass spectrometry and protein correlation profiling. Mol. Cell. Proteomics 2007, 6:2045-2057.
40. He M., Pei Z., Mohsen A.W., Watkins P., Murdoch G., Van Veldhoven P.P., Ensenauer R., Vockley J. Identification and characterization of new long chain acyl-CoA dehydrogenases. Mol. Genet. Metab. 2011, 102:418-429.
41. Antonenkov V.D., Hiltunen J.K. Transfer of metabolites across the peroxisomal membrane. Biochim. Biophys. Acta 2012, 1822:1374-1386.
42. Schafer A., Kerssen D., Veenhuis M., Kunau W.H., Schliebs W. Functional similarity between the peroxisomal PTS2 receptor binding protein Pex18p and the N-terminal half of the PTS1 receptor Pex5p. Mol. Cell. Biol. 2004, 24:8895-8906.
43. Titorenko V.I., Nicaud J.M., Wang H., Chan H., Rachubinski R.A. Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J. Cell Biol. 2002, 156:481-494.
44. Patkar R.N., Ramos-Pamplona M., Gupta A.P., Fan Y., Naqvi N.I. Mitochondrial beta-oxidation regulates organellar integrity and is necessary for conidial germination and invasive growth in Magnaporthe oryzae. Mol. Microbiol. 2012, 86:1345-1363.
45. Schrader M., Fahimi H.D. Growth and division of peroxisomes. Int. Rev. Cytol. 2006, 255:237-290.
46. Hoepfner D., Schildknegt D., Braakman I., Philippsen P., Tabak H.F. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 2005, 122:85-95.
47. Sheibani S., Richard V.R., Beach A., Leonov A., Feldman R., Mattie S., Khelghatybana L., Piano A., Greenwood M., Vali H., Titorenko V.I. Macromitophagy, neutral lipids synthesis, and peroxisomal fatty acid oxidation protect yeast from "liponecrosis", a previously unknown form of programmed cell death. Cell Cycle 2014, 13:138-147.
48. Wanders R.J., Komen J., Kemp S. Fatty acid omega-oxidation as a rescue pathway for fatty acid oxidation disorders in humans. FEBS Lett. 2011, 278:182-194.
49. Gronemeyer T., Wiese S., Ofman R., Bunse C., Pawlas M., Hayen H., Eisenacher M., Stephan C., Meyer H.E., Waterham H.R., Erdmann R., Wanders R.J., Warscheid B. The proteome of human liver peroxisomes: identification of five new peroxisomal constituents by a label-free quantitative proteomics survey. PLoS ONE 2013, 8:e57395.
50. Havemeyer A., Bittner F., Wollers S., Mendel R., Kunze T., Clement B. Identification of the missing component in the mitochondrial benzamidoxime prodrug-converting system as a novel molybdenum enzyme. J. Biol. Chem. 2006, 281:34796-34802.
51. Nazarko T.Y., Ozeki K., Till A., Ramakrishnan G., Lotfi P., Yan M., Subramani S. Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J. Cell Biol. 2014, 204:541-557.
52. Distel B., Erdmann R., Gould S.J., Blobel G., Crane D.I., Cregg J.M., Dodt G., Fujiki Y., Goodman J.M., Just W.W., Kiel J.A., Kunau W.H., Lazarow P.B., Mannaerts G.P., Moser H.W., Osumi T., Rachubinski R.A., Roscher A., Subramani S., Tabak H.F., Tsukamoto T., Valle D., van der Klei I., van Veldhoven P.P., Veenhuis M. A unified nomenclature for peroxisome biogenesis factors. J. Cell Biol. 1996, 135:1-3.
53. Tanabe Y., Maruyama J.I., Yamaoka S., Yahagi D., Matsuo I., Tsutsumi N., Kitamoto K. Peroxisomes are involved in biotin biosynthesis in Aspergillus and Arabidopsis. J. Biol. Chem. 2011.
54. Freitag J., Ast J., Linne U., Stehlik T., Martorana D., Bolker M., Sandrock B. Peroxisomes contribute to biosynthesis of extracellular glycolipids in fungi. Mol. Microbiol. 2014, 93:24-36.
55. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
56. Baes M., Van Veldhoven P.P. Mouse models for peroxisome biogenesis defects and beta-oxidation enzyme deficiencies. Biochim. Biophys. Acta 2012, 1822:1489-1500.
57. Klose J., Kronstad J.W. The multifunctional beta-oxidation enzyme is required for full symptom development by the biotrophic maize pathogen Ustilago maydis. Eukaryot. Cell 2006, 5:2047-2061.
58. Kretschmer M., Klose J., Kronstad J.W. Defects in mitochondrial and peroxisomal beta-oxidation influence virulence in the maize pathogen Ustilago maydis. Eukaryot. Cell 2012, 11:1055-1066.
59. Freitag J., Ast J., Bolker M. Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 2012, 485:522-525.
60. Lockshon D., Surface L.E., Kerr E.O., Kaeberlein M., Kennedy B.K. The sensitivity of yeast mutants to oleic acid implicates the peroxisome and other processes in membrane function. Genetics 2007, 175:77-91.
61. Speijer D., Manjeri G.R., Szklarczyk R. How to deal with oxygen radicals stemming from mitochondrial fatty acid oxidation. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2014, 369:20130446.
62. Gabaldon T. Evolutionary considerations on the origin of peroxisomes from the endoplasmic reticulum, and their relationships with mitochondria. Cell Mol. Life Sci. 2014, 71:2379-2382.
63. Speijer D. Oxygen radicals shaping evolution: why fatty acid catabolism leads to peroxisomes while neurons do without it: FADH(2)/NADH flux ratios determining mitochondrial radical formation were crucial for the eukaryotic invention of peroxisomes and catabolic tissue differentiation. BioEssays 2011, 33:88-94.
64. Okumoto K., Kametani Y., Fujiki Y. Two proteases, trypsin domain-containing 1 (Tysnd1) and peroxisomal lon protease (PsLon), cooperatively regulate fatty acid beta-oxidation in peroxisomal matrix. J. Biol. Chem. 2011, 286:44367-44379.
65. Swigonova Z., Mohsen A.W., Vockley J. Acyl-CoA dehydrogenases: dynamic history of protein family evolution. J. Mol. Evol. 2009, 69:176-193.
66. Ochman H., Daubin V., Lerat E. A bunch of fun-guys: the whole-genome view of yeast evolution. Trends Genet. 2005, 21:1-3.
67. Gostincar C., Turk M., Gunde-Cimerman N. The evolution of fatty acid desaturases and cytochrome b5 in eukaryotes. J. Membr. Biol. 2010, 233:63-72.
68. Lederer F. The cytochrome b5-fold: an adaptable module. Biochimie 1994, 76:674-692.
69. 2 release from intact peroxisomes. Biochem. J. 2002, 363:483-491.
70. Finkel T. Signal transduction by reactive oxygen species. J. Cell Biol. 2011, 194:7-15.
71. Diano S., Liu Z.W., Jeong J.K., Dietrich M.O., Ruan H.B., Kim E., Suyama S., Kelly K., Gyengesi E., Arbiser J.L., Belsham D.D., Sarruf D.A., Schwartz M.W., Bennett A.M., Shanabrough M., Mobbs C.V., Yang X., Gao X.B., Horvath T.L. Peroxisome proliferation-associated control of reactive oxygen species sets melanocortin tone and feeding in diet-induced obesity. Nat. Med. 2011, 17:1121-1127.
72. Zhang J., Kim J., Alexander A., Cai S., Tripathi D.N., Dere R., Tee A.R., Tait-Mulder J., Di Nardo A., Han J.M., Kwiatkowski E., Dunlop E.A., Dodd K.M., Folkerth R.D., Faust P.L., Kastan M.B., Sahin M., Walker C.L. A tuberous sclerosis complex signalling node at the peroxisome regulates mTORC1 and autophagy in response to ROS. Nat. Cell Biol. 2013, 15:1186-1196.