Peroxisomal ABC transporters and β-oxidation during the life cycle of the filamentous fungus Podospora anserina

Fungal Genetics and Biology

Volumn 46, Issue 1, 2009, Pages 55-66

  Boisnard, Stéphanie ^a   Espagne, Eric ^a   Zickler, Denise ^a   Bourdais, Anne ^a   Riquet, Anne Laure ^a   Berteaux Lecellier, Véronique ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Oxidation; Filamentous fungi; Mitochondria; Peroxisomal ABC transporters; Peroxisomes

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER 2; ABC TRANSPORTER A1; BUTYRYL COENZYME A DEHYDROGENASE; CARBON; ENOYL COENZYME A HYDRATASE; FUNGAL PROTEIN; LONG CHAIN FATTY ACID; OLEIC ACID; PROTEIN FOX2; PROTEIN PEX2; PROTEIN PEX5; PROTEIN PEX7; UNCLASSIFIED DRUG;

ARTICLE; ASCOSPORE; BIOGENESIS; CELL MATURATION; CELL ORGANELLE; CONTROLLED STUDY; FATTY ACID OXIDATION; FUNGAL DEVELOPMENT; FUNGUS MUTANT; GENE DELETION; GERMINATION; LIFE CYCLE; MEIOSIS; MITOCHONDRION; NONHUMAN; PEROXISOME; PODOSPORA ANSERINA; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

ATP-BINDING CASSETTE TRANSPORTERS; FATTY ACIDS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; MITOCHONDRIA; OLEIC ACID; OXIDATION-REDUCTION; PEROXISOMES; PODOSPORA; SPORES, FUNGAL;

FUNGI; PODOSPORA ANSERINA;

EID: 57749204336     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2008.10.006     Document Type: Article

References (61)

1. Aubourg P., and Dubois-Dalcq M. X-linked adrenoleukodystrophy enigma: how does the ALD peroxisomal transporter mutation affect CNS glia?. Glia 29 (2000) 186-190
2. Baes M., Huyghe S., Carmeliet P., Declercq P.E., Collen D., Mannaerts G.P., and Van Veldhoven P.P. Inactivation of the peroxisomal multifunctional protein-2 in mice impedes the degradation of not only 2-methyl-branched fatty acids and bile acid intermediates but also of very long chain fatty acids. J. Biol. Chem. 275 (2000) 16329-16336
3. Bartowski E.J., Katermann F.R.H., and Buxton D.R. Influence of exogenous fatty acids on cottonseed germination. Physiol. Plant 44 (1978) 153-156
4. Berteaux-Lecellier V., Picard M., Thompson-Coffe C., Zickler D., Panvier-Adoutte A., and Simonet J.M. A nonmammalian homolog of the PAF1 gene (Zellweger syndrome) discovered as a gene involved in caryogamy in the fungus Podospora anserina. Cell 81 (1995) 1043-1051
5. Boisnard S., Zickler D., Picard M., and Berteaux-Lecellier V. Overexpression of a human and a fungal ABC transporter similarly suppresses the differentiation defects of a fungal peroxisomal mutant but introduces pleiotropic cellular effects. Mol. Microbiol. 49 (2003) 1287-1296
6. Bonnet C., Espagne E., Zickler D., Boisnard S., Bourdais A., and Berteaux-Lecellier V. The peroxisomal import proteins PEX2, PEX5 and PEX7 are differently involved in Podospora anserina sexual cycle. Mol. Microbiol. 62 (2006) 157-169
7. Buechler C., Boettcher A., Bared S.M., Probst M.C., and Schmitz G. The carboxyterminus of the ATP-binding cassette transporter A1 interacts with a beta2-syntrophin/utrophin complex. Biochem. Biophys. Res. Commun. 293 (2002) 759-765
8. Carroll A.M., Sweigard J.A., and Valent-Central B. Improved vectors for selecting resistance to hygromycin. Fungal Genet. Newsl. 41 (1994) 22
9. Chelstowska A., and Butow R.A. RTG genes in yeast that function in communication between mitochondria and the nucleus are also required for expression of genes encoding peroxisomal proteins. J. Biol. Chem. 270 (1995) 18141-18146
10. Claros M.G., and Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241 (1996) 779-786
11. Cooper T.G., and Beevers H. Mitochondria and glyoxysomes from castor bean endosperm. Enzyme constituents and catalytic capacity. J. Biol. Chem. 244 (1969) 3507-3513
12. Coppin E., de Renty C., and Debuchy R. The function of the coding sequences for the putative pheromone precursors in Podospora anserina is restricted to fertilization. Eukaryot. Cell 4 (2005) 407-420
13. Coppin E., and Debuchy R. Co-expression of the mating-type genes involved in internuclear recognition is lethal in Podospora anserina. Genetics 155 (2000) 657-669
14. Coppin E., and Silar P. Identification of PaPKS1, a polyketide synthase involved in melanin formation and its use as a genetic tool in Podospora anserina. Mycol. Res. 111 (2007) 901-908
15. Dean M., and Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu. Rev. Genomics Hum. Genet. 6 (2005) 123-142
16. Dieuaide M., Couee I., Pradet A., and Raymond P. Effects of glucose starvation on the oxidation of fatty acids by maize root tip mitochondria and peroxisomes: evidence for mitochondrial fatty acid beta-oxidation and acyl-CoA dehydrogenase activity in a higher plant. Biochem. J. 296 (1993) 199-207
17. Dirkx R., Vanhorebeek I., Martens K., Schad A., Grabenbauer M., Fahimi D., Declercq P., Van Veldhoven P.P., and Baes M. Absence of peroxisomes in mouse hepatocytes causes mitochondrial and ER abnormalities. Hepatology 41 (2005) 868-878
18. El-Khoury R., Sellem C.H., Coppin E., Boivin A., Maas M.F., Debuchy R., and Sainsard-Chanet A. Gene deletion and allelic replacement in the filamentous fungus Podospora anserina. Curr. Genet. 53 (2008) 249-258
19. Espagne E., Lespinet O., Malagnac F., Da Silva C., Jaillon O., Porcel B.M., Couloux A., Aury J.M., Segurens B., Poulain J., Anthouard V., Grossetete S., Khalili H., Coppin E., Dequard-Chablat M., Picard M., Contamine V., Arnaise S., Bourdais A., Berteaux-Lecellier V., Gautheret D., de Vries R.P., Battaglia E., Coutinho P.M., Danchin E.G., Henrissat B., Khoury R.E., Sainsard-Chanet A., Boivin A., Pinan-Lucarre B., Sellem C.H., Debuchy R., Wincker P., Weissenbach J., and Silar P. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 9 (2008) R77
20. Footitt S., Slocombe S.P., Larner V., Kurup S., Wu Y., Larson T., Graham I., Baker A., and Holdsworth M. Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 21 (2002) 2912-2922
21. Fossa A., Beyer A., Pfitzner E., Wenzel B., and Kunau W.H. Molecular cloning, sequencing and sequence analysis of the fox-2 gene of Neurospora crassa encoding the multifunctional beta-oxidation protein. Mol. Gen. Genet. 247 (1995) 95-104
22. Fujimura S., Nakagawa T., Ito T., Matsufuji Y., Miyaji T., and Tomizuka N. Peroxisomal metabolism is regulated by an oxygen-recognition system through organelle crosstalk between the mitochondria and peroxisomes. Yeast 24 (2007) 491-498
23. Gartner J., Obie C., Watkins P., and Valle D. Restoration of peroxisome biogenesis in a peroxisome-deficient mammalian cell line by expression of either the 35 kDa or the 70 kDa peroxisomal membrane proteins. J. Inherit. Metab. Dis. 17 (1994) 327-329
24. Goldfisher S., Moore C.L., Johnson A.B., Spiro A.J., Valsami M.P., Ritch R.H., Norton W.T., Rapin I., and Gartner L. Peroxisomal and mitochondrial defects in the cerebro-hepato-renal syndrome. Science 182 (1973) 62-64
25. Gomez B.L., and Nosanchuk J.D. Melanin and fungi. Curr. Opin. Infect. Dis. 16 (2003) 91-96
26. Goodrich-Tanrikulu M., Howe K., Stafford A., and Nelson M.A. Changes in fatty acid composition of Neurospora crassa accompany sexual development and ascospore germination. Microbiology 144 (1998) 1713-1720
27. Goodrich-Tanrikulu M., Jacobson D.J., Stafford A.E., Lin J.T., and McKeon T.A. Characterization of Neurospora crassa mutants isolated following repeat-induced point mutation of the beta subunit of fatty acid synthase. Curr. Genet. 36 (1999) 147-152
28. Hashimoto T. Peroxisomal beta-oxidation enzymes. Cell Biochem. Biophys. 32 (2000) 63-72
29. Hettema E.H., van Roermund C.W., Distel B., van den Berg M., Vilela C., Rodrigues-Pousada C., Wanders R.J., and Tabak H.F. 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
30. Hiltunen J.K., Mursula A.M., Rottensteiner H., Wierenga R.K., Kastaniotis A.J., and Gurvitz A. The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 27 (2003) 35-64
31. Hughes J.L., Poulos A., Robertson E., Chow C.W., Sheffield L.J., Christodoulou J., and Carter R.F. Pathology of hepatic peroxisomes and mitochondria in patients with peroxisomal disorders. Virchows Arch. A Pathol. Anat. Histopathol. 416 (1990) 255-264
32. Huyghe S., Schmalbruch H., De Gendt K., Verhoeven G., Guillou F., Van Veldhoven P.P., and Baes M. Peroxisomal multifunctional protein 2 is essential for lipid homeostasis in Sertoli cells and male fertility in mice. Endocrinology 147 (2006) 2228-2236
33. Hynes M.J., Murray S.L., Khew G.S., and Davis M.A. Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics 178 (2008) 1355-1369
34. Klose J., and Kronstad J.W. The multifunctional beta-oxidation enzyme is required for full symptom development by the biotrophic maize pathogen Ustilago maydis. Eukaryot. Cell 5 (2006) 2047-2061
35. Kunau W.H., Dommes V., and Schulz H. beta-oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog. Lipid Res. 34 (1995) 267-342
36. Lecellier G., and Silar P. Rapid methods for nucleic acids extraction from Petri dish-grown mycelia. Curr. Genet. 25 (1994) 122-123
37. Liao X.S., Small W.C., Srere P.A., and Butow R.A. Intramitochondrial functions regulate nonmitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 11 (1991) 38-46
38. Maggio-Hall L.A., and Keller N.P. Mitochondrial beta-oxidation in Aspergillus nidulans. Mol Microbiol. 54 (2004) 1173-1185
39. Maggio-Hall L.A., Lyne P., Wolff J.A., and Keller N.P. A single acyl-CoA dehydrogenase is required for catabolism of isoleucine, valine and short-chain fatty acids in Aspergillus nidulans. Fungal Genet. Biol. 45 (2007) 180-189
40. Malagnac F., Lalucque H., Lepere G., and Silar P. Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet. Biol. 41 (2004) 982-997
41. Mannaerts G.P., Van Veldhoven P.P., and Casteels M. Peroxisomal lipid degradation via beta- and alpha-oxidation in mammals. Cell Biochem. Biophys. 32 (2000) 73-87
42. McGuinness M.C., Lu J.F., Zhang H.P., Dong G.X., Heinzer A.K., Watkins P.A., Powers J., and Smith K.D. Role of ALDP (ABCD1) and mitochondria in X-linked adrenoleukodystrophy. Mol. Cell. Biol. 23 (2003) 744-753
43. Moore-Landecker E. Physiology and biochemistry of ascosarp induction and development. Mycol. Res. 96 (1992) 705-716
44. Mosser J., Douar A.M., Sarde C.O., Kioschis P., Feil R., Moser H., Poustka A.M., Mandel J.L., and Aubourg P. Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361 (1993) 726-730
45. Oezen I., Rossmanith W., Forss-Petter S., Kemp S., Voigtlander T., Moser-Thier K., Wanders R.J., Bittner R.E., and Berger J. Accumulation of very long-chain fatty acids does not affect mitochondrial function in adrenoleukodystrophy protein deficiency. Hum. Mol. Genet. 14 (2005) 1127-1137
46. Petrova V.Y., Drescher D., Kujumdzieva A.V., and Schmitt M.J. Dual targeting of yeast catalase A to peroxisomes and mitochondria. Biochem. J. 380 (2004) 393-400
47. Pfaffl M.W., Horgan G.W., and Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30 (2002) e36
48. Platta H.W., and Erdmann R. Peroxisomal dynamics. Trends Cell Biol. 17 (2007) 474-484
49. Rizet G., and Engelmann C. Contribution à l'étude génétique d'un ascomycète tétrasporé: Podospora anserina. Rehm. Rev. Cytol. Biol. Veg. 11 (1949) 201-304
50. Ruprich-Robert G., Berteaux-Lecellier V., Zickler D., Panvier-Adoutte A., and Picard M. Identification of six loci in which mutations partially restore peroxisome biogenesis and/or alleviate the metabolic defect of pex2 mutants in Podospora. Genetics 161 (2002) 1089-1099
51. Ruprich-Robert G., Zickler D., Berteaux-Lecellier V., Velot C., and Picard M. Lack of mitochondrial citrate synthase discloses a new meiotic checkpoint in a strict aerobe. EMBO J. 21 (2002) 6440-6451
52. Shani N., Sapag A., and Valle D. Characterization and analysis of conserved motifs in a peroxisomal ATP-binding cassette transporter. J. Biol. Chem. 271 (1996) 8725-8730
53. Shimozawa N., Tsukamoto T., Suziki Y., Orii T., Shirayoshi Y., Mori T., and Fujiki Y. A human gene responsible for Zellweger syndrome that affects peroxisome assembly. Science 255 (1992) 1132-1134
54. Silar P., Barreau C., Debuchy R., Kicka S., Turcq B., Sainsard-Chanet A., Sellem C.H., Billault A., Cattolico L., Duprat S., and Weissenbach J. Characterization of the genomic organization of the region bordering the centromere of chromosome V of Podospora anserina by direct sequencing. Fungal Genet. Biol. 39 (2003) 250-263
55. Theodoulou F.L., Holdsworth M., and Baker A. Peroxisomal ABC transporters. FEBS Lett. 580 4 (2006) 1139-1155
56. Thompson-Coffe C., and Zickler D. How the cytoskeleton recognizes and sorts nuclei of opposite mating type during the sexual cycle in filamentous ascomycetes. Dev. Biol. 165 (1994) 257-271
57. Tsitsigiannis D.I., and Keller N.P. Oxylipins as developmental and host-fungal communication signals. Trends Microbiol. 15 (2007) 109-118
58. Tsitsigiannis D.I., Kowieski T.M., Zarnowski R., and Keller N.P. Endogenous lipogenic regulators of spore balance in Aspergillus nidulans. Eukaryot. Cell 3 (2004) 1398-1411
59. Wanders R., and Waterham H. Peroxisomal disorders I: biochemistry and genetics of peroxisome biogenesis disorders. Clin. Genet. 67 (2005) 107-133
60. Wanders R.J. Metabolic and molecular basis of peroxisomal disorders: a review. Am. J. Med. Genet. A 126 (2004) 355-375
61. Wanders R.J., Visser W.F., van Roermund C.W., Kemp S., and Waterham H.R. The peroxisomal ABC transporter family. Pflugers Arch. 453 (2007) 719-734