Role of peroxisomes in the biosynthesis and secretion of β-lactams and other secondary metabolites

Journal of Industrial Microbiology and Biotechnology

Volumn 39, Issue 3, 2012, Pages 367-382

  Martín, Juan Francisco ^a   Ullán, Ricardo V ^a   García Estrada, Carlos ^a  

^a Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

Author keywords

Lactam biosynthesis; Bile acid metabolism; Mycotoxins; Peroxins; Peroxisomes

Indexed keywords

ADICILLIN; AMINOADIPIC ACID; AUXIN; BETA LACTAM ANTIBIOTIC; BETA LACTAM DERIVATIVE; BILE ACID; CEPHALOSPORIN; CHOLESTEROL; CYSTEINE; DEACETOXYCEPHALOSPORIN C; GLYCOLYTIC ENZYME; HYDROGEN PEROXIDE; ISOPENICILLIN N; JASMONIC ACID; LEUKOTRIENE DERIVATIVE; MATRIX PROTEIN; MYCOTOXIN; PENICILLIN G; PEROXIN; PHENYLACETYLENE; PIPECOLIC ACID; POLYAMINE DERIVATIVE; PURINE DERIVATIVE; VALINE;

ANTIBIOTIC BIOSYNTHESIS; AUTOPHAGY; BIOGENESIS; BIOSYNTHESIS; CATABOLISM; CELL ORGANELLE; CEPHALOSPORIUM ACREMONIUM; ENZYME DEGRADATION; FATTY ACID OXIDATION; MICROBODY; NONHUMAN; PENICILLIUM CHRYSOGENUM; PEROXISOMAL TARGETING SIGNAL; PEROXISOME; PEXOPHAGY; REVIEW;

ACYLTRANSFERASES; AMINO ACID SEQUENCE; BETA-LACTAMS; BIOLOGICAL TRANSPORT; CEPHALOSPORINS; FUNGI; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; PENICILLIN-BINDING PROTEINS; PENICILLINS; PENICILLIUM CHRYSOGENUM; PEROXISOMES; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

ACREMONIUM CHRYSOGENUM; EUKARYOTA; PENICILLIUM CHRYSOGENUM;

EID: 84859833488     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-011-1063-z     Document Type: Review

References (154)

1. Agne B, Meindl NM, Niederho VK, Einwächter H, Rehling P, Sickmann A, Meyer HE, Girzalsky W, Kunau WH (2003) Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol Cell 11:635-646 (Pubitemid 36385119)
2. Aharonowitz Y, Cohen G, Martín JF (1992) Penicillin and cephalosporin biosynthetic genes: structure, organization, regulation and evolution. Annu Rev Microbiol 46:461-495
3. Alvarez E, Cantoral JM, Barredo JL, Díez B, Martín JF (1987) PuriWcation to homogeneity and characterization of the acyl-CoA:6-APA acyltransferase of Penicillium chrysogenum. Antimicrob Agents Chemother 31:1675-1682 (Pubitemid 17157624)
4. Alvarez E, Meesschaert B, Montenegro E, Gutiérrez S, Díez B, Barredo JL, Martín JF (1993) The isopenicillin N acyltransferase of Penicillium chrysogenum has isopenicillin N amidohydrolase, 6-aminopenicillanic acid acyltransferase and penicillin amidase acitivies, all of which are encoded by the single pen DE gene. Eur J Biochem 215:323-332 (Pubitemid 23224316)
5. Ashmarina LI, Rusnak N, Miziorko HM, Mitchell GA (1994) 3-Hydroxy-3-methylglutaryl-CoA lyase is present in mouse and human liver peroxisomes. J Biol Chem 269:31929-33132
6. Baldwin JE, Bird JW, Field RA, O'Callaghan NM, SchoYeld CJ (1990) Isolation and partial characterization of ACV synthetase from Cephalosporium acremonium and Streptomyces clavuligerus. J Antibiot 43:1055-1057 (Pubitemid 20274076)
7. Barredo JL, van Solingen P, Díez B, Álvarez E, Cantoral JM, Kattevilder A, Smaal EB, Groenen MA, Veenstra AE, Martín JF (1989) Cloning and characterization of the acyl-coenzyme A: 6-aminopenicillanic-acid- acyltransferase gene of Penicillium chrysogenum. Gene 83:291-300 (Pubitemid 20001136)
8. Barrios-González J, Montenegro E, Martín JF (1993) Penicillin production by mutants resistant to phenylacetic acid. J Ferm Bioeng 76:455-458 (Pubitemid 24038690)
9. Brakhage AA (1997) Molecular regulation of penicillin biosynthesis in Aspergillus (Emericella) nidulans. FEMS Microbiol Lett 148:1-10 (Pubitemid 27128348)
10. Braverman N, Dodt G, Gould SJ, Valle D (1998) An isoform of pex5p, the human PTS1 receptor, is required for the import of PTS2 proteins into peroxisomes. Human Mol Genet 7:1195-1205 (Pubitemid 28383050)
11. Brocard C, Kragler F, Simon MM, Schuster T, Hartig A (1994) The tetratricopeptide repeat-domain of the PAS10 protein of Saccharomyces cerevisiae is essential for binding the peroxisomal targeting signal-SKL. Biochem Biophys Res Commun 204: 1016-1022
12. Cantoral JM, Gutiérrez S, Fierro F, Gil-Espinosa S, van Liempt H, Martín JF (1993) Biochemical characterization and molecular genetics of nine mutants of Penicillium chrysogenum impaired in penicillin biosynthesis. J Biol Chem 268:737-744 (Pubitemid 23021385)
13. Chang CC, Warren DS, Sacksteder KA, Gould SJ (1999) PEX12 binds PEX5 and PEX10 and acts downstream of receptor docking in peroxisomal matrix protein import. J Cell Biol 147:761-774
14. Dammai V, Subramani S (2001) The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol. Cell 105:187-196 (Pubitemid 32429509)
15. De Duve C, Baudhuin P (1966) Peroxisomes (microbodies and related particles). Physiol Rev 46:323-357
16. de Hoop MJ, Ab G (1992) Import of proteins into peroxisomes and other microbodies. Biochem J 286:657-669
17. Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thalianaenzymes, products, regulation. Plant Biol 8:297-306 (Pubitemid 43854058)
18. Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, Shum B (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141:668-681
19. Dodt G, Gould SJ (1996) Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J Cell Biol 135:1763-1774 (Pubitemid 27036439)
20. Dotzlaf JE, Yeh WK (1987) CopuriWcation and characterization of deacetoxycephalosporin C synthetase/hydroxylase from Cephalsoporium acremonium. J Bacteriol 169:1611-1618 (Pubitemid 17063490)
21. Dyer JM, McNew JA, Goodman JM (1996) The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J Cell Biol 133:269-280 (Pubitemid 26132529)
22. Einwächter H, Sowinski S, Kunau WH, Schliebs W (2001) Yarrowia lipolytica Pex20p, Saccharomyces cerevisiae Pex18p/Pex21p and mammalian Pex5pL fulWl a common function in the early steps of the peroxisomal PTS2 import pathway. EMBO Rep 2:1035-1039 (Pubitemid 33130612)
23. Elgersma Y, Kwast L, van den Berg M, Snyder WB, Distel B, Subramani S, Tabak HF (1997) Overexpression of Pex15p, a phosphorylated peroxisomal integral membrane protein required for peroxisome assembly in S.cerevisiae, causes proliferation of the endoplasmic reticulum membrane. EMBO J 16:7326-7341 (Pubitemid 28010493)
24. Epstein E, Nissen SJ, Sutter EG (1991) Indole-3-acetic acid and indole-3-butyric acid in tissues in carrot inoculated with Agrobacterium rhizogenes. J Plant Growth Reg 10:97-1100
25. Erdmann R, Blobel G (1996) IdentiWcation of Pex13p a peroxisomal membrane receptor for the PTS1 recognition factor. J Cell Biol 135:111-121 (Pubitemid 26337741)
26. Erdmann R, Schliebs W (2005) Peroxisomal matrix protein import: the transient pore model. Natl Rev Mol Cell Biol 6:738-742 (Pubitemid 41742797)
27. Evers ME, Trip H, van den Berg MA, Bovenberg RA, Driessen AJ (2004) Compartmentalization and transport in β-lactam antibiotics biosynthesis. Adv Biochem Eng Biotechnol 88:111-135
28. Fan J, Quan S, Orth T, Awai C, Chory J, Hu J (2005) The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol 139:231-239 (Pubitemid 43951607)
29. Fang Y, Morrell JC, Jones JM, Gould SJ (2004) PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins. J Cell Biol 164:863-875 (Pubitemid 38366898)
30. Ferdinandusse S, Houten SM (2006) Peroxisomes and bile acid biosynthesis. Biochim Biophys Acta 1763:1427-1440 (Pubitemid 44880477)
31. Flaspohler JA, Rickoll WL, Beverley SM, Parsons M (1997) Functional identiWcation of a Leishmania gene related to the peroxin 2 gene reveals common ancestry of glycosomes and peroxisomes. Mol Cell Biol 17:1093-1101 (Pubitemid 27097338)
32. Fransen M, Brees C, Baumgart E, Vanhooren JC, Baes M, Mannaerts GP, Van Veldhoven PP (1995) IdentiWcation and characterization of the putative human peroxisomal C-terminal targeting signal import receptor. J Biol Chem 270:7731-7736
33. Fujiki Y, Matsuzono Y, Matsuzaki T, Fransen M (2006) Import of peroxisomal membrane proteins: the interplay of Pex3pand Pex19p-mediated interactions. Biochim Biophys Acta 1763:1639-1646 (Pubitemid 44880487)
34. Gabaldón T (2010) Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci 365:765-773
35. García-Estrada C, Vaca I, Fierro F, Sjollema K, Veenhuis M, Martín JF (2008) The unprocessed preprotein form IATC103S of the isopenicillin N acyltransferase is transported inside peroxisomes and regulates its self-processing. Fungal Genet Biol 45:1043-1052
36. García-Estrada C, Vaca I, Ullán RV, van den Berg MA, Bovenberg RA, Martín JF (2009) Molecular characterization of a fungal gene paralogue of the penicillin penDE gene of Penicillium chrysogenum. BMC Microbiol 9:104-119
37. Geisbrecht BV, Collins CS, Reuber BE, Gould SJ (1998) Disruption of a PEX1-PEX6 interaction is the most common cause of the neurologic disorders Zellweger syndrome, neonatal adrenoleukodystrophy, and infantile Refsum disease. Proc Natl Acad Sci U S A 95:8630-8635 (Pubitemid 28350539)
38. Glover JR, Andrews DW, Rachubinski RA (1994) Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc Natl Acad Sci U S A 91:10541-10545 (Pubitemid 24329034)
39. Gould SJ, Kalish JE, Morrell JC, Bjorkman J, Urquhart AJ, Crane DI (1996) Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTS1 receptor. J Cell Biol 135:85-95 (Pubitemid 26337739)
40. Grou CP, Carvalho AF, Pinto MP, Wiese S, Piechura H, Meyer HE, Warscheid B, Sá-Miranda C, Azevedo JE (2008) Members of the E2D (UbcH5) family mediate the ubiquitination of the conserved cysteine of Pex5p, the peroxisomal import receptor. J Biol Chem 283:14190-14197
41. Gutiérrez S, Díez B, Montenegro E, Martín JF (1991) Characterization of the Cephalosporium acremonium pcbAB gene encoding β-aminoadipyl-cysteinyl-valine synthetase, a large multidomain peptide synthetase: linkage to the pcbC gene as a cluster of early cephalosporin biosynthetic genes and evidence of multiple functional domains. J Bacteriol 173:2354-2365
42. Gutiérrez S, Velasco J, Fernández FJ, Martín JF (1992) The cefG gene of Cephalosporium acremonium is linked to the cefEF gene and encodes a deacetylcephalosporin C acetyltransferase closely related to homoserine O-acetyltransferase. J Bacteriol 174:3056-3064
43. Gutiérrez S, Fierro F, Casqueiro J, Martín JF (1999) Gene organization and plasticity of the β-lactam genes in diVerent Wlamentous fungi. Anton van Leeu 75:21-31
44. Halbach A, Rucktaschel R, Rottensteiner H, Erdmann R (2009) The N-domain of Pex22p can functionally replace the Pex3p N-domain in targeting and peroxisome formation. J Biol Chem 284:3906-3916
45. Hart DT, Misset O, Edwards SW, Opperdoes FR (1984) Comparison of the glycosomes (microbodies) isolated from Trypanosoma brucei blood stream form and cultured procyclic trypomastigotes. Mol Biochem Parasitol 12:25-35 (Pubitemid 14056234)
46. Hayashi M, Yagi M, Nito K, Kamada T, Nishimura M (2005) DiVerential contribution of two peroxisomal protein receptors to the maintenance of peroxisomal functions in Arabidopsis. J Biol Chem 280:14829-14835 (Pubitemid 40562832)
47. Heiland I, Erdmann R (2005) Biogenesis of peroxisomes. Topogenesis of the peroxisomal membrane and matrix proteins. FEBS J 272:2362-2372 (Pubitemid 40705058)
48. HoVmeister D, Keller NP (2007) Natural products of Wlamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24:393-416 (Pubitemid 46496563)
49. Honsho M, Fujiki Y (2001) Topogenesis of peroxisomal membrane protein requires a short, positively charged interveningloop sequence and Xanking hydrophobic segments. J Biol Chem 276:9375-9382
50. Hu J, Aguirre M, Peto C, Alonso J, Ecker J, Chory J (2002) A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 297:405-409 (Pubitemid 34790771)
51. Imazaki A, Tanaka A, Harimoto Y, Yamamoto M, Akimitsu K, Park P, Tsuge T (2010) Contribution of peroxisomes to secondary metabolism and pathogenicity in the fungal plant pathogen. Alternaria Alternata 9:682-694
52. Islinger M, Li KW, Seitz J, Völkl A, Lüers GH (2009) Hitchhiking of Cu/Zn superoxide dismutase to peroxisomes-evidence for a natural piggyback import mechanism in mammals. TraYc 10:1711-1721
53. Jami MS, García-Estrada C, Barreiro C, Cuadrado AA, Salehi-Najafabadi Z, Martín JF (2010) The Penicillium chrysogenum extracellular proteome. Conversion from a food-rotting strain to a versatile cell factory for white biotechnology. Mol Cell Proteomics 9:2729-2744
54. Jedd G, Chua NH (2000) A new self-assembled peroxisomal vesicle required for eYcient resealing of the plasma membrane. Nat Cell Biol 2:226-231
55. Jones JM, Morrell JC, Gould SJ (2004) PEX19 is a predominantly cytosolic chaperone and import receptor for class 1 peroxisomal membrane proteins. J Cell Biol 164:57-67 (Pubitemid 38082457)
56. Kiel JA, Hilbrands RE, van der Klei IJ, Rasmussen SW, Salomons FA, van der Heide M, Faber KN, Cregg JM, Veenhuis M (1999) Hansenula polymorpha Pex1p and Pex6p are peroxisomeassociated AAA proteins that functionally and physically interact. Yeast 15:1059-1078 (Pubitemid 29387021)
57. Kiel JA, Hilbrands RE, Bovenberg RAL, Veenhuis M (2000) Isolation of Penicillium chrysogenum PEX1 and PEX6 encoding AAA proteins involved in peroxisome biogenesis. Appl Microbiol Biotechnol 54:234-242
58. Kiel JA, van den Berg M, Bovenberg RAL, van der Klei IJ, Veenhuis M (2004) Penicillium chrysogenum Pex5p mediates diVerential sorting of PTS1 proteins to microbodies of the methylotrophic yeast Hansenula polymorpha. Fungal Genet Biol 41:708-720 (Pubitemid 38748575)
59. Kiel JA, van der Klei IJ, van den Berg MA, Bovenberg RAL, Veenhuis M (2005) Overproduction of a single protein, Pc-Pcx11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet Biol 42:154-164 (Pubitemid 40163993)
60. Kiel JA, Veenhuis M, van der Klei IJ (2006) PEX genes in fungal genomes: common, rare or redundant. TraYc 7:1291-1303 (Pubitemid 44364168)
61. Koch A, Schneider G, Lüers GH, Schrader M (2004) Peroxisome elongation and constriction but not Wssion can occur independently of dynamin-like protein 1. J Cell Sci 117:3995-4006 (Pubitemid 39207335)
62. Koetsier MJ, Jekel PA, van den Berg MA, Bovenberg RA, Janssen DB (2010) Characterization of a phenylacetate-CoA ligase from Penicillium chrysogenum. Biochem J 417:467-476
63. Kotti TJ, Savolainen K, Helander HM, Yagi A, Novikov DK, Kalkkinen N, Conzelmann E, Hiltunen JK, Schmitz W (2000) In mouse alpha -methylacyl-CoA racemase, the same gene product is simultaneously located in mitochondria and peroxisomes. J Biol Chem 275:20887-20895 (Pubitemid 30457684)
64. Kunze M et al (2006) A central role for the peroxisomal membrane in glyoxylate cycle function. Biochim Biophys Acta 1763:1441-1452 (Pubitemid 44883390)
65. Lamas-Maceiras M, Vaca I, Rodríguez E, Casqueiro J, Martín JF (2006) AmpliWcation and disruption of the phenylacetyl-CoA ligase gene of Penicillium chrysogenum encoding an aryl-capping enzyme that supplies phenylacetic acid to the isopenicillin N acyltransferase. Biochem J 395:147-155
66. Lazarow PB (2006) The import receptor Pex7p and the PTS2 targeting sequence. Biochim Biophys Acta 1763:1599-1604 (Pubitemid 44880472)
67. Liu F, Ng SK, Lu Y, Low W, Lai J, Jedd G (2008) Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180:325-339 (Pubitemid 351185919)
68. Lübbe C, Wolfe S, Demain AL (1986) Isopenicillin N epimerase activity in a high cephalosporin-producing strain of Cephalosporium acremonium. Appl Microbiol Biotechnol 23:367-368 (Pubitemid 16131890)
69. Ma C, Schumann U, Rayapuram N, Subramani S (2009) The peroxisomal matrix import of Pex8p requires only PTS receptors and Pex14p. Mol Biol Cell 20:3680-3689
70. Managadze D, Würtz C, Sichting M, Niehaus G, Veenhuis M, Rottensteiner H (2007) The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and Woronin bodies. TraYc 8:687-701 (Pubitemid 46785151)
71. Markham P, Collinge AJ (1987) Woronin bodies of Wlamentous fungi. FEMS Microbiol Rev 46:1-11
72. Martín JF (2000) Molecular control of expression of penicillin biosynthesis genes in fungi: regulatory proteins interact with a bidirectional promoter region. J Bacteriol 182:2355-2362 (Pubitemid 30212889)
73. Martín JF, Liras P (1989) Enzymes involved in penicillin, cephalosporin and cephamycin biosynthesis. In: Fiechter A (ed) Advances in biochemical engineering/biotechnology. Springer, Berlin, pp 153-187
74. Martín JF, Ullán RV, Casqueiro FJ (2004) Novel genes involved in Cephalosporin biosynthesis: The three-component isopenicillin N epimerase system. In: Brakhage A (ed) Advances in biochemical engineering-biotechnology. Springer, Berlin, pp 91-109
75. Martín JF, Ullán RV, García-Estrada C (2010) Regulation and compartmentalization of β-lactam biosynthesis. Microb Biotechnol 3:285-299
76. Matsumoto N, Tamura S, Fujiki Y (2003) The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes. Nat Cell Biol 5:454-460 (Pubitemid 36592269)
77. Matsumura T, Otera H, Fujiki Y (2000) Disruption of the interaction of the longer isoform of Pex5p, Pex5pL, with Pex7p abolishes peroxisome targeting signal type 2 protein import in mammals. Study with a novel Pex5-impaired Chinese hamster ovary cell mutant. J Biol Chem 275:21715-21721 (Pubitemid 30481880)
78. Matsuzono Y, Matsuzaki T, Fujiki Y (2006) Functional domain mapping of peroxin Pex19p: interaction with Pex3p is essential for function and translocation. J Cell Sci 119:3539-3550 (Pubitemid 44501859)
79. Maynard EL, Gatto GJ Jr, Berg JM (2004) Pex5p binding aYnities for canonical and noncanonical PTS1 peptides. Proteins 55:856-861 (Pubitemid 38702945)
80. Meinecke M, Cizmowski C, Schliebs W, Krüger V, Beck S, Wagner R, Erdmann R (2010) The peroxisomal importomer constitutes a large and highly dynamic pore. Nat Cell Biol 12:273-277
81. Montenegro E, Barredo JL, Gutiérrez S, Díez B, Alvarez E, Martín JF (1990) Cloning, characterization of the acyl-CoA:6-amino penicillanic acid acyltransferase gene of Aspergillus nidulans and likage to the isopenicillin N synthase gene. Mol Gen Genet 221:322-330 (Pubitemid 20195849)
82. Motley A, Lumb MJ, Oatey PB, Jennings PR, De Zoysa PA, Wanders RJ, Tabak HF, Danpure CJ (1995) Mammalian alanine/glyoxylate aminotransferase 1 is imported into peroxisomes via the PTS1 translocation pathway. Increased degeneracy and context speciWcity of the mammalian PTS1 motif and implications for the peroxisome-to-mitochondrion mistargeting of AGT in primary hyperoxaluria type 1. J Cell Biol 131:95-109
83. Mullen RT, Lee MS, Flynn CR, Trelease RN (1997) Diverse amino acid residues function within the type 1 peroxisomal targeting signal. Implications for the role of accessory residues upstream of the type 1 peroxisomal targeting signal. Plant Physiol 115:881-889 (Pubitemid 28378746)
84. Müller WH, van der Krift TP, Krouwer AJ, Wösten HA, van der Voort LH, Smaal EB, Verkleij AJ (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J 10:489-495 (Pubitemid 21905500)
85. Müller WH, Bovenberg RAL, Groothuis MH, Kattevilder F, Smaal EB, Van der Voort LHM, Verkleij AJ (1992) Involvement of microbodies in penicillin biosynthesis. Biochim et Biophys Acta 1116:210-213
86. Munck JM, Motley AM, Nuttall JM, Hettema EH (2009) A dual function for Pex3p in peroxisome formation and inheritance. J Cell Biol 187:463-471
87. Nair DM, Purdue PE, Lazarow PB (2004) Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae. J Cell Biol 167:599-604 (Pubitemid 39565141)
88. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003) Motif reWnement of the peroxisomal targeting signal 1 and evaluation of taxon-speciWc diVerences. J Mol Biol 328:567-579 (Pubitemid 36438574)
89. Nito K, Hayashi M, Nishimura M (2002) Direct interaction and determination of binding domains among peroxisomal import factors in Arabidopsis thaliana. Plant Cell Physiol 43:355-366 (Pubitemid 34514224)
90. Nyathi Y, Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochim Biophys Acta 1763:1478-1495 (Pubitemid 44880467)
91. Oku M, Sakai Y (2010) Peroxisomes as dynamic organelles: autophagic degradation. FEBS J 277:3289-3294
92. Opalinski L, Veenhuis M, van der Klei I (2011) Peroxisomes: membrane events accompanying peroxisome proliferation. Int J Biochem Cell Biol 43:847-851
93. Opalinski L, Kiel JA, Williams C, Veenhuis M, van der Klei IJ (2011) Membrane curvature during peroxisome Wssion requires Pex11. EMBO J 30:5-16
94. Opperdoes FR (1984) Localization of the initial steps in alkoxyphospholipid biosynthesis in glycosomes (microbodies) of Trypanosoma Brucei. FEBS Lett 169:35-39
95. Otera H, Harano T, Honsho M, Ghaedi K, Mukai S, Tanaka A, Kawai A, Shimizu N, Fujiki Y (2000) The mammalian peroxin Pex5pL, the longer isoform of the mobile peroxisome targeting signal (PTS) type 1 transporter, translocates the Pex7p.PTS2 protein complex into peroxisomes via its initial docking site, Pex14p. J Biol Chem 275:21703-21714 (Pubitemid 30481879)
96. Otzen M, Wang D, Lunenborg MG, van der Klei IJ (2005) Hansenula polymorpha Pex20p is an oligomer that binds the peroxisomal targeting signal 2 (PTS2). J Cell Sci 118:3409-3418 (Pubitemid 41246096)
97. Parsons M (2004) Glycosomes: parasites and the divergence of peroxisomal purpose. Mol Microbiol 53:717-724 (Pubitemid 39036953)
98. Perry RJ, Mast FD, Rachubinski RA (2009) Endoplasmic reticulum-associated secretory proteins Sec20p, Sec39p, and Dsl1p are involved in peroxisome biogenesis. Eukaryot Cell 8:830-843
99. Platta HW, El Magraoui F, Schlee D, Grunau S, Girzalsky W, Erdmann R (2007) Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J Cell Biol 177:197-204 (Pubitemid 46658631)
100. Platta HW, El Magraoui F, Bäumer BE, Schlee D, Girzalsky W, Erdmann R (2009) Pex2 and pex12 function as protein-ubiquitin ligases in peroxisomal protein import. Mol Cell Biol 29:5505-5516
101. Pracharoenwattana I, Smith SM (2008) When is a peroxisome not a peroxisome? Trends Plant Sci 13:522-525
102. Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and Wssion molecules? Natl Rev Mol Cell Biol 5:133-147 (Pubitemid 38160256)
103. Purdue PE, Lazarow PB (1996) Targeting of human catalase to peroxisomes is dependent upon a novel COOH-terminal peroxisomal targeting sequence. J Cell Biol 134:849-862 (Pubitemid 26278212)
104. Purdue PE, Yang X, Lazarow PB (1998) Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J Cell Biol 143:1859-1869 (Pubitemid 29022609)
105. Rachubinski RA, Subramani S (1995) How proteins penetrate peroxisomes? Cell 83:525-528
106. Ramón NM, Bartel B (2010) Interdependence of the peroxisometargeting receptors in Arabidopsis thaliana: PEX7 facilitates PEX5 accumulation and import of PTS1 cargo into peroxisomes. Mol Biol Cell 21:1263-1271
107. Ramos FR, López-Nieto MJ, Martín JF (1985) Isopenicillin N synthetase of Penicillium chrysogenum, an enzyme that converts β-(L-aminoadipyl)-L-cysteinyl-D-valine to isopenicillin N. Antimicrob Agents Chemother 27:380-387 (Pubitemid 15144704)
108. Rottensteiner H, Kramer A, Lorenzen S, Stein K, Landgraf C, Volkmer-Engert R, Erdmann R (2004) Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol Biol Cell 15:3406-3417 (Pubitemid 38850133)
109. Rucktäschel R, Girzalsky W, Erdmann R (2011) Protein import machineries of peroxisomes. Biochim Biophys Acta 1808:892-900
110. Sakai Y, Oku M, van der Klei IJ, Kiel JA (2006) Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta 1763:1767-1775 (Pubitemid 44880462)
111. Samsom SM, Belagaje R, Blankenship DT, Chapman JL, Perry D, Skatrud PL, van Frank RM, Abraham EP, Baldwin JE, Queener SW, Ingolia TD (1985) Isolation, sequence determination and expression in Escherichia coli of the isopenicillin N synthetase gene from Cephalosporium acremonium. Nature 318:191-194 (Pubitemid 16192590)
112. Samsom SM, Dotzlaf JF, Slisz ML, Becker GW, van Frank RM, Veal LE, Yeh WK, Miller JR, Queener SW, Ingolia TD (1987) Cloning and expression of the fungal expandase/hydroxylase gene involved in cephalosporin biosynthesis. Bio/Technol 5:1207-1214
113. Saraya R, Veenhuis M, van der Klei IJ (2010) Peroxisomes as dynamic organelles: peroxisome abundance in yeast. FEBS J 277:3279-3288
114. Scheidegger A, Kuenzi MT, Nuesch J (1984) Partial puriWcation and catalitical properties of a bifunctional enzyme in the biosynthetic pathway of β-lactams in Acremonium chrysogenum. J Antibiot 37:522-531 (Pubitemid 14101512)
115. Schliebs W, Kunau WH (2006) PTS2 co-receptors: diverse proteins with common features. Biochim Biophys Acta 1763:1605-1612 (Pubitemid 44880476)
116. Schneider K, Kienow L, Schmelzer E, Colby T, Bartsch M, Miersch O, Wasternack C, Kombrink E, Stuible H-P (2005) A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J Bio Chem 280:13962-13972 (Pubitemid 40517297)
117. Schumann U, Wanner G, Veenhuis M, Schmid M, Gietl C (2003) AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc Natl Acad Sci U S A 100:9626-9631 (Pubitemid 37033978)
118. Sichting M, Schell-Steven A, Prokisch H, Erdmann R, Rottensteiner H (2003) Pex7p and Pex20p of Neurospora crassa function together in PTS2-dependent protein import into peroxisomes. Mol Biol Cell 14:810-821 (Pubitemid 36237034)
119. Soukupova M, Sprenger C, Gorgas K, Kunau W-H, Dodt G(1999) IdentiWcation and characterization of the human peroxin PEX3. Eur J Cell Biol 78:357-374 (Pubitemid 29317372)
120. Sparkes IA, Brandizzi F, Slocombe SP, El-Shami M, Hawes C, Baker A (2003) An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol 133:1809-1819 (Pubitemid 38047310)
121. Sparkes IA, Hawes C, Baker A (2005) AtPEX2 and AtPEX10 are targeted to peroxisomes independently of known endoplasmic reticulum traYcking routes. Plant Physiol 139:690-700 (Pubitemid 43907099)
122. Spröte P, Brakhage AA, Hynes MJ (2009) Contribution of peroxisomes to penicillin biosynthesis in Aspergillus nidulans. Eukaryot Cell 8:421-423
123. Subramani S (1993) Protein import into peroxisomes and biogenesis of the organelle. Annu Rev Cell Biol 9:445-478
124. Swinkels BW, Gould SJ, Subramani S (1992) Targeting eYciencies of various permutations of the consensus C-terminal tripeptide peroxisomal targeting signal. FEBS Lett 305:133-136
125. Tabak HF, Murk JL, Braakman I, Geuze HJ (2003) Peroxisomes start their life in the endoplasmic reticulum. TraYc 4:512-518 (Pubitemid 36896543)
126. Tabak HF, van der Zand A, Braakman I (2008) Peroxisomes: minted by the ER. Curr Opin Cell Biol 20:393-400
127. Teijeira F, Ullán RV, Guerra SM, García-Estrada C, Vaca I, Martín JF (2009) The transporter CefM involved in translocation of biosynthetic intermediates is essential for cephalosporin production. Biochem J 418:113-124
128. Titorenko VI, Rachubinski RA (1998) Mutants of the yeast Yarrowia lipolytica defective in protein exit from the endoplasmic reticulum are also defective in peroxisome biogenesis. Mol Cell Biol 18:2789-2803 (Pubitemid 28183448)
129. Titorenko VI, Terlecky SR (2011) Peroxisome metabolism and cellular aging. TraYc 12:252-259
130. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:153-164
131. Ullán RV, Liu G, Casqueiro J, Gutiérrez S, Bañuelos O, Martín JF (2002) The cefT gene of Acremonium chrysogenum C10 encodes a putative multidrug eZux pump protein that signiWcantly increases cephalosporin C production. Mol Genet Genom 267:673-683
132. Ullán RV, Casqueiro J, Bañuelos O, Fernández FJ, Gutiérrez S, Martín JF (2002) A novel epimerization system in fungal secondary metabolism involved in the conversion of isopenicillin N into penicillin N in Acremonium chrysogenum. J Biol Chem 277:46216-46225 (Pubitemid 35417613)
133. Ullán RV, Teijeira F, Guerra SM, Vaca I, Martín JF (2010) Characterization of a novel peroxisome membrane protein essential for conversion of isopenicillin N into cephalosporin C. Biochem J 432:227-236
134. Van Ael E, Fransen M (2006) Targeting signals in peroxisomal membrane proteins. Biochim Biophys Acta 1763:1629-1638 (Pubitemid 44883384)
135. van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJ, García-Estrada C, Fedorova ND, Harris DM, Heijne WH, Joardar V, Kiel JA, Kovalchuk A, Martín JF, Nierman WC, Nijland JG, Pronk JT, Roubos JA, van der Klei IJ, van Peij NN, Veenhuis M, von Döhren H, Wagner C, Wortman J, Bovenberg RA (2008) Genome sequencing and analysis of the Wlamentous fungus Penicillium chrysogenum. Nature Biotechnol 26:1161-1168
136. van de Kamp M, Driessen AJ, Konings WN (1999) Compartmentalization and transport in β-lactam antibiotic biosynthesis by Wlamentous fungi. Antonie Van Leeuwenhoek 75:41-78 (Pubitemid 29306750)
137. van der Klei IJ, Veenhuis M (1997) Yeast peroxisomes: function and biogenesis of a versatile cell organelle. Trends Microbiol 5:502-509 (Pubitemid 28020375)
138. van der Klei IJ, Veenhuis M (2006) Yeast and Wlamentous fungi as model organisms in microbody research. Biochim Biophys Acta 1763:1364-1373 (Pubitemid 44880483)
139. van der Lende TR, van de Kamp M, Berg M, Sjollema K, Bovenberg RAL, Veenhuis M et al (2002) Delta-(Lalpha-Aminoadipyl)-L-cysteinyl-D-valine synthetase, that mediates the Wrst committed step in penicillin biosynthesis, is a cytosolic enzyme. Fungal Genet Biol 37:49-55
140. Velasco J, Gutierrez S, Campoy S, Martin JF (1999) Molecular characterization of the Acremonium chrysogenum cefG gene product: the native deacetylcephalosporin C acetyltransferase is not processed into subunits. Biochem J 337:379-385
141. Wanders RJ, Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 75:295-332 (Pubitemid 44118035)
142. Wang FQ, Liu J, Dai M, Ren ZH, Su CY, He JG (2007) Molecular cloning and functional identiWcation of a novel phenylacetyl-CoA ligase gene from Penicillium chrysogenum. Biochem Biophys Res Commun 360:453-458 (Pubitemid 47030364)
143. Wanner G, Theimer RR (1982) Two types of microbodies in Neurospora crassa. Ann N Y Acad Sci 386:269-284
144. Watkins PA, Howard AE, Mihalik SJ (1994) Phytanic acid must be activated to phytanoyl-CoA prior to its β-oxidation in rat liver peroxisomes. Biochim Biophys Acta 1214:288-294 (Pubitemid 24312454)
145. Weber H (2002) Fatty acid-derived signals in plants. Trends Plant Sci 7:217-224 (Pubitemid 36725944)
146. Wiemer EAC, Ijlst L, Van Roy J, Wanders RJA, Opperdoes FR (1996) IdentiWcation of 2-enoyl coenzyme A hydratase and NADP+-dependent
147. Williams C, van den Berg M, Sprenger RR, Distel B (2007) A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J Biol Chem 282:22534-22543 (Pubitemid 47267315)
148. Williams C, van den Berg M, Geers E, Distel B (2008) Pex10p functions as an E3 ligase for the Ubc4p-dependent ubiquitination of Pex5p. Biochem Biophys Res Commun 374:620-624
149. Wolf J, Schliebs W, Erdmann R (2010) Peroxisomes as dynamic organelles: peroxisomal matrix protein import. FEBS J 277: 3268-3278
150. Woodward AW, Bartel B (2005) The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol Biol Cell 16:573-583 (Pubitemid 40165556)
151. Yu ZL, Liu J, Wang FQ, Dai M, Zhao BH, He JG, Zhang H (2011) Cloning and characterization of a novel CoA-ligase gene from Penicillium chrysogenum. Folia Microbiol (Praha) 56:246-252
152. Yuan P, Jedd G, Kumaran D, Swaminathan S, Shio H, Hewitt D, Chua NH, Swaminathan K (2003) A HEX-1 crystal lattice required for Woronin body function in Neurospora crassa. Nat Struct Biol 10:264-270 (Pubitemid 36418750)
153. Zolman BK, Yoder A, Bartel B (2000) Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 156:1323-1337
154. Zolman BK, Bartel B (2004) An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proc Natl Acad Sci U S A 101:1786-1791 (Pubitemid 38234232)