De novo peroxisome biogenesis in penicillium chrysogenum is not dependent on the pex11 family members or pex16

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Opaliński, Lukasz ^a   Bartoszewska, Magdalena ^a   Fekken, Susan ^a   Liu, Haiyin ^a   de Boer, Rinse ^a   van der Klei, Ida ^a   Veenhuis, Marten ^a   Kiel, Jan A K W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN PEX11; PROTEIN PEX16; PROTEIN PEX3; UNCLASSIFIED DRUG; FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; PENICILLIN G;

ARTICLE; BIOGENESIS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGAL CELL; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; NONHUMAN; NUCLEOTIDE SEQUENCE; PENICILLIUM CHRYSOGENUM; PEROXISOME; PEX16 GENE; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; GENE INACTIVATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; ULTRASTRUCTURE;

FUNGI; MAMMALIA; PENICILLIUM CHRYSOGENUM;

FUNGAL PROTEINS; GENE KNOCKOUT TECHNIQUES; GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; PENICILLIN G; PENICILLIUM CHRYSOGENUM; PEROXISOMES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 84859811841     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035490     Document Type: Article

References (50)

1. Aksam EB, de Vries B, van der Klei IJ, Kiel JA, (2009) Preserving organelle vitality: peroxisomal quality control mechanisms in yeast. FEMS Yeast Res 9: 808-820.
2. Bartoszewska M, Opalinski L, Veenhuis M, van der Klei IJ, (2011) The significance of peroxisomes in secondary metabolite biosynthesis in filamentous fungi. Biotechnol Lett 33: 1921-1931.
3. van der Klei IJ, Veenhuis M, (2006) Yeast and filamentous fungi as model organisms in microbody research. Biochim Biophys Acta 1763: 1364-1373.
4. Martin JF, Ullan RV, Garcia-Estrada C, (2012) Role of peroxisomes in the biosynthesis and secretion of beta-lactams and other secondary metabolites. J Ind Microbiol Biotechnol 39: 367-382.
5. Nuttall JM, Motley A, Hettema EH, (2011) Peroxisome biogenesis: recent advances. Curr Opin Cell Biol 23: 421-426.
6. Saraya R, Veenhuis M, van der Klei IJ, (2010) Peroxisomes as dynamic organelles: peroxisome abundance in yeast. FEBS J 277: 3279-3288.
7. Saraya R, Krikken AM, Veenhuis M, van der Klei IJ, (2011) Peroxisome reintroduction in Hansenula polymorpha requires Pex25 and Rho1. J Cell Biol 193: 885-900.
8. Huber A, Koch J, Kragler F, Brocard C, Hartig A, (2012) A Subtle Interplay Between Three Pex11 Proteins Shapes De Novo Formation and Fission of Peroxisomes. Traffic 13: 157-167.
9. Lam SK, Yoda N, Schekman R, (2011) A vesicle carrier that mediates peroxisome protein traffic from the endoplasmic reticulum. Proc Natl Acad Sci U S A 108: E51-52.
10. Agrawal G, Joshi S, Subramani S, (2011) Cell-free sorting of peroxisomal membrane proteins from the endoplasmic reticulum. Proc Natl Acad Sci U S A 108: 9113-9118.
11. Nagotu S, Saraya R, Otzen M, Veenhuis M, van der Klei IJ, (2008) Peroxisome proliferation in Hansenula polymorpha requires Dnm1p which mediates fission but not de novo formation. Biochim Biophys Acta 1783: 760-769.
12. Motley AM, Hettema EH, (2007) Yeast peroxisomes multiply by growth and division. J Cell Biol 178: 399-410.
13. Koch J, Brocard C, (2011) Membrane elongation factors in organelle maintenance: the case of peroxisome proliferation. Biomol Concepts 2: 353-364.
14. Koch J, Pranjic K, Huber A, Ellinger A, Hartig A, et al. (2010) PEX11 family members are membrane elongation factors that coordinate peroxisome proliferation and maintenance. J Cell Sci 123: 3389-3400.
15. Lingard MJ, Trelease RN, (2006) Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation. J Cell Sci 119: 1961-1972.
16. Opalinski L, Kiel JA, Williams C, Veenhuis M, van der Klei IJ, (2011) Membrane curvature during peroxisome fission requires Pex11. EMBO J 30: 5-16.
17. Opalinski L, Veenhuis M, van der Klei IJ, (2011) Peroxisomes: membrane events accompanying peroxisome proliferation. Int J Biochem Cell Biol 43: 847-851.
18. Zhang X, Hu J, (2010) The Arabidopsis chloroplast division protein DYNAMIN-RELATED PROTEIN5B also mediates peroxisome division. Plant Cell 22: 431-442.
19. Lingard MJ, Gidda SK, Bingham S, Rothstein SJ, Mullen RT, et al. (2008) Arabidopsis PEROXIN11c-e, FISSION1b, and DYNAMIN-RELATED PROTEIN3A cooperate in cell cycle-associated replication of peroxisomes. Plant Cell 20: 1567-1585.
20. Motley AM, Ward GP, Hettema EH, (2008) Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p. J Cell Sci 121: 1633-1640.
21. Kuravi K, Nagotu S, Krikken AM, Sjollema K, Deckers M, et al. (2006) Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J Cell Sci 119: 3994-4001.
22. Hoepfner D, van den Berg M, Philippsen P, Tabak HF, Hettema EH, (2001) A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J Cell Biol 155: 979-990.
23. Opalinski L, Kiel JA, Homan TG, Veenhuis M, van der Klei IJ, (2010) Penicillium chrysogenum Pex14/17p-a novel component of the peroxisomal membrane that is important for penicillin production. FEBS J 277: 3203-3218.
24. Meijer WH, Gidijala L, Fekken S, Kiel JA, van den Berg MA, et al. (2010) Peroxisomes are required for efficient penicillin biosynthesis in Penicillium chrysogenum. Appl Environ Microbiol 76: 5702-5709.
25. Kiel JA, van der Klei IJ, van den Berg MA, Bovenberg RA, Veenhuis M, (2005) Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet Biol 42: 154-164.
26. van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, et al. (2008) Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol 26: 1161-1168.
27. Kiel JA, Veenhuis M, van der Klei IJ, (2006) PEX genes in fungal genomes: common, rare or redundant. Traffic 7: 1291-1303.
28. Honsho M, Tamura S, Shimozawa N, Suzuki Y, Kondo N, et al. (1998) Mutation in PEX16 is causal in the peroxisome-deficient Zellweger syndrome of complementation group D. Am J Hum Genet 63: 1622-1630.
29. Honsho M, Hiroshige T, Fujiki Y, (2002) The membrane biogenesis peroxin Pex16p. Topogenesis and functional roles in peroxisomal membrane assembly. J Biol Chem 277: 44513-44524.
30. Karnik SK, Trelease RN, (2007) Arabidopsis peroxin 16 trafficks through the ER and an intermediate compartment to pre-existing peroxisomes via overlapping molecular targeting signals. J Exp Bot 58: 1677-1693.
31. Karnik SK, Trelease RN, (2005) Arabidopsis peroxin 16 coexists at steady state in peroxisomes and endoplasmic reticulum. Plant Physiol 138: 1967-1981.
32. Kim PK, Mullen RT, Schumann U, Lippincott-Schwartz J, (2006) The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER. J Cell Biol 173: 521-532.
33. Matsuzaki T, Fujiki Y, (2008) The peroxisomal membrane protein import receptor Pex3p is directly transported to peroxisomes by a novel Pex19p- and Pex16p-dependent pathway. J Cell Biol 183: 1275-1286.
34. Toro AA, Araya CA, Cordova GJ, Arredondo CA, Cardenas HG, et al. (2009) Pex3p-dependent peroxisomal biogenesis initiates in the endoplasmic reticulum of human fibroblasts. J Cell Biochem 107: 1083-1096.
35. Gidijala L, Bovenberg RA, Klaassen P, van der Klei IJ, Veenhuis M, et al. (2008) Production of functionally active Penicillium chrysogenum isopenicillin N synthase in the yeast Hansenula polymorpha. BMC Biotechnol 8: 29.
36. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning, a Laboratory Manual, 2nd edition Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
37. Cantoral JM, Díez B, Barredo JL, Alvarez E, Martín JF, (1987) High-frequency transformation of Penicillium chrysogenum. Biotechnology 5: 494-497.
38. Kiel JA, van den Berg MA, Fusetti F, Poolman B, Bovenberg RA, et al. (2009) Matching the proteome to the genome: the microbody of penicillin-producing Penicillium chrysogenum cells. Funct Integr Genomics 9: 167-184.
39. Waterham HR, Titorenko VI, Haima P, Cregg JM, Harder W, et al. (1994) The Hansenula polymorpha PER1 gene is essential for peroxisome biogenesis and encodes a peroxisomal matrix protein with both carboxy- and amino-terminal targeting signals. J Cell Biol 127: 737-749.
40. Guo T, Gregg C, Boukh-Viner T, Kyryakov P, Goldberg A, et al. (2007) A signal from inside the peroxisome initiates its division by promoting the remodeling of the peroxisomal membrane. J Cell Biol 177: 289-303.
41. Eitzen GA, Szilard RK, Rachubinski RA, (1997) Enlarged peroxisomes are present in oleic acid-grown Yarrowia lipolytica overexpressing the PEX16 gene encoding an intraperoxisomal peripheral membrane peroxin. J Cell Biol 137: 1265-1278.
42. Kiel JA, van den Berg M, Bovenberg RA, van der Klei IJ, Veenhuis M, (2004) Penicillium chrysogenum Pex5p mediates differential sorting of PTS1 proteins to microbodies of the methylotrophic yeast Hansenula polymorpha. Fungal Genet Biol 41: 708-720.
43. Schliebs W, Kunau WH, (2004) Peroxisome membrane biogenesis: the stage is set. Curr Biol 14: R397-399.
44. Li X, Gould SJ, (2003) The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J Biol Chem 278: 17012-17020.
45. Gandre-Babbe S, van der Bliek AM, (2008) The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 19: 2402-2412.
46. Koch A, Yoon Y, Bonekamp NA, McNiven MA, Schrader M, (2005) A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 16: 5077-5086.
47. Muller WH, van der Krift TP, Krouwer AJ, Wosten HA, van der Voort LH, et al. (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J 10: 489-495.
48. Antonenkov VD, Hiltunen JK, (2011) Transfer of metabolites across the peroxisomal membrane. Biochim Biophys Acta.
49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
50. Van de Peer Y, De Wachter R, (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10: 569-570.