Peroxisome biogenesis occurs in an unsynchronized manner in close association with the endoplasmic reticulum in temperature-sensitive Yarrowia lipolytica Pex3p mutants

Molecular Biology of the Cell

Volumn 14, Issue 3, 2003, Pages 939-957

  Bascom, Roger A ^a   Chan, Honey ^a   Rachubinski, Richard A ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX PROTEIN; MEMBRANE PROTEIN; PROTEIN KAR2P; PROTEIN PEX3P; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL FRACTIONATION; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; CULTURE MEDIUM; ENDOPLASMIC RETICULUM; GENE CLUSTER; GENE OVEREXPRESSION; GENE SEQUENCE; IMMUNOHISTOCHEMISTRY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PRIORITY JOURNAL; REPORTER GENE; SEQUENCE ANALYSIS; TEMPERATURE SENSITIVITY; YARROWIA LIPOLYTICA;

ACETYL-COA C-ACETYLTRANSFERASE; AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; ENDOPLASMIC RETICULUM; GENES, REPORTER; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PEROXISOMES; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; TEMPERATURE; YARROWIA;

YARROWIA LIPOLYTICA;

EID: 0037343124     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-10-0633     Document Type: Article

References (46)

1. Aitchison, J.D., Szilard, R.K., Nuttley, W.M., and Rachubinski, R.A. (1992). Antibodies directed against a yeast carboxy-terminal peroxisomal targeting signal specifically recognize peroxisomal proteins from various yeasts. Yeast 8, 721-734.
2. Ausubel, F.J., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1994). Current Protocols in Molecular Biology, New York: John Wiley & Sons.
3. Blanchette-Mackie, E.J., Dwyer, N.K., Barber, T., Coxey, R.A., Takeda, T., Rondinone, C.M., Theodorakis, J.L., Greenberg, A.S., and Londos, C. (1995). Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36, 1211-1226.
4. Brown, D.A. (2001). Lipid droplets: proteins floating on a pool of fat. Curr. Biol. 11, R446-R449.
5. Chang, C.C., South, S., Warren, D., Jones, J., Moser, A.B., Moser, H.W., and Gould, S.J. (1999). Metabolic control of peroxisome abundance. J. Cell Sci. 112, 1579-1590.
6. Chapman, K.D., and Trelease, R.N. (1991). Acquisition of membrane lipids by differentiating glyoxysomes: role of lipid bodies. J. Cell Biol. 115, 995-1007.
7. Eitzen, G.A., Szilard, R.K., and Rachubinski, R.A. (1997). Enlarged peroxisomes are present in oleic acid-grown Yarrowia lipolytica over-expressing the PEX16 gene encoding an intraperoxisomal peripheral membrane peroxin. J. Cell Biol. 137, 1265-1278.
8. Eitzen, G.A., Titorenko, V.I., Smith, J.J., Veenhuis, M., Szilard, R.K., and Rachubinski, R.A. (1996). The Yarrowia lipolytica gene PAY5 encodes a peroxisomal integral membrane protein homologous to the mammalian peroxisome assembly factor PAF-1. J. Biol. Chem. 271, 20300-20306.
9. Erdmann, R., and Blobel, G. (1995). Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J. Cell Biol. 128, 509-523.
10. Faber, K.N., Haan, G.J., Baerends, R.J., Kram, A.M., and Veenhuis, M. (2002). Normal peroxisome development from vesicles induced by truncated Hansenula polymorpha Pex3p. J. Biol. Chem. 277, 11026-11033.
11. Goodman, J.M., Trapp, S.B., Hwang, H., and Veenhuis, M. (1990). Peroxisomes induced in Candida boidinii by methanol, oleic acid and D-alanine vary in metabolic function but share common integral membrane proteins. J. Cell Sci. 97, 193-204.
12. Götte, K., Girzalsky, W., Linkert, M., Baumgart, E., Kammerer, S., Kunau, W.-H., and Erdmann, R. (1998). Pex19p, a farnesylated protein essential for peroxisome biogenesis. Mol. Cell. Biol. 18, 616-628.
13. Gould, S.J., and Valle, D. (2000). Peroxisome biogenesis disorders: genetics and cell biology. Trends Genet. 16, 340-345.
14. Harlow, E., and Lane, D. (1999). Using Antibodies. A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
15. Hettema, E.H., Girzalsky, W., van den Berg, M., Erdmann, R., and Distel, B. (2000). Saccharomyces cerevisiae Pex3p and Pex19p are required for proper localization and stability of peroxisomal membrane proteins. EMBO J. 19, 223-233.
16. Kerscher, S.J., Eschemann, A., Okun, P.M., and Brandt, U. (2001). External alternative NADH:ubiquinone oxidoreductase redirected to the internal face of the mitochondrial inner membrane rescues complex I deficiency in Yarrow lipolytica. J. Cell Sci. 114, 3915-3921.
17. Kutay, U., Hartmann, E., and Rapoport, T.A. (1993). A class of membrane proteins with a C-terminal anchor. Trends Cell Biol. 3, 72-75.
18. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
19. Lazarow, P.B., and Fujiki, Y. (1985). Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1, 489-530.
20. Marshall, P.A., Krimkevich, Y.I., Lark, R.H., Dyer, J.M., Veenhuis, M., and Goodman, J.M. (1995). Pmp27 promotes peroxisomal proliferation. J. Cell Biol. 129, 345-355.
21. Murphy, D.J., and Vance, J. (1999). Mechanisms of lipid-body formation. Trends Biochem. Sci. 24, 109-115.
22. Nuttley, W.M., Brade, A.M., Gaillardin, C., Eitzen, G.A., Glover, J.R., Aitchison, J.D., and Rachubinski, R.A. (1993). Rapid identification and characterization of peroxisomal assembly mutants in Yarrowia lipolytica. Yeast 9, 507-517.
23. Prattes, S., Horl, G., Hammer, A., Blaschitz, A., Graier, W.F., Sattler, W., Zechner, R., and Steyrer, E. (2000). Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures. J. Cell Sci. 113, 2977-2989.
24. Pringle, J.R. (1975). Induction, selection, and experimental uses of temperature-sensitive and other conditional mutants of yeast. Methods Cell Biol. 12, 233-272.
25. Purdue, P.E., and Lazarow, P.B. (2001). Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17, 701-752.
26. Sakai, Y., Koller, A., Rangell, L.K., Keller, G.A., and Subramani, S. (1998). Peroxisome degradation by microautophagy in Pichia pastoris: identification of specific steps and morphological intermediates. J. Cell Biol. 141, 625-636.
27. Santos, M.J., Imanaka, T., Shio, H., Small, G.M., and Lazarow, P.B. (1988). Peroxisomal membrane ghosts in Zellweger syndrome - aberrant organelle assembly. Science 239, 1536-1538.
28. Schrader, M., Reuber, B.E., Morrell, J.C., Jimenez-Sanchez, G., Obie, C., Stroh, T.A., Valle, D., Schroer, T.A., and Gould, S.J. (1998). Expression of PEX11β mediates peroxisome proliferation in the absence of external stimuli. J. Biol. Chem. 273, 29607-29614.
29. Smith, J.J., Brown, T.W., Eitzen, G.A., and Rachubinski, R.A. (2000). Regulation of peroxisome size and number by fatty acid β-oxidation in the yeast Yarrowia lipolytica. J. Biol. Chem. 275, 20168-20178.
30. Smith, J.J., Marelli, M., Christmas, R.H., Vizeacoumar, F.J., Dilworth, D.J., Ideker, T., Galitski, T., Dimitrov, K., Rachubinski, R.A., and Aitchison, J.D. (2002). Transcriptome profiling to identify genes involved in peroxisome assembly and function. J. Cell Biol. 158, 259-271.
31. Snyder, W.B., Koller, A., Choy, A.J., and Subramani, S. (2000). The peroxin Pex19p interacts with multiple, integral membrane proteins at the peroxisomal membrane. J. Cell Biol. 149, 1171-1177.
32. Soukupova, M., Sprenger, C., Gorgas, K., Kunau, W.-H., and Dodt, G. (1999). Identification and characterization of the human peroxin PEX3. Eur. J. Cell Biol. 78, 357-374.
33. South, S.T., Baumgart, E., and Gould, S.J. (2001). Inactivation of the endoplasmic reticulum protein translocation factor, Sec61p, or its homolog, Ssh1p, does not affect peroxisome biogenesis. Proc. Natl. Acad. Sci. USA 98, 12027-12031.
34. South, S.T., Sacksteder, K.A., Li, X., Liu, Y., and Gould, S.J. (2000). Inhibitors of COPI and COPII do not block PEX3-mediated peroxisome synthesis. J. Cell Biol. 149, 1345-1360.
35. Subramani, S. (1998). Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement. Physiol. Rev. 78, 171-188.
36. Subramani, S., Antonius, K., and Synder, W.B. (2000). Import of peroxisomal matrix and membrane proteins. Annu. Rev. Biochem. 69, 399-418.
37. Szilard, R.K., Titorenko, V.I., Veenhuis, M., and Rachubinski, R.A. (1995). Pay32p of the yeast Yarrowia lipolytica is an intraperoxisomal component of the matrix protein translocation machinery. J. Cell Biol. 131, 1453-1469.
38. Tam, Y.Y.C., and Rachubinski, R.A. (2002). Yarrowia lipolytica cells mutant for the PEX24 gene encoding a peroxisomal membrane peroxin mislocalize peroxisomal proteins and accumulate membrane structures containing both peroxisomal matrix and membrane proteins. Mol. Biol. Cell 13, 2681-2691.
39. Titorenko, V.I., and Rachubinski, R.A. (2000). Peroxisomal membrane fusion requires two AAA family ATPases, Pex1p and Pex6p. J. Cell Biol. 150, 881-886.
40. Titorenko, V.I., and Rachubinski, R.A. (2001). The life cycle of the peroxisome. Nature Rev. Mol. Cell Biol. 2, 357-368.
41. Titorenko, V.I., Chan, H., and Rachubinski, R.A. (2000). Fusion of small peroxisomal vesicles in vitro reconstructs an early step in the in vivo multistep peroxisome assembly pathway of Yarrowia lipolytica. J. Cell Biol. 148, 29-43.
42. Titorenko, V.I., and Rachubinski, R.A. (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.
43. Titorenko, V.I., Ogrydziak, D.M., and Rachubinski, R.A. (1997). Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17, 5210-5226.
44. van den Bosch, H., Schutgens, R.B.H., Wanders, R.J.A., and Tager, J.M. (1992). Biochemistry of peroxisomes. Annu. Rev. Biochem. 61, 157-197.
45. Wang, H.J., Le Dall, M.-T., Waché, Y., Laroche, C., Belin, J.-M., Gaillardin, C., and Nicaud, J.-M. (1999). Evaluation of acyl coenzyme A oxidase (Aox) isoenzyme function in the n-alkane-assimilating yeast Yarrowia lipolytica. J. Bacteriol. 181, 5140-5148.
46. Zweytick, D., Athenstaedt, K., and Daum, G. (2000). Intracellular lipid particles of eukaryotic cells. Biochim. Biophys. Acta 1469, 101-120.