Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome


Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome

Guo, Tong and Kit, Yuriy Y. and Nicaud, Jean-Marc and Le Dall, Marie-Thérèse and Sears, S. Kelly and Vali, Hojatollah and Chan, Honey and Rachubinski, Richard A. and Titorenko, Vladimir I. (2003) Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome. The Journal of Cell Biology, 162 (7). pp. 1255-1266. ISSN 0021-9525

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We describe an unusual mechanism for organelle division. In the yeast Yarrowia lipolytica, only mature peroxisomes contain the complete set of matrix proteins. These mature peroxisomes assemble from several immature peroxisomal vesicles in a multistep pathway. The stepwise import of distinct subsets of matrix proteins into different immature intermediates along the pathway causes the redistribution of a peroxisomal protein, acyl-CoA oxidase (Aox), from the matrix to the membrane. A significant redistribution of Aox occurs only in mature peroxisomes. Inside mature peroxisomes, the membrane-bound pool of Aox interacts with Pex16p, a membrane-associated protein that negatively regulates the division of early intermediates in the pathway. This interaction inhibits the negative action of Pex16p, thereby allowing mature peroxisomes to divide.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Authors:Guo, Tong and Kit, Yuriy Y. and Nicaud, Jean-Marc and Le Dall, Marie-Thérèse and Sears, S. Kelly and Vali, Hojatollah and Chan, Honey and Rachubinski, Richard A. and Titorenko, Vladimir I.
Journal or Publication:The Journal of Cell Biology
Date:22 September 2003
ID Code:7565
Deposited On:11 May 2011 12:50
Last Modified:11 May 2011 12:50
Bonifacino, J.S., and E.C. Dell'Angelica. 1998. Immunoprecipitation. In Current Protocols in Cell Biology. J.S. Bonifacino, M. Dasso, J.B. Harford, J. Lippincott-Schwartz, and K. Yamada, editors. John Wiley & Sons Inc., New York. 7.2.1–7.2.21.

Chang, C.C., S. South, D. Warren, J. Jones, A.B. Moser, H.W. Moser, and S.J. Gould. 1999. Metabolic control of peroxisome abundance. J. Cell Sci. 112:1579–1590.

Eitzen, G.A., R.K. Szilard, and R.A. Rachubinski. 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.

Eitzen, G.A., V.I. Titorenko, J.J. Smith, M. Veenhuis, R.K. Szilard, and R.A. Rachubinski. 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.

Faber, K.N., J.A. Heyman, and S. Subramani. 1998. Two AAA family peroxins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes. Mol. Cell. Biol. 18:936–943.

Fan, C.Y., J. Pan, N. Usuda, A.V. Yeldandi, M.S. Rao, and J.K. Reddy. 1998. Steatohepatitis, spontaneous peroxisome proliferation and liver tumors in mice lacking peroxisomal fatty acyl-CoA oxidase. Implications for peroxisome proliferator-activated receptor α natural ligand metabolism. J. Biol. Chem. 273:15639–15645.

Goodman, J.M., S.B. Tramp, H. Hang, and M. Veenhuis. 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.

Gould, S.J., and D. Valle. 2000. Peroxisome biogenesis disorders: genetics and cell biology. Trends Genet. 16:340–345.

Heinemann, P., and W.W. Just. 1992. Peroxisomal protein import. In vivo evidence for a novel translocation competent compartment. FEBS Lett. 300:179–182.

Lazarow, P.B., and Y. Fujiki. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489–530.

Li, X., and S.J. Gould. 2002. PEX11 promotes peroxisome division independently of peroxisome metabolism. J. Cell Biol. 156:643–651.

Lüers, G., T. Hashimoto, H.D. Fahimi, and A. Völkl. 1993. Biogenesis of peroxisomes: isolation and characterization of two distinct peroxisomal populations from normal and regenerating rat liver. J. Cell Biol. 121:1271–1280.

Matsuzono, Y., N. Kinoshita, S. Tamura, N. Shimozawa, M. Hamasaki, K. Ghaedi, R.J.A. Wanders, Y. Suzuki, N. Kondo, and Y. Fujiki. 1999. Human PEX19: cDNA cloning by functional complementation, mutational analysis in a patient with Zellweger syndrome and potential role in peroxisomal membrane assembly. Proc. Natl. Acad. Sci. USA. 96:2116–2121.

Poll-Thé, B.T., F. Roels, H. Ogier, J. Scotto, J. Vamecq, R.B. Schutgens, R.J. Wanders, C.W. van Roermund, M.J. van Wijland, A.W. Schram, et al. 1988. A new peroxisomal disorder with enlarged peroxisomes and a specific deficiency of acyl-CoA oxidase (pseudo-neonatal adrenoleukodystrophy). Am. J. Hum. Genet. 42:422–434.

Purdue, P.E., and P.B. Lazarow. 2001. Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17:701–752.

Sacksteder, K.A., and S.J. Gould. 2000. The genetics of peroxisome biogenesis. Annu. Rev. Genet. 34:623–652.

Smith, J.J., R.K. Szilard, M. Marelli, and R.A. Rachubinski. 1997. The peroxi Pex17p of the yeast Yarrowia lipolytica is associated peripherally with the peroxisomal membrane and is required for the import of a subset of matrix proteins. Mol. Cell. Biol. 17:2511–2520.

Smith, J.J., T.W. Brown, G.A. Eitzen, and R.A. Rachubinski. 2000. Regulation of peroxisome size and number by fatty acid β-oxidation in the yeast Yarrowia lipolytica. J. Biol. Chem. 275:20168–20178.

Snyder, W.B., K.N. Faber, T.J. Wenzel, A. Koller, G.H. Luers, L. Rangell, G.A. Keller, and S. Subramani. 1999. Pex19p interacts with Pex3p and Pex10p and is essential for peroxisome biogenesis in Pichia pastoris. Mol. Biol. Cell. 10:1745–1761.

South, S.T., and S.J. Gould. 1999. Peroxisome synthesis in the absence of preexisting peroxisomes. J. Cell Biol. 144:255–266.

Subramani, S., A. Koller, and W.B. Snyder. 2000. Import of peroxisomal matrix and membrane proteins. Annu. Rev. Biochem. 69:399–418.

Szilard, R.K., V.I. Titorenko, M. Veenhuis, and R.A. Rachubinski. 1995. Pay32p of the yeast Yarrowia lipolytica is an intraperoxisomal component of the matrix protein translocation machinery. J. Cell Biol. 131:1453–1469.

Tan, X., H.R. Waterham, M. Veenhuis, and J.M. Cregg. 1995. The Hansenula polymorpha PER8 gene encodes a novel peroxisomal integral membrane protein involved in proliferation. J. Cell Biol. 128:307–319.

Titorenko, V.I., and R.A. Rachubinski. 2000. Peroxisomal membrane fusion requires two AAA family ATPases, Pex1p and Pex6p. J. Cell Biol. 150:881–886.

Titorenko, V.I., and R.A. Rachubinski. 2001a. Dynamics of peroxisome assembly and function. Trends Cell Biol. 11:22–29.

Titorenko, V.I., and R.A. Rachubinski. 2001b. The life cycle of the peroxisome. Nat. Rev. Mol. Cell Biol. 2:357–368.

Titorenko, V.I., G.A. Eitzen, and R.A. Rachubinski. 1996. Mutations in the PAY5 gene of the yeast Yarrowia lipolytica cause the accumulation of multiple subpopulations of peroxisomes. J. Biol. Chem. 271:20307–20314.

Titorenko, V.I., J.J. Smith, R.K. Szilard, and R.A. Rachubinski. 1998. Pex20p of the yeast Yarrowia lipolytica is required for the oligomerization of thiolase in the cytosol and for its targeting to the peroxisome. J. Cell Biol. 142:403–420.

Titorenko, V.I., H. Chan, and R.A. Rachubinski. 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.

Titorenko, V.I., J.-M. Nicaud, H. Wang, H. Chan, and R.A. Rachubinski. 2002. Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J. Cell Biol. 156:481–494.

van Roermund, C.W.T., M. van den Berg, and R.J. Wanders. 1995. Localization of peroxisomal 3-oxoacyl-CoA thiolase in particles of varied density in rat liver: implications for peroxisome biogenesis. Biochim. Biophys. Acta. 1245:348–358.

van Roermund, C.W.T., H.F. Tabak, M. van den Berg, R.J.A. Wanders, and E.H. Hettema. 2000. Pex11p plays a primary role in medium-chain fatty acid oxidation, a process that affects peroxisome number and size in Saccharomyces cerevisiae. J. Cell Biol. 150:489–498.

Veenhuis, M., and J.M. Goodman. 1990. Peroxisomal assembly: membrane proliferation precedes the induction of the abundant matrix proteins in the methylotrophic yeast Candida boidinii. J. Cell Sci. 96:583–590.

Wang, H.J., M.T. Le Dall, Y. Waché, C. Laroche, J.M. Belin, C. Gaillardin, and J.M. Nicaud. 1999. Evaluation of acyl coenzyme A oxidase (Aox) isozyme function in the n-alkane-assimilating yeast Yarrowia lipolytica. J. Bacteriol. 181:5140–5148.

Wilcke, M., K. Hultenby, and S.E.H. Alexson. 1995. Novel peroxisomal populations in subcellular fractions from rat liver. Implications for peroxisome structure and biogenesis. J. Biol. Chem. 270:6949–6958.

Xu, Z., K. Sato, and W. Wickner. 1998. LMA1 binds to vacuoles at Sec18p (NSF), transfers upon ATP hydrolysis to a t-SNARE (Vam3p) complex, and is released during fusion. Cell. 93:1125–1134.
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