Guo, Tong and Gregg, Christopher and Boukh-Viner, Tatiana and Kyryakov, Pavlo and Goldberg, Alexander A. and Bourque, Simon D. and Banu, Farhana and Haile, Sandra and Milijevic, Svetlana and San, Karen Hung Yeung and Solomon, Jonathan and Wong, Vivianne and Titorenko, Vladimir I. (2007) A signal from inside the peroxisome initiates its division by promoting the remodeling of the peroxisomal membrane. Journal of Cell Biology, 177 (2). pp. 289-303. ISSN 1540-8140
- Published Version
Official URL: http://dx.doi.org/10.1083/jcb.200609072
We define the dynamics of spatial and temporal reorganization of the team of proteins and lipids serving peroxisome division. The peroxisome becomes competent for division only after it acquires the complete set of matrix proteins involved in lipid metabolism. Overloading the peroxisome with matrix proteins promotes the relocation of acyl-CoA oxidase (Aox), an enzyme of fatty acid β-oxidation, from the matrix to the membrane. The binding of Aox to Pex16p, a membrane-associated peroxin required for peroxisome biogenesis, initiates the biosynthesis of phosphatidic acid and diacylglycerol (DAG) in the membrane. The formation of these two lipids and the subsequent transbilayer movement of DAG initiate the assembly of a complex between the peroxins Pex10p and Pex19p, the dynamin-like GTPase Vps1p, and several actin cytoskeletal proteins on the peroxisomal surface. This protein team promotes membrane fission, thereby executing the terminal step of peroxisome division.
|Divisions:||Concordia University > Faculty of Arts and Science > Biology|
|Authors:||Guo, Tong and Gregg, Christopher and Boukh-Viner, Tatiana and Kyryakov, Pavlo and Goldberg, Alexander A. and Bourque, Simon D. and Banu, Farhana and Haile, Sandra and Milijevic, Svetlana and San, Karen Hung Yeung and Solomon, Jonathan and Wong, Vivianne and Titorenko, Vladimir I.|
|Journal or Publication:||Journal of Cell Biology|
|Date:||16 April 2007|
|Digital Object Identifier (DOI):||10.1083/jcb.200609072|
|Deposited By:||DANIELLE DENNIE|
|Deposited On:||10 May 2011 21:40|
|Last Modified:||24 Aug 2016 21:26|
Athenstaedt, K., and G. Daum. 1999. Phosphatidic acid, a key intermediate in lipid metabolism. Eur. J. Biochem. 266:1–16.
Bankaitis, V.A. 2002. Slick recruitment to the Golgi. Science. 295:290–291.
Behnia, R., and S. Munro. 2005. Organelle identity and the signposts for membrane traffic. Nature. 438:597–604.
Boukh-Viner, T., T. Guo, A. Alexandrian, A. Cerracchio, C. Gregg, S. Haile, R. Kyskan, S. Milijevic, D. Oren, J. Solomon, et al. 2005. Dynamic ergosterol- and ceramide-rich domains in the peroxisomal membrane serve as an organizing platform for peroxisome fusion. J. Cell Biol. 168:761–773.
Carman, G.M., and G.S. Han. 2006. Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem. Sci. 31:694–699.
Chernomordik, L.V., and M.M. Kozlov. 2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72:175–207.
Colanzi, A., C. Suetterlin, and V. Malhotra. 2003. Cell-cycle-specific Golgi fragmentation: how and why? Curr. Opin. Cell Biol. 15:462–467.
Corda, D., A. Colanzi, and A. Luini. 2006. The multiple activities of CtBP/BARS proteins: the Golgi view. Trends Cell Biol. 16:167–173.CrossRefMedline↵ De Matteis, M., A. Godi, and D. Corda. 2002. Phosphoinositides and the Golgi complex. Curr. Opin. Cell Biol. 14:434–447.
Diaz Anel, A.M., and V. Malhotra. 2005. PKCη is required for β1γ2/β3γ2- and PKD-mediated transport to the cell surface and the organization of the Golgi apparatus. J. Cell Biol. 169:83–91.
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.
Farsad, K., and P. De Camilli. 2003. Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15:372–381.
Fratti, R.A., Y. Jun, A.J. Merz, N. Margolis, and W. Wickner. 2004. Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. J. Cell Biol. 167:1087–1098.
Fried, B., and J. Sherma. 1999. Thin-Layer Chromatography. Marcel Dekker, Inc., New York. 499 pp.
Guo, T., Y.Y. Kit, J.-M. Nicaud, M.-T. Le Dall, S.K. Sears, H. Vali, H. Chan, R.A. Rachubinski, and V.I. Titorenko. 2003. Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome. J. Cell Biol. 162:1255–1266.
Hannun, Y.A., C. Luberto, and K.M. Argraves. 2001. Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry. 40:4893–4903.CrossRefMedline↵ Hoepfner, D., M. van den Berg, P. Philippsen, H.F. Tabak, and E.H. Hettema. 2001. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155:979–990.
Holthuis, J.C., and T.P. Levine. 2005. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6:209–220.CrossRefMedline↵ Jiménez, C.R., L. Huang, Y. Qiu, and A.L. Burlingame. 1998. Searching sequence databases over the Internet: protein identification using MS-Fit. In Current Protocols in Protein Science. J.E. Coligan, B.M. Dunn, H.L. Ploegh, D.W. Speicher, and P.T. Wigfield, editors. John Wiley and Sons, New York. 16.5.1–16.5.6.
Johnson, J.E., J. Giorgione, and A.C. Newton. 2000. The C1 and C2 domains of protein kinase C are independent membrane targeting modules, with specificity for phosphatidylserine conferred by the C1 domain. Biochemistry. 39:11360–11369.
Kooijman, E.E., V. Chupin, B. de Kruijff, and K.N.J. Burger. 2003. Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic. 4:162–174.
Lambkin, G.R., and R.A. Rachubinski. 2001. Yarrowia lipolytica cells mutant for the peroxisomal peroxin Pex19p contain structures resembling wild-type peroxisomes. Mol. Biol. Cell. 12:3353–3364.
McMahon, H.T., and J.L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 438:590–596.
Munro, S. 2003. Earthworms and lipid couriers. Nature. 426:775–776.
Newmyer, S.L., A. Christensen, and S. Sever. 2003. Auxilin-dynamin interactions link the uncoating ATPase chaperone machinery with vesicle formation. Dev. Cell. 4:929–940.
Olazabal, I.M., and L.M. Machesky. 2001. Abp1p and cortactin, new “hand-holds” for actin. J. Cell Biol. 154:679–682.
Osteryoung, K.W., and J. Nunnari. 2003. The division of endosymbiotic organelles. Science. 302:1698–1704.Abstract/FREE Full Text↵ Peters, C., T.L. Baars, S. Bühler, and A. Mayer. 2004. Mutual control of membrane fission and fusion proteins. Cell. 119:667–678.
Praefcke, G.J., and H.T. McMahon. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5:133–147.
Pruyne, D., and A. Bretscher. 2000. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113:365–375.
Rieder, S.E., and S.D. Emr. 2000. Isolation of subcellular fractions from the yeast Saccharomyces cerevisiae. In Current Protocols in Cell Biology. J.S. Bonifacino, M. Dasso, J.B. Harford, J. Lippincott-Schwartz, and K.M. Yamada, editors. John Wiley and Sons, New York. 3.8.1–3.8.68.
Schneiter, R., B. Brugger, R. Sandhoff, G. Zellnig, A. Leber, M. Lampl, K. Athenstaedt, C. Hrastnik, S. Eder, G. Daum, et al. 1999. Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J. Cell Biol. 146:741–754.
Schrader, M. 2006. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta. 1763:531–541.
Shemesh, T., A. Luini, V. Malhotra, K.N. Burger, and M.M. Kozlov. 2003. Prefission constriction of Golgi tubular carriers driven by local lipid metabolism: a theoretical model. Biophys. J. 85:3813–3827.
Shevchenko, A., O.N. Jensen, A.V. Podtelejnikov, F. Sagliocco, M. Wilm, O. Vorm, P. Mortensen, A. Shevchenko, H. Boucherie, and M. Mann. 1996. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. USA. 93:14440–14445.
Shorter, J., and G. Warren. 2002. Golgi architecture and inheritance. Annu. Rev. Cell Dev. Biol. 18:379–420.
Sillence, D.J., and F.M. Platt. 2004. Glycosphingolipids in endocytic membrane transport. Semin. Cell Dev. Biol. 15:409–416.
Sprong, H., P. van der Sluijs, and G. van Meer. 2001. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2:504–513.
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.
Thoms, S., and R. Erdmann. 2005. Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation. FEBS J. 272:5169–5181.
Titorenko, V.I., and R.T. Mullen. 2006. Peroxisome biogenesis: the peroxisomal endomembrane system and the role of the ER. J. Cell Biol. 174:11–17.
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.
van Meer, G., and H. Sprong. 2004. Membrane lipids and vesicular traffic. Curr. Opin. Cell Biol. 16:373–378.CrossRefMedline↵ Voelker, D.R. 2005. Bridging gaps in phospholipid transport. Trends Biochem. Sci. 30:396–404.
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.
Warren, D.T., P.D. Andrews, C.W. Gourlay, and K.R. Ayscough. 2002. Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics. J. Cell Sci. 115:1703–1715.
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.
Yan, M., N. Rayapuram, and S. Subramani. 2005. The control of peroxisome number and size during division and proliferation. Curr. Opin. Cell Biol. 17:376–383.
Youle, R.J., and M. Karbowski. 2005. Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6:657–663.Medline↵ Zimmerberg, J., and M.M. Kozlov. 2006. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:9–19.
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