Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 23 January 2004:
Vol. 303. no. 5657, pp. 531 - 534
DOI: 10.1126/science.1092425
Prev | Table of Contents | Next

Reports

Role of LBPA and Alix in Multivesicular Liposome Formation and Endosome Organization

Hirotami Matsuo,1* Julien Chevallier,1 Nathalie Mayran,1 Isabelle Le Blanc,1 Charles Ferguson,3 Julien Fauré,4 Nathalie Sartori Blanc,5 Stefan Matile,2 Jacques Dubochet,5 Rémy Sadoul,4 Robert G. Parton,3 Francis Vilbois,6 Jean Gruenberg1{dagger}

What are the components that control the assembly of subcellular organelles in eukaryotic cells? Although membranes can clearly be distorted by cytosolic factors, very little is known about the intrinsic mechanisms that control the biogenesis, shape, and organization of organellar membranes. Here, we found that the unconventional phospholipid lysobisphosphatidic acid (LBPA) could induce the formation of multivesicular liposomes that resembled the multivesicular endosomes that exist where this lipid is found in vivo. This process depended on the same pH gradient that exists across endosome membranes in vivo and was selectively controlled by Alix. In turn, Alix regulated the organization of LBPA-containing endosomes in vivo.

1 Department of Biochemistry, University of Geneva, 30 quai Ernest Ansermet, 1211 Geneva 4, Switzerland.
2 Department of Organic Chemistry, University of Geneva, 30 quai Ernest Ansermet, 1211 Geneva 4, Switzerland.
3 Institute for Molecular Bioscience, Center for Microscopy and Microanalysis and School of Biomedical Sciences, University of Queensland, Queensland 4072, Australia.
4 Neurodégénérescence et Plasticité Inserm–Université Joseph Fourier, Hôpital A. Michallon, 38043 Grenoble Cedex 9, France.
5 Laboratoire d'Analyse Ultrastructurale, University of Lausanne, 1015 Lausanne, Switzerland.
6 Serono Pharmaceutical Research Institute, 1228 Plan-les-Ouates, Switzerland.



* Present address: Department of Chemical Pharmacy, Shujitsu University, 1-6-1 Nishigawara, Okayama 703–8516, Japan.

{dagger} To whom correspondence should be addressed. E-mail: jean.gruenberg{at}biochem.unige.ch

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The role of negatively charged lipids in lysosomal phospholipase A2 function.
A. Abe and J. A. Shayman (2009)
J. Lipid Res. 50, 2027-2035
   Abstract »    Full Text »    PDF »
Divergent Bro1 Domains Share the Capacity To Bind Human Immunodeficiency Virus Type 1 Nucleocapsid and To Enhance Virus-Like Particle Production.
S. Popov, E. Popova, M. Inoue, and H. G. Gottlinger (2009)
J. Virol. 83, 7185-7193
   Abstract »    Full Text »    PDF »
ALCAT1 is a polyglycerophospholipid acyltransferase potently regulated by adenine nucleotide and thyroid status.
J. Cao, W. Shen, Z. Chang, and Y. Shi (2009)
Am J Physiol Endocrinol Metab 296, E647-E653
   Abstract »    Full Text »    PDF »
Selective decrease of bis(monoacylglycero)phosphate content in macrophages by high supplementation with docosahexaenoic acid.
J. Bouvier, K. A. Zemski Berry, F. Hullin-Matsuda, A. Makino, S. Michaud, A. Geloen, R. C. Murphy, T. Kobayashi, M. Lagarde, and I. Delton-Vandenbroucke (2009)
J. Lipid Res. 50, 243-255
   Abstract »    Full Text »    PDF »
MHC class II transport at a glance.
A. C. Berger and P. A. Roche (2009)
J. Cell Sci. 122, 1-4
   Full Text »    PDF »
Alix and ALG-2 Are Involved in Tumor Necrosis Factor Receptor 1-induced Cell Death.
A.-L. Mahul-Mellier, F. Strappazzon, A. Petiot, C. Chatellard-Causse, S. Torch, B. Blot, K. Freeman, L. Kuhn, J. Garin, J.-M. Verna, et al. (2008)
J. Biol. Chem. 283, 34954-34965
   Abstract »    Full Text »    PDF »
Annexin A8 Regulates Late Endosome Organization and Function.
V. Goebeler, M. Poeter, D. Zeuschner, V. Gerke, and U. Rescher (2008)
Mol. Biol. Cell 19, 5267-5278
   Abstract »    Full Text »    PDF »
In Vitro Budding of Intralumenal Vesicles into Late Endosomes Is Regulated by Alix and Tsg101.
T. Falguieres, P.-P. Luyet, C. Bissig, C. C. Scott, M.-C. Velluz, and J. Gruenberg (2008)
Mol. Biol. Cell 19, 4942-4955
   Abstract »    Full Text »    PDF »
Lysobisphosphatidic Acid Controls Endosomal Cholesterol Levels.
J. Chevallier, Z. Chamoun, G. Jiang, G. Prestwich, N. Sakai, S. Matile, R. G. Parton, and J. Gruenberg (2008)
J. Biol. Chem. 283, 27871-27880
   Abstract »    Full Text »    PDF »
Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes.
K. Trajkovic, C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brugger, and M. Simons (2008)
Science 319, 1244-1247
   Abstract »    Full Text »    PDF »
Plasma membrane deformation by circular arrays of ESCRT-III protein filaments.
P. I. Hanson, R. Roth, Y. Lin, and J. E. Heuser (2008)
J. Cell Biol. 180, 389-402
   Abstract »    Full Text »    PDF »
Late Endosomal Traffic of the Epidermal Growth Factor Receptor Ensures Spatial and Temporal Fidelity of Mitogen-activated Protein Kinase Signaling.
N. Taub, D. Teis, H. L. Ebner, M. W. Hess, and L. A. Huber (2007)
Mol. Biol. Cell 18, 4698-4710
   Abstract »    Full Text »    PDF »
Endocytic Trafficking of Sphingomyelin Depends on Its Acyl Chain Length.
M. Koivusalo, M. Jansen, P. Somerharju, and E. Ikonen (2007)
Mol. Biol. Cell 18, 5113-5123
   Abstract »    Full Text »    PDF »
Role of the V-ATPase in Regulation of the Vacuolar Fission Fusion Equilibrium.
T. L. Baars, S. Petri, C. Peters, and A. Mayer (2007)
Mol. Biol. Cell 18, 3873-3882
   Abstract »    Full Text »    PDF »
De novo biosynthesis of the late endosome lipid, bis(monoacylglycero)phosphate.
F. Hullin-Matsuda, K. Kawasaki, I. Delton-Vandenbroucke, Y. Xu, M. Nishijima, M. Lagarde, M. Schlame, and T. Kobayashi (2007)
J. Lipid Res. 48, 1997-2008
   Abstract »    Full Text »    PDF »
Split-Ubiquitin Two-Hybrid Assay To Analyze Protein-Protein Interactions at the Endosome: Application to Saccharomyces cerevisiae Bro1 Interacting with ESCRT Complexes, the Doa4 Ubiquitin Hydrolase, and the Rsp5 Ubiquitin Ligase.
E. Nikko and B. Andre (2007)
Eukaryot. Cell 6, 1266-1277
   Abstract »    Full Text »    PDF »
The Clathrin Adaptor Complex AP-1 Binds HIV-1 and MLV Gag and Facilitates Their Budding.
G. Camus, C. Segura-Morales, D. Molle, S. Lopez-Verges, C. Begon-Pescia, C. Cazevieille, P. Schu, E. Bertrand, C. Berlioz-Torrent, and E. Basyuk (2007)
Mol. Biol. Cell 18, 3193-3203
   Abstract »    Full Text »    PDF »
Essential Role of Ubiquitin-Specific Protease 8 for Receptor Tyrosine Kinase Stability and Endocytic Trafficking In Vivo.
S. Niendorf, A. Oksche, A. Kisser, J. Lohler, M. Prinz, H. Schorle, S. Feller, M. Lewitzky, I. Horak, and K.-P. Knobeloch (2007)
Mol. Cell. Biol. 27, 5029-5039
   Abstract »    Full Text »    PDF »
The Vaccinia Virus F13L YPPL Motif Is Required for Efficient Release of Extracellular Enveloped Virus.
K. M. Honeychurch, G. Yang, R. Jordan, and D. E. Hruby (2007)
J. Virol. 81, 7310-7315
   Abstract »    Full Text »    PDF »
Potent Rescue of Human Immunodeficiency Virus Type 1 Late Domain Mutants by ALIX/AIP1 Depends on Its CHMP4 Binding Site.
Y. Usami, S. Popov, and H. G. Gottlinger (2007)
J. Virol. 81, 6614-6622
   Abstract »    Full Text »    PDF »
Involvement of host cellular multivesicular body functions in hepatitis B virus budding.
T. Watanabe, E. M. Sorensen, A. Naito, M. Schott, S. Kim, and P. Ahlquist (2007)
PNAS 104, 10205-10210
   Abstract »    Full Text »    PDF »
A Genetic Screen for Mycobacterium tuberculosis Mutants Defective for Phagosome Maturation Arrest Identifies Components of the ESX-1 Secretion System.
J. A. MacGurn and J. S. Cox (2007)
Infect. Immun. 75, 2668-2678
   Abstract »    Full Text »    PDF »
Alix (AIP1) is a vasopressin receptor (V2R)-interacting protein that increases lysosomal degradation of the V2R.
X. Yi, R. Bouley, H. Y. Lin, S. Bechoua, T.-x. Sun, E. del Re, T. Shioda, M. K. Raychowdhury, H. A. J. Lu, A. B. Abou-Samra, et al. (2007)
Am J Physiol Renal Physiol 292, F1303-F1313
   Abstract »    Full Text »    PDF »
Anti-bis(monoacylglycero)phosphate antibody accumulates acetylated LDL-derived cholesterol in cultured macrophages.
I. Delton-Vandenbroucke, J. Bouvier, A. Makino, N. Besson, J.-F. Pageaux, M. Lagarde, and T. Kobayashi (2007)
J. Lipid Res. 48, 543-552
   Abstract »    Full Text »    PDF »
The YLDL Sequence within Sendai Virus M Protein Is Critical for Budding of Virus-Like Particles and Interacts with Alix/AIP1 Independently of C Protein.
T. Irie, Y. Shimazu, T. Yoshida, and T. Sakaguchi (2007)
J. Virol. 81, 2263-2273
   Abstract »    Full Text »    PDF »
Alix Facilitates the Interaction between c-Cbl and Platelet-derived Growth Factor beta-Receptor and Thereby Modulates Receptor Down-regulation.
J. Lennartsson, P. Wardega, U. Engstrom, U. Hellman, and C.-H. Heldin (2006)
J. Biol. Chem. 281, 39152-39158
   Abstract »    Full Text »    PDF »
Involvement of the Conserved Adaptor Protein Alix in Actin Cytoskeleton Assembly.
S. Pan, R. Wang, X. Zhou, G. He, J. Koomen, R. Kobayashi, L. Sun, J. Corvera, G. E. Gallick, and J. Kuang (2006)
J. Biol. Chem. 281, 34640-34650
   Abstract »    Full Text »    PDF »
The Ca2+-binding Protein ALG-2 Is Recruited to Endoplasmic Reticulum Exit Sites by Sec31A and Stabilizes the Localization of Sec31A.
A. Yamasaki, K. Tani, A. Yamamoto, N. Kitamura, and M. Komada (2006)
Mol. Biol. Cell 17, 4876-4887
   Abstract »    Full Text »    PDF »
The multiple personalities of Alix..
G. Odorizzi (2006)
J. Cell Sci. 119, 3025-3032
   Abstract »    Full Text »    PDF »
Localized PtdIns 3,5-P2 synthesis to regulate early endosome dynamics and fusion.
O. C. Ikonomov, D. Sbrissa, and A. Shisheva (2006)
Am J Physiol Cell Physiol 291, C393-C404
   Abstract »    Full Text »    PDF »
Beta-amyloid accumulation impairs multivesicular body sorting by inhibiting the ubiquitin-proteasome system..
C. G. Almeida, R. H. Takahashi, and G. K. Gouras (2006)
J. Neurosci. 26, 4277-4288
   Abstract »    Full Text »    PDF »
Control of Bro1-Domain Protein Rim20 Localization by External pH, ESCRT Machinery, and the Saccharomyces cerevisiae Rim101 Pathway.
J. H. Boysen and A. P. Mitchell (2006)
Mol. Biol. Cell 17, 1344-1353
   Abstract »    Full Text »    PDF »
Degradation of Endocytosed Epidermal Growth Factor and Virally Ubiquitinated Major Histocompatibility Complex Class I Is Independent of Mammalian ESCRTII.
K. Bowers, S. C. Piper, M. A. Edeling, S. R. Gray, D. J. Owen, P. J. Lehner, and J. P. Luzio (2006)
J. Biol. Chem. 281, 5094-5105
   Abstract »    Full Text »    PDF »
The HIV lipidome: A raft with an unusual composition.
B. Brugger, B. Glass, P. Haberkant, I. Leibrecht, F. T. Wieland, and H.-G. Krausslich (2006)
PNAS 103, 2641-2646
   Abstract »    Full Text »    PDF »
Alix, Making a Link between Apoptosis-Linked Gene-2, the Endosomal Sorting Complexes Required for Transport, and Neuronal Death In Vivo.
A.-L. Mahul-Mellier, F. J. Hemming, B. Blot, S. Fraboulet, and R. Sadoul (2006)
J. Neurosci. 26, 542-549
   Abstract »    Full Text »    PDF »
LIN-12/Notch trafficking and regulation of DSL ligand activity during vulval induction in Caenorhabditis elegans.
D. D. Shaye and I. Greenwald (2005)
Development 132, 5081-5092
   Abstract »    Full Text »    PDF »
Constitutive Activation of the pH-Responsive Rim101 Pathway in Yeast Mutants Defective in Late Steps of the MVB/ESCRT Pathway.
M. Hayashi, T. Fukuzawa, H. Sorimachi, and T. Maeda (2005)
Mol. Cell. Biol. 25, 9478-9490
   Abstract »    Full Text »    PDF »
The Secreted Form of Dengue Virus Nonstructural Protein NS1 Is Endocytosed by Hepatocytes and Accumulates in Late Endosomes: Implications for Viral Infectivity.
S. Alcon-LePoder, M.-T. Drouet, P. Roux, M.-P. Frenkiel, M. Arborio, A.-M. Durand-Schneider, M. Maurice, I. Le Blanc, J. Gruenberg, and M. Flamand (2005)
J. Virol. 79, 11403-11411
   Abstract »    Full Text »    PDF »
AIP1/Alix Is a Binding Partner of Sendai Virus C Protein and Facilitates Virus Budding.
T. Sakaguchi, A. Kato, F. Sugahara, Y. Shimazu, M. Inoue, K. Kiyotani, Y. Nagai, and T. Yoshida (2005)
J. Virol. 79, 8933-8941
   Abstract »    Full Text »    PDF »
Alix regulates cortical actin and the spatial distribution of endosomes.
A. Cabezas, K. G. Bache, A. Brech, and H. Stenmark (2005)
J. Cell Sci. 118, 2625-2635
   Abstract »    Full Text »    PDF »
A Mutation in dVps28 Reveals a Link between a Subunit of the Endosomal Sorting Complex Required for Transport-I Complex and the Actin Cytoskeleton in Drosophila.
E. A. Sevrioukov, N. Moghrabi, M. Kuhn, and H. Kramer (2005)
Mol. Biol. Cell 16, 2301-2312
   Abstract »    Full Text »    PDF »
Interaction of the Mammalian Endosomal Sorting Complex Required for Transport (ESCRT) III Protein hSnf7-1 with Itself, Membranes, and the AAA+ ATPase SKD1.
Y. Lin, L. A. Kimpler, T. V. Naismith, J. M. Lauer, and P. I. Hanson (2005)
J. Biol. Chem. 280, 12799-12809
   Abstract »    Full Text »    PDF »
The Role of LIP5 and CHMP5 in Multivesicular Body Formation and HIV-1 Budding in Mammalian Cells.
D. M. Ward, M. B. Vaughn, S. L. Shiflett, P. L. White, A. L. Pollock, J. Hill, R. Schnegelberger, W. I. Sundquist, and J. Kaplan (2005)
J. Biol. Chem. 280, 10548-10555
   Abstract »    Full Text »    PDF »
From The Cover: Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes.
K. Bacia, P. Schwille, and T. Kurzchalia (2005)
PNAS 102, 3272-3277
   Abstract »    Full Text »    PDF »
Src Phosphorylation of Alix/AIP1 Modulates Its Interaction with Binding Partners and Antagonizes Its Activities.
M. H. H. Schmidt, I. Dikic, and O. Bogler (2005)
J. Biol. Chem. 280, 3414-3425
   Abstract »    Full Text »    PDF »
Identification and Characterization of a Gene Encoding Human LPGAT1, an Endoplasmic Reticulum-associated Lysophosphatidylglycerol Acyltransferase.
Y. Yang, J. Cao, and Y. Shi (2004)
J. Biol. Chem. 279, 55866-55874
   Abstract »    Full Text »    PDF »
Multivesicular Body-ESCRT Components Function in pH Response Regulation in Saccharomyces cerevisiae and Candida albicans.
W. Xu, F. J. Smith Jr., R. Subaran, and A. P. Mitchell (2004)
Mol. Biol. Cell 15, 5528-5537
   Abstract »    Full Text »    PDF »
Rab9 GTPase Regulates Late Endosome Size and Requires Effector Interaction for Its Stability.
I. G. Ganley, K. Carroll, L. Bittova, and S. Pfeffer (2004)
Mol. Biol. Cell 15, 5420-5430
   Abstract »    Full Text »    PDF »
Alix/AIP1 Antagonizes Epidermal Growth Factor Receptor Downregulation by the Cbl-SETA/CIN85 Complex.
M. H. H. Schmidt, D. Hoeller, J. Yu, F. B. Furnari, W. K. Cavenee, I. Dikic, and O. Bogler (2004)
Mol. Cell. Biol. 24, 8981-8993
   Abstract »    Full Text »    PDF »
Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes.
N. Luhtala and G. Odorizzi (2004)
J. Cell Biol. 166, 717-729
   Abstract »    Full Text »    PDF »
Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway.
L. Abrami, M. Lindsay, R. G. Parton, S. H. Leppla, and F. G. van der Goot (2004)
J. Cell Biol. 166, 645-651
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)