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Vol. 11, Issue 2, 467-480, February 2000
and
*Structural Cell Biology Unit, Department of Medical Anatomy, The
Panum Institute, University of Copenhagen, DK-2200 Copenhagen, Denmark;
and The molecular machinery behind lysosome biogenesis and the
maintenance of the perinuclear aggregate of late endocytic structures is not well understood. A likely candidate for being part of this machinery is the small GTPase Rab7, but it is unclear whether this
protein is associated with lysosomes or plays any role in the
regulation of the perinuclear lysosome compartment. Previously, Rab7
has mainly been implicated in transport from early to late endosomes.
We have now used a new approach to analyze the role of Rab7: transient
expression of Enhanced Green Fluorescent Protein (EGFP)-tagged Rab7 wt
and mutant proteins in HeLa cells. EGFP-Rab7 wt was associated with
late endocytic structures, mainly lysosomes, which aggregated and fused
in the perinuclear region. The size of the individual lysosomes as well
as the degree of perinuclear aggregation increased with the expression
levels of EGFP-Rab7 wt and, more dramatically, the active EGFP-Rab7Q67L
mutant. In contrast, upon expression of the dominant-negative mutants
EGFP-Rab7T22N and EGFP-Rab7N125I, which localized mainly to the
cytosol, the perinuclear lysosome aggregate disappeared and lysosomes,
identified by colocalization of cathepsin D and lysosome-associated
membrane protein-1, became dispersed throughout the cytoplasm, they
were inaccessible to endocytosed molecules such as low-density
lipoprotein, and their acidity was strongly reduced, as
determined by decreased accumulation of the acidotropic probe
LysoTracker Red. In contrast, early endosomes associated with Rab5 and
the transferrin receptor, late endosomes enriched in the
cation-independent mannose 6-phosphate receptor, and the
trans-Golgi network, identified by its enrichment in
TGN-38, were unchanged. These data demonstrate for the first time that
Rab7, controlling aggregation and fusion of late endocytic structures/lysosomes, is essential for maintenance of the perinuclear lysosome compartment.
Dipartimento di Biologia e Patologia Cellulare e
Molecolare "L. Califano" and Centro di Endocrinologia ed Oncologia
Sperimentale "G. Salvatore" del Consiglio Nazionale delle
Richerche, Università of Napoli "Federico II," 80131 Napoli,
Italy
Online version of this article contains
video material. Online version available at www.molbiolcell.org.
These authors contributed equally to this work.
§
Corresponding author. E-mail address:
b.v.deurs{at}mai.ku.dk.
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C. Fiorini, B. Mograbi, L. Cronier, I. Bourget, X. Decrouy, M. Nebout, B. Ferrua, A. Malassine, M. Samson, P. Fenichel, et al. Dominant negative effect of connexin33 on gap junctional communication is mediated by connexin43 sequestration J. Cell Sci., September 15, 2004; 117(20): 4665 - 4672. [Abstract] [Full Text] [PDF]
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S. Jager, C. Bucci, I. Tanida, T. Ueno, E. Kominami, P. Saftig, and E.-L. Eskelinen Role for Rab7 in maturation of late autophagic vacuoles J. Cell Sci., September 15, 2004; 117(20): 4837 - 4848. [Abstract] [Full Text] [PDF]
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D. B. Scott, I. Michailidis, Y. Mu, D. Logothetis, and M. D. Ehlers Endocytosis and Degradative Sorting of NMDA Receptors by Conserved Membrane-Proximal Signals J. Neurosci., August 11, 2004; 24(32): 7096 - 7109. [Abstract] [Full Text] [PDF]
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R. E. Harrison, J. H. Brumell, A. Khandani, C. Bucci, C. C. Scott, X. Jiang, B. B. Finlay, and S. Grinstein Salmonella Impairs RILP Recruitment to Rab7 during Maturation of Invasion Vacuoles Mol. Biol. Cell, July 1, 2004; 15(7): 3146 - 3154. [Abstract] [Full Text] [PDF]
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J. J. Rose, J. F. Foley, P. M. Murphy, and S. Venkatesan On the Mechanism and Significance of Ligand-induced Internalization of Human Neutrophil Chemokine Receptors CXCR1 and CXCR2 J. Biol. Chem., June 4, 2004; 279(23): 24372 - 24386. [Abstract] [Full Text] [PDF]
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M. G. Gutierrez, D. B. Munafo, W. Beron, and M. I. Colombo Rab7 is required for the normal progression of the autophagic pathway in mammalian cells J. Cell Sci., June 1, 2004; 117(13): 2687 - 2697. [Abstract] [Full Text] [PDF]
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T. R. Jeffries, S. K. Dove, R. H. Michell, and P. J. Parker PtdIns-specific MPR Pathway Association of a Novel WD40 Repeat Protein, WIPI49 Mol. Biol. Cell, June 1, 2004; 15(6): 2652 - 2663. [Abstract] [Full Text] [PDF]
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M. Marsman, I. Jordens, C. Kuijl, L. Janssen, and J. Neefjes Dynein-mediated Vesicle Transport Controls Intracellular Salmonella Replication Mol. Biol. Cell, June 1, 2004; 15(6): 2954 - 2964. [Abstract] [Full Text] [PDF]
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J. Dong, W. Chen, A. Welford, and A. Wandinger-Ness The Proteasome {alpha}-Subunit XAPC7 Interacts Specifically with Rab7 and Late Endosomes J. Biol. Chem., May 14, 2004; 279(20): 21334 - 21342. [Abstract] [Full Text] [PDF]
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J. R. Junutula, A. M. De Maziere, A. A. Peden, K. E. Ervin, R. J. Advani, S. M. van Dijk, J. Klumperman, and R. H. Scheller Rab14 Is Involved in Membrane Trafficking between the Golgi Complex and Endosomes Mol. Biol. Cell, May 1, 2004; 15(5): 2218 - 2229. [Abstract] [Full Text] [PDF]
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Y. Li, A. Wandinger-Ness, J. R. Goldenring, and T. L. Cover Clustering and Redistribution of Late Endocytic Compartments in Response to Helicobacter pylori Vacuolating Toxin Mol. Biol. Cell, April 1, 2004; 15(4): 1946 - 1959. [Abstract] [Full Text] [PDF]
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L. B. Dale, J. L. Seachrist, A. V. Babwah, and S. S. G. Ferguson Regulation of Angiotensin II Type 1A Receptor Intracellular Retention, Degradation, and Recycling by Rab5, Rab7, and Rab11 GTPases J. Biol. Chem., March 26, 2004; 279(13): 13110 - 13118. [Abstract] [Full Text] [PDF]
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H. Rosen, V. Glukhman, T. Feldmann, E. Fridman, and D. Lichtstein Cardiac Steroids Induce Changes in Recycling of the Plasma Membrane in Human NT2 Cells Mol. Biol. Cell, March 1, 2004; 15(3): 1044 - 1054. [Abstract] [Full Text] [PDF]
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T. Wang, K. K. Wong, and W. Hong A Unique Region of RILP Distinguishes It from Its Related Proteins in Its Regulation of Lysosomal Morphology and Interaction with Rab7 and Rab34 Mol. Biol. Cell, February 1, 2004; 15(2): 815 - 826. [Abstract] [Full Text] [PDF]
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R. M. Henry, A. D. Hoppe, N. Joshi, and J. A. Swanson The uniformity of phagosome maturation in macrophages J. Cell Biol., January 19, 2004; 164(2): 185 - 194. [Abstract] [Full Text] [PDF]
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 A. Mazel, Y. Leshem, B. S. Tiwari, and A. Levine Induction of Salt and Osmotic Stress Tolerance by Overexpression of an Intracellular Vesicle Trafficking Protein AtRab7 (AtRabG3e) Plant Physiology, January 1, 2004; 134(1): 118 - 128. [Abstract] [Full Text] [PDF]
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 M. Y. Nahm, S. W. Kim, D. Yun, S. Y. Lee, M. J. Cho, and J. D. Bahk Molecular and Biochemical Analyses of OsRab7, a Rice Rab7 Homolog Plant Cell Physiol., December 15, 2003; 44(12): 1341 - 1349. [Abstract] [Full Text] [PDF]
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X. Chen, S. A. Ernst, and J. A. Williams Dominant Negative Rab3D Mutants Reduce GTP-bound Endogenous Rab3D in Pancreatic Acini J. Biol. Chem., December 12, 2003; 278(50): 50053 - 50060. [Abstract] [Full Text] [PDF]
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K. A. Rzomp, L. D. Scholtes, B. J. Briggs, G. R. Whittaker, and M. A. Scidmore Rab GTPases Are Recruited to Chlamydial Inclusions in Both a Species-Dependent and Species-Independent Manner Infect. Immun., October 1, 2003; 71(10): 5855 - 5870. [Abstract] [Full Text] [PDF]
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V. Poupon, A. Stewart, S. R. Gray, R. C. Piper, and J. P. Luzio The Role of mVps18p in Clustering, Fusion, and Intracellular Localization of Late Endocytic Organelles Mol. Biol. Cell, October 1, 2003; 14(10): 4015 - 4027. [Abstract] [Full Text] [PDF]
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R. E. Harrison, C. Bucci, O. V. Vieira, T. A. Schroer, and S. Grinstein Phagosomes Fuse with Late Endosomes and/or Lysosomes by Extension of Membrane Protrusions along Microtubules: Role of Rab7 and RILP Mol. Cell. Biol., September 15, 2003; 23(18): 6494 - 6506. [Abstract] [Full Text] [PDF]
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K. Mizuno, A. Kitamura, and T. Sasaki Rabring7, a Novel Rab7 Target Protein with a RING Finger Motif Mol. Biol. Cell, September 1, 2003; 14(9): 3741 - 3752. [Abstract] [Full Text] [PDF]
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 S.-N. Huang, M. A. Phelps, and P. W. Swaan Involvement of Endocytic Organelles in the Subcellular Trafficking and Localization of Riboflavin J. Pharmacol. Exp. Ther., August 1, 2003; 306(2): 681 - 687. [Abstract] [Full Text] [PDF]
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R. Nazarian, J. M. Falcon-Perez, and E. C. Dell'Angelica Biogenesis of lysosome-related organelles complex 3 (BLOC-3): A complex containing the Hermansky-Pudlak syndrome (HPS) proteins HPS1 and HPS4 PNAS, July 22, 2003; 100(15): 8770 - 8775. [Abstract] [Full Text] [PDF]
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A. Otomo, S. Hadano, T. Okada, H. Mizumura, R. Kunita, H. Nishijima, J. Showguchi-Miyata, Y. Yanagisawa, E. Kohiki, E. Suga, et al. ALS2, a novel guanine nucleotide exchange factor for the small GTPase Rab5, is implicated in endosomal dynamics Hum. Mol. Genet., July 15, 2003; 12(14): 1671 - 1687. [Abstract] [Full Text] [PDF]
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O. V. Vieira, C. Bucci, R. E. Harrison, W. S. Trimble, L. Lanzetti, J. Gruenberg, A. D. Schreiber, P. D. Stahl, and S. Grinstein Modulation of Rab5 and Rab7 Recruitment to Phagosomes by Phosphatidylinositol 3-Kinase Mol. Cell. Biol., April 1, 2003; 23(7): 2501 - 2514. [Abstract] [Full Text] [PDF]
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F. Ulloa and F. X. Real Benzyl-N-acetyl-alpha -D-galactosaminide Induces a Storage Disease-like Phenotype by Perturbing the Endocytic Pathway J. Biol. Chem., March 28, 2003; 278(14): 12374 - 12383. [Abstract] [Full Text] [PDF]
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G.-H. Fan, L. A. Lapierre, J. R. Goldenring, and A. Richmond Differential regulation of CXCR2 trafficking by Rab GTPases Blood, March 15, 2003; 101(6): 2115 - 2124. [Abstract] [Full Text] [PDF]
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S. Duclos, R. Corsini, and M. Desjardins Remodeling of endosomes during lysosome biogenesis involves `kiss and run' fusion events regulated by rab5 J. Cell Sci., March 1, 2003; 116(5): 907 - 918. [Abstract] [Full Text] [PDF]
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N. Naslavsky, R. Weigert, and J. G. Donaldson Convergence of Non-clathrin- and Clathrin-derived Endosomes Involves Arf6 Inactivation and Changes in Phosphoinositides Mol. Biol. Cell, February 1, 2003; 14(2): 417 - 431. [Abstract] [Full Text] [PDF]
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