Abstract
Snf7p (sucrose non-fermenting) and Vps20p (vacuolar protein-sorting) are small coil-coiled proteins involved in yeast MVB (multivesicular body) structure, formation and function. In the present study, we report the identification of three human homologues of yeast Snf7p, designated hSnf7-1, hSnf7-2 and hSnf7-3, and a single human Vps20p homologue, designated hVps20, that may have similar roles in humans. Immunofluorescence studies showed that hSnf7-1 and hSnf7-3 localized in large vesicular structures that also co-localized with late endosomal/lysosomal structures induced by overexpressing an ATPase-defective Vps4-A mutant. In contrast, overexpressed hVps20 showed a typical endosomal membrane-staining pattern, and co-expression of hVps20 with Snf7-1 dispersed the large Snf7-staining vesicles. Interestingly, overexpression of both hSnf7 and hVps20 proteins induced a post-endosomal defect in cholesterol sorting. To explore possible protein-protein interactions involving hSnf7 proteins, we used information from yeast genomic studies showing that yeast Snf7p can interact with proteins involved in MVB function. Using a glutathione S-transferase-capture approach with several mammalian homologues of such yeast Snf7p-interacting proteins, we found that all three hSnf7s interacted with mouse AIP1 [ALG-2 (apoptosis-linked gene 2) interacting protein 1], a mammalian Bro1p [BCK1 (bypass of C kinase)-like resistance to osmotic shock]-containing protein involved in cellular vacuolization and apoptosis. Whereas mapping experiments showed that the N-terminus of AIP1 containing both a Bro1 and an alpha-helical domain were required for interaction with hSnf7-1, Snf7-1 did not interact with another human Bro1-containing molecule, rhophilin-2. Co-immunoprecipitation experiments confirmed the in vivo interaction of hSnf7-1 and AIP1. Additional immunofluorescence experiments showed that hSnf7-1 recruited cytosolic AIP1 to the Snf7-induced vacuolar-like structures. Together these results suggest that mammalian Vps20, AIP1 and Snf7 proteins, like their yeast counterparts, play roles in MVB function.
MeSH Terms
Amino Acid Sequence
Animals
COS Cells
Carrier Proteins/chemistry,metabolism,physiology
Cell Line
Cell Line, Tumor
Chlorocebus aethiops
Cholesterol/metabolism
Cloning, Molecular
Endosomal Sorting Complexes Required for Transport
Endosomes/chemistry
HeLa Cells/chemistry
Humans
Lysosomes/chemistry
Membrane Proteins/chemistry,metabolism,physiology
Molecular Sequence Data
Nuclear Proteins/chemistry,metabolism,physiology
Protein Interaction Mapping
Saccharomyces cerevisiae Proteins/chemistry,metabolism,physiology
Sequence Homology, Amino Acid
Transport Vesicles/chemistry
Vesicular Transport Proteins
Chemicals
CHMP4A protein, human
CHMP6 protein, human
Carrier Proteins
Endosomal Sorting Complexes Required for Transport
Membrane Proteins
Nuclear Proteins
SNF7 protein, S cerevisiae
Saccharomyces cerevisiae Proteins
Vesicular Transport Proteins
Cholesterol
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Peck Jeremy W
Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057, U.S.A.
Bowden Emma T
Burbelo Peter D
References (31)
31 references, click to expand
-
ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking.
Mol Biol Cell. 2000 Jan;11(1):227-39
PMID: 10637304
-
Alix, a novel mouse protein undergoing calcium-dependent interaction with the apoptosis-linked-gene 2 (ALG-2) protein.
Cell Death Differ. 1999 Feb;6(2):124-9
PMID: 10200558
-
The glioma-associated protein SETA interacts with AIP1/Alix and ALG-2 and modulates apoptosis in astrocytes.
J Biol Chem. 2000 Jun 23;275(25):19275-81
PMID: 10858458
-
SETA is a multifunctional adapter protein with three SH3 domains that binds Grb2, Cbl, and the novel SB1 proteins.
Cell Signal. 2000 Dec;12(11-12):769-79
PMID: 11152963
-
The phagosome proteome: insight into phagosome functions.
J Cell Biol. 2001 Jan 8;152(1):165-80
PMID: 11149929
-
A family of small coiled-coil-forming proteins functioning at the late endosome in yeast.
Mol Biol Cell. 2001 Mar;12(3):711-23
PMID: 11251082
-
A comprehensive two-hybrid analysis to explore the yeast protein interactome.
Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4569-74
PMID: 11283351
-
Molecular cloning of PalBH, a mammalian homologue of the Aspergillus atypical calpain PalB.
Biochim Biophys Acta. 2001 Jan 26;1517(2):316-9
PMID: 11342116
-
Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles.
J Immunol. 2001 Jun 15;166(12):7309-18
PMID: 11390481
-
CHMP1 functions as a member of a newly defined family of vesicle trafficking proteins.
J Cell Sci. 2001 Jul;114(Pt 13):2395-404
PMID: 11559748
-
Overexpression of Hp95 induces G1 phase arrest in confluent HeLa cells.
Differentiation. 2001 Jun;67(4-5):139-53
PMID: 11683497
-
Yeast PalA/AIP1/Alix homolog Rim20p associates with a PEST-like region and is required for its proteolytic cleavage.
J Bacteriol. 2001 Dec;183(23):6917-23
PMID: 11698381
-
Functional organization of the yeast proteome by systematic analysis of protein complexes.
Nature. 2002 Jan 10;415(6868):141-7
PMID: 11805826
-
Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization.
J Biol Chem. 2002 Aug 9;277(32):29108-15
PMID: 12034747
-
Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.
Dev Cell. 2002 Aug;3(2):271-82
PMID: 12194857
-
Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body.
Dev Cell. 2002 Aug;3(2):283-9
PMID: 12194858
-
The RhoA-binding protein, rhophilin-2, regulates actin cytoskeleton organization.
J Biol Chem. 2002 Nov 15;277(46):43924-32
PMID: 12221077
-
Receptor downregulation and multivesicular-body sorting.
Nat Rev Mol Cell Biol. 2002 Dec;3(12):893-905
PMID: 12461556
-
YPXL/I is a protein interaction motif recognized by aspergillus PalA and its human homologue, AIP1/Alix.
Mol Cell Biol. 2003 Mar;23(5):1647-55
PMID: 12588984
-
Bro1 is an endosome-associated protein that functions in the MVB pathway in Saccharomyces cerevisiae.
J Cell Sci. 2003 May 15;116(Pt 10):1893-903
PMID: 12668726
-
Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway.
Traffic. 2003 Apr;4(4):222-31
PMID: 12694561
-
The ALG-2-interacting protein Alix associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting.
J Biol Chem. 2003 Oct 3;278(40):39104-13
PMID: 12860994
-
Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants.
Mol Biol Cell. 1992 Dec;3(12):1389-402
PMID: 1493335
-
Molecular and genetic analysis of the SNF7 gene in Saccharomyces cerevisiae.
Genetics. 1993 Sep;135(1):17-23
PMID: 8224817
-
A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases.
J Biol Chem. 1995 Dec 8;270(49):29071-4
PMID: 7493928
-
Endocytosis and molecular sorting.
Annu Rev Cell Dev Biol. 1996;12:575-625
PMID: 8970738
-
Characterization of the pH signal transduction pathway gene palA of Aspergillus nidulans and identification of possible homologs.
J Bacteriol. 1997 Mar;179(5):1832-5
PMID: 9045850
-
The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function.
EMBO J. 1998 Jun 1;17(11):2982-93
PMID: 9606181
-
Cloning of AIP1, a novel protein that associates with the apoptosis-linked gene ALG-2 in a Ca2+-dependent reaction.
J Biol Chem. 1999 Jan 15;274(3):1533-40
PMID: 9880530
-
Identification and cloning of xp95, a putative signal transduction protein in Xenopus oocytes.
J Biol Chem. 1999 Feb 26;274(9):5522-31
PMID: 10026166
-
A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae.
Nature. 2000 Feb 10;403(6770):623-7
PMID: 10688190