Molecular characterization of Rab11-FIP3 binding to ARF GTPases

Schonteich, Eric; Pilli, Manohar; Simon, Glenn C.; Matern, Hugo; Junutula, Jagath R.; Sentz, Danielle; Holmes, Randall K.; Prekeris, Rytis

doi:10.1016/j.ejcb.2007.05.004

Cited by 49 publications

(56 citation statements)

References 49 publications

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“…Arf5 bound to two constructs (FIP3C and FIP3C.565) strongly and two constructs (FIP3C.End695 and FIP3C. End651) weakly, consistent with the binding site for Arf5 in the C-terminal half of coiled-coil region of FIP3 as previously reported (Shiba et al, 2006;Schonteich et al, 2007). In contrast, the ASAP1 recombinant protein interacted with four constructs (FIP3C to FIP3C.565) to a similar extent, but much less with two constructs (FIP3C.650 and FIP3C.680) comprised of the C-terminus, supporting the conclusion that ASAP1 binds to the coiled-coil region.…”

Section: Identification and Characterization Of Fip3 As An Asap1-intesupporting

confidence: 60%

“…FIP3 is comprised of an N-terminal Pro-rich domain, two EF-hand motifs and, in the C-terminal half of the molecule, a coiled-coil domain. Rab11 and Arf5/6 bind to C-terminal end and C-terminal half of the coiled-coil domain, respectively (Prekeris et al, 2001;Shiba et al, 2006;Schonteich et al, 2007). The domain also mediates homodimerization and heterodimer formation with other FIPs, which also contain coiled-coil domain in their C-terminal region (Wallace et al, 2002;Eathiraj et al, 2006;Shiba et al, 2006;Horgan et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

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Arf GTPase-activating Protein ASAP1 Interacts with Rab11 Effector FIP3 and Regulates Pericentrosomal Localization of Transferrin Receptor–positive Recycling Endosome

Inoue

Prekeris

et al. 2008

MBoC

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ADP-ribosylation factors (Arfs) and Arf GTPase-activating proteins (GAPs) are key regulators of membrane trafficking and the actin cytoskeleton. The Arf GAP ASAP1 contains an N-terminal BAR domain, which can induce membrane tubulation. Here, we report that the BAR domain of ASAP1 can also function as a protein binding site. Two-hybrid screening identified FIP3, which is a putative Arf6-and Rab11-effector, as a candidate ASAP1 BAR domain-binding protein. Both coimmunoprecipitation and in vitro pulldown assays confirmed that ASAP1 directly binds to FIP3 through its BAR domain. ASAP1 formed a ternary complex with Rab11 through FIP3. FIP3 binding to the BAR domain stimulated ASAP1 GAP activity against Arf1, but not Arf6. ASAP1 colocalized with FIP3 in the pericentrosomal endocytic recycling compartment. Depletion of ASAP1 or FIP3 by small interfering RNA changed the localization of transferrin receptor, which is a marker of the recycling endosome, in HeLa cells. The depletion also altered the trafficking of endocytosed transferrin. These results support the conclusion that ASAP1, like FIP3, functions as a component of the endocytic recycling compartment. INTRODUCTIONArf family GTP-binding proteins and their GTPase-activating proteins (Arf GAPs) play crucial roles for membrane traffic and actin remodeling (D'Souza-Schorey and Chavrier, 2006;Gillingham and Munro, 2007). Arf GAPs share the same catalytic domain, the Arf GAP domain, which is responsible for GTP hydrolysis. In humans, 31 genes encoding proteins with Arf GAP domains have been found. They are classified into several subfamilies based on their domain structures Inoue and Randazzo, 2007). Three subfamilies, ArfGAPs, SMAPs, and GITs, have an Arf GAP domain at the N-terminus of the molecules. In contrast, the others, which are called AZAP-family Arf GAPs, contain an Arf GAP domain following a pleckstrin homology (PH) domain in the middle of the protein. They are subdivided into four subfamilies, ASAPs, ACAPs, ARAPs, and AGAPs.ASAP1 is one of the best-characterized Arf GAPs. In addition to PH and Arf GAP domains, ASAP1 contains an N-terminal Bin, Amphiphysin, and Rvs167/Rvs161 (BAR) domain and, in the C-terminal half of the protein, a proline (Pro)-rich domain and Src homology 3 (SH3) domain. Other ASAP isoforms, ASAP2 and ASAP3, have similar domain structures and high homology, especially in the Arf GAP domains, although ASAP3 lacks C-terminal SH3 domain (Ha et al., 2008). Through its Pro-rich and SH3 domains, ASAP1 interacts with a number of proteins, which are mainly adhesion-and actin cytoskeleton-related proteins including Src, focal adhesion kinase (FAK), Crk/CrkL, and cortactin (Brown et al., 1998;Liu et al., 2002;Oda et al., 2003;Onodera et al., 2005;Bharti et al., 2007). ASAP1 is a component of three integrated membrane/actin cytoskeleton structures: focal adhesions, circular dorsal ruffles (CDRs) and invadopodia/podosomes. ASAP1 associates with focal adhesions in fibroblasts . The focal adhesion localization depends on the interaction of ASAP1 with FA...

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Section: Identification and Characterization Of Fip3 As An Asap1-intesupporting

confidence: 60%

Section: Discussionmentioning

confidence: 99%

Arf GTPase-activating Protein ASAP1 Interacts with Rab11 Effector FIP3 and Regulates Pericentrosomal Localization of Transferrin Receptor–positive Recycling Endosome

Inoue

Prekeris

et al. 2008

MBoC

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“…The roles of FIP3 and FIP4 (Rab11 family-interacting protein 3 and 4), which are dual effectors of Rab11 and Arf6 and associate with recycling endosomes in interphase cells, are the subject of debate. One previous study suggested that Arf6 is recruited to the Flemming body independently of Rab11-and FIP3-containing endosomes (Fielding et al, 2005), whereas other studies have proposed that Arf6 requires an interaction with Rab11-and FIP3-positive endosomes to be targeted to the cleavage furrow (Schonteich et al, 2007;Montagnac et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Structural basis for Arf6-MKLP1 complex formation on the Flemming body responsible for cytokinesis

et al. 2012

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A small GTPase, Arf6, is involved in cytokinesis by localizing to the Flemming body (the midbody). However, it remains unknown how Arf6 contributes to cytokinesis. Here, we demonstrate that Arf6 directly interacts with mitotic kinesin-like protein 1 (MKLP1), a Flemming body-localizing protein essential for cytokinesis. The crystal structure of the Arf6-MKLP1 complex reveals that MKLP1 forms a homodimer flanked by two Arf6 molecules, forming a 2:2 heterotetramer containing an extended b-sheet composed of 22 b-strands that spans the entire heterotetramer, suitable for interaction with a concave membrane surface at the cleavage furrow. We show that, during cytokinesis, Arf6 is first accumulated around the cleavage furrow and, prior to abscission, recruited onto the Flemming body via interaction with MKLP1. We also show by structure-based mutagenesis and siRNAmediated knockdowns that the complex formation is required for completion of cytokinesis. A model based on these results suggests that the Arf6-MKLP1 complex plays a crucial role in cytokinesis by connecting the microtubule bundle and membranes at the cleavage plane.

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“…Cyk4 is a subunit of the Centralspindlin complex that is localized at the midbody during cytokinesis (Glotzer, 2005). In addition, FIP3 also was shown to bind Arf6 GTPase, an endocytic protein that is known to be required for cytokinesis Schonteich et al, 2007). Interestingly, Arf6 also binds the Sec10 subunit of the exocyst complex (Prigent et al, 2003).…”

Section: Rab11-endosomesmentioning

confidence: 99%