The Arabidopsis Endosomal Sorting Complex Required for Transport III Regulates Internal Vesicle Formation of the Prevacuolar Compartment and Is Required for Plant Development

Yi Cai; Xiaohong Zhuang; Caiji Gao; Xiangfeng Wang; Liwen Jiang

doi:10.1104/pp.114.238378

Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development

PLANT PHYSIOLOGY ◽

10.1104/pp.16.00240 ◽

2016 ◽

Vol 171 (1) ◽

pp. 251-264 ◽

Cited By ~ 24

Author(s):

Rafael Andrade Buono ◽

Julio Paez-Valencia ◽

Nathan D. Miller ◽

Kaija Goodman ◽

Christoph Spitzer ◽

...

Keyword(s):

Plant Development ◽

Endosomal Sorting

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Bro1 stimulates Vps4 to promote intralumenal vesicle formation during multivesicular body biogenesis

The Journal of Cell Biology ◽

10.1083/jcb.202102070 ◽

2021 ◽

Vol 220 (8) ◽

Author(s):

Chun-Che Tseng ◽

Shirley Dean ◽

Brian A. Davies ◽

Ishara F. Azmi ◽

Natalya Pashkova ◽

...

Keyword(s):

Multivesicular Body ◽

Vesicle Formation ◽

Multivesicular Bodies ◽

Membrane Remodeling ◽

Endosomal Sorting ◽

Aaa Atpase ◽

Ubiquitin Binding ◽

Stimulation Of ◽

Cargo Sorting

Endosomal sorting complexes required for transport (ESCRT-0, -I, -II, -III) execute cargo sorting and intralumenal vesicle (ILV) formation during conversion of endosomes to multivesicular bodies (MVBs). The AAA-ATPase Vps4 regulates the ESCRT-III polymer to facilitate membrane remodeling and ILV scission during MVB biogenesis. Here, we show that the conserved V domain of ESCRT-associated protein Bro1 (the yeast homologue of mammalian proteins ALIX and HD-PTP) directly stimulates Vps4. This activity is required for MVB cargo sorting. Furthermore, the Bro1 V domain alone supports Vps4/ESCRT–driven ILV formation in vivo without efficient MVB cargo sorting. These results reveal a novel activity of the V domains of Bro1 homologues in licensing ESCRT-III–dependent ILV formation and suggest a role in coordinating cargo sorting with membrane remodeling during MVB sorting. Moreover, ubiquitin binding enhances V domain stimulation of Vps4 to promote ILV formation via the Bro1–Vps4–ESCRT-III axis, uncovering a novel role for ubiquitin during MVB biogenesis in addition to facilitating cargo recognition.

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The Ubiquitin Ligase Itch and Ubiquitination Regulate BFRF1-Mediated Nuclear Envelope Modification for Epstein-Barr Virus Maturation

Journal of Virology ◽

10.1128/jvi.01235-16 ◽

2016 ◽

Vol 90 (20) ◽

pp. 8994-9007 ◽

Cited By ~ 21

Author(s):

Chung-Pei Lee ◽

Guan-Ting Liu ◽

Hsiu-Ni Kung ◽

Po-Ting Liu ◽

Yen-Tzu Liao ◽

...

Keyword(s):

Nuclear Envelope ◽

Ubiquitin Ligase ◽

Epstein Barr Virus ◽

Regulatory Mechanisms ◽

Vesicle Formation ◽

Endosomal Sorting ◽

Virus Maturation ◽

Barr Virus ◽

Nuclear Egress ◽

Epstein Barr

ABSTRACTThe cellular endosomal sorting complex required for transport (ESCRT) was recently found to mediate important morphogenesis processes at the nuclear envelope (NE). We previously showed that the Epstein-Barr virus (EBV) BFRF1 protein recruits the ESCRT-associated protein Alix to modulate NE structure and promote EBV nuclear egress. Here, we uncover new cellular factors and mechanisms involved in this process. BFRF1-induced NE vesicles are similar to those observed following EBV reactivation. BFRF1 is ubiquitinated, and elimination of possible ubiquitination by either lysine mutations or fusion of a deubiquitinase hampers NE-derived vesicle formation and virus maturation. While it interacts with multiple Nedd4-like ubiquitin ligases, BFRF1 preferentially binds Itch ligase. We show that Itch associates with Alix and BFRF1 and is required for BFRF1-induced NE vesicle formation. Our data demonstrate that Itch, ubiquitin, and Alix control the BFRF1-mediated modulation of the NE and EBV maturation, uncovering novel regulatory mechanisms of nuclear egress of viral nucleocapsids.IMPORTANCEThe nuclear envelope (NE) of eukaryotic cells not only serves as a transverse scaffold for cellular processes, but also as a natural barrier for most DNA viruses that assemble their nucleocapsids in the nucleus. Previously, we showed that the cellular endosomal sorting complex required for transport (ESCRT) machinery is required for the nuclear egress of EBV. Here, we further report the molecular interplay among viral BFRF1, the ESCRT adaptor Alix, and the ubiquitin ligase Itch. We found that BFRF1-induced NE vesicles are similar to those observed following EBV reactivation. The lysine residues and the ubiquitination of BFRF1 regulate the formation of BFRF1-induced NE-derived vesicles and EBV maturation. During the process, a ubiquitin ligase, Itch, preferably associates with BFRF1 and is required for BFRF1-induced NE vesicle formation. Therefore, our data indicate that Itch, ubiquitin, and Alix control the BFRF1-mediated modulation of the NE, suggesting novel regulatory mechanisms for ESCRT-mediated NE modulation.

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Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation

The Journal of Cell Biology ◽

10.1083/jcb.201310114 ◽

2014 ◽

Vol 205 (1) ◽

pp. 33-49 ◽

Cited By ~ 99

Author(s):

Manuel Alonso Y Adell ◽

Georg F. Vogel ◽

Mehrshad Pakdel ◽

Martin Müller ◽

Herbert Lindner ◽

...

Keyword(s):

Membrane Proteins ◽

Adenosine Triphosphatase ◽

Electron Tomography ◽

Vesicle Formation ◽

Multivesicular Bodies ◽

Membrane Remodeling ◽

Yeast Genetics ◽

Endosomal Sorting ◽

Distinct Membrane

Five endosomal sorting complexes required for transport (ESCRTs) mediate the degradation of ubiquitinated membrane proteins via multivesicular bodies (MVBs) in lysosomes. ESCRT-0, -I, and –II interact with cargo on endosomes. ESCRT-II also initiates the assembly of a ringlike ESCRT-III filament consisting of Vps20, Snf7, Vps24, and Vps2. The AAA–adenosine triphosphatase Vps4 disassembles and recycles the ESCRT-III complex, thereby terminating the ESCRT pathway. A mechanistic role for Vps4 in intraluminal vesicle (ILV) formation has been unclear. By combining yeast genetics, biochemistry, and electron tomography, we find that ESCRT-III assembly on endosomes is required to induce or stabilize the necks of growing MVB ILVs. Yet, ESCRT-III alone is not sufficient to complete ILV biogenesis. Rather, binding of Vps4 to ESCRT-III, coordinated by interactions with Vps2 and Snf7, is coupled to membrane neck constriction during ILV formation. Thus, Vps4 not only recycles ESCRT-III subunits but also cooperates with ESCRT-III to drive distinct membrane-remodeling steps, which lead to efficient membrane scission at the end of ILV biogenesis in vivo.

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Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes

The Journal of Cell Biology ◽

10.1083/jcb.200606113 ◽

2006 ◽

Vol 175 (5) ◽

pp. 715-720 ◽

Cited By ~ 104

Author(s):

Daniel P. Nickerson ◽

Matthew West ◽

Greg Odorizzi

Keyword(s):

Vesicle Formation ◽

Multivesicular Bodies ◽

Vesicle Budding ◽

Endosomal Sorting ◽

Essential Step ◽

Adenosine Triphosphatases ◽

Cargo Proteins ◽

Endosomal Membranes ◽

Cargo Sorting

The sorting of transmembrane cargo proteins into the lumenal vesicles of multivesicular bodies (MVBs) depends on the recruitment of endosomal sorting complexes required for transport (ESCRTs) to the cytosolic face of endosomal membranes. The subsequent dissociation of ESCRT complexes from endosomes requires Vps4, a member of the AAA family of adenosine triphosphatases. We show that Did2 directs Vps4 activity to the dissociation of ESCRT-III but has no role in the dissociation of ESCRT-I or -II. Surprisingly, vesicle budding into the endosome lumen occurs in the absence of Did2 function even though Did2 is required for the efficient sorting of MVB cargo proteins into lumenal vesicles. This uncoupling of MVB cargo sorting and lumenal vesicle formation suggests that the Vps4-mediated dissociation of ESCRT-III is an essential step in the sorting of cargo proteins into MVB vesicles but is not a prerequisite for the budding of vesicles into the endosome lumen.

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Bro1 directly stimulates Vps4 activity to promote Intralumenal Vesicle Formation during Multivesicular Body biogenesis

10.1101/2020.07.27.223255 ◽

2020 ◽

Author(s):

Chun-che Tseng ◽

Shirley Dean ◽

Brian A. Davies ◽

Ishara F. Azmi ◽

Natalya Pashkova ◽

...

Keyword(s):

Multivesicular Body ◽

Vesicle Formation ◽

Multivesicular Bodies ◽

Membrane Remodeling ◽

Endosomal Sorting ◽

Aaa Atpase ◽

Evolutionarily Conserved ◽

Carboxyl Terminal ◽

Yeast Homolog ◽

Direct Regulation

AbstractEndosomal sorting complexes required for transport (ESCRT-0, -I, -II, -III) form intralumenal vesicles (ILVs) during the conversion of endosomes to multivesicular bodies (MVBs). The assembly and disassembly of an ESCRT-III polymer facilitates membrane remodeling and scission during this process. The ESCRT-III-associated protein Bro1 (the yeast homolog of mammalian proteins ALIX and HD-PTP) promotes ESCRT-III assembly and inhibits disassembly of ESCRT-III filaments by impeding Vps4, a AAA-ATPase that dismantles ESCRT-III polymers. Here we show that the evolutionarily conserved “V domain” of Bro1-family proteins directly stimulate Vps4 ATPase activity and this activity is enhanced by interaction with ubiquitin. Surprisingly, a carboxyl-terminal fragment of Bro1 containing the V domain supports ILV formation but not sorting of cargo into ILVs, revealing that these two processes can be uncoupled. These studies implicate Bro1 as a factor coordinating cargo sorting with direct regulation of Vps4 to modulate ESCRT-III driven ILV formation during MVB biogenesis.

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