UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes

Bikash Choudhary, Madhushree Kamak, Neena Ratnakaran, Jitendra Kumar, Anjali Awasthi, Chun Li, Ken C.Q. Nguyen, Kunihiro Matsumoto, Naoki Hisamoto, Sandhya P. Koushika

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

JIP3/UNC-16/dSYD is a MAPK-scaffolding protein with roles in protein trafficking. We show that it is present on the Golgi and is necessary for the polarized distribution of synaptic vesicle proteins (SVPs) and dendritic proteins in neurons. UNC-16 excludes Golgi enzymes from SVP transport carriers and facilitates inclusion of specific SVPs into the same transport carrier. The SVP trafficking roles of UNC-16 are mediated through LRK-1, whose localization to the Golgi is reduced in unc-16 animals. UNC-16, through LRK-1, also enables Golgi-localization of the μ-subunit of the AP-1 complex. AP1 regulates the size but not the composition of SVP transport carriers. Additionally, UNC-16 and LRK-1 through the AP-3 complex regulates the composition but not the size of the SVP transport carrier. These early biogenesis steps are essential for dependence on the synaptic vesicle motor, UNC-104 for axonal transport. Our results show that UNC-16 and its downstream effectors, LRK-1 and the AP complexes function at the Golgi and/or post-Golgi compartments to control early steps of SV biogenesis. The UNC-16 dependent steps of exclusion, inclusion and motor recruitment are critical for polarized distribution of neuronal cargo.

Original languageEnglish (US)
Article numbere1007100
JournalPLoS Genetics
Volume13
Issue number11
DOIs
StatePublished - Nov 1 2017

Fingerprint

trafficking
protein transport
Synaptic Vesicles
Transcription Factor AP-1
Protein Transport
vesicle
protein
Proteins
scaffolding proteins
Axonal Transport
proteins
synaptic vesicles
cargo
neurons
Neurons
enzyme
Enzymes
enzymes
animal

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Choudhary, B., Kamak, M., Ratnakaran, N., Kumar, J., Awasthi, A., Li, C., ... Koushika, S. P. (2017). UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes. PLoS Genetics, 13(11), [e1007100]. https://doi.org/10.1371/journal.pgen.1007100

UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes. / Choudhary, Bikash; Kamak, Madhushree; Ratnakaran, Neena; Kumar, Jitendra; Awasthi, Anjali; Li, Chun; Nguyen, Ken C.Q.; Matsumoto, Kunihiro; Hisamoto, Naoki; Koushika, Sandhya P.

In: PLoS Genetics, Vol. 13, No. 11, e1007100, 01.11.2017.

Research output: Contribution to journalArticle

Choudhary, B, Kamak, M, Ratnakaran, N, Kumar, J, Awasthi, A, Li, C, Nguyen, KCQ, Matsumoto, K, Hisamoto, N & Koushika, SP 2017, 'UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes', PLoS Genetics, vol. 13, no. 11, e1007100. https://doi.org/10.1371/journal.pgen.1007100
Choudhary, Bikash ; Kamak, Madhushree ; Ratnakaran, Neena ; Kumar, Jitendra ; Awasthi, Anjali ; Li, Chun ; Nguyen, Ken C.Q. ; Matsumoto, Kunihiro ; Hisamoto, Naoki ; Koushika, Sandhya P. / UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes. In: PLoS Genetics. 2017 ; Vol. 13, No. 11.
@article{67f39f7dd7aa4cce9fc549c0044e27e2,
title = "UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes",
abstract = "JIP3/UNC-16/dSYD is a MAPK-scaffolding protein with roles in protein trafficking. We show that it is present on the Golgi and is necessary for the polarized distribution of synaptic vesicle proteins (SVPs) and dendritic proteins in neurons. UNC-16 excludes Golgi enzymes from SVP transport carriers and facilitates inclusion of specific SVPs into the same transport carrier. The SVP trafficking roles of UNC-16 are mediated through LRK-1, whose localization to the Golgi is reduced in unc-16 animals. UNC-16, through LRK-1, also enables Golgi-localization of the μ-subunit of the AP-1 complex. AP1 regulates the size but not the composition of SVP transport carriers. Additionally, UNC-16 and LRK-1 through the AP-3 complex regulates the composition but not the size of the SVP transport carrier. These early biogenesis steps are essential for dependence on the synaptic vesicle motor, UNC-104 for axonal transport. Our results show that UNC-16 and its downstream effectors, LRK-1 and the AP complexes function at the Golgi and/or post-Golgi compartments to control early steps of SV biogenesis. The UNC-16 dependent steps of exclusion, inclusion and motor recruitment are critical for polarized distribution of neuronal cargo.",
author = "Bikash Choudhary and Madhushree Kamak and Neena Ratnakaran and Jitendra Kumar and Anjali Awasthi and Chun Li and Nguyen, {Ken C.Q.} and Kunihiro Matsumoto and Naoki Hisamoto and Koushika, {Sandhya P.}",
year = "2017",
month = "11",
day = "1",
doi = "10.1371/journal.pgen.1007100",
language = "English (US)",
volume = "13",
journal = "PLoS Genetics",
issn = "1553-7390",
publisher = "Public Library of Science",
number = "11",

}

TY - JOUR

T1 - UNC-16/JIP3 regulates early events in synaptic vesicle protein trafficking via LRK-1/LRRK2 and AP complexes

AU - Choudhary, Bikash

AU - Kamak, Madhushree

AU - Ratnakaran, Neena

AU - Kumar, Jitendra

AU - Awasthi, Anjali

AU - Li, Chun

AU - Nguyen, Ken C.Q.

AU - Matsumoto, Kunihiro

AU - Hisamoto, Naoki

AU - Koushika, Sandhya P.

PY - 2017/11/1

Y1 - 2017/11/1

N2 - JIP3/UNC-16/dSYD is a MAPK-scaffolding protein with roles in protein trafficking. We show that it is present on the Golgi and is necessary for the polarized distribution of synaptic vesicle proteins (SVPs) and dendritic proteins in neurons. UNC-16 excludes Golgi enzymes from SVP transport carriers and facilitates inclusion of specific SVPs into the same transport carrier. The SVP trafficking roles of UNC-16 are mediated through LRK-1, whose localization to the Golgi is reduced in unc-16 animals. UNC-16, through LRK-1, also enables Golgi-localization of the μ-subunit of the AP-1 complex. AP1 regulates the size but not the composition of SVP transport carriers. Additionally, UNC-16 and LRK-1 through the AP-3 complex regulates the composition but not the size of the SVP transport carrier. These early biogenesis steps are essential for dependence on the synaptic vesicle motor, UNC-104 for axonal transport. Our results show that UNC-16 and its downstream effectors, LRK-1 and the AP complexes function at the Golgi and/or post-Golgi compartments to control early steps of SV biogenesis. The UNC-16 dependent steps of exclusion, inclusion and motor recruitment are critical for polarized distribution of neuronal cargo.

AB - JIP3/UNC-16/dSYD is a MAPK-scaffolding protein with roles in protein trafficking. We show that it is present on the Golgi and is necessary for the polarized distribution of synaptic vesicle proteins (SVPs) and dendritic proteins in neurons. UNC-16 excludes Golgi enzymes from SVP transport carriers and facilitates inclusion of specific SVPs into the same transport carrier. The SVP trafficking roles of UNC-16 are mediated through LRK-1, whose localization to the Golgi is reduced in unc-16 animals. UNC-16, through LRK-1, also enables Golgi-localization of the μ-subunit of the AP-1 complex. AP1 regulates the size but not the composition of SVP transport carriers. Additionally, UNC-16 and LRK-1 through the AP-3 complex regulates the composition but not the size of the SVP transport carrier. These early biogenesis steps are essential for dependence on the synaptic vesicle motor, UNC-104 for axonal transport. Our results show that UNC-16 and its downstream effectors, LRK-1 and the AP complexes function at the Golgi and/or post-Golgi compartments to control early steps of SV biogenesis. The UNC-16 dependent steps of exclusion, inclusion and motor recruitment are critical for polarized distribution of neuronal cargo.

UR - http://www.scopus.com/inward/record.url?scp=85036635673&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85036635673&partnerID=8YFLogxK

U2 - 10.1371/journal.pgen.1007100

DO - 10.1371/journal.pgen.1007100

M3 - Article

VL - 13

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 11

M1 - e1007100

ER -