Positioning of endoplasmic reticulum exit sites around the Golgi depends on BicaudalD2 and Rab6 activity

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Positioning of endoplasmic reticulum exit sites around the Golgi depends on BicaudalD2 and Rab6 activity. / Shomron, Olga; Hirschberg, Koret; Burakov, Anton; Kamentseva, Rimma; Kornilova, Elena; Nadezhdina, Elena; Brodsky, Ilya.

In: Traffic, Vol. 22, No. 3, 03.2021, p. 64-77.

Research output: Contribution to journal › Article › peer-review

Author

Shomron, Olga ; Hirschberg, Koret ; Burakov, Anton ; Kamentseva, Rimma ; Kornilova, Elena ; Nadezhdina, Elena ; Brodsky, Ilya. / Positioning of endoplasmic reticulum exit sites around the Golgi depends on BicaudalD2 and Rab6 activity. In: Traffic. 2021 ; Vol. 22, No. 3. pp. 64-77.

BibTeX

@article{87dcaba45b664d74b4fb760dcc8b009b,

title = "Positioning of endoplasmic reticulum exit sites around the Golgi depends on BicaudalD2 and Rab6 activity",

abstract = "The endoplasmic reticulum (ER) is involved in biogenesis, modification and transport of secreted and membrane proteins. The ER membranes are spread throughout the cell cytoplasm as well as the export domains known as ER exit sites (ERES). A subpopulation of ERES is centrally localized proximal to the Golgi apparatus. The significance of this subpopulation on ER-to-Golgi transport remains unclear. Transport carriers (TCs) form at the ERES via a COPII-dependent mechanism and move to Golgi on microtubule (MT) tracks. It was shown previously that ERES are distributed along MTs and undergo chaotic short-range movements and sporadic rapid long-range movements. The long-range movements of ERES are impaired by either depolymerization of MTs or inhibition of dynein, suggesting that ERES central concentration is mediated by dynein activity. We demonstrate that the processive movements of ERES are frequently coupled with the TC departure. Using the Sar1a[H79G]-induced ERES clustering at the perinuclear region, we identified BicaudalD2 (BicD2) and Rab6 as components of the dynein adaptor complex which drives perinuclear ERES concentration at the cell center. BicD2 partially colocalized with ERES and with TC. Peri-Golgi ERES localization was significantly affected by inhibition of BicD2 function with its N-terminal fragment or inhibition of Rab6 function with its dominant-negative mutant. Golgi accumulation of secretory protein was delayed by inhibition of Rab6 and BicD2. Thus, we conclude that a BicD2/Rab6 dynein adaptor is required for maintenance of Golgi-associated ERES. We propose that Golgi-associated ERES may enhance the efficiency of the ER-to-Golgi transport.",

keywords = "COPII, dynactin, dynein, ER-to-Golgi transport, microtubule, VSVG, Biological Transport, Microtubules, Intracellular Membranes, Golgi Apparatus/metabolism, Endoplasmic Reticulum/metabolism, Protein Transport",

author = "Olga Shomron and Koret Hirschberg and Anton Burakov and Rimma Kamentseva and Elena Kornilova and Elena Nadezhdina and Ilya Brodsky",

year = "2021",

month = mar,

doi = "10.1111/tra.12774",

language = "English",

volume = "22",

pages = "64--77",

journal = "Traffic",

issn = "1398-9219",

publisher = "Wiley-Blackwell",

number = "3",

}

RIS

TY - JOUR

T1 - Positioning of endoplasmic reticulum exit sites around the Golgi depends on BicaudalD2 and Rab6 activity

AU - Shomron, Olga

AU - Hirschberg, Koret

AU - Burakov, Anton

AU - Kamentseva, Rimma

AU - Kornilova, Elena

AU - Nadezhdina, Elena

AU - Brodsky, Ilya

PY - 2021/3

Y1 - 2021/3

N2 - The endoplasmic reticulum (ER) is involved in biogenesis, modification and transport of secreted and membrane proteins. The ER membranes are spread throughout the cell cytoplasm as well as the export domains known as ER exit sites (ERES). A subpopulation of ERES is centrally localized proximal to the Golgi apparatus. The significance of this subpopulation on ER-to-Golgi transport remains unclear. Transport carriers (TCs) form at the ERES via a COPII-dependent mechanism and move to Golgi on microtubule (MT) tracks. It was shown previously that ERES are distributed along MTs and undergo chaotic short-range movements and sporadic rapid long-range movements. The long-range movements of ERES are impaired by either depolymerization of MTs or inhibition of dynein, suggesting that ERES central concentration is mediated by dynein activity. We demonstrate that the processive movements of ERES are frequently coupled with the TC departure. Using the Sar1a[H79G]-induced ERES clustering at the perinuclear region, we identified BicaudalD2 (BicD2) and Rab6 as components of the dynein adaptor complex which drives perinuclear ERES concentration at the cell center. BicD2 partially colocalized with ERES and with TC. Peri-Golgi ERES localization was significantly affected by inhibition of BicD2 function with its N-terminal fragment or inhibition of Rab6 function with its dominant-negative mutant. Golgi accumulation of secretory protein was delayed by inhibition of Rab6 and BicD2. Thus, we conclude that a BicD2/Rab6 dynein adaptor is required for maintenance of Golgi-associated ERES. We propose that Golgi-associated ERES may enhance the efficiency of the ER-to-Golgi transport.

AB - The endoplasmic reticulum (ER) is involved in biogenesis, modification and transport of secreted and membrane proteins. The ER membranes are spread throughout the cell cytoplasm as well as the export domains known as ER exit sites (ERES). A subpopulation of ERES is centrally localized proximal to the Golgi apparatus. The significance of this subpopulation on ER-to-Golgi transport remains unclear. Transport carriers (TCs) form at the ERES via a COPII-dependent mechanism and move to Golgi on microtubule (MT) tracks. It was shown previously that ERES are distributed along MTs and undergo chaotic short-range movements and sporadic rapid long-range movements. The long-range movements of ERES are impaired by either depolymerization of MTs or inhibition of dynein, suggesting that ERES central concentration is mediated by dynein activity. We demonstrate that the processive movements of ERES are frequently coupled with the TC departure. Using the Sar1a[H79G]-induced ERES clustering at the perinuclear region, we identified BicaudalD2 (BicD2) and Rab6 as components of the dynein adaptor complex which drives perinuclear ERES concentration at the cell center. BicD2 partially colocalized with ERES and with TC. Peri-Golgi ERES localization was significantly affected by inhibition of BicD2 function with its N-terminal fragment or inhibition of Rab6 function with its dominant-negative mutant. Golgi accumulation of secretory protein was delayed by inhibition of Rab6 and BicD2. Thus, we conclude that a BicD2/Rab6 dynein adaptor is required for maintenance of Golgi-associated ERES. We propose that Golgi-associated ERES may enhance the efficiency of the ER-to-Golgi transport.

KW - COPII

KW - dynactin

KW - dynein

KW - ER-to-Golgi transport

KW - microtubule

KW - VSVG

KW - Biological Transport

KW - Microtubules

KW - Intracellular Membranes

KW - Golgi Apparatus/metabolism

KW - Endoplasmic Reticulum/metabolism

KW - Protein Transport

UR - http://www.scopus.com/inward/record.url?scp=85098198489&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/64a9c65e-cdc9-3110-80de-8def41fdffe7/

U2 - 10.1111/tra.12774

DO - 10.1111/tra.12774

M3 - Article

C2 - 33314495

AN - SCOPUS:85098198489

VL - 22

SP - 64

EP - 77

JO - Traffic

JF - Traffic

SN - 1398-9219

IS - 3

ER -

ID: 76656246