UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner

Tokiro Ishikawa, Takuya Toyama, Yuki Nakamura, Kentaro Tamada, Hitomi Shimizu, Satoshi Ninagawa, Tetsuya Okada, Yasuhiro Kamei, Tomoko Ishikawa-Fujiwara, Takeshi Todo, Eriko Aoyama, Masaharu Takigawa, Akihiro Harada, Kazutoshi Mori

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

The unfolded protein response (UPR) handles unfolded/misfolded proteins accumulated in the endoplasmic reticulum (ER). However, it is unclear how vertebrates correctly use the total of ten UPR transducers. We have found that ER stress occurs physiologically during early embryonic development in medaka fish and that the smooth alignment of notochord cells requires ATF6 as a UPR transducer, which induces ER chaperones for folding of type VIII (short-chain) collagen. After secretion of hedgehog for tissue patterning, notochord cells differentiate into sheath cells, which synthesize type II collagen. In this study, we show that this vacuolization step requires both ATF6 and BBF2H7 as UPR transducers and that BBF2H7 regulates a complete set of genes (Sec23/24/13/31, Tango1, Sedlin, and KLHL12) essential for the enlargement of COP II vesicles to accommodate long-chain collagen for export, leading to the formation of the perinotochordal basement membrane. Thus, the most appropriate UPR transducer is activated to cope with the differing physiological ER stresses of different content types depending on developmental stage.

Original languageEnglish
Pages (from-to)1761-1774
Number of pages14
JournalJournal of Cell Biology
Volume216
Issue number6
DOIs
Publication statusPublished - Jun 1 2017

Fingerprint

Unfolded Protein Response
Collagen Type II
Transducers
Notochord
Endoplasmic Reticulum Stress
Endoplasmic Reticulum
Non-Fibrillar Collagens
Oryzias
Protein Unfolding
Hedgehogs
Basement Membrane
Embryonic Development
Vertebrates
Fishes
Collagen
Genes

ASJC Scopus subject areas

  • Cell Biology

Cite this

Ishikawa, T., Toyama, T., Nakamura, Y., Tamada, K., Shimizu, H., Ninagawa, S., ... Mori, K. (2017). UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner. Journal of Cell Biology, 216(6), 1761-1774. https://doi.org/10.1083/jcb.201609100

UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner. / Ishikawa, Tokiro; Toyama, Takuya; Nakamura, Yuki; Tamada, Kentaro; Shimizu, Hitomi; Ninagawa, Satoshi; Okada, Tetsuya; Kamei, Yasuhiro; Ishikawa-Fujiwara, Tomoko; Todo, Takeshi; Aoyama, Eriko; Takigawa, Masaharu; Harada, Akihiro; Mori, Kazutoshi.

In: Journal of Cell Biology, Vol. 216, No. 6, 01.06.2017, p. 1761-1774.

Research output: Contribution to journalArticle

Ishikawa, T, Toyama, T, Nakamura, Y, Tamada, K, Shimizu, H, Ninagawa, S, Okada, T, Kamei, Y, Ishikawa-Fujiwara, T, Todo, T, Aoyama, E, Takigawa, M, Harada, A & Mori, K 2017, 'UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner', Journal of Cell Biology, vol. 216, no. 6, pp. 1761-1774. https://doi.org/10.1083/jcb.201609100
Ishikawa, Tokiro ; Toyama, Takuya ; Nakamura, Yuki ; Tamada, Kentaro ; Shimizu, Hitomi ; Ninagawa, Satoshi ; Okada, Tetsuya ; Kamei, Yasuhiro ; Ishikawa-Fujiwara, Tomoko ; Todo, Takeshi ; Aoyama, Eriko ; Takigawa, Masaharu ; Harada, Akihiro ; Mori, Kazutoshi. / UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner. In: Journal of Cell Biology. 2017 ; Vol. 216, No. 6. pp. 1761-1774.
@article{3b5cc7b8ccbd401b9c98fcd6eccfc87f,
title = "UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner",
abstract = "The unfolded protein response (UPR) handles unfolded/misfolded proteins accumulated in the endoplasmic reticulum (ER). However, it is unclear how vertebrates correctly use the total of ten UPR transducers. We have found that ER stress occurs physiologically during early embryonic development in medaka fish and that the smooth alignment of notochord cells requires ATF6 as a UPR transducer, which induces ER chaperones for folding of type VIII (short-chain) collagen. After secretion of hedgehog for tissue patterning, notochord cells differentiate into sheath cells, which synthesize type II collagen. In this study, we show that this vacuolization step requires both ATF6 and BBF2H7 as UPR transducers and that BBF2H7 regulates a complete set of genes (Sec23/24/13/31, Tango1, Sedlin, and KLHL12) essential for the enlargement of COP II vesicles to accommodate long-chain collagen for export, leading to the formation of the perinotochordal basement membrane. Thus, the most appropriate UPR transducer is activated to cope with the differing physiological ER stresses of different content types depending on developmental stage.",
author = "Tokiro Ishikawa and Takuya Toyama and Yuki Nakamura and Kentaro Tamada and Hitomi Shimizu and Satoshi Ninagawa and Tetsuya Okada and Yasuhiro Kamei and Tomoko Ishikawa-Fujiwara and Takeshi Todo and Eriko Aoyama and Masaharu Takigawa and Akihiro Harada and Kazutoshi Mori",
year = "2017",
month = "6",
day = "1",
doi = "10.1083/jcb.201609100",
language = "English",
volume = "216",
pages = "1761--1774",
journal = "Journal of Cell Biology",
issn = "0021-9525",
publisher = "Rockefeller University Press",
number = "6",

}

TY - JOUR

T1 - UPR transducer BBF2H7 allows export of type II collagen in a cargo- and developmental stage- specific manner

AU - Ishikawa, Tokiro

AU - Toyama, Takuya

AU - Nakamura, Yuki

AU - Tamada, Kentaro

AU - Shimizu, Hitomi

AU - Ninagawa, Satoshi

AU - Okada, Tetsuya

AU - Kamei, Yasuhiro

AU - Ishikawa-Fujiwara, Tomoko

AU - Todo, Takeshi

AU - Aoyama, Eriko

AU - Takigawa, Masaharu

AU - Harada, Akihiro

AU - Mori, Kazutoshi

PY - 2017/6/1

Y1 - 2017/6/1

N2 - The unfolded protein response (UPR) handles unfolded/misfolded proteins accumulated in the endoplasmic reticulum (ER). However, it is unclear how vertebrates correctly use the total of ten UPR transducers. We have found that ER stress occurs physiologically during early embryonic development in medaka fish and that the smooth alignment of notochord cells requires ATF6 as a UPR transducer, which induces ER chaperones for folding of type VIII (short-chain) collagen. After secretion of hedgehog for tissue patterning, notochord cells differentiate into sheath cells, which synthesize type II collagen. In this study, we show that this vacuolization step requires both ATF6 and BBF2H7 as UPR transducers and that BBF2H7 regulates a complete set of genes (Sec23/24/13/31, Tango1, Sedlin, and KLHL12) essential for the enlargement of COP II vesicles to accommodate long-chain collagen for export, leading to the formation of the perinotochordal basement membrane. Thus, the most appropriate UPR transducer is activated to cope with the differing physiological ER stresses of different content types depending on developmental stage.

AB - The unfolded protein response (UPR) handles unfolded/misfolded proteins accumulated in the endoplasmic reticulum (ER). However, it is unclear how vertebrates correctly use the total of ten UPR transducers. We have found that ER stress occurs physiologically during early embryonic development in medaka fish and that the smooth alignment of notochord cells requires ATF6 as a UPR transducer, which induces ER chaperones for folding of type VIII (short-chain) collagen. After secretion of hedgehog for tissue patterning, notochord cells differentiate into sheath cells, which synthesize type II collagen. In this study, we show that this vacuolization step requires both ATF6 and BBF2H7 as UPR transducers and that BBF2H7 regulates a complete set of genes (Sec23/24/13/31, Tango1, Sedlin, and KLHL12) essential for the enlargement of COP II vesicles to accommodate long-chain collagen for export, leading to the formation of the perinotochordal basement membrane. Thus, the most appropriate UPR transducer is activated to cope with the differing physiological ER stresses of different content types depending on developmental stage.

UR - http://www.scopus.com/inward/record.url?scp=85021797146&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85021797146&partnerID=8YFLogxK

U2 - 10.1083/jcb.201609100

DO - 10.1083/jcb.201609100

M3 - Article

VL - 216

SP - 1761

EP - 1774

JO - Journal of Cell Biology

JF - Journal of Cell Biology

SN - 0021-9525

IS - 6

ER -