A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog

Xiao Tang; Rong Chen; Vince St Dollente Mesias; Tingxuan Wang; Ying Wang; Kristina Poljak; Xinyu Fan; Hanchi Miao; Junjie Hu; Liang Zhang; Jinqing Huang; Shuhuai Yao; Elizabeth A Miller; Yusong Guo

doi:10.1073/pnas.2113991119

A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog

Xiao Tang, Rong Chen, Vince St Dollente Mesias, Tingxuan Wang, Ying Wang, Kristina Poljak, Xinyu Fan, Hanchi Miao, Junjie Hu, Liang Zhang, Jinqing Huang, Shuhuai Yao, Elizabeth A Miller, Yusong Guo

Molecular Cell and Developmental Biology

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Abstract

SignificanceSonic Hedgehog (Shh) is a key signaling molecule that plays important roles in embryonic patterning, cell differentiation, and organ development. Although fundamentally important, the molecular mechanisms that regulate secretion of newly synthesized Shh are still unclear. Our study reveals a role for the cargo receptor, SURF4, in facilitating export of Shh from the endoplasmic reticulum (ER) via a ER export signal. In addition, our study provides evidence suggesting that proteoglycans promote the dissociation of SURF4 from Shh at the Golgi, suggesting a SURF4-to-proteoglycan relay mechanism. These analyses provide insight into an important question in cell biology: how do cargo receptors capture their clients in one compartment, then disengage at their destination?

Original language	English
Article number	e2113991119
Number of pages	12
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	11
DOIs	https://doi.org/10.1073/pnas.2113991119
Publication status	Published - 15 Mar 2022

Keywords

Endoplasmic Reticulum/metabolism
Hedgehog Proteins/genetics
Humans
Membrane Proteins/genetics
Protein Transport/physiology
Proteoglycans/metabolism

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10.1073/pnas.2113991119Licence: CC BY

Final Published VersionFinal published version, 2.18 MBLicence: CC BY

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Tang, X., Chen, R., Mesias, V. S. D., Wang, T., Wang, Y., Poljak, K., Fan, X., Miao, H., Hu, J., Zhang, L., Huang, J., Yao, S., Miller, E. A., & Guo, Y. (2022). A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog. Proceedings of the National Academy of Sciences of the United States of America, 119(11), Article e2113991119. https://doi.org/10.1073/pnas.2113991119

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title = "A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog",

abstract = "SignificanceSonic Hedgehog (Shh) is a key signaling molecule that plays important roles in embryonic patterning, cell differentiation, and organ development. Although fundamentally important, the molecular mechanisms that regulate secretion of newly synthesized Shh are still unclear. Our study reveals a role for the cargo receptor, SURF4, in facilitating export of Shh from the endoplasmic reticulum (ER) via a ER export signal. In addition, our study provides evidence suggesting that proteoglycans promote the dissociation of SURF4 from Shh at the Golgi, suggesting a SURF4-to-proteoglycan relay mechanism. These analyses provide insight into an important question in cell biology: how do cargo receptors capture their clients in one compartment, then disengage at their destination?",

keywords = "Endoplasmic Reticulum/metabolism, Hedgehog Proteins/genetics, Humans, Membrane Proteins/genetics, Protein Transport/physiology, Proteoglycans/metabolism",

author = "Xiao Tang and Rong Chen and Mesias, {Vince St Dollente} and Tingxuan Wang and Ying Wang and Kristina Poljak and Xinyu Fan and Hanchi Miao and Junjie Hu and Liang Zhang and Jinqing Huang and Shuhuai Yao and Miller, {Elizabeth A} and Yusong Guo",

year = "2022",

month = mar,

day = "15",

doi = "10.1073/pnas.2113991119",

language = "English",

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journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Tang, X, Chen, R, Mesias, VSD, Wang, T, Wang, Y, Poljak, K, Fan, X, Miao, H, Hu, J, Zhang, L, Huang, J, Yao, S, Miller, EA & Guo, Y 2022, 'A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog', Proceedings of the National Academy of Sciences of the United States of America, vol. 119, no. 11, e2113991119. https://doi.org/10.1073/pnas.2113991119

A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog. / Tang, Xiao; Chen, Rong; Mesias, Vince St Dollente et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 119, No. 11, e2113991119, 15.03.2022.

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

TY - JOUR

T1 - A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog

AU - Tang, Xiao

AU - Chen, Rong

AU - Mesias, Vince St Dollente

AU - Wang, Tingxuan

AU - Wang, Ying

AU - Poljak, Kristina

AU - Fan, Xinyu

AU - Miao, Hanchi

AU - Hu, Junjie

AU - Zhang, Liang

AU - Huang, Jinqing

AU - Yao, Shuhuai

AU - Miller, Elizabeth A

AU - Guo, Yusong

PY - 2022/3/15

Y1 - 2022/3/15

N2 - SignificanceSonic Hedgehog (Shh) is a key signaling molecule that plays important roles in embryonic patterning, cell differentiation, and organ development. Although fundamentally important, the molecular mechanisms that regulate secretion of newly synthesized Shh are still unclear. Our study reveals a role for the cargo receptor, SURF4, in facilitating export of Shh from the endoplasmic reticulum (ER) via a ER export signal. In addition, our study provides evidence suggesting that proteoglycans promote the dissociation of SURF4 from Shh at the Golgi, suggesting a SURF4-to-proteoglycan relay mechanism. These analyses provide insight into an important question in cell biology: how do cargo receptors capture their clients in one compartment, then disengage at their destination?

AB - SignificanceSonic Hedgehog (Shh) is a key signaling molecule that plays important roles in embryonic patterning, cell differentiation, and organ development. Although fundamentally important, the molecular mechanisms that regulate secretion of newly synthesized Shh are still unclear. Our study reveals a role for the cargo receptor, SURF4, in facilitating export of Shh from the endoplasmic reticulum (ER) via a ER export signal. In addition, our study provides evidence suggesting that proteoglycans promote the dissociation of SURF4 from Shh at the Golgi, suggesting a SURF4-to-proteoglycan relay mechanism. These analyses provide insight into an important question in cell biology: how do cargo receptors capture their clients in one compartment, then disengage at their destination?

KW - Endoplasmic Reticulum/metabolism

KW - Hedgehog Proteins/genetics

KW - Humans

KW - Membrane Proteins/genetics

KW - Protein Transport/physiology

KW - Proteoglycans/metabolism

U2 - 10.1073/pnas.2113991119

DO - 10.1073/pnas.2113991119

M3 - Article

C2 - 35271396

SN - 0027-8424

VL - 119

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 11

M1 - e2113991119

ER -

A SURF4-to-proteoglycan relay mechanism that mediates the sorting and secretion of a tagged variant of sonic hedgehog

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