The Tiam1 guanine nucleotide exchange factor is auto-inhibited by its pleckstrin homology coiled-coil extension domain
Abstract
T-cell lymphoma invasion and metastasis 1 (Tiam1) is a Dbl-family guanine nucleotide exchange factor (GEF) that specifically activates the Rho-family GTPase Rac1 in response to upstream signals, thereby regulating cellular processes including cell adhesion and migration. Tiam1 contains multiple domains, including an N-terminal pleckstrin homology coiled-coiled extension (PHn-CC-Ex) and catalytic Dbl homology and C-terminal pleckstrin homology (DH-PHc) domain. Previous studies indicate that larger fragments of Tiam1, such as the region encompassing the N-terminal to C-terminal pleckstrin homology domains (PHn-PHc), are auto-inhibited. However, the domains in this region responsible for inhibition remain unknown. Here, we show that the PHn-CC-Ex domain inhibits Tiam1 GEF activity by directly interacting with the catalytic DH-PHc domain, preventing Rac1 binding and activation. Enzyme kinetics experiments suggested that Tiam1 is auto-inhibited through occlusion of the catalytic site rather than by allostery. Small angle X-ray scattering and ensemble modeling yielded models of the PHn-PHc fragment that indicate it is in equilibrium between “open” and “closed” conformational states. Lastly, single-molecule experiments support a model in which conformational sampling between the open and closed states of Tiam1 contributes to Rac1 dissociation. Our results highlight the role of the PHn-CC-Ex domain in Tiam1 GEF regulation and suggest a combinatorial model formore »
- Publication Date:
- Research Org.:
- Bettis Atomic Power Lab. (BAPL), West Mifflin, PA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Inst. of Health; National Science Foundation (NSF)
- OSTI Identifier:
- 1432852
- Grant/Contract Number:
- AC02-05CH11231; AC02-06CH11357; R01 GM108617; MCB-0953080; NIH 5T32GM008365
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 292; Journal Issue: 43; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; enzyme kinetics; guanine nucleotide exchange factor (GEF); inhibition mechanism; Ras-related C3 botulinum toxin substrate 1 (Rac1); small-angle X-ray scattering (SAXS); single-molecule total internal reflection fluorescence microscopy; Tiam1; auto-inhibition; in vitro GEF assays
Citation Formats
Xu, Zhen, Gakhar, Lokesh, Bain, Fletcher E., Spies, Maria, and Fuentes, Ernesto J.. The Tiam1 guanine nucleotide exchange factor is auto-inhibited by its pleckstrin homology coiled-coil extension domain. United States: N. p., 2017.
Web. doi:10.1074/jbc.M117.799114.
Xu, Zhen, Gakhar, Lokesh, Bain, Fletcher E., Spies, Maria, & Fuentes, Ernesto J.. The Tiam1 guanine nucleotide exchange factor is auto-inhibited by its pleckstrin homology coiled-coil extension domain. United States. https://doi.org/10.1074/jbc.M117.799114
Xu, Zhen, Gakhar, Lokesh, Bain, Fletcher E., Spies, Maria, and Fuentes, Ernesto J.. Thu .
"The Tiam1 guanine nucleotide exchange factor is auto-inhibited by its pleckstrin homology coiled-coil extension domain". United States. https://doi.org/10.1074/jbc.M117.799114. https://www.osti.gov/servlets/purl/1432852.
@article{osti_1432852,
title = {The Tiam1 guanine nucleotide exchange factor is auto-inhibited by its pleckstrin homology coiled-coil extension domain},
author = {Xu, Zhen and Gakhar, Lokesh and Bain, Fletcher E. and Spies, Maria and Fuentes, Ernesto J.},
abstractNote = {T-cell lymphoma invasion and metastasis 1 (Tiam1) is a Dbl-family guanine nucleotide exchange factor (GEF) that specifically activates the Rho-family GTPase Rac1 in response to upstream signals, thereby regulating cellular processes including cell adhesion and migration. Tiam1 contains multiple domains, including an N-terminal pleckstrin homology coiled-coiled extension (PHn-CC-Ex) and catalytic Dbl homology and C-terminal pleckstrin homology (DH-PHc) domain. Previous studies indicate that larger fragments of Tiam1, such as the region encompassing the N-terminal to C-terminal pleckstrin homology domains (PHn-PHc), are auto-inhibited. However, the domains in this region responsible for inhibition remain unknown. Here, we show that the PHn-CC-Ex domain inhibits Tiam1 GEF activity by directly interacting with the catalytic DH-PHc domain, preventing Rac1 binding and activation. Enzyme kinetics experiments suggested that Tiam1 is auto-inhibited through occlusion of the catalytic site rather than by allostery. Small angle X-ray scattering and ensemble modeling yielded models of the PHn-PHc fragment that indicate it is in equilibrium between “open” and “closed” conformational states. Lastly, single-molecule experiments support a model in which conformational sampling between the open and closed states of Tiam1 contributes to Rac1 dissociation. Our results highlight the role of the PHn-CC-Ex domain in Tiam1 GEF regulation and suggest a combinatorial model for GEF inhibition and activation of the Rac1 signaling pathway.},
doi = {10.1074/jbc.M117.799114},
journal = {Journal of Biological Chemistry},
number = 43,
volume = 292,
place = {United States},
year = {2017},
month = {9}
}
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