Coupling sensor to enzyme in the voltage sensing phosphatase

Yu, Yawei; Zhang, Lin; Li, Baobin; Fu, Zhu; Brohawn, Stephen G.; Isacoff, Ehud Y.

doi:10.1038/s41467-024-50319-8

Coupling sensor to enzyme in the voltage sensing phosphatase

Journal Article · Tue Jul 30 00:00:00 EDT 2024 · Nature Communications

DOI:https://doi.org/10.1038/s41467-024-50319-8· OSTI ID:2470965

^[1]; Zhang, Lin ^[1]; ^[2]; ^[1]; ^[1]; ^[3]

University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States); Fudan University, Shanghai (China)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Voltage-sensing phosphatases (VSPs) dephosphorylate phosphoinositide (PIP) signaling lipids in response to membrane depolarization. VSPs possess an S4-containing voltage sensor domain (VSD), resembling that of voltage-gated cation channels, and a lipid phosphatase domain (PD). The mechanism by which voltage turns on enzyme activity is unclear. Structural analysis and modeling suggest several sites of VSD-PD interaction that could couple voltage sensing to catalysis. Voltage clamp fluorometry reveals voltage-driven rearrangements in three sites implicated earlier in enzyme activation—the VSD-PD linker, gating loop and R loop—as well as the N-terminal domain, which has not yet been explored. N-terminus mutations perturb both rearrangements in the other segments and enzyme activity. Our results provide a model for a dynamic assembly by which S4 controls the catalytic site.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470965

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (28)

Coupling of Ci-VSP Modules Requires a Combination of Structure and Electrostatics within the Linker Hobiger, Kirstin; Utesch, Tillmann; Mroginski, Maria Andrea Biophysical Journal, Vol. 102, Issue 6 https://doi.org/10.1016/j.bpj.2012.02.027	journal	March 2012
A Genetically Encoded Fluorescent Probe in Mammalian Cells Chatterjee, Abhishek; Guo, Jiantao; Lee, Hyun Soo Journal of the American Chemical Society, Vol. 135, Issue 34 https://doi.org/10.1021/ja4059553	journal	August 2013
Genetic Incorporation of a Small, Environmentally Sensitive, Fluorescent Probe into Proteins in Saccharomyces cerevisiae Lee, Hyun Soo; Guo, Jiantao; Lemke, Edward A. Journal of the American Chemical Society, Vol. 131, Issue 36 https://doi.org/10.1021/ja904896s	journal	August 2009
Activation of inwardly rectifying K+ channels by distinct PtdIns(4,5)P2 interactions Zhang, Hailin; He, Cheng; Yan, Xixin Nature Cell Biology, Vol. 1, Issue 3 https://doi.org/10.1038/11103	journal	June 1999
Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor Murata, Yoshimichi; Iwasaki, Hirohide; Sasaki, Mari Nature, Vol. 435, Issue 7046 https://doi.org/10.1038/nature03650	journal	May 2005
Allosteric substrate switching in a voltage-sensing lipid phosphatase Grimm, Sasha S.; Isacoff, Ehud Y. Nature Chemical Biology, Vol. 12, Issue 4 https://doi.org/10.1038/nchembio.2022	journal	February 2016
Electrochemical coupling in the voltage-dependent phosphatase Ci-VSP Kohout, Susy C.; Bell, Sarah C.; Liu, Lijun Nature Chemical Biology, Vol. 6, Issue 5 https://doi.org/10.1038/nchembio.349	journal	April 2010
A glutamate switch controls voltage-sensitive phosphatase function Liu, Lijun; Kohout, Susy C.; Xu, Qiang Nature Structural & Molecular Biology, Vol. 19, Issue 6 https://doi.org/10.1038/nsmb.2289	journal	May 2012
Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain Li, Qufei; Wanderling, Sherry; Paduch, Marcin Nature Structural & Molecular Biology, Vol. 21, Issue 3 https://doi.org/10.1038/nsmb.2768	journal	February 2014
Subunit organization and functional transitions in Ci-VSP Kohout, Susy C.; Ulbrich, Maximilian H.; Bell, Sarah C. Nature Structural & Molecular Biology, Vol. 15, Issue 1 https://doi.org/10.1038/nsmb1320	journal	December 2007
Structural basis for pH gating of the two-pore domain K+ channel TASK2 Li, Baobin; Rietmeijer, Robert A.; Brohawn, Stephen G. Nature, Vol. 586, Issue 7829 https://doi.org/10.1038/s41586-020-2770-2	journal	September 2020
Voltage-sensing phosphatase (Vsp) regulates endocytosis-dependent nutrient absorption in chordate enterocytes Ratanayotha, Adisorn; Matsuda, Makoto; Kimura, Yukiko Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03916-6	journal	September 2022
Dynamics of internal pore opening in KV channels probed by a fluorescent unnatural amino acid Kalstrup, T.; Blunck, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 20 https://doi.org/10.1073/pnas.1220398110	journal	April 2013
Voltage-dependent motion of the catalytic region of voltage-sensing phosphatase monitored by a fluorescent amino acid Sakata, Souhei; Jinno, Yuka; Kawanabe, Akira Proceedings of the National Academy of Sciences, Vol. 113, Issue 27 https://doi.org/10.1073/pnas.1604218113	journal	June 2016
Polarized PtdIns(4,5)P ₂ distribution mediated by a voltage-sensing phosphatase (VSP) regulates sperm motility Kawai, Takafumi; Miyata, Haruhiko; Nakanishi, Hiroki Proceedings of the National Academy of Sciences, Vol. 116, Issue 51 https://doi.org/10.1073/pnas.1916867116	journal	November 2019
Interaction between S4 and the phosphatase domain mediates electrochemical coupling in voltage-sensing phosphatase (VSP) Mizutani, Natsuki; Kawanabe, Akira; Jinno, Yuka Proceedings of the National Academy of Sciences, Vol. 119, Issue 26 https://doi.org/10.1073/pnas.2200364119	journal	June 2022
Mechanism of voltage gating in the voltage-sensing phosphatase Ci-VSP Shen, Rong; Meng, Yilin; Roux, Benoît Proceedings of the National Academy of Sciences, Vol. 119, Issue 44 https://doi.org/10.1073/pnas.2206649119	journal	October 2022
Enzyme Domain Affects the Movement of the Voltage Sensor in Ascidian and Zebrafish Voltage-sensing Phosphatases Hossain, Md. Israil; Iwasaki, Hirohide; Okochi, Yoshifumi Journal of Biological Chemistry, Vol. 283, Issue 26 https://doi.org/10.1074/jbc.M706184200	journal	June 2008
Coupling between the voltage-sensing and phosphatase domains of Ci-VSP Villalba-Galea, Carlos A.; Miceli, Francesco; Taglialatela, Maurizio Journal of General Physiology, Vol. 134, Issue 1 https://doi.org/10.1085/jgp.200910215	journal	June 2009
Sensing charges of the Ciona intestinalis voltage-sensing phosphatase Villalba-Galea, Carlos A.; Frezza, Ludivine; Sandtner, Walter The Journal of General Physiology, Vol. 142, Issue 5 https://doi.org/10.1085/jgp.201310993	journal	October 2013
Dimerization of the voltage-sensing phosphatase controls its voltage-sensing and catalytic activity Rayaprolu, Vamseedhar; Royal, Perrine; Stengel, Karen Journal of General Physiology, Vol. 150, Issue 5 https://doi.org/10.1085/jgp.201812064	journal	April 2018
Dual-Specific Protein and Lipid Phosphatase PTEN and Its Biological Functions Tu, Taojian; Chen, Jingyu; Chen, Lulu Cold Spring Harbor Perspectives in Medicine, Vol. 10, Issue 1 https://doi.org/10.1101/cshperspect.a036301	journal	September 2019
Depolarization activates the phosphoinositide phosphatase Ci‐VSP, as detected in Xenopus oocytes coexpressing sensors of PIP₂ Murata, Yoshimichi; Okamura, Yasushi The Journal of Physiology, Vol. 583, Issue 3 https://doi.org/10.1113/jphysiol.2007.134775	journal	September 2007
Phosphoinositide Phosphatases: Emerging Roles As Voltage Sensors? Worby, C. A. Molecular Interventions, Vol. 5, Issue 5 https://doi.org/10.1124/mi.5.5.5	journal	October 2005
Direct Physical Measure of Conformational Rearrangement Underlying Potassium Channel Gating Mannuzzu, L. M.; Moronne, M. M.; Isacoff, E. Y. Science, Vol. 271, Issue 5246 https://doi.org/10.1126/science.271.5246.213	journal	January 1996
PIP ₂ Is a Necessary Cofactor for Ion Channel Function: How and Why? Suh, Byung-Chang; Hille, Bertil Annual Review of Biophysics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.biophys.37.032807.125859	journal	June 2008
The Linker Pivot in Ci-VSP: The Key to Unlock Catalysis Hobiger, Kirstin; Utesch, Tillmann; Mroginski, Maria Andrea PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0070272	journal	July 2013
The hydrophobic nature of a novel membrane interface regulates the enzyme activity of a voltage-sensing phosphatase Kawanabe, Akira; Hashimoto, Masaki; Nishizawa, Manami eLife, Vol. 7 https://doi.org/10.7554/eLife.41653	journal	November 2018

Similar Records

Molecular Coupling of S4 to a K⁺ Channel's Slow Inactivation Gate

Journal Article · Sun Oct 15 20:00:00 EDT 2000 · Journal of General Physiology · OSTI ID:1625205

Dual regulation of hEAG1 channels by phosphatidylinositol 4,5-bisphosphate

Journal Article · Sat Sep 15 00:00:00 EDT 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23134283

Direct physical measure of conformational rearrangement underlying potassium channel gating

Journal Article · Thu Jan 11 23:00:00 EST 1996 · Science · OSTI ID:263056

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Biochemistry
Fluorescence spectroscopy
Molecular conformation
Science & Technology - Other Topics

Coupling sensor to enzyme in the voltage sensing phosphatase

Citation Formats

References (28)

Similar Records

Related Subjects