Temperature Dependent Activity of the Voltage-Gated Proton Channel

Overview

Journal Adv Exp Med Biol

Specialties Biology
General Medicine

Date 2024 Sep 17

PMID 39289277

Authors

Yuichiro Fujiwara

Affiliations

Soon will be listed here.

Abstract

Voltage-gated proton channel (Hv) has activity of proton transport following electrochemical gradient of proton. Hv is expressed in neutrophils and macrophages of which functions are physiologically temperature-sensitive. Hv is also expressed in human sperm cells and regulates their locomotion. H transport through Hv is both regulated by membrane potential and pH difference across biological membrane. It is also reported that properties of Hv such as proton conductance and gating are highly temperature-dependent. Hv consists of the N-terminal cytoplasmic domain, the voltage sensor domain (VSD), and the C-terminal coiled-coil domain, and H permeates through VSD voltage-dependently. The functional unit of Hv is a dimer via the interaction between C-terminal coiled-coils assembly domain. We have reported that the coiled-coil domain of Hv has the nature of dissociation around our bodily temperature and mutational change of the coiled-coil affected temperature-sensitive gating, especially its temperature threshold. The temperature-sensitive gating is assessed from two separate points: temperature threshold and temperature dependence. In this chapter, I describe physiological roles and molecular structure mechanisms of Hv by mainly focusing on thermosensitive properties.

References

Acharya A, Ruvinov S, Gal J, Moll J, Vinson C . A heterodimerizing leucine zipper coiled coil system for examining the specificity of a position interactions: amino acids I, V, L, N, A, and K. Biochemistry. 2002; 41(48):14122-31. DOI: 10.1021/bi020486r. View

Acharya A, Rishi V, Vinson C . Stability of 100 homo and heterotypic coiled-coil a-a' pairs for ten amino acids (A, L, I, V, N, K, S, T, E, and R). Biochemistry. 2006; 45(38):11324-32. DOI: 10.1021/bi060822u. View

Akey D, Malashkevich V, Kim P . Buried polar residues in coiled-coil interfaces. Biochemistry. 2001; 40(21):6352-60. DOI: 10.1021/bi002829w. View

Alabi A, Bahamonde M, Jung H, Kim J, Swartz K . Portability of paddle motif function and pharmacology in voltage sensors. Nature. 2007; 450(7168):370-5. PMC: 2709416. DOI: 10.1038/nature06266. View

Berger T, Isacoff E . The pore of the voltage-gated proton channel. Neuron. 2011; 72(6):991-1000. PMC: 3244940. DOI: 10.1016/j.neuron.2011.11.014. View

Byerly L, Suen Y . Characterization of proton currents in neurones of the snail, Lymnaea stagnalis. J Physiol. 1989; 413:75-89. PMC: 1189089. DOI: 10.1113/jphysiol.1989.sp017642. View

Capasso M, Bhamrah M, Henley T, Boyd R, Langlais C, Cain K . HVCN1 modulates BCR signal strength via regulation of BCR-dependent generation of reactive oxygen species. Nat Immunol. 2010; 11(3):265-72. PMC: 3030552. DOI: 10.1038/ni.1843. View

Capitano M, Nemeth M, Mace T, Salisbury-Ruf C, Segal B, McCarthy P . Elevating body temperature enhances hematopoiesis and neutrophil recovery after total body irradiation in an IL-1-, IL-17-, and G-CSF-dependent manner. Blood. 2012; 120(13):2600-9. PMC: 3460682. DOI: 10.1182/blood-2012-02-409805. View

Cherny V, DeCoursey T . pH-dependent inhibition of voltage-gated H(+) currents in rat alveolar epithelial cells by Zn(2+) and other divalent cations. J Gen Physiol. 1999; 114(6):819-38. PMC: 2230650. DOI: 10.1085/jgp.114.6.819. View

10.

Cherny V, Murphy R, Sokolov V, Levis R, DeCoursey T . Properties of single voltage-gated proton channels in human eosinophils estimated by noise analysis and by direct measurement. J Gen Physiol. 2003; 121(6):615-28. PMC: 2217352. DOI: 10.1085/jgp.200308813. View

11.

Chodniewicz D, Alteraifi A, Zhelev D . Experimental evidence for the limiting role of enzymatic reactions in chemoattractant-induced pseudopod extension in human neutrophils. J Biol Chem. 2004; 279(23):24460-6. DOI: 10.1074/jbc.M312764200. View

12.

DeCoursey T . Voltage-gated proton channels and other proton transfer pathways. Physiol Rev. 2003; 83(2):475-579. DOI: 10.1152/physrev.00028.2002. View

13.

DeCoursey T, Cherny V . Potential, pH, and arachidonate gate hydrogen ion currents in human neutrophils. Biophys J. 1993; 65(4):1590-8. PMC: 1225885. DOI: 10.1016/S0006-3495(93)81198-6. View

14.

DeCoursey T, Cherny V . Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J Gen Physiol. 1998; 112(4):503-22. PMC: 2229433. DOI: 10.1085/jgp.112.4.503. View

15.

DeCoursey T, Cherny V, DeCoursey A, Xu W, Thomas L . Interactions between NADPH oxidase-related proton and electron currents in human eosinophils. J Physiol. 2001; 535(Pt 3):767-81. PMC: 2278831. DOI: 10.1111/j.1469-7793.2001.00767.x. View

16.

Deng Y, Liu J, Zheng Q, Eliezer D, Kallenbach N, Lu M . Antiparallel four-stranded coiled coil specified by a 3-3-1 hydrophobic heptad repeat. Structure. 2006; 14(2):247-55. PMC: 7126439. DOI: 10.1016/j.str.2005.10.010. View

17.

El Chemaly A, Okochi Y, Sasaki M, Arnaudeau S, Okamura Y, Demaurex N . VSOP/Hv1 proton channels sustain calcium entry, neutrophil migration, and superoxide production by limiting cell depolarization and acidification. J Exp Med. 2009; 207(1):129-39. PMC: 2812533. DOI: 10.1084/jem.20091837. View

18.

Fujiwara Y, Kurokawa T, Takeshita K, Kobayashi M, Okochi Y, Nakagawa A . The cytoplasmic coiled-coil mediates cooperative gating temperature sensitivity in the voltage-gated H(+) channel Hv1. Nat Commun. 2012; 3:816. DOI: 10.1038/ncomms1823. View

19.

Fujiwara Y, Kurokawa T, Takeshita K, Nakagawa A, Larsson H, Okamura Y . Gating of the designed trimeric/tetrameric voltage-gated H+ channel. J Physiol. 2012; 591(3):627-40. PMC: 3577547. DOI: 10.1113/jphysiol.2012.243006. View

20.

Fujiwara Y, Takeshita K, Nakagawa A, Okamura Y . Structural characteristics of the redox-sensing coiled coil in the voltage-gated H+ channel. J Biol Chem. 2013; 288(25):17968-75. PMC: 3689942. DOI: 10.1074/jbc.M113.459024. View