Molecular determinants of Hv1 proton channel inhibition by guanidine derivatives

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

Volumn 111, Issue 27, 2014, Pages 9971-9976

  Hong, Liang ^a   Kim, Iris H ^a   Tombola, Francesco ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

HVCN1 blocker; Macrophage; Microglial cell

Indexed keywords

2 GUANIDINOBENZIMIDAZOLE; ARGININE; ASPARTIC ACID; BENZIMIDAZOLE; CATION CHANNEL; GUANIDINE DERIVATIVE; HV1 VOLTAGE GATED PROTON CHANNEL; IMIDAZOLE; PHENYLALANINE; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; MACROPHAGE; MEMBRANE PERMEABILITY; MOLECULAR INTERACTION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON TRANSPORT; STEADY STATE; SYNTHESIS; XENOPUS LAEVIS;

HVCN1 BLOCKER; MACROPHAGE; MICROGLIAL CELL;

ANIMALS; CELLS, CULTURED; GUANIDINES; HUMANS; ION CHANNEL GATING; ION CHANNELS; XENOPUS LAEVIS;

EID: 84903954494     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1324012111     Document Type: Article

References (45)

1. Wu LJ, et al. (2012) The voltage-gated proton channel Hv1 enhances brain damage from ischemic stroke. Nat Neurosci 15(4):565-573.
2. DeCoursey TE (2013) Voltage-gated proton channels: Molecular biology, physiology, and pathophysiology of the H(V) family. Physiol Rev 93(2):599-652.
3. DeCoursey TE, Morgan D, Cherny VV (2003) The voltage dependence of NADPH oxidase reveals why phagocytes need proton channels. Nature 422(6931):531-534. (Pubitemid 36433649)
4. Ramsey IS, Ruchti E, Kaczmarek JS, Clapham DE (2009) Hv1 proton channels are required for high-level NADPH oxidase-dependent superoxide production during the phagocyte respiratory burst. Proc Natl Acad Sci USA 106(18):7642-7647.
5. El Chemaly A, et al. (2010) VSOP/Hv1 proton channels sustain calcium entry, neutrophil migration, and superoxide production by limiting cell depolarization and acidification. J Exp Med 207(1):129-139.
6. Capasso M, et al. (2010) HVCN1 modulates BCR signal strength via regulation of BCR-dependent generation of reactive oxygen species. Nat Immunol 11(3):265-272.
7. Wang Y, Li SJ,Wu X, Che Y, Li Q (2012) Clinicopathological and biological significance of human voltage-gated proton channel Hv1 protein overexpression in breast cancer. J Biol Chem 287(17):13877-13888.
8. Wang Y, Wu X, Li Q, Zhang S, Li SJ (2013) Human voltage-gated proton channel hv1: A new potential biomarker for diagnosis and prognosis of colorectal cancer. PLoS ONE 8(8):e70550.
9. Ramsey IS, Moran MM, Chong JA, Clapham DE (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440(7088):1213-1216.
10. Sasaki M, Takagi M, Okamura Y (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312(5773):589-592.
11. Yu FH, Catterall WA (2004) The VGL-chanome: A protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004(253):re15.
12. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435(7046):1239-1243. (Pubitemid 40943089)
13. Li SJ, et al. (2010) The role and structure of the carboxyl-terminal domain of the human voltage-gated proton channel Hv1. J Biol Chem 285(16):12047-12054.
14. Fujiwara Y, et al. (2012) The cytoplasmic coiled-coil mediates cooperative gating temperature sensitivity in the voltage-gated H(+) channel Hv1. Nat Commun 3:816.
15. Lee SY, Letts JA, Mackinnon R (2008) Dimeric subunit stoichiometry of the human voltage-dependent proton channel Hv1. Proc Natl Acad Sci USA 105(22):7692-7695. (Pubitemid 351872700)
16. Tombola F, Ulbrich MH, Isacoff EY (2008) The voltage-gated proton channel Hv1 has two pores, each controlled by one voltage sensor. Neuron 58(4):546-556. (Pubitemid 351672357)
17. Koch HP, et al. (2008) Multimeric nature of voltage-gated proton channels. Proc Natl Acad Sci USA 105(26):9111-9116.
18. Hille B (2001) Ion Channels of Excitable Membranes (Sinauer, Sunderland, MA), 3rd Ed.
19. Wulff H, Castle NA, Pardo LA (2009) Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov 8(12):982-1001.
20. Swartz KJ, MacKinnon R (1995) An inhibitor of the Kv2.1 potassium channel isolated from the venom of a Chilean tarantula. Neuron 15(4):941-949.
21. Wang J, et al. (2011) Mapping the receptor site for alpha-scorpion toxins on a Na+ channel voltage sensor. Proc Natl Acad Sci USA 108(37):15426-15431.
22. Börjesson SI, Elinder F (2011) An electrostatic potassium channel opener targeting the final voltage sensor transition. J Gen Physiol 137(6):563-577.
23. Li P, et al. (2013) The gating charge pathway of an epilepsy-associated potassium channel accommodates chemical ligands. Cell Res 23(9):1106-1118.
24. Peretz A, et al. (2010) Targeting the voltage sensor of Kv7.2 voltage-gated K+ channels with a new gating-modifier. Proc Natl Acad Sci USA 107(35):15637-15642.
25. Hong L, Pathak MM, Kim IH, Ta D, Tombola F (2013) Voltage-sensing domain of voltage-gated proton channel Hv1 shares mechanism of block with pore domains. Neuron 77(2):274-287.
26. Takeshita K, et al. (2014) X-ray crystal structure of voltage-gated proton channel. Nat Struct Mol Biol 21(4):352-357.
27. Hidalgo P, MacKinnon R (1995) Revealing the architecture of a K+ channel pore through mutant cycles with a peptide inhibitor. Science 268(5208):307-310.
28. Horovitz A, Fersht AR (1990) Strategy for analysing the co-operativity of intramolecular interactions in peptides and proteins. J Mol Biol 214(3):613-617.
29. Musset B, et al. (2011) Aspartate 112 is the selectivity filter of the human voltage-gated proton channel. Nature 480(7376):273-277.
30. Berger TK, Isacoff EY (2011) The pore of the voltage-gated proton channel. Neuron 72(6):991-1000.
31. Morgan D, et al. (2013) Peregrination of the selectivity filter delineates the pore of the human voltage-gated proton channel hHV1. J Gen Physiol 142(6):625-640.
32. Wood ML, et al. (2012) Water wires in atomistic models of the Hv1 proton channel. Biochim Biophys Acta 1818(2):286-293.
33. Kulleperuma K, et al. (2013) Construction and validation of a homology model of the human voltage-gated proton channel hHV1. J Gen Physiol 141(4):445-465.
34. Song JH, Marszalec W, Kai L, Yeh JZ, Narahashi T (2012) Antidepressants inhibit proton currents and tumor necrosis factor-α production in BV2 microglial cells. Brain Res 1435:15-23.
35. DeCoursey TE, Cherny VV (1996) Voltage-activated proton currents in human THP-1 monocytes. J Membr Biol 152(2):131-140. (Pubitemid 26266045)
36. Sakai H, et al. (2013) Increases in intracellular pH facilitate endocytosis and decrease availability of voltage-gated proton channels in osteoclasts and microglia. J Physiol 591(Pt 23):5851-5866.
37. Ramsey IS, et al. (2010) An aqueous H+ permeation pathway in the voltage-gated proton channel Hv1. Nat Struct Mol Biol 17(7):869-875.
38. Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328(5974):67-73.
39. Lacroix JJ, Bezanilla F (2011) Control of a final gating charge transition by a hydrophobic residue in the S2 segment of a K+ channel voltage sensor. Proc Natl Acad Sci USA 108(16):6444-6449.
40. Gonzalez C, Koch HP, Drum BM, Larsson HP (2010) Strong cooperativity between subunits in voltage-gated proton channels. Nat Struct Mol Biol 17(1):51-56.
41. Li Q, Wanderling S, Perozo E (2014) The resting state of human proton channel from functional and structural determinations. Biophys J 106(2):745a.
42. Li Q, et al. (2014) Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain. Nat Struct Mol Biol 21(3):244-252.
43. Liman ER, Tytgat J, Hess P (1992) Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9(5):861-871.
44. Tetko IV, et al. (2005) Virtual computational chemistry laboratory - design and description. J Comput Aided Mol Des 19(6):453-463. (Pubitemid 41613292)
45. Gonzalez C, Rebolledo S, Perez ME, Larsson HP (2013) Molecular mechanism of voltage sensing in voltage-gated proton channels. J Gen Physiol 141(3):275-285.