The voltage-gated proton channel hv1/vsop inhibits neutrophil granule release

Journal of Leukocyte Biology

Volumn 99, Issue 1, 2016, Pages 7-19

  Okochi, Yoshifumi ^a   Aratani, Yasuaki ^b   Adissu, Hibret A ^c   Miyawaki, Nana ^a   Sasaki, Mari ^a,e   Suzuki, Kazuo ^d,f,g   Okamura, Yasushi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^e LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^f TEIKYO UNIVERSITY   (Japan)

^g CHIBA UNIVERSITY   (Japan)

Author keywords

Inflammation; Proton channel

Indexed keywords

CATALASE; ELASTASE; IMMUNOGLOBULIN G; PROTON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; VOLTAGE GATED PROTON CHAQNNEL HV1; HV1 PROTON CHANNEL, MOUSE; ION CHANNEL; PEROXIDASE; PROTEIN BINDING;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AZUROPHILIC GRANULE; CANDIDIASIS; CELL ACTIVATION; CELL FUNCTION; CELL GRANULE; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOCYTOSIS; GENE; GENE INACTIVATION; HVCN1 GENE; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MOUSE; NEUTROPHIL; NEUTROPHIL GRANULE; NONHUMAN; OXIDATIVE STRESS; PNEUMONIA; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; DEGRANULATION; FEMALE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; MICROBIOLOGY; PATHOLOGY; PROTEIN TRANSPORT; SECRETORY VESICLE;

ANIMALS; CELL DEGRANULATION; CELL MEMBRANE; CYTOPLASMIC GRANULES; EXOCYTOSIS; FEMALE; IMMUNOGLOBULIN G; ION CHANNELS; LUNG; MICE; MICE, KNOCKOUT; NADPH OXIDASE; NEUTROPHILS; PEROXIDASE; PROTEIN BINDING; PROTEIN TRANSPORT; SECRETORY VESICLES;

EID: 84953455582     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3HI0814-393R     Document Type: Article

References (70)

1. Capasso, M., Bhamrah, M. K., Henley, T., Boyd, R. S., Langlais, C., Cain, K., Dinsdale, D., Pulford, K., Khan, M., Musset, B., Cherny, V. V., Morgan, D., Gascoyne, R. D., Vigorito, E., DeCoursey, T. E., MacLennan, I. C., Dyer, M. J. (2010) HVCN1 modulates BCR signal strength via regulation of BCR-dependent generation of reactive oxygen species. Nat. Immunol. 11, 265–272.
2. Sasaki, M., Tojo, A., Okochi, Y., Miyawaki, N., Kamimura, D., Yamaguchi, A., Murakami, M., Okamura, Y. (2013) Autoimmune disorder phenotypes in Hvcn1-deficient mice. Biochem. J. 450, 295–301.
3. Okochi, Y., Sasaki, M., Iwasaki, H., Okamura, Y. (2009) Voltage-gated proton channel is expressed on phagosomes. Biochem. Biophys. Res. Commun. 382, 274–279.
4. El Chemaly, A., Okochi, Y., Sasaki, M., Arnaudeau, S., Okamura, Y., Demaurex, N. (2010) VSOP/Hv1 proton channels sustain calcium entry, neutrophil migration, and superoxide production by limiting cell depolarization and acidification. J. Exp. Med. 207, 129–139.
5. Ramsey, I. S., Ruchti, E., Kaczmarek, J. S., Clapham, D. E. (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, 7642–7647.
6. Fujiwara, Y., Kurokawa, T., Takeshita, K., Kobayashi, M., Okochi, Y., Nakagawa, A., Okamura, Y. (2012) The cytoplasmic coiled-coil mediates cooperative gating temperature sensitivity in the voltage-gated H(+) channel Hv1. Nat. Commun. 3, 816.
7. Koch, H. P., Kurokawa, T., Okochi, Y., Sasaki, M., Okamura, Y., Larsson, H. P. (2008) Multimeric nature of voltage-gated proton channels. Proc. Natl. Acad. Sci. USA 105, 9111–9116.
8. Decoursey, T. E. (2003) Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83, 475–579.
9. Demaurex, N., El Chemaly, A. (2010) Physiological roles of voltage-gated proton channels in leukocytes. J. Physiol. 588, 4659–4665.
10. Okamura, Y. (2012) Voltage-gated proton channels. Comprehensive Biophysics 6.8, 199-222.
11. Nauseef, W. M. (2007) How human neutrophils kill and degrade microbes: an integrated view. Immunol. Rev. 219, 88–102.
12. Faurschou, M., Borregaard, N. (2003) Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5, 1317–1327.
13. Lacy, P. (2006) Mechanisms of degranulation in neutrophils. Allergy Asthma Clin. Immunol. 2, 98–108.
14. Lacy, P. (2005) The role of Rho GTPases and SNAREs in mediator release from granulocytes. Pharmacol. Ther. 107, 358–376.
15. Sengeløv, H., Kjeldsen, L., Borregaard, N. (1993) Control of exocytosis in early neutrophil activation. J. Immunol. 150, 1535–1543.
16. Borregaard, N., Cowland, J. B. (1997) Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89, 3503–3521.
17. Nüsse, O., Serrander, L., Lew, D. P., Krause, K. H. (1998) Ca2+-induced exocytosis in individual human neutrophils: high- and low-affinity granule populations and submaximal responses. EMBO J. 17, 1279–1288.
18. Barrowman, M. M., Cockcroft, S., Gomperts, B. D. (1986) Two roles for guanine nucleotides in the stimulus-secretion sequence of neutrophils. Nature 319, 504–507.
19. Nüsse, O., Lindau, M. (1988) The dynamics of exocytosis in human neutrophils. J. Cell Biol. 107, 2117–2123.
20. Klebanoff, S. J. (2005) Myeloperoxidase: friend and foe. J. Leukoc. Biol. 77, 598–625.
21. Minakami, R., Sumimotoa, H. (2006) Phagocytosis-coupled activation of the superoxide-producing phagocyte oxidase, a member of the NADPH oxidase (nox) family. Int. J. Hematol. 84, 193–198.
22. Reeves, E. P., Lu, H., Jacobs, H. L., Messina, C. G., Bolsover, S., Gabella, G., Potma, E. O., Warley, A., Roes, J., Segal, A. W. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416, 291–297.
23. Klebanoff, S. J., Kettle, A. J., Rosen, H., Winterbourn, C. C., Nauseef, W. M. (2013) Myeloperoxidase: a front-line defender against phagocytosed microorganisms. J. Leukoc. Biol. 93, 185–198.
24. Moraes, T. J., Zurawska, J. H., Downey, G. P. (2006) Neutrophil granule contents in the pathogenesis of lung injury. Curr. Opin. Hematol. 13, 21–27.
25. Soehnlein, O., Lindbom, L. (2010) Phagocyte partnership during the onset and resolution of inflammation. Nat. Rev. Immunol. 10, 427–439.
26. Pham, C. T. (2006) Neutrophil serine proteases: specific regulators of inflammation. Nat. Rev. Immunol. 6, 541–550.
27. DeCoursey, T. E., Morgan, D., Cherny, V. V. (2003) The voltage dependence of NADPH oxidase reveals why phagocytes need proton channels. Nature 422, 531–534.
28. Aratani, Y., Kura, F., Watanabe, H., Akagawa, H., Takano, Y., Suzuki, K., Maeda, N., Koyama, H. (2000) Differential host susceptibility to pulmonary infections with bacteria and fungi in mice deficient in myeloperoxidase. J. Infect. Dis. 182, 1276–1279.
29. Abdel-Latif, D., Steward, M., Macdonald, D. L., Francis, G. A., Dinauer, M. C., Lacy, P. (2004) Rac2 is critical for neutrophil primary granule exocytosis. Blood 104, 832–839.
30. Dypbukt, J. M., Bishop, C., Brooks, W. M., Thong, B., Eriksson, H., Kettle, A. J. (2005) A sensitive and selective assay for chloramine production by myeloperoxidase. Free Radic. Biol. Med. 39, 1468–1477.
31. Krawisz, J. E., Sharon, P., Stenson, W. F. (1984) Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87, 1344–1350.
32. Mócsai, A., Ligeti, E., Lowell, C. A., Berton, G. (1999) Adhesiondependent degranulation of neutrophils requires the Src family kinases Fgr and Hck. J. Immunol. 162, 1120–1126.
33. Xu, H., Ploplis, V. A., Castellino, F. J. (2006) A coagulation factor VII deficiency protects against acute inflammatory responses in mice. J. Pathol. 210, 488–496.
34. Cannon, G. J., Swanson, J. A. (1992) The macrophage capacity for phagocytosis. J. Cell Sci. 101, 907–913.
35. Yong, E. C., Chi, E. Y., Chen, W. J., Kuo, C. C. (1986) Degradation of Chlamydia trachomatis in human polymorphonuclear leukocytes: an ultrastructural study of peroxidase-positive phagolysosomes. Infect. Immun. 53, 427–431.
36. Sato, T. (1968) A modified method for lead staining of thin sections. J. Electron Microsc. (Tokyo) 17, 158–159.
37. Odajima, T., Yamazaki, I. (1970) Myeloperoxidase of the leukocyte of normal blood. I. Reaction of myeloperoxidase with hydrogen peroxide. Biochim. Biophys. Acta 206, 71–77.
38. Rosenberger, C. M., Gallo, R. L., Finlay, B. B. (2004) Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc. Natl. Acad. Sci. USA 101, 2422–2427.
39. Petheo, G. L., Orient, A., Baráth, M., Kovács, I., Réthi, B., Lányi, A., Rajki, A., Rajnavölgyi, E., Geiszt, M. (2010) Molecular and functional characterization of Hv1 proton channel in human granulocytes. PLoS One 5, e14081.
40. Kobayashi, T., Robinson, J. M., Seguchi, H. (1998) Identification of intracellular sites of superoxide production in stimulated neutrophils. J. Cell Sci. 111, 81–91.
41. Takeshita, K., Sakata, S., Yamashita, E., Fujiwara, Y., Kawanabe, A., Kurokawa, T., Okochi, Y., Matsuda, M., Narita, H., Okamura, Y., Nakagawa, A. (2014) X-ray crystal structure of voltage-gated proton channel. Nat. Struct. Mol. Biol. 21, 352–357.
42. Marinho, H. S., Real, C., Cyrne, L., Soares, H., Antunes, F. (2014) Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2, 535–562.
43. Hattori, H., Subramanian, K. K., Sakai, J., Jia, Y., Li, Y., Porter, T. F., Loison, F., Sarraj, B., Kasorn, A., Jo, H., Blanchard, C., Zirkle, D., McDonald, D., Pai, S. Y., Serhan, C. N., Luo, H. R. (2010) Small-molecule screen identifies reactive oxygen species as key regulators of neutrophil chemotaxis. Proc. Natl. Acad. Sci. USA 107, 3546–3551.
44. Canton, J., Khezri, R., Glogauer, M., Grinstein, S. (2014) Contrasting phagosome pH regulation and maturation in human M1 and M2 macrophages. Mol. Biol. Cell 25, 3330–3341.
45. Nishikimi, A., Fukuhara, H., Su, W., Hongu, T., Takasuga, S., Mihara, H., Cao, Q., Sanematsu, F., Kanai, M., Hasegawa, H., Tanaka, Y., Shibasaki, M., Kanaho, Y., Sasaki, T., Frohman, M. A., Fukui, Y. (2009) Sequential regulation of DOCK2 dynamics by two phospholipids during neutrophil chemotaxis. Science 324, 384–387.
46. Bréchard, S., Tschirhart, E. J. (2008) Regulation of superoxide production in neutrophils: role of calcium influx. J. Leukoc. Biol. 84, 1223–1237.
47. Korchak, H. M., Vienne, K., Rutherford, L. E., Wilkenfeld, C., Finkelstein, M. C., Weissmann, G. (1984) Stimulus response coupling in the human neutrophil. II. Temporal analysis of changes in cytosolic calcium and calcium efflux. J. Biol. Chem. 259, 4076–4082.
48. Eng, E. W., Bettio, A., Ibrahim, J., Harrison, R. E. (2007) MTOC reorientation occurs during FcgammaR-mediated phagocytosis in macrophages. Mol. Biol. Cell 18, 2389–2399.
49. Aratani, Y., Koyama, H., Nyui, S., Suzuki, K., Kura, F., Maeda, N. (1999) Severe impairment in early host defense against Candida albicans in mice deficient in myeloperoxidase. Infect. Immun. 67, 1828–1836.
50. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173–182.
51. Sasaki, M., Takagi, M., Okamura, Y. (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312, 589–592.
52. Ramsey, I. S., Moran, M. M., Chong, J. A., Clapham, D. E. (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440, 1213–1216.
53. Li, S., Yamauchi, A., Marchal, C. C., Molitoris, J. K., Quilliam, L. A., Dinauer, M. C. (2002) Chemoattractant-stimulated Rac activation in wildtype and Rac2-deficient murine neutrophils: preferential activation of Rac2 and Rac2 gene dosage effect on neutrophil functions. J. Immunol. 169, 5043–5051.
54. Mollapour, E., Linch, D. C., Roberts, P. J. (2001) Activation and priming of neutrophil nicotinamide adenine dinucleotide phosphate oxidase and phospholipase A(2) are dissociated by inhibitors of the kinases p42 (ERK2) and p38(SAPK) and by methyl arachidonyl fluorophosphonate, the dual inhibitor of cytosolic and calcium-independent phospholipase A (2). Blood 97, 2469–2477.
55. Kunisaki, Y., Nishikimi, A., Tanaka, Y., Takii, R., Noda, M., Inayoshi, A., Watanabe, K., Sanematsu, F., Sasazuki, T., Sasaki, T., Fukui, Y. (2006) DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis. J. Cell Biol. 174, 647–652.
56. Mitchell, T., Lo, A., Logan, M. R., Lacy, P., Eitzen, G. (2008) Primary granule exocytosis in human neutrophils is regulated by Rac-dependent actin remodeling. Am. J. Physiol. Cell Physiol. 295, C1354–C1365.
57. Kim, C., Dinauer, M. C. (2001) Rac2 is an essential regulator of neutrophil nicotinamide adenine dinucleotide phosphate oxidase activation in response to specific signaling pathways. J. Immunol. 166, 1223–1232.
58. García-García, E., Rosales, C. (2002) Signal transduction during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 72, 1092–1108.
59. Burgoyne, R. D., Morgan, A. (2003) Secretory granule exocytosis. Physiol. Rev. 83, 581–632.
60. Di Virgilio, F., Lew, D. P., Pozzan, T. (1984) Protein kinase C activation of physiological processes in human neutrophils at vanishingly small cytosolic Ca2+ levels. Nature 310, 691–693.
61. Reth, M. (2002) Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 3, 1129–1134.
62. Yamauchi, A., Marchal, C. C., Molitoris, J., Pech, N., Knaus, U., Towe, J., Atkinson, S. J., Dinauer, M. C. (2005) Rac GTPase isoform-specific regulation of NADPH oxidase and chemotaxis in murine neutrophils in vivo. Role of the C-terminal polybasic domain. J. Biol. Chem. 280, 953–964.
63. Ueyama, T., Eto, M., Kami, K., Tatsuno, T., Kobayashi, T., Shirai, Y., Lennartz, M. R., Takeya, R., Sumimoto, H., Saito, N. (2005) Isoformspecific membrane targeting mechanism of Rac during Fc gamma Rmediated phagocytosis: positive charge-dependent and independent targeting mechanism of Rac to the phagosome. J. Immunol. 175, 2381–2390.
64. Hawkins, M., Pope, B., Maciver, S. K., Weeds, A. G. (1993) Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry 32, 9985–9993.
65. Tang, W., Zhang, Y., Xu, W., Harden, T. K., Sondek, J., Sun, L., Li, L., Wu, D. (2011) A PLCb/PI3Kg-GSK3 signaling pathway regulates cofilin phosphatase slingshot2 and neutrophil polarization and chemotaxis. Dev. Cell 21, 1038–1050.
66. Heyworth, P. G., Robinson, J. M., Ding, J., Ellis, B. A., Badwey, J. A. (1997) Cofilin undergoes rapid dephosphorylation in stimulated neutrophils and translocates to ruffled membranes enriched in products of the NADPH oxidase complex. Evidence for a novel cycle of phosphorylation and dephosphorylation. Histochem. Cell Biol. 108, 221–233.
67. Sun, C. X., Magalhães, M. A., Glogauer, M. (2007) Rac1 and Rac2 differentially regulate actin free barbed end formation downstream of the fMLP receptor. J. Cell Biol. 179, 239–245.
68. Frantz, C., Barreiro, G., Dominguez, L., Chen, X., Eddy, R., Condeelis, J., Kelly, M. J., Jacobson, M. P., Barber, D. L. (2008) Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding. J. Cell Biol. 183, 865–879.
69. Tkalcevic, J., Novelli, M., Phylactides, M., Iredale, J. P., Segal, A. W., Roes, J. (2000) Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 12, 201–210.
70. Korkmaz, B., Horwitz, M. S., Jenne, D. E., Gauthier, F. (2010) Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol. Rev. 62, 726–759.