Calcium influx, a new potential therapeutic target in the control of neutrophil-dependent inflammatory diseases in bovines

Veterinary Immunology and Immunopathology

Volumn 143, Issue 1-2, 2011, Pages 1-10

  Burgos, R A ^a   Conejeros, I ^a   Hidalgo, M A ^a   Werling, D ^b   Hermosilla, C ^b  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Bovine; Calcium channel; Inflammation; Neutrophils; SOCE

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; CALCIUM; FLUFENAMIC ACID; THAPSIGARGIN;

ACIDIFICATION; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CATTLE; CELL FUNCTION; CELL MEMBRANE; CELL TRANSPORT; COW; DEGRANULATION; DRUG INHIBITION; INFLAMMATORY DISEASE; LEUKOCYTE ACTIVATION; LUNG CONGESTION; NEUTROPHIL; NONHUMAN; PH; RESPIRATORY BURST; RESPIRATORY DISTRESS; REVIEW; STORE OPERATED CALCIUM ENTRY CHANNEL;

ANIMALS; CALCIUM SIGNALING; CATTLE; CATTLE DISEASES; CELL DEGRANULATION; FEMALE; HYDROGEN-ION CONCENTRATION; INFLAMMATION; MALE; MODELS, BIOLOGICAL; NEUTROPHIL ACTIVATION; NEUTROPHILS; RESPIRATORY BURST;

BOVINAE;

EID: 79961021531     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2011.05.037     Document Type: Review

References (141)

1. Guide to Receptors and Channels (GRAC), 2009. 4th ed. Br. J. Pharmacol. 158 (Suppl. 1), S1-S254.
2. Abbot N.C., Spence V.A., Swanson-Beck J., Carnochan F.M., Gibbs J.H., Lowe J.G. Assessment of the respiratory metabolism in the skin from transcutaneous measurements of pO2 and pCO2: potential for non-invasive monitoring of response to tuberculin skin testing. Tubercle 1990, 71:15-22.
3. Allard B., Long E., Block E., Zhao X. Dependence of superoxide anion production on extracellular and intracellular calcium ions and protein kinase C in PMA-stimulated bovine neutrophils. Can. J. Vet. Res. 1999, 63:13-17.
4. Anderson B.H., Watson D.L., Colditz I.G. The effect of dexamethasone on some immunological parameters in cattle. Vet. Res. Commun. 1999, 23:399-413.
5. Baggiolini M., Horisberger U., Gennaro R., Dewald B. Identification of three types of granules in neutrophils of ruminants. Ultrastructure of circulating and maturing cells. Lab. Invest. 1985, 52:151-158.
6. Bankers-Fulbright J.L., Kephart G.M., Bartemes K.R., Kita H., O'Grady S.M. Platelet-activating factor stimulates cytoplasmic alkalinization and granule acidification in human eosinophils. J. Cell Sci. 2004, 117:5749-5757.
7. Behrendt J.H., Ruiz A., Zahner H., Taubert A., Hermosilla C. Neutrophil extracellular trap formation as innate immune reactions against the apicomplexan parasite Eimeria bovis. Vet. Immunol. Immunopathol. 2010, 133:1-8.
8. Bergamini C.M., Gambetti S., Dondi A., Cervellati C. Oxygen, reactive oxygen species and tissue damage. Curr. Pharm. Des. 2004, 10:1611-1626.
9. Berridge M.J. Capacitative calcium entry. Biochem. J 1995, 312(Pt 1):1-11.
10. Borregaard N. Development of neutrophil granule diversity. Ann. N. Y. Acad. Sci. 1997, 832:62-68.
11. Borregaard N., Kjeldsen L., Lollike K., Sengelov H. Granules and secretory vesicles of the human neutrophil. Clin. Exp. Immunol. 1995, 1(Suppl. 101):6-9.
12. Borregaard N., Schwartz J.H., Tauber A.I. Proton secretion by stimulated neutrophils. Significance of hexose monophosphate shunt activity as source of electrons and protons for the respiratory burst. J. Clin. Invest. 1984, 74:455-459.
13. Borregaard N., Sorensen O.E., Theilgaard-Monch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007, 28:340-345.
14. Boulay F., Naik N., Giannini E., Tardif M., Brouchon L. Phagocyte chemoattractant receptors. Ann. N. Y. Acad. Sci. 1997, 832:69-84.
15. Brechard S., Melchior C., Plancon S., Schenten V., Tschirhart E.J. Store-operated Ca2+ channels formed by TRPC1, TRPC6 and Orai1 and non-store-operated channels formed by TRPC3 are involved in the regulation of NADPH oxidase in HL-60 granulocytes. Cell Calcium 2008, 44:492-506.
16. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
17. Brinkmann V., Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 2007, 5:577-582.
18. Brown G.E., Stewart M.Q., Bissonnette S.A., Elia A.E., Wilker E., Yaffe M.B. Distinct ligand-dependent roles for p38 MAPK in priming and activation of the neutrophil NADPH oxidase. J. Biol. Chem. 2004, 279:27059-27068.
19. Brunkhorst B.A., Kraus E., Coppi M., Budnick M., Niederman R. Propionate induces polymorphonuclear leukocyte activation and inhibits formylmethionyl-leucyl-phenylalanine-stimulated activation. Infect. Immun. 1992, 60:2957-2968.
20. Burgos R.A., Hidalgo M.A., Figueroa C.D., Conejeros I., Hancke J.L. New potential targets to modulate neutrophil function in inflammation. Mini Rev. Med. Chem. 2009, 9:153-168.
21. Burlacu A., Jinga V., Gafencu A.V., Simionescu M. Severity of oxidative stress generates different mechanisms of endothelial cell death. Cell Tissue Res. 2001, 306:409-416.
22. Chand N., Eyre P. Nonsteroidal anti-inflammatory drugs: a review. New applications in hypersensitivity reactions of cattle and horses. Can. J. Comp. Med. 1977, 41:233-240.
23. Chang L.C., Madsen S.A., Toelboell T., Weber P.S., Burton J.L. Effects of glucocorticoids on Fas gene expression in bovine blood neutrophils. J. Endocrinol. 2004, 183:569-583.
24. Conejeros I., Jara E., Carretta M.D., Alarcon P., Hidalgo M.A., Burgos R.A. 2-Aminoethoxydiphenyl borate (2-APB) reduces respiratory burst, MMP-9 release and CD11b expression, and increases l-selectin shedding in bovine neutrophils. Res. Vet. Sci. 2010.
25. Conejeros I., Patterson R., Burgos R.A., Hermosilla C., Werling D. Induction of reactive oxygen species in bovine neutrophils is CD11b, but not dectin-1-dependent. Vet. Immunol. Immunopathol. 2011, 139:308-312.
26. Corl C.M., Gandy J.C., Sordillo L.M. Platelet activating factor production and proinflammatory gene expression in endotoxin-challenged bovine mammary endothelial cells. J. Dairy Sci. 2008, 91:3067-3078.
27. Coverdale J.A., Tyler H.D., Quigley J.D., Brumm J.A. Effect of various levels of forage and form of diet on rumen development and growth in calves. J. Dairy Sci. 2004, 87:2554-2562.
28. Cox G. Glucocorticoid treatment inhibits apoptosis in human neutrophils. Separation of survival and activation outcomes. J. Immunol. 1995, 154:4719-4725.
29. Cudd L., Clarke C., Clinkenbeard K., Shelton M., Clinkenbeard P., Murphy G. Role of intracellular calcium in Pasteurella haemolytica leukotoxin-induced bovine neutrophil leukotriene B4 production and plasma membrane damage. FEMS Microbiol. Lett. 1999, 172:123-129.
30. Daffern P.J., Jagels M.A., Hugli T.E. Multiple epithelial cell-derived factors enhance neutrophil survival. Regulation by glucocorticoids and tumor necrosis factor-alpha. Am. J. Respir. Cell Mol. Biol. 1999, 21:259-267.
31. Dahlgren C., Johansson A., Lundqvist H., Bjerrum O.W., Borregaard N. Activation of the oxygen-radical-generating system in granules of intact human neutrophils by a calcium ionophore (ionomycin). Biochimica et Biophysica Acta (BBA) Molecular Cell Research 1992, 1137:182-188.
32. Dale M.M., Penfield A. Synergism between phorbol ester and A23187 in superoxide production by neutrophils. FEBS Lett. 1984, 175:170-172.
33. Dang P.M., Stensballe A., Boussetta T., Raad H., Dewas C., Kroviarski Y., Hayem G., Jensen O.N., Gougerot-Pocidalo M.A., El-Benna J. A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J. Clin. Invest. 2006, 116:2033-2043.
34. De Vito P. The sodium/hydrogen exchanger: a possible mediator of immunity. Cell. Immunol. 2006, 240:69-85.
35. DeChatelet L.R., Lees C.J., Walsh C.E., Long G.D., Shirley P.S. Comparison of the calcium ionophore and phorbol myristate acetate on the initiation of the respiratory burst in human neutrophils. Infect. Immun. 1982, 38:969-974.
36. DeHaven W.I., Smyth J.T., Boyles R.R., Bird G.S., Putney J.W. Complex actions of 2-aminoethyldiphenyl borate on store-operated calcium entry. J. Biol. Chem. 2008, 283:19265-19273.
37. Demaurex N., Lew D.P., Krause K.H. Cyclopiazonic acid depletes intracellular Ca2+ stores and activates an influx pathway for divalent cations in HL-60 cells. J. Biol. Chem. 1992, 267:2318-2324.
38. Dore M., Slauson D.O., Suyemoto M.M., Neilsen N.R. Calcium mobilization in C5a-stimulated adult and newborn bovine neutrophils. Inflammation 1990, 14:71-82.
39. Downey G.P., Fukushima T., Fialkow L., Waddell T.K. Intracellular signaling in neutrophil priming and activation. Semin. Cell Biol. 1995, 6:345-356.
40. Edlow D.W., Sheldon W.H. The pH of inflammatory exudates. Proc. Soc. Exp. Biol. Med. 1971, 137:1328-1332.
41. El-Benna J., Dang P.M., Gougerot-Pocidalo M.A. Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin. Immunopathol. 2008, 30:279-289.
42. El-Benna J., Dang P.M., Gougerot-Pocidalo M.A., Elbim C. Phagocyte NADPH oxidase: a multicomponent enzyme essential for host defenses. Arch. Immunol. Ther. Exp. (Warsz) 2005, 53:199-206.
43. Faurschou M., Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 2003, 5:1317-1327.
44. Foyouzi-Youssefi R., Petersson F., Lew D.P., Krause K.H., Nusse O. Chemoattractant-induced respiratory burst: increases in cytosolic Ca2+ concentrations are essential and synergize with a kinetically distinct second signal. Biochem. J 1997, 322(Pt 3):709-718.
45. Fuchs T.A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., Weinrauch Y., Brinkmann V., Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007, 176:231-241.
46. Fukushima T., Waddell T.K., Grinstein S., Goss G.G., Orlowski J., Downey G.P. Na+/H+ exchange activity during phagocytosis in human neutrophils: role of Fc gamma receptors and tyrosine kinases. J. Cell Biol. 1996, 132:1037-1052.
47. Gallois A., Bueb J.L., Tschirhart E. Effect of SK&F 96365 on extracellular Ca2+-dependent O2-production in neutrophil-like HL-60 cells. Eur. J. Pharmacol. 1998, 361:293-298.
48. Gende O.A. Capacitative calcium influx and intracellular pH cross-talk in human platelets. Platelets 2003, 14:9-14.
49. Gennaro R., Dewald B., Horisberger U., Gubler H.U., Baggiolini M. A novel type of cytoplasmic granule in bovine neutrophils. J. Cell Biol. 1983, 96:1651-1661.
50. Granfeldt D., Samuelsson M., Karlsson A. Capacitative Ca2+ influx and activation of the neutrophil respiratory burst. Different regulation of plasma membrane- and granule-localized NADPH-oxidase. J. Leukoc. Biol. 2002, 71:611-617.
51. Grimshaw M.J., Balkwill F.R. Inhibition of monocyte and macrophage chemotaxis by hypoxia and inflammation-a potential mechanism. Eur. J. Immunol. 2001, 31:480-489.
52. Gupta A.K., Joshi M.B., Philippova M., Erne P., Hasler P., Hahn S., Resink T.J. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett. 2010, 584:3193-3197.
53. Hallett M.B., Davies E.V., Campbell A.K. Oxidase activation in individual neutrophils is dependent on the onset and magnitude of the Ca2+ signal. Cell Calcium 1990, 11:655-663.
54. Hallett M.B., Lloyds D. Neutrophil priming: the cellular signals that say 'amber' but not 'green'. Immunol. Today 1995, 16:264-268.
55. Hauser C.J., Fekete Z., Adams J.M., Garced M., Livingston D.H., Deitch E.A. PAF-mediated Ca2+ influx in human neutrophils occurs via store-operated mechanisms. J. Leukoc. Biol. 2001, 69:63-68.
56. He L.P., Hewavitharana T., Soboloff J., Spassova M.A., Gill D.L. A functional link between store-operated and TRPC channels revealed by the 3,5-bis(trifluoromethyl)pyrazole derivative, BTP2. J. Biol. Chem. 2005, 280:10997-11006.
57. Heiner I., Eisfeld J., Halaszovich C.R., Wehage E., Jungling E., Zitt C., Luckhoff A. Expression profile of the transient receptor potential (TRP) family in neutrophil granulocytes: evidence for currents through long TRP channel 2 induced by ADP-ribose and NAD. Biochem. J 2003, 371:1045-1053.
58. Heiner I., Eisfeld J., Luckhoff A. Role and regulation of TRP channels in neutrophil granulocytes. Cell Calcium 2003, 33:533-540.
59. Heiner I., Eisfeld J., Warnstedt M., Radukina N., Jungling E., Luckhoff A. Endogenous ADP-ribose enables calcium-regulated cation currents through TRPM2 channels in neutrophil granulocytes. Biochem. J 2006, 398:225-232.
60. Heiner I., Radukina N., Eisfeld J., Kuhn F., Luckhoff A. Regulation of TRPM2 channels in neutrophil granulocytes by ADP-ribose: a promising pharmacological target. Naunyn. Schmiedebergs Arch. Pharmacol. 2005, 371:325-333.
61. Hidalgo M.A., Ojeda F., Eyre P., LaBranche T.P., Smith C., Hancke J.L., Burgos R.A. Platelet-activating factor increases pH(i) in bovine neutrophils through the PI3K-ERK1/2 pathway. Br. J. Pharmacol. 2004, 141:311-321.
62. Hill A.W., Frost A.J., Brooker B.E. Progressive pathology of severe Escherichia coli mastitis in dairy cows. Res. Vet. Sci. 1984, 37:179-187.
63. Hsuan S.L., Kannan M.S., Jeyaseelan S., Prakash Y.S., Sieck G.C., Maheswaran S.K. Pasteurella haemolytica A1-derived leukotoxin and endotoxin induce intracellular calcium elevation in bovine alveolar macrophages by different signaling pathways. Infect. Immun. 1998, 66:2836-2844.
64. Itagaki K., Hauser C.J. Sphingosine 1-phosphate, a diffusible calcium influx factor mediating store-operated calcium entry. J. Biol. Chem. 2003, 278:27540-27547.
65. Itagaki K., Kannan K.B., Livingston D.H., Deitch E.A., Fekete Z., Hauser C.J. Store-operated calcium entry in human neutrophils reflects multiple contributions from independently regulated pathways. J. Immunol. 2002, 168:4063-4069.
66. Itagaki K., Kannan K.B., Singh B.B., Hauser C.J. Cytoskeletal reorganization internalizes multiple transient receptor potential channels and blocks calcium entry into human neutrophils. J. Immunol. 2004, 172:601-607.
67. Kankaanranta H., Moilanen E. Flufenamic and tolfenamic acids inhibit calcium influx in human polymorphonuclear leukocytes. Mol. Pharmacol. 1995, 47:1006-1013.
68. Kankaanranta H., Moilanen E., Lindberg K., Vapaatalo H. Pharmacological control of human polymorphonuclear leukocyte degranulation by fenamates and inhibitors of receptor-mediated calcium entry and protein kinase C. Biochem. Pharmacol. 1995, 50:197-203.
69. Kim J.H., Suk M.H., Yoon D.W., Lee S.H., Hur G.Y., Jung K.H., Jeong H.C., Lee S.Y., Lee S.Y., Suh I.B., Shin C., Shim J.J., In K.H., Yoo S.H., Kang K.H. Inhibition of matrix metalloproteinase-9 prevents neutrophilic inflammation in ventilator-induced lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 2006, 291:L580-587.
70. Kirchberger T., Moreau C., Wagner G.K., Fliegert R., Siebrands C.C., Nebel M., Schmid F., Harneit A., Odoardi F., Flugel A., Potter B.V., Guse A.H. 8-Bromo-cyclic inosine diphosphoribose: towards a selective cyclic ADP-ribose agonist. Biochem. J 2009, 422:139-149.
71. Konig T., Schuberth H.J., Leibold W., Zerbe H. Dexamethasone depresses the expression of l-selectin but not the in vivo migration of bovine neutrophils into the uterus. Theriogenology 2006, 65:1227-1241.
72. Kopaniak M.M., Issekutz A.C., Movat H.Z. Kinetics of acute inflammation induced by E. coli in rabbits. Quantitation of blood flow, enhanced vascular permeability, hemorrhage, and leukocyte accumulation. Am. J. Pathol. 1980, 98:485-498.
73. Krautwurst D., Seifert R., Hescheler J., Schultz G. Formyl peptides and ATP stimulate Ca2+ and Na+ inward currents through non-selective cation channels via G-proteins in dibutyryl cyclic AMP-differentiated HL-60 cells. Involvement of Ca2+ and Na+ in the activation of beta-glucuronidase release and superoxide production. Biochem. J 1992, 288(Pt 3):1025-1035.
74. Lardner A. The effects of extracellular pH on immune function. J. Leukoc. Biol. 2001, 69:522-530.
75. Le Poul E., Loison C., Struyf S., Springael J.Y., Lannoy V., Decobecq M.E., Brezillon S., Dupriez V., Vassart G., Van Damme J., Parmentier M., Detheux M. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 2003, 278:25481-25489.
76. Leung Y.M., Kwan C.Y. Current perspectives in the pharmacological studies of store-operated Ca2+ entry blockers. Jpn. J. Pharmacol. 1999, 81:253-258.
77. Lew P.D., Monod A., Waldvogel F.A., Dewald B., Baggiolini M., Pozzan T. Quantitative analysis of the cytosolic free calcium dependency of exocytosis from three subcellular compartments in intact human neutrophils. J. Cell Biol. 1986, 102:2197-2204.
78. Li S., Westwick J., Cox B., Poll C.T. TRP channels as drug targets. Novartis Found. Symp. 2004, 258:204-213. discussion 213-221, 263-206.
79. Li S.W., Westwick J., Poll C.T. Receptor-operated Ca2+ influx channels in leukocytes: a therapeutic target?. Trends Pharmacol. Sci. 2002, 23:63-70.
80. Lippolis J.D., Reinhardt T.A., Goff J.P., Horst R.L. Neutrophil extracellular trap formation by bovine neutrophils is not inhibited by milk. Vet. Immunol. Immunopathol. 2006, 113:248-255.
81. Madsen-Bouterse S.A., Rosa G.J., Burton J.L. Glucocorticoid modulation of Bcl-2 family members A1 and Bak during delayed spontaneous apoptosis of bovine blood neutrophils. Endocrinology 2006, 147:3826-3834.
82. Mahomed A.G., Anderson R. Activation of human neutrophils with chemotactic peptide, opsonized zymosan and the calcium ionophore A23187, but not with a phorbol ester, is accompanied by efflux and store-operated influx of calcium. Inflammation 2000, 24:559-569.
83. Martin-Requero A., Daza F.J., Hermida O.G., Butta N., Parrilla R. Role of Ca2+ and protein kinase C in the receptor-mediated activation of Na+/H+ exchange in isolated liver cells. Biochem. J 1997, 325(Pt 3):631-636.
84. McClenahan D., Fagliari J., Evanson O., Weiss D. Role of inflammatory mediators in priming, activation, and deformability of bovine neutrophils. Am. J. Vet. Res. 2000, 61:492-498.
85. McClenahan D.J., Evanson O.A., Weiss D.J. In vitro evaluation of the role of platelet-activating factor and interleukin-8 in Mannheimia haemolytica-induced bovine pulmonary endothelial cell injury. Am. J. Vet. Res. 2002, 63:394-401.
86. McClenahan D.J., Fagliari J.J., Evanson O.A., Weiss D.J. Role of platelet-activating factor in alveolar septal injury associated with experimentally induced pneumonic pasteurellosis in calves. Am. J. Vet. Res. 2000, 61:248-254.
87. McMeekin S.R., Dransfield I., Rossi A.G., Haslett C., Walker T.R. E-selectin permits communication between PAF receptors and TRPC channels in human neutrophils. Blood 2006, 107:4938-4945.
88. Merritt J.E., Armstrong W.P., Benham C.D., Hallam T.J., Jacob R., Jaxa-Chamiec A., Leigh B.K., McCarthy S.A., Moores K.E., Rink T.J. SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem. J 1990, 271:515-522.
89. Mitchell G.B., Al-Haddawi M.H., Clark M.E., Beveridge J.D., Caswell J.L. Effect of corticosteroids and neuropeptides on the expression of defensins in bovine tracheal epithelial cells. Infect. Immun. 2007, 75:1325-1334.
90. Monk P.N., Partridge L.J. Characterization of a complement-fragment-C5a-stimulated calcium-influx mechanism in U937 monocytic cells. Biochem. J 1993, 295(Pt 3):679-684.
91. Moraes T.J., Zurawska J.H., Downey G.P. Neutrophil granule contents in the pathogenesis of lung injury. Curr. Opin. Hematol. 2006, 13:21-27.
92. Muroski M.E., Roycik M.D., Newcomer R.G., Van den Steen P.E., Opdenakker G., Monroe H.R., Sahab Z.J., Sang Q.X. Matrix metalloproteinase-9/gelatinase B is a putative therapeutic target of chronic obstructive pulmonary disease and multiple sclerosis. Curr. Pharm. Biotechnol. 2008, 9:34-46.
93. Nagahata H., Higuchi H., Inanami O., Kuwabara M. Costimulatory effects of complement receptor type 3 and Fc receptor for IgG (FcgammaR) on superoxide production and signal transduction in bovine neutrophils. J. Vet. Med. Sci. 2007, 69:993-997.
94. Nagaji J. The role of protein kinase C and [Ca2+]i in superoxide anion synthesis and myeloperoxidase degranulation of human neutrophils. Kurume Med. J. 1999, 46:157-162.
95. Nakao S., Fujii A., Niederman R. Alteration of cytoplasmic Ca2+ in resting and stimulated human neutrophils by short-chain carboxylic acids at neutral pH. Infect. Immun. 1992, 60:5307-5311.
96. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 2006, 6:173-182.
97. Niessen H.W., Kuijpers T.W., Roos D., Verhoeven A.J. Release of azurophilic granule contents in fMLP-stimulated neutrophils requires two activation signals, one of which is a rise in cytosolic free Ca2+. Cell. Signal. 1991, 3:625-633.
98. Ortiz-Carranza O., Czuprynski C.J. Activation of bovine neutrophils by Pasteurella haemolytica leukotoxin is calcium dependent. J. Leukoc. Biol. 1992, 52:558-564.
99. Osaki M., Sumimoto H., Takeshige K., Cragoe E.J., Hori Y., Minakami S. Na+/H+ exchange modulates the production of leukotriene B4 by human neutrophils. Biochem. J 1989, 257:751-758.
100. Palić D., Andreasen C.B., Ostojić J., Tell R.M., Roth J.A. Zebrafish (Danio rerio) whole kidney assays to measure neutrophil extracellular trap release and degranulation of primary granules. J. Immunol. Methods 2007, 319:87-97.
101. Parekh A.B., Putney J.W. Store-operated calcium channels. Physiol. Rev. 2005, 85:757-810.
102. Patterson R.L., van Rossum D.B., Gill D.L. Store-operated Ca2+ entry: evidence for a secretion-like coupling model. Cell 1999, 98:487-499.
103. Perraud A.L., Fleig A., Dunn C.A., Bagley L.A., Launay P., Schmitz C., Stokes A.J., Zhu Q., Bessman M.J., Penner R., Kinet J.P., Scharenberg A.M. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 2001, 411:595-599.
104. Plaizier J.C., Krause D.O., Gozho G.N., McBride B.W. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. Vet. J. 2008, 176:21-31.
105. Putney J.W. Pharmacology of capacitative calcium entry. Mol. Interventions 2001, 1:84-94.
106. Rausch P.G., Moore T.G. Granule enzymes of polymorphonuclear neutrophils: a phylogenetic comparison. Blood 1975, 46:913-919.
107. Richter J., Olsson I., Andersson T. Correlation between spontaneous oscillations of cytosolic free Ca2+ and tumor necrosis factor-induced degranulation in adherent human neutrophils. J. Biol. Chem. 1990, 265:14358-14363.
108. Robinson J.M., Badwey J.A., Karnovsky M.L., Karnovsky M.J. Superoxide release by neutrophils: synergistic effects of a phorbol ester and a calcium ionophore. Biochem. Biophys. Res. Commun. 1984, 122:734-739.
109. Roos A., Boron W.F. Intracellular pH. Physiol. Rev. 1981, 61:296-434.
110. Rotstein O.D., Nasmith P.E., Grinstein S. The Bacteroides by-product succinic acid inhibits neutrophil respiratory burst by reducing intracellular pH. Infect. Immun. 1987, 55:864-870.
111. Rotstein O.D., Vittorini T., Kao J., McBurney M.I., Nasmith P.E., Grinstein S. A soluble Bacteroides by-product impairs phagocytic killing of Escherichia coli by neutrophils. Infect. Immun. 1989, 57:745-753.
112. Ryter S.W., Kim H.P., Hoetzel A., Park J.W., Nakahira K., Wang X., Choi A.M. Mechanisms of cell death in oxidative stress. Antioxid. Redox Signal. 2007, 9:49-89.
113. Salmon M.D., Ahluwalia J. Discrimination between receptor- and store-operated Ca(2+) influx in human neutrophils. Cell. Immunol. 2010, 265:1-5.
114. Sandoval A., Trivinos F., Sanhueza A., Carretta D., Hidalgo M.A., Hancke J.L., Burgos R.A. Propionate induces pH((i)) changes through calcium flux, ERK1/2, p38, and PKC in bovine neutrophils. Vet. Immunol. Immunopathol. 2007, 115:286-298.
115. Sandoval A.J., Riquelme J.P., Carretta M.D., Hancke J.L., Hidalgo M.A., Burgos R.A. Store-operated calcium entry mediates intracellular alkalinization, ERK1/2, and Akt/PKB phosphorylation in bovine neutrophils. J. Leukoc. Biol. 2007, 82:1266-1277.
116. Schaff U.Y., Yamayoshi I., Tse T., Griffin D., Kibathi L., Simon S.I. Calcium flux in neutrophils synchronizes beta2 integrin adhesive and signaling events that guide inflammatory recruitment. Ann. Biomed. Eng. 2008, 36:632-646.
117. Schorr W., Swandulla D., Zeilhofer H.U. Mechanisms of IL-8-induced Ca2+ signaling in human neutrophil granulocytes. Eur. J. Immunol. 1999, 29:897-904.
118. Segal A.W. How neutrophils kill microbes. Annu. Rev. Immunol. 2005, 23:197-223.
119. Sengelov H., Kjeldsen L., Borregaard N. Control of exocytosis in early neutrophil activation. J. Immunol. 1993, 150:1535-1543.
120. Simchowitz L. Chemotactic factor-induced activation of Na+/H+ exchange in human neutrophils. II. Intracellular pH changes. J. Biol. Chem. 1985, 260:13248-13255.
121. Simchowitz L., Cragoe E.J. Regulation of human neutrophil chemotaxis by intracellular pH. J. Biol. Chem. 1986, 261:6492-6500.
122. Simmen H.P., Blaser J. Analysis of pH and pO2 in abscesses, peritoneal fluid, and drainage fluid in the presence or absence of bacterial infection during and after abdominal surgery. Am. J. Surg. 1993, 166:24-27.
123. Smith J.A. Neutrophils, host defense, and inflammation: a double-edged sword. J. Leukoc. Biol. 1994, 56:672-686.
124. Smyth J.T., Dehaven W.I., Jones B.F., Mercer J.C., Trebak M., Vazquez G., Putney J.W. Emerging perspectives in store-operated Ca2+ entry: roles of Orai, Stim and TRP. Biochim. Biophys. Acta 2006, 1763:1147-1160.
125. Starkus J., Beck A., Fleig A., Penner R. Regulation of TRPM2 by extra- and intracellular calcium. J. Gen. Physiol. 2007, 130:427-440.
126. Stehle H.W., Leblebicioglu B., Walters J.D. Short-chain carboxylic acids produced by gram-negative anaerobic bacteria can accelerate or delay polymorphonuclear leukocyte apoptosis in vitro. J. Periodontol. 2001, 72:1059-1063.
127. Steinckwich N., Frippiat J.P., Stasia M.J., Erard M., Boxio R., Tankosic C., Doignon I., Nusse O. Potent inhibition of store-operated Ca2+ influx and superoxide production in HL60 cells and polymorphonuclear neutrophils by the pyrazole derivative BTP2. J. Leukoc. Biol. 2007.
128. Strnad C.F., Wong K. Effect of the calcium ionophore A23187 on superoxide generation in phorbol ester stimulated human neutrophils. Can. J. Physiol. Pharmacol. 1985, 63:1543-1546.
129. Swain S.D., Bunger P.L., Sipes K.M., Nelson L.K., Jutila K.L., Boylan S.M., Quinn M.T. Platelet-activating factor induces a concentration-dependent spectrum of functional responses in bovine neutrophils. J. Leukoc. Biol. 1998, 64:817-827.
130. Tarlowe M.H., Kannan K.B., Itagaki K., Adams J.M., Livingston D.H., Hauser C.J. Inflammatory chemoreceptor cross-talk suppresses leukotriene B4 receptor 1-mediated neutrophil calcium mobilization and chemotaxis after trauma. J. Immunol. 2003, 171:2066-2073.
131. Taylor C.W. Store-operated Ca2+ entry: a STIMulating stOrai. Trends Biochem. Sci. 2006, 31:597-601.
132. Togashi K., Inada H., Tominaga M. Inhibition of the transient receptor potential cation channel TRPM2 by 2-aminoethoxydiphenyl borate (2-APB). Br. J. Pharmacol. 2008, 153:1324-1330.
133. Trevani A.S., Andonegui G., Giordano M., Lopez D.H., Gamberale R., Minucci F., Geffner J.R. Extracellular acidification induces human neutrophil activation. J. Immunol. 1999, 162:4849-4857.
134. Urban C.F., Reichard U., Brinkmann V., Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell. Microbiol. 2006, 8:668-676.
135. Valentin F., Bueb J., Capdeville-Atkinson C., Tschirhart E. Rac-1-mediated O2-secretion requires Ca2+ influx in neutrophil-like HL-60 cells. Cell Calcium 2001, 29:409-415.
136. van Zwieten R., Wever R., Hamers M.N., Weening R.S., Roos D. Extracellular proton release by stimulated neutrophils. J. Clin. Invest. 1981, 68:310-313.
137. Waller K.P. Modulation of endotoxin-induced inflammation in the bovine teat using antagonists/inhibitors to leukotrienes, platelet activating factor and interleukin 1 beta. Vet. Immunol. Immunopathol. 1997, 57:239-251.
138. Wessely-Szponder J., Bobowiec R., Martelli F., Wojcik M., Kosior-Korzecka U. Assessment of neutrophil components as markers of lung injury in the course of bovine respiratory tract infections. Pol. J. Vet. Sci. 2004, 7:157-161.
139. Yamamori T., Inanami O., Sumimoto H., Akasaki T., Nagahata H., Kuwabara M. Relationship between p38 mitogen-activated protein kinase and small GTPase Rac for the activation of NADPH oxidase in bovine neutrophils. Biochem. Biophys. Res. Commun. 2002, 293:1571-1578.
140. Yamamoto S., Shimizu S., Kiyonaka S., Takahashi N., Wajima T., Hara Y., Negoro T., Hiroi T., Kiuchi Y., Okada T., Kaneko S., Lange I., Fleig A., Penner R., Nishi M., Takeshima H., Mori Y. TRPM2-mediated Ca2+ influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat. Med. 2008, 14:738-747.
141. Zitt C., Strauss B., Schwarz E.C., Spaeth N., Rast G., Hatzelmann A., Hoth M. Potent inhibition of Ca2+ release-activated Ca2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J. Biol. Chem. 2004, 279:12427-12437.