The Pore-forming Leukotoxins from S. aureus Involve Ca2+ Release-Activated Ca2+ Channels and Other Types of Ca2+ Channels in Ca2+ Entry into Neutrophils
International Journal of Microbiology and Biotechnology
Volume 5, Issue 2, June 2020, Pages: 55-68
Received: Apr. 13, 2020; Accepted: Apr. 30, 2020; Published: May 15, 2020
Views 146      Downloads 52
Authors
Leïla Staali, Department of Biotechnology, Natural and Life Sciences Faculty, Ahmed Ben Bella Oran1-University, Oran, Algeria; Bacteriology Institute of Medical Faculty, Louis Pasteur University, Strasbourg, France
Didier André Colin, Bacteriology Institute of Medical Faculty, Louis Pasteur University, Strasbourg, France
Article Tools
Follow on us
Abstract
The pore-forming bi-component leukotoxins from Staphylococcus aureus induce two independent cellular events 1) the formation of trans-membrane pores not permeable to divalent ions and 2) the opening of pre-existing Ca2+ channels in human polymorphonuclear neutrophils (PMNs). The influx of Ca2+ and Mn2+ (Mn2+ was used as a Ca2+ surrogate) in Fura2-loaded human PMNs was determined by spectrofluorometry techniques. The present study showed that, in the presence of extracellular Ca2+, the staphylococcal HlgA/HlgB γ-hemolysin induced a rapid Ca2+ release from internal Ca2+ stores before the onset of a Mn2+ (Ca2+) influx. The sustained increase of Ca2+ and Mn2+ influx was partially inhibited by the ionic blockers of Ca2+ Release-Activated Ca2+ (CRAC) channels, La3+ and Ni2+. Furthermore, the incubation of human PMNs with either TMB8 or thapsigargin did inhibit significantly the Ca2+ release mediated by leukotoxins simultanously to a clear decrease of Ca2+ and Mn2+ influx. The internal Ca2+ release induced by γ-hemolysin was also inhibited by PMNs pretreatment with a pertussis toxin, NaF, caffeine, ryanodine, cinnarizine and flunarizine and consequently, the Mn2+ (Ca2+) influx was significantly reduced. Moreover, different Ca2+ signaling pathways blockers such as U73122, staurosporine, thyrphostin A9 and okadaic acid were tested on the leukotoxins activity. Taken together, this work provided evidence that, in the presence of extracellular Ca2+, bi-component staphylococcal leukotoxins provoked in human PMNs after a specific binding to their membrane receptors, a rapid depletion of internal Ca2+ stores mediating a CRAC channels activation. This Ca2+-dependent mechanism seems likely to be associated to the heterotrimeric G-proteins activation. Interestingly, in the absence of extracellular Ca2+, the staphylococcal leukotoxins tested induced the opening of an important divalent ions (Ca2+, Mn2+, Ni2+) pathway not sensitive to CRAC channels blockers. Consequently, we strongly suggested that other types of Ca2+ channels might be involved in bi-component leukotoxins activity, including Ca2+ channels dependent on the protein kinase C activation.
Keywords
Pore-forming Toxin, Leukotoxin, γ-hemolysin, Ca2+ Channels, S. aureus, Neutrophils, CRAC Channels, Spectrofluorometry
To cite this article
Leïla Staali, Didier André Colin, The Pore-forming Leukotoxins from S. aureus Involve Ca2+ Release-Activated Ca2+ Channels and Other Types of Ca2+ Channels in Ca2+ Entry into Neutrophils, International Journal of Microbiology and Biotechnology. Vol. 5, No. 2, 2020, pp. 55-68. doi: 10.11648/j.ijmb.20200502.13
Copyright
Copyright © 2020 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
References
[1]
Alouf JE (2003) Molecular features of the cytolytic pore-forming bacterial protein toxins. Folia Microbiol. (Praha) 48 (1): 5-16.
[2]
Los FCO, Randis TM, Aroian RV, Ratner AJ (2013) Role of Pore-forming toxins in bacterial infectious diseases. Microbiol. Mol. Biol. Reviews 77 (2): 173-207.
[3]
Smith M, Price SA (1938) Staphylococcus γ-hemolysin. J. Pathol. Bacteriol. 47: 379-393.
[4]
Guyonnet F, Plommet M (1970) Hémolysine gamma de Staphylococcus aureus: Purification et propriétés. Ann. Inst. Pasteur 118: 19-33.
[5]
Taylor AG, Bernheimer AW (1974) Further characterization of staphylococcal gamma-hemolysin. Infect. Immun. 10: 54-59.
[6]
Prévost G, Couppié P, P, Prévost P, Gayet S, Petiau P, Cribier B, Monteil H, Piémont Y (1995) Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J. Med. Microbiol. 42: 237-245.
[7]
Rahman A, Nariya H, Izaki K, Kato I, Kamio Y (1992) Molecular cloning and nucleotide sequence of leukocidin F-component gene (lukF) for methicillin resistant Staphylococcus aureus. Biochem. Biophys. Res. Commun. 184: 640-646.
[8]
Rahman A, Izaki K, Kamio Y (1993) Gamma-hemolysin genes in the same familiy with lukF and lukS genes in methicillin resistant Staphylococcus aureus. Biosc. Biochem. 57: 1234-1236.
[9]
Cooney J, Kienle Z, Foster TJ, O’Toole PW (1993) The gamma-hemolysin locus of Staphylococcus aureus comprises three linked genes, two of which are identical to the genes for F and S components of leukocidin. Infect. Immun. 61: 768-771.
[10]
Panton PN, Velentin FCO (1932) Staphylococcal toxin. Lancet. 222: 506-508.
[11]
Prévost G, Cribier B, Couppié P, Petiau P, Supersac G, Finck-Barbancon V, Monteil H, Piémont Y (1995) Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC49775 are encoded by distinct loci and have different biological activities. Infect. Immun. 63: 4121-4129.
[12]
Finck-Barbançon V, Duportail G, Meunier O, Colin DA (1993) Pore formation by a two-component leukocidin from Staphylococcus aureus within the membrane of human polymorphonuclear leukocytes. Biochim. Biophys. Acta. 1128: 275-282.
[13]
Colin DA, Mazurier I, Sire S, Finck-Barbançon V (1994) Interaction of the two components of leukocicin from Staphylococcus aureus with human polymorphonuclear leukocyte membranes: sequenctiel binding and subsequent activation. Infect. Immun. 62: 3184-3188.
[14]
Meunier O, Falkenrodt A, Monteil H, Colin DA (1995) Application of fllow cytometry in toxinology: Pathophysiology of human polymorphonuclear leucocytes damaged by a pore-forming toxin from Staphylococcus aureus. Cytometry 21: 241-247.
[15]
Staali L, Monteil H, Colin DA (1998) The pore-forming leukotoxins from Staphylococcus aureus open Ca2+ channels in human polymorphonuclear neutrophils. J. Membr. Biol. 162: 209-216.
[16]
Menestrina G (1986) Ionic channels formed by Staphylococcus aureus alpha-toxin: voltage dependent inhibition by di- and trivalent cations. J. membr. Biol. 90: 177-190.
[17]
Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE (1996) Structure of the Staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1866.
[18]
Andersson T, Dahlgren C, Pozzan T, Stendahl O, Lew PD (1986) Characterization of fMet-Leu-Phe receptor-mediated Ca2+ influx across the plasma membrane of human neutrophils. Mol. Pharmacol. 30: 437-443.
[19]
Von Tscharner V, Prod’hom B, Baggiolini M, Reuter H (1986) Ion channels in human neutrophils activated by a rise in free cytosolic calcium concentration. Nature 324: 369-372.
[20]
Demaurex N, Schlegel W, Varnai P, Mayr G, Lew DP, Krause KH (1992) Regulation of Ca2+ influx in myeloid cells. Role of plasma membrane potentiel, inositiol phosphates, cytosolic free Ca2+, and filling state of intracellular Ca2+ stores. J. Clin. Invest. 90: 830-839.
[21]
Clementi E, Meldolesi J (1996) Pharmacological and functional properties of voltage-independent Ca2+ channels. Cell Calcium 19: 269-279.
[22]
Bird GS, Aziz O, Lievremont JP, Wedel BJ, Trebak M, Vazquez G, Putney JW (2004) Mechanisms of phospholipase C-regulated calcium entry. Curr. Mol. Med. 4: 291-301.
[23]
Berridge MJ (1984) Inositol triphosphate, a novel second messenger in cellular signal transduction. Nature 312: 315-321.
[24]
Xu X, Kitamura K, Lau KS, Muallem S, Miller RT (1995) Differential regulation of Ca2+ release-activated Ca2+ influx by heterotrimeric G proteins. J. Biol. Chem. 270: 29169-29175.
[25]
Quelle FW, Sato N, Witthuhn BA, Inhorn RC, Eder M, Miyajima A, Griffin JD, Ihle JN (1994) JAK2 associates with the beta c chain of the receptor of granulocytes-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol. Cell Biol. 14: 4335-4341.
[26]
Putney JW, Bird G StJ (1993) The signal for capacitative calcium entry. Cell. 75: 199-201.
[27]
Putney JW (2010) Pharmacology of store-operated calcium channels. Mol. Interv. 10: 209-2018.
[28]
Montero M, Alvarez J, Garcia-Sancho J (1991) Agonist-induced Ca2+ influx in human neutrophils is secondary to the emptying of intracellular calcium stores. Biochem. J. 277: 73-79.
[29]
Montero M, Garcia-Sancho J, Alvarez J (1993) Transiet inhibition by chemotactic peptide of a store-operated Ca2+ entry pathway in human neutrophils. J. Biol. Chem. 268: 13055-13061.
[30]
Montero M, Garcia-Sancho J, Alvarez J (1994) Phosphorylation down-regulates the sore-operated Ca2+ entry pathway of human neutrophils. J. Biol. Chem. 269: 3963-3967.
[31]
Demaurex N, Monod A, Lew DP, Krause KH (1994) Characterization of receptor-mediated and store-regulated Ca2+ influx in human neutrophils. Biochem. J. 297: 595-601.
[32]
Montero M, Garcia-Sancho J, Alvarez J (1994) Activation by chemotactic peptide of a receptor-operated Ca2+ entry pathway in differenciated HLA60 cells. J. Biol. Chem. 269: 29451-29456.
[33]
Bouillot S, Reboud E, Huber P (2018) Functional connsequences of calcium influx promoted by bacterial pore-forming toxins. Toxins 10: 387.
[34]
Fink D, Contreras ML, Lelkes PI, Lazarovici P (1989) Staphylococcus aureus alpha-toxin activates phospholipases and induces a Ca2+ influx in PC12 cells. Cell. Signal. 1, 387-393.
[35]
Streb H, Irvine RF, Berridge MJ, Schulz I (1983) Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-triphosphate. Nature 306: 67-69.
[36]
Berridge MJ (2009) Inositol triphosphate and calcium signalling mechanisms. Biochim. Biophy. Acta. 1793: 933-940.
[37]
Bird GS, Putney JW (2005) Capacitative calcium entry supports calcium oscillations in human embryonic kidney cells. J. Physiol. 562: 679-706.
[38]
Wedel B, Boyles RR, Putney JW, Bird GS (2007) Role of the store-operated calcium entry proteins, Stim 1 and Orai 1, in muscarinic-cholinergic receptor stimulated calcium oscillations in human embryonic kidney cells. J. Physiol. 579: 679-689.
[39]
Hopf FW, Reddy P, Hong J, Steinhardt RA (1996) A capacitative calcium current in cultured skeletal muscle cells in mediated by the calcium-specific leak channel and inhibited by dihydropyridine compounds. J. Biol. Chem. 271: 22358-22367.
[40]
Yamazaki M, Molski TFP, Stevens T, Huang CK, Becker EL, Sha’afi RL (1991) Modulation of leukotriene B4 and platelet activating factor binding to neutrophils. Am. J. Physiol. 261: C515-C520.
[41]
Marriote I, Kenneth LB, Mason MJ (1994) Role of intracellular Ca2+ stores in the regulation of electrogenic plasma membrane Ca2+ uptake in a B-lymphocytic cell line. J. Cell. Physiol. 161: 441-448.
[42]
Aussel C, Marhaba R, Pelassy C, Breittmayer JP (1996) Submicromolar La3+ concentration block the calcium release-activated channel, and impair CD69 and CD25 expression in CD3- or thapsigargin-activated Jurkat cells. Biochem J. 313: 909-913.
[43]
Bird GS, DeHaven WI, Smyth JT, Putney JW (2008) Methods for studying store-operated calcium entry. Methods 46: 204-212; doi: 103390/toxins10100387.
[44]
Takemura H, Hughes AR, Thastrup O, Putney JW (1989) Activation of calcium entry by the tumor promotor, thapsigargin, in parotid acinar cells. Evidence that an intracellular calcium pool, and not an inositol phosphate, regulates calcium fluxes at the plasma membrane. J. Biol. Chem. 264, 12266-12271.
[45]
Jackson TR, Paterson SI, Thastrup O, Hanley MR (1988) A novel tumour promotor, thapsigargin, transiently increases cytoplasmic free Ca2+ without generation of inositol phosphates in NG115-401L neuronal cells. Biochem. J. 253: 81-86.
[46]
Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature (London) 355: 353-356.
[47]
Foder B, Scharff O, Thastrup O (1989) Ca2+ transiets and Mn2+ entry in human neutrophils induced by thapsigargin. Cell Calcium 10: 477-490.
[48]
Lytton J, Westlin M, Hanley MR (1991) Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca2+-ATPase family of calcium pumps. J. Biol. Chem. 266: 17067-17017.
[49]
Zweifach A, Lewis RS (1995) Slow calcium-dependent inactivation of depletion-activated calcium current. Store-dependent and –independent mechanisms. J. Biol. Chem. 270: 14445-14451.
[50]
Tinel H, Wehner F, Sauer H (1994) Intracellular Ca2+ release and Ca2+ influx during regulatory volume decrease in IMCD cells. Am. J. Physiol. 267: 130-8.
[51]
Grune S, Engelking LR, Anwer MS (1993) Role of intracellular calcium and protein kinases in the activation of hepatic Na+/Taurocholate co-transport by cyclic AMP. J. Biol. Chem. 268 (24): 17734-17741.
[52]
Favre CJ, Nüsse O, Lew DP, Krausse KH (1996) Store-operated Ca2+ influx: what is the message from the stores to the membrane? J. Lab. Clin. Med. 128: 19-26.
[53]
Berridge MJ (1996) Capacitative Ca2+-entry-sifting through the evidence for CIF. Biochem. J. 312: 1-11.
[54]
Berlin RD, Preston SF (1993) Okadaïc acid uncouples calcium entry from depletion of intracellular stores. Cell Calcium 14: 379-386.
[55]
Putney JWJr (1990) Capacitative Ca2+ entry revisited. Cell Calcium 11: 611-624.
[56]
Marhaba R, Mary F, Pelassy C, Stanescu AT, Aussel C, Breittmayer JP (1996) Tyrphostin A9 inhibits calcium release-dependent phosphorylations and calcium entry via calcium release-activated channel in Jurkat cells. J. Immunol. 157: 1468-1473.
[57]
Randriamampita C, Tsien RY (1995) Degradation of a calcium influx factor (CIF) can be blocked by phosphatase inhibitors or, chelation of Ca2+. J. Biol. Chem. 270: 29-32.
[58]
Wang JP (1996) U-73122, an aminosteroid phospholipase C inhibitor, may also block Ca2+ influx through phospholipase C-independent mechanism in neutrophil activation. Naunyn Schmieddebergs Arch. Pharmacol. 353: 599-605.
[59]
Jan CR, HO CM, Wu SN, Tseng CJ (1998) The phospholipase C inhibitor U73122 increases cytosolic calcium in MDCK cells by activating calcium influx and releasing stored calcium. Life Sciences 63: 895-908.
[60]
Valencia L, Melendez E, Namorado MC, Martin D, Bidet M, Poujeol P, Reyes JL (2004) Parathyroid hormone increase cytosolic calcium in neonatal nephron through protein kinase C pathway. Pediatr. Nephrol. 19 (10): 1093-101.
[61]
Hammerschmidt S, Vogel T, Jockel S, Gessner C, Seyfarth H-J, Gillissen A, Wirtz H (2007) Protein kinase C inhibition attenuates hypochlorite-induced acute lung injury. Respiratory Medecine 101: 1205-1211.
[62]
Fasolato C, Zottinin M, Zacchetti D, Meldolesi J, Pozzan T (1991) Intracellular Ca2+ pools in PC12 cells. Three intracellular pools are distinguished by their turnover and mechanisms of Ca2+ accumulation, storage, and release. J. Biol. Chem. 266: 20159-20167.
[63]
Zacchetti D, Clementi E, Fasolato C, Lorenzon P, Zottini M, Grohavaz F, Fumagalli G, Pozzan T, Meldolesi J (1991) Intracellular Ca2+ pools in PC12 cells. A unique, rapidly exchanging pool is sensitive to both inositol 1, 4, 5-triphosphate and caffeine-ryanodine. J. Biol. Chem. 266: 20152-20158.
[64]
Palade P, Dettbarn C, Alderson B, Volpe P (1989) Pharmacologic differenciation between inositol-1,4,5-triphosphate-induced Ca2+ release and Ca2+-or caffeine-induced Ca2+ release from intracellular membrane systems. Mol. Pharmacol. 36: 673-680.
[65]
Seiler SM, Arnold AJ, Stanton HC (1987) Inhibitors of inositol triphosphate-induced Ca2+ release from isolated platelet membrane vesicles. Biochem. Pharmacol. 36: 3331-3337.
[66]
McNulty TJ, Taylor CW (1993) Caffeine-stimulated Ca2+ release from the intracellular stores of hepatocytes is not mediated by ryanodine receptors. Biochem. J. 291: 799-801.
[67]
Kahn RA (1991) Fluoride is not an activator of the smaller (20-25 kDa) GTP-binding proteins. J. Biol. Chem. 266: 15595-15597.
[68]
Fernando KC, Barritt GJ (1994) Evidence from studies with hepatocyte suspensions that store-operated Ca2+ inflow requires a pertussis toxin-sensitive trimeric G-protein. Biochem. J. 303: 351-356.
[69]
Berven LA, Crouch MF, Katsis F, Kemp BE, Harland LM, Barritt GJ (1995) Evidence that the pertussis toxin-sensitive trimeric GTP-binding protein Gi2 is required for agonist- and store-activated Ca2+ inflow in hepatocytes. Biol. Chem. J. 270: 25893-25897.
[70]
Hoth M, Penner R (1993) Calcium release-activated calcium current in rat mast cells. J. Physiol. 465: 359-386.
[71]
Dolmetsch RE, Lewis RS (1994) Signaling between intracellular Ca2+ stores and depletion-activated Ca2+ channels generates Ca2+ oscillations in T lymphocytes. J. Gen. Physiol. 103: 365-388.
[72]
Parekh AB, Terlau H, Stühmer W (1993) Depletion of InsP3 stores activates a Ca2+ and K+ current by means of a phosphatase and a diffusible messenger. Nature (London) 364: 814-818.
[73]
Tojyo Y, Tanimura A, Matsumoto Y (1995) Suppression of capacitative Ca2+ entry by serine/threonine phosphatases inhibitors in rat parotid acinar cells. J. JPN. Pharmacol. 69: 381-389.
[74]
Socci R, Chu A, Reinach P, Meszaros LG (1993) In situ Ca2+-induced Ca2+ release from a ryanodine-sensitive intracellular Ca2+ stores in corneal epithelial cells. Com. Biochem. Physiol. 106: 793-797.
[75]
Dupont G, Goldbeter A (1993) One-pool model for Ca2+ oxcillations involving Ca2+ and inositol 1,4,5-triphosphate as co-agonists for Ca2+ release. Cell Calcium 14: 311-322.
[76]
Berven LA, Barritt GL (1994) A role for a pertussis toxin-sensitive trimeric G-protein in store-operated Ca2+ inflow in hepathocytes (1994). FEBS Letters 346: 235-240.
[77]
Brandt S, Dougherty RW, Lapetina EG, Niedel J (1985) Pertussis toxin inhibits chemotactic peptide-stimulated generation of inositol phosphates and lysosomal enzyme secretion in human leukemic (HL-60) cells. Proc. Nat. Acad. Sci. USA 82: 3277-3280.
[78]
Guaduchon V, Werner S, Prévost G, Monteil H, Colin DA (2001) Flow cytometry determination of Panton-Valentin leukocidin S component binding. Infect. Immun. 69: 2390-2395.
[79]
Spaan AN, Henry T, van Rooijen WJM, Perret M, Badiou C, Aerts PC, Kemrnik J, de Haas CJC, van Kessel KPM, Vandenesch F, Lina G, van Strijp JAG (2013) The staphylococcal toxin Panton-Valentin targets human C5a receptors. Cell Host Microbe. 13: 584-594.
[80]
Spaan AN, et al. (2014) The staphylococcal toxins gamma-hemolysin AB and CB differentially target phagocytes by employing specific chemokine receptors. Nat. Commun. 5: 543-548.
[81]
Reyes-Robles T, Alonzo F, Koshaya L, Lacy DB, Unutmaz D, Torres VJ (2013) Staphylococcus aureus leukotoxin ED targets the chemokine receptors CXCR1 and CXCR2 to kill leukocytes and promotes infection. Cell Host Microbe 14: 453-459.
[82]
Randriamampita C, Bismuth G, Trautmann A (1991) Ca2+-induced Ca2+ release amplifies the Ca2+ response elicited by inositol triphosphate in macrophages. Cell regul. 2: 513-522.
[83]
Pettit EJ, Davies EV, Hallett MB (1997) The microanatomy of calcium stores in human neutrophils: Relationship of structure to function. Histol. Histopathol. 12: 479-490.
[84]
Zweifach A, Lewis RS (1996) Calcium-dependent potentiation of store-operated calcium channels in T lymphocytes. J. Gen. Physiol. 107: 597-610.
[85]
Venkatakrishnan AJ, et al. (2013) Molecular signatures of G-proteins coupled receptors. Nature. 494: 185-194.
[86]
Tournamille C, Colin Y, Cartron JP, Le Van Kim C (1995) Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat. Genet. 10: 224-228.
[87]
Pruenster M, Rot A (2006) Throwing light on DARC. Biochem. Soc. Trans. 34: 1005-1008.
[88]
Pareck AB (2010) Store-operated CRAC channels: Function in health and disease. Nature Reviews Drug Discovery 9: 399-410.
[89]
Wenzel-Seifert K, Krautwurst D, Lentzen H, Seifert R (1996) Concavalin A and mistletoe lectin I differentially activate cation entry and exocytosis in human neutrophils: lectins may activate multiple subtypes of cation channels. J. Leukocyte Biol. 60: 345-355.
[90]
Woodin AM (1970) Staphylococcal leucocidin, in Microbial Toxins Vol: III, eds. Montie, TC, Kadis S, Ajl SJ (Academic press, New York and London), pp. 327-355.
[91]
Woodin Am (1972) Adenylate cyclase and the function of cyclic adenosine 3,5-monophosphate in the leucocidin-treated leucocyte. Biochim. Biophys. Acta 260: 406-415.
[92]
Noda M, Kato I, Hyrayama T, Matsuda F (1981) Mode of action of staphylococcal leukocidin effects of the S and F components on the activities of membrane-associated enzymes of rabbit polymorphonuclear leukocytes. Infect. Immun. 35: 38-45.
ADDRESS
Science Publishing Group
1 Rockefeller Plaza,
10th and 11th Floors,
New York, NY 10020
U.S.A.
Tel: (001)347-983-5186