Alpha hemolysin induces an increase of erythrocytes calcium: A FLIM 2-Photon Phasor analysis approach

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Sanchez, Susana ^a,b   Bakás, Laura ^c,d   Gratton, Enrico ^a   Herlax, Vanesa ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c Universidad Nacional de La Plata ^*  (Argentina)

^d UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; CALCIUM; HEMOLYSIN;

ANALYTIC METHOD; ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL VIRULENCE; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENDOTHELIUM CELL; EPITHELIUM CELL; ERYTHROCYTE; ESCHERICHIA COLI; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; GRANULOCYTE; HEMOLYSIS; IMAGE ANALYSIS; MONOCYTE; NONHUMAN; QUANTUM YIELD; SIGNAL TRANSDUCTION; TWO PHOTON PHASOR PLOT ANALYSIS; ANIMAL; BLOOD; CALIBRATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; METABOLISM; PHOTON; PHYSIOLOGY; RABBIT;

ESCHERICHIA COLI; ORYCTOLAGUS CUNICULUS;

ANIMALS; CALCIUM; CALIBRATION; ERYTHROCYTES; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEMOLYSIN PROTEINS; PHOTONS; RABBITS;

EID: 79959238505     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021127     Document Type: Article

References (41)

1. Bhadki S, Bailey H, Valava A, Walev I, Walker B, et al. (1996) Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototype of pore-forming bacterial cytolisins. Arch Microbiol 165: 73-79.
2. Bhakdi S, Mackman N, Nicaud JM, Holland I, (1986) Escherichia coli hemolysin may damage target cell membranes by generating transmembrane pores. Infect Immun 52: 63-69.
3. Grimminger F, Sibelius U, BHadki S, Suttorp N, Seeger W, (1991) Escherichia coli hemolysin is a potent inducer of phosphoinositide hydrolysis and related metabolic responses in human neutrophils. JClin Invest 88: 1531-1539.
4. Grimminger F, Rose F, Sibelius U, Meinhardt M, Potzsch B, et al. (1997) Human endothelial cell activation and mediator release in response to the bacterial exotoxins Escherichia coli hemolysin and staphylococcal-toxin. J Immunol 159: 1909-1916.
5. Laestadius A, Richter- Dahlfors A, Aper A, (2002) Dual effects of Escherichia coli α-hemolysin on rat renal proximal tubule cells. Kidney International 62: 2035-2042.
6. Uhlen P, Laestadius A, Jahnukainen T, Soderblom T, Backhed F, et al. (2000) Alpha-haemolysin of uropathogenic E. coli induces Ca2_ oscillations in renal epithelial cells. Nature 405: 694-697.
7. Koschinski A, Repp H, Unver H, Dreyer F, Brockmeier D, et al. (2006) Why Escherichia coli α-hemolysin induces calcium oscillations in mammalian cells-the pore is on its own. FASEB J pp. E80-E87.
8. Moayeri M, Welch R, (1994) Effects of temperature, time, and toxin concentration on lesion formation by the Escherichia coli hemolysin. Infection and immunity 62: 4124-4134.
9. Moayeri M, Welch R, (1997) Prelytic and lytic Conformation of erythrocyte-associated Escherichia coli hemolysin. Infection and immunity 65: 2233-2239.
10. Schindel C, Zitzer A, Schulte B, Gerhards A, Stanley P, et al. (2001) Interaction of Escherichia coli hemolysin with biological membranes: A study using cysteine scanning mutagenesis. Eur J Biochem 268: 800-808.
11. Ostolaza H, Goñi FM, (1995) Interaction of the bacterial protein toxin alpha-haemolysin with model membranes: protein binding does not always lead to lytic activity. FEBS Lett 371: 303-306.
12. Herlax V, Maté S, Rimoldi O, (2009) Relevance of fatty acid covalently bound to Escherichia coli α-Hemolysin and membrane microdomains in the oligomerization process. J Biol Chem 284: 25199-25210.
13. Skals M, Jensen U, Ousingsawat J, Kunzelmann K, Leipziger J, et al. (2010) Escherichia coli alpha-hemolysin triggers shrinkage of erythrocytes via K(Ca)3.1 and TMEM16A channels with subsequent phosphatidylserine exposure. J Biol Chem 285: 15557-15565.
14. Skals M, Jorgensen NR, Leipziger J, Praetorius HA, (2009) Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc Natl Acad Sci U S A 106: 4030-4035.
15. Kaestner L, Tabellion W, Weiss E, Bernhardt I, Lipp P, (2006) Calcium imaging of individual erythrocytes: problems and approaches. Cell Calcium 39: 13-19.
16. Celli A, Sánchez S, Behne M, Hazlett T, Gratton E, et al. (2010) The epidermal Ca2+gradient: Measurement using the phasor representation of fluorescent lifetime imaging. Biophys J 98: 911-921.
17. Noomnarm U, Clegg RM, (2009) Fluorescence lifetimes: fundamentals and interpretations. Photosynth Res 101: 181-194.
18. Digman M, Caiolfa V, Zamai M, Gratton E, (2008) The phasor approach to fluorescence ifetime imaging analysis. Biophys J 94: L14-16.
19. Barreiro O, Zamai M, Yanez-Mo M, Tejera E, Lopez-Romero P, et al. (2008) Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J Cell Biol 183: 527-542.
20. Hanson KM, Behne MJ, Barry NP, Mauro TM, Gratton E, et al. (2002) Two-photon fluorescence lifetime imaging of the skin stratum corneum pH gradient. Biophys J 83: 1682-1690.
21. Snyder IS, Zwadyk P, (1969) Some factors affecting production and assay of Escherichia coli hemolysin. J Gen Microbiol 5: 133-143.
22. Soloaga A, Ramirez JM, Goñi FM, (1998) Reversible denaturation, self aggregation and membrane activity of Escherichia coli α-Hemolysin, a protein stable in 6 M Urea. Biochemistry 37: 6387-6393.
23. Garcia-Marcos A, Sánchez S, Parada P, Eid J, Jameson D, et al. (2008) Yeast ribosomal stalk heterogeneity in vivo shown by two-photon FCS and molecular brightness analysis. Biophys J 94: 2884-2890.
24. Jameson D, Gratton E, Hall R, (1984) The measurement and analysis of heterogeneous emissions by multifrequency phase and modulation fluorometry. Appl Spectrosc Rev 20: 55-106.
25. Clayton A, Hanley Q, Verveer P, (2004) Graphical representation and multicomponent analysis of single-frequency fluorescence lifetime imaging microscopy data. J Microsc 213: 1-5.
26. Redford G, Clegg R, (2005) Polar plot representation for frequency-domain analysis of fluorescence lifetimes. J Fluoresc 15: 805-815.
27. James NG, Ross JA, Stefl M, Jameson DM, (2011) Applications of phasor plots to in vitro protein studies. Anal Biochem 410: 70-76.
28. Stefl M, James NG, Ross JA, Jameson DM, (2011) Applications of phasors to in vitro time-resolved fluorescence measurements. Anal Biochem 410: 62-69.
29. Jameson D, Gratton E, Alpert B, (1984) Oxygen distribution and migration within Mbdes Fe and Hbdes Fe. Multifrequency phase and modulation fluorometry study. Biophys J 45: 795-803.
30. Tiffert T, Bookchin RM, Lew VL, (2003) Calcium homeostasis in normal and abnormal human red cells; In: Bernhardt I, Ellory JC, editors. Berlin pp. 373-405.
31. Föller M, Shumilina E, Lam R, Mohamed W, Kasinathan R, et al. (2007) Induction of suicidal erythrocyte death by listeriolysin from Listeria monocytogenes. Cell Physiol Biochem 20: 1051-1060.
32. Takahashi A, Camacho P, Lechleiter JD, Herman B, (1999) Measurement of intracellular calcium. Physiol Rev 79: 1089-1125.
33. Kaestner L, Juzeniene A, Moan J, (2004) Erythrocytes-the 'house elves' of photodynamic therapy. Photochem Photobiol Sci 3: 981-989.
34. Herrmann A, Devaux PF, (1990) Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochim Biophys Acta 1027: 41-46.
35. Soupene E, Kuypers FA, (2006) Identification of an erythroid ATP-dependent aminophospholipid transporter. Br J Haematol 133: 436-438.
36. Zhou Q, Zhao J, Stout JG, Luhm RA, Wiedmer T, et al. (1997) Molecular cloning of human plasma membrane phospholipid scramblase. A protein mediating transbilayer movement of plasma membrane phospholipids. J Biol Chem 272: 18240-18244.
37. Zhao J, Zhou Q, Wiedmer T, Sims PJ, (1998) Level of expression of phospholipid scramblase regulates induced movement of phosphatidylserine to the cell surface. J Biol Chem 273: 6603-6606.
38. Kuypers FA, (1998) Phospholipid asymmetry in health and disease. Curr Opin Hematol 5: 122-131.
39. Bitbol M, Fellmann P, Zachowski A, Devaux PF, (1987) Ion regulation of phosphatidylserine and phosphatidylethanolamine outside-inside translocation in human erythrocytes. Biochim Biophys Acta 904: 268-282.
40. Woon LA, Holland JW, Kable EP, Roufogalis BD, (1999) Ca2+ sensitivity of phospholipid scrambling in human red cell ghosts. Cell Calcium 25: 313-320.
41. Bakás L, Chanturiya A, Herlax V, Zimmerberg J, (2006) Paradoxical lipid dependence of pores formed by Escherichia coli α-hemolysin in planar phospholipids bilayer membranes. Biophys J 91: 3748-3755.