Enhanced eryptosis following gramicidin exposure

Toxins

Volumn 7, Issue 5, 2015, Pages 1396-1410

  Malik, Abaid ^a   Bissinger, Rosi ^a   Liu, Guoxing ^a   Liu, Guilai ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Calcium; Cell volume; Eryptosis; Gramicidin; Oxidative stress; Phosphatidylserine; ROS

Indexed keywords

CALCIUM ION; CERAMIDE; DICHLORODIHYDROFLUORESCEIN DIACETATE; FLUO 3; GRAMICIDIN; LIPOCORTIN 5; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; ANTIINFECTIVE AGENT; CALCIUM;

ANTIGEN BINDING; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL COUNTING; CELL DEATH; CELL STIMULATION; CELL SURFACE; CELL VOLUME; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG EXPOSURE; ERYPTOSIS; ERYTHROCYTE MEMBRANE; FLOW CYTOMETRY; FLUORESCENCE; HEMOLYSIS; HUMAN; HUMAN CELL; MEAN CORPUSCULAR VOLUME; OXIDATIVE STRESS; UPREGULATION; CELL SIZE; DRUG EFFECTS; ERYTHROCYTE; METABOLISM;

ANTI-BACTERIAL AGENTS; CALCIUM; CELL DEATH; CELL SIZE; CERAMIDES; ERYTHROCYTES; GRAMICIDIN; HUMANS; OXIDATIVE STRESS; PHOSPHATIDYLSERINES; REACTIVE OXYGEN SPECIES;

EID: 84929332247     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins7051396     Document Type: Article

References (69)

1. Mogi, T.; Kita, K. Gramicidin S and polymyxins: The revival of cationic cyclic peptide antibiotics. Cell. Mol. Life Sci. 2009, 66, 3821–3826.
2. Andersen, O.S.; Koeppe, R.E., 2nd; Roux, B. Gramicidin channels. IEEE Trans. Nanobiosci. 2005, 4, 10–20.
3. Kelkar, D.A.; Chattopadhyay, A. The gramicidin ion channel: A model membrane protein. Biochim. Biophys. Acta 2007, 1768, 2011–2025.
4. Seoh, S.A.; Busath, D. The permeation properties of small organic cations in gramicidin a channels. Biophys. J. 1993, 64, 1017–1028.
5. Bourinbaiar, A.S.; Coleman, C.F. The effect of gramicidin, a topical contraceptive and antimicrobial agent with anti-hiv activity, against herpes simplex viruses type 1 and 2 in vitro. Arch Virol. 1997, 142, 2225–2235.
6. Bourinbaiar, A.S.; Lee, C.H. Synergistic effect of gramicidin and edta in inhibiting sperm motility and cervical mucus penetration in vitro. Contraception 1996, 54, 367–372.
7. Centola, G.M. Dose-response effects of gramicidin-d, edta, and nonoxynol-9 on sperm motion parameters and acrosome status. Contraception 1998, 58, 35–38.
8. Prenner, E.J.; Lewis, R.N.; McElhaney, R.N. The interaction of the antimicrobial peptide gramicidin s with lipid bilayer model and biological membranes. Biochim. Biophys. Acta 1999, 1462, 201–221.
9. Bourinbaiar, A.S.; Krasinski, K.; Borkowsky, W. Anti-HIV effect of gramicidin in vitro: Potential for spermicide use. Life Sci. 1994, 54, PL5–PL9.
10. Wijesinghe, D.; Arachchige, M.C.; Lu, A.; Reshetnyak, Y.K.; Andreev, O.A. pH dependent transfer of nano-pores into membrane of cancer cells to induce apoptosis. Sci. Rep. 2013, 3, 3560.
11. Lang, P.A.; Kaiser, S.; Myssina, S.; Wieder, T.; Lang, F.; Huber, S.M. Role of Ca2+-activated K+ channels in human erythrocyte apoptosis. Am. J. Physiol. Cell Physiol. 2003, 285, C1553–C1560.
12. Lang, E.; Qadri, S.M.; Lang, F. Killing me softly-suicidal erythrocyte death. Int. J. Biochem. Cell Biol. 2012, 44, 1236–1243.
13. Abed, M.; Towhid, S.T.; Mia, S.; Pakladok, T.; Alesutan, I.; Borst, O.; Gawaz, M.; Gulbins, E.; Lang, F. Sphingomyelinase-induced adhesion of eryptotic erythrocytes to endothelial cells. Am. J. Physiol. Cell Physiol. 2012, 303, C991–C999.
14. Lau, I.P.; Chen, H.; Wang, J.; Ong, H.C.; Leung, K.C.; Ho, H.P.; Kong, S.K. In vitro effect of ctab- and peg-coated gold nanorods on the induction of eryptosis/erythroptosis in human erythrocytes. Nanotoxicology 2012, 6, 847–856.
15. Maellaro, E.; Leoncini, S.; Moretti, D.; Del Bello, B.; Tanganelli, I.; De Felice, C.; Ciccoli, L. Erythrocyte caspase-3 activation and oxidative imbalance in erythrocytes and in plasma of type 2 diabetic patients. Acta Diabetol. 2013, 50, 489–495.
16. Jilani, K.; Qadri, S.M.; Lang, F. Geldanamycin-induced phosphatidylserine translocation in the erythrocyte membrane. Cell Physiol. Biochem. 2013, 32, 1600–1609.
17. Vota, D.M.; Maltaneri, R.E.; Wenker, S.D.; Nesse, A.B.; Vittori, D.C. Differential erythropoietin action upon cells induced to eryptosis by different agents. Cell Biochem. Biophys. 2013, 65, 145–157.
18. Zappulla, D. Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: Adaptations to co2 increases? J. Cardiometab. Syndr. 2008, 3, 30–34.
19. Zbidah, M.; Lupescu, A.; Jilani, K.; Lang, F. Stimulation of suicidal erythrocyte death by fumagillin. Basic Clin. Pharmacol. Toxicol. 2013, 112, 346–351.
20. Abed, M.; Herrmann, T.; Alzoubi, K.; Pakladok, T.; Lang, F. Tannic acid induced suicidal erythrocyte death. Cell Physiol. Biochem. 2013, 32, 1106–1116.
21. Ahmed, M.S.; Langer, H.; Abed, M.; Voelkl, J.; Lang, F. The uremic toxin acrolein promotes suicidal erythrocyte death. Kidney Blood Press. Res. 2013, 37, 158–167.
22. Ghashghaeinia, M.; Cluitmans, J.C.; Toulany, M.; Saki, M.; Koberle, M.; Lang, E.; Dreischer, P.; Biedermann, T.; Duszenko, M.; Lang, F.; et al. Age sensitivity of nfkappab abundance and programmed cell death in erythrocytes induced by nfkappab inhibitors. Cell Physiol. Biochem. 2013, 32, 801–813.
23. Alzoubi, K.; Honisch, S.; Abed, M.; Lang, F. Triggering of suicidal erythrocyte death by penta-o-galloyl-beta-d-glucose. Toxins 2014, 6, 54–65.
24. Jilani, K.; Lang, F. Carmustine-induced phosphatidylserine translocation in the erythrocyte membrane. Toxins 2013, 5, 703–716.
25. Jilani, K.; Enkel, S.; Bissinger, R.; Almilaji, A.; Abed, M.; Lang, F. Fluoxetine induced suicidal erythrocyte death. Toxins 2013, 5, 1230–1243.
26. Lupescu, A.; Bissinger, R.; Jilani, K.; Lang, F. Triggering of suicidal erythrocyte death by celecoxib. Toxins 2013, 5, 1543–1554.
27. Lupescu, A.; Jilani, K.; Zbidah, M.; Lang, F. Patulin-induced suicidal erythrocyte death. Cell Physiol. Biochem. 2013, 32, 291–299.
28. Abed, M.; Zoubi, K.A.; Theurer, M.; Lang, F. Effect of dermaseptin on erythrocytes. Basic Clin. Pharmacol. Toxicol. 2013, 113, 347–352.
29. Arnold, M.; Lang, E.; Modicano, P.; Bissinger, R.; Faggio, C.; Abed, M.; Lang, F. Effect of nitazoxanide on erythrocytes. Basic Clin. Pharmacol. Toxicol. 2014, 114, 421–426.
30. Oswald, G.; Alzoubi, K.; Abed, M.; Lang, F. Stimulation of suicidal erythrocyte death by ribavirin. Basic Clin. Pharmacol. Toxicol. 2014, 114, 311–317.
31. Bissinger, R.; Malik, A.; Jilani, K.; Lang, F. Triggering of erythrocyte cell membrane scrambling by salinomycin. Basic Clin. Pharmacol. Toxicol. 2014, 115, 396–402.
32. Abed, M.; Feger, M.; Alzoubi, K.; Pakladok, T.; Frauenfeld, L.; Geiger, C.; Towhid, S.T.; Lang, F. Sensitization of erythrocytes to suicidal erythrocyte death following water deprivation. Kidney Blood Press. Res. 2013, 37, 567–578.
33. Alzoubi, K.; Calabròa, S.; Bissinger, R.; Abed, M.; Faggio, C.; Lang, F. Stimulation of suicidal erythrocyte death by artesunate. Cell Physiol. Biochem. 2014, 34, 2232–2244.
34. Arnold, M.; Bissinger, R.; Lang, F. Mitoxantrone-induced suicidal erythrocyte death. Cell Physiol. Biochem. 2014, 34, 1756–1767.
35. Bissinger, R.; Fischer, S.; Jilani, K.; Lang, F. Stimulation of erythrocyte death by phloretin. Cell Physiol. Biochem. 2014, 34, 2256–2265.
36. Bissinger, R.; Lupescu, A.; Zelenak, C.; Jilani, K.; Lang, F. Stimulation of eryptosis by cryptotanshinone. Cell Physiol. Biochem. 2014, 34, 432–442.
37. Bissinger, R.; Modicano, P.; Frauenfeld, L.; Lang, E.; Jacobi, J.; Faggio, C.; Lang, F. Estramustine-induced suicidal erythrocyte death. Cell Physiol. Biochem. 2013, 32, 1426–1436.
38. Jacobi, J.; Lang, E.; Bissinger, R.; Frauenfeld, L.; Modicano, P.; Faggio, C.; Abed, M.; Lang, F. Stimulation of erythrocyte cell membrane scrambling by mitotane. Cell Physiol. Biochem. 2014, 33, 1516–1526.
39. Lupescu, A.; Bissinger, R.; Herrmann, T.; Oswald, G.; Jilani, K.; Lang, F. Induction of suicidal erythrocyte death by novobiocin. Cell Physiol. Biochem. 2014, 33, 670–680.
40. Lupescu, A.; Bissinger, R.; Warsi, J.; Jilani, K.; Lang, F. Stimulation of erythrocyte cell membrane scrambling by gedunin. Cell Physiol. Biochem. 2014, 33, 1838–1848.
41. Malik, A.; Bissinger, R.; Calabro, S.; Faggio, C.; Jilani, K.; Lang, F. Aristolochic acid induced suicidal erythrocyte death. Kidney Blood Press. Res. 2014, 39, 408–419.
42. Tesoriere, L.; Attanzio, A.; Allegra, M.; Cilla, A.; Gentile, C.; Livrea, M.A. Oxysterol mixture in hypercholesterolemia-relevant proportion causes oxidative stress-dependent eryptosis. Cell Physiol. Biochem. 2014, 34, 1075–1089.
43. Voelkl, J.; Alzoubi, K.; Mamar, A.K.; Ahmed, M.S.; Abed, M.; Lang, F. Stimulation of suicidal erythrocyte death by increased extracellular phosphate concentrations. Kidney Blood Press. Res. 2013, 38, 42–51.
44. Zhang, R.; Xiang, Y.; Ran, Q.; Deng, X.; Xiao, Y.; Xiang, L.; Li, Z. Involvement of calcium, reactive oxygen species, and atp in hexavalent chromium-induced damage in red blood cells. Cell Physiol. Biochem. 2014, 34, 1780–1791.
45. Jilani, K.; Qadri, S.M.; Lang, E.; Zelenak, C.; Rotte, A.; Bobbala, D.; Lang, F. Stimulation of erythrocyte phospholipid scrambling by enniatin A. Mol. Nutr. Food Res. 2011, 55 (Suppl. 2), S294–S302.
46. Lui, J.C.; Wong, J.W.; Suen, Y.K.; Kwok, T.T.; Fung, K.P.; Kong, S.K. Cordycepin induced eryptosis in mouse erythrocytes through a Ca2+-dependent pathway without caspase-3 activation. Arch. Toxicol. 2007, 81, 859–865.
47. Mahmud, H.; Mauro, D.; Qadri, S.M.; Foller, M.; Lang, F. Triggering of suicidal erythrocyte death by amphotericin b. Cell Physiol. Biochem. 2009, 24, 263–270.
48. Nguyen, D.B.; Wagner-Britz, L.; Maia, S.; Steffen, P.; Wagner, C.; Kaestner, L.; Bernhardt, I. Regulation of phosphatidylserine exposure in red blood cells. Cell Physiol. Biochem. 2011, 28, 847–856.
49. Schneider, J.; Nicolay, J.P.; Foller, M.; Wieder, T.; Lang, F. Suicidal erythrocyte death following cellular K+ loss. Cell Physiol. Biochem. 2007, 20, 35–44.
50. Siraskar, B.; Ballal, A.; Bobbala, D.; Foller, M.; Lang, F. Effect of amphotericin b on parasitemia and survival of plasmodium berghei-infected mice. Cell Physiol. Biochem. 2010, 26, 347–354.
51. Salvagno, G.L.; Sanchis-Gomar, F.; Picanza, A.; Lippi, G. Red blood cell distribution width: A simple parameter with multiple clinical applications. Crit. Rev. Clin. Lab. Sci. 2015, in press.
52. Orlov, S.N.; Platonova, A.A.; Hamet, P.; Grygorczyk, R. Cell volume and monovalent ion transporters: Their role in cell death machinery triggering and progression. Am. J. Physiol. Cell Physiol. 2013, 305, C361–C372.
53. Harrison, H.E.; Bunting, H.; Ordway, N.K.; Albrink, W.S. The pathogenesis of the renal injury produced in the dog by hemoglobin or methemoglobin. J. Exp. Med. 1947, 86, 339–356.
54. Foller, M.; Bobbala, D.; Koka, S.; Huber, S.M.; Gulbins, E.; Lang, F. Suicide for survival—Death of infected erythrocytes as a host mechanism to survive malaria. Cell Physiol. Biochem. 2009, 24, 133–140.
55. Kirk, K. Membrane transport in the malaria-infected erythrocyte. Physiol. Rev. 2001, 81, 495–537.
56. Ayi, K.; Giribaldi, G.; Skorokhod, A.; Schwarzer, E.; Prendergast, P.T.; Arese, P. 16alpha-bromoepiandrosterone, an antimalarial analogue of the hormone dehydroepiandrosterone, enhances phagocytosis of ring stage parasitized erythrocytes: A novel mechanism for antimalarial activity. Antimicrob. Agents Chemother. 2002, 46, 3180–3184.
57. Ayi, K.; Turrini, F.; Piga, A.; Arese, P. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: A common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 2004, 104, 3364–3371.
58. Cappadoro, M.; Giribaldi, G.; O’Brien, E.; Turrini, F.; Mannu, F.; Ulliers, D.; Simula, G.; Luzzatto, L.; Arese, P. Early phagocytosis of glucose-6-phosphate dehydrogenase (g6pd)-deficient erythrocytes parasitized by plasmodium falciparum may explain malaria protection in g6pd deficiency. Blood 1998, 92, 2527–2534.
59. Koka, S.; Huber, S.M.; Boini, K.M.; Lang, C.; Foller, M.; Lang, F. Lead decreases parasitemia and enhances survival of plasmodium berghei-infected mice. Biochem. Biophys. Res. Commun. 2007, 363, 484–489.
60. Koka, S.; Lang, C.; Niemoeller, O.M.; Boini, K.M.; Nicolay, J.P.; Huber, S.M.; Lang, F. Influence of no synthase inhibitor l-name on parasitemia and survival of plasmodium berghei infected mice. Cell Physiol. Biochem. 2008, 21, 481–488.
61. Borst, O.; Abed, M.; Alesutan, I.; Towhid, S.T.; Qadri, S.M.; Foller, M.; Gawaz, M.; Lang, F. Dynamic adhesion of eryptotic erythrocytes to endothelial cells via cxcl16/sr-psox. Am. J. Physiol. Cell Physiol. 2012, 302, C644–C651.
62. Andrews, D.A.; Low, P.S. Role of red blood cells in thrombosis. Curr. Opin. Hematol. 1999, 6, 76–82.
63. Chung, S.M.; Bae, O.N.; Lim, K.M.; Noh, J.Y.; Lee, M.Y.; Jung, Y.S.; Chung, J.H. Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 414–421.
64. Zwaal, R.F.; Comfurius, P.; Bevers, E.M. Surface exposure of phosphatidylserine in pathological cells. Cell Mol. Life Sci. 2005, 62, 971–988.
65. Closse, C.; Dachary-Prigent, J.; Boisseau, M.R. Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br. J. Haematol. 1999, 107, 300–302.
66. Gallagher, P.G.; Chang, S.H.; Rettig, M.P.; Neely, J.E.; Hillery, C.A.; Smith, B.D.; Low, P.S. Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 2003, 101, 4625–4627.
67. Pandolfi, A.; di Pietro, N.; Sirolli, V.; Giardinelli, A.; di Silvestre, S.; Amoroso, L.; di Tomo, P.; Capani, F.; Consoli, A.; Bonomini, M. Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J. Cell. Physiol. 2007, 213, 699–709.
68. Wood, B.L.; Gibson, D.F.; Tait, J.F. Increased erythrocyte phosphatidylserine exposure in sickle cell disease: Flow-cytometric measurement and clinical associations. Blood 1996, 88, 1873–1880.
69. Kahn, S.E.; Watkins, B.F.; Bermes, E.W., Jr. An evaluation of a spectrophotometric scanning technique for measurement of plasma hemoglobin. Ann. Clin. Lab. Sci. 1981, 11, 126–131.