Induction of suicidal erythrocyte death by novobiocin

Cellular Physiology and Biochemistry

Volumn 33, Issue 3, 2014, Pages 670-680

  Lupescu, Adrian ^a   Bissinger, Rosi ^a   Herrmann, Tabea ^a   Oswald, Gergely ^a   Jilani, Kashif ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Calcium; Cell volume; Eryptosis; Phosphatidylserine

Indexed keywords

AMINOCOUMARIN DERIVATIVE; CALCIUM ION; CERAMIDE; HEAT SHOCK PROTEIN 90; HYPOXIA INDUCIBLE FACTOR; LIPOCORTIN 5; NOVOBIOCIN; PHOSPHATIDYLSERINE; PHOSPHOLIPID; CALCIUM;

ARTICLE; CELL DEATH; CELL MEMBRANE; CELL SURVIVAL; CELL VOLUME; CONTROLLED STUDY; DRUG EFFECT; ERYPTOSIS; ERYTHROCYTE; ERYTHROCYTE LIFESPAN; ERYTHROCYTE MEMBRANE; EXTRACELLULAR CALCIUM; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TRANSPORT; CALCIUM SIGNALING; CYTOLOGY; DRUG EFFECTS; METABOLISM; BINDING AFFINITY; CELL DISRUPTION; ERYTHROCYTE VOLUME; FLUORESCENCE;

ANNEXIN A5; CALCIUM; CALCIUM SIGNALING; CELL DEATH; CERAMIDES; ERYTHROCYTES; HUMANS; NOVOBIOCIN;

EID: 84895932369     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000358643     Document Type: Article

References (96)

1. Wu D, Zhang R, Zhao R, Chen G, Cai Y, Jin J: A novel function of novobiocin: disrupting the interaction of HIF 1alpha and p300/CBP through direct binding to the HIF1alpha C-terminal activation domain. PLoS One 2013;8:e62014.
2. Hoggarth JH, Ritchie DA: Expression of novobiocin resistance genes in the novobiocin-producing organism Streptomyces niveus. J Appl Bacteriol 1995;78:543-547.
3. Matthews SB, Vielhauer GA, Manthe CA, Chaguturu VK, Szabla K, Matts RL, Donnelly AC, Blagg BS, Holzbeierlein JM: Characterization of a novel novobiocin analogue as a putative C-terminal inhibitor of heat shock protein 90 in prostate cancer cells. Prostate 2010;70:27-36.
4. Donnelly A, Blagg BS: Novobiocin and additional inhibitors of the Hsp90 C-terminal nucleotide-binding pocket. Curr Med Chem 2008;15:2702-2717.
5. Gunaherath GM, Marron MT, Wijeratne EM, Whitesell L, Gunatilaka AA: Synthesis and biological evaluation of novobiocin analogues as potential heat shock protein 90 inhibitors. Bioorg Med Chem 2013;21:5118-5129.
6. Neckers L: Heat shock protein 90: the cancer chaperone. J Biosci 2007;32:517-530.
7. Stravopodis DJ, Margaritis LH, Voutsinas GE: Drug-mediated targeted disruption of multiple protein activities through functional inhibition of the Hsp90 chaperone complex. Curr Med Chem 2007;14:3122-3138.
8. Lang F, Gulbins E, Lerche H, Huber SM, Kempe DS, Föller M: Eryptosis, a window to systemic disease. Cell Physiol Biochem 2008;22;373-380.
9. + channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 2003;285:C1553-C1560.
10. 2+ leak of human erythrocytes. Cell Physiol Biochem 2008;21:183-192.
11. Foller M, Sopjani M, Koka S, Gu S, Mahmud H, Wang K, Floride E, Schleicher E, Schulz E, Munzel T, Lang F: Regulation of erythrocyte survival by AMP-activated protein kinase. FASEB J 2009;23:1072-1080.
12. Lang PA, Kaiser S, Myssina S, Birka C, Weinstock C, Northoff H, Wieder T, Lang F, Huber SM: Effect of Vibrio parahaemolyticus haemolysin on human erythrocytes. Cell Microbiol 2004;6:391-400.
13. 2+ -dependent K transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 1993;92:520-526.
14. Berg CP, Engels IH, Rothbart A, Lauber K, Renz A, Schlosser SF, Schulze-Osthoff K, Wesselborg S: Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ 2001;8:1197-1206.
15. Lang F, Gulbins E, Lang PA, Zappulla D, Foller M: Ceramide in suicidal death of erythrocytes. Cell Physiol Biochem 2010;26:21-28.
16. Klarl BA, Lang PA, Kempe DS, Niemoeller OM, Akel A, Sobiesiak M, Eisele K, Podolski M, Huber SM, Wieder T, Lang F: Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion. Am J Physiol Cell Physiol 2006;290:C244-C253.
17. Bhavsar SK, Bobbala D, Xuan NT, Foller M, Lang F: Stimulation of suicidal erythrocyte death by alpha-lipoic acid. Cell Physiol Biochem 2010;26:859-868.
18. Foller M, Huber SM, Lang F: Erythrocyte programmed cell death. IUBMB Life 2008;60:661-668.
19. Foller M, Mahmud H, Gu S, Wang K, Floride E, Kucherenko Y, Luik S, Laufer S, Lang F: Participation of leukotriene C(4) in the regulation of suicidal erythrocyte death. J Physiol Pharmacol 2009;60:135-143.
20. Lau IP, Chen H, Wang J, Ong HC, Leung KC, Ho HP, Kong SK: In vitro effect of CTAB- and PEG-coated gold nanorods on the induction of eryptosis/ erythroptosis in human erythrocytes. Nanotoxicology 2012;6:847-856.
21. 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.
22. Foller M, Feil S, Ghoreschi K, Koka S, Gerling A, Thunemann M, Hofmann F, Schuler B, Vogel J, Pichler B, Kasinathan RS, Nicolay JP, Huber SM, Lang F, Feil R: Anemia and splenomegaly in cGKI-deficient mice. Proc Natl Acad Sci USA 2008;105:6771-6776.
23. Bhavsar SK, Gu S, Bobbala D, Lang F: Janus kinase 3 is expressed in erythrocytes, phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death. Cell Physiol Biochem 2011;27:547-556.
24. Kucherenko Y, Zelenak C, Eberhard M, Qadri SM, Lang F: Effect of casein kinase 1alpha activator pyrvinium pamoate on erythrocyte ion channels. Cell Physiol Biochem 2012;30:407-417.
25. Zelenak C, Eberhard M, Jilani K, Qadri SM, Macek B, Lang F: Protein kinase CK1alpha regulates erythrocyte survival. Cell Physiol Biochem 2012;29:171-180.
26. Gatidis S, Zelenak C, Fajol A, Lang E, Jilani K, Michael D, Qadri SM, Lang F: p38 MAPK activation and function following osmotic shock of erythrocytes. Cell Physiol Biochem 2011;28:1279-1286.
27. Zelenak C, Foller M, Velic A, Krug K, Qadri SM, Viollet B, Lang F, Macek B: Proteome analysis of erythrocytes lacking AMP-activated protein kinase reveals a role of PAK2 kinase in eryptosis. J Proteome Res 2011;10:1690-1697.
28. Lupescu A, Shaik N, Jilani K, Zelenak C, Lang E, Pasham V, Zbidah M, Plate A, Bitzer M, Foller M, Qadri SM, Lang F: Enhanced Erythrocyte Membrane Exposure of Phosphatidylserine Following Sorafenib Treatment: An in vivo and in vitro Study. Cell Physiol Biochem 2012;30:876-888.
29. Shaik N, Lupescu A, Lang F: Sunitinib-sensitive suicidal erythrocyte death. Cell Physiol Biochem 2012;30:512-522.
30. Abed M, Towhid ST, 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:C991-999.
31. Abed M, Towhid ST, Shaik N, Lang F: Stimulation of suicidal death of erythrocytes by rifampicin. Toxicology 2012;302:123-128.
32. Bottger E, Multhoff G, Kun JF, Esen M: Plasmodium falciparum-infected erythrocytes induce granzyme B by NK cells through expression of host-Hsp70. PLoS One 2012;7:e33774.
33. Felder KM, Hoelzle K, Ritzmann M, Kilchling T, Schiele D, Heinritzi K, Groebel K, Hoelzle LE: Hemotrophic mycoplasmas induce programmed cell death in red blood cells. Cell Physiol Biochem 2011;27:557-564.
34. Firat U, Kaya S, Cim A, Buyukbayram H, Gokalp O, Dal MS, Tamer MN: Increased caspase-3 immunoreactivity of erythrocytes in STZ diabetic rats. Exp Diabetes Res 2012;2012:316384.
35. Ganesan S, Chaurasiya ND, Sahu R, Walker LA, Tekwani BL: Understanding the mechanisms for metabolism-linked hemolytic toxicity of primaquine against glucose 6-phosphate dehydrogenase deficient human erythrocytes: evaluation of eryptotic pathway. Toxicology 2012;294:54-60.
36. 2+ rise and membrane permeabilization. Arch Toxicol 2012;86:741-752.
37. Ghashghaeinia M, Cluitmans JC, Akel A, Dreischer P, Toulany M, Koberle M, Skabytska Y, Saki M, Biedermann T, Duszenko M, Lang F, Wieder T, Bosman GJ: The impact of erythrocyte age on eryptosis. Br J Haematol 2012;157:606-614.
38. Ghashghaeinia M, Toulany M, Saki M, Bobbala D, Fehrenbacher B, Rupec R, Rodemann HP, Ghoreschi K, Rocken M, Schaller M, Lang F, Wieder T: The NFkB pathway inhibitors Bay 11-7082 and parthenolide induce programmed cell death in anucleated Erythrocytes. Cell Physiol Biochem 2011;27:45-54.
39. Jilani K, Lupescu A, Zbidah M, Abed M, Shaik N, Lang F: Enhanced Apoptotic Death of Erythrocytes Induced by the Mycotoxin Ochratoxin A. Kidney Blood Press Res 2012;36:107-118.
40. 2+ entry, ceramide formation and suicidal death of erythrocytes. Toxicol In Vitro 2013;27:52-58.
41. Kucherenko YV, Lang F: Inhibitory Effect of Furosemide on Non-Selective Voltage-Independent Cation Channels in Human Erythrocytes. Cell Physiol Biochem 2012;30:863-875.
42. Lang E, Jilani K, Zelenak C, Pasham V, Bobbala D, Qadri SM, Lang F: Stimulation of suicidal erythrocyte death by benzethonium. Cell Physiol Biochem 2011;28:347-354.
43. Lang E, Qadri SM, Jilani K, Zelenak C, Lupescu A, Schleicher E, Lang F: Carbon monoxide-sensitive apoptotic death of erythrocytes. Basic Clin Pharmacol Toxicol 2012;111:348-355.
44. Lang F, Qadri SM: Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif 2012;33:125-130.
45. 2+ Entry, Ceramide Formation, and Apoptotic Death of Erythrocytes Triggered by Plumbagin. J Nat Prod 2012;75:1956-1961.
46. Lupescu A, Jilani K, Zbidah M, Lang F: Induction of apoptotic erythrocyte death by rotenone. Toxicology 2012;300:132-137.
47. Lupescu A, Jilani K, Zelenak C, Zbidah M, Qadri SM, Lang F: Hexavalent chromium-induced erythrocyte membrane phospholipid asymmetry. Biometals 2012;25:309-318.
48. Polak-Jonkisz D, Purzyc L: Ca Influx versus Efflux during Eryptosis in Uremic Erythrocytes. Blood Purif 2012;34:209-210.
49. Qadri SM, Bauer J, Zelenak C, Mahmud H, Kucherenko Y, Lee SH, Ferlinz K, Lang F: Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death. Cell Physiol Biochem 2011;28:339-346.
50. Qadri SM, Kucherenko Y, Lang F: Beauvericin induced erythrocyte cell membrane scrambling. Toxicology 2011;283:24-31.
51. Qadri SM, Kucherenko Y, Zelenak C, Jilani K, Lang E, Lang F: Dicoumarol activates Ca -permeable cation channels triggering erythrocyte cell membrane scrambling. Cell Physiol Biochem 2011;28:857-864.
52. Qian EW, Ge DT, Kong SK: Salidroside protects human erythrocytes against hydrogen peroxide-induced apoptosis. J Nat Prod 2012;75:531-537.
53. 2+ entry and suicidal erythrocyte death by naringin. Cell Physiol Biochem 2012;30:678-686.
54. Vota DM, Maltaneri RE, Wenker SD, Nesse AB, Vittori DC: Differential erythropoietin action upon cells induced to eryptosis by different agents. Cell Biochem Biophys 2013;65:145-157.
55. 2+ dependent phosphatidylserine externalisation in red blood cells from normal individuals and sickle cell patients. Cell Calcium 2012;51:51-56.
56. Zappulla D: Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J Cardiometab Syndr 2008;3:30-34.
57. Zbidah M, Lupescu A, Jilani K, Lang F: Stimulation of suicidal erythrocyte death by fumagillin. Basic Clin Pharmacol Toxicol 2013;112:346-351.
58. Zbidah M, Lupescu A, Shaik N, Lang F: Gossypol-induced suicidal erythrocyte death. Toxicology 2012;302:101-105.
59. Zelenak C, Pasham V, Jilani K, Tripodi PM, Rosaclerio L, Pathare G, Lupescu A, Faggio C, Qadri SM, Lang F: Tanshinone IIA stimulates erythrocyte phosphatidylserine exposure. Cell Physiol Biochem 2012;30:282-294.
60. Lang E, Qadri SM, Lang F: Killing me softly - suicidal erythrocyte death. Int J Biochem Cell Biol 2012;44:1236-1243.
61. Calderon-Salinas JV, Munoz-Reyes EG, Guerrero-Romero JF, Rodriguez-Moran M, Bracho-Riquelme RL, Carrera-Gracia MA, Quintanar-Escorza MA: Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol Cell Biochem 2011;357:171-179.
62. Nicolay JP, Schneider J, Niemoeller OM, Artunc F, Portero-Otin M, Haik G Jr, Thornalley PJ, Schleicher E, Wieder T, Lang F: Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 2006;18:223-232.
63. Myssina S, Huber SM, Birka C, Lang PA, Lang KS, Friedrich B, Risler T, Wieder T, Lang F: Inhibition of erythrocyte cation channels by erythropoietin. J Am Soc Nephrol 2003;14:2750-2757.
64. Lang PA, Beringer O, Nicolay JP, Amon O, Kempe DS, Hermle T, Attanasio P, Akel A, Schafer R, Friedrich B, Risler T, Baur M, Olbricht CJ, Zimmerhackl LB, Zipfel PF, Wieder T, Lang F: Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med (Berl) 2006;84:378-388.
65. Kempe DS, Akel A, Lang PA, Hermle T, Biswas R, Muresanu J, Friedrich B, Dreischer P, Wolz C, Schumacher U, Peschel A, Gotz F, Doring G, Wieder T, Gulbins E, Lang F: Suicidal erythrocyte death in sepsis. J Mol Med 2007;85:269-277.
66. Bobbala D, Alesutan I, Foller M, Huber SM, Lang F: Effect of anandamide in Plasmodium Berghei-infected mice. Cell Physiol Biochem 2010;26:355-362.
67. Foller M, Bobbala D, Koka S, Huber SM, 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.
68. Koka S, Bobbala D, Lang C, Boini KM, Huber SM, Lang F: Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem 2009;23:191-198.
69. Lang PA, Schenck M, Nicolay JP, Becker JU, Kempe DS, Lupescu A, Koka S, Eisele K, Klarl BA, Rubben H, Schmid KW, Mann K, Hildenbrand S, Hefter H, Huber SM, Wieder T, Erhardt A, Haussinger D, Gulbins E, Lang F: Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 2007;13:164-170.
70. 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.
71. Lang PA, Kasinathan RS, Brand VB, Duranton C, Lang C, Koka S, Shumilina E, Kempe DS, Tanneur V, Akel A, Lang KS, Foller M, Kun JF, Kremsner PG, Wesselborg S, Laufer S, Clemen CS, Herr C, Noegel AA, Wieder T, Gulbins E, Lang F, Huber SM: Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem 2009;24:415-428.
72. Kempe DS, Lang PA, Duranton C, Akel A, Lang KS, Huber SM, Wieder T, Lang F: Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J 2006;20:368-370.
73. Qadri SM, Mahmud H, Lang E, Gu S, Bobbala D, Zelenak C, Jilani K, Siegfried A, Foller M, Lang F: Enhanced suicidal erythrocyte death in mice carrying a loss-of-function mutation of the adenomatous polyposis coli gene. J Cell Mol Med 2012;16:1085-1093.
74. Birka C, Lang PA, Kempe DS, Hoefling L, Tanneur V, Duranton C, Nammi S, Henke G, Myssina S, Krikov M, Huber SM, Wieder T, Lang F: Enhanced susceptibility to erythrocyte "apoptosis" following phosphate depletion. Pflugers Arch 2004;448:471-477.
75. Marcu MG, Schulte TW, Neckers L: Novobiocin and related coumarins and depletion of heat shock protein 90-dependent signaling proteins. J Natl Cancer Inst 2000;92:242-248.
76. Shelton SN, Shawgo ME, Matthews SB, Lu Y, Donnelly AC, Szabla K, Tanol M, Vielhauer GA, Rajewski RA, Matts RL, Blagg BS, Robertson JD: KU135, a novel novobiocin-derived C-terminal inhibitor of the 90-kDa heat shock protein, exerts potent antiproliferative effects in human leukemic cells. Mol Pharmacol 2009;76:1314-1322.
77. Calamia V, de Andres MC, Oreiro N, Ruiz-Romero C, Blanco FJ: Hsp90beta inhibition modulates nitric oxide production and nitric oxide-induced apoptosis in human chondrocytes. BMC Musculoskelet Disord 2011;12:237.
78. Singh G, Jayanarayan KG, Dey CS: Novobiocin induces apoptosis-like cell death in topoisomerase II over-expressing arsenite resistant Leishmania donovani. Mol Biochem Parasitol 2005;141:57-69.
79. Donnelly AC, Mays JR, Burlison JA, Nelson JT, Vielhauer G, Holzbeierlein J, Blagg BS: The design, synthesis, and evaluation of coumarin ring derivatives of the novobiocin scaffold that exhibit antiproliferative activity. J Org Chem 2008;73:8901-8920.
80. Burlison JA, Avila C, Vielhauer G, Lubbers DJ, Holzbeierlein J, Blagg BS: Development of novobiocin analogues that manifest anti-proliferative activity against several cancer cell lines. J Org Chem 2008;73:2130-2137.
81. Burlison JA, Neckers L, Smith AB, Maxwell A, Blagg BS: Novobiocin: redesigning a DNA gyrase inhibitor for selective inhibition of hsp90. J Am Chem Soc 2006;128:15529-15536.
82. Jung WS, Shin S, Park IK: Novobiocin inhibits the self-splicing of the primary transcripts of T4 phage thymidylate synthase gene. Mol Cell Biochem 2008;314:143-149.
83. Su Y, Hu P, Lee SH, Sinko PJ: Using novobiocin as a specific inhibitor of breast cancer resistant protein to assess the role of transporter in the absorption and disposition of topotecan. J Pharm Pharm Sci 2007;10:519-536.
84. Duan P, You G: Novobiocin is a potent inhibitor for human organic anion transporters. Drug Metab Dispos 2009;37:1203-1210.
85. Lu Y, Ansar S, Michaelis ML, Blagg BS: Neuroprotective activity and evaluation of Hsp90 inhibitors in an immortalized neuronal cell line. Bioorg Med Chem 2009;17:1709-1715.
86. Brand VB, Sandu CD, Duranton C, Tanneur V, Lang KS, Huber SM, Lang F: Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell Physiol Biochem 2003;13:347-356.
87. Bookchin RM, Ortiz OE, Lew VL: Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog Clin Biol Res 1987;240:193-200.
88. Harrison HE, Bunting H, Ordway NK, Albrink WS: The Pathogenesis of the Renal Injury Produced in the Dog by Hemoglobin or Methemoglobin. J Exp Med 1947;86:339-356.
89. Borst O, Abed M, Alesutan I, Towhid ST, Qadri SM, 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.
90. Andrews DA, Low PS: Role of red blood cells in thrombosis. Curr Opin Hematol 1999;6:76-82.
91. Closse C, Dachary-Prigent J, Boisseau MR: Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999;107:300-302.
92. Gallagher PG, Chang SH, Rettig MP, Neely JE, Hillery CA, Smith BD, Low PS: Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 2003;101:4625-4627.
93. 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.
94. Wood BL, Gibson DF, Tait JF: Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 1996;88:1873-1880.
95. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS, Chung JH: Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 2007;27:414-421.
96. Zwaal RF, Comfurius P, Bevers EM: Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005;62:971-988.