Licochalcone A Induced Suicidal Death of Human Erythrocytes

Cellular Physiology and Biochemistry

Volumn 37, Issue 5, 2015, Pages 2060-2070

  Egler, Jasmin ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Calcium; Cell volume; Eryptosis; Oxidative stress; Phosphatidylserine

Indexed keywords

CERAMIDE; FLUO 3; HEMOGLOBIN; LICOCHALCONE A; LIPOCORTIN 5; PHOSPHATIDYLSERINE; ANILINE DERIVATIVE; CALCIUM; CHALCONE DERIVATIVE; XANTHENE DERIVATIVE;

ARTICLE; CELL SURFACE; CELL VOLUME; DRUG EFFECT; DRUG EXPOSURE; ERYTHROCYTE; EXTRACELLULAR CALCIUM; FLOW CYTOMETRY; FLUORESCENCE; HEMOGLOBIN BLOOD LEVEL; HEMOLYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; SUICIDE; APOPTOSIS; CELL SIZE; DRUG EFFECTS; METABOLISM;

ANILINE COMPOUNDS; APOPTOSIS; CALCIUM; CELL SIZE; CERAMIDES; CHALCONES; ERYTHROCYTES; FLOW CYTOMETRY; HEMOLYSIS; HUMANS; PHOSPHATIDYLSERINES; XANTHENES;

EID: 84948173022     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000438565     Document Type: Article

References (96)

1. Dunlap TL, Wang S, Simmler C, Chen SN, Pauli GF, Dietz BM, Bolton JL: Differential Effects of Glycyrrhiza Species on Genotoxic Estrogen Metabolism: Licochalcone A Downregulates P450 1B1, whereas Isoliquiritigenin Stimulates It. Chem Res Toxicol 2015;28:1584-1594.
2. Tsai JP, Hsiao PC, Yang SF, Hsieh SC, Bau DT, Ling CL, Pai CL, Hsieh YH: Licochalcone A suppresses migration and invasion of human hepatocellular carcinoma cells through downregulation of MKK4/JNK via NF-kappaB mediated urokinase plasminogen activator expression. PLoS One 2014;9:e86537.
3. Zhao H, Jiang JT, Zheng QS: [Advance in studies on pharmacological effects of licochalcone A]. Zhongguo Zhong Yao Za Zhi 2013;38:3814-3818.
4. Park JM, Park SH, Hong KS, Han YM, Jang SH, Kim EH, Hahm KB: Special licorice extracts containing lowered glycyrrhizin and enhanced licochalcone A prevented Helicobacter pylori-initiated, salt diet-promoted gastric tumorigenesis. Helicobacter 2014;19:221-236.
5. Feldman M, Grenier D: Cranberry proanthocyanidins act in synergy with licochalcone A to reduce Porphyromonas gingivalis growth and virulence properties, and to suppress cytokine secretion by macrophages. J Appl Microbiol 2012;113:438-447.
6. Fontes LB, Dos Santos Dias D, de Carvalho LS, Mesquita HL, da Silva Reis L, Dias AT, Da Silva Filho AA, do Amaral Correa JO: Immunomodulatory effects of licochalcone A on experimental autoimmune encephalomyelitis. J Pharm Pharmacol 2014;66:886-894.
7. Kim JS, Park MR, Lee SY, Kim do K, Moon SM, Kim CS, Cho SS, Yoon G, Im HJ, You JS, Oh JS, Kim SG: Licochalcone A induces apoptosis in KB human oral cancer cells via a caspase-dependent FasL signaling pathway. Oncol Rep 2014;31:755-762.
8. Hao H, Hui W, Liu P, Lv Q, Zeng X, Jiang H, Wang Y, Zheng X, Zheng Y, Li J, Zhou X, Jiang Y: Effect of licochalcone A on growth and properties of Streptococcus suis. PLoS One 2013;8:e67728.
9. Shen H, Zeng G, Tang G, Cai X, Bi L, Huang C, Yang Y: Antimetastatic effects of licochalcone A on oral cancer via regulating metastasis-associated proteases. Tumour Biol 2014;35:7467-7474.
10. Shang F, Ming L, Zhou Z, Yu Y, Sun J, Ding Y, Jin Y: The effect of licochalcone A on cell-aggregates ECM secretion and osteogenic differentiation during bone formation in metaphyseal defects in ovariectomized rats. Biomaterials 2014;35:2789-2797.
11. Yao K, Chen H, Lee MH, Li H, Ma W, Peng C, Song NR, Lee KW, Bode AM, Dong Z, Dong Z: Licochalcone A, a natural inhibitor of c-Jun N-terminal kinase 1. Cancer Prev Res (Phila) 2014;7:139-149.
12. Tsai JP, Lee CH, Ying TH, Lin CL, Lin CL, Hsueh JT, Hsieh YH: Licochalcone A induces autophagy through PI3K/Akt/mTOR inactivation and autophagy suppression enhances Licochalcone A-induced apoptosis of human cervical cancer cells. Oncotarget 2015;
13. Cho JJ, Chae JI, Yoon G, Kim KH, Cho JH, Cho SS, Cho YS, Shim JH: Licochalcone A, a natural chalconoid isolated from Glycyrrhiza inflata root, induces apoptosis via Sp1 and Sp1 regulatory proteins in oral squamous cell carcinoma. Int J Oncol 2014;45:667-674.
14. Zeng G, Shen H, Yang Y, Cai X, Xun W: Licochalcone A as a potent antitumor agent suppresses growth of human oral cancer SCC-25 cells in vitro via caspase-3 dependent pathways. Tumour Biol 2014;35:6549-6555.
15. Park MR, Kim SG, Cho IA, Oh D, Kang KR, Lee SY, Moon SM, Cho SS, Yoon G, Kim CS, Oh JS, You JS, Kim do K, Seo YS, Im HJ, Kim JS: Licochalcone-A induces intrinsic and extrinsic apoptosis via ERK1/2 and p38 phosphorylation-mediated TRAIL expression in head and neck squamous carcinoma FaDu cells. Food Chem Toxicol 2015;77:34-43.
16. Yang P, Tuo L, Wu Q, Cao X: Licochalcone-A sensitizes human esophageal carcinoma cells to TRAIL-mediated apoptosis by proteasomal degradation of XIAP. Hepatogastroenterology 2014;61:1229-1234.
17. Hao W, Yuan X, Yu L, Gao C, Sun X, Wang D, Zheng Q: Licochalcone A-induced human gastric cancer BGC-823 cells apoptosis by regulating ROS-mediated MAPKs and PI3K/AKT signaling pathways. Sci Rep 2015;5:10336.
18. Xiao XY, Hao M, Yang XY, Ba Q, Li M, Ni SJ, Wang LS, Du X: Licochalcone A inhibits growth of gastric cancer cells by arresting cell cycle progression and inducing apoptosis. Cancer Lett 2011;302:69-75.
19. Choi AY, Choi JH, Hwang KY, Jeong YJ, Choe W, Yoon KS, Ha J, Kim SS, Youn JH, Yeo EJ, Kang I: Licochalcone A induces apoptosis through endoplasmic reticulum stress via a phospholipase Cgamma1-, Ca(2+)-, and reactive oxygen species-dependent pathway in HepG2 human hepatocellular carcinoma cells. Apoptosis 2014;19:682-697.
20. Kim KH, Yoon G, Cho JJ, Cho JH, Cho YS, Chae JI, Shim JH: Licochalcone A induces apoptosis in malignant pleural mesothelioma through downregulation of Sp1 and subsequent activation of mitochondria-related apoptotic pathway. Int J Oncol 2015;46:1385-1392.
21. Jiang J, Yuan X, Zhao H, Yan X, Sun X, Zheng Q: Licochalcone A inhibiting proliferation of bladder cancer T24 cells by inducing reactive oxygen species production. Biomed Mater Eng 2014;24:1019-1025.
22. Yuan X, Li D, Zhao H, Jiang J, Wang P, Ma X, Sun X, Zheng Q: Licochalcone A-induced human bladder cancer T24 cells apoptosis triggered by mitochondria dysfunction and endoplasmic reticulum stress. Biomed Res Int 2013;2013:474272.
23. Fu Y, Hsieh TC, Guo J, Kunicki J, Lee MY, Darzynkiewicz Z, Wu JM: Licochalcone-A, a novel flavonoid isolated from licorice root (Glycyrrhiza glabra), causes G2 and late-G1 arrests in androgen-independent PC-3 prostate cancer cells. Biochem Biophys Res Commun 2004;322:263-270.
24. Rafi MM, Rosen RT, Vassil A, Ho CT, Zhang H, Ghai G, Lambert G, DiPaola RS: Modulation of bcl-2 and cytotoxicity by licochalcone-A, a novel estrogenic flavonoid. Anticancer Res 2000;20:2653-2658.
25. Yo YT, Shieh GS, Hsu KF, Wu CL, Shiau AL: Licorice and licochalcone-A induce autophagy in LNCaP prostate cancer cells by suppression of Bcl-2 expression and the mTOR pathway. J Agric Food Chem 2009;57:8266-8273.
26. Kim YJ, Jung EB, Myung SC, Kim W, Lee CS: Licochalcone A enhances geldanamycin-induced apoptosis through reactive oxygen species-mediated caspase activation. Pharmacology 2013;92:49-59.
27. Lee CS, Kwak SW, Kim YJ, Lee SA, Park ES, Myung SC, Kim W, Lee MS, Lee JJ: Guanylate cyclase activator YC-1 potentiates apoptotic effect of licochalcone A on human epithelial ovarian carcinoma cells via activation of death receptor and mitochondrial pathways. Eur J Pharmacol 2012;683:54-62.
28. Huang HC, Tsai LL, Tsai JP, Hsieh SC, Yang SF, Hsueh JT, Hsieh YH: Licochalcone A inhibits the migration and invasion of human lung cancer cells via inactivation of the Akt signaling pathway with downregulation of MMP-1/-3 expression. Tumour Biol 2014;35:12139-12149.
29. Funakoshi-Tago M, Tago K, Nishizawa C, Takahashi K, Mashino T, Iwata S, Inoue H, Sonoda Y, Kasahara T: Licochalcone A is a potent inhibitor of TEL-Jak2-mediated transformation through the specific inhibition of Stat3 activation. Biochem Pharmacol 2008;76:1681-1693.
30. Park SY, Kim EJ, Choi HJ, Seon MR, Lim SS, Kang YH, Choi MS, Lee KW, Yoon Park JH: Anti-carcinogenic effects of non-polar components containing licochalcone A in roasted licorice root. Nutr Res Pract 2014;8:257-266.
31. Song NR, Kim JE, Park JS, Kim JR, Kang H, Lee E, Kang YG, Son JE, Seo SG, Heo YS, Lee KW: Licochalcone A, a polyphenol present in licorice, suppresses UV-induced COX-2 expression by targeting PI3K, MEK1, and B-Raf. Int J Mol Sci 2015;16:4453-4470.
32. He W, Wu JJ, Ning J, Hou J, Xin H, He YQ, Ge GB, Xu W: Inhibition of human cytochrome P450 enzymes by licochalcone A, a naturally occurring constituent of licorice. Toxicol In Vitro 2015;29:1569-1576.
33. Kuhnl J, Roggenkamp D, Gehrke SA, Stab F, Wenck H, Kolbe L, Neufang G: Licochalcone A activates Nrf2 in vitro and contributes to licorice extract-induced lowered cutaneous oxidative stress in vivo. Exp Dermatol 2015;24:42-47.
34. Han J, Wang D, Yu B, Wang Y, Ren H, Zhang B, Wang Y, Zheng Q: Cardioprotection against ischemia/reperfusion by licochalcone B in isolated rat hearts. Oxid Med Cell Longev 2014;2014:134862.
35. Yuan X, Niu HT, Wang PL, Lu J, Zhao H, Liu SH, Zheng QS, Li CG: Cardioprotective Effect of Licochalcone D against Myocardial Ischemia/Reperfusion Injury in Langendorff-Perfused Rat Hearts. PLoS One 2015;10:e0128375.
36. Zhou M, Liu L, Wang W, Han J, Ren H, Zheng Q, Wang D: Role of licochalcone C in cardioprotection against ischemia/reperfusion injury of isolated rat heart via antioxidant, anti-inflammatory, and anti-apoptotic activities. Life Sci 2015;132:27-33.
37. Han JY, Park SH, Yang JH, Kim MG, Cho SS, Yoon G, Cheon SH, Ki SH: Licochalcone Suppresses LXRalpha-Induced Hepatic Lipogenic Gene Expression through AMPK/Sirt1 Pathway Activation. Toxicol Res 2014;30:19-25.
38. Wananukul S, Chatproedprai S, Chunharas A, Limpongsanuruk W, Singalavanija S, Nitiyarom R, Wisuthsarewong W: Randomized, double-blind, split-side, comparison study of moisturizer containing licochalcone A and 1% hydrocortisone in the treatment of childhood atopic dermatitis. J Med Assoc Thai 2013;96:1135-1142.
39. Chu X, Jiang L, Wei M, Yang X, Guan M, Xie X, Wei J, Liu D, Wang D: Attenuation of allergic airway inflammation in a murine model of asthma by Licochalcone A. Immunopharmacol Immunotoxicol 2013;35:653-661.
40. Kim SH, Yang M, Xu JG, Yu X, Qian XJ: Role of licochalcone A on thymic stromal lymphopoietin expression: implications for asthma. Exp Biol Med (Maywood) 2015;240:26-33.
41. Ming L, Jin F, Huang P, Luo H, Liu W, Zhang L, Yuan W, Zhang Y, Jin Y: Licochalcone A up-regulates of FasL in mesenchymal stem cells to strengthen bone formation and increase bone mass. Sci Rep 2014;4:7209.
42. Oh GS, Lee GG, Yoon J, Oh WK, Kim SW: Selective inhibition of liver X receptor alpha-mediated lipogenesis in primary hepatocytes by licochalcone A. Chin Med 2015;10:8.
43. Quan HY, Baek NI, Chung SH: Licochalcone A prevents adipocyte differentiation and lipogenesis via suppression of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein pathways. J Agric Food Chem 2012;60:5112-5120.
44. Quan HY, Kim SJ, Kim do Y, Jo HK, Kim GW, Chung SH: Licochalcone A regulates hepatic lipid metabolism through activation of AMP-activated protein kinase. Fitoterapia 2013;86:208-216.
45. Bak EJ, Choi KC, Jang S, Woo GH, Yoon HG, Na Y, Yoo YJ, Lee Y, Jeong Y, Cha JH: Licochalcone F alleviates glucose tolerance and chronic inflammation in diet-induced obese mice through Akt and p38 MAPK. Clin Nutr 2015;10.1016/j.clnu.2015.03.005
46. Yuan X, Li T, Xiao E, Zhao H, Li Y, Fu S, Gan L, Wang Z, Zheng Q, Wang Z: Licochalcone B inhibits growth of bladder cancer cells by arresting cell cycle progression and inducing apoptosis. Food Chem Toxicol 2014;65:242-251.
47. Zhao H, Yuan X, Jiang J, Wang P, Sun X, Wang D, Zheng Q: Antimetastatic effects of licochalcone B on human bladder carcinoma T24 by inhibition of matrix metalloproteinases-9 and NF-small ka, CyrillicB activity. Basic Clin Pharmacol Toxicol 2014;115:527-533.
48. Chang HJ, Yoon G, Park JS, Kim MH, Baek MK, Kim NH, Shin BA, Ahn BW, Cheon SH, Jung YD: Induction of apoptosis by the licochalcone E in endothelial cells via modulation of NF-kappaB and Bcl-2 Family. Biol Pharm Bull 2007;30:2290-2293.
49. Kwon SJ, Park SY, Kwon GT, Lee KW, Kang YH, Choi MS, Yun JW, Jeon JH, Jun JG, Park JH: Licochalcone E present in licorice suppresses lung metastasis in the 4T1 mammary orthotopic cancer model. Cancer Prev Res (Phila) 2013;6:603-613.
50. Zhou T, Deng X, Qiu J: Antimicrobial activity of licochalcone E against Staphylococcus aureus and its impact on the production of staphylococcal alpha-toxin. J Microbiol Biotechnol 2012;22:800-805.
51. Lang E, Qadri SM, Lang F: Killing me softly-suicidal erythrocyte death. Int J Biochem Cell Biol 2012;44:1236-1243.
52. Lang PA, Kaiser S, Myssina S, Wieder T, Lang F, Huber SM: Role of Ca2+-activated K+ channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 2003;285:C1553-C1560.
53. 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.
54. 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.
55. Andrews DA, Low PS: Role of red blood cells in thrombosis. Curr Opin Hematol 1999;6:76-82.
56. 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.
57. Zwaal RF, Comfurius P, Bevers EM: Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005;62:971-988.
58. 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.
59. Closse C, Dachary-Prigent J, Boisseau MR: Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999;107:300-302.
60. Gallagher PG, Chang SH, Rettig M P, Neely JE, Hillery CA, Smith BD, Low PS: Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 2003;101:4625-4627.
61. 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.
62. 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.
63. Abed M, Feger M, Alzoubi K, Pakladok T, Frauenfeld L, Geiger C, Towhid ST, Lang F: Sensitization of erythrocytes to suicidal erythrocyte death following water deprivation. Kidney Blood Press Res 2013;37:567-578.
64. Voelkl J, Alzoubi K, Mamar AK, Ahmed MS, Abed M, Lang F: Stimulation of suicidal erythrocyte death by increased extracellular phosphate concentrations. Kidney Blood Press Res 2013;38:42-51.
65. Abed M, Artunc F, Alzoubi K, Honisch S, Baumann D, Foller M, Lang F: Suicidal erythrocyte death in end-stage renal disease. J Mol Med (Berl) 2014;92:871-879.
66. Ahmed MS, Langer H, Abed M, Voelkl J, Lang F: The uremic toxin acrolein promotes suicidal erythrocyte death. Kidney Blood Press Res 2013;37:158-167.
67. Polak-Jonkisz D, Purzyc L: Ca(2+) influx versus efflux during eryptosis in uremic erythrocytes. Blood Purif 2012;34:209-210; author reply 210.
68. 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.
69. 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.
70. Nicolay J P, 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.
71. Lang E, Gatidis S, Freise NF, Bock H, Kubitz R, Lauermann C, Orth HM, Klindt C, Schuier M, Keitel V, Reich M, Liu G, Schmidt S, Xu HC, Qadri SM, Herebian D, Pandyra AA, Mayatepek E, Gulbins E, Lang F, Haussinger D, Lang KS, Foller M, Lang PA: Conjugated bilirubin triggers anemia by inducing erythrocyte death. Hepatology 2015;61:275-284.
72. 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 (Berl) 2007;85:273-281.
73. 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.
74. Jilani K, Lang F: Carmustine-induced phosphatidylserine translocation in the erythrocyte membrane. Toxins (Basel) 2013;5:703-716.
75. 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.
76. Zappulla D: Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J Cardiometab Syndr 2008;3:30-34.
77. Lupescu A, Jilani K, Zbidah M, Lang F: Patulin-induced suicidal erythrocyte death. Cell Physiol Biochem 2013;32:291-299.
78. Abed M, Zoubi KA, Theurer M, Lang F: Effect of dermaseptin on erythrocytes. Basic Clin Pharmacol Toxicol 2013;113:347-352.
79. Ghashghaeinia M, Cluitmans JC, Toulany M, Saki M, Koberle M, Lang E, Dreischer P, Biedermann T, Duszenko M, Lang F, Bosman GJ, Wieder T: Age Sensitivity of NFkappaB Abundance and Programmed Cell Death in Erythrocytes Induced by NFkappaB Inhibitors. Cell Physiol Biochem 2013;32:801-813.
80. Alzoubi K, Honisch S, Abed M, Lang F: Triggering of Suicidal Erythrocyte Death by Penta-O-galloyl-beta-d-glucose. Toxins (Basel) 2014;6:54-65.
81. Jilani K, Enkel S, Bissinger R, Almilaji A, Abed M, Lang F: Fluoxetine induced suicidal erythrocyte death. Toxins (Basel) 2013;5:1230-1243.
82. Lupescu A, Bissinger R, Jilani K, Lang F: Triggering of suicidal erythrocyte death by celecoxib. Toxins (Basel) 2013;5:1543-1554.
83. 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.
84. Oswald G, Alzoubi K, Abed M, Lang F: Stimulation of suicidal erythrocyte death by ribavirin. Basic Clin Pharmacol Toxicol 2014;114:311-317.
85. 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.
86. 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.
87. Arnold M, Bissinger R, Lang F: Mitoxantrone-induced suicidal erythrocyte death. Cell Physiol Biochem 2014;34:1756-1767.
88. Bissinger R, Fischer S, Jilani K, Lang F: Stimulation of Erythrocyte Death by Phloretin. Cell Physiol Biochem 2014;34:2256-2265.
89. Bissinger R, Lupescu A, Zelenak C, Jilani K, Lang F: Stimulation of eryptosis by cryptotanshinone. Cell Physiol Biochem 2014;34:432-442.
90. 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.
91. 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.
92. 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.
93. 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.
94. Tesoriere L, Attanzio A, Allegra M, Cilla A, Gentile C, Livrea MA: Oxysterol mixture in hypercholesterolemia-relevant proportion causes oxidative stress-dependent eryptosis. Cell Physiol Biochem 2014;34:1075-1089.
95. 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.
96. Pagano M, Faggio C: The use of erythrocyte fragility to assess xenobiotic cytotoxicity. Cell Biochem Funct 2015;33:351-355.