Stimulation of eryptosis by combretastatin A4 phosphate disodium (CA4P)

Cellular Physiology and Biochemistry

Volumn 38, Issue 3, 2016, Pages 969-981

  Signoretto, Elena ^a,b   Bissinger, Rosi ^a   Castagna, Michela ^b   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Calcium; Cell membrane scrambling; Cell volume; Eryptosis; Phosphatidylserine

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; COMBRETASTATIN A4 PHOSPHATE; GLUTATHIONE; HEMOGLOBIN; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; CERAMIDE; STILBENE DERIVATIVE;

ARTICLE; CELL DEATH; CELL STIMULATION; CONTROLLED STUDY; CYTOTOXICITY; ERYTHROCYTE MEMBRANE; ERYTHROCYTE VOLUME; EXTRACELLULAR CALCIUM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HEMOGLOBIN DETERMINATION; HEMOLYSIS; HUMAN; HUMAN CELL; NORMAL HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; CELL SIZE; CYTOLOGY; DRUG EFFECTS; ERYPTOSIS; ERYTHROCYTE; METABOLISM;

CALCIUM; CELL SIZE; CERAMIDES; ERYPTOSIS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; GLUTATHIONE; HUMANS; PHOSPHATIDYLSERINES; REACTIVE OXYGEN SPECIES; STILBENES;

EID: 84962469235     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000443049     Document Type: Article

References (120)

1. Abma E, Daminet S, Smets P, Ni Y, de Rooster H: Combretastatin A4-phosphate and its potential in veterinary oncology: a review. Vet Comp Oncol 2015;10.1111/vco.12150
2. Daswani VP, Ayesa U, Venegas B, Chong PL: Concentration-Induced J-Aggregate Formation Causes a Biphasic Change in the Release of trans-Combretastatin A4 Disodium Phosphate from Archaeosomes and the Subsequent Cytotoxicity on Mammary Cancer Cells. Mol Pharm 2015;12:3724-3734.
3. Feng D, Menger MD, Laschke MW: Vascular disrupting effects of combretastatin A4 phosphate on murine endometriotic lesions. Fertil Steril 2013;100:1459-1467.
4. Greene LM, O'Boyle NM, Nolan DP, Meegan MJ, Zisterer DM: The vascular targeting agent Combretastatin-A4 directly induces autophagy in adenocarcinoma-Derived colon cancer cells. Biochem Pharmacol 2012;84:612-624.
5. Li J, Chen F, Feng Y, Cona MM, Yu J, Verbruggen A, Zhang J, Oyen R, Ni Y: Diverse responses to vascular disrupting agent combretastatin a4 phosphate: a comparative study in rats with hepatic and subcutaneous tumor allografts using MRI biomarkers, microangiography, and histopathology. Transl Oncol 2013;6:42-50.
6. Liu P, Qin Y, Wu L, Yang S, Li N, Wang H, Xu H, Sun K, Zhang S, Han X, Sun Y, Shi Y: A phase I clinical trial assessing the safety and tolerability of combretastatin A4 phosphate injections. Anticancer Drugs 2014;25:462-471.
7. Nagaiah G, Remick SC: Combretastatin A4 phosphate: a novel vascular disrupting agent. Future Oncol 2010;6:1219-1228.
8. Su J, Laursen BE, Eskildsen-Helmond Y, Horsman MR, Simonsen U: The vascular-Disrupting agent, combretastatin-A4-phosphate, enhances neurogenic vasoconstriction in rat small arteries. Eur J Pharmacol 2012;695:104-111.
9. Welford AF, Biziato D, Coffelt SB, Nucera S, Fisher M, Pucci F, Di Serio C, Naldini L, De Palma M, Tozer GM, Lewis CE: TIE2-Expressing macrophages limit the therapeutic efficacy of the vascular-Disrupting agent combretastatin A4 phosphate in mice. J Clin Invest 2011;121:1969-1973.
10. Zhu J, Xu X, Hu M, Qiu L: Co-Encapsulation of Combretastatin-A4 Phosphate and Doxorubicin in Polymersomes for Synergistic Therapy of Nasopharyngeal Epidermal Carcinoma. J Biomed Nanotechnol 2015;11:997-1006.
11. Siemann DW, Chaplin DJ, Walicke PA: A review and update of the current status of the vasculature-Disabling agent combretastatin-A4 phosphate (CA4P). Expert Opin Investig Drugs 2009;18:189-197.
12. Wang H, Sun X, Chen F, De Keyzer F, Yu J, Landuyt W, Vandecaveye V, Peeters R, Bosmans H, Hermans R, Marchal G, Ni Y: Treatment of rodent liver tumor with combretastatin a4 phosphate: noninvasive therapeutic evaluation using multiparametric magnetic resonance imaging in correlation with microangiography and histology. Invest Radiol 2009;44:44-53.
13. Chen G, Horsman MR, Pedersen M, Pang Q, Stodkilde-Jorgensen H: The effect of combretastatin A4 disodium phosphate and 5,6-Dimethylxanthenone-4-Acetic acid on water diffusion and blood perfusion in tumours. Acta Oncol 2008;47:1071-1076.
14. Gaya A, Daley F, Taylor NJ, Tozer G, Qureshi U, Padhani A, Pedley RB, Begent R, Wellsted D, Stirling JJ, Rustin G: Relationship between human tumour angiogenic profile and combretastatin-induced vascular shutdown: an exploratory study. Br J Cancer 2008;99:321-326.
15. McPhail LD, Griffiths JR, Robinson SP: Assessment of tumor response to the vascular disrupting agents 5,6-Dimethylxanthenone-4-Acetic acid or combretastatin-A4-phosphate by intrinsic susceptibility magnetic resonance imaging. Int J Radiat Oncol Biol Phys 2007;69:1238-1245.
16. Zhao D, Richer E, Antich PP, Mason RP: Antivascular effects of combretastatin A4 phosphate in breast cancer xenograft assessed using dynamic bioluminescence imaging and confirmed by MRI. FASEB J 2008;22:2445-2451.
17. Ley CD, Horsman MR, Kristjansen PE: Early effects of combretastatin-A4 disodium phosphate on tumor perfusion and interstitial fluid pressure. Neoplasia 2007;9:108-112.
18. Ng QS, Goh V, Carnell D, Meer K, Padhani AR, Saunders MI, Hoskin PJ: Tumor antivascular effects of radiotherapy combined with combretastatin a4 phosphate in human non-small-cell lung cancer. Int J Radiat Oncol Biol Phys 2007;67:1375-1380.
19. Cooney MM, Ortiz J, Bukowski RM, Remick SC: Novel vascular targeting/disrupting agents: combretastatin A4 phosphate and related compounds. Curr Oncol Rep 2005;7:90-95.
20. Vincent L, Kermani P, Young LM, Cheng J, Zhang F, Shido K, Lam G, Bompais-Vincent H, Zhu Z, Hicklin DJ, Bohlen P, Chaplin DJ, May C, Rafii S: Combretastatin A4 phosphate induces rapid regression of tumor neovessels and growth through interference with vascular endothelial-cadherin signaling. J Clin Invest 2005;115:2992-3006.
21. Zhao D, Jiang L, Hahn EW, Mason RP: Tumor physiologic response to combretastatin A4 phosphate assessed by MRI. Int J Radiat Oncol Biol Phys 2005;62:872-880.
22. West CM, Price P: Combretastatin A4 phosphate. Anticancer Drugs 2004;15:179-187.
23. Anderson HL, Yap JT, Miller MP, Robbins A, Jones T, Price PM: Assessment of pharmacodynamic vascular response in a phase I trial of combretastatin A4 phosphate. J Clin Oncol 2003;21:2823-2830.
24. Chaplin DJ: Drug based approaches for targeting tumor vasculature: development of combretastatin A4 phosphate. Pathophysiol Haemost Thromb 2003;33:S9-10.
25. Galbraith SM, Maxwell RJ, Lodge MA, Tozer GM, Wilson J, Taylor NJ, Stirling JJ, Sena L, Padhani AR, Rustin GJ: Combretastatin A4 phosphate has tumor antivascular activity in rat and man as demonstrated by dynamic magnetic resonance imaging. J Clin Oncol 2003;21:2831-2842.
26. Stevenson JP, Rosen M, Sun W, Gallagher M, Haller DG, Vaughn D, Giantonio B, Zimmer R, Petros WP, Stratford M, Chaplin D, Young SL, Schnall M, O'Dwyer PJ: Phase I trial of the antivascular agent combretastatin A4 phosphate on a 5-Day schedule to patients with cancer: magnetic resonance imaging evidence for altered tumor blood flow. J Clin Oncol 2003;21:4428-4438.
27. Chaplin DJ, Hill SA: The development of combretastatin A4 phosphate as a vascular targeting agent. Int J Radiat Oncol Biol Phys 2002;54:1491-1496.
28. Dowlati A, Robertson K, Cooney M, Petros WP, Stratford M, Jesberger J, Rafie N, Overmoyer B, Makkar V, Stambler B, Taylor A, Waas J, Lewin JS, McCrae KR, Remick SC: A phase I pharmacokinetic and translational study of the novel vascular targeting agent combretastatin a-4 phosphate on a single-Dose intravenous schedule in patients with advanced cancer. Cancer Res 2002;62:3408-3416.
29. Rojiani AM, Li L, Rise L, Siemann DW: Activity of the vascular targeting agent combretastatin A-4 disodium phosphate in a xenograft model of AIDS-Associated Kaposi's sarcoma. Acta Oncol 2002;41:98-105.
30. Beauregard DA, Hill SA, Chaplin DJ, Brindle KM: The susceptibility of tumors to the antivascular drug combretastatin A4 phosphate correlates with vascular permeability. Cancer Res 2001;61:6811-6815.
31. Beauregard DA, Pedley RB, Hill SA, Brindle KM: Differential sensitivity of two adenocarcinoma xenografts to the anti-vascular drugs combretastatin A4 phosphate and 5,6-Dimethylxanthenone-4-Acetic acid, assessed using MRI and MRS. NMR Biomed 2002;15:99-105.
32. Griggs J, Metcalfe JC, Hesketh R: Targeting tumour vasculature: the development of combretastatin A4. Lancet Oncol 2001;2:82-87.
33. Griggs J, Hesketh R, Smith GA, Brindle KM, Metcalfe JC, Thomas GA, Williams ED: Combretastatin-A4 disrupts neovascular development in non-neoplastic tissue. Br J Cancer 2001;84:832-835.
34. Beauregard DA, Thelwall PE, Chaplin DJ, Hill SA, Adams GE, Brindle KM: Magnetic resonance imaging and spectroscopy of combretastatin A4 prodrug-induced disruption of tumour perfusion and energetic status. Br J Cancer 1998;77:1761-1767.
35. Chaplin DJ, Pettit GR, Hill SA: Anti-vascular approaches to solid tumour therapy: evaluation of combretastatin A4 phosphate. Anticancer Res 1999;19:189-195.
36. Wakaskar RR, Bathena SP, Tallapaka SB, Ambardekar VV, Gautam N, Thakare R, Simet SM, Curran SM, Singh RK, Dong Y, Vetro JA: Peripherally cross-linking the shell of core-shell polymer micelles decreases premature release of physically loaded combretastatin A4 in whole blood and increases its mean residence time and subsequent potency against primary murine breast tumors after IV administration. Pharm Res 2015;32:1028-1044.
37. Yao N, Ren K, Jiang C, Gao M, Huang D, Lu X, Lou B, Peng F, Yang A, Wang X, Ni Y, Zhang J: Combretastatin A4 phosphate treatment induces vasculogenic mimicry formation of W256 breast carcinoma tumor in vitro and in vivo. Tumour Biol 2015;36:8499-8510.
38. Li J, Cona MM, Chen F, Feng Y, Zhou L, Zhang G, Nuyts J, de Witte P, Zhang J, Yu J, Oyen R, Verbruggen A, Ni Y: Sequential systemic administrations of combretastatin A4 Phosphate and radioiodinated hypericin exert synergistic targeted theranostic effects with prolonged survival on SCID mice carrying bifocal tumor xenografts. Theranostics 2013;3:127-137.
39. Fu XH, Li J, Zou Y, Hong YR, Fu ZX, Huang JJ, Zhang SZ, Zheng S: Endostar enhances the antineoplastic effects of combretastatin A4 phosphate in an osteosarcoma xenograft. Cancer Lett 2011;312:109-116.
40. Nathan P, Zweifel M, Padhani AR, Koh DM, Ng M, Collins DJ, Harris A, Carden C, Smythe J, Fisher N, Taylor NJ, Stirling JJ, Lu SP, Leach MO, Rustin GJ, Judson I: Phase I trial of combretastatin A4 phosphate (CA4P) in combination with bevacizumab in patients with advanced cancer. Clin Cancer Res 2012;18:3428-3439.
41. He X, Li S, Huang H, Li Z, Chen L, Ye S, Huang J, Zhan J, Lin T: A pharmacokinetic and safety study of single dose intravenous combretastatin A4 phosphate in Chinese patients with refractory solid tumours. Br J Clin Pharmacol 2011;71:860-870.
42. Ng QS, Mandeville H, Goh V, Alonzi R, Milner J, Carnell D, Meer K, Padhani AR, Saunders MI, Hoskin PJ: Phase Ib trial of radiotherapy in combination with combretastatin-A4-phosphate in patients with non-small-cell lung cancer, prostate adenocarcinoma, and squamous cell carcinoma of the head and neck. Ann Oncol 2012;23:231-237.
43. Shao H, Ni Y, Dai X, Zhang J, Chen F, Fan G, Sun Z, Li Y, Zhou H, Xu K: Diffusion-weighted MR imaging allows monitoring the effect of combretastatin A4 phosphate on rabbit implanted VX2 tumor model: 12-Day dynamic results. Eur J Radiol 2012;81:578-583.
44. Meyer T, Gaya AM, Dancey G, Stratford MR, Othman S, Sharma SK, Wellsted D, Taylor NJ, Stirling JJ, Poupard L, Folkes LK, Chan PS, Pedley RB, Chester KA, Owen K, Violet JA, Malaroda A, Green AJ, Buscombe J, Padhani AR, Rustin GJ, Begent RH: A phase I trial of radioimmunotherapy with 131I-A5B7 anti-CEA antibody in combination with combretastatin-A4-phosphate in advanced gastrointestinal carcinomas. Clin Cancer Res 2009;15:4484-4492.
45. Rustin GJ, Shreeves G, Nathan PD, Gaya A, Ganesan TS, Wang D, Boxall J, Poupard L, Chaplin DJ, Stratford MR, Balkissoon J, Zweifel M: A Phase Ib trial of CA4P (combretastatin A-4 phosphate), carboplatin, and paclitaxel in patients with advanced cancer. Br J Cancer 2010;102:1355-1360.
46. Zweifel M, Jayson GC, Reed NS, Osborne R, Hassan B, Ledermann J, Shreeves G, Poupard L, Lu SP, Balkissoon J, Chaplin DJ, Rustin GJ: Phase II trial of combretastatin A4 phosphate, carboplatin, and paclitaxel in patients with platinum-resistant ovarian cancer. Ann Oncol 2011;22:2036-2041.
47. Koh DM, Blackledge M, Collins DJ, Padhani AR, Wallace T, Wilton B, Taylor NJ, Stirling JJ, Sinha R, Walicke P, Leach MO, Judson I, Nathan P: Reproducibility and changes in the apparent diffusion coefficients of solid tumours treated with combretastatin A4 phosphate and bevacizumab in a two-centre phase I clinical trial. Eur Radiol 2009;19:2728-2738.
48. Mitrus I, Sochanik A, Cichon T, Szala S: Combination of combretastatin A4 phosphate and doxorubicin-containing liposomes affects growth of B16-F10 tumors. Acta Biochim Pol 2009;56:161-165.
49. Salmon BA, Siemann DW: Characterizing the tumor response to treatment with combretastatin A4 phosphate. Int J Radiat Oncol Biol Phys 2007;68:211-217.
50. Lankester KJ, Maxwell RJ, Pedley RB, Dearling JL, Qureshi UA, El-Emir E, Hill SA, Tozer GM: Combretastatin A-4-phosphate effectively increases tumor retention of the therapeutic antibody, 131I-A5B7, even at doses that are sub-optimal for vascular shut-Down. Int J Oncol 2007;30:453-460.
51. Badn W, Kalliomaki S, Widegren B, Sjogren HO: Low-Dose combretastatin A4 phosphate enhances the immune response of tumor hosts to experimental colon carcinoma. Clin Cancer Res 2006;12:4714-4719.
52. Thomas CD, Walczak C, Kaffy J, Pontikis R, Jouanneau J, Volk A: Early effects of combretastatin A4 phosphate assessed by anatomic and carbogen-based functional magnetic resonance imaging on rat bladder tumors implanted in nude mice. Neoplasia 2006;8:587-595.
53. Young SL, Chaplin DJ: Combretastatin A4 phosphate: background and current clinical status. Expert Opin Investig Drugs 2004;13:1171-1182.
54. Cooney MM, Radivoyevitch T, Dowlati A, Overmoyer B, Levitan N, Robertson K, Levine SL, DeCaro K, Buchter C, Taylor A, Stambler BS, Remick SC: Cardiovascular safety profile of combretastatin a4 phosphate in a single-Dose phase I study in patients with advanced cancer. Clin Cancer Res 2004;10:96-100.
55. Kirwan IG, Loadman PM, Swaine DJ, Anthoney DA, Pettit GR, Lippert JW, 3rd, Shnyder SD, Cooper PA, Bibby MC: Comparative preclinical pharmacokinetic and metabolic studies of the combretastatin prodrugs combretastatin A4 phosphate and A1 phosphate. Clin Cancer Res 2004;10:1446-1453.
56. Dziba JM, Marcinek R, Venkataraman G, Robinson JA, Ain KB: Combretastatin A4 phosphate has primary antineoplastic activity against human anaplastic thyroid carcinoma cell lines and xenograft tumors. Thyroid 2002;12:1063-1070.
57. Rustin GJ, Galbraith SM, Anderson H, Stratford M, Folkes LK, Sena L, Gumbrell L, Price PM: Phase I clinical trial of weekly combretastatin A4 phosphate: clinical and pharmacokinetic results. J Clin Oncol 2003;21:2815-2822.
58. Hill SA, Chaplin DJ, Lewis G, Tozer GM: Schedule dependence of combretastatin A4 phosphate in transplanted and spontaneous tumour models. Int J Cancer 2002;102:70-74.
59. Galbraith SM, Chaplin DJ, Lee F, Stratford MR, Locke RJ, Vojnovic B, Tozer GM: Effects of combretastatin A4 phosphate on endothelial cell morphology in vitro and relationship to tumour vascular targeting activity in vivo. Anticancer Res 2001;21:93-102.
60. Dorr RT, Dvorakova K, Snead K, Alberts DS, Salmon SE, Pettit GR: Antitumor activity of combretastatin-A4 phosphate, a natural product tubulin inhibitor. Invest New Drugs 1996;14:131-137.
61. Grosios K, Loadman PM, Swaine DJ, Pettit GR, Bibby MC: Combination chemotherapy with combretastatin A-4 phosphate and 5-fluorouracil in an experimental murine colon adenocarcinoma. Anticancer Res 2000;20:229-233.
62. Yeung SC, She M, Yang H, Pan J, Sun L, Chaplin D: Combination chemotherapy including combretastatin A4 phosphate and paclitaxel is effective against anaplastic thyroid cancer in a nude mouse xenograft model. J Clin Endocrinol Metab 2007;92:2902-2909.
63. Lin HL, Chiou SH, Wu CW, Lin WB, Chen LH, Yang YP, Tsai ML, Uen YH, Liou JP, Chi CW: Combretastatin A4-induced differential cytotoxicity and reduced metastatic ability by inhibition of AKT function in human gastric cancer cells. J Pharmacol Exp Ther 2007;323:365-373.
64. Ding X, Zhang Z, Li S, Wang A: Combretastatin A4 phosphate induces programmed cell death in vascular endothelial cells. Oncol Res 2011;19:303-309.
65. Lang E, Lang F: Mechanisms and pathophysiological significance of eryptosis, the suicidal erythrocyte death. Semin Cell Dev Biol 2015;39:35-42.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. Alzoubi K, Egler J, Abed M, Lang F: Enhanced Eryptosis Following Auranofin Exposure. Cell Physiol Biochem 2015;37:1018-1028.
72. Arnold M, Bissinger R, Lang F: Mitoxantrone-induced suicidal erythrocyte death. Cell Physiol Biochem 2014;34:1756-1767.
73. 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.
74. Bissinger R, Barking S, Alzoubi K, Liu G, Liu G, Lang F: Stimulation of Suicidal Erythrocyte Death by the Antimalarial Drug Mefloquine. Cell Physiol Biochem 2015;36:1395-1405.
75. Bissinger R, Bouguerra G, Stockinger K, Abbes S, Lang F: Triggering of Suicidal Erythrocyte Death by Topotecan. Cell Physiol Biochem 2015;37:1607-1618.
76. Bissinger R, Fischer S, Jilani K, Lang F: Stimulation of Erythrocyte Death by Phloretin. Cell Physiol Biochem 2014;34:2256-2265.
77. Bissinger R, Lupescu A, Zelenak C, Jilani K, Lang F: Stimulation of eryptosis by cryptotanshinone. Cell Physiol Biochem 2014;34:432-442.
78. Bouguerra G, Aljanadi O, Bissinger R, Abbes S, Lang F: Embelin-Induced Phosphatidylserine Translocation in the Erythrocyte Cell Membrane. Cell Physiol Biochem 2015;37:1629-1640.
79. Bouguerra G, Bissinger R, Abbes S, Lang F: Stimulation of Eryptosis by Narasin. Cell Physiol Biochem 2015;37:1807-1816.
80. Bouguerra G, Bissinger R, Abbes S, Lang F: Zopolrestat Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015;37:1537-1546.
81. Briglia M, Fazio A, Faggio C, Laufer S, Alzoubi K, Lang F: Triggering of Suicidal Erythrocyte Death by Ruxolitinib. Cell Physiol Biochem 2015;37:768-778.
82. Briglia M, Fazio A, Signoretto E, Faggio C, Lang F: Edelfosine Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015;37:2221-2230.
83. Calabro S, Alzoubi K, Faggio C, Laufer S, Lang F: Triggering of Suicidal Erythrocyte Death Following Boswellic Acid Exposure. Cell Physiol Biochem 2015;37:131-142.
84. Egler J, Lang F: Licochalcone A Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015;37:2060-2070.
85. Faggio C, Alzoubi K, Calabro S, Lang F: Stimulation of suicidal erythrocyte death by PRIMA-1. Cell Physiol Biochem 2015;35:529-540.
86. Fazio A, Briglia M, Faggio C, Alzoubi K, Lang F: Stimulation of Suicidal Erythrocyte Death by Garcinol. Cell Physiol Biochem 2015;37:805-815.
87. 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.
88. Lang E, Jilani K, Bissinger R, Rexhepaj R, Zelenak C, Lupescu A, Lang F, Qadri SM: Vitamin D-Rich Diet in Mice Modulates Erythrocyte Survival. Kidney Blood Press Res 2015;40:403-412.
89. Lang E, Zelenak C, Eberhard M, Bissinger R, Rotte A, Ghashghaeinia M, Lupescu A, Lang F, Qadri SM: Impact of Cyclin-Dependent Kinase CDK4 Inhibition on Eryptosis. Cell Physiol Biochem 2015;37:1178-1186.
90. Lupescu A, Bissinger R, Goebel T, Salker MS, Alzoubi K, Liu G, Chirigiu L, Mack AF, Qadri SM, Lang F: Enhanced suicidal erythrocyte death contributing to anemia in the elderly. Cell Physiol Biochem 2015;36:773-783.
91. 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.
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. Officioso A, Alzoubi K, Manna C, Lang F: Clofazimine Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015;37:331-341.
95. Oswald G, Alzoubi K, Abed M, Lang F: Stimulation of suicidal erythrocyte death by ribavirin. Basic Clin Pharmacol Toxicol 2014;114:311-317.
96. Peter T, Bissinger R, Enkel S, Alzoubi K, Oswald G, Lang F: Programmed erythrocyte death following in vitro Treosulfan treatment. Cell Physiol Biochem 2015;35:1372-1380.
97. Stockinger K, Bissinger R, Bouguerra G, Abbes S, Lang F: Enhanced Eryptosis Following Exposure to Carnosic Acid. Cell Physiol Biochem 2015;37:1779-1791.
98. 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.
99. Waibel S, Bissinger R, Bouguerra G, Abbes S, Lang F: Saquinavir Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015;37:1973-1982.
100. Zierle J, Bissinger R, Egler J, Lang F: Lapatinib Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015;37:2275-2287.
101. 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.
102. 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.
103. Andrews DA, Low PS: Role of red blood cells in thrombosis. Curr Opin Hematol 1999;6:76-82.
104. 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.
105. Zwaal RF, Comfurius P, Bevers EM: Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005;62:971-988.
106. Closse C, Dachary-Prigent J, Boisseau MR: Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999;107:300-302.
107. 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.
108. 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.
109. 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.
110. 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.
111. 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.
112. 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.
113. 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.
114. Polak-Jonkisz D, Purzyc L: Ca(2+) influx versus efflux during eryptosis in uremic erythrocytes. Blood Purif 2012;34:209-210; author reply 210.
115. 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.
116. 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.
117. 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.
118. 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.
119. 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.
120. 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.