Ca2+-dependent suicidal erythrocyte death following zearalenone exposure

Archives of Toxicology

Volumn 87, Issue 10, 2013, Pages 1821-1828

  Jilani, Kashif ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Calcium; Cell volume; Eryptosis; Phosphatidylserine; Zearalenone

Indexed keywords

CALCIUM ION; HEMOGLOBIN; LIPOCORTIN 5; PHOSPHATIDYLSERINE; ZEARALENONE;

ARTICLE; CALCIUM CELL LEVEL; CATION TRANSPORT; CELL DEATH; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; ERYPTOSIS; ERYTHROCYTE MEMBRANE; ERYTHROCYTE VOLUME; EXPOSURE; EXTRACELLULAR CALCIUM; FLUORESCENCE; HEMOLYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION;

ANNEXIN A5; APOPTOSIS; CALCIUM; CELL SIZE; ERYTHROCYTES; HEMOGLOBINS; HEMOLYSIS; HUMANS; PHOSPHATIDYLSERINES; ZEARALENONE;

EID: 84885428597     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-013-1037-1     Document Type: Article

References (103)

1. Abed M, Towhid ST, Mia S et al (2012a) Sphingomyelinase-induced adhesion of eryptotic erythrocytes to endothelial cells. Am J Physiol Cell Physiol 303(9):C991-C999. doi: 10.1152/ajpcell.00239.2012
2. Abed M, Towhid ST, Shaik N, Lang F (2012b) Stimulation of suicidal death of erythrocytes by rifampicin. Toxicology doi: 10.1016/j.tox.2012.10.006
3. Abid-Essefi S, Baudrimont I, Hassen W et al (2003) DNA fragmentation, apoptosis and cell cycle arrest induced by zearalenone in cultured DOK, Vero and Caco-2 cells: prevention by vitamin E. Toxicology 192(2-3):237-248
4. Ahamed S, Foster JS, Bukovsky A, Wimalasena J (2001) Signal transduction through the Ras/Erk pathway is essential for the mycoestrogen zearalenone-induced cell-cycle progression in MCF-7 cells. Mol Carcinog 30(2):88-98
5. Andrews DA, Low PS (1999) Role of red blood cells in thrombosis. Curr Opin Hematol 6(2):76-82
6. Ayed-Boussema I, Ouanes Z, Bacha H, Abid S (2007) Toxicities induced in cultured cells exposed to zearalenone: apoptosis or mutagenesis? J Biochem Mol Toxicol 21(3):136-144. doi: 10.1002/jbt.20171
7. Ayed-Boussema I, Bouaziz C, Rjiba K et al (2008) The mycotoxin zearalenone induces apoptosis in human hepatocytes (HepG2) via p53-dependent mitochondrial signaling pathway. Toxicol In Vitro 22(7):1671-1680. doi: 10.1016/j.tiv.2008.06.016
8. Banjerdpongchai R, Kongtawelert P, Khantamat O et al (2010) Mitochondrial and endoplasmic reticulum stress pathways cooperate in zearalenone-induced apoptosis of human leukemic cells. J Hematol Oncol 3:50. doi: 10.1186/1756-8722-3-50
9. Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16(3):497-516
10. Berg CP, Engels IH, Rothbart A et al (2001) Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ 8(12):1197-1206
11. Berthiller F, Crews C, Dall'asta C et al (2013) Masked mycotoxins: a review. Mol Nutr Food Res 57(1):165-186. doi: 10.1002/mnfr.201100764
12. Bhavsar SK, Bobbala D, Xuan NT, Foller M, Lang F (2010) Stimulation of suicidal erythrocyte death by alpha-lipoic acid. Cell Physiol Biochem 26(6):859-868
13. Bhavsar SK, Gu S, Bobbala D, Lang F (2011) Janus kinase 3 is expressed in erythrocytes, phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death. Cell Physiol Biochem 27(5):547-556. doi: 10.1159/000329956
14. Birka C, Lang PA, Kempe DS et al (2004) Enhanced susceptibility to erythrocyte "apoptosis" following phosphate depletion. Pflugers Archiv 448(5):471-477
15. Bobbala D, Alesutan I, Foller M, Huber SM, Lang F (2010) Effect of anandamide in plasmodium Berghei-infected mice. Cell Physiol Biochem 26(3):355-362
16. Bookchin RM, Ortiz OE, Lew VL (1987) Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog Clin Biol Res 240:193-200
17. Borst O, Abed M, Alesutan I et al (2012) Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Physiol Cell Physiol 302(4):C644-C651
18. Bottger E, Multhoff G, Kun JF, Esen M (2012) Plasmodium falciparum-infected erythrocytes induce granzyme B by NK cells through expression of host-Hsp70. PLoS One 7(3):e33774. doi: 10.1371/journal.pone. 0033774
19. Bouaziz C, Sharaf El Dein O, El Golli E et al (2008) Different apoptotic pathways induced by zearalenone, T-2 toxin and ochratoxin A in human hepatoma cells. Toxicology 254(1-2):19-28. doi: 10.1016/j.tox.2008.08.020
20. Bouaziz C, Martel C, Sharaf el dein O et al (2009) Fusarial toxin-induced toxicity in cultured cells and in isolated mitochondria involves PTPC-dependent activation of the mitochondrial pathway of apoptosis. Toxicol Sci 110(2):363-375. doi: 10.1093/toxsci/kfp117
21. Brand VB, Sandu CD, Duranton C et al (2003) Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell Physiol Biochem 13(6):347-356
22. Brugnara C, de Franceschi L, Alper SL (1993) Inhibition of Ca(2+)-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 92(1):520-526
23. Calderon-Salinas JV, Munoz-Reyes EG, Guerrero-Romero JF et al (2011) Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol Cell Biochem 357(1-2):171-179
24. Chung SM, Bae ON, Lim KM et al (2007) Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 27(2):414-421
25. Closse C, Dachary-Prigent J, Boisseau MR (1999) Phosphatidylserine- related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 107(2):300-302
26. Doll S, Danicke S (2011) The Fusarium toxins deoxynivalenol (DON) and zearalenone (ZON) in animal feeding. Prev Vet Med 102(2):132-145. doi: 10.1016/j.prevetmed.2011.04.008
27. Doric M, Radovic S, Babic M, Kuskunovic S, Tomic I, Selak I (2007) Zearalenone-induced lymphophagocytosis (T cell apoptosis) on the rat's thymus. Bosn J Basic Med Sci 7(1):66-70
28. Felder KM, Hoelzle K, Ritzmann M et al (2011) Hemotrophic mycoplasmas induce programmed cell death in red blood cells. Cell Physiol Biochem 27(5):557-564. doi: 10.1159/000329957
29. Ficheux AS, Sibiril Y, Parent-Massin D (2012) Co-exposure of fusarium mycotoxins: in vitro myelotoxicity assessment on human hematopoietic progenitors. Toxicon 60(6):1171-1179. doi: 10.1016/j.toxicon.2012.08.001
30. Firat U, Kaya S, Cim A et al (2012) Increased caspase-3 immunoreactivity of erythrocytes in STZ diabetic rats. Exp Diabetes Res 2012:316384. doi: 10.1155/2012/316384
31. Foller M, Feil S, Ghoreschi K et al (2008a) Anemia and splenomegaly in cGKI-deficient mice. Proc Natl Acad Sci USA 105(18):6771-6776
32. Foller M, Huber SM, Lang F (2008b) Erythrocyte programmed cell death. IUBMB Life 60(10):661-668. doi: 10.1002/iub.106
33. Foller M, Kasinathan RS, Koka S et al (2008c) TRPC6 contributes to the Ca(2+) leak of human erythrocytes. Cell Physiol Biochem 21(1-3):183-192
34. Foller M, Bobbala D, Koka S, Huber SM, Gulbins E, Lang F (2009a) Suicide for survival-death of infected erythrocytes as a host mechanism to survive malaria. Cell Physiol Biochem 24(3-4):133-140
35. Foller M, Mahmud H, Gu S et al (2009b) Participation of leukotriene C(4) in the regulation of suicidal erythrocyte death. J Physiol Pharmacol 60(3):135-143
36. Foller M, Sopjani M, Koka S et al (2009c) Regulation of erythrocyte survival by AMP-activated protein kinase. FASEB J 23(4):1072-1080
37. Gallagher PG, Chang SH, Rettig MP et al (2003) Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 101(11):4625-4627
38. Ganesan S, Chaurasiya ND, Sahu R, Walker LA, Tekwani BL (2012) Understanding the mechanisms for metabolism-linked hemolytic toxicity of primaquine against glucose 6-phosphate dehydrogenase deficient human erythrocytes: evaluation of eryptotic pathway. Toxicology 294(1):54-60. doi: 10.1016/j.tox.2012.01.015
39. Gao M, Cheung KL, Lau IP et al (2012) Polyphyllin D induces apoptosis in human erythrocytes through Ca(2)(+) rise and membrane permeabilization. Arch Toxicol 86(5):741-752. doi: 10.1007/s00204-012-0808-4
40. Gatidis S, Zelenak C, Fajol A et al (2011) p38 MAPK activation and function following osmotic shock of erythrocytes. Cell Physiol Biochem 28(6):1279-1286
41. Ghashghaeinia M, Toulany M, Saki M et al (2011) The NFkB pathway inhibitors Bay 11-7082 and parthenolide induce programmed cell death in anucleated Erythrocytes. Cell Physiol Biochem 27(1):45-54. doi: 10.1159/000325204
42. Ghashghaeinia M, Cluitmans JC, Akel A et al (2012) The impact of erythrocyte age on eryptosis. Br J Haematol 157(5):606-614. doi: 10.1111/j.1365-2141.2012.09100.x
43. Jee Y, Noh EM, Cho ES, Son HY (2010) Involvement of the Fas and Fas ligand in testicular germ cell apoptosis by zearalenone in rat. J Vet Sci 11(2):115-119
44. Jilani K, Lupescu A, Zbidah M, Abed M, Shaik N, Lang F (2012a) Enhanced apoptotic death of erythrocytes induced by the mycotoxin ochratoxin A. Kidney Blood Press Res 36(1):107-118. doi: 10.1159/000341488
45. Jilani K, Lupescu A, Zbidah M, Shaik N, Lang F (2012b) Withaferin A-stimulated Ca(2+) entry, ceramide formation and suicidal death of erythrocytes. Toxicol In Vitro. doi: 10.1016/j.tiv.2012.09.004
46. Kempe DS, Lang PA, Duranton C et al (2006) Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J 20(2):368-370
47. Kempe DS, Akel A, Lang PA et al (2007) Suicidal erythrocyte death in sepsis. J Mol Med 85(3):269-277
48. Kim IH, Son HY, Cho SW, Ha CS, Kang BH (2003) Zearalenone induces male germ cell apoptosis in rats. Toxicol Lett 138(3):185-192
49. Klarl BA, Lang PA, Kempe DS et al (2006) Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion. Am J Physiol Cell Physiol 290(1):C244-C253
50. Koka S, Bobbala D, Lang C, Boini KM, Huber SM, Lang F (2009) Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem 23(1-3):191-198
51. Kouadio JH, Dano SD, Moukha S, Mobio TA, Creppy EE (2007) Effects of combinations of Fusarium mycotoxins on the inhibition of macromolecular synthesis, malondialdehyde levels, DNA methylation and fragmentation, and viability in Caco-2 cells. Toxicon 49(3):306-317. doi: 10.1016/j.toxicon.2006. 09.029
52. Kucherenko YV, Lang F (2012) Inhibitory effect of furosemide on non-selective voltage-independent cation channels in human erythrocytes. Cell Physiol Biochem 30(4):863-875. doi: 10.1159/000341464
53. Kucherenko Y, Zelenak C, Eberhard M, Qadri SM, Lang F (2012) Effect of casein kinase 1alpha activator pyrvinium pamoate on erythrocyte ion channels. Cell Physiol Biochem 30(2):407-417. doi: 10.1159/000339034
54. Lang F, Qadri SM (2012) Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif 33(1-3):125-130
55. Lang PA, Kaiser S, Myssina S, Wieder T, Lang F, Huber SM (2003) Role of Ca2+ -activated K+ channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 285(6):C1553-C1560
56. Lang PA, Beringer O, Nicolay JP et al (2006) Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med 84(5):378-388
57. Lang PA, Schenck M, Nicolay JP et al (2007) Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 13(2):164-170
58. Lang F, Gulbins E, Lerche H, Huber SM, Kempe DS, Foller M (2008) Eryptosis, a window to systemic disease. Cell Physiol Biochem 22(5-6):373-380
59. Lang PA, Kasinathan RS, Brand VB et al (2009) Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem 24(5-6):415-428
60. Lang F, Gulbins E, Lang PA, Zappulla D, Foller M (2010) Ceramide in suicidal death of erythrocytes. Cell Physiol Biochem 26(1):21-28
61. Lang E, Jilani K, Zelenak C et al (2011) Stimulation of suicidal erythrocyte death by benzethonium. Cell Physiol Biochem 28(2):347-354. doi: 10.1159/000331751
62. Lang E, Qadri SM, Jilani K et al (2012a) Carbon monoxide-sensitive apoptotic death of erythrocytes. Basic Clin Pharmacol Toxicol 111(5):348-355. doi: 10.1111/j.1742-7843.2012.00915.x
63. Lang E, Qadri SM, Lang F (2012b) Killing me softly - suicidal erythrocyte death. Int J Biochem Cell Biol 44(8):1236-1243. doi: 10.1016/j.biocel.2012.04. 019
64. Lau IP, Chen H, Wang J, et al. (2011) In vitro effect of CTAB- and PEG-coated gold nanorods on the induction of eryptosis/erythroptosis in human erythrocytes. Nanotoxicology. doi: 10.3109/17435390.2011.625132
65. Lupescu A, Jilani K, Zbidah M, Lang E, Lang F (2012a) Enhanced Ca(2+) Entry, Ceramide Formation, and Apoptotic Death of Erythrocytes Triggered by Plumbagin. J Nat Prod. doi: 10.1021/np300611r
66. Lupescu A, Jilani K, Zbidah M, Lang F (2012b) Induction of apoptotic erythrocyte death by rotenone. Toxicology 300(3):132-137. doi: 10.1016/j.tox.2012.06.007
67. Lupescu A, Jilani K, Zelenak C, Zbidah M, Qadri SM, Lang F (2012c) Hexavalent chromium-induced erythrocyte membrane phospholipid asymmetry. Biometals 25(2):309-318. doi: 10.1007/s10534-011-9507-5
68. Lupescu A, Shaik N, Jilani K et al (2012d) Enhanced erythrocyte membrane exposure of phosphatidylserine following sorafenib treatment: an in vivo and in vitro study. Cell Physiol Biochem 30(4):876-888. doi: 10.1159/000341465
69. Maellaro E, Leoncini S, Moretti D, et al. (2011) Erythrocyte caspase-3 activation and oxidative imbalance in erythrocytes and in plasma of type 2 diabetic patients. Acta Diabetol [Epub ahead of print]
70. Malovrh T, Jakovac-Strajn B (2010) Feed contaminated with fusarium toxins alter lymphocyte proliferation and apoptosis in primiparous sows during the perinatal period. Food Chem Toxicol 48(10):2907-2912. doi: 10.1016/j.fct.2010. 07.026
71. Massart F, Saggese G (2010) Oestrogenic mycotoxin exposures and precocious pubertal development. Int J Androl 33(2):369-376. doi: 10.1111/j.1365-2605.2009.01009.x
72. Minervini F, Giannoccaro A, Fornelli F, Dell'Aquila ME, Minoia P, Visconti A (2006) Influence of mycotoxin zearalenone and its derivatives (alpha and beta zearalenol) on apoptosis and proliferation of cultured granulosa cells from equine ovaries. Reprod Biol Endocrinol 4:62. doi: 10.1186/1477-7827-4-62
73. Myssina S, Huber SM, Birka C et al (2003) Inhibition of erythrocyte cation channels by erythropoietin. J Am Soc Nephrol 14(11):2750-2757
74. Nicolay JP, Schneider J, Niemoeller OM et al (2006) Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 18(4-5):223-232. doi: 10.1159/000097669
75. Pandolfi A, Di Pietro N, Sirolli V et al (2007) Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J Cell Physiol 213(3):699-709
76. Pazaiti A, Kontos M, Fentiman IS (2012) ZEN and the art of breast health maintenance. Int J Clin Pract 66(1):28-36. doi: 10.1111/j.1742-1241.2011.02805.x
77. Pillay D, Chuturgoon AA, Nevines E, Manickum T, Deppe W, Dutton MF (2002) The quantitative analysis of zearalenone and its derivatives in plasma of patients with breast and cervical cancer. Clin Chem Lab Med 40(9):946-951. doi: 10.1515/CCLM.2002.166
78. Polak-Jonkisz D, Purzyc L (2012) Ca Influx versus Efflux during eryptosis in uremic erythrocytes. Blood Purif 34(3-4):209-210. doi: 10.1159/000341627
79. Qadri SM, Bauer J, Zelenak C et al (2011a) Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death. Cell Physiol Biochem 28(2):339-346. doi: 10.1159/000331750
80. Qadri SM, Kucherenko Y, Lang F (2011b) Beauvericin induced erythrocyte cell membrane scrambling. Toxicology 283(1):24-31. doi: 10.1016/j.tox.2011.01. 023
81. Qadri SM, Kucherenko Y, Zelenak C, Jilani K, Lang E, Lang F (2011c) Dicoumarol activates Ca2+-permeable cation channels triggering erythrocyte cell membrane scrambling. Cell Physiol Biochem 28(5):857-864. doi: 10.1159/000335800
82. Qadri SM, Mahmud H, Lang E et al (2012) Enhanced suicidal erythrocyte death in mice carrying a loss-of-function mutation of the adenomatous polyposis coli gene. J Cell Mol Med 16(5):1085-1093. doi: 10.1111/j.1582-4934.2011.01387.x
83. Qian EW, Ge DT, Kong SK (2012) Salidroside protects human erythrocytes against hydrogen peroxide-induced apoptosis. J Nat Prod 75(4):531-537. doi: 10.1021/np200555s
84. Salah-Abbes JB, Abbes S, Abdel-Wahhab MA, Oueslati R (2010) In-vitro free radical scavenging, antiproliferative and anti-zearalenone cytotoxic effects of 4-(methylthio)-3-butenyl isothiocyanate from Tunisian Raphanus sativus. J Phar Pharmacol 62(2):231-239. doi: 10.1211/jpp.62.02.0011
85. Shaik N, Lupescu A, Lang F (2012a) Sunitinib-sensitive suicidal erythrocyte death. Cell Physiol Biochem 30(3):512-522. doi: 10.1159/000341434
86. Shaik N, Zbidah M, Lang F (2012b) Inhibition of Ca(2+) entry and suicidal erythrocyte death by naringin. Cell Physiol Biochem 30(3):678-686. doi: 10.1159/000341448
87. Siraskar B, Ballal A, Bobbala D, Foller M, Lang F (2010) Effect of amphotericin B on parasitemia and survival of plasmodium berghei-infected mice. Cell Physiol Biochem 26(3):347-354
88. Vlata Z, Porichis F, Tzanakakis G, Tsatsakis A, Krambovitis E (2006) A study of zearalenone cytotoxicity on human peripheral blood mononuclear cells. Toxicol Lett 165(3):274-281. doi: 10.1016/j.toxlet.2006.05.001
89. Vota DM, Maltaneri RE, Wenker SD, Nesse AB, Vittori DC (2012) Differential Erythropoietin Action upon Cells Induced to Eryptosis by Different Agents. Cell Biochem Biophys. doi: 10.1007/s12013-012-9408-4
90. Wegulo SN (2012) Factors influencing deoxynivalenol accumulation in small grain cereals. Toxins 4(11):1157-1180. doi: 10.3390/toxins4111157
91. Weiss E, Cytlak UM, Rees DC, Osei A, Gibson JS (2012) Deoxygenation-induced and Ca(2+) dependent phosphatidylserine externalisation in red blood cells from normal individuals and sickle cell patients. Cell Calcium 51(1):51-56. doi: 10.1016/j.ceca.2011.10.005
92. Wood BL, Gibson DF, Tait JF (1996) Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 88(5):1873-1880
93. Yazar S, Omurtag GZ (2008) Fumonisins, trichothecenes and zearalenone in cereals. Int J Mol Sci 9(11):2062-2090. doi: 10.3390/ijms9112062
94. Yu Z, Zhang L, Wu D, Liu F (2005) Anti-apoptotic action of zearalenone in MCF-7 cells. Ecotoxicol Environ Saf 62(3):441-446. doi: 10.1016/j.ecoenv.2004. 10.003
95. Yu JY, Zheng ZH, Son YO, Shi X, Jang YO, Lee JC (2011) Mycotoxin zearalenone induces AIF- and ROS-mediated cell death through p53- and MAPK-dependent signaling pathways in RAW264.7 macrophages. Toxicol In Vitro 25(8):1654-1663. doi: 10.1016/j.tiv.2011.07.002
96. Zappulla D (2008) Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J Cardiometab Syndr 3(1):30-34
97. Zbidah M, Lupescu A, Jilani K, Lang F (2012a) Stimulation of Suicidal Erythrocyte Death by Fumagillin. Basic Clin Pharmacol Toxicol. doi: 10.1111/bcpt.12033
98. Zbidah M, Lupescu A, Shaik N, Lang F (2012b) Gossypol-induced suicidal erythrocyte death. Toxicology. doi: 10.1016/j.tox.2012.09.010
99. Zelenak C, Foller M, Velic A et al (2011) Proteome analysis of erythrocytes lacking AMP-activated protein kinase reveals a role of PAK2 kinase in eryptosis. J Proteome Res 10(4):1690-1697. doi: 10.1021/pr101004j
100. Zelenak C, Eberhard M, Jilani K, Qadri SM, Macek B, Lang F (2012a) Protein kinase CK1alpha regulates erythrocyte survival. Cell Physiol Biochem 29(1-2):171-180. doi: 10.1159/000337598
101. Zelenak C, Pasham V, Jilani K et al (2012b) Tanshinone IIA stimulates erythrocyte phosphatidylserine exposure. Cell Physiol Biochem 30(1):282-294. doi: 10.1159/000339064
102. Zhu L, Yuan H, Guo C et al (2012) Zearalenone induces apoptosis and necrosis in porcine granulosa cells via a caspase-3- and caspase-9-dependent mitochondrial signaling pathway. J Cell Physiol 227(5):1814-1820. doi: 10.1002/jcp.22906
103. Zwaal RF, Comfurius P, Bevers EM (2005) Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62(9):971-988