Endoplasmic reticulum stress cooperates in zearalenone-induced cell death of RAW 264.7 macrophages

International Journal of Molecular Sciences

Volumn 16, Issue 8, 2015, Pages 19780-19795

  Chen, Fenglei ^a   Li, Qian ^a   Zhang, Zhe ^a   Lin, Pengfei ^a   Lei, Lanjie ^a   Wang, Aihua ^a   Jin, Yaping ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

CHOP; Endoplasmic reticulum stress; RAW 264.7 macrophages; Zearalenone

Indexed keywords

ZEARALENONE; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; DDIT3 PROTEIN, MOUSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; MACROPHAGE; MICROPHOTOGRAPHY; MTT ASSAY; NECROSIS; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL LINE; CELL SURVIVAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; MOUSE;

LENTIVIRUS;

ANIMALS; APOPTOSIS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; MACROPHAGES; MICE; PHENYLBUTYRATES; TRANSCRIPTION FACTOR CHOP; ZEARALENONE;

EID: 84939832681     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160819780     Document Type: Article

References (43)

1. Bennett, J.W.; Klich, M. Mycotoxins. Clin. Microbiol. Rev. 2003, 16, 497–516.
2. Richard, J.L. Some major mycotoxins and their mycotoxicoses—An overview. Int. J. Food Microbiol. 2007, 119, 3-10.
3. Gonzalez Pereyra, M.L.; Pereyra, C.M.; Ramirez, M.L.; Rosa, C.A.; Dalcero, A.M.; Cavaglieri, L.R. Determination of mycobiota and mycotoxins in pig feed in central argentina. Lett. Appl. Microbiol. 2008, 46, 555-561.
4. Kuiper, G.G.; Lemmen, J.G.; Carlsson, B.; Corton, J.C.; Safe, S.H.; van der Saag, P.T.; van der Burg, B.; Gustafsson, J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 1998, 139, 4252-4263.
5. Zinedine, A.; Soriano, J.M.; Molto, J.C.; Manes, J. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food Chem. Toxicol. 2007, 45, 1-18.
6. Zwierzchowski, W.; Przybylowicz, M.; Obremski, K.; Zielonka, L.; Skorska-Wyszynska, E.; Gajecka, M.; Polak, M.; Jakimiuk, E.; Jana, B.; Rybarczyk, L.; et al.Level of zearalenone in blood serum and lesions in ovarian follicles of sexually immature gilts in the course of zearalenone micotoxicosis. Pol. J. Vet. Sci. 2005, 8, 209-218.
7. Abbes, S.; Salah-Abbes, J.B.; Ouanes, Z.; Houas, Z.; Othman, O.; Bacha, H.; Abdel-Wahhab, M.A.; Oueslati, R. Preventive role of phyllosilicate clay on the immunological and biochemical toxicity of zearalenone in Balb/c mice. Int. Immunopharmacol. 2006, 6, 1251-1258.
8. Luongo, D.; de Luna, R.; Russo, R.; Severino, L. Effects of four Fusarium toxins (fumonisin B1, α-zearalenol, nivalenol and deoxynivalenol) on porcine whole-blood cellular proliferation. Toxicon 2008, 52, 156-162.
9. Marin, D.E.; Taranu, I.; Burlacu, R.; Manda, G.; Motiu, M.; Neagoe, I.; Dragomir, C.; Stancu, M.; Calin, L. Effects of zearalenone and its derivatives on porcine immune response. Toxicol. In Vitro 2011, 25, 1981-1988.
10. Marin, D.E.; Taranu, I.; Burlacu, R.; Tudor, D.S. Effects of zearalenone and its derivatives on the innate immune response of swine. Toxicon 2010, 56, 956-963.
11. Ben Salah-Abbes, J.; Abbes, S.; Houas, Z.; Abdel-Wahhab, M.A.; Oueslati, R. Zearalenone induces immunotoxicity in mice: Possible protective effects of radish extract (Raphanus sativus). J. Pharm. Pharmacol. 2008, 60, 761-770.
12. Hueza, I.M.; Raspantini, P.C.; Raspantini, L.E.; Latorre, A.O.; Gorniak, S.L. Zearalenone, an estrogenic mycotoxin, is an immunotoxic compound. Toxins 2014, 6, 1080-1095.
13. Abbes, S.; Ouanes, Z.; ben Salah-Abbes, J.; Houas, Z.; Oueslati, R.; Bacha, H.; Othman, O. The protective effect of hydrated sodium calcium aluminosilicate against haematological, biochemical and pathological changes induced by zearalenone in mice. Toxicon 2006, 47, 567-574.
14. Bouaziz, C.; El Dein, O.S.; El Golli, E.; Abid-Essefi, S.; Brenner, C.; Lemaire, C.; Bacha, H. Different apoptotic pathways induced by zearalenone, T-2 toxin and ochratoxin A in human hepatoma cells. Toxicology 2008, 254, 19-28.
15. Ouanes, Z.; Abid, S.; Ayed, I.; Anane, R.; Mobio, T.; Creppy, E.E.; Bacha, H. Induction of micronuclei by zearalenone in vero monkey kidney cells and in bone marrow cells of mice: Protective effect of vitamin E. Mutat. Res. 2003, 538, 63-70.
16. Gao, F.; Jiang, L.P.; Chen, M.; Geng, C.Y.; Yang, G.; Ji, F.; Zhong, L.F.; Liu, X.F. Genotoxic effects induced by zearalenone in a human embryonic kidney cell line. Mutat. Res. 2013, 755, 6-10.
17. Abid-Essefi, S.; Baudrimont, I.; Hassen, W.; Ouanes, Z.; Mobio, T.A.; Anane, R.; Creppy, E.E.; Bacha, H. DNA fragmentation, apoptosis and cell cycle arrest induced by zearalenone in cultured DOK, Vero and Caco-2 cells: Prevention by vitamin E. Toxicology2003, 192, 237-248.
18. Ayed-Boussema, I.; Bouaziz, C.; Rjiba, K.; Valenti, K.; Laporte, F.; Bacha, H.; Hassen, W. The mycotoxin zearalenone induces apoptosis in human hepatocytes (HepG2) via p53-dependent mitochondrial signaling pathway. Toxicol. In Vitro 2008, 22, 1671-1680.
19. Lu, J.; Yu, J.Y.; Lim, S.S.; Son, Y.O.; Kim, D.H.; Lee, S.A.; Shi, X.; Lee, J.C. Cellular mechanisms of the cytotoxic effects of the zearalenone metabolites α-zearalenol and β-zearalenol on RAW264.7 macrophages. Toxicol. In Vitro 2013, 27, 1007-1017.
20. Yu, J.Y.; Zheng, Z.H.; Son, Y.O.; Shi, X.; Jang, Y.O.; Lee, J.C. Mycotoxin zearalenone induces AIF- and ROS-mediated cell death through p53- and MAPK-dependent signaling pathways in RAW264.7 macrophages. Toxicol. In Vitro 2011, 25, 1654-1663.
21. Puthalakath, H.; O’Reilly, L.A.; Gunn, P.; Lee, L.; Kelly, P.N.; Huntington, N.D.; Hughes, P.D.; Michalak, E.M.; McKimm-Breschkin, J.; Motoyama, N.; et al.ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129, 1337-1349.
22. Yamaguchi, H.; Wang, H.G. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J. Biol. Chem.2004, 279, 45495-45502.
23. Wang, X.Z.; Ron, D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP kinase. Science 1996, 272, 1347-1349.
24. Li, J.; Lee, B.; Lee, A.S. Endoplasmic reticulum stress-induced apoptosis: Multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and noxa by p53. J. Biol. Chem.2006, 281, 7260-7270.
25. Mori, K. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 2000, 101, 451-454.
26. Li, J.; Wang, J.J.; Yu, Q.; Wang, M.; Zhang, S.X. Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett. 2009, 583, 1521-1527.
27. Ron, D.; Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Bio. 2007, 8, 519-529.
28. Endo, M.; Mori, M.; Akira, S.; Gotoh, T. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J. Immunol. 2006, 176, 6245-6253.
29. Banjerdpongchai, R.; Kongtawelert, P.; Khantamat, O.; Srisomsap, C.; Chokchaichamnankit, D.; Subhasitanont, P.; Svasti, J. Mitochondrial and endoplasmic reticulum stress pathways cooperate in zearalenone-induced apoptosis of human leukemic cells. J. Hematol. Oncol. 2010, 3, 50.
30. Lin, P.; Chen, F.; Sun, J.; Zhou, J.; Wang, X.; Wang, N.; Li, X.; Zhang, Z.; Wang, A.; Jin, Y. Mycotoxin zearalenone induces apoptosis in mouse leydig cells via an endoplasmic reticulum stress-dependent signalling pathway. Reprod. Toxicol. 2015, 52, 71-77.
31. Abid-Essefi, S.; Bouaziz, C.; Golli-Bennour, E.E.; Ouanes, Z.; Bacha, H. Comparative study of toxic effects of zearalenone and its two major metabolites α-zearalenol and β-zearalenol on cultured human Caco-2 cells. J. Biochem. Mol. Toxicol. 2009, 23, 233-243.
32. Grosse, Y.; Chekir-Ghedira, L.; Huc, A.; Obrecht-Pflumio, S.; Dirheimer, G.; Bacha, H.; Pfohl-Leszkowicz, A. Retinol, ascorbic acid and α-tocopherol prevent DNA adduct formation in mice treated with the mycotoxins ochratoxin a and zearalenone. Cancer Lett.1997, 114, 225-229.
33. Hassen, W.; Ayed-Boussema, I.; Oscoz, A.A.; Lopez Ade, C.; Bacha, H. The role of oxidative stress in zearalenone-mediated toxicity in Hep G2 cells: Oxidative DNA damage, gluthatione depletion and stress proteins induction. Toxicology 2007, 232, 294-302.
34. Ouanes, Z.; Ayed-Boussema, I.; Baati, T.; Creppy, E.E.; Bacha, H. Zearalenone induces chromosome aberrations in mouse bone marrow: Preventive effect of 17β-estradiol, progesterone and vitamin E. Mutat. Res. 2005, 565, 139-149.
35. Zhu, L.; Yuan, H.; Guo, C.; Lu, Y.; Deng, S.; Yang, Y.; Wei, Q.; Wen, L.; He, Z. Zearalenone induces apoptosis and necrosis in porcine granulosa cells via a caspase-3- and caspase-9-dependent mitochondrial signaling pathway. J. Cell. Physiol. 2012, 227, 1814-1820.
36. Wang, Y.; Zheng, W.; Bian, X.; Yuan, Y.; Gu, J.; Liu, X.; Liu, Z.; Bian, J. Zearalenone induces apoptosis and cytoprotective autophagy in primary Leydig cells. Toxicol. Lett. 2014, 226, 182-191.
37. Rao, R.V.; Poksay, K.S.; Castro-Obregon, S.; Schilling, B.; Row, R.H.; del Rio, G.; Gibson, B.W.; Ellerby, H.M.; Bredesen, D.E. Molecular components of a cell death pathway activated by endoplasmic reticulum stress. J. Biol. Chem. 2004, 279, 177-187.
38. Barone, M.V.; Crozat, A.; Tabaee, A.; Philipson, L.; Ron, D. CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest. Gene Dev. 1994, 8, 453-464.
39. Oyadomari, S.; Koizumi, A.; Takeda, K.; Gotoh, T.; Akira, S.; Araki, E.; Mori, M. Targeted disruption of the CHOP gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Investig. 2002, 109, 525-532.
40. Ron, D.; Habener, J.F. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Gene Dev. 1992, 6, 439-453.
41. McCullough, K.D.; Martindale, J.L.; Klotz, L.O.; Aw, T.Y.; Holbrook, N.J. GADD153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol.2001, 21, 1249-1259.
42. Gotoh, T.; Terada, K.; Oyadomari, S.; Mori, M. Hsp70-Dnaj chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ. 2004, 11, 390-402.
43. Gotoh, T.; Oyadomari, S.; Mori, K.; Mori, M. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP. J. Biol. Chem. 2002, 277, 12343-12350.