Ochratoxin a inhibits mouse embryonic development by activating a mitochondrion-dependent apoptotic signaling pathway

International Journal of Molecular Sciences

Volumn 14, Issue 1, 2013, Pages 935-953

  Hsuuw, Yan Der ^a   Chan, Wen Hsiung ^b   Yu, Jau Song ^c  

^a NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^b CHUNG YUAN CHRISTIAN UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Blastocyst; Development; Ochratoxin A; ROS

Indexed keywords

OCHRATOXIN; CARCINOGEN; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BLASTOCYST; CELL COUNT; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY TEST; DEVELOPMENTAL STAGE; DEVELOPMENTAL TOXICITY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO GROWTH; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NICK END LABELING; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; EMBRYO TRANSFER; FEMALE; FLUORESCENCE MICROSCOPY; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; METABOLISM; MITOCHONDRION; NIDATION; PREGNANCY;

MUS;

ANIMALS; APOPTOSIS; BLASTOCYST; CARCINOGENS; CELL PROLIFERATION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO IMPLANTATION; EMBRYO TRANSFER; EMBRYONIC DEVELOPMENT; FEMALE; MALE; MICE, INBRED ICR; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; OCHRATOXINS; PREGNANCY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84872179187     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14010935     Document Type: Article

References (62)

1. Council of Agricultural Science and Technology (CAST). Mycotoxins: Risks in Plant, Animal, and Human Systems; CAST: Ames, IA, USA, 2003.
2. IPCS. Safety evaluation of certain mycotoxins in food. WHO Food Addit. Ser. 2001, 47, 103-415.
3. Walker, R. Risk assessment of ochratoxin: Current views of the European Scientific Committee on Food, the JECFA and the Codex Committee on Food Additives and Contaminants. Adv. Exp. Med. Biol. 2002, 504, 249-255.
4. Pfohl-Leszkowicz, A.; Manderville, R.A. Ochratoxin A: An overview on toxicity and carcinogenicity in animals and humans. Mol. Nutr. Food Res. 2007, 51, 61-99.
5. Zhang, X.; Boesch-Saadatmandi, C.; Lou, Y.; Wolffram, S.; Huebbe, P.; Rimbach, G. Ochratoxin A induces apoptosis in neuronal cells. Genes Nutr. 2009, 4, 41-48.
6. Sava, V.; Reunova, O.; Velasquez, A.; Harbison, R.; Sanchez-Ramos, J. Acute neurotoxic effects of the fungal metabolite ochratoxin-A. Neurotoxicology 2006, 27, 82-92.
7. Kanisawa, M.; Suzuki, S. Induction of renal and hepatic tumors in mice by ochratoxin A, a mycotoxin. Gann = Gan 1978, 69, 599-600.
8. Kanisawa, M. Pathogenesis of human cancer development due to environmental factors. Gan No Rinsho 1984, 30, 1445-1456.
9. Boorman, G. NTP Technical Report on the Toxicology and Carcinogenesis Studies of Ochratoxin A (CAS No. 303-47-9) in F344/N Rats (Gavage Studies), NTP TR 358, NIH Publication No. 89-2813. National Institute of Health: North Carolina, NC, USA, 1989.
10. Bouaziz, C.; Sharaf el dein, O.; Martel, C.; Golli, E.E.; Abid-Essefi, S.; Brenner, C.; Lemaire, C.; Bacha, H. Molecular events involved in ochratoxin A induced mitochondrial pathway of apoptosis, modulation by Bcl-2 family members. Environ. Toxicol. 2011, 26, 579-590.
11. Pfohl-Leszkowicz, A.; Manderville, R.A. An update on direct genotoxicity as a molecular mechanism of ochratoxin a carcinogenicity. Chem. Res. Toxicol. 2012, 25, 252-262.
12. Hardy, K. Cell death in the mammalian blastocyst. Mol. Hum. Reprod. 1997, 3, 919-925.
13. Hardy, K.; Stark, J.; Winston, R.M. Maintenance of the inner cell mass in human blastocysts from fragmented embryos. Biol. Reprod. 2003, 68, 1165-1169.
14. Byrne, A.T.; Southgate, J.; Brison, D.R.; Leese, H.J. Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J. Reprod. Fertil. 1999, 117, 97-105.
15. Hsuuw, Y.D.; Chang, C.K.; Chan, W.H.; Yu, J.S. Curcumin prevents methylglyoxal-induced oxidative stress and apoptosis in mouse embryonic stem cells and blastocysts. J. Cell. Physiol. 2005, 205, 379-386.
16. Chan, W.H. Ginkgolide B induces apoptosis and developmental injury in mouse embryonic stem cells and blastocysts. Hum. Reprod. 2006, 21, 2985-2995.
17. Chan, W.H. Impact of genistein on maturation of mouse oocytes, fertilization, and fetal development. Reprod. Toxicol. 2009, 28, 52-58.
18. Chan, W.H. Effects of citrinin on maturation of mouse oocytes, fertilization, and fetal development in vitro and in vivo. Toxicol. Lett. 2008, 180, 28-32.
19. Chan, W.H. Ginkgolides induce apoptosis and decrease cell numbers in mouse blastocysts. Biochem. Biophys. Res. Commun. 2005, 338, 1263-1267.
20. Jacobson, M.D. Reactive oxygen species and programmed cell death. Trends Biochem. Sci. 1996, 21, 83-86.
21. Thompson, C.B. Apoptosis in the pathogenesis and treatment of disease. Science 1995, 267, 1456-1462.
22. Brill, A.; Torchinsky, A.; Carp, H.; Toder, V. The role of apoptosis in normal and abnormal embryonic development. J. Assist. Reprod. Genet. 1999, 16, 512-519.
23. Lotz, K.; Proff, P.; Bienengraeber, V.; Fanghaenel, J.; Gedrange, T.; Weingaertner, J. Apoptosis as a creative agent of embryonic development of bucca, mentum and nasolacrimal duct. An in vivo study in rats. J. Craniomaxillofac. Surg. 2006, 34, S8-S13.
24. Weingaertner, J.; Proff, P.; Bienengraeber, V.; Gedrange, T.; Fanghaenel, J.; Lotz, K. In vivo study of apoptosis as a creative agent of embryonic development of the primary nasal duct in rats. J. Craniomaxillofac. Surg. 2006, 34, S3-S7.
25. Huang, F.J.; Shen, C.C.; Chang, S.Y.; Wu, T.C.; Hsuuw, Y.D. Retinoic acid decreases the viability of mouse blastocysts in vitro. Hum. Reprod. 2003, 18, 130-136.
26. Shang, E.H.; Wu, R.S. Aquatic hypoxia is a teratogen and affects fish embryonic development. Environ. Sci. Technol. 2004, 38, 4763-4767.
27. Detmar, J.; Rabaglino, T.; Taniuchi, Y.; Oh, J.; Acton, B.M.; Benito, A.; Nunez, G.; Jurisicova, A. Embryonic loss due to exposure to polycyclic aromatic hydrocarbons is mediated by Bax. Apoptosis 2006, 11, 1413-1425.
28. Li, J.; Yin, S.; Dong, Y.; Fan, L.; Hu, H. p53 activation inhibits ochratoxin A-induced apoptosis in monkey and human kidney epithelial cells via suppression of JNK activation. Biochem. Biophys. Res. Commun. 2011, 411, 458-463.
29. Golli-Bennour, E.E.; Kouidhi, B.; Bouslimi, A.; Abid-Essefi, S.; Hassen, W.; Bacha, H. Cytotoxicity and genotoxicity induced by aflatoxin B1, ochratoxin A, and their combination in cultured Vero cells. J. Biochem. Mol. Toxicol. 2010, 24, 42-50.
30. Klaric, M.S.; Zeljezic, D.; Rumora, L.; Peraica, M.; Pepeljnjak, S.; Domijan, A.M. A potential role of calcium in apoptosis and aberrant chromatin forms in porcine kidney PK15 cells induced by individual and combined ochratoxin A and citrinin. Arch. Toxicol. 2012, 86, 97-107.
31. Sauvant, C.; Holzinger, H.; Gekle, M. Proximal tubular toxicity of ochratoxin A is amplified by simultaneous inhibition of the extracellular signal-regulated kinases 1/2. J. Pharmacol. Exp. Ther. 2005, 313, 234-241.
32. Hood, R.D.; Naughton, M.J.; Hayes, A.W. Prenatal effects of Ochratoxin A in hamsters. Teratology 1976, 13, 11-14.
33. Mayura, K.; Reddy, R.V.; Hayes, A.W.; Berndt, W.O. Embryocidal, fetotoxic and teratogenic effects of ochratoxin A in rats. Toxicology 1982, 25, 175-185.
34. Mayura, K.; Edwards, J.F.; Maull, E.A.; Phillips, T.D. The effects of ochratoxin A on postimplantation rat embryos in culture. Arch. Environ. Contam. Toxicol. 1989, 18, 411-415.
35. Chan, W.H.; Shiao, N.H. Effect of citrinin on mouse embryonic development in vitro and in vivo. Reprod. Toxicol. 2007, 24, 120-125.
36. Chan, W.H. Citrinin induces apoptosis via a mitochondria-dependent pathway and inhibition of survival signals in embryonic stem cells, and causes developmental injury in blastocysts. Biochem. J. 2007, 404, 317-326.
37. Chan, W.H. Citrinin induces apoptosis in mouse embryonic stem cells. IUBMB Life 2008, 60, 171-179.
38. Yu, F.; Watts, R.N.; Zhang, X.D.; Borrow, J.M.; Hersey, P. Involvement of BH3-only proapoptotic proteins in mitochondrial-dependent Phenoxodiol-induced apoptosis of human melanoma cells. Anticancer Drugs 2006, 17, 1151-1161.
39. Criollo, A.; Galluzzi, L.; Chiara Maiuri, M.; Tasdemir, E.; Lavandero, S.; Kroemer, G. Mitochondrial control of cell death induced by hyperosmotic stress. Apoptosis 2007, 12, 3-18.
40. Yoon, S.; Cong, W.T.; Bang, Y.; Lee, S.N.; Yoon, C.S.; Kwack, S.J.; Kang, T.S.; Lee, K.Y.; Choi, J.K.; Choi, H.J. Proteome response to ochratoxin A-induced apoptotic cell death in mouse hippocampal HT22 cells. Neurotoxicology 2009, 30, 666-676.
41. Sava, V.; Velasquez, A.; Song, S.; Sanchez-Ramos, J. Adult hippocampal neural stem/progenitor cells in vitro are vulnerable to the mycotoxin ochratoxin-A. Toxicol. Sci. 2007, 98, 187-197.
42. El Golli Bennour, E.; Rodriguez-Enfedaque, A.; Bouaziz, C.; Ladjimi, M.; Renaud, F.; Bacha, H. Toxicities induced in cultured human hepatocarcinoma cells exposed to ochratoxin A: Oxidative stress and apoptosis status. J. Biochem. Mol. Toxicol. 2009, 23, 87-96.
43. Wangikar, P.B.; Dwivedi, P.; Sinha, N. Effect in rats of simultaneous prenatal exposure to ochratoxin A and aflatoxin B1. I. Maternal toxicity and fetal malformations. Birth Defects Res. B 2004, 71, 343-351.
44. Biro, K.; Barna-Vetro, I.; Pecsi, T.; Szabo, E.; Winkler, G.; Fink-Gremmels, J.; Solti, L. Evaluation of spermatological parameters in ochratoxin A-Challenged boars. Theriogenology 2003, 60, 199-207.
45. Patil, R.D.; Dwivedi, P.; Sharma, A.K. Critical period and minimum single oral dose of ochratoxin A for inducing developmental toxicity in pregnant Wistar rats. Reprod. Toxicol. 2006, 22, 679-687.
46. Jennings-Gee, J.E.; Tozlovanu, M.; Manderville, R.; Miller, M.S.; Pfohl-Leszkowicz, A.; Schwartz, G.G. Ochratoxin A: In utero exposure in mice induces adducts in testicular DNA. Toxins 2010, 2, 1428-1444.
47. Cross, J.C.; Werb, Z.; Fisher, S.J. Implantation and the placenta: key pieces of the development puzzle. Science 1994, 266, 1508-1518.
48. Pampfer, S.; de Hertogh, R.; Vanderheyden, I.; Michiels, B.; Vercheval, M. Decreased inner cell mass proportion in blastocysts from diabetic rats. Diabetes 1990, 39, 471-476.
49. Kelly, S.M.; Robaire, B.; Hales, B.F. Paternal cyclophosphamide treatment causes postimplantation loss via inner cell mass-specific cell death. Teratology 1992, 45, 313-318.
50. Tam, P.P. Postimplantation development of mitomycin C-treated mouse blastocysts. Teratology 1988, 37, 205-212.
51. Chen, C.C.; Chan, W.H. Impact effects of puerarin on mouse embryonic development. Reprod. Toxicol. 2009, 28, 530-535.
52. Long, L.H.; Clement, M.V.; Halliwell, B. Artifacts in cell culture: Rapid generation of hydrogen peroxide on addition of (-)-epigallocatechin, (-)-epigallocatechin gallate, (+)-catechin, and quercetin to commonly used cell culture media. Biochem. Biophys. Res. Commun. 2000, 273, 50-53.
53. Halliwell, B. Oxidative stress in cell culture: An under-appreciated problem? FEBS Lett. 2003, 540, 3-6.
54. Liu, J.; Wang, Y.; Cui, J.; Xing, L.; Shen, H.; Wu, S.; Lian, H.; Wang, J.; Yan, X.; Zhang, X. Ochratoxin A induces oxidative DNA damage and G1 phase arrest in human peripheral blood mononuclear cells in vitro. Toxicol. Lett. 2012, 211, 164-171.
55. Kumar, R.; Ansari, K.M.; Chaudhari, B.P.; Dhawan, A.; Dwivedi, P.D.; Jain, S.K.; Das, M. Topical application of ochratoxin a causes DNA damage and tumor initiation in mouse skin. PLoS One 2012, 7, e47280.
56. Hardy, K.; Handyside, A.H.; Winston, R.M. The human blastocyst: Cell number, death and allocation during late preimplantation development in vitro. Development 1989, 107, 597-604.
57. Gardner, R.L.; Davies, T.J. Lack of coupling between onset of giant transformation and genome endoreduplication in the mural trophectoderm of the mouse blastocyst. J. Exp. Zool. 1993, 265, 54-60.
58. Huang, F.J.; Wu, T.C.; Tsai, M.Y. Effect of retinoic acid on implantation and post-implantation development of mouse embryos in vitro. Hum. Reprod. 2001, 16, 2171-2176.
59. Witschi, E. Characterization of Developmental Stages. Part II. Rat. In Biology Data Book, 2nd ed.; Federation of American Societies of Experimental Biologies: Washington, DC, USA, 1972; pp. 178-180.
60. Armant, D.R.; Kaplan, H.A.; Lennarz, W.J. Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts. Dev. Biol. 1986, 116, 519-523.
61. Pampfer, S.; Wuu, Y.D.; Vanderheyden, I.; de Hertogh, R. In vitro study of the carry-over effect associated with early diabetic embryopathy in the rat. Diabetologia 1994, 37, 855-862.
62. Chan, W.H. Embryonic toxicity of sanguinarine through apoptotic processes in mouse blastocysts. Toxicol. Lett. 2011, 205, 285-292.