Emodin and [6]-gingerol lessen hypoxia-induced embryotoxicities in cultured mouse whole embryos via upregulation of hypoxia-inducible factor 1α and intracellular superoxide dismutases

Reproductive Toxicology

Volumn 31, Issue 4, 2011, Pages 513-518

  Yon, Jung Min ^a   Baek, In Jeoung ^b   Lee, Beom Jun ^a   Yun, Young Won ^a   Nam, Sang Yoon ^a  

^a Chungbuk National University   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

Antioxidants; Emodin; Gingerol; HIF 1 ; Hypoxia; Mouse whole embryo culture; SOD

Indexed keywords

(6) GINGEROL; ANTIOXIDANT; CELL ENZYME; COPPER ZINC SUPEROXIDE DISMUTASE; EMODIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MANGANESE SUPEROXIDE DISMUTASE; MANGANESE TETRAKIS (4 BENZOIC ACID)PORPHYRIN; MESSENGER RNA; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; EMBRYO; EMBRYOTOXICITY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION REGULATION; HYPOXIA; MALE; MOUSE; NONHUMAN; ONTOGENY; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; CATECHOLS; CELL HYPOXIA; CYTOPROTECTION; EMBRYO CULTURE TECHNIQUES; EMBRYO, MAMMALIAN; EMODIN; FATTY ALCOHOLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GESTATIONAL AGE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; METALLOPORPHYRINS; MICE; MICE, INBRED ICR; OXIDATIVE STRESS; RNA, MESSENGER; SUPEROXIDE DISMUTASE; UP-REGULATION;

EID: 79956342661     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.02.011     Document Type: Article

References (54)

1. Rodesch F., Simon P., Donner C., Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992, 80:283-285.
2. Burton G.J., Hempstock J., Jauniaux E. Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 2003, 6:84-96.
3. Andras N., Marina G., Kristina V., Richard B. Manipulating the mouse embryo. A laboratory manual 2002, 237-241. John Inglis, New York. 3rd ed. I. John, C. Judy (Eds.).
4. Ream M., Ray A.M., Chandra R., Chikaraishi D.M. Early fetal hypoxia leads to growth restriction and myocardial thinning. Am J Physiol Regul Integr Comp Physiol 2008, 295:R583-R595.
5. Li R., Chase M., Jung S.K., Smith P.J., Loeken M.R. Hypoxic stress in diabetic pregnancy contributes to impaired embryo gene expression and defective development by inducing oxidative stress. Am J Physiol Endocrinol Metab 2005, 289:E591-E599.
6. Webster W.S., Abela D. The effect of hypoxia in development. Birth Defects Res Clin Embryo Today 2007, 81:215-228.
7. Ornoy A. Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy. Reprod Toxicol 2007, 24:31-41.
8. Chen E.Y., Fujinaga M., Giaccia A.J. Hypoxic microenvironment within an embryo induces apoptosis and is essential for proper morphological development. Teratology 1999, 60(4):215-225.
9. Schipani E., Ryan H.E., Didrickson S., Kobayashi T., Knight M., Johnson R.S. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev 2001, 15(21):2865-2876.
10. Dennery P.A. Effects of oxidative stress on embryonic development. Birth Defects Res Clin Embryo Today 2007, 81:155-162.
11. McCord J.M., Fridovich I. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 1969, 244:6049-6055.
12. Crapo J.D., Oury T., Rabouille C., Slot J.W., Chang L.Y. Copper, zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc Natl Acad Sci U S A 1992, 89:10405-10409.
13. Okado-Matsumoto A., Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 2001, 276:38388-38393.
14. Weisiger R.A., Fridovich I. Mitochondrial superoxide simutase site of synthesis and intramitochondrial localization. J Biol Chem 1973, 248:4793-4796.
15. Tapsell L.C., Hemphill I., Cobiac L., Patch C.S., Sullivan D.R., Fenech M., et al. Health benefits of herbs and spices: the past, the present, the future. Med J Aust 2006, 185:S4-S24.
16. Dang S.S., Zhang X., Jia X.L., Cheng Y.A., Song P., Liu E.Q., et al. Protective effects of emodin and astragalus polysaccharides on chronic hepatic injury in rats. Chin Med J (Engl) 2008, 121:1010-1014.
17. Ding Y., Zhao L., Mei H., Zhang S.L., Huang Z.H., Duan Y.Y., et al. Exploration of emodin to treat alpha-naphthylisothiocyanate-induced cholestatic hepatitis via anti-inflammatory pathway. Eur J Pharmacol 2008, 590:377-386.
18. Sekiwa Y., Kubota K., Kobayashi A. Isolation of novel glucosides related to gingerdiol from ginger and their antioxidative activities. J Agric Food Chem 2000, 48:373-377.
19. Ahmad N., Katiyar S.K., Mukhtar H. Antioxidants in chemoprevention of skin cancer. Curr Probl Dermatol 2001, 29:128-139.
20. Grzanna R., Lindmark L., Frondoza C.G. Ginger - an herbal medicinal product with broad anti-inflammatory actions. J Med Food 2005, 8:125-132.
21. Ahmed R.S., Suke S.G., Seth V., Chakraborti A., Tripathi A.K., Banerjee B.D. Protective effects of dietary ginger (Zingiber officinales Rosc.) on lindane-induced oxidative stress in rats. Phytother Res 2008, 22:902-906.
22. Ling X., Liu D. Temporal and spatial profiles of cell loss after spinal cord injury: reduction by a metalloporphyrin. J Neurosci Res 2007, 85:2175-2185.
23. New D.A. Whole-embryo culture and the study of mammalian embryos during organogenesis. Biol Rev Camb Philos Soc 1978, 53:81-122.
24. Van Maele-Fabry G., Delhaise F., Picard J.J. Morphogenesis and quantification of the development of post-implantation mouse embryos. Toxicol In Vitro 1990, 4:149-156.
25. Bewley G.C. cDNA and deduced amino acid sequence of murine Cu-Zn superoxide dismutase. Nucleic Acids Res 1988, 16:2728.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25(4):402-408.
27. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 7:248-254.
28. Kingdom J.C., Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta 1997, 18:613-621.
29. Guzy R.D., Hoyos B., Robin E., Chen H., Liu L., Mansfield K.D., et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 2005, 1:401-408.
30. Mansfield K.D., Guzy R.D., Pan Y., Young R.M., Cash T.P., Schumacker P.T., et al. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 2005, 1:393-399.
31. Weisiger R.A., Fridovich I. Mitochondrial superoxide simutase Site of synthesis and intramitochondrial localization. J Biol Chem 1973, 248:4793-4796.
32. Beyer W., Imlay J., Fridovich I. Superoxide dismutases. Prog Nucleic Acid Res Mol Biol 1991, 40:221-253.
33. Poranen A.K., Ekblad U., Uotila P., Ahotupa M. Lipid peroxidation and antioxidants in normal and pre-eclamptic pregnancies. Placenta 1996, 17:401-405.
34. Wang Y., Walsh S.W. Antioxidant activities and mRNA expression of superoxide dismutase, catalase, and glutathione peroxidase in normal and preeclamptic placentas. J Soc Gynecol Investig 1996, 3:179-184.
35. Hagay Z.J., Weiss Y., Zusman I., Peled-Kamar M., Reece E.A., Eriksson U.J., et al. Prevention of diabetes-associated embryopathy by overexpression of the free radical scavenger copper zinc superoxide dismutase in transgenic mouse embryos. Am J Obstet Gynecol 1995, 173:1036-1041.
36. Lipton J.W., Gyawali S., Borys E.D., Koprich J.B., Ptaszny M., McGuire S.O. Prenatal cocaine administration increases glutathione and alpha-tocopherol oxidation in fetal rat brain. Brain Res Dev Brain Res 2003, 147:77-84.
37. Gareskog M., Eriksson U.J., Wentzel P. Combined supplementation of folic acid and vitamin E diminishes diabetes-induced embryotoxicity in rats. Birth Defects Res Clin Mol Teratol 2006, 76:483-490.
38. Wentzel P., Eriksson U.J. Ethanol-induced fetal dysmorphogenesis in the mouse is diminished by high antioxidative capacity of the mother. Toxicol Sci 2006 2006, 92:416-422.
39. Wentzel P., Rydberg U., Eriksson U.J. Antioxidative treatment diminishes ethanol-induced congenital malformations in the rat. Alcohol Clin Exp Res 2006, 30:1752-1760.
40. Kim M.R., Lee K.N., Yon J.M., Lee S.R., Jin Y., Baek I.J., et al. Capsaicin prevents ethanol-induced teratogenicity in cultured mouse whole embryos. Reprod Toxicol 2008, 26(3-4):292-297.
41. Lee S.R., Kim M.R., Yon J.M., Baek I.J., Lee B.J., Ahn B., et al. Effects of ginsenosides on organogenesis and expression of glutathione peroxidase genes in cultured rat embryos. J Reprod Dev 2008, 54:164-170.
42. Kuhad A., Tirkey N., Pilkhwal S., Chopra K. 6-Gingerol prevents cisplatin-induced acute renal failure in rats. Biofactors 2006, 26(3):189-200.
43. Mallikarjuna K., Sahitya Chetan P., Sathyavelu Reddy K., Rajendra W. Ethanol toxicity: rehabilitation of hepatic antioxidant defense system with dietary ginger. Fitoterapia 2008, 79:174-178.
44. Patel M.N. Metalloporphyrins improve the survival of Sod2-deficient neurons. Aging Cell 2003, 2:219-222.
45. Richard D.E., Berra E., Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem 2000, 275:26765-26771.
46. Görlach A., Diebold I., Schini-Kerth V.B., Berchner-Pfannschmidt U., Roth U., Brandes R.P., et al. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: role of the p22(phox)-containing NADPH oxidase. Circ Res 2001, 89:47-54.
47. Kietzmann T., Freimann S., Bratke J., Jungermann K. Regulation of the gluconeogenic phosphoenolpyruvate carboxykinase and glycolytic aldolase A gene expression by O2 in rat hepatocyte cultures Involvement of hydrogen peroxide as mediator in the response to O2. FEBS Lett 1996, 388:228-232.
48. Guzy R.D., Hoyos B., Robin E., Chen H., Liu L., Mansfield K.D., et al. Mitochondrial complex III is required for hypoxiainduced ROS production and cellular oxygen sensing. Cell Metab 2005, 1:401-408.
49. Chandel N.S., McClintock D.S., Feliciano C.E., Wood T.M., Melendez J.A., Rodriguez A.M., et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000, 275:25130-25138.
50. Huang L.E., Arany Z., Livingston D.M., Bunn H.F. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 1996, 271:32253-32259.
51. Chang T.C., Huang C.J., Tam K., Chen S.F., Tan K.T., Tsai M.S., et al. Stabilization of hypoxia-inducible factor-1{alpha} by prostacyclin under prolonged hypoxia via reducing reactive oxygen species level in endothelial cells. J Biol Chem 2005, 280:36567-36574.
52. Srinivas V., Leshchinsky I., Sang N., King M.P., Minchenko A., Caro J. Oxygen sensing and HIF-1 activation does not require an active mitochondrial respiratory chain electron-transfer pathway. J Biol Chem 2001, 276:21995-21998.
53. Wellman T.L., Jenkins J., Penar P.L., Tranmer B., Zahr R., Lounsbury K.M. Nitric oxide and reactive oxygen species exert opposing effects on the stability of hypoxia inducible factor-1α (HIF-1α) in explants of human pial arteries. FASEB J 2004, 18(2):379-381.
54. Iyer N.V., Kotch L.E., Agani F., Leung S.W., Laughner E., Wenger R.H., et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998, 12:149-162.