The Nrf2 Activator Vinylsulfone Reduces High Glucose-Induced Neural Tube Defects by Suppressing Cellular Stress and Apoptosis

Reproductive Sciences

Volumn 23, Issue 8, 2016, Pages 993-1000

  Dong, Daoyin ^a   Reece, E Albert ^a,b   Yang, Peixin ^a,b  

^a Gynecology and Reproductive Sciences ^*  (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; diabetic embryopathy; high glucose; Nrf2 activator; oxidative stress

Indexed keywords

3 NITROTYROSINE; 4 HYDROXYNONENAL; BINDING IMMUNOGLOBULIN PROTEIN; BINDING PROTEIN; CASPASE 3; CASPASE 8; CHALCONE DERIVATIVE; GLUCOSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INOSITOL 1 PHOSPHATASE; INOSITOL REQUIRING PROTEIN 1ALPHA; LIPID HYDROPEROXIDE; MESSENGER RNA; PHOSPHOPROTEIN; PHOSPHORYLATED PROTEIN KINASE RNA LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG; VINYLSULFONE; X BOX BINDING PROTEIN 1; CASP3 PROTEIN, MOUSE; CASP8 PROTEIN, MOUSE; DIVINYL SULFONE; NFE2L2 PROTEIN, MOUSE; SULFONE; TRANSCRIPTION FACTOR NRF2; XBP1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL PROTECTION; CELL STRESS; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME INHIBITION; MALE; MOUSE; NEURAL TUBE DEFECT; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RAT; RNA SPLICING; AGONISTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FEMALE; METABOLISM; NEURAL TUBE DEFECTS;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 8; ENDOPLASMIC RETICULUM STRESS; FEMALE; GLUCOSE; MICE; MICE, INBRED C57BL; NEURAL TUBE DEFECTS; NF-E2-RELATED FACTOR 2; RNA, MESSENGER; SULFONES; X-BOX BINDING PROTEIN 1;

EID: 84978287465     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719115625846     Document Type: Article

References (68)

1. Yang P, Reece EA, Wang F, Gabbay-Benziv R,. Decoding the oxidative stress hypothesis in diabetic embryopathy through proapoptotic kinase signaling. Am J Obstetr Gynecol. 2015; 212 (5): 569-579.
2. Wang F, Reece EA, Yang P,. Advances in revealing the molecular targets downstream of oxidative stress-induced proapoptotic kinase signaling in diabetic embryopathy. Am J Obstet Gynecol. 2015; 213 (2): 125-134.
3. Gabbay-Benziv R, Reece EA, Wang F, Yang P,. Birth defects in pregestational diabetes: Defect range, glycemic threshold and pathogenesis. World J Diabetes. 2015; 6 (3): 481-488.
4. Dincer Y, Akcay T, Alademir Z, Ilkova H,. Assessment of DNA base oxidation and glutathione level in patients with type 2 diabetes. Mutat Res. 2002; 505 (1-2): 75-81.
5. Sakamaki H, Akazawa S, Ishibashi M, et al. Significance of glutathione-dependent antioxidant system in diabetes-induced embryonic malformations. Diabetes. 1999; 48 (5): 1138-1144.
6. Wolff SP., Diabetes mellitus and free radicals. Free radicals, transition metals and oxidative stress in the aetiology of diabetes mellitus and complications. Br Med Bull. 1993; 49 (3): 642-652.
7. Baynes JW,. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991; 40 (4): 405-412.
8. Droge W,. Free radicals in the physiological control of cell function. Physiol Rev. 2002; 82 (1): 47-95.
9. Evans JL, Goldfine ID, Maddux BA, Grodsky GM,. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev. 2002; 23 (5): 599-622.
10. Dong J, Sulik KK, Chen SY,. Nrf2-mediated transcriptional induction of antioxidant response in mouse embryos exposed to ethanol in vivo: implications for the prevention of fetal alcohol spectrum disorders. Antioxid Redox Signal. 2008; 10 (12): 2023-2033.
11. Wang F, Fisher SA, Zhong J, Wu Y, Yang P,. Superoxide Dismutase 1 in vivo Ameliorates Maternal Diabetes-Induced Apoptosis and Heart Defects through Restoration of Impaired Wnt Signaling. Circ Cardiovasc Genet. 2015; 8 (5): 665-676.
12. Dong D, Reece EA, Lin X, Wu Y, AriasVillela N, Yang P,. New development of the yolk sac theory in diabetic embryopathy: molecular mechanism and link to structural birth defects[published online September 30, 2015]. Am J Obstet Gynecol. 2015.
13. Pinter E, Reece EA, Leranth CZ, et al. Yolk sac failure in embryopathy due to hyperglycemia: ultrastructural analysis of yolk sac differentiation associated with embryopathy in rat conceptuses under hyperglycemic conditions. Teratology. 1986; 33 (1): 73-84.
14. Reece EA, Pinter E, Leranth CZ, et al. Ultrastructural analysis of malformations of the embryonic neural axis induced by in vitro hyperglycemic conditions. Teratology. 1985; 32 (3): 363-373.
15. Li J, Wang JJ, Yu Q, Wang M, Zhang SX,. Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett. 2009; 583 (9): 1521-1527.
16. Lupachyk S, Watcho P, Stavniichuk R, Shevalye H, Obrosova IG,. Endoplasmic reticulum stress plays a key role in the pathogenesis of diabetic peripheral neuropathy. Diabetes. 2013; 62 (3): 944-952.
17. Wang F, Reece EA, Yang P,. Superoxide dismutase 1 overexpression in mice abolishes maternal diabetes-induced endoplasmic reticulum stress in diabetic embryopathy. Am J Obstet Gynecol. 2013; 209 (4): 345. e1-e7.
18. Li X, Xu C, Yang P,. c-Jun NH2-terminal kinase 1/2 and endoplasmic reticulum stress as interdependent and reciprocal causation in diabetic embryopathy. Diabetes. 2013; 62 (2): 599-608.
19. Wang F, Wu Y, Quon MJ, Li X, Yang P,. ASK1 mediates the teratogenicity of diabetes in the developing heart by inducing ER stress and inhibiting critical factors essential for cardiac development. Am J Physiol Endocrinol Metab. 2015; 309 (5): E487-E499.
20. Wu Y, Wang F, Fu M, Wang C, Quon MJ, Yang P,. Cellular stress, excessive apoptosis, and the effect of metformin in a mouse model of type 2 diabetic embryopathy. Diabetes. 2015; 64 (7): 2526-2536.
21. Wu Y, Wang F, Reece EA, Yang P,. Curcumin ameliorates high glucose-induced neural tube defects by suppressing cellular stress and apoptosis. Am J Obstet Gynecol. 2015; 212 (6): 802. e1-e8.
22. Gu H, Yu J, Dong D, Zhou Q, Wang JY, Yang P,. The miR-322-TRAF3 circuit mediates the pro-apoptotic effect of high glucose on neural stem cells. Toxicol Sci. 2015; 144 (1): 186-196.
23. Wang F, Wu Y, Gu H, et al. Ask1 gene deletion blocks maternal diabetes-induced endoplasmic reticulum stress in the developing embryo by disrupting the unfolded protein response signalosome. Diabetes. 2015; 64 (3): 973-988.
24. Yang P, Li X, Xu C, Reece EA, Zielke HR, Wang F,. Maternal hyperglycemia activates an ASK1-FoxO3a-caspase 8 pathway that leads to embryonic neural tube defects. Sci Signal. 2013; 6 (290): ra74.
25. Wang F, Weng H, Quon MJ, et al. Dominant negative FADD dissipates the proapoptotic signalosome of the unfolded protein response in diabetic embryopathy. Am J Physiol Endocrinol Metab. 2015; 309 (10): E861-E873.
26. Gu H, Yu J, Dong D, et al. High glucose-repressed CITED2 expression through miR-200b triggers the unfolded protein response and endoplasmic reticulum stress. Diabetes. 2016; 65 (1): 149-163.
27. Li X, Weng H, Reece EA, Yang P,. SOD1 overexpression in vivo blocks hyperglycemia-induced specific PKC isoforms: substrate activation and consequent lipid peroxidation in diabetic embryopathy. Am J Obstet Gynecol. 2011; 205 (1): 84. e1-e6.
28. Yang P, Li H,. Epigallocatechin-3-gallate ameliorates hyperglycemia-induced embryonic vasculopathy and malformation by inhibition of Foxo3a activation. Am J Obstet Gynecol. 2010; 203 (1): 75. e1-e6.
29. Reece EA, Wu YK, Zhao Z, Dhanasekaran D,. Dietary vitamin and lipid therapy rescues aberrant signaling and apoptosis and prevents hyperglycemia-induced diabetic embryopathy in rats. Am J Obstet Gynecol. 2006; 194 (2): 580-585.
30. Reece EA, Wu YK, Wiznitzer A, et al. Dietary polyunsaturated fatty acid prevents malformations in offspring of diabetic rats. Am J Obstet Gynecol. 1996; 175 (4 pt 1): 818-823.
31. Xu C, Li X, Wang F, Weng H, Yang P,. Trehalose prevents neural tube defects by correcting maternal diabetes-suppressed autophagy and neurogenesis. Am J Physiol Endocrinol Metab. 2013; 305 (5): E667-E678.
32. Correa A, Botto L, Liu Y, Mulinare J, Erickson JD,. Do multivitamin supplements attenuate the risk for diabetes-associated birth defects? Pediatrics. 2003; 111 (5 pt 2): 1146-1151.
33. Zhong J, Reece EA, Yang P,. Punicalagin exerts protective effect against high glucose-induced cellular stress and neural tube defects. Biochem Biophys Res Commun. 2015; 467 (2): 179-184.
34. Grodstein F, O'Brien J, Kang JH, et al. Long-term multivitamin supplementation and cognitive function in men: a randomized trial. Ann Intern Med. 2013; 159 (12): 806-814.
35. Guallar E, Stranges S, Mulrow C, Appel LJ, Miller ER III,. Enough is enough: Stop wasting money on vitamin and mineral supplements. Ann Intern Med. 2013; 159 (12): 850-851.
36. Kensler TW, Wakabayashi N, Biswal S,. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007; 47: 89-116.
37. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, et al. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci U S A. 2004; 101 (7): 2040-2045.
38. de Vries HE, Witte M, Hondius D, et al. Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med. 2008; 45 (10): 1375-1383.
39. Sporn MB, Liby KT,. NRF2 and cancer: the good, the bad and the importance of context. Nat Rev Cancer. 2012; 12 (8): 564-571.
40. Li J, Ichikawa T, Villacorta L, et al. Nrf2 protects against maladaptive cardiac responses to hemodynamic stress. Arterioscler Thromb Vasc Biol. 2009; 29 (11): 1843-1850.
41. Tan Y, Ichikawa T, Li J, et al. Diabetic downregulation of Nrf2 activity via ERK contributes to oxidative stress-induced insulin resistance in cardiac cells in vitro and in vivo. Diabetes. 2011; 60 (2): 625-633.
42. Lee Y, Shin DH, Kim JH, et al. Caffeic acid phenethyl ester-mediated Nrf2 activation and IkappaB kinase inhibition are involved in NFkappaB inhibitory effect: structural analysis for NFkappaB inhibition. Eur J Pharmacol. 2010; 643 (1): 21-28.
43. Dinkova-Kostova AT, Liby KT, Stephenson KK, et al. Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc Natl Acad Sci U S A. 2005; 102 (12): 4584-4589.
44. Yates MS, Tauchi M, Katsuoka F, et al. Pharmacodynamic characterization of chemopreventive triterpenoids as exceptionally potent inducers of Nrf2-regulated genes. Mol Cancer Ther. 2007; 6 (1): 154-162.
45. Zheng H, Whitman SA, Wu W, et al. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes. 2011; 60 (11): 3055-3066.
46. Woo SY, Kim JH, Moon MK, et al. Discovery of vinyl sulfones as a novel class of neuroprotective agents toward Parkinson's disease therapy. J Med Chem. 2014; 57 (4): 1473-1487.
47. Weng H, Li X, Reece EA, Yang P,. SOD1 suppresses maternal hyperglycemia-increased iNOS expression and consequent nitrosative stress in diabetic embryopathy. Am J Obstet Gynecol. 2012; 206 (5): 448. e1-e7.
48. Ma Q,. Role of nrf2 in oxidative stress and toxicity. Ann Rev Pharmacol Toxicol. 2013; 53: 401-426.
49. Kaspar JW, Niture SK, Jaiswal AK,. Nrf2: INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med. 2009; 47 (9): 1304-1309.
50. Cullinan SB, Gordan JD, Jin J, Harper JW, Diehl JA,. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol. 2004; 24 (19): 8477-8486.
51. Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M,. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol. 2004; 24 (24): 10941-10953.
52. Dhakshinamoorthy S, Long DJ 2nd, Jaiswal AK,. Antioxidant regulation of genes encoding enzymes that detoxify xenobiotics and carcinogens. Curr Top Cell Regul. 2000; 36: 201-216.
53. Zhang DD,. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev. 2006; 38 (4): 769-789.
54. Kobayashi M, Yamamoto M,. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzyme Regul. 2006; 46: 113-140.
55. Copple IM, Goldring CE, Kitteringham NR, Park BK,. The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 2008; 246 (1): 24-33.
56. Hybertson BM, Gao B,. Role of the Nrf2 signaling system in health and disease. Clin Genet. 2014; 86 (5): 447-452.
57. Bhakkiyalakshmi E, Sireesh D, Rajaguru P, Paulmurugan R, Ramkumar KM,. The emerging role of redox-sensitive Nrf2-Keap1 pathway in diabetes. Pharmacol Res. 2015; 91: 104-114.
58. Garber K,. Biochemistry: a radical treatment. Nature. 2012; 489 (7417): S4-S6.
59. Chuengsamarn S, Rattanamongkolgul S, Luechapudiporn R, Phisalaphong C, Jirawatnotai S,. Curcumin extract for prevention of type 2 diabetes. Diabetes Care. 2012; 35 (11): 2121-2127.
60. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB,. Bioavailability of curcumin: problems and promises. Mol Pharm. 2007; 4 (6): 807-818.
61. Li H, Zhang L, Wang F, et al. Attenuation of glomerular injury in diabetic mice with tert-butylhydroquinone through nuclear factor erythroid 2-related factor 2-dependent antioxidant gene activation. Am J Nephrol. 2011; 33 (4): 289-297.
62. Hirose M, Yada H, Hakoi K, Takahashi S, Ito N,. Modification of carcinogenesis by alpha-tocopherol, t-butylhydroquinone, propyl gallate and butylated hydroxytoluene in a rat multi-organ carcinogenesis model. Carcinogenesis. 1993; 14 (4): 2359-2364.
63. Pergola PE, Raskin P, Toto RD, et al. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med. 2011; 365 (4): 327-336.
64. Di Carlo G, Mascolo N, Izzo AA, Capasso F,. Flavonoids: old and new aspects of a class of natural therapeutic drugs. Life Sci. 1999; 65 (4): 337-353.
65. Singh P, Anand A, Kumar V,. Recent developments in biological activities of chalcones: a mini review. Eur J Med Chem. 2014; 85: 758-777.
66. Vahakangas K, Myllynen P,. Drug transporters in the human blood-placental barrier. Br J Pharmacol. 2009; 158 (3): 665-678.
67. Rangel LP, Winter E, Gauthier C, et al. New structure-activity relationships of chalcone inhibitors of breast cancer resistance protein: polyspecificity toward inhibition and critical substitutions against cytotoxicity. Drug Des Devel Ther. 2013; 7: 1043-1052.
68. Parveen Z, Brunhofer G, Jabeen I, Erker T, Chiba P, Ecker GF,. Synthesis, biological evaluation and 3D-QSAR studies of new chalcone derivatives as inhibitors of human P-glycoprotein. Bioorg Med Chem. 2014; 22 (7): 2311-2319.