Superoxide dismutase 1 overexpression in mice abolishes maternal diabetes-induced endoplasmic reticulum stress in diabetic embryopathy

American Journal of Obstetrics and Gynecology

Volumn 209, Issue 4, 2013, Pages 345.e1-345.e7

  Wang, Fang ^a   Reece, E Albert ^a   Yang, Peixin ^a  

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

Author keywords

diabetic embryopathy; endoplasmic reticulum stress; oxidative stress; superoxide dismutase 1 transgenic mice

Indexed keywords

CALNEXIN; COPPER ZINC SUPEROXIDE DISMUTASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; PROTEIN DISULFIDE ISOMERASE; PROTEIN IRE1; X BOX BINDING PROTEIN 1; DDIT3 PROTEIN, MOUSE; DNA BINDING PROTEIN; ERN1 PROTEIN, MOUSE; HEAT SHOCK PROTEIN; INITIATION FACTOR 2; MOLECULAR CHAPERONE GRP78; PDIA3 PROTEIN, MOUSE; PERK KINASE; PROTEIN KINASE R; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RIBONUCLEASE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC EMBRYOPATHY; EMBRYO; EMBRYOPATHY; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; IN VIVO STUDY; MALE; MATERNAL DIABETES MELLITUS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA SPLICING; WESTERN BLOTTING; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; DISEASE MODEL; FETUS DISEASE; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PREGNANCY DIABETES MELLITUS; TRANSGENIC MOUSE;

ANIMALS; CALNEXIN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EIF-2 KINASE; EMBRYO, MAMMALIAN; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; EUKARYOTIC INITIATION FACTOR-2; FEMALE; FETAL DISEASES; HEAT-SHOCK PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OXIDATIVE STRESS; PREGNANCY; PREGNANCY IN DIABETICS; PROTEIN DISULFIDE-ISOMERASES; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

EID: 84884671487     PISSN: 00029378     EISSN: 10976868     Source Type: Journal    
DOI: 10.1016/j.ajog.2013.06.037     Document Type: Article

References (53)

1. A. Correa, S.M. Gilboa, and L.M. Besser Diabetes mellitus and birth defects Am J Obstet Gynecol 199 2008 237.e1 237.e9
2. P. Yang, and E.A. Reece Role of HIF-1alpha in maternal hyperglycemia-induced embryonic vasculopathy Am J Obstet Gynecol 204 2011 332.e1 332.e7
3. P. Yang, and H. Li Epigallocatechin-3-gallate ameliorates hyperglycemia-induced embryonic vasculopathy and malformation by inhibition of Foxo3a activation Am J Obstet Gynecol 203 2010 75.e1 75.e6
4. Y. Cao, Z. Zhao, R.L. Eckert, and E.A. Reece Protein kinase Cbeta2 inhibition reduces hyperglycemia-induced neural tube defects through suppression of a caspase 8-triggered apoptotic pathway Am J Obstet Gynecol 204 2011 226.e1 226.e5
5. P. Yang, Y. Cao, and H. Li Hyperglycemia induces inducible nitric oxide synthase gene expression and consequent nitrosative stress via c-Jun N-terminal kinase activation Am J Obstet Gynecol 203 2010 185.e5 185.e11
6. X. Yang, L.A. Borg, and U.J. Eriksson Altered metabolism and superoxide generation in neural tissue of rat embryos exposed to high glucose Am J Physiol 272 1997 E173 E180
7. E. Sivan, Y.C. Lee, Y.K. Wu, and E.A. Reece Free radical scavenging enzymes in fetal dysmorphogenesis among offspring of diabetic rats Teratology 56 1997 343 349
8. E. Sivan, E.A. Reece, Y.K. Wu, C.J. Homko, M. Polansky, and M. Borenstein Dietary vitamin E prophylaxis and diabetic embryopathy: morphologic and biochemical analysis Am J Obstet Gynecol 175 1996 793 799
9. Z.J. Hagay, Y. Weiss, and I. Zusman Prevention of diabetes-associated embryopathy by overexpression of the free radical scavenger copper zinc superoxide dismutase in transgenic mouse embryos Am J Obstet Gynecol 173 1995 1036 1041
10. E. Szegezdi, S.E. Logue, A.M. Gorman, and A. Samali Mediators of endoplasmic reticulum stress-induced apoptosis EMBO Rep 7 2006 880 885
11. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 2007 519 529
12. D. Ron, and S.R. Hubbard How IRE1 reacts to ER stress Cell 132 2008 24 26
13. H.P. Harding, Y. Zhang, and D. Ron Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase Nature 397 1999 271 274
14. K. Lee, W. Tirasophon, and X. Shen IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response Genes Dev 16 2002 452 466
15. H. Zinszner, M. Kuroda, and X. Wang CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum Genes Dev 12 1998 982 995
16. X. Li, C. Xu, and P. Yang c-Jun NH2-terminal kinase 1/2 and endoplasmic reticulum stress as interdependent and reciprocal causation in diabetic embryopathy Diabetes 62 2013 599 608
17. X. Li, H. Weng, C. Xu, E.A. Reece, and P. Yang Oxidative stress-induced JNK1/2 activation triggers proapoptotic signaling and apoptosis that leads to diabetic embryopathy Diabetes 61 2012 2084 2092
18. P. Yang, Z. Zhao, and E.A. Reece Involvement of c-Jun N-terminal kinases activation in diabetic embryopathy Biochem Biophys Res Commun 357 2007 749 754
19. H. Weng, X. Li, E.A. Reece, and P. Yang SOD1 suppresses maternal hyperglycemia-increased iNOS expression and consequent nitrosative stress in diabetic embryopathy Am J Obstet Gynecol 206 2012 448.e1 448.e7
20. X. Li, H. Weng, E.A. Reece, and P. Yang SOD1 overexpression in vivo blocks hyperglycemia-induced specific PKC isoforms: substrate activation and consequent lipid peroxidation in diabetic embryopathy Am J Obstet Gynecol 205 2011 84.e1 84.e6
21. S. Hanada, M. Harada, and H. Kumemura Oxidative stress induces the endoplasmic reticulum stress and facilitates inclusion formation in cultured cells J Hepatol 47 2007 93 102
22. P. Yang, Z. Zhao, and E.A. Reece Activation of oxidative stress signaling that is implicated in apoptosis with a mouse model of diabetic embryopathy Am J Obstet Gynecol 198 2008 130.e1 130.e7
23. P. Yang, Z. Zhao, and E.A. Reece Blockade of c-Jun N-terminal kinase activation abrogates hyperglycemia-induced yolk sac vasculopathy in vitro Am J Obstet Gynecol 198 2008 321.e1 321.e7
24. E.A. Reece, Y.K. Wu, Z. Zhao, and D. Dhanasekaran Dietary vitamin and lipid therapy rescues aberrant signaling and apoptosis and prevents hyperglycemia-induced diabetic embryopathy in rats Am J Obstet Gynecol 194 2006 580 585
25. Y. Groner, O. Elroy-Stein, and K.B. Avraham Cell damage by excess CuZnSOD and Down's syndrome Biomed Pharmacother 48 1994 231 240
26. M.E. Gurney, H. Pu, and A.Y. Chiu Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation Science 264 1994 1772 1775
27. M.F. Greene, J.W. Hare, J.P. Cloherty, B.R. Benacerraf, and J.S. Soeldner First-trimester hemoglobin A1 and risk for major malformation and spontaneous abortion in diabetic pregnancy Teratology 39 1989 225 231
28. E. Miller, J.W. Hare, and J.P. Cloherty Elevated maternal hemoglobin A1c in early pregnancy and major congenital anomalies in infants of diabetic mothers N Engl J Med 304 1981 1331 1334
29. M. Boyce, K.F. Bryant, and C. Jousse A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress Science 307 2005 935 939
30. C. Hetz The unfolded protein response: controlling cell fate decisions under ER stress and beyond Nat Rev Mol Cell Biol 13 2012 89 102
31. A. Kaser, A.H. Lee, and A. Franke XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease Cell 134 2008 743 756
32. Z. Zhao Endoplasmic reticulum stress in maternal diabetes-induced cardiac malformations during critical cardiogenesis period Birth Defects Res B Dev Reprod Toxicol 95 2012 1 6
33. E.A. Reece, and Y.K. Wu Prevention of diabetic embryopathy in offspring of diabetic rats with use of a cocktail of deficient substrates and an antioxidant Am J Obstet Gynecol 176 1997 790 797 discussion 797-8
34. H.R. Kim, G.H. Lee, E.Y. Cho, S.W. Chae, T. Ahn, and H.J. Chae Bax inhibitor 1 regulates ER-stress-induced ROS accumulation through the regulation of cytochrome P450 2E1 J Cell Sci 122 2009 1126 1133
35. E.A. Reece, Y.K. Wu, and A. Wiznitzer Dietary polyunsaturated fatty acid prevents malformations in offspring of diabetic rats Am J Obstet Gynecol 175 1996 818 823
36. A. Correa, S.M. Gilboa, and L.D. Botto Lack of periconceptional vitamins or supplements that contain folic acid and diabetes mellitus-associated birth defects Am J Obstet Gynecol 206 2012 218.e1 218.e13
37. A. Conde-Agudelo, R. Romero, J.P. Kusanovic, and S.S. Hassan Supplementation with vitamins C and E during pregnancy for the prevention of preeclampsia and other adverse maternal and perinatal outcomes: a systematic review and metaanalysis Am J Obstet Gynecol 204 2011 503.e1 503.e12
38. R.P. Gunatilake, and J.H. Perlow Obesity and pregnancy: clinical management of the obese gravida Am J Obstet Gynecol 204 2011 106 119
39. P.M. Catalano, and S. Hauguel-De Mouzon Is it time to revisit the Pedersen hypothesis in the face of the obesity epidemic? Am J Obstet Gynecol 204 2011 479 487
40. M.M. Hedderson, M.A. Williams, V.L. Holt, N.S. Weiss, and A. Ferrara Body mass index and weight gain prior to pregnancy and risk of gestational diabetes mellitus Am J Obstet Gynecol 198 2008 409.e1 409.e7
41. S.J. Herring, E. Oken, and S.L. Rifas-Shiman Weight gain in pregnancy and risk of maternal hyperglycemia Am J Obstet Gynecol 201 2009 61.e1 61.e7
42. H.R. Hull, J.C. Thornton, and Y. Ji Higher infant body fat with excessive gestational weight gain in overweight women Am J Obstet Gynecol 205 2011 211.e1 211.e7
43. A.M. Lynch, R.H. Eckel, and J.R. Murphy Prepregnancy obesity and complement system activation in early pregnancy and the subsequent development of preeclampsia Am J Obstet Gynecol 206 2012 428.e1 428.e8
44. E.R. Cardozo, L.M. Neff, and M.E. Brocks Infertility patients' knowledge of the effects of obesity on reproductive health outcomes Am J Obstet Gynecol 207 2012 509.e1 509.e10
45. K.B. Wolfe, R.A. Rossi, and C.R. Warshak The effect of maternal obesity on the rate of failed induction of labor Am J Obstet Gynecol 205 2011 128.e1 128.e7
46. D.R. Halloran, N.E. Marshall, R.M. Kunovich, and A.B. Caughey Obesity trends and perinatal outcomes in black and white teenagers Am J Obstet Gynecol 207 2012 492.e1 492.e7
47. A. Khatibi, A.L. Brantsaeter, and V. Sengpiel Prepregnancy maternal body mass index and preterm delivery Am J Obstet Gynecol 207 2012 212.e1 212.e7
48. S. Mornar, L.N. Chan, S. Mistretta, A. Neustadt, S. Martins, and M. Gilliam Pharmacokinetics of the etonogestrel contraceptive implant in obese women Am J Obstet Gynecol 207 2012 110.e1 110.e6
49. A.M. Stuebe, M.B. Landon, and Y. Lai Maternal BMI, glucose tolerance, and adverse pregnancy outcomes Am J Obstet Gynecol 207 2012 62.e1 62.e7
50. L.M. Yee, Y.W. Cheng, M. Inturrisi, and A.B. Caughey Effect of gestational weight gain on perinatal outcomes in women with type 2 diabetes mellitus using the 2009 Institute of Medicine guidelines Am J Obstet Gynecol 205 2011 257.e1 257.e6
51. H.A. Roeder, T.R. Moore, and G.A. Ramos Insulin pump dosing across gestation in women with well-controlled type 1 diabetes mellitus Am J Obstet Gynecol 207 2012 324.e1 324.e5
52. K.E. Yanit, J.M. Snowden, Y.W. Cheng, and A.B. Caughey The impact of chronic hypertension and pregestational diabetes on pregnancy outcomes Am J Obstet Gynecol 207 2012 333.e1 333.e6
53. M. Loset, S.B. Mundal, and M.P. Johnson A transcriptional profile of the decidua in preeclampsia Am J Obstet Gynecol 204 2011 84.e1 84.e27