Advances in revealing the molecular targets downstream of oxidative stress-induced proapoptotic kinase signaling in diabetic embryopathy

American Journal of Obstetrics and Gynecology

Volumn 213, Issue 2, 2015, Pages 125-134

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

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

Author keywords

apoptosis; birth defects; kinase signaling; maternal diabetes; oxidative stress

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; CASPASE 8; GLUCOSE; MITOGEN ACTIVATED PROTEIN KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHRL1; TUMOR NECROSIS FACTOR RECEPTOR 1; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE 9; SUPEROXIDE DISMUTASE;

APOPTOSIS; CONGENITAL HEART MALFORMATION; DIABETES MELLITUS; DIABETIC EMBRYOPATHY; EMBRYOPATHY; GENE OVEREXPRESSION; GLUCOSE METABOLISM; HUMAN; HYPERGLYCEMIA; MATERNAL DIABETES MELLITUS; MOLECULAR DYNAMICS; NEURAL TUBE DEFECT; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; FEMALE; FETUS DISEASE; METABOLISM; PREGNANCY; PREGNANCY DIABETES MELLITUS;

APOPTOSIS; CASPASE 8; FEMALE; FETAL DISEASES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MAP KINASE KINASE KINASE 5; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; OXIDATIVE STRESS; PREGNANCY; PREGNANCY IN DIABETICS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84937973607     PISSN: 00029378     EISSN: 10976868     Source Type: Journal    
DOI: 10.1016/j.ajog.2015.01.016     Document Type: Review

References (124)

1. 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
2. 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
3. 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
4. F. Wang, E.A. Reece, and P. Yang Superoxide dismutase 1 overexpression in mice abolishes maternal diabetes-induced endoplasmic reticulum stress in diabetic embryopathy Am J Obstet Gynecol 209 2013 345.e1 345.e7
5. C. Xu, X. Li, F. Wang, H. Weng, and P. Yang Trehalose prevents neural tube defects by correcting maternal diabetes-suppressed autophagy and neurogenesis Am J Physiol Endocrinol Metab 305 2013 E667 E678
6. 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
7. P. Yang, X. Li, C. Xu, and et al. Maternal hyperglycemia activates an ASK1-FoxO3a-caspase 8 pathway that leads to embryonic neural tube defects Sci Signal 6 2013 ra74
8. 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
9. D.S. Feig, and V.A. Palda Type 2 diabetes in pregnancy: a growing concern Lancet 359 2002 1690 1692
10. Z.J. Hagay, Y. Weiss, I. Zusman, and 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 173 1995 1036 1041
11. 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
12. 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
13. 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
14. 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
15. E.E. Santo, P. Stroeken, P.V. Sluis, J. Koster, R. Versteeg, and E.M. Westerhout FOXO3a is a major target of inactivation by PI3K/AKT signaling in aggressive neuroblastoma Cancer Res 73 2013 2189 2198
16. F. Wang, Y. Wu, H. Gu, and et al. Ask1 gene deletion blocks maternal diabetes-induced endoplasmic reticulum stress in the developing embryo by disrupting the unfolded protein response signalosome Diabetes 2014 Sep 23 [Epub ahead of print]
17. H. Nishitoh, M. Saitoh, Y. Mochida, and et al. ASK1 is essential for JNK/SAPK activation by TRAF2 Mol Cell 2 1998 389 395
18. K. Tobiume, A. Matsuzawa, T. Takahashi, and et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis EMBO Rep 2 2001 222 228
19. E.A. Reece, Y.K. Wu, A. Wiznitzer, and et al. Dietary polyunsaturated fatty acid prevents malformations in offspring of diabetic rats Am J Obstet Gynecol 175 1996 818 823
20. H. Sakamaki, S. Akazawa, M. Ishibashi, and et al. Significance of glutathione-dependent antioxidant system in diabetes-induced embryonic malformations Diabetes 48 1999 1138 1144
21. R.A. Trocino, S. Akazawa, M. Ishibashi, and et al. Significance of glutathione depletion and oxidative stress in early embryogenesis in glucose-induced rat embryo culture Diabetes 44 1995 992 998
22. P.C. Jenkinson, D. Anderson, and S.D. Gangolli Malformations induced in cultured rat embryos by enzymically generated active oxygen species Teratog Carcinog Mutagen 6 1986 547 554
23. T.I. Chang, M. Horal, S.K. Jain, F. Wang, R. Patel, and M.R. Loeken Oxidant regulation of gene expression and neural tube development: insights gained from diabetic pregnancy on molecular causes of neural tube defects Diabetologia 46 2003 538 545
24. U.J. Eriksson, P. Wentzel, H.S. Minhas, and P.J. Thornalley Teratogenicity of 3-deoxyglucosone and diabetic embryopathy Diabetes 47 1998 1960 1966
25. P. Wentzel, N. Welsh, and U.J. Eriksson Developmental damage, increased lipid peroxidation, diminished cyclooxygenase-2 gene expression, and lowered prostaglandin E2 levels in rat embryos exposed to a diabetic environment Diabetes 48 1999 813 820
26. J.D. Morrow, K.E. Hill, R.F. Burk, T.M. Nammour, K.F. Badr, and L.J. Roberts 2nd A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism Proc Natl Acad Sci USA 87 1990 9383 9387
27. N.K. Gopaul, E.E. Anggard, A.I. Mallet, D.J. Betteridge, S.P. Wolff, and J. Nourooz-Zadeh Plasma 8-epi-PGF2 alpha levels are elevated in individuals with non-insulin dependent diabetes mellitus FEBS Lett 368 1995 225 229
28. T. Decsi, H. Minda, R. Hermann, and et al. Polyunsaturated fatty acids in plasma and erythrocyte membrane lipids of diabetic children Prostaglandins Leukot Essential Fatty Acids 67 2002 203 210
29. R. Li, M. Chase, S.K. Jung, P.J. Smith, and M.R. Loeken Hypoxic stress in diabetic pregnancy contributes to impaired embryo gene expression and defective development by inducing oxidative stress Am J Physiol Endocrinol Metab 289 2005 E591 E599
30. A. Ornoy, V. Zaken, and R. Kohen Role of reactive oxygen species (ROS) in the diabetes-induced anomalies in rat embryos in vitro: reduction in antioxidant enzymes and low-molecular-weight antioxidants (LMWA) may be the causative factor for increased anomalies Teratology 60 1999 376 386
31. V. Zaken, R. Kohen, and A. Ornoy Vitamins C and E improve rat embryonic antioxidant defense mechanism in diabetic culture medium Teratology 64 2001 33 44
32. J. Cederberg, and U.J. Eriksson Decreased catalase activity in malformation-prone embryos of diabetic rats Teratology 56 1997 350 357
33. S. Moncada, R.M. Palmer, and E.A. Higgs Nitric oxide: physiology, pathophysiology, and pharmacology Pharmacol Rev 43 1991 109 142
34. Q.P. Lee, and M.R. Juchau Dysmorphogenic effects of nitric oxide (NO) and NO-synthase inhibition: studies with intra-amniotic injections of sodium nitroprusside and NG-monomethyl-L-arginine Teratology 49 1994 452 464
35. N. Plachta, A. Traister, and M. Weil Nitric oxide is involved in establishing the balance between cell cycle progression and cell death in the developing neural tube Exp Cell Res 288 2003 354 362
36. Q. Feng, W. Song, X. Lu, and et al. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase Circulation 106 2002 873 879
37. I. Topel, A. Stanarius, and G. Wolf Distribution of the endothelial constitutive nitric oxide synthase in the developing rat brain: an immunohistochemical study Brain Res 788 1998 43 48
38. A. Jawerbaum, E.T. Gonzalez, V. Novaro, A. Faletti, D. Sinner, and M.A. Gimeno Increased prostaglandin E generation and enhanced nitric oxide synthase activity in the non-insulin-dependent diabetic embryo during organogenesis Reprod Fertil Dev 10 1998 191 196
39. A. Jawerbaum, D. Sinner, V. White, and et al. Modulation of PGE2 generation in the diabetic embryo: effect of nitric oxide and superoxide dismutase Prostaglandins Leukot Essential Fatty Acids 64 2001 127 133
40. A. Jawerbaum, R. Higa, V. White, and et al. Peroxynitrites and impaired modulation of nitric oxide concentrations in embryos from diabetic rats during early organogenesis Reproduction (Cambridge, England) 130 2005 695 703
41. A. Jawerbaum, and E. Gonzalez The role of alterations in arachidonic acid metabolism and nitric oxide homeostasis in rat models of diabetes during early pregnancy Curr Pharmaceut Des 11 2005 1327 1342
42. C. Szabo Multiple pathways of peroxynitrite cytotoxicity Toxicol Lett 140-141 2003 105 112
43. H.M. Shen, and Z.G. Liu JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species Free Radic Biol Med 40 2006 928 939
44. E.C. Dempsey, A.C. Newton, D. Mochly-Rosen, and et al. Protein kinase C isozymes and the regulation of diverse cell responses Am J Physiol 279 2000 L429 L438
45. M.M. Wright, and C.R. McMaster Phospholipid synthesis, diacylglycerol compartmentation, and apoptosis Biol Res 35 2002 223 229
46. Y. Hiramatsu, N. Sekiguchi, M. Hayashi, and et al. Diacylglycerol production and protein kinase C activity are increased in a mouse model of diabetic embryopathy Diabetes 51 2002 2804 2810
47. Z. Zhiyong, Y.K. Wu, and E.A. Reece Demonstration of the essential role of protein kinase C isoforms in hyperglycemia-induced embryonic malformations Reprod Sci (Thousand Oaks, CA) 15 2008 349 356
48. E.A. Reece, X.D. Ma, Y.K. Wu, and D. Dhanasekaran Aberrant patterns of cellular communication in diabetes-induced embryopathy. I. Membrane signalling J Matern Fetal Neonatal Med 11 2002 249 253
49. E.A. Reece, X.D. Ma, Z. Zhao, Y.K. Wu, and D. Dhanasekaran Aberrant patterns of cellular communication in diabetes-induced embryopathy in rats: II, apoptotic pathways Am J Obstet Gynecol 192 2005 967 972
50. M. Saitoh, H. Nishitoh, M. Fujii, and et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1 EMBO J 17 1998 2596 2606
51. U. Ozcan, Q. Cao, E. Yilmaz, and et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461
52. M. Horal, Z. Zhang, R. Stanton, A. Virkamaki, and M.R. Loeken Activation of the hexosamine pathway causes oxidative stress and abnormal embryo gene expression: involvement in diabetic teratogenesis Birth Defects Res 70 2004 519 527
53. H. Forsberg, U.J. Eriksson, and N. Welsh Apoptosis in embryos of diabetic rats Pharmacol Toxicol 83 1998 104 111
54. S.A. Phelan, M. Ito, and M.R. Loeken Neural tube defects in embryos of diabetic mice: role of the Pax-3 gene and apoptosis Diabetes 46 1997 1189 1197
55. F. Sun, E. Kawasaki, S. Akazawa, and et al. Apoptosis and its pathway in early post-implantation embryos of diabetic rats Diabetes Res Clin Pract 67 2005 110 118
56. K.H. Moley Hyperglycemia and apoptosis: mechanisms for congenital malformations and pregnancy loss in diabetic women Trends Endocrinol Metab 12 2001 78 82
57. U.J. Eriksson, L.A. Borg, J. Cederberg, and et al. Pathogenesis of diabetes-induced congenital malformations Upsala J Med Sci 105 2000 53 84
58. E.L. Fine, M. Horal, T.I. Chang, G. Fortin, and M.R. Loeken Evidence that elevated glucose causes altered gene expression, apoptosis, and neural tube defects in a mouse model of diabetic pregnancy Diabetes 48 1999 2454 2462
59. B.P. Kang, S. Frencher, V. Reddy, A. Kessler, A. Malhotra, and L.G. Meggs High glucose promotes mesangial cell apoptosis by oxidant-dependent mechanism Am J Physiol Renal Physiol 284 2003 F455 F466
60. S. Ueda, H. Masutani, H. Nakamura, T. Tanaka, M. Ueno, and J. Yodoi Redox control of cell death Antioxid Redox Signal 4 2002 405 414
61. S.V. Kyosseva Mitogen-activated protein kinase signaling Int Rev Neurobiol 59 2004 201 220
62. M. Torres, and H.J. Forman Redox signaling and the MAP kinase pathways BioFactors (Oxford, England) 17 2003 287 296
63. C. Widmann, S. Gibson, M.B. Jarpe, and G.L. Johnson Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human Physiol Rev 79 1999 143 180
64. J.M. Kyriakis, and J. Avruch Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation Physiol Rev 81 2001 807 869
65. K. Tobiume, M. Saitoh, and H. Ichijo Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer J Cell Physiol 191 2002 95 104
66. R.J. Davis Signal transduction by the JNK group of MAP kinases Cell 103 2000 239 252
67. Q. Zhang, G. Zhang, F. Meng, and H. Tian Biphasic activation of apoptosis signal-regulating kinase 1-stress-activated protein kinase 1-c-Jun N-terminal protein kinase pathway is selectively mediated by Ca2+-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors involving oxidative stress following brain ischemia in rat hippocampus Neurosci Lett 337 2003 51 55
68. T. Watanabe, K. Otsu, T. Takeda, and et al. Apoptosis signal-regulating kinase 1 is involved not only in apoptosis but also in non-apoptotic cardiomyocyte death Biochem Biophys Res Commun 333 2005 562 567
69. H. Kadowaki, H. Nishitoh, F. Urano, and et al. Amyloid beta induces neuronal cell death through ROS-mediated ASK1 activation Cell Death Different 12 2005 19 24
70. T. Yokoi, K. Fukuo, O. Yasuda, and et al. Apoptosis signal-regulating kinase 1 mediates cellular senescence induced by high glucose in endothelial cells Diabetes 55 2006 1660 1665
71. T. Wada, and J.M. Penninger Mitogen-activated protein kinases in apoptosis regulation Oncogene 23 2004 2838 2849
72. A. Lin, and B. Dibling The true face of JNK activation in apoptosis Aging Cell 1 2002 112 116
73. M.C. Wang, D. Bohmann, and H. Jasper JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling Cell 121 2005 115 125
74. M.A. Essers, S. Weijzen, A.M. de Vries-Smits, and et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK EMBO J 23 2004 4802 4812
75. A. Lin Activation of the JNK signaling pathway: breaking the brake on apoptosis Bioessays 25 2003 17 24
76. M. Torres Mitogen-activated protein kinase pathways in redox signaling Front Biosci 8 2003 d369 d391
77. N. Sata, H. Klonowski-Stumpe, B. Han, D. Haussinger, and C. Niederau Menadione induces both necrosis and apoptosis in rat pancreatic acinar AR4-2J cells Free Radic Biol Med 23 1997 844 850
78. M. Ding, J. Li, S.S. Leonard, and et al. Differential role of hydrogen peroxide in UV-induced signal transduction Mol Cell Biochem 234-235 2002 81 90
79. W.H. Chan, C.C. Wu, and J.S. Yu Curcumin inhibits UV irradiation-induced oxidative stress and apoptotic biochemical changes in human epidermoid carcinoma A431 cells J Cell Biochem 90 2003 327 338
80. S.A. Lee, A. Dritschilo, and M. Jung Role of ATM in oxidative stress-mediated c-Jun phosphorylation in response to ionizing radiation and CdCl2 J Biol Chem 276 2001 11783 11790
81. Y. Li, Y. Arita, H.C. Koo, J.M. Davis, and J.A. Kazzaz Inhibition of c-Jun N-terminal kinase pathway improves cell viability in response to oxidant injury Am J Resp Cell Mol Biol 29 2003 779 783
82. Y.S. Kim, D.Y. Jhon, and K.Y. Lee Involvement of ROS and JNK1 in selenite-induced apoptosis in Chang liver cells Exp Mol Med 36 2004 157 164
83. S.O. Yoon, S.J. Park, S.Y. Yoon, C.H. Yun, and A.S. Chung Sustained production of H(2)O(2) activates pro-matrix metalloproteinase-2 through receptor tyrosine kinases/phosphatidylinositol 3-kinase/NF-kappa B pathway J Biol Chem 277 2002 30271 30282
84. M. Yoshizumi, T. Kogame, Y. Suzaki, and et al. Ebselen attenuates oxidative stress-induced apoptosis via the inhibition of the c-Jun N-terminal kinase and activator protein-1 signalling pathway in PC12 cells Br J Pharmacol 136 2002 1023 1032
85. C. Dong, D.D. Yang, C. Tournier, and et al. JNK is required for effector T-cell function but not for T-cell activation Nature 405 2000 91 94
86. Q.B. She, N. Chen, A.M. Bode, R.A. Flavell, and Z. Dong Deficiency of c-Jun-NH(2)-terminal kinase-1 in mice enhances skin tumor development by 12-O-tetradecanoylphorbol-13-acetate Cancer Res 62 2002 1343 1348
87. C.Y. Kuan, D.D. Yang, D.R. Samanta Roy, R.J. Davis, P. Rakic, and R.A. Flavell The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development Neuron 22 1999 667 676
88. F. Urano, X. Wang, A. Bertolotti, and et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666
89. A.K. Srivastava High glucose-induced activation of protein kinase signaling pathways in vascular smooth muscle cells: a potential role in the pathogenesis of vascular dysfunction in diabetes (review) Int J Mol Med 9 2002 85 89
90. R. Kikkawa, D. Koya, and M. Haneda Progression of diabetic nephropathy Am J Kidney Dis 41 2003 S19 S21
91. C.P. Bagowski, W. Xiong, and J.E. Ferrell Jr. c-Jun N-terminal kinase activation in Xenopus laevis eggs and embryos. A possible non-genomic role for the JNK signaling pathway J Biol Chem 276 2001 1459 1465
92. M.J. Anderson, C.S. Viars, S. Czekay, W.K. Cavenee, and K.C. Arden Cloning and characterization of three human forkhead genes that comprise an FKHR-like gene subfamily Genomics 47 1998 187 199
93. T. Kajihara, M. Jones, L. Fusi, and et al. Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization Mol Endocrinol (Baltimore, MD) 20 2006 2444 2455
94. H. Tran, A. Brunet, J.M. Grenier, and et al. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein Science 296 2002 530 534
95. S. Rokudai, N. Fujita, O. Kitahara, Y. Nakamura, and T. Tsuruo Involvement of FKHR-dependent TRADD expression in chemotherapeutic drug-induced apoptosis Mol Cell Biol 22 2002 8695 8708
96. Z.Z. Chong, F. Li, and K. Maiese Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease Prog Neurobiol 75 2005 207 246
97. T. Finkel Redox-dependent signal transduction FEBS Letters 476 2000 52 54
98. A. Brunet, L.B. Sweeney, J.F. Sturgill, and et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase Science 303 2004 2011 2015
99. G.J. Kops, T.B. Dansen, P.E. Polderman, and et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress Nature 419 2002 316 321
100. J. Gilley, P.J. Coffer, and J. Ham FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons J Cell Biol 162 2003 613 622
101. V. Modur, R. Nagarajan, B.M. Evers, and J. Milbrandt FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer J Biol Chem 277 2002 47928 47937
102. T. Suhara, H.S. Kim, L.A. Kirshenbaum, and K. Walsh Suppression of Akt signaling induces Fas ligand expression: involvement of caspase and Jun kinase activation in Akt-mediated Fas ligand regulation Mol Cell Biol 22 2002 680 691
103. E.W. Lam, R.E. Francis, and M. Petkovic FOXO transcription factors: key regulators of cell fate Biochem Soc Trans 34 2006 722 726
104. A. Brunet, A. Bonni, M.J. Zigmond, and et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 96 1999 857 868
105. J. Sunayama, F. Tsuruta, N. Masuyama, and Y. Gotoh JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3 J Cell Biol 170 2005 295 304
106. E.L. Greer, and A. Brunet FOXO transcription factors at the interface between longevity and tumor suppression Oncogene 24 2005 7410 7425
107. S. Shukla, N. Bhaskaran, G.T. Maclennan, and S. Gupta Deregulation of FoxO3a accelerates prostate cancer progression in TRAMP mice Prostate 73 2013 1507 1517
108. M.R. Abid, K. Yano, S. Guo, and et al. Forkhead transcription factors inhibit vascular smooth muscle cell proliferation and neointimal hyperplasia J Biol Chem 280 2005 29864 29873
109. Y. Wang, Y. Zhou, and D.T. Graves FOXO transcription factors: their clinical significance and regulation BioMed Res Int 2014 2014 925350
110. B.J. Willcox, T.A. Donlon, Q. He, and et al. FOXO3A genotype is strongly associated with human longevity Proc Natl Acad Sci USA 105 2008 13987 13992
111. H. Hsu, J. Xiong, and D.V. Goeddel The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation Cell 81 1995 495 504
112. H. Hsu, H.B. Shu, M.G. Pan, and D.V. Goeddel TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways Cell 84 1996 299 308
113. A.M. Chinnaiyan, C.G. Tepper, M.F. Seldin, and et al. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis J Biol Chem 271 1996 4961 4965
114. M.P. Boldin, E.E. Varfolomeev, Z. Pancer, I.L. Mett, J.H. Camonis, and D. Wallach A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain J Biol Chem 270 1995 7795 7798
115. G.L. Yount, G. Afshar, S. Ries, and et al. Transcriptional activation of TRADD mediates p53-independent radiation-induced apoptosis of glioma cells Oncogene 20 2001 2826 2835
116. G.L.A. Beckles, and P.E. Thompson-Reid Diabetes & women's health across the life stages: a public health perspective 2001 US Dept. of Health and Human Services, Centers for Disease Control and Prevention Silver Spring, MD
117. 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
118. X. Zhou, G.Y. Zhang, J. Wang, S.L. Lu, J. Cao, and L.Z. Sun A novel bridge between oxidative stress and immunity: the interaction between hydrogen peroxide and human leukocyte antigen G in placental trophoblasts during preeclampsia Am J Obstet Gynecol 206 2012 447.e7 447.e16
119. R.O. Bahado-Singh, R. Akolekar, A. Chelliah, and et al. Metabolomic analysis for first-trimester trisomy 18 detection Am J Obstet Gynecol 209 2013 65.e1 65.e9
120. R.O. Bahado-Singh, R. Akolekar, R. Mandal, and et al. Metabolomic analysis for first-trimester Down syndrome prediction Am J Obstet Gynecol 208 2013 371.e1 371.e8
121. R.O. Bahado-Singh, R. Ertl, R. Mandal, and et al. Metabolomic prediction of fetal congenital heart defect in the first trimester Am J Obstet Gynecol 211 2014 240.e1 240.e14
122. S.E. Parker, M.M. Yazdy, S.C. Tinker, A.A. Mitchell, and M.M. Werler The impact of folic acid intake on the association among diabetes mellitus, obesity, and spina bifida Am J Obstet Gynecol 209 2013 239.e1 239.e8
123. A. Correa, S.M. Gilboa, L.D. Botto, and et al. 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
124. G.P. Oakley Jr. Failing to prevent birth defects caused by maternal diabetes mellitus Am J Obstet Gynecol 206 2012 179 180