C-Jun NH2-terminal kinase 1/2 and endoplasmic reticulum stress as interdependent and reciprocal causation in diabetic embryopathy

Diabetes

Volumn 62, Issue 2, 2013, Pages 599-608

  Li, Xuezheng ^a,b   Xu, Cheng ^a   Yang, Peixin ^a  

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

^b YANBIAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; BIOLOGICAL MARKER; CASPASE 3; CASPASE 8; CHAPERONE; GLUCOSE; MITOGEN ACTIVATED PROTEIN KINASE 9; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX1; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; CASP3 PROTEIN, MOUSE; CASP8 PROTEIN, MOUSE; SOX1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC EMBRYOPATHY; EMBRYO; EMBRYO CULTURE; EMBRYOPATHY; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; HYPERGLYCEMIA; MOUSE; NEURAL STEM CELL; NEURAL TUBE DEFECT; NEUROEPITHELIUM; NEURULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; FETUS DISEASE; GENE DELETION; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PREGNANCY; PREGNANCY DIABETES MELLITUS;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CASPASE 3; CASPASE 8; DIABETES MELLITUS, EXPERIMENTAL; ENDOPLASMIC RETICULUM STRESS; FEMALE; FETAL DISEASES; GENE DELETION; HYPERGLYCEMIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; MOLECULAR CHAPERONES; NEURAL TUBE DEFECTS; NEUROEPITHELIAL CELLS; NEURULATION; PHENYLBUTYRATES; PREGNANCY; PREGNANCY IN DIABETICS; SOXB1 TRANSCRIPTION FACTORS;

MLCS; MLOWN;

EID: 84873043548     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-0026     Document Type: Article

References (44)

1. Becerra JE, Khoury MJ, Cordero JF, Erickson JD. Diabetes mellitus during pregnancy and the risks for specific birth defects: a population-based case-control study. Pediatrics 1990;85:1-9
2. Correa A, Gilboa SM, Besser LM, et al. Diabetes mellitus and birth defects. Am J Obstet Gynecol 2008;199:237.e1-9
3. Yang X, Borg LA, Eriksson UJ. Altered metabolism and superoxide generation in neural tissue of rat embryos exposed to high glucose. Am J Physiol 1997;272:E173-E180
4. Phelan SA, Ito M, Loeken MR. Neural tube defects in embryos of diabetic mice: role of the Pax-3 gene and apoptosis. Diabetes 1997;46:1189-1197
5. Gäreskog M, Cederberg J, Eriksson UJ, Wentzel P. Maternal diabetes in vivo and high glucose concentration in vitro increases apoptosis in rat embryos. Reprod Toxicol 2007;23:63-74
6. Yang P, Zhao Z, Reece EA. Activation of oxidative stress signaling that is implicated in apoptosis with a mouse model of diabetic embryopathy. Am J Obstet Gynecol 2008;198:130.e1-7
7. Salbaum JM, Kappen C. Neural tube defect genes and maternal diabetes during pregnancy. Birth Defects Res A Clin Mol Teratol 2010;88:601-611
8. Pavlinkova G, Salbaum JM, Kappen C. Maternal diabetes alters tran-scriptional programs in the developing embryo. BMC Genomics 2009;10: 274
9. Wentzel P, Gäreskog M, Eriksson UJ. Decreased cardiac glutathione per-oxidase levels and enhanced mandibular apoptosis in malformed embryos of diabetic rats. Diabetes 2008;57:3344-3352
10. Yang X, Borg LA, Eriksson UJ. Altered mitochondrial morphology of rat embryos in diabetic pregnancy. Anat Rec 1995;241:255-267
11. 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;32:363-373
12. Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006;7:880-885
13. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529
14. Ron D, Hubbard SR. How IRE1 reacts to ER stress. Cell 2008;132:24-26
15. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999;397:271-274
16. Lee K, Tirasophon W, Shen X, et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 2002;16:452-466
17. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998;12:982-995
18. Reece EA, Ma XD, Zhao Z, Wu YK, Dhanasekaran D. Aberrant patterns of cellular communication in diabetes-induced embryopathy in rats: II, apo-ptotic pathways. Am J Obstet Gynecol 2005;192:967-972
19. Forsberg H, Eriksson UJ, Welsh N. Apoptosis in embryos of diabetic rats. Pharmacol Toxicol 1998;83:104-111
20. Sun F, Kawasaki E, Akazawa S, et al. Apoptosis and its pathway in early post-implantation embryos of diabetic rats. Diabetes Res Clin Pract 2005; 67:110-118
21. Yang P, Zhao Z, Reece EA. Involvement of c-Jun N-terminal kinases activation in diabetic embryopathy. Biochem Biophys Res Commun 2007;357: 749-754
22. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000;287:664-666
23. Hagay ZJ, Weiss Y, Zusman I, 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
24. Yang P, Reece EA. Role of HIF-1alpha in maternal hyperglycemia-induced embryonic vasculopathy. Am J Obstet Gynecol 2011;204:332.e1-7
25. Eriksson UJ, Dahlström E, Hellerström C. Diabetes in pregnancy. Skeletal malformations in the offspring of diabetic rats after intermittent withdrawal of insulin in early gestation. Diabetes 1983;32:1141-1145
26. Sugimura Y, Murase T, Oyama K, et al. Prevention of neural tube defects by loss of function of inducible nitric oxide synthase in fetuses of a mouse model of streptozotocin-induced diabetes. Diabetologia 2009;52:962-971
27. Kamimoto Y, Sugiyama T, Kihira T, et al. Transgenic mice overproducing human thioredoxin-1, an antioxidative and anti-apoptotic protein, prevents diabetic embryopathy. Diabetologia 2010;53:2046-2055
28. Massa V, Savery D, Ybot-Gonzalez P, et al. Apoptosis is not required for mammalian neural tube closure. Proc Natl Acad Sci USA 2009;106:8233-8238
29. Reece EA, Ji I, Wu YK, Zhao Z. Characterization of differential gene expression profiles in diabetic embryopathy using DNA microarray analysis. Am J Obstet Gynecol 2006;195:1075-1080
30. Reece EA, Wu YK. Prevention of diabetic embryopathy in offspring of diabetic rats with use of a cocktail of deficient substrates and an antiox-idant. Am J Obstet Gynecol 1997;176:790-797; discussion 797-798
31. Yang P, Zhao Z, Reece EA. Blockade of c-Jun N-terminal kinase activation abrogates hyperglycemia-induced yolk sac vasculopathy in vitro. Am J Obstet Gynecol 2008;198:321.e1-7
32. Yang P, Li H. Epigallocatechin-3-gallate ameliorates hyperglycemia- induced embryonic vasculopathy and malformation by inhibition of Foxo3a activation. Am J Obstet Gynecol 2010;203:75.e1-6
33. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006;313:1137-1140
34. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by en-doplasmic reticulum stress. Nat Cell Biol 2011;13:184-190
35. Kim HR, Lee GH, Cho EY, Chae SW, Ahn T, Chae HJ. Bax inhibitor 1 regulates ER-stress-induced ROS accumulation through the regulation of cytochrome P450 2E1. J Cell Sci 2009;122:1126-1133
36. Naderi J, Hung M, Pandey S. Oxidative stress-induced apoptosis in dividing fibroblasts involves activation of p38 MAP kinase and over-expression of Bax: resistance of quiescent cells to oxidative stress. Apoptosis 2003;8:91-100
37. Pugazhenthi S, Nesterova A, Jambal P, et al. Oxidative stress-mediated down-regulation of bcl-2 promoter in hippocampal neurons. J Neurochem 2003;84:982-996
38. Gäreskog M, Eriksson UJ, Wentzel P. Combined supplementation of folic acid and vitamin E diminishes diabetes-induced embryotoxicity in rats. Birth Defects Res A Clin Mol Teratol 2006;76:483-490
39. Ventura JJ, Cogswell P, Flavell RA, Baldwin AS Jr, Davis RJ. JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev 2004;18:2905-2915
40. Cowan KJ, Diamond MI, Welch WJ. Polyglutamine protein aggregation and toxicity are linked to the cellular stress response. Hum Mol Genet 2003;12: 1377-1391
41. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 2003;115:61-70
42. Ni HM, Baty CJ, Li N, et al. Bid agonist regulates murine hepatocyte proliferation by controlling endoplasmic reticulum calcium homeostasis. Hepatology 2010;52:338-348
43. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 1999;22:667-676
44. Li X, Weng H, Xu C, Reece EA, Yang P. Oxidative stress-induced JNK1/2 activation triggers pro-apoptotic signaling and apoptosis that leads to diabetic embryopathy. Diabetes 2012;61:2084-2092