Cellular stress, excessive apoptosis, and the effect of metformin in a mouse model of type 2 diabetic embryopathy

Diabetes

Volumn 64, Issue 7, 2015, Pages 2526-2536

  Wu, Yanqing ^a   Fang, Wang ^a   Fu, Mao ^a   Cheng, Wang ^b   Quon, Michael J ^a   Yang, Peixin ^a  

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

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA IRE1 PROTEIN; CALNEXIN; CASPASE 3; CASPASE 8; FATTY ACID; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INSULIN; MESSENGER RNA; METFORMIN; PERK PROTEIN; PROTEIN; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE 1A; PROTEIN IRE1; UNCLASSIFIED DRUG; CASPASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL STRESS; CONTROLLED STUDY; DIET INDUCED OBESITY; DRUG EFFECT; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FATTY ACID BLOOD LEVEL; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; LIPID PEROXIDATION; MALE; MATERNAL DIABETES MELLITUS; MOUSE; NEURAL TUBE DEFECT; NEUROEPITHELIUM CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE INSULIN SENSITIVITY CHECK INDEX; TREATMENT OUTCOME; TREATMENT RESPONSE; UPREGULATION; WEIGHT GAIN; ANIMAL; C57BL MOUSE; COMPLICATION; DIABETES MELLITUS, TYPE 2; DISEASE MODEL; METABOLISM; NEURAL TUBE DEFECTS; PHYSIOLOGICAL STRESS; PREGNANCY; PREGNANCY DIABETES MELLITUS;

ANIMALS; APOPTOSIS; CASPASES; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; FEMALE; MALE; METFORMIN; MICE; MICE, INBRED C57BL; NEURAL TUBE DEFECTS; OXIDATIVE STRESS; PREGNANCY; PREGNANCY IN DIABETICS; STRESS, PHYSIOLOGICAL;

EID: 84940874434     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1683     Document Type: Article

References (47)

1. International Diabetes Federation. Diabetes in pregnancy: Protecting maternal health [article online]. Available from http://www.idf.org/sites/default/files/Policy-Briefing-DiabetesInPregancy.pdf. Accessed 9 June 2014
2. Lawrence JM, Contreras R, Chen W, Sacks DA. Trends in the prevalence of preexisting diabetes and gestational diabetes mellitus among a racially/ethnically diverse population of pregnant women, 1999-2005. Diabetes Care 2008;31:899-904
3. Becerra JE, Khoury MJ, Cordero JF, Erickson JD. Diabetes mellitus during pregnancy and the risks for specific birth defects: A population-based casecontrol study. Pediatrics 1990;85:1-9
4. Ramos-Arroyo MA, Rodriguez-Pinilla E, Cordero JF. Maternal diabetes: The risk for specific birth defects. Eur J Epidemiol 1992;8:503-508
5. Correa A, Gilboa SM, Besser LM, et al. Diabetes mellitus and birth defects. Am J Obstet Gynecol 2008;199:237.e1-237.e9
6. Loffredo CA, Wilson PD, Ferencz C. Maternal diabetes: An independent risk factor for major cardiovascular malformations with increased mortality of affected infants. Teratology 2001;64:98-106
7. Reece EA, Wu YK. Prevention of diabetic embryopathy in offspring of diabetic rats with use of a cocktail of deficient substrates and an antioxidant. Am J Obstet Gynecol 1997;176:790-797; discussion 797-798
8. 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.e1-130.e7
9. Yang P, Li X, Xu C, et al. Maternal hyperglycemia activates an ASK1-FoxO3a-caspase 8 pathway that leads to embryonic neural tube defects. Sci Signal 2013;6:ra74
10. 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;205:84. e1-84.e6
11. Li X, Weng H, Xu C, Reece EA, Yang P. Oxidative stress-induced JNK1/2 activation triggers proapoptotic signaling and apoptosis that leads to diabetic embryopathy. Diabetes 2012;61:2084-2092
12. 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;62:599-608
13. 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;209:345.e1-345.e7
14. 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 2014;64:973-988
15. Wentzel P, Gäreskog M, Eriksson UJ. Decreased cardiac glutathione peroxidase levels and enhanced mandibular apoptosis in malformed embryos of diabetic rats. Diabetes 2008;57:3344-3352
16. 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
17. 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
18. Sakamaki H, Akazawa S, Ishibashi M, et al. Significance of glutathionedependent antioxidant system in diabetes-induced embryonic malformations. Diabetes 1999;48:1138-1144
19. 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.e1-75.e6
20. Yang P, Cao Y, Li H. Hyperglycemia induces inducible nitric oxide synthase gene expression and consequent nitrosative stress via c-Jun N-terminal kinase activation. Am J Obstet Gynecol 2010;203:185.e5-185.e11
21. 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:E667-E678
22. Salbaum JM, Kappen C. Neural tube defect genes and maternal diabetes during pregnancy. Birth Defects Res A Clin Mol Teratol 2010;88:601-611
23. Salbaum JM, Kruger C, Zhang X, et al. Altered gene expression and spongiotrophoblast differentiation in placenta from a mouse model of diabetes in pregnancy. Diabetologia 2011;54:1909-1920
24. Greene MF, Hare JW, Cloherty JP, Benacerraf BR, Soeldner JS. Firsttrimester hemoglobin A1 and risk for major malformation and spontaneous abortion in diabetic pregnancy. Teratology 1989;39:225-231
25. Miller E, Hare JW, Cloherty JP, et al. Elevated maternal hemoglobin A1c in early pregnancy and major congenital anomalies in infants of diabetic mothers. N Engl J Med 1981;304:1331-1334
26. Winzell MS, Ahrén B. The high-fat diet-fed mouse: A model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 2004;53(Suppl. 3):S215-S219
27. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 1988;37:1163-1167
28. Smyth JW, Hong TT, Gao D, et al. Limited forward trafficking of connexin 43 reduces cell-cell coupling in stressed human and mouse myocardium. J Clin Invest 2010;120:266-279
29. Yang P, Reece EA. Role of HIF-1a in maternal hyperglycemia-induced embryonic vasculopathy. Am J Obstet Gynecol 2011;204:332.e1-332.e7
30. 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.e1-321.e7
31. Rattan R, Graham RP, Maguire JL, Giri S, Shridhar V. Metformin suppresses ovarian cancer growth and metastasis with enhancement of cisplatin cytotoxicity in vivo. Neoplasia 2011;13:483-491
32. Hou M, Venier N, Sugar L, et al. Protective effect of metformin in CD1 mice placed on a high carbohydrate-high fat diet. Biochem Biophys Res Commun 2010;397:537-542
33. Mao-Ying QL, Kavelaars A, Krukowski K, et al. The anti-diabetic drug metformin protects against chemotherapy-induced peripheral neuropathy in a mouse model. PLoS One 2014;9:e100701
34. Hundal RS, Krssak M, Dufour S, et al. Mechanism by which metformin reduces glucose production in type 2 diabetes. Diabetes 2000;49:2063-2069
35. Lee HY, Wei D, Loeken MR. Lack of metformin effect on mouse embryo AMPK activity: Implications for metformin treatment during pregnancy. Diabetes Metab Res Rev 2014;30:23-30
36. Reece EA, Wiznitzer A, Homko CJ, Hagay Z, Wu YK. Synchronization of the factors critical for diabetic teratogenesis: An in vitro model. Am J Obstet Gynecol 1996;174:1284-1288
37. Adam PA, Teramo K, Raiha N, Gitlin D, Schwartz R. Human fetal insulin metabolism early in gestation. Response to acute elevation of the fetal glucose concentration and placental transfer of human insulin-I-131. Diabetes 1969;18: 409-416
38. Prasadan K, Daume E, Preuett B, et al. Glucagon is required for early insulin-positive differentiation in the developing mouse pancreas. Diabetes 2002; 51:3229-3236
39. 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. 13 January 2015 [Epub ahead of print]
40. Wang F, Reece EA, Yang P. Oxidative stress is responsible for maternal diabetes-impaired transforming growth factor beta signaling in the developing mouse heart. Am J Obstet Gynecol 2015;212:650.e1-650.e11
41. Wu Y, Wang F, Reece EA, Yang P. Curcumin ameliorates high glucoseinduced neural tube defects by suppressing cellular stress and apoptosis. Am J Obstet Gynecol. 13 January 2015 [Epub ahead of print]
42. Yang P, Reece EA, Wang F, Gabbay-Benziv R. Decoding the oxidative stress hypothesis in diabetic embryopathy through proapoptotic kinase signaling. Am J Obstet Gynecol 2015;212:569-579
43. 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;144:186-196
44. Pani L, Horal M, Loeken MR. Polymorphic susceptibility to the molecular causes of neural tube defects during diabetic embryopathy. Diabetes 2002;51: 2871-2874
45. Machado AF, Zimmerman EF, Hovland DN Jr, Weiss R, Collins MD. Diabetic embryopathy in C57BL/6J mice. Altered fetal sex ratio and impact of the splotch allele. Diabetes 2001;50:1193-1199
46. 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
47. 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