Influence of maternal metabolism and parental genetics on fetal maldevelopment in diabetic rat pregnancy

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 10, 2012, Pages

  Ejdesjo A ^a   Wentzel, P ^a   Eriksson, U J ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Diabetes; Gene expression; Malformations; Teratogenic

Indexed keywords

3 HYDROXYBUTYRIC ACID; ALDEHYDE REDUCTASE; AMINO ACID; ASPARAGINE; BONE MORPHOGENETIC PROTEIN 4; CITRULLINE; COMPLEMENTARY DNA; COPPER ZINC SUPEROXIDE DISMUTASE; CYSTINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTAMIC ACID; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE PEROXIDASE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LEUCINE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SONIC HEDGEHOG PROTEIN; TAURINE; TRYPTOPHAN; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLEFT LIP; CLEFT PALATE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EPIGENETICS; FEMALE; FETUS; FETUS DEVELOPMENT; FETUS MALFORMATION; GENE EXPRESSION; GENOTYPE; GLUCOSE BLOOD LEVEL; INBRED STRAIN; MALE; METABOLISM; MICROGNATHIA; NEURAL TUBE DEFECT; NONHUMAN; ONCOGENE RET; PREGNANCY; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; PROTO ONCOGENE; RAT; REAL TIME POLYMERASE CHAIN REACTION; TERATOGENICITY;

ALDEHYDE REDUCTASE; AMINO ACIDS; ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DINOPROST; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEART DEFECTS, CONGENITAL; LIPIDS; MALE; MANDIBLE; PREGNANCY; PREGNANCY IN DIABETICS; RATS; RATS, INBRED WF; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84861131933     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00661.2011     Document Type: Article

References (80)

1. Aberg A, Westbom L, Kallen B. Congenital malformations among infants whose mothers had gestational diabetes or preexisting diabetes. Early Hum Dev 61: 85-95, 2001.
2. Aerts L, Van Assche FA. Low taurine, gamma-aminobutyric acid and carnosine levels in plasma of diabetic pregnant rats: consequences for the offspring. J Perinat Med 29: 81-84, 2001.
3. Bergmeyer H. Methods of Enzymatic Analysis, Weinheim, Germany: Verlag Chemie, 1983.
4. Bergstrom RM, Erila T, Pirskanen R. Teratogenic effects of the amino acid leucine in the chicken. Experientia 23: 767-768, 1967.
5. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
6. Buchanan TA, Denno KM, Sipos GF, Sadler Diabetic teratogenesis TW. In vitro evidence for a multifactorial etiology with little contribution from glucose per se. Diabetes 43: 656-660, 1994.
7. Carmichael SL, Shaw GM, Yang W, Abrams B, Lammer EJ. Maternal stressful life events and risks of birth defects. Epidemiology 18: 356-361, 2007.
8. Casson IF, Clarke CA, Howard CV, McKendrick O, Pennycook S, Pharoah PO, Platt MJ, Stanisstreet M, van Velszen D, Walkinshaw S. Outcomes of pregnancy in insulin dependent diabetic women: results of a five year population cohort study. Br Med J 315: 275-278, 1997.
9. Cederberg J, Eriksson UJ. Decreased catalase activity in malformationprone embryos of diabetic rats. Teratology 56: 350-357, 1997.
10. Cederberg J, Galli J, Luthman H, Eriksson UJ. Increased mRNA levels of Mn-SOD and catalase in embryos of diabetic rats from a malformationresistant strain. Diabetes 49: 101-107, 2000.
11. Cedergren M, Kallen B. Maternal obesity and the risk for orofacial clefts in the offspring. Cleft Palate Craniofac J 42: 367-371, 2005.
12. Chatzistavrou E, Ross RB, Tompson BD, Johnston MC. Predisposing factors to formation of cleft lip and palate: inherited craniofacial skeletal morphology. Cleft Palate Craniofac J 41: 613-621, 2004.
13. Cherif H, Reusens B, Ahn MT, Hoet JJ, Remacle C. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol 159: 341-348, 1998.
14. Coughlan MT, Thorburn DR, Penfold SA, Laskowski A, Harcourt BE, Sourris KC, Tan AL, Fukami K, Thallas-Bonke V, Nawroth PP, Brownlee M, Bierhaus A, Cooper ME, Forbes JM. RAGE-induced cytosolic ROS promote mitochondrial superoxide generation in diabetes. J Am Soc Nephrol 20: 742-752, 2009.
15. Dixon MJ, Marazita ML, Beaty TH, Murray JC. Cleft lip and palate: understanding genetic and environmental influences. Nat Rev Genet 12: 167-178, 2000.
16. Du X, Matsumura T, Edelstein D, Rossetti L, Zsengeller Z, Szabo C, Brownlee M. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest 112: 1049-1057, 2003.
17. Dumoulin JC, Evers JL, Bras M, Pieters MH, Geraedts JP. Positive effect of taurine on preimplantation development of mouse embryos in vitro. J Reprod Fertil 94: 373-380, 1992.
18. Eidem I, Stene LC, Henriksen T, Hanssen KF, Vangen S, Vollset SE, Joner G. Congenital anomalies in newborns of women with type 1 diabetes: nationwide population-based study in Norway, 1999-2004. Acta Obstet Gynecol Scand 89: 1403-1411, 2010.
19. Ejdesjo A, Wentzel P, Eriksson UJ. Genetic and environmental influence on diabetic rat embryopathy. Am J Physiol Endocrinol Metab 300: E454-E467, 2011.
20. Erickson RP, Karolyi IJ, Diehl SR. Correlation of susceptibility to 6-aminonicotinamide and hydrocortisone-induced cleft palate. Life Sci 76: 2071-2078, 2005.
21. Eriksson UJ. Importance of genetic predisposition and maternal environment for the occurrence of congenital malformations in offspring of diabetic rats. Teratology 37: 365-374, 1988.
22. Eriksson UJ, Borg LA. Diabetes and embryonic malformations. Role of substrate-induced free-oxygen radical production for dysmorphogenesis in cultured rat embryos. Diabetes 42: 411-419, 1993.
23. Eriksson UJ, Borg LA. Protection by free oxygen radical scavenging enzymes against glucose-induced embryonic malformations in vitro. Diabetologia 34: 325-331, 1991.
24. Eriksson UJ, Dahlstrom E, Larsson KS, Hellerstrom C. Increased incidence of congenital malformations in the offspring of diabetic rats and their prevention by maternal insulin therapy. Diabetes 31: 1-6, 1982.
25. Eriksson UJ, den Bieman M, Prins JB, van Zutphen LFM. Differences in susceptibility for diabetes-induced malformations in separated rat colonies of common origin. In: 4th FELASA Symposium. Lyon, France: Fondation Marcel Márieux, 1990, p. 53-57.
26. Eriksson UJ, Naeser P, Brolin SE. Increased accumulation of sorbitol in offspring of manifest diabetic rats. Diabetes 35: 1356-1363, 1986.
27. Eriksson UJ, Wentzel P, Minhas HS, Thornalley PJ. Teratogenicity of 3-deoxyglucosone and diabetic embryopathy. Diabetes 47: 1960-1966, 1998.
28. Evers IM, de Valk HW, Visser GH. Male predominance of congenital malformations in infants of women with type 1 diabetes. Diabetes Care 32: 1194-1195, 2009.
29. Evers IM, de Valk HW, Visser GH. Risk of complications of pregnancy in women with type 1 diabetes: nationwide prospective study in the Netherlands. Br Med J 328: 915, 2004.
30. Gareskog M, Wentzel P. Altered protein kinase C activation associated with rat embryonic dysmorphogenesis. Pediatr Res 56: 849-857, 2004.
31. Hagay ZJ, Weiss Y, Zusman I, Peled-Kamar M, Reece EA, Eriksson UJ, Groner Y. 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: 1036-1041, 1995.
32. Hashimoto M, Akazawa S, Akazawa M, Akashi M, Yamamoto H, Maeda Y, Yamaguchi Y, Yamasaki H, Tahara D, Nakanishi T. Effects of hyperglycaemia on sorbitol and myo-inositol contents of cultured embryos: treatment with aldose reductase inhibitor and myo-inositol supplementation. Diabetologia 33: 597-602, 1990.
33. Hiramatsu Y, Sekiguchi N, Hayashi M, Isshiki K, Yokota T, King GL, Loeken MR. Diacylglycerol production and protein kinase C activity are increased in a mouse model of diabetic embryopathy. Diabetes 51: 2804-2810, 2002.
34. Hod M, Star S, Passonneau JV, Unterman TG, Freinkel N. Effect of hyperglycemia on sorbitol and myo-inositol content of cultured rat conceptus: failure of aldose reductase inhibitors to modify myo-inositol depletion and dysmorphogenesis. Biochem Biophys Res Commun 140: 974-980, 1986.
35. Honein MA, Rasmussen SA, Reefhuis J, Romitti PA, Lammer EJ, Sun L, Correa A. Maternal smoking and environmental tobacco smoke exposure and the risk of orofacial clefts. Epidemiology 18: 226-233, 2007.
36. Horal M, Zhang Z, Stanton R, Virkamaki A, Loeken MR. Activation of the hexosamine pathway causes oxidative stress and abnormal embryo gene expression: involvement in diabetic teratogenesis. Birth Defects Res A Clin Mol Teratol 70: 519-527, 2004.
37. Horton WE Jr, Sadler TW. Effects of maternal diabetes on early embryogenesis Alterations in morphogenesis produced by the ketone body, B-hydroxybutyrate. Diabetes 32: 610-616, 1983.
38. Ikubo N, Saito M, Tsounapi P, Dimitriadis F, Ohmasa F, Inoue S, Shimizu S, Kinoshita Y, Satoh K. Protective effect of taurine on diabetic rat endothelial dysfunction. Biomed Res 32: 187-193, 2011.
39. Jugessur A, Shi M, Gjessing HK, Lie RT, Wilcox AJ, Weinberg CR, Christensen K, Boyles AL, Daack-Hirsch S, Nguyen TT, Christiansen L, Lidral AC, Murray JC. Maternal genes and facial clefts in offspring: a comprehensive search for genetic associations in two population-based cleft studies from Scandinavia. PLoS One 5: e11493, 2000.
40. Juriloff DM, Harris MJ, Dewell SL. A digenic cause of cleft lip in A-strain mice and definition of candidate genes for the two loci. Birth Defects Res A Clin Mol Teratol 70: 509-518, 2004.
41. Juriloff DM, Harris MJ, McMahon AP, Carroll TJ, Lidral AC. Wnt9b is the mutated gene involved in multifactorial nonsyndromic cleft lip with or without cleft palate in A/WySn mice, as confirmed by a genetic complementation test. Birth Defects Res A Clin Mol Teratol 76: 574-579, 2006.
42. Lauszus FF, Gron PL, Klebe JG. Association of polymorphism of methylene-tetrahydro-folate-reductase with urinary albumin excretion rate in type 1 diabetes mellitus but not with preeclampsia, retinopathy, and preterm delivery. Acta Obstet Gynecol Scand 80: 803-806, 2001.
43. Lee AT, Plump A, DeSimone C, Cerami A, Bucala R. A role for DNA mutations in diabetes-associated teratogenesis in transgenic embryos. Diabetes 44: 20-24, 1995.
44. Lee AT, Reis D, Eriksson UJ. Hyperglycemia-induced embryonic dysmorphogenesis correlates with genomic DNA mutation frequency in vitro and in vivo. Diabetes 48: 371-376, 1999.
45. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
46. Mao DW, Zhao YP, Li SR, Che JH, Tan WH. Study of teratogenicity of hyperglycemia on neural tube defects and antagonistic effect of taurine. Zhonghua Fu Chan Ke Za Zhi 39: 169-172, 2004.
47. Miller E, Hare JW, Cloherty JP, Dunn PJ, Gleason RE, Soeldner JS, Kitzmiller JL. Elevated maternal hemoglobin A1c in early pregnancy and major congenital anomalies in infants of diabetic mothers. N Engl J Med 304: 1331-1334, 1981.
48. Moloney MA, Casey RG, O'Donnell DH, Fitzgerald P, Thompson C, Bouchier-Hayes DJ. Two weeks taurine supplementation reverses endothelial dysfunction in young male type 1 diabetics. Diab Vasc Dis Res 7: 300-310, 2010.
49. Naidu RC. Teratogenic effects of tryptophane on the development of chick embryo. Experientia 30: 1462-1463, 1974.
50. Nash P, Olovsson M, Eriksson UJ. Placental dysfunction in Suramintreated rats: impact of maternal diabetes and effects of antioxidative treatment. J Soc Gynecol Investig 12: 174-184, 2005.
51. Nemer G, Fadlalah F, Usta J, Nemer M, Dbaibo G, Obeid M, Bitar F. A novel mutation in the GATA4 gene in patients with Tetralogy of Fallot. Hum Mutat 27: 293-294, 2006.
52. Nonaka K, Sasaki Y, Martin DA, Nakata M. Effect of the dam strain on the spontaneous incidence of cleft lip and palate and intrauterine growth of CL/Fr mouse fetuses. J Assist Reprod Genet 12: 447-452, 1995.
53. Nordquist N, Luthman H, Pettersson U, Eriksson UJ. Linkage study of embryopathy-Polygenic inheritance of diabetes-induced skeletal malformations in the rat. Reprod Toxicol 2012; Jan 2 [Epub ahead of print].
54. Otani H, Tanaka O, Tatewaki R, Naora H, Yoneyama T. Diabetic environment and genetic predisposition as causes of congenital malformations in NOD mouse embryos. Diabetes 40: 1245-1250, 1991.
55. Ou CY, Stevenson RE, Brown VK, Schwartz CE, Allen WP, Khoury MJ, Rozen R, Oakley GP Jr, Adams MJ, Jr. 5,10 Methylenetetrahydrofolate reductase genetic polymorphism as a risk factor for neural tube defects. Am J Med Genet 63: 610-614, 1996.
56. Pani L, Horal M, Loeken MR. Polymorphic susceptibility to the molecular causes of neural tube defects during diabetic embryopathy. Diabetes 51: 2871-2874, 2002.
57. Plamondon JA, Harris MJ, Mager DL, Gagnier L, Juriloff DM. The clf2 gene has an epigenetic role in the multifactorial etiology of cleft lip and palate in the A/WySn mouse strain. Birth Defects Res A Clin Mol Teratol 91: 716-727, 2011.
58. Ray JG, O'Brien TE, Chan WS. Preconception care and the risk of congenital anomalies in the offspring of women with diabetes mellitus: a meta-analysis. Qjm 94: 435-444, 2001.
59. Ray JG, Vermeulen MJ, Meier C, Wyatt PR. Risk of congenital anomalies detected during antenatal serum screening in women with pregestational diabetes. Q J Med 97: 651-653, 2004.
60. Sakamaki H, Akazawa S, Ishibashi M, Izumino K, Takino H, Yamasaki H, Yamaguchi Y, Goto S, Urata Y, Kondo T, Nagataki S. Significance of glutathione-dependent antioxidant system in diabetesinduced embryonic malformations. Diabetes 48: 1138-1144, 1999.
61. Salbaum JM, Kappen C. Neural tube defect genes and maternal diabetes during pregnancy. Birth Defects Res A Clin Mol Teratol 88: 601-611, 2010.
62. Shum L, Sadler TW. Embryonic catch-up growth after exposure to the ketone body D, L,-β-hydroxybutyrate in vitro. Teratology 38: 369-379, 1988.
63. Sivan E, Lee YC, Wu YK, Reece EA. Free radical scavenging enzymes in fetal dysmorphogenesis among offspring of diabetic rats. Teratology 56: 343-349, 1997.
64. Spilson SV, Kim HJ, Chung KC. Association between maternal diabetes mellitus and newborn oral cleft. Ann Plast Surg 47: 477-481, 2001.
65. Steel JM, Johnstone FD, Smith AF, Duncan LJ. Five years' experience of a "prepregnancy" clinic for insulin-dependent diabetics. Br Med J (Clin Res Ed) 285: 353-356, 1982.
66. Styrud J, Thunberg L, Nybacka O, Eriksson UJ. Correlations between maternal metabolism and deranged development in the offspring of normal and diabetic rats. Pediatr Res 37: 343-353, 1995.
67. Sussman I, Matschinsky FM. Diabetes affects sorbitol and myo-inositol levels of neuroectodermal tissue during embryogenesis in rat. Diabetes 37: 974-981, 1988.
68. Suzuki S, Marazita ML, Cooper ME, Miwa N, Hing A, Jugessur A, Natsume N, Shimozato K, Ohbayashi N, Suzuki Y, Niimi T, Minami K, Yamamoto M, Altannamar TJ, Erkhembaatar T, Furukawa H, Daack-Hirsch S, L'Heureux J, Brandon CA, Weinberg SM, Neiswanger K, Deleyiannis FW, de Salamanca JE, Vieira AR, Lidral AC, Martin JF, Murray JC. Mutations in BMP4 are associated with subepithelial, microform, and overt cleft lip. Am J Hum Genet 84: 406-411, 2009.
69. Thomason HA, Dixon MJ, Dixon J. Facial clefting in Tp63 deficient mice results from altered Bmp4, Fgf8 and Shh signaling. Dev Biol 321: 273-282, 2008.
70. Trocino RA, Akazawa S, Ishibashi M, Matsumoto K, Matsuo H, Yamamoto H, Goto S, Urata Y, Kondo T, Nagataki S. Significance of glutathione depletion and oxidative stress in early embryogenesis in glucose-induced rat embryo culture. Diabetes 44: 992-998, 1995.
71. Vieira AR, Karras JC, Orioli IM, Castilla EE, Murray JC. Genetic origins in a South American clefting population. Clin Genet 62: 458-463, 2002.
72. Weksler-Zangen S, Yaffe P, Ornoy A. Reduced SOD activity and increased neural tube defects in embryos of the sensitive but not of the resistant Cohen diabetic rats cultured under diabetic conditions. Birth Defects Res A Clin Mol Teratol 67: 429-437, 2003.
73. Wentzel P, Ejdesjo A, Eriksson UJ. Maternal diabetes in vivo and high glucose in vitro diminish GAPDH activity in rat embryos. Diabetes 52: 1222-1228, 2003.
74. Wentzel P, Eriksson UJ. 8-Iso-PGF(2alpha) administration generates dysmorphogenesis and increased lipid peroxidation in rat embryos in vitro. Teratology 66: 164-168, 2002.
75. Wentzel P, Thunberg L, Eriksson UJ. Teratogenic effect of diabetic serum is prevented by supplementation of superoxide dismutase and N-acetylcysteine in rat embryo culture. Diabetologia 40: 7-14, 1997.
76. Wlodarczyk BJ, Palacios AM, Chapa CJ, Zhu H, George TM, Finnell RH. Genetic basis of susceptibility to teratogen induced birth defects. Am J Med Genet C Semin Med Genet 157: 215-226, 2011.
77. Wu RR, Lyons PA, Wang A, Sainsbury AJ, Chung S, Palmer TN. Effects of galactose feeding on aldose reductase gene expression. J Clin Invest 92: 155-159, 1993.
78. Yang X, Borg LA, Eriksson UJ. Altered metabolism and superoxide generation in neural tissue of rat embryos exposed to high glucose. Am J Physiol Endocrinol Metab 272: E173-E180, 1997.
79. Ylinen K, Aula P, Stenman UH, Kesaniemi-Kuokkanen T, Teramo K. Risk of minor and major fetal malformations in diabetics with high haemoglobin A1c values in early pregnancy. Br Med J (Clin Res Ed) 289: 345-346, 1984.
80. Zaken V, Kohen R, Ornoy A. Vitamins C and E improve rat embryonic antioxidant defense mechanism in diabetic culture medium. Teratology 64: 33-44, 2001.