Oxidative stress promotes the increase of matrix metalloproteinases-2 and -9 activities in the feto-placental unit of diabetic rats

References

• Schwartz R, Teramo KA. Effects of diabetic pregnancy on the fetus and newborn. Semin Perinatol 2000; 24: 120–135
   PubMed Web of Science ®Google Scholar
• Desoye G, Shafrir E. The human placenta in diabetic pregnancy. Diabetes Rev 1996; 4: 70–89
   Google Scholar
• Eriksson UJ, Cederberg J, Wentzel P. Congenital malformations in offspring of diabetic mothers. Animal and human studies. Rev Endocr Metab Disord 2003; 4: 79–93
   PubMed Web of Science ®Google Scholar
• Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Oxford University Press, UK 1999
   Google Scholar
• Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000; 404: 787–790
   PubMed Web of Science ®Google Scholar
• Lin Y, Berg AH, Iyengar P, Lam T, Giacca A, Combs TP, Rajala MW, Du X, Rollman B, Li W, Hawkins M, Barzilai N, Rhodes CJ, Fantus IG, Brownlee M, Scherer PE. The hyperglycemia-induced inflammatory response in adipocytes. The role of reactive oxygen species. J Biol Chem 2005; 280: 1626–4617
   Web of Science ®Google Scholar
• Jain SK. Hyperglycemia can cause membrane lipid peroxidation and osmotic fragility in human red blood cells. J Biol Chem 1989; 264: 21340–21345
   PubMed Web of Science ®Google Scholar
• Jain SK, McVie R. Hyperketonemia can increase lipid peroxidation and lower gluthathione levels in human erythrocytes in vitro and in type 1 diabetic patients. Diabetes 1999; 48: 1850–1855
   PubMed Web of Science ®Google Scholar
• Martín-Gallán P, Carrascosa A, Gussinyé M, Domínguez C. Biomarkers of diabetes-associated oxidative stress and antioxidant status in young diabetic patients with or without subclinical complications. Free Radic Biol Med 2003; 34: 1474–1563
   Web of Science ®Google Scholar
• White V, Jawerbaum A, Sinner D, Pustovrh C, Capobianco E, González E. Oxidative stress and altered prostanoid production in the placenta of streptozotocin-induced diabetic rats. Reprod Fertil Dev 2002; 14: 117–123
   PubMed Web of Science ®Google Scholar
• Cederberg J, Basu S, Eriksson UJ. Increased rate of lipid peroxidation and protein carbonylation in experimental diabetic pregnancy. Diabetologia 2001; 44: 766–774
   PubMed Web of Science ®Google Scholar
• Viana M, Aruoma O, Herrera E, Bonet B. Oxidative damage in pregnant diabetic rats and their embryos. Free Radic Biol Med 2000; 29: 1115–1121
   PubMed Web of Science ®Google Scholar
• Pustovrh C, Jawerbaum A, Sinner D, Pesaresi M, Baier M, Gimeno M, González E. Membrane-type matrix metalloproteinase-9 activity in placental tissue from patients with pregestational and gestational diabetes mellitus. Reprod Fertil Dev 2000; 12: 269–275
   PubMed Web of Science ®Google Scholar
• Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 2004; 122: 369–382
   PubMed Web of Science ®Google Scholar
• Sivan E, Lee Y, Wu Y, Reece A. Free radical scavenging enzymes in fetal dysmorphogenesis among offspring of diabetic rats. Teratology 1997; 56: 343–349
   PubMedGoogle Scholar
• Weksler-Zangen S, Yaffe O, 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 (Part A) 2003; 67: 429–437
   PubMedGoogle Scholar
• Lyall F, Gibson J, Greer I, Brockman D, Eis A, Myatt L. Increased nitrotyrosine in the diabetic placenta. Evidence for oxidative stress. Diabetes Care 1998; 21: 1753–1758
   PubMed Web of Science ®Google Scholar
• Siman CM, Eriksson UJ. Vitamin E decreases the occurrence of malformations in the offspring of diabetic rats. Diabetes 1997; 46: 1054–1061
   PubMed Web of Science ®Google Scholar
• Sivan E, Reece A, Wu Y, Homko C, Polansky M, Borenstein M. Dietary vitamin E prophylaxis and diabetic embryopathy: Morphologic and biochemical analysis. Am J Obstet Gynecol 1996; 175: 793–799
   PubMed Web of Science ®Google Scholar
• Nelson K, Melendez A. Mitochondrial redox control of matrix metalloproteinases. Free Radic Biol Med 2004; 37: 768–784
   PubMed Web of Science ®Google Scholar
• Grant GA, Goldberg GI, Wilhelm SM, He C, Eisen AZ. Activation of extracellular matrix metalloproteases by proteases and organomercurials. Matrix 1992; 1(Suppl 1)217–226
   PubMedGoogle Scholar
• Somerville RPT, Oblander SA, Apte SS. Matrix metalloproteinases: Old dogs with new tricks. Genome Biol 2003; 4: 216–226
   PubMed Web of Science ®Google Scholar
• Belkhiri A, Richards C, Whaley M, McQueen SA, Orr FW. Increased expression of activated matriz metalloproteinase-2 by human endothelial cells after sublethal H2O2 exposure. Lab Investig 1997; 77: 539–553
   Web of Science ®Google Scholar
• Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, Galis ZS. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metaloproteinases in vitro: Implications for atherosclerotic plaque stability. J Clin Investig 1996; 98: 2572–2579
   PubMed Web of Science ®Google Scholar
• Wenk J, Brenneisen P, Wlaschek M, Poswig A, Briviba K, Oberley TD, Scharffetter-Kochanek K. Stable overexpression of manganese superoxide dismutase in mitochondria identifies hydrogen peroxide as a major oxidant in the AP-1 mediated induction of matrix-degrading metalloprotease-1. J Biol Chem 1999; 274: 22869–25876
   Web of Science ®Google Scholar
• Buhimschi IA, Kramer WB, Buhimschi CS, Thompson LP, Weiner CP. Reduction-oxidation (redox) state regulation of matrix metalloproteinase activity in human fetal membranes. Am J Obstet Gynecol 2000; 182: 458–464
   PubMed Web of Science ®Google Scholar
• Mandal M, Mandal A, Das S, Chakraborti T, Chakraborti S. Clinical implications of matrix metalloproteinases. Mol Cell Biochem 2003; 252: 305–329
   PubMed Web of Science ®Google Scholar
• Okamoto T, Niu R, Yamada S, Osawa M. Reduced expression of tissue inhibitor of metalloproteinase (TIMP)-2 in gestational trophoblastic diseases. Mol Hum Reprod 2002; 8: 392–398
   PubMed Web of Science ®Google Scholar
• Imper V, Van Wart HE. Substrate specificity and mechanisms of substrate recognition of the matrix metalloproteinases. Matrix metalloproteinases, WC Parks, RP Mecham. Academic Press, USA 1998; 219–242
   Google Scholar
• Hulboy DL, Rudolph LA, Matrisian LM. Matrix metalloproteinases as mediators of reproductive function. Mol Hum Reprod 1997; 3: 27–57
   PubMed Web of Science ®Google Scholar
• Vu TH, Werb Z. Matrix metalloproteinases: Effectors of development and normal physiology. Genes Dev 2000; 14: 2123–2133
   PubMed Web of Science ®Google Scholar
• Teesalu T, Mason R, Basset P, Blasi F, Talarico D. Expression of matrix metalloproteinases during murine chorioallantoic placenta maturation. Dev Dyn 1999; 214: 248–258
   PubMed Web of Science ®Google Scholar
• Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: Key pieces of the development puzzle. Science 1994; 226: 1508–1518
   Google Scholar
• Kheradmand F, Rishi K, Werb Z. Signalling through the EFG receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J Cell Sci 2002; 115: 839–848
   PubMed Web of Science ®Google Scholar
• Novaro V, Pustovrh C, Colman-Lerner A, Radisky D, Lo Nostro F, Paz D, Jawerbaum A, Gonzalez E. Nitric oxide induces gelatinase A (matrix metalloproteinase 2) during rat embryo implantation. Fertil Steril 2002; 78: 1278–1287
   PubMed Web of Science ®Google Scholar
• Jawerbaum A, Gonzalez E. Effects of maternal hyperglycemia during embryo development. Curr Pharm Design 2005; 11: 1327–1342
   PubMed Web of Science ®Google Scholar
• Pustovrh C, Jawerbaum A, Sinner D, White V, Capobianco E, González E. Metalloproteinase 2 activity and modulation in uterus from neonatal-streptozotocin-induced diabetic rats during embryo implantation. Reprod Fertil Develop 2002; 12: 479–485
   Google Scholar
• Pustovrh C, Jawerbaum A, Capobianco E, White V, López-Costa JJ, González E. Increased matrix metalloproteinases 2 and 9 in placenta of diabetic rats at midgestation. Placenta 2005; 26: 339–348
   PubMed Web of Science ®Google Scholar
• Portha B, Picon L, Rosselin G. Chemical diabetes in the adult rat as the spontaneous evolution of neonatal diabetes. Diabetologia 1979; 17: 371–377
   PubMed Web of Science ®Google Scholar
• Woessner JF, Taplin C. Purification and properties of a small latent matrix metalloproteinase of the rat uterus. J Biol Chem 1988; 263: 16918–16925
   PubMed Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351–358
   PubMed Web of Science ®Google Scholar
• Aebi H. Catalase in vitro. Methods Enzymol 1984; 105: 121–126
   PubMed Web of Science ®Google Scholar
• Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 1972; 247: 3170–3175
   PubMed Web of Science ®Google Scholar
• Solberg H, Rinkenberger J, Dano K, Werb Z, Lund L. A functional overlap of plasminogen and MMPs regulates vascularization during placental development. Development 2003; 130: 4439–4450
   PubMed Web of Science ®Google Scholar
• Novaro V, Colman Lerner A, Valdillo Ortega FV, Jawerbaum A, Paz D, Lo Nostro F, Pustovrh C, Gimeno MF, González E. Regulation of metalloproteinases by nitric oxide in human trophoblast cell in culture. Reprod Fertil Dev 2001; 13: 411–420
   PubMed Web of Science ®Google Scholar
• Radealli T, Varastehpour A, Catalano P, Hauguel-de Mouzon S. Gestational diabetes induces placental genes for chronic stress and inflammatory pathways. Diabetes 2003; 52: 2951–2958
   PubMed Web of Science ®Google Scholar
• Babawale MO, Lovat S, Mayhew TM, Lammiman MJ, James DK, Leach L. Effects of gestational diabetes on junctional adhesion molecules in human term placental vasculature. Diabetologia 2000; 43: 1185–1196
   PubMed Web of Science ®Google Scholar
• Mayhew TM. Enhanced fetoplacental angiogenesis in pre-gestational diabetes mellitus: The extra growth is exclusively longitudinal and not accompanied by microvascular remodelling. Diabetologia 2002; 45: 1434–1439
   PubMed Web of Science ®Google Scholar
• Coughlan MT, Vervaart PP, Permezel M, Gergiou HM, Rice GE. Altered placental oxidative stress status in gestational diabetes mellitus. Placenta 2004; 25: 78–84
   PubMed Web of Science ®Google Scholar
• Kinalski M, Telejko B, Kowalska I, Urban J, Kinalska I. Evaluation of lipid peroxidation products and antioxidative enzymes activity in cord blood and placental homogenates of pregnant diabetic women. Ginekol Pol 1999; 70: 57–61
   PubMedGoogle Scholar
• Fine E, Horal M, Chang T, Fortin G, Loeken M. Hyperglycemia is responsible for altered gene expression apoptosis and neural tube defects associated with diabetic pregnancy. Diabetes 1999; 48: 2454–2462
   PubMed Web of Science ®Google Scholar
• El-Hage S, Singh SM. Temporal expression of genes encoding free radical-metabolzing enzymes is associated with higher mRNA levels during in utero development in mice. Dev Genet 1990; 11: 149–159
   PubMedGoogle Scholar
• Khan JY, Black S. Developmental changes in murine brain antioxidant enzymes. Pediatr Res 2003; 54: 77–82
   PubMed Web of Science ®Google Scholar
• Ratajska A, Cleutjens JPM. Embryogenesis of the rat heart: The expression of collagenases. Basic Res Cardiol 2002; 97: 189–197
   PubMed Web of Science ®Google Scholar
• Miettinen P, Huotari MA, Koivisto T, Ustinov J, Palgi J, Rasilainen S, Lehtonen E, Keski-Oja J, Otonkoski T. Impaired migration and delayed differentiation of pancreatic islet cells in mice lacking EGF-receptors. Development 2000; 127: 2617–2627
   PubMed Web of Science ®Google Scholar
• Piper JM. Lung maturation in diabetes and pregnancy: If and when to test. Semin Perinatol 2002; 26: 206–209
   PubMed Web of Science ®Google Scholar
• Van Assche FA, Holemans K, Aerts L. Long-term consequences for offspring of diabetes during pregnancy. Br Med Bull 2001; 60: 173–182
   PubMed Web of Science ®Google Scholar