Oxygen modulates the response of first-trimester trophoblasts to hyperglycemia

American Journal of Pathology

Volumn 180, Issue 1, 2012, Pages 153-164

  Fröhlich, Julia D ^a   Huppertz, Berthold ^a   Abuja, Peter M ^a   König, Julia ^a   Desoye, Gernot ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; OXYGEN; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL COUNT; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CYTOSOL; EMBRYO DEVELOPMENT; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; MITOCHONDRION; PLACENTA DEVELOPMENT; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; TROPHOBLAST;

ANTIMETABOLITES; ANTIOXIDANTS; CELL PROLIFERATION; CELLS, CULTURED; DIABETES, GESTATIONAL; ENZYME INHIBITORS; FEMALE; HUMANS; HYDROGEN PEROXIDE; HYPERGLYCEMIA; MAP KINASE SIGNALING SYSTEM; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; OXYGEN; PREGNANCY; PREGNANCY TRIMESTER, FIRST; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; TROPHOBLASTS; UP-REGULATION;

EID: 83455164916     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.09.012     Document Type: Article

References (51)

1. E. Jauniaux, G.J. Burton Pathophysiology of histological changes in early pregnancy loss Placenta 26 2005 114 123 (Pubitemid 40246999)
2. B. Huppertz Placental origins of preeclampsia: challenging the current hypothesis Hypertension 51 2008 970 975 (Pubitemid 351398986)
3. G.J. Burton, E. Jauniaux, D.S. Charnock-Jones The influence of the intrauterine environment on human placental development Int J Dev Biol 54 2010 303 312
4. B.M. Sibai Risk factors, pregnancy complications, and prevention of hypertensive disorders in women with pregravid diabetes mellitus J Matern Fetal Med 9 2000 62 65 (Pubitemid 30176215)
5. K. Mammon, R. Keshet, S. Savion, O. Pekar, Z. Zaslavsky, A. Fein, V. Toder, A. Torchinsky Diabetes-induced fetal growth retardation is associated with suppression of NF-kappaB activity in embryos Rev Diabet Stud 2 2005 27 34
6. J.D. Biggers, M.C. Summers Impact of hyperglycemia on early embryo development and embryopathy: in vitro experiments using a mouse model Hum Reprod 23 2008 2874 2875
7. N. Freinkel Banting Lecture 1980 Of pregnancy and progeny Diabetes 29 1980 1023 1035 (Pubitemid 11017928)
8. J.F. Pedersen, L. Molsted-Pedersen, H.B. Mortensen Fetal growth delay and maternal hemoglobin A1c in early diabetic pregnancy Obstet Gynecol 64 1984 351 352 (Pubitemid 14073453)
9. Z.A. Brown, J.L. Mills, B.E. Metzger, R.H. Knopp, J.L. Simpson, L. Jovanovic-Peterson, K. Scheer, M.I. Van Allen, J.H. Aarons, G.F. Reed Early sonographic evaluation for fetal growth delay and congenital malformations in pregnancies complicated by insulin-requiring diabetes National Institute of Child Health and Human Development Diabetes in Early Pregnancy Study Diabetes Care 15 1992 613 619
10. M. Thame, C. Osmond, F. Bennett, R. Wilks, T. Forrester Fetal growth is directly related to maternal anthropometry and placental volume Eur J Clin Nutr 58 2004 894 900 (Pubitemid 38923188)
11. U. Weiss, M. Cervar, P. Puerstner, O. Schmut, J. Haas, R. Mauschitz, G. Arikan, G. Desoye Hyperglycaemia in vitro alters the proliferation and mitochondrial activity of the choriocarcinoma cell lines BeWo JAR and JEG-3 as models for human first-trimester trophoblast Diabetologia 44 2001 209 219 (Pubitemid 32156206)
12. J.F. Pedersen, S. Sorensen, L. Molsted-Pedersen Serum levels of human placental lactogen, pregnancy-associated plasma protein A and endometrial secretory protein PP14 in first trimester of diabetic pregnancy Acta Obstet Gynecol Scand 77 1998 155 158 (Pubitemid 28075381)
13. B. Huppertz, M. Gauster, K. Orendi, J. Konig, G. Moser Oxygen as modulator of trophoblast invasion J Anat 215 2009 14 20
14. E. Jauniaux, A.L. Watson, J. Hempstock, Y.P. Bao, J.N. Skepper, G.J. Burton Onset of maternal arterial blood flow and placental oxidative stress A possible factor in human early pregnancy failure Am J Pathol 157 2000 2111 2122
15. G.J. Burton Oxygen, the Janus gas; its effects on human placental development and function J Anat 215 2009 27 35
16. C.K. Roberts, K.K. Sindhu Oxidative stress and metabolic syndrome Life Sci 84 2009 705 712
17. S.W. Choi, I.F. Benzie, S.W. Ma, J.J. Strain, B.M. Hannigan Acute hyperglycemia and oxidative stress: direct cause and effect? Free Radic Biol Med 44 2008 1217 1231
18. P.A. Dennery Effects of oxidative stress on embryonic development Birth Defects Res C Embryo Today 81 2007 155 162 (Pubitemid 350086244)
19. P. Wentzel, A. Ejdesjo, U.J. Eriksson Maternal diabetes in vivo and high glucose in vitro diminish GAPDH activity in rat embryos Diabetes 52 2003 1222 1228 (Pubitemid 36523360)
20. P. Wentzel, U.J. Eriksson Antioxidants diminish developmental damage induced by high glucose and cyclooxygenase inhibitors in rat embryos in vitro Diabetes 47 1998 677 684 (Pubitemid 28160461)
21. W. Qi, X. Chen, R.E. Gilbert, Y. Zhang, M. Waltham, M. Schache, D.J. Kelly, C.A. Pollock High glucose-induced thioredoxin-interacting protein in renal proximal tubule cells is independent of transforming growth factor-beta1 Am J Pathol 171 2007 744 754 (Pubitemid 47440974)
22. E. Peuchant, J.L. Brun, V. Rigalleau, L. Dubourg, M.J. Thomas, J.Y. Daniel, J.J. Leng, H. Gin Oxidative and antioxidative status in pregnant women with either gestational or type 1 diabetes Clin Biochem 37 2004 293 298 (Pubitemid 38314883)
23. L. Myatt Review: reactive oxygen and nitrogen species and functional adaptation of the placenta Placenta 31 Suppl 2010 S66 S69
24. L. Myatt, X. Cui Oxidative stress in the placenta Histochem Cell Biol 122 2004 369 382 (Pubitemid 39506594)
25. L. Gao, G.E. Mann Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signaling Cardiovasc Res 82 2009 9 20
26. D.X. Zhang, D.D. Gutterman Mitochondrial reactive oxygen species-mediated signaling in endothelial cells Am J Physiol Heart Circ Physiol 292 2007 H2023 H2031
27. M.P. Murphy How mitochondria produce reactive oxygen species Biochem J 417 2009 1 13
28. A. Makino, B.T. Scott, W.H. Dillmann Mitochondrial fragmentation and superoxide anion production in coronary endothelial cells from a mouse model of type 1 diabetes Diabetologia 53 2010 1783 1794
29. U. Hiden, C. Wadsack, N. Prutsch, M. Gauster, U. Weiss, H.G. Frank, U. Schmitz, C. Fast-Hirsch, M. Hengstschlager, A. Potgens, A. Ruben, M. Knofler, P. Haslinger, B. Huppertz, M. Bilban, P. Kaufmann, G. Desoye The first trimester human trophoblast cell line ACH-3P: a novel tool to study autocrine/paracrine regulatory loops of human trophoblast subpopulations-TNF-alpha stimulates MMP15 expression BMC Dev Biol 7 2007 137
30. C.M. Palmeira, A.P. Rolo, J. Berthiaume, J.A. Bjork, K.B. Wallace Hyperglycemia decreases mitochondrial function: the regulatory role of mitochondrial biogenesis Toxicol Appl Pharmacol 225 2007 214 220 (Pubitemid 350088064)
31. Q. Gao, Y.M. Gao Hyperglycemic condition disturbs the proliferation and cell death of neural progenitors in mouse embryonic spinal cord Int J Dev Neurosci 25 2007 349 357 (Pubitemid 350051329)
32. M. Rajesh, P. Mukhopadhyay, S. Batkai, B. Mukhopadhyay, V. Patel, G. Hasko, C. Szabo, J.G. Mabley, L. Liaudet, P. Pacher Xanthine oxidase inhibitor allopurinol attenuates the development of diabetic cardiomyopathy J Cell Mol Med 13 2009 2330 2341
33. J.R. Henderson, H. Swalwell, S. Boulton, P. Manning, C.J. McNeil, M.A. Birch-Machin Direct, real-time monitoring of superoxide generation in isolated mitochondria Free Radic Res 43 2009 796 802
34. U. Hiden, G. Desoye The human placenta in diabetes A Practical Manual of Diabetes in Pregnancy D.R. McCance, M. Maresh, D.A. Sacks, 2010 Wiley-Blackwell Oxford UK 26 33
35. G.L. King, M.R. Loeken Hyperglycemia-induced oxidative stress in diabetic complications Histochem Cell Biol 122 2004 333 338 (Pubitemid 39506591)
36. E. Favaro, I. Miceli, B. Bussolati, M. Schmitt-Ney, P. Cavallo Perin, G. Camussi, M.M. Zanone Hyperglycemia induces apoptosis of human pancreatic islet endothelial cells: effects of pravastatin on the Akt survival pathway Am J Pathol 173 2008 442 450
37. Y. Kobayashi, K. Naruse, Y. Hamada, E. Nakashima, K. Kato, N. Akiyama, H. Kamiya, A. Watarai, M. Nakae, Y. Oiso, J. Nakamura Human proinsulin C-peptide prevents proliferation of rat aortic smooth muscle cells cultured in high-glucose conditions Diabetologia 48 2005 2396 2401 (Pubitemid 41618932)
38. S. Di Paolo, L. Gesualdo, E. Ranieri, G. Grandaliano, F.P. Schena High glucose concentration induces the overexpression of transforming growth factor-beta through the activation of a platelet-derived growth factor loop in human mesangial cells Am J Pathol 149 1996 2095 2106 (Pubitemid 26415226)
39. J.S. Huang, L.Y. Chuang, J.Y. Guh, Y.J. Huang, M.S. Hsu Antioxidants attenuate high glucose-induced hypertrophic growth in renal tubular epithelial cells Am J Physiol Renal Physiol 293 2007 F1072 F1082
40. T. Cindrova-Davies, O. Spasic-Boskovic, E. Jauniaux, D.S. Charnock-Jones, G.J. Burton Nuclear factor-kappa B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress: effects of antioxidant vitamins Am J Pathol 170 2007 1511 1520 (Pubitemid 47339297)
41. M.A. Ihnat, J.E. Thorpe, C.D. Kamat, C. Szabo, D.E. Green, L.A. Warnke, Z. Lacza, A. Cselenyak, K. Ross, S. Shakir, L. Piconi, R.C. Kaltreider, A. Ceriello Reactive oxygen species mediate a cellular 'memory' of high glucose stress signaling Diabetologia 50 2007 1523 1531 (Pubitemid 46879013)
42. J.M. Forbes, M.T. Coughlan, M.E. Cooper Oxidative stress as a major culprit in kidney disease in diabetes Diabetes 57 2008 1446 1454
43. P. Weidig, D. McMaster, U. Bayraktutan High glucose mediates pro-oxidant and antioxidant enzyme activities in coronary endothelial cells Diabetes Obes Metab 6 2004 432 441 (Pubitemid 39409794)
44. T. Matsunami, Y. Sato, T. Sato, S. Ariga, T. Shimomura, M. Yukawa Oxidative stress and gene expression of antioxidant enzymes in the streptozotocin-induced diabetic rats under hyperbaric oxygen exposure Int J Clin Exp Pathol 3 2009 177 188
45. C.J. Jones, U. Weiss, C.M. Siman, G. Desoye Mitochondria from human trophoblast and embryonic liver cells are resistant to hyperglycaemia-associated high-amplitude swelling Diabetologia 44 2001 389 391 (Pubitemid 32234470)
46. J. Sun, Y. Xu, S. Sun, Y. Sun, X. Wang Intermittent high glucose enhances cell proliferation and VEGF expression in retinal endothelial cells: the role of mitochondrial reactive oxygen species Mol Cell Biochem 343 2010 27 35
47. Y. Peng, K.H. Kwok, P.H. Yang, S.S. Ng, J. Liu, O.G. Wong, M.L. He, H.F. Kung, M.C. Lin Ascorbic acid inhibits ROS production NF-kappa B activation and prevents ethanol-induced growth retardation and microencephaly Neuropharmacology 48 2005 426 434 (Pubitemid 40250006)
48. C. Leloup, C. Tourrel-Cuzin, C. Magnan, M. Karaca, J. Castel, L. Carneiro, A.L. Colombani, A. Ktorza, L. Casteilla, L. Penicaud Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion Diabetes 58 2009 673 681
49. S. Poncin, I.M. Colin, B. Decallonne, I. Clinckspooor, M.C. Many, J.F. Denef, A.C. Gerard N-acetylcysteine and 15 deoxy-{delta}12,14-prostaglandin J2 exert a protective effect against autoimmune thyroid destruction in vivo but not against interleukin-1{alpha}/interferon {gamma}-induced inhibitory effects in thyrocytes in vitro Am J Pathol 177 2010 219 228
50. Y.H. Chen, S.J. Lin, F.Y. Lin, T.C. Wu, C.R. Tsao, P.H. Huang, P.L. Liu, Y.L. Chen, J.W. Chen High glucose impairs early and late endothelial progenitor cells by modifying nitric oxide-related but not oxidative stress-mediated mechanisms Diabetes 56 2007 1559 1568
51. C. Peiro, N. Lafuente, N. Matesanz, E. Cercas, J.L. Llergo, S. Vallejo, L. Rodriguez-Manas, C.F. Sanchez-Ferrer High glucose induces cell death of cultured human aortic smooth muscle cells through the formation of hydrogen peroxide Br J Pharmacol 133 2001 967 974 (Pubitemid 32762405)