Vascular dysfunction in the diabetic placenta: Causes and consequences

Journal of Anatomy

Volumn 215, Issue 1, 2009, Pages 69-76

  Leach, Lopa ^a,b   Taylor, Alice ^a   Sciota, Flavia ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b QUEEN S MEDICAL CENTRE   (United Kingdom)

Author keywords

Human placental vessels; Hyperglycaemia; Hyperinsulinaemia; Occludin; Vascular endothelial cadherin

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BETA CATENIN; CELL ADHESION MOLECULE; VASCULOTROPIN;

ANGIOGENESIS; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CONFERENCE PAPER; ENDOTHELIUM; GENE EXPRESSION REGULATION; GENE FUNCTION; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; MATERNAL DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PLACENTA; PRIORITY JOURNAL; TIGHT JUNCTION; VASCULAR DISEASE;

CAPILLARY PERMEABILITY; DIABETES MELLITUS, TYPE 1; FEMALE; HUMANS; HYPERGLYCEMIA; HYPERINSULINISM; NEOVASCULARIZATION, PATHOLOGIC; PLACENTA; PREGNANCY; PREGNANCY IN DIABETICS;

EID: 67449137959     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2009.01098.x     Document Type: Conference Paper

References (85)

1. Aiello LP, Avery RL, Arrigg PG, et al. (1994) Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331, 1480-1487.
2. Antonetti DA, Barber AJ, Khin SE, et al. (1998) Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content. Vascular endothelial growth factor decreases occludin in retinal endothelial cells. Diabetes 47, 1953-1959.
3. Babawale MO, Lovat S, Mayhew TM, Lammiman MJ, James DK, Leach L (2000) Effects of gestational diabetes on junctional adhesion molecules in human term placenta vasculature. Diabetologia 43, 1185-1196.
4. Bazzoni G, Dejana E (2003) Endothelial cell-to-cell junctions: Molecular organization and role in vascular homeostasis. Physiol Rev 84, 869-901.
5. Ben-Ze'ev A, Geiger B (1998) Differential molecular interactions of β-catenin and plakoglobin in adhesion, signalling and cancer. Curr Opin Cell Biol 10, 629-639.
6. Boden G, Vaidyula VR, Homko C, Cheung P, Rao AK (2007) Circulating tissue factor procoagulant activity and thrombin generation in patients with type 2 diabetes: Effects of insulin and glucose. J Clin Endocrinol Metab 92, 4352-4358.
7. Bohlen HG, Nase GP (2001) Arteriolar nitric oxide concentration is decreased during hyperglycemia-induced betaII PKC activation. Am J Physiol Heart Circ Physiol 280, H621-627.
8. Brownlee M, Cerami A, Vlassara H (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 318, 1315-1321.
9. Bucala R, Tracey KJ, Cerami A (1991) Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilatation in experimental diabetes. J Clin Invest 87, 432-438.
10. Caveda L, Martin-Padura I, Navarro P, et al. (1996) Inhibition of cultured cell growth by vascular endothelial cadherin (cadherin-5/ VE-cadherin). J Clin Invest 98, 886-893.
11. Chakravarthy U, Hayes RG, Stitt AW, McAuley E, Archer DB (1998) Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products. Diabetes 47, 945-952.
12. Chaturvedi N, Fuller JH, Pokras F, et al. (2001) Circulating plasma vascular endothelial growth factor and microvascular complications of Type 1 diabetes mellitus: The influence of ACE inhibition. Diabet Med 18, 288-294.
13. Chekir C, Nakatsuka M, Noguchi S, et al. (2006) Accumulation of advanced glycation end products in women with preeclampsia: Possible involvement of placental oxidative and nitrative stress. Placenta 27, 225-233.
14. Chiarelli F, Cipollone F, Romano F, et al. (2000) Increased circulating nitric oxide in young patients with type 1 diabetes and persistent microalbuminuria: Relation to glomerular hyperfiltration. Diabetes 49, 1258-1263.
15. Cohen AW, Carbajal JM, Schaeffer RC (1999) VEGF stimulates tyrosine phosphorylation of β-catenin and small-pore endothelial barrier dysfunction. Am J Physiol 277, H2038-2049.
16. Conacci-Sorrell M, Zhurinsky J, Ben-Ze'en A (2002) The cadherin-catenin adhesion system in signalling and cancer. J Clin Invest 109, 987-991.
17. Cooper ME, Vranes D, Youssef S, et al. (1999) Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes 48, 2229-2239.
18. Craven PA, Davidson CM, DeRubertis FR (1990) Increase in diacylglycerol mass in isolated glomeruli by glucose from de novo synthesis of glycerolipids. Diabetes 39, 667-674.
19. Demir R, Kayisli UA, Cayli S, Huppertz B (2006) Sequential steps during vasculogenesis and angiogenesis in the very early human placenta. Placenta 27, 535-539.
20. Derubertis FR, Craven PA (1994) Activation of protein kinase C in glomerular cells in diabetes. Mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes 43, 1-8.
21. Desoye G, Hartmann M, Blaschitz A, et al. (1994) Insulin receptors in syncytiotrophoblast and fetal endothelium of human placenta. Immunohistochemical evidence for developmental changes in distribution pattern. Histochemistry 101, 277-285.
22. Dominguez C, Ruiz E, Gussinye M, Carrascosa A (1998) Oxidative stress at onset and in early stages of type 1 diabetes in children and adolescents. Diabetes Care 21, 1736-1742.
23. Dye JF, Leach L, Clark P, Firth JA (2001) Cyclic AMP and acidic fibroblast growth factor have opposing effects on tight and adherens junctions in microvascular endothelial cells in vitro. Microvasc Res 62, 94-113.
24. Dye JF, Laurence L, Leach L, Linge LC, Firth JA, Clark P (2004) Distinct patterns of in vitro angiogenic behaviour of human microvascular endothelial cells are determined by extracellular matrices. Endothelium 11, 151-167.
25. Ejaz S, Chekarova I, Ejaz A, Sohail A, Lim CW (2008) Importance of pericytes and mechanisms of pericyte loss during diabetes retinopathy. Diabetes Obes Metab 10, 53-63.
26. Ericsson A, Säljö K, Sjöstrand E, et al. (2007) Brief hyperglycaemia in the early pregnant rat increases fetal weight at term by stimulating placental growth and affecting placental nutrient transport. J Physiol 581, 1323-1332.
27. Escudero C, Sobrevia L (2008) A hypothesis for preeclampsia: Adenosine and inducible nitric oxide synthase in human placental microvascular endothelium. Placenta 29, 469-483.
28. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W (1998) Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 111, 1853-1865.
29. Ettelaie C, Su S, Li C, Collier ME (2008) Tissue factor-containing microparticles released from mesangial cells in response to high glucose and AGE induce tube formation in microvascular cells. Microvasc Res 76, 152-160.
30. Ferrara N (2002) Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis: Therapeutic implications. Semin Oncol 29, 10-14.
31. Ferrara N (2004) Vascular endothelial growth factor: Basic science and clinical progress. Endocr Rev 25, 581-611.
32. Forster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130, 55-70.
33. Gabbay, KH (1973) The sorbitol pathway and the complications of diabetes. N Engl J Med 288, 831-836.
34. Ghiso N, Rohan RM, Amano S, Garland R, Adamis AP (1999) Suppression of hypoxia-associated vascular endothelial growth factor gene expression by nitric oxide via cGMP. Invest Ophthalmol Vis Sci 40, 1033-1039.
35. Giebel SJ, Menicucci G, McGuire PG, Das A (2005) Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest 85, 597-607.
36. Harhaj NS, Felinski EA, Wolpert EB, Sundstrom JM, Gardner TW, Antonetti DA (2006) VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest Ophthalmol Vis Sci 47, 5106-5115.
37. Hiden U, Glitzner E, Hartmann M, Desoye G (2009) Insulin and the IGF system in the human placenta of normal and diabetic pregnancies. J Anat (in press).
38. Ido Y, Williamson JR (1997) Hyperglycemic cytosolic reductive stress 'pseudohypoxia': Implications for diabetic retinopathy. Invest Ophthalmol Vis Sci 38, 1467-1470.
39. Ido Y, Chang K, Williamson JR (2004) NADH augments blood flow in physiologically activated retina and visual cortex. Proc Natl Acad Sci USA 101, 653-658.
40. Inoguchi T, Battan R, Handler E, Sportsman JR, Heath W, King GL (1992) Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc Natl Acad Sci USA 89, 11059-11063.
41. Jansson T, Cetin I, Powell TL, et al. (2006) Placental transport and metabolism in fetal overgrowth - a workshop report. Placenta 27, S109-113.
42. Jauniaux E, Burton GJ (2006) Villous histomorphometry and placental bed biopsy investigation in Type I diabetic pregnancies. Placenta 27, 468-474.
43. Kario K, Matsuo T, Kobayashi H, Matsuo M, Sakata T, Miyata T (1995) Activation of tissue factor-induced coagulation and endothelial cell dysfunction in non-insulin-dependent diabetic patients with microalbuminuria. Arterioscler Thromb Vasc Biol 15, 1114-1120.
44. Kelly DJ, Buck D, Cox AJ, Zhang Y, Gilbert RE (2007) Effects on protein kinase C-beta inhibition on glomerular vascular endothelial growth factor expression and endothelial cells in advanced experimental diabetic nephropathy. Am J Physiol Renal Physiol 293, F565-574.
45. Konishi H, Nakatsuka M, Chekir C, et al. (2004) Advanced glycation end products induce secretion of chemokines and apoptosis in human first trimester trophoblasts. Hum Reprod 19, 2156-2162.
46. Kuboki K, Jiang ZY, Takahara N, et al. (2000) Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo. A specific vascular action of insulin. Circulation 101, 676-681.
47. Kwaan HC (1992) Changes in blood coagulation, platelet function, and plasminogen-plasmin system in diabetes. Diabetes 41, 32-35.
48. Lampugnani MG, Resnati M, Raiteri M, et al. (1992) A novel-endothelial specific membrane protein is a marker of cell-cell contacts. J Cell Biol 118, 1511-1522.
49. Lappas M, Permezel M, Rice GE (2007) Advanced glycation endproducts mediate pro-inflammatory actions in human gestational tissues via nuclear factor-κB and extracellular signal-regulated kinase 1/2. J Endocrinol 193, 269-277.
50. Leach L, Firth JA (1992) Fine structure of the paracellular junctions of terminal villous capillaries in the perfused human placenta. Cell Tissue Res 268, 447-452.
51. Leach L, Eaton BM, Westcott EDA, Firth JA (1995) The effects of histamine on endothelial permeability, structure and adhesion molecules of the paracellular junctional complexes of perfused term human placental microvessels. Microvasc Res 50, 323-337.
52. Leach L, Lammiman MJ, Babawale MO, et al. (2000) Molecular organisation of tight and adherens junctions in the human placental vascular tree. Placenta 21, 547-557.
53. Leach L, Babawale MO, Anderson M, Lammiman M (2002) Vasculogenesis, angiogenesis and the molecular organisation of endothelial junctions in the early human placenta. J Vasc Res 39, 246-259.
54. Leach L, Gray C, Staton S, et al. (2004) Vascular endothelial cadherin and β-catenin in human fetoplacental vessels of pregnancies complicated by Type 1 diabetes: Associations with angiogenesis and perturbed barrier function. Diabetologia 47, 695-709.
55. Lee IG, Chae SL, Kim JC (2006) Involvement of circulating endothelial progenitor cells and vasculogenic factors in the pathogenesis of diabetic retinopathy. Eye 20, 546-552.
56. Liu F, Xia M, Xu A (2008) Expression of VEGF, iNOS, and eNOS is increased in cochlea of diabetic rat. Acta Otolaryngol 128, 1178-1186.
57. Lucas J, Thomas R, Ikram A, Leach L (2008) The effect of fetal hyperinsulemia on human placental vascular function: Perfusion of fetal microvascular bed results in increased vascular leakage and loss of junctional beta-catenin. Microcirculation 15, 672-673.
58. Lyall F, Gibson JL, Greer IA, Brockman DE, Eis AL, Myatt L (1998) Increased nitrotyrosine in the diabetic placenta: Evidence for oxidative stress. Diabetes Care 21, 1753-1758.
59. Mayhew, TM (2002) Enhanced fetoplacental angiogenesis in pre-gestational diabetes mellitus: The extra growth is exclusively longitudinal and not accompanied by microvascular remodelling. Diabetologia 45, 1434-1439.
60. Navaratna D, McGuire PG, Menicucci G, Das A (2007) Proteolytic degradation of VE-cadherin alters the blood-retinal barrier in diabetes. Diabetes 56, 2380-2387.
61. Nishikawa T, Edelstein D, Du XL, et al. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404, 787-790.
62. Nold JL, Georgieff MK (2004) Infants of diabetic mothers. Pediatr Clin North Am 51, 619-637.
63. Parenti A, Morbidelli L, Cui XL, et al. (1998) Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase1/2 activation in postcapillary endothelium. J Biol Chem 273, 4220-4226.
64. Poulaki V, Qin WY, Joussen AM, et al. (2002) Acute intensive insulin therapy exacerbates diabetic blood-retinal barrier breakdown via hypoxia-inducible factor-l alpha and VEGF. J Clin Invest 109, 805-815.
65. Pugliese G, Tilton RG, Williamson JR (1991) Glucose-induced metabolic imbalances in the pathogenesis of diabetic vascular disease. Diabetes Metab Rev 7, 35-59.
66. Rutland CS, Latunde-Dada AO, Thorpe A, Plant R, Langley-Evans S, Leach L (2007) Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta 28, 734-742.
67. Schneeberger EE, Lynch RD (2004) The tight junction: A multifunctional complex. Am J Physiol Cell Physiol 286, C1213-1228.
68. Shiba T, Inoguchi T, Sportsman JR, Heath WF, Bursell S, King GL (1993) Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am J Physiol 265, E783-793.
69. Singh VP, Le B, Khode R, Baker KM, Kumar R (2008) Intracellular angiotensin II production in diabetic rats is correlated with cardiomyocyte apoptosis, oxidative stress, and cardiac fibrosis. Diabetes 57, 3297-3306.
70. Sosenko IR, Kitzmiller JL, Loo SW, Blix P, Rubenstein AH, Gabbay KH (1979) The infant of the diabetic mother: Correlation of increased cord C-peptide levels with macrosomia and hypoglycemia N Engl J Med 301, 859-862.
71. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986) Identification of ZO-1: A high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103, 755-766.
72. Stitt AW, Moore JE, Sharkey JA, et al. (1998) Advanced glycation end products in vitreous: Structural and functional implications for diabetic vitreopathy. Invest Ophthalmol Vis Sci 39, 2517-2523.
73. Sung SH, Ziyadeh FN, Wang A, Pyagay PE, Kanwar YS, Chen S (2006) Blockade of vascular endothelial growth factor signaling ameliorates diabetic albuminuria in mice. J Am Soc Nephrol 17, 3093-3104.
74. Sweet IR, Gilbert M, Maloney E, Hockenbery DM, Schwartz MW, Kim F (2009) Endothelial inflammation induced by excess glucose is associated with cytosolic glucose 6-phosphate but not increased mitochondrial respiration. Diabetologia 52, 921-931.
75. Teasdale F (1983) Histomorphometry of the human placenta in class B diabetes mellitus. Placenta 4, 1-12.
76. Thornalley P, Wolff S, Crabbe J, Stern A (1984) The autoxidation of glyceraldehyde and other simple monosaccharides under physiological conditions catalysed by buffer ions. Biochim Biophys Acta 797, 276-287.
77. Tilton RG, Kawamura T, Chang KC, et al. (1997) Vascular dysfunction induced by elevated glucose levels in rats is mediated by vascular endothelial growth factor. J Clin Invest 99, 2192-2202.
78. Tsukita S, Furuse M (1999) Occludin and claudins in tight-junction strands: Leading or supporting players? Trends Cell Biol 9, 268-273.
79. Vareniuk I, Pavlov IA, Obrosova IG (2008) Inducible nitric oxide synthase gene deficiency counteracts multiple manifestations of peripheral neuropathy in a streptozotocin-induced mouse model of diabetes. Diabetologia 51, 2126-2133.
80. Vestweber D (2008) VE-cadherin. The major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Throm Vasc Biol 28, 223.
81. Wright TJ, Leach L, Jones P (2002) Dynamics of vascular endothelial-cadherin and β-catenin localisation by vascular endothelial growth factor-induced angiogenesis in human umbilical vein cells. Exp Cell Res 280, 159-168.
82. Xia L, Wang H, Munk S, et al. (2007) Reactive oxygen species, PKC-beta1, and PKC-zeta mediate high-glucose-induced vascular endothelial growth factor expression in mesangial cells. Am J Physiol Endocrinol Metab 293, E1280-1288.
83. Yan SD, Schmidt AM, Anderson GM, et al. (1994) Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 269, 9889-9897.
84. Yang Z, Laubach VE, French BA, Kron IL (2009) Acute hyperglycemia enhances oxidative stress and exacerbates myocardial infarction by activating nicotinamide adenine dinucleotide phosphate oxidase during reperfusion. J Thorac Cardiovasc Surg 137, 723-729.
85. Ziche M, Morbidelli L, Choudhuri R, et al. (1997) Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99, 2625-2634.