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

Volumn 47, Issue 4, 2004, Pages 695-709

  Leach, L ^a   Gray, C ^a   Staton, S ^a   Babawale, M O ^a   Gruchy, A ^a   Foster, C ^a   Mayhew, T M ^a   James, D K ^b  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

catenin; Angiogenesis; Diabetes; Endothelium; Placenta; Tracer leakage; Vascular endothelial cadherin; Vascular endothelial growth factor

Indexed keywords

BETA CATENIN; CADHERIN; DEXTRAN DERIVATIVE; PHOSPHOTYROSINE; TRACER; VASCULOTROPIN;

ANGIOGENESIS; ANTIBODY LABELING; ARTICLE; BIRTH WEIGHT; BLOOD PLACENTA BARRIER; CELL PROLIFERATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DISEASE DURATION; FEMALE; FETOPLACENTAL UNIT; FLUORESCENCE MICROSCOPY; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INSULIN DEPENDENT DIABETES MELLITUS; MICROSCOPY; MICROVASCULATURE; PLACENTA LOCALIZATION; PLACENTA PERFUSION; PLACENTA VILLUS; PLACENTA WEIGHT; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STEREOMETRY; TROPHOBLAST; VASCULAR ENDOTHELIUM;

ADULT; BETA CATENIN; BLOOD GLUCOSE; BLOTTING, WESTERN; CADHERINS; CAPILLARY PERMEABILITY; CYTOSKELETAL PROTEINS; DIABETES MELLITUS, TYPE 1; DIABETIC ANGIOPATHIES; ENDOTHELIUM, VASCULAR; FEMALE; FETUS; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; HUMANS; INFANT, NEWBORN; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PLACENTA; PREGNANCY; PREGNANCY IN DIABETICS; PREGNANCY OUTCOME; REGIONAL BLOOD FLOW; TRANS-ACTIVATORS;

EID: 2442667946     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-004-1341-7     Document Type: Article

References (49)

1. Benirschke K, Kaufmann P (2000) Pathology of the human placenta, 4th edn. Springer, New York
2. Mayhew TM (2002) Fetoplacental angiogenesis during gestation is biphasic, longitudinal and occurs by proliferation and remodelling of vascular endothelial cells. Placenta 23:742-750
3. Teasdale F (1983) Histomorphometry of the human placenta in class B diabetes mellitus. Placenta 4:1-12
4. 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
5. Mayhew TM, Sørensen FB, Klebe JG, Jackson MR (1994) Growth and maturation of villi in placentae from well-controlled diabetic women. Placenta 15:57-65
6. Sander B, Larsen M, Engler C, Lund-Andersen H, Parving HH (1994) Early changes in diabetic retinopathy: capillary loss and blood-retina barrier permeability in relation to metabolic control. Acta Ophthalmol 72:553-559
7. Dejana E (1996) Endothelial adherens junctions: Implications in the control of vascular permeability and angiogenesis. J Clin Invest 98:1949-1953
8. Carmeliet P, Lampugnani MG, Moons L et al. (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147-157
9. Carmeliet P, Collen D (2000) Molecular basis of angiogenesis. Role of VEGF and VE-cadherin. Ann NY Acad Sci 902:249-262
10. 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 3:246-259
11. Leach L, Lammiman MJ, Babawale MO et al. (2000) Molecular organization of tight and adherens junctions in the human placental vascular tree. Placenta 21:547-557
12. Leach L, Eaton BM, Westcott EDA, Firth JA (1995) Effect of histamine on endothelial permeability and structure and adhesion molecules of the paracellular junctions of perfused human term placental microvessels. Microvasc Res 50:323-337
13. Wright TJ, Leach L, Shaw PE, 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
14. Ilan N, Tucker A, Madri JA (2003) Vascular endothelial growth factor expression, β-catenin tyrosine phosphorylation, and endothelial proliferative behaviour: a pathway for transformation? Lab Invest 83:1105-1115
15. 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
16. Kevil CG, Payne DK, Mire E, Alexander JS (1998) Vascular permeability factor/vascular endothelial cell growth factor- mediated permeability occurs through disorganization of endothelial junctional proteins. J Biol Chem 273:15099-15103
17. Antonetti DA, Barber AJ, Khin SK, Lieth E, Tarbell JM, Gardner TW (1998) Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content. Diabetes 47:1953-1959
18. Gottardi CJ, Gumbiner BM (2001) Adhesion signaling: how β-catenin interacts with its partners. Curr Biol 11:792-794
19. Liu C, Li Y, Semenov M et al. (2002) Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837-847
20. Gory-Faure S, Prandini MH, Pointu H et al. (1999) Role of vascular endothelial cadherin in vascular morphogenesis. Development 126:2093-2102
21. Conacci-Sorrell M, Zhurinsky J, Ben-Ze'ev A (2002) The cadherin-catenin adhesion system in signaling and cancer. J Clin Invest 109:987-991
22. Lampugnani MG, Zanetti A, Corada M et al. (2003) Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, β-catenin, and the phosphatase DEP-1/CD148. J Cell Biol 161:793-804
23. Babawale MO, Lovat S, Mayhew TM, Lammiman MJ, James DK, Leach L (2000) Effects of gestational diabetes on junctional adhesion molecules in human term placental vasculature. Diabetologia 43:1185-1196
24. Eaton BM, Leach L, Firth JA (1993) Permeability of perfused term human placental microvessels. J Physiol 463:141-155
25. Gardosi J (1997) Customized growth curves. Clin Obstet Gynecol 40:715-722
26. 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
27. Sasaki K, Kurose A, Ishida Y, Matsuta M (1994) Estimation of S-phase fraction in tumour tissue sections by immunohistochemical staining if PCNA. J Histochem Cytochem 42:957-960
28. Mayhew TM (1997) Recent applications of the new stereology have thrown fresh light on how the human placenta grows and develops its form. J Microsc 186:155-163
29. Gundersen HJG, Jensen E (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263
30. Guo M, Wu M, Granger HJ, Yuan SY (2004) Transference of recombinant VE-cadherin cytoplasmic domain alters endothelial junctional integrity and microvascular permeability. J Physiol 554:78-88
31. Gao X, Kouklis P, Xu N et al. (2000) Reversibility of increased microvessel permeability in response to VE-cadherin disassembly. Am J Physiol Lung Cell Mol Physiol 279:L1218-L1225
32. Biswas P, Canosa S, Schoenfeld J, Schoenfeld D, Tucker A, Madri JA (2003) PECAM-1 promotes β-catenin accumulation and stimulates endothelial cell proliferation. Biochem Biophys Res Commun 303:212-218
33. Hilsted J, Christensen NJ (1992) Dual effect of insulin on plasma volume and transcapillary albumin transport. Diabetologia 35:99-103
34. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9:669-676
35. Dor Y, Porat R, Keshet E (2001) Vascular endothelial growth factor and vascular adjustments to perturbation in oxygen hemostasis. Am J Physiol Cell Physiol 280:C1367-C1374
36. Caro J, Erslev AJ, Silver R, Miller O, Birgegard G (1982) Erythropoietin production in response to anemia or hypoxia in the newborn rat. Blood 60:984-988
37. Costa-Giomi P, Caro J, Weinmann R (1990) Enhancement by hypoxia of human erythropoietin gene transcription in vitro. J Biol Chem 265:10185-10188
38. Mayhew TM, Charnock-Jones DS, Kaufmann P (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis III. Changes in complicated pregnancies. Placenta 25:127-129
39. Zhang ZG, Zhang L, Jiang Q et al. (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106:829-838
40. Thurston G (2002) Complementary actions of VEGF and angiopoetin-1 on blood vessel growth and leakage. J Anat 200:575-580
41. Bates DO, Hillman NJ, Pocok TM, Neal CR (2002) Regulation of microvascular permeability by vascular endothelial growth factors. J Anat 200:581-597
42. Glover V, Leach L (2003) Perfusion of human placental vessels with VEGF: Effect on leakage of 76 kDa dextran and junctional organisation. J Vasc Res 40:306 (Abstract)
43. Helske S, Vuorela P, Carpen O, Hornig C, Weich H, Halmesmaki E (2001) Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentas from normal and complicated pregnancies. Mol Hum Reprod 7:205-210
44. Ward BJ, Bauman KF, Firth JA (1988) Interendothelial junctions of cardiac capillaries in rats: their structure and permeability properties. Cell Tissue Res 252:57-66
45. Wong RK, Baldwin AL, Heimark RL (1999) Cadherin-5 redistribution at sites of TNF-alpha and IFN-gamma-induced permeability in mesenteric venules. Am J Physiol 276:H736-H748
46. McDonald DM (1994) Endothelial gaps and permeability of venules in rat tracheas exposed to inflammatory stimuli. Am J Physiol 266:L61-L83
47. Dvorak AM, Kohn S, Morgan ES, Fox P, Nagy JA, Dvorak HF (1996) The vesiculo-vacuolar organelle (VVO): a distinct endothelial cell structure that provides a transcellular pathway for macromolecular extravasation. J Leukoc Biol 59:100-115
48. Teasdale F (1985) Histomorphometry of the human placenta in class C diabetes mellitus. Placenta 6:69-82
49. Jirkovska M, Kubinova L, Janacek J, Moravcova M, Krejci V, Karen P (2002) Topological properties and spatial organization of villous capillaries in normal and diabetic placentas. J Vasc Res 39:268-278