Effect of impaired glucose tolerance during pregnancy on the expression of VEGF receptors in human placenta

Reproduction, Fertility and Development

Volumn 20, Issue 7, 2008, Pages 789-801

  Marini, M ^a   Vichi, D ^a   Toscano, A ^a   Thyrion, G D Zappoli ^a   Bonaccini, L ^a   Parretti, E ^a   Gheri, G ^a   Pacini, A ^a   Sgambati, E ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; PREGNANCY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA; TROPHOBLAST; WESTERN BLOTTING;

ADULT; BASE SEQUENCE; CASE-CONTROL STUDIES; DIABETES, GESTATIONAL; DNA PRIMERS; FEMALE; GENE EXPRESSION; GLUCOSE INTOLERANCE; HUMANS; IMMUNOHISTOCHEMISTRY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 51949116916     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD08032     Document Type: Article

References (67)

1. Babawale, M. O., Lovat, S., Mayhew, T. M., Lammiman, M. J., James, D. K., and Leach, L. (2000). Effects of gestational diabetes on junctional adhesion molecules in human term placental vasculature. Diabetologia 43, 1185-1196. doi:10.1007/S001250051511
2. Bajoria, R., Sooranna, S. R., Ward, B. S., and Chatterjee, R. (2002). Prospective function of placental leptin at maternal-fetal interface. Placenta 23, 103-115. doi:10.1053/PLAC.2001.0769
3. Berkus, M. D., and Langer, O. (1993). Glucose tolerance test: degree of glucose abnormality correlates with neonatal outcome. Obstet. Gynecol. 81, 344-348.
4. Biri, A., Onan, A., Devrim, E., Babacan, F., Kavutcu, M., and Durak, I. (2006). Oxidant status in maternal and cord plasma and placental tissue in gestational diabetes. Placenta 27, 327-332. doi:10.1016/J. PLACENTA.2005.01.002
5. Bradford, M. M. (1976). 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. doi:10.1016/0003-2697(76) 90527-3
6. Carpenter, M.W., and Coustan, D. R. (1982). Criteria for screening test for gestational diabetes. Am. J. Obstet. Gynecol. 144, 768-773.
7. Cetin, I., Santis, M. S., and Taricco, E. (2005). Maternal and fetal amino acid concentrations in normal pregnancies and in pregnancies with gestational diabetes mellitus. Am. J. Obstet. Gynecol. 192, 610-617. doi:10.1016/J.AJOG.2004.08.011
8. Challier, J., Galtier, M., Bintein, T., Cortez, A., Lepercq, J., and Hauguelde Mouzon, S. (2003). Placental leptin receptor isoforms in normal and pathological pregnancies. Placenta 24, 92-99. doi:10.1053/PLAC. 2002.0805
9. Chen, J., Tan, B., Karteris, E., Zervou, S., Digby, J., Hillhouse, E. W., Vatish, M., and Randeva, H. S. (2006). Secretion of adiponectin by human placenta: differential modulation of adiponectin and its receptors by cytokines. Diabetologia 49, 1292-1302. doi:10.1007/S00125-006-0194-7
10. Cheung, C. Y. (1997). Vascular endothelial growth factor: possible role in fetal development and placental function. J. Soc. Gynecol. Investig. 4, 169-177. doi:10.1016/S1071-5576(97)00025-7
11. Clark, D. E., Smith, S. K., Sharkey, A.M., and Charnock-Jones, D. S. (1996). Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum. Reprod. 11, 1090-1098.
12. Cooper, J. C., Sharkey, A. M., McLaren, J., Charnock-Jones, D. S., and Smith, S. K. (1995). Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J. Reprod. Fertil. 105, 205-213.
13. Cooper, M. E., Vranes, D., Youssef, S., Stacker, S. A., Cox, A. J., et al. (1999). Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes 48, 2229-2239. doi:10.2337/DIABETES.48.11.2229
14. Coughlan, M. T., Vervaart, P. P., Permezel, M., Georgiou, H. M., and Rice, G. E. (2004). Altered placental oxidative stress status in gestational diabetes mellitus. Placenta 25, 78-84. doi:10.1016/S0143-4004(03) 00183-8
15. Crocker, I. P., Strachan, B. K., Lash, G. E., Cooper, S., Warren, A. Y., and Baker, P. N. (2001). Vascular endothelial growth factor but not placental growth factor promotes trophoblast syncytialisation in vitro. J. Soc. Gynecol. Investig. 8, 341-346. doi:10.1016/S1071-5576(01)00134-4
16. De Vries, C., Escobedo, J., Ueno, H., Houch, K., Ferrara, N., and Williams, L. T. (1992). The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255, 989-991. doi:10.1126/SCIENCE.1312256
17. Demir, R., Kayisli, U. A., Seval, Y., Celik-Ozenci, C., Korgun, E. T., Demir-Wensten, A. Y., and Huppertz, B. (2004). Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta 25, 560-572. doi:10.1016/J.PLACENTA.2003.11.011
18. Desoye, G., Korgun, E. T., Ghaffari-Tabrizi, N., and Hahn, T. (2002). Is fetal macrosomia in adequately-controlled diabetic women the results of a placental defect? - a hypothesis. J. Matern. Fetal Neonatal Med. 11, 258-261. doi:10.1080/713605520
19. Dunk, C., and Ahmed, A. (2001). Expression of VEGF-C and activation of its receptors VEGFR-2 and VEGFR-3 in trophoblast. Histol. Histopathol. 16, 359-375.
20. Enholm, B., Jussila, L., Karkkainen, M., and Alitalo, K. (1998). Vascular endothelial growth factor-C: a growth factor for lymphatic and blood vascular endothelial cells. Trends Cardiovasc. Med. 8, 292-297. doi:10.1016/S1050-1738(98)00026-7
21. Favier, J., and Corvol, P. (2001). Physiological angiogenesis. Therapie 56, 455-463.
22. Gaither, K., Quraishi, A. N., and Illsely, N. P. (1999). Diabetes alters the expression and activity of the human placental GLUT1 glucose transporter. J. Clin. Endocrinol. Metab. 84, 695-701. doi:10.1210/JC.84.2.695
23. Garcia Carrapato, M. R. (2003). The offspring of gestational diabetes. J. Perinat. Med. 31, 5-11.
24. Gu, B., Alexander, J. S., Gu, Y., Zhang, Y., Lewis, D. F., and Wang, Y. (2006). Expression of lymphatic vascular endothelial hyaluronan receptor-1 (LYVE-1) in the human placenta. Lymphat. Res. Biol. 4, 11-17. doi:10.1089/LRB.2006.4.11
25. Hasan, R. N., Phukan, S., and Harada, S. (2003). Differential regulation of early growth response gene-1 expression by insulin and glucose in vascular endothelial cells. Arterioscler. Thromb.Vasc. Biol. 23, 988-993. doi:10.1161/01.ATV.0000071351.07784.19
26. Heinig, J., Wilhem, S., Muller, H., Breise, V., Bittorf, T., and Brock, J. (2000). Determination of cytokine mRNA-expression in term human placenta of patients with gestational hypertension, intrauterine growth retardation and gestational diabetes mellitus using polymerase chain reaction. Zentralbl. Gynakol. 122, 413-418. doi:10.1055/S-2000-10606
27. Helske, S., Vourela, P., Carpén, O., Horning, C., Weich, H., and Halmesmäki, E. (2001). Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentae from normal and complicated pregnancies. Mol. Hum. Reprod. 7, 205-210. doi:10.1093/MOLEHR/7.2.205
28. Janota, J., Pomyje, J., Toth, D., Sosna, O., Živný, J., Kuzel, D., Straňák, Z., Nečas, E., and Živný, J. H. (2003). Expression of angiopoietic factors in normal and type-I diabetes human placenta: a pilot study. Eur. J. Obstet. Gynecol. Reprod. Biol. 111, 153-156. doi:10.1016/S0301-2115(03)00204-5
29. Jansson, T., Ekstrand, J., Wennergren, M., and Powell, T. L. (2001). Placental glucose transport in gestational diabetes mellitus.Am. J. Obstet. Gynecol. 184, 111-116. doi:10.1067/MOB.2001.108075
30. Jansson, T., Ekstrand, Y., Björn, C., Wennergren, M., and Powell, T. L. (2002). Alteration in the activity of placental amino acid transporters in pregnancies complicated by diabetes. Diabetes 51, 2214-2219. doi:10.2337/DIABETES.51.7.2214
31. Jirkovská, M., Kubinová, L., Janácek, J., Moravcová, M., Krejcí, V., and Karen, P. (2002). Topological properties and spatial organization of villous capillaries in normal and diabetic placentas. J. Vasc. Res. 39, 268-278. doi:10.1159/000063692
32. Joukov, V., Pajusola, K., Kaipainen, A., Chilov, D., Lahtinen, I., Kukk, E., Saksala, O., Kalkkinen, N., and Alitalo, K. (1996). A novel vascular endothelial growth factor, VEGF-C, is the ligand for the Flt-4 receptor tyrosine kinase (VEGFR-3). EMBO J. 15, 290-298.
33. Kaufmann, R. C., McBride, P., Amankwah, K. S., and Huffman, D. G. (1992). The effect of minor degrees of glucose intolerance on the incidence of neonatal macrosomia. Obstet. Gynecol. 80, 97-101.
34. Kim, B. S., Chen, J., Weinstein, T., Noiri, E., and Goligorsky, M. S. (2002). VEGF expression in hypoxia and hyperglycaemia: reciprocal effect on branching angiogenesis in epithelial-endothelial co-cultures. J. Am. Soc. Nephrol. 13, 2027-2036. doi:10.1097/01.ASN.0000024436.00520.D8
35. King, R. G., Osmond, D. T., Brennecke, S. P., and Gude, N. M. (2003). Effect of fetal macrosomia on human placental glucose transport and utilization in insulin-treated gestational diabetes. J. Perinat. Med. 31, 475-483. doi:10.1515/JPM.2003.073
36. Kingdom, J., Huppertz, B., Seaward, G., and Kaufmann, P. (2000). Development of the placental villous tree and its consequences for fetal growth. Eur. J. Obstet. Gynecol. Reprod. Biol. 92, 35-43. doi:10.1016/S0301-2115(00)00423-1
37. Klagsbrun, M., and D'Amore, P. (1996). Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev. 7, 259-270. doi:10.1016/S1359-6101(96)00027-5
38. Lash, G. E., Cartwright, J. E., Whitley, G. S., Trew, A. J., and Baker, P. N. (1999). The effects of angiogenic growth factors on extravillous trophoblast invasion and motility. Placenta 20, 661-667. doi:10.1053/PLAC.1999.0427
39. Lea, R. G., Howe, D., Hannah, L. T., Bonneau, O., Hunter, L., and Hoggard, N. (2000). Placental leptin in normal, diabetic and fetal growth-retarded pregnancies. Mol. Hum. Reprod. 6, 763-739. doi:10.1093/MOLEHR/6.8.763
40. Madazli, R., Tuten, A., Calay, Z., Uzun, H., Uludag, S., and Ocak, V. (2008). The incidence of placental abnormalities, maternal and cord plasma malondialdehyde and vascular endothelial growth factor levels in women with gestational diabetes mellitus and nondiabetic control. Gynecol. Obstet. Invest. 65, 227-232. doi:10.1159/000113045
41. Maglione, D., Guerriero, V., Viglietto, G., Delli-Bovi, P., and Persico, M. G. (1991). Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc. Natl. Acad. Sci. USA 88, 9267-9271. doi:10.1073/PNAS.88.20.9267
42. Mayhew, T. M., and Sampson, C. (2003). Maternal diabetes mellitus is associated with altered deposition of fibrin-type fibrinoid at the villous surface in term placentae. Placenta 24, 524-531. doi:10.1053/PLAC.2002.0953
43. Moses, R. G., and Calvert, D. (1995). Pregnancy outcomes in women without gestational diabetes mellitus to the maternal glucose level. Is there a continuum of risk? Diabetes Care 18, 1527-1533. doi:10.2337/DIACARE.18.12.1527
44. Myatt, L., and Cui, X. (2004). Oxidative stress in the placenta. Histochem. Cell Biol. 122, 369-382. doi:10.1007/S00418-004-0677-X
45. Ni, Y., May, V., Braas, K., and Osol, G. (1997). Pregnancy augments uteroplacental vascular endothelial growth factor gene expression and vasodilator effects. Am. J. Physiol. 273, H938-H944.
46. Osmond, D. T. D., King, R. G., Brennecke, S. P., and Gude, N. M. (2001). Placental glucose transport and utilisation is altered at term in insulin-treated, gestational-diabetic patients. Diabetologia 44, 1133-1139. doi:10.1007/S001250100609
47. Page, N. M., Kemp, C. F., Butlin, D. J., and Lowry, P. J. (2002). Placental peptides as markers of gestational disease. Reproduction 123, 487-495. doi:10.1530/REP.0.1230487
48. Parretti, E., Carignani, L., Cioni, R., Bartoli, E., Borri, P., La Torre, P., Mecacci, F., Martini, E., Scarselli, G., and Mello, G. (2003). Sonographic evaluation of fetal growth and body composition inwomen with different degrees of normal glucose metabolism. Diabetes Care 26, 2741-2748. doi:10.2337/DIACARE.26.10.2741
49. +-ATPase activity and expression in syncytiotrophoblast plasma membrane in pregnancies complicated by diabetes. Placenta 23, 386-391. doi:10.1053/PLAC.2002.0807
50. Pietryga, M., Biczysko, W., Wender-Ozegowska, E., Brazert, J., Bieganska, E., and Biczysko, R. (2004). Ultrastructure examination of the placenta in pregnancy complicated by diabetes mellitus. Ginekol. Pol. 75, 111-118.
51. Radaelli, T., Varastehpour, A., Catalano, P., and Hauguel-de Monzon, S. (2003). Gestational diabetes induces placental genes for chronic stress and inflammatory pathways. Diabetes 52, 2951-2958. doi:10.2337/DIABETES.52.12.2951
52. Saldeen, P., Olofsson, P., and Laurini, R. N. (2002a). Signs of platelet activation, but not lipid peroxidation, in fetal blood associated with functional and structural umbilicoplacental lesions in pregnancies complicated by impaired glucose metabolism. J. Matern. Fetal Neonatal Med. 12, 165-171. doi:10.1080/713605645
53. Saldeen, P., Olofsson, P., and Laurini, R. N. (2002b). Structural, functional and circulatory placental changes associated with impaired glucose metabolism. Eur. J. Obstet. Gynecol. Reprod. Biol. 105, 136-142.
54. Sgambati, E., Marini, M., Zappoli Thyrion, G. D., Parretti, E., Mello, G., Orlando, C., Simi, L., Tricarico, C., Gheri, G., and Brizzi, E. (2004). VEGF expression in the placenta from pregnancies complicated by hypertensive disorders. BJOG 111, 564-570. doi:10.1007/S00418-007-0312-8
55. Sgambati, E., Marini, M., Vichi, D., Zappoli Thyrion, G. D., Parretti, E., Mello, G., and Gheri, G. (2007). Distribution of the glycoconjugate oligosaccharides in the human placenta from pregnancies complicated by altered glycaemia: lectin histochemistry. Histochem. Cell Biol. 128, 263-273. doi:10.1007/S00418-007-0312-8
56. Shore, V. H., Wang, T. H., Wang, C. L., Torry, R. J., Caudle, M. R., and Torry, D. S. (1997). Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 18, 657-665. doi:10.1016/S0143-4004(97)90007-2
57. Szukiewicz, D., Szukiewicz, A., Maslinska, D., Szewczyk, G., and Watroba, M. (2003). Mast cell-derived vascular endothelial growth factor (VEGF) and microvascular density in diabetic placentae. Inflamm. Res. 52(Suppl. 1), S9-S10. doi:10.1007/S000110300030
58. Taylor, C. M., Stevens, H., Anthony, F. W., and Wheeler, T. (1997). Influence of hypoxia on vascular endothelial growth factor and chorionic gonadotrophin production in the trophoblast-derived cell lines: JEG, Jar and BeWo. Placenta 18, 451-458. doi:10.1016/S0143-4004(97)80047-1
59. Terman, B. I., Dougher-Vermazen, M., Carrion, M. E., Dimitrov, D., Armellino, D. C., Gospodarowicz, D., and Böhlen, P. (1992). Identification of the KDR tyrosine kinase as a receptor for vascular endothelial growth factor. Biochem. Biophys. Res. Commun. 187, 1579-1586. doi:10.1016/0006-291X(92)90483-2
60. Thomas, A., Kaur, S., and Somville, T. (2002). Abnormal glucose screening test followed by normal glucose tolerance test and pregnancy outcome. Saudi Med. J. 23, 814-818.
61. Torry, D. S., and Torry, R. J. (1997). Angiogenesis and the expression of vascular endothelial growth factor in endometrium and placenta. Am. J. Reprod. Immunol. 37, 21-29.
62. Vuorela, P., and Halmesmäki, E. (2006). Vascular endothelial growth factor, its receptors, and the Tie receptors in the placental bed of women with preeclampsia, diabetes, and intrauterine growth retardation. Am. J. Perinatol. 23, 255-264. doi:10.1055/S-2006-939562
63. Vuorela, P., Hatva, E., Lymbaussakis, A., Kaipainen, A., Joukov, V., Persico, M. G., Alitalo, K., and Halmesmaki, E. (1997). Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol. Reprod. 56, 489-494. doi:10.1095/BIOLREPROD56.2.489
64. Yang, W. C., Su, T. H., Yang, Y. C., Chang, S. C., Chen, C. Y., and Chen, C. P. (2005). Altered perlecan expression in placental development and gestational diabetes mellitus. Placenta 26, 780-788. doi:10.1016/J.PLACENTA.2004.11.002
65. Younes, B., Baez-Giangreco, A., al-Nuaim, L., al-Hakeem, A., and Abu Talib, Z. (1996). Basement membrane thickening in the placenta from diabetic women. Pathol. Int. 46, 100-104. http://www.publish.csiro.au/ journals/rfd
66. Zhao, B., Cai, J., and Boulton, M. (2004). Expression of placenta growth factor is regulated by both VEGF and hyperglycaemia via VEGFR-2. Microvasc. Res. 68, 239-246. doi:10.1016/J.MVR.2004.07.004
67. Zygmunt, M. (2001). Placental circulation: Clinical significance. Early Pregnancy 5, 72-73.