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Disease Markers
Volume 2016, Article ID 7124186, 13 pages
http://dx.doi.org/10.1155/2016/7124186
Research Article

Increased Umbilical Cord PAI-1 Levels in Placental Insufficiency Are Associated with Fetal Hypoxia and Angiogenesis

1Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030, USA
2Children’s Health Research Institute, Departments of Biochemistry and Pediatrics, University of Western Ontario, London, ON, Canada N6C 2V5

Received 22 September 2015; Revised 12 December 2015; Accepted 16 December 2015

Academic Editor: Irene Rebelo

Copyright © 2016 Maxim D. Seferovic and Madhulika B. Gupta. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. J. P. Barker, C. Osmond, J. Golding, D. Kuh, and M. E. J. Wadsworth, “Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease,” British Medical Journal, vol. 298, no. 6673, pp. 564–567, 1989. View at Publisher · View at Google Scholar · View at Scopus
  2. D. J. P. Barker, C. Osmond, P. D. Winter, B. Margetts, and S. J. Simmonds, “Weight in infancy and death from ischaemic heart disease,” The Lancet, vol. 334, no. 8663, pp. 577–580, 1989. View at Publisher · View at Google Scholar · View at Scopus
  3. D. J. P. Barker, C. N. Martyn, C. Osmond, C. N. Hales, and C. H. D. Fall, “Growth in utero and serum cholesterol concentrations in adult life,” British Medical Journal, vol. 307, no. 6918, pp. 1524–1527, 1993. View at Publisher · View at Google Scholar · View at Scopus
  4. L. A. Joss-Moore, Y. Wang, M. S. Campbell et al., “Uteroplacental insufficiency increases visceral adiposity and visceral adipose PPARgamma2 expression in male rat offspring prior to the onset of obesity,” Early Human Development, vol. 86, no. 3, pp. 179–185, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. M. D. Seferovic, D. M. Goodspeed, D. M. Chu et al., “Heritable IUGR and adult metabolic syndrome are reversible and associated with alterations in the metabolome following dietary supplementation of 1-carbon intermediates,” The FASEB Journal, vol. 29, no. 6, pp. 2640–2652, 2015. View at Publisher · View at Google Scholar
  6. T. M. Mayhew, D. S. Charnock-Jones, and P. Kaufmann, “Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies,” Placenta, vol. 25, no. 2-3, pp. 127–139, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Basu, G. Menicucci, J. Maestas, A. Das, and P. McGuire, “Plasminogen activator inhibitor-1 (PAI-1) facilitates retinal angiogenesis in a model of oxygen-induced retinopathy,” Investigative Ophthalmology and Visual Science, vol. 50, no. 10, pp. 4974–4981, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Bajou, A. Noël, R. D. Gerard et al., “Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization,” Nature Medicine, vol. 4, no. 8, pp. 923–928, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Bajou, C. Maillard, M. Jost et al., “Host-derived plasminogen activator inhibitor-1 (PAI-1) concentration is critical for in vivo tumoral angiogenesis and growth,” Oncogene, vol. 23, no. 41, pp. 6986–6990, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. G. A. McMahon, E. Petitclerc, S. Stefansson et al., “Plasminogen activator inhibitor-1 regulates tumor growth and angiogenesis,” The Journal of Biological Chemistry, vol. 276, no. 36, pp. 33964–33968, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Almholt, B. S. Nielsen, T. L. Frandsen, N. Brünner, K. Danø, and M. Johnsen, “Metastasis of transgenic breast cancer in plasminogen activator inhibitor-1 gene-deficient mice,” Oncogene, vol. 22, no. 28, pp. 4389–4397, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Annecke, M. Schmitt, U. Euler et al., “uPA and PAI-1 in breast cancer: review of their clinical utility and current validation in the prospective NNBC-3 trial,” Advances in Clinical Chemistry, vol. 45, pp. 31–45, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. M. J. Duffy, “Urokinase plasminogen activator and its inhibitor, PAI-1, as prognostic markers in breast cancer: from pilot to level 1 evidence studies,” Clinical Chemistry, vol. 48, no. 8, pp. 1194–1197, 2002. View at Google Scholar · View at Scopus
  14. N. Harbeck, R. E. Kates, and M. Schmitt, “Clinical relevance of invasion factors urokinase-type plasminogen activator and plasminogen activator inhibitor type 1 for individualized therapy decisions in primary breast cancer is greatest when used in combination,” Journal of Clinical Oncology, vol. 20, no. 4, pp. 1000–1007, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. M. D. Sternlicht, A. M. Dunning, D. H. Moore et al., “Prognostic value of PAI1 in invasive breast cancer: evidence that tumor-specific factors are more important than genetic variation in regulating PAI1 expression,” Cancer Epidemiology Biomarkers and Prevention, vol. 15, no. 11, pp. 2107–2114, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. M. S. Pepper, N. Ferrara, L. Orci, and R. Montesano, “Vascular endothelial growth factor (VEGF) induces plasminogen activators and plasminogen activator inhibitor-1 in microvascular endothelial cells,” Biochemical and Biophysical Research Communications, vol. 181, no. 2, pp. 902–906, 1991. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Estellés, J. Gilabert, M. Keeton et al., “Altered expression of plasminogen activator inhibitor type 1 in placentas from pregnant women with preeclampsia and/or intrauterine fetal growth retardation,” Blood, vol. 84, no. 1, pp. 143–150, 1994. View at Google Scholar · View at Scopus
  18. B. J. Hunt, H. Missfelder-Lobos, M. Parra-Cordero et al., “Pregnancy outcome and fibrinolytic, endothelial and coagulation markers in women undergoing uterine artery Doppler screening at 23 weeks,” Journal of Thrombosis and Haemostasis, vol. 7, no. 6, pp. 955–961, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Bellart, R. Gilabert, J. Fontcuberta, E. Carreras, R. M. Miralles, and L. Cabero, “Coagulation and fibrinolytic parameters in normal pregnancy and in pregnancy complicated by intrauterine growth retardation,” American Journal of Perinatology, vol. 15, no. 2, pp. 81–85, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Boutsikou, G. Mastorakos, M. Kyriakakou et al., “Circulating levels of inflammatory markers in intrauterine growth restriction,” Mediators of Inflammation, vol. 2010, Article ID 790605, 7 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Villar, G. Carroli, D. Wojdyla et al., “Preeclampsia, gestational hypertension and intrauterine growth restriction, related or independent conditions?” American Journal of Obstetrics and Gynecology, vol. 194, no. 4, pp. 921–931, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Chinni, D. Colaizzo, G. L. Tiscia et al., “Markers of haemostasis and angiogenesis in placentae from gestational vascular complications: impairment of mechanisms involved in maintaining intervillous blood flow,” Thrombosis Research, vol. 125, no. 3, pp. 267–271, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Estellés, J. Gilabert, S. Grancha et al., “Abnormal expression of type 1 plasminogen activator inhibitor and tissue factor in severe preeclampsia,” Thrombosis and Haemostasis, vol. 79, no. 3, pp. 500–508, 1998. View at Google Scholar · View at Scopus
  24. D. S. Charnock-Jones, P. Kaufmann, and T. M. Mayhew, “Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation,” Placenta, vol. 25, no. 2-3, pp. 103–113, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Zygmunt, F. Herr, K. Münstedt, U. Lang, and O. D. Liang, “Angiogenesis and vasculogenesis in pregnancy,” European Journal of Obstetrics Gynecology & Reproductive Biology, vol. 110, supplement, pp. S10–S18, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. P. H. Andraweera, G. A. Dekker, J. A. Laurence, and C. T. Roberts, “Placental expression of VEGF family mRNA in adverse pregnancy outcomes,” Placenta, vol. 33, no. 6, pp. 467–472, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Barut, A. Barut, B. D. Gun et al., “Intrauterine growth restriction and placental angiogenesis,” Diagnostic Pathology, vol. 5, article 24, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. T. R. H. Regnault, H. L. Galan, T. A. Parker, and R. V. Anthony, “Placental development in normal and compromised pregnancies—a review,” Placenta, vol. 23, supplement A, pp. S119–S129, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. T. R. H. Regnault, B. de Vrijer, H. L. Galan et al., “The relationship between transplacental O2 diffusion and placental expression of PlGF, VEGF and their receptors in a placental insufficiency model of fetal growth restriction,” The Journal of Physiology, vol. 550, no. 2, pp. 641–656, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Fink, A. Kazlauskas, L. Poellinger, P. Ebbesen, and V. Zachar, “Identification of a tightly regulated hypoxia-response element in the promoter of human plasminogen activator inhibitor-1,” Blood, vol. 99, no. 6, pp. 2077–2083, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. T. E. Arbuckle, R. Wilkins, and G. J. Sherman, “Birth weight percentiles by gestational age in Canada,” Obstetrics & Gynecology, vol. 81, no. 1, pp. 39–48, 1993. View at Google Scholar · View at Scopus
  32. M. D. Seferovic, S. Chen, D. M. Pinto, and M. B. Gupta, “Altered liver secretion of vascular regulatory proteins in hypoxic pregnancies stimulate angiogenesis in vitro,” Journal of Proteome Research, vol. 10, no. 4, pp. 1495–1504, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. D. J. Hill, G. J. M. Tevaarwerk, E. Arany et al., “Fibroblast growth factor-2 (FGF-2) is present in maternal and cord serum, and in the mother is associated with a binding protein immunologically related to the FGF receptor-1,” Journal of Clinical Endocrinology and Metabolism, vol. 80, no. 6, pp. 1822–1831, 1995. View at Google Scholar · View at Scopus
  34. D. Donovan, N. J. Brown, E. T. Bishop, and C. E. Lewis, “Comparison of three in vitro human ‘angiogenesis’ assays with capillaries formed in vivo,” Angiogenesis, vol. 4, no. 2, pp. 113–121, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Nodwell, L. Carmichael, M. Ross, and B. Richardson, “Placental compared with umbilical cord blood to assess fetal blood gas and acid-base status,” Obstetrics and Gynecology, vol. 105, no. 1, pp. 129–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. V. H. Shore, T.-H. Wang, C.-L. Wang, R. J. Torry, M. R. Caudle, and D. S. Torry, “Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast,” Placenta, vol. 18, no. 8, pp. 657–665, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Khaliq, C. Dunk, J. Jiang et al., “Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for ‘placental hyperoxia’ in intrauterine growth restriction,” Laboratory Investigation, vol. 79, no. 2, pp. 151–170, 1999. View at Google Scholar · View at Scopus
  38. A. Malamitsi-Puchner, T. Boutsikou, E. Economou et al., “Vascular endothelial growth factor and placenta growth factor in intrauterine growth-restricted fetuses and neonates,” Mediators of Inflammation, vol. 2005, no. 5, pp. 293–297, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Ahmed and M. D. Kilby, “Hypoxia or hyperoxia in placental insufficiency?” The Lancet, vol. 350, no. 9081, pp. 826–827, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. J. C. P. Kingdom and P. Kaufmann, “Oxygen and placental villous development: origins of fetal hypoxia,” Placenta, vol. 18, no. 8, pp. 613–616, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Ahmed, X. F. Li, C. Dunk, M. J. Whittle, D. I. Rushton, and T. Rollason, “Colocalisation of vascular endothelial growth factor and its flt-1 receptor in human placenta,” Growth Factors, vol. 12, no. 3, pp. 235–243, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. A. M. Sharkey, D. S. Charnock-Jones, C. A. Boocock, K. D. Brown, and S. K. Smith, “Expression of mRNA for vascular endothelial growth factor in human placenta,” Journal of Reproduction and Fertility, vol. 99, no. 2, pp. 609–615, 1993. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Vuorela, E. Hatva, A. Lymboussaki et al., “Expression of vascular endothelial growth factor and placenta growth factor in human placenta,” Biology of Reproduction, vol. 56, no. 2, pp. 489–494, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Olofsson, E. Korpelainen, M. S. Pepper et al., “Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 20, pp. 11709–11714, 1998. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Bajou, V. Masson, R. D. Gerard et al., “The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic strategies,” The Journal of Cell Biology, vol. 152, no. 4, pp. 777–784, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Stefansson and D. A. Lawrence, “The serpin PAI-1 inhibits cell migration by blocking integrin αvβ3 binding to vitronectin,” Nature, vol. 383, no. 6599, pp. 441–443, 1996. View at Publisher · View at Google Scholar
  47. S. Labied, S. Blacher, P. Carmeliet et al., “Transient reduction of placental angiogenesis in PAI-1-deficient mice,” Physiological Genomics, vol. 43, no. 4, pp. 188–198, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Ferroni, M. Roselli, I. Portarena et al., “Plasma plasminogen activator inhibitor-1 (PAI-1) levels in breast cancer—relationship with clinical outcome,” Anticancer Research, vol. 34, no. 3, pp. 1153–1161, 2014. View at Google Scholar · View at Scopus
  49. B. P. Schneider and K. D. Miller, “Angiogenesis of breast cancer,” Journal of Clinical Oncology, vol. 23, no. 8, pp. 1782–1790, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Krebs, L. M. Macara, R. Leiser, A. W. Bowman, I. A. Greer, and J. C. P. Kingdom, “Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree,” American Journal of Obstetrics and Gynecology, vol. 175, no. 6, pp. 1534–1542, 1996. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Macara, J. C. P. Kingdom, P. Kaufmann et al., “Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms,” Placenta, vol. 17, no. 1, pp. 37–48, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Kaufmann, T. M. Mayhew, and D. S. Charnock-Jones, “Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy,” Placenta, vol. 25, no. 2-3, pp. 114–126, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. J. I. Jones, W. H. Busby Jr., G. Wright, C. E. Smith, N. M. Kimack, and D. R. Clemmons, “Identification of the sites of phosphorylation in insulin-like growth factor binding protein-1. Regulation of its affinity by phosphorylation of serine 101,” The Journal of Biological Chemistry, vol. 268, no. 2, pp. 1125–1131, 1993. View at Google Scholar · View at Scopus
  54. M. D. Seferovic, R. Ali, H. Kamei et al., “Hypoxia and leucine deprivation induce human insulin-like growth factor binding protein-1 hyperphosphorylation and increase its biological activity,” Endocrinology, vol. 150, no. 1, pp. 220–231, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. C. S. Watson, P. Bialek, M. Anzo, J. Khosravi, S.-P. P. Yee, and V. K. M. Han, “Elevated circulating insulin-like growth factor binding protein-1 is sufficient to cause fetal growth restriction,” Endocrinology, vol. 147, no. 3, pp. 1175–1186, 2013. View at Publisher · View at Google Scholar · View at Scopus