Skip to main content

Advertisement

SpringerLink
Log in

Vascular Endothelial Growth Factor Activation of Intramembranous Absorption: A Critical Pathway for Amniotic Fluid Volume Regulation

  • Review
  • Published:
The Journal of the Society for Gynecologic Investigation: JSGI Aims and scope Submit manuscript

Abstract

Objective

The purpose of this review is to propose a critical role for vascular endothelial growth factor (VEGF) in mediating the transfer of amniotic fluid from the amniotic compartment through the fetal membranes and fetal surface of the placenta into fetal blood.

Methods

Experimental findings in humans and animal models on the action of VEGF in mediating fluid transfer are reviewed and interpreted in order to postulate a proposed mechanism for VEGF regulation of amniotic fluid absorption through the fetal membranes and placenta.

Results

Recent scientific advances suggest that up-regulation of VEGF gene expression in the amnion and chorion is associated with increased transfer of amniotic fluid into fetal blood. The possible mechanisms of action for VEGF appear to involve regulation of intramembranous blood vessel proliferation and membrane transport via passive permeation as well as nonpassive transcytotic vesicular movement of fluid.

Conclusion

Currently evolving concepts suggest that amniotic fluid volume is regulated through modulation of the rate of intramembranous absorption of amniotic fluid by both passive and nonpassive mechanisms. The permeability factor VEGF appears to be a critical regulator of amniotic fluid transport in the fetal membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Konduri GG, Fewell JE. Oligohydramnios. In: Brace RA, Ross MG, Robilliard JE, eds. Fetal and neonatal body fluids: The scientific basis for clinical practice. Perinatology Press, 1989:157–74.

    Google Scholar 

  2. Healy DL. Polyhydramnios: An alternative hypothesis. In: Brace RA, Ross MG, Robilliard JE, eds. Fetal and neonatal body fluids: The scientific basis for clinical practice. Perinatology Press, 1989:175–85.

    Google Scholar 

  3. Brace RA. Progress toward understanding the regulation of amniotic fluid volume: Water and solute fluxes in and through the fetal extraplacental membranes. Placenta 1995;16:1–18.

    Article  CAS  PubMed  Google Scholar 

  4. Gilbert WM, Brace RA. The missing link in amniotic fluid volume regulation: Intramembranous absorption. Obstet Gynecol 1989;74:748–54.

    CAS  PubMed  Google Scholar 

  5. Ross MG, Brace RA. Amniotic fluid biology—basic and clinical aspects. J Matern Fetal Med 2001;10:2–109.

    Article  CAS  PubMed  Google Scholar 

  6. Gilbert WM, Brace RA. Novel determination of filtration coefficient of ovine placenta and intramembranous pathway. Am J Physiol 1990;259:R1281–8.

    CAS  PubMed  Google Scholar 

  7. Jang PR, Brace RA. Amniotic fluid composition changes during urine drainage and tracheoesophageal occlusion in fetal sheep. Am J Obstet Gynecol 1992;167:1732–41.

    Article  CAS  PubMed  Google Scholar 

  8. Matsumoto LC, Cheung CY, Brace RA. Effect of esophageal ligation on amniotic fluid volume and urinary flow rate in fetal sheep. Am J Obstet Gynecol 2000;182:699–705.

    Article  CAS  PubMed  Google Scholar 

  9. Faber JJ, Anderson DF. Regulatory response of intramembranous absorption of amniotic fluid to infusion of exogenous fluid in sheep. Am J Physiol 1999;277:R236–42.

    CAS  PubMed  Google Scholar 

  10. Matsumoto LC, Cheung CY, Brace RA. Prolonged hypoxia increases urinary flow without the development of polyhydramnios in the ovine fetus. Am J Obstet Gynecol 2001;184:1008–14.

    Article  CAS  PubMed  Google Scholar 

  11. Daneshmand SS, Cheung CY, Brace RA. Regulation of amniotic fluid volume by intramembranous absorption in sheep: Role of passive permeability and vascular endothelial growth factor. Am J Obstet Gynecol 2003;188:786–93.

    Article  PubMed  Google Scholar 

  12. Abramovich DR, Page KR. Pathways of water exchange in the fetoplacental unit at mid-pregnancy. J Obstet Gynecol Br Commonw 1972;79:1099–102.

    Article  CAS  Google Scholar 

  13. Gitlin D, Kumate J, Morales C, Noriega L, Arevalo N. The turnover of amniotic fluid protein in the human conceptus. Am J Obset Gynecol 1972;113:632–45.

    Article  CAS  Google Scholar 

  14. Heller L. Intrauterine amino acid feeding of the fetus. In: Bode H, Warshaw J, eds. Parenternal nutrition in infancy and childhood. Plenum Press, 1974:206–13.

    Chapter  Google Scholar 

  15. Schrder HJ, Dehne K, Andreas TH, Rago S, Rybakowshki CH. Diffusive transfer of water and glucose across the chorionic plate of the isolated human term placenta. Placenta 1999;20:59–63.

    Article  Google Scholar 

  16. Reynolds WA, Pitkin RM, Hodaria AA. Transfer of iodide into amniotic fluid by the normal and the nephrectomized subhuman primate fetus. Am J Obstet Gynecol 1969;104:633–41.

    Article  CAS  PubMed  Google Scholar 

  17. Gilbert WM, Eby-Wilkens E, Tarantal AF. The missing link in rhesus monkey amniotic fluid volume regulation: Intramembranous absorption. Obstet Gynecol 1997;89:462–5.

    Article  CAS  PubMed  Google Scholar 

  18. Brace RA, Gilbert WM, Thornburg KL. Vascularization of the ovine amnion and chorion: A morphometric characterization of the surface area of the intramembranous pathway. Am J Obstet Gynecol 1992;161:1747–55.

    Article  Google Scholar 

  19. Gilbert WM, Cheung CY, Brace RA. Rapid intramembranous absorption into the fetal circulation of arginine vasopressin injected intraamniotically. Am J Obstet Gynecol 1991;164:1013–20.

    Article  CAS  PubMed  Google Scholar 

  20. Kullama LK, Agnew CL, Day L, Ervin MT, Ross MG. Ovine fetal swallowing and renal responses to oligohydramnios. Am J Physiol 1994;266:R972–8.

    CAS  PubMed  Google Scholar 

  21. Ross MG, Sherman DJ, Schreyer P, Ervin MG, Day L, Humme J. Fetal rehydration via intraamniotic fluid: Contribution of fetal swallowing. Pediatr Res 1991;29:214–7.

    Article  CAS  PubMed  Google Scholar 

  22. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989;246:1306–9.

    Article  CAS  PubMed  Google Scholar 

  23. Conolly DT. Vascular permeability factor: A unique regulator of blood vessel function. J Cell Biochem 1991;47:219–23.

    Article  Google Scholar 

  24. Senger DR, Perruzzi CA, Feder J, Dvorak HF. A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. J Cancer Res 1986;46:5629–32.

    CAS  Google Scholar 

  25. Terman BI, Dougher-Vermazen M, Carrion ME, et al. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun 1992;187:1579–86.

    Article  CAS  PubMed  Google Scholar 

  26. DeVries C, Escobedo JA, Ueno H, Houck K, Ferrera N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992;255:989–91.

    Article  CAS  Google Scholar 

  27. Ferrara N, Davis-Symth T. The biology of vascular endothelial growth factor. Endocr Rev 1997;18:4–25.

    Article  CAS  PubMed  Google Scholar 

  28. Sharkey AM, Charnock-Jones DS, Boocock CA, Brown KD, Smith SK. Expression of mRNA for vascular endothelial growth factor in human placenta. J Reprod Fertil 1993;99:609–15.

    Article  CAS  PubMed  Google Scholar 

  29. Jackson MR, Carney EW, Lye SJ, Ritchie JW. Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation. Placenta 1994;15:341–53.

    Article  CAS  PubMed  Google Scholar 

  30. Shiraishi S, Nakagawa K, Kinukawa N, Nakano H, Sueishi K. Immunochemical localization of vascular endothelial growth factor in the human placenta. Placenta 1996;17:111–21.

    Article  CAS  PubMed  Google Scholar 

  31. Ahmed A, Li XF, Dunk C, Whittle MJ, Rushton DI, Rollason T. Colocalisation of vascular endothelial growth factor and its Flt-1 receptor in human placenta. Growth Factors 1995;12:235–43.

    Article  CAS  PubMed  Google Scholar 

  32. Charnock-Jones DS, Sharkey AM, Boocock CA, Ahmed A, Pleven R, Ferrara N, Smith SK. Vascular endothelial growth factor receptor localization and activation in human trophoblast and choriocarcinoma cells. Biol Reprod 1994;51:524–30.

    Article  CAS  PubMed  Google Scholar 

  33. Cooper JC, Sharkey AM, McLaren J, Charnock-Jones DS, Smith SK. Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J Reprod Fertil 1995;105:205–13.

    Article  CAS  PubMed  Google Scholar 

  34. Clark DE, Smith SK, Sharley AM, Charnock-Jones DS. Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod 1996;11:1090–8.

    Article  CAS  PubMed  Google Scholar 

  35. Vuckovic M, Ponting J, Terman BI, Niketic V, Seif MW, Kuman S. Expression of the vascular endothelial growth factor receptor KDR, in human placenta. J Anat 1996;188:361–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Bogic LV, Brace RA, Cheung CY. Cellular localization of vascular endothelial growth factor in ovine placenta and fetal membranes. Placenta 2000;21:203–9.

    Article  CAS  PubMed  Google Scholar 

  37. Barleon B, Hauser S, Schollman C, et al. Differential expression of the two VEGF receptors flt and KDR in placenta and vascular endothelial cells. J Cell Biochem 1994;54:56–66.

    Article  CAS  PubMed  Google Scholar 

  38. Winther H, Ahmed A, Dantzer V. Immunochemical localization of vascular endothelial growth factor (VEGF) and its two specific receptors, flt-1 and KDR, in the porcine placenta and non-pregnant uterus. Placenta 1999;20:35–43.

    Article  CAS  PubMed  Google Scholar 

  39. Cheung CY, Brace RA. Developmental expression of vascular endothelial growth factor and its receptors in ovine placenta and fetal membranes. J Soc Gynecol Investig 1999;6:179–85.

    Article  CAS  PubMed  Google Scholar 

  40. Bogic LV, Brace RA, Cheung CY. Developmental expression of vascular endothelial growth factor (VEGF) receptors and VEGF binding in ovine placenta and fetal membranes. Placenta 2001;22:265–75.

    Article  CAS  PubMed  Google Scholar 

  41. Cheung CY, Brace RA. Ovine vascular endothelial growth factor: Nucleotide sequence and expression in fetal tissues. Growth Factors 1998;16:11–22.

    Article  CAS  PubMed  Google Scholar 

  42. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW. The vascular endothelial growth factor family: Identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 1991;91:1806–14.

    Article  Google Scholar 

  43. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, et al. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 1993;48:1120–8.

    Article  CAS  PubMed  Google Scholar 

  44. Anthony FW, Wheeler T, Elcock CL, Pickett M, Thomas EJ. Short report: Identification of a specific pattern of vascular endothelial growth factor mRNA expression in human placenta and cultured placental fibroblasts. Placenta 1994;15:557–61.

    Article  CAS  PubMed  Google Scholar 

  45. Cheung CY, Singh M, Ebaugh MJ, Brace RA. Vascular endothelial growth factor gene expression in ovine placenta and fetal membranes. Am J Obstet Gynecol 1995;173:753–9.

    Article  CAS  PubMed  Google Scholar 

  46. Ferrara N, Houck K, Jakeman L, Leung DW. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr Rev 1992;13:18–32.

    Article  CAS  PubMed  Google Scholar 

  47. Matsumoto LC, Bogic LV, Brace RA, Cheung CY. Fetal esophageal ligation induces VEGF expression in fetal membranes. Am J Obstet Gynecol 2001;184:175–84.

    Article  CAS  PubMed  Google Scholar 

  48. Vintzileos AM, Fleming AD, Scorza WE, et al. Relationship between fetal biophysical activities and umbilical cord blood gas values. Am J Obstet Gynecol 1991;165:707–13.

    Article  CAS  PubMed  Google Scholar 

  49. Cock ML, McCrabb GJ, Wlodek ME, Harding R. Effects of prolonged hypoxemia on fetal renal function and amniotic fluid volume in sheep. Am J Obstet Gynecol 1997;176:320–6.

    Article  CAS  PubMed  Google Scholar 

  50. Wlodek ME, Brace RA, Cock ML, Hooper SB, Harding R. Endocrine responses of fetal sheep to prolonged hypoxemia with and without acidemia: Relation to urine production. Am J Physiol 1995;268:F868–75.

    CAS  PubMed  Google Scholar 

  51. Brace RA, Wlodek ME, McCrabb GJ, Harding R. Swallowing and urine flow responses of the ovine fetus to 24 hours of hypoxia. Am J Physiol 1994;266:R1345–52.

    CAS  PubMed  Google Scholar 

  52. Sherman DJ, Ross MG, Day L, Humme J, Ervin MG. Fetal swallowing: Response to graded maternal hypoxemia. J Appl Physiol 1991;71:1856–61.

    Article  CAS  PubMed  Google Scholar 

  53. Matsumoto LC, Bogie LV, Brace RA, Cheung CY. Prolonged hypoxia up-regulates vascular endothelial growth factor messenger RNA expression in ovine fetal membranes and placenta. Am J Obstet Gynecol 2002;186:303–10.

    Article  CAS  PubMed  Google Scholar 

  54. Brace RA. Fetal blood volume, urine flow, swallowing and amniotic fluid volume responses to long-term intravascular saline infusions. Am J Obstet Gynecol 1989;161:1049–54.

    Article  CAS  PubMed  Google Scholar 

  55. Walker DW, Mitchell MD. Prostaglandins in urine of foetal lambs. Nature 1978;271:161–2.

    Article  CAS  PubMed  Google Scholar 

  56. Kelly EJ, Newell SJ, Brownlee KG, et al. Role of epidermal growth factor and transforming growth factor alpha in the developing stomach. Arch Dis Child Fetal Neonatal Ed 1997;76:F158–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Varner MW, Dildy GA, Hunter C, Dudley DJ, Clark SL, Mitchell MD. Amniotic fluid epidermal growth factor levels in normal and abnormal pregnancies. J Soc Gynecol Investig 1996;3:17–9.

    Article  CAS  PubMed  Google Scholar 

  58. Koizumi N, Inatomi T, Sotozono C, Fullwood NJ, Quantock AJ, Kinoshita S. Growth factor mRNA and protein in preserved human amniotic membrane. Current Eye Res 2000;20:173–7.

    Article  CAS  Google Scholar 

  59. Kudolo GB, DeFronzo RA. Urinary platelet-activating factor excretion is elevated in non-insulin dependent diabetes mellitus. Prostaglandins Other Lipid Mediators 1999;57:87–98.

    Article  CAS  PubMed  Google Scholar 

  60. Fagerudd JA, Groop PH, Honkanen E, Teppo AM, Greonhagen-Riska C. Urinary excretion of TGF-beta 1, PDGF-BB and fibronectin in insulin-dependent diabetes mellitus patients. Kidney Int 1997;63:S195–7.

    CAS  Google Scholar 

  61. Szabo A, Lutz J, Schleimer K, et al. Effect of angiotensin-converting enzyme inhibition on growth factor mRNA in chronic renal allograft rejection in the rat. Kidney Int 2000;57:982–91.

    Article  CAS  PubMed  Google Scholar 

  62. Sawdy RJ, Slater DM, Dennes WJ, Sullivan MH, Bennett PR. The roles of the cyclooxygenases types one and two in prostaglandin synthesis in human fetal membranes at term. Placenta 2000;21:54–7.

    Article  CAS  PubMed  Google Scholar 

  63. Ben-Av P, Crofford LJ, Wilder RL, Hla T. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: A potential mechanism for inflammatory angiogenesis. FEBS Lett 1995;372:83–7.

    Article  CAS  PubMed  Google Scholar 

  64. Höper MM, Voelkel NF, Bates TO, et al. Prostaglandins induce vascular endothelial growth factor in a human monocytic cell line and rat lungs via cAMP. Am J Respir Cell Mol Biol 1997;17:748–56.

    Article  PubMed  Google Scholar 

  65. Goldman CK, Kim J, Wong WL, King V, Brock T, Gillespie GY. Epidermal growth factor stimulates vascular endothelial growth factor production by human malignant glioma cells: A model of glioblastoma multiforme pathophysiology. Mol Biol Cell 1993;4:121–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Gille J, Swerlick RA, Caughman SW. Transforming growth factor-α-induced transcriptional activation of the vascular permeability factor (VPF/VEGF) gene requires AP-2-dependent DNA binding and transactivation. EMBO J 1997;16:750–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Pertovaara L, Kaipainen A, Mustonen T, et al. Vascular endothelial growth factor is induced in responses to transforming growth factor-beta in fibroblastic and epithelial cells. J Biol Chem 1994;269:6271–4.

    CAS  PubMed  Google Scholar 

  68. Ahmed A, Dearn S, Shams M, et al. Localization, quantification, and activation of platelet-activating factor receptor in human endometrium during the menstrual cycle: PAF stimulates NO, VEGF, and FAK. FASEB J 1998;12:831–43.

    Article  CAS  PubMed  Google Scholar 

  69. Nauck M, Roth M, Tamm M, et al. Induction of vascular endothelial growth factor by platelet-activating factor and platelet-derived growth factor is down-regulated by corticosteroids. Am J Respir Cell Mol Biol 1997;16:398–406.

    Article  CAS  PubMed  Google Scholar 

  70. Brogi E, Wu T, Namiki A, Isner JM. Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only. Circulation 1994;90:649–52.

    Article  CAS  PubMed  Google Scholar 

  71. Williams B, Quinn-Baker A, Gallagher B. Serum and plateletderived growth factor-induced expression of vascular permeability factor mRNA by human vascular smooth muscle cells in vitro. Clin Sci 1995;88:141–7.

    Article  CAS  Google Scholar 

  72. Perkins DJ, Kniss DA. Rapid and transient induction of cyclooxygenase 2 by epidermal growth factor in human amnionderived WISH cells. Biochem J 1997;321:677–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Casey ML, Korte K, MacDonald PC. Epidermal growth factor stimulation of prostaglandin E2 biosynthesis in amnion cells. J Biol Chem 1988;263:7846–54.

    CAS  PubMed  Google Scholar 

  74. Smith SK, Kelly RW. Effect of platelet-activating factor on the release of PGF2α and PGE2 by separated cells of human endometrium. J Reprod Fertil 1988;82:271–6.

    Article  CAS  PubMed  Google Scholar 

  75. Alvi SA, Brown NL, Bennett PR, Elder MG, Sullivan MH. Corticotrophin-releasing hormone and platelet-activating factor induce transcription of the type-2 cyclo-oxygenase gene in human fetal membranes. Mol Hum Reprod 1999;5:476–80.

    Article  CAS  PubMed  Google Scholar 

  76. Ershov AV, Bazan NG. Induction of cyclooxygenase-2 gene expression in retinal pigment epithelium cells by photoreceptor rod outer segment phagocytosis and growth factors. J Neurosci Res 1999;58:254–61.

    Article  CAS  PubMed  Google Scholar 

  77. Ladoux A, Freiin C. Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart. Biochem Biophys Res Commun 1993;195:1005–10.

    Article  CAS  PubMed  Google Scholar 

  78. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843–8.

    Article  CAS  PubMed  Google Scholar 

  79. Minchenko A, Bauer T, Salceda A, Caro J. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab Invest 1994;71:374–9.

    CAS  PubMed  Google Scholar 

  80. Liu Y, Cox SR, Morita T, Kourembnas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ Res 1995;77:638–43.

    Article  CAS  PubMed  Google Scholar 

  81. Ikeda E, Achen MG, Breier G, Risau W. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 1995;270:19761–6.

    Article  CAS  PubMed  Google Scholar 

  82. Shima DT, Deutsch U, D’Amore PA. Hypoxic induction of vascular endothelial growth factor (VEGF) in human epithelial cells is mediated by increases in mRNA stability. FEBS Lett 1995;370:203–8.

    Article  CAS  PubMed  Google Scholar 

  83. Levy AP, Levy NS, Goldberg MA. Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J Biol Chem 1996;271:2746–53.

    Article  CAS  PubMed  Google Scholar 

  84. Claffey KP, Shih SC, Mullen A, et al. Identification of human VPF/VEGF 3′ untranslated region mediating hypoxia-induced mRNA stability. Mol Biol Cell 1998;9:469–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ji YS, Xu Q, Schmedtje JF Jr. Hypoxia induces high-mobilitygroup protein I (Y) and transcription of the cyclooxygenasegene 2 in human vascular endothelium. Circ Res 1998;83:295–304.

    Article  CAS  PubMed  Google Scholar 

  86. Schmedtje JF Jr, YS Ji, Liu WL, Dubois RN, Runge MS. Hypoxia induces cyclooxygenase-2 via the NF-kappaB transcription factor in human vascular endothelial cells. J Biol Chem 1997;272:601–8.

    Article  CAS  PubMed  Google Scholar 

  87. Chida M, Voelkel NF. Effects of acute and chronic hypoxia on rat lung cyclooxygenase. Am J Physiol 1996;270:L872–8.

    CAS  PubMed  Google Scholar 

  88. Akiséu M, Keulteursay N, Coker I, Heuseyinov A. Platelet-activating factor is an important mediator in hypoxic ischemic brain injury in the newborn rat. Flunarizine and Ginkgo biloba extract reduce PAF concentration in the brain. Biol Neonate 1998;74:439–44.

    Article  Google Scholar 

  89. Chen D, Chen W. Changes of distribution of platelet activating factor in the lung of rats with hypoxic pulmonary hypertension. Chin Med Sci J 1996;109:776–9.

    CAS  Google Scholar 

  90. Cai Y, Han M, Luo L, Song W, Zhou X. Increased expression of PDGF and c-myc genes in lungs and pulmonary arteries of pulmonary hypertensive rats induced by hypoxia. Chin Med Sci J 1996;11:152–6.

    CAS  PubMed  Google Scholar 

  91. Berg JT, Breen EC, Fu Z, Matheu-Costello O, West JB. Alveolar hypoxia increases gene expression of extracellular matrix proteins and platelet-derived growth factor-36 in lung parenchyma. Am J Respir Crit Care Med 1998;158:1920–8.

    Article  CAS  PubMed  Google Scholar 

  92. Starvi GT, Hong Y, Zachary IC, et al. Hypoxia and platelet-derived growth factor-36 synergistically upregulate the expression of vascular endothelial growth factor in vascular smooth ceUs. FEBS Lett 1995;358:311–5.

    Article  Google Scholar 

  93. Faber JJ, Anderson DF. Absorption of amniotic fluid by amniochonon in sheep. Am J Physiol 2002;282:H850–4.

    CAS  Google Scholar 

  94. Parry-Jones E, Priya S. A study of the elasticity and tension of fetal membranes and of the relation of the area of the gestational sac to the area of the uterine cavity. Br J Obstet Gynaecol 1976;83:205–12.

    Article  CAS  PubMed  Google Scholar 

  95. Millar LK, Stollberg J, DeBuque L, Bryant-Greenwood G. Fetal membrane distention: Determination of the intrauterine surface area and distention of the fetal membranes preterm and at term. Am J Obstet Gynecol 2000;182:128–34.

    Article  CAS  PubMed  Google Scholar 

  96. Breier G. Angiogenesis in embryonic development—a review. Placenta 2000;14:S11–5.

    Article  CAS  Google Scholar 

  97. Ong S, Lash G, Baker PN. Angiogenesis and placental growth in normal and compromised pregnancies. Baillieres Clin Obstet Gynaecol 2000;14:969–80.

    Article  CAS  Google Scholar 

  98. Le V, McLaughlin J, Brace RA, Cheung CY. Vascular endothelial growth factor induced proliferation of ovine umbilical vein endothelial cells. J Soc Gynecol Investig 1998;5(Suppl):158A.

    Article  Google Scholar 

  99. Ku DD, Zaleski JK, Liu S, Brock TA. Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am J Physiol 1993;265:H586–92.

    CAS  PubMed  Google Scholar 

  100. Yang HT, Yan Z, Abraham JA, Terjung RL. VEGF121- and 36 FGF- induced increase in collateral blood flow requires normal nitric oxide production. Am J Physiol 2001;280:H1097–104.

    Article  CAS  Google Scholar 

  101. Banbury J, Siemionow M, Porvasnik S, Petras S, Browne E. Improved perfusion after subcritical ischemia in muscle flaps treated with vascular endothelial growth factor. Plast Reconstr Surg 2000;106:1541–6.

    Article  CAS  PubMed  Google Scholar 

  102. Cherng JM, Lin CM, Lin CL, et al. Effects of VEGF121 and/or VEGF165 gene transfection on collateral circulation development. J Formos Med Assoc 2000;99:603–11.

    CAS  PubMed  Google Scholar 

  103. Hedriana HL, Brace RA, Gilbert WM. Changes in blood flow to the ovine chorion and amnion across gestation. J Soc Gynecol Investig 1995;2:727–34.

    CAS  PubMed  Google Scholar 

  104. Lingwood BE, Wintour EM. Permeability of ovine amnion and amniochorion on urea and water. Obstet Gynecol 1983;61:227–32.

    CAS  PubMed  Google Scholar 

  105. Wintour EM, Lingwood BE, Towstoless MK. Passive permeability of ovine amnion and allantois to chloride—gestational changes. Placenta 1988;9:599–606.

    Article  CAS  PubMed  Google Scholar 

  106. Michel CC. Capillaries, caveolae, calcium and cyclic nucleotides: A new look at microvascular permeability. J Mol Cell Cardiol 1998;30:2541–6.

    Article  CAS  PubMed  Google Scholar 

  107. Palade GE, Bruns RR. Structural modulations of plasmalemma vesicles. J Cell Biol 1968;37:633–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Rothberg KG, Heuser JE, Donzeil WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 1992;68:673–82.

    Article  CAS  PubMed  Google Scholar 

  109. Michel CC, Curry FE. Microvascular permeability. Physiol Rev 1999;79:703–61.

    Article  CAS  PubMed  Google Scholar 

  110. Bautzmann H, Schmidt W, Lemburg P. Experimental electron-and light-microscopical studies on the function of the amnion— apparatus of the chick, the cat and man. Anat Anz 1960;108:305–11.

    CAS  PubMed  Google Scholar 

  111. Armstrong WD, Wilt JC, Pritchard ET. Vacuolation in the human amnion cell studied by time-lapse photography and electron microscopy. Am J Obstet Gynecol 1968;102:932–48.

    Article  CAS  PubMed  Google Scholar 

  112. King BF. Cell surface specializations and intercellular junctions in human amniotic epithelium: An electron microscopic and freeze-fracture study. Anat Rec 1982;203:73–8.

    Article  CAS  PubMed  Google Scholar 

  113. Shandley L, Alcorn D, Wintour EM. Ovine amniotic and allantoic epithelia across gestation. Anat Rec 1997;248:542–53.

    Article  CAS  PubMed  Google Scholar 

  114. Lyden TW, Anderson CL, Robinson JM. The endothelium but not the syncytiotrophoblast of human placenta expresses caveolae. Placenta 2002;23:640–52.

    Article  PubMed  Google Scholar 

  115. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 1992;267:26031–7.

    CAS  PubMed  Google Scholar 

  116. Bates DO, Curry FE. Vascular endothelial growth factor increases hydraulic conductivity of isolated perfused microvessels. Am J Physiol 1996;271:H2520–8.

    CAS  PubMed  Google Scholar 

  117. Fujii E, Irie K, Ohba KI, et al. Role of nitric oxide, prostaglandins and tyrosine kinase in vascular endothelial growth factor-induced increase in vascular permeability in mouse skin. Naunyn-Shmiedebergs Arch Pharmacol 1997;356:475–80.

    Article  CAS  Google Scholar 

  118. Feng D, Nagy JA, Pyne K, Hammel I, Dvorak HF, Dvorak AM. Pathways of macromolecular extravasation across microvascular endothelium in response to VPF/VEGF and other vasoactive mediators. Microcirculation 1999;6:23–44.

    Article  CAS  PubMed  Google Scholar 

  119. Kohn S, Nagy J, Dvorak H, Dvorak A. Pathways of macromolecular tracer transport across venules and small veins. Structural basis for the hyperpermeability of tumor blood vessels. Lab Invest 1992;67:596–607.

    CAS  PubMed  Google Scholar 

  120. Vasile E, Hong Q, Dvorak HF, Dvorak AM. Caveolae and vesiculo/vacuolar organelles in bovine capillary endothelial cells cultured with VPF/VEGF on floating matrigel/collagen gels. J Histochem Cytochem 1999;47:159–67.

    Article  CAS  PubMed  Google Scholar 

  121. Chen J, Braet F, Brodsky S, et al. VEGF-induced mobilization of caveolae and increase in permeability of endothelial cells. Am J Physiol 2002;282:C1053–63.

    Article  CAS  Google Scholar 

  122. Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W. Vascular endothelial growth factor induces endothelial genestrations in vitro. J Cell Biol 1998;140:947–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Feng Y, Venema VJ, Venema RC, Tsai N, Behzadian MA, Caldwell RB. VEGF-induced permeability increase is mediated by caveolae. Invest Ophthalmol Vis Sci 1999;40:157–67.

    CAS  PubMed  Google Scholar 

  124. Liu J, Razani B, Tang S, Terman BI, Ware JA, Lisanti MP. Angiogenesis activators and inhibitors differentially regulate caveolin-1 expression and caveolae formation in vascular endothelial cells. J Biol Chem 1999;274:15781–5.

    Article  CAS  PubMed  Google Scholar 

  125. Carmeliet P, Ferreira V, Briere G, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996;380:435–9.

    Article  CAS  PubMed  Google Scholar 

  126. Ferrara N, Carver-Moore K, Chen H, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380:439–42.

    Article  CAS  PubMed  Google Scholar 

  127. Shalaby F, Rossant J, Yamaguchi TP, et al. Failure of blood island formation and vasculogenesis in Flk-1 deficient mice. Nature 1995;376:62–6.

    Article  CAS  PubMed  Google Scholar 

  128. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995;376:66–70.

    Article  CAS  PubMed  Google Scholar 

  129. Wang D, Donner DB, Warren RS. Homeostatic modulation of cell surface KDR and Flt1 expression and expression of the vascular endothelial cell growth factor (VEGF) receptor mRNAs by VEGF. J Biol Chem 2000;275:15905–11.

    Article  CAS  PubMed  Google Scholar 

  130. Shen BQ, Lee DY, Gerber HP, Keyt BA, Ferrar N, Zioncheck TF. Homologous up-regulation of KDR/Flk-1 receptor expression by vascular endothelial growth factor in vitro. J Biol Chem 1998;273:29979–85.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Perinatal Medicine, Department of Reproductive Medicine, University of California at San Diego, 9500 Gilman Drive, La Jolla, California, 92093-0802, USA

    Cecilia Y. Cheung PhD

Authors
  1. Cecilia Y. Cheung PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cecilia Y. Cheung PhD.

Additional information

Supported in part by Public Health Service Awards HD 33054 and HD 35890 from the National Institute of Child Health and Human Development.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cheung, C.Y. Vascular Endothelial Growth Factor Activation of Intramembranous Absorption: A Critical Pathway for Amniotic Fluid Volume Regulation. Reprod. Sci. 11, 63–74 (2004). https://doi.org/10.1016/j.jsgi.2003.09.002

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.jsgi.2003.09.002

Key words

Search

Navigation