Placenta
Volume 29, Issue 10 , Pages 840-847 , October 2008

Aquaporins and Fetal Fluid Balance

  • H. Liu
  • ,
  • Z. Zheng
  • ,
  • E.M. Wintour

      Affiliations

    • Corresponding Author InformationCorresponding author. Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria, 3800, Australia. Tel.: +61 3 99052508; fax: +61 3 99052547.

,Accepted 24 July 2008.

References 

  1. Jeyaseelan K, Sepramaniam S, Armugam A, Wintour EM. Aquaporins: a promising target for drug development. Expert Opin Ther Targets. 2006;10:889–909
  2. Agre P. Nobel Lecture. Aquaporin water channels. Biosci Rep. 2004;24:127–163
  3. Saparov SM, Liu K, Agre P, Pohl P. Fast and selective ammonia transport by aquaporin-8. J Biol Chem. 2007;282:5296–5301
  4. Beall MH, Wang S, Yang B, Chaudhri N, Amidi F, Ross MG. Placental and membrane aquaporin water channels: correlation with amniotic fluid volume and composition. Placenta. 2007;28:421–428
  5. Beall MH, van den Wijngaard JP, van Gemert MJ, Ross MG. Regulation of amniotic fluid volume. Placenta. 2007;28:824–832
  6. Liu H, Wintour EM. Aquaporins in development – a review. Reprod Biol Endocrinol. 2005;3:18
  7. Belge H, Devuyst O. Aquaporin-1 – a water channel on the move. Nephrol Dial Transplant. 2006;21:2069–2071
  8. Liang HT, Feng XC, Ma TH. Water channel activity of plasma membrane affects chondrocyte migration and adhesion. Clin Exp Pharmacol Physiol. 2008;35:7–10
  9. Papadopoulos MC, Saadoun S, Verkman AS. Aquaporins and cell migration. Pflugers Arch. 2007;
  10. Camerino GM, Nicchia GP, Dinardo MM, Ribatti D, Svelto M, Frigeri A. In vivo silencing of aquaporin-1 by RNA interference inhibits angiogenesis in the chick embryo chorioallantoic membrane assay. Cell Mol Biol (Noisy-le-grand). 2006;52:51–56
  11. Brownbill P, Sibley CP. Regulation of transplacental water transfer: the role of fetoplacental venous tone. Placenta. 2006;27:560–567
  12. Stulc J. Placental transfer of inorganic ions and water. Physiol Rev. 1997;77:805–836
  13. Towstoless MK, Congiu M, Coghlan JP, Wintour EM. Placental and renal control of plasma osmolality in chronically cannulated ovine fetus. Am J Physiol. 1987;253:R389–R395
  14. Umber A, Chohan MA. Intravenous maternal hydration in third trimester oligohydramnios: effect on amniotic fluid volume. J Coll Physicians Surg Pak. 2007;17:336–339
  15. Brace RA. Physiology of amniotic fluid volume regulation. Clin Obstet Gynecol. 1997;40:280–289
  16. Lingwood BE, Wintour EM. Amniotic fluid volume and in vivo permeability of ovine fetal membranes. Obstet Gynecol. 1984;64:368–372
  17. Magann EF, Chauhan SP, Doherty DA, Lutgendorf MA, Magann MI, Morrison JC. A review of idiopathic hydramnios and pregnancy outcomes. Obstet Gynecol Surv. 2007;62:795–802
  18. Magann EF, Chauhan SP, Doherty DA, Magann MI, Morrison JC. The evidence for abandoning the amniotic fluid index in favor of the single deepest pocket. Am J Perinatol. 2007;24:549–555
  19. Jaba B, Mohiuddin AS, Dey SN, Khan NA, Talukder SI. Ultrasonographic determination of amniotic fluid volume in normal pregnancy. Mymensingh Med J. 2005;14:121–124
  20. Fok WY, Chan LY, Lau TK. The influence of fetal position on amniotic fluid index and single deepest pocket. Ultrasound Obstet Gynecol. 2006;28:162–165
  21. Wintour EM, Shandley L. Effects of fetal fluid balance on amniotic fluid volume. Semin Perinatol. 1993;17:158–172
  22. Butkus A, Earnest L, Jeyaseelan K, Moritz K, Johnston H, Tenis N, et al. Ovine aquaporin-2: cDNA cloning, ontogeny and control of renal gene expression. Pediatr Nephrol. 1999;13:379–390
  23. Wintour EM, Moritz KM. Comparative aspects of fetal renal development. Equine Vet J Suppl. 1997;51–58
  24. Eisenbeiss C, Welzel J, Eichler W, Klotz K. Influence of body water distribution on skin thickness: measurements using high-frequency ultrasound. Br J Dermatol. 2001;144:947–951
  25. Cartlidge P. The epidermal barrier. Semin Neonatol. 2000;5:273–280
  26. Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K. Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss. J Histochem Cytochem. 1999;47:1275–1286
  27. Sougrat R, Morand M, Gondran C, Barre P, Gobin R, Bonte F, et al. Functional expression of AQP3 in human skin epidermis and reconstructed epidermis. J Invest Dermatol. 2002;118:678–685
  28. Jain A, Rutter N, Cartlidge PH. Influence of antenatal steroids and sex on maturation of the epidermal barrier in the preterm infant. Arch Dis Child Fetal Neonatal Ed. 2000;83:F112–F116
  29. Bor NM, Karpuzoglu T, Hamzadi T, Edguer E, Kis M. Role of fetal skin in circulation of amniotic fluid. Arch Int Physiol Biochim. 1970;78:69–78
  30. Hardman MJ, Sisi P, Banbury DN, Byrne C. Patterned acquisition of skin barrier function during development. Development. 1998;125:1541–1552
  31. Seeds AE. Current concepts of amniotic fluid dynamics. Am J Obstet Gynecol. 1980;138:575–586
  32. Agren J, Zelenin S, Hakansson M, Eklof AC, Aperia A, Nejsum LN, et al. Transepidermal water loss in developing rats: role of aquaporins in the immature skin. Pediatr Res. 2003;53:558–565
  33. Moritz KM, Dodic M, Wintour EM. Kidney development and the fetal programming of adult disease. Bioessays. 2003;25:212–220
  34. Lee SM, Park SK, Shim SS, Jun JK, Park JS, Syn HC. Measurement of fetal urine production by three-dimensional ultrasonography in normal pregnancy. Ultrasound Obstet Gynecol. 2007;30:281–286
  35. Touboul C, Boulvain M, Picone O, Levaillant JM, Frydman R, Senat MV. Normal fetal urine production rate estimated with 3-dimensional ultrasonography using the rotational technique (virtual organ computer-aided analysis). Am J Obstet Gynecol. 2008;
  36. Devuyst O, Burrow CR, Smith BL, Agre P, Knepper MA, Wilson PD. Expression of aquaporins-1 and -2 during nephrogenesis and in autosomal dominant polycystic kidney disease. Am J Physiol. 1996;271:F169–F183
  37. Wintour EM, Earnest L, Alcorn D, Butkus A, Shandley L, Jeyaseelan K. Ovine AQP1: cDNA cloning, ontogeny, and control of renal gene expression. Pediatr Nephrol. 1998;12:545–553
  38. Dane B, Yayla M, Dane C, Cetin A. Prenatal diagnosis of Bartter syndrome with biochemical examination of amniotic fluid: case report. Fetal Diagn Ther. 2007;22:206–208
  39. Harding R, Hooper SB. Regulation of lung expansion and lung growth before birth. J Appl Physiol. 1996;81:209–224
  40. Agre P. The aquaporin water channels. Proc Am Thorac Soc. 2006;3:5–13
  41. King LS, Nielsen S, Agre P. Aquaporins in complex tissues. I. Developmental patterns in respiratory and glandular tissues of rat. Am J Physiol. 1997;273:C1541–C1548
  42. Liu H, Hooper SB, Armugam A, Dawson N, Ferraro T, Jeyaseelan K, et al. Aquaporin gene expression and regulation in the ovine fetal lung. J Physiol. 2003;551:503–514
  43. King LS, Nielsen S, Agre P. Aquaporin-1 water channel protein in lung: ontogeny, steroid-induced expression, and distribution in rat. J Clin Invest. 1996;97:2183–2191
  44. Cole TJ, Solomon NM, Van Driel R, Monk JA, Bird D, Richardson SJ, et al. Altered epithelial cell proportions in the fetal lung of glucocorticoid receptor null mice. Am J Respir Cell Mol Biol. 2004;30:613–619
  45. Yasui M, Serlachius E, Lofgren M, Belusa R, Nielsen S, Aperia A. Perinatal changes in expression of aquaporin-4 and other water and ion transporters in rat lung. J Physiol. 1997;505:3–11(Pt 1)
  46. Takayasu H, Nakazawa N, Montedonico S, Puri P. Reduced expression of aquaporin 5 water channel in nitrofen-induced hypoplastic lung with congenital diaphragmatic hernia rat model. J Pediatr Surg. 2007;42:415–419
  47. Condino AA, Barleycorn AA, Lu W, Maheshwari A, Christensen RD, Calhoun DA. Abnormal intestinal histology in neonates with congenital anomalies of the gastrointestinal tract. Biol Neonate. 2004;85:145–150
  48. El-Haddad MA, Desai M, Gayle D, Ross MG. In utero development of fetal thirst and appetite: potential for programming. J Soc Gynecol Investig. 2004;11:123–130
  49. Ross MG, Nijland MJ. Fetal swallowing: relation to amniotic fluid regulation. Clin Obstet Gynecol. 1997;40:352–365
  50. Matsumoto LC, Cheung CY, Brace RA. Increased urinary flow without development of polyhydramnios in response to prolonged hypoxia in the ovine fetus. Am J Obstet Gynecol. 2001;184:1008–1014
  51. Minei LJ, Suzuki K. Role of fetal deglutition and micturition in the production and turnover of amniotic fluid in the monkey. Obstet Gynecol. 1976;48:177–181
  52. Wintour EM, Barnes A, Brown EH, Hardy KJ, Horacek I, McDougall JG, et al. Regulation of amniotic fluid volume and composition in the ovine fetus. Obstet Gynecol. 1978;52:689–693
  53. Cock ML, Wlodek ME, Hooper SB, McCrabb GJ, Harding R. The effects of twenty-four hours of reduced uterine blood flow on fetal fluid balance in sheep. Am J Obstet Gynecol. 1994;170:1442–1451
  54. 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;188:786–793
  55. Faber J, Anderson D, Hohimer R, Yang Q, Giraud G, Davis L. Function curve of the membranes that regulate amniotic fluid volume in sheep. Am J Physiol Heart Circ Physiol. 2005;289:H146–H150
  56. Yang Q, Davis L, Hohimer A, Faber J, Anderson D. Regulatory response to washout of amniotic fluid in sheep. Am J Physiol Heart Circ Physiol. 2005;288:H1339–H1343
  57. Jablonski EM, McConnell NA, Hughes FM, Huet-Hudson YM. Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol Reprod. 2003;69:1481–1487
  58. Lindsay LA, Murphy CR. Redistribution of aquaporins in uterine epithelial cells at the time of implantation in the rat. Acta Histochem. 2004;106:299–307
  59. Lindsay LA, Murphy CR. Aquaporin-1 increases in the rat myometrium during early pregnancy. J Mol Histol. 2004;35:75–79
  60. Lindsay LA, Murphy CR. Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy. Reproduction. 2006;131:369–378
  61. Lindsay LA, Murphy CR. Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat. J Mol Histol. 2007;38:87–95
  62. Richard C, Gao J, Brown N, Reese J. Aquaporin water channel genes are differentially expressed and regulated by ovarian steroids during the periimplantation period in the mouse. Endocrinology. 2003;144:1533–1541
  63. Kobayashi M, Takahashi E, Miyagawa S, Watanabe H, Iguchi T. Chromatin immunoprecipitation-mediated target identification proved aquaporin 5 is regulated directly by estrogen in the uterus. Genes Cells. 2006;11:1133–1143
  64. He RH, Sheng JZ, Luo Q, Jin F, Wang B, Qian YL, et al. Aquaporin-2 expression in human endometrium correlates with serum ovarian steroid hormones. Life Sci. 2006;79:423–429
  65. Hildenbrand A, Lalitkumar L, Nielsen S, Gemzell-Danielsson K, Stavreus-Evers A. Expression of aquaporin 2 in human endometrium. Fertil Steril. 2006;86:1452–1458
  66. Li X, Yu H, Koide SS. The water channel gene in human uterus. Biochem Mol Biol Int. 1994;32:371–377
  67. Mobasheri A, Wray S, Marples D. Distribution of AQP2 and AQP3 water channels in human tissue microarrays. J Mol Histol. 2005;36:1–14
  68. Pan H, Sun CC, Zhou CY, Huang HF. Expression of aquaporin-1 in normal, hyperplasic, and carcinomatous endometria. Int J Gynaecol Obstet. 2008;
  69. Mints M, Hildenbrand A, Lalitkumar LP, Andersson S, Nielsen S, Gemzell-Danielsson K, et al. Expression of aquaporin-1 in endometrial blood vessels in menorrhagia. Int J Mol Med. 2007;19:407–411
  70. Anderson J, Brown N, Mahendroo MS, Reese J. Utilization of different aquaporin water channels in the mouse cervix during pregnancy and parturition and in models of preterm and delayed cervical ripening. Endocrinology. 2006;147:130–140
  71. de Wilde J, Wilting SM, Meijer CJ, van de Wiel MA, Ylstra B, Snijders PJ, et al. Gene expression profiling to identify markers associated with deregulated hTERT in HPV-transformed keratinocytes and cervical cancer. Int J Cancer. 2008;122:877–888
  72. Johnston H, Koukoulas I, Jeyaseelan K, Armugam A, Earnest L, Baird R, et al. Ontogeny of aquaporins 1 and 3 in ovine placenta and fetal membranes. Placenta. 2000;21:88–99
  73. Umenishi F, Verkman AS, Gropper MA. Quantitative analysis of aquaporin mRNA expression in rat tissues by RNase protection assay. DNA Cell Biol. 1996;15:475–480
  74. Baird R, Wintour EM. Placentae with haemophagous zones and water channel proteins; a cautionary tale. Placenta. 2000;21:587–588
  75. Ribatti D, Frigeri A, Nico B, Nicchia GP, De Giorgis M, Roncali L, et al. Aquaporin-1 expression in the chick embryo chorioallantoic membrane. Anat Rec. 2002;268:85–89
  76. Xiang Y, Ma B, Li T, Gao JW, Yu HM, Li XJ. Acetazolamide inhibits aquaporin-1 protein expression and angiogenesis. Acta Pharmacol Sin. 2004;25:812–816
  77. Damiano A, Zotta E, Goldstein J, Reisin I, Ibarra C. Water channel proteins AQP3 and AQP9 are present in syncytiotrophoblast of human term placenta. Placenta. 2001;22:776–781
  78. Wang S, Chen J, Au KT, Ross MG. Expression of aquaporin 8 and its up-regulation by cyclic adenosine monophosphate in human WISH cells. Am J Obstet Gynecol. 2003;188:997–1001
  79. Wang S, Chen J, Beall M, Zhou W, Ross MG. Expression of aquaporin 9 in human chorioamniotic membranes and placenta. Am J Obstet Gynecol. 2004;191:2160–2167
  80. Wang S, Chen J, Huang B, Ross MG. Cloning and cellular expression of aquaporin 9 in ovine fetal membranes. Am J Obstet Gynecol. 2005;193:841–848
  81. Wang S, Kallichanda N, Song W, Ramirez BA, Ross MG. Expression of aquaporin-8 in human placenta and chorioamniotic membranes: evidence of molecular mechanism for intramembranous amniotic fluid resorption. Am J Obstet Gynecol. 2001;185:1226–1231
  82. Damiano AE, Zotta E, Ibarra C. Functional and molecular expression of AQP9 channel and UT-A transporter in normal and preeclamptic human placentas. Placenta. 2006;27:1073–1081
  83. Baisden B, Sonne S, Joshi RM, Ganapathy V, Shekhawat PS. Antenatal dexamethasone treatment leads to changes in gene expression in a murine late placenta. Placenta. 2007;28:1082–1090
  84. Mann SE, Ricke EA, Yang BA, Verkman AS, Taylor RN. Expression and localization of aquaporin 1 and 3 in human fetal membranes. Am J Obstet Gynecol. 2002;187:902–907
  85. Eis AW, Mitchell MD, Myatt L. Endothelin transfer and endothelin effects on water transfer in human fetal membranes. Obstet Gynecol. 1992;79:411–415
  86. Lingwood BE, Wintour EM. Permeability of ovine amnion and amniochorion to urea and water. Obstet Gynecol. 1983;61:227–232
  87. Mann SE, Ricke EA, Torres EA, Taylor RN. A novel model of polyhydramnios: amniotic fluid volume is increased in aquaporin 1 knockout mice. Am J Obstet Gynecol. 2005;192:2041–2044[discussion 2044–2046]
  88. Mann SE, Dvorak N, Gilbert H, Taylor RN. Steady-state levels of aquaporin 1 mRNA expression are increased in idiopathic polyhydramnios. Am J Obstet Gynecol. 2006;194:884–887
  89. Wang S, Amidi F, Beall M, Gui L, Ross MG. Aquaporin 3 expression in human fetal membranes and its up-regulation by cyclic adenosine monophosphate in amnion epithelial cell culture. J Soc Gynecol Investig. 2006;13:181–185
  90. Feng X, Li P, Qiu G, Wang S, Li G, Shang L, et al. Human exposure to methylmercury through rice intake in mercury mining areas, Guizhou province, China. Environ Sci Technol. 2008;42:326–332
  91. Li P, Feng X, Qiu G, Shang L, Wang S. Mercury exposure in the population from Wuchuan mercury mining area, Guizhou, China. Sci Total Environ. 2008;395:72–79
  92. Murphy D, Dancis B, Brown JR. The evolution of core proteins involved in microRNA biogenesis. BMC Evol Biol. 2008;8:92
  93. Donker RB, Mouillet JF, Nelson DM, Sadovsky Y. The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol Hum Reprod. 2007;13:273–279
  94. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science. 2007;318:1931–1934
  95. Kedde M, Agami R. Interplay between microRNAs and RNA-binding proteins determines developmental processes. Cell Cycle. 2008;7:899–903
  96. Wang G, Wang X, Wang Y, Yang JY, Li L, Nephew KP, et al. Identification of transcription factor and microRNA binding sites in responsible to fetal alcohol syndrome. BMC Genomics. 2008;9(Suppl. 1):S19
  97. O'Neill JS, Hastings MH. Circadian clocks: timely interference by microRNAs. Curr Biol. 2007;17:R760–R762
  98. Cheng HY, Papp JW, Varlamova O, Dziema H, Russell B, Curfman JP, et al. Obrietan, microRNA modulation of circadian-clock period and entrainment. Neuron. 2007;54:813–829
  99. Bibikova M, Laurent LC, Ren B, Loring JF, Fan JB. Unraveling epigenetic regulation in embryonic stem cells. Cell Stem Cell. 2008;2:123–134
  100. Stadler BM, Ruohola-Baker H. Small RNAs: keeping stem cells in line. Cell. 2008;132:563–566
  101. Pineles BL, Romero R, Montenegro D, Tarca AL, Han YM, Kim YM, et al. Distinct subsets of microRNAs are expressed differentially in the human placentas of patients with preeclampsia. Am J Obstet Gynecol. 2007;196(261):e261–e266
  102. Montenegro D, Romero R, Pineles BL, Tarca AL, Kim YM, Draghici S, et al. Differential expression of microRNAs with progression of gestation and inflammation in the human chorioamniotic membranes. Am J Obstet Gynecol. 2007;197(289):e281–e286
  103. Blow N. Small RNAs: delivering the future. Nature. 2007;450:1117–1120

PII: S0143-4004(08)00222-1

doi: 10.1016/j.placenta.2008.07.010

Placenta
Volume 29, Issue 10 , Pages 840-847 , October 2008