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Loss of Aquaporin-3 in Placenta and Fetal Membranes Induces Growth Restriction in Mice

  • Seo, Min Joon (Dept. of Emergency Medicine, College of Medicine, Dong-A University) ;
  • Lim, Ju Hyun (Dept. of Physiology, College of Medicine, Dong-A University) ;
  • Kim, Dong-Hwan (Human Life Research Center, Dong-A University) ;
  • Bae, Hae-Rahn (Dept. of Physiology, College of Medicine, Dong-A University)
  • Received : 2018.07.31
  • Accepted : 2018.09.10
  • Published : 2018.09.30

Abstract

Aquaporin (AQP) 3, a facilitated transporter of water and glycerol, expresses in placenta and fetal membranes, but the detailed localization and function of AQP3 in placenta remain unclear. To elucidate a role of AQP3 in placenta, we defined the expression and cellular localization of AQP3 in placenta and fetal membranes, and investigated the structural and functional differences between wild-type and AQP3 null mice. Gestational sacs were removed during mid-gestational period and amniotic fluid was aspirated for measurements of volume and composition. Fetuses with attached placenta and fetal membranes were weighed and processed for histological assessment. AQP3 strongly expressed in basolateral membrane of visceral yolk sac cells of fetal membrane, the syncytiotrophoblasts of the labyrinthine placenta and fetal nucleated red blood cell membrane. Mice lacking AQP3 did not exhibit a significant defect in differentiation of trophoblast stem cells and normal placentation. However, AQP3 null fetuses were smaller than their control litter mates in spite of a decrease in litter size. The total amniotic fluid volume per gestational sac was reduced, but the amniotic fluid-to-fetal weight ratio was increased in AQP3 null mice compared with wild-type mice. Glycerol, free fatty acid and triglyceride levels in amniotic fluid of AQP3 null mice were significantly reduced, whereas lactate level increased when compared to those of wild-type mice. These results suggest a role for AQP3 in supplying nutrients from yolk sac and maternal blood to developing fetus by facilitating transport of glycerol in addition to water, and its implication for the fetal growth in utero.

Keywords

References

  1. Beall MH, van den Wijngaard JPHM, van Gemert MJC, Ross MG (2007) Amniotic fluid water dynamics. Placenta 28:816-823. https://doi.org/10.1016/j.placenta.2006.11.009
  2. Brace RA (1997) Physiology of amniotic fluid volume regulation. Clin Obstet Gynecol 40:280-289. https://doi.org/10.1097/00003081-199706000-00005
  3. Campbell FM, Bush PG, Veerkamp JH, Dutta-Roy AK (1998) Detection and cellular localization of plasma membrane-associated and cytoplasmic fatty acid-binding proteins in human placenta. Placenta 19:409-415.
  4. Carter AM (2007) Animal models of human placentation-A review. Placenta 28:S41-S47. https://doi.org/10.1016/j.placenta.2006.11.002
  5. Cox B, Kotlyar M, Evangelou AI, Ignatchenko V, Ignatchenko A, Whiteley K, Jurisica I, Adamson SL, Rossant J, Kislinger T (2009) Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol 5:279. https://doi.org/10.1038/msb.2009.37
  6. Cross JC, Simmons DG, Watson ED (2003) Chorioallanoic morphogenesis and formation of the placental villous tree. Ann N Y Acad Sci 995:84-93. https://doi.org/10.1111/j.1749-6632.2003.tb03212.x
  7. Cross JC, Werb Z, Fisher SJ (1994) Implantation and the placenta: Key pieces of the development puzzle. Science 266:1508-1518. https://doi.org/10.1126/science.7985020
  8. Damiano A, Zotta E, Goldstein J, Reisin I, Ibarra C (2001) Water channel proteins AQP3 and AQP9 are present in syncytiotrophoblast of human term placenta. Placenta 22:776-781. https://doi.org/10.1053/plac.2001.0717
  9. De Falco M, Cobellis L, Torella M, Acone G, Varano L, Sellitti A, Ragucci A, Coppola G, Cassandro R, Laforgia V, Varano L, De Luca A (2007) Down-regulation of aquaporin 4 in human placenta throughout pregnancy. In Vivo 21:813-817.
  10. Enders AC, Carter AM (2006) Comparative placentation: Some interesting modifications for histotrophic nutrition-A review. Placenta 27:S11-S16.
  11. Freyer C, Renfree MB (2008) The mammalian yolk sac placenta. J Exp Zoolog B Mol Dev Evol 312B:545-554.
  12. Gil-Sanchez A, Demmelmair H, Parrilla JJ, Koletzko B, Larque E (2011) Mechanisms involved in the selective transfer of long chain polyunsaturated fatty acids to the fetus. Front Genet 2:57.
  13. Hara M, Ma T, Verkman AS (2002) Selectively reduced glycerol in skin of squaporin-3-deficienct mice may account for impaired hydration, elasticity, and barrier recovery. J Biol Chem 227:46616-46621.
  14. Herrera E (2002) Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocrine 19:43-45. https://doi.org/10.1385/ENDO:19:1:43
  15. Herrera E, Amusquivar E, Lopez-Soldado I, Ortega H (2006) Maternal lipid metabolism and placental lipid transfer. Horm Res Paediatr 65:59-64. https://doi.org/10.1159/000091507
  16. Hua Y, Jiang W, Zhang W, Shen Q, Chen M, Zhu X (2013) Expression and significance of aquaporins during pregnancy. Front Biosci 18:1373-1383. https://doi.org/10.2741/4186
  17. Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107-117. https://doi.org/10.1007/s10157-008-0118-6
  18. Jiang SS, Zhu XJ, Ding SD, Wang JJ, Jiang LL, Jiang WX, Zhu XQ (2012) Expression and localization of aquaporins 8 and 9 in term placenta with oligohydramnios. Reprod Sci 19:1276-1284. https://doi.org/10.1177/1933719112450328
  19. Klein S, Holland OB, Wolfe RR (1990) Importance of blood glucose concentration in regulating lipolysis during fasting in humans. Am J Physiol 258:E32-E39.
  20. Kobayashi K, Yasui M (2010) Cellular and subcellular localization of aquaporins 1, 3, 8, and 9 in amniotic membranes during pregnancy in mice. Cell Tissue Res 342:307-316. https://doi.org/10.1007/s00441-010-1065-6
  21. Liu H, Zheng Z, Wintour EM (2008) Aquaporins and fetal fluid balance. Placenta 29:840-847. https://doi.org/10.1016/j.placenta.2008.07.010
  22. Ma T, Song Y, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (2000) Nephogenic diabetic insipidus in mice lacking aquaporin-3 water channels. Proc Natl Acad Sci U.S.A. 97:4386-4391. https://doi.org/10.1073/pnas.080499597
  23. Madsen EM, Lindegaard MLS, Andersen CB, Damm P, Nielsen LB (2004) Human placenta secretes apolipoprotein B-100-containing lipoproteins. J Biol Chem 275:55271-55276.
  24. Mann SE, Ricke EA, Torres EA, Tayilor RN (2005) A novel model of polyhydramnios: Amniotic fluid volume is increased in aquaporin 1 knock-out mice. Am J Obstet Gynecol 192:2041-2046. https://doi.org/10.1016/j.ajog.2005.02.046
  25. Mann SE, Ricke EA, Yang BA, Verkman AS, Taylor RN (2002) Expression and localization of aquaporin 1 and 3 in human fetal membranes. Am J Obstet Gynecol 187:902-907. https://doi.org/10.1067/mob.2002.127168
  26. Maurer ME, Cooper JA (2005) Endocytosis of megalin by visceral endoderm cells requires the Dab2 adaptor protein. J Cell Sci 118:5345-5355. https://doi.org/10.1242/jcs.02650
  27. Novak DA, Beveridge MJ (2000) Anionic amino acid transporter expression in late gestation rodent yolk sac. Placenta 21:834-839. https://doi.org/10.1053/plac.2000.0557
  28. Palis J, Yoder MC (2001) Yolk-sac hematopoiesis: The first blood cells of mouse and man. Exp Hematol 29:927-936. https://doi.org/10.1016/S0301-472X(01)00669-5
  29. Plonne D, Winkler L, Franke H, Dargel R (1992) The visceral yolk sac-an important site of synthesis and secretion of apolipoprotein B containing lipoproteins in the feto-placental unit of the rat. Biochim Biophys Acta 1127:174-185. https://doi.org/10.1016/0005-2760(92)90275-Z
  30. Rossant J, Cross JC (2001) Placental development: Lessons from mouse mutants. Nat Rev Genet 5:538-548.
  31. Schaffer JE, Lodish HF (1994) Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79:427-436. https://doi.org/10.1016/0092-8674(94)90252-6
  32. Sheng G, Foley AC (2012) Diversification and conservation of the extraembryonic tissues in mediating nutrient uptake during amniote development. Ann NY Acad Sci 1271:97-103. https://doi.org/10.1111/j.1749-6632.2012.06726.x
  33. Takata K, Kasahara T, Kasahara M, Ezaki O, Hirano H (1994) Immunolocalization of glucose transporter GLUT1 in the rat placental barrier: Possible role of GLUT1 and the gap junction in the transport of glucose across the placental barrier. Cell Tissue Res 276:411-418. https://doi.org/10.1007/BF00343939
  34. Verkman AS (2005) Novel roles of aquaporins revealed by phenotype analysis of knock-out mice. Rev Physiol Biochem Pharmacol 155:31-55.
  35. Verkman AS (2011) Aquaporins at a glance. J Cell Sci 124:2107-2112. https://doi.org/10.1242/jcs.079467
  36. Wang F, Feng XC, Li YM, Yang H, Ma TH (2006) Aquaporins as potential drug targets. Acta Pharmacol Sin 27:395-401. https://doi.org/10.1111/j.1745-7254.2006.00318.x
  37. Zhu XQ, Jiang SS, Zhu XJ, Zou SW, Wang YH, Hu YC (2009) Expression of aquaporin 1 and aquaporin 3 in fetal membranes and placenta in human term pregnancies with oligohydramnios. Placenta 30:670-676. https://doi.org/10.1016/j.placenta.2009.05.010
  38. Zhu X, Jiang S, Hu Y, Zheng X, Zou S, Wang Y, Zhu X (2010) The expression of aquaporin 8 and aquaporin 9 in fetal membranes and placenta in term pregnancies complicated by idiopathic polyhydramnios. Early Hum Dev 86:657-663. https://doi.org/10.1016/j.earlhumdev.2010.07.012