Skip to main content

Advertisement

SpringerLink
Log in

Regional Expression of Aquaporin 1, 4, and 9 in the Brain During Pregnancy

  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Pregnancy is a state of physiologic adaptation, with significant changes in cardiovascular, renal, and hemodynamic systems. Aquaporins (AQPs) may play a role in facilitating these changes. While AQP expression has been assessed in several organs during pregnancy, little is known about its expression in the brain during pregnancy. Therefore, this study assesses the regional expression of AQP1, 4, and 9 during pregnancy and the postpartum period using real-time quantitative polymerase chain reaction. The authors show that AQP1, 4, and 9 are expressed in the anterior and posterior cerebrum, cerebellum, and brainstem of nonpregnant, midpregnant, late pregnant, and postpartum rats. The regional distribution pattern of AQP4 and 9 remained similar during gestation, whereas this pattern changed for AQP1. The expression levels of AQP1, 4, and 9 in the brainstem did not change with gestation, whereas changes were found in the anterior cerebrum for AQP4 and in the posterior cerebrum and cerebellum for all AQPs.

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. Agre P, King LS, Yasui M, et al. Aquaporin water channels- from atomic structure to clinical medicine. J Physiol. 2002; 542:3–16.

    Article  CAS  PubMed  Google Scholar 

  2. Tsukaguchi H, Shayakul C, Berger UV, et al. Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem. 1998;273:24737–24743.

    Article  CAS  PubMed  Google Scholar 

  3. Agre P, Bonhivers M, Borgnia MJ. The aquaporins: blueprints for cellular plumbing systems. JBiol Chem. 1998;273:14659–14662.

    Article  CAS  Google Scholar 

  4. Badaut J, Brunet JF, Regli L. Aquaporins in the brain: from aqueduct to “multi-duct.” Metab Brain Dis. 2007;22:251–263.

    Article  CAS  PubMed  Google Scholar 

  5. Badaut J, Lasbennes F, Magistretti PJ, Regli L. Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab. 2002;22:367–378.

    Article  CAS  PubMed  Google Scholar 

  6. Nielsen S, Smith BL, Christensen EI, Agre P. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci U S A. 1993;90:7275–7279.

    Article  CAS  PubMed  Google Scholar 

  7. Praetorius J, Nielsen S. Distribution of sodium transporters and aquaporin-1 in the human choroid plexus. Am J Physiol Cell Physiol. 2006;291:C59–C67.

    Article  CAS  PubMed  Google Scholar 

  8. Oshio K, Watanabe H, Song Y, Verkman AS, Manley GT. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel aquaporin-1. FASEB J. 2005;19:76–78.

    Article  CAS  PubMed  Google Scholar 

  9. Venero JL, Vizuete ML, Ilundain AA, Machado A, Echevarria M, Cano J. Detailed localization of aquaporin-4 messenger RNA in the CNS: preferential expression in periventricular organs. Neuroscience. 1999;94:239–250.

    Article  CAS  PubMed  Google Scholar 

  10. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci. 1997;17:171–180.

    Article  CAS  PubMed  Google Scholar 

  11. Amiry-Moghaddam M, Ottersen OP. The molecular basis of water transport in the brain. Nat Rev Neurosci. 2003;4:991–1001.

    Article  CAS  PubMed  Google Scholar 

  12. Kobayashi H, Minami S, Itoh S, et al. Aquaporin subtypes in rat cerebral microvessels. Neurosci Lett. 2001;297:163–166.

    Article  CAS  PubMed  Google Scholar 

  13. Ishida H, Takemori K, Dote K, Ito H. Expression of glucose transporter-1 and aquaporin-4 in the cerebral cortex of stroke-prone spontaneously hypertensive rats in relation to the blood-brain barrier function. Am J Hypertens. 2006;19:33–39.

    Article  CAS  PubMed  Google Scholar 

  14. Nagelhus EA, Mathiisen TM, Ottersen OP. Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience. 2004;129:905–913.

    Article  CAS  PubMed  Google Scholar 

  15. Badaut J, Nehlig A, Verbavatz J, Stoeckel M, Freund-Mercier MJ, Lasbennes F. Hypervascularization in the magnocellular nuclei of the rat hypothalamus: relationship with the distribution of aquaporin-4 and markers of energy metabolism. J Neuroendocrinol. 2000;12:960–969.

    Article  CAS  PubMed  Google Scholar 

  16. Elkjaer M, Vajda Z, Nejsum LN, et al. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun. 2000;276:1118–1128.

    Article  CAS  PubMed  Google Scholar 

  17. Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L. Distribution of aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience. 2004;128:27–38.

    Article  CAS  PubMed  Google Scholar 

  18. Quick AM, Cipolla MJ. Pregnancy-induced up-regulation of aquaporin-4 protein in brain and its role in eclampsia. FASEB J. 2005;19:170–175.

    Article  CAS  PubMed  Google Scholar 

  19. Monga M. Maternal cardiovascular and renal adaptation to pregnancy. In: Creasy R, Resnik R, Iams J, eds. Maternal-Fetal Medicine: Principles and Practice. Philadelphia, PA: Saunders; 2004:111–120.

    Google Scholar 

  20. Robson SC, Hunter S, Boys RJ, Dunlop W. Serial study of factors influencing changes in cardiac output during human pregnancy. Am J Physiol. 1989;256:H1060–1065.

    CAS  PubMed  Google Scholar 

  21. Ohara M, Martin PY, Xu DL, et al. Upregulation of aquaporin 2 water channel expression in pregnant rats. J Clin Invest. 1998;101:1076–1083.

    Article  CAS  PubMed  Google Scholar 

  22. 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.

    Article  CAS  PubMed  Google Scholar 

  23. Dolman D, Drndarski S, Abbott NJ, Rattray M. Induction of aquaporin 1 but not aquaporin 4 messenger RNA in rat primary brain microvessel endothelial cells in culture. J Neurochem. 2005;93:825–833.

    Article  CAS  PubMed  Google Scholar 

  24. Taniguchi M, Yamashita T, Kumura E, et al. Induction of aquaporin-4 water channel mRNA after focal cerebral ischemia in rat. Brain Res Mol Brain Res. 2000;78:131–137.

    Article  CAS  PubMed  Google Scholar 

  25. Ribeiro Mde C, Hirt L, Bogousslavsky J, Regli L, Badaut J. Time course of aquaporin expression after transient focal cerebral ischemia in mice. J Neurosci Res. 2006;83:1231–1240.

    Article  PubMed  Google Scholar 

  26. Amiry-Moghaddam M, Otsuka T, Hurn PD, et al. An alphasyntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci U S A. 2003;100:2106–2111.

    Article  CAS  PubMed  Google Scholar 

  27. Meng S, Qiao M, Lin L, Del Bigio MR, Tomanek B, Tuor UI. Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur J Neurosci. 2004;19:2261–2269.

    Article  PubMed  Google Scholar 

  28. Saadoun S, Papadopoulos MC, Davies DC, Krishna S, Bell BA. Aquaporin-4 expression is increased in oedematous human brain tumours. JNeurol Neurosurg Psychiatry. 2002;72:262–265.

    Article  CAS  Google Scholar 

  29. Vizuete ML, Venero JL, Vargas C, et al. Differential upregulation of aquaporin-4 mRNA expression in reactive astrocytes after brain injury: potential role in brain edema. Neurobiol Dis. 1999;6:245–258.

    Article  CAS  PubMed  Google Scholar 

  30. Ke C, Poon WS, Ng HK, Pang JC, Chan Y. Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci Lett. 2001;301:21–24.

    Article  CAS  PubMed  Google Scholar 

  31. Kiening KL, van Landeghem FK, Schreiber S, et al. Decreased hemispheric aquaporin-4 is linked to evolving brain edema following controlled cortical impact injury in rats. Neurosci Lett. 2002;324:105–108.

    Article  CAS  PubMed  Google Scholar 

  32. Manley GT, Fujimura M, Ma T, et al. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med. 2000;6:159–163.

    Article  CAS  PubMed  Google Scholar 

  33. Papadopoulos MC, Manley GT, Krishna S, Verkman AS. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 2004;18:1291–1293.

    Article  CAS  PubMed  Google Scholar 

  34. Sibai BM. Diagnosis, prevention, and management of eclampsia. Obstet Gynecol. 2005;105:402–410.

    Article  PubMed  Google Scholar 

  35. Cunningham FG, Twickler D. Cerebral edema complicating eclampsia. Am J Obstet Gynecol. 2000;182:94–100.

    Article  CAS  PubMed  Google Scholar 

  36. Zeeman GG, Fleckenstein JL, Twickler DM, Cunningham FG. Cerebral infarction in eclampsia. Am J Obstet Gynecol. 2004;190:714–720.

    Article  PubMed  Google Scholar 

  37. Lopez-Llera M. Main clinical types and subtypes of eclampsia. Am J Obstet Gynecol. 1992;166:4–9.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Neurology, Obstetrics/Gynecology, and Pharmacology, University of Vermont, Burlington, USA

    Marchien J. Wiegman BS, Lisa V. Bullinger BS & Marilyn J. Cipolla PhD

  2. Department of Obstetrics/Gynecology, University Medical Center Groningen, Groningen, The Netherlands

    Marchien J. Wiegman BS

  3. University of Vermont DNA Analysis Core Facility, Burlington, USA

    Meghan M. Kohlmeyer BS & Timothy C. Hunter MS

Authors
  1. Marchien J. Wiegman BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lisa V. Bullinger BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meghan M. Kohlmeyer BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Timothy C. Hunter MS
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marilyn J. Cipolla PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marilyn J. Cipolla PhD.

Additional information

Work was performed at the University of Vermont, Department of Neurology, and the DNA Analysis Core Facility, Burlington, Vermont.

We gratefully acknowledge the support of the American Heart Association Established Investigator Award 0540081N (to MJC) and the National Institutes of Health National Institute of Neurologic Disorders and Stroke grant NS045940 (to MJC). We also acknowledge the continued support of the Totman Medical Research Trust.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wiegman, M.J., Bullinger, L.V., Kohlmeyer, M.M. et al. Regional Expression of Aquaporin 1, 4, and 9 in the Brain During Pregnancy. Reprod. Sci. 15, 506–516 (2008). https://doi.org/10.1177/1933719107311783

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719107311783

Key words

Search

Navigation