Skip to main content

Comparison of cardiovascular aquaporin-1 changes during water restriction between 25- and 50-day-old rats

Abstract

Purpose

Aquaporin-1 (AQP1) is the predominant water channel in the heart, linked to cardiovascular homeostasis. Our aim was to study cardiovascular AQP1 distribution and protein levels during osmotic stress and subsequent hydration during postnatal growth.

Methods

Rats aged 25 and 50 days were divided in: 3d-WR: water restriction 3 days; 3d-WAL: water ad libitum 3 days; 6d-WR+ORS: water restriction 3 days + oral rehydration solution (ORS) 3 days; and 6d-WAL: water ad libitum 6 days. AQP1 was evaluated by immunohistochemistry and western blot in left ventricle, right atrium and thoracic aorta.

Results

Water restriction induced a hypohydration state in both age groups (40 and 25 % loss of body weight in 25- and 50-day-old rats, respectively), reversible with ORS therapy. Cardiac AQP1 was localized in the endocardium and endothelium in both age groups, being evident in cardiomyocytes membrane only in 50-day-old 3d-WR group, which presented increased protein levels of AQP1; no changes were observed in the ventricle of pups. In vascular tissue, AQP1 was present in the smooth muscle of pups; in the oldest group, it was found in the endothelium, increasing after rehydration in smooth muscle. No differences were observed between control groups 3d-WAL and 6d-WAL of both ages.

Conclusion

Our findings suggest that cardiovascular AQP1 can be differentially regulated in response to hydration status in vivo, being this response dependent on postnatal growth. The lack of adaptive mechanisms of mature animals in young pups may indicate an important role of this water channel in maintaining fluid balance during hypovolemic state.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    Manz F (2007) Hydration in children. J Am Coll Nutr 26:562S–569S

    Article  Google Scholar 

  2. 2.

    Steiner M, DeWalt D, Byerley J (2004) Is this child dehydrated? JAMA 291:2746–2754

    CAS  Article  Google Scholar 

  3. 3.

    Zelenina M, Zelenin S, Aperia A (2005) Water channels (aquaporins) and their role for postnatal adaptation. Pediatr Res 57:47R–53R

    Article  Google Scholar 

  4. 4.

    Fellet AL, Arza PR, Nuñez M, Arranz CT, Balaszczuk AM (2011) Hypovolemic state: age-related influence of water restriction on cardiac nitric oxide synthase in rats. Eur J Nutr 50:657–664

    CAS  Article  Google Scholar 

  5. 5.

    Dowell RT (1984) Nutritional modification of rat heart postnatal development. Am J Physiol 246:H332–H338

    CAS  Google Scholar 

  6. 6.

    Ishii T, Kuwaki T, Masuda Y, Fukuda Y (2001) Postnatal development of blood pressure and baroreflex in mice. Auton Neurosci 94:34–41

    CAS  Article  Google Scholar 

  7. 7.

    Davey Smith GD, Leary S, Ness A (2006) The ALSPAC study team could dehydration in infancy lead to high blood pressure? J Epidemiol Community Health 60:142–143

    Google Scholar 

  8. 8.

    Lawlor D, Smith G, Mitchell R, Ebrahim S (2006) Adult blood pressure and climate conditions in infancy: a test of the hypothesis that dehydration in infancy is associated with higher adult blood pressure. Am J Epidemiol 163:608–614

    Article  Google Scholar 

  9. 9.

    Egan JR, Butler TL, Au CG, Tan YM, North KN, Winlaw DS (2006) Myocardial water handling and the role of aquaporins. Biochem Biophys Acta 1758:1043–1052

    CAS  Article  Google Scholar 

  10. 10.

    Butler T, Au C, Yang B, Egan J, Tan Y, Hardeman E et al (2006) Cardiac aquaporin expression in humans, rats, and mice. Am J Physiol Heart Circ Physiol 29:H705–H713

    Article  Google Scholar 

  11. 11.

    Shanahan CM, Connolly DL, Tyson KL, Cary NR, Osbourn JK, Agre P et al (1999) Aquaporin-1 is expressed by vascular smooth muscle cells and mediates rapid water transport across vascular cell membranes. J Vasc Res 36:353–362

    CAS  Article  Google Scholar 

  12. 12.

    Verkman AS (2002) Aquaporin water channels and endothelial cell function. J Anat 200:617–627

    CAS  Article  Google Scholar 

  13. 13.

    Miller RT (2004) Aquaporin in the heart—only for water? J Mol Cell Cardiol 36:653–654

    CAS  Article  Google Scholar 

  14. 14.

    Ran X, Wang H, Chen Y, Zeng Z, Zhou Q, Zheng R et al (2010) Aquaporin-1 expression and angiogenesis in rabbit chronic myocardial ischemia is decreased by acetazolamide. Heart Vessels 25:237–247

    Article  Google Scholar 

  15. 15.

    Jonker S, Davis LE, Van Der Bilt JD, Hadder B, Hohimer AR, Giraud GD et al (2003) Anaemia stimulates aquaporin 1 expression in the fetal sheep heart. Exp Physiol 88:691–698

    CAS  Article  Google Scholar 

  16. 16.

    Jenq W, Mathieson I, Ihara W, Ramirez G (1998) Aquaporin-1: an osmoinducible water channel in cultured mIMCD-3 Cells. Biochem Biophys Res Comun 245:804–809

    CAS  Article  Google Scholar 

  17. 17.

    Bouley R, Palomino Z, Tang SS, Nunes P, Kobori H, Lu HA et al (2009) Angiotensin II and hypertonicity modulate proximal tubular aquaporin 1 expression. Am J Physiol Renal Physiol 297:F1575–F1586

    CAS  Article  Google Scholar 

  18. 18.

    Ota T, Kuwahara M, Fan S, Terada Y, Akiba T, Sasaki S et al (2002) Expression of aquaporin-1 in the peritoneal tissues: localization and regulation by hyperosmolality. Perit Dial Int 22:307–315

    CAS  Google Scholar 

  19. 19.

    Caeiro JP, DuPont HL, Albrecht H, Ericsson CD (1999) Oral rehydration therapy plus loperamide versus loperamide alone in the treatment of traveler’s diarrhea. Clin Infect Dis 28:1286–1289

    CAS  Article  Google Scholar 

  20. 20.

    Gao J, Wang X, Chang Y, Zhang J, Song Q, Yu H et al (2006) Acetazolamide inhibits osmotic water permeability by interaction with aquaporin-1. Anal Biochem 350:165–170

    CAS  Article  Google Scholar 

  21. 21.

    Balaszczuk AM, Tomat A, Bellucci S, Fellet A, Arranz C (2002) Nitric oxide synthase blockade and body fluid volumes. Braz J Med Biol Res 35:131–134

    CAS  Article  Google Scholar 

  22. 22.

    Zhang H, Verkman AS (2009) Aquaporin-1 tunes pain perception by interaction with Nav1.8 Na channels in dorsal root ganglion neurons. J Biol Chem 285:5896–5906

    Article  Google Scholar 

  23. 23.

    Wathen JE, MacKenzie T, Bothner JP (2004) Usefulness of the serum electrolyte panel in the management of pediatric dehydration treated with intravenously administered fluids. Pediatrics 114:1227–1234

    Article  Google Scholar 

  24. 24.

    Devuyst O, Nielsen S, Cosyns JP, Smith BL, Agre P, Squifflet JP et al (1998) Aquaporin-1 and endothelial nitric oxide synthase expression in capillary endothelia of human peritoneum. Am J Physiol Heart Circ Physiol 275:H234–H242

    CAS  Google Scholar 

  25. 25.

    Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV et al (2006) Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J 20:1974–1981

    CAS  Article  Google Scholar 

  26. 26.

    Herrera M, Garvin JL (2007) Novel role of AQP-1 in NO-dependent vasorelaxation. Am J Physiol Renal Physiol 292:1443–1451

    Article  Google Scholar 

  27. 27.

    Umenishi F, Schrier RW (2003) Hypertonicity-induced Aquaporin-1 expression is mediated by the activation of MAPK pathways and hypertonicity-responsive element in the AQP1 gene. J Biol Chem 278:15765–15770

    CAS  Article  Google Scholar 

  28. 28.

    Leitch V, Agre P, King LS (2001) Altered ubiquitination and stability of aquaporin-1 in hypertonic stress. PNAS 98:2894–2898

    CAS  Article  Google Scholar 

  29. 29.

    Burg MB, Ferraris JD, Dmitrieva NI (2007) Cellular response to hyperosmotic stresses. Physiol Rev 87:1441–1474

    CAS  Article  Google Scholar 

  30. 30.

    Yeung CH, Callies C, Rojek A, Nielsen S, Cooper TG (2009) Aquaporin isoforms involved in physiological volume regulation of murine spermatozoa. Biol Reprod 80:350–357

    CAS  Article  Google Scholar 

  31. 31.

    Bondy C, Chin E, Smith BL, Preston GM, Agre P (1993) Developmental gene expression and tissue distribution of the CHIP28 water-channel protein. PNAS 90:4500–4504

    CAS  Article  Google Scholar 

  32. 32.

    Yamamoto T, Sasaki S, Fushimi K, Ishibashi K, Yaoita E, Kawasaki K, Fujinaka H, Marumo F, Kihara I (1997) Expression of AQP family in rat kidneys during development and maturation. Am J Physiol Renal Physiol 272:F198–F204

    CAS  Google Scholar 

  33. 33.

    Muñoz-Cabello AM, Villadiego J, Toledo-Aral JJ, López-Barneo J, Echevarría M (2010) AQP1 mediates water transport in the carotid body. Eur J Physiol 459:775–783

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the University of Buenos Aires, Argentina, Grant 20020100100068. The authors wish to thank Carla Martinez and Myriam Nuñez from University of Buenos Aires, School of Pharmacy and Biochemistry, for assistance in statistical analysis.

Conflict of interest

The authors declare no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Vanina A. Netti.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Netti, V.A., Vatrella, M.C., Chamorro, M.F. et al. Comparison of cardiovascular aquaporin-1 changes during water restriction between 25- and 50-day-old rats. Eur J Nutr 53, 287–295 (2014). https://doi.org/10.1007/s00394-013-0527-5

Download citation

Keywords

  • Aquaporin-1
  • Dehydration
  • Heart
  • Postnatal growth
  • Vascular tissue