Skip to main content
SpringerLink
Log in

Clinical application of aquaporin research: aquaporin-1 in the peritoneal membrane

  • Invited Review
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Peritoneal dialysis (PD) is an established mode of renal replacement therapy based on the exchange of fluid and solutes between blood and a dialysate that has been instilled in the peritoneal cavity. The dialysis process involves osmosis, as well as diffusive and convective transports through the highly vascularized peritoneal membrane. Computer simulations predicted that the membrane contains ultrasmall pores responsible for the selective transport of water across the capillary endothelium during crystalloid osmosis. The distribution of the water channel aquaporin-1 (AQP1), as well as its molecular structure ensuring an exquisite selectivity for water, fit with the characteristics of the ultrasmall pore. Peritoneal transport studies using AQP1 knockout mice demonstrated that the osmotic water flux across the peritoneal membrane is mediated by AQP1. This water transport accounts for 50% of the ultrafiltration during PD. Treatment with high-dose corticosteroids upregulates the expression of AQP1 in peritoneal capillaries, resulting in increased water transport and ultrafiltration in rats. AQP1 may also play a role during inflammation, as vascular proliferation and leukocyte recruitment are both decreased in mice lacking AQP1. These data illustrate the potential of the peritoneal membrane as an experimental model in the investigation of the role of AQP1 in the endothelium at baseline and during inflammation. They emphasize the critical role of AQP1 during PD and suggest that manipulating AQP1 expression could be clinically useful in PD patients.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Agre P (2004) Aquaporin water channels (Nobel Lecture). Angew Chem Int Ed Engl 43:4278–4290

    Article  PubMed  CAS  Google Scholar 

  2. Carlsson O, Nielsen S, el Zakaria R, Rippe B (1996) In vivo inhibition of transcellular water channels (aquaporin-1) during acute peritoneal dialysis in rats. Am J Physiol 271:H2254–H2262

    PubMed  CAS  Google Scholar 

  3. Churchill DN, Thorpe KE, Nolph KD, Keshaviah PR, Oreopoulos DG, Page D (1998) Increased peritoneal membrane transport is associated with decreased patient and technique survival for continuous peritoneal dialysis patients. The Canada–USA (CANUSA) Peritoneal Dialysis Study Group. J Am Soc Nephrol 9:1285–1292

    PubMed  CAS  Google Scholar 

  4. Combet S, Balligand JL, Lameire N, Goffin E, Devuyst O (2000) A specific method for measurement of nitric oxide synthase enzymatic activity in peritoneal biopsies. Kidney Int 57:332–338

    Article  PubMed  CAS  Google Scholar 

  5. Combet S, Van Landschoot M, Moulin P, Piech A, Verbavatz JM, Goffin E, Balligand JL, Lameire N, Devuyst O (1999) Regulation of aquaporin-1 and nitric oxide synthase isoforms in a rat model of acute peritonitis. J Am Soc Nephrol 10:2185–2196

    PubMed  CAS  Google Scholar 

  6. Davies SJ, Phillips L, Griffiths AM, Russell LH, Naish PF, Russell GI (1998) What really happens to people on long-term peritoneal dialysis. Kidney Int 54:2207–2217

    Article  PubMed  CAS  Google Scholar 

  7. Denker BM, Smith BL, Kuhajda FP, Agre P (1988) Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642

    PubMed  CAS  Google Scholar 

  8. Devuyst O, Nielsen S, Cosyns JP, Smith BL, Agre P, Squifflet JP, Pouthier D, Goffin E (1998) quaporin-1 and endothelial nitric oxide synthase expression in capillary endothelia of human peritoneum. Am J Physiol 275:H234–H242

    PubMed  CAS  Google Scholar 

  9. Ferrier ML, Combet S, van Landschoot M, Stoenoiu MS, Cnops Y, Lameire N, Devuyst O (20001) Inhibition of nitric oxide synthase reverses changes in peritoneal permeability in a rat model of acute peritonitis. Kidney Int 60:2343–2350

    Article  Google Scholar 

  10. Flessner MF (2005) The transport barrier in intraperitoneal therapy. Am J Physiol Renal Physiol 288:F433–F442

    Article  PubMed  CAS  Google Scholar 

  11. Goffin E, Combet S, Jamar F, Cosyns JP, Devuyst O (1999) Expression of aquaporin-1 in a long-term peritoneal dialysis patient with impaired transcellular water transport. Am J Kidney Dis 33:383–388

    Article  PubMed  CAS  Google Scholar 

  12. Gokal R, Mallick NP (1999) Peritoneal dialysis. Lancet 353:823–828

    Article  PubMed  CAS  Google Scholar 

  13. King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698

    Article  PubMed  CAS  Google Scholar 

  14. King LS, Nielsen S, Agre P (1996) Aquaporin-1 water channel protein in lung: ontogeny, steroid-induced expression, and distribution in rat. J Clin Invest 97:2183–2191

    Article  PubMed  CAS  Google Scholar 

  15. Kishida K, Kuriyama H, Funahashi T, Shimomura I, Kihara S, Ouchi N, Nishida M, Nishizawa H, Matsuda M, Takahashi M, Hotta K, Nakamura T, Yamashita S, Tochino Y, Matsuzawa Y (2000) Aquaporin adipose, a putative glycerol channel in adipocytes. J Biol Chem 275:20896–20902

    Article  PubMed  CAS  Google Scholar 

  16. Kone BC (1997) Nitric oxide in renal health and disease. Am J Kidney Dis 30:311–333

    Article  PubMed  CAS  Google Scholar 

  17. Krane CM, Goldstein DL (2007) Comparative functional analysis of aquaporins/glyceroporins in mammals and anurans. Mamm Genome 18:452–462

    Article  PubMed  CAS  Google Scholar 

  18. Krediet RT (2000) The physiology of peritoneal solute transport and ultrafiltration. In: Gokal R, Khanna R, Krediet RT, Nolph KD (eds) Textbook of peritoneal dialysis. Kluwer, Dordrecht, pp 135–172

    Google Scholar 

  19. Lai KN, Li FK, Lan HY, Tang S, Tsang AW, Chan DT, Leung JC (2001) Expression of aquaporin-1 in human peritoneal mesothelial cells and its upregulation by glucose in vitro. J Am Soc Nephrol 12:1036–1045

    PubMed  CAS  Google Scholar 

  20. Lysaght MJ (2002) Maintenance dialysis population dynamics: current trends and long-term implications. J Am Soc Nephrol 13:S37–S40

    Article  PubMed  Google Scholar 

  21. Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1998) Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J Biol Chem 273:4296–4299

    Article  PubMed  CAS  Google Scholar 

  22. Maeda N, Funahashi T, Hibuse T, Nagasawa A, Kishida K, Kuriyama H, Nakamura T, Kihara S, Shimomura I, Matsuzawa Y (2004) Adaptation to fasting by glycerol transport through aquaporin 7 in adipose tissue. Proc Natl Acad Sci U S A 101:17801–17806

    Article  PubMed  CAS  Google Scholar 

  23. Moon C, King LS, Agre P (1997) Aqp1 expression in erythroleukemia cells: genetic regulation of glucocorticoid and chemical induction. Am J Physiol 273:C1562–C1570

    PubMed  CAS  Google Scholar 

  24. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605

    Article  PubMed  CAS  Google Scholar 

  25. Ni J, Cnops Y, Debaix H, Boisdé I, Verbavatz JM, Devuyst O (2005) Functional and molecular characterization of a peritoneal dialysis model in the C57BL/6J mouse. Kidney Int 67:2021–2031

    Article  PubMed  CAS  Google Scholar 

  26. Ni J, Moulin P, Gianello P, Feron O, Balligand JL, Devuyst O (2003) Mice that lack endothelial nitric oxide synthase are protected against functional and structural modifications induced by acute peritonitis. J Am Soc Nephrol 14:3205–3216

    Article  PubMed  CAS  Google Scholar 

  27. Ni J, Verbavatz JM, Rippe A, Boisdé I, Moulin P, Rippe B, Verkman AS, Devuyst O (2006) Aquaporin-1 plays an essential role in water permeability and ultrafiltration during peritoneal dialysis. Kidney Int 69:1518–1525

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  29. Nishino T, van Loo G, Moulin P, Beyaert R, Verkman AS, Devuyst O (2007) Aquaporin-1 modulates vascular proliferation and inflammatory response during acute infection. J Am Soc Nephrol 18:112A

    Google Scholar 

  30. Nolph KD, Ghods A, Brown PA, Miller F, Harris PD, Pyle K, Popovich R (1977) Effects of nitroprusside on peritoneal mass transfer coefficients and microvascular physiology. ASAIO Trans 23:210–218

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  32. Preston GM, Piaza Caroll T, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cells CHIP 28 protein. Science 256:385–387

    Article  PubMed  CAS  Google Scholar 

  33. Rippe B, Stelin G, Haraldsson B (1991) Computer simulations of peritoneal fluid transport in CAPD. Kidney Int 40:315–325

    Article  PubMed  CAS  Google Scholar 

  34. Rippe B, Venturoli D, Simonsen O, de Arteaga J (2004) Fluid and electrolyte transport across the peritoneal membrane during CAPD according to the three-pore model. Perit Dial Int 24:10–27

    PubMed  CAS  Google Scholar 

  35. Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792

    Article  PubMed  CAS  Google Scholar 

  36. Skowronski MT, Lebeck J, Rojek A, Praetorius J, Füchtbauer EM, Frokiaer J, Nielsen S (2007) AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. Am J Physiol Renal Physiol 292:F956–F965

    Article  PubMed  CAS  Google Scholar 

  37. Smit W, de Waart DR, Struijk DG, Krediet RT (2000) Peritoneal transport characteristics with glycerol-based dialysate in peritoneal dialysis. Perit Dial Int 20:557–565

    PubMed  CAS  Google Scholar 

  38. Smit W, Struijk DG, Ho-Dac-Pannekeet MM, Krediet RT (2004) Quantification of free water transport in peritoneal dialysis. Kidney Int 66:849–854

    Article  PubMed  Google Scholar 

  39. Stoenoiu MS, Ni J, Verkaeren C, Debaix H, Jonas JC, Lameire N, Verbavatz JM, Devuyst O (2003) Corticosteroids induce expression of aquaporin-1 and increase transcellular water transport in rat peritoneum. J Am Soc Nephrol 14:555–565

    Article  PubMed  CAS  Google Scholar 

  40. Teitelbaum I, Burkart J (2003) Peritoneal dialysis. Am J Kidney Dis 42:1082–1096

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  42. White R, Granger DN (2000) The peritoneal microcirculation in peritoneal dialysis. In: Gokal R, Khanna R, Krediet RT, Nolph KD (eds) Textbook of peritoneal dialysis. Kluwer, Dordrecht, pp 107–133

    Google Scholar 

  43. Yang B, Folkesson HG, Yang J, Matthay MA, Ma T, Verkman AS (1999) Reduced osmotic water permeability of the peritoneal barrier in aquaporin-1 knockout mice. Am J Physiol 276:C76–C81

    PubMed  CAS  Google Scholar 

  44. Zeidel ML, Ambudkar SV, Smith BL, Agre P (1992) Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 31:7436–7440

    Article  PubMed  CAS  Google Scholar 

  45. Zeidel ML, Nielsen S, Smith BL, Ambudkar SV, Maunsbach AB, Agre P (1994) Ultrastructure, pharmacologic inhibition, and transport selectivity of aquaporin channel-forming integral protein in proteoliposomes. Biochemistry 33:1606–1615

    Article  PubMed  CAS  Google Scholar 

  46. Zweers MM, Douma CE, de Waart DR, Korevaar JC, Krediet RT, Struijk DG (2001) Amphotericin B, mercury chloride and peritoneal transport in rabbits. Clin Nephrol 56:60–68

    PubMed  CAS  Google Scholar 

Download references

Acknowledgment

Our studies are supported in part by the Belgian agencies FNRS and FRSM, the ARC 05/10-328, the Société de Néphrologie (Paris, France), and grants from Baxter Healthcare and the Sumitomo Life Social Welfare Services Foundation. We thank P. Agre, J.-L. Balligand, S. Combet, P. Deen, C. Delporte, G. Gillerot, E. Goffin, H. Debaix, R. Krediet, N. Lameire, B. Lindholm, P. Moulin, S. Nielsen, A. Rippe, B. Rippe, S. Sasaki, M. Stoenoiu, N. Topley, S. Uchida, J.-M. Verbavatz, and A. S. Verkman for fruitful collaborations and discussions, and Y. Cnops, H. Debaix, and S. Druart for superb technical assistance in developing the dialysis techniques in mouse models.

Author information

Authors and Affiliations

  1. Division of Renal Care Unit, Second Department of Internal Medicine, Nagasaki University School of Medicine, Nagasaki, Japan

    Tomoya Nishino

  2. Division of Nephrology, Université Catholique de Louvain Medical School, 10 Avenue Hippocrate, 1200, Brussels, Belgium

    Olivier Devuyst

Authors
  1. Tomoya Nishino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olivier Devuyst
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olivier Devuyst.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nishino, T., Devuyst, O. Clinical application of aquaporin research: aquaporin-1 in the peritoneal membrane. Pflugers Arch - Eur J Physiol 456, 721–727 (2008). https://doi.org/10.1007/s00424-007-0402-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-007-0402-4

Keywords

Search

Navigation