Membrane dynamics of the water transport protein aquaporin-1 in intact human red cells

Biophysical Journal

Volumn 76, Issue 2, 1999, Pages 1136-1144

  Cho, Michael R ^a   Knowles, David W ^b   Smith, Barbara L ^d   Moulds, John J ^c   Agre, Peter ^d   Mohandas, Narla ^b   Golan, David E ^a,e  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Gamma Biologicals Inc   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN;

ARTICLE; BLEACHING; DIFFUSION; ERYTHROCYTE MEMBRANE; HUMAN; MOLECULAR DYNAMICS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STEREOSPECIFICITY;

EID: 0032987718     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77278-4     Document Type: Article

References (49)

1. Agre, P., G. M. Preston, B. L. Smith, J. S. Jung, S. Raina, C. Moon, W. B. Guggino, and S. Nielsen. 1993. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol. 265:F463-F476.
2. Axelrod, D., D. E. Koppel, J. Schlessinger, E. Elson, and W. W. Webb. 1976. Mobility measurements by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16:1055-1069.
3. Bennett, V. 1983. Proteins involved in membrane-cytoskeleton association in human erythrocyte: spectrin, ankyrin, and band 3. Methods Enzymol. 96:313-324.
4. Berk, D. A., and R. M. Hochmuth. 1992. Lateral mobility of integral proteins in red blood cell tethers. Biophys. J. 61:9-18.
5. Bevington, P. R. 1969. Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York.
6. Chasis, J. A., N. Mohandas, and S. Shohet. 1985. Erythrocyte membrane rigidity induced by glycophorin A-ligand interaction. Evidence for a ligand-induced association between glycophorin A and skeletal proteins. J. Clin. Invest. 75:1919-1926.
7. Chasis, J. A., M. Reid, R. Jensen, and N. Mohandas. 1988. Signal transduction by glycophorin A: role of extracellular and cytoplasmic domains in a modulatable process. J. Cell Biol. 107:1351-1357.
8. Cheng, A., A. van Hoek, M. Yeager, A. Verkman, and A. Mitra. 1997. Three-dimensional organization of a human water channel. Nature. 387:627-630.
9. Cho, M. R., S. W. Eber, S. E. Lux, and D. E. Golan. 1999. Regulation of band 3 rotational mobility by ankyrin in intact human red cells. Biochemistry. In press.
10. Corbett, J. D., P. Agre, J. Palek, and D. E. Golan. 1994a. Differential control of band 3 lateral and rotational mobility in intact red cells. J. Clin. Invest. 94:683-688.
11. Corbett, J. D., M. R. Cho, and D. E. Golan. 1994b. Deoxygenation affects fluorescence photobleaching recovery measurements of red cell membrane protein lateral mobility. Biophys. J. 66:25-30.
12. Corbett, J. D., and D. E. Golan. 1993. Band 3 and glycophorin are progressively aggregated in density-fractionated sickle and normal red blood cells. J. Clin. Invest. 91:208-217.
13. r 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263:15634-15642.
14. Discher, D. E., and N. Mohandas. 1996. Kinematics of red cell aspiration by fluorescence-imaged microdeformation. Biophys. J. 71:1680-1694.
15. Discher, D. E., N. Mohandas, and E. A. Evans. 1994. Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science. 266:1032-1035.
16. Discher, D. E., R. Winardi, P. Schischmanoff, M. Parra, J. Conboy, and N. Mohandas. 1995. Mechanochemistry of protein 4.1's spectrin-actin-binding domain: ternary complex interactions, membrane binding, network integration, structural strengthening. J. Cell Biol. 130:897-907.
17. Ecelbarger, C., J. Terris, G. Frindt, M. Echevarria, D. Marples, S. Nielsen, and M. Knepper. 1995. Aquaporin-3 water channel localization and regulation in rat kidney. Am J. Physiol. 269:F663-F672.
18. Elkjaer, M., H. Birn, P. Agre, E. Christensen, and S. Nielsen. 1995. Effects of microtubule disruption on endocytosis, membrane recycling and polarized distribution of aquaporin-1 and gp330 in proximal tubule cells. Eur. J. Cell Biol. 67:57-72.
19. Feder, T. J., I. Brust-Mascher, J. P. Slattery, B. Baird, and W. W. Webb. 1996. Constrained diffusion or immobile fraction on cell surface: a new interpretation. Biophys. J. 70:2767-2773.
20. Frigeri, A., M. A. Gropper, F. Umenishi, M. Kawashima, D. Brown, and A. S. Verkman. 1995. Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J. Cell Sci. 108:2993-3002.
21. Golan, D. E. 1989. Red blood cell membrane protein and lipid diffusion. In Red Cell Membrane. P. Agre and J. C. Parker, editors. Marcel Dekker, New York, 367-400.
22. Golan, D. E., M. R. Alecio, W. R. Veatch, and R. R. Rando. 1984. Lateral mobility of phospholipid and cholesterol in the human erythrocyte membrane: effects of protein-lipid interactions. Biochemistry. 23: 332-339.
23. Golan, D. E., J. D. Corbett, C. Korsgren, H. S. Thatte, S. Hayette, Y. Yawata, and C. M. Cohen. 1996. Control of band 3 lateral and rotational mobility by band 4.2 in intact erythrocytes: release of band 3 oligomers from low-affinity binding sites. Biophys. J. 70:1534-1542.
24. Golan, D. E., and W. Veatch. 1980. Lateral mobility of band 3 in the human erythrocyte membrane studied by fluorescence photobleaching recovery: evidence for control by cytoskeletal interactions. Proc. Natl. Acad. Sci. USA. 77:2537-2541.
25. Jarolim, P., H. L. Lubin, S. C. Liu, M. R. Cho, V. Brabec, L. H. Derick, S. J. Yi, S. T. Saad, S. Alper, C. Brugnara, D. E. Golan, and J. Palek. 1994. Duplication of 10 nucleotides in the erythroid band 3 (AE1) gene in a kindred with hereditary spherocytosis and band 3 protein deficiency. J. Clin. Invest. 93:121-130.
26. Jung, J. S., G. M. Preston, B. L. Smith, W. B. Guggino, and P. Agre. 1994. Molecular structure of the water channel through aquaporin CHIP: the hourglass model. J. Biol. Chem. 269:14648-14654.
27. Knowles, D. W., J. A. Chasis, E. A. Evans, and N. Mohandas. 1994. Cooperative action between band 3 and glycophorin A in human erythrocytes: immobilization of band 3 induced by antibodies to glycophorin A. Biophys. J. 66:1726-1732.
28. Knowles, D. W., L. Tilley, N. Mohandas, and J. A. Chasis. 1997. Erythrocyte membrane vesiculation: model for the molecular mechanism of protein sorting. Proc. Natl. Acad. Sci. USA. 94:12969-12974.
29. Lacey, P. A., J. Robinson, M. L. Collins, D. G. Bailey, C. C. Evans, J. J. Moulds, and G. L. Daniels. 1987. Studies on the blood of a Co(a-b-) proposita and her family. Transfusion. 27:268-271.
30. Li, H., S. Lee, and B. Jap. 1997. Molecular design of aquaporin-1 water channel as revealed by electron crystallography. Nature Struct. Biol. 4:263-265.
31. Liu, S. C., J. Palek, S. J. Yi, P. E. Nichols, L. H. Derick, S. S. Chiou, D. Amato, J. D. Corbett, M. R. Cho, and D. E. Golan. 1995. Molecular basis of altered red cell membrane properties in Southeast Asian ovalocytosis: role of the mutant band 3 protein in band 3 oligomerization and retention by the membrane skeleton. Blood. 86:349-358.
32. Liu, S. C, S. Zhai, J. Palek, D. E. Golan, K. Amato, G. Hassan, T. Nurse, D. Babona, T. Coetzer, P. Jarolim, M. Zaik, and S. Borwein. 1990. Molecular defect of the band 3 protein in Southeast Asian ovalocytosis. N. Engl. J. Med. 323:1530-1538.
33. Lux, S. E., and J. Palek. 1995. Disorders of the red cell membrane. In Blood: Principles and Practice of Hematology. R. I. Handin, S. E. Lux, and T. P. Stossel, editors. J. B. Lippincott, Philadelphia. 1701-1818.
34. Marinelli, R., L. Pham, P. Agre, and N. LaRusso. 1997. Secretin promotes osmotic water transport in rat cholangiocytes by increasing aquaporin-1 water channels in plasma membrane. Evidence for a secretin-induced vesicular translocation of aquaporin-1. J. Biol. Chem. 272: 12984-12988.
35. Minton, A. P. 1989. Lateral diffusion of membrane proteins in protein-rich membranes: a simple hard particle model for concentration dependence of the two-dimensional diffusion coefficient. Biophys. J. 55:805-808.
36. Mohandas, N., and E. Evans. 1994. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Biophys. Biomol. Struct. 23:787-818.
37. Moulds, J. J., D. Mallory, and V. Zodin. 1978. Placental eluates: an economical source of antibodies. Transfusion. 18:388-389 (Abstr.).
38. Nash, G. B., and W. B. Gratzer. 1993. Structural determinants of the rigidity of the red cell membrane. Biorheology. 30:397-407.
39. Nielsen, S., L. King, B. Christensen, and P. Agre. 1997. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am. J. Physiol. 273:C1549-C1561.
40. Nielsen, S., B. L. Smith, E. I. Christensen, M. A. Knepper, and P. Agre. 1993. Distribution of aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc. Natl. Acad. Sci. USA. 90: 7275-7279.
41. Preston, G. M., B. L. Smith, M. L. Zeidel, J. J. Moulds, and P. Agre. 1994. Mutations in aquaporin-1 in phenotypically normal humans without functional CHIP water channels. Science. 265:1585-1587.
42. Rubin, H. 1963. Antibody elution from red blood cells. J. Clin. Pathol. 16:70-73.
43. Schnitzer, J. E., and P. Oh. 1996. Aquaporin-1 in plasma membrane and caveolae provides mercury-sensitive water channels across lung endothelium. Am. J. Physiol. 270:H416-H422.
44. r 28,000 transmembrane protein exists as a multi-subunit oligomer similar to channel proteins. J. Biol. Chem. 266:6407-6415.
45. Smith, B. L., G. M. Preston, F. A. Spring, D. J. Anstee, and P. Agre. 1994. Human red cell aquaporin CHIP. I. Molecular characterization of ABH and Colton blood group antigens. J. Clin. Invest. 94:1043-1049.
46. Stolpen, A., D. E. Golan, and J. S. Pober. 1988. Tumor necrosis factor and immune interferon act in concert to slow the lateral diffusion of proteins and lipids in human endothelial cell membranes. J. Cell Biol. 107: 781-789.
47. Terris, J., C. A. Ecelbarger, S. Nielsen, and M. A. Knepper. 1995. Longterm regulation of four renal aquaporins in rats. Am. J. Physiol. 271: F414-F422.
48. Walz, T., T. Hirai, K. Murata, J. Heymann, K. Mitsuoka, Y. Fujiyoshi, B. Smith, P. Agre, and A. Engel. 1997. The three-dimensional structure of aquaporin-1. Nature. 387:624-627.
49. Zeidel, M., S. Ambudkar, B. L. Smith, and P. Agre. 1992. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry. 31:7436-7440.