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. 2000 Nov 15;352(Pt 1):183–190.

Lentil seed aquaporins form a hetero-oligomer which is phosphorylated by a Mg(2+)-dependent and Ca(2+)-regulated kinase.

P Harvengt 1, A Vlerick 1, B Fuks 1, R Wattiez 1, J M Ruysschaert 1, F Homble 1
PMCID: PMC1221445  PMID: 11062071

Abstract

In plants, aquaporins regulate the water flow through membranes during growth, development and stress responses. We have isolated two isoforms of the aquaporin family from the protein-storage vacuoles of lentil (Lens culinaris Med.) seeds. Chemical cross-linking experiments showed that both isoforms belong to the same oligomer in the membrane and are phosphorylated by a membrane-bound protein kinase. We assigned the kinase activity to a 52 kDa protein that is magnesium-dependent and calcium-regulated.

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Selected References

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  1. Cabiaux V., Oberg K. A., Pancoska P., Walz T., Agre P., Engel A. Secondary structures comparison of aquaporin-1 and bacteriorhodopsin: a Fourier transform infrared spectroscopy study of two-dimensional membrane crystals. Biophys J. 1997 Jul;73(1):406–417. doi: 10.1016/S0006-3495(97)78080-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cheng A., van Hoek A. N., Yeager M., Verkman A. S., Mitra A. K. Three-dimensional organization of a human water channel. Nature. 1997 Jun 5;387(6633):627–630. doi: 10.1038/42517. [DOI] [PubMed] [Google Scholar]
  3. Chrispeels M. J., Agre P. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci. 1994 Oct;19(10):421–425. doi: 10.1016/0968-0004(94)90091-4. [DOI] [PubMed] [Google Scholar]
  4. Daniels M. J., Chaumont F., Mirkov T. E., Chrispeels M. J. Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell. 1996 Apr;8(4):587–599. doi: 10.1105/tpc.8.4.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Daniels M. J., Chrispeels M. J., Yeager M. Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J Mol Biol. 1999 Dec 17;294(5):1337–1349. doi: 10.1006/jmbi.1999.3293. [DOI] [PubMed] [Google Scholar]
  6. Davies G. E., Stark G. R. Use of dimethyl suberimidate, a cross-linking reagent, in studying the subunit structure of oligomeric proteins. Proc Natl Acad Sci U S A. 1970 Jul;66(3):651–656. doi: 10.1073/pnas.66.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Estruch J. J., Kadwell S., Merlin E., Crossland L. Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8837–8841. doi: 10.1073/pnas.91.19.8837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fairbanks G., Steck T. L., Wallach D. F. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 1971 Jun 22;10(13):2606–2617. doi: 10.1021/bi00789a030. [DOI] [PubMed] [Google Scholar]
  9. Fernandez-Patron C., Hardy E., Sosa A., Seoane J., Castellanos L. Double staining of coomassie blue-stained polyacrylamide gels by imidazole-sodium dodecyl sulfate-zinc reverse staining: sensitive detection of coomassie blue-undetected proteins. Anal Biochem. 1995 Jan 1;224(1):263–269. doi: 10.1006/abio.1995.1039. [DOI] [PubMed] [Google Scholar]
  10. Harmon A. C., Putnam-Evans C., Cormier M. J. A calcium-dependent but calmodulin-independent protein kinase from soybean. Plant Physiol. 1987 Apr;83(4):830–837. doi: 10.1104/pp.83.4.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Heymann J. B., Agre P., Engel A. Progress on the structure and function of aquaporin 1. J Struct Biol. 1998;121(2):191–206. doi: 10.1006/jsbi.1997.3951. [DOI] [PubMed] [Google Scholar]
  12. Höfte H., Chrispeels M. J. Protein sorting to the vacuolar membrane. Plant Cell. 1992 Aug;4(8):995–1004. doi: 10.1105/tpc.4.8.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Johnson K. D., Chrispeels M. J. Tonoplast-bound protein kinase phosphorylates tonoplast intrinsic protein. Plant Physiol. 1992 Dec;100(4):1787–1795. doi: 10.1104/pp.100.4.1787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Johnson K. D., Herman E. M., Chrispeels M. J. An abundant, highly conserved tonoplast protein in seeds. Plant Physiol. 1989 Nov;91(3):1006–1013. doi: 10.1104/pp.91.3.1006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson K. D., Höfte H., Chrispeels M. J. An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GIpF). Plant Cell. 1990 Jun;2(6):525–532. doi: 10.1105/tpc.2.6.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jung J. S., Preston G. M., Smith B. L., Guggino W. B., Agre P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem. 1994 May 20;269(20):14648–14654. [PubMed] [Google Scholar]
  17. Kameshita I., Fujisawa H. A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel. Anal Biochem. 1989 Nov 15;183(1):139–143. doi: 10.1016/0003-2697(89)90181-4. [DOI] [PubMed] [Google Scholar]
  18. Kuwahara M., Fushimi K., Terada Y., Bai L., Marumo F., Sasaki S. cAMP-dependent phosphorylation stimulates water permeability of aquaporin-collecting duct water channel protein expressed in Xenopus oocytes. J Biol Chem. 1995 May 5;270(18):10384–10387. doi: 10.1074/jbc.270.18.10384. [DOI] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Lagrée V., Froger A., Deschamps S., Hubert J. F., Delamarche C., Bonnec G., Thomas D., Gouranton J., Pellerin I. Switch from an aquaporin to a glycerol channel by two amino acids substitution. J Biol Chem. 1999 Mar 12;274(11):6817–6819. doi: 10.1074/jbc.274.11.6817. [DOI] [PubMed] [Google Scholar]
  21. Maurel C., Kado R. T., Guern J., Chrispeels M. J. Phosphorylation regulates the water channel activity of the seed-specific aquaporin alpha-TIP. EMBO J. 1995 Jul 3;14(13):3028–3035. doi: 10.1002/j.1460-2075.1995.tb07305.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maurel Christophe. AQUAPORINS AND WATER PERMEABILITY OF PLANT MEMBRANES. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):399–429. doi: 10.1146/annurev.arplant.48.1.399. [DOI] [PubMed] [Google Scholar]
  23. Preston G. M., Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11110–11114. doi: 10.1073/pnas.88.24.11110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Putnam-Evans C. L., Harmon A. C., Cormier M. J. Purification and characterization of a novel calcium-dependent protein kinase from soybean. Biochemistry. 1990 Mar 13;29(10):2488–2495. doi: 10.1021/bi00462a008. [DOI] [PubMed] [Google Scholar]
  25. Reizer J., Reizer A., Saier M. H., Jr The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional differentiation of the two repeated halves of the proteins. Crit Rev Biochem Mol Biol. 1993;28(3):235–257. doi: 10.3109/10409239309086796. [DOI] [PubMed] [Google Scholar]
  26. Sasaki S., Ishibashi K., Marumo F. Aquaporin-2 and -3: representatives of two subgroups of the aquaporin family colocalized in the kidney collecting duct. Annu Rev Physiol. 1998;60:199–220. doi: 10.1146/annurev.physiol.60.1.199. [DOI] [PubMed] [Google Scholar]
  27. Smith B. L., Agre P. Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem. 1991 Apr 5;266(10):6407–6415. [PubMed] [Google Scholar]
  28. Walz T., Hirai T., Murata K., Heymann J. B., Mitsuoka K., Fujiyoshi Y., Smith B. L., Agre P., Engel A. The three-dimensional structure of aquaporin-1. Nature. 1997 Jun 5;387(6633):624–627. doi: 10.1038/42512. [DOI] [PubMed] [Google Scholar]
  29. Walz T., Smith B. L., Agre P., Engel A. The three-dimensional structure of human erythrocyte aquaporin CHIP. EMBO J. 1994 Jul 1;13(13):2985–2993. doi: 10.1002/j.1460-2075.1994.tb06597.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wattiez R., Hermans C., Bernard A., Lesur O., Falmagne P. Human bronchoalveolar lavage fluid: two-dimensional gel electrophoresis, amino acid microsequencing and identification of major proteins. Electrophoresis. 1999 Jun;20(7):1634–1645. doi: 10.1002/(SICI)1522-2683(19990601)20:7<1634::AID-ELPS1634>3.0.CO;2-J. [DOI] [PubMed] [Google Scholar]
  31. Yuasa T., Muto S. Ca(2+)-dependent protein kinase from the halotolerant green alga Dunaliella tertiolecta: partial purification and Ca(2+)-dependent association of the enzyme to the microsomes. Arch Biochem Biophys. 1992 Jul;296(1):175–182. doi: 10.1016/0003-9861(92)90560-j. [DOI] [PubMed] [Google Scholar]
  32. van Hoek A. N., Hom M. L., Luthjens L. H., de Jong M. D., Dempster J. A., van Os C. H. Functional unit of 30 kDa for proximal tubule water channels as revealed by radiation inactivation. J Biol Chem. 1991 Sep 5;266(25):16633–16635. [PubMed] [Google Scholar]

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