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. 1998 Jan 1;329(Pt 1):101–106. doi: 10.1042/bj3290101

Structure of the trigonal crystal form of bovine annexin IV.

G Zanotti 1, G Malpeli 1, F Gliubich 1, C Folli 1, M Stoppini 1, L Olivi 1, A Savoia 1, R Berni 1
PMCID: PMC1219019  PMID: 9405281

Abstract

The structure of a trigonal crystal form of N-terminally truncated [des-(1-9)] bovine annexin IV, an annexin variant that exhibits the distinctive property of binding both phospholipids and carbohydrates in a Ca2+-dependent manner, has been determined at 3 A (0.3 nm) resolution -space group: R3; cell parameters: a=b=118.560 (8) A and c=82.233 (6) A-. The overall structure of annexin IV, crystallized in the absence of Ca2+ ions, is highly homologous to that of the other known members of the annexin family. The trimeric assembly in the trigonal crystals of annexin IV is quite similar to that found previously in non-isomorphous crystals of human, chicken and rat annexin V and to the subunit arrangement in half of the hexamer of hydra annexin XII. Moreover, it resembles that found in two-dimensional crystals of human annexin V bound to phospholipid monolayers. The propensity of several annexins to generate similar trimeric arrays supports the hypothesis that trimeric complexes of such annexins, including annexin IV, may represent the functional units that interact with membranes.

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Selected References

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  1. Benz J., Bergner A., Hofmann A., Demange P., Göttig P., Liemann S., Huber R., Voges D. The structure of recombinant human annexin VI in crystals and membrane-bound. J Mol Biol. 1996 Aug 2;260(5):638–643. doi: 10.1006/jmbi.1996.0426. [DOI] [PubMed] [Google Scholar]
  2. Benz J., Bergner A., Hofmann A., Demange P., Göttig P., Liemann S., Huber R., Voges D. The structure of recombinant human annexin VI in crystals and membrane-bound. J Mol Biol. 1996 Aug 2;260(5):638–643. doi: 10.1006/jmbi.1996.0426. [DOI] [PubMed] [Google Scholar]
  3. Bewley M. C., Boustead C. M., Walker J. H., Waller D. A., Huber R. Structure of chicken annexin V at 2.25-A resolution. Biochemistry. 1993 Apr 20;32(15):3923–3929. doi: 10.1021/bi00066a011. [DOI] [PubMed] [Google Scholar]
  4. Brünger A. T., Kuriyan J., Karplus M. Crystallographic R factor refinement by molecular dynamics. Science. 1987 Jan 23;235(4787):458–460. doi: 10.1126/science.235.4787.458. [DOI] [PubMed] [Google Scholar]
  5. Burger A., Berendes R., Liemann S., Benz J., Hofmann A., Göttig P., Huber R., Gerke V., Thiel C., Römisch J. The crystal structure and ion channel activity of human annexin II, a peripheral membrane protein. J Mol Biol. 1996 Apr 12;257(4):839–847. doi: 10.1006/jmbi.1996.0205. [DOI] [PubMed] [Google Scholar]
  6. Concha N. O., Head J. F., Kaetzel M. A., Dedman J. R., Seaton B. A. Annexin V forms calcium-dependent trimeric units on phospholipid vesicles. FEBS Lett. 1992 Dec 14;314(2):159–162. doi: 10.1016/0014-5793(92)80964-i. [DOI] [PubMed] [Google Scholar]
  7. Concha N. O., Head J. F., Kaetzel M. A., Dedman J. R., Seaton B. A. Rat annexin V crystal structure: Ca(2+)-induced conformational changes. Science. 1993 Sep 3;261(5126):1321–1324. doi: 10.1126/science.8362244. [DOI] [PubMed] [Google Scholar]
  8. Demange P., Voges D., Benz J., Liemann S., Göttig P., Berendes R., Burger A., Huber R. Annexin V: the key to understanding ion selectivity and voltage regulation? Trends Biochem Sci. 1994 Jul;19(7):272–276. doi: 10.1016/0968-0004(94)90002-7. [DOI] [PubMed] [Google Scholar]
  9. Favier-Perron B., Lewit-Bentley A., Russo-Marie F. The high-resolution crystal structure of human annexin III shows subtle differences with annexin V. Biochemistry. 1996 Feb 13;35(6):1740–1744. doi: 10.1021/bi952092o. [DOI] [PubMed] [Google Scholar]
  10. Hamman H. C., Gaffey L. C., Lynch K. R., Creutz C. E. Cloning and characterization of a cDNA encoding bovine endonexin (chromobindin 4). Biochem Biophys Res Commun. 1988 Oct 31;156(2):660–667. doi: 10.1016/s0006-291x(88)80893-3. [DOI] [PubMed] [Google Scholar]
  11. Huber R., Römisch J., Paques E. P. The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes. EMBO J. 1990 Dec;9(12):3867–3874. doi: 10.1002/j.1460-2075.1990.tb07605.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jost M., Gerke V. Mapping of a regulatory important site for protein kinase C phosphorylation in the N-terminal domain of annexin II. Biochim Biophys Acta. 1996 Oct 11;1313(3):283–289. doi: 10.1016/0167-4889(96)00101-2. [DOI] [PubMed] [Google Scholar]
  13. Junker M., Creutz C. E. Ca(2+)-dependent binding of endonexin (annexin IV) to membranes: analysis of the effects of membrane lipid composition and development of a predictive model for the binding interaction. Biochemistry. 1994 Aug 2;33(30):8930–8940. doi: 10.1021/bi00196a010. [DOI] [PubMed] [Google Scholar]
  14. Kawasaki H., Avila-Sakar A., Creutz C. E., Kretsinger R. H. The crystal structure of annexin VI indicates relative rotation of the two lobes upon membrane binding. Biochim Biophys Acta. 1996 Oct 11;1313(3):277–282. doi: 10.1016/0167-4889(96)00100-0. [DOI] [PubMed] [Google Scholar]
  15. Kojima K., Ogawa H. K., Seno N., Matsumoto I. Affinity purification and affinity characterization of carbohydrate-binding proteins in bovine kidney. J Chromatogr. 1992 Apr 24;597(1-2):323–330. doi: 10.1016/0021-9673(92)80127-g. [DOI] [PubMed] [Google Scholar]
  16. Kojima K., Yamamoto K., Irimura T., Osawa T., Ogawa H., Matsumoto I. Characterization of carbohydrate-binding protein p33/41: relation with annexin IV, molecular basis of the doublet forms (p33 and p41), and modulation of the carbohydrate binding activity by phospholipids. J Biol Chem. 1996 Mar 29;271(13):7679–7685. doi: 10.1074/jbc.271.13.7679. [DOI] [PubMed] [Google Scholar]
  17. Liemann S., Benz J., Burger A., Voges D., Hofmann A., Huber R., Göttig P. Structural and functional characterisation of the voltage sensor in the ion channel human annexin V. J Mol Biol. 1996 May 17;258(4):555–561. doi: 10.1006/jmbi.1996.0268. [DOI] [PubMed] [Google Scholar]
  18. Liemann S., Lewit-Bentley A. Annexins: a novel family of calcium- and membrane-binding proteins in search of a function. Structure. 1995 Mar 15;3(3):233–237. doi: 10.1016/s0969-2126(01)00152-6. [DOI] [PubMed] [Google Scholar]
  19. Luecke H., Chang B. T., Mailliard W. S., Schlaepfer D. D., Haigler H. T. Crystal structure of the annexin XII hexamer and implications for bilayer insertion. Nature. 1995 Nov 30;378(6556):512–515. doi: 10.1038/378512a0. [DOI] [PubMed] [Google Scholar]
  20. Malherbe P., Köhler C., Da Prada M., Lang G., Kiefer V., Schwarcz R., Lahm H. W., Cesura A. M. Molecular cloning and functional expression of human 3-hydroxyanthranilic-acid dioxygenase. J Biol Chem. 1994 May 13;269(19):13792–13797. [PubMed] [Google Scholar]
  21. Porte F., de Santa Barbara P., Phalipou S., Liautard J. P., Widada J. S. Change in the N-terminal domain conformation of annexin I that correlates with liposome aggregation is impaired by Ser-27 to Glu mutation that mimics phosphorylation. Biochim Biophys Acta. 1996 Apr 16;1293(2):177–184. doi: 10.1016/0167-4838(95)00220-0. [DOI] [PubMed] [Google Scholar]
  22. RAMACHANDRAN G. N., RAMAKRISHNAN C., SASISEKHARAN V. Stereochemistry of polypeptide chain configurations. J Mol Biol. 1963 Jul;7:95–99. doi: 10.1016/s0022-2836(63)80023-6. [DOI] [PubMed] [Google Scholar]
  23. Raynal P., Pollard H. B. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta. 1994 Apr 5;1197(1):63–93. doi: 10.1016/0304-4157(94)90019-1. [DOI] [PubMed] [Google Scholar]
  24. Rojas E., Pollard H. B., Haigler H. T., Parra C., Burns A. L. Calcium-activated endonexin II forms calcium channels across acidic phospholipid bilayer membranes. J Biol Chem. 1990 Dec 5;265(34):21207–21215. [PubMed] [Google Scholar]
  25. Swairjo M. A., Seaton B. A. Annexin structure and membrane interactions: a molecular perspective. Annu Rev Biophys Biomol Struct. 1994;23:193–213. doi: 10.1146/annurev.bb.23.060194.001205. [DOI] [PubMed] [Google Scholar]
  26. Voges D., Berendes R., Burger A., Demange P., Baumeister W., Huber R. Three-dimensional structure of membrane-bound annexin V. A correlative electron microscopy-X-ray crystallography study. J Mol Biol. 1994 Apr 29;238(2):199–213. doi: 10.1006/jmbi.1994.1281. [DOI] [PubMed] [Google Scholar]
  27. Weng X., Luecke H., Song I. S., Kang D. S., Kim S. H., Huber R. Crystal structure of human annexin I at 2.5 A resolution. Protein Sci. 1993 Mar;2(3):448–458. doi: 10.1002/pro.5560020317. [DOI] [PMC free article] [PubMed] [Google Scholar]

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