Calcium-dependent Tetramer Formation of S100A8 and S100A9 is Essential for Biological Activity

Journal of Molecular Biology

Volumn 359, Issue 4, 2006, Pages 961-972

  Leukert, Nadja ^a   Vogl, Thomas ^a   Strupat, Kerstin ^b   Reichelt, Rudolf ^a   Sorg, Clemens ^a   Roth, Johannes ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b THERMO FISHER SCIENTIFIC   (Germany)

Author keywords

calcium binding; EF hand mutants; S100 proteins; tetramerization; tubulin polymerization

Indexed keywords

HETERODIMER; HOMODIMER; OLIGOMER; PROTEIN S 100; S100 CALCIUM BINDING PROTEIN A8; S100 CALCIUM BINDING PROTEIN A9; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; BIOLOGICAL ACTIVITY; CELL MIGRATION; CENTRIFUGATION; DENSITY; EXPERIMENTATION; MASS SPECTROMETRY; MICROTUBULE ASSEMBLY; MODULATION; MUTATION; OLIGOMERIZATION; PHAGOCYTE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REGULATORY MECHANISM; TWO HYBRID SYSTEM; YEAST;

EID: 33744813581     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.04.009     Document Type: Article

References (41)

1. Odink K., Cerletti N., Bruggen J., Clerc R.G., Tarcsay L., Zwadlo G., et al. Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature 330 (1987) 80-82
2. Hogg N., Allen C., and Edgeworth J. Monoclonal antibody 5.5 reacts with p8,14, a myeloid molecule associated with some vascular endothelium. Eur. J. Immunol. 19 (1989) 1053-1061
3. Kelly S.E., Jones D.B., and Fleming S. Calgranulin expression in inflammatory dermatoses. J. Pathol. 159 (1989) 17-21
4. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 33 (2001) 637-668
5. Heizmann C.W., Fritz G., and Schafer B.W. S100 proteins: structure, functions and pathology. Front. Biosci. 7 (2002) d1356-d1368
6. Skelton N.J., Kordel J., Akke M., Forsen S., and Chazin W.J. Signal transduction versus buffering activity in Ca(2+)-binding proteins. Nature Struct. Biol. 1 (1994) 239-245
7. Deloulme J.C., Assard N., Mbele G.O., Mangin C., Kuwano R., and Baudier J. S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo. J. Biol. Chem. 275 (2000) 35302-35310
8. Gribenko A.V., Hopper J.E., and Makhatadze G.I. Molecular characterization and tissue distribution of a novel member of the S100 family of EF-hand proteins. Biochemistry 40 (2001) 15538-15548
9. Tarabykina S., Kriajevska M., Scott D.J., Hill T.J., Lafitte D., Derrick P.J., et al. Heterocomplex formation between metastasis-related protein S100A4 (Mts1) and S100A1 as revealed by the yeast two-hybrid system. FEBS Letters 475 (2000) 187-191
10. Teigelkamp S., Bhardwaj R.S., Roth J., Meinardus-Hager G., Karas M., and Sorg C. Calcium-dependent complex assembly of the myeloic differentiation proteins MRP-8 and MRP-14. J. Biol. Chem. 266 (1991) 13462-13467
11. Wang G., Rudland P.S., White M.R., and Barraclough R. Interaction in vivo and in vitro of the metastasis-inducing S100 protein, S100A4 (p9Ka) with S100A1. J. Biol. Chem. 275 (2000) 11141-11146
12. Yang Q., O'Hanlon D., Heizmann C.W., and Marks A. Demonstration of heterodimer formation between S100B and S100A6 in the yeast two-hybrid system and human melanoma. Expt. Cell Res. 246 (1999) 501-509
13. Moroz O.V., Antson A.A., Dodson E.J., Burrell H.J., Grist S.J., Lloyd R.M., et al. The structure of S100A12 in a hexameric form and its proposed role in receptor signalling. Acta Crystallog. sect. D 58 (2002) 407-413
14. Novitskaya V., Grigorian M., Kriajevska M., Tarabykina S., Bronstein I., Berezin V., et al. Oligomeric forms of the metastasis-related Mts1 (S100A4) protein stimulate neuronal differentiation in cultures of rat hippocampal neurons. J. Biol. Chem. 275 (2000) 41278-41286
15. Ostendorp, T., Kroneck, P. M. H., Heizmann, C. W., & Fritz, G. (2004). The crystal structure of human S100B reveals a novel octameric assembly; implications for RAGE signalling. 8th Meeting of the European Calcium Society, pp. 122. Available online at http://www.ulb.ac.be/assoc/ecs/docs/poster_2_50.doc
16. Vogl T., Roth J., Sorg C., Hillenkamp F., and Strupat K. Calcium-induced noncovalently linked tetramers of MRP8 and MRP14 detected by ultraviolet matrix-assisted laser desorption/ionization mass spectrometry. J. Am. Soc. Mass Spectrom. 10 (1999) 1124-1130
17. Hunter M.J., and Chazin W.J. High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J. Biol. Chem. 273 (1998) 12427-12435
18. Propper C., Huang X., Roth J., Sorg C., and Nacken W. Analysis of the MRP8-MRP14 protein-protein interaction by the two-hybrid system suggests a prominent role of the C-terminal domain of S100 proteins in dimer formation. J. Biol. Chem. 274 (1999) 183-188
19. Strupat K., Rogniaux H., Van Dorsselaer A., Roth J., and Vogl T. Calcium-induced noncovalently linked tetramers of MRP8 and MRP14 are confirmed by electrospray ionization-mass analysis. J. Am. Soc. Mass Spectrom. 11 (2000) 780-788
20. Rammes A., Roth J., Goebeler M., Klempt M., Hartmann M., and Sorg C. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J. Biol. Chem. 272 (1997) 9496-9502
21. Vogl T., Ludwig S., Goebeler M., Strey A., Thorey I.S., Reichelt R., et al. MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood 104 (2004) 4260-4268
22. Rety S., Sopkova J., Renouard M., Osterloh D., Gerke V., Tabaries S., et al. The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nature Struct. Biol. 6 (1999) 89-95
23. 2+ coordination, by genetic engineering. J. Biol. Chem. 267 (1992) 15469-15474
24. Vogl T., Propper C., Hartmann M., Strey A., Strupat K., van den B.C., et al. S100A12 is expressed exclusively by granulocytes and acts independently from MRP8 and MRP14. J. Biol. Chem. 274 (1999) 25291-25296
25. Roth J., Vogl T., Sorg C., and Sunderkotter C. Phagocyte-specific S100 proteins: a novel group of proinflammatory molecules. Trends Immunol. 24 (2003) 155-158
26. Kim E.J., and Helfman D.M. Characterization of the metastasis-associated protein, S100A4. Roles of calcium binding and dimerization in cellular localization and interaction with myosin. J. Biol. Chem. 278 (2003) 30063-30073
27. Zhang S., Wang G., Liu D., Bao Z., Fernig D.G., Rudland P.S., and Barraclough R. The C-terminal region of S100A4 is important for its metastasis-inducing properties. Oncogene 24 (2005) 4401-4411
28. Markowitz J., Rustandi R.R., Varney K.M., Wilder P.T., Udan R., Wu S.L., et al. Calcium-binding properties of wild-type and EF-hand mutants of S100B in the presence and absence of a peptide derived from the C-terminal negative regulatory domain of p53. Biochemistry 44 (2005) 7305-7314
29. Gundersen G.G., and Cook T.A. Microtubules and signal transduction. Curr. Opin. Cell Biol. 11 (1999) 81-94
30. Nabi I.R. The polarization of the motile cell. J. Cell Sci. 112 (1999) 1803-1811
31. Thyberg J., and Moskalewski S. Role of microtubules in the organization of the Golgi complex. Expt. Cell Res. 246 (1999) 263-279
32. Waterman-Storer C.M., and Salmon E. Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr. Opin. Cell Biol. 11 (1999) 61-67
33. Davey G.E., Murmann P., Hoechli M., Tanaka T., and Heizmann C.W. Calcium-dependent translocation of S100A11 requires tubulin filaments. Biochim. Biophys. Acta 1498 (2000) 220-232
34. Donato R. Perspectives in S-100 protein biology. Review article. Cell Calcium 12 (1991) 713-726
35. Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim. Biophys. Acta 1450 (1999) 191-231
36. Sorci G., Agneletti A.L., and Donato R. Effects of S100A1 and S100B on microtubule stability. An in vitro study using triton-cytoskeletons from astrocyte and myoblast cell lines. Neuroscience 99 (2000) 773-783
37. Lewis S.A., Wang D.H., and Cowan N.J. Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science 242 (1988) 936-939
38. Lewis S.A., Ivanov I.E., Lee G.H., and Cowan N.J. Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau. Nature 342 (1989) 498-505
39. Lewis S.A., and Cowan N. Microtubule bundling. Nature 345 (1990) 674
40. Wallis K.T., Azhar S., Rho M.B., Lewis S.A., Cowan N.J., and Murphy D.B. The mechanism of equilibrium binding of microtubule-associated protein 2 to microtubules. Binding is a multi-phasic process and exhibits positive cooperativity. J. Biol. Chem. 268 (1993) 15158-15167
41. Nagai K., and Thogersen H.C. Synthesis and sequence-specific proteolysis of hybrid proteins produced in Escherichia coli. Methods Enzymol. 153 (1987) 461-481