Cysteine 81 is critical for the interaction of s100a4 and myosin-IIA

Biochemistry

Volumn 50, Issue 33, 2011, Pages 7218-7227

  Dulyaninova, Natalya G ^a   Hite, Karen M ^b   Zencheck, Wendy D ^a   Scudiero, Dominic A ^b   Almo, Steven C ^a   Shoemaker, Robert H ^c   Bresnick, Anne R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b SAIC FREDERICK INC   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEINS; CELLULAR ACTIVITIES; COVALENT MODIFICATIONS; HUMAN PATHOLOGIES; INFLAMMATORY DISORDERS; METASTATIC DISEASE; OVER-EXPRESSION; REGULATORY MECHANISM; SMALL MOLECULES; TARGET BINDING;

DISEASES; MASS SPECTROMETRY; PATHOLOGY;

AMINO ACIDS;

ALANINE; CALCIUM; CALVASCULIN; CYSTEINE; CYSTEINE 81; MYOSIN IIA; NSC 95397; PROTEIN INHIBITOR; SERINE; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; HUMAN; MASS SPECTROMETRY; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION;

CDC25 PHOSPHATASES; CHROMATOGRAPHY, LIQUID; CYSTEINE; CYTOSKELETON; HUMANS; NAPHTHOQUINONES; NONMUSCLE MYOSIN TYPE IIA; PEPTIDE FRAGMENTS; PROTEIN BINDING; RECOMBINANT PROTEINS; S100 PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 80051721562     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200853y     Document Type: Article

References (46)

1. Zimmer, D. B., Cornwall, E. H., Landar, A., and Song, W. (1995) The S100 protein family: history, function, and expression Brain Res. Bull. 37, 417-429
2. Marenholz, I., Heizmann, C. W., and Fritz, G. (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature) Biochem. Biophys. Res. Commun. 322, 1111-1122 (Pubitemid 39164640)
3. Rety, S., Sopkova, J., Renouard, M., Osterloh, D., Gerke, V., Tabaries, S., Russo-Marie, F., and Lewit-Bentley, A. (1999) The crystal structure of a complex of p11 with the annexin II N-terminal peptide Nat. Struct. Biol. 6, 89-95 (Pubitemid 29232429)
4. Rustandi, R. R., Baldisseri, D. M., and Weber, D. J. (2000) Structure of the negative regulatory domain of p53 bound to S100B(betabeta) Nat. Struct. Biol. 7, 570-574 (Pubitemid 30445914)
5. Bhattacharya, S., Large, E., Heizmann, C. W., Hemmings, B., and Chazin, W. J. (2003) Structure of the Ca2+/S100B/NDR kinase peptide complex: insights into S100 target specificity and activation of the kinase Biochemistry 42, 14416-14426 (Pubitemid 37531986)
6. Donato, R. (2003) Intracellular and extracellular roles of S100 proteins Microsc. Res. Tech. 60, 540-551
7. Santamaria-Kisiel, L., Rintala-Dempsey, A. C., and Shaw, G. S. (2006) Calcium-dependent and -independent interactions of the S100 protein family Biochem. J. 396, 201-214 (Pubitemid 43837235)
8. Heizmann, C. W., Ackermann, G. E., and Galichet, A. (2007) Pathologies involving the S100 proteins and RAGE Subcell Biochem. 45, 93-138
9. Schneider, M., Hansen, J. L., and Sheikh, S. P. (2008) S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J. Mol. Med. 86, 507-522
10. Grigorian, M., Ambartsumian, N., and Lukanidin, E. (2008) Metastasis-inducing S100A4 protein: implication in non-malignant human pathologies Curr. Mol. Med. 8, 492-496
11. Helfman, D. M., Kim, E. J., Lukanidin, E., and Grigorian, M. (2005) The metastasis associated protein S100A4: role in tumour progression and metastasis Br. J. Cancer 92, 1955-1958 (Pubitemid 40897415)
12. Garrett, S. C., Varney, K. M., Weber, D. J., and Bresnick, A. R. (2006) S100A4, a mediator of metastasis J. Biol. Chem. 281, 677-680
13. Takenaga, K., Nakamura, Y., Sakiyama, S., Hasegawa, Y., Sato, K., and Endo, H. (1994) Binding of pEL98 protein, an S100-related calcium-binding protein, to nonmuscle tropomyosin J. Cell Biol. 124, 757-768 (Pubitemid 24085784)
14. Kriajevska, M. V., Cardenas, M. N., Grigorian, M. S., Ambartsumian, N. S., Georgiev, G. P., and Lukanidin, E. M. (1994) Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene J. Biol. Chem. 269, 19679-19682 (Pubitemid 24250873)
15. Grigorian, M., Andresen, S., Tulchinsky, E., Kriajevska, M., Carlberg, C., Kruse, C., Cohn, M., Ambartsumian, N., Christensen, A., Selivanova, G., and Lukanidin, E. (2001) Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction J. Biol. Chem. 276, 22699-22708
16. Kriajevska, M., Fischer-Larsen, M., Moertz, E., Vorm, O., Tulchinsky, E., Grigorian, M., Ambartsumian, N., and Lukanidin, E. (2002) Liprin beta 1, a member of the family of LAR transmembrane tyrosine phosphatase-interacting proteins, is a new target for the metastasis-associated protein S100A4 (Mts1) J. Biol. Chem. 277, 5229-5235 (Pubitemid 34975654)
17. Li, Z. H. and Bresnick, A. R. (2006) The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA Cancer Res. 66, 5173-5180 (Pubitemid 43844940)
18. Ismail, T. M., Fernig, D. G., Rudland, P. S., Terry, C. J., Wang, G., and Barraclough, R. (2008) The basic C-terminal amino acids of calcium-binding protein S100A4 promote metastasis Carcinogenesis 29, 2259-2266
19. Li, Z. H., Dulyaninova, N. G., House, R. P., Almo, S. C., and Bresnick, A. R. (2010) S100A4 regulates macrophage chemotaxis Mol. Biol. Cell 21, 2598-2610
20. Malashkevich, V. N., Dulyaninova, N. G., Ramagopal, U. A., Liriano, M. A., Varney, K. M., Knight, D., Brenowitz, M., Weber, D. J., Almo, S. C., and Bresnick, A. R. (2010) Phenothiazines inhibit S100A4 function by inducing protein oligomerization Proc. Natl. Acad. Sci. U. S. A. 107, 8605-8610
21. Garrett, S. C., Hodgson, L., Rybin, A., Toutchkine, A., Hahn, K. M., Lawrence, D. S., and Bresnick, A. R. (2008) A biosensor of S100A4 metastasis factor activation: inhibitor screening and cellular activation dynamics Biochemistry 47, 986-996
22. Li, Z.-H., Spektor, A., Varlamova, O., and Bresnick, A. R. (2003) Mts1 regulates the assembly of nonmuscle myosin-IIA Biochemistry 42, 14258-14266 (Pubitemid 37499423)
23. Andre, I. and Linse, S. (2002) Measurement of Ca2+-binding constants of proteins and presentation of the CaLigator software Anal. Biochem. 305, 195-205 (Pubitemid 34666792)
24. Lazo, J. S., Nemoto, K., Pestell, K. E., Cooley, K., Southwick, E. C., Mitchell, D. A., Furey, W., Gussio, R., Zaharevitz, D. W., Joo, B., and Wipf, P. (2002) Identification of a potent and selective pharmacophore for Cdc25 dual specificity phosphatase inhibitors Mol. Pharmacol. 61, 720-728 (Pubitemid 34273150)
25. Nishikawa, Y., Carr, B. I., Wang, M., Kar, S., Finn, F., Dowd, P., Zheng, Z. B., Kerns, J., and Naganathan, S. (1995) Growth inhibition of hepatoma cells induced by vitamin K and its analogs J. Biol. Chem. 270, 28304-28310
26. Kar, S., Lefterov, I. M., Wang, M., Lazo, J. S., Scott, C. N., Wilcox, C. S., and Carr, B. I. (2003) Binding and inhibition of Cdc25 phosphatases by vitamin K analogues Biochemistry 42, 10490-10497 (Pubitemid 37071449)
27. Malashkevich, V. N., Varney, K. M., Garrett, S. C., Wilder, P. T., Knight, D., Charpentier, T. H., Ramagopal, U. A., Almo, S. C., Weber, D. J., and Bresnick, A. R. (2008) Structure of Ca2+-bound S100A4 and its interaction with peptides derived from nonmuscle myosin-IIA Biochemistry 47, 5111-5126 (Pubitemid 351620749)
28. Gingras, A. R., Basran, J., Prescott, A., Kriajevska, M., Bagshaw, C. R., and Barsukov, I. L. (2008) Crystal structure of the Ca(2+)-form and Ca(2+)-binding kinetics of metastasis-associated protein, S100A4 FEBS Lett. 582, 1651-1656
29. Pathuri, P., Vogeley, L., and Luecke, H. (2008) Crystal structure of metastasis-associated protein S100A4 in the active calcium-bound form J. Mol. Biol. 383, 62-77
30. Badyal, S. K., Basran, J., Bhanji, N., Kim, J. H., Chavda, A. P., Jung, H. S., Craig, R., Elliott, P. R., Irvine, A. F., Barsukov, I. L., Kriajevska, M., and Bagshaw, C. R. (2011) Mechanism of the Ca(2)+-dependent interaction between S100A4 and tail fragments of nonmuscle myosin heavy chain IIA J. Mol. Biol. 405, 1004-1026
31. Brisson, M., Nguyen, T., Wipf, P., Joo, B., Day, B. W., Skoko, J. S., Schreiber, E. M., Foster, C., Bansal, P., and Lazo, J. S. (2005) Redox regulation of Cdc25B by cell-active quinolinediones Mol. Pharmacol. 68, 1810-1820 (Pubitemid 41656028)
32. Vogt, A., McDonald, P. R., Tamewitz, A., Sikorski, R. P., Wipf, P., Skoko, J. J., 3rd, and Lazo, J. S. (2008) A cell-active inhibitor of mitogen-activated protein kinase phosphatases restores paclitaxel-induced apoptosis in dexamethasone-protected cancer cells Mol. Cancer Ther. 7, 330-340 (Pubitemid 351302526)
33. Panchal, R. G., Ulrich, R. L., Bradfute, S. B., Lane, D., Ruthel, G., Kenny, T. A., Iversen, P. L., Anderson, A. O., Gussio, R., Raschke, W. C., and Bavari, S. (2009) Reduced expression of CD45 protein-tyrosine phosphatase provides protection against anthrax pathogenesis J. Biol. Chem. 284, 12874-12885
34. Valente, C., Moreira, R., Guedes, R. C., Iley, J., Jaffar, M., and Douglas, K. T. (2007) The 1,4-naphthoquinone scaffold in the design of cysteine protease inhibitors Bioorg. Med. Chem. 15, 5340-5350 (Pubitemid 46887667)
35. Lai, T. S., Liu, Y., Tucker, T., Daniel, K. R., Sane, D. C., Toone, E., Burke, J. R., Strittmatter, W. J., and Greenberg, C. S. (2008) Identification of chemical inhibitors to human tissue transglutaminase by screening existing drug libraries Chem. Biol. 15, 969-978
36. Contour-Galcera, M. O., Sidhu, A., Prevost, G., Bigg, D., and Ducommun, B. (2007) What's new on CDC25 phosphatase inhibitors Pharmacol. Ther. 115, 1-12 (Pubitemid 46990550)
37. Soares, K. M., Blackmon, N., Shun, T. Y., Shinde, S. N., Takyi, H. K., Wipf, P., Lazo, J. S., and Johnston, P. A. (2010) Profiling the NIH Small Molecule Repository for compounds that generate H2O2 by redox cycling in reducing environments Assay Drug Dev. Technol. 8, 152-174
38. Han, Y., Shen, H., Carr, B. I., Wipf, P., Lazo, J. S., and Pan, S. S. (2004) NAD(P)H:quinone oxidoreductase-1-dependent and -independent cytotoxicity of potent quinone Cdc25 phosphatase inhibitors J. Pharmacol. Exp. Ther. 309, 64-70 (Pubitemid 38393115)
39. Peyregne, V. P., Kar, S., Ham, S. W., Wang, M., Wang, Z., and Carr, B. I. (2005) Novel hydroxyl naphthoquinones with potent Cdc25 antagonizing and growth inhibitory properties Mol. Cancer Ther. 4, 595-602 (Pubitemid 40601841)
40. Goch, G., Vdovenko, S., Kozlowska, H., and Bierzynski, A. (2005) Affinity of S100A1 protein for calcium increases dramatically upon glutathionylation FEBS J. 272, 2557-2565 (Pubitemid 40705075)
41. Orre, L. M., Pernemalm, M., Lengqvist, J., Lewensohn, R., and Lehtio, J. (2007) Up-regulation, modification, and translocation of S100A6 induced by exposure to ionizing radiation revealed by proteomics profiling Mol. Cell. Proteomics 6, 2122-2131
42. Lim, S. Y., Raftery, M., Cai, H., Hsu, K., Yan, W. X., Hseih, H. L., Watts, R. N., Richardson, D., Thomas, S., Perry, M., and Geczy, C. L. (2008) S-nitrosylated S100A8: novel anti-inflammatory properties J. Immunol. 181, 5627-5636
43. Lim, S. Y., Raftery, M. J., Goyette, J., and Geczy, C. L. (2010) S-glutathionylation regulates inflammatory activities of S100A9 J. Biol. Chem. 285, 14377-14388
44. Wright, N. T., Cannon, B. R., Wilder, P. T., Morgan, M. T., Varney, K. M., Zimmer, D. B., and Weber, D. J. (2009) Solution structure of S100A1 bound to the CapZ peptide (TRTK12) J. Mol. Biol. 386, 1265-1277
45. Berridge, M. J., Lipp, P., and Bootman, M. D. (2000) The versatility and universality of calcium signalling Nat. Rev. Mol. Cell Biol. 1, 11-21
46. Haugen, M. H., Flatmark, K., Mikalsen, S. O., and Malandsmo, G. M. (2008) The metastasis-associated protein S100A4 exists in several charged variants suggesting the presence of posttranslational modifications BMC Cancer 8, 172