Binding of calcium, magnesium, and target peptides to CDC31, the centrin of yeast Saccharomyces cerevisiae

Biochemistry

Volumn 50, Issue 29, 2011, Pages 6409-6422

  Miron, Simona ^e   Durand, Dominique ^c   Chilom, Claudia ^a,b,f   Pérez, Javier ^d   Craescu, Constantin T ^a,b  

^a INSTITUT CURIE   (France)

^b Centre Universitaire   (France)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^d SYNCHROTRON SOLEIL   (France)

^e University of Bucharest ^*  (France)

^f UNIVERSITY OF BUCHAREST   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPATHIC; BIOPHYSICAL TECHNIQUES; C-TERMINAL DOMAINS; CALCIUM BINDING PROTEINS; CELL DIVISIONS; CENTRINS; EF-HAND; HELIX CONTENT; HYDROPHOBIC AMINO ACIDS; ISOTHERMAL TITRATION CALORIMETRY; MIXED SITES; N-TERMINAL DOMAINS; NATURAL TARGETS; NUCLEAR EXPORT; PROTEIN TARGETS; RESTING CELLS; SMALL ANGLE X-RAY SCATTERING; TARGET SURFACE; YEAST SACCHAROMYCES CEREVISIAE;

AMINO ACIDS; BINDING ENERGY; CELL PROLIFERATION; CONFORMATIONS; MAGNESIUM; PEPTIDES; PLANTS (BOTANY); X RAY SCATTERING; YEAST;

CALCIUM;

CALCIUM; CENTRIN; MAGNESIUM; MESSENGER RNA; PEPTIDE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CONTROLLED STUDY; HYDROPHOBICITY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; X RAY CRYSTALLOGRAPHY; YEAST;

AMINO ACID SEQUENCE; CALCIUM; CALCIUM-BINDING PROTEINS; CALORIMETRY; CELL CYCLE PROTEINS; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MAGNESIUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; THERMODYNAMICS;

SACCHAROMYCES CEREVISIAE;

EID: 79960478493     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200518d     Document Type: Article

References (49)

1. Schiebel, E. and Bornens, M. (1995) In search of a function for centrins Trends Cell Biol. 5, 197-201
2. Salisbury, J. L., Suino, K. M., Busby, R., and Springett, M. (2002) Centrin-2 is required for centriole duplication in mammalian cells Curr. Biol. 12, 1287-1292 (Pubitemid 34869878)
3. Sanders, M. A. and Salisbury, J. L. (1994) Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii J. Cell Biol. 124, 795-805 (Pubitemid 24085787)
4. Araki, M., Masutani, C., Takemura, M., Uchida, A., Sugasawa, K., Kondoh, J., Ohkuma, Y., and Hanaoka, F. (2001) Centrosome protein centrin 2/caltractin 1 is part of the Xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair J. Biol. Chem. 276, 18665-18672
5. Miron, S., Duchambon, P., Blouquit, Y., Durand, D., and Craescu, C. T. (2008) The carboxy-terminal domain of Xeroderma pigmentosum complementation group C protein, involved in TFIIH and centrin binding, is highly disordered Biochemistry 47, 1403-1413 (Pubitemid 351198716)
6. Resendes, K. K., Rasala, B. A., and Forbes, D. J. (2008) Centrin 2 localizes to the vertebrate nuclear pore and plays a role in mRNA and protein export Mol. Cell. Biol. 28, 1755-1769
7. Fischer, T., Rodriguez-Navarro, S., Pereira, G., Racz, A., Schiebel, E., and Hurt, E. (2004) Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery Nat. Cell Biol. 6, 840-848 (Pubitemid 39207249)
8. Chen, L. and Madura, K. (2008) Centrin/Cdc31 is a novel regulator of protein degradation Mol. Cell. Biol. 28, 1829-1840
9. Spang, A., Courtney, I., Fackler, U., Matzner, M., and Schiebel, E. (1993) The calcium-binding protein cell division cycle 31 of Saccharomyces cerevisiae is a component of the half bridge of the spindle pole body J. Cell Biol. 123, 405-416 (Pubitemid 23313964)
10. Paoletti, A., Bordes, N., Haddad, R., Schwartz, C. L., Chang, F., and Bornens, M. (2003) Fission yeast cdc31p is a component of the half-bridge and controls SPB duplication Mol. Biol. Cell 14, 2793-2808 (Pubitemid 36871522)
11. Adams, I. R. and Kilmartin, J. V. (2000) Spindle pole body duplication: a model for centrosome duplication? Trends Cell Biol. 10, 329-335 (Pubitemid 30445240)
12. Byers, B. (1981) Multiple roles of the spindle pole bodies in the life cycle of Saccharomyces cerevisiae. Molecular Genetics in Yeast, Alfred Benzon Symposium 16 (von Wettstein, D., Friis, J., Kielland-Brand, M., and Stenderup, A., Eds.) pp 119-131, Munksgaard, Copenhagen, Denmark.
13. Biggins, S. and Rose, M. D. (1994) Direct Interaction between Yeast Spindle Pole Body Components: Karlp Is Required for Cdc31p Localization to the Spindle Pole Body J. Cell Biol. 4, 843-852 (Pubitemid 24151179)
14. Spang, A., Courtney, I., Grein, K., Matzner, M., and Schiebel, E. (1995) The Cdc31p- binding protein Kar1p is a component of the half bridge of the yeast spindle pole body J. Cell Biol. 128, 863-877
15. Jaspersen, S. L., Giddings, J. T. H., and Winey, M. (2002) Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p J. Cell Biol. 159, 945-956 (Pubitemid 36055750)
16. Kilmartin, J. V. (2003) Sfi1p has conserved centrin-binding sites and an essential function in budding yeast spindle body duplication J. Cell Biol. 162, 1211-1221 (Pubitemid 37210878)
17. Li, S., Sandercock, A. M., Conduit, P., Robinson, C. V., Williams, R. L., and Kilmartin, J. V. (2006) Structural role of Sfi1p-centrin filaments in budding yeast spindle pole body duplication J. Cell Biol. 173, 867-877
18. Martinez-Sanz, J., Yang, A., Blouquit, Y., Duchambon, P., Assairi, L., and Craescu, C. T. (2006) Binding of human centrin 2 to the centrosomal protein hSfi1 FEBS J. 273, 4504-4515 (Pubitemid 44401601)
19. Popescu, A., Miron, S., Blouquit, Y., Duchambon, P., and Craescu, C. T. (2003) Xeroderma pigmentosum group C protein possesses a high affinity binding site for human centrin 2 and calmodulin J. Biol. Chem. 278, 40252-40261 (Pubitemid 37248593)
20. Nishi, R., Okuda, Y., Wanatabe, E., Mori, T., Iwai, S., Masutani, C., Sugasawa, K., and Hanoka, F. (2005) Centrin 2 stimulates nucleotide excission repair by interacting with Xeroderma pigmentosum group C protein Mol. Cell. Biol. 25, 5664-5674 (Pubitemid 40853600)
21. Cox, J. A., Tirone, F., Durussel, I., Firanescu, C., Blouquit, Y., Duchambon, P., and Craescu, C. T. (2005) Calcium and magnesium binding to human centrin 3 and interaction with target peptides Biochemistry 44, 840-850 (Pubitemid 40129644)
22. Durussel, I., Blouquit, Y., Middendorp, S., Craescu, C. T., and Cox, J. A. (2000) Cation- and peptide-binding properties of human centrin 2 FEBS Lett. 472, 208-212 (Pubitemid 30224465)
23. Veeraraghavan, S., Fagan, P. A., Hu, H., Lee, V., Harper, J. F., Bessie, H., and Chazin, W. J. (2002) Structural independence of the two EF-hand domains of caltractin J. Biol. Chem. 277, 28564-28571 (Pubitemid 41079283)
24. 2+-controlled target binding Biochemistry 49, 4383-4394
25. Geier, B. M., Wiech, H., and Schiebel, E. (1996) Binding of centrins and yeast calmodulin to synthetic peptides corresponding to binding sites in the spindle pole body components Kar1p and Spc110p J. Biol. Chem. 271, 28366-28374 (Pubitemid 26374654)
26. Jani, D., Lutz, S., Marshall, N. J., Fischer, T., Köhler, A., Ellisdon, A. M., Hurt, E., and Stewart, M. (2009) Sus1, Cdc31, and the Sac3 CID region form a conserved interaction platform that promotes nuclear pore association and mRNA export Mol. Cell 33, 727-737
27. Charbonnier, J. B., Renaud, E., Miron, S., Le Du, M. H., Blouquit, Y., Duchambon, P., Christova, P., Shosheva, A., Rose, T., Angulo, J. F., and Craescu, C. T. (2007) Structural, thermodynamic, and cellular characterization of human centrin 2 interaction with Xeroderma pigmentosum group C protein J. Mol. Biol. 373, 1032-1046 (Pubitemid 47500171)
28. Colowick, S. P. and Womack, F. C. (1969) Binding of diffusible molecules by macromolecules: rapid measurement by rate of dialysis J. Biol. Chem. 244, 774-747
29. Cox, J. A. (1996) in Guidbook to the Calcium-Binding Proteins (Celio, M. R., Pauls, T., and Schwaller, B., Eds.) pp 1-12, Oxford University Press, Oxford.
30. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260 (Pubitemid 32006234)
31. David, G. and Pérez, J. (2009) Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline J. Appl. Crystallogr. 42, 892-900
32. Mertens, H. D. and Svergun, D. I. (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering J. Struct. Biol. 172, 128-141
33. Milos, M., Schaer, J. J., Comte, M., and Cox, J. A. (1986) Calcium-proton and calcium-magnesium antagonisms in calmodulin: microcalorimetric and potentiometric analyses Biochemistry 25, 6279-6287 (Pubitemid 17204067)
34. Tanaka, T. and Hidaka, H. (1980) Hydrophobic regions function in calmodulin-enzyme(s) interactions J. Biol. Chem. 255, 11078-11080
35. Davis, T. N. (1995) Calcium in Saccharomyces cervisiae Adv. Second Messenger Phospoprotein Res. 30, 339-358
36. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25, 495-503 (Pubitemid 23564996)
37. Svergun, D. I., Petoukhov, M. V., and Koch, M. H. (2001) Determination of domain structure of proteins from X-ray solution scattering Biophys. J. 80, 2946-2953 (Pubitemid 32521666)
38. Yap, K. L., Kim, J., Truong, K., Sherman, M., Yuan, T., and Ikura, M. (2000) Calmodulin Target Database J. Struct. Funct. Genomics 1, 8-14
39. 2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae J. Biol. Chem. 277, 33075-33080 (Pubitemid 34984823)
40. Popa, C. V., Dumitru, I., Ruta, L. L., Danet, A. F., and Farcasanu, I. C. (2010) Exogenous oxidative stress induces Ca2+ release in the yeast Saccharomyces cerevisiae FEBS J. 277, 4027-4038
41. 2+- influx and mating Mol. Cell. Biol. 14, 8259-8271
42. Bonilla, M., Nastase, K., and Cunningham, K. W. (2002) Essential role of calcineurin in response to endoplasmic reticulum stress EMBO J. 21, 2343-2353 (Pubitemid 34546707)
43. Cox, J. A., Comte, M., and Stein, E. A. (1981) Calmodulin-free skeletal muscle troponin C prepared in the absence of urea Biochem. J. 195, 205-311
44. Haiech, J., Klee, C. B., and Demaille, J. G. (1981) Effects of cations on affinity of calmodulin for calcium: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes Biochemistry 20, 3890-3897 (Pubitemid 11009231)
45. 2+-dependent interactions of calmodulin with target sequences Protein Sci. 9, 2477-2488 (Pubitemid 32105730)
46. Martinez-Sanz, J., Kateb, F., Assairi, L., Blouquit, Y., Bodenhausen, G., Abergel, D., Mouawad, L., and Craescu, C. T. (2010) Structure, Dynamics and Thermodynamics of the human Centrin 2/hSfi1 complex J. Mol. Biol. 395, 191-204
47. Geiser, J. R., van Tuinen, D., Brockerhoff, S. E., Neff, M. M., and Davis, T. N. (1991) Can calmodulin function without binding calcium? Cell 65, 1-20
48. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering Nucleic Acids Res. 16, 10881-10890
49. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: multiple sequence alignments in PostScript Bioinformatics 15, 305-308 (Pubitemid 29213756)