221
Views
1
CrossRef citations to date
0
Altmetric
Research Articles

Canonical structural-binding modes in the calmodulin–target protein complexes

, , , , & ORCID Icon
Pages 7582-7594 | Received 11 May 2022, Accepted 04 Sep 2022, Published online: 15 Sep 2022

References

  • Aasland, R., Abrams, C., Ampe, C., Ball, L. J., Bedford, M. T., Cesareni, G., Gimona, M., Hurley, J. H., Jarchau, T., Lehto, V. P., Lemmon, M. A., Linding, R., Mayer, B. J., Nagai, M., Sudol, M., Walter, U., & Winder, S. J. (2002). Normalization of nomenclature for peptide motifs as ligands of modular protein domains. FEBS Letters, 513(1), 141–144. https://doi.org/10.1016/S0014-5793(01)03295-1
  • Andreeva, A., Howorth, D., Brenner, S. E., Hubbard, T. J., Chothia, C., & Murzin, A. G. (2004). SCOP database in 2004: Refinements integrate structure and sequence family data. Nucleic Acids Research, 32(Database issue), D226–229. https://doi.org/10.1093/nar/gkh039
  • Ataman, Z. A., Gakhar, L., Sorensen, B. R., Hell, J. W., & Shea, M. A. (2007). The NMDA receptor NR1 C1 region bound to calmodulin: Structural insights into functional differences between homologous domains. Structure (London, England: 1993), 15(12), 1603–1617. https://doi.org/10.1016/j.str.2007.10.012
  • Atreya, H. S., Sahu, S. C., Bhattacharya, A., Chary, K. V., & Govil, G. (2001). NMR derived solution structure of an EF-hand calcium-binding protein from Entamoeba histolytica. Biochemistry, 40(48), 14392–14403. https://doi.org/10.1021/bi0114978
  • Babu, Y. S., Sack, J. S., Greenhough, T. J., Bugg, C. E., Means, A. R., & Cook, W. J. (1985). Three-dimensional structure of calmodulin. Nature, 315(6014), 37–40. https://doi.org/10.1038/315037a0
  • Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., & Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28(1), 235–242. https://doi.org/10.1093/nar/28.1.235
  • Chagot, B., & Chazin, W. J. (2011). Solution NMR structure of Apo-calmodulin in complex with the IQ motif of human cardiac sodium channel NaV1.5. Journal of Molecular Biology, 406(1), 106–119. https://doi.org/10.1016/j.jmb.2010.11.046
  • Chen, W., Shen, Z., Asteriti, S., Chen, Z., Ye, F., Sun, Z., Wan, J., Montell, C., Hardie, R. C., Liu, W., & Zhang, M. (2021). Calmodulin binds to Drosophila TRP with an unexpected mode. Structure (London, England: 1993), 29(4), 330–344.e4.e334. https://doi.org/10.1016/j.str.2020.11.016
  • Clapperton, J. A., Martin, S. R., Smerdon, S. J., Gamblin, S. J., & Bayley, P. M. (2002). Structure of the complex of calmodulin with the target sequence of calmodulin-dependent protein kinase I: Studies of the kinase activation mechanism. Biochemistry, 41(50), 14669–14679. https://doi.org/10.1021/bi026660t
  • Collu, G., Bierig, T., Krebs, A.-S., Engilberge, S., Varma, N., Guixà-González, R., Sharpe, T., Deupi, X., Olieric, V., Poghosyan, E., & Benoit, R. M. (2022). Chimeric single alpha-helical domains as rigid fusion protein connections for protein nanotechnology and structural biology. Structure (London, England: 1993), 30(1), 95–106.e7.e107. https://doi.org/10.1016/j.str.2021.09.002
  • Creon, A., Josts, I., Niebling, S., Huse, N., & Tidow, H. (2018). Conformation-specific detection of calmodulin binding using the unnatural amino acid p-azido-phenylalanine (AzF) as an IR-sensor. Structural Dynamics (Melville, NY), 5(6), 064701. https://doi.org/10.1063/1.5053466
  • de Lima Morais, D. A., Fang, H., Rackham, O. J., Wilson, D., Pethica, R., Chothia, C., & Gough, J. (2011). SUPERFAMILY 1.75 including a domain-centric gene ontology method. Nucleic Acids Research, 39(Database issue), D427–434. https://doi.org/10.1093/nar/gkq1130
  • Denessiouk, K., Permyakov, S., Denesyuk, A., Permyakov, E., & Johnson, M. S. (2014). Two structural motifs within canonical EF-hand calcium-binding domains identify five different classes of calcium buffers and sensors. PloS One, 9(10), e109287. https://doi.org/10.1371/journal.pone.0109287
  • Denesyuk, A. I., Permyakov, S. E., Johnson, M. S., Permyakov, E. A., & Denessiouk, K. (2017a). Building kit for metal cation binding sites in proteins. Biochemical & Biophysical Research Communications, 494(1–2), 311–317. https://doi.org/10.1016/j.bbrc.2017.10.034
  • Denesyuk, A. I., Permyakov, S. E., Johnson, M. S., Permyakov, E. A., & Denessiouk, K. (2017b). Novel calcium recognition constructions in proteins: Calcium blade and EF-hand zone. Biochemical & Biophysical Research Communications, 483(3), 958–963. https://doi.org/10.1016/j.bbrc.2017.01.040
  • Dosztányi, Z., Csizmok, V., Tompa, P., & Simon, I. (2005). IUPred: Web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics (Oxford, England), 21(16), 3433–3434. https://doi.org/10.1093/bioinformatics/bti541
  • Dunlap, T. B., Guo, H.-F., Cook, E. C., Holbrook, E., Rumi-Masante, J., Lester, T. E., Colbert, C. L., Vander Kooi, C. W., & Creamer, T. P. (2014). Stoichiometry of the calcineurin regulatory domain–calmodulin complex. Biochemistry, 53(36), 5779–5790. https://doi.org/10.1021/bi5004734
  • Elshorst, B., Hennig, M., Försterling, H., Diener, A., Maurer, M., Schulte, P., Schwalbe, H., Griesinger, C., Krebs, J., Schmid, H., Vorherr, T., & Carafoli, E. (1999). NMR solution structure of a complex of calmodulin with a binding peptide of the Ca2+ pump. Biochemistry, 38(38), 12320–12332. https://doi.org/10.1021/bi9908235
  • Fallon, J. L., Halling, D. B., Hamilton, S. L., & Quiocho, F. A. (2005). Structure of calmodulin bound to the hydrophobic IQ domain of the cardiac Ca(v)1.2 calcium channel. Structure (London, England: 1993), 13(12), 1881–1886. https://doi.org/10.1016/j.str.2005.09.021
  • Gardill, B. R., Rivera-Acevedo, R. E., Tung, C. C., & Van Petegem, F. (2019). Crystal structures of Ca(2+)-calmodulin bound to NaV C-terminal regions suggest role for EF-hand domain in binding and inactivation. Proceedings of the National Academy of Sciences of the United States of America, 116(22), 10763–10772. https://doi.org/10.1073/pnas.1818618116
  • Gomes, A. V., Barnes, J. A., & Vogel, H. J. (2000). Spectroscopic characterization of the interaction between calmodulin-dependent protein kinase I and calmodulin. Archives of Biochemistry & Biophysics, 379(1), 28–36. https://doi.org/10.1006/abbi.2000.1827
  • Graether, S. P., Heinonen, T. Y., Raharjo, W. H., Jin, J. P., & Mak, A. S. (1997). Tryptophan residues in caldesmon are major determinants for calmodulin binding. Biochemistry, 36(2), 364–369. https://doi.org/10.1021/bi962008k
  • Gsponer, J., Christodoulou, J., Cavalli, A., Bui, J. M., Richter, B., Dobson, C. M., & Vendruscolo, M. (2008). A coupled equilibrium shift mechanism in calmodulin-mediated signal transduction. Structure (London, England: 1993), 16(5), 736–746. https://doi.org/10.1016/j.str.2008.02.017
  • Halling, D. B., Georgiou, D. K., Black, D. J., Yang, G., Fallon, J. L., Quiocho, F. A., Pedersen, S. E., & Hamilton, S. L. (2009). Determinants in CaV1 channels that regulate the Ca2+ sensitivity of bound calmodulin. The Journal of Biological Chemistry, 284(30), 20041–20051. https://doi.org/10.1074/jbc.M109.013326
  • Hoeflich, K. P., & Ikura, M. (2002). Calmodulin in action: Diversity in target recognition and activation mechanisms. Cell, 108(6), 739–742. https://doi.org/10.1016/S0092-8674(02)00682-7
  • Holt, C., Hamborg, L., Lau, K., Brohus, M., Sørensen, A. B., Larsen, K. T., Sommer, C., Van Petegem, F., Overgaard, M. T., & Wimmer, R. (2020). The arrhythmogenic N53I variant subtly changes the structure and dynamics in the calmodulin N-terminal domain, altering its interaction with the cardiac ryanodine receptor. The Journal of Biological Chemistry, 295(22), 7620–7634. https://doi.org/10.1074/jbc.RA120.013430
  • Hornbeck, P. V., Kornhauser, J. M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B., Latham, V., & Sullivan, M. (2012). PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Research, 40(Database issue), D261–270. https://doi.org/10.1093/nar/gkr1122
  • Ishida, H., Nakashima, K., Kumaki, Y., Nakata, M., Hikichi, K., & Yazawa, M. (2002). The solution structure of apocalmodulin from Saccharomyces cerevisiae implies a mechanism for its unique Ca2+ binding property. Biochemistry, 41(52), 15536–15542. https://doi.org/10.1021/bi020330r
  • Ishida, T., & Kinoshita, K. (2007). PrDOS: Prediction of disordered protein regions from amino acid sequence. Nucleic Acids Research, 35(Web Server Issue), W460–464. https://doi.org/10.1093/nar/gkm363
  • Jurado, L. A., Chockalingam, P. S., & Jarrett, H. W. (1999). Apocalmodulin. Physiological Reviews, 79(3), 661–682. https://doi.org/10.1152/physrev.1999.79.3.661
  • Keller, J. P. (2017). Solution of the structure of a calmodulin–peptide complex in a novel configuration from a variably twinned data set. Acta Crystallographica. Section D, Structural Biology, 73(Pt 1), 22–31. https://doi.org/10.1107/S2059798316019318
  • Komolov, K. E., Sulon, S. M., Bhardwaj, A., van Keulen, S. C., Duc, N. M., Laurinavichyute, D. K., Lou, H. J., Turk, B. E., Chung, K. Y., Dror, R. O., & Benovic, J. L. (2021). Structure of a GRK5–calmodulin complex reveals molecular mechanism of GRK activation and substrate targeting. Molecular Cell, 81(2), 323–339.e11.e311. https://doi.org/10.1016/j.molcel.2020.11.026
  • Kraulis, P. J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. Journal of Applied Crystallography, 24(5), 946–950. https://doi.org/10.1107/S0021889891004399
  • Kretsinger, R. H., & Nockolds, C. E. (1973). Carp muscle calcium-binding protein. II. Structure determination and general description. The Journal of Biological Chemistry, 248(9), 3313–3326. http://www.ncbi.nlm.nih.gov/pubmed/4700463
  • Kretsinger, R. H., Rudnick, S. E., & Weissman, L. J. (1986). Crystal structure of calmodulin. Journal of Inorganic Biochemistry, 28(2-3), 289–302. https://doi.org/10.1016/0162-0134(86)80093-9
  • Kursula, P., Vahokoski, J., & Wilmanns, M. (2006). Recognition of human death-associated protein kinases by calmodulin.
  • Lau, S. Y., Procko, E., & Gaudet, R. (2012). Distinct properties of Ca2+-calmodulin binding to N- and C-terminal regulatory regions of the TRPV1 channel. The Journal of General Physiology, 140(5), 541–555. https://doi.org/10.1085/jgp.201210810
  • Liu, Y., Zheng, X., Mueller, G. A., Sobhany, M., DeRose, E. F., Zhang, Y., London, R. E., & Birnbaumer, L. (2012). Crystal structure of calmodulin binding domain of orai1 in complex with Ca2+ calmodulin displays a unique binding mode. The Journal of Biological Chemistry, 287(51), 43030–43041. https://doi.org/10.1074/jbc.M112.380964
  • Majava, V., & Kursula, P. (2009). Domain swapping and different oligomeric States for the complex between calmodulin and the calmodulin-binding domain of calcineurin a. PloS One, 4(4), e5402. https://doi.org/10.1371/journal.pone.0005402
  • Marlow, M. S., & Wand, A. J. (2006). Conformational dynamics of calmodulin in complex with the calmodulin-dependent kinase kinase alpha calmodulin-binding domain. Biochemistry, 45(29), 8732–8741. https://doi.org/10.1021/bi060420m
  • Maximciuc, A. A., Putkey, J. A., Shamoo, Y., & Mackenzie, K. R. (2006). Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode. Structure (London, England: 1993), 14(10), 1547–1556. https://doi.org/10.1016/j.str.2006.08.011
  • Meador, W. E., Means, A. R., & Quiocho, F. A. (1992). Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulinpeptide complex. Science (New York, NY), 257(5074), 1251–1255. https://doi.org/10.1126/science.1519061
  • Meszaros, B., Simon, I., & Dosztanyi, Z. (2009). Prediction of protein binding regions in disordered proteins. PLoS Computational Biology, 5(5), e1000376. https://doi.org/10.1371/journal.pcbi.1000376
  • Mishra, K., Fuenzalida-Werner, J. P., Pennacchietti, F., Janowski, R., Chmyrov, A., Huang, Y., Zakian, C., Klemm, U., Testa, I., Niessing, D., Ntziachristos, V., & Stiel, A. C. (2022). Genetically encoded photo-switchable molecular sensors for optoacoustic and super-resolution imaging. Nature Biotechnology, 40(4), 598–605. https://doi.org/10.1038/s41587-021-01100-5
  • Murzin, A. G., Brenner, S. E., Hubbard, T., & Chothia, C. (1995). SCOP: A structural classification of proteins database for the investigation of sequences and structures. Journal of Molecular Biology, 247(4), 536–540. https://doi.org/10.1006/jmbi.1995.0159
  • Ng, H. L., Alber, T. A., & Wand, A. J. (2010). Calmodulin bound to peptide from calmodulin kinase II (CaMKII).
  • Ng, H. L., Greenstein, A., Marletta, M., Wand, A. J., & Alber, T. (2010). Structural diversity in calmodulin recognition of nitric oxide synthases.
  • O'Neil, K. T., & DeGrado, W. F. (1990). How calmodulin binds its targets: Sequence independent recognition of amphiphilic alpha-helices. Trends in Biochemical Sciences, 15(2), 59–64. https://doi.org/10.1016/0968-0004(90)90177-D
  • Oates, M. E., Romero, P., Ishida, T., Ghalwash, M., Mizianty, M. J., Xue, B., Dosztányi, Z., Uversky, V. N., Obradovic, Z., Kurgan, L., Dunker, A. K., & Gough, J. (2013). D(2)P(2): Database of disordered protein predictions. Nucleic Acids Research, 41(Database issue), D508–516. https://doi.org/10.1093/nar/gks1226
  • Obradovic, Z., Peng, K., Vucetic, S., Radivojac, P., & Dunker, A. K. (2005). Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins: Structure, Function, & Bioinformatics, 61(S7), 176–182. https://doi.org/10.1002/prot.20735
  • Osawa, M., Swindells, M. B., Tanikawa, J., Tanaka, T., Mase, T., Furuya, T., & Ikura, M. (1998). Solution structure of calmodulin-W-7 complex: The basis of diversity in molecular recognition. Journal of Molecular Biology, 276(1), 165–176. https://doi.org/10.1006/jmbi.1997.1524
  • Patel, N., Stengel, F., Aebersold, R., & Gold, M. G. (2017). Molecular basis of AKAP79 regulation by calmodulin. Nature Communications, 8(1), 1681. https://doi.org/10.1038/s41467-017-01715-w
  • Peng, K., Radivojac, P., Vucetic, S., Dunker, A. K., & Obradovic, Z. (2006). Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics, 7(1), 208. https://doi.org/10.1186/1471-2105-7-208
  • Permyakov, E. A. (2009). Metalloproteomics. John Wiley & Sons Inc.
  • Permyakov, E. A., & Kretsinger, R. H. (2011). Calcium binding proteins. John Wiley & Sons.
  • Rodríguez-Castañeda, F., Maestre-Martínez, M., Coudevylle, N., Dimova, K., Junge, H., Lipstein, N., Lee, D., Becker, S., Brose, N., Jahn, O., Carlomagno, T., & Griesinger, C. (2010). Modular architecture of Munc13/calmodulin complexes: Dual regulation by Ca2+ and possible function in short-term synaptic plasticity. The EMBO Journal, 29(3), 680–691. https://doi.org/10.1038/emboj.2009.373
  • Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., & Dunker, A. K. (2001). Sequence complexity of disordered protein. Proteins: Structure, Function, & Genetics, 42(1), 38–48. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd = Retrieve&db = PubMed&dopt = Citation&list_uids=11093259
  • Sarhan, M. F., Tung, C. C., Van Petegem, F., & Ahern, C. A. (2012). Crystallographic basis for calcium regulation of sodium channels. Proceedings of the National Academy of Sciences of the United States of America, 109(9), 3558–3563. https://doi.org/10.1073/pnas.1114748109
  • Sobolev, V., Sorokine, A., Prilusky, J., Abola, E. E., & Edelman, M. (1999). Automated analysis of interatomic contacts in proteins. Bioinformatics (Oxford, England), 15(4), 327–332. https://doi.org/10.1093/bioinformatics/15.4.327
  • Song, J.-G., Kostan, J., Grishkovskaya, I., & K, D.-C. (2014). Crystal structure of the plectin 1a actin-binding domain/N-terminal domain of calmodulin complex.
  • Strulovich, R., Tobelaim, W. S., Attali, B., & Hirsch, J. A. (2016). Structural insights into the M-channel proximal C-terminus/calmodulin complex. Biochemistry, 55(38), 5353–5365. https://doi.org/10.1021/acs.biochem.6b00477
  • Tidow, H., & Nissen, P. (2013). Structural diversity of calmodulin binding to its target sites. The FEBS Journal, 280(21), 5551–5565. https://doi.org/10.1111/febs.12296
  • Tidow, H., Poulsen, L. R., Andreeva, A., Knudsen, M., Hein, K. L., Wiuf, C., Palmgren, M. G., & Nissen, P. (2012). A bimodular mechanism of calcium control in eukaryotes. Nature, 491(7424), 468–472. https://doi.org/10.1038/nature11539
  • Valentine, K. G., Ng, H. L., Schneeweis, J. K., Kranz, J. K., Frederick, K. K., Alber, T., & Wand, A. J. (2007a). Ultrahigh resolution crystal structure of calmodulin–smooth muscle light kinase peptide complex.
  • Valentine, K. G., Ng, H. L., Schneeweis, L., Kranz, J. K., Frederick, K. K., Alber, T., & Wand, A. J. (2007b). Crystal structure of calmodulin–neuronal nitric oxide synthase complex. https://doi.org/10.2210/pdb2O60/pdb
  • Vlach, J., Samal, A. B., & Saad, J. S. (2014). Solution structure of calmodulin bound to the binding domain of the HIV-1 matrix protein. The Journal of Biological Chemistry, 289(12), 8697–8705. https://doi.org/10.1074/jbc.M113.543694
  • Wall, M. E., Clarage, J. B., & Phillips, G. N. (1997). Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering. Structure (London, England: 1993), 5(12), 1599–1612. https://doi.org/10.1016/S0969-2126(97)00308-0
  • Walsh, I., Martin, A. J., Di Domenico, T., & Tosatto, S. C. (2012). ESpritz: Accurate and fast prediction of protein disorder. Bioinformatics (Oxford, England), 28(4), 503–509. https://doi.org/10.1093/bioinformatics/btr682
  • Weljie, A. M., & Vogel, H. J. (2000). Tryptophan fluorescence of calmodulin binding domain peptides interacting with calmodulin containing unnatural methionine analogues. Protein Engineering, 13(1), 59–66. https://doi.org/10.1093/protein/13.1.59
  • Williams, R. J. P. (1999). Calcium: The developing role of its chemistry in biological evolution. In E. Carafoli & C. B. Klee (Eds.), Calcium as a cellular regulator (pp. 3–27). Oxford University Press.
  • Wilson, M. A., & Brunger, A. T. (2000). The 1.0 A crystal structure of Ca(2+)-bound calmodulin: An analysis of disorder and implications for functionally relevant plasticity. Journal of Molecular Biology, 301(5), 1237–1256. https://doi.org/10.1006/jmbi.2000.4029
  • Yamauchi, E., Nakatsu, T., Matsubara, M., Kato, H., & Taniguchi, H. (2003). Crystal structure of a MARCKS peptide containing the calmodulin-binding domain in complex with Ca2+-calmodulin. Nature Structural Biology, 10(3), 226–231. https://doi.org/10.1038/nsb900
  • Yap, K. L., Kim, J., Truong, K., Sherman, M., Yuan, T., & Ikura, M. (2000). Calmodulin target database. Journal of Structural & Functional Genomics, 1(1), 8–14. https://doi.org/10.1023/A:1011320027914
  • Yu, Q., Anderson, D. E., Kaur, R., Fisher, A. J., & Ames, J. B. (2021). The crystal structure of calmodulin bound to the cardiac ryanodine receptor (RyR2) at residues Phe4246-Val4271 reveals a fifth calcium binding site. Biochemistry, 60(14), 1088–1096. https://doi.org/10.1021/acs.biochem.1c00152
  • Zhang, M., Abrams, C., Wang, L., Gizzi, A., He, L., Lin, R., Chen, Y., Loll, P. J., Pascal, J. M., & Zhang, J-f (2012). Structural basis for calmodulin as a dynamic calcium sensor. Structure (London, England: 1993), 20(5), 911–923. https://doi.org/10.1016/j.str.2012.03.019
  • Zhang, M., Pascal, J. M., & Zhang, J. F. (2013). Unstructured to structured transition of an intrinsically disordered protein peptide in coupling Ca(2)(+)-sensing and SK channel activation. Proceedings of the National Academy of Sciences of the United States of America, 110(12), 4828–4833. https://doi.org/10.1073/pnas.1220253110
  • Zhang, M., & Yuan, T. (1998). Molecular mechanisms of calmodulin’s functional versatility. Biochemistry & Cell Biology = Biochimie et Biologie Cellulaire, 76(2–3), 313–323. https://doi.org/10.1139/bcb-76-2-3-313

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.