The number and location of EF hand motifs dictates the calcium dependence of polycystin-2 function

FASEB Journal

Volumn 28, Issue 5, 2014, Pages 2332-2346

  Kuo, Ivana Y ^a   Keeler, Camille ^a   Corbin, Rachel ^a   Ćelić, Andjelka ^a   Petri, Edward T ^a,b   Hodsdon, Michael E ^a   Ehrlich, Barbara E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NOVI SAD   (Serbia)

Author keywords

Intracellular release; Ion channels; Kidney; Signaling; TRP channels

Indexed keywords

CALCIUM; POLYCYSTIN 2;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOINFORMATICS; BIOPHYSICS; CALCIUM BINDING; CALCIUM SIGNALING; CELL FUNCTION; CONTROLLED STUDY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; LLC PK1 CELL LINE; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTON NUCLEAR MAGNETIC RESONANCE; WILD TYPE;

INTRACELLULAR RELEASE; ION CHANNELS; KIDNEY; SIGNALING; TRP CHANNELS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CALCIUM CHANNELS; CELL LINE; COMPUTATIONAL BIOLOGY; EF HAND MOTIFS; HUMANS; KIDNEY; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; PROTEIN BINDING; SEA URCHINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SWINE; TRPP CATION CHANNELS;

EID: 84901020482     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-247106     Document Type: Article

References (37)

1. Yoshiba, S., Shiratori, H., Kuo, I. Y., Kawasumi, A., Shinohara, K., Nonaka, S., Asai, Y., Sasaki, G., Belo, J. A., Sasaki, H., Nakai, J., Dworniczak, B., Ehrlich, B. E., Pennekamp, P., and Hamada, H. (2012) Cilia at the node of mouse embryos sense fluid flow for left-right determination via Pkd2. Science 338, 226-231
2. Nauli, S. M., Alenghat, F. J., Luo, Y., Williams, E., Vassilev, P., Li, X., Elia, A. E., Lu, W., Brown, E. M., Quinn, S. J., Ingber, D. E., and Zhou, J. (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33, 129-137
3. Sharif-Naeini, R., Folgering, J. H., Bichet, D., Duprat, F., Lauritzen, I., Arhatte, M., Jodar, M., Dedman, A., Chatelain, F. C., Schulte, U., Retailleau, K., Loufrani, L., Patel, A., Sachs, F., Delmas, P., Peters, D. J., and Honore, E. (2009) Polycystin-1 and-2 dosage regulates pressure sensing. Cell 139, 587-596
4. Koulen, P., Cai, Y., Geng, L., Maeda, Y., Nishimura, S., Witzgall, R., Ehrlich, B. E., and Somlo, S. (2002) Polycystin-2 is an intracellular calcium release channel. Nat. Cell. Biol. 4, 191-197
5. Berridge, M. J., Bootman, M. D., and Roderick, H. L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529
6. Cai, Y., Anyatonwu, G., Okuhara, D., Lee, K. B., Yu, Z., Onoe, T., Mei, C. L., Qian, Q., Geng, L., Wiztgall, R., Ehrlich, B. E., and Somlo, S. (2004) Calcium dependence of polycystin-2 channel activity is modulated by phosphorylation at Ser812. J. Biol. Chem. 279, 19987-19995
7. Kuo, I. Y., and Ehrlich, B. E. (2012) Ion channels in renal disease. Chem. Rev. 112, 6353-6372
8. Yu, Y., Ulbrich, M. H., Li, M. H., Buraei, Z., Chen, X. Z., Ong, A. C., Tong, L., Isacoff, E. Y., and Yang, J. (2009) Structural and molecular basis of the assembly of the TRPP2/PKD1 complex. Proc. Natl. Acad. Sci. U. S. A. 106, 11558-11563
9. Giamarchi, A., Feng, S., Rodat-Despoix, L., Xu, Y., Bubenshchikova, E., Newby, L. J., Hao, J., Gaudioso, C., Crest, M., Lupas, A. N., Honore, E., Williamson, M. P., Obara, T., Ong, A. C., and Delmas, P. (2010) A polycystin-2 (TRPP2) dimerization domain essential for the function of heteromeric polycystin complexes. EMBO J. 29, 1176-1191
10. Sammels, E., Devogelaere, B., Mekahli, D., Bultynck, G., Missiaen, L., Parys, J. B., Cai, Y., Somlo, S., and De Smedt, H. (2010) Polycystin-2 activation by inositol 1,4,5-trisphosphate-induced Ca2β release requires its direct association with the inositol 1,4,5-trisphosphate receptor in a signaling microdomain. J. Biol. Chem. 285, 18794-18805
11. Celic, A., Petri, E. T., Demeler, B., Ehrlich, B. E., and Boggon, T. J. (2008) Domain mapping of the polycystin-2 C-terminal tail using de novo molecular modeling and biophysical analysis. J. Biol. Chem. 283, 28305-28312
12. Hateboer, N., Veldhuisen, B., Peters, D., Breuning, M. H., San-Millan, J. L., Bogdanova, N., Coto, E., van Dijk, M. A., Afzal, A. R., Jeffery, S., Saggar-Malik, A. K., Torra, R., Dimitrakov, D., Martinez, I., de Castro, S. S., Krawczak, M., and Ravine, D. (2000) Location of mutations within the PKD2 gene influences clinical outcome. Kidney Int. 57, 1444-1451
13. Harris, P. C., and Torres, V. E. (2009) Polycystic kidney disease. Annu. Rev. Med. 60, 321-337
14. Schulze, C., Sticht, H., Meyerhoff, P., and Dietrich, P. (2011) Differential Contribution of EF-hands to the Ca(2)(-)-dependent Activation in the Plant Two-pore Channel TPC1. Plant. J. 68, 424-432
15. Brunet, S., Scheuer, T., Klevit, R., and Catterall, W. A. (2005) Modulation of CaV1.2 channels by Mg2β acting at an EF-hand motif in the COOH-terminal domain. J. Gen. Physiol. 126, 311-323
16. Chagot, B., Potet, F., Balser, J. R., and Chazin, W. J. (2009) Solution NMR structure of the C-terminal EF-hand domain of human cardiac sodium channel NaV1.5. J. Biol. Chem. 284, 6436-6445
17. Miloushev, V. Z., Levine, J. A., Arbing, M. A., Hunt, J. F., Pitt, G. S., and Palmer, A. G., 3rd (2009) Solution structure of the NaV1.2 C-terminal EF-hand domain. J. Biol. Chem. 284, 6446-6454
18. Capozzi, F., Casadei, F., and Luchinat, C. (2006) EF-hand protein dynamics and evolution of calcium signal transduction: an NMR view. J. Biol. Inorg. Chem. 11, 949-962
19. Gifford, J. L., Walsh, M. P., and Vogel, H. J. (2007) Structures and metal-ion-binding properties of the Ca2β-binding helixloop-helix EF-hand motifs. Biochem. J. 405, 199-221
20. Chazin, W. J. (2011) Relating form and function of EF-hand calcium binding proteins. Acc. Chem. Res. 44, 171-179
21. Grabarek, Z. (2006) Structural basis for diversity of the EF-hand calcium-binding proteins. J. Mol. Biol. 359, 509-525
22. Petri, E. T., Celic, A., Kennedy, S. D., Ehrlich, B. E., Boggon, T. J., and Hodsdon, M. E. (2010) Structure of the EF-hand domain of polycystin-2 suggests a mechanism for Ca2β-dependent regulation of polycystin-2 channel activity. Proc. Natl. Acad. Sci. U. S. A. 107, 9176-9181
23. Ćelíc, A. S., Petri, E. T., Benbow, J., Hodsdon, M. E., Ehrlich, B. E., and Boggon, T. J. (2012) Calcium-induced conformational changes in the C-terminal tail of polycystin-2 are necessary for channel gating. J. Biol. Chem. 287, 17232-17240
24. Neill, A. T., Moy, G. W., and Vacquier, V. D. (2004) Polycystin-2 associates with the polycystin-1 homolog, suREJ3, and localizes to the acrosomal region of sea urchin spermatozoa. Mol. Reprod. Dev. 67, 472-477
25. Palmer, A. G., 3rd. (1997) Probing molecular motion by NMR. Curr. Opin. Struct. Biol. 7, 732-737
26. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
27. Bhattacharya, A., Tejero, R., and Montelione, G. T. (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66, 778-795
28. Zweckstetter, M., and Bax, A. (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J. Am. Chem. Soc. 122, 3791-3792
29. Holm, L., and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-549
30. Keeler, C., Poon, G., Kuo, I. Y., Ehrlich, B. E., and Hodsdon, M. E. (2013) An explicit formulation approach for the analysis of calcium binding to EF-hand proteins using isothermal titration calorimetry. Biophys. J. 105, 2843-2853
31. Biekofsky, R. R., Martin, S. R., Browne, J. P., Bayley, P. M., and Feeney, J. (1998) Ca2β coordination to backbone carbonyl oxygen atoms in calmodulin and other EF-hand proteins: 15N chemical shifts as probes for monitoring individual-site Ca2β coordination. Biochemistry (Mosc.) 37, 7617-7629
32. Herrmann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227
33. Mekahli, D., Sammels, E., Luyten, T., Welkenhuyzen, K., van den Heuvel, L. P., Levtchenko, E. N., Gijsbers, R., Bultynck, G., Parys, J. B., De Smedt, H., and Missiaen, L. (2012) Polycystin-1 and polycystin-2 are both required to amplify inositol-trisphosphate-induced Ca2β release. Cell Calcium 51, 452-458
34. Anyatonwu, G. I., Estrada, M., Tian, X., Somlo, S., and Ehrlich, B. E. (2007) Regulation of ryanodine receptor-dependent calcium signaling by polycystin-2. Proc. Natl. Acad. Sci. U. S. A. 104, 6454-6459
35. Li, Y., Wright, J. M., Qian, F., Germino, G. G., and Guggino, W. B. (2005) Polycystin 2 interacts with type I inositol 1,4,5-trisphosphate receptor to modulate intracellular Ca2β signaling. J. Biol. Chem. 280, 41298-41306
36. Dereeper, A., Audic, S., Claverie, J. M., and Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC 10, 8
37. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-469