Mutation of Ser-50 and Cys-66 in Snapin modulates protein structure and stability

Biochemistry

Volumn 51, Issue 16, 2012, Pages 3470-3484

  Navarro, Aaron ^a   Encinar, José A ^a   López Méndez, Blanca ^b   Aguado Llera, David ^a   Prieto, Jesús ^c   Gómez, Javier ^a   Martínez Cruz, Luís Alfonso ^b   Millet, Oscar ^b   González Ros, José Manuel ^a   Fernández Ballester, Gregorio ^a   Neira, José L ^a,d   Ferrer Montiel, Antonio ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b CIC BIOGUNE   (Spain)

^c Structural Biology and Biocomputing Programme   (Spain)

^d UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR ACTIVITIES; HELICAL STRUCTURES; HIGHER ORDER; IN-VITRO; PROTEIN DIMERIZATION; PROTEIN KINASE A; PROTEIN STRUCTURES; PROTEIN THERMAL STABILITY; SECONDARY STRUCTURE ELEMENTS; SECONDARY STRUCTURES; SNARE PROTEINS; TETRAMERS; WILD TYPES;

DIMERIZATION; MOLECULAR BIOLOGY; OLIGOMERIZATION; OLIGOMERS; PHOSPHORYLATION; THERMODYNAMIC STABILITY;

PROTEINS;

CYCLIC AMP DEPENDENT PROTEIN KINASE; OLIGOMER; PROTEIN; SNAPIN; SNARE PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; DIMERIZATION; INFRARED SPECTROSCOPY; MUTAGENESIS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; THERMOSTABILITY; WILD TYPE;

CYSTEINE; MUTATION; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; SERINE; SNARE PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; VESICULAR TRANSPORT PROTEINS;

EID: 84860156451     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201574t     Document Type: Article

References (50)

1. Sudhof, T. C. (2004) The synaptic vesicle cycle Annu. Rev. Neurosci. 27, 509-547
2. Sudhof, T. C. and Rothman, J. E. (2009) Membrane fusion: Grappling with SNARE and SM proteins Science 323, 474-477
3. Wojcik, S. M. and Brose, N. (2007) Regulation of membrane fusion in synaptic excitation-secretion coupling: Speed and accuracy matter Neuron 55, 11-24
4. Chen, Y. A. and Scheller, R. H. (2001) SNARE-mediated membrane fusion Nat. Rev. Mol. Cell Biol. 2, 98-106
5. Calakos, N., Bennett, M. K., Peterson, K. E., and Scheller, R. H. (1994) Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking Science 263, 1146-1149
6. Huntwork, S. and Littleton, J. T. (2007) A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth Nat. Neurosci. 10, 1235-1237
7. Schoch, S., Castillo, P. E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R. C., and Sudhof, T. C. (2002) RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone Nature 415, 321-326
8. Xue, M., Ma, C., Craig, T. K., Rosenmund, C., and Rizo, J. (2008) The Janus-faced nature of the C(2)B domain is fundamental for synaptotagmin-1 function Nat. Struct. Mol. Biol. 15, 1160-1168
9. 2+ binding to synaptotagmin-1 C2 domains mediate neurotransmitter release Proc. Natl. Acad. Sci. U.S.A. 106, 16469-16474
10. Chapman, E. R. (2008) How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615-641
11. Tucker, W. C., Edwardson, J. M., Bai, J., Kim, H. J., Martin, T. F., and Chapman, E. R. (2003) Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells J. Cell Biol. 162, 199-209
12. Bai, J., Wang, C. T., Richards, D. A., Jackson, M. B., and Chapman, E. R. (2004) Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions Neuron 41, 929-942
13. Ilardi, J. M., Mochida, S., and Sheng, Z. H. (1999) Snapin: A SNARE-associated protein implicated in synaptic transmission Nat. Neurosci. 2, 119-124
14. Vites, O., Rhee, J. S., Schwarz, M., Rosenmund, C., and Jahn, R. (2004) Reinvestigation of the role of snapin in neurotransmitter release J. Biol. Chem. 279, 26251-26256
15. Ruder, C., Reimer, T., Delgado-Martinez, I., Hermosilla, R., Engelsberg, A., Nehring, R., Dorken, B., and Rehm, A. (2005) EBAG9 adds a new layer of control on large dense-core vesicle exocytosis via interaction with Snapin Mol. Biol. Cell 16, 1245-1257
16. Chheda, M. G., Ashery, U., Thakur, P., Rettig, J., and Sheng, Z. H. (2001) Phosphorylation of Snapin by PKA modulates its interaction with the SNARE complex Nat. Cell Biol. 3, 331-338
17. Thakur, P., Stevens, D. R., Sheng, Z. H., and Rettig, J. (2004) Effects of PKA-mediated phosphorylation of Snapin on synaptic transmission in cultured hippocampal neurons J. Neurosci. 24, 6476-6481
18. Pan, P. Y., Tian, J. H., and Sheng, Z. H. (2009) Snapin facilitates the synchronization of synaptic vesicle fusion Neuron 61, 412-424
19. Starcevic, M. and Dell'Angelica, E. C. (2004) Identification of snapin and three novel proteins (BLOS1, BLOS2, and BLOS3/reduced pigmentation) as subunits of biogenesis of lysosome-related organelles complex-1 (BLOC-1) J. Biol. Chem. 279, 28393-28401
20. Morenilla-Palao, C., Planells-Cases, R., Garcia-Sanz, N., and Ferrer-Montiel, A. (2004) Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity J. Biol. Chem. 279, 25665-25672
21. Krapivinsky, G., Mochida, S., Krapivinsky, L., Cibulsky, S. M., and Clapham, D. E. (2006) The TRPM7 ion channel functions in cholinergic synaptic vesicles and affects transmitter release Neuron 52, 485-496
22. Buxton, P., Zhang, X. M., Walsh, B., Sriratana, A., Schenberg, I., Manickam, E., and Rowe, T. (2003) Identification and characterization of Snapin as a ubiquitously expressed SNARE-binding protein that interacts with SNAP23 in non-neuronal cells Biochem. J. 375, 433-440
23. Tian, J. H., Wu, Z. X., Unzicker, M., Lu, L., Cai, Q., Li, C., Schirra, C., Matti, U., Stevens, D., Deng, C., Rettig, J., and Sheng, Z. H. (2005) The role of Snapin in neurosecretion: Snapin knock-out mice exhibit impaired calcium-dependent exocytosis of large dense-core vesicles in chromaffin cells J. Neurosci. 25, 10546-10555
24. Valente, P., García-Sanz, N., Gomis, A., Fernández- Carvajal, A., Fernández-Ballester, G., Viana, F., Belmonte, C., and Ferrer-Montiel, A. (2008) Identification of molecular determinants of channel gating in the transient receptor potential box of vanilloid receptor I FASEB J. 222, 3298-3309
25. Miroux, B. and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels J. Mol. Biol. 260, 289-298
26. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182, 319-326
27. Alcaraz, L. A., del álamo, M., Barrera, F. N., Mateu, M. G., and Neira, J. L. (2007) Flexibility in HIV-1 assembly subunits: Solution structure of the monomeric C-terminal domain of the capsid protein Biophys. J. 93, 1264-1276
28. Blanes-Mira, C., Merino, J. M., Valera, E., Fernandez-Ballester, G., Gutierrez, L. M., Viniegra, S., Perez-Paya, E., and Ferrer-Montiel, A. (2004) Small peptides patterned after the N-terminus domain of SNAP25 inhibit SNARE complex assembly and regulated exocytosis J. Neurochem. 88, 124-135
29. Facchiano, A. and Ragone, R. (2003) Modification of Job's method for determining the stoichiometry of protein-protein complexes Anal. Biochem. 313, 170-172
30. Muro-Pastor, M. I., Barrera, F. N., Reyes, J. C., Florencio, F. J., and Neira, J. L. (2003) The inactivating factor of glutamine synthetase, IF7, is a "natively unfolded" protein Protein Sci. 12, 1443-1454
31. Woody, R. W. (1995) Circular dichroism Methods Enzymol. 246, 34-71
32. Encinar, J. A., Mallo, G. V., Mizyrycki, C., Giono, L., Gonzalez-Ros, J. M., Rico, M., Canepa, E., Moreno, S., Neira, J. L., and Iovanna, J. L. (2001) Human p8 is a HMG-I/Y-like protein with DNA binding activity enhanced by phosphorylation J. Biol. Chem. 276, 2742-2751
33. Echabe, I., Encinar, J. A., and Arrondo, J. L. R. (1997) Removal of spectral noise in the quantitation of protein structure through infrared band decomposition Biospectroscopy 3, 469-475
34. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 2, 661-665
35. Czypionka, A., de los Panos, O. R., Mateu, M. G., Barrera, F. N., Hurtado-Gomez, E., Gomez, J., Vidal, M., and Neira, J. L. (2007) The isolated C-terminal domain of Ring1B is a dimer made of stable, well-structured monomers Biochemistry 46, 12764-12776
36. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38, 16424-16431
37. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling Biophys. J. 78, 1606-1619
38. Laue, T. M. S., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer-aided Interpretation of Analytical Sedimentation Data For Proteins. In Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., Eds.) pp 90-125, The Royal Society of Chemistry, Cambridge, U.K.
39. Minton, A. P. (1994) Conservation of signal: A new algorithm for the elimination of the reference concentration as an independently variable parameter in the analysis of sedimentation equilibrium. In Modern analytical ultracentrifugation (Schuster, T. H. and Lave, T. H., Eds.) pp 81-92, Birkhaüser, Boston.
40. Kelly, S. M. and Price, N. C. (2000) The use of circular dichroism in the investigation of protein structure and function Curr. Protein Pept. Sci. 1, 349-384
41. Casares, S., Sadqi, M., Lopez-Mayorga, O., Conejero-Lara, F., and van Nuland, N. A. (2004) Detection and characterization of partially unfolded oligomers of the SH3 domain of α-spectrin Biophys. J. 86, 2403-2413
42. Atkins, P. W. and De Paula, J. (2006) Physical Chemistry, Oxford University Press, Oxford, U.K.
43. Cooper, T. M. and Woody, R. W. (1990) The effect of conformation on the CD of interacting helices: A theoretical study of tropomyosin Biopolymers 30, 657-676
44. Whitmore, L. and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32, W668-W673
45. Whitmore, L. and Wallace, B. A. (2008) Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases Biopolymers 89, 392-400
46. Wüthrich, K. (1986) NMR of proteins and nucleic acids, John Wiley & Sons, Inc., New York.
47. Fasshauer, D., Antonin, W., Margittai, M., Pabst, S., and Jahn, R. (1999) Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties J. Biol. Chem. 274, 15440-15446
48. Tompa, P. (2002) Intrinsically unstructured proteins Trends Biochem. Sci. 27, 527-533
49. Dyson, H. J. and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6, 197-208
50. Pace, C. N. and Scholtz, J. M. (1998) A helix propensity scale based on experimental studies of peptides and proteins Biophys. J. 75, 422-427