The main-chain dynamics of the dynamin pleckstrin homology (PH) domain in solution: Analysis of 15N relaxation with monomer/dimer equilibration

Journal of Molecular Biology

Volumn 266, Issue 1, 1997, Pages 173-194

  Fushman, David ^a   Cahill, Sean ^a   Cowburn, David ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Dynamin; Monomer dimer equilibration; NMR relaxation; Pleckstrin homology domain; Protein dynamics

Indexed keywords

DIMER; DYNAMIN; MONOMER; NITROGEN 15; PLECKSTRIN;

ARTICLE; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY;

EID: 0031566963     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0771     Document Type: Article

References (66)

1. 9k. J. Am. Chem. Soc. 115:1993;9832-9833.
2. 15N in macromolecules. Chem. Phys. Letters. 175:1990;477-482.
3. 15N in macromolecules. Chem. Phys. Letters. 187:1991;317-324.
4. Brünger A. T. X-PLOR. Version 3.1. A System for X-ray Crystallography and NMR. 1992.
5. Brüschweiler R., Wright P. NMR order parameters of biomolecules: a new analytical representation and application to the Gaussian axial fluctuation model. J. Am. Chem. Soc. 116:1994;8426-8427.
6. Carr H. Y., Purcel E. M. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys. Rev. 94:1954;630-632.
7. 15N nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112:1990;4989-4991.
8. DebBurman S. K., Ptasienski J., Boetticher E., Lomansney J. W., Benovic J. L., Hosey M. M. Lipid-mediated regulation of G protein-coupled receptor kinases 2 and 3. J. Biol. Chem. 270:1995;5742-5747.
9. Dellwo M. J., Wand A. J. Model-independent and model-dependent analysis of the global and internal dynamics of cyclosporin A. J. Am. Chem. Soc. 111:1989;4571-4578.
10. Downing A. K., Driscoll P. C., Gout I., Salim K., Zvelebil M. J., Waterfield M. D. Three-dimensional solution structure of the pleckstrin homology domain from dynamin. Curr. Biol. 4:1994;884-891.
11. Eccles C., Güntert P., Billeter M., Wüthrich K. Efficient analysis of protein 2D NMR spectra using the software package EASY. J. Biomol. NMR. 1:1991;111-130.
12. Ferguson K. M., Lemmon M. A., Schlessinger J., Sigler P. B. Crystal structure at 2.2 Å of the pleckstrin homology domain from human dynamic. Cell. 79:1994;199-209.
13. Ferguson K. M., Lemmon M. A., Schlessinger J., Sigler P. B. Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell. 83:1995;1037-1045.
14. Fushman D., Weisemann R., Thüring H., Rüterjans H. Determination of the backbone dynamics of ribonuclease T1 and its 2′GMP complex using molecular dynamics simulations and NMR relaxation data. J. Biomol. NMR. 4:1994a;61-78.
15. Fushman D., Ohlenschläger O., Rüterjans H. Backbone dynamics of ribonuclease T1 and its complex with 2′GMP studied by two-dimensional heteronuclear NMR spectroscopy. J. Biomol. Struct. Dynam. 11:1994b;1377-1402.
16. Fushman D., Cahill S., Lemmon M., Schlessinger J., Cowburn D. Solution structure of the pleckstrin homology domain of dynamin by heteronuclear NMR spectroscopy. Proc. Natl Acad. Sci. USA. 92:1995;816-820.
17. Garcia de la Torre J., Bloomfield V. A. Hydrodynamic properties of complex, rigid, biological macromolecules: theory and applications. Quart. Rev. Biophys. 14:1981;81-139.
18. Gibson T. J., Hyvönen M., Musacchio A., Saraste M., Birney E. PH domain: the first anniversary. Trends Biochem. Sci. 19:1994;349-353.
19. Goldman M. Interference effects in the relaxation of a part of unlike spin-1/2 nuclei. J. Magn. Reson. 60:1984;437-452.
20. Grigliatti T. A., Hall L., Rosenbluth R., Suzuki D. T. Temperature-sensitive mutations in Drosophila melanogaster. XIV. A selection of immobile adults. Mol. Genet. 120:1973;107-114.
21. 2O in protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc. 115:1993;12593-12594.
22. Harlan J. E., Hajduk P. J., Yoon H. S., Fesik S. W. Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature. 371:1994;168-170.
23. Haslam R. L., Kolde H. B., Hemmings B. A. Pleckstrin domain homology. Nature. 363:1993;309-310.
24. Herskovits J. S., Shpetner H. S., Burgess C. C., Vallee R. B. Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122:1993;565-578.
25. Hinshaw J. E., Schmid S. L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature. 374:1995;190-192.
26. Hyvönen M., Macias M. J., Nilges M., Oshkinat H., Saraste M., Wilmanns M. Structure of the binding site for inositol phosphates in a PH domain. EMBO J. 14:1995;4676-4685.
27. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry. 28:1989;8972-8979.
28. 2values in proteins. J. Magn. Reson. 97:1992;359-375.
29. Koenig S. H. Brownian motion of an ellipsoid. Correction to Perrin's results. Biopolymers. 14:1975;2421-2423.
30. Konishi H., Kuroda S., Kikkawa U. The pleckstrin homology domain of RAC protein kinase associates with the regulatory domain of protein kinase C zeta. Biochem. Biophys. Res. Commun. 205:1994;1770-1775.
31. 9kstudied by two-dimensional proton detected NMR spectroscopy. Biochemistry. 31:1992;4856-4866.
32. Lemmon M. A., Ladbury J. E. Thermodynamic studies of tyrosyl-phosphopeptide binding to the SH2 domain of p56lck. Biochemistry. 33:1994;5070-5076.
33. Lemmon M. A., Ferguson K. M., O'Brien R., Sigler P. B., Schlessinger J. Specific and high-affinity binding of inositol phosphates to an isolates pleckstrin homology domain. Proc. Natl Acad. Sci. USA. 92:1995;10472-10476.
34. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. J. Am. Chem. Soc. 104:1982;4546-4559.
35. Macias M. J., Musacchio A., Postingl H., Nilges H., Saraste M., Oschkinat H. Structure of the PH domain from β-spectrin. Nature. 369:1994;675-677.
36. Makhatadze G. I., Medvedkin V. N., Privalov P. L. Partial molar volumes of polypeptides and their constituent groups in aqueous solution over a broad temperature range. Biopolymers. 30:1990;1001-1010.
37. Mandel A., Akke M., Palmer A. Backbone dynamics of E. coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246:1995;144-163.
38. Marshall A. G. Calculation of NMR relaxation times for quadrupolar nuclei in the presence of chemical exchange. J. Chem. Phys. 52:1970;2527-2534.
39. Mayer B. J., Ren R., Clark K., Baltimore D. A putative modular domain present in diverse signaling molecules. Cell. 73:1993;629-630.
40. Meiboom S., Gill D. Modified spin-echo method for measuring nuclear spin relaxation times. Rev. Sci. Instrum. 29:1958;688-691.
41. Musacchio A., Gibson T., Rice P., Thompson J., Saraste M. The PH domain: a common piece in the structural patchwork of signaling proteins (Review). Trends Biochem. Sci. 18:1993;343-348.
42. 15N NMR spectroscopy. Eur. J. Biochem. 219:1994;887-896.
43. Palmer A. G., III, Cavanagh J., Wright P. E., Rance M. Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J. Magn. Reson. 93:1991;151-170.
44. Palmer A. G., III, Skelton N. J., Chazin W. J., Wright P. E., Rance M. Suppression of the effects of cross-correlation between dipolar and anisotropic chemical shift relaxation mechanisms in the measurement of spin-spin relaxation rates. Mol. Phys. 75:1992;699-711.
45. Piotto M., Saudek V., Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:1992;661-665.
46. βψsubunits and lipid. J. Biol. Chem. 270:1995;11707-11710.
47. Press W. H., Flannery B. P., Teukolsky S. A., Vetterling W. T. Numerical Recipes. 1989;Cambridge University Press, Cambridge.
48. Quennouille M. H. Notes on bias in estimation. Biometrica. 43:1956;353-360.
49. Robinson M. S. The role of clathrin, adaptors and dynamin in endocytosis (Review). Curr. Opin. Cell Biol. 6:1994;538-544.
50. Rykaert J. P., Cicotti G., Berendsen H. J. C. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:1977;327.
51. Shaw G. Identification of novel pleckstrin homology (PH) domains provides a hypothesis for PH domain function. Biochem. Biophys. Res. Commun. 195:1993;1145-1151.
52. 15N spin relaxation measurements. J. Magn. Reson. B102:1993;253-264.
53. 1H detection. J. Magn. Reson. 73:1987;375-379.
54. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson. 102A:1993;241-245.
55. Takei K., McPherson P. S., Schmid S. L., De Camili P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature. 374:1995;186-190.
56. Timm D., Salim K., Gout I., Guruprasad L., Waterfield M., Blundell T. Crystal structure of the pleckstrin homology domain from dynamin. Nature Struct. Biol. 1:1994;782-788.
57. 15N NMR relaxation. J. Am. Chem. Soc. 117:1995;12562-12566.
58. Touhara K., Koch W. J., Hawes B., Lefkowitz R. Mutational analysis of the pleckstrin homology domain of the beta-adrenergic receptor kinase-differential effects on G(β-δ) and phosphatidylinositol 4,5-bisphosphate binding. J. Biol. Chem. 270:1995;17000-17005.
59. Van der Bliek A. M., Redelmeier T. E., Damke H., Tisdale E. J., Meyerowitz E. M., Schmid S. L. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122:1993;553-563.
60. Wang D. S., Shaw R., Winkelman J. C., Shaw G. Binding of PH domains of β-adrenergic receptor kinase and β-spectrin to WD40/β-transducin repeat containing regions of the β-subunit of trimeric G-proteins. Biochem. Biophys. Res. Commun. 203:1994;29-35.
61. Woessner D. E. Nuclear spin relaxation in ellipsoids undergoing rotational Brownian motion. J. Chem. Phys. 37:1962;647-654.
62. Wu D., Chen A., Johnson C. S. An improved diffusion-ordered spectroscopy experiment incorporating bipolar gradient pulses. J. Magn. Reson. A115:1995;260-264.
63. Yao L., Kawakami Y., Kawakami T. The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C. Proc. Natl Acad. Sci. USA. 91:1994;9175-9179.
64. Yoon H. S., Hajduk P. J., Petros A. M., Olejniczak E. T., Meadows R. P., Fesik S. W. Solution structure of a pleckstrin-homology domain. Nature. 369:1994;672-675.
65. Zhang P., Talluri S., Deng H., Branton D., Wagner G. Solution structure of the pleckstrin homology domain of Drosophila beta-spectrin. Structure. 3:1995;1185-1195.
66. Zheng J., Cahill S. M., Lemmon M. A., Fushman D., Schlessinger J., Cowburn D. Identification of the binding site for acidic phospholipids on the PH domain of dynamin: implications for stimulation of GTPase activity. J. Mol. Biol. 255:1996;14-21.