Triphosphate induced dimerization of human guanylate binding protein 1 involves association of the C-terminal helices: A joint double electron-electron resonance and FRET Study

Biochemistry

Volumn 53, Issue 28, 2014, Pages 4590-4600

  Vöpel, Tobias ^a   Hengstenberg, Carola S ^a   Peulen, Thomas Otavio ^b   Ajaj, Yathrib ^b   Seidel, Claus A M ^b   Herrmann, Christian ^a   Klare, Johann P ^c  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERS; ELECTRON RESONANCE; ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; HYDROLYSIS; MAGNETIC RESONANCE; MOLECULAR DYNAMICS; PROTEINS;

CONFORMATIONAL CHANGE; DOUBLE ELECTRON-ELECTRON RESONANCE; MEMBRANE LOCALIZATION; MODEL-FREE ANALYSIS; MOLECULAR DYNAMICS SIMULATIONS; RESONANCE ENERGY TRANSFER; STRUCTURAL INVESTIGATION; TIME-RESOLVED FLUORESCENCE SPECTROSCOPY;

DIMERIZATION;

DIMER; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN 1; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; NUCLEOSIDE TRIPHOSPHATE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DIMERIZATION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIMULATION; SITE DIRECTED MUTAGENESIS; SPIN LABELING;

FLUORESCENCE RESONANCE ENERGY TRANSFER; GTP-BINDING PROTEINS; HUMANS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84904662230     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500524u     Document Type: Article

References (65)

1. Praefcke, G. J. K. and McMahon, H. T. (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell. Biol. 5, 133-147
2. Cheng, Y.-S., Colonno, R. J., and Yin, F. H. (1983) Interferon Induction of Fibroblast Proteins with Guanylate Binding Activity J. Biol. Chem. 258, 7746-7750
3. Anderson, S. L., Carton, J. M., Lou, J., Xing, L., and Rubin, B. Y. (1999) Interferon-Induced Guanylate Binding Protein-1 (GBP-1) Mediates an Antiviral Effect against Vesicular Stomatitis Virus and Encephalomyocarditis Virus Virology 256, 8-14
4. Itsui, Y., Sakamoto, N., Kanikuma, S., Nakagawa, M., Sekine-Osajima, Y., Tasaka-Fujita, M., Nishimura-Sakurai, Y., Suda, G., Karakama, Y., Mishima, K., Yamamoto, M., Watanabe, T., Ueyama, M., Funaoka, Y., Sazuma, S., and Watanabe, M. (2009) Antiviral effects of the interferon-induced protein guanylate binding protein 1 and its interaction with the hepatitis C virus NS5B protein Hepatology 50, 1727-1737
5. Naschberger, E., Lubeseder-Martellato, C., Meyer, N., Gessner, R., Kremmer, E., Gessner, A., and Stürzl, M. (2006) Human Guanylate Binding Protein-1 Is a Secreted GTPase Present in Increased Concentrations in the Cerebrospinal Fluid of Patients with Bacterial Meningitis Am. J. Pathol. 169, 1088-1099
6. Tietzel, I., El-Haibi, C., and Carabeo, R. A. (2009) Human Guanylate Binding Proteins Potentiate the Anti-Chlamydia Effects of Interferon-γ PLoS One 4, e6499
7. Zhu, Z., Shi, Z., Yan, W., Wei, J., Shao, D., Deng, X., Wang, S., Li, B., Tong, G., and Ma, Z. (2013) Nonstructural Protein 1 of Influenza A Virus Interacts with Human Guanylate-Binding Protein 1 to Antagonize Antiviral Activity PLoS One 8, e55920
8. Selleck, E., Fentress, Sarah J., Beatty, W. L., Degrandi, D., Pfeffer, K., Virgin, H. W., MacMicking, J. D., and Sibley, L. D. (2013) Guanylate-binding Protein 1 (Gbp1) Contributes to Cell-autonomous Immunity against Toxoplasma gondii PLoS Pathogens 9, e1003320
9. Guenzi, E., Töpolt, K., Lubeseder-Martellato, C., Naschberger, E., Benilli, R., Albini, A., and Stürzl, M. (2003) The guanylate binding protein-1 GTPase controls the invasive and angiogenic capability of endothelial cells through inhibition of MMP-1 expression EMBO J. 22, 3772-3782
10. Weinländer, K., Naschberger, E., Lehmann, M. H., Tripal, P., Paster, W., Stockinger, H., Hohenadl, C., and Stürzl, M. (2008) Guanylate binding protein-1 inhibits spreading and migration of endothelial cells through induction of integrin α4 expression FASEB J. 22, 4168-4178
11. Naschberger, E., Croner, R. S., Merkel, S., Dimmler, A., Tripal, P., Amann, K. U., Kremmer, E., Brueckl, W. M., Papadopoulos, T., Hohenadl, C., Hohenberger, W., and Stürzl, M. (2008) Angiostatic immune reaction in colorectal carcinoma: Impact on survival and perspectives for antiangiogenic therapy Int. J. Cancer 123, 2120-2129
12. Li, M., Mukasa, A., del-Mar Inda, M., Zhang, J., Chin, L., Cavenee, W., and Furnari, F. (2011) Guanylate binding protein 1 is a novel effector of EGFR-driven invasion in glioblastoma J. Exp. Med. 208, 2657-2673
13. Yu, C. J., Chang, K. P., Chang, Y. J., Hsu, C. W., Liang, Y., Yu, J. S., Chi, L. M., Chang, Y. S., and Wu, C. C. (2011) Identification of Guanylate-Binding Protein 1 as a Potential Oral Cancer Marker Involved in Cell Invasion Using Omics-Based Analysis J. Proteome Res. 10, 3778-3788
14. Lipnik, K., Naschberger, E., Gonin-Laurent, N., Kodajova, P., Petznek, H., Rungaldier, S., Asigiano, S., Ferrini, S., Stürzl, M., and Hohenadl, C. (2010) Interferon γ-Induced Human Guanylate Binding Protein 1 Inhibits Mammary Tumor Growth in Mice Mol. Med. 16, 177-187
15. Desarnaud, F., Geck, P., Parkin, C., Carpinito, G., and Makarovskiy, A. N. (2011) Gene expression profiling of the androgen independent prostate cancer cells demonstrates complex mechanisms mediating resistance to docetaxel Cancer Biol. Ther. 11, 204-212
16. Duan, Z., Foster, R., Brakora, K. A., Yusuf, R. Z., and Seiden, M. V. (2006) GBP1 overexpression is associated with a paclitaxel resistance phenotype Cancer Chemother. Pharmacol. 57, 25-33
17. Prakash, B., Praefcke, G. J. K., Renault, L., Wittinghofer, A., and Herrmann, C. (2000) Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins Nature 403, 567-571
18. Cheng, Y.-S., Becker-Manley, M. F., Chow, T. P., and Horan, D. C. J. (1985) Affinity purification of an interferon-induced human guanylate-binding protein and its characterization Biol. Chem. 260, 15834-15839
19. Praefcke, G. J. K., Geyer, M., Schwemmle, M., Kalbitzer, H. R., and Herrmann, C. (1999) Nucleotide-binding characteristics of human guanylate-binding protein 1 (hGBP1) and identification of the third GTP-binding motif J. Mol. Biol. 292, 321-332
20. Praefcke, G. J. K., Kloep, S., Benscheid, U., Lilie, H., Prakash, B., and Herrmann, C. (2004) Identification of Residues in the Human Guanylate-binding Protein 1 Critical for Nucleotide Binding and Cooperative GTP Hydrolysis J. Mol. Biol. 344, 257-269
21. Cheng, Y.-S., Patterson, C. E., and Staeheli, P. (1991) Interferon-induced guanylate-binding proteins lack an N(T)KXD consensus motif and bind GMP in addition to GDP and GTP Mol. Cell. Biol. 11, 4717-4725
22. Kunzelmann, S., Praefcke, G. J. K., and Herrmann, C. (2006) Transient Kinetic Investigation of GTP Hydrolysis Catalyzed by Interferon-g-induced hGBP1 (Human Guanylate Binding Protein 1) J. Biol. Chem. 281, 28627-28635
23. Ghosh, A., Praefcke, G. J. K., Renault, L., Wittinghofer, A., and Herrmann, C. (2006) How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP Nature 440, 101-104
24. Prakash, B., Renault, L., Praefcke, G. J. K., Herrmann, C., and Wittinghofer, A. (2000) Triphosphate structure of guanylate-binding protein 1 and implications for nucleotide binding and GTPase mechanism EMBO J. 19, 4555-4564
25. Kunzelmann, S., Praefcke, G. J. K., and Herrmann, C. (2005) Nucleotide Binding and Self-Stimulated GTPase Activity of Human Guanylate-Binding Protein 1 (hGBP1) Methods Enzymol. 404, 512-527
26. Gasper, R., Meyer, S., Gotthardt, K., Sirajuddin, M., and Wittinghofer, A. (2009) It takes two to tango: regulation of G proteins by dimerization Nat. Rev. Mol. Cell. Biol. 10, 423-429
27. Vöpel, T., Syguda, A., Britzen-Laurent, N., Kunzelmann, S., Lüdemann, M. B., Dovengerds, C., Stürzl, M., and Herrmann, C. (2010) Mechanism of GTPase activity induced self-assembly of human guanylate binding protein 1 J. Mol. Biol. 400, 63-70
28. Vöpel, T., Kunzelmann, S., and Herrmann, C. (2009) Nucleotide dependent cysteine reactivity of hGBP1 uncovers a domain movement during GTP hydrolysis FEBS Lett. 583, 1923-1927
29. Syguda, A., Bauer, M., Benscheid, U., Ostler, N., Naschberger, E., Ince, S., Stürzl, M., and Herrmann, C. (2012) Tetramerisation of human guanylate binding protein 1 is mediated by coiled coil formation of the C-terminal α-helices FEBS J. 279, 2544-2554
30. Martin, R. E., Pannier, M., Diederich, F., Gramlich, V., Hubrich, M., and Spiess, H. W. (1998) Determination of End-to-End Distances in a Series of TEMPO Diradicals of up to 2.8 nm Length with a New Four-Pulse Double Electron Electron Resonance Experiment Angew. Chem. Int. Ed. 37, 2833-2837
31. Pannier, M., Veit, S., Godt, A., Jeschke, G., and Spiess, H. W. (2000) Dead-Time Free Measurement of Dipole-Dipole Interactions between Electron Spins J. Magn. Reson. 142, 331-340
32. Klare, J. P. and Steinhoff, H.-J. (2009) Spin Labeling EPR Photosynth. Res. 102, 377-390
33. Meyer, S., Böhme, S., Krüger, A., Steinhoff, H.-J., Klare, J. P., and Wittinghofer, A. (2009) Kissing G domains of MnmE monitored by X-ray crystallography and pulse EPR Spectroscopy PLoS Biol. 7, e1000212
34. Böhme, S., Meyer, S., Krüger, A., Steinhoff, H.-J., Wittinghofer, A., and Klare, J. P. (2010) Stabilization of G domain conformations in the tRNA modifying MnmE/GidA complex observed with DEER spectroscopy J. Biol. Chem. 285, 16991-17000
35. Kravets, E., Degrandi, D., Weidtkamp-Peters, S., Konermann, C., Felekyan, S., Darkazanli, J. M., Praefcke, G. J., Seidel, C. A., Schmitt, L., Smits, S. H., and Pfeffer, K. J. (2012) The GTPase activity of murine guanylate-binding protein 2 (mGBP2) controls the intracellular localization and recruitment to the parasitophorous vacuole of Toxoplasma gondii J. Biol. Chem. 287, 27452-27466
36. Rothwell, P. J., Berger, S., Kensch, O., Felekyan, S., Antonik, M., Wöhrl, B. M., Restle, T., Goody, R. S., and Seidel, C. A. M. (2003) Multiparameter single-molecule fluorescence spectroscopy reveals heterogeneity of HIV-1 reverse transcriptase:primer/template complexes Proc. Natl. Acad. Sci. U.S.A. 100, 1655-1660
37. Sindbert, S., Kalinin, S., Nguyen, H., Kienzler, A., Bannwarth, W., Appel, B., Müller, S., and Seidel, C. A. M. (2011) Accurate Distance Determination of Nucleic Acids via Förster Resonance Energy Transfer: Implications of Dye Linker Length and Rigidity J. Am. Chem. Soc. 133, 2463-2480
38. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182, 319-326
39. Altenbach, C., https://sites.google.com/site/altenbach/labview-programs/ epr-programs/short-distances.
40. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J. E., Timmel, C. R., Hilger, D., and Jung, H. (2006) DeerAnalysis2006-a comprehensive software package for analyzing pulsed ELDOR data Appl. Magn. Reson. 30, 473-498
41. Tikhonov, A. N. and Arsenin, V. Y. (1977) Solutions of Ill-Posed Problems, Wiley, New York.
42. Polyhach, Y., Bordignon, E., and Jeschke, G. (2011) Rotamer libraries of spin labelled cysteines for protein studies Phys. Chem. Chem. Phys. 13, 2356-2366
43. OConnor, D. V. and Phillips, D. (1984) Time-Correlated Single Photon Counting, Academic Press, New York.
44. Muschielok, A., Andrecka, J., Jawhari, A., Bruckner, F., Cramer, P., and Michaelis, J. (2008) A nano-positioning system for macromolecular structural analysis Nature Methods 5, 965-971
45. Kalinin, S., Peulen, T., Sindbert, S., Rothwell, P. J., Berger, S., Restle, T., Goody, R. S., Gohlke, H., and Seidel, C. A. M. (2012) A toolkit and benchmark study for FRET-restrained high-precision structural modeling Nat. Methods 9, 1218-1225
46. Kalinin, S. and Johansson, L. B. (2004) Energy Migration and Transfer Rates Are Invariant to Modeling the Fluorescence Relaxation by Discrete and Continuous Distributions of Lifetimes J. Phys. Chem. B 108, 3092-3097
47. Livesey, A. K. and Skilling, J. (1985) Maximum Entropy Theory Acta Crystallogr., Sect. A 41, 113-122
48. Brochon, J. C. (1994) Maximum entropy method of data analysis in time-resolved spectroscopy Methods Enzymol. 240, 262-311
49. Metropolis, N., Rosenbluth, A., Rosenbluth, M., Teller, A., and Teller, E. (1953) Equation of State Calculations by Fast Computing Machines J. Chem. Phys. 21, 1087-1092 S.
50. Hastings, W. K. (1970) Monte Carlo sampling methods using Markov chains and their applications Biometrika 57, 97-109 S.
51. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3 rd ed., Springer, New York.
52. Gregory, P. (2005) Baysian Logical Data Analysis for the Physical Sciences, Cambridge University Press, New York.
53. Krieger, E., Koraimann, G., and Vriend, G. (2002) Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field Proteins 47, 393-402
54. Konagurthu, A. S., Whisstock, J. C., Stuckey, P. J., and Lesk, A. M. (2006) MUSTANG: A multiple structural alignment algorithm Proteins 64, 559-574
55. Wehner, M., Kunzelmann, S., and Herrmann, C. (2012) The guanine cap of hGBP1 is responsible for dimerization and self-activation of GTP hydrolysis FEBS J. 279, 203-210
56. Dale, R. E., Eisinger, J., and Blumberg, W. E. (1979) Theorientational freedom of molecular probes orientation factor in intramolecular energy transfer Biophys. J. 26, 161-193
57. Abdullah, N., Balakumari, M., and Sau, A. K. (2010) Dimerization and Its Role in GMP Formation by Human Guanylate Binding Proteins Biophys. J. 99, 2235-2244
58. Nantais, D. E., Schwemmle, M., Stickney, J. T., Vestal, D. J., and Buss, J. E. (1996) Prenylation of an interferon-gamma-induced GTP-binding protein: the human guanylate binding protein, huGBP1 J. Leukoc. Biol. 60, 423-431
59. Britzen-Laurent, N., Bauer, M., Berton, V., Fischer, N., Syguda, A., Reipschläger, S., Naschberger, E., Herrmann, C., and Stürzl, M. (2010) Intracellular Trafficking of Guanylate-Binding Proteins Is Regulated by Heterodimerization in a Hierarchical Manner PLoS One 5, e14246
60. Hancock, J. F., Paterson, H., and Marshall, C. J. (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane Cell 63, 133-139
61. Wright, L. P. and Philips, M. R. (2006) CAAX modification and membrane targeting of Ras J. Lipid Res. 47, 883-891
62. Low, H. H. and Löwe, J. (2006) A bacterial dynamin-like protein Nature 444, 766-769
63. Ford, M. G. J., Jenni, S., and Nunnari, J. (2011) The crystal structure of dynamin Nature 477, 561-566
64. Chappie, J. S., Mears, J. A., Fang, S., Leonard, M., Schmid, S. L., Milligan, R. A., Hinshaw, J. E., and Dyda, F. (2011) A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke Cell 147, 209-222
65. Gao, S., von der Malsburg, A., Dick, A., Faelber, K., Schröder, G. F., Haller, O., Kochs, G., and Daumke, O. (2011) Structure of myxovirus resistance protein A reveals intra- and intermolecular domain interactions required for the antiviral function Immunity 35, 514-525