Guanylate binding proteins directly attack toxoplasma gondii via supramolecular complexes

eLife

Volumn 5, Issue JANUARY2016, 2016, Pages

  Kravets, Elisabeth ^a   Degrandi, Daniel ^a   Ma, Qijun ^a   Peulen, Thomas Otavio ^a   Klümpers, Verena ^a,b   Felekyan, Suren ^a   Kühnemuth, Ralf ^a   Weidtkamp Peters, Stefanie ^a   Seidel, Claus Am ^a   Pfeffer, Klaus ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN 1; GUANINE NUCLEOTIDE BINDING PROTEIN 2; GUANINE NUCLEOTIDE BINDING PROTEIN 3; GUANINE NUCLEOTIDE BINDING PROTEIN 5; GUANINE NUCLEOTIDE BINDING PROTEIN 6; GUANOSINE TRIPHOSPHATE; UNCLASSIFIED DRUG; GBP2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION CONSTANT; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNITY; IMMUNOFLUORESCENCE TEST; ISOPRENYLATION; MOLECULAR INTERACTION; MONTE CARLO METHOD; MOUSE; MULTIPARAMETER FLUORESCENCE IMAGE SPECTROSCOPY; NONHUMAN; OLIGOMERIZATION; PARASITE CONTROL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MULTIMERIZATION; SUPRAMOLECULAR CHEMISTRY; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRANSIENT TRANSFECTION; ANIMAL; CELL MEMBRANE; CELL SURVIVAL; CELL VACUOLE; DRUG EFFECT; FLUORESCENCE IMAGING; IMMUNOLOGY; METABOLISM; MICROSCOPY; PARASITOLOGY; PHYSIOLOGY; SPECTROSCOPY; TOXOPLASMA;

ANIMALS; CELL MEMBRANE; CELL SURVIVAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GTP-BINDING PROTEINS; MICE; MICROSCOPY; OPTICAL IMAGING; PROTEIN MULTIMERIZATION; SPECTROMETRY, X-RAY EMISSION; TOXOPLASMA; VACUOLES;

EID: 84961951364     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.11479.001     Document Type: Article

References (58)

1. Becker W. 2005. Advanced Time-Correlated Single Photon Counting Techniques. Berlin, Heidelberg: Springer Berlin Heidelberg.
2. Britzen-Laurent N, Bauer M, Berton V, Fischer N, Syguda A, Reipschlager S, Naschberger E, Herrmann C, Sturzl M. 2010. Intracellular trafficking of guanylate-binding proteins is regulated by heterodimerization in a hierarchical manner. PLoS ONE 5:e14246. doi: 10.1371/journal.pone.0014246
3. Choi J, Park S, Biering SB, Selleck E, Liu CY, Zhang X, Fujita N, Saitoh T, Akira S, Yoshimori T, Sibley LD, Hwang S, Virgin HW. 2014. The parasitophorous vacuole membrane of toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity 40:924-935. doi: 10.1016/j.immuni.2014.05.006
4. Decker T, Stockinger S, Karaghiosoff M, Muller M, Kovarik P. 2002. IFNs and STATs in innate immunity to microorganisms. Journal of Clinical Investigation 109:1271-1277. doi: 10.1172/JCI0215770
5. Degrandi D, Konermann C, Beuter-Gunia C, Kresse A, Wurthner J, Kurig S, Beer S, Pfeffer K. 2007. Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. The Journal of Immunology 179:7729-7740. doi: 10.4049/jimmunol.179.11.7729
6. Degrandi D, Kravets E, Konermann C, Beuter-Gunia C, Klumpers V, Lahme S, Wischmann E, Mausberg AK, Beer-Hammer S, Pfeffer K. 2013. Murine guanylate binding protein 2 (mGBP2) controls toxoplasma gondii replication. Proceedings of the National Academy of Sciences of the United States of America 110:294-299. doi: 10.1073/pnas.1205635110
7. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G, Baker NA. 2007. PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Research 35:W522-W525. doi: 10.1093/nar/gkm276
8. Evers TH, van Dongen EMWM, Faesen AC, Meijer EW, Merkx M. 2006. Quantitative understanding of the energy transfer between fluorescent proteins connected via flexible peptide linkers. Biochemistry 45:13183­-13192. doi: 10.1021/bi061288t
9. Ewald SE, Chavarria-Smith J, Boothroyd JC. 2014. NLRP1 is an inflammasome sensor for toxoplasma gondii. Infection and Immunity 82:460-468. doi: 10.1128/IAI.01170-13
10. Faelber K, Posor Y, Gao S, Held M, Roske Y, Schulze D, Haucke V, Noee F, Daumke O. 2011. Crystal structure of nucleotide-free dynamin. Nature 477:556-560. doi: 10.1038/nature10369
11. Fiser A, Sali A. 2003. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol 374:461-491. doi: 10.1016/S0076-6879(03)74020-8
12. Forster T. 1949. Experimentelle und theoretische untersuchung des zwischenmolekularen ubergangs von elektronenanregungsenergie. Zeitschrift Fur Naturforschung Section a-a Journal of Physical Sciences 4:321-­327.
13. Gazzinelli RT, Mendonca-Neto R, Lilue J, Howard J, Sher A. 2014. Innate resistance against toxoplasma gondii: an evolutionary tale of mice, cats, and men. Cell Host Microbe 15:132-138. doi: 10.1016/j.chom.2014.01.004
14. Ghosh A, Praefcke GJK, Renault L, Wittinghofer A, Herrmann C. 2006. How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature 440:101-104. doi: 10.1038/nature04510
15. Giepmans BN, Adams SR, Ellisman MH, Tsien RY. 2006. The fluorescent toolbox for assessing protein location and function. Science 312:217-224. doi: 10.1126/science.1124618
16. Gorfu G, Cirelli KM, Melo MB, Mayer-Barber K, Crown D, Koller BH, Masters S, Sher A, Leppla SH, Moayeri M, Saeij JPJ, Grigg ME. 2014. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to toxoplasma gondii. mBio 5:e01117-01113. doi: 10.1128/mBio.01117-13
17. Haldar AK, Saka HA, Piro AS, Dunn JD, Henry SC, Taylor GA, Frickel EM, Valdivia RH, Coers J. 2013. IRG and GBP host resistance factors target aberrant, "non-self" vacuoles characterized by the missing of “self” IRGM proteins. PLoS Pathogens 9:e1003414-e1003414. doi: 10.1371/journal.ppat.1003414
18. Haldar AK, Piro AS, Pilla DM, Yamamoto M, Coers J. 2014. The E2-like conjugation enzyme Atg3 promotes binding of IRG and gbp proteins to chlamydia- and toxoplasma-containing vacuoles and host resistance. PLoS ONE 9:e86684. doi: 10.1371/journal.pone.0086684
19. Haldar AK, Foltz C, Finethy R, Piro AS, Feeley EM, Pilla-Moffett DM, Komatsu M, Frickel E-M, Coers J. 2015. Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proceedings of the National Academy of Sciences of the United States of America 112:E5628-E5637. doi: 10.1073/pnas.1515966112
20. Kalinin S, Peulen T, Sindbert S, Rothwell PJ, Berger S, Restle T, Goody RS, Gohlke H, Seidel CAM. 2012. A toolkit and benchmark study for FRET-restrained high-precision structural modeling. Nature Methods 9:1218­1225. doi: 10.1038/nmeth.2222
21. Kask P, Palo K, Fay N, Brand L, Mets Ulo, Ullmann D, Jungmann J, Pschorr J, Gall K. 2000. Two-dimensional fluorescence intensity distribution analysis: theory and applications. Biophysical Journal 78:1703-1713. doi: 101016/S0006-3495(00)76722-1
22. Kollner M, Wolfrum J. 1992. How many photons are necessary for fluorescence-lifetime measurements? Chemical Physics Letters 200:199-204. doi: 10.1016/0009-2614(92)87068-Z
23. Kravets E, Degrandi D, Weidtkamp-Peters S, Ries B, Konermann C, Felekyan S, Dargazanli JM, Praefcke GJK, Seidel CAM, Schmitt L, Smits SHJ, Pfeffer K. 2012. The GTPase activity of murine guanylate-binding protein 2 (mGBP2) controls the intracellular localization and recruitment to the parasitophorous vacuole of toxoplasma gondii. Journal of Biological Chemistry 287:27452-27466. doi: 10.1074/jbc.M112.379636
24. Kresse A, Konermann C, Degrandi D, Beuter-Gunia C, Wuerthner J, Pfeffer K, Beer S. 2008. Analyses of murine GBP homology clusters based on in silico, in vitro and in vivo studies. BMC Genomics 9:158. doi: 10.1186/1471-2164-9-158
25. Kudryavtsev V, Felekyan S, Wozniak AK, Ktonig M, Sandhagen C, Kuhnemuth R, Seidel CAM, Oesterhelt F. 2006. Monitoring dynamic systems with multiparameter fluorescence imaging. Analytical and Bioanalytical Chemistry 387:71-82. doi: 10.1007/s00216-006-0917-0
26. Lakowicz JR. 2006. Principles of Fluorescence Spectroscopy. Boston, MA: Springer US. doi: 10.1007/978-0-387­46312-4
27. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJ, Yap GS. 2006. Vacuolar and plasma membrane stripping and autophagic elimination of toxoplasma gondii in primed effector macrophages. Journal of Experimental Medicine 203:2063-2071. doi: 10.1084/jem.20061318
28. MacMicking JD. 2012. Interferon-inducible effector mechanisms in cell-autonomous immunity. Nature Reviews Immunology 12:367-382. doi: 10.1038/nri3210
29. Man SM, Karki R, Malireddi RKS, Neale G, Vogel P, Yamamoto M, Lamkanfi M, Kanneganti T-D. 2015. The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by francisella infection. Nature Immunology 16:467-475. doi: 10.1038/ni.3118
30. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, Howard JC. 2005. Disruption of toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathogens 1:e24. doi: 10.1371/journal.ppat.0010024
31. Melzer T, Duffy A, Weiss LM, Halonen SK. 2008. The gamma interferon (iFN-)-inducible GTP-binding protein IGTP is necessary for toxoplasma vacuolar disruption and induces parasite egression in IFN-stimulated astrocytes. Infection and Immunity 76:4883-4894. doi: 10.1128/IAI.01288-07
32. Meunier E, Dick MS, Dreier RF, Schurmann N, Broz DK, Warming S, Roose-Girma M, Bumann D, Kayagaki N, Takeda K, Yamamoto M, Broz P. 2014. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509:366-370. doi: 10.1038/nature13157
33. Meunier E, Wallet P, Dreier RF, Costanzo S, Anton L, Ruhl S, Dussurgey S, Dick MS, Kistner A, Rigard M, Degrandi D, Pfeffer K, Yamamoto M, Henry T, Broz P. 2015. Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with francisella novicida. Nature Immunology 16:476-484. doi: 10.1038/ni.3119
34. Ohshima J, Lee Y, Sasai M, Saitoh T, Su Ma J, Kamiyama N, Matsuura Y, Pann-Ghill S, Hayashi M, Ebisu S, Takeda K, Akira S, Yamamoto M. 2014. Role of mouse and human autophagy proteins in IFN- -induced cell-autonomous responses against toxoplasma gondii. The Journal of Immunology 192:3328-3335. doi: 10.4049/ jimmunol.1302822
35. Olszewski MA, Gray J, Vestal DJ. 2006. In silico genomic analysis of the human and murine guanylate-binding protein (gBP) gene clusters. Journal of Interferon Cytokine Research 26:328-352. doi: 10.1089/jir.2006.26.328
36. Pham E, Chiang J, Li I, Shum W, Truong K. 2007. A computational tool for designing FRET protein biosensors by rigid-body sampling of their conformational space. Structure 15:515-523. doi: 10.1016/j.str.2007.03.009
37. Pilla DM, Hagar JA, Haldar AK, Mason AK, Degrandi D, Pfeffer K, Ernst RK, Yamamoto M, Miao EA, Coers J. 2014. Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proceedings of the National Academy of Sciences of the United States of America 111:6046-6051. doi: 10.1073/pnas.1321700111
38. Praefcke GJK, Kloep S, Benscheid U, Lilie H, Prakash B, Herrmann C. 2004. Identification of residues in the human guanylate-binding protein 1 critical for nucleotide binding and cooperative GTP hydrolysis. Journal of Molecular Biology 344:257-269. doi: 10.1016/j.jmb.2004.09.026
39. Praefcke GJK, McMahon HT. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules? Nature Reviews Molecular Cell Biology 5:133-147. doi: 10.1038/nrm1313
40. Prakash B, Praefcke GJK, Renault L, Wittinghofer A, Herrmann C. 2000a. Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins. Nature 403:567-571. doi: 10.1038/35000617
41. Prakash B. 2000b. Triphosphate structure of guanylate-binding protein 1 and implications for nucleotide binding and GTPase mechanism. The EMBO Journal 19:4555-1564. doi: 10.1093/emboj/19.17.4555
42. Ridders C. 1979. A new algorithm for computing a single root of a real continuous function. IEEE Transactions on Circuits and Systems 26:979-980. doi: 10.1109/TCS.1979.1084580
43. Selleck EM, Fentress SJ, Beatty WL, Degrandi D, Pfeffer K, Virgin HW, MacMicking JD, Sibley LD. 2013. Guanylate-binding protein 1 (gbp1) contributes to cell-autonomous immunity against toxoplasma gondii. PLoS Pathogens 9:e1003320. doi: 10.1371/journal.ppat.1003320
44. Shanno DF, Kettler PC. 1970. Optimal conditioning of quasi-newton methods. Mathematics of Computation 24:657. doi: 10.1090/S0025-5718-1970-0274030-6
45. Sisamakis E, Valeri A, Kalinin S, Rothwell PJ, Seidel CAM. 2010. Accurate single-molecule fret studies using multiparameter fluorescence detection. Methods in Enzymology, Vol 475: Single Molecule Tools, Pt B 475:455-­514. doi: 10.1016/S0076-6879(10)75018-7
46. Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp-Peters S, Pinto KG, Kirschner GK, Schmid JB, Wink RH, Hulsewede A, Felekyan S, Seidel CAM, Simon R. 2013. Moderation of arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Current Biology 23:362-371. doi: 10.1016/j.cub.2013.01.045
47. Suhling K, Siegel J, Phillips D, French PMW, Leveque-Fort S, Webb SED, Davis DM. 2002. Imaging the environment of green fluorescent protein. Biophysical Journal 83:3589-3595. doi: 10.1016/S0006-3495(02)75359-9
48. Vestal DJ, Gorbacheva VY, Sen GC. 2000. Different subcellular localizations for the related interferon-induced GTPases, MuGBP-1 and MuGBP-2: implications for different functions? Journal of Interferon Cytokine Research 20:991-1000. doi: 10.1089/10799900050198435
49. Vestal DJ, Jeyaratnam JA. 2011. The guanylate-binding proteins: emerging insights into the biochemical properties and functions of this family of large interferon-induced guanosine triphosphatase. Journal of Interferon Cytokine Research 31:89-97. doi: 10.1089/jir.2010.0102
50. Vinogradov SA, Wilson DF. 2000. Recursive maximum entropy algorithm and its application to the luminescence lifetime distribution recovery. Applied Spectroscopy 54:849-855. doi: 10.1366/0003702001950210
51. Vopel T, Hengstenberg CS, Peulen T-O, Ajaj Y, Seidel CAM, Herrmann C, Klare JP. 2014. 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 53:4590-4600. doi: 10.1021/bi500524u
52. Weidtkamp-Peters S, Felekyan S, Bleckmann A, Simon R, Becker W, Kuhnemuth R, Seidel CAM. 2009. Multiparameter fluorescence image spectroscopy to study molecular interactions. Photochemical Photobiological Sciences 8:470-480. doi: 10.1039/b903245m
53. Widengren J, Kudryavtsev V, Antonik M, Berger S, Gerken M, Seidel CAM. 2006. Single-molecule detection and identification of multiple species by multiparameter fluorescence detection. Analytical Chemistry 78:2039-­2050. doi: 10.1021/ac0522759
54. Wu B, Chen Y, Muller JD. 2009. Fluorescence fluctuation spectroscopy of mCherry in living cells. Biophysical Journal 96:2391-2404. doi: 10.1016/j.bpj.2008.12.3902
55. Yamamoto M, Okuyama M, Ma JS, Kimura T, Kamiyama N, Saiga H, Ohshima J, Sasai M, Kayama H, Okamoto T, Huang DCS, Soldati-Favre D, Horie K, Takeda J, Takeda K. 2012. A cluster of interferon-gamma-inducible p65 GTPases plays a critical role in host defense against toxoplasma gondii. Immunity 37:302-313. doi: 10.1016/j.immuni.2012.06.009
56. Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, Miller BC, Cadwell K, Delgado MA, Ponpuak M, Green KG, Schmidt RE, Mizushima N, Deretic V, Sibley LD, Virgin HW. 2008. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4:458-469. doi: 10.1016/j.chom.2008.10.003
57. Zhao Y, Ferguson DJP, Wilson DC, Howard JC, Sibley LD, Yap GS. 2009a. Virulent toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages. The Journal of Immunology 182:3775-3781. doi: 10.4049/jimmunol.0804190
58. Zhao YO, Khaminets A, Hunn JP, Howard JC. 2009b. Disruption of the toxoplasma gondii parasitophorous vacuole by IFNgamma-inducible immunity-related GTPases (iRG proteins) triggers necrotic cell death. PLoS Pathogens 5:e1000288. doi: 10.1371/journal.ppat.1000288