The immunity-related GTPase Irga6 dimerizes in a parallel head-to-head fashion

BMC Biology

Volumn 14, Issue 1, 2016, Pages

  Schulte, Kathrin ^a   Pawlowski, Nikolaus ^b,d   Faelber, Katja ^a   Fröhlich, Chris ^a   Howard, Jonathan ^b,c   Daumke, Oliver ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d BAYER PHARMA AG   (Germany)

Author keywords

Dimerization; Dynamin superfamily; GTPase; Innate immunity; IRG proteins; Oligomerization

Indexed keywords

GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; IIGP1 PROTEIN, MOUSE;

ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; GENETICS; HYDROLYSIS; METABOLISM; MOLECULAR MODEL; MOUSE; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MICE; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 84959366207     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-016-0236-7     Document Type: Article

References (49)

1. MacMicking JD, Taylor GA, McKinney JD. Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science. 2003;302(5645):654-9. doi: 10.1126/science.1088063.
2. Feng CG, Collazo-Custodio CM, Eckhaus M, Hieny S, Belkaid Y, Elkins K, et al. Mice deficient in LRG-47 display increased susceptibility to mycobacterial infection associated with the induction of lymphopenia. J Immunol. 2004;172(2):1163-8.
3. Collazo CM, Yap GS, Sempowski GD, Lusby KC, Tessarollo L, Vande Woude GF, et al. Inactivation of LRG-47 and IRG-47 reveals a family of interferon gamma-inducible genes with essential, pathogen-specific roles in resistance to infection. J Exp Med. 2001;194(2):181-8.
4. Santiago HC, Feng CG, Bafica A, Roffe E, Arantes RM, Cheever A, et al. Mice deficient in LRG-47 display enhanced susceptibility to Trypanosoma cruzi infection associated with defective hemopoiesis and intracellular control of parasite growth. J Immunol. 2005;175(12):8165-72.
5. Taylor GA, Collazo CM, Yap GS, Nguyen K, Gregorio TA, Taylor LS, et al. Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc Natl Acad Sci U S A. 2000;97(2):751-5.
6. Butcher BA, Greene RI, Henry SC, Annecharico KL, Weinberg JB, Denkers EY, et al. p47 GTPases regulate Toxoplasma gondii survival in activated macrophages. Infect Immun. 2005;73(6):3278-86. doi: 10.1128/IAI.73.6.3278-3286.2005.
7. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, et al. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog. 2005;1(3):e24. doi: 10.1371/journal.ppat.0010024.
8. Henry SC, Daniell XG, Burroughs AR, Indaram M, Howell DN, Coers J, et al. Balance of Irgm protein activities determines IFN-gamma-induced host defense. J Leukoc Biol. 2009;85(5):877-85. doi: 10.1189/jlb.1008599.
9. Taylor GA, Feng CG, Sher A. p47 GTPases: regulators of immunity to intracellular pathogens. Nat Rev Immunol. 2004;4(2):100-9. doi: 10.1038/nri1270.
10. Martens S, Howard J. The interferon-inducible GTPases. Annu Rev Cell Dev Biol. 2006;22:559-89. doi: 10.1146/annurev.cellbio.22.010305.104619.
11. Hunn JP, Feng CG, Sher A, Howard JC. The immunity-related GTPases in mammals: a fast-evolving cell-autonomous resistance system against intracellular pathogens. Mamm Genome. 2011;22(1-2):43-54. doi: 10.1007/s00335-010-9293-3.
12. Bekpen C, Marques-Bonet T, Alkan C, Antonacci F, Leogrande MB, Ventura M, et al. Death and resurrection of the human IRGM gene. PLoS Genet. 2009;5(3):e1000403. doi: 10.1371/journal.pgen.1000403.
13. Taylor GA, Stauber R, Rulong S, Hudson E, Pei V, Pavlakis GN, et al. The inducibly expressed GTPase localizes to the endoplasmic reticulum, independently of GTP binding. J Biol Chem. 1997;272(16):10639-45.
14. Martens S, Sabel K, Lange R, Uthaiah R, Wolf E, Howard JC. Mechanisms regulating the positioning of mouse p47 resistance GTPases LRG-47 and IIGP1 on cellular membranes: retargeting to plasma membrane induced by phagocytosis. J Immunol. 2004;173(4):2594-606.
15. Zhao YO, Khaminets A, Hunn JP, Howard JC. Disruption of the Toxoplasma gondii parasitophorous vacuole by IFNgamma-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death. PLoS Pathog. 2009;5(2):e1000288. doi: 10.1371/journal.ppat.1000288.
16. Khaminets A, Hunn JP, Konen-Waisman S, Zhao YO, Preukschat D, Coers J, et al. Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell Microbiol. 2010;12(7):939-61. doi: 10.1111/j.1462-5822.2010.01443.x.
17. Zhao Y, Yap GS. Toxoplasma's arms race with the host interferon response: a menage a trois of ROPs. Cell Host Microbe. 2014;15(5):517-8. doi: 10.1016/j.chom.2014.05.002.
18. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJ, et al. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med. 2006;203(9):2063-71. doi: 10.1084/jem.20061318.
19. Melzer T, Duffy A, Weiss LM, Halonen SK. The gamma interferon (IFN-gamma)-inducible GTP-binding protein IGTP is necessary for toxoplasma vacuolar disruption and induces parasite egression in IFN-gamma-stimulated astrocytes. Infect Immun. 2008;76(11):4883-94. doi: 10.1128/IAI.01288-07.
20. Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC. Inactive and active states of the interferon-inducible resistance GTPase, Irga6, in vivo. J Biol Chem. 2008;283(46):32143-51. doi: 10.1074/jbc.M804846200.
21. Hunn JP, Koenen-Waisman S, Papic N, Schroeder N, Pawlowski N, Lange R, et al. Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO J. 2008;27(19):2495-509. doi: 10.1038/emboj.2008.176.
22. Uthaiah RC, Praefcke GJ, Howard JC, Herrmann C. IIGP1, an interferon-gamma-inducible 47-kDa GTPase of the mouse, showing cooperative enzymatic activity and GTP-dependent multimerization. J Biol Chem. 2003;278(31):29336-43. doi: 10.1074/jbc.M211973200.
23. Ghosh A, Uthaiah R, Howard J, Herrmann C, Wolf E. Crystal structure of IIGP1: a paradigm for interferon-inducible p47 resistance GTPases. Mol Cell. 2004;15(5):727-39. doi: 10.1016/j.molcel.2004.07.017.
24. Pawlowski N, Khaminets A, Hunn JP, Papic N, Schmidt A, Uthaiah RC, et al. The activation mechanism of Irga6, an interferon-inducible GTPase contributing to mouse resistance against Toxoplasma gondii. BMC Biol. 2011;9:7. doi: 10.1186/1741-7007-9-7.
25. Chappie JS, Mears JA, Fang S, Leonard M, Schmid SL, Milligan RA, et al. A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell. 2011;147(1):209-22. doi: 10.1016/j.cell.2011.09.003.
26. Chappie JS, Acharya S, Leonard M, Schmid SL, Dyda F. G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature. 2010;465(7297):435-40. doi: 10.1038/nature09032.
27. Rennie ML, McKelvie SA, Bulloch EM, Kingston RL. Transient dimerization of human MxA promotes GTP hydrolysis, resulting in a mechanical power stroke. Structure. 2014;22(10):1433-45. doi: 10.1016/j.str.2014.08.015.
28. Dick A, Graf L, Olal D, von der Malsburg A, Gao S, Kochs G, et al. Role of nucleotide binding and GTPase domain dimerization in dynamin-like myxovirus resistance protein A for GTPase activation and antiviral activity. J Biol Chem. 2015;290(20):12779-92. doi: 10.1074/jbc.M115.650325.
29. Ghosh A, Praefcke GJ, Renault L, Wittinghofer A, Herrmann C. How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature. 2006;440(7080):101-4.
30. Byrnes LJ, Sondermann H. Structural basis for the nucleotide-dependent dimerization of the large G protein atlastin-1/SPG3A. Proc Natl Acad Sci U S A. 2011;108(6):2216-21. doi: 10.1073/pnas.1012792108.
31. Bian X, Klemm RW, Liu TY, Zhang M, Sun S, Sui XW, et al. Structures of the atlastin GTPase provide insight into homotypic fusion of endoplasmic reticulum membranes. Proc Natl Acad Sci U S A. 2011;108(10):3976-81. doi: 10.1073/pnas.1101643108.
32. Low HH, Lowe J. A bacterial dynamin-like protein. Nature. 2006;444(7120):766-9. doi: 10.1038/nature05312.
33. Low HH, Sachse C, Amos LA, Lowe J. Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell. 2009;139(7):1342-52. doi: 10.1016/j.cell.2009.11.003.
34. Egea PF, Shan SO, Napetschnig J, Savage DF, Walter P, Stroud RM. Substrate twinning activates the signal recognition particle and its receptor. Nature. 2004;427(6971):215-21. doi: 10.1038/nature02250.
35. Faelber K, Gao S, Held M, Posor Y, Haucke V, Noe F, et al. Oligomerization of dynamin superfamily proteins in health and disease. Prog Mol Biol Transl Sci. 2013;117:411-43. doi: 10.1016/B978-0-12-386931-9.00015-5.
36. Sirajuddin M, Farkasovsky M, Hauer F, Kuhlmann D, Macara IG, Weyand M, et al. Structural insight into filament formation by mammalian septins. Nature. 2007;449(7160):311-5. doi: 10.1038/nature06052.
37. Sun YJ, Forouhar F, Li Hm HM, Tu SL, Yeh YH, Kao S, et al. Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon. Nat Struct Biol. 2002;9(2):95-100. doi: 10.1038/nsb744.
38. Schwefel D, Frohlich C, Eichhorst J, Wiesner B, Behlke J, Aravind L, et al. Structural basis of oligomerization in septin-like GTPase of immunity-associated protein 2 (GIMAP2). Proc Natl Acad Sci U S A. 2010;107(47):20299-304. doi: 10.1073/pnas.1010322107.
39. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature. 2007;449(7164):923-7. doi: 10.1038/nature06173.
40. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol. 1993;229(1):105-24. doi: 10.1006/jmbi.1993.1012.
41. Leslie AG. The integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr. 2006;62:48-57.
42. Kabsch W. XDS. Acta Crystallogr D Biol Crystallogr. 2010;66:125-32.
43. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40:658-74.
44. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66(Pt 4):486-501. doi: 10.1107/S0907444910007493.
45. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst. 2010;D66:213-21.
46. Brunger AT. Free R, value: cross-validation in crystallography. Methods Enzymol. 1997;277:366-96.
47. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Cryst. 1976;A32:922-3.
48. Chen VB, Arendall 3rd WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr. 2010;66(Pt 1):12-21. doi: 10.1107/S0907444909042073.
49. Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007;372:774-97.