The structural basis for membrane binding and pore formation by lymphocyte perforin (original) (raw)

• Tschopp, J., Masson, D. & Stanley, K. K. Structural/functional similarity between proteins involved in complement- and cytotoxic T-lymphocyte-mediated cytolysis. Nature 322, 831–834 (1986)
  Article CAS ADS Google Scholar
• Shinkai, Y., Takio, K. & Okumura, K. Homology of perforin to the ninth component of complement (C9). Nature 334, 525–527 (1988)
  Article CAS ADS Google Scholar
• Lichtenheld, M. G. et al. Structure and function of human perforin. Nature 335, 448–451 (1988)
  Article CAS ADS Google Scholar
• Lowin, B., Hahne, M., Mattmann, C. & Tschopp, J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 370, 650–652 (1994)
  Article CAS ADS Google Scholar
• Kägi, D. et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369, 31–37 (1994)
  Article ADS Google Scholar
• Young, J. D., Cohn, Z. A. & Podack, E. R. The ninth component of complement and the pore-forming protein (perforin 1) from cytotoxic T cells: structural, immunological, and functional similarities. Science 233, 184–190 (1986)
  Article CAS ADS Google Scholar
• Voskoboinik, I., Smyth, M. J. & Trapani, J. A. Perforin-mediated target-cell death and immune homeostasis. Nature Rev. Immunol. 6, 940–952 (2006)
  Article CAS Google Scholar
• Rosado, C. J. et al. A common fold mediates vertebrate defense and bacterial attack. Science 317, 1548–1551 (2007)
  Article CAS ADS Google Scholar
• Hadders, M. A., Beringer, D. X. & Gros, P. Structure of C8α-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317, 1552–1554 (2007)
  Article CAS ADS Google Scholar
• Tilley, S. J., Orlova, E. V., Gilbert, R. J., Andrew, P. W. & Saibil, H. R. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121, 247–256 (2005)
  Article CAS Google Scholar
• Dang, T. X., Hotze, E. M., Rouiller, I., Tweten, R. K. & Wilson-Kubalek, E. M. Prepore to pore transition of a cholesterol-dependent cytolysin visualized by electron microscopy. J. Struct. Biol. 150, 100–108 (2005)
  Article CAS Google Scholar
• Slade, D. J. et al. Crystal structure of the MACPF domain of human complement protein C8α in complex with the C8γ subunit. J. Mol. Biol. 379, 331–342 (2008)
  Article CAS Google Scholar
• Rossjohn, J., Feil, S. C., McKinstry, W. J., Tweten, R. K. & Parker, M. W. Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 89, 685–692 (1997)
  Article CAS Google Scholar
• Hurley, J. H. & Misra, S. Signaling and subcellular targeting by membrane-binding domains. Annu. Rev. Biophys. Biomol. Struct. 29, 49–79 (2000)
  Article CAS Google Scholar
• Baran, K. et al. The molecular basis for perforin oligomerization and transmembrane pore assembly. Immunity 30, 684–695 (2009)
  Article CAS Google Scholar
• Shepard, L. A. et al. Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an α-helical to β-sheet transition identified by fluorescence spectroscopy. Biochemistry 37, 14563–14574 (1998)
  Article CAS Google Scholar
• Shatursky, O. et al. The mechanism of membrane insertion for a cholesterol-dependent cytolysin: a novel paradigm for pore-forming toxins. Cell 99, 293–299 (1999)
  Article CAS Google Scholar
• Urrea Moreno, R. et al. Functional assessment of perforin C2 domain mutations illustrates the critical role for calcium-dependent lipid binding in perforin cytotoxic function. Blood 113, 338–346 (2009)
  Article Google Scholar
• Podack, E. R., Young, J. D. & Cohn, Z. A. Isolation and biochemical and functional characterization of perforin 1 from cytolytic T-cell granules. Proc. Natl Acad. Sci. USA 82, 8629–8633 (1985)
  Article CAS ADS Google Scholar
• Young, J. D., Nathan, C. F., Podack, E. R., Palladino, M. A. & Cohn, Z. A. Functional channel formation associated with cytotoxic T-cell granules. Proc. Natl Acad. Sci. USA 83, 150–154 (1986)
  Article CAS ADS Google Scholar
• Voskoboinik, I. et al. Calcium-dependent plasma membrane binding and cell lysis by perforin are mediated through its C2 domain: a critical role for aspartate residues 429, 435, 483, and 485 but not 491. J. Biol. Chem. 280, 8426–8434 (2005)
  Article CAS Google Scholar
• Shin, O. H. et al. Munc13 C2B domain is an activity-dependent Ca2+ regulator of synaptic exocytosis. Nature Struct. Mol. Biol. 17, 280–288 (2010)
  Article CAS Google Scholar
• Czajkowsky, D. M., Hotze, E. M., Shao, Z. & Tweten, R. K. Vertical collapse of a cytolysin prepore moves its transmembrane β-hairpins to the membrane. EMBO J. 23, 3206–3215 (2004)
  Article CAS Google Scholar
• Grobler, J. A. & Hurley, J. H. Similarity between C2 domain jaws and immunoglobulin CDRs. Nature Struct. Biol. 4, 261–262 (1997)
  Article CAS Google Scholar
• Ramachandran, R., Tweten, R. K. & Johnson, A. E. The domains of a cholesterol-dependent cytolysin undergo a major FRET-detected rearrangement during pore formation. Proc. Natl Acad. Sci. USA 102, 7139–7144 (2005)
  Article CAS ADS Google Scholar
• Dourmashkin, R. R., Deteix, P., Simone, C. B. & Henkart, P. Electron microscopic demonstration of lesions in target cell membranes associated with antibody-dependent cellular cytotoxicity. Clin. Exp. Immunol. 42, 554–560 (1980)
  CAS PubMed PubMed Central Google Scholar
• Thiery, J. et al. Perforin activates clathrin- and dynamin-dependent endocytosis, which is required for plasma membrane repair and delivery of granzyme B for granzyme-mediated apoptosis. Blood 115, 1582–1593 (2010)
  Article CAS Google Scholar
• Bird, C. H. et al. Cationic sites on granzyme B contribute to cytotoxicity by promoting its uptake into target cells. Mol. Cell. Biol. 25, 7854–7867 (2005)
  Article CAS Google Scholar
• Brickner, A. & Sodetz, J. M. Functional domains of the α subunit of the eighth component of human complement: identification and characterization of a distinct binding site for the γ chain. Biochemistry 24, 4603–4607 (1985)
  Article CAS Google Scholar
• Strong, M. et al. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 103, 8060–8065 (2006)
  Article CAS ADS Google Scholar
• Kabsch, W. Xds. Acta Crystallogr. D 66, 125–132 (2010)
  Article CAS Google Scholar
• Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D 62, 72–82 (2006)
  Article Google Scholar
• Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215–230 (2007)
  CAS Google Scholar
• Sheldrick, G. M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D 66, 479–485 (2010)
  Article CAS Google Scholar
• de la Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472–494 (1997)
  Article CAS Google Scholar
• Abrahams, J. P. & Leslie, A. G. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D 52, 30–42 (1996)
  Article CAS Google Scholar
• Cowtan, K. D. & Zhang, K. Y. Density modification for macromolecular phase improvement. Prog. Biophys. Mol. Biol. 72, 245–270 (1999)
  Article CAS Google Scholar
• Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D 62, 1002–1011 (2006)
  Article Google Scholar
• Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010)
  Article CAS Google Scholar
• Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010)
  Article CAS Google Scholar
• Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240–255 (1997)
  Article CAS Google Scholar
• Bricogne, G. et al. BUSTER, version 2.8.0 (Global Phasing Ltd, Cambridge, UK, 2009)
• Collaborative Computational Project, 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760–763 (1994)
  Article Google Scholar
• Vriend, G. WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52–56 (1990)
  Article CAS Google Scholar
• Konagurthu, A. S., Whisstock, J. C., Stuckey, P. J. & Lesk, A. M. MUSTANG: a multiple structural alignment algorithm. Proteins 64, 559–574 (2006)
  Article CAS Google Scholar
• DeLano, W. L. The PyMOL molecular graphics system. (DeLano Scientific, Palo Alto, 2008); 〈http://www.pymol.org〉.
• Davis, I. W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375–383 (2007)
  Article ADS Google Scholar
• Crowther, R. A., Henderson, R. & Smith, J. M. MRC image processing programs. J. Struct. Biol. 116, 9–16 (1996)
  Article CAS Google Scholar
• Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82–97 (1999)
  Article CAS Google Scholar
• van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17–24 (1996)
  Article CAS Google Scholar
• Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190–199 (1996)
  Article CAS Google Scholar
• White, H. E., Saibil, H. R., Ignatiou, A. & Orlova, E. V. Recognition and separation of single particles with size variation by statistical analysis of their images. J. Mol. Biol. 336, 453–460 (2004)
  Article CAS Google Scholar
• Pettersen, E. F. et al. UCSF Chimera — a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004)
  Article CAS Google Scholar
• Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781–1802 (2005)
  Article CAS Google Scholar
• Kawasaki, A. et al. Perforin, a pore-forming protein detectable by monoclonal antibodies, is a functional marker for killer cells. Int. Immunol. 2, 677–684 (1990)
  Article CAS Google Scholar
• Sutton, V. R. et al. Measuring cell death mediated by cytotoxic lymphocytes or their granule effector molecules. Methods 44, 241–249 (2008)
  Article CAS Google Scholar
• Sun, J. et al. Expression and purification of recombinant human granzyme B from Pichia pastoris. Biochem. Biophys. Res. Commun. 261, 251–255 (1999)
  Article CAS Google Scholar