Human perforin permeabilizing activity, but not binding to lipid membranes, is affected by pH

Molecular Immunology

Volumn 47, Issue 15, 2010, Pages 2492-2504

  Praper, Tilen ^a,b   Beseničar, Mojca Podlesnik ^a,b   Istinič, Helena ^a   Podlesek, Zdravko ^a   Metkar, Sunil S ^b   Froelich, Christopher J ^b   Anderluh, Gregor ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

Author keywords

MACPF domain; Perforin; PH dependence; Pore forming proteins; Surface plasmon resonance

Indexed keywords

CALCIUM; EPIDERMAL GROWTH FACTOR; EPITOPE; MEMBRANE LIPID; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY PF 344; MONOCLONAL ANTIBODY PF 80; MONOMER; PERFORIN; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; HUMAN; HUMAN CELL; LIPID MEMBRANE; MEMBRANE BINDING; MEMBRANE PERMEABILITY; MOLECULAR INTERACTION; MOLECULAR MECHANICS; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; SURFACE PLASMON RESONANCE;

EID: 77955515984     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.06.001     Document Type: Article

References (40)

1. Anderluh G., Beseničar M., Kladnik A., Lakey J.H., Maček P. Properties of nonfused liposomes immobilized on an L1 Biacore chip and their permeabilization by a eukaryotic pore-forming toxin. Anal. Biochem. 2005, 344:43-52.
2. Anderluh G., Gokce I., Lakey J.H. Expression of proteins using the third domain of the Escherichia coli periplasmic-protein TolA as a fusion partner. Protein Exp. Purif. 2003, 28:173-181.
3. Anderluh G., Lakey J.H. Disparate proteins use similar architectures to damage membranes. Trends Biochem. Sci. 2008, 33:482-490.
4. Baran K., Dunstone M., Chia J., Ciccone A., Browne K.A., Clarke C.J., Lukoyanova N., Saibil H., Whisstock J.C., Voskoboinik I., Trapani J.A. The molecular basis for perforin oligomerization and transmembrane pore assembly. Immunity 2009, 30:684-695.
5. Bavdek A., Gekara N.O., Priselac D., Gutiérrez, Aguirre I., Darji A., Chakraborty T., Maček P., Lakey J.H., Weiss S., Anderluh G. Sterol and pH interdependence in the binding, oligomerization, and pore formation of Listeriolysin O. Biochemistry 2007, 46:4425-4437.
6. Beseničar M., Maček P., Lakey J.H., Anderluh G. Surface plasmon resonance in protein-membrane interactions. Chem. Phys. Lipids 2006, 141:169-178.
7. Burkhardt J.K., Hester S., Lapham C.K., Argon Y. The lytic granules of natural killer cells are dual-function organelles combining secretory and pre-lysosomal compartments. J. Cell Biol. 1990, 111:2327-2340.
8. Clark R.H., Stinchcombe J.C., Day A., Blott E., Booth S., Bossi G., Hamblin T., Davies E.G., Griffiths G.M. Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat. Immunol. 2003, 4:1111-1120.
9. a values in proteins. Proteins 2002, 48:388-403.
10. Fraser S.A., Karimi R., Michalak M., Hudig D. Perforin lytic activity is controlled by calreticulin. J. Immunol. 2000, 164:4150-4155.
11. Froelich C.J., Turbov J., Hanna W. Human perforin: rapid enrichment by immobilized metal affinity chromatography (IMAC) for whole cell cytotoxicity assays. Biochem. Biophys. Res. Commun. 1996, 229:44-49.
12. Grimsley G.R., Scholtz J.M., Pace C.N. A summary of the measured pK values of the ionizable groups in folded proteins. Protein Sci. 2009, 18:247-251.
13. Hadders M.A., Beringer D.X., Gros P. Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 2007, 317:1552-1554.
14. Heuck A.P., Hotze E.M., Tweten R.K., Johnson A.E. Mechanism of membrane insertion of a multimeric beta-barrel protein: perfringolysin O creates a pore using ordered and coupled conformational changes. Mol. Cell 2000, 6:1233-1242.
15. Ishiura S., Matsuda K., Koizumi H., Tsukahara T., Arahata K., Sugita H. Calcium is essential for both the membrane binding and lytic activity of pore-forming protein (perforin) from cytotoxic T-lymphocyte. Mol. Immunol. 1990, 27:803-807.
16. Kataoka T., Togashi K., Takayama H., Takaku K., Nagai K. Inactivation and proteolytic degradation of perforin within lytic granules upon neutralization of acidic pH. Immunology 1997, 91:493-500.
17. Kristan K., Viero G., Maček P., Dalla S.M., Anderluh G. The equinatoxin N-terminus is transferred across planar lipid membranes and helps to stabilize the transmembrane pore. FEBS J. 2007, 274:539-550.
18. Masson D., Peters P.J., Geuze H.J., Borst J., Tschopp J. Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry 1990, 29:11229-11235.
19. McCann F.E., Vanherberghen B., Eleme K., Carlin L.M., Newsam R.J., Goulding D., Davis D.M. The size of the synaptic cleft and distinct distributions of filamentous actin, ezrin, CD43, and CD45 at activating and inhibitory human NK cell immune synapses. J. Immunol. 2003, 170:2862-2870.
20. Metkar S.S., Wang B., Aguilar-Santelises M., Raja S.M., Uhlin-Hansen L., Podack E., Trapani J.A., Froelich C.J. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity 2002, 16:417-428.
21. Metkar S.S., Wang B., Froelich C.J. Detection of functional cell surface perforin by flow cytometry. J. Immunol. Methods 2005, 299:117-127.
22. Nalefski E.A., Falke J.J. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 1996, 5:2375-2390.
23. Peterlin P., Arrigler V. Electroformation in a flow chamber with solution exchange as a means of preparation of flaccid giant vesicles. Colloids Surf. B Biointerfaces 2008, 64:77-87.
24. Peters P.J., Borst J., Oorschot V., Fukuda M., Krahenbuhl O., Tschopp J., Slot J.W., Geuze H.J. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 1991, 173:1099-1109.
25. Pipkin M.E., Lieberman J. Delivering the kiss of death: progress on understanding how perforin works. Curr. Opin. Immunol. 2007, 19:301-308.
26. Ponting C.P., Parker P.J. Extending the C2 domain family: C2s in PKCs delta, epsilon, eta, theta, phospholipases, GAPs, and perforin. Protein Sci. 1996, 5:162-166.
27. 2+-binding domain. J. Biol. Chem. 1998, 273:15879-15882.
28. Rosado C.J., Buckle A.M., Law R.H., Butcher R.E., Kan W.T., Bird C.H., Ung K., Browne K.A., Baran K., Bashtannyk-Puhalovich T.A., Faux N.G., Wong W., Porter C.J., Pike R.N., Ellisdon A.M., Pearce M.C., Bottomley S.P., Emsley J., Smith A.I., Rossjohn J., Hartland E.L., Voskoboinik I., Trapani J.A., Bird P.I., Dunstone M.A., Whisstock J.C. A common fold mediates vertebrate defense and bacterial attack. Science 2007, 317:1548-1551.
29. Rosado C.J., Kondos S., Bull T.E., Kuiper M.J., Law R.H., Buckle A.M., Voskoboinik I., Bird P.I., Trapani J.A., Whisstock J.C., Dunstone M.A. The MACPF/CDC family of pore-forming toxins. Cell Microbiol. 2008, 10:1765-1774.
30. Stenger S., Hanson D.A., Teitelbaum R., Dewan P., Niazi K.R., Froelich C.J., Ganz T., Thoma-Uszynski S., Melian A., Bogdan C., Porcelli S.A., Bloom B.R., Krensky A.M., Modlin R.L. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998, 282:121-125.
31. Stinchcombe J.C., Bossi G., Booth S., Griffiths G.M. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 2001, 15:751-761.
32. Sutton V.R., Waterhouse N.J., Baran K., Browne K., Voskoboinik I., Trapani J.A. Measuring cell death mediated by cytotoxic lymphocytes or their granule effector molecules. Methods 2008, 44:241-249.
33. 2+-dependent receptor molecule for lymphocyte perforin. Nature 1989, 337:272-274.
34. Tweten R.K. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 2005, 73:6199-6209.
35. Uellner R., Zvelebil M.J., Hopkins J., Jones J., MacDougall L.K., Morgan B.P., Podack E., Waterfield M.D., Griffiths G.M. Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J. 1997, 16:7287-7296.
36. Voskoboinik I., Smyth M.J., Trapani J.A. Perforin-mediated target-cell death and immune homeostasis. Nat. Rev. Immunol. 2006, 6:940-952.
37. Voskoboinik I., Thia M.C., Fletcher J., Ciccone A., Browne K., Smyth M.J., Trapani J.A. 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. 2005, 280:8426-8434.
38. Young J.D., Damiano A., DiNome M.A., Leong L.G., Cohn Z.A. Dissociation of membrane binding and lytic activities of the lymphocyte pore-forming protein (perforin). J. Exp. Med. 1987, 165:1371-1382.
39. Zuber B., Levitsky V., Jonsson G., Paulie S., Samarina A., Grundstrom S., Metkar S., Norell H., Callender G.G., Froelich C., Ahlborg N. Detection of human perforin by ELISpot and ELISA: ex vivo identification of virus-specific cells. J. Immunol. Methods 2005, 302:13-25.
40. Zuber B., Quigley M.F., Critchfield J.W., Shacklett B.L., Abel K., Miller C.J., Morner A., Paulie S., Ahlborg N., Sandberg J.K. Detection of macaque perforin expression and release by flow cytometry, immunohistochemistry, ELISA, and ELISpot. J. Immunol. Methods 2006, 312:45-53.