Perforin forms transient pores on the target cell plasma membrane to facilitate rapid access of granzymes during killer cell attack

Blood

Volumn 121, Issue 14, 2013, Pages 2659-2668

  Lopez, Jamie A ^a,b,c   Susanto, Olivia ^a   Jenkins, Misty R ^a,b,c   Lukoyanova, Natalya ^d   Sutton, Vivien R ^a   Law, Ruby H P ^e   Johnston, Angus ^f   Bird, Catherina H ^e   Bird, Phillip I ^e   Whisstock, James C ^e   Trapani, Joseph A ^a,b,f   Saibil, Helen R ^d   Voskoboinik, Ilia ^a,b,c,g  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b Molecular Imaging and Therapeutic Nuclear Medicine at Peter MacCallum Cancer Centre and Sir Peter MacCallum Department of Oncology at University of Melbourne   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e MONASH UNIVERSITY   (Australia)

^f Department of Chemical and Biomolecular Engineering ^*  (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CYCLODEXTRIN; CALCIUM ION; CASPASE; GRANZYME B; PERFORIN; PROTEIN BID; COMPLEMENT MEMBRANE ATTACK COMPLEX; GRANZYME; PERFORIN 1, MOUSE; PORE FORMING CYTOTOXIC PROTEIN;

APOPTOSIS; ARTICLE; CALCIUM INTAKE; CD8+ T LYMPHOCYTE; CELL MEMBRANE; CELL PERMEABILIZATION; CYTOPLASM; CYTOTOXIC LYMPHOCYTE; DIFFUSION; EFFECTOR CELL; ELECTRON MICROSCOPY; ENDOCYTOSIS; EXOCYTOSIS; FEMALE; FLUORESCENCE; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; KILLER CELL; LYMPHOCYTE; MICROSCOPY; NATURAL KILLER CELL; PH; PRIORITY JOURNAL; TARGET CELL; ANIMAL; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; HELA CELL; IMMUNOLOGY; LEUKEMIA CELL LINE; METABOLISM; MOUSE; TIME;

ANIMALS; APOPTOSIS; CELL MEMBRANE; COMPLEMENT MEMBRANE ATTACK COMPLEX; ENDOCYTOSIS; EXOCYTOSIS; GRANZYMES; HELA CELLS; HUMANS; JURKAT CELLS; KILLER CELLS, NATURAL; MICE; PORE FORMING CYTOTOXIC PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TIME FACTORS;

MLCS; MLOWN;

EID: 84876174174     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-07-446146     Document Type: Article

References (43)

1. Podack ER, Dennert G. Assembly of two types of tubules with putative cytolytic function by cloned natural killer cells. Nature. 1983;302(5907): 442-445.
2. Dourmashkin RR, Deteix P, Simone CB, et al. Electron microscopic demonstration of lesions in target cell membranes associated with antibody-dependent cellular cytotoxicity. Clin Exp Immunol. 1980;42(3):554-560.
3. Shinkai Y, Takio K, Okumura K. Homology of perforin to the ninth component of complement (C9). Nature. 1988;334(6182):525-527.
4. de Saint Basile G, Ménasché G, Fischer A. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat Rev Immunol. 2010;10(8):568-579.
5. Shi L, Mai S, Israels S, et al. Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization. J Exp Med. 1997;185(5):855-866.
6. Bird CH, Sun J, Ung K, et al. Cationic sites on granzyme B contribute to cytotoxicity by promoting its uptake into target cells. Mol Cell Biol. 2005;25(17):7854-7867.
7. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol. 2002;2(10):735-747.
8. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science. 1999;286(5446):1957-1959.
9. Chia J, Yeo KP, Whisstock JC, et al. Temperature sensitivity of human perforin mutants unmasks subtotal loss of cytotoxicity, delayed FHL, and a predisposition to cancer. Proc Natl Acad Sci USA. 2009;106(24):9809-9814.
10. Law RHP, Lukoyanova N, Voskoboinik I, et al. The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature. 2010;468(7322):447-451.
11. Keefe D, Shi L, Feske S, et al. Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity. 2005;23(3):249-262.
12. Thiery J, Keefe D, Boulant S, et al. Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol. 2011;12(8):770-777.
13. Thiery J, Keefe D, Saffarian S, 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. 2010; 115(8):1582-1593.
14. Praper T, Sonnen AF-P, Kladnik A, et al. Perforin activity at membranes leads to invaginations and vesicle formation. Proc Natl Acad Sci USA. 2011; 108(52):21016-21021.
15. Froelich CJ, Orth K, Turbov J, et al. New paradigm for lymphocyte granule-mediated cytotoxicity. Target cells bind and internalize granzyme B, but an endosomolytic agent is necessary for cytosolic delivery and subsequent apoptosis. J Biol Chem. 1996;271(46): 29073-29079.
16. Browne KA, Blink E, Sutton VR, et al. Cytosolic delivery of granzyme B by bacterial toxins: evidence that endosomal disruption, in addition to transmembrane pore formation, is an important function of perforin. Mol Cell Biol. 1999;19(12): 8604-8615.
17. Praper T, Sonnen A, Viero G, et al. Human perforin employs different avenues to damage membranes. J Biol Chem. 2011;286(4): 2946-2955.
18. Dang TX, Hotze EM, Rouiller I, et al. Prepore to pore transition of a cholesterol-dependent cytolysin visualized by electron microscopy. J Struct Biol. 2005;150(1):100-108.
19. Sutton VR, Davis JE, Cancilla M, et al. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J Exp Med. 2000;192(10): 1403-1414.
20. Willoughby CA, Bull HG, Garcia-Calvo M, et al. Discovery of potent, selective human granzyme B inhibitors that inhibit CTL mediated apoptosis. Bioorg Med Chem Lett. 2002;12(16):2197-2200.
21. Poenie M, Tsien RY, Schmitt-Verhulst AM. Sequential activation and lethal hit measured by [Ca21]i in individual cytolytic T cells and targets. EMBO J. 1987;6(8):2223-2232.
22. Metkar SS, Wang B, Aguilar-Santelises M, et al. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity. 2002;16(3):417-428.
23. Metkar SS, Wang B, Catalan E, et al. Perforin rapidly induces plasma membrane phospholipid flip-flop. PLoS ONE. 2011;6(9):e24286.
24. Waterhouse NJ, Sutton VR, Sedelies KA, et al. Cytotoxic T lymphocyte-induced killing in the absence of granzymes A and B is unique and distinct from both apoptosis and perforin-dependent lysis. J Cell Biol. 2006;173(1):133-144.
25. Renkin EM. Filtration, diffusion, and molecular sieving through porous cellulose membranes. J Gen Physiol. 1954;38(2):225-243.
26. Rieger AM, Hall BE, Luong T, et al. Conventional apoptosis assays using propidium iodide generate a significant number of false positives that prevent accurate assessment of cell death. J Immunol Methods. 2010;358(1-2):81-92.
27. Sedelies KA, Ciccone A, Clarke CJP, et al. Blocking granule-mediated death by primary human NK cells requires both protection of mitochondria and inhibition of caspase activity. Cell Death Differ. 2008;15(4):708-717.
28. Browne KA, Johnstone RW, Jans DA, et al. Filamin (280-kDa actin-binding protein) is a caspase substrate and is also cleaved directly by the cytotoxic T lymphocyte protease granzyme B during apoptosis. J Biol Chem. 2000;275(50): 39262-39266.
29. Sutton VR, Vaux DL, Trapani JA. Bcl-2 prevents apoptosis induced by perforin and granzyme B, but not that mediated by whole cytotoxic lymphocytes. J Immunol. 1997;158(12): 5783-5790.
30. Maul-Pavicic A, Chiang SCC, Rensing-Ehl A, et al. ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc Natl Acad Sci USA. 2011;108(8):3324-3329.
31. Idone V, Tam C, Goss JW, et al. Repair of injured plasma membrane by rapid Ca21-dependent endocytosis. J Cell Biol. 2008;180(5):905-914.
32. Gruenberg J, Maxfield FR. Membrane transport in the endocytic pathway. Curr Opin Cell Biol. 1995; 7(4):552-563.
33. Voskoboinik I, Thia M-C, Fletcher J, 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. 2005;280(9):8426-8434.
34. Praper T, Besenicar MP, Istinic H, et al. Human perforin permeabilizing activity, but not binding to lipid membranes, is affected by pH. Mol Immunol. 2010;47(15):2492-2504.
35. Phillips K, de la Peña AH. The combined use of the Thermofluor assay and ThermoQ analytical software for the determination of protein stability and buffer optimization as an aid in protein crystallization. Curr Protoc Mol Biol. 2011;94: 10.28.1-10.28.15.
36. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol. 2007;8(11):917-929.
37. Kawasaki Y, Saito T, Shirota-Someya Y, et al. Cell death-associated translocation of plasma membrane components induced by CTL. J Immunol. 2000;164(9):4641-4648.
38. Walev I, Bhakdi SC, Hofmann F, et al. Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O. Proc Natl Acad Sci USA. 2001;98(6):3185-3190.
39. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(21)-regulated exocytosis of lysosomes. Cell. 2001;106(2):157-169.
40. Trapani JA, Jans DA, Jans PJ, et al. Efficient nuclear targeting of granzyme B and the nuclear consequences of apoptosis induced by granzyme B and perforin are caspase-dependent, but cell death is caspase-independent. J Biol Chem. 1998;273(43):27934-27938.
41. Trapani JA, Jans P, Smyth MJ, et al. Perforin-dependent nuclear entry of granzyme B precedes apoptosis, and is not a consequence of nuclear membrane dysfunction. Cell Death Differ. 1998; 5(6):488-496.
42. Trapani JA, Sutton VR, Thia KYT, et al. A clathrin/ dynamin- and mannose-6-phosphate receptor-independent pathway for granzyme B-induced cell death. J Cell Biol. 2003;160(2):223-233.
43. Gerasimenko JV, Tepikin AV, Petersen OH, et al. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr Biol. 1998;8(24): 1335-1338.