Protecting a serial killer: Pathways for perforin trafficking and self-defence ensure sequential target cell death

Trends in Immunology

Volumn 33, Issue 8, 2012, Pages 406-412

  Lopez, Jamie A ^a,b   Brennan, Amelia J ^a,b   Whisstock, James C ^c   Voskoboinik, Ilia ^a,b   Trapani, Joseph A ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GRANZYME B; MEMBRANE ENZYME; PERFORIN;

CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DIFFUSION; ENDOPLASMIC RETICULUM; EXOCYTOSIS; NONHUMAN; OLIGOMERIZATION; REVIEW; SECRETORY GRANULE; SYNAPSE; TARGET CELL DESTRUCTION;

ANIMALS; CELL DEATH; HUMANS; PERFORIN; PHAGOCYTOSIS; PROTEIN TRANSPORT; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84864140772     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2012.04.001     Document Type: Review

References (87)

1. Stinchcombe J.C., et al. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 2006, 443:462-465.
2. Stinchcombe J.C., Griffiths G.M. Secretory mechanisms in cell-mediated cytotoxicity. Annu. Rev. Cell Dev. Biol. 2007, 23:495-517.
3. de Saint Basile G., et al. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat. Rev. Immunol. 2010, 10:568-579.
4. Menager M.M., et al. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 2007, 8:257-267.
5. Stepp S.E., et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science 1999, 286:1957-1959.
6. Menasche G., et al. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 2000, 25:173-176.
7. Feldmann J., et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 2003, 115:461-473.
8. Menasche G., et al. Primary hemophagocytic syndromes point to a direct link between lymphocyte cytotoxicity and homeostasis. Immunol. Rev. 2005, 203:165-179.
9. Fischer A., et al. Genetic defects affecting lymphocyte cytotoxicity. Curr. Opin. Immunol. 2007, 19:348-353.
10. Cote M., et al. Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J. Clin. Invest. 2009, 119:3765-3773.
11. zur Stadt U., et al. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11. Hum. Mol. Genet. 2005, 14:827-834.
12. Henter J.I., et al. HLH-2004: Diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr. Blood Cancer 2007, 48:124-131.
13. zur Stadt U., et al. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am. J. Hum. Genet. 2009, 85:482-492.
14. Bird C.H., et al. Selective regulation of apoptosis: the cytotoxic lymphocyte serpin proteinase inhibitor 9 protects against granzyme B-mediated apoptosis without perturbing the Fas cell death pathway. Mol. Cell. Biol. 1998, 18:6387-6398.
15. Sun J., et al. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J. Biol. Chem. 1996, 271:27802-27809.
16. Brennan A.J., et al. Protection from endogenous perforin: glycans and the C terminus regulate exocytic trafficking in cytotoxic lymphocytes. Immunity 2011, 34:879-892.
17. Law R.H., et al. The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 2010, 468:447-451.
18. Bryceson Y.T., et al. Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 2007, 110:1906-1915.
19. Janka G., Zur Stadt U. Familial and acquired hemophagocytic lymphohistiocytosis. Hematology. Am. Soc. Hematol. Educ. Program 2005, 82-88.
20. Meeths M., et al. Spectrum of clinical presentations in familial hemophagocytic lymphohistiocytosis type 5 patients with mutations in STXBP2. Blood 2010, 116:2635-2643.
21. Brown A.C., et al. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol. 2011, 9:e1001152.
22. Rak G.D., et al. Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol. 2011, 9:e1001151.
23. Lopez J.A., et al. Identification of a distal GLUT4 trafficking event controlled by actin polymerization. Mol. Biol. Cell 2009, 20:3918-3929.
24. Liu D., et al. Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 2009, 31:99-109.
25. Maul-Pavicic A., et al. ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3324-3329.
26. Beal A.M., et al. Kinetics of early T cell receptor signaling regulate the pathway of lytic granule delivery to the secretory domain. Immunity 2009, 31:632-642.
27. Liu D., et al. Two modes of lytic granule fusion during degranulation by natural killer cells. Immunol. Cell Biol. 2011, 89:728-738.
28. Berke G., Fishelson Z.V. Localization of aggregated cell surface antigens of target cells bound to cytotoxic T lymphocytes. J. Exp. Med. 1975, 142:1011-1016.
29. Rothstein T.L., et al. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J. Immunol. 1978, 121:1652-1656.
30. Kupfer A., et al. On the mechanism of unidirectional killing in mixtures of two cytotoxic T lymphocytes. Unidirectional polarization of cytoplasmic organelles and the membrane-associated cytoskeleton in the effector cell. J. Exp. Med. 1986, 163:489-498.
31. Blumenthal R., et al. Liposomes as targets for granule cytolysin from cytotoxic large granular lymphocyte tumors. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:5551-5555.
32. 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. 2005, 280:8426-8434.
33. Balaji K.N., et al. Surface cathepsin B protects cytotoxic lymphocytes from self-destruction after degranulation. J. Exp. Med. 2002, 196:493-503.
34. Baran K., et al. Cytotoxic T lymphocytes from cathepsin B-deficient mice survive normally in vitro and in vivo after encountering and killing target cells. J. Biol. Chem. 2006, 281:30485-30491.
35. Dourmashkin R.R., et al. Electron microscopic demonstration of lesions in target cell membranes associated with antibody-dependent cellular cytotoxicity. Clin. Exp. Immunol. 1980, 42:554-560.
36. Podack E.R., Dennert G. Assembly of two types of tubules with putative cytolytic function by cloned natural killer cells. Nature 1983, 302:442-445.
37. Podack E.R., et al. Isolation and biochemical and functional characterization of perforin 1 from cytolytic T-cell granules. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:8629-8633.
38. Young J.D., et al. Functional channel formation associated with cytotoxic T-cell granules. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:150-154.
39. Shinkai Y., et al. Homology of perforin to the ninth component of complement (C9). Nature 1988, 334:525-527.
40. Baran K., et al. The molecular basis for perforin oligomerization and transmembrane pore assembly. Immunity 2009, 30:684-695.
41. Rosado C.J., et al. A common fold mediates vertebrate defense and bacterial attack. Science 2007, 317:1548-1551.
42. Hadders M.A., et al. Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 2007, 317:1552-1554.
43. Aleshin A.E., et al. Structure of complement C6 suggests a mechanism for initiation and unidirectional, sequential assembly of the membrane attack complex (MAC). J. Biol. Chem. 2012, 287:10210-10222.
44. Froelich C.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, 271:29073-29079.
45. Pinkoski M.J., et al. Entry and trafficking of granzyme B in target cells during granzyme B-perforin-mediated apoptosis. Blood 1998, 92:1044-1054.
46. Browne K.A., 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, 19:8604-8615.
47. Metkar S.S., et al. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity 2002, 16:417-428.
48. Reddy A., et al. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 2001, 106:157-169.
49. Sutton V.R., 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, 192:1403-1414.
50. Waterhouse N.J., et al. A central role for Bid in granzyme B-induced apoptosis. J. Biol. Chem. 2005, 280:4476-4482.
51. Jans D.A., et al. BCL-2 blocks perforin-induced nuclear translocation of granzymes concomitant with protection against the nuclear events of apoptosis. J. Biol. Chem. 1999, 274:3953-3961.
52. Trapani J.A., et al. Perforin-dependent nuclear entry of granzyme B precedes apoptosis, and is not a consequence of nuclear membrane dysfunction. Cell Death Differ. 1998, 5:488-496.
53. Shi L., et al. Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization. J. Exp. Med. 1997, 185:855-866.
54. Praper T., et al. Perforin activity at membranes leads to invaginations and vesicle formation. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:21016-21021.
55. Thiery J., et al. Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat. Immunol. 2011, 12:770-777.
56. Keefe D., et al. Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity 2005, 23:249-262.
57. 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 2010, 115:1582-1593.
58. Idone V., et al. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J. Cell Biol. 2008, 180:905-914.
59. Pham C.T., Ley T.J. Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:8627-8632.
60. Sutton V.R., et al. Residual active granzyme B in cathepsin C-null lymphocytes is sufficient for perforin-dependent target cell apoptosis. J. Cell Biol. 2007, 176:425-433.
61. D'Angelo M.E., et al. Cathepsin H is an additional convertase of pro-granzyme B. J. Biol. Chem. 2010, 285:20514-20519.
62. Uellner R., et al. Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J. 1997, 16:7287-7296.
63. Praper T., et al. Human perforin permeabilizing activity, but not binding to lipid membranes, is affected by pH. Mol. Immunol. 2010, 47:2492-2504.
64. Iacovache I., et al. Dual chaperone role of the C-terminal propeptide in folding and oligomerization of the pore-forming toxin aerolysin. PLoS Pathog. 2011, 7:e1002135.
65. Howard S.P., Buckley J.T. Activation of the hole-forming toxin aerolysin by extracellular processing. J. Bacteriol. 1985, 163:336-340.
66. Abrami L., et al. The pore-forming toxin proaerolysin is activated by furin. J. Biol. Chem. 1998, 273:32656-32661.
67. Griffiths G.M., Isaaz S. Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 1993, 120:885-896.
68. Ni X., Morales C.R. The lysosomal trafficking of acid sphingomyelinase is mediated by sortilin and mannose 6-phosphate receptor. Traffic 2006, 7:889-902.
69. Hernandez-Pigeon H., et al. Human keratinocytes acquire cellular cytotoxicity under UV-B irradiation. Implication of granzyme B and perforin. J. Biol. Chem. 2006, 281:13525-13532.
70. Hernandez-Pigeon H., et al. UVA induces granzyme B in human keratinocytes through MIF: implication in extracellular matrix remodeling. J. Biol. Chem. 2007, 282:8157-8164.
71. McIlroy D., et al. A triple-mutated allele of granzyme B incapable of inducing apoptosis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2562-2567.
72. Thia K.Y., Trapani J.A. The granzyme B gene is highly polymorphic in wild mice but essentially invariant in common inbred laboratory strains. Tissue Antigens 2007, 70:198-204.
73. Estebanez-Perpina E., et al. Crystal structure of the caspase activator human granzyme B, a proteinase highly specific for an Asp-P1 residue. Biol. Chem. 2000, 381:1203-1214.
74. Kaiserman D., et al. The major human and mouse granzymes are structurally and functionally divergent. J. Cell Biol. 2006, 175:619-630.
75. Davis J.E., et al. Dependence of granzyme B-mediated cell death on a pathway regulated by Bcl-2 or its viral homolog, BHRF1. Cell Death Differ. 2000, 7:973-983.
76. Gaafar A., et al. Defective gammadelta T-cell function and granzyme B gene polymorphism in a cohort of newly diagnosed breast cancer patients. Exp. Hematol. 2009, 37:838-848.
77. Girnita D.M., et al. Genotypic variation and phenotypic characterization of granzyme B gene polymorphisms. Transplantation 2009, 87:1801-1806.
78. Espinoza L.J., et al. Genetic variants of human granzyme B predict transplant outcomes after HLA matched unrelated bone marrow transplantation for myeloid malignancies. PLoS ONE 2011, 6:e23827.
79. Sun J., et al. Granzyme B encoded by the commonly occurring human RAH allele retains pro-apoptotic activity. J. Biol. Chem. 2004, 279:16907-16911.
80. Voskoboinik I., et al. Perforin: structure, function, and role in human immunopathology. Immunol. Rev. 2010, 235:35-54.
81. Trambas C., et al. A single amino acid change, A91V, leads to conformational changes that can impair processing to the active form of perforin. Blood 2005, 106:932-937.
82. Voskoboinik I., et al. Perforin activity and immune homeostasis: the common A91V polymorphism in perforin results in both presynaptic and postsynaptic defects in function. Blood 2007, 110:1184-1190.
83. Chia J., et al. Temperature sensitivity of human perforin mutants unmasks subtotal loss of cytotoxicity, delayed FHL, and a predisposition to cancer. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:9809-9814.
84. Clementi R., et al. Variations of the perforin gene in patients with autoimmunity/lymphoproliferation and defective Fas function. Blood 2006, 108:3079-3084.
85. Santoro A., et al. A single amino acid change A91V in perforin: a novel, frequent predisposing factor to childhood acute lymphoblastic leukemia?. Haematologica 2005, 90:697-698.
86. Mancebo E., et al. Familial hemophagocytic lymphohistiocytosis in an adult patient homozygous for A91V in the perforin gene, with tuberculosis infection. Haematologica 2006, 91:1257-1260.
87. Brennan A.J., et al. Perforin deficiency and susceptibility to cancer. Cell Death Differ. 2010, 17:607-615.