Secretory mechanisms in cell-mediated cytotoxicity

Annual Review of Cell and Developmental Biology

Volumn 23, Issue , 2007, Pages 495-517

  Stinchcombe, Jane C ^a   Griffiths, Gillian M ^a  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Centrosome; Cytotoxic T lymphocyte; Immunological synapse; Polarized secretion

Indexed keywords

GRANZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PERFORIN; T LYMPHOCYTE RECEPTOR;

CELL FUNCTION; CELL MEDIATED CYTOTOXICITY; CELL POLARITY; CELL SECRETION; CYTOTOXIC T LYMPHOCYTE; HUMAN; IMMUNE SYSTEM; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; REVIEW; ALBINISM; CELL MEMBRANE; CENTROSOME; CYTOTOXICITY; GENETIC DISORDER; GENETICS; IMMUNE DEFICIENCY; IMMUNOLOGY; METABOLISM; MICROTUBULE ORGANIZING CENTER; SECRETION; ULTRASTRUCTURE;

ALBINISM; CELL MEMBRANE; CELL POLARITY; CENTROSOME; CYTOTOXICITY, IMMUNOLOGIC; GENETIC DISEASES, INBORN; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; LYSOSOMES; MICROTUBULE-ORGANIZING CENTER; T-LYMPHOCYTES, CYTOTOXIC;

EID: 38449096740     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.23.090506.123521     Document Type: Review

References (103)

1. Ardouin L, Bracke M, Mathiot A, Pagakis SN, Norton T, et al. 2003. Vav1 transduces TCR signals required for LFA-1 function and cell polarization at the immunological synapse. Eur. J. Immunol. 33:790-97
2. Augustin I, Rosenmund C, Sudhof TC, Brose N. 1999. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400:457-61
3. Baetz K, Isaaz S, Griffiths GM. 1995. Loss of cytotoxic T lymphocyte function in Chediak-Higashi syndrome arises from a secretory defect that prevents lytic granule exocytosis. J. Immunol. 154:6122-31
4. Balaji KN, Schaschke N, Machleidt W, Catalfamo M, Henkart PA. 2002. Surface cathepsin B protects cytotoxic lymphocytes from self-destruction after degranulation. J. Exp. Med. 196:493-503
5. Baran K, Ciccone A, Peters C, Yagita H, Bird PI, et al. 2006. Cytotoxic T lymphocytes from cathepsin B-deficient mice survive normally in vitro and in vivo after encountering and killing target cells. J. Biol. Chem. 281:30485-91
6. Barbosa MD, Barrat FJ, Tchernev VT, Nguyen QA, Mishra VS, et al. 1997. Identification of mutations in two major mRNA isoforms of the Chediak-Higashi syndrome gene in human and mouse. Hum. Mol. Genet. 6:1091-98
7. Bashford CL, Menestrina G, Henkart PA, Pasternak CF. 1988. Cell damage by cytolysin. Spontaneous recovery and reversible inhibition by divalent cations. J. Immunol. 141:3965-74
8. Betz A, Okamoto M, Benseler F, Brose N. 1997. Direct interaction of the rat unc-13 homologue Munc13-1 with the N terminus of syntaxin. J. Biol. Chem. 272:2520-26
9. Billadeau DD, Burkhardt JK. 2006. Regulation of cytoskeletal dynamics at the immune synapse: New stars join the actin troupe. Traffic 7:1451-60
10. Blanchard N, Di Bartolo V, Hivroz C. 2002. In the immune synapse, ZAP-70 controls T cell polarization and recruitment of signaling proteins but not formation of the synaptic pattern. Immunity 17:389-99
11. Blott EJ, Bossi G, Clark R, Zvelebil M, Griffiths GM. 2001. Fas ligand is targeted to secretory lysosomes via a proline-rich domain in its cytoplasmic tail. J. Cell Sci. 114:2405-16
12. Blott EJ, Griffiths GM. 2002. Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 3:122-31
13. Bossi G, Griffiths GM. 1999. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat. Med. 5:90-96
14. Bowers WE, de Duve C. 1967. Lysosomes in lymphoid tissue. II. Intracellular distribution of acid hydrolases. J. Cell Biol. 32:339-48
15. Burkhardt JK, Hester S, Argon Y. 1989. Two proteins targeted to the same lytic granule compartment undergo very different posttranslational processing. Proc. Natl. Acad. Sci. USA 86:7128-32
16. Burkhardt JK, Hester S, Lapham CK, Argon Y. 1990. The lytic granules of natural killer cells are dual-function organelles combining secretory and prelysosomal compartments. J. Cell Biol. 111:2327-40
17. Choudhuri K, Wiseman D, Brown MH, Gould K, Van Der Merwe PA. 2005. T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436:578-82
18. Clark RH, Stinchcombe JC, Day A, Blott E, Booth S, et al. 2003. Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat. Immunol. 4:1111-20
19. Combs J, Kim SJ, Tan S, Ligon LA, Holzbaur EL, et al. 2006. Recruitment of dynein to the Jurkat immunological synapse. Proc. Natl. Acad. Sci. USA 103:14883-88
20. Cullen SP, Adrain C, Luthi AU, Duriez PJ, Martin SJ. 2007. Human and murine granzyme B exhibit divergent substrate preferences. J. Cell Biol. 176:435-44
21. Das V, Nal B, Dujeancourt A, Thoulouze MI, Galli T, et al. 2004. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse: involvement of SNARE complexes. Immunity 20:577-88
22. de Duve C. 2005. The lysosome turns fifty. Nat. Cell Biol. 7:847-49
23. de Souza N, Vallier LG, Fares H, Greenwald I. 2007. SEL-2, the C. elegans neurobeachin/LRBA homolog, is a negative regulator of lin-12/Notch activity and affects endosomal traffic in polarized epithelial cells. Development 134:691-702
24. Dell'Angelica EC, Mullins C, Caplan S, Bonifacino JS. 2000. Lysosome-related organelles. FASEB J. 14:1265-78
25. Depoil D, Zaru R, Guiraud M, Chauveau A, Harriague J, et al. 2005. Immunological synapses are versatile structures enabling selective T cell polarization. Immunity 22:185-94
26. Feldmann J, Callebaut I, Raposo G, Certain S, Bacq D, et al. 2003. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115:461-73
27. Froelich CJ, Orth K, Turbov J, Seth P, Gottlieb R, et al. 1996. 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. 271:29073-79
28. Fukuda M. 2006. Rab27 and its effectors in secretory granule exocytosis: a novel docking machinery composed of a Rab27 • effector complex. Biochem. Soc. Trans. 34:691-95
29. Geiger B, Rosen D, Berke G. 1982. Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J. Cell Biol. 95:137-43
30. Gomes AQ, Ali BR, Ramalho JS, Godfrey RF, Barral DC, et al. 2003. Membrane targeting of Rab GTPases is influenced by the prenylation motif. Mol. Biol. Cell 14:1882-99
31. Gomes ER, Jani S, Gundersen GG. 2005. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121:451-63
32. Gomez TS, Kumar K, Medeiros RB, Shimizu Y, Leibson PJ, Billadeau DD. 2007. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 26:177-90
33. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, et al. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221-27
34. Griffiths GM, Isaaz S. 1993. Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 120:885-96
35. Gromley A, Yeaman C, Rosa J, Redick S, Chen CT, et al. 2005. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123:75-87
36. Gudima GO, Vorobjev IA, Chentsov Yu S. 1988. Centriolar location during blood cell spreading and motion in vitro: an ultrastructural analysis. J. Cell Sci. 89(Pt. 2):225-41
37. Hall BS, Smith E, Langer W, Jacobs LA, Goulding D, Field MC. 2005. Developmental variation in Rab11-dependent trafficking in Trypanosoma brucei. Eukaryot. Cell 4:971-80
38. Huizing M, Sarangarajan R, Strovel E, Zhao Y, Gahl WA, Boissy RE. 2001. AP-3 mediates tyrosinase but not TRP-1 trafficking in human melanocytes. Mol. Biol. Cell 12:2075-85
39. Hume AN, Collinson LM, Hopkins CR, Strom M, Barral DC, et al. 2002. The leaden gene product is required with Rab27a to recruit myosin Va to melanosomes in melanocytes. Traffic 3:193-202
40. Hume AN, Collinson LM, Rapak A, Gomes AQ, Hopkins CR, Seabra MC. 2001. Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J. Cell Biol. 152:795-808
41. Ishikawa H, Kubo A, Tsukita S, Tsukita S. 2005. Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat. Cell Biol. 7:517-24
42. Jenne DE, Tschopp J. 1988. Granzymes, a family of serine proteases released from granules of cytolytic T lymphocytes upon T cell receptor stimulation. Immunol. Rev. 103:53-71
43. Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, et al. 2001. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dyneindynactin motors. Curr. Biol. 11:1680-85
44. Jordens I, Westbroek W, Marsman M, Rocha N, Mommaas M, et al. 2006. Rab7 and Rab27a control two motor protein activities involved in melanosomal transport. Pigment Cell Res. 19:412-23
45. Kaiserman D, Bird CH, Sun J, Matthews A, Ung K, et al. 2006. The major human and mouse granzymes are structurally and functionally divergent. J. Cell Biol. 175:619-30
46. Kayagaki N, Kawasaki A, Ebata T, Ohmoto H, Ikeda S, et al. 1995. Metalloproteinase-mediated release of human Fas ligand. J. Exp. Med. 182:1777-83
47. Khodosh R, Augsburger A, Schwarz TL, Garrity PA. 2006. Bchs, a BEACH domain protein, antagonizes Rab11 in synapse morphogenesis and other developmental events. Development 133:4655-65
48. Krummel MF, Macara I. 2006. Maintenance and modulation of T cell polarity. Nat. Immunol. 7:1143-49
49. Kuhn JR, Poenie M. 2002. Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity 16:111-21
50. Kupfer A, Dennert G. 1984. Reorientation of the microtubule-organizing center and the Golgi apparatus in cloned cytotoxic lymphocytes triggered by binding to lysable target cells. J. Immunol. 133:2762-66
51. Kuta AE, Bashford CL, Pasternak CA, Reynolds CW, Henkart PA. 1991. Characterization of nonlytic cytolysin-membrane intermediates. Mol. Immunol. 28:1263-70
52. Lansbergen G, Akhmanova A. 2006. Microtubule plus end: a hub of cellular activities. Traffic 7:499-507
53. Ludford-Menting MJ, Oliaro J, Sacirbegovic F, Cheah ET, Pedersen N, et al. 2005. A network of PDZ-containing proteins regulates T cell polarity and morphology during migration and immunological synapse formation. Immunity 22:737-48
54. Menager MM, Menasche G, Romao M, Knapnougel P, HoCH, et al. 2007. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8:257-67
55. Menasche G, Pastural E, Feldmann J, Certain S, Ersoy F, et al. 2000. Mutations in RAB27a cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 25:173-76
56. Michaux G, Cutler DF. 2004. How to roll an endothelial cigar: the biogenesis of Weibel-Palade bodies. Traffic 5:69-78
57. Miletic AV, Swat M, Fujikawa K, Swat W. 2003. Cytoskeletal remodeling in lymphocyte activation. Curr. Opin. Immunol. 15:261-68
58. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395:82-86
59. Neeft M, Wieffer M, de Jong AS, Negroiu G, Metz CH, et al. 2005. Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. Mol. Biol. Cell 16:731-41
60. Oetting WS, King RA. 1999. Molecular basis of albinism: mutations and polymorphisms of pigmentation genes associated with albinism. Hum. Mutat. 13:99-115
61. Ohadi M, Lalloz MR, Sham P, Zhao J, Dearlove AM, et al. 1999. Localization of a gene for familial hemophagocytic lymphohistiocytosis at chromosome 9q21.3-22 by homozygosity mapping. Am. J. Hum. Genet. 64:165-71
62. Paul WE, Seder RA. 1994. Lymphocyte responses and cytokines. Cell 76:241-51
63. Pazour GJ, Witman GB. 2003. The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15:105-10
64. Peden AA, Oorschot V, Hesser BA, Austin CD, Scheller RH, Klumperman J. 2004. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 164:1065-76
65. Perez N, Virelizier JL, Arenzana-Seisdedos F, Fischer A, Griscelli C. 1984. Impaired natural killer activity in lymphohistiocytosis syndrome. J. Pediatr. 104:569-73
66. Perou CM, Leslie JD, Green W, Li L, Ward DM, Kaplan J. 1997. The Beige/Chediak-Higashi syndrome gene encodes a widely expressed cytosolic protein. J. Biol. Chem. 272:29790-94
67. Persson T, Calafat J, Janssen H, Karawajczyk M, Carlsson SR, Egesten A. 2002. Specific granules of human eosinophils have lysosomal characteristics: presence of lysosome-associated membrane proteins and acidification upon cellular activation. Biochem. Biophys. Res. Commun. 291:844-54
68. Peters PJ, Borst J, Oorschot V, Fukuda M, Krahenbuhl O, et al. 1991. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173:1099-109
69. Piel M, Nordberg J, Euteneuer U, Bornens M. 2001. Centrosome-dependent exit of cytokinesis in animal cells. Science 291:1550-53
70. Poenie M, Kuhn J, Combs J. 2004. Real-time visualization of the cytoskeleton and effector functions in T cells. Curr. Opin. Immunol. 16:428-38
71. Pruyne D, Legesse-Miller A, Gao L, Dong Y, Bretscher A. 2004. Mechanisms of polarized growth and organelle segregation in yeast. Annu. Rev. Cell Dev. Biol. 20:559-91
72. Purbhoo MA, Irvine DJ, Huppa JB, Davis MM. 2004. T cell killing does not require the formation of a stable mature immunological synapse. Nat. Immunol. 5:524-30
73. Revell PA, Grossman WJ, Thomas DA, Cao X, Behl R, et al. 2005. Granzyme B and the downstream granzymes C and/or F are important for cytotoxic lymphocyte functions. J. Immunol. 174:2124-31
74. Roder JC, Haliotis T, Klein M, Korec S, Jett JR, et al. 1980. A new immunodeficiency disorder in humans involving NK cells. Nature 284:553-55
75. Round JL, Humphries LA, Tomassian T, Mittelstadt P, Zhang M, Miceli MC. 2007. Scaffold protein Dlgh1 coordinates alternative p38 kinase activation, directing T cell receptor signals toward NFAT but not NF-?B transcription factors. Nat. Immunol. 8:154-61
76. Round JL, Tomassian T, Zhang M, Patel V, Schoenberger SP, Miceli MC. 2005. Dlgh1 coordinates actin polymerization, synaptic T cell receptor and lipid raft aggregation, and effector function in T cells. J. Exp. Med. 201:419-30
77. Schneider P, Holler N, Bodmer JL, Hahne M, Frei K, et al. 1998. Conversion of membrane-bound Fas (CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187:1205-13
78. Seabra MC, Coudrier E. 2004. Rab GTPases and myosin motors in organelle motility. Traffic 5:393-99
79. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, Bhawan S, Certain S, et al. 1999. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science 286:1957-59
80. Stinchcombe J, Bossi G, Griffiths GM. 2004. Linking albinism and immunity: the secrets of secretory lysosomes. Science 305:55-59
81. Stinchcombe JC, Barral DC, Mules EH, Booth S, Hume AN, et al. 2001a. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152:825-34
82. Stinchcombe JC, Bossi G, Booth S, Griffiths GM. 2001b. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15:751-61
83. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:462-65
84. Stinchcombe JC, Page LJ, Griffiths GM. 2000. Secretory lysosome biogenesis in cytotoxic T lymphocytes from normal and Chediak Higashi syndrome patients. Traffic 1:435-44
85. Stowers L, Yelon D, Berg LJ, Chant J. 1995. Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. Proc. Natl. Acad. Sci. USA 92:5027-31
86. Su Y, Balice-Gordon RJ, Hess DM, Landsman DS, Minarcik J, et al. 2004. Neurobeachin is essential for neuromuscular synaptic transmission. J. Neurosci. 24:3627-36
87. Suzuki A, Ohno S. 2006. The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119:979-87
88. Tolmachova T, Anders R, Stinchcombe J, Bossi G, Griffiths GM, et al. 2004. A general role for Rab27a in secretory cells. Mol. Biol. Cell 15:332-44
89. Trapani JA, Sutton VR, Thia KY, Li YQ, Froelich CJ, et al. 2003. A clathrin/dynamin- and mannose-6-phosphate receptor-independent pathway for granzyme B-induced cell death. J. Cell Biol. 160:223-33
90. Uellner R, Zvelebil MJ, Hopkins J, Jones J, MacDougall LK, et al. 1997. Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J. 16:7287-96
91. Valdez AC, Cabaniols JP, Brown MJ, Roche PA. 1999. Syntaxin 11 is associated with SNAP-23 on late endosomes and the trans-Golgi network. J. Cell Sci. 112(Pt. 6):845-54
92. Varma R, Campi G, Yokosuka T, Saito T, Dustin ML. 2006. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25:117-27
93. Watanabe T, Noritake J, Kaibuchi K. 2005. Roles of IQGAP1 in cell polarization and migration. Novartis Found. Symp. 269:92, 223-30
94. Waterhouse NJ, Sedelies KA, Trapani JA. 2006. Role of Bid-induced mitochondrial outer membrane permeabilization in granzyme B-induced apoptosis. Immunol. Cell Biol. 84:72-78
95. Wiedemann A, Depoil D, Faroudi M, Valitutti S. 2006. Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proc. Natl. Acad. Sci. USA 103:10985-90
96. Wilson SM, Yip R, Swing DA, O'Sullivan TN, Zhang Y, et al. 2000. A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc. Natl. Acad. Sci. USA 97:7933-38
97. Wu X, Hammer JA 3rd. 2000. Making sense of melanosome dynamics in mouse melanocytes. Pigment Cell Res. 13:241-47
98. Wu XS, Rao K, Zhang H, Wang F, Sellers JR, et al. 2002. Identification of an organelle receptor for myosin-Va. Nat. Cell Biol. 4:271-78
99. Wu XS, Tsan GL, Hammer JA 3rd. 2005. Melanophilin and myosin Va track the microtubule plus end on EB1. J. Cell Biol. 171:201-7
100. Xavier R, Rabizadeh S, Ishiguro K, Andre N, Ortiz JB, et al. 2004. Discs large (Dlg1) complexes in lymphocyte activation. J. Cell Biol. 166:173-78
101. Yago N, Bowers WE. 1975. Unique cathepsin D-type proteases in rat thoracic duct lymphocytes and in rat lymphoid tissues. J. Biol. Chem. 250:4749-54
102. Zuccato E, Blott EJ, Holt O, Sigismund S, Shaw M, et al. 2007. Sorting of Fas ligand to secretory lysosomes is regulated by mono-ubiquitylation and phosphorylation. J. Cell Sci. 120:191-99
103. zur Stadt U, Schmidt S, Kasper B, Beutel K, Diler AS, et al. 2005. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11. Hum. Mol. Genet. 14:827-34