Cortical actin recovery at the immunological synapse leads to termination of lytic granule secretion in cytotoxic T lymphocytes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 32, 2017, Pages E6585-E6594

  Ritter, Alex T ^a,b   Kapnick, Senta M ^c   Murugesan, Sricharan ^d   Schwartzberg, Pamela L ^c   Griffiths, Gillian M ^b   Lippincott Schwartz, Jennifer ^a,e  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Actin; Cytotoxic T lymphocytes; Lytic granule secretion; PIP2; RAB27a

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; ACTIN; ACTIN BINDING PROTEIN; DIACYLGLYCEROL; INOSITOL 1,4,5 TRISPHOSPHATE; IONOMYCIN; LATRUNCULIN A; OVALBUMIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE C GAMMA1; RAB27A PROTEIN; RAPAMYCIN; T LYMPHOCYTE RECEPTOR; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RAB27A PROTEIN, MOUSE; RAS RELATED PROTEIN RAB 27A;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE; CELL POPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; COS-7 CELL LINE; CYTOTOXIC T LYMPHOCYTE; DEPOLYMERIZATION; ENZYME INHIBITION; FEMALE; IMMUNOLOGICAL SYNAPSE; MALE; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRUCTURED ILLUMINATION MICROSCOPY; SYNAPSE; T LYMPHOCYTE ACTIVATION; TARGET CELL; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; ANIMAL; CD8+ T LYMPHOCYTE; CYTOLOGY; GENETICS; IMMUNOLOGY; SECRETORY VESICLE; TRANSGENIC MOUSE;

ACTINS; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; IMMUNOLOGICAL SYNAPSES; MICE; MICE, TRANSGENIC; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; RAB27 GTP-BINDING PROTEINS; SECRETORY VESICLES;

EID: 85026852222     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1710751114     Document Type: Article

References (56)

1. Halle S, et al. (2016) In vivo killing capacity of cytotoxic T cells is limited and involves dynamic interactions and T cell cooperativity. Immunity 44:233–245.
2. Quann EJ, Merino E, Furuta T, Huse M (2009) Localized diacylglycerol drives the polarization of the microtubule-organizing center in T cells. Nat Immunol 10:627–635.
3. Bossi G, et al. (2002) The secretory synapse: The secrets of a serial killer. Immunol Rev 189:152–160.
4. Ming M, Schirra C, Becherer U, Stevens DR, Rettig J (2015) Behavior and properties of mature lytic granules at the immunological synapse of human cytotoxic T lymphocytes. PLoS One 10:e0135994.
5. Lyubchenko TA, Wurth GA, Zweifach A (2001) Role of calcium influx in cytotoxic T lymphocyte lytic granule exocytosis during target cell killing. Immunity 15: 847–859.
6. Stinchcombe JC, Bossi G, Booth S, Griffiths GM (2001) The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15:751–761.
7. Wollman R, Meyer T (2012) Coordinated oscillations in cortical actin and Ca2+ correlate with cycles of vesicle secretion. Nat Cell Biol 14:1261–1269.
8. Porat-Shliom N, Milberg O, Masedunskas A, Weigert R (2013) Multiple roles for the actin cytoskeleton during regulated exocytosis. Cell Mol Life Sci 70:2099–2121.
9. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM (2006) Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443: 462–465.
10. Ritter AT, et al. (2015) Actin depletion initiates events leading to granule secretion at the immunological synapse. Immunity 42:864–876.
11. Tsun A, et al. (2011) Centrosome docking at the immunological synapse is controlled by Lck signaling. J Cell Biol 192:663–674.
12. Zhao F, Cannons JL, Dutta M, Griffiths GM, Schwartzberg PL (2012) Positive and negative signaling through SLAM receptors regulate synapse organization and thresholds of cytolysis. Immunity 36:1003–1016.
13. Keefe D, et al. (2005) Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity 23:249–262.
14. Chen TW, et al. (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295–300.
15. Sneller MC, et al. (1997) Clincal, immunologic, and genetic features of an autoimmune lymphoproliferative syndrome associated with abnormal lymphocyte apoptosis. Blood 89:1341–1348.
16. Dennert G, Podack ER (1983) Cytolysis by H-2-specific T killer cells. Assembly of tubular complexes on target membranes. J Exp Med 157:1483–1495.
17. Masson D, Tschopp J (1985) Isolation of a lytic, pore-forming protein (perforin) from cytolytic T-lymphocytes. J Biol Chem 260:9069–9072.
18. Henkart P, et al. (1985) The role of cytoplasmic granules in cytotoxicity by large granular lymphocytes and cytotoxic T lymphocytes. Adv Exp Med Biol 184:121–138.
19. Poenie M, Epel D (1987) Ultrastructural localization of intracellular calcium stores by a new cytochemical method. J Histochem Cytochem 35:939–956.
20. Riedl J, et al. (2008) Lifeact: A versatile marker to visualize F-actin. Nat Methods 5: 605–607.
21. Bunnell SC, Kapoor V, Trible RP, Zhang W, Samelson LE (2001) Dynamic actin polymerization drives T cell receptor-induced spreading: A role for the signal transduction adaptor LAT. Immunity 14:315–329.
22. Barda-Saad M, et al. (2005) Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat Immunol 6:80–89.
23. Li D, et al. (2015) Advanced imaging. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics. Science 349:aab3500.
24. Shibasaki Y, et al. (1997) Massive actin polymerization induced by phosphatidylinositol-4-phosphate 5-kinase in vivo. J Biol Chem 272:7578–7581.
25. Gilmore AP, Burridge K (1996) Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381:531–535.
26. Apgar JR (1995) Activation of protein kinase C in rat basophilic leukemia cells stimulates increased production of phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate: Correlation with actin polymerization. Mol Biol Cell 6: 97–108.
27. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761–789.
28. Weiss A, Samelson LE (2003) T-lymphocyte activation. Fundamental Immunology, ed Paul WE (Lippincott-Raven, New York), pp 321–363.
29. Rhee SG (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281–312.
30. Balla T, Varnai P (2009) Visualization of cellular phosphoinositide pools with GFP-fused protein-domains. Curr Protoc Cell Biol Chapter 24:Unit 24.4.
31. Szentpetery Z, Balla A, Kim YJ, Lemmon MA, Balla T (2009) Live cell imaging with protein domains capable of recognizing phosphatidylinositol 4,5-bisphosphate; a comparative study. BMC Cell Biol 10:67.
32. Bleasdale JE, et al. (1989) Inhibition of phospholipase C dependent processes by U-73, 122. Adv Prostaglandin Thromboxane Leukot Res 19:590–593.
33. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175:377–382.
34. Zoncu R, et al. (2007) Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci USA 104:3793–3798.
35. Clark RH, et al. (2003) Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat Immunol 4:1111–1120.
36. Rak GD, Mace EM, Banerjee PP, Svitkina T, Orange JS (2011) Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol 9:e1001151.
37. Brown AC, et al. (2011) Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol 9:e1001152.
38. Orci L, Gabbay KH, Malaisse WJ (1972) Pancreatic beta-cell web: Its possible role in insulin secretion. Science 175:1128–1130.
39. Giner D, et al. (2005) Real-time dynamics of the F-actin cytoskeleton during secretion from chromaffin cells. J Cell Sci 118:2871–2880.
40. Villanueva J, et al. (2012) The F-actin cortex in chromaffin granule dynamics and fusion: A minireview. J Mol Neurosci 48:323–327.
41. Torregrosa-Hetland CJ, et al. (2011) The F-actin cortical network is a major factor influencing the organization of the secretory machinery in chromaffin cells. J Cell Sci 124:727–734.
42. Yi J, Wu XS, Crites T, Hammer JA, 3rd (2012) Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells. Mol Biol Cell 23:834–852.
43. Beemiller P, Jacobelli J, Krummel MF (2012) Integration of the movement of signaling microclusters with cellular motility in immunological synapses. Nat Immunol 13: 787–795.
44. Babich A, et al. (2012) F-actin polymerization and retrograde flow drive sustained PLCγ1 signaling during T cell activation. J Cell Biol 197:775–787.
45. Scott CC, et al. (2005) Phosphatidylinositol-4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J Cell Biol 169:139–149.
46. Martínez-Martín N, et al. (2011) T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase-dependent phagocytosis. Immunity 35:208–222.
47. Goodridge HS, et al. (2011) Activation of the innate immune receptor Dectin-1 upon formation of a ‘phagocytic synapse’. Nature 472:471–475.
48. Niedergang F, Di Bartolo V, Alcover A (2016) Comparative anatomy of phagocytic and immunological synapses. Front Immunol 7:18.
49. Huang JF, et al. (1999) TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science 286:952–954.
50. Braiman A, Barda-Saad M, Sommers CL, Samelson LE (2006) Recruitment and activation of PLCgamma1 in T cells: A new insight into old domains. EMBO J 25:774–784.
51. Wilson SM, et al. (2000) A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc Natl Acad Sci USA 97:7933–7938.
52. Stinchcombe JC, et al. (2001) Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152:825–834.
53. Haddad EK, Wu X, Hammer JA, 3rd, Henkart PA (2001) Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J Cell Biol 152:835–842.
54. Davis SJ, van der Merwe PA (2006) The kinetic-segregation model: TCR triggering and beyond. Nat Immunol 7:803–809.
55. Hogquist KA, et al. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76:17–27.
56. Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873–1877.