Distinct role of Rab27a in granule movement at the plasma membrane and in the cytosol of NK cells

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-12

  Liu, Dongfang ^a   Meckel, Tobias ^a   Long, Eric O ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAB27A PROTEIN; RAB PROTEIN; RAB27A PROTEIN, HUMAN; RAB27A PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL GRANULE; CELL LINE; CELL MEMBRANE; CELL MOTION; CELL PERMEABILIZATION; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; HUMAN; HUMAN CELL; MICROTUBULE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN FUNCTION; STEADY STATE; ANIMAL; C3H MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM;

ANIMALS; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; CYTOPLASMIC GRANULES; CYTOSOL; HUMANS; KILLER CELLS, NATURAL; MICE; MICE, INBRED C3H; RAB GTP-BINDING PROTEINS;

EID: 77958466893     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012870     Document Type: Article

References (62)

1. Lodoen MB, Lanier LL (2006) Natural killer cells as an initial defense against pathogens. Curr Opin Immunol 18: 391-398.
2. Bossi G, Griffiths GM (2005) CTL secretory lysosomes: biogenesis and secretion of a harmful organelle. Semin Immunol 17: 87-94.
3. Trapani JA, Smyth MJ (2002) Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2: 735-747.
4. 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. NatMed 5: 90-96.
5. Stinchcombe JC, Griffiths GM (2007) Secretory mechanisms in cell-mediated cytotoxicity. Annu Rev Cell Dev Biol 23: 495-517.
6. Carpen O, Virtanen I, Lehto VP, Saksela E (1983) Polarization of NK cell cytoskeleton upon conjugation with sensitive target cells. J Immunol 131: 2695-2698.
7. Kupfer A, Dennert G, Singer SJ (1983) Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc Natl Acad Sci USA 80: 7224-7228.
8. Katz P, Zaytoun AM, Lee JH, Jr. (1982) Mechanisms of human cell-mediated cytotoxicity. III. Dependence of natural killing on microtubule and microfilament integrity. J Immunol 129: 2816-2825.
9. Lyubchenko TA, Wurth GA, Zweifach A (2003) The actin cytoskeleton and cytotoxic T lymphocytes: evidence for multiple roles that could affect granule exocytosis-dependent target cell killing. J Physiol 547: 835-847.
10. Wulfing C, Purtic B, Klem J, Schatzle JD (2003) Stepwise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc Natl Acad Sci USA 100: 7767-7772.
11. Liu D, Bryceson YT, Meckel T, Vasiliver-Shamis G, Dustin ML, et al. (2009) Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 31: 99-109.
12. Liu D, Xu L, Yang F, Li D, Gong F, et al. (2005) Rapid biogenesis and sensitization of secretory lysosomes in NK cells mediated by target-cell recognition. Proc Natl Acad Sci USA 102: 123-127.
13. Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO (2005) Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med 202: 1001-1012.
14. Kim HS, Das A, Gross CC, Bryceson YT, Long EO (2010) Synergistic signals for natural cytotoxicity are required to overcome inhibition by c-Cbl ubiquitin ligase. Immunity 32: 175-186.
15. Griscelli C, Durandy A, Guy-Grand D, Daguillard F, Herzog C, et al. (1978) A syndrome associating partial albinism and immunodeficiency. Am J Med 65: 691-702.
16. Sanal O, Ersoy F, Tezcan I, Metin A, Yel L, et al. (2002) Griscelli disease: genotype-phenotype correlation in an array of clinical heterogeneity. J Clin Immunol 22: 237-243.
17. 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: 173-176.
18. Stinchcombe JC, Barral DC, Mules EH, Booth S, Hume AN, et al. (2001) Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152: 825-834.
19. Ohbayashi N, Mamishi S, Ishibashi K, Maruta Y, Pourakbari B, et al. (2010) Functional characterization of two RAB27A missense mutations found in Griscelli syndrome type 2. Pigment Cell Melanoma Res.
20. 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: 7933-7938.
21. Hume AN, Ushakov DS, Tarafder AK, Ferenczi MA, Seabra MC (2007) Rab27a and MyoVa are the primary Mlph interactors regulating melanosome transport in melanocytes. J Cell Sci 120: 3111-3122.
22. 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.
23. Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S (2002) Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol Chem 277: 3805-3808.
24. Steyer JA, Almers W (1999) Tracking single secretory granules in live chromaffin cells by evanescent-field fluorescence microscopy. Biophys J 76: 2262-2271.
25. Axelrod D (2001) Total internal reflection fluorescence microscopy in cell biology. Traffic 2: 764-774.
26. Li D, Xiong J, Qu A, Xu T (2004) Three-dimensional tracking of single secretory granules in live PC12 cells. Biophys J 87: 1991-2001.
27. 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: 2327-2340.
28. 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: 1099-1109.
29. O'Keefe JP, Gajewski TF (2005) Cutting edge: cytotoxic granule polarization and cytolysis can occur without central supramolecular activation cluster formation in CD8+ effector T cells. J Immunol 175: 5581-5585.
30. 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.
31. Stinchcombe J, Bossi G, Griffiths GM (2004) Linking albinism and immunity: the secrets of secretory lysosomes. Science 305: 55-59.
32. 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: 1111-1120.
33. Mentlik AN, Sanborn KB, Holzbaur EL, Orange JS (2010) Rapid lytic granule convergence to the MTOC in natural killer cells is dependent on dynein but not cytolytic commitment. Mol Biol Cell 21: 2241-2256.
34. Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED (1994) Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871.
35. Bubb MR, Spector I, Beyer BB, Fosen KM (2000) Effects of jasplakinolide on the kinetics of actin polymerization. An explanation for certain in vivo observations. J Biol Chem 275: 5163-5170.
36. Saxton MJ, Jacobson K (1997) Single-particle tracking: applications to membrane dynamics. Annu Rev Biophys Biomol Struct 26: 373-399.
37. Orange JS, Harris KE, Andzelm MM, Valter MM, Geha RS, et al. (2003) The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci USA 100: 14151-14156.
38. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM (2006) Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443: 462-465.
39. Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, et al. (2000) Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys J 78: 2863-2877.
40. Jung SR, Kim MH, Hille B, Koh DS (2009) Control of granule mobility and exocytosis by Ca2+ -dependent formation of F-actin in pancreatic duct epithelial cells. Traffic 10: 392-410.
41. Sanborn KB, Rak GD, Maru SY, Demers K, Difeo A, et al. (2009) Myosin IIA associates with NK cell lytic granules to enable their interaction with F-actin and function at the immunological synapse. J Immunol 182: 6969-6984.
42. Goode BL, Drubin DG, Barnes G (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12: 63-71.
43. Rogers SL, Gelfand VI (2000) Membrane trafficking, organelle transport, and the cytoskeleton. Curr Opin Cell Biol 12: 57-62.
44. Wu X, Jung G, Hammer JA, 3rd (2000) Functions of unconventional myosins. Curr Opin Cell Biol 12: 42-51.
45. Chen Y, Wang Y, Ji W, Xu P, Xu T (2008) A pre-docking role for microtubules in insulin-stimulated glucose transporter 4 translocation. FEBS J 275: 705-712.
46. Lopes VS, Ramalho JS, Owen DM, Karl MO, Strauss O, et al. (2007) The ternary Rab27a-Myrip-Myosin VIIa complex regulates melanosome motility in the retinal pigment epithelium. Traffic 8: 486-499.
47. Bahadoran P, Aberdam E, Mantoux F, Busca R, Bille K, et al. (2001) Rab27a: A key to melanosome transport in human melanocytes. J Cell Biol 152: 843-850.
48. Hong W (2005) Cytotoxic T lymphocyte exocytosis: bring on the SNAREs! Trends Cell Biol 15: 644-650.
49. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, et al. (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19-30; sup pp 11-13.
50. Johnson JL, Brzezinska AA, Tolmachova T, Munafo DB, Ellis BA, et al. (2009) Rab27a and Rab27b Regulate Neutrophil Azurophilic Granule Exocytosis and NADPH oxidase Activity by Independent Mechanisms. Traffic.
51. Kasai K, Ohara-Imaizumi M, Takahashi N, Mizutani S, Zhao S, et al. (2005) Rab27a mediates the tight docking of insulin granules onto the plasma membrane during glucose stimulation. J Clin Invest 115: 388-396.
52. 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: 691-695.
53. Holt O, Kanno E, Bossi G, Booth S, Daniele T, et al. (2008) Slp1 and Slp2-a localize to the plasma membrane of CTL and contribute to secretion from the immunological synapse. Traffic 9: 446-457.
54. Menasche G, Menager MM, Lefebvre JM, Deutsch E, Athman R, et al. (2008) A newly identified isoform of Slp2a associates with Rab27a in cytotoxic T cells and participates to cytotoxic granule secretion. Blood 112: 5052-5062.
55. Arimura N, Kimura T, Nakamuta S, Taya S, Funahashi Y, et al. (2009) Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev Cell 16: 675-686.
56. Brzezinska AA, Johnson JL, Munafo DB, Crozat K, Beutler B, et al. (2008) The Rab27a effectors JFC1/Slp1 and Munc13-4 regulate exocytosis of neutrophil granules. Traffic 9: 2151-2164.
57. Menager MM, Menasche G, Romao M, Knapnougel P, Ho CH, et al. (2007) Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat Immunol 8: 257-267.
58. Wood SM, Meeths M, Chiang SC, Bechensteen AG, Boelens JJ, et al. (2009) Different NK cell activating receptors preferentially recruit Rab27a or Munc13- 4 to perforin-containing granules for cytotoxicity. Blood.
59. Wehrle-Haller B, Imhof BA (2003) Actin, microtubules and focal adhesion dynamics during cell migration. Int J Biochem Cell Biol 35: 39-50.
60. Schmoranzer J, Goulian M, Axelrod D, Simon SM (2000) Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J Cell Biol 149: 23-32.
61. Schutz GJ, Schindler H, Schmidt T (1997) Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophys J 73: 1073-1080.
62. Kusumi A, Sako Y, Yamamoto M (1993) Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J 65: 2021-2040.