PI5KI-dependent signals are critical regulators of the cytolytic secretory pathway

Blood

Volumn 111, Issue 8, 2008, Pages 4165-4172

  Micucci, Federica ^a   Capuano, Cristina ^a   Marchetti, Enzo ^b   Piccoli, Mario ^a   Frati, Luigi ^a,c   Santoni, Angela ^a,b   Galandrini, Ricciarda ^a,b  

^a Pasteur Institute   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c IRCCS NEUROMED   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 5 KINASE TYPE I ALPHA; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 5 KINASE TYPE I GAMMA; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG; 1-PHOSPHATIDYLINOSITOL-4-PHOSPHATE 5-KINASE; CELL SURFACE RECEPTOR; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; ISOENZYME; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA; PHOSPHOTRANSFERASE; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY GRANULE; SIGNAL TRANSDUCTION; CELL CULTURE; CYTOLOGY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYMOLOGY; GENE SILENCING; METABOLISM; SECRETION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; ENZYME ACTIVATION; GENE SILENCING; GREEN FLUORESCENT PROTEINS; HUMANS; INTERFERON TYPE II; ISOENZYMES; KILLER CELLS, NATURAL; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOLIPASE C GAMMA; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 43249090885     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-08-108886     Document Type: Article

References (59)

1. Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol. 2001;1:41-49.
2. Clark R, Griffiths GM. Lytic granules, secretory lysosomes and disease. Curr Opin Immunol. 2003;15:516-521.
3. Vyas YM, Maniar H, Dupont B. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and non cytolytic natural killer cell immune synapses. Immunol Rev. 2002;189:161-178.
4. Bryceson YT, March ME, Ljunggren HG, Long EO. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev. 2006;214:73-91.
5. Jiang K, Zhong B, Gilvary DL, et al. Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol. 2000;1:419-425.
6. Upshaw JL, Schoon RA, Dick CJ, Billadeau DD, Leibson PJ. The isoforms of phospholipase C-gamma are differentially used by distinct human NK activating receptors. J Immunol. 2005;175:213-218.
7. Tassi I, Presti R, Kim S, Yokoyama WM, Gilfillan S, Colonna M. Phospholipase C-gamma 2 is a critical signaling mediator for murine NK cell activating receptors. J Immunol. 2005;175:749-754.
8. Garaux A, Kim N, Bell SE, et al. Phospholipase C-gamma2 is essential for NK cell cytotoxicity and innate immunity to malignant and virally infected cells. Blood. 2006;107:994-1002.
9. Fruman DA, Meyers RE, Cantley LC. Phospho-inositide kinases. Annu Rev Biochem. 1998;67:481-507.
10. Martin TF. PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol. 2001;13:493-499.
11. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443:651-657.
12. Ishihara H, Shibasaki Y, Kizuki N, et al. Gloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase. J Biol Chem. 1996;271:23611-23614.
13. Loijens JC, Anderson RA. Type I phosphatidylinositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family. J Biol Chem. 1996;271:32937-32943.
14. Tolias KF, Rameh LE, Ishihara H, et al. Type I phosphatidylinositol-4- phosphate 5-kinases synthesize the novel lipids phosphatidylinositol 3,5-bisphosphate and phosphatidylinositol 5-phos-phate. J Biol Chem. 1998;273:18040-18046.
15. Doughman RL, Firestone AJ, Anderson RA. Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place. J Membr Biol. 2003;194:77-89.
16. Ling K. Doughman RL, Firestone AJ, Bunce MW, Anderson RA. Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature. 2002;420:89-93.
17. Di Paolo G, Moskowitz HS, Gipson K, et al. Impaired Ptdlns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature. 2004;431:415-422.
18. Padron D, Wang YJ, Yamamoto M, Yin H, Roth MG. Phosphatidylinositol phosphate 5-kinase Ibeta recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J Cell Biol. 2003;162:693-701.
19. Coppolino MG, Dierckman R, Loijens J, et al. Inhibition of phosphatidylinositol-4-phosphate 5-kinase lalpha impairs localized actin remodeling and suppresses phagocytosis. J Biol Chem. 2002;277:43849-43857.
20. Doughman RL, Firestone AJ, Wojtasiak ML, Bunce MW, Anderson RA. Membrane ruffling requires coordination between type lalpha phosphatidylinositol phosphate kinase and Rac signaling. J Biol Chem. 2003;278:23036-23045.
21. Stauffer TP, Ahn S, Meyer T. Receptor-induced transient reduction in plasma membrane Ptdlns(4,5)P2 concentration monitored in living cells. Curr Biol. 1998;8:343-346.
22. Varnai P, Balla T. Visualization of phosphoinositides that bind pleckstrin homology domains: calcium-and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol. 1998;143:501-510.
23. Scott CC, Dobson W, Botelho RJ, et al. Phosphatidylinositol-4,5- bisphosphate hydrolysis directs actin remodeling during phagocytosis. J Cell Biol. 2005;169:139-149.
24. Zufferey R, Dull T, Mandel RJ, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol. 1998;72:9873-9880.
25. Micucci F, Zingoni A, Piccoli M, Frati L, Santoni A, Galandrini R. High-efficient lentiviral vector-mediated gene transfer into primary human NK cells. Exp Hematol. 2006;34:1344-1352.
26. Wang YJ, Li WH, Wang J, et al. Critical role of PIP5KIγ87 in lnsP3-mediated Ca(2+) signaling. J Cell Biol. 2004;167:1005-1010.
27. Rubinson DA, Dillon CP, Kwiatkowski AV, et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet. 2003;33:401-406.
28. Galandrini R, Micucci F, Tassi I, et al. Arf6: a new player in FcgammaRIIIA lymphocyte-mediated cytotoxicity. Blood. 2005;106:577-583.
29. Holz RW, Hlubek MD, Sorensen SD, et al. A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (Ptdlns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane Ptdlns-4,5-P2 as being important in exocytosis. J Biol Chem. 2000;275:17878-17885.
30. Botelho RJ, Teruel M. Dierckman R, et al. Localized biphasic changes in phosphatidylinositol-4,5- bisphosphate at sites of phagocytosis. J Cell Biol. 2000;151:1353-1368.
31. Tassi I, Colonna M. The cytotoxicity receptor CRACC (CS-1) recruits EAT-2 and activates the PI3K and phospholipase C gamma signaling pathways in human NK cells. J Immunol. 2005;175:7996-8002.
32. Colucci F, Rosmaraki E, Bregenholt S, et al. Functional dichotomy in natural killer cell signaling: Vav1-dependent and -independent mechanisms. J Exp Med. 2001;193:1413-1424.
33. Watanabe D, Hashimoto S, Ishiai M, et al. Four tyrosine residues in phospholipase C-gamma 2, identified as Btk-dependent phosphorylation sites, are required for B cell antigen receptor-coupled calcium signaling. J Biol Chem. 2001;276:38595-38601.
34. Golub T, Caroni P. PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol. 2005;169:151-165.
35. Xu C, Watras J, Loew LM. Kinetic analysis of receptor-activated phosphoinositide turnover. J Cell Biol. 2003;161:779-791.
36. McLaughlin S, Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 2005;438:605-611.
37. Yang SA, Carpenter CL, Abrams CS. Rho and Rho-kinase mediate thrombin-induced phosphatidylinositol 4-phosphate 5-kinase trafficking in platelets. J Biol Chem. 2004;279:42331-42336.
38. Sasaki J, Sasaki T, Yamazaki M, et al. Regulation of anaphylactic responses by phosphatidylinositol phosphate kinase type lα. J Exp Med. 2005;201:859-870.
39. Stinchcombe J, Bossi G, Griffiths GM. Linking albinism and immunity: the secrets of secretory lysosomes. Science. 2004;305:55-59.
40. Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005;202:1001-1012.
41. BonnemaJD, Karnitz LM, Schoon RA, Abraham RT, Leibson PJ. Fc receptor stimulation of phosphatidylinositol 3-kinase in natural killer cells is associated with protein kinase G-independent granule release and cell-mediated cytotoxicity. J Exp Med. 1994;180:1427-1435.
42. Billadeau DD, Brumbaugh KM, Dick CJ, Schoon RA, Bustelo XR, Leibson PJ. The Vav-Rac1 pathway in cytotoxic lymphocytes regulates the generation of cell-mediated killing. J Exp Med. 1998;188:549-559.
43. Galandrini R, Palmieri G, Piccoli M, Frati L, Santoni A. Role tor the Rac1 exchange factor Vav in the signaling pathways leading to NK cell cytotoxicity. J Immunol. 1999;162:3148-3152.
44. Saci A, Carpenter CL. RhoAGTPase regulates B cell receptor signaling. Mol Cell. 2005;17:205-214.
45. Campbell RB, Liu F, Ross AH. Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J Biol Chem. 2003;278:33617-33620.
46. Berridge MJ, Lipp P, Bootman M D. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol. 2000;1:11-21.
47. Lyubchenko TA, Wurth GA, Zweifach A. Role of calcium influx in cytotoxic T lymphocyte lytic granule exocytosis during target cell killing. Immunity. 2001;15:847-859.
48. Saito K, Tolias KF, Saci A, et al. BTK regulates Ptdlns-4,5-P2 synthesis: importance for calcium signaling and PI3K activity. Immunity. 2003;19:669-678.
49. 2+ in Fc gamma R(CD16)-induced transcription and expression of lymphokine genes. J Exp Med. 1989;169:549-567.
50. Chuang SS, Kumaresan PR, Mathew PA. 2B4 (CD244)-mediated activation of cytotoxicity and IFN-gamma release in human NK cells involves distinct pathways. J Immunol. 2001;67:6210-6216.
51. Huse M, Lillemeier BF, Kuhns MS, Chen DS, Davis MM. T cells use two directionally distinct pathways for cytokine secretion. Nat Immunol. 2006;7:247-255.
52. Fowler KT, Andrews NW, Huleatt JW. Expression and function of synaptotagmin VII in CTLs. J Immunol. 2007;178:1498-1504.
53. Bai J, Tucker WC, Chapman ER. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat Struct Mol Biol. 2004;1:36-44.
54. Leibson PJ, Midthun DE, Windebank KP, Abraham RT. Transmembrane signaling during natural killer cell-mediated cytotoxicity: regulation by protein kinase G activation. J Immunol. 1990;145:1498-1504.
55. 55.Papayannopoulos V, Co C, Prehoda KE, Snapper S, Taunton J, Lim WA. A polybasic motif allows N-WASP to act as a sensor of PIP(2) density. Mol Cell. 2005;17:181-191.
56. Orange JS, Ramesh N, Remold-O'Donnell E, et al. Wiskott-Aldrich syndrome protein is required for NKcell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc Natl Acad Sci USA. 2002;99:11351-11356.
57. Gismondi A, Cifaldi L, Mazza C, et al. Impaired natural and CD16- mediated NK cell cytotoxicity in patients with WAS and XLT ability of IL-2 to correct NK cell functional defect. Blood. 2004; 104:436-443.
58. Aoyagi K, SugayaT, Umeda M, Yamamoto S, Terakawa S, Takahashi M. The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J Biol Chem. 2005;280:17346-17352.
59. Bryceson YT, Rudd E, Zheng C, et al. Defective cytotoxic lymphocyte degranulation in syntaxin-11-deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood. 2007;110:1906-1915.