Multiphasic dynamics of phosphatidylinositol 4-phosphate during phagocytosis

Molecular Biology of the Cell

Volumn 28, Issue 1, 2017, Pages 128-140

  Levin, Roni ^a,b   Hammond, Gerald R V ^c   Balla, Tamas ^d   Camilli, Pietro De ^e   Fairn, Gregory D ^b,f   Grinstein, Sergio ^a,b,f  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

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

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; DIACYLGLYCEROL; GREEN FLUORESCENT PROTEIN; HYDROLASE; IMMUNOGLOBULIN G; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4 KINASE 2A; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL KINASE; PHOSPHOLIPASE C; PROTEIN; PROTEIN KINASE LYN; RAPAMYCIN; SAC2 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; MINOR HISTOCOMPATIBILITY ANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 4-PHOSPHATE; PHOSPHATIDYLINOSITOL PHOSPHATE 4-KINASE; PHOSPHOTRANSFERASE; PI4KIIIALPHA PROTEIN, HUMAN; POLYPHOSPHOINOSITIDE; RAB PROTEIN;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CELL MATURATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSOL; DIMERIZATION; DYNAMICS; ELECTROPORATION; FLUORESCENCE; GENE SILENCING; GOLGI COMPLEX; HETEROLOGOUS EXPRESSION; HYDROLYSIS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SPACE; LYSOSOME; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PHAGOLYSOSOME; PHAGOSOME; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAW 264.7 CELL LINE; TIME-LAPSE VIDEO MICROSCOPY; TRANSIENT EXPRESSION; ANIMAL; ENDOSOME; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 4-KINASE; ANIMALS; ENDOSOMES; LYSOSOMES; MACROPHAGES; MICE; MINOR HISTOCOMPATIBILITY ANTIGENS; PHAGOCYTOSIS; PHAGOSOMES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RAB GTP-BINDING PROTEINS; RAW 264.7 CELLS;

EID: 85008178602     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-06-0451     Document Type: Article

References (54)

1. Azzoni L, Kamoun M, Salcedo TW, Kanakaraj P, Perussia B (1992). Stimulation of Fc gamma RIIIA results in phospholipase C-gamma 1 tyrosine phosphorylation and p56lck activation. J Exp Med 176, 1745-1750.
2. Balla A, Kim YJ, Varnai P, Szentpetery Z, Knight Z, Shokat KM, Balla T (2008). Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIalpha. Mol Biol Cell 19, 711-721.
3. Balla A, Tuymetova G, Barshishat M, Geiszt M, Balla T (2002). Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J Biol Chem 277, 20041-20050.
4. Balla A, Tuymetova G, Tsiomenko A, Várnai P, Balla T (2005). A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol Biol Cell 16, 1282-1295.
5. Balla T (2013). Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93, 1019-1137.
6. Bohdanowicz M, Balkin DM, De Camilli P, Grinstein S (2012). Recruitment of OCRL and Inpp5B to phagosomes by Rab5 and APPL1 depletes phosphoinositides and attenuates Akt signaling. Mol Biol Cell 23, 176-187.
7. Bohdanowicz M, Cosío G, Backer JM, Grinstein S (2010). Class I and class III phosphoinositide 3-kinases are required for actin polymerization that propels phagosomes. J Cell Biol 191, 999-1012.
8. Bohdanowicz M, Schlam D, Hermansson M, Rizzuti D, Fairn GD, Ueyama T, Somerharju P, Du G, Grinstein S (2013). Phosphatidic acid is required for the constitutive ruffling and macropinocytosis of phagocytes. Mol Biol Cell 24, 1700-1712, S1-S7.
9. Botelho RJ, Teruel M, Dierckman R, Anderson R, Wells A, York JD, Meyer T, Grinstein S (2000). Localized biphasic changes in phosphatidylinositol-4, 5-bisphosphate at sites of phagocytosis. J Cell Biol 151, 1353-1368.
10. Boura E, Nencka R (2015). Phosphatidylinositol 4-kinases: function, structure, and inhibition. Exp Cell Res 337, 136-145.
11. Brombacher E, Urwyler S, Ragaz C, Weber SS, Kami K, Overduin M, Hilbi H (2009). Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J Biol Chem 284, 4846-4856.
12. Cantalupo G, Alifano P, Roberti V, Bruni CB, Bucci C (2001). Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J 20, 683-693.
13. Charpentier TH, Waldo GL, Barrett MO, Huang W, Zhang Q, Harden TK, Sondek J (2014). Membrane-induced allosteric control of phospholipase C-β isozymes. J Biol Chem 289, 29545-29557.
14. Chung J, Nakatsu F, Baskin JM, De Camilli P (2015). Plasticity of PI4KIIIα interactions at the plasma membrane. EMBO Rep 16, 312-320.
15. Cox D, Tseng CC, Bjekic G, Greenberg S (1999). A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J Biol Chem 274, 1240-1247.
16. Downey GP, Botelho RJ, Butler JR, Moltyaner Y, Chien P, Schreiber AD, Grinstein S (1999). Phagosomal maturation, acidification, and inhibition of bacterial growth in nonphagocytic cells transfected with FcgammaRIIA receptors. J Biol Chem 274, 28436-28444.
17. Elliott MR, Ravichandran KS (2010). Clearance of apoptotic cells: implications in health and disease. J Cell Biol 189, 1059-1070.
18. Fairn GD, Grinstein S (2012). How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33, 397-405.
19. Fairn GD, Ogata K, Botelho RJ, Stahl PD, Anderson RA, De Camilli P, Meyer T, Wodak S, Grinstein S (2009). An electrostatic switch displaces phosphatidylinositol phosphate kinases from the membrane during phagocytosis. J Cell Biol 187, 701-714.
20. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA (1999). ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4, 5)P2 on the Golgi complex. Nat Cell Biol 1, 280-287.
21. Graham TR, Burd CG (2011). Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 21, 113-121.
22. Hammond GRV, Fischer MJ, Anderson KE, Holdich J, Koteci A, Balla T, Irvine RF (2012). PI4P and PI(4, 5)P2 are essential but independent lipid determinants of membrane identity. Science 337, 727-730.
23. Hammond GRV, Machner MP, Balla T (2014). A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J Cell Biol 205, 113-126.
24. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S (2003). Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 23, 6494-6506.
25. Hsu F, Hu F, Mao Y (2015). Spatiotemporal control of phosphatidylinositol 4-phosphate by Sac2 regulates endocytic recycling. J Cell Biol 209, 97-110.
26. Indik Z, Kelly C, Chien P, Levinson AI, Schreiber AD (1991). Human Fc gamma RII, in the absence of other Fc gamma receptors, mediates a phagocytic signal. J Clin Invest 88, 1766-1771.
27. Jeschke A, Zehethofer N, Lindner B, Krupp J, Schwudke D, Haneburger I, Jovic M, Backer JM, Balla T, Hilbi H, Haas A (2015). Phosphatidylinositol 4-phosphate and phosphatidylinositol 3-phosphate regulate phagolysosome biogenesis. Proc Natl Acad Sci USA 112, 4636-4641.
28. Johansson M, Lehto M, Tanhuanpää K, Cover TL, Olkkonen VM (2005). The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol Biol Cell 16, 5480-5492.
29. Johansson M, Rocha N, Zwart W, Jordens I, Janssen L, Kuijl C, Olkkonen VM, Neefjes J (2007). Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J Cell Biol 176, 459-471.
30. Jovi'c M, Kean MJ, Szentpetery Z, Polevoy G, Gingras A-C, Brill JA, Balla T (2012). Two phosphatidylinositol 4-kinases control lysosomal delivery of the Gaucher disease enzyme, β-glucocerebrosidase. Mol Biol Cell 23, 1533-1545.
31. Ketel K, Krauss M, Nicot A-S, Puchkov D, Wieffer M, Müller R, Subramanian D, Schultz C, Laporte J, Haucke V (2016). A phosphoinositide conversion mechanism for exit from endosomes. Nature 529, 408-412.
32. Levin R, Grinstein S, Canton J (2016). The life cycle of phagosomes: formation, maturation, and resolution. Immunol Rev 273, 156-179.
33. Levin R, Grinstein S, Schlam D (2015). Phosphoinositides in phagocytosis and macropinocytosis. Biochim Biophys Acta 1851, 805-823.
34. Liao F, Shin HS, Rhee SG (1992). Tyrosine phosphorylation of phospholipase C-gamma 1 induced by cross-linking of the high-affinity or low-affinity Fc receptor for IgG in U937 cells. Proc Natl Acad Sci USA 89, 3659-3663.
35. Lorenzo O, Urbé S, Clague MJ (2006). Systematic analysis of myotubularins: heteromeric interactions, subcellular localisation and endosome related functions. J Cell Sci 119, 2953-2959.
36. Marshall JG, Booth JW, Stambolic V, Mak T, Balla T, Schreiber AD, Meyer T, Grinstein S (2001). Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis. J Cell Biol 153, 1369-1380.
37. Minogue S, Chu KME, Westover EJ, Covey DF, Hsuan JJ, Waugh MG (2010). Relationship between phosphatidylinositol 4-phosphate synthesis, membrane organization, and lateral diffusion of PI4KIIalpha at the trans-Golgi network. J Lipid Res 51, 2314-2324.
38. Nakatsu F, Baskin JM, Chung J, Tanner LB, Shui G, Lee SY, Pirruccello M, Hao M, Ingolia NT, Wenk MR, De Camilli P (2012). PtdIns4P synthesis by PI4KIIIα at the plasma membrane and its impact on plasma membrane identity. J Cell Biol 199, 1003-1016.
39. Nakatsu F, Messa M, Nández R, Czapla H, Zou Y, Strittmatter SM, De Camilli P (2015). Sac2/INPP5F is an inositol 4-phosphatase that functions in the endocytic pathway. J Cell Biol 209, 85-95.
40. Ostrowski PP, Fairn GD, Grinstein S, Johnson DE (2016). Cresyl violet: a superior fluorescent lysosomal marker. Traffic 17, 1313- 1321.
41. Salazar G, Craige B, Wainer BH, Guo J, De Camilli P, Faundez V (2005). Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol Biol Cell 16, 3692-3704.
42. Scott CC, Dobson W, Botelho RJ, Coady-Osberg N, Chavrier P, Knecht DA, Heath C, Stahl P, Grinstein S (2005). Phosphatidylinositol-4, 5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J Cell Biol 169, 139-149.
43. Shindo M, Irie K, Masuda A, Ohigashi H, Shirai Y, Miyasaka K, Saito N (2003). Synthesis and phorbol ester binding of the cysteine-rich domains of diacylglycerol kinase (DGK) isozymes. DGKgamma and DGKbeta are new targets of tumor-promoting phorbol esters. J Biol Chem 278, 18448-18454.
44. Sicart A, Katan M, Egea G, Sarri E (2015). PLCγ1 participates in protein transport and diacylglycerol production triggered by cargo arrival at the Golgi. Traffic 16, 250-266.
45. Stauffer TP, Ahn S, Meyer T (1998). Receptor-induced transient reduction in plasma membrane PtdIns(4, 5)P2 concentration monitored in living cells. Curr Biol 8, 343-346.
46. Swanson JA (2014). Phosphoinositides and engulfment. Cell Microbiol 16, 1473-1483.
47. Szentpetery Z, Várnai P, Balla T (2010). Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc Natl Acad Sci USA 107, 8225-8230.
48. Tsujita K, Itoh T, Ijuin T, Yamamoto A, Shisheva A, Laporte J, Takenawa T (2004). Myotubularin regulates the function of the late endosome through the gram domain-phosphatidylinositol 3, 5-bisphosphate interaction. J Biol Chem 279, 13817-13824.
49. Vieira OV, Botelho RJ, Rameh L, Brachmann SM, Matsuo T, Davidson HW, Schreiber A, Backer JM, Cantley LC, Grinstein S (2001). Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol 155, 19-25.
50. Vieira OV, Bucci C, Harrison RE, Trimble WS, Lanzetti L, Gruenberg J, Schreiber AD, Stahl PD, Grinstein S (2003). Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol Cell Biol 23, 2501-2514.
51. Wang H, Sun H-Q, Zhu X, Zhang L, Albanesi J, Levine B, Yin H (2015). GABARAPs regulate PI4P-dependent autophagosome:lysosome fusion. Proc Natl Acad Sci USA 112, 7015-7020.
52. Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL (2003). Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299-310.
53. Wu X, Chi RJ, Baskin JM, Lucast L, Burd CG, De Camilli P, Reinisch KM (2014). Structural insights into assembly and regulation of the plasma membrane phosphatidylinositol 4-kinase complex. Dev Cell 28, 19-29.
54. Zhang L, Malik S, Pang J, Wang H, Park KM, Yule DI, Blaxall BC, Smrcka AV (2013). Phospholipase Cϵ hydrolyzes perinuclear phosphatidylinositol 4-phosphate to regulate cardiac hypertrophy. Cell 153, 216-227.