Phosphoinositides in phagocytosis and macropinocytosis

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 6, 2015, Pages 805-823

  Levin, Roni ^a   Grinstein, Sergio ^a,b   Schlam, Daniel ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

Bacterial pathogen; Fc receptor; Macrophage; Macropinocytosis; Phagocytosis; Phosphoinositide

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CELL SURFACE RECEPTOR; GLYCEROPHOSPHOLIPID; IMMUNOGLOBULIN G; PATTERN RECOGNITION RECEPTOR; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,5 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RAB PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; WORTMANNIN; FC RECEPTOR; OPSONIN; PHOSPHATIDYLINOSITOL;

ARTICLE; BACTERIA; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL FUNCTION; CELL MATURATION; CELL MEMBRANE; ENDOSOME; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYME SPECIFICITY; HOST CELL; HUMAN; INTERNALIZATION; LYSOSOME; MAMMAL CELL; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPSONIZATION; PARTICLE SIZE; PHAGOCYTE; PHAGOCYTOSIS; PHAGOLYSOSOME; PHAGOSOME; PHOSPHOLIPID SYNTHESIS; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; BACTERIUM; CELLULAR IMMUNITY; GENE EXPRESSION REGULATION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS);

BACTERIA; GENE EXPRESSION REGULATION; HUMANS; IMMUNE EVASION; IMMUNITY, CELLULAR; MACROPHAGES; OPSONIN PROTEINS; PHAGOCYTOSIS; PHAGOSOMES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOLS; PINOCYTOSIS; RECEPTORS, IGG; SIGNAL TRANSDUCTION;

EID: 84925665455     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.09.005     Document Type: Review

References (196)

1. M. Bohdanowicz, D. Schlam, M. Hermansson, D. Rizzuti, G.D. Fairn, and T. Ueyama et al. Phosphatidic acid is required for the constitutive ruffling and macropinocytosis of phagocytes Mol. Biol. Cell 2013 10.1091/mbc.E12-11-0789
2. R.S. Flannagan, R.E. Harrison, C.M. Yip, K. Jaqaman, and S. Grinstein Dynamic macrophage "probing" is required for the efficient capture of phagocytic targets J. Cell Biol. 191 2010 1205 1218 10.1083/jcb.201007056
3. M.A. West, A.R. Prescott, E.L. Eskelinen, A.J. Ridley, and C. Watts Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation Curr. Biol. 10 2000 839 848
4. P. Beemiller, Y. Zhang, S. Mohan, E. Levinsohn, I. Gaeta, and A.D. Hoppe et al. A Cdc42 activation cycle coordinated by PI 3-kinase during Fc receptor-mediated phagocytosis Mol. Biol. Cell 21 2010 470 480 10.1091/mbc.E08-05-0494
5. N. Araki, M.T. Johnson, and J.A. Swanson A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages J. Cell Biol. 135 1996 1249 1260
6. O.V. Vieira, R.J. Botelho, and S. Grinstein Phagosome maturation: aging gracefully Biochem. J. 366 2002 689 704 10.1042/BJ20020691
7. G. Di Paolo, and P. De Camilli Phosphoinositides in cell regulation and membrane dynamics Nature 443 2006 651 657 10.1038/nature05185
8. T.G. Kutateladze Translation of the phosphoinositide code by PI effectors Nat. Chem. Biol. 6 2010 507 513 10.1038/nchembio.390
9. A. Simonsen, A.E. Wurmser, S.D. Emr, and H. Stenmark The role of phosphoinositides in membrane transport Curr. Opin. Cell Biol. 13 2001 485 492
10. H. Ham, A. Sreelatha, and K. Orth Manipulation of host membranes by bacterial effectors Nat. Rev. Microbiol. 9 2011 10.1038/nrmicro2602
11. S. Grinstein Phagocytosis here and now Traffic Cph. Den. 13 2012 1041 10.1111/j.1600-0854.2012.01383.x
12. R.S. Flannagan, V. Jaumouillé, and S. Grinstein The cell biology of phagocytosis Annu. Rev. Pathol. 7 2012 61 98 10.1146/annurev-pathol-011811-132445
13. R.J. Botelho, C.C. Scott, and S. Grinstein Phosphoinositide involvement in phagocytosis and phagosome maturation Curr. Top. Microbiol. Immunol. 282 2004 1 30
14. A.D. Hoppe, and J.A. Swanson Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis Mol. Biol. Cell 15 2004 3509 3519 10.1091/mbc.E03-11-0847
15. K.S. Ravichandran Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums J. Exp. Med. 207 2010 1807 1817 10.1084/jem.20101157
16. P.M. Henson, and D.A. Hume Apoptotic cell removal in development and tissue homeostasis Trends Immunol. 27 2006 244 250 10.1016/j.it.2006.03.005
17. S. Nagata, R. Hanayama, and K. Kawane Autoimmunity and the clearance of dead cells Cell 140 2010 619 630 10.1016/j.cell.2010.02.014
18. J. Savill, and V. Fadok Corpse clearance defines the meaning of cell death Nature 407 2000 784 788 10.1038/35037722
19. D.H. Jones, J. Nusbacher, and C.L. Anderson Fc receptor-mediated binding and endocytosis by human mononuclear phagocytes: monomeric IgG is not endocytosed by U937 cells and monocytes J. Cell Biol. 100 1985 558 564
20. S. Ghazizadeh, J.B. Bolen, and H.B. Fleit Physical and functional association of Src-related protein tyrosine kinases with Fc gamma RII in monocytic THP-1 cells J. Biol. Chem. 269 1994 8878 8884
21. S. Carréno, E. Caron, C. Cougoule, L.J. Emorine, and I. Maridonneau-Parini p59Hck isoform induces F-actin reorganization to form protrusions of the plasma membrane in a Cdc42- and Rac-dependent manner J. Biol. Chem. 277 2002 21007 21016 10.1074/jbc.M201212200
22. A.V. Wang, P.R. Scholl, and R.S. Geha Physical and functional association of the high affinity immunoglobulin G receptor (Fc gamma RI) with the kinases Hck and Lyn J. Exp. Med. 180 1994 1165 1170
23. I. Ibarrola, P.J. Vossebeld, C.H. Homburg, M. Thelen, D. Roos, and A.J. Verhoeven Influence of tyrosine phosphorylation on protein interaction with FcgammaRIIa Biochim. Biophys. Acta 1357 1997 348 358
24. S. Greenberg, P. Chang, D.C. Wang, R. Xavier, and B. Seed Clustered SYK tyrosine kinase domains trigger phagocytosis Proc. Natl. Acad. Sci. U. S. A. 93 1996 1103 1107
25. H. Gu, R.J. Botelho, M. Yu, S. Grinstein, and B.G. Neel Critical role for scaffolding adapter Gab2 in Fc gamma R-mediated phagocytosis J. Cell Biol. 161 2003 1151 1161 10.1083/jcb.200212158
26. S. Tridandapani, T.W. Lyden, J.L. Smith, J.E. Carter, K.M. Coggeshall, and C.L. Anderson The adapter protein LAT enhances fcgamma receptor-mediated signal transduction in myeloid cells J. Biol. Chem. 275 2000 20480 20487 10.1074/jbc.M909462199
27. R.J. Botelho, M. Teruel, R. Dierckman, R. Anderson, A. Wells, and J.D. York et al. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis J. Cell Biol. 151 2000 1353 1368
28. J. Saarikangas, H. Zhao, and P. Lappalainen Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides Physiol. Rev. 90 2010 259 289 10.1152/physrev.00036.2009
29. R. Rohatgi, P. Nollau, H.Y. Ho, M.W. Kirschner, and B.J. Mayer Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway J. Biol. Chem. 276 2001 26448 26452 10.1074/jbc.M103856200
30. R. Rohatgi, H.Y. Ho, and M.W. Kirschner Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate J. Cell Biol. 150 2000 1299 1310
31. R.C. May, E. Caron, A. Hall, and L.M. Machesky Involvement of the Arp2/3 complex in phagocytosis mediated by FcgammaR or CR3 Nat. Cell Biol. 2 2000 246 248 10.1038/35008673
32. H. Park, and D. Cox Cdc42 regulates Fc gamma receptor-mediated phagocytosis through the activation and phosphorylation of Wiskott-Aldrich syndrome protein (WASP) and neural-WASP Mol. Biol. Cell 20 2009 4500 4508 10.1091/mbc.E09-03-0230
33. E. Caron, and A. Hall Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases Science 282 1998 1717 1721
34. A.L.Y. Koh, C.X. Sun, F. Zhu, and M. Glogauer The role of Rac1 and Rac2 in bacterial killing Cell. Immunol. 235 2005 92 97 10.1016/j.cellimm.2005.07.005
35. J.A. Swanson, M.T. Johnson, K. Beningo, P. Post, M. Mooseker, and N. Araki A contractile activity that closes phagosomes in macrophages J. Cell Sci. 112 Pt 3 1999 307 316
36. D. Cox, J.S. Berg, M. Cammer, J.O. Chinegwundoh, B.M. Dale, and R.E. Cheney et al. Myosin X is a downstream effector of PI(3)K during phagocytosis Nat. Cell Biol. 4 2002 469 477 10.1038/ncb805
37. S.J. Isakoff, T. Cardozo, J. Andreev, Z. Li, K.M. Ferguson, and R. Abagyan et al. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast EMBO J. 17 1998 5374 5387 10.1093/emboj/17.18.5374
38. A. Savina, and S. Amigorena Phagocytosis and antigen presentation in dendritic cells Immunol. Rev. 219 2007 143 156 10.1111/j.1600-065X.2007.00552.x
39. P.R. Scholl, D. Ahern, and R.S. Geha Protein tyrosine phosphorylation nduced via the IgG receptors Fc gamma Ri and Fc gamma RII in the human monocytic cell line THP-1 J. Immunol. Baltim. Md 1950 149 1992 1751 1757
40. L.S. Mayorga, F. Bertini, and P.D. Stahl Fusion of newly formed phagosomes with endosomes in intact cells and in a cell-free system J. Biol. Chem. 266 1991 6511 6517
41. M. Desjardins, N.N. Nzala, R. Corsini, and C. Rondeau Maturation of phagosomes is accompanied by changes in their fusion properties and size-selective acquisition of solute materials from endosomes J. Cell Sci. 110 Pt 18 1997 2303 2314
42. R.S. Flannagan, G. Cosío, and S. Grinstein Antimicrobial mechanisms of phagocytes and bacterial evasion strategies Nat. Rev. Microbiol. 7 2009 355 366 10.1038/nrmicro2128
43. J.M. Kinchen, and K.S. Ravichandran Phagosome maturation: going through the acid test Nat. Rev. Mol. Cell Biol. 9 2008 781 795 10.1038/nrm2515
44. C. Bucci, R.G. Parton, I.H. Mather, H. Stunnenberg, K. Simons, and B. Hoflack et al. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway Cell 70 1992 715 728
45. M. Kitano, M. Nakaya, T. Nakamura, S. Nagata, and M. Matsuda Imaging of Rab5 activity identifies essential regulators for phagosome maturation Nature 453 2008 241 245 10.1038/nature06857
46. O.V. Vieira, C. Bucci, R.E. Harrison, W.S. Trimble, L. Lanzetti, and J. Gruenberg et al. Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase Mol. Cell. Biol. 23 2003 2501 2514 10.1128/MCB.23.7.2501-2514.2003
47. O.J. Driskell, A. Mironov, V.J. Allan, and P.G. Woodman Dynein is required for receptor sorting and the morphogenesis of early endosomes Nat. Cell Biol. 9 2007 113 120 10.1038/ncb1525
48. D. Cox, D.J. Lee, B.M. Dale, J. Calafat, and S. Greenberg A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis Proc. Natl. Acad. Sci. U. S. A. 97 2000 680 685
49. M.T. Damiani, M. Pavarotti, N. Leiva, A.J. Lindsay, M.W. McCaffrey, and M.I. Colombo Rab coupling protein associates with phagosomes and regulates recycling from the phagosomal compartment Traffic Cph. Den. 5 2004 785 797 10.1111/j.1600-0854.2004.00220.x
50. K.M. Lucin, C.E. O'Brien, G. Bieri, E. Czirr, K.I. Mosher, and R.J. Abbey et al. Microglial Beclin 1 regulates retromer trafficking and phagocytosis and is impaired in Alzheimer's disease Neuron 79 2013 873 886 10.1016/j.neuron.2013.06.046
51. W.L. Lee, M.-K. Kim, A.D. Schreiber, and S. Grinstein Role of ubiquitin and proteasomes in phagosome maturation Mol. Biol. Cell 16 2005 2077 2090 10.1091/mbc.E04-06-0464
52. T. Wollert, and J.H. Hurley Molecular mechanism of multivesicular body biogenesis by ESCRT complexes Nature 464 2010 864 869 10.1038/nature08849
53. T. Muzioł, E. Pineda-Molina, R.B. Ravelli, A. Zamborlini, Y. Usami, and H. Göttlinger et al. Structural basis for budding by the ESCRT-III factor CHMP3 Dev. Cell 10 2006 821 830 10.1016/j.devcel.2006.03.013
54. M. Desjardins, L.A. Huber, R.G. Parton, and G. Griffiths Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus J. Cell Biol. 124 1994 677 688
55. R.E. Harrison, C. Bucci, O.V. Vieira, T.A. Schroer, and S. Grinstein Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP Mol. Cell. Biol. 23 2003 6494 6506 10.1128/MCB.23.18.6494-6506.2003
56. M. Johansson, N. Rocha, W. Zwart, I. Jordens, L. Janssen, and C. Kuijl et al. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin J. Cell Biol. 176 2007 459 471 10.1083/jcb.200606077
57. R. Rojas, T. van Vlijmen, G.A. Mardones, Y. Prabhu, A.L. Rojas, and S. Mohammed et al. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7 J. Cell Biol. 183 2008 513 526 10.1083/jcb.200804048
58. D.M. Ward, J. Pevsner, M.A. Scullion, M. Vaughn, and J. Kaplan Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages Mol. Biol. Cell 11 2000 2327 2333
59. R.F. Collins, A.D. Schreiber, S. Grinstein, and W.S. Trimble Syntaxins 13 and 7 function at distinct steps during phagocytosis J. Immunol. 169 2002 3250 3256 10.4049/jimmunol.169.6.3250
60. G. Griffiths, B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld The mannose 6-phosphate receptor and the biogenesis of lysosomes Cell 52 1988 329 341
61. L.R. Carraro-Lacroix, V. Jaumouillé, G.D. Fairn, and S. Grinstein A weak base-generating system suitable for selective manipulation of lysosomal pH Traffic Cph. Den. 12 2011 1490 1500 10.1111/j.1600-0854.2011.01266.x
62. K.K. Huynh, and S. Grinstein Regulation of vacuolar pH and its modulation by some microbial species Microbiol. Mol. Biol. Rev. 71 2007 452 462 10.1128/MMBR.00003-07
63. B. Turk, I. Dolenc, V. Turk, and J.G. Bieth Kinetics of the pH-induced inactivation of human cathepsin L Biochem. Mosc. 32 1993 375 380
64. N. Jabado, A. Jankowski, S. Dougaparsad, V. Picard, S. Grinstein, and P. Gros Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane J. Exp. Med. 192 2000 1237 1248
65. A.H. Gordon, P.D. Hart, and M.R. Young Ammonia inhibits phagosome-lysosome fusion in macrophages Nature 286 1980 79 80
66. P.L. Masson, J.F. Heremans, and E. Schonne Lactoferrin, an iron-binding protein in neutrophilic leukocytes J. Exp. Med. 130 1969 643 658
67. M. Zanetti Cathelicidins, multifunctional peptides of the innate immunity J. Leukoc. Biol. 75 2004 39 48 10.1189/jlb.0403147
68. T. Ganz Defensins: antimicrobial peptides of innate immunity Nat. Rev. Immunol. 3 2003 710 720 10.1038/nri1180
69. C.S. Pillay, E. Elliott, and C. Dennison Endolysosomal proteolysis and its regulation Biochem. J. 363 2002 417 429
70. S. McLaughlin, and D. Murray Plasma membrane phosphoinositide organization by protein electrostatics Nature 438 2005 605 611 10.1038/nature04398
71. A. Godi, P. Pertile, R. Meyers, P. Marra, G.D. Tullio, and C. Iurisci et al. ARF mediates recruitment of PtdIns-4-OH kinase-β and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex Nat. Cell Biol. 1 1999 280 287 10.1038/12993
72. M.P. Czech PIP2 and PIP3: complex roles at the cell surface Cell 100 2000 603 606 10.1016/S0092-8674(00)80696-0
73. M. Bohdanowicz, and S. Grinstein Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis Physiol. Rev. 93 2013 69 106 10.1152/physrev.00002.2012
74. S. Mondal, S. Ghosh-Roy, F. Loison, Y. Li, Y. Jia, and C. Harris et al. PTEN negatively regulates engulfment of apoptotic cells by modulating activation of Rac GTPase J. Immunol. Baltim. Md 1950 187 2011 5783 5794 10.4049/jimmunol.1100484
75. F.D. Brown, A.L. Rozelle, H.L. Yin, T. Balla, and J.G. Donaldson Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic J. Cell Biol. 154 2001 1007 1017 10.1083/jcb.200103107
76. 2 Biochem. J. 422 2009 23 35 10.1042/BJ20090428
77. G.D. Fairn, K. Ogata, R.J. Botelho, P.D. Stahl, R.A. Anderson, and P. De Camilli et al. An electrostatic switch displaces phosphatidylinositol phosphate kinases from the membrane during phagocytosis J. Cell Biol. 187 2009 701 714 10.1083/jcb.200909025
78. P.A.O. Weernink, K. Meletiadis, S. Hommeltenberg, M. Hinz, H. Ishihara, and M. Schmidt et al. Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42 J. Biol. Chem. 279 2004 7840 7849 10.1074/jbc.M312737200
79. K.F. Tolias, L.C. Cantley, and C.L. Carpenter Rho family GTPases bind to phosphoinositide kinases J. Biol. Chem. 270 1995 17656 17659
80. K.F. Tolias, J.H. Hartwig, H. Ishihara, Y. Shibasaki, L.C. Cantley, and C.L. Carpenter Type Ialpha phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly Curr. Biol. 10 2000 153 156
81. A. Honda, M. Nogami, T. Yokozeki, M. Yamazaki, H. Nakamura, and H. Watanabe et al. Phosphatidylinositol 4-phosphate 5-kinase α is a downstream effector of the small g protein arf6 in membrane ruffle formation Cell 99 1999 521 532 10.1016/S0092-8674(00)81540-8
82. N. Divecha, M. Roefs, J.R. Halstead, S. D'Andrea, M. Fernandez-Borga, and L. Oomen et al. Interaction of the type Ialpha PIPkinase with phospholipase D: a role for the local generation of phosphatidylinositol 4, 5-bisphosphate in the regulation of PLD2 activity EMBO J. 19 2000 5440 5449 10.1093/emboj/19.20.5440
83. Z.B. Mehta, G. Pietka, and M. Lowe The cellular and physiological functions of the Lowe syndrome protein OCRL1 Traffic Cph. Den. 15 2014 471 487 10.1111/tra.12160
84. M. Bohdanowicz, D.M. Balkin, P. De Camilli, and S. Grinstein Recruitment of OCRL and Inpp5B to phagosomes by Rab5 and APPL1 depletes phosphoinositides and attenuates Akt signaling Mol. Biol. Cell 23 2012 176 187 10.1091/mbc.E11-06-0489
85. S.V. Voronov, S.G. Frere, S. Giovedi, E.A. Pollina, C. Borel, and H. Zhang et al. Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down's syndrome Proc. Natl. Acad. Sci. U. S. A. 105 2008 9415 9420 10.1073/pnas.0803756105
86. V. Jaumouillé, and S. Grinstein Receptor mobility, the cytoskeleton, and particle binding during phagocytosis Curr. Opin. Cell Biol. 23 2011 22 29 10.1016/j.ceb.2010.10.006
87. V. Martel, C. Racaud-Sultan, S. Dupe, C. Marie, F. Paulhe, and A. Galmiche et al. Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides J. Biol. Chem. 276 2001 21217 21227 10.1074/jbc.M102373200
88. G.D. Paolo, H.S. Moskowitz, K. Gipson, M.R. Wenk, S. Voronov, and M. Obayashi et al. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking Nature 431 2004 415 422 10.1038/nature02896
89. K. Hamada, T. Shimizu, T. Matsui, S. Tsukita, and T. Hakoshima Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain EMBO J. 19 2000 4449 4462 10.1093/emboj/19.17.4449
90. B.-C. Suh, and B. Hille Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate Curr. Opin. Neurobiol. 15 2005 370 378 10.1016/j.conb.2005.05.005
91. Y. Lee, S.-M. Song, H.S. Park, S. Kim, E.-H. Koh, and M.S. Choi et al. Elevation of oleate-activated phospholipase D activity during thymic atrophy Immunology 107 2002 435 443
92. S.S. Iyer, J.A. Barton, S. Bourgoin, and D.J. Kusner Phospholipases D1 and D2 coordinately regulate macrophage phagocytosis J. Immunol. Baltim. Md 1950 173 2004 2615 2623
93. D.J. Kusner, C.F. Hall, and S. Jackson Fc gamma receptor-mediated activation of phospholipase D regulates macrophage phagocytosis of IgG-opsonized particles J. Immunol. Baltim. Md 1950 162 1999 2266 2274
94. M. Falasca, S.K. Logan, V.P. Lehto, G. Baccante, M.A. Lemmon, and J. Schlessinger Activation of phospholipase Cγ by PI 3-kinase-induced PH domain-mediated membrane targeting EMBO J. 17 1998 414 422 10.1093/emboj/17.2.414
95. L. Azzoni, M. Kamoun, T.W. Salcedo, P. Kanakaraj, and B. Perussia Stimulation of Fc gamma RIIIA results in phospholipase C-gamma 1 tyrosine phosphorylation and p56lck activation J. Exp. Med. 176 1992 1745 1750
96. F. Liao, H.S. Shin, and S.G. Rhee 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. U. S. A. 89 1992 3659 3663
97. T. Yeung, M. Terebiznik, L. Yu, J. Silvius, W.M. Abidi, and M. Philips et al. Receptor activation alters inner surface potential during phagocytosis Science 313 2006 347 351 10.1126/science.1129551
98. A. Chaudhary, J. Chen, Q.M. Gu, W. Witke, D.J. Kwiatkowski, and G.D. Prestwich Probing the phosphoinositide 4,5-bisphosphate binding site of human profilin I Chem. Biol. 5 1998 273 281
99. V.Y. Gorbatyuk, N.J. Nosworthy, S.A. Robson, N.P.S. Bains, M.W. Maciejewski, and C.G. Dos Remedios et al. Mapping the phosphoinositide-binding site on chick cofilin explains how PIP2 regulates the cofilin-actin interaction Mol. Cell 24 2006 511 522 10.1016/j.molcel.2006.10.007
100. P.A. Janmey, and T.P. Stossel Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate Nature 325 1987 362 364 10.1038/325362a0
101. J.A. Cooper, and D. Sept New insights into mechanism and regulation of actin capping protein Int. Rev. Cell Mol. Biol. 267 2008 183 206 10.1016/S1937-6448(08)00604-7
102. H. Miki, K. Miura, and T. Takenawa N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases EMBO J. 15 1996 5326 5335
103. A. Bretscher, K. Edwards, and R.G. Fehon ERM proteins and merlin: integrators at the cell cortex Nat. Rev. Mol. Cell Biol. 3 2002 586 599 10.1038/nrm882
104. M.G. Coppolino, R. Dierckman, J. Loijens, R.F. Collins, M. Pouladi, and J. Jongstra-Bilen et al. Inhibition of phosphatidylinositol-4-phosphate 5-kinase Iα impairs localized actin remodeling and suppresses phagocytosis J. Biol. Chem. 277 2002 43849 43857 10.1074/jbc.M209046200
105. Y.S. Mao, M. Yamaga, X. Zhu, Y. Wei, H.-Q. Sun, and J. Wang et al. Essential and unique roles of PIP5K-gamma and -alpha in Fcgamma receptor-mediated phagocytosis J. Cell Biol. 184 2009 281 296 10.1083/jcb.200806121
106. C.C. Scott, W. Dobson, R.J. Botelho, N. Coady-Osberg, P. Chavrier, and D.A. Knecht et al. Phosphatidylinositol-4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis J. Cell Biol. 169 2005 139 149 10.1083/jcb.200412162
107. D. Cox, C.-C. Tseng, G. Bjekic, and S. Greenberg A requirement for phosphatidylinositol 3-kinase in pseudopod extension J. Biol. Chem. 274 1999 1240 1247 10.1074/jbc.274.3.1240
108. E. Oancea, M.N. Teruel, A.F. Quest, and T. Meyer Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells J. Cell Biol. 140 1998 485 498
109. T. Ueyama, M.R. Lennartz, Y. Noda, T. Kobayashi, Y. Shirai, and K. Rikitake et al. Superoxide production at phagosomal cup/phagosome through βI protein kinase C during FcγR-mediated phagocytosis in microglia J. Immunol. 173 2004 4582 4589
110. D. Schlam, M. Bohdanowicz, A. Chatgilialoglu, A. Chatilialoglu, B.E. Steinberg, and T. Ueyama et al. Diacylglycerol kinases terminate diacylglycerol signaling during the respiratory burst leading to heterogeneous phagosomal NADPH oxidase activation J. Biol. Chem. 288 2013 23090 23104 10.1074/jbc.M113.457606
111. 2 + hotspots that boost phagocytosis Curr. Biol. 22 2012 1990 1997 10.1016/j.cub.2012.08.049
112. T. Bengtsson, M.E. Jaconi, M. Gustafson, K.E. Magnusson, J.M. Theler, and D.P. Lew et al. Actin dynamics in human neutrophils during adhesion and phagocytosis is controlled by changes in intracellular free calcium Eur. J. Cell Biol. 62 1993 49 58
113. R. He, M. Nanamori, H. Sang, H. Yin, M.C. Dinauer, and R.D. Ye Reconstitution of chemotactic peptide-induced nicotinamide adenine dinucleotide phosphate (reduced) oxidase activation in transgenic COS-phox cells J. Immunol. Baltim. Md 1950 173 2004 7462 7470
114. N. Cheng, R. He, J. Tian, M.C. Dinauer, and R.D. Ye A critical role of protein kinase C delta activation loop phosphorylation in formyl-methionyl-leucyl-phenylalanine-induced phosphorylation of p47(phox) and rapid activation of nicotinamide adenine dinucleotide phosphate oxidase J. Immunol. Baltim. Md 1950 179 2007 7720 7728
115. P. Nunes, and N. Demaurex The role of calcium signaling in phagocytosis J. Leukoc. Biol. 88 2010 57 68 10.1189/jlb.0110028
116. M.E. Jaconi, D.P. Lew, J.L. Carpentier, K.E. Magnusson, M. Sjögren, and O. Stendahl Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils J. Cell Biol. 110 1990 1555 1564
117. H.M. Loovers, A. Kortholt, H. de Groote, L. Whitty, R.L. Nussbaum, and P.J.M. van Haastert Regulation of phagocytosis in Dictyostelium by the inositol 5-phosphatase OCRL homolog Dd5P4 Traffic Cph. Den. 8 2007 618 628 10.1111/j.1600-0854.2007.00546.x
118. S. Marion, J. Mazzolini, F. Herit, P. Bourdoncle, N. Kambou-Pene, and S. Hailfinger et al. The NF-κB signaling protein Bcl10 regulates actin dynamics by controlling AP1 and OCRL-bearing vesicles Dev. Cell 23 2012 954 967 10.1016/j.devcel.2012.09.021
119. F. Frischknecht, and M. Way Surfing pathogens and the lessons learned for actin polymerization Trends Cell Biol. 11 2001 30 38 10.1016/S0962-8924(00)01871-7
120. M.P. Sheetz Cell control by membrane-cytoskeleton adhesion Nat. Rev. Mol. Cell Biol. 2 2001 392 396 10.1038/35073095
121. M.R. Terebiznik, O.V. Vieira, S.L. Marcus, A. Slade, C.M. Yip, and W.S. Trimble et al. Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella Nat. Cell Biol. 4 2002 766 773 10.1038/ncb854
122. Y. Fu, and J.E. Galán A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion Nature 401 1999 293 297 10.1038/45829
123. M.A. Bakowski, V. Braun, G.Y. Lam, T. Yeung, W.D. Heo, and T. Meyer et al. The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole Cell Host Microbe 7 2010 453 462 10.1016/j.chom.2010.05.011
124. K. Niebuhr, N. Jouihri, A. Allaoui, P. Gounon, P.J. Sansonetti, and C. Parsot IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation Mol. Microbiol. 38 2000 8 19
125. C.A. Broberg, L. Zhang, H. Gonzalez, M.A. Laskowski-Arce, and K. Orth A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity Science 329 2010 1660 1662 10.1126/science.1192850
126. J. Viaud, F. Lagarrigue, D. Ramel, S. Allart, G. Chicanne, and L. Ceccato et al. Phosphatidylinositol 5-phosphate regulates invasion through binding and activation of Tiam1 Nat. Commun. 5 2014 4080 10.1038/ncomms5080
127. L.E. Rameh, and L.C. Cantley The role of phosphoinositide 3-kinase lipid products in cell function J. Biol. Chem. 274 1999 8347 8350
128. M. Palmieri, C.J. Nowell, M. Condron, J. Gardiner, A.B. Holmes, and J. Desai et al. Analysis of cellular phosphatidylinositol (3,4,5)-trisphosphate levels and distribution using confocal fluorescent microscopy Anal. Biochem. 406 2010 41 50 10.1016/j.ab.2010.06.033
129. B. Vanhaesebroeck, and M.D. Waterfield Signaling by distinct classes of phosphoinositide 3-kinases Exp. Cell Res. 253 1999 239 254 10.1006/excr.1999.4701
130. T. Maehama, and J.E. Dixon The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate J. Biol. Chem. 273 1998 13375 13378
131. H.J. McCrea, and P. De Camilli Mutations in phosphoinositide metabolizing enzymes and human disease Physiology Bethesda Md. 24 2009 8 16 10.1152/physiol.00035.2008
132. J.G. Marshall, J.W. Booth, V. Stambolic, T. Mak, T. Balla, and A.D. Schreiber et al. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis J. Cell Biol. 153 2001 1369 1380
133. K. Kwiatkowska, and A. Sobota Signaling pathways in phagocytosis BioEssays 21 1999 422 431 10.1002/(SICI)1521-1878(199905)21:5<422::AID-BIES9>3.0.CO;2-#
134. L.A. Kamen, J. Levinsohn, and J.A. Swanson Differential association of phosphatidylinositol 3-kinase, SHIP-1, and PTEN with forming phagosomes Mol. Biol. Cell 18 2007 2463 2472 10.1091/mbc.E07-01-0061
135. L. Bajno, X.R. Peng, A.D. Schreiber, H.P. Moore, W.S. Trimble, and S. Grinstein Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation J. Cell Biol. 149 2000 697 706
136. V. Braun, V. Fraisier, G. Raposo, I. Hurbain, J.-B. Sibarita, and P. Chavrier et al. TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages EMBO J. 23 2004 4166 4176 10.1038/sj.emboj.7600427
137. 2 + signalling in HL60 neutrophils J. Cell Sci. 119 2006 443 451 10.1242/jcs.02756
138. H. Sason, M. Milgrom, A.M. Weiss, N. Melamed-Book, T. Balla, and S. Grinstein et al. Enteropathogenic Escherichia coli subverts phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 3,4,5-trisphosphate upon epithelial cell infection Mol. Biol. Cell 20 2009 544 555 10.1091/mbc.E08-05-0516
139. X. Li, X. Wang, X. Zhang, M. Zhao, W.L. Tsang, and Y. Zhang et al. Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics Proc. Natl. Acad. Sci. U. S. A. 110 2013 21165 21170 10.1073/pnas.1311864110
140. M. Samie, X. Wang, X. Zhang, A. Goschka, X. Li, and X. Cheng et al. A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis Dev. Cell 26 2013 511 524 10.1016/j.devcel.2013.08.003
141. A.J. McCartney, Y. Zhang, and L.S. Weisman Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance BioEssays 36 2014 52 64 10.1002/bies.201300012
142. P. Berger, C. Schaffitzel, I. Berger, N. Ban, and U. Suter Membrane association of myotubularin-related protein 2 is mediated by a pleckstrin homology-GRAM domain and a coiled-coil dimerization module Proc. Natl. Acad. Sci. U. S. A. 100 2003 12177 12182 10.1073/pnas.2132732100
143. D.J. Gillooly, I.C. Morrow, M. Lindsay, R. Gould, N.J. Bryant, and J.M. Gaullier et al. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells EMBO J. 19 2000 4577 4588 10.1093/emboj/19.17.4577
144. L. Stephens, F.T. Cooke, R. Walters, T. Jackson, S. Volinia, and I. Gout et al. Characterization of a phosphatidylinositol-specific phosphoinositide 3-kinase from mammalian cells Curr. Biol. 4 1994 203 214
145. J.M. Backer The regulation and function of Class III PI3Ks: novel roles for Vps34 Biochem. J. 410 2008 1 17 10.1042/BJ20071427
146. Y. Yan, and J.M. Backer Regulation of class III (Vps34) PI3Ks Biochem. Soc. Trans. 35 2007 239 241 10.1042/BST0350239
147. O.V. Vieira, R.J. Botelho, L. Rameh, S.M. Brachmann, T. Matsuo, and H.W. Davidson et al. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation J. Cell Biol. 155 2001 19 26 10.1083/jcb.200107069
148. L.K. MacDougall, J. Domin, and M.D. Waterfield A family of phosphoinositide 3-kinases in Drosophila identifies a new mediator of signal transduction Curr. Biol. 5 1995 1404 1415
149. M. Ferron, and J. Vacher Characterization of the murine Inpp4b gene and identification of a novel isoform Gene 376 2006 152 161 10.1016/j.gene.2006.02.022
150. C.G. Burd, and S.D. Emr Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains Mol. Cell 2 1998 157 162
151. T.T. Ching, D.S. Wang, A.L. Hsu, P.J. Lu, and C.S. Chen Identification of multiple phosphoinositide-specific phospholipases D as new regulatory enzymes for phosphatidylinositol 3,4, 5-trisphosphate J. Biol. Chem. 274 1999 8611 8617
152. J.T. Murray, C. Panaretou, H. Stenmark, M. Miaczynska, and J.M. Backer Role of Rab5 in the recruitment of hVps34/p150 to the early endosome Traffic Cph. Den. 3 2002 416 427
153. M.-P. Stein, Y. Feng, K.L. Cooper, A.M. Welford, and A. Wandinger-Ness Human VPS34 and p150 are Rab7 interacting partners Traffic Cph. Den. 4 2003 754 771
154. M.A. Lemmon Phosphoinositide recognition domains Traffic 4 2003 201 213 10.1034/j.1600-0854.2004.00071.x
155. A. Simonsen, R. Lippé, S. Christoforidis, J.M. Gaullier, A. Brech, and J. Callaghan et al. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion Nature 394 1998 494 498 10.1038/28879
156. J. He, M. Vora, R.M. Haney, G.S. Filonov, C.A. Musselman, and C.G. Burd et al. Membrane insertion of the FYVE domain is modulated by pH Proteins 76 2009 852 860 10.1002/prot.22392
157. A. Mishra, S. Eathiraj, S. Corvera, and D.G. Lambright Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of early endosomal autoantigen 1 (EEA1) Proc. Natl. Acad. Sci. U. S. A. 107 2010 10866 10871 10.1073/pnas.1000843107
158. A. Simonsen, J.M. Gaullier, A. D'Arrigo, and H. Stenmark The Rab5 effector EEA1 interacts directly with syntaxin-6 J. Biol. Chem. 274 1999 28857 28860
159. R.A. Fratti, J.M. Backer, J. Gruenberg, S. Corvera, and V. Deretic Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest J. Cell Biol. 154 2001 631 644 10.1083/jcb.200106049
160. O.V. Vieira, R.E. Harrison, C.C. Scott, H. Stenmark, D. Alexander, and J. Liu et al. Acquisition of Hrs, an essential component of phagosomal maturation, is impaired by mycobacteria Mol. Cell. Biol. 24 2004 4593 4604
161. G.E. Cozier, J. Carlton, A.H. McGregor, P.A. Gleeson, R.D. Teasdale, and H. Mellor et al. The phox homology (PX) domain-dependent, 3-phosphoinositide-mediated association of sorting nexin-1 with an early sorting endosomal compartment is required for its ability to regulate epidermal growth factor receptor degradation J. Biol. Chem. 277 2002 48730 48736 10.1074/jbc.M206986200
162. P. Burda, S.M. Padilla, S. Sarkar, and S.D. Emr Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps34 PtdIns 3-kinase J. Cell Sci. 115 2002 3889 3900
163. S. Dupré-Crochet, M. Erard, and O. Nüße ROS production in phagocytes: why, when, and where? J. Leukoc. Biol. 94 2013 657 670 10.1189/jlb.1012544
164. K. Roepstorff, I. Rasmussen, M. Sawada, C. Cudre-Maroux, P. Salmon, and G. Bokoch et al. Stimulus-dependent regulation of the phagocyte NADPH oxidase by a VAV1, Rac1, and PAK1 signaling axis J. Biol. Chem. 283 2008 7983 7993 10.1074/jbc.M708281200
165. D.R. Ambruso, C. Knall, A.N. Abell, J. Panepinto, A. Kurkchubasche, and G. Thurman et al. Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation Proc. Natl. Acad. Sci. U. S. A. 97 2000 4654 4659 10.1073/pnas.080074897
166. P. Nunes, N. Demaurex, and M.C. Dinauer Regulation of the NADPH oxidase and associated ion fluxes during phagocytosis Traffic Cph. Den. 14 2013 1118 1131 10.1111/tra.12115
167. T. Ueyama, T. Tatsuno, T. Kawasaki, S. Tsujibe, Y. Shirai, and H. Sumimoto et al. A regulated adaptor function of p40phox: distinct p67phox membrane targeting by p40phox and by p47phox Mol. Biol. Cell 18 2007 441 454 10.1091/mbc.E06-08-0731
168. T. Ueyama, T. Kusakabe, S. Karasawa, T. Kawasaki, A. Shimizu, and J. Son et al. Sequential binding of cytosolic Phox complex to phagosomes through regulated adaptor proteins: evaluation using the novel monomeric Kusabira-Green system and live imaging of phagocytosis J. Immunol. Baltim. Md 1950 181 2008 629 640
169. W. Tian, X.J. Li, N.D. Stull, W. Ming, C.-I. Suh, and S.A. Bissonnette et al. Fc gamma R-stimulated activation of the NADPH oxidase: phosphoinositide-binding protein p40phox regulates NADPH oxidase activity after enzyme assembly on the phagosome Blood 112 2008 3867 3877 10.1182/blood-2007-11-126029
170. K. Pethe, D.L. Swenson, S. Alonso, J. Anderson, C. Wang, and D.G. Russell Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation Proc. Natl. Acad. Sci. U. S. A. 101 2004 13642 13647 10.1073/pnas.0401657101
171. 2 +/calmodulin-PI3K hVPS34 cascade J. Exp. Med. 198 2003 653 659 10.1084/jem.20030527
172. R.A. Fratti, J. Chua, I. Vergne, and V. Deretic Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest Proc. Natl. Acad. Sci. 100 2003 5437 5442 10.1073/pnas.0737613100
173. J.P. Lim, and P.A. Gleeson Macropinocytosis: an endocytic pathway for internalising large gulps Immunol. Cell Biol. 89 2011 836 843 10.1038/icb.2011.20
174. J.A. Swanson Shaping cups into phagosomes and macropinosomes Nat. Rev. Mol. Cell Biol. 9 2008 639 649 10.1038/nrm2447
175. C.C. Norbury, L.J. Hewlett, A.R. Prescott, N. Shastri, and C. Watts Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages Immunity 3 1995 783 791
176. F. Sallusto, M. Cella, C. Danieli, and A. Lanzavecchia Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products J. Exp. Med. 182 1995 389 400
177. J. Mercer, and A. Helenius Virus entry by macropinocytosis Nat. Cell Biol. 11 2009 510 520 10.1038/ncb0509-510
178. C. Commisso, S.M. Davidson, R.G. Soydaner-Azeloglu, S.J. Parker, J.J. Kamphorst, and S. Hackett et al. Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells Nature 497 2013 633 637 10.1038/nature12138
179. E.L. Racoosin, and J.A. Swanson Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages J. Exp. Med. 170 1989 1635 1648
180. D. Bar-Sagi, and J.R. Feramisco Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by Ras proteins Science 233 1986 1061 1068
181. J.A. Swanson Phorbol esters stimulate macropinocytosis and solute flow through macrophages J. Cell Sci. 94 Pt 1 1989 135 142
182. S. Futaki, I. Nakase, A. Tadokoro, T. Takeuchi, and A.T. Jones Arginine-rich peptides and their internalization mechanisms Biochem. Soc. Trans. 35 2007 784 787 10.1042/BST0350784
183. N. Araki, M. Hamasaki, Y. Egami, and T. Hatae Effect of 3-methyladenine on the fusion process of macropinosomes in EGF-stimulated A431 cells Cell Struct. Funct. 31 2006 145 157
184. N. Araki, Y. Egami, Y. Watanabe, and T. Hatae Phosphoinositide metabolism during membrane ruffling and macropinosome formation in EGF-stimulated A431 cells Exp. Cell Res. 313 2007 1496 1507 10.1016/j.yexcr.2007.02.012
185. S. Yoshida, A.D. Hoppe, N. Araki, and J.A. Swanson Sequential signaling in plasma-membrane domains during macropinosome formation in macrophages J. Cell Sci. 122 2009 3250 3261 10.1242/jcs.053207
186. T.P. Welliver, and J.A. Swanson A growth factor signaling cascade confined to circular ruffles in macrophages Biol. Open. 1 2012 754 760 10.1242/bio.20121784
187. M. Maekawa, S. Terasaka, Y. Mochizuki, K. Kawai, Y. Ikeda, and N. Araki et al. Sequential breakdown of 3-phosphorylated phosphoinositides is essential for the completion of macropinocytosis Proc. Natl. Acad. Sci. U. S. A. 111 2014 E978 E987 10.1073/pnas.1311029111
188. J. Hasegawa, E. Tokuda, T. Tenno, K. Tsujita, H. Sawai, and H. Hiroaki et al. SH3YL1 regulates dorsal ruffle formation by a novel phosphoinositide-binding domain J. Cell Biol. 193 2011 901 916 10.1083/jcb.201012161
189. L. Lanzetti, A. Palamidessi, L. Areces, G. Scita, and P.P. Di Fiore Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases Nature 429 2004 309 314 10.1038/nature02542
190. M.J. Clague, C. Thorpe, and A.T. Jones Phosphatidylinositol 3-kinase regulation of fluid phase endocytosis FEBS Lett. 367 1995 272 274
191. M. Amyere, B. Payrastre, U. Krause, P. Van Der Smissen, A. Veithen, and P.J. Courtoy Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C Mol. Biol. Cell 11 2000 3453 3467
192. S. Dowler, R.A. Currie, D.G. Campbell, M. Deak, G. Kular, and C.P. Downes et al. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities Biochem. J. 351 2000 19 31
193. S. Srivastava, P. Choudhury, Z. Li, G. Liu, V. Nadkarni, and K. Ko et al. Phosphatidylinositol 3-phosphate indirectly activates KCa3.1 via 14 amino acids in the carboxy terminus of KCa3.1 Mol. Biol. Cell 17 2006 146 154 10.1091/mbc.E05-08-0763
194. G. Morrot, S. Cribier, P.F. Devaux, D. Geldwerth, J. Davoust, and J.F. Bureau et al. Asymmetric lateral mobility of phospholipids in the human erythrocyte membrane Proc. Natl. Acad. Sci. U. S. A. 83 1986 6863 6867
195. U. Golebiewska, J.G. Kay, T. Masters, S. Grinstein, W. Im, and R.W. Pastor et al. Evidence for a fence that impedes the diffusion of phosphatidylinositol 4,5-bisphosphate out of the forming phagosomes of macrophages Mol. Biol. Cell 22 2011 3498 3507 10.1091/mbc.E11-02-0114
196. T.P. Welliver, S.L. Chang, J.J. Linderman, and J.A. Swanson Ruffles limit diffusion in the plasma membrane during macropinosome formation J. Cell Sci. 124 2011 4106 4114 10.1242/jcs.091538