Evidence for a fence that impedes the diffusion of phosphatidylinositol 4,5-bisphosphate out of the forming phagosomes of macrophages

Molecular Biology of the Cell

Volumn 22, Issue 18, 2011, Pages 3498-3507

  Golebiewska, Urszula ^a,b   Kay, Jason G ^c   Masters, Thomas ^d   Grinstein, Sergio ^c   Im, Wonpil ^e   Pastor, Richard W ^f   Scarlata, Suzanne ^a   McLaughlin, Stuart ^a,d  

^a STONY BROOK UNIVERSITY   (United States)

^b QUEENSBOROUGH COMMUNITY COLLEGE   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e UNIVERSITY OF KANSAS   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SEPTIN;

ARTICLE; CELL LINE; CELL MEMBRANE; DIFFUSION COEFFICIENT; MACROPHAGE; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION;

ACTIN CYTOSKELETON; ANIMALS; ANTIBODIES, IMMOBILIZED; CELL LINE; CELL MEMBRANE; DIFFUSION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; MACROPHAGES; MICE; MICROINJECTIONS; MICROSCOPY, FLUORESCENCE; MICROSPHERES; PHAGOCYTOSIS; PHAGOSOMES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; TIME-LAPSE IMAGING;

EID: 80052847053     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-02-0114     Document Type: Article

References (60)

1. Aoyagi K, Sugaya T, Umeda M, Yamamoto S, Terakawa S, Takahashi M (2005). The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J Biol Chem 280, 17346-17352. (Pubitemid 41389204)
2. Araki N, Johnson MT, Swanson JA (1996). A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis in macrophages. J Cell Biol 135, 1249-1260. (Pubitemid 27014597)
3. Barral Y, Mermall V, Mooseker MS, Snyder M (2000). Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol Cell 5, 841-851.
4. 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, 1353-1367. (Pubitemid 32047586)
5. Coppolino MG, Dierckman R, Loijen J, Collins RF, Pouladi M, Jongstra-Bilen J, Schreiber AD, Trimble WS, Anderson R, Grinstein S (2002). Inhibition of phosphatidylinositol-4-phosphate 5-kinase Iα impairs localized actin remodeling and suppresses phagocytosis. J Biol Chem 277, 43849-43875.
6. Corbett-Nelson EF, Mason D, Marshall JG, Collette Y, Grinstein S (2006). Signaling-dependent immobilization of acylated proteins in the inner monolayer of the plasma membrane. J Cell Biol 174, 255-265. (Pubitemid 44079860)
7. Cougoule C, Wiedemann A, Lim J, Caron E (2004). Phagocytosis, an alternative model system for the study of cell adhesion. Semin Cell Dev Biol 15, 679-689. (Pubitemid 39550247)
8. Di Paolo G, De Camilli P (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 433, 651-657. (Pubitemid 44564702)
9. 2 in its place. J Membrane Biol 194, 77-89.
10. Elson EL, Rigler R (2001). Fluorescence Correlation Spectroscopy. Theory and Applications, Berlin: Springer-Verlag.
11. Emoto K, Inadome H, Kanaho Y, Narumiya S, Umeda M (2005). Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J Biol Chem 280, 37901-37907. (Pubitemid 41642402)
12. Estey MP, Kim MS, Trimble WS (2011). Septins. Curr Biol 21, R384-R387.
13. Faty M, Fink M, Barral Y (2002). Septins: a ring to part mother and daughter. Curr Genet 41, 123-131. (Pubitemid 36097256)
14. Field SJ, Madson N, Kerr ML, Galbraith KAA, Kennedy CE, Tahiliani M, Wilkins A, Cantley LC (2005). PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr Biol 15, 1407-1412.
15. Finger FP (2005). Reining in cytokinesis with a septin corral. Bioessays 27, 5-8.
16. Froese CD, Trimble WS (2008). The functions of septins in mammals. In: The Septins, eds. PA Hall, SE Hilary Russell, JR Pringle, Chichester, United Kingdom: John Wiley & Sons, 187-210.
17. Fujita A, Cheng J, Tauchi-Sato K, Takenawa T, Fujimoto T (2009). A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc Natl Acad Sci USA 106, 9256-9261.
18. 2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys J 86, 2188-2207.
19. Garrenton LS, Stefan CJ, McMurray MA, Emr SD, Thorner J (2010). Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5- bisphosphate distribution is required for MAPK signaling. Proc Natl Acad Sci USA 107, 11805-11810.
20. 2) in the plasma membrane of cells. Mol Biol Cell 19, 1663-1669.
21. Hall PA, Russell SEH, Pringle JR, eds. (2008). The Septins, Chichester, United Kingdom: John Wiley & Sons.
22. Hammond GRV, Sim Y, Lagnado L, Irvine RF (2009). Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. J Cell Biol 184, 297-308.
23. Haustein E, Schwille P (2007). Fluorescence correlation spectroscopy: novel variations of an established technique. Annu Rev Biophys Biomol Struct 36, 151-169. (Pubitemid 46998114)
24. Hilgemann DW (2007). Local PIP2 signals: when, where and how? Pflugers Arch 455, 55-67.
25. Hinchliffe KA, Ciruela A, Irvine RF (1998). PIPkins1, their substrates and their products: new functions for old enzymes. Biochim Biophys Acta 1436, 87-104.
26. Huang Y-W, Yan M, Collins RF, DiCiccio JE, Grinstein S, Trimble WS (2008). Mammalian septins are required for phagosome formation. Mol Biol Cell 19, 1717-1726. (Pubitemid 351805123)
27. James DJ, Khodthong C, Kowalchyk JA, Martin TFJ (2008). Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J Cell Biol 182, 355-366.
28. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Furiwara T (2005). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high speed single molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34, 351-378.
29. Kusumi A, Shirai YM, Koyama-Honda I, Suzuki KGN, Fujiwara TK (2010). Hierarchical organization of the plasma membrane: investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett 584, 1814-1823.
30. Lam AD, Tryoen-Toth P, Tsai B, Vitale N, Stuenkel EL (2008). SNARE-catalyzed fusion events are regulated by syntaxin1a-lipid interactions. Mol Biol Cell 19, 485-497. (Pubitemid 351272138)
31. Lingwood D, Simons K (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
32. Liu P, Sudhaharan T, Koh RML, Hwang LC, Ahmed S, Maruyama IN, Wohland T (2007). Investigation of the dimerization of proteins from the epidermal growth factor receptor family by single wavelength fluorescence cross-correlation spectroscopy. Biophys J 93, 684-698. (Pubitemid 47057833)
33. Mao YS, Yin HL (2007). Regulation of the actin cytoskeleton by phosphatidylinositol 4-phosphate 5 kinases. Pflugers Arch 455, 5-18. (Pubitemid 47403983)
34. Mao YS et al. (2009). Essential and unique roles of PIP5K-γ and -α in Fcγ receptor-mediated phagocytosis. J Cell Biol 184, 281-296.
35. 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 Fcγ receptor-mediated phagocytosis. J Cell Biol 153, 1369-1380. (Pubitemid 34286123)
36. McLaughlin S, Murray D (2005). Plasma membrane phosphoinositide organization by membrane electrostatics. Nature 438, 605-611. (Pubitemid 41740564)
37. McLaughlin S, Wang J, Gambhir A, Murray D (2002). PIP2 and proteins: interactions, organization and information flow. Annu Rev Biophys Biomol Struct 31, 151-175. (Pubitemid 34666829)
38. McMurray MA, Thorner J (2009). Septins: molecular partitioning and the generation of cellular asymmetry. Cell Division 4, 18.
39. Melikyan GB, Deriy BN, Ok DC, Cohen FS (1996). Voltage-dependent translocation of R18 and DiI across lipid bilayers leads to fluorescence changes. Biophys J 71, 2680-2691. (Pubitemid 26367730)
40. Milosevic I, Sorensen JB, Lang T, Krauss M, Nagy G, Haucke V, Jahn R, Neher E (2005). Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci 25, 2557-2565. (Pubitemid 40365167)
41. Morone N, Fujiwara T, Murase K, Kasai R, Ike H, Yuasa S, Usakura J, Kusume A (2006). Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J Cell Biol 174, 851-862. (Pubitemid 44373734)
42. Oh Y, Bi E (2011). Septin structure and function in yeast and beyond. Trends Cell Biol 21, 141-148.
43. Petrasek Z, Schwille P (2008). Precise measurement of diffusion coefficients using scanning fluorescence correlation spectroscopy. Biophys J 94, 1437-48.
44. Raucher D, Stauffer T, Chen W, Shen K, Guo S, York JD, Sheetz MP, Meyer T (2000). Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228. (Pubitemid 30064910)
45. Ruttinger S, Buschmann V, Kramer B, Erdmann R, Macdonald R, Koberling F (2008). Comparison and accuracy of methods to determine the confocal volume for quantitative fluorescence correlation spectroscopy. J Microsc 232, 343-352.
46. Santarius M, Lee CH, Anderson RA (2006). Supervised membrane swimming: small G-protein lifeguards regulate PIPK signaling and monitor intracellular PtdIns(4,5)P2 pools. Biochem J 398, 1-13. (Pubitemid 44231296)
47. Schmidt K, Nichols BJ (2004). A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells. Curr Biol 14, 1002-1006. (Pubitemid 38722615)
48. 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. (Pubitemid 40562921)
49. Sirajuddin M, Farkosovsky M, Hauer F, Kuhlmann D, Macara IG, Weyland M, Stark H, Wittinghofer A (2007). Structural insight into filament formation by mammalian septins. Nature 449, 311-315. (Pubitemid 47443471)
50. Steinberg BE, Grinstein S (2009). Pathogen destruction versus intracellular survival: the role of lipids as phagosomal fate determinants. In: Methods in Molecular Biology. Macrophages and Dendritic Cells, ed. NE Reiner, New York: Humana Press, 2002-2011.
51. Stuart LM, Ezekowitz RAB (2005). Phagocytosis: elegant complexity. Immunity 22, 539-550. (Pubitemid 40719190)
52. Swaney KF, Huang C-H, Devreotes PN (2010). Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys 39, 365-289.
53. Swanson JA (2008). Shaping cups into phagosomes and macropinosomes. Nature Rev Mol Cell Biol 9, 639-649.
54. Takizawa PA, DeRisi JL, Wilhelm JE, Vale RD (2000). Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290, 341-344.
55. 2+ signaling in mast cells. J Cell Sci 122, 2567-2574.
56. Weernink PAO, Schmidt M, Jakobs KH (2004). Regulation and cellular roles of phosphoinositide 5-kinases. Eur J Pharmacol 500, 87-99. (Pubitemid 39303999)
57. 2 synthesizing enzyme at the synapse. Neuron 32, 79-88.
58. Williams D, Vicogne J, Zaitseva I, McLaughlin S, Pessin JE (2009). Evidence that electrostatic interactions between vesicle-associated membrane protein 2 and acidic phospholipids may modulate the fusion of transport vesicles with the plasma membrane. Mol Biol Cell 20, 4910-4919.
59. Yeung T, Ozdamar B, Paroutis P, Grinstein S (2006). Lipid metabolism and dynamics during phagocytosis. Curr Opin Cell Biol 18, 429-437. (Pubitemid 44016055)
60. Yoshida S, Bartolini S, Pellman D (2009). Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev 23, 810-823.