A direct role for phosphatidylinositol-4,5-bisphosphate in unconventional secretion of fibroblast growth factor 2

Traffic

Volumn 9, Issue 7, 2008, Pages 1204-1217

  Temmerman, Koen ^a   Ebert, Antje D ^a   Müller, Hans Michael ^a   Sinning, Irmgard ^a   Tews, Ivo ^a   Nickel, Walter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Fibroblast growth factor 2; Membrane translocation; Phosphatidylinositol 4,5 bisphosphate; Phosphoinositides; Protein targeting; Protein lipid interaction; Unconventional protein secretion

Indexed keywords

CHOLESTEROL; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; NEOMYCIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL ASSAY; CELL MEMBRANE; CELL TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; LIPID BILAYER; MEMBRANE LEAFLET; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN SECRETION; PROTEIN TARGETING; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; FIBROBLAST GROWTH FACTOR 2; HELA CELLS; HUMANS; LIPID BILAYERS; LIPIDS; MICE; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING;

EID: 46349098379     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00749.x     Document Type: Article

References (43)

1. Nugent MA, Iozzo RV. Fibroblast growth factor-2. Int J Biochem Cell Biol 2000; 32: 115-120.
2. Bikfalvi A, Klein S, Pintucci G, Rifkin DB. Biological roles of fibroblast growth factor-2. Endocr Rev 1997; 18: 26-45.
3. Nickel W. The mystery of nonclassical protein secretion. Eur J Biochem 2003; 270: 2109-2119.
4. Nickel W. Unconventional secretory routes: Direct protein export across the plasma membrane of mammalian cells. Traffic 2005; 6: 607-614.
5. Prudovsky I, Mandinova A, Soldi R, Bagala C, Graziani I, Landriscina M, Tarantini F, Duarte M, Bellum S, Doherty H, Maciag T. The non-classical export routes: FGF1 and IL-1{alpha} point the way. J Cell Sci 2003; 116: 4871-4881.
6. Florkiewicz RZ, Majack RA, Buechler RD, Florkiewicz E. Quantitative export of FGF-2 occurs through an alternative, energy-dependent, non-ER/ Golgi pathway. J Cell Physiol 1995; 162: 388-399.
7. Schäfer T, Zentgraf H, Zehe C, Brügger B, Bernhagen J, Nickel W. Unconventional secretion of fibroblast growth factor 2 is mediated by direct translocation across the plasma membrane of mammalian cells. J Biol Chem 2004; 279: 6244-6251.
8. Zehe C, Engling A, Wegehingel S, Schafer T, Nickel W. Cell-surface heparan sulfate proteoglycans are essential components of the unconventional export machinery of FGF-2. Proc Natl Acad Sci U S A 2006; 103: 15479-15484.
9. Nickel W. Unconventional secretion: An extracellular trap for export of fibroblast growth factor 2. J Cell Sci 2007; 120: 2295-2299.
10. Seelenmeyer C, Wegehingel S, Tews I, Kunzler M, Aebi M, Nickel W. Cell surface counter receptors are essential components of the unconventional export machinery of galectin-1. J Cell Biol 2005; 171: 373-381.
11. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006; 443: 651-657.
12. Behnia R, Munro S. Organelle identity and the signposts for membrane traffic. Nature 2005; 438: 597-604.
13. McLaughlin S, Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 2005; 438: 605-611.
14. Stenmark H, Aasland R, Driscoll PC. The phosphatidylinositol 3-phosphate-binding FYVE finger. FEBS Lett 2002; 513: 77-84.
15. Lemmon MA. Phosphoinositide recognition domains. Traffic 2003; 4: 201-213.
16. Ellson CD, Andrews S, Stephens LR, Hawkins PT. The PX domain: A new phosphoinositide-binding module. J Cell Sci 2002; 115: 1099-1105.
17. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 2006; 314: 1458-1461.
18. Kastrup JS, Eriksson ES, Dalboge H, Flodgaard H. X-ray structure of the 154-amino-acid form of recombinant human basic fibroblast growth factor. Comparison with the truncated 146-amino-acid form. Acta Crystallogr D Biol Crystallogr 1997; 53: 160-168.
19. Rusnati M, Tanghetti E, Urbinati C, Tulipano G, Marchesini S, Ziche M, Presta M. Interaction of fibroblast growth factor-2 (FGF-2) with free gangliosides: Biochemical characterization and biological consequences in endothelial cell cultures. Mol Biol Cell 1999; 10: 313-327.
20. Lumry R, Rajender S. Enthalpy-entropy compensation phenomena in water solutions of proteins and small molecules: A ubiquitous property of water. Biopolymers 1970; 9: 1125-1227.
21. Flicker K, Neuwirth M, Strohmeier M, Kappes B, Tews I, Macheroux P. Structural and thermodynamic insights into the assembly of the heteromeric pyridoxal phosphate synthase from Plasmodium falciparum. J Mol Biol 2007; 374: 732-748.
22. Milosevic I, Sorensen JB, Lang T, Krauss M, Nagy G, Haucke V, Jahn R, Neher E. Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci 2005; 25: 2557-2565.
23. McLaughlin S, Wang J, Gambhir A, Murray D. PIP(2) and proteins: interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 2002; 31: 151-175.
24. Pike LJ, Miller JM. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem 1998; 273: 22298-22304.
25. Fernandes F, Loura LM, Fedorov A, Prieto M. Absence of clustering of phosphatidylinositol-(4,5)-bisphosphate in fluid phosphatidylcholine. J Lipid Res 2006; 47: 1521-1525.
26. Chen R, Kang VH, Chen J, Shope JC, Torabinejad J, DeWald DB, Prestwich GD. A monoclonal antibody to visualize PtdIns(3,4,5)P(3) in cells. J Histochem Cytochem 2002; 50: 697-708.
27. Arbuzova A, Martushova K, Hangyas-Mihalyne G, Morris AJ, Ozaki S, Prestwich GD, McLaughlin S. Fluorescently labeled neomycin as a probe of phosphatidylinositol-4, 5-bisphosphate in membranes. Biochim Biophys Acta 2000; 1464: 35-48.
28. Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci U S A 2003; 100: 13964-13969.
29. Backhaus R, Zehe C, Wegehingel S, Kehlenbach A, Schwappach B, Nickel W. Unconventional protein secretion: Membrane translocation of FGF-2 does not require protein unfolding. J Cell Sci 2004; 117: 1727-1736.
30. Engling A, Backhaus R, Stegmayer C, Zehe C, Seelenmeyer C, Kehlenbach A, Schwappach B, Wegehingel S, Nickel W. Biosynthetic FGF-2 is targeted to non-lipid raft microdomains following translocation to the extracellular surface of CHO cells. J Cell Sci 2002; 115: 3619-3631.
31. Carpenter CL, Cantley LC. Phosphoinositide kinases. Curr Opin Cell Biol 1996; 8: 153-158.
32. Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P. GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 2000; 149: 1455-1472.
33. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000; 351: 95-105.
34. Powis G, Bonjouklian R, Berggren MM, Gallegos A, Abraham R, Ashendel C, Zalkow L, Matter WF, Dodge J, Grindey G, Vlahos CJ. Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res 1994; 54: 2419-2423.
35. Doughman RL, Firestone AJ, Anderson RA. Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place. J Membr Biol 2003; 194: 77-89.
36. Rameh LE, Tolias KF, Duckworth BC, Cantley LC. A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate. Nature 1997; 390: 192-196.
37. Anderson RA, Boronenkov IV, Doughman SD, Kunz J, Loijens JC. Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J Biol Chem 1999; 274: 9907-9910.
38. Wenk MR, De Camilli P. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: Insights from vesicle recycling in nerve terminals. Proc Natl Acad Sci U S A 2004; 101: 8262-8269.
39. Owen DJ, Collins BM, Evans PR. Adaptors for clathrin coats: Structure and function. Annu Rev Cell Dev Biol 2004; 20: 153-191.
40. Gaidarov I, Keen JH. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J Cell Biol 1999; 146: 755-764.
41. Höning S, Ricotta D, Krauss M, Spate K, Spolaore B, Motley A, Robinson M, Robinson C, Haucke V, Owen DJ. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 2005; 18: 519-531.
42. Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 2003; 114: 299-310.
43. van Meer G. Lipids of the Golgi membrane. Trends Cell Biol 1998; 8: 29-33.