Unconventional secretory routes: Direct protein export across the plasma membrane of mammalian cells

Traffic

Volumn 6, Issue 8, 2005, Pages 607-614

  Nickel, Walter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

FGF 1; FGF 2; Fibroblast growth factor; Galectin; Galectin 1; HASPB; Hydrophilic acylated surface protein; Membrane translocation; Non classical protein export; Protein targeting; Unconventional protein secretion

Indexed keywords

ANGIOGENIC FACTOR; BACTERIAL PROTEIN; EXOPROTEIN; FIBROBLAST GROWTH FACTOR 2; HYDROPHILIC ACYLATED SURFACE PROTEIN B; MEMBRANE PROTEIN; PROTEIN; SECRETORY PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL SECRETION; CYTOPLASM; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; LEISHMANIA; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW;

ANIMALS; ANTIGENS, PROTOZOAN; CELL MEMBRANE; EUKARYOTIC CELLS; EXOCYTOSIS; FIBROBLAST GROWTH FACTOR 2; HUMANS; MEMBRANE TRANSPORT PROTEINS; PROTEIN CONFORMATION; PROTEIN TRANSPORT; PROTEINS; PROTOZOAN PROTEINS;

EID: 21844468743     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2005.00302.x     Document Type: Review

References (56)

1. Schatz G, Dobberstein B. Common principles of protein translocation across membranes. Science 1996;271:1519-1526.
2. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R. Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 2004;20:87-123.
3. Keller P, Simons K. Post-Golgi biosynthetic trafficking. J Cell Sci 1997;11(Pt 24):3001-3009.
4. Palace G. Intracellular aspects of the process of protein synthesis. Science 1975;189:347-358.
5. Cleves AE. Protein transports: the nonclassical ins and outs. Curr Biol 1997;7:R318-R320.
6. Hughes RC. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1999;1473:172-185.
7. Nickel W. The mystery of nonclassical protein secretion. Eur J Biochem 2003;270:2109-2119.
8. 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-1α point the way. J Cell Sci 2003;116(Pt 24):4871-4881.
9. Nugent MA, Iozzo RV. Fibroblast growth factor-2. Int J Biochem Cell Biol 2000;32:115-120.
10. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. Apoptosis of T cells mediated by galectin-1. Nature 1995;378:736-739.
11. Braddock M, Quinn A. Targeting IL-1 in inflammatory disease: new opportunities for therapeutic intervention. Nat Rev Drug Discov 2004;3:330-339.
12. Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect 2002;4:449-460.
13. McKean PG, Denny PW, Knuepfer E, Keen JK, Smith DF. Phenotypic changes associated with deletion and overexpression of a stage-regulated gene family in Leishmania. Cell Microbiol 2001;3:511-523.
14. Clark R, Griffiths GM. Lytic granules, secretory lysosomes and disease. Curr Opin Immunol 2003;15:516-521.
15. Stinchcombe J, Bossi G, Griffiths GM. Linking albinism and immunity: the secrets of secretory lysosomes. Science 2004;305:55-59.
16. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G. The biogenesis and functions of exosomes. Traffic 2002;3:321-330.
17. Stahl PD, Barbieri MA. Multivesicular bodies and multivesicular endosomes: the "ins and outs" of endosomal traffic. Sci STKE 2002;2002:PE32.
18. Cleves AE, Kelly RB. Rehearsing the ABCs. Protein translocation. Curr Biol 1996;6:276-278.
19. Martinez MC, Tesse A, Zobairi F, Andriantsitohaina R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol 2005;288:H1004-H1009.
20. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: two sides of the coin. Physiology (Bethesda) 2005;20:22-27.
21. Freyssinet JM. Cellular microparticles: what are they bad or good for? J Thromb Haemost 2003;1:1655-1662.
22. Rubartelli A, Cozzolino F, Talio M, Sitia R. A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J 1990;9:1503-1510.
23. Andrei C, Dazzi C, Lotti L, Torrisi MR, Chimini G, Rubartelli A. The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol Biol Cell 1999;10:1463-1475.
24. Andrei C, Margiocco P, Poggi A, Lotti LV, Torrisi MR, Rubartelli A. Phospholipases C and A2 control lysosome-mediated IL-1beta secretion: implications for inflammatory processes. Proc Natl Acad Sci USA 2004;101:9745-9750.
25. Hamon Y, Luciani MF, Becq F, Verrier B, Rubartelli A, Chimini G. Interleukin-1 beta secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood 1997;90:2911-2915.
26. Zhou X, Engel T, Goepfert C, Erren M, Assmann G, von Eckardstein A. The ATP binding cassette transporter A1 contributes to the secretion of interleukin 1 beta from macrophages but not from monocytes. Biochem Biophys Res Commun 2002;291:598-604.
27. Raggers RJ, Pomorski T, Holthuis JC, Kalin N, van Meer G. Lipid traffic: the ABC of transbilayer movement. Traffic 2000;11:226-234.
28. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME, Rubartelli A. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 2002;3:995-1001.
29. Flieger O, Engling A, Bucala R, Lue H, Nickel W, Bernhagen J. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett 2003;551:78-86.
30. Bonaldi T, Talamo F, Scaffidi P, Ferrara D, Porto A, Bachi A, Rubartelli A, Agresti A, Bianchi ME. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 2003;22:5551-5560.
31. Schafer 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.
32. Stegmayer C, Kehlenbach A, Tournaviti S, Wegehingel S, Zehe C, Denny P, Smith DF, Schwappach B, Nickel W. Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant. J Cell Sci 2005;118(Pt 3):517-527.
33. Denny PW, Gokool S, Russell DG, Field MC, Smith DF. Acylation-dependent protein export in Leishmania. J Biol Chem 2000;275:11017-11025.
34. Resh MD. Membrane targeting of lipid modified signal transduction proteins. Subcell Biochem 2004;37:217-232.
35. Jackson A, Friedman S, Zhan X, Engleka KA, Forough R, Maciag T. Heat shock induces the release of fibroblast growth factor 1 from NIH 3T3 cells. Proc Natl Acad Sci USA 1992;89:10691-10695.
36. Jackson A, Tarantini F, Gamble S, Friedman S, Maciag T. The release of fibroblast growth factor-1 from NIH 3T3 cells in response to temperature involves the function of cysteine residues. J Biol Chem 1995;270:33-36.
37. Shi J, Friedman S, Maciag T. A carboxyl-terminal domain in fibroblast growth factor (FGF)-2 inhibits FGF-1 release in response to heat shock in vitro. J Biol Chem 1997;272:1142-1147.
38. Landriscina M, Soldi R, Bagala C, Micucci I, Bellum S, Tarantini F, Prudovsky I, Maciag T. S100a13 participates in the release of fibroblast growth factor 1 in response to heat shock in vitro. J Biol Chem 2001;276:22544-22552.
39. Prudovsky I, Bagala C, Tarantini F, Mandinova A, Soldi R, Bellum S, Maciag T. The intracellular translocation of the components of the fibroblast growth factor 1 release complex precedes their assembly prior to export. J Cell Biol 2002;158:201-208.
40. Cooper DN, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol 1990;110:1681-1691.
41. Mehul B, Hughes RC. Plasma membrane targetting, vesicular budding and release of galectin 3 from the cytoplasm of mammalian cells during secretion. J Cell Sci 1997;110(Pt 10):1169-1178.
42. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, Amigorena S. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001;166:7309-7318.
43. Taverna S, Ghersi G, Ginestra A, Rigogliuso S, Pecorella S, Alaimo G, Saladino F, Dolo V, Dell'Era P, Pavan A, Pizzolanti G, Mignatti P, Presta M, Vittorelli ML. Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells. J Biol Chem 2003; 278: 51911-51919.
44. 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.
45. Gloe T, Sohn HY, Meininger GA, Pohl U. Shear stress-induced release of basic fibroblast growth factor from endothelial cells is mediated by matrix interaction via integrin alpha(v)beta3. J Biol Chem 2002;277: 23453-23458.
46. Helenius A, Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 2004;73:1019-1049.
47. Trombetta ES, Parodi AJ. Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol 2003;19:649-676.
48. Eilers M, Schatz G. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 1986;322: 228-232.
49. Wienhues U, Becker K, Schleyer M, Guiard B, Tropschug M, Horwich AL, Pfanner N, Neupert W. Protein folding causes an arrest of preprotein translocation into mitochondria in vivo. J Cell Biol 1991;115: 1601-1609.
50. 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.
51. Titorenko VI, Nicaud JM, Wang H, Chan H, Rachubinski RA. Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J Cell Biol 2002;156: 481-494.
52. Robinson C, Bolhuis A. Tat-dependent protein targeting in prokaryotes and chloroplasts. Biochim Biophys Acta 2004;1694:135-147.
53. Hynds PJ, Robinson D, Robinson C. The sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J Biol Chem 1998;273:34868-34874.
54. DeLisa MP, Tullman D, Georgiou G. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci USA 2003;100:6115-6120.
55. Tarantini F, Gamble S, Jackson A, Maciag T. The cysteine residue responsible for the release of fibroblast growth factor-1 resides in a domain independent of the domain for phosphatidylserine binding. J Biol Chem 1995;270:29039-29042.
56. Muesch A, Hartmann E, Rohde K, Rubartelli A, Sitia R, Rapoport TA. A novel pathway for secretory proteins? Trends Biochem Sci 1990;15:86-88.