A Direct Role for ATP1A1 in Unconventional Secretion of Fibroblast Growth Factor 2

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3654-3665

  Zacherl, Sonja ^a   La Venuta, Giuseppe ^a   Müller, Hans Michael ^a   Wegehingel, Sabine ^a   Dimou, Eleni ^a   Sehr, Peter ^b   Lewis, Joe D ^b   Erfle, Holger ^a   Pepperkok, Rainer ^b   Nickel, Walter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; MACHINERY;

CYTOPLASMIC DOMAINS; FIBROBLAST GROWTH FACTOR 2; INNER LEAFLETS; MACHINERY COMPONENTS;

PHYSIOLOGY;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); FIBROBLAST GROWTH FACTOR 2; MEMBRANE PROTEIN; OUABAIN; PHOSPHATIDYLINOSITOL; RNA; SECRETORY PROTEIN; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1A1; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B3; ATP1A1 PROTEIN, HUMAN; ATP1B1 PROTEIN, HUMAN; ATP1B3 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BETA CHAIN; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RNA INTERFERENCE; CHEMISTRY; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; PROTEIN TERTIARY STRUCTURE; SECRETORY PATHWAY;

FIBROBLAST GROWTH FACTOR 2; HELA CELLS; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SECRETORY PATHWAY; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84922438022     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.590067     Document Type: Article

References (40)

1. Rothman, J. E. (1994) Mechanisms of intracellular protein transport. Nature 372, 55-63.
2. Rothman, J. E., and Wieland, F. T. (1996) Protein sorting by transport vesicles. Science 272, 227-234.
3. Schekman, R., and Orci, L. (1996) Coat proteins and vesicle budding. Science 271, 1526-1533.
4. Rapoport, T. A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669.
5. Hegde, R. S., and Ploegh, H. L. (2010) Quality and quantity control at the endoplasmic reticulum. Curr. Opin. Cell Biol. 22, 437-446.
6. Sitia, R., and Braakman, I. (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426, 891-894.
7. Rabouille, C., Malhotra, V., and Nickel, W. (2012) Diversity in unconventional protein secretion. J. Cell Sci. 125, 5251-5255.
8. Nickel, W. (2003) The mystery of nonclassical protein secretion: A current view on cargo proteins and potential export routes. Eur. J. Biochem. 270, 2109-2119.
9. Prudovsky, I., Tarantini, F., Landriscina, M., Neivandt, D., Soldi, R., Kirov, A., Small, D., Kathir, K. M., Rajalingam, D., and Kumar, T. K. (2008) Secretion without Golgi. J. Cell Biochem. 103, 1327-1343.
10. Dinarello, C. A. (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550.
11. Presta, M., Dell'Era, P., Mitola, S., Moroni, E., Ronca, R., and Rusnati, M. (2005) Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 16, 159-178.
12. Nickel, W. (2005) Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6, 607-614.
13. Schäfer, T., Zentgraf, H., Zehe, C., Brügger, B., Bernhagen, J., and Nickel, W. (2004) Unconventional secretion of fibroblast growth factor 2 is mediated by direct translocation across the plasma membrane of mammalian cells. J. Biol. Chem. 279, 6244-6251.
14. Temmerman, K., Ebert, A. D., Müller, H. M., Sinning, I., Tews, I., and Nickel, W. (2008) A direct role for phosphatidylinositol-4, 5-bisphosphate in unconventional secretion of fibroblast growth factor 2. Traffic 9, 1204-1217.
15. Temmerman, K., and Nickel, W. (2009) A novel flow cytometric assay to quantify interactions between proteins and membrane lipids. J. Lipid Res. 50, 1245-1254.
16. Nickel, W. (2011) The unconventional secretory machinery of fibroblast growth factor 2. Traffic 12, 799-805.
17. Steringer, J. P., Bleicken, S., Andreas, H., Zacherl, S., Laussmann, M., Temmerman, K., Contreras, F. X., Bharat, T. A., Lechner, J., Müller, H. M., Briggs, J. A., García-Sáez, A. J., and Nickel, W. (2012) Phosphatidylinositol 4, 5-bisphosphate (PI(4, 5)P2)-dependent oligomerization of fibroblast growth factor 2 (FGF2) triggers the formation of a lipidic membrane pore implicated in unconventional secretion. J. Biol. Chem. 287, 27659-27669.
18. Zehe, C., Engling, A., Wegehingel, S., Schäfer, T., and Nickel, W. (2006) Cell-surface heparan sulfate proteoglycans are essential components of the unconventional export machinery of FGF-2. Proc. Natl. Acad. Sci. U.S.A. 103, 15479-15484.
19. Nickel, W. (2007) Unconventional secretion: An extracellular trap for export of fibroblast growth factor 2. J. Cell Sci. 120, 2295-2299.
20. Nickel, W., and Seedorf, M. (2008) Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells. Annu. Rev. Cell Dev. Biol. 24, 287-308.
21. Ebert, A. D., Laussmann, M., Wegehingel, S., Kaderali, L., Erfle, H., Reichert, J., Lechner, J., Beer, H. D., Pepperkok, R., and Nickel, W. (2010) Teckinase- mediated phosphorylation of fibroblast growth factor 2 is essential for unconventional secretion. Traffic 11, 813-826.
22. Steringer, J. P., Muller, H. M., and Nickel, W. (2014) Unconventional secretion of fibroblast growth factor 2: A novel type of protein translocation across membranes? J. Mol. Biol. 10.1016/j.jmb.2014.07.012.
23. Backhaus, R., Zehe, C., Wegehingel, S., Kehlenbach, A., Schwappach, B., and Nickel, W. (2004) Unconventional protein secretion: membrane translocation of FGF-2 does not require protein unfolding. J. Cell Sci. 117, 1727-1736.
24. Torrado, L. C., Temmerman, K., Müller, H. M., Mayer, M. P., Seelenmeyer, C., Backhaus, R., and Nickel, W. (2009) An intrinsic quality-control mechanism ensures unconventional secretion of fibroblast growth factor 2 in a folded conformation. J. Cell Sci. 122, 3322-3329.
25. Kaplan, J. H. (2002) Biochemistry of Na, K-ATPase. Annu. Rev. Biochem. 71, 511-535.
26. +-ATPase in the plasma membrane of HeLa cells. J. Cell Sci. 121, 2159-2168.
27. Dahl, J. P., Binda, A., Canfield, V. A., and Levenson, R. (2000) Participation of Na, K-ATPase in FGF-2 secretion: rescue of ouabain-inhibitable FGF-2 secretion by ouabain-resistant Na, K-ATPase subunits. Biochemistry 39, 14877-14883.
28. +-ATPase. J. Biol. Chem. 273, 544-551.
29. Erfle, H., Neumann, B., Rogers, P., Bulkescher, J., Ellenberg, J., and Pepperkok, R. (2008) Work flow for multiplexing siRNA assays by solid-phase reverse transfection in multiwell plates. J. Biomol. Screen. 13, 575-580.
30. Engling, A., Backhaus, R., Stegmayer, C., Zehe, C., Seelenmeyer, C., Kehlenbach, A., Schwappach, B., Wegehingel, S., and Nickel, W. (2002) Biosynthetic FGF-2 is targeted to non-lipid raft microdomains following translocation to the extracellular surface of CHO cells. J. Cell Sci. 115, 3619-3631.
31. Stegmayer, C., Kehlenbach, A., Tournaviti, S., Wegehingel, S., Zehe, C., Denny, P., Smith, D. F., Schwappach, B., and Nickel, W. (2005) Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant. J. Cell Sci. 118, 517-527.
32. Aftab, O., Nazir, M., Fryknäs, M., Hammerling, U., Larsson, R., and Gustafsson, M. G. (2014) Label free high throughput screening for apoptosis inducing chemicals using time-lapse microscopy signal processing. Apoptosis 19, 1411-1418.
33. Miller, M. K., Bang, M. L., Witt, C. C., Labeit, D., Trombitas, C., Watanabe, K., Granzier, H., McElhinny, A. S., Gregorio, C. C., and Labeit, S. (2003) The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules. J. Mol. Biol. 333, 951-964.
34. Taouji, S., Dahan, S., Bosse, R., and Chevet, E. (2009) Current screens based on the AlphaScreen technology for deciphering cell signalling pathways. Curr. Genomics 10, 93-101.
35. Lazar, G. A., Dang, W., Karki, S., Vafa, O., Peng, J. S., Hyun, L., Chan, C., Chung, H. S., Eivazi, A., Yoder, S. C., Vielmetter, J., Carmichael, D. F., Hayes, R. J., and Dahiyat, B. I. (2006) Engineered antibody Fc variants with enhanced effector function. Proc. Natl. Acad. Sci. U.S.A. 103, 4005-4010.
36. +-ATPase. J. Biol. Chem. 269, 19659-19662.
37. Nickel, W. (2010) Pathways of unconventional protein secretion. Curr. Opin. Biotechnol. 21, 621-626.
38. Mano, H. (1999) Tec family of protein-tyrosine kinases: An overview of their structure and function. Cytokine Growth Factor Rev. 10, 267-280.
39. Schaeffer, E. M., and Schwartzberg, P. L. (2000) Tec family kinases in lymphocyte signaling and function. Curr. Opin. Immunol. 12, 282-288.
40. Nickel, W., and Rabouille, C. (2009) Mechanisms of regulated unconventional protein secretion. Nat. Rev. Mol. Cell Biol. 10, 148-155.