Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant

Journal of Cell Science

Volumn 118, Issue 3, 2005, Pages 517-527

  Stegmayer, Carolin ^a   Kehlenbach, Angelika ^b   Tournaviti, Stella ^a   Wegehingel, Sabine ^a   Zehe, Christoph ^a   Denny, Paul ^c   Smith, Deborah F ^c   Schwappach, Blanche ^b   Nickel, Walter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Zentrum fur Molec Biol Heidelberg   (Germany)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Acylation; Cell surface expression; Fibroblast growth factor 2; Hydrophilic acylated surface protein; Leishmania parasites; Non classical protein export; SH4 domain; Surface coat

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; MEMBRANE PROTEIN; MYRISTIC ACID; PALMITIC ACID; PROTEIN HASPB; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ACYLATION; ANGIOGENESIS; ANIMAL CELL; ARTICLE; BIOACCUMULATION; BIOGENESIS; BIOTINYLATION; CELL FRACTIONATION; CELL LINE; CELL MUTANT; CLONAL VARIATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; HAMSTER; LEISHMANIA; MAMMAL CELL; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; NONHUMAN; OVARY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TARGETING; PROTEIN TRANSPORT; REPORTER GENE; WILD TYPE;

ACYLATION; ANIMALS; ANTIGENS, PROTOZOAN; BIOTINYLATION; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSOL; DOXYCYCLINE; FATTY ACIDS; FIBROBLAST GROWTH FACTOR 2; FLOW CYTOMETRY; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; LEISHMANIA; MEMBRANE PROTEINS; MUTAGENESIS, INSERTIONAL; MUTATION; PARASITES; PEPTIDE FRAGMENTS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE;

EID: 14644399785     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01645     Document Type: Article

References (53)

1. Alce, T. M., Gokool, S., McGhie, D., Stager, S. and Smith, D. F. (1999). Expression of hydrophilic surface proteins in infective stages of Leishmania donovani. Mol. Biochem. Parasitol. 102, 191-196.
2. Andrei, C., Dazzi, C., Lotti, L., Torrisi, M. R., Chimini, G. and Rubartelli, A. (1999). The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 10, 1463-1475.
3. Andrei, C., Margiocco, P., Poggi, A., Lotti, L. V., Torrisi, M. R. and Rubartelli, A. (2004). Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 101, 9745-9750.
4. 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.
5. Bijlmakers, M. J. and Marsh, M. (1999). Trafficking of an acylated cytosolic protein: newly synthesized p56(lck) travels to the plasma membrane via the exocytic pathway. J. Cell Biol. 145, 457-468.
6. Bijlmakers, M. J. and Marsh, M. (2003). The on-off story of protein palmitoylation. Trends Cell Biol. 13, 32-42.
7. Cleves, A. E. (1997). Protein transports: the nonclassical ins and outs. Curr. Biol. 7, R318-R320.
8. Cleves, A. E., Cooper, D. N., Barondes, S. H. and Kelly, R. B. (1996). A new pathway for protein export in Saccharomyces cerevisiae. J. Cell Biol. 133, 1017-1026.
9. Cooper, D. N. and Barondes, S. H. (1990). Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J. Cell Biol. 110, 1681-1691.
10. Denny, P. W., Gokool, S., Russell, D. G., Field, M. C. and Smith, D. F. (2000). Acylation-dependent protein export in Leishmania. J. Biol. Chem. 275, 11017-11025.
11. 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.
12. Fishburn, C. S., Herzmark, P., Morales, J. and Bourne, H. R. (1999). Gbetagamma and palmitate target newly synthesized Galphaz to the plasma membrane. J. Biol. Chem. 274, 18793-18800.
13. Flieger, O., Engling, A., Bucala, R., Lue, H., Nickel, W. and Bernhagen, J. (2003). Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett. 551, 78-86.
14. Flinn, H. M., Rangarajan, D. and Smith, D. F. (1994). Expression of a hydrophilic surface protein in infective stages of Leishmania major. Mol. Biochem. Parasitol. 65, 259-270.
15. Florkiewicz, R. Z., Majack, R. A., Buechler, R. D. and Florkiewicz, E. (1995). Quantitative export of FGF-2 occurs through an alternative, energy-dependent, non-ER/Golgi pathway. J. Cell Physiol. 162, 388-399.
16. Fujiki, Y., Hubbard, A. L., Fowler, S. and Lazarow, P. B. (1982). Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102.
17. Futter, C. E., Gibson, A., Allchin, E. H., Maxwell, S., Ruddock, L. J., Odorizzi, G., Domingo, D., Trowbridge, I. S. and Hopkins, C. R. (1998). In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules. J. Cell Biol. 141, 611-623.
18. Hughes, R. C. (1999). Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473, 172-185.
19. Jackson, A., Friedman, S., Zhan, X., Engleka, K. A., Forough, R. and Maciag, T. (1992). Heat shock induces the release of fibroblast growth factor 1 from NIH 3T3 cells. Proc. Natl. Acad. Sci. USA 89, 10691-10695.
20. Jackson, A., Tarantini, F., Gamble, S., Friedman, S. and Maciag, T. (1995). The release of fibroblast growth factor-1 from NTH 3T3 cells in response to temperature involves the function of cysteine residues. J. Biol. Chem. 270, 33-36.
21. Keenan, R. J., Freymann, D. M., Stroud, R. M. and Walter, P. (2001). The signal recognition particle. Annu. Rev. Biochem. 70, 755-775.
22. Landriscina, M., Bagala, C., Mandinova, A., Soldi, R., Micucci, I., Bellum, S., Prudovsky, I. and Maciag, T. (2001a). Copper induces the assembly of a multiprotein aggregate implicated in the release of fibroblast growth factor 1 in response to stress. J. Biol. Chem. 276, 25549-25557.
23. Landriscina, M., Soldi, R., Bagala, C., Micucci, I., Bellum, S., Tarantini, F., Prudovsky, I. and Maciag, T. (2001b). S100a13 participates in the release of fibroblast growth factor 1 in response to heat shock in vitro. J. Biol. Chem. 276, 22544-22552.
24. LaVallee, T. M., Tarantini, F., Gamble, S., Carreira, C. M., Jackson, A. and Maciag, T. (1998). Synaptotagmin-1 is required for fibroblast growth factor-1 release. J. Biol. Chem. 273, 22217-22223.
25. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S. and Klausner, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with Brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
26. Liu, X., Constantinescu, S. N., Sun, Y., Bogan, J. S., Hirsch, D., Weinberg, R. A. and Lodish, H. F. (2000). Generation of mammalian cells stably expressing multiple genes at predetermined levels. Anal. Biochem. 280, 20-28.
27. Lutomski, D., Fouillit, M., Bourin, P., Mellottee, D., Denize, N., Pontet, M., Bladier, D., Caron, M. and Joubert-Caron, R. (1997). Externalization and binding of galectin-1 on cell surface of K562 cells upon erythroid differentiation. Glycobiology 7, 1193-1199.
28. Mandinova, A., Soldi, R., Graziani, I., Bagala, C., Bellum, S., Landriscina, M., Tarantini, F., Prudovsky, I. and Maciag, T. (2003). S100A13 mediates the copper-dependent stress-induced release of IL-1alpha from both human U937 and murine NIH 3T3 cells. J. Cell Sci. 116, 2687-2696.
29. McKean, P. G., Trenholme, K. R., Rangarajan, D., Keen, J. K. and Smith, D. F. (1997). Diversity in repeat-containing surface proteins of Leishmania major. Mol. Biochem. Parasitol. 86, 225-235.
30. McKean, P. G., Denny, P. W., Knuepfer, E., Keen, J. K. and Smith, D. F. (2001). Phenotypic changes associated with deletion and overexpression of a stage-regulated gene family in Leishmania. Cell. Microbiol. 3, 511-523.
31. Mignatti, P. and Rifkin, D. B. (1991). Release of basic fibroblast growth factor, an angiogenic factor devoid of secretory signal sequence: a trivial phenomenon or a novel secretion mechanism? J. Cell. Biochem. 47, 201-207.
32. Mignatti, P., Morimoto, T. and Rifkin, D. B. (1992). Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell Physiol. 151, 81-93.
33. Misumi, Y., Miki, A., Takatsuki, A., Tamura, G. and Ikehara, Y. (1986). Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 261, 11398-11403.
34. Muesch, A., Hartmann, E., Rohde, K., Rubartelli, A., Sitia, R. and Rapoport, T. A. (1990). A novel pathway for secretory proteins? Trends Biochem. Sci. 15, 86-88.
35. Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., Kreis, T. E. and Warren, G. (1995). Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131, 1715-1726.
36. Nickel, W. (2003). The mystery of nonclassical protein secretion. Eur. J. Biochem. 270, 2109-2119.
37. Nickel, W., Brügger, B. and Wieland, F. T. (2002). Vesicular transport: the core machinery of COPI recruitment and budding. J. Cell Sci. 115, 3235-3240.
38. Orci, L., Tagaya, M., Amherdt, M., Perrelet, A., Donaldson, J. G., Lippincott-Schwartz, J., Klausner, R. D. and Rothman, J. E. (1991). Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae. Cell 64 1183-1195.
39. Palade, G. (1975). Intracellular aspects of the process of protein synthesis. Science 189, 347-358.
40. Pimenta, P. F., Pinto da Silva, P., Rangarajan, D., Smith, D. F. and Sacks, D. L. (1994). Leishmania major: association of the differentially expressed gene B protein and the surface lipophosphoglycan as revealed by membrane capping. Exp. Parasitol. 79, 468-479.
41. Prudovsky, I., Bagala, C., Tarantini, F., Mandinova, A., Soldi, R., Bellum, S. and Maciag, T. (2002). The intracellular translocation of the components of the fibroblast growth factor 1 release complex precedes their assembly prior to export. J. Cell Biol. 158, 201-208.
42. Prudovsky, I., Mandinova, A., Soldi, R., Bagala, C., Graziani, I., Landriscina, M., Tarantini, F., Duarte, M., Bellum, S., Doherty, H. et al. (2003). The non-classical export routes: FGF1 and IL-1 {alpha} point the way. J. Cell Sci. 116, 4871-4881.
43. Rangarajan, D., Gokool, S., McCrossan, M. V. and Smith, D. F. (1995). The gene B protein localises to the surface of Leishmania major parasites in the absence of metacyclic stage lipophosphoglycan. J. Cell Sci. 108, 3359-3366.
44. Rothman, J. E. (1994). Mechanisms of intracellular protein transport. Nature 372, 55-63.
45. Rothman, J. E. and Wieland, F. T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
46. Rubartelli, A. and Sitia, R. (1991). Interleukin 1 beta and thioredoxin are secreted through a novel pathway of secretion. Biochem. Soc. Trans. 19, 255-259.
47. Rubartelli, A., Cozzolino, F., Talio, M. and Sitia, R. (1990). A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 9, 1503-1510.
48. 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.
49. Seelenmeyer, C., Wegehingel, S., Lechner, J. and Nickel, W. (2003). The cancer antigen CA125 represents a novel counter receptor for galectin-1. J. Cell Sci. 116, 1305-1318.
50. Shin, J. T., Opalenik, S. R., Wehby, J. N., Mahesh, V. K., Jackson, A., Tarantini, F., Maciag, T. and Thompson, J. A. (1996). Serum-starvation induces the extracellular appearance of FGF-1. Biochim. Biophys. Acta 1312, 27-38.
51. Tarantini, F., LaVallee, T., Jackson, A., Gamble, S., Carreira, C. M., Garfinkel, S., Burgess, W. H. and Maciag, T. (1998). The extravesicular domain of synaptotagmin-1 is released with the latent fibroblast growth factor-1 homodimer in response to heat shock. J. Biol. Chem. 273, 22209-22216.
52. Trudel, C., Faure-Desire, V., Florkiewicz, R. Z. and Baird, A. (2000). Translocation of FGF2 to the cell surface without release into conditioned media. J. Cell Physiol. 185, 260-268.
53. van't Hof, W. and Resh, M. D. (1997). Rapid plasma membrane anchoring of newly synthesized p59fyn: selective requirement for NH2-terminal myristoylation and palmitoylation at cysteine-3. J. Cell Biol. 136, 1023-1035.