TRC40 can deliver short secretory proteins to the Sec61 translocon

Journal of Cell Science

Volumn 125, Issue 15, 2012, Pages 3612-3620

  Johnson, Nicholas ^a   Vilardi, Fabio ^b   Lang, Sven ^c,d   Leznicki, Pawel ^a   Zimmermann, Richard ^c   High, Stephen ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Asna 1; Eeyarestatin I; Endoplasmic reticulum; Post translational translocation; Tail anchored protein; WRB protein

Indexed keywords

APELIN; CARRIER PROTEIN; COMPLEMENTARY DNA; EEYARESTATIN I PROTEIN; PREPROCECROPIN A; SEC61 PROTEIN; SECRETORY PROTEIN; STATHERIN; TRANSLOCON; TRC40 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CECROPIA MOTH; ENDOPLASMIC RETICULUM; ENZYME INHIBITION; ENZYME SUBSTRATE; IN VITRO STUDY; MOTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; ARSENITE TRANSPORTING ATPASES; DOGS; ENDOPLASMIC RETICULUM; HSC70 HEAT-SHOCK PROTEINS; HUMANS; HYDRAZONES; HYDROXYUREA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RABBITS; SALIVARY PROTEINS AND PEPTIDES;

EUKARYOTA; HYALOPHORA CECROPIA; MAMMALIA;

EID: 84863900755     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.102608     Document Type: Article

References (54)

1. Abell, B. M., Jung, M., Oliver, J. D., Knight, B. C., Tyedmers, J., Zimmermann, R. and High, S. (2003). Tail-anchored and signal-anchored proteins utilize overlapping pathways during membrane insertion. J. Biol. Chem. 278, 5669-5678.
2. Abell, B. M., Rabu, C., Leznicki, P., Young, J. C. and High, S. (2007). Post- translational integration of tail-anchored proteins is facilitated by defined molecular chaperones. J. Cell Sci. 120, 1743-1751.
3. Adamus, G., Zam, Z. S., Arendt, A., Palczewski, K., McDowell, J. H. and Hargrave, P. A. (1991). Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application. Vision Res. 31, 17-31.
4. Aletrari, M. O., McKibbin, C., Williams, H., Pawar, V., Pietroni, P., Lord, J. M., Flitsch, S. L., Whitehead, R., Swanton, E., High, S. et al. (2011). Eeyarestatin 1 interferes with both retrograde and anterograde intracellular trafficking pathways. PLoS ONE 6, e22713.
5. Brodsky, J. L. (2010). The special delivery of a tail-anchored protein: why it pays to use a dedicated courier. Mol. Cell 40, 5-7.
6. Brogden, K. A. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250.
7. Castan-Laurell, I., Dray, C., Attané, C., Duparc, T., Knauf, C. and Valet, P. (2011). Apelin, diabetes, and obesity. Endocrine 40, 1-9.
8. Colombo, S. F., Longhi, R. and Borgese, N. (2009). The role of cytosolic proteins in the insertion of tail-anchored proteins into phospholipid bilayers. J. Cell Sci. 122, 2383-2392.
9. Cross, B. C., McKibbin, C., Callan, A. C., Roboti, P., Piacenti, M., Rabu, C., Wilson, C. M., Whitehead, R., Flitsch, S. L., Pool, M. R. et al. (2009a). Eeyarestatin I inhibits Sec61-mediated protein translocation at the endoplasmic reticulum. J. Cell Sci. 122, 4393-4400.
10. Cross, B. C., Sinning, I., Luirink, J. and High, S. (2009b). Delivering proteins for export from the cytosol. Nat. Rev. Mol. Cell Biol. 10, 255-264.
11. Dierks, T., Klappa, P., Wiech, H., Zimmermann, R., Lindquist, S., Welch, W. J., Viitanen, P. and Lorimer, G. H. (1993). The role of molecular chaperones in protein transport into the endoplasmic reticulum. Philos. Trans. R. Soc. Lond. B Biol. Sci. 339, 335-341.
12. Erdmann, F., Jung, M., Eyrisch, S., Lang, S., Helms, V., Wagner, R. and Zimmermann, R. (2009). Lanthanum ions inhibit the mammalian Sec61 complex in its channel dynamics and protein transport activity. FEBS Lett. 583, 2359-2364.
13. Falcão-Pires, I. and Leite-Moreira, A. F. (2005). Apelin: a novel neurohumoral modulator of the cardiovascular system. Pathophysiologic importance and potential use as a therapeutic target. Rev. Port. Cardiol. 24, 1263-1276.
14. Favaloro, V., Spasic, M., Schwappach, B. and Dobberstein, B. (2008). Distinct targeting pathways for the membrane insertion of tail-anchored (TA) proteins. J. Cell Sci. 121, 1832-1840.
15. Frith, M. C., Forrest, A. R., Nourbakhsh, E., Pang, K. C., Kai, C., Kawai, J., Carninci, P., Hayashizaki, Y., Bailey, T. L. and Grimmond, S. M. (2006). The abundance of short proteins in the mammalian proteome. PLoS Genet. 2, e52.
16. Hassdenteufel, S., Schäuble, N., Cassella, P., Leznicki, P., Müller, A., High, S., Jung, M. and Zimmermann, R. (2011). Ca2+-calmodulin inhibits tail-anchored protein insertion into the mammalian endoplasmic reticulum membrane. FEBS Lett. 585, 3485-3490.
17. Hegde, R. S. and Keenan, R. J. (2011). Tail-anchored membrane protein insertion into the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 12, 787-798.
18. Hessa, T., Sharma, A., Mariappan, M., Eshleman, H. D., Gutierrez, E. and Hegde, R. S. (2011). Protein targeting and degradation are coupled for elimination of mislocalized proteins. Nature 475, 394-397.
19. Klappa, P., Mayinger, P., Pipkorn, R., Zimmermann, M. and Zimmermann, R. (1991). A microsomal protein is involved in ATP-dependent transport of presecretory proteins into mammalian microsomes. EMBO J. 10, 2795-2803.
20. Klappa, P., Zimmermann, M. and Zimmermann, R. (1994). The membrane proteins TRAMp and sec61 alpha p may be involved in post-translational transport of presecretory proteins into mammalian microsomes. FEBS Lett. 341, 281-287.
21. Kutay, U., Hartmann, E. and Rapoport, T. A. (1993). A class of membrane proteins with a C-terminal anchor. Trends Cell Biol. 3, 72-75.
22. Kutay, U., Ahnert-Hilger, G., Hartmann, E., Wiedenmann, B. and Rapoport, T. A. (1995). Transport route for synaptobrevin via a novel pathway of insertion into the endoplasmic reticulum membrane. EMBO J. 14, 217-223.
23. Lakkaraju, A. K. K., Thankappan, R., Mary, C., Garrison, J. L., Taunton, J. and Strub, K. (2012). Efficient secretion of small proteins in mammalian cells relies on Sec62-dependent posttranslational translocation. Mol. Biol. Cell. 23, 2712-2722.
24. Lang, S., Benedix, J., Fedeles, S. V., Schorr, S., Schirra, C., Schäuble, N., Jalal, C., Greiner, M., Haßdenteufel, S., Tatzelt, J. et al. (2012). Different effects of Sec61a, Sec62 and Sec63 depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J. Cell Sci. 125, 1958-1969.
25. Leznicki, P., Clancy, A., Schwappach, B. and High, S. (2010). Bat3 promotes the membrane integration of tail-anchored proteins. J. Cell Sci. 123, 2170-2178.
26. Leznicki, P., Warwicker, J. and High, S. (2011). A biochemical analysis of the constraints of tail-anchored protein biogenesis. Biochem. J. 436, 719-727.
27. Mariappan, M., Li, X., Stefanovic, S., Sharma, A., Mateja, A., Keenan, R. J. and Hegde, R. S. (2010). A ribosome-associating factor chaperones tail-anchored membrane proteins. Nature 466, 1120-1124.
28. Mariappan, M., Mateja, A., Dobosz, M., Bove, E., Hegde, R. S. and Keenan, R. J. (2011). The mechanism of membrane-associated steps in tail-anchored protein insertion. Nature 477, 61-66.
29. McKibbin, C., Mares, A., Piacenti, M., Williams, H., Roboti, P., Puumalainen, M., Callan, A. C., Lesiak-Mieczkowska, K., Linder, S., Harant, H. et al. (2011). Inhibition of protein translocation at the endoplasmic reticulum promotes activation of the unfolded protein response. Biochem. J. 442, 639-648.
30. Müller, G. and Zimmermann, R. (1987). Import of honeybee prepromelittin into the endoplasmic reticulum: structural basis for independence of SRP and docking protein. EMBO J. 6, 2099-2107.
31. Müller, G. and Zimmermann, R. (1988). Import of honeybee prepromelittin into the endoplasmic reticulum: energy requirements for membrane insertion. EMBO J. 7, 639-648.
32. Ng, D. T., Brown, J. D. and Walter, P. (1996). Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134, 269-278.
33. Rabu, C., Wipf, P., Brodsky, J. L. and High, S. (2008). A precursor-specific role for Hsp40/Hsc70 during tail-anchored protein integration at the endoplasmic reticulum. J. Biol. Chem. 283, 27504-27513.
34. Rabu, C., Schmid, V., Schwappach, B. and High, S. (2009). Biogenesis of tail- anchored proteins: the beginning for the end? J. Cell Sci. 122, 3605-3612.
35. Rapoport, T. A., Matlack, K. E., Plath, K., Misselwitz, B. and Staeck, O. (1999). Posttranslational protein translocation across the membrane of the endoplasmic reticulum. Biol. Chem. 380, 1143-1150.
36. Richards, R., Scholz, I., Powers, C., Skach, W. R. and Früh, K. (2011). The cytoplasmic domain of rhesus cytomegalovirus Rh178 interrupts translation of major histocompatibility class I leader peptide-containing proteins prior to translocation. J. Virol. 85, 8766-8776.
37. Schatz, G. and Dobberstein, B. (1996). Common principles of protein translocation across membranes. Science 271, 1519-1526.
38. Schlenstedt, G. and Zimmermann, R. (1987). Import of frog prepropeptide GLa into microsomes requires ATP but does not involve docking protein or ribosomes. EMBO J. 6, 699-703.
39. Schlenstedt, G., Gudmundsson, G. H., Boman, H. G. and Zimmermann, R. (1990). A large presecretory protein translocates both cotranslationally, using signal recognition particle and ribosome, and post-translationally, without these ribonu- cleoparticles, when synthesized in the presence of mammalian microsomes. J. Biol. Chem. 265, 13960-13968.
40. Schlenstedt, G., Gudmundsson, G. H., Boman, H. G. and Zimmermann, R. (1992). Structural requirements for transport of preprocecropinA and related presecretory proteins into mammalian microsomes. J. Biol. Chem. 267, 24328-24332.
41. Schlesinger, D. H. and Hay, D. I. (1977). Complete covalent structure of statherin, a tyrosine-rich acidic peptide which inhibits calcium phosphate precipitation from human parotid saliva. J. Biol. Chem. 252, 1689-1695.
42. Schuldiner, M., Metz, J., Schmid, V., Denic, V., Rakwalska, M., Schmitt, H. D., Schwappach, B. and Weissman, J. S. (2008). The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134, 634-645.
43. Shao, S. and Hegde, R. S. (2011). A calmodulin-dependent translocation pathway for small secretory proteins. Cell 147, 1576-1588.
44. Simpson, P. J., Schwappach, B., Dohlman, H. G. and Isaacson, R. L. (2010). Structures of Get3, Get4, and Get5 provide new models for TA membrane protein targeting. Structure 18, 897-902.
45. Stefanovic, S. and Hegde, R. S. (2007). Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128, 1147-1159.
46. Stefer, S., Reitz, S., Wang, F., Wild, K., Pang, Y. Y., Schwarz, D., Bomke, J., Hein, C., Löhr, F., Bernhard, F. et al. (2011). Structural basis for tail-anchored membrane protein biogenesis by the Get3-receptor complex. Science 333, 758-762.
47. Vilardi, F., Lorenz, H. and Dobberstein, B. (2011). WRB is the receptor for TRC40/ Asna1-mediated insertion of tail-anchored proteins into the ER membrane. J. Cell Sci. 124, 1301-1307.
48. Wang, F., Brown, E. C., Mak, G., Zhuang, J. and Denic, V. (2010). A chaperone cascade sorts proteins for posttranslational membrane insertion into the endoplasmic reticulum. Mol. Cell 40, 159-171.
49. Wiech, H., Sagstetter, M., Müller, G. and Zimmermann, R. (1987). The ATP requiring step in assembly of M13 procoat protein into microsomes is related to preservation of transport competence of the precursor protein. EMBO J. 6, 1011-1016
50. Yabal, M., Brambillasca, S., Soffientini, P., Pedrazzini, E., Borgese, N. and Makarow, M. (2003). Translocation of the C terminus of a tail-anchored protein across the endoplasmic reticulum membrane in yeast mutants defective in signal peptide-driven translocation. J. Biol. Chem. 278, 3489-3496.
51. Zimmermann, R. and Mollay, C. (1986). Import of honeybee prepromelittin into the endoplasmic reticulum. Requirements for membrane insertion, processing, and sequestration. J. Biol. Chem. 261, 12889-12895.
52. Zimmermann, R., Sagstetter, M., Lewis, M. J. and Pelham, H. R. (1988). Seventy- kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes. EMBO J. 7, 2875-2880.
53. Zimmermann, R., Zimmermann, M., Wiech, H., Schlenstedt, G., Müller, G., Morel, F., Klappa, P., Jung, C. and Cobet, W. W. (1990). Ribonucleoparticle-independent transport of proteins into mammalian microsomes. J. Bioenerg. Biomembr. 22, 711- 723.
54. Zimmermann, R., Eyrisch, S., Ahmad, M. and Helms, V. (2011). Protein translocation across the ER membrane. Biochim. Biophys. Acta 1808, 912-924.