Protein domains involved in assembly in the endoplasmic reticulum promote vacuolar delivery when fused to secretory GFP, indicating a protein quality control pathway for degradation in the plant vacuole

Molecular Plant

Volumn 1, Issue 6, 2008, Pages 1067-1076

  Foresti, Ombretta ^a   De Marchis, Francesca ^b   De Virgilio, Maddalena ^a   Klein, Eva M ^a   Arcioni, Sergio ^b   Bellucci, Michele ^b   Vitale, Alessandro ^a  

^a CNR Consiglio Nazionale delle Ricerche   (Italy)

^b CNR   (Italy)

Author keywords

Endoplasmic reticulum; Protein degradation; Protein traffic; Vacuole

Indexed keywords

ANIMALIA; ZEA MAYS;

EID: 70349232046     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssn066     Document Type: Article

References (39)

1. Anelli, T., and Sitia, R. (2008). Protein quality control in the early secretory pathway. EMBO J. 27, 315-327.
2. Gopalan, C. (1997). Co-expression of the maize d- and b-zein genes results in stable accumulation of d-zein in ER-derived protein bodies formed by b-zein. Plant Cell. 9, 1683-1696.
3. Bassham, D.C., and Raikhel, N.V. (2000). Unique features of the plant vacuolar sorting machinery. Curr. Opin. Cell Biol. 12, 491-495.
4. Bellucci, M., Alpini, A., Paolocci, F., Cong, L., and Arcioni, S. (2000). Accumulation of maize c-zein and c-zein:KDEL to high levels in tobacco leaves and differential increase of BiP synthesis in transformants. Theor. Appl. Genet. 101, 796-804.
5. Boevink, P., Martin, B., Oparka, K., Cruz, S.S., and Hawes, C. (1999). Transport of virally expressed green fluorescent protein through the secretory pathway in tobacco leaves is inhibited by cold shock and brefeldin A. Planta. 208, 392-440.
6. Bollini, R., Van der Wilden, W., and Chrispeels, M.J. (1982). A precursor of the reserve protein, phaseolin, is transiently associated with the endoplasmic reticulum of developing Phaseolus vulgaris cotyledons. Physiol. Plant. 55, 82-92.
7. Brandizzi, F., Hanton, S., daSilva, L.L., Boevink, P., Evans, D., Oparka, K., Denecke, J., and Hawes, C. (2003). ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J. 34, 269-281.
8. Coleman, C.E., Herman, E.M., Takasaki, K., and Larkins, B.A. (1996). The maize c-zein sequesters a-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm. Plant Cell. 8, 2335-2345.
9. Coughlan, C.M., Walker, J.L., Cochran, J.C., Wittrup, K.D., and Brodsky, J.L. (2004). Degradation of mutated bovine pancreatic trypsin inhibitor in the yeast vacuole suggests post-endoplasmic reticulum protein quality control. J. Biol. Chem. 279, 15289-15297.
10. Craddock, C.P., Hunter, P.R., Szakacs, E., Hinz, G., Robinson, D.G., and Frigerio, L. (2008). Lack of a vacuolar sorting receptor leads to non-specific missorting of soluble vacuolar proteins in Arabidopsis seeds. Traffic. 9, 408-416.
11. daSilva, L.L., Taylor, J.P., Hadlington, J.L., Hanton, S.L., Snowden, C.J., Fox, S.J., Foresti, O., Brandizzi, F., and Denecke, J. (2005). Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell. 17, 132-148.
12. de Virgilio, M., De Marchis, F., Bellucci, M., Mainieri, D., Rossi, M., Benvenuto, E., Arcioni, S., and Vitale, A. (2008). The human immunodeficiency virus antigen Nef forms protein bodies in leaves of transgenic tobacco when fused to zeolin. J. Exp Bot. [Epub ahead of print].
13. Ding, W.X., Ni, H.M., Gao, W., Hou, Y.F., Melan, M.A., Chen, X., Stolz, D.B., Shao, Z.M., and Yin, X.M. (2007). Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J. Biol. Chem. 282, 4702-4710.
14. Dombrowski, J.E., Gomez, L., Chrispeels, M.J., and Raikhel, N.V. (1994). Targeting of proteins to the vacuole, 2nd edn, In Plant Molecular Biology Manual, Gelvin S.B. and Schilperoort R.A., eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 1-29.
15. Foresti, O., Frigerio, L., Holkeri, H., de Virgilio, M., Vavassori, S., and Vitale, A. (2003). A phaseolin domain involved directly in trimer assembly is a determinant for binding by the chaperone BiP. Plant Cell. 15, 2464-2475.
16. Frigerio, L., de Virgilio, M., Prada, A., Faoro, F., and Vitale, A. (1998). Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. Plant Cell. 10, 1031-1042.
17. Frigerio, L., Foresti, O., Hernández Felipe, D., Neuhaus, J.-M., and Vitale, A. (2001a). The C-terminal tetrapeptide of phaseolin is sufficient to target green fluorescent protein to the vacuole. J. Plant Physiol. 158, 499-503.
18. Frigerio, L., Pastres, A., Prada, A., and Vitale, A. (2001b). Influence of KDEL on the fate of trimeric or assembly-defective phaseolin: selective use of an alternative route to vacuoles. Plant Cell. 13, 1109-1126.
19. Gomord, V., Denmat, L.-A., Fitchette-Lainè , A.-C., Satiat-Jeunemaitre, B., Hawes, C., and Faye, L. (1997). The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J. 11, 313-325.
20. Haseloff, J., Siemering, K.R., Prasher, D.C., and Hodge, S. (1997). Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl Acad. Sci. U S A. 94, 2122-2127.
21. Hoffman, L.M., Donaldson, D.D., and Herman, E.M. (1988). A modified storage protein is synthesized, processed, and degraded in the seeds of transgenic plants. Plant Mol. Biol. 11, 717-729.
22. Hoffman, L.M., Donaldson, D.D., Bookland, R., Rashka, K., and Herman,E.M.(1987).Synthesisandproteinbodydepositionofmaize 15-KD zein in transgenic tobacco seeds. EMBO J. 6, 3213-3221.
23. Hong, E., Davidson, A.R., and Kaiser, C.A. (1996). A pathway for targeting soluble misfolded proteins to the yeast vacuole. J. Cell Biol. 135, 623-633.
24. Jürgens, G. (2004). Membrane trafficking in plants. Annu. Rev. Cell Dev. Biol. 20, 481-504.
25. Kruse, K.B., Brodsky, J.L., and McCracken, A.A. (2006). Characterization of an ERAD gene as VPS30/ATG6 reveals two alternative and functionally distinct protein quality control pathways: one for soluble Z variant of human a-1 proteinase inhibitor (A1PiZ) and another for aggregates of A1PiZ. Mol. Biol. Cell. 17, 203-212.
26. Mainieri, D., Rossi, M., Archinti, M., Bellucci, M., De Marchis, F., Vavassori, S., Pompa, A., Arcioni, S., and Vitale, A. (2004). Zeolin: a new recombinant storage protein constructed using maize c-zein and bean phaseolin. Plant Physiol. 136, 3447-3456.
27. Pedrazzini, E., Giovinazzo, G., Bielli, A., de Virgilio, M., Frigerio, L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A., and Vitale, A. (1997). Protein quality control along the route to the plant vacuole. Plant Cell. 9, 1869-1880.
28. Pimpl, P., Taylor, J.P., Snowden, C., Hillmer, S., Robinson, D.G., and Denecke, J. (2006). Golgi-mediated vacuolar sorting of the endoplasmic reticulum chaperone BiP may play an active role in quality control within the secretory pathway. Plant Cell. 18, 198-211.
29. Pompa, A., and Vitale, A. (2006). Retention of a bean phaseolin/ maize gamma-zein fusion in the endoplasmic reticulum depends on disulfide bond formation. Plant Cell. 18, 2608-2621.
30. Pueyo, J.J., Chrispeels, M.J., and Herman, E.M. (1995). Degradation of transport-competent destabilized phaseolin with a signal for retention in the endoplasmic reticulum occurs in the vacuole. Planta. 196, 586-596.
31. Purhonen, P., Pursiainen, K., and Reunanen, H. (1997). Effects of brefeldin A on autophagy in cultured rat fibroblasts. Eur. J. Cell Biol. 74, 63-67.
32. Reichel, C., Mathur, J., Eckes, P., Langenkemper, K., Koncz, C., Schell, J., Reiss, B., and Maas, C. (1996). Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proc. Natl Acad. Sci. U S A. 93, 5888-5893.
33. Shewry, P.R., and Halford, N.G. (2002). Cereal seed storage proteins: structures, properties and role in grain utilization. J. Exp. Bot. 53, 947-958.
34. Shimada, T., Fuji, K., Tamura, K., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003). Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 100, 16095-16100.
35. Tamura, K., Yamada, K., Shimada, T., and Hara-Nishimura, I. (2004). Endoplasmic reticulum-resident proteins are constitutively transported to vacuoles for degradation. Plant J. 39, 393-402.
36. Teckman, J.H., and Perlmutter, D.H. (2000). Retention of mutant alpha(1)-antitrypsin Z in endoplasmic reticulum is associated with an autophagic response. Am. J Physiol. Gastrointest. Liver Physiol. 279, G961-G974.
37. Vitale, A., and Boston, R.S. (2008). Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic. [Epub ahead of print].
38. Vitale, A., Bielli, A., and Ceriotti, A. (1995). The binding protein associates with monomeric phaseolin. Plant Physiol. 107, 1411-1418.
39. Zheng, H., Kunst, L., Hawes, C., and Moore, I. (2004). A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus. Plant J. 37, 398-414.