Signal peptide-regulated toxicity of a plant ribosome-inactivating protein during cell stress

Plant Journal

Volumn 65, Issue 2, 2011, Pages 218-229

  Marshall, Richard S ^a   D'Avila, Francesca ^a,c   Di Cola, Alessandra ^b,d   Traini, Roberta ^a,e   Spanò, Laura ^b   Fabbrini, Maria Serena ^a   Ceriotti, Aldo ^a  

^a CNR Consiglio Nazionale delle Ricerche   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d RUBBER RESEARCH INSTITUTE OF MALAYSIA   (Malaysia)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

endoplasmic reticulum; ribosome inactivating protein; ricin; saporin; signal peptide; toxicity

Indexed keywords

ENDOPLASMIC RETICULUM; RIBOSOME-INACTIVATING PROTEIN; RICIN; SAPORIN; SIGNAL PEPTIDE;

CATALYST ACTIVITY; OPTICAL COMMUNICATION; PEPTIDES; TOBACCO;

TOXICITY;

CHAPERONE; HYBRID PROTEIN; ISOPROTEIN; PROTEIN SYNTHESIS INHIBITOR; RIBOSOME INACTIVATING PROTEIN 1; SAPORIN; SIGNAL PEPTIDE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; INTRACELLULAR SPACE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN TRANSPORT; PROTOPLAST; RIBOSOME; SAPONARIA; TOBACCO;

AMINO ACID SEQUENCE; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, PLANT; GLYCOSYLATION; INTRACELLULAR SPACE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN ISOFORMS; PROTEIN SORTING SIGNALS; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; PROTOPLASTS; RECOMBINANT FUSION PROTEINS; RIBOSOME INACTIVATING PROTEINS, TYPE 1; RIBOSOMES; SAPONARIA; STRESS, PHYSIOLOGICAL; TOBACCO;

NICOTIANA TABACUM;

EID: 78651385566     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04413.x     Document Type: Article

References (71)

1. Bagga, S., Seth, D., and, Batra, J.K., (2003) The cytotoxic activity of the ribosome inactivating protein saporin-6 is attributed to its rRNA N-glycosidase and internucleosomal DNA fragmentation activities. J. Biol. Chem. 278, 4813-4820.
2. Baykal, U., and, Tumer, N.E., (2007) The C-terminus of pokeweed antiviral protein has distinct roles in transport to the cytosol, ribosome depurination and cytotoxicity. Plant J. 49, 995-1007.
3. Bendtsen, J.D., Nielsen, H., von Heijne, G., and, Brunak, S., (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795.
4. Butterworth, A.G., and, Lord, J.M., (1983) Ricin and Ricinus communis agglutinin subunits are all derived from a single-size polypeptide precursor. Eur. J. Biochem. 137, 57-65.
5. Carzaniga, R., Sinclair, L., Fordham-Skelton, A.P., Harris, N., and, Croy, R.R.D., (1994) Cellular and subcellular distribution of saporins, type I ribosome-inactivating proteins, in soapwort (Saponaria officinalis L.). Planta, 194, 461-470.
6. Ceriotti, A., and, Roberts, L.M., (2006) Endoplasmic reticulum-associated protein degradation in plant cells. In Plant Cell Monographs: The Plant Endoplasmic Reticulum (, Robinson, D.G., ed.). Berlin/Heidelberg, Germany: Springer-Verlag, pp. 75-98.
7. Ceriotti, A., Pedrazzini, E., De Silvestris, M., and, Vitale, A., (1995) Import into the endoplasmic reticulum. In Methods in Cell Biology, Volume 50, Part B: Methods in Plant Cell Biology (, Galbraith, D.W., Bourque, D.P., and, Bohnert, H.J., eds). San Diego, USA: Academic Press, pp. 295-308.
8. Ceriotti, A., Vitale, A., Paris, N., Frigerio, L., Neuhaus, J.M., Hillmer, S., and, Robinson, D.G., (2003) Plant cell biology. In Essential Cell Biology, Volume 1: Cell Structure (, Davey, J., and, Lord, J.M., eds). New York, USA: Oxford University Press, pp. 133-161.
9. Chamberlain, K.L., Marshall, R.S., Jolliffe, N.A., Frigerio, L., Ceriotti, A., Lord, J.M., and, Roberts, L.M., (2008) Ricin B chain targeted to the endoplasmic reticulum of tobacco protoplasts is degraded by a CDC48- and vacuole-independent mechanism. J. Biol. Chem. 283, 33276-33286.
10. Cho, H.J., Kim, S., Kim, M., and, Kim, B.D., (2001) Production of transgenic male sterile tobacco plants with the cDNA encoding a ribosome inactivating protein from Dianthus sinensis L. Mol. Cells, 3, 326-333.
11. Corrado, G., Delli Bovi, P., Ciliento, R., Gaudio, L., Di Maro, A., Aceto, S., Lorito, M., and, Rao, R., (2005) Inducible expression of a Phytolacca heterotepala ribosome inactivating protein leads to enhanced resistance against major fungal pathogens in tobacco. Phytopathology, 95, 206-215.
12. Dai, W.D., Bonos, S., Guo, Z., Meyer, W.A., Day, P.R., and, Belanger, F.C., (2003) Expression of pokeweed antiviral proteins in creeping bentgrass. Plant Cell Rep. 21, 497-502.
13. Denecke, J., Goldman, M.H.S., Demolder, J., Seurinck, J., and, Botterman, J., (1991) The tobacco luminal binding protein is encoded by a multigene family. Plant Cell, 3, 1025-1035.
14. Desvoyes, B., Poyet, J.L., Schlick, J.L., Adami, P., Jouvenot, M., and, Dulieu, P., (1997) Identification of a biological inactive complex form of pokeweed antiviral protein. FEBS Lett. 410, 303-308.
15. Di Cola, A., Marcozzi, G., Balestrini, R., and, Spanà, L., (1999) Localisation of a type I ribosome inactivating protein, luffin, in adult and embryonic tissues of Luffa cilindrica L. Roem. J. Exp. Bot. 50, 573-579.
16. Di Cola, A., Frigerio, L., Lord, J.M., Ceriotti, A., and, Roberts, L.M., (2001) Ricin A chain without its partner B chain is degraded after retrotranslocation from the endoplasmic reticulum to the cytosol in plant cells. Proc. Natl Acad. Sci. USA, 98, 14726-14731.
17. Di Cola, A., Frigerio, L., Lord, J.M., Roberts, L.M., and, Ceriotti, A., (2005) Endoplasmic reticulum-associated degradation of ricin A chain has unique and plant-specific features. Plant Physiol. 137, 287-296.
18. Dickinson, C.D., Floener, L.A., Lilley, G.G., and, Nielsen, N.C., (1987) Self-assembly of proglycinin and hybrid proglycinin synthesised in vitro from cDNA. Proc. Natl Acad. Sci. USA, 84, 5525-5529.
19. Endo, Y., and, Tsurugi, K., (1987) RNA N-glycosidase activity of ricin A chain: mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J. Biol. Chem. 262, 8128-8130.
20. Fabbrini, M.S., Carpani, D., Soria, M.R., and, Ceriotti, A., (2000) Cytosolic immunization allows the expression of preATF-saporin chimeric toxin in eukaryotic cells. FASEB J. 14, 391-398.
21. Frigerio, L., Vitale, A., Lord, J.M., Ceriotti, A., and, Roberts, L.M., (1998) Free ricin A chain, proricin, and native toxin have different cellular fates when expressed in tobacco protoplasts. J. Biol. Chem. 273, 14194-14199.
22. Frigerio, L., Jolliffe, N.A., Di Cola, A., Felipe, D.H., Paris, N., Neuhaus, J.M., Lord, J.M., Ceriotti, A., and, Roberts, L.M., (2001) The internal propeptide of the ricin precursor carries a sequence-specific determinant for vacuolar sorting. Plant Physiol. 126, 167-175.
23. Gavel, Y., and, von Heijne, G., (1990) Sequence differences between glycosylated or non-glycosylated Asn-X-Ser/Thr acceptor sites: implications for protein engineering. Protein Eng. 3, 433-442.
24. Hartley, M.R., and, Lord, J.M., (2004) Cytotoxic ribosome inactivating lectins from plants. Biochim. Biophys. Acta, 1701, 1-14.
25. Hatsugai, N., Iwasaki, S., Tamura, K., Kondo, M., Fuji, K., Ogasawara, K., Nishimura, M., and, Hara-Nishimura, I., (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev. 23, 2496-2506.
26. Hazes, B., and, Read, R.J., (1997) Accumulating evidence suggests that several AB toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry, 36, 11051-11054.
27. Hiraiwa, N., Kondo, M., Nishimura, M., and, Hara-Nishimura, I., (1997) An aspartic endopeptidase is involved in the breakdown of propeptides from storage proteins in protein storage vacuoles of plants. Eur. J. Biochem. 246, 133-141.
28. Hong, Y., Saunders, K., Hartley, M.R., and, Stanley, J., (1996) Resistance to geminivirus infection by virus-induced expression of dianthin in transgenic plants. Virology, 220, 119-127.
29. Iwata, Y., and, Koizumi, N., (2005) Unfolded protein response followed by induction of cell death in cultured tobacco cells treated with tunicamycin. Planta, 220, 804-807.
30. Jarosch, E., Taxis, C., Volkwein, C., Bordallo, J., Finley, D., Wolf, D.H., and, Sommer, T., (2002) Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4, 134-139.
31. Jelitto-Van Dooren, E.P.W.M., Vidal, S., and, Denecke, J., (1999) Anticipating endoplasmic reticulum stress: a novel early response before pathogenesis-related gene induction. Plant Cell, 11, 1935-1943.
32. Jolliffe, N.A., Ceriotti, A., Frigerio, L., and, Roberts, L.M., (2003) The position of the proricin vacuolar targeting signal is functionally important. Plant Mol. Biol. 51, 631-641.
33. Jolliffe, N.A., Brown, J.C., Neuman, U., Vicré, M., Bachi, A., Hawes, C., Ceriotti, A., Roberts, L.M., and, Frigerio, L., (2004) Transport of ricin and 2S albumin precursors to the storage vacuoles of Ricinus communis endosperm involves the Golgi and VSR-like receptors. Plant J. 39, 821-833.
34. Jolliffe, N.A., Di Cola, A., Marsden, C.J., Lord, J.M., Ceriotti, A., Frigerio, L., and, Roberts, L.M., (2006) The N-terminal ricin propeptide influences the fate of ricin A chain in tobacco protoplasts. J. Biol. Chem. 281, 23377-23385.
35. Kang, S.W., Rane, N.S., Kim, S.J., Garrison, J.L., Taunton, J., and, Hegde, R.S., (2006) Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell, 127, 999-1013.
36. Krishnan, R., McDonald, K.A., Dandekar, A.M., Jackman, A.P., and, Falk, B., (2002) Expression of recombinant trichosanthin, a ribosome inactivating protein, in transgenic tobacco. J. Biotechnol. 97, 69-88.
37. Kyte, J., and, Doolittle, R.F., (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
38. Levine, C.G., Mitra, D., Sharma, A., Smith, C.L., and, Hegde, R.S., (2005) The efficiency of protein compartmentalization into the secretory pathway. Mol. Biol. Cell, 16, 279-291.
39. Lodge, J.K., Kaniewski, W.K., and, Tumer, N.E., (1993) Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proc. Natl Acad. Sci. USA, 90, 7089-7093.
40. Lombardi, A., Bursomanno, S., Lopardo, T., Traini, R., Colombatti, M., Ippoliti, R., Flavell, D.J., Flavell, S.U., Ceriotti, A., and, Fabbrini, M.S., (2010a) Pichia pastoris as a host for secretion of toxic saporin chimeras. FASEB J. 24, 253-265.
41. Lombardi, A., Marshall, R.S., Savino, C., Fabbrini, M.S., and, Ceriotti, A., (2010b) Type I ribosome inactivating proteins from Saponaria officinalis. In Plant Cell Monographs: Toxic Plant Proteins (, Lord, J.M., and, Hartley, M.R., eds). Berlin/Heidelberg, Germany: Springer-Verlag, pp. 55-78.
42. Maliga, P., Sz-Breznovits, A., and, Marton, L., (1973) Streptomycin-resistant plants from callus culture of haploid tobacco. Nature New Biol. 244, 29-30.
43. Maras, B., Ippoliti, R., De Luca, E., Lendaro, E., Bellelli, A., Barra, D., Bossa, F., and, Brunori, M., (1990) The amino acid sequence of a ribosome-inactivating protein from Saponaria officinalis seeds. Biochem. Int. 21, 831-838.
44. Marshall, R.S., Jolliffe, N.A., Ceriotti, A., Snowden, C.J., Lord, J.M., Frigerio, L., and, Roberts, L.M., (2008) The role of CDC48 in the retrotranslocation of non-ubiquitinated toxin substrates in plant cells. J. Biol. Chem. 283, 15869-15877.
45. Martin, W., Nock, S., Meyer-Gauen, G., Häger, K.P., Jensen, U., and, Cerff, R., (1993) A method for isolation of cDNA-quality mRNA from immature seeds of a gymnosperm rich in polyphenolics. Plant Mol. Biol. 22, 555-556.
46. May, M.J., Hartley, M.R., Roberts, L.M., Krieg, P.A., Osborn, R.W., and, Lord, J.M., (1989) Ribosome inactivation by ricin A chain: a sensitive method to assess the activity of wild-type and mutant polypeptides. EMBO J. 8, 301-308.
47. Melchers, L.S., Sela-Buurlage, M.B., Vloemans, S.A., Woloshuk, C.P., Van Roekel, J.S., Pen, J., van den Elzen, P.J., and, Cornelissen, B.J., (1993) Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and β-1,3-glucanase in transgenic plants. Plant Mol. Biol. 21, 583-593.
48. Moazed, D., Robertson, J.M., and, Noller, H.F., (1998) Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S rRNA. Nature, 334, 362-364.
49. Nielsen, K., and, Boston, R.S., (2001) Ribosome-inactivating proteins: a plant perspective. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 785-816. (Pubitemid 33720055)
50. Orsi, A., Fioriti, L., Chiesa, R., and, Sitia, R., (2006) Conditions of endoplasmic reticulum stress favour the accumulation of cytosolic prion protein. J. Biol. Chem. 281, 30431-30438.
51. 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.
52. Peumans, W.J., Hao, Q., and, Van Damme, E.J.M., (2001) Ribosome-inactivating proteins from plants: more than RNA N-glycosidases. FASEB J. 15, 1493-1506.
53. Pittaluga, E., Poma, A., Tucci, A., and, Spanà, L., (2005) Expression and characterisation of mutant forms of saporin in Escherichia coli. J. Biotechnol. 117, 263-266.
54. Rabinovich, E., Kerem, A., Fröhlich, K.U., Diamant, N., and, Bar-Nun, S., (2002) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22, 626-634.
55. Rane, N.S., Kang, S.W., Chakrabarti, O., Feigenbaum, L., and, Hegde, R.S., (2008) Reduced translocation of nascent prion protein during ER stress contributes to neurodegeneration. Dev. Cell, 15, 359-370.
56. Rane, N.S., Chakrabarti, O., Feigenbaum, L., and, Hegde, R.S., (2010) Signal sequence insufficiency contributes to neurodegeneration caused by transmembrane prion protein. J. Cell Biol. 188, 515-526.
57. Ready, M.P., Brown, D.T., and, Robertus, J.D., (1986) Extracellular localisation of pokeweed antiviral protein. Proc. Natl Acad. Sci. USA, 83, 5053-5056.
58. Savino, C., Federici, L., Ippoliti, R., Lendaro, E., and, Tsernoglou, D., (2000) The crystal structure of saporin SO6 from Saponaria officinalis and its interaction with the ribosome. FEBS Lett. 470, 239-243.
59. Scheele, G., and, Jacoby, R., (1982) Conformational changes associated with proteolytic processing of presecretory proteins allow glutathione-catalysed formation of native disulphide bonds. J. Biol. Chem. 257, 12277-12282.
60. Shaffer, K.L., Sharma, A., Snapp, E.L., and, Hegde, R.S., (2005) Regulation of protein compartmentalization expands the diversity of protein function. Dev. Cell, 9, 545-554.
61. Shinshi, H., Wenzler, H., Neuhaus, J.M., Felix, G., Hofsteenge, J., and, Meins, F.J., (1988) Evidence for N- and C-terminal processing of a plant defense-related enzyme: primary structure of tobacco prepro-β-1,3- glucanase. Proc. Natl Acad. Sci. USA, 85, 5541-5545.
62. Smirnov, S., Shulaev, V., and, Tumer, N.E., (1997) Expression of pokeweed antiviral protein in transgenic plants induces virus resistance in grafted wild-type plants independently of salicylic acid accumulation and pathogenesis-related protein synthesis. Plant Physiol. 114, 1113-1121.
63. Stirpe, F., Gasperi-Campani, A., Barbieri, L., Falasca, A., Abbondanza, A., and, Stevens, W.A., (1983) Ribosome inactivating proteins from seeds of Saponaria officinalis L. (soapwort), Agrostemma githago L. (corn cockle) and Asparagus officinalis L. (asparagus), and from latex of Hura crepitans L. (sandbox tree). Biochem. J. 216, 617-625.
64. Tartarini, A., Pittaluga, E., Marcozzi, G., Testone, G., Rodrigues-Pousada, R.A., Giannino, D., and, Spanà, L., (2010) Differential expression of saporin genes upon wounding, ABA treatment and leaf development. Physiol. Plant. 140, 141-152.
65. Taylor, S., Massiah, A., Lomonossoff, G., Roberts, L.M., Lord, J.M., and, Hartley, M.R., (1994) Correlation between the activities of five ribosome-inactivating proteins in depurination of tobacco ribosomes and inhibition of tobacco mosaic virus infection. Plant J. 5, 827-835.
66. Tumer, N.E., Hwang, D.J., and, Bonness, M., (1997) C-terminal deletion mutant of pokeweed antiviral protein inhibits viral infection but does not depurinate host ribosomes. Proc. Natl Acad. Sci. USA, 94, 3866-3871.
67. Vandenbussche, F., Peumans, W.J., Desmyter, S., Proost, P., Ciani, M., and, Van Damme, E.J.M., (2004) The type I and type II ribosome inactivating proteins from Iris confer transgenic tobacco plants local but not systemic protection against viruses. Planta, 220, 211-221.
68. Vitale, A., and, Boston, R.S., (2008) Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic, 9, 1581-1588.
69. Ye, Y., Meyer, H.H., and, Rapoport, T.A., (2001) The AAA-ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature, 414, 652-656.
70. Yoshinari, S., Koresawa, S., Yokota, S., Sawamoto, H., Tamura, M., and, Endo, Y., (1997) Gypsophilin, a new type I ribosome inactivating protein from Gypsophila elegans: purification, enzymatic characterization, and subcellular localization. Biosci. Biotechnol. Biochem. 61, 324-331.
71. Zoubenko, O., Hudak, K., and, Tumer, N.E., (2000) A non-toxic pokeweed antiviral protein mutant inhibits pathogen infection via a novel salicylic acid-independent pathway. Plant Mol. Biol. 44, 219-229.