Abstract
The toxicity of plant proteins, later identified as ribosome-inactivating proteins (RIPs), was described more than a century ago and their enzymatic activity was established more than 30 years ago. However, their physiological role and related biological activities are still uncertain. Therefore, despite the body of literature, research on RIPs is ongoing. This review deals with new RIPs being purified, sequenced, characterized, and cloned, and an increasing number of 3D-structures that are determined at high resolution. This is the case of the five type 1 RIPs (PD-S1-3, PD-L1/2, PD-L3/4, dioicin 1, and dioicin 2) from seeds and leaves of the ombú tree (Phytolacca dioica L.), native of the grassy pampas of Argentina. The data collected so far will contribute to our understanding of important issues of RIP research: (1) identifying structural determinants responsible for new enzymatic activities such as the DNA cleaving activity; (2) glycosylation and its influence on the catalytic and biological activities; (3) cellular localization of endogenous RIPs and their physiological role(s).
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Notes
- 1.
The genus Phytolacca is suspected to contain a toxic saponin, which causes enteritis with vomiting, abdominal pain and diarrhea. The illness may be fatal (cfr. Saunders Comprehensive Veterinary Dictionary, 3rd edn. © 2007 Elsevier, Inc.). No information is reported of a likely involvement in the symptoms of ribosome-inactivating proteins. Poisoning of cattle and chickens from Phytolacca dioica L. (packalacca) or Phytolacca dodecandra l'Herit were reported (Storie et al. 1992; Mugera 1970).
- 2.
Synonym: P. decandra L.
- 3.
Synonyms: Phytolacca acinosa Maxim. and Phytolacca kaempferi (A. Gray).
- 4.
The ombú tree was introduced in Italy from South America. The plant (also called umbú tree) grows to a height and spread of 60 ft (20 m) or more, often with multiple trunks developing from an enormous base resembling a giant pedestal. The huge base may be 3–6 ft tall (1–2 m) and 95 ft (30 m) in circumference. Ombú tree is native of the grassy pampas of Argentina, usually widely spaced and the only trees for miles. It is dioecious, and the female tree produces large quantities of white, fleshy fruits. It is a salt-resistant species, often planted near the sea.
- 5.
Synonyms and common names. Synonyms (from www.hear.org/pier/species/phytolacca_dioica.htm): Phytolacca arborea Moq., Phytolacca populifolia Salisb., Pircunia dioica Moq., Sarcoca dioica Rafin. Common names (English language): belhambra, packalacca (also trade name) and phytolacca; (Spanish language) bella sombra tree, belombra, ombú and umbú (the last two also trade names).
- 6.
Synonym: Phytolacca abissynica Hoffm.
- 7.
Synonym: Phytolacca octandra L.
- 8.
The protein sequence data of P. dioica RIPs have been deposited in the UniProtKB with accession numbers P34967 for PD-S2, P84853 for PD-L1/2, P84854 for PD-L3/4 and P85208 for dioicin 2.
References
Aceto S, Di Maro A, Conforto B, Siniscalco GS, Parente A, Delli Bovi P, Gaudio L (2005) Nicking activity on pBR322 DNA of ribosome-inactivating proteins from Phytolacca dioica L. leaves. Biol Chem 386:307–317
Adams RLP, Knowler JT, Leader DP (1986) Degradation and modification of nucleic acids. In: The biochemistry of the nucleic acids, 10th edn. Chapman and Hall, London, p 87
Ago H, Kataoka J, Tsuge H, Habuka N, Inagaki E et al (1994) X-ray structure of a pokeweed antiviral protein, coded by a new genomic clone, at 0.23 nm resolution. A model structure provides a suitable electrostatic field for substrate binding. Eur J Biochem 225:369–374
Ak P, Benham CJ (2005) Susceptibility to superhelically driven DNA duplex destabilization: a highly conserved property of yeast replication origins. PLoS Comput Biol 1:e7
Amir-Aslani A, Mauffret O, Bittoun P, Sourgen F, Monnot M, Lescot E, Fennandjian S (1995) Hairpins in a DNA site for topoisomerase II studied by 1H- and 31P-NMR. Nucleic Acids Res 23:3850–3857
Arias FJ, Rojo MA, Ferreras MJ, Iglesias R, Muñoz R, Rocher A, Mendez E, Barbieri L, Girbés T (1992) Isolation and partial characterization of a new ribosome-inactivating protein from Petrocoptis glaucifolia (Lag.) Boiss. Planta 186:532–540
Bagga S, Seth D, Batra JK (2003) The cytotoxic activity of ribosome-inactivating protein saporin-6 is attributed to its rRNA N-glycosidase and internucleosomal DNA fragmentation activities. J Biol Chem 278:4813–4820
Barbieri L, Valbonesi P, Righi F, Zuccheri G, Monti G, Gorini P, Samorì B, Stirpe F (2000) Polynucleotide:adenosine glycosidase is the sole activity of ribosome-inactivating proteins on DNA. J Biochem (Tokyo) 128:883–889
Barbieri L, Brigotti M, Perocco P, Carnicelli D, Ciani M, Mercatali L, Stirpe F (2003) Ribosome-inactivating proteins depurinate poly(ADP-ribosyl)ated poly(ADP-ribose) polymerase and have transforming activity for 3T3 fibroblasts. FEBS Lett 538:178–182
Battelli MG, Lorenzoni E, Stirpe F, Cella R, Parisi B (1984) Differential effect of ribosome-inactivating proteins on plant ribosomes activity and plant cells growth. J Exp Bot 155:882–889
Battelli MG, Barbieri L, Stirpe F (1990) Toxicity of, and histological lesions caused by, ribosome-inactivating proteins, their IgG-conjugates, and their homopolymers. Acta Pathol Microbiol Immunol Scand 98:585–593
Battelli MG, Montacuti V, Stirpe F (1992) High sensitivity of cultured human trophoblasts to ribosome-inactivating proteins. Exp Cell Res 201:109–112
Benham CJ, Bi C (2004) The analysis of stress-induced duplex destabilization in long genomic DNA sequences. J Comput Biol 11:519–543
Boehr DD, Farley AR, Wright GD, Cox JR (2002) Analysis of the pi–pi stacking interactions between the aminoglycoside antibiotic kinase APH(3′)-IIIa and its nucleotide ligands. Chem Biol 9:1209–1217
Brigotti M, Alfieri R, Sestili P, Bonelli M, Petronini PG, Guidarelli A, Barbieri L, Stirpe F, Sperti S (2002) Damage to nuclear DNA induced by Shiga toxin 1 and ricin in human endothelial cells. FASEB J 16:365–372
Carzaniga R, Sinclair L, Fordharm-Skelton AP, Harris N, Croy RDR (1994) Cellular and subcellular distribution of saporins, type-1 ribosome-inactivating proteins, in soapwort (Saponaria officinalis L.). Planta 194:461–470
Ceriotti A, Duranti M, Bollini R (1998) Effects of N-glycosylation on the folding and structure of plant proteins. J Exp Bot 49:1091–1103
Chambery A, Pisante M, Di Maro A, Di Zazzo E, Ruvo M, Costantini S, Colonna G, Parente A (2007) Invariant Ser211 is involved in the catalysis of PD-L4, type I RIP from Phytolacca dioica leaves. Proteins 67:209–218
Chambery A, Di Maro A, Parente A (2008) Primary structure and glycan moiety characterization of PD-Ss, type 1 ribosome-inactivating proteins from Phytolacca dioica L. seeds, by precursor ion discovery on a Q-TOF mass spectrometer. Phytochemistry 69:1973–1982
Dallal JA, Irvin JD (1978) Enzymatic inactivation of eukaryotic ribosomes by the pokeweed antiviral protein. FEBS Lett 89:257–259
Day PJ, Lord JM, Roberts LM (1998) The deoxyribonuclease activity attributed to ribosome-inactivating proteins is due to contamination. Eur J Biochem 258:540–545
Del Vecchio Blanco F, Bolognesi A, Malorni A, Sande MJ, Savino G, Parente A (1997) Complete amino-acid sequence of PD-S2, a new ribosome-inactivating protein from seeds of Phytolacca dioica L. Biochim Biophys Acta 1338:137–144
Desai NA, Shankar V (2003) Single-strand-specific nucleases. FEMS Microbiol Rev 26:457–491
Di Maro A, Del Vecchio Blanco F, Savino G, Parente A (1995) Isolation and characterization of a nicked form of the single-chain ribosome inactivating protein from seeds of Phytolacca dioica L. In: First European symposium of the protein society, vol 4, Protein Science, Davos, Switzerland, p 128 (com 495)
Di Maro A, Valbonesi P, Bolognesi A, Stirpe F, De Luca P et al (1999) Isolation and characterization of four type-1 ribosome-inactivating proteins, with polynucleotide:adenosine glycosidase activity, from leaves of Phytolacca dioica L. Planta 208:125–131
Di Maro A, Chambery A, Daniele A, Casoria P, Parente A (2007) Isolation and characterization of heterotepalins, type 1 ribosome-inactivating proteins from Phytolacca heterotepala leaves. Phytochemistry 68:767–776
Di Maro A, Di Giovannantonio L, Delli Bovi P, De Andrés SF, Parente A (2008) N-terminal amino acid sequences of intact and cleaved forms of mung bean nuclease. Planta Med 74:588–590
Di Maro A, Chambery A, Carafa V, Costantini S, Colonna G et al (2009) Structural characterization and comparative modeling of PD-Ls 1–3, type 1 ribosome-inactivating proteins from summer leaves of Phytolacca dioica L. Biochimie 91:352–363
Duggar BM, Armstrong JK (1925) The effect of treating the virus of TMV with juices of various plants. Ann Missouri Bot Garden 12:359–366
Elbein AD (1991) The role of N-linked oligosaccharides in glycoprotein function. Trends Biotechnol 9:346–352
Esnouf RM (1999) Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr D Biol Crystallogr 55:938–940
Faoro F, Conforto B, Di Maro A, Parente A, Iriti M (2009) Activation of plant defence response contributes to the antiviral activity of diocin 2 from Phytolacca dioica. IOBC/wprs Bull 44:53–57
Fermani S, Falini G, Ripamonti A, Polito L, Stirpe F et al (2005) The 1.4 angstroms structure of dianthin 30 indicates a role of surface potential at the active site of type 1 ribosome inactivating proteins. J Struct Biol 149:204–212
Girbés T, Ferreras JM, Arias FJ, Stirpe F (2004) Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. Mini Rev Med Chem 4:461–476
Guo Q, Zhou W, Too HM, Li J, Liu Y et al (2003) Substrate binding and catalysis in trichosanthin occur in different sites as revealed by the complex structures of several E85 mutants. Protein Eng 16:391–396
Hao Q, Peumans WJ, Van Damme EJ (2001) Type-1 ribosome-inactivating protein from iris (Iris hollandica var. Professor Blaauw) binds specific genomic DNA fragments. Biochem J 357:875–880
Hou X, Chen M, Chen L, Meehan EJ, Xie J et al (2007) X-ray sequence and crystal structure of luffaculin 1, a novel type 1 ribosome-inactivating protein. BMC Struct Biol 7:29
Houston LL, Ramakrishnan S, Hermodson MA (1983) Seasonal variations in different forms of pokeweed antiviral protein, a potent inactivator of ribosomes. J Biol Chem 258:9601–9604
Huang Y, Kowalski D (2003) Web-Thermodyn: sequence analysis software for profiling DNA helical stability. Nucleic Acids Res 31:3819–3821
Huang Q, Liu S, Tang Y, Jin S, Wang Y (1995) Studies on crystal structures, active-centre geometry and depurinating mechanism of two ribosome-inactivating proteins. Biochem J 309:285–298
Iglesias R, Pérez Y, Citores L, Ferreras JM, Méndez E, Girbés T (2008) Elicitor-dependent expression of the ribosome-inactivating protein beetin is developmentally regulated. J Exp Bot 59:1215–1223
Irvin JD (1975) Purification and partial characterization of the antiviral protein from Phytolacca americana which inhibits eukaryotic protein synthesis. Arch Biochem Biophys 169:522–528
Irvin JD, Kelly T, Robertus JD (1980) Purification and properties of a second antiviral protein from Phytolacca americana which inactivates eukaryotic ribosomes. Arch Biochem Biophys 200:418–425
Kassanis B, Kleczkowska I (1948) The isolation and some properties of a virus-inhibiting protein from Phytolacca esculenta. J Gen Microbiol 2:143–153
Kawade K, Masuda K (2009) Transcriptional control of two ribosome-inactivating protein genes expressed in spinach (Spinacia oleracea) embryos. Plant Physiol Biochem 47:327–334
Kowalski D, Kroeker WD, Laskowski MSR (1976) Mung bean nuclease I. Physical, chemical, and catalytical properties. Biochemistry 15:4457–4463
Kowalski D, Natale DA, Eddy MG (1988) Stable DNA unwinding, not ‘breathing’, accounts for single-strand-specific nuclease hypersensitivity of specific A + T-rich sequences. Proc Natl Acad Sci USA 85:9464–9468
Kurinov IV, Uckun FM (2003) High resolution X-ray structure of potent anti-HIV pokeweed antiviral protein-III. Biochem Pharmacol 65:1709–1717
Kurinov IV, Myers DE, Irvin JD, Uckun FM (1999) X-ray crystallographic analysis of the structural basis for the interactions of pokeweed antiviral protein with its active site inhibitor and ribosomal RNA substrate analogs. Protein Sci 8:1765–1772
Ling J, Liu WY, Wang TP (1994) Cleavage of supercoiled double-stranded DNA by several ribosome-inactivating proteins in vitro. FEBS Lett 345:143–146
Lis H, Sharon N (1993) Protein glycosylation. Structural and functional aspects. Eur J Biochem 218:1–27
Mugera GM (1970) Phytolacca dodecandra l'Herit toxicity in livestock in Kenya. Bull Epizoot Dis Afr 18:41–43
Nicolas E, Gooyer ID, Taraschi TF (1997) An additional mechanism of ribosome-inactivating protein cytotoxicity: degradation of extrachromosomal DNA. Biochem J 327:413–417
O’Connor SE, Imperiali B (1996) Modulation of protein structure and function by asparagine-linked glycosylation. Chem Biol 3:803–812
Obrig TG, Irvin JD, Hardesty B (1973) The effect of an antiviral peptide on the ribosomal reactions of the peptide elongation enzymes, EF-I and EF-II. Arch Biochem Biophys 155:278–289
Parente A, De Luca P, Bolognesi A, Barbieri L, Battelli MG, Abbondanza A, Sande JWM, Gigliano SG, Tazzari PL, Stirpe F (1993) Purification and partial characterization of single-chain ribosome-inactivating proteins from the seeds of Phytolacca dioica L. Biochim Biophys Acta 1216:43–49
Parente A, Conforto P, Di Maro A, Chambery A, De Luca P, Bolognesi A, Iriti M, Faoro F (2008) Type 1 ribosome-inactivating proteins from Phytolacca dioica L. leaves: differential seasonal and age expression, and cellular localization. Planta 228:963–975
Park S-W, Lawrence CB, Linden JC, Vivanco JM (2002) Isolation and characterization of a novel ribosome-inactivating protein from root cultures of pokeweed and its mechanism of secretion from roots. Plant Physiol 130:164–178
Park S-W, Vepachedu R, Owens RA, Vivanco JM (2004a) The N-glycosidase activity of the ribosome-inactivating protein ME1 targets single-stranded regions of nucleic acids independent of sequence or structural motifs. J Biol Chem 279:34165–34174
Park S-W, Vepachedu R, Sharma N, Vivanco JM (2004b) Ribosome inactivating proteins in plant biology. Planta 219:1093–1096
Rajamohan F, Venkatachalam TK, Irvin JD, Uckun FM (1999) Pokeweed antiviral protein isoforms PAP-I, PAP-II, and PAP-III depurinate RNA of human immunodeficiency virus (HIV)-1. Biochem Biophys Res Commun 260:453–458
Ready MP, Adams RP, Robertus JD (1984) Dodecandrin, a new ribosome-inhibiting protein from Phytolacca dodecandra. Biochim Biophys Acta 791:314–319
Ready MP, Brown DT, Robertus JD (1986) Extracellular localization of pokeweed antiviral protein. Proc Natl Acad Sci USA 83:5053–5056
Ren J, Wang Y, Dong Y, Stuart DI (1994) The N-glycosidase mechanism of ribosome-inactivating proteins implied by crystal structures of alpha-momorcharin. Structure 2:7–16
Roncuzzi L, Gasperi-Campani A (1996) DNA-nuclease activity of the single-chain ribosome-inactivating proteins dianthin 30, saporin 6 and gelonin. FEBS Lett 392:16–20
Ruggiero A, Chambery A, Di Maro A, Pisante M, Parente A et al (2007a) Crystallization and preliminary X-ray diffraction analysis of PD-L4, a ribosome inactivating protein from Phytolacca dioica L. leaves. Protein Pept Lett 14:97–100
Ruggiero A, Chambery A, Di Maro A, Mastroianni A, Parente A et al (2007b) Crystallization and preliminary X-ray diffraction analysis of PD-L1, a highly glycosylated ribosome inactivating protein with DNase activity. Protein Pept Lett 14:407–409
Ruggiero A, Chambery A, Di Maro A, Parente A, Berisio R (2008) Atomic resolution (1.1 A) structure of the ribosome-inactivating protein PD-L4 from Phytolacca dioica L. leaves. Proteins 71:8–15
Ruggiero A, Di Maro A, Severino V, Chambery A, Berisio R (2009) Crystal structure of PD-L1, a ribosome inactivating protein from Phytolacca dioica L. leaves with the property to induce DNA cleavage. Biopolymers 91:1135–1142
Savino C, Federici L, Ippoliti R, Lendaro E, Tsernoglou D (2000) The crystal structure of saporin SO6 from Saponaria officinalis and its interaction with the ribosome. FEBS Lett 470:239–243
Sawasaki T, Nishihara M, Endo Y (2008) RIP and RALyase cleave the sarcin/ricin domain, a critical domain for ribosome function, during senescence of wheat coleoptiles. Biochim Biophys Res Commun 370:561–565
Schmidt A, Lamzin VS (2002) Veni, vidi, vici – atomic resolution unravelling the mysteries of protein function. Curr Opin Struct Biol 12:698–703
Sharon N, Lis H (1993) Carbohydrates in cell recognition. Sci Am 268:82–89
Sheflin LG, Kowalski D (1985) Altered DNA conformation detected by mung bean nuclease occur in promoter and terminator regions of supercoiled pBR322 DNA. Nucleic Acids Res 13:6137–6154
Song SK, Choi Y, Moon YH, Kim SG, Choi YD, Lee JS (2000) Systemic induction of a Phytolacca insularis antiviral protein gene by mechanical wounding, jasmonic acid, and abscisic acid. Plant Mol Biol 43:439–450
Stirpe F, Battelli MG (2006) Ribosome-inactivating proteins: progress and problems. Cell Mol Life Sci 63:1850–1866
Storie GJ, McKenzie RA, Fraser IR (1992) Suspected packalacca (Phytolacca dioica) poisoning of cattle and chickens. Aust Vet J 69:21–22
Strocchi P, Barbieri L, Stirpe F (1992) Immunological properties of ribosome-inactivating proteins and a saporin immunotoxin. J Immunol Methods 155:57–63
Tazzari PL, Bolognesi A, de Totero D, Falini B, Lemoli RM, Soria MR, Pileri S, Gobbi M, Stein H, Flenghi L et al (1992) Ber-H2 (anti-CD30)-saporin immunotoxin: a new tool for the treatment of Hodgkin's disease and CD30+ lymphoma: in vitro evaluation. Br J Haematol 81:203–211
Thomsen S, Hansen HS, Nyman U (1991) Ribosome-inhibiting proteins from in vitro cultures of Phytolacca dodecandra. Planta Med 57:232–236
Touloupakis E, Gessmann R, Kavelaki K, Christofakis E, Petratos K et al (2006) Isolation, characterization, sequencing and crystal structure of charybdin, a type 1 ribosome-inactivating protein from Charybdis maritima agg. FEBS J 273:2684–2692
Varki A (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97–130
Vesnaver G, Chang CN, Eisenberg M, Grollman AP, Breslauer KJ (1989) Influence of abasic and anucleosidic sites on the stability, conformation, and melting behavior of a DNA duplex: correlations of thermodynamic and structural data. Proc Natl Acad Sci USA 86:3614–3618
Vrielink A, Sampson N (2003) Sub-angstrom resolution enzyme X-ray structures: is seeing believing? Curr Opin Struct Biol 13:709–715
Wang P, Tumer NE (1999a) Pokeweed antiviral protein cleaves double-stranded supercoiled DNA using the same active site required to depurinate rRNA. Nucleic Acids Res 27:1900–1905
Wang YX, Neamati N, Jacob J, Palmer I, Stahl SJ, Kaufman JD, Huang PL, Huang PL, Winslow HE, Pommier Y et al (1999b) Solution structure of anti-HIV-1 and antitumor protein MAP30: structural insights into multiple functions. Cell 99:433–442
Wheat D (1977) Successive cambia in the stem of Phytolacca dioica. Am J Bot 64:1209–1217
Wyss DF, Wagner G (1996) The structural role of sugars in glycoproteins. Curr Opin Biotechnol 7:409–416
Yoshinari S, Yokota S, Sawamoto H, Koresawa S, Tamura M, Endo Y (1996) Purification, characterization and subcellular localization of a type-1 ribosome-inactivating protein from the sarcocarp of Cucurbita pepo. Eur J Biochem 242:585–591
Yoshinari S, Koresawa S, Yokota S, Sawamoto H, Tamura M, Endo Y (1997) Gypsophilin, a new type 1 ribosome-inactivating protein from Gypsophila elegans: purification, enzymatic characterization, and subcellular localization. Biosci Biotechnol Biochem 61:324–331
Zacchia E, Tamburino R, Di Maro A, Parente A (2009) Isolamento e caratterizzazione di forme tagliate di una proteina inattivante i ribosomi da semi di Phytolacca dioica L. Giornate Scientifiche della SUN, VIS-1. http://www.gsa.unina2.it/index.php?option=com_wrapper&Itemid=42
Zeng ZH, He XL, Li HM, Hu Z, Wang DC (2003) Crystal structure of pokeweed antiviral protein with well-defined sugars from seeds at 1.8 Å resolution. J Struct Biol 141:171–178
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Parente, A., Berisio, R., Chambery, A., Di Maro, A. (2010). Type 1 Ribosome-Inactivating Proteins from the Ombú Tree (Phytolacca dioica L.). In: Lord, J., Hartley, M. (eds) Toxic Plant Proteins. Plant Cell Monographs, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12176-0_5
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