Abstract
Euphorbiaceae, also known as the spurge family, is a large group of flowering plants. Despite being tropical natives, they are now widespread. Due to its medicinal and commercial importance, this family of plants attracted a lot of attention in the scientific community. The distinctive characteristic of the family is production of milky latex, which is a rich source of several lectins, the proteins that bind carbohydrates. Although their function is unclear, they are believed to defend plants against damaging phytopathogenic microorganisms, insects, and predatory animals. Additionally, they serve as crucial metabolic regulators under a variety of stressors. Detection, separation, purification, and characterization of lectins from the Euphorbiaceae family – mostly from the latex of plants – began over 40 years ago. This effort produced over 35 original research papers that were published. However, no systematic review that compiles these published data has been presented yet. This review summarizes and describes several procedures and protocols employed for extraction and purification of lectins belonging to this family. Physicochemical properties and biological activities of the lectins, along with their medicinal and pharmacological properties, have also been analyzed. Additionally, using examples of ricin and ricin agglutinin, we have structurally analyzed characteristics of the lectin known as Ribosome Inactivating Protein Type II (RIP-Type II) that belongs to this family. We anticipate that this review article will offer a useful compendium of information on this important family of lectins, show the scientists involved in lectin research the gaps in our knowledge, and offer insights for future research.
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References
Raj, S. P., Solomon, P. R., Thangaraj, B., Raj, S. P., Solomon, P. R., and Thangaraj, B. (2022) Euphorbiaceae, Biodiesel from Flowering Plants, Springer, pp. 207-290, https://doi.org/10.1007/978-981-16-4775-8_18.
Raju, A. S., and Ezradanam, V. (2002) Pollination ecology and fruiting behaviour in a monoecious species, Jatropha curcas L. (Euphorbiaceae), Curr. Sci., 83, 1395-1398.
Di Stefano, V., Pitonzo, R., and Schillaci, D. (2011) Chemical constituents and antiproliferative activity of Euphorbia bivonae, Chem. Nat. Compounds, 47, 660, https://doi.org/10.1007/s10600-011-0026-y.
Webster, G. L. (1967) The genera of Euphorbiaceae in the southeastern United States, J. Arnold Arboretum, 48, 363-430, https://doi.org/10.5962/p.185727.
Olsen, K. M., and Schaal, B. A. (1999) Evidence on the origin of cassava: phylogeography of Manihot esculenta, Proc. Natl. Acad. Sci. USA, 96, 5586-5591, https://doi.org/10.1073/pnas.96.10.5586.
Lopez, C., Soto, M., Restrepo, S., Piégu, B., Cooke, R., Delseny, M., Tohme, J., and Verdier, V. (2005) Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray, Plant Mol. Biol., 57, 393-410, https://doi.org/10.1007/s11103-004-7819-3.
Abdudeen, A., Selim, M. Y., Sekar, M., and Elgendi, M. (2023) Jatropha’s rapid developments and future opportunities as a renewable source of biofuel – a review, Energies, 16, 828, https://doi.org/10.3390/en16020828.
Martins, C. G., Appel, M. H., Coutinho, D. S. S., Soares, I. P., Fischer, S., de Oliveira, B. C., Fachi, M. M., Pontarolo, R., Bonatto, S. J. R., Fernandes, L. C., Iagher, F., and de Souza, L. M. (2020) Consumption of latex from Euphorbia tirucalli L. promotes a reduction of tumor growth and cachexia, and immunomodulation in Walker 256 tumor-bearing rats, J. Ethnopharmacol., 255, 112722, https://doi.org/10.1016/j.jep.2020.112722.
Mali, P. Y., and Panchal, S. S. (2017) Euphorbia tirucalli L. : review on morphology, medicinal uses, phytochemistry and pharmacological activities, Asian Pac. J. Tropical Biomed., 7, 603-613, https://doi.org/10.1016/j.apjtb.2017.06.002.
Peumans, W. J., and Damme, E. J. V. (1998) Plant lectins: versatile proteins with important perspectives in biotechnology, Biotechnol. Genet. Engin. Rev., 15, 199-228, https://doi.org/10.1080/02648725.1998.10647956.
Hamid, R., Masood, A., Wani, I. H., and Rafiq, S. (2013) Lectins: proteins with diverse applications, J. Appl. Pharmaceut. Sci., 3, S93-S103.
Wolin, I. A., Heinrich, I. A., Nascimento, A. P. M., Welter, P. G., Sosa, L. d. V., De Paul, A. L., Zanotto-Filho, A., Nedel, C. B., Lima, L. D., and Osterne, V. J. S. (2021) ConBr lectin modulates MAPKs and Akt pathways and triggers autophagic glioma cell death by a mechanism dependent upon caspase-8 activation, Biochimie, 180, 186-204, https://doi.org/10.1016/j.biochi.2020.11.003.
Santos, A. F., Da Silva, M., Napoleão, T., Paiva, P., Correia, M. D. S., and Coelho, L. (2014) Lectins: Function, structure, biological properties andpotential applications, Curr. Top. Pept. Protein Res., 15, 41-62.
Polito, L., Bortolotti, M., Battelli, M. G., Calafato, G., and Bolognesi, A. (2019) Ricin: an ancient story for a timeless plant toxin, Toxins, 11, 324, https://doi.org/10.3390/toxins11060324.
Benjamaa, R., Moujanni, A., Kaushik, N., Choi, E. H., Essamadi, A. K., and Kaushik, N. K. (2022) Euphorbia species latex: a comprehensive review on phytochemistry and biological activities, Front. Plant Sci., 13, 1008881, https://doi.org/10.3389/fpls.2022.1008881.
Mwine, T. J., and Van Damme, P. (2011) Evaluation of pesticidal properties of Euphorbia tirucalli L. (Euphorbiaceae) against selected pests, Afrika Focus, 24, 119-121, https://doi.org/10.21825/af.v24i1.18035.
Jawade, A. A., Pingle, S. K., Tumane, R. G., Sharma, A. S., Ramteke, A. S., and Jain, R. K. (2016) Isolation and characterization of lectin from the leaves of Euphorbia tithymaloides (L.), Tropical Plant Res., 3, 634-641, https://doi.org/10.22271/tpr.2016.v3.i3.083.
Van Deenen, N., Prüfer, D., and Schulze Gronover, C. (2011) A latex lectin from Euphorbia trigona is a potent inhibitor of fungal growth, Biol. Plant., 55, 335-339, https://doi.org/10.1007/s10535-011-0049-z.
Kusuma, V., and Kottapalli, S. (2023) Purification and characterization of a novel anti-tumour galactose binding lectin from Euphorbia caducifolia latex, bioRxiv, https://doi.org/10.1101/2023.03.10.532027.
Siritapetawee, J., Limphirat, W., Wongviriya, W., Maneesan, J., and Samosornsuk, W. (2018) Isolation and characterization of a galactose-specific lectin (EantH) with antimicrobial activity from Euphorbia antiquorum L. latex, Int. J. Biol. Macromol., 120, 1846-1854, https://doi.org/10.1016/j.ijbiomac.2018.09.206.
Nsimba-Lubaki, M., Allen, A. K., and Peumans, W. J. (1986) Isolation and partial characterization of latex lectins from three species of the genus Euphorbia (Euphorbiaceae), Physiol. Plant., 67, 193-198, https://doi.org/10.1111/j.1399-3054.1986.tb02442.x.
Bhat, G. G., Shetty, K. N., Nagre, N. N., Neekhra, V. V., Lingaraju, S., Bhat, R. S., Inamdar, S. R., Suguna, K., and Swamy, B. M. (2010) Purification, characterization and molecular cloning of a monocot mannose-binding lectin from Remusatia vivipara with nematicidal activity, Glycoconjug. J., 27, 309-320, https://doi.org/10.1007/s10719-010-9279-0.
Wittsuwannakul, R., Wititsuwannakul, D., and Sakulborirug, C. (1998) A lectin from the bark of the rubber tree (Hevea brasiliensis), Phytochemistry, 47, 183-187, https://doi.org/10.1016/S0031-9422(97)00329-4.
Torky, Z. A. (2016) Antiviral activity of euphorbia lectin against herpes simplex virus 1 and its antiproliferative activity against human cancer cell-line, J. Antiviral. Antiretroviral., 8, 107-116, https://doi.org/10.4172/jaa.1000145.
Rafiq, S., Qadir, S., Wani, I. H., Ganie, S. A., Masood, A., and Hamid, R. (2014) Purification and partial characterization of a fructose-binding lectin from the leaves of Euphorbia helioscopia, Pak. J. Pharm. Sci., 27, 1805-1810.
Seshagirirao, K., and Prasad, M. N. V. (1995) Purification and partial charaterization of a lectin from Euphorbia neriifolia latex, Biochem. Mol. Biol. Int., 35, 1199-1204.
Seshagirirao, K. (1995) Purification and partial characterization of a lectin from Pedilanthus tithymaloides latex, Biochem. Arch., 11, 197-202.
Stirpe, F., Licastro, F., Morini, M. C., Parente, A., Savino, G., Abbondanza, A., Bolognesi, A., Falasca, A. I., and Rossi, C. A. (1993) Purification and partial characterization of a mitogenic lectin from the latex of Euphorbia marginata, Biochim. Biophys. Acta Gen. Subj., 1158, 33-39, https://doi.org/10.1016/0304-4165(93)90093-N.
Lynn, K., and Clevette-Radford, N. (1986) Lectins from latices of euphorbia and elaeophorbia species, Phytochemistry, 25, 1553-1557, https://doi.org/10.1016/S0031-9422(00)81207-8.
Inamdar, S. R., Murugiswamy, B., and Madaiah, M. (1988) Purification and characterization of a lectin from Euphorbia nivulia Buch. Ham. latex, Int. J. Peptide Protein Res., 31, 35-46, https://doi.org/10.1111/j.1399-3011.1988.tb00004.x.
Nsimba-Lubaki, M., Peumans, W. J., and Carlier, A. R. (1983) Isolation and partial characterization of a lectin from Euphorbia heterophylla seeds, Biochem. J., 215, 141, https://doi.org/10.1042/bj2150141.
Villanueva, J., Quirós, L. M., and Castañón, S. (2015) Purification and partial characterization of a ribosome-inactivating protein from the latex of Euphorbia trigona Miller with cytotoxic activity toward human cancer cell lines, Phytomedicine, 22, 689-695, https://doi.org/10.1016/j.phymed.2015.04.006.
Al Gaali, A., Modawe, G., Ahmed, R. M., and Konozy, E. H. (2019) Isolation of Jatropha curcas seeds isolectins with variable affinity for human and animal blood types, Sudan J. Med. Sci., 14, 202-209, https://doi.org/10.18502/sjms.v14i4.5900.
Thomas, T. S., and Li, S. L. (1980) Purification and physicochemical properties of ricins and agglutinins from Ricinus communis, Eur. J. Biochem., 105, 453-459, https://doi.org/10.1111/j.1432-1033.1980.tb04520.x.
Santana, S. S., Gennari-Cardoso, M. L., Carvalho, F. C., Roque-Barreira, M. C., Santiago, A. d. S., Alvim, F. C., and Pirovani, C. P. (2014) Eutirucallin, a RIP-2 type lectin from the latex of Euphorbia tirucalli L. presents proinflammatory properties, PLoS One, 9, e88422, https://doi.org/10.1371/journal.pone.0088422.
Davey, F., and Nelson, D. (1977) Periodic Acid Schiff (PAS) Stain, in Hematology (Williams, W. J., Buetler, E., Erslev, A. J., and Rundles, R. W., eds) McGraw-Hill, New York.
Konozy, E. H., Bernardes, E. S., Rosa, C., Faca, V., Greene, L. J., and Ward, R. J. (2003) Isolation, purification, and physicochemical characterization of a D-galactose-binding lectin from seeds of Erythrina speciosa, Arch. Biochem. Biophys., 410, 222-229, https://doi.org/10.1016/S0003-9861(02)00695-1.
Barbieri, L., Falasca, A., Franceschi, C., Licastro, F., Rossi, C., and Stirpe, F. (1983) Purification and properties of two lectins from the latex of the euphorbiaceous plants Hura crepitans L. (sand-box tree) and Euphorbia characias L. (Mediterranean spurge), Biochem. J., 215, 433-439, https://doi.org/10.1042/bj2150433.
Dias-Baruffi, M., Sakamoto, M., Rossetto, S., Vozari-Hampe, M., and Roque-Barreira, M. C. (2000) Neutrophil migration and aggregation induced by euphorbin, a lectin from the latex of Euphorbia milii, var. milii, Inflamm. Res., 49, 732-736, https://doi.org/10.1007/s000110050654.
Irazoqui, F. J., Vozari-Hampe, M. M., Lardone, R. D., Villarreal, M. A., Sendra, V. G., Montich, G. G., Trindade, V. M., Clausen, H., and Nores, G. A. (2005) Fine carbohydrate recognition of Euphorbia milii lectin, Biochem. Biophys. Res. Commun., 336, 14-21, https://doi.org/10.1016/j.bbrc.2005.08.028.
Richter, A., Mota, C., Santiago, F., and Barbosa, M. (2014) Evaluation of the antitumor effect of lectin obtained from the latex of Euphorbia tirucalli against tumor cells of Ehrlich, BMC Proc., 8, P38, https://doi.org/10.1186/1753-6561-8-S4-P38.
Palharini, J. G., Richter, A. C., Silva, M. F., Ferreira, F. B., Pirovani, C. P., Naves, K. S., Goulart, V. A., Mineo, T. W., Silva, M. J., and Santiago, F. M. (2017) Eutirucallin: a lectin with antitumor and antimicrobial properties, Front. Cell. Infect. Microbiol., 7, 136, https://doi.org/10.3389/fcimb.2017.00136.
Souza, M. A., Amâncio-Pereira, F., Cardoso, C. R. B., Silva, A. G. D., Silva, E. G., Andrade, L. R., Pena, J. D. O., Lanza, H., and Afonso-Cardoso, S. R. (2005) Isolation and partial characterization of a D-galactose-binding lectin from the latex of Synadenium carinatum, Braz. Arch. Biol. Technol., 48, 705-716, https://doi.org/10.1590/S1516-89132005000600005.
Tsaneva, M., and Van Damme, E. J. (2020) 130 years of plant lectin research, Glycoconjug. J., 37, 533-551, https://doi.org/10.1007/s10719-020-09942-y.
Van Holle, S., and Van Damme, E. J. (2015) Distribution and evolution of the lectin family in soybean (Glycine max), Molecules, 20, 2868-2891, https://doi.org/10.3390/molecules20022868.
Osman, M. E.-F. M., Dirar, A. I., and Konozy, E. H. E. (2022) Genome-wide screening of lectin putative genes from Sorghum bicolor L., distribution in QTLs and a probable implications of lectins in abiotic stress tolerance, BMC Plant Biol., 22, 397, https://doi.org/10.1186/s12870-022-03792-6.
Lin, J.-Y., Tserng, K.-Y., Chen, C.-C., Lin, L.-T., and Tung, T.-C. (1970) Abrin and ricin: new anti-tumour substances, Nature, 227, 292-293, https://doi.org/10.1038/227292a0.
Worbs, S., Skiba, M., Söderström, M., Rapinoja, M.-L., Zeleny, R., Russmann, H., Schimmel, H., Vanninen, P., Fredriksson, S.-Å., and Dorner, B. G. (2015) Characterization of ricin and R. communis agglutinin reference materials, Toxins, 7, 4906-4934, https://doi.org/10.3390/toxins7124856.
Pohl, P., Antonenko, Y. N., Evtodienko, V. Y., Pohl, E. E., Saparov, S. M., Agapov, I. I., and Tonevitsky, A. G. (1998) Membrane fusion mediated by ricin and viscumin, Biochim. Biophys. Acta Biomembr., 1371, 11-16, https://doi.org/10.1016/S0005-2736(98)00024-8.
Brandt, N., Chikishev, A. Y., Sotnikov, A., Savochkina, Y. A., Agapov, I., and Tonevitsky, A. (2005) Ricin, ricin agglutinin, and the ricin binding subunit structural comparison by Raman spectroscopy, J. Mol. Structure, 735, 293-298, https://doi.org/10.1016/j.molstruc.2004.09.032.
Konareva, N., Gabdulkhakov, A., Eschenburg, S., Stoeva, S., Popov, A., Krauspenhaar, R., Andrianova, M., Savochkina, Y., Agapov, I., and Tonevitskii, A. (2001) Topology of the polypeptide chain in the complex of agglutinin from castor bean seeds with β-D-galactose in the crystalline state, Crystallogr. Rep., 46, 792-800, https://doi.org/10.1134/1.1405866.
Sphyris, N., Lord, J. M., Wales, R., and Roberts, L. M. (1995) Mutational Analysis of the ricinus lectin B-chains: galactose-binding ability of the 2β subdomain of Ricinus communis agglutinin B-chain, J. Biol. Chem., 270, 20292-20297, https://doi.org/10.1074/jbc.270.35.20292.
Frankel, A. E., Burbage, C., Fu, T., Tagge, E., Chandler, J., and Willingham, M. C. (1996) Ricin toxin contains at least three galactose-binding sites located in B chain subdomains 1α, 1β, and 2γ, Biochemistry, 35, 14749-14756, https://doi.org/10.1021/bi960798s.
Peumans, W. J., and Van Damme, E. (1995) Lectins as plant defense proteins, Plant Physiol., 109, 347, https://doi.org/10.1104/pp.109.2.347.
Barre, A., Bourne, Y., Van Damme, E. J., and Rougé, P. (2019) Overview of the structure–function relationships of mannose-specific lectins from plants, algae and fungi, Int. J. Mol. Sci., 20, 254, https://doi.org/10.3390/ijms20020254.
Wu, J. H., Singh, T., Herp, A., and Wu, A. M. (2006) Carbohydrate recognition factors of the lectin domains present in the Ricinus communis toxic protein (ricin), Biochimie, 88, 201-217, https://doi.org/10.1016/j.biochi.2005.07.007.
Wu, A. M., Wu, J. H., Singh, T., Lai, L.-J., Yang, Z., and Herp, A. (2006) Recognition factors of Ricinus communis agglutinin 1 (RCA1), Mol. Immunol., 43, 1700-1715, https://doi.org/10.1016/j.molimm.2005.09.008.
Wu, J. H., Herp, A., and Wu, A. M. (1993) Defining carbohydrate specificity of Ricinus communis agglutinin as Ga1β1→4GlcNAc (II)> Galβ1→3GlcNAc (I)> Galα1→3Gal (B)> Galβ1→3GalNAc (T), Mol. Immunol., 30, 333-339, https://doi.org/10.1016/0161-5890(93)90062-G.
Wang, Y., Yu, G., Han, Z., Yang, B., Hu, Y., Zhao, X., Wu, J., Lv, Y., and Chai, W. (2011) Specificities of Ricinus communis agglutinin 120 interaction with sulfated galactose, FEBS Lett., 585, 3927-3934, https://doi.org/10.1016/j.febslet.2011.10.035.
Hua, J., Liu, Y., Xiao, C.-J., Jing, S.-X., Luo, S.-H., and Li, S.-H. (2017) Chemical profile and defensive function of the latex of Euphorbia peplus, Phytochemistry, 136, 56-64, https://doi.org/10.1016/j.phytochem.2016.12.021.
Bleuler-martínez, S., Butschi, A., Garbani, M., Wälti, M. A., Wohlschlager, T., Potthoff, E., Sabotiĉ, J., Pohleven, J., Lüthy, P., Hengartner, M. O., Aebi, M., and Künzler, M. (2011) A lectin-mediated resistance of higher fungi against predators and parasites, Mol. Ecol., 20, 3056-3070, https://doi.org/10.1111/j.1365-294X.2011.05093.x.
Konozy, E. H. E., Osman, M. E. M., Dirar, A. I., and Ghartey-Kwansah, G. (2022) Plant lectins: a new antimicrobial frontier, Biomed. Pharmacother., 155, 113735, https://doi.org/10.1016/j.biopha.2022.113735.
Schrot, J., Weng, A., and Melzig, M. F. (2015) Ribosome-inactivating and related proteins, Toxins, 7, 1556-1615, https://doi.org/10.3390/toxins7051556.
Olsnes, S., Refsnes, K., and Pihl, A. (1974) Mechanism of action of the toxic lectins abrin and ricin, Nature, 249, 627-631, https://doi.org/10.1038/249627a0.
De Zaeytijd, J., and Van Damme, E. J. (2017) Extensive evolution of cereal ribosome-inactivating proteins translates into unique structural features, activation mechanisms, and physiological roles, Toxins, 9, 123, https://doi.org/10.3390/toxins9040123.
Acosta, W., Ayala, J., Dolan, M. C., and Cramer, C. L. (2015) RTB Lectin: a novel receptor-independent delivery system for lysosomal enzyme replacement therapies, Sci. Rep., 5, 14144, https://doi.org/10.1038/srep14144.
O’Hara, J. M., and Mantis, N. J. (2013) Neutralizing monoclonal antibodies against ricin’s enzymatic subunit interfere with protein disulfide isomerase-mediated reduction of ricin holotoxin in vitro, J. Immunol. Methods, 395, 71-78, https://doi.org/10.1016/j.jim.2013.06.004.
Yermakova, A., Klokk, T. I., O’Hara, J. M., Cole, R., Sandvig, K., and Mantis, N. J. (2016) Neutralizing monoclonal antibodies against disparate epitopes on ricin toxin’s enzymatic subunit interfere with intracellular toxin transport, Sci. Rep., 6, 22721, https://doi.org/10.1038/srep22721.
Lord, M. J., Jolliffe, N. A., Marsden, C. J., Pateman, C. S., Smith, D. C., Spooner, R. A., Watson, P. D., and Roberts, L. M. (2003) Ricin: mechanisms of cytotoxicity, Toxicol. Rev., 22, 53-64, https://doi.org/10.2165/00139709-200322010-00006.
Franke, H., Scholl, R., and Aigner, A. (2019) Ricin and Ricinus communis in pharmacology and toxicology-from ancient use and “Papyrus Ebers” to modern perspectives and “poisonous plant of the year 2018”, Naunyn Schmiedebergs Arch. Pharmacol., 392, 1181-1208, https://doi.org/10.1007/s00210-019-01691-6.
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E.H.E.K. provided the idea and supervised the work, wrote a major part of the initial draft, and revised the final version. M.E.M.O. wrote parts of the first draft, analyzed the structures, and participated in preparation of illustrations. A.I.D. participated in the analysis of structures and preparation of illustrations.
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Konozy, E.H.E., Osman, M.E.M. & Dirar, A.I. A Comprehensive Review on Euphorbiaceae lectins: Structural and Biological Perspectives. Biochemistry Moscow 88, 1956–1969 (2023). https://doi.org/10.1134/S0006297923110238
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DOI: https://doi.org/10.1134/S0006297923110238