BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

A Novel Mannose-binding Tuber Lectin from Typhonium divaricatum (L.) Decne (family Araceae) with Antiviral Activity Against HSV-II and Anti-proliferative Effect on Human Cancer Cell Lines

  • Luo, Yongting (College of Life Sciences, Sichuan University) ;
  • Xu, Xiaochao (College of Life Sciences, Sichuan University) ;
  • Liu, Jiwei (College of Life Sciences, Sichuan University) ;
  • Li, Jian (College of Life Sciences, Sichuan University) ;
  • Sun, Yisheng (College of Life Sciences, Sichuan University) ;
  • Liu, Zhen (College of Life Sciences, Sichuan University) ;
  • Liu, Jinzhi (College of Life Sciences, Sichuan University) ;
  • Damme, Els Van (Department of Molecular Biotechnology, Ghent University) ;
  • Balzarini, Jan (Rega Institute for Medical Research, Katholieke University Leuven) ;
  • Bao, Jinku (College of Life Sciences, Sichuan University)
  • Published : 2007.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

A novel mannose-binding tuber lectin with in vitro antiproliferative activity towards human cancer cell lines and antiviral activity against HSV-II was isolated from fresh tubers of a traditional Chinese medicinal herb, Typhonium divaricatum (L.) Decne by a combined procedure involving extraction, ammonium sulfate precipitation, ion exchange chromatography on DEAE-SEPHAROSE, CM-SEPHAROSE and gel-filtration on sephacryl S-200. The apparent molecular mass of the purified Typhonium divaricatum lectin (TDL) was 48 kDa. TDL exhibits hemagglutinating activity toward rabbit erythrocytes at 0.95 $\mu$g/ml, and its activity could be strongly inhibited by mannan, ovomucoid, asialofetuin and thyroglobulin. TDL showed antiproliferative activity towards some well established human cancer cell lines, e.g. Pro-01 (56.7 $\pm$ 6.8), Bre-04 (41.5 $\pm$ 4.8), and Lu-04 (11.4 $\pm$ 0.3). The anti-HSV-II activity of TDL was elucidated by testing its HSV-II infection inhibitory activity in Vero cells with $TC_50$ and $EC_50$ of 5.176 mg/ml and 3.054 $\mu$g/ml respectively. The full-length cDNA sequence of TDL was 1145 bp and contained an 813-bp open reading frame (ORF) encoding a 271 amino acid precursor of 29-kDa. Homology analysis showed that TDL had high homology with many other mannose-binding lectins. Secondary and three-dimensional structures analyses showed that TDL is heterotetramer and similar with lectins from mannose-binding lectin superfamily, especially those from family Araceae.

Keywords

References

  1. Allen, A. K. (1995) Purification and characterization of an Nacetyllactosamine- specific lectin from tubers of Arum maculatum. Biochim. Biophys. Acta 1244, 129-132 https://doi.org/10.1016/0304-4165(94)00210-O
  2. Andrews, P. (1964) Estimation of molecular weights of proteins by Sephadex gel-filtration. Biochem. J. 91, 222-233 https://doi.org/10.1042/bj0910222
  3. Bains, J. S., Singh, T. J., Kamboj, S. S., Nijjar, K. K., Agrewal, J. N., Kumar, V., Kumar, A. and Saxena, A. K. (2005) Mitogenic and anti-proliferative activity of a lectin from the tubers of Voodoo lily (Sauromatum venosum). Biochim. Biophys. Acta 1723, 163-174 https://doi.org/10.1016/j.bbagen.2005.02.006
  4. Barre, A., Van Damme, E. J. M., Peumans, W. J. and Rouge, P. (1996) Structure-function relationship of monocot mannosebinding lectins. Plant Physiol. 112, 1531-1540 https://doi.org/10.1104/pp.112.4.1531
  5. Gaboriaud, C., Bissery, V., Benchetrit, T. and Mornon, J. P. (1987) Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences. FEBS Lett. 224, 149-155 https://doi.org/10.1016/0014-5793(87)80439-8
  6. Goldstein, I. J., Hufhes, R. C., Monsigny, M., Osawa, T. and Sharon, N. (1980) What should be called a lectin? Nature 285, 66
  7. Hirai, M., Nakamura, K., Imai, T. and Sato, T. (1993) cDNAs encoding for storage proteins in the tubers of taro (Colocasia esculenta Schott ). Jpn. J. Genet. 68, 229-236 https://doi.org/10.1266/jjg.68.229
  8. Karasaki, Y., Tsukamoto, S., Mizusaki, K., Sugiura, T. and Gotoh, S. (2001) A garlic lectin exerted an antitumor activity and induced apoptosis in human tumor cells. Food Res. Int. 34, 7-13 https://doi.org/10.1016/S0963-9969(00)00122-8
  9. Kaur, M., Singh, K., Rup, P. J., Saxena, A.K., Khan, R. H. Mohd, T. A., Sukhdev Singh Kamboj, S. S. and Singh, J. (2006) A tuber lectin from Arisaema helleborifolium Schott with antiinsect activity against melon fruit fly, Bactrocera cucurbitae (Coquillett) and anti-cancer effect on human cancer cell lines. Arch. Biochem. Biophys. 445, 156-165 https://doi.org/10.1016/j.abb.2005.10.021
  10. Kodama, E., Shigeta, S., Suzuki, T. and De Clercq, E. (1996) Application of a gastric cancer cell line (MKN-28) for antiadenovirus screening using the MTT method. Antiviral Res. 31, 159-164 https://doi.org/10.1016/0166-3542(96)06966-5
  11. Kong, W. W., Deng, Z. X., Fei, J., Wang, Q., Sun, X. F. and Tang, K. X. (2006) Characterization of a mannose-binding lectin gene from Typhonium divaricatum (L.) Decne. Afr. J. Biotechnol. 5, 793-799
  12. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 https://doi.org/10.1038/227680a0
  13. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with folin phenol reagent. J. Biol. Chem. 193, 265-275
  14. Marchetti, M., Mastromarino, P., Rieti, S., Seganti, L. and Orsi, N. (1995) Inhibition of herpes simplex, rabies and rubella viruses by lectins with defferent specificities. Res. Virol. 146, 211-215 https://doi.org/10.1016/0923-2516(96)80581-4
  15. Mo, H. Q., Rice, K. G., Evers, D. L., Winter, H. C., Peumans, W. J., Van Damme, E. J. M. and Goldstein, I. J. (1999) Xanthosoma sagittifolium tubers contain a lectin with two different types of carbohydrate-binding sites. J. Biol. Chem. 274, 33300-33305 https://doi.org/10.1074/jbc.274.47.33300
  16. Monks, A., Scudiero, D., Skehan, P., Shoemaker, R., Paull, K., Vistica, D., Hose, C., Langley, J., Cronise, P. and Vaigro-Wolff, A. (1991) Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J. Natl. Cancer Inst. 83, 757-766 https://doi.org/10.1093/jnci/83.11.757
  17. Oda Y. and Minami K. (1986), Isolation and characterization of a lectin from tulip bulbs, Tulipa gesneriana. Eur. J. Biochem. 159, 239-245 https://doi.org/10.1111/j.1432-1033.1986.tb09859.x
  18. Okada, Y. and Kim, J. (1972) Incubation of concanavalin A with enveloped viruses and host cells. Virology 50, 507-515 https://doi.org/10.1016/0042-6822(72)90401-1
  19. Sandu, R. S., Arora, J. S., Chopra, S. K., Pelia, S. S., Kamboj, S. S., Naidu, Y. C. and Nath, I. (1990) Occurrence and isolation of new lectins of plants, fungi, and bacteria; in Lectins, Biology, Biochemistry, Clinical Biochemistry, Kocourek, J. and Freed, D. L. J. (eds.), pp. 19-33, Sigma Chem. Co., USA
  20. Shangary, S., Singh, J., Kamboj, S. S., Kamboj, K. K. and Sandhu, R. S. (1995) Purification and properties of four monocot lectins from the family araceae. Phytochemistry 40, 449-445 https://doi.org/10.1016/0031-9422(95)00229-Z
  21. Sharon, N. and Lis, H. (1989) Lectins as cell recognition molecules. Science 246, 227-234 https://doi.org/10.1126/science.2552581
  22. Singh, J., Singh, J. and Kamboj, S. S. (2004) A novel mitogenic and antiproliferative lectin from a wild cobra lily, Arisaema flavum. Biochem. Biophys. Res. Commun. 318, 1057-1065 https://doi.org/10.1016/j.bbrc.2004.04.135
  23. Van Damme, E. J. M., Goldstein, I. J., Vercammen, G., Vuylsteke, J. and Peumans, W. J. (1992) Lectins of members of the Amaryllidaceae are encoded by multigene families which show extensive homologies. Physiol. Plantarum. 86, 245-252 https://doi.org/10.1034/j.1399-3054.1992.860209.x
  24. Van Damme, E. J. M., Goossens, K., Smeets, K., Van Leuven, F., Verhaert, P. and Peumans, W. J. (1995a) The major tuber storage protein of araceae species is a lectin. Characterization and molecular cloning of the lectin from Arum maculatum. Plant Physiol. 107, 1147-1158 https://doi.org/10.1104/pp.107.4.1147
  25. Van Damme, E. J. M., Smeets, K. and Peumans, W. J. (1995b) The mannose binding monocot lectins and their genes; in: Lectins, BioMedical Perspectives, Pusztai, A. J., Bardocz, S. (eds.), pp. 59-80, Taylor and Francis Ltd, London, U.K.
  26. Van Damme, E. J. M., Peumans, W. J., Barre, A. and Rouge, P. (1998) Plant lectins: A composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Crit. Rev. Plant Sci. 17, 575-692 https://doi.org/10.1080/07352689891304276
  27. Von Heijine, G. (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14, 4683-4690 https://doi.org/10.1093/nar/14.11.4683
  28. Wang, H., Gao, J. and Ng, T. B. (2000) A new lectin with highly potent antihepatoma and antisarcoma activities from the oyster mushroom Pleurotus ostreatus. Biochem. Biophys. Res. Commun. 275, 810-816 https://doi.org/10.1006/bbrc.2000.3373
  29. Wrigh, L. M., Reynolds, C. D., Rizkallah, P. J., Allen, A. K., Van Damme, E. J. M., Donovan, M. J. and Peumans, W. J. (1999) Structural characterisation of the native fetuin-binding protein Scilla campanulata agglutinin: a novel two-domain lectin. FEBS Lett. 468, 19-22 https://doi.org/10.1016/S0014-5793(00)01109-1

Cited by

  1. Prokaryotic expression and bioactivity analysis of N-terminus domain of Pinellia ternata agglutinin using alkaline phosphatase signal peptide vol.89, pp.1, 2013, https://doi.org/10.1016/j.pep.2013.03.001
  2. Recombinant expression of Polygonatum cyrtonema lectin with anti-viral, apoptosis-inducing activities and preliminary crystallization vol.46, pp.2, 2011, https://doi.org/10.1016/j.procbio.2010.10.005
  3. Purification of a mannose-binding lectin Pinellia ternata agglutinin and its induction of apoptosis in Bel-7404 cells vol.93, 2014, https://doi.org/10.1016/j.pep.2013.09.018
  4. Bauhinia forficata lectin (BfL) induces cell death and inhibits integrin-mediated adhesion on MCF7 human breast cancer cells vol.1840, pp.7, 2014, https://doi.org/10.1016/j.bbagen.2014.03.009
  5. Isolation and characterization of a novel lectin with antifungal and antiproliferative activities from Sophora alopecuroides seeds vol.44, pp.7, 2012, https://doi.org/10.1093/abbs/gms037
  6. Isolation and characterization of a French bean hemagglutinin with antitumor, antifungal, and anti-HIV-1 reverse transcriptase activities and an exceptionally high yield vol.17, pp.6, 2010, https://doi.org/10.1016/j.phymed.2009.07.017
  7. Bioinformatics analyses of the mannose-binding lectins from Polygonatum cyrtonema, Ophiopogon japonicus and Liparis noversa with antiproliferative and apoptosis-inducing activities vol.16, pp.6-7, 2009, https://doi.org/10.1016/j.phymed.2008.12.010
  8. Cytotoxic effect and apoptosis induction by Bothrops leucurus venom lectin on tumor cell lines vol.59, pp.7-8, 2012, https://doi.org/10.1016/j.toxicon.2012.03.002
  9. Extraction and Purification of a Lectin from Red Kidney Bean and Preliminary Immune Function Studies of the Lectin and Four Chinese Herbal Polysaccharides vol.2010, 2010, https://doi.org/10.1155/2010/217342
  10. Molecular characterization and expression analysis of Lily-type lectin (Sm LTL) in turbot Scophthalmus maximus, and its response to Vibrio anguillarum 2018, https://doi.org/10.1007/s00343-017-6268-1
  11. Anti-tumor and anti-viral activities of Galanthus nivalis agglutinin (GNA)-related lectins vol.30, pp.3, 2013, https://doi.org/10.1007/s10719-012-9440-z
  12. Anti-allergic Hydroxy Fatty Acids from Typhonium blumei Explored through ChemGPS-NP vol.8, 2017, https://doi.org/10.3389/fphar.2017.00356
  13. Typhonium blumei extract inhibits proliferation of human lung adenocarcinoma A549 cells via induction of cell cycle arrest and apoptosis vol.135, pp.2, 2011, https://doi.org/10.1016/j.jep.2011.03.048
  14. First report of a haemagglutinin-induced apoptotic pathway in breast cancer cells vol.30, pp.5, 2010, https://doi.org/10.1042/BSR20090059
  15. Toxins for Transgenic Resistance to Hemipteran Pests vol.4, pp.12, 2012, https://doi.org/10.3390/toxins4060405
  16. Characterization, molecular cloning, and in silico analysis of a novel mannose-binding lectin from Polygonatum odoratum (Mill.) with anti-HSV-II and apoptosis-inducing activities vol.18, pp.8-9, 2011, https://doi.org/10.1016/j.phymed.2010.11.001
  17. Clematis montana lectin, a novel mannose-binding lectin from traditional Chinese medicine with antiviral and apoptosis-inducing activities vol.30, pp.10, 2009, https://doi.org/10.1016/j.peptides.2009.06.027
  18. Isolation and characterization of a lectin with potentially exploitable activities from caper (Capparis spinosa) seeds vol.29, pp.5, 2009, https://doi.org/10.1042/BSR20080110
  19. Glycosylation of dengue virus glycoproteins and their interactions with carbohydrate receptors: possible targets for antiviral therapy vol.161, pp.7, 2016, https://doi.org/10.1007/s00705-016-2855-2
  20. The attack of the phytopathogens and the trumpet solo: Identification of a novel plant antifungal peptide with distinct fold and disulfide bond pattern vol.95, pp.10, 2013, https://doi.org/10.1016/j.biochi.2013.06.027
  21. Anti-inflammatory and Antinociceptive Activity of Chitin-binding Lectin from Canna Limbata Seeds vol.171, pp.8, 2013, https://doi.org/10.1007/s12010-013-0470-1
  22. Expression and characterization of two domains of Pinellia ternata agglutinin (PTA), a plant agglutinin from Pinellia ternata with antifungal activity vol.26, pp.3, 2010, https://doi.org/10.1007/s11274-009-0204-2
  23. Characterisation of a novel monomeric lectin (AML) from Astragalus membranaceus with anti-proliferative activity vol.122, pp.3, 2010, https://doi.org/10.1016/j.foodchem.2010.03.015
  24. Nebrodeolysin, a novel hemolytic protein from mushroom Pleurotus nebrodensis with apoptosis-inducing and anti-HIV-1 effects vol.16, pp.2-3, 2009, https://doi.org/10.1016/j.phymed.2008.07.004
  25. Molecular mechanisms ofLycoris aureaagglutinin-induced apoptosis and G2/M cell cycle arrest in human lung adenocarcinoma A549 cells, bothin vitroandin vivo vol.46, pp.3, 2013, https://doi.org/10.1111/cpr.12034
  26. In silico identification of novel hevein-like peptide precursors vol.38, pp.1, 2012, https://doi.org/10.1016/j.peptides.2012.07.025
  27. In vitro Antiviral Activity of Crinum latifolium Lectin Against Poxvirus Replication vol.8, pp.7, 2008, https://doi.org/10.3923/jbs.2008.1236.1240
  28. Antiproliferation and apoptosis of human tumor cell lines by a lectin (AMML) of Astragalus mongholicus vol.16, pp.6-7, 2009, https://doi.org/10.1016/j.phymed.2008.12.024
  29. High mannose N-glycan binding lectin from Remusatia vivipara (RVL) limits cell growth, motility and invasiveness of human breast cancer cells vol.93, 2017, https://doi.org/10.1016/j.biopha.2017.06.081
  30. Purification, characterization and molecular cloning of a monocot mannose-binding lectin from Remusatia vivipara with nematicidal activity vol.27, pp.3, 2010, https://doi.org/10.1007/s10719-010-9279-0
  31. Fish lily type lectin-1 contains β-prism architecture: Immunological characterization vol.56, pp.4, 2013, https://doi.org/10.1016/j.molimm.2013.06.020
  32. Transgenic Tobacco Expressing Zephyranthes grandiflora Agglutinin Confers Enhanced Resistance to Aphids vol.158, pp.3, 2009, https://doi.org/10.1007/s12010-008-8418-6
  33. Narcissus tazetta lectin shows strong inhibitory effects against respiratory syncytial virus, influenza A (H1N1, H3N2, H5N1) and B viruses vol.35, pp.1, 2010, https://doi.org/10.1007/s12038-010-0012-8
  34. Characterization of chickpea (Cicer arietinum L.) lectin for biological activity vol.24, pp.3, 2018, https://doi.org/10.1007/s12298-018-0508-5
  35. Overview of the Structure–Function Relationships of Mannose-Specific Lectins from Plants, Algae and Fungi vol.20, pp.2, 2019, https://doi.org/10.3390/ijms20020254