High-mannose type N-glycan binding specificity of a novel lectin from the red alga (Betaphycus gelatinus)

Le Dinh Hung, Le Thi Doan Thuc
Author affiliations

Authors

  • Le Dinh Hung Nhatrang Institute of Technology Research and Application-Vietnam Academy of Science and Technology
  • Le Thi Doan Thuc

DOI:

https://doi.org/10.15625/1811-4989/17/4/13697

Keywords:

Betaphycus gelatinus, carbohydrate-binding specificity, high-mannose type N-glycan, lectin, red alga, stable

Abstract

The red alga, Betaphycus gelatinus is one of carrageenan sources in the world. The lectin from the red alga B. gelatinus was isolated by a combination of aqueous ethanol extraction, ethanol precipitation, ion-exchange chromatography and gel filtration chromatography and was designated as BGL after the specific name of alga. Lectin gave a single band with molecular mass of about 19,000 Da in both non-reducing and reducing SDS-PAGE conditions, therefore lectin exists in monomer form. The hemagglutination activities of BGL were stable over a wide range of pH from 3 to 10, temperature up 60 oC and not affected by either the presence of EDTA or addition of divalent cations, indicating that lectin requires no metal for biological activity. The hemagglutination activities of BGL were not inhibited by monosaccharides and glycoproteins, D-glucose, D-mannose, D-galactose, D-xylose, N-acetyl-galactosamine, N-acetyl-glucosamine, N-acetyl-neuraminic acid, N-acety-D-mannosamine, transferrin and fetuin, but strongly inhibited by glycoproteins bearing high-mannose type N-glycan, such as yeast mannan and porcine thyroglobulin. Lectin BGL is specific for N-glycans and may recognize terminal (α1–3) or (α1–6)-linked mannose residues in structure Man(α1-6)[Man(α1-3)]Man(α1-6)[Man(α1-3)]Man(β1-4)GlcNAc(β1-4)GlcNAc of N-glycans. High-mannose type N-glycan binding specificities of this lectin highly resemble with those of the anti-cancer, anti-virus and anti-bacteria lectins from the red algae, carrageenophytes, including Eucheuma serra (ESA-2), Eucheuma denticulatum (EDA-2), Kappaphycus striatum (KSA-2), Kappaphycus alvarezii (KAA-1 and KAA-2) and Solieria filiformis (SfL1 and SfL2). The red alga B. gelatinus could promise to be a good source of valuable lectins for application in biochemistry and biomedicine.

Downloads

Download data is not yet available.

References

Ainouz IL, Sampaio AH, Benevides NMB, Freitas ALP, Costa FHF, Carvalho MC, Pinheiro-Joventino F (1992) Agglutination of enzyme treated erythrocytes by Brazilian marine algae. Bot Mar 35: 475–479.

Balzarini J (2007) Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses? Antivir Chem Chemother 18: 1–11.

Barre A, Bourne Y, Van Damme EJM, Pierre Rougé P (2019) Overview of the structure–function relationships of mannose-specific lectins from plants, algae and fungi. Int J Mol Sci doi:10.3390/ijms20020254.

Chaves RP, da Silva SR, Neto LGN, Carneiro RF, da Silva ALC, Sampaio AH, de Sousa BL, Cabral MG, Videira PA, Teixeira EH, Nagano CS (2018) Structural characterization of two isolectins from the marine red alga Solieria filiformis (Kützing) P.W. Gabrielson and their anticancer effect on MCF-7 breast cancer cells. Int J Biol Macromol 107: 1320-1329.

Chiles TC, Bird KT (1989) A comparative study of the animal erythrocyte agglutinins from marine algae. Comp Biochem Physiol 94B: 107–111.

Freitas ALP, Teixeira DIA, Costa FHF, Farias WRL, Lobato ASC, Sampaio AH, Benevides NMB (1997) A new survey of Brazilian marine algae for agglutinins. J Appl Phycol 9: 495–501.

Fukuda Y, Sugahara T, Ueno M, Fukuta Y, Ochi Y, Akiyama K, Miyazaki T, Masuda S, Kawakubo A, Kato K (2006) The anti-tumor effect of Euchema serra agglutinin on colon

cancer cells in vitro and in vivo. Anti-Cancer Drugs 17:943–947.

Hayashi K, Walde P, Miyazaki T, Sakayama K, Nakamura A, Kameda K, Masuda S, Umakoshi H, Kato K (2012) Active targeting to osteosarcoma cells and apoptotic cell death induction by the novel lectin Eucheuma serra agglutinin isolated from a marine red alga. J Drug Deliv doi:10.1155/2012/842785.

Hirayama M, Shibata H, Imamura K, Sakaguchi T, Hori K (2016) High-mannose specific lectin and its recombinants from a Carrageenophyta Kappaphycus alvarezii represent

a potent anti-HIV activity through high-affinity binding to the viral envelope glycoprotein gp120. Mar Biotechnol 18: 144-160.

Hori K, Oiwa C, Miyazawa K, Ito K (1988) Evidence for wide distribution of agglutinins in marine algae. Bot Mar 31: 133–138.

Hori K, Miyazawa K, Ito K (1990) Some common properties of lectins from marine algae. Hydrobiologia 204/205: 561-566.

Hori K, Sato Y, Ito K, Fujiwara Y, Iwamoto Y, Makino H, Kawakubo A (2007) Strict specificity for high-mannose type N-glycans and primary structure of a red alga Eucheuma serra lectin. Glycobiology 17: 479–491.

Kawakubo A, Makino H, Ohnishi J, Hirohara H, Hori K (1997) The marine red alga Eucheuma serra J Agardh, a high yielding source of two isolectins. J Appl Phycol 9: 331–338.

Kawakubo A, Makino H, Ohnishi J, Hirohara H, Hori K (1999) Occurrence of highly yielded lectins homologous within the genus Eucheuma. J Appl Phycol 11: 149–156.

LaemmLi UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.

Le Dinh Hung, Sato T, Shibata H, Hori K (2009a) Biochemical comparison of lectins among three different color strains of the red alga Kappaphycus alvarezii. Fish Sci 75: 723-730.

Le Dinh Hung, Hori K, Huynh Quang Nang, Tran Kha, Le Thi Hoa (2009b) Seasonal changes in growth rate, carrageenan yield and lectin content in the red alga Kappaphycus alvarezii cultivated in Camranh Bay, Vietnam. J Appl Phycol 21: 265-272.

Le Dinh Hung, Hori K, Huynh Quang Nang (2009c) Screening and preliminary characterization of hemagglutinins in Vietnamese marine algae. J Appl Phycol 21: 89-97.

Le Dinh Hung, Sato Y, Hori K (2011) High-mannose N-glycan-specific lectins from the red alga Kappaphycus striatum (Carrageenophyte). Phytochemistry 72: 855-861.

Le Dinh Hung, Bui Minh Ly, Vo Thi Dieu Trang, Ngo Thi Duy Ngoc, Le Thi Hoa, Phan Thi Hoai Trinh (2012) A new screening for hemagglutinins from Vietnamese marine macroalgae. J Appl Phycol 24: 227- 235.

Le Dinh Hung, Hirayama, M, Bui Minh Ly, Hori K (2015a) Purification, primary structure, and biological activity of high-mannose N-glycan-specific lectin from the cultivated Eucheuma denticulatum. J Appl Phycol 27: 1657-1669.

Le Dinh Hung, Hirayama, M, Bui Minh Ly, Hori K (2015b) Biological activity, cDNA cloning and primary structure of lectin KSA-2 from the cultivated red alga Kappaphycus striatum (Schmitz) Doty ex Silva. Phytochem Lett 14: 99-105.

Le Dinh Hung, Makoto Hirayama, Kanji Hori (2016) Cloning and characterizing cDNA sequences coding high-mannose N-glycan binding lectins from cultivated red algae Eucheuma denticulatum and Kappaphycus striatum. Vietnam J Biotechnol 14: 327-336.

Le Dinh Hung, Le Thi Hoa, Le Nhu Hau, Dinh Thanh Trung (2018) The lectin accumulation, growth rate, carrageenan yield, and quality from the red alga Kappaphycus striatus cultivated at Camranh Bay, Vietnam. J Appl Phycol

https://doi.org/10.1007/s10811-018-1692-y.

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275.

Mu J, Hirayama M, Sato Y, Morimoto K, Hori K (2017) A novel high-mannose specific lectin from the green alga Halimeda renschii exhibits a potent anti-influenza virus activity through high-affinity binding to the viral hemagglutinin. Mar Drugs doi:10.3390/md15080255.

Omokawa Y, Miyazaki T, Walde P, Akiyama K, Sugahara T, Masuda S, Inada A, Ohnishi Y, Saeki T, Kato K (2010) In vitro and in vivo anti-tumor effects of novel Span 80 vesicles containing immobilized Eucheuma serra agglutinin. Int J Pharm 389: 157–167.

Sato Y, Morimoto K, Hirayama M, Hori K (2011a) High mannose-specific lectin (KAA-2) from the red alga Kappaphycus alvarezii potently inhibits influenza virus infection in a strain-independent manner. Biochem Biophys Res Commun 405: 291–296.

Sato Y, Hirayama M, Morimoto K, Yamamoto N, Okuyama S, Hori K (2011b) High mannose-binding lectin with preference for the cluster of α1–2-mannose from the green alga Boodlea coacta is a potent entry inhibitor of HIV-1 and influenza viruses. J Biol Chem 286: 19446–19458.

Sato Y, Morimoto K, Kubo T, Sakaguchi T, Nishizono A, Hirayama M, Hori K (2015) Entry inhibition of influenza viruses with high mannose binding lectin ESA-2 from the red alga Eucheuma serra through the recognition of viral hemagglutinin. Mar Drugs 13: 3454-3465.

Sharon N, Lis H (2003) Lectins, second ed. Kluwer Academic Publishers, The Netherlands

Sugawara T, Ohama Y, Fukuda A, Hayashi M, Kato K (2001) The cytotoxic effect of Eucheuma serra agglutinin (ESA) on cancer cells and its application to molecular probe for drug delivery system using lipid vesicles. Cytotechnology 36: 93–99.

Tsuji T, Yamamoto K, Irimura T, Osawa T (1981) Structure of carbohydrate unit A of porcine thyroglobulin. J Biochem 195: 691-699.

Wopereis S, Lefeber DJ, Morava E, Wevers RA (2006) Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects: A Review. Clinical Chemistry 52: 574-600.

Xiong C, Li W, Liu H, Zhang W, Dou J, Bai X, Du Y, Ma X (2006) A normal mucin-binding lectin from the sponge Craniella australiensis. Comp Biochem Physiol, Part C 143: 9–16.

Yamamoto K, Tsuji T, Irimura T, Osawa T (1981) The structure of carbohydrate unit B of porcine thyroglobulin. J Biochem 195: 701-713.

Ziólkowska NE, Wlodawer A (2006) Structural studies of algal lectins with anti-HIV activity. Acta Biochim Pol 53: 617–626.

Downloads

Published

02-11-2020

How to Cite

Hung, L. D., & Thi Doan Thuc, L. (2020). High-mannose type N-glycan binding specificity of a novel lectin from the red alga (Betaphycus gelatinus). Vietnam Journal of Biotechnology, 17(4), 709–718. https://doi.org/10.15625/1811-4989/17/4/13697

Issue

Section

Articles

Most read articles by the same author(s)