N-acetylneuraminic acid specific lectin and antibacterial activity from the red alga Gracilaria canaliculata Sonder
Section:
Physiology, Biochemistry. BiophysicsIssue:
Vol. 31 No. 2 (2021)Pages:
126–140DOI:
https://doi.org/10.15407/alg31.02.126Abstract
A new lectin from the marine red alga Gracilaria canaliculata (GCL) was isolated by a combination of aqueous ethanol extraction, ethanol precipitation, ion exchange and filtration chromatography. Lectin gave a single band with molecular mass of 22,000 Da in both non-reducing and reducing SDS-PAGE conditions, indicating that GCL is a monomeric protein. The hemagglutination activities of GCL 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. Lectin GCL had high affinity for N-acetylneuraminic acid through interacting with the acetamido group at equatorial C2 position of these sugar residues, suggesting that GCL is specific for N-acetylneuraminic acid. Furthermore, GCL inhibited the growth of human and shrimp pathogenic bacteria, Staphylococcus aureus and Vibrio alginolyticus, although it did not affect the growth of Escherichia coli, Enterobacter cloace, Vibrio parahaemolyticus and V. harveyi. The red alga G. canaliculata may promise to be a source of valuable lectins for application as antibacterial agents.
Keywords:
antibacterial activity, carbohydrate binding specificity, Gracilaria canaliculata, lectin, red algaFull text
References
Barre A., Simplicien M., Benoist H., Van Damme ElsJM., Rougé P. 2019. Mannose-specific lectins from marine algae: Diverse structural scaffolds associated to common virucidal and anti-cancer properties. Mar. Drugs. 17(8): 440. https://doi.org/10.3390/md17080440 https://www.ncbi.nlm.nih.gov/pubmed/31357490 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6723950
Barre A., Van Damme ElsJM., Simplicien M., Benoist H., Rougé P. 2020. Man-Specific, GalNAc/T/Tn-Specific and Neu5Ac-Specific Seaweed Lectins as Glycan Probes for the SARS-CoV-2 (COVID-19) Coronavirus. Mar. Drugs. 18(11): 1–543. https://doi.org/10.3390/md18110543 https://www.ncbi.nlm.nih.gov/pubmed/33138151 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693892
Boonsri N., Rudtanatip T., Withyachumnarnkul B., Wongprasert K. 2017. Protein extract from red seaweed Gracilaria fisheri prevents acute hepatopancreatic necrosis disease (AHPND) infection in shrimp. J. Appl. Phycol. 29(3): 1597–1608. https://doi.org/10.1007/s10811-016-0969-2
Charungchitrak S., Petsom A., Sangvanich P., Karnchanatat A. 2011. Antifungal and antibacterial activities of lectin from the seeds of Archidendron jiringa Nielsen. Food Chem. 126(3): 1025–1032. https://doi.org/10.1016/j.foodchem.2010.11.114
Chaves R.P., da Silva S.R., Neto L.G.N., Carneiro R.F., da Silva A.L.C., Sampaio A.H. 2018a. 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. https://doi.org/10.1016/j.ijbiomac.2017.09.116 https://www.ncbi.nlm.nih.gov/pubmed/28970169
Chaves R.N., da Silva S.R., da Silva J.P.F.A., Carneiro R.F., de Sousa B.L., Abreu J.O., Carvalho F.C.T., Rocha C.R.C., Farias W.R.L., de Sousa O.V., Silva A.L.C., Sampaio A.H., Nagano C.S. 2018b. Meristiella echinocarpa lectin (MEL): a new member of the OAAH-lectin family. J. Appl. Phycol. 30: 2629–2638. https://doi.org/10.1007/s10811-018-1473-7 https://doi.org/10.1007/s10811-018-1473-7
Freitas A.L.P., Teixeira D.I.A., Costa F.H.F., Farias W.R.L., Lobato A.S.C., Sampaio A.H. 1997. A new survey of Brazilian marine algae for agglutinins. J. Appl. Phycol. 9: 495–501. https://doi.org/10.1023/A:1007917108581
Hanisch F.G., Hacker J., Schroten H. 1993. Specificity of S fimbriae on recombinant Escherichia coli: preferential binding to gangliosides expressing NeuGc alpha (2-3)Gal and NeuAc alpha (2-8)NeuAc. Infect. Immun. 61(5): 2108–2115. https://doi.org/10.1128/iai.61.5.2108-2115.1993 https://www.ncbi.nlm.nih.gov/pubmed/8097494
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(1): 144-160 https://doi.org/10.1007/s10126-015-9677-1 https://doi.org/10.1007/s10126-015-9684-2 https://doi.org/10.1007/s10126-016-9694-8 https://www.ncbi.nlm.nih.gov/pubmed/27166832 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7608414
Hori K., Miyazawa K., Fusetani N., Hashimoto K., Ito K. 1986. Hypnins, low-molecular weight peptidic agglutinins isolated from a marine red alga Hypnea japonica. Biochim. Biophys. Acta. 873: 228–236. https://doi.org/10.1016/0167-4838(86)90049-X
Hori K., Miyazawa K., Ito K. 1990. Some common properties of lectins from marine algae. Hydrobiologia. 204/205: 561–566. https://doi.org/10.1007/BF00040287
Hung L.D., Trinh P.T.H. 2020. Structure and anticancer activity of a new lectin from the cultivated red alga, Kappaphycus striatus. J. Nat. Med. 75(1): 223–231. https://doi.org/10.1007/s11418-020-01455-0 https://www.ncbi.nlm.nih.gov/pubmed/33025357 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7538373
Hung L.D., Hori K., Nang H.Q. 2009. Screening and preliminary characterization of hemag-glutinins in Vietnamese marine algae. J. Appl. Phycol. 21: 89–97. https://doi.org/10.1007/s10811-008-9330-8
Hung L.D., Ly B.M., Trang V.T.D., Ngoc N.T.D., Hoa L.T., Trinh P.T.H. 2012. A new screening for hemagglutinins from Vietnamese marine macroalgae. J. Appl. Phycol. 24: 227–235. https://doi.org/10.1007/s10811-011-9671-6
Hung L.D., Hirayama M., Ly B.M., Hori K. 2015. Purification, primary structure, and biological activity of high-mannose N-glycan-specific lectin from the cultivated. Eucheuma denticulatum. J. Appl. Phycol. 27: 1657–1669. https://doi.org/10.1007/s10811-014-0441-0 https://www.ncbi.nlm.nih.gov/pubmed/32214663 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7088313
Iwanaga S., Lee B.L. 2005. Recent advances in the innate immunity of invertebrate animals. J. Biochem. Mol. Biol. 38: 128–150. https://doi.org/10.5483/BMBRep.2005.38.2.128 https://www.ncbi.nlm.nih.gov/pubmed/15826490
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 https://www.ncbi.nlm.nih.gov/pubmed/5432063
Leite Y.F.M.M., Silva L.M.C.M., Amorim R.C.N., Freire E.A., Jorge D.M.M., Grangeiro T.B. 2005. Purification of a lectin from the marine red alga Gracilaria ornata and its effect on the development of the cowpea weevil Callosobruchus maculatus (Coleoptera: Bruchidae). Biochim. Biophys. Acta. 1724(1-2): 137–145. https://doi.org/10.1016/j.bbagen.2005.03.017 https://www.ncbi.nlm.nih.gov/pubmed/15869843
Lehmanna F.б Tiralongob E., Tiralongo J. 2006. Sialic acid-specific lectins: occurrence, specificity and function. Cell. Mol. Life Sci. 63: 1331–1354. https://doi.org/10.1007/s00018-005-5589-y https://www.ncbi.nlm.nih.gov/pubmed/16596337 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7079783
Liao W.R., Lin J.Y., Shieh W.Y., Jeng W.L., Huang R. 2003. Antibiotic activity of lectins from marine algae against marine vibrios. J. Ind. Microbiol. Biotechnol. 30: 433–439. https://doi.org/10.1007/s10295-003-0068-7 https://www.ncbi.nlm.nih.gov/pubmed/12884128
Lima M.E.P., Carneiro M.E., Nascimento A.E., Grangeiro T.B., Holanda M.L., Amorim R.C.N. 2005. Purification of a lectin from the marine red alga Gracilaria cornea and its effects on the Cattle Tick Boophilus microplus (Acari: Ixodidae). J. Agric. Food Chem. 53: 6414–6419. https://doi.org/10.1021/jf0509660 https://www.ncbi.nlm.nih.gov/pubmed/16076127
Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265–275. https://doi.org/10.1016/S0021-9258(19)52451-6
Mandal C., Mandal C. 1990. Sialic acid binding lectins. Experientia. 46: 433–441. https://doi.org/10.1007/BF01954221 https://www.ncbi.nlm.nih.gov/pubmed/2189746
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. 15(8): 255. https://doi.org/ https://doi.org/10.3390/md15080255 https://www.ncbi.nlm.nih.gov/pubmed/28813016 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5577609
Okamoto R., Hori K., Miyazawa K., Ito K. 1990. Isolation and characterization of a new hemagglutinin from the red alga Gracilaria bursa-pastoris. Experientia. 46(9): 975–977. https://doi.org/10.1007/BF01939393 https://www.ncbi.nlm.nih.gov/pubmed/2209806
O'Keefe B.R., Giomarelli B., Barnard D.L., Shenoy S.R., Chan P.K.S., McMahon J.B. 2010. Broad-spectrum in vitro activity and in vivo efficacy of the antiviral protein Griffithsin against emerging viruses of the family Coronaviridae. J. Virol. 84(5): 2511–2521. https://doi.org/10.1128/JVI.02322-09 https://www.ncbi.nlm.nih.gov/pubmed/20032190 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2820936
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. Com. 405(2): 291–296. https://doi.org/10.1016/j.bbrc.2011.01.031 https://www.ncbi.nlm.nih.gov/pubmed/21219864 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7092952
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(22): 19446–19458. https://doi.org/10.1074/jbc.M110.216655 https://www.ncbi.nlm.nih.gov/pubmed/21460211 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3103324
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(6): 3454–3465. https://doi.org/10.3390/md13063454 https://www.ncbi.nlm.nih.gov/pubmed/26035023 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4483639
Schauer R., Kelm S., Reuter G., Roggentin P., Shaw L. 1995. In: Biology of the Sialic Acids. Boston, MA: Springer. Pp. 7–67. https://doi.org/10.1007/978-1-4757-9504-2_2
Schultze B., Gross H.J., Brossmer R., Herrler G. 1991. The S protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinant. J. Virol. 65(11): 6232–6237. https://doi.org/10.1128/jvi.65.11.6232-6237.1991 https://www.ncbi.nlm.nih.gov/pubmed/1920630
Sharon N., Lis L. 1989. Lectins as cell recognition molecules. Science. 246(4927): 227–234. https://doi.org/10.1126/science.2552581 https://www.ncbi.nlm.nih.gov/pubmed/2552581
Sharon N., Lis H. 2003. In: Lectins. 2nd ed. Dordrecht, The Netherlands: Kluwer Acad. Publ. 450 p.
Sohrab S.S., Suhail M., Kamal M.A., Ahmad F., Azhar E.I. 2020. The emergence of human pathogenic Coronaviruses: Lectins as antivirals for SARS-CoV-2. Curr. Pharm. Des. 26(41): 5286–5292. https://doi.org/10.2174/1381612826666200821120409 https://www.ncbi.nlm.nih.gov/pubmed/32954998
Suzuki Y. 2005. Sialobiology of influenza: Molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull. 28(3): 399–408. https://doi.org/10.1248/bpb.28.399 https://www.ncbi.nlm.nih.gov/pubmed/15744059
Tsuji T., Yamamoto K., Irimura T., Osawa T. 1981. Structure of carbohydrate unit A of porcine thyroglobulin. J. Biochem. 195(3): 691–699. https://doi.org/10.1042/bj1950691 https://www.ncbi.nlm.nih.gov/pubmed/7316979 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1162942
Unemo M., Aspholm-Hurtig M., Ilver D., Bergstrom J., Boren T., Danielsson D., Susann T. 2005. The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J. Biol Chem. 280(15): 15390–15397. https://doi.org/10.1074/jbc.M412725200 https://www.ncbi.nlm.nih.gov/pubmed/15689619
Van den Eijnden D.H., Joziasse D.H. 1993. Enzymes associated with glycosylation. Curr. Opin. Struct. Biol. 3: 711–721. https://doi.org/10.1016/0959-440X(93)90054-O
Wopereis S., Lefeber D.J., Morava E., Wevers R.A. 2006. Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects: A Review. Clin. Chem. 52(4): 574–600. https://doi.org/10.1373/clinchem.2005.063040 https://www.ncbi.nlm.nih.gov/pubmed/16497938
Yamamoto K., Tsuji T., Irimura T., Osawa T. 1981. The structure of carbohydrate unit B of porcine thyroglobulin. J. Biochem. 195(3): 701–713. https://doi.org/10.1042/bj1950701 https://www.ncbi.nlm.nih.gov/pubmed/7316980 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1162943
Zeng F.Y., Gabius H.J. 1992. Sialic Acid-Binding Proteins: Characterization, Biological Function and Application. Z. Naturforsch. C. 47(9-10): 641–653. https://doi.org/10.1515/znc-1992-9-1001 https://www.ncbi.nlm.nih.gov/pubmed/1449590
