The new member of OAAH-family lectins from the cultivated red alga Eucheuma denticulatum in Vietnam
Section:
Flora and GeographyIssue:
Vol. 35 No. 3 (2025)Pages:
194-209DOI:
https://doi.org/10.15407/alg35.03.194Abstract
The red alga Eucheuma denticulatum is an economically important food species extensively cultivated in Vietnam. In this study, complementary DNA (cDNA) cloning based on the rapid amplification of cDNA ends (RACE) methods elucidated the full-length sequence of a new lectin-like protein (named EDL)from this alga. The cDNA cloning of thelectin-like protein encoded a polypeptide of 268 amino acids including an initiating methionine. The deduced amino acid sequence of lectin-like protein composed of four tandem repeated domains of about 67 amino acids and sharing 45% sequence identity.The primary structure of the lectin-like protein, EDL, highly resemble with those of the anti-virus and anti-cancer high-mannose N-glycan specific lectins in lower organisms including Oscillatoria agardhii NIES-240 (OAA) from cyanobacterium, Burkholderia oklahomensis EO147 (BOA), Myxococcus xanthus (MBHA) and Pseudomonas fluorescens Pf0-1 (PFL) from proteobacteria, Eucheuma serra (ESA-2), Eucheuma denticulatum (EDA-2), Kappaphycus striatus (KSA-1 and KSA-2), Kappaphycus alvarezii (KAA-1 and KAA-2) and Solieria filiformis (SfL-1 and SfL-2) from carrageenophyte red algae. The high resemblance in structure with anti-virus and anti-cancer lectins suggests that the cultivated red alga E. denticulatum could also be a good source of functional protein (lectin) for application.
Keywords:
amino acid sequence, carrageenophytes, cDNA of lectin-like protein, EDL, Eucheuma denticulatumFull text
References
Balzarini J. 2007. Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses. Antivir. Chem. Chemother. 18(1): 1–11. https://doi.org/10.1177/095632020701800101 https://www.ncbi.nlm.nih.gov/pubmed/17354647
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): 543. https://doi.org/10.3390/md18110543 https://www.ncbi.nlm.nih.gov/pubmed/33138151 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693892
Bewley C.A., Cai M., Ray S., Ghirlando R., Yamaguchi M., Muramoto K. 2004. New carbohydrate specificity and HIV-1 fusion blocking activity of the cyanobacterial protein MVL: NMR, ITC and sedimentation equilib-rium studies. J. Mol. Biol. 339(4): 901–914. https://doi.org/10.1016/j.jmb.2004.04.019 https://www.ncbi.nlm.nih.gov/pubmed/15165858 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2650105
Bokesch H.R., O'Keefe B.R., McKee T.C., Pannell L.K., Patterson G.M., Gardella R.S., Sowder R.C., Turpin J., Watson K., Buckheit R.W., Boyd M.R. 2003. A potent novel anti-HIV protein from the cultured cyanobacterium Scytonema varium. Biochem. 42: 2578–2584. https://doi.org/10.1021/bi0205698 https://www.ncbi.nlm.nih.gov/pubmed/12614152
Boyd M.R., Gustafson K.R., Mcmahon J.B., Shoemaker R.H., O'Keefe B.R., Mori T., Gulakowski R.J., Wu L., Rivera M.I., Laurencot C.M., Currens M.J., Cardellina I.I.J.H., Buckheit Jr.R.W., Nara P.L., Pannell L.K., Sowder I.I.R.C., Henderson L.E. 1997. Discovery of cyanovirin-N, a novel human immunodeficiency virus inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob. Agents Chemother. 41: 1521–1530. https://doi.org/10.1128/AAC.41.7.1521 https://www.ncbi.nlm.nih.gov/pubmed/9210678 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC163952
Cavalier-Smith T. 2000. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5(4): 174–182. https://doi.org/10.1016/S1360-1385(00)01598-3 https://www.ncbi.nlm.nih.gov/pubmed/10740299
Chaves R.P., da Silva S.R., Neto L.G.N., Carneiro R.F., da Silva A.L.C., Sampaio A.H., de Sousa B.L., Cabral M.G., Videira P.A., Teixeira E.H., Nagano C.S. 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. https://doi.org/10.1016/j.ijbiomac.2017.09.116 https://www.ncbi.nlm.nih.gov/pubmed/28970169
Chiba H., Inokoshi J., Okamoto M., Asanuma S., Matsuzaki K., Iwama M., Mizumoto K., Tanaka H., Oheda M., Fujita K., Nakashima H., Shinose M., Takahashi Y., Omura S. 2001. Actinohivin, a novel anti-HIV protein from an actinomycete that inhibits syncytium formation: isolation, characterization, and biological activities. Biochem. Biophys. Res. Commun. 282(2): 595–601. https://doi.org/10.1006/bbrc.2001.4495 https://www.ncbi.nlm.nih.gov/pubmed/11401502
Chisholm J.R.M., Dauga C., Ageron E., Grimont P.A.D., Jaubert J.M. 1996. Roots in mixotrophic algae. Nature. 381: 382. https://doi.org/10.1038/381382a0
Fourçans A., De Oteyza T.G., Wieland A., Solé A., Diestra E., Bleijswijk J.V., Grimalt J.O., Kühl M., Esteve I., Muyzer G., Caumette P., Duran R. 2004. Characterization of functional bacterial groups in a hypersaline microbial mat community (Salins-de-Giraud, Camargue, France). FEMS Microbiol. Ecol. 51(1): 55–70. https://doi.org/10.1016/j.femsec.2004.07.012 https://www.ncbi.nlm.nih.gov/pubmed/16329855
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 Eucheuma serra agglutinin on colon cancer cells in vitro and in vivo. Anticanc. Drugs. 17(8): 943–947. https://doi.org/10.1097/01.cad.0000224458.13651.b4 https://www.ncbi.nlm.nih.gov/pubmed/16940804
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. https://doi.org/10.1155/2012/842785 (Online Library). https://www.ncbi.nlm.nih.gov/pubmed/23346404 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3543805
Helle F., Wychowski C., Vu-Dac N., Gustafson K.R., Voisset C., Dubuisson J. 2006. Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans. J. Biol. Chem. 281(35): 25177–25183. https://doi.org/10.1074/jbc.M602431200 https://www.ncbi.nlm.nih.gov/pubmed/16809348
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://www.ncbi.nlm.nih.gov/pmc/articles/PMC7608414
Hori K., Matsubara K., Miyasawa K. 2000. Primary structures of two hemaglutinins from marine red alga Hypnea japonica. Biochim. Biophys. Acta. 1474(2): 226–236. https://doi.org/10.1016/S0304-4165(00)00008-8
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 serralectin. Glycobiology. 17(5): 479–491. https://doi.org/10.1093/glycob/cwm007 https://www.ncbi.nlm.nih.gov/pubmed/17259190
Hung L.D., Trinh P.T.H. 2021. 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., Hirayama M., Ly B.M., 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(4): 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
Hung L.D., Hirayama M., Ly B.M., 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. https://doi.org/10.1016/j.phytol.2015.09.012
Imai K., Nakai K. 2010. Prediction of subcellular locations of proteins: where to proceed. Proteomics. 10(22): 3970–3983. https://doi.org/10.1002/pmic.201000274 https://www.ncbi.nlm.nih.gov/pubmed/21080490
Koharudin L.M.I., Gronenborn A.M. 2014. Antiviral lectins as potential HIV microbicides. Curr. Opin. Virol. 7: 95–100. https://doi.org/10.1016/j.coviro.2014.05.006 https://www.ncbi.nlm.nih.gov/pubmed/25010042 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4149946
Koharudin L.M.I., Furey W., Gronenborn A.M. 2011. Novel fold and carbohydrate specificity of from Oscillatoria agardhii the potent Anti-HIV cyanobacterial lectin. J. Biol. Chem. 286(2): 1588–1597. https://doi.org/10.1074/jbc.M110.173278 https://www.ncbi.nlm.nih.gov/pubmed/20961847 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3020767
Koharudin L.M.I., Kollipara S., Aiken C., Gronenborn A.M. 2012. Structural insights into the anti-HIV activity of the Oscillatoria agardhii agglutinin homolog lectin family. J. Biol. Chem. 287(40): 33796–33811. https://doi.org/10.1074/jbc.M112.388579 https://www.ncbi.nlm.nih.gov/pubmed/22865886 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3460475
Moreira D., Le Guyader H., Philippe H. 2000. The origin of red algae and theevolution of chloroplasts. Nature. 405(6782): 69–72. https://doi.org/10.1038/35011054 https://www.ncbi.nlm.nih.gov/pubmed/10811219
Mori T., O'Keefe B.R., Sowder R.C., Bringans S., Gardella R.S., Berg S., Cochran P., Turpin J.A., Buckheit R.W., McMahon J.B.Jr., Boyd M.R. 2005. Isolation and characterization of griffithsin, a novel HIV-inactivating protein, from the red alga Griffithsia sp. J. Biol. Chem. 280(10): 9345–9353. https://doi.org/10.1074/jbc.M411122200 https://www.ncbi.nlm.nih.gov/pubmed/15613479
Mu J., Hirayama M., Sato Y., Morimoto K., Hori K.A. 2017. 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/10.3390/md15080255 https://www.ncbi.nlm.nih.gov/pubmed/28813016 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5577609
O'Keefe B.R., Giomarelli B., Barnard D.L., Shenoy S.R., Chan P.K., McMahon J.B., Palmer K.E., Barnett B.W., Meyerholz D.K., Wohlford-Lenane C.L., McCray P.B.Jr. 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
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. https://doi.org/10.1016/j.ijpharm.2010.01.033 https://www.ncbi.nlm.nih.gov/pubmed/20100554
Romeo J.M., Esmon B., Zusman D.R. 1986. Nucleotide sequence of the myxobacterium hemagglutinin gene contains four homologous domains. Proc. Natl. Acad. Sci. USA. 83(17): 6332–6336. https://doi.org/10.1073/pnas.83.17.6332 https://www.ncbi.nlm.nih.gov/pubmed/3092212 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC386497
Romero J.A.F., Paglini M.G., Priano C., Koroch A., Rodríguez Y., James Sailer J., Teleshova N. 2021. Algal and Cyanobacterial Lectins and Their Antimicrobial Properties. Mar. Drugs. 19(12): 687. https://doi.org/10.3390/md19120687 https://www.ncbi.nlm.nih.gov/pubmed/34940686 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8707200
Sato T., Hori K. 2009. Cloning, expression, and characterization of a novel anti-HIV lectin from the cultured cyanobacterium Oscillatoria agardhii. Fish. Sci. 75: 743–753. https://doi.org/10.1007/s12562-009-0074-4
Sato Y., Okuyama S., Hori K. 2007. Primary structure and carbohydrate-binding specificity of a potent anti-HIV lectin isolated from the filamentous cyanobacterium Oscillatoria agardhii. J. Biol. Chem. 282(15): 11021–11029. https://doi.org/10.1074/jbc.M701252200 https://www.ncbi.nlm.nih.gov/pubmed/17314091
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(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., Yanagihara K., Seyama T. 2012. High mannose-binding antiviral lectin PFL from Pseudomonas fluorescens Pf0-1 promotes cell death of gastric cancer cell MKN28 via interaction with α2-integrin. PLos One. 7(9): e45922. https://doi.org/10.1371/journal.pone.0045922 https://www.ncbi.nlm.nih.gov/pubmed/23029318 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3447791
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
Sharon N., Lis H. 2003. Lectins. 2nd ed. Dordrecht: Kluwer Acad. Publ. 454 p.
Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., Söding J., Thompson J.D., Higgins D.G. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7: 539. https://doi.org/10.1038/msb.2011.75 https://www.ncbi.nlm.nih.gov/pubmed/21988835 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3261699
Sugahara T., Ohama Y., Fukuda A., Hayashi M., Kawakubo A., 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(1-3): 93–99. https://doi.org/10.1023/A:1014057407251 https://www.ncbi.nlm.nih.gov/pubmed/19003319 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3449660
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30(12): 2725–2729. https://doi.org/10.1093/molbev/mst197 https://www.ncbi.nlm.nih.gov/pubmed/24132122 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3840312
Whitley M.J., Furey W., Kollipara S., Gronenborn A.M. 2013. Burkholderia oklahomensis agglutinin is a canonical twodomain OAA-family lectin: structures, carbohydrate binding, and anti-HIV activity. FEBS J. 280(9): 2056–2067. https://doi.org/10.1111/febs.12229 https://www.ncbi.nlm.nih.gov/pubmed/23480609 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3745830