Carbohydrate-Binding Agents: Potential of Repurposing for COVID-19 Therapy

Author(s): Rajesh Kumar Gupta*, Girish R. Apte, Kiran Bharat Lokhande, Satyendra Mishra, Jayanta K. Pal

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 11 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

With the emergence of the novel severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), the whole world is suffering from atypical pneumonia, which resulted in more than 559,047 deaths worldwide. In this time of crisis and urgency, the only hope comes from new candidate vaccines and potential antivirals. However, formulating new vaccines and synthesizing new antivirals are a laborious task. Therefore, considering the high infection rate and mortality due to COVID-19, utilization of previous information, and repurposing of existing drugs against valid viral targets have emerged as a novel drug discovery approach in this challenging time. The transmembrane spike (S) glycoprotein of coronaviruses (CoVs), which facilitates the virus’s entry into the host cells, exists in a homotrimeric form and is covered with N-linked glycans. S glycoprotein is known as the main target of antibodies having neutralizing potency and is also considered as an attractive target for therapeutic or vaccine development. Similarly, targeting of N-linked glycans of S glycoprotein envelope of CoV via carbohydrate-binding agents (CBAs) could serve as an attractive therapeutic approach for developing novel antivirals. CBAs from natural sources like lectins from plants, marine algae and prokaryotes and lectin mimics like Pradimicin-A (PRM-A) have shown antiviral activities against CoV and other enveloped viruses. However, the potential use of CBAs specifically lectins was limited due to unfavorable responses like immunogenicity, mitogenicity, hemagglutination, inflammatory activity, cellular toxicity, etc. Here, we reviewed the current scenario of CBAs as antivirals against CoVs, presented strategies to improve the efficacy of CBAs against CoVs; and studied the molecular interactions between CBAs (lectins and PRM-A) with Man9 by molecular docking for potential repurposing against CoVs in general, and SARSCoV- 2, in particular.

Keywords: Lectin, COVID-19, SARS-CoV-2, carbohydrate binding agents, pradimicin-A, CBAS.

[1]
Cherian, S.S.; Agrawal, M.; Basu, A.; Abraham, P.; Gangakhedkar, R.R.; Bhargava, B. Perspectives for repurposing drugs for the coronavirus disease. Indian J. Med. Res., 2020, 151(2), 160-171.
[2]
World Health Organization Coronavirus: Disease (COVID-19) Dashboard https://covid19.who.int/
[4]
Tortorici, M.A.; Veesler, D. Structural insights into coronavirus entry. Adv. Virus Res., 2019, 105, 93-116.
[http://dx.doi.org/10.1016/bs.aivir.2019.08.002] [PMID: 31522710]
[5]
Hoffmann, M.; Kleine-Weber, H.; Pöhlmann, S. A Multibasic Cleavage Site in the Spike Protein of SARS-CoV-2 Is Essential for Infection of Human Lung Cells. Mol. Cell, 2020, 78(4), 779-784.e5.
[http://dx.doi.org/10.1016/j.molcel.2020.04.022] [PMID: 32362314]
[6]
Rossen, J.W.; de Beer, R.; Godeke, G.J.; Raamsman, M.J.; Horzinek, M.C.; Vennema, H.; Rottier, P.J. The viral spike protein is not involved in the polarized sorting of coronaviruses in epithelial cells. J. Virol., 1998, 72(1), 497-503.
[http://dx.doi.org/10.1128/JVI.72.1.497-503.1998] [PMID: 9420251]
[7]
Walls, A.C.; Tortorici, M.A.; Frenz, B.; Snijder, J.; Li, W.; Rey, F.A.; DiMaio, F.; Bosch, B.J.; Veesler, D. Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat. Struct. Mol. Biol., 2016, 23(10), 899-905.
[http://dx.doi.org/10.1038/nsmb.3293] [PMID: 27617430]
[8]
Walls, A.C.; Xiong, X.; Park, Y.J.; Tortorici, M.A.; Snijder, J.; Quispe, J.; Cameroni, E.; Gopal, R.; Dai, M.; Lanzavecchia, A.; Zambon, M.; Rey, F.A.; Corti, D.; Veesler, D. Unexpected Receptor Functional Mimicry Elucidates Activation of Coronavirus Fusion. Cell, 2019, 176(5), 1026-1039.e15.
[http://dx.doi.org/10.1016/j.cell.2018.12.028] [PMID: 30712865]
[9]
Walls, A.C.; Park, Y.J.; Tortorici, M.A.; Wall, A.; McGuire, A.T.; Veesler, D. Structure, Function, and Antigenicity of the SARS- CoV-2 Spike Glycoprotein. Cell, 2020, 181(2), 281-292.e6.
[http://dx.doi.org/10.1016/j.cell.2020.02.058] [PMID: 32155444]
[10]
Xiong, X.; Tortorici, M.A.; Snijder, J.; Yoshioka, C.; Walls, A.C.; Li, W.; McGuire, A.T.; Rey, F.A.; Bosch, B.J.; Veesler, D. Glycan Shield and Fusion Activation of a Deltacoronavirus Spike Glycoprotein Fine-Tuned for Enteric Infections. J. Virol., 2018, 92(4), e01628-17.
[PMID: 29093093]
[11]
Watanabe, Y.; Allen, J.D.; Wrapp, D.; McLellan, J.S.; Crispin, M. Site-specific glycan analysis of the SARS-CoV-2 spike. Science, 2020, 369(6501), 330-333.
[PMID: 32366695]
[12]
Chiodo, F.; Bruijns, SCM.; Rodriguez, E.; Li, RJE.; Molinaro, A.; Silipo, A.; Lorenzo, FD.; Dagmar, GR.; Yury, VB.; Vicente, VB.; van Kooyk, Y. Novel ACE2-Independent Carbohydrate-Binding of SARS-CoV-2 Spike Protein to Host Lectins and Lung Microbiota bioRxiv, 2020.
[http://dx.doi.org/10.1101/2020.05.13.092478]
[13]
Peumans, W.J.; Zhang, W.; Barre, A.; Houlès Astoul, C.; Balint-Kurti, P.J.; Rovira, P.; Rougé, P.; May, G.D.; Van Leuven, F.; Truffa-Bachi, P.; Van Damme, E.J. Fruit-specific lectins from banana and plantain. Planta, 2000, 211(4), 546-554.
[http://dx.doi.org/10.1007/s004250000307] [PMID: 11030554]
[14]
Barre, A.; Simplicien, M.; Benoist, H.; Van Damme, E.J.M.; Rougé, P. Mannose-Specific Lectins from Marine Algae: Diverse Structural Scaffolds Associated to Common Virucidal and Anti- Cancer Properties. Mar. Drugs, 2019, 17(8), 440.
[http://dx.doi.org/10.3390/md17080440] [PMID: 31357490]
[15]
Singh, R.S.; Walia, A.K.; Khattar, J.S.; Singh, D.P.; Kennedy, J.F. Cyanobacterial lectins characteristics and their role as antiviral agents. Int. J. Biol. Macromol., 2017, 102, 475-496.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.04.041] [PMID: 28437766]
[16]
Vankadari, N.; Wilce, J.A. Emerging WuHan (COVID-19) coronavirus: glycan shield and structure prediction of spike glycoprotein and its interaction with human CD26. Emerg. Microbes Infect., 2020, 9(1), 601-604.
[http://dx.doi.org/10.1080/22221751.2020.1739565] [PMID: 32178593]
[17]
Gupta, B.; Sadaria, D.; Warrier, V.U.; Kirtonia, A.; Kant, R.; Awasthi, A.; Baligar, P.; Pal, J.K.; Yuba, E.; Sethi, G.; Garg, M.; Gupta, R.K. Plant lectins and their usage in preparing targeted nanovaccines for cancer immunotherapy. Semin. Cancer Biol., 2020, S1044-579X(20)30038-9.
[http://dx.doi.org/10.1016/j.semcancer.2020.02.005] [PMID: 32068087]
[18]
Mitchell, C.A.; Ramessar, K.; O’Keefe, B.R. Antiviral lectins: Selective inhibitors of viral entry. Antiviral Res., 2017, 142, 37-54.
[http://dx.doi.org/10.1016/j.antiviral.2017.03.007] [PMID: 28322922]
[19]
Takeuchi, T.; Hara, T.; Naganawa, H.; Okada, M.; Hamada, M.; Umezawa, H.; Gomi, S.; Sezaki, M.; Kondo, S. New antifungal antibiotics, benanomicins A and B from an actinomycete. J.Antibiot. (Tokyo), 1988, 41(6), 807-811.
[http://dx.doi.org/10.7164/antibiotics.41.807] [PMID: 3403377]
[20]
Oki, T.; Konishi, M.; Tomatsu, K.; Tomita, K.; Saitoh, K.; Tsunakawa, M.; Nishio, M.; Miyaki, T.; Kawaguchi, H. Pradimicin, a novel class of potent antifungal antibiotics. J. Antibiot. (Tokyo), 1988, 41(11), 1701-1704.
[http://dx.doi.org/10.7164/antibiotics.41.1701] [PMID: 3198502]
[21]
Tanabe-Tochikura, A.; Tochikura, T.S.; Yoshida, O.; Oki, T.; Yamamoto, N. Pradimicin A inhibition of human immunodeficiency virus: attenuation by mannan. Virology, 1990, 176(2), 467-473.
[http://dx.doi.org/10.1016/0042-6822(90)90016-K] [PMID: 2345961]
[22]
Tanabe-Tochikura, A.; Tochikura, T.S.; Blakeslee, J.R., Jr; Olsen, R.G.; Mathes, L.E. Anti-human immunodeficiency virus (HIV) agents are also potent and selective inhibitors of feline immunodeficiency virus (FIV)-induced cytopathic effect: development of a new method for screening of anti-FIV substances in vitro. Antiviral Res., 1992, 19(2), 161-172.
[http://dx.doi.org/10.1016/0166-3542(92)90075-G] [PMID: 1332602]
[23]
Krokhin, O.; Li, Y.; Andonov, A.; Feldmann, H.; Flick, R.; Jones, S.; Stroeher, U.; Bastien, N.; Dasuri, K.V.; Cheng, K.; Simonsen, J.N.; Perreault, H.; Wilkins, J.; Ens, W.; Plummer, F.; Standing, K.G. Mass spectrometric characterization of proteins from the SARS virus: a preliminary report. Mol. Cell. Proteomics, 2003, 2(5), 346-356.
[http://dx.doi.org/10.1074/mcp.M300048-MCP200] [PMID: 12775768]
[24]
Keyaerts, E.; Vijgen, L.; Pannecouque, C.; Van Damme, E.; Peumans, W.; Egberink, H.; Balzarini, J.; Van Ranst, M. Plant lectins are potent inhibitors of coronaviruses by interfering with two targets in the viral replication cycle. Antiviral Res., 2007, 75(3), 179-187.
[http://dx.doi.org/10.1016/j.antiviral.2007.03.003] [PMID: 17428553]
[25]
van der Meer, F.J.; de Haan, C.A.; Schuurman, N.M.; Haijema, B.J.; Peumans, W.J.; Van Damme, E.J.; Delputte, P.L.; Balzarini, J.; Egberink, H.F. Antiviral activity of carbohydrate-binding agents against Nidovirales in cell culture. Antiviral Res., 2007, 76(1), 21-29.
[http://dx.doi.org/10.1016/j.antiviral.2007.04.003] [PMID: 17560666]
[26]
van der Meer, F.J.; de Haan, C.A.; Schuurman, N.M.; Haijema, B.J.; Verheije, M.H.; Bosch, B.J.; Balzarini, J.; Egberink, H.F. The carbohydrate-binding plant lectins and the non-peptidic antibiotic pradimicin A target the glycans of the coronavirus envelope glycoproteins. J. Antimicrob. Chemother., 2007, 60(4), 741-749.
[http://dx.doi.org/10.1093/jac/dkm301] [PMID: 17704516]
[27]
Ziółkowska, N.E.; O’Keefe, B.R.; Mori, T.; Zhu, C.; Giomarelli, B.; Vojdani, F.; Palmer, K.E.; McMahon, J.B.; Wlodawer, A. Domain-swapped structure of the potent antiviral protein griffithsin and its mode of carbohydrate binding. Structure, 2006, 14(7), 1127-1135.
[http://dx.doi.org/10.1016/j.str.2006.05.017] [PMID: 16843894]
[28]
Ziółkowska, N.E.; Shenoy, S.R.; O’Keefe, B.R.; McMahon, J.B.; Palmer, K.E.; Dwek, R.A.; Wormald, M.R.; Wlodawer, A. Crystallographic, thermodynamic, and molecular modeling studies of the mode of binding of oligosaccharides to the potent antiviral protein griffithsin. Proteins, 2007, 67(3), 661-670.
[http://dx.doi.org/10.1002/prot.21336] [PMID: 17340634]
[29]
Mori, T.; O’Keefe, B.R.; Sowder, R.C., II; Bringans, S.; Gardella, R.; Berg, S.; Cochran, P.; Turpin, J.A.; Buckheit, R.W., Jr; McMahon, J.B.; Boyd, M.R. Isolation and characterization of griffithsin, a novel HIV-inactivating protein, from the red alga Griffithsia sp. J. Biol. Chem., 2005, 280(10), 9345-9353.
[http://dx.doi.org/10.1074/jbc.M411122200] [PMID: 15613479]
[30]
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 Broad-spectrum in vitro activity and in vivo efficacy of the antiviral protein griffithsin against emerging viruses of the family Coronaviridae. J. Virol., 2010, 84(5), 2511-2521.
[http://dx.doi.org/10.1128/JVI.02322-09] [PMID: 20032190]
[31]
Barton, C.; Kouokam, J.C.; Lasnik, A.B.; Foreman, O.; Cambon, A.; Brock, G.; Montefiori, D.C.; Vojdani, F.; McCormick, A.A.; O’Keefe, B.R.; Palmer, K.E. Activity of and effect of subcutaneous treatment with the broad-spectrum antiviral lectin griffithsin in two laboratory rodent models. Antimicrob. Agents Chemother., 2014, 58(1), 120-127.
[http://dx.doi.org/10.1128/AAC.01407-13] [PMID: 24145548]
[32]
Barton, C.; Kouokam, J.C.; Hurst, H.; Palmer, K.E. Pharmacokinetics of the Antiviral Lectin Griffithsin Administered by Different Routes Indicates Multiple Potential Uses. Viruses, 2016, 8(12), E331.
[http://dx.doi.org/10.3390/v8120331] [PMID: 27999325]
[33]
Millet, J.K.; Séron, K.; Labitt, R.N.; Danneels, A.; Palmer, K.E.; Whittaker, G.R.; Dubuisson, J.; Belouzard, S. Middle East respiratory syndrome coronavirus infection is inhibited by griffithsin. Antiviral Res., 2016, 133, 1-8.
[http://dx.doi.org/10.1016/j.antiviral.2016.07.011] [PMID: 27424494]
[34]
Shenoy, S.R.; O’Keefe, B.R.; Bolmstedt, A.J.; Cartner, L.K.; Boyd, M.R. Selective interactions of the human immunodeficiency virus-inactivating protein cyanovirin-N with high-mannose oligosaccharides on gp120 and other glycoproteins. J. Pharmacol. Exp. Ther., 2001, 297(2), 704-710.
[PMID: 11303061]
[35]
Shahzad-ul-Hussan, S.; Gustchina, E.; Ghirlando, R.; Clore, G.M.; Bewley, C.A. Solution structure of the monovalent lectin microvirin in complex with Man(alpha)(1-2)Man provides a basis for anti-HIV activity with low toxicity. J. Biol. Chem., 2011, 286(23), 20788-20796.
[http://dx.doi.org/10.1074/jbc.M111.232678] [PMID: 21471192]
[36]
Huskens, D.; Férir, G.; Vermeire, K.; Kehr, J.C.; Balzarini, J.; Dittmann, E.; Schols, D. Microvirin, a novel alpha(1,2)-mannose-specific lectin isolated from Microcystis aeruginosa, has anti-HIV-1 activity comparable with that of cyanovirin-N but a much higher safety profile. J. Biol. Chem., 2010, 285(32), 24845-24854.
[http://dx.doi.org/10.1074/jbc.M110.128546] [PMID: 20507987]
[37]
Bewley, C.A.; Cai, M.; Ray, S.; Ghirlando, R.; Yamaguchi, M.; Muramoto, K. New carbohydrate specificity and HIV-1 fusion blocking activity of the cyanobacterial protein MVL: NMR, ITC and sedimentation equilibrium studies. J. Mol. Biol., 2004, 339(4), 901-914.
[http://dx.doi.org/10.1016/j.jmb.2004.04.019] [PMID: 15165858]
[38]
Hoorelbeke, B.; Huskens, D.; Férir, G.; François, K.O.; Takahashi, A.; Van Laethem, K.; Schols, D.; Tanaka, H.; Balzarini, J. Actinohivin, a broadly neutralizing prokaryotic lectin, inhibits HIV-1 infection by specifically targeting high-mannose-type glycans on the gp120 envelope. Antimicrob. Agents Chemother., 2010, 54(8), 3287-3301.
[http://dx.doi.org/10.1128/AAC.00254-10] [PMID: 20498311]
[39]
Alexandre, K.B.; Gray, E.S.; Mufhandu, H.; McMahon, J.B.; Chakauya, E.; O’Keefe, B.R.; Chikwamba, R.; Morris, L. The lectins griffithsin, cyanovirin-N and scytovirin inhibit HIV-1 binding to the DC-SIGN receptor and transfer to CD4(+) cells. Virology, 2012, 423(2), 175-186.
[http://dx.doi.org/10.1016/j.virol.2011.12.001] [PMID: 22209231]
[40]
Alexandre, K.B.; Gray, E.S.; Lambson, B.E.; Moore, P.L.; Choge, I.A.; Mlisana, K.; Karim, S.S.; McMahon, J.; O’Keefe, B.; Chikwamba, R.; Morris, L. Mannose-rich glycosylation patterns on HIV-1 subtype C gp120 and sensitivity to the lectins, Griffithsin, Cyanovirin-N and Scytovirin. Virology, 2010, 402(1), 187-196.
[http://dx.doi.org/10.1016/j.virol.2010.03.021] [PMID: 20392471]
[41]
Balzarini, J. Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses? Antivir. Chem. Chemother., 2007, 18(1), 1-11.
[http://dx.doi.org/10.1177/095632020701800101] [PMID: 17354647]
[42]
Balzarini, J. Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy. Nat. Rev. Microbiol., 2007, 5(8), 583-597.
[http://dx.doi.org/10.1038/nrmicro1707] [PMID: 17632570]
[43]
Parker, A.S.; Choi, Y.; Griswold, K.E.; Bailey-Kellogg, C. Structure-guided deimmunization of therapeutic proteins. J. Comput. Biol., 2013, 20(2), 152-165.
[http://dx.doi.org/10.1089/cmb.2012.0251] [PMID: 23384000]
[44]
Choi, Y.; Griswold, K.E.; Bailey-Kellogg, C. Structure-based redesign of proteins for minimal T-cell epitope content. J. Comput. Chem., 2013, 34(10), 879-891.
[http://dx.doi.org/10.1002/jcc.23213] [PMID: 23299435]
[45]
Choi, Y.; Verma, D.; Griswold, K.E.; Bailey-Kellogg, C. EpiSweep: Computationally Driven Reengineering of Therapeutic Proteins to Reduce Immunogenicity While Maintaining Function. Methods Mol. Biol., 2017, 1529, 375-398.
[http://dx.doi.org/10.1007/978-1-4939-6637-0_20] [PMID: 27914063]
[46]
Swanson, M.D.; Boudreaux, D.M.; Salmon, L.; Chugh, J.; Winter, H.C.; Meagher, J.L.; André, S.; Murphy, P.V.; Oscarson, S.; Roy, R.; King, S.; Kaplan, M.H.; Goldstein, I.J.; Tarbet, E.B.; Hurst, B.L.; Smee, D.F.; de la Fuente, C.; Hoffmann, H.H.; Xue, Y.; Rice, C.M.; Schols, D.; Garcia, J.V.; Stuckey, J.A.; Gabius, H.J.; Al-Hashimi, H.M.; Markovitz, D.M. Engineering a therapeutic lectin by uncoupling mitogenicity from antiviral activity. Cell, 2015, 163(3), 746-758.
[http://dx.doi.org/10.1016/j.cell.2015.09.056] [PMID: 26496612]
[47]
Liu, X.; Testa, B.; Fahr, A. Lipophilicity and its relationship with passive drug permeation. Pharm. Res., 2011, 28(5), 962-977.
[http://dx.doi.org/10.1007/s11095-010-0303-7] [PMID: 21052797]
[48]
Tolle-Sander, S.; Lentz, K.A.; Maeda, D.Y.; Coop, A.; Polli, J.E. Increased acyclovir oral bioavailability via a bile acid conjugate. Mol. Pharm., 2004, 1(1), 40-48.
[http://dx.doi.org/10.1021/mp034010t] [PMID: 15832499]
[49]
Fragopoulou, E.; Nomikos, T.; Karantonis, H.C.; Apostolakis, C.; Pliakis, E.; Samiotaki, M.; Panayotou, G.; Antonopoulou, S. Biological activity of acetylated phenolic compounds. J. Agric. Food Chem., 2007, 55(1), 80-89.
[http://dx.doi.org/10.1021/jf0627221] [PMID: 17199317]
[50]
Aburaki, S.; Yamashita, Y.; Ohnuma, T.; Kamachi, H.; Moriyama, T.; Masuyoshi, S.; Kamei, H.; Konishi, M.; Oki, T. Synthesis and antifungal activity of pradimicin derivatives. Modifications of the sugar part. J. Antibiot. (Tokyo), 1993, 46(4), 631-640.
[http://dx.doi.org/10.7164/antibiotics.46.631] [PMID: 8501006]
[51]
Trott, O.; Olson, A.J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem., 2010, 31(2), 455-461.
[PMID: 19499576]
[52]
Kim, S.; Thiessen, P.A.; Bolton, E.E.; Chen, J.; Fu, G.; Gindulyte, A.; Han, L.; He, J.; He, S.; Shoemaker, B.A.; Wang, J.; Yu, B.; Zhang, J.; Bryant, S.H. PubChem Substance and Compound databases. Nucleic Acids Res., 2016, 44(D1), D1202-D1213.
[http://dx.doi.org/10.1093/nar/gkv951] [PMID: 26400175]
[53]
Release, S. 2019-4: Maestro; Schrodinger, LLC: New York, NY, 2019.
[54]
Gabius, H.J. The magic of the sugar code. Trends Biochem. Sci., 2015, 40(7), 341.
[http://dx.doi.org/10.1016/j.tibs.2015.04.003] [PMID: 26006324]
[55]
Dimitrov, D.S. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol., 2004, 2(2), 109-122.
[http://dx.doi.org/10.1038/nrmicro817] [PMID: 15043007]
[56]
Akkouh, O.; Ng, T.B.; Singh, S.S.; Yin, C.; Dan, X.; Chan, Y.S.; Pan, W.; Cheung, R.C. Lectins with anti-HIV activity: a review. Molecules, 2015, 20(1), 648-668.
[http://dx.doi.org/10.3390/molecules20010648] [PMID: 25569520]
[57]
Swanson, M.D.; Winter, H.C.; Goldstein, I.J.; Markovitz, D.M. A lectin isolated from bananas is a potent inhibitor of HIV replication. J. Biol. Chem., 2010, 285(12), 8646-8655.
[http://dx.doi.org/10.1074/jbc.M109.034926] [PMID: 20080975]
[58]
Lifson, J.; Coutré, S.; Huang, E.; Engleman, E. Role of envelope glycoprotein carbohydrate in human immunodeficiency virus (HIV) infectivity and virus-induced cell fusion. J. Exp. Med., 1986, 164(6), 2101-2106.
[http://dx.doi.org/10.1084/jem.164.6.2101] [PMID: 3640800]
[59]
Balzarini, J.; Neyts, J.; Schols, D.; Hosoya, M.; Van Damme, E.; Peumans, W.; De Clercq, E. The mannose-specific plant lectins from Cymbidium hybrid and Epipactis helleborine and the (N-acetylglucosamine)n-specific plant lectin from Urtica dioica are potent and selective inhibitors of human immunodeficiency virus and cytomegalovirus replication in vitro. Antiviral Res., 1992, 18(2), 191-207.
[http://dx.doi.org/10.1016/0166-3542(92)90038-7] [PMID: 1329650]
[60]
Li, Y.; Liao, X.; Chen, G.; Yap, Y.; Zhang, X. Cloning, expression and purification of Microcystis viridis lectin in Escherichia coli. Mol. Biotechnol., 2011, 47(2), 105-110.
[http://dx.doi.org/10.1007/s12033-010-9315-0] [PMID: 20652446]
[61]
Capell, T.; Twyman, R.M.; Armario-Najera, V.; Ma, J.K.; Schillberg, S.; Christou, P. Potential Applications of Plant Biotechnology against SARS-CoV-2. Trends Plant Sci., 2020, 25(7), 635-643.
[http://dx.doi.org/10.1016/j.tplants.2020.04.009] [PMID: 32371057]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 11
Year: 2020
Page: [1085 - 1096]
Pages: 12
DOI: 10.2174/1389203721666200918153717
Price: $65

Article Metrics

PDF: 25
HTML: 3
PRC: 1