Plant Antifungal Lectins: Mechanism of Action and Targets on Human Pathogenic Fungi

Page: [284 - 294] Pages: 11

  • * (Excluding Mailing and Handling)

Abstract

Lectins are proteins characterized by their ability to specifically bind different carbohydrate motifs. This feature is associated with their endogenous biological function as well as with multiple applications. Plants are important natural sources of these proteins; however, only a reduced group was shown to display antifungal activity. Although it is hypothesized that the target of lectins is the fungal cell wall, the mechanism through which they exert the antifungal action is poorly understood. This topic is relevant to improve treatment against pathogens of importance for human health. In this context, mechanisms pointing to essential attributes for virulence instead of the viability of the pathogen emerge as a promising approach. This review provides the current knowledge on the action mechanism of plant antifungal lectins and their putative use for the development of novel active principles against fungal infections.

Keywords: Plant lectins, antifungal, Candida, action mechanism, virulence attributes, adherence, morphological transition, biofilm, quorum sensing.

Graphical Abstract

[1]
Peumans, W.J.; Van Damme, E.J.M. Lectins as plant defense proteins. Plant Physiol., 1995, 109(2), 347-352.
[http://dx.doi.org/10.1104/pp.109.2.347] [PMID: 7480335]
[2]
Garcia-Pino, A.; Buts, L.; Wyns, L.; Imberty, A.; Loris, R. How a plant lectin recognizes high mannose oligosaccharides. Plant Physiol., 2007, 144(4), 1733-1741.
[http://dx.doi.org/10.1104/pp.107.100867] [PMID: 17556509]
[3]
Liang, P.H.; Wang, S.K.; Wong, C.H. Quantitative analysis of carbohydrate-protein interactions using glycan microarrays: determination of surface and solution dissociation constants. J. Am. Chem. Soc., 2007, 129(36), 11177-11184.
[http://dx.doi.org/10.1021/ja072931h] [PMID: 17705486]
[4]
Komath, S.S.; Kavitha, M.; Swamy, M.J. Beyond carbohydrate binding: new directions in plant lectin research. Org. Biomol. Chem., 2006, 4(6), 973-988.
[http://dx.doi.org/10.1039/b515446d] [PMID: 16525538]
[5]
Wong, J.H.; Ng, T.B.; Cheung, R.C.; Ye, X.J.; Wang, H.X.; Lam, S.K.; Lin, P.; Chan, Y.S.; Fang, E.F.; Ngai, P.H.; Xia, L.X.; Ye, X.Y.; Jiang, Y.; Liu, F. Proteins with antifungal properties and other medicinal applications from plants and mushrooms. Appl. Microbiol. Biotechnol., 2010, 87(4), 1221-1235.
[http://dx.doi.org/10.1007/s00253-010-2690-4] [PMID: 20532758]
[6]
Melnycova, N.M.; Mykhakiv, L.M.; Mamneko, P.M.; Kots, S.Y. The areas of application for plant lectins. Biopoly Cell, 2013, 29, 357-366.
[http://dx.doi.org/10.7124/bc.00082A]
[7]
Breitenbach Barroso Coelho, L.C.; Marcelino Dos Santos Silva, P.; Felix de Oliveira, W.; de Moura, M.C.; Viana Pontual, E.; Soares Gomes, F.; Guedes Paiva, P.M.; Napoleão, T.H.; Dos Santos Correia, M.T. Lectins as antimicrobial agents. J. Appl. Microbiol., 2018, 125(5), 1238-1252.
[http://dx.doi.org/10.1111/jam.14055] [PMID: 30053345]
[8]
Tucker-Burden, C.; Chappa, P.; Krishnamoorthy, M.; Gerwe, B.A.; Scharer, C.D.; Heimburg-Molinaro, J.; Harris, W.; Usta, S.N.; Eilertson, C.D.; Hadjipanayis, C.G.; Stice, S.L.; Brat, D.J.; Nash, R.J. Lectins identify glycan biomarkers on glioblastoma-derived cancer stem cells. Stem Cells Dev., 2012, 21(13), 2374-2386.
[http://dx.doi.org/10.1089/scd.2011.0369]
[9]
Wanchoo, A.; Lewis, M.W.; Keyhani, N.O. Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and haemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology, 2009, 155(Pt 9), 3121-3133.
[http://dx.doi.org/10.1099/mic.0.029157-0] [PMID: 19608611]
[10]
Coelho, L.C.; Silva, P.M.; Lima, V.L.; Pontual, E.V.; Paiva, P.M.; Napoleão, T.H.; Correia, M.T. Lectins, Interconnecting Proteins with Biotechnological/Pharmacological and Therapeutic Applications. Evid. Based Complement. Alternat. Med., 2017, 2017 1594074
[http://dx.doi.org/10.1155/2017/1594074] [PMID: 28367220]
[11]
Van Damme, E.J.; Peumans, W.J.; Barre, A.; Rougé, P. Plant lectins: a composite of several dictinct families of structurally and evolutionary related proteins with diverse biological roles. Crit. Rev. Plant Sci., 1998, 17, 575-692.
[http://dx.doi.org/10.1016/S0735-2689(98)00365-7]
[12]
Lam, S.K.; Ng, T.B. Lectins: production and practical applications. Appl. Microbiol. Biotechnol., 2010, 189(1), 45-55.
[13]
Dang, L.; Van Damme, E.J.M. Toxic proteins in plants. Phytochemistry, 2015, 117, 51-64.
[http://dx.doi.org/10.1016/j.phytochem.2015.05.020] [PMID: 26057229]
[14]
Yan, J.; Yuan, S.S.; Jiang, L.L.; Ye, X.J.; Ng, T.B.; Wu, Z.J. Plant antifungal proteins and their applications in agriculture. Appl. Microbiol. Biotechnol., 2015, 99(12), 4961-4981.
[http://dx.doi.org/10.1007/s00253-015-6654-6] [PMID: 25971197]
[15]
Hirota, K.; Yumoto, H.; Sapaar, B.; Matsuo, T.; Ichikawa, T.; Miyake, Y. Pathogenic factors in Candida biofilm-related infectious diseases. J. Appl. Microbiol., 2017, 122(2), 321-330.
[http://dx.doi.org/10.1111/jam.13330] [PMID: 27770500]
[16]
Perlin, D.S.; Rautemaa-Richardson, R.; Alastruey-Izquierdo, A. The global problem of antifungal resistance: prevalence, mechanisms, and management. Lancet Infect. Dis., 2017, 17(12), e383-e392.
[http://dx.doi.org/10.1016/S1473-3099(17)30316-X] [PMID: 28774698]
[17]
Tiraboschi, I.N.; Pozzi, N.C.; Farías, L.; García, S.; Fernández, N.B. [Epidemiology, species, antifungal resistance and outcome of candidemia in a university hospital in Buenos Aires, Argentina for 16 years] Rev. Chilena Infectol., 2017, 34(5), 431-440.
[http://dx.doi.org/10.4067/S0716-10182017000500431] [PMID: 29488584]
[18]
Hirano, R.; Sakamoto, Y.; Kitazawa, J.; Yamamoto, S.; Kayaba, H. Epidemiology, practice patterns, and prognostic factors for candidemia; and characteristics of fourteen patients with breakthrough Candida bloodstream infections: a single tertiary hospital experience in Japan. Infect. Drug Resist., 2018, 11, 821-833.
[http://dx.doi.org/10.2147/IDR.S156633] [PMID: 29910625]
[19]
Goemaere, B.; Becker, P.; Van Wijngaerden, E.; Maertens, J.; Spriet, I.; Hendrickx, M.; Lagrou, K. Increasing candidaemia incidence from 2004 to 2015 with a shift in epidemiology in patients preexposed to antifungals. Mycoses, 2018, 61(2), 127-133.
[http://dx.doi.org/10.1111/myc.12714] [PMID: 29024057]
[20]
Odds, F.C.; Brown, A.J.; Gow, N.A. Antifungal agents: mechanisms of action. Trends Microbiol., 2003, 11(6), 272-279.
[http://dx.doi.org/10.1016/S0966-842X(03)00117-3] [PMID: 12823944]
[21]
Pappas, P.G.; Kauffman, C.A.; Andes, D.; Benjamin, D.K., Jr; Calandra, T.F.; Edwards, J.E., Jr; Filler, S.G.; Fisher, J.F.; Kullberg, B.J.; Ostrosky-Zeichner, L.; Reboli, A.C.; Rex, J.H.; Walsh, T.J.; Sobel, J.D. Infectious Diseases Society of America. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin. Infect. Dis., 2009, 48(5), 503-535.
[http://dx.doi.org/10.1086/596757] [PMID: 19191635]
[22]
Spampinato, C.; Leonardi, D. Candida infections, causes, targets, and resistance mechanisms: traditional and alternative antifungal agents. BioMed Res. Int., 2013, 2013 204237
[http://dx.doi.org/10.1155/2013/204237] [PMID: 23878798]
[23]
Katragkou, A.; Alexander, E.L.; Eoh, H.; Raheem, S.K.; Roilides, E.; Walsh, T.J. Effects of fluconazole on the metabolomic profile of Candida albicans. J. Antimicrob. Chemother., 2016, 71(3), 635-640.
[http://dx.doi.org/10.1093/jac/dkv381] [PMID: 26668236]
[24]
Nett, J.E.; Andes, D.R. Antifungal agents: spectrum of activity, pharmacology, and clinical indications. Infect. Dis. Clin. North Am., 2016, 30(1), 51-83.
[http://dx.doi.org/10.1016/j.idc.2015.10.012] [PMID: 26739608]
[25]
Pemán, J.; Cantón, E.; Espinel-Ingroff, A. Antifungal drug resistance mechanisms. Expert Rev. Anti Infect. Ther., 2009, 7(4), 453-460.
[http://dx.doi.org/10.1586/eri.09.18] [PMID: 19400764]
[26]
Mesa-Arango, A.C.; Scorzoni, L.; Zaragoza, O. It only takes one to do many jobs: Amphotericin B as antifungal and immunomodulatory drug. Front. Microbiol., 2012, 3, 286.
[http://dx.doi.org/10.3389/fmicb.2012.00286] [PMID: 23024638]
[27]
Dadar, M.; Tiwari, R.; Karthik, K.; Chakraborty, S.; Shahali, Y.; Dhama, K. Candida albicans - Biology, molecular characterization, pathogenicity, and advances in diagnosis and control - An update. Microb. Pathog., 2018, 117, 128-138.
[http://dx.doi.org/10.1016/j.micpath.2018.02.028] [PMID: 29454824]
[28]
Kourkoumpetis, T.K.; Velmahos, G.C.; Ziakas, P.D.; Tampakakis, E.; Manolakaki, D.; Coleman, J.J.; Mylonakis, E. The effect of cumulative length of hospital stay on the antifungal resistance of Candida strains isolated from critically ill surgical patients. Mycopathologia, 2011, 171(2), 85-91.
[http://dx.doi.org/10.1007/s11046-010-9369-3] [PMID: 20927595]
[29]
Santana, G.; Albuquerque, L.; Simões, D.; Coelho, L.; Paiva, P.; Gusmão, N. Isolation of lectin from opuntia ficus-indica cladodes. Acta Hortic., 2009, 811(811), 281-286.
[http://dx.doi.org/10.17660/ActaHortic.2009.811.37]
[30]
Pinheiro, A.Q.; Melo, D.F.; Macedo, L.M.; Freire, M.G.; Rocha, M.F.; Sidrim, J.J.; Brilhante, R.S.; Teixeira, E.H.; Campello, C.C.; Pinheiro, D.C.; Lima, M.G. Antifungal and marker effects of Talisia esculenta lectin on Microsporum canis in vitro. J. Appl. Microbiol., 2009, 107(6), 2063-2069.
[http://dx.doi.org/10.1111/j.1365-2672.2009.04387.x] [PMID: 19558469]
[31]
Gomes, B.S.; Siqueira, A.B.; de Cássia Carvalho Maia, R.; Giampaoli, V.; Teixeira, E.H.; Arruda, F.V.; do Nascimento, K.S.; de Lima, A.N.; Souza-Motta, C.M.; Cavada, B.S.; Porto, A.L. Antifungal activity of lectins against yeast of vaginal secretion. Braz. J. Microbiol., 2012, 43(2), 770-778.
[http://dx.doi.org/10.1590/S1517-83822012000200042] [PMID: 24031889]
[32]
Klafke, G.B.; Borsuk, S.; Gonçales, R.A.; Arruda, F.V.; Carneiro, V.A.; Teixeira, E.H.; Coelho da Silva, A.L.; Cavada, B.S.; Dellagostin, O.A.; Pinto, L.S. Inhibition of initial adhesion of oral bacteria through a lectin from Bauhinia variegata L. var. variegata expressed in Escherichia coli. J. Appl. Microbiol., 2013, 115(5), 1222-1230.
[http://dx.doi.org/10.1111/jam.12318] [PMID: 23910219]
[33]
Vasconcelos, M.A.; Arruda, F.V.; Carneiro, V.A.; Silva, H.C.; Nascimento, K.S.; Sampaio, A.H.; Cavada, B.; Teixeira, E.H.; Henriques, M.; Pereira, M.O. Effect of algae and plant lectins on planktonic growth and biofilm formation in clinically relevant bacteria and yeasts. BioMed Res. Int., 2014, 2014 365272
[http://dx.doi.org/10.1155/2014/365272] [PMID: 24982871]
[34]
Gautam, A.K.; Gupta, N.; Narvekar, D.T.; Bhadkariya, R.; Bhagyawant, S.S. Characterization of chickpea (Cicer arietinum L.) lectin for biological activity. Physiol. Mol. Biol. Plants, 2018, 24(3), 389-397.
[http://dx.doi.org/10.1007/s12298-018-0508-5] [PMID: 29692547]
[35]
da Silva, J.D.F.; da Silva, S.P.; da Silva, P.M.; Vieira, A.M.; de Araújo, L.C.C.; de Albuquerque Lima, T.; de Oliveira, A.P.S.; do Nascimento Carvalho, L.V.; da Rocha Pitta, M.G.; de Melo Rêgo, M.J.B.; Pinheiro, I.O.; Zingali, R.B.; do Socorro de Mendonça Cavalcanti, M.; Napoleão, T.H.; Paiva, P.M.G. Portulaca elatior root contains a trehalose-binding lectin with antibacterial and antifungal activities. Int. J. Biol. Macromol., 2019, 126, 291-297.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.12.188] [PMID: 30583005]
[36]
Kumar, S.; Kapoor, V.; Gill, K.; Singh, K.; Xess, I.; Das, S.N.; Dey, S. Antifungal and antiproliferative protein from Cicer arietinum: a bioactive compound against emerging pathogens. BioMed Res. Int., 2014, 2014387203
[http://dx.doi.org/10.1155/2014/387203] [PMID: 24963482]
[37]
Procópio, T.F.; de Siqueira Patriota, L.L.; de Moura, M.C.; da Silva, P.M.; de Oliveira, A.P.; do Nascimento Carvalho, L.V.; de Albuquerque Lima, T.; Soares, T.; da Silva, T.D. Breitenbach Barroso Coelho. L.C.; da Rocha Pitta, M.G.; de Melo Rêgo, M.J.; Bressan Queiroz de Figueiredo, R.C.; Guedes Paiva, P.M.; Napoleão, T.H. CasuL: A new lectin isolated from Calliandra surinamensis leaf pinnulae with cytotoxicity tocancer cells, antimicrobial activity and antibiofim effect. Int. J. Biol. Macromol., 2017, 98, 419-429.
[PMID: 28174088]
[38]
Neto, J.X.S.; Pereira, M.L.; Oliveira, J.T.A.; Rocha-Bezerra, L.C.B.; Lopes, T.D.P.; Costa, H.P.S.; Sousa, D.O.B.; Rocha, B.A.M.; Grangeiro, T.B.; Freire, J.E.C.; Monteiro-Moreira, A.C.O.; Lobo, M.D.P.; Brilhante, R.S.N.; Vasconcelos, I.M. A Chitin-binding protein purified from Moringa oleifera seeds presents anticandidal activity by increasing cell membrane permeability and reactive oxygen species production. Front. Microbiol., 2017, 8, 980.
[http://dx.doi.org/10.3389/fmicb.2017.00980] [PMID: 28634471]
[39]
da Silva, P.M.; de Moura, M.C.; Gomes, F.S.; da Silva Trentin, D.; Silva de Oliveira, A.P.; de Mello, G.S.V.; da Rocha Pitta, M.G.; de Melo Rego, M.J.B.; Coelho, L.C.B.B.; Macedo, A.J.; de Figueiredo, R.C.B.Q.; Paiva, P.M.G.; Napoleão, T.H. PgTeL, the lectin found in Punica granatum juice, is an antifungal agent against Candida albicans and Candida krusei. Int. J. Biol. Macromol., 2018, 108, 391-400.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.12.039] [PMID: 29225175]
[40]
Ferreira, G.R.S.; Brito, J.S.; Procópio, T.F.; Santos, N.D.L.; de Lima, B.J.R.C.; Coelho, L.C.B.B.; Navarro, D.M.D.A.F.; Paiva, P.M.G.; Soares, T.; de Moura, M.C.; Napoleão, T.H. Antimicrobial potential of Alpinia purpurata lectin (ApuL): Growth inhibitory action, synergistic effects in combination with antibiotics, and antibiofilm activity. Microb. Pathog., 2018, 124, 152-162.
[http://dx.doi.org/10.1016/j.micpath.2018.08.027] [PMID: 30142463]
[41]
Regente, M.; Taveira, G.B.; Pinedo, M.; Elizalde, M.M.; Ticchi, A.J.; Diz, M.S.; Carvalho, A.O.; de la Canal, L.; Gomes, V.M. A sunflower lectin with antifungal properties and putative medical mycology applications. Curr. Microbiol., 2014, 69(1), 88-95.
[http://dx.doi.org/10.1007/s00284-014-0558-z] [PMID: 24623187]
[42]
Del Rio, M.; de la Canal, L.; Pinedo, M.; Mora-Montes, H.M.; Regente, M. Effects of the binding of a Helianthus annuus lectin to Candida albicans cell wall on biofilm development and adhesion to host cells. Phytomedicine, 2019, 58 152875
[http://dx.doi.org/10.1016/j.phymed.2019.152875] [PMID: 30884454]
[43]
Lenardon, M.D.; Munro, C.A.; Gow, N.A. Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol., 2010, 13(4), 416-423.
[http://dx.doi.org/10.1016/j.mib.2010.05.002] [PMID: 20561815]
[44]
Waris, G.; Ahsan, H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J. Carcinog., 2006, 5, 14.
[http://dx.doi.org/10.1186/1477-3163-5-14] [PMID: 16689993]
[45]
Kowaltowski, A.J.; de Souza-Pinto, N.C.; Castilho, R.F.; Vercesi, A.E. Mitochondria and reactive oxygen species. Free Radic. Biol. Med., 2009, 47(4), 333-343.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.05.004] [PMID: 19427899]
[46]
Scandalios, J.G. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz. J. Med. Biol. Res., 2005, 38(7), 995-1014.
[http://dx.doi.org/10.1590/S0100-879X2005000700003] [PMID: 16007271]
[47]
Scorzoni, L.; de Paula, E. Silva, A.C.; Marcos, C.M.; Assato, P.A.; de Melo, W.C.; de Oliveira, H.C.; Costa-Orlandi, C.B.; Mendes-Giannini, M.J.; Fusco-Almeida, A.M. Antifungal therapy: New advances in the understanding and treatment of mycosis. Front. Microbiol., 2017, 8, 36.
[http://dx.doi.org/10.3389/fmicb.2017.00036] [PMID: 28167935]
[48]
Romo, J.A.; Pierce, C.G.; Chaturvedi, A.K.; Lazzell, A.L.; McHardy, S.F.; Saville, S.P.; Lopez-Ribot, J.L. Development of anti- virulence approaches for candidiasis via a novel series of small-molecule inhibitors of Candida albicans filamentation. MBio, 2017, 8(6), 1991-17.
[49]
Sharma, J.; Rosiana, S.; Razzaq, I.; Shapiro, R.S. Linking cellular morphogenesis with antifungal treatment and susceptibility in Candida pathogens. J. Fungi (Basel), 2019, 5(1), 17.
[http://dx.doi.org/10.3390/jof5010017] [PMID: 30795580]
[50]
Zhu, W.; Filler, S.G. Interactions of Candida albicans with epithelial cells. Cell. Microbiol., 2010, 12(3), 273-282.
[http://dx.doi.org/10.1111/j.1462-5822.2009.01412.x] [PMID: 19919567]
[51]
Hall, R.A.; Gow, N.A. Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol. Microbiol., 2013, 90(6), 1147-1161.
[http://dx.doi.org/10.1111/mmi.12426] [PMID: 24125554]
[52]
Saville, S.P.; Lazzell, A.L.; Bryant, A.P.; Fretzen, A.; Monreal, A.; Solberg, E.O. Inhibition of filamentation can be used to treat disseminated candidiasis. Antimicrob. Agents Chemother., 2006, 50(10), 3312-3316.
[http://dx.doi.org/10.1128/AAC.00628-06] [PMID: 17005810]
[53]
Kadosh, D.; Lopez-Ribot, J.L. Candida albicans: adapting to succeed. Cell Host Microbe, 2013, 14(5), 483-485.
[http://dx.doi.org/10.1016/j.chom.2013.10.016] [PMID: 24237692]
[54]
Cavalheiro, M.; Teixeira, M.C. Candida biofilms: threats, challenges, and promising strategies. Front. Med. (Lausanne), 2018, 5, 28.
[http://dx.doi.org/10.3389/fmed.2018.00028] [PMID: 29487851]
[55]
Olsen, I. Biofilm-specific antibiotic tolerance and resistance. Eur. J. Clin. Microbiol. Infect. Dis., 2015, 34(5), 877-886.
[http://dx.doi.org/10.1007/s10096-015-2323-z] [PMID: 25630538]
[56]
Goswami, R.; Pohare, S.; Raut, J.; Karuppayil, S. Cell surface hydrophobicity as a virulence factor in Candida albicans. Biosci. Biotechnol. Res. Asia, 2017, 14, 1503-1511.
[http://dx.doi.org/10.13005/bbra/2598]
[57]
Rabin, N.; Zheng, Y.; Opoku-Temeng, C.; Du, Y.; Bonsu, E.; Sintim, H.O. Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Med. Chem., 2015, 7(4), 493-512.
[http://dx.doi.org/10.4155/fmc.15.6] [PMID: 25875875]
[58]
Padder, S.A.; Prasad, R.; Shah, A.H. Quorum sensing: A less known mode of communication among fungi. Microbiol. Res., 2018, 210, 51-58.
[http://dx.doi.org/10.1016/j.micres.2018.03.007] [PMID: 29625658]
[59]
Cottier, F.; Mühlschlegel, F.A. Communication in fungi. Int. J. Microbiol., 2012, 2012 351832
[http://dx.doi.org/10.1155/2012/351832] [PMID: 21961006]
[60]
Albuquerque, L.P.; Santana, G.M.; Napoleão, T.H.; Coelho, L.C.; Silva, M.V.; Paiva, P.M. Antifungal activity of Microgramma vacciniifolia rhizome lectin on genetically distinct Fusarium oxysporum f. sp. lycopersici races. Appl. Biochem. Biotechnol., 2014, 172(2), 1098-1105.
[http://dx.doi.org/10.1007/s12010-013-0600-9] [PMID: 24142386]
[61]
Polke, M.; Leonhardt, I.; Kurzai, O.; Jacobsen, I.D. Farnesol signalling in Candida albicans - more than just communication. Crit. Rev. Microbiol., 2018, 44(2), 230-243.
[http://dx.doi.org/10.1080/1040841X.2017.1337711] [PMID: 28609183]
[62]
Hornby, J.M.; Nickerson, K.W. Enhanced production of farnesol by Candida albicans treated with four azoles. Antimicrob. Agents Chemother., 2004, 48(6), 2305-2307.
[http://dx.doi.org/10.1128/AAC.48.6.2305-2307.2004] [PMID: 15155241]
[63]
Mosel, D.D.; Dumitru, R.; Hornby, J.M.; Atkin, A.L.; Nickerson, K.W. Farnesol concentrations required to block germ tube formation in Candida albicans in the presence and absence of serum. Appl. Environ. Microbiol., 2005, 71(8), 4938-4940.
[http://dx.doi.org/10.1128/AEM.71.8.4938-4940.2005] [PMID: 16085901]
[64]
Navarathna, D.H.; Hornby, J.M.; Hoerrmann, N.; Parkhurst, A.M.; Duhamel, G.E.; Nickerson, K.W. Enhanced pathogenicity of Candida albicans pre-treated with subinhibitory concentrations of fluconazole in a mouse model of disseminated candidiasis. J. Antimicrob. Chemother., 2005, 56(6), 1156-1159.
[http://dx.doi.org/10.1093/jac/dki383] [PMID: 16239285]
[65]
Alem, M.A.; Oteef, M.D.; Flowers, T.H.; Douglas, L.J. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot. Cell, 2006, 5(10), 1770-1779.
[http://dx.doi.org/10.1128/EC.00219-06] [PMID: 16980403]
[66]
Cottier, F.; Mühlschlegel, F.A. Communication in fungi. Int. J. Microbiol., 2012. 2012351832
[http://dx.doi.org/10.1155/2012/351832] [PMID: 21961006]
[67]
Fischer, G.J.; Keller, N.P. Production of cross-kingdom oxylipins by pathogenic fungi: An update on their role in development and pathogenicity. J. Microbiol., 2016, 54(3), 254-264.
[http://dx.doi.org/10.1007/s12275-016-5620-z] [PMID: 26920885]
[68]
Nigam, S.; Ciccoli, R.; Ivanov, I.; Sczepanski, M.; Deva, R. On mechanism of quorum sensing in Candida albicans by 3(R)-hydroxy-tetradecaenoic acid. Curr. Microbiol., 2011, 62(1), 55-63.
[http://dx.doi.org/10.1007/s00284-010-9666-6] [PMID: 20509029]
[69]
Ghosh, S.; Navarathna, D.H.; Roberts, D.D.; Cooper, J.T.; Atkin, A.L.; Petro, T.M.; Nickerson, K.W. Arginine-induced germ tube formation in Candida albicans is essential for escape from murine macrophage line RAW 264.7. Infect. Immun., 2009, 77(4), 1596-1605.
[http://dx.doi.org/10.1128/IAI.01452-08] [PMID: 19188358]
[70]
Hall, R.A.; De Sordi, L.; Maccallum, D.M.; Topal, H.; Eaton, R.; Bloor, J.W.; Robinson, G.K.; Levin, L.R.; Buck, J.; Wang, Y.; Gow, N.A.; Steegborn, C.; Mühlschlegel, F.A. CO(2) acts as a signalling molecule in populations of the fungal pathogen Candida albicans. PLoS Pathog., 2010, 6(11) e1001193
[http://dx.doi.org/10.1371/journal.ppat.1001193] [PMID: 21124988]
[71]
Huang, G.; Srikantha, T.; Sahni, N.; Yi, S.; Soll, D.R. CO(2) regulates white-to-opaque switching in Candida albicans. Curr. Biol., 2009, 19(4), 330-334.
[http://dx.doi.org/10.1016/j.cub.2009.01.018] [PMID: 19200725]
[72]
Roberts, D.D.; Goldstein, I.J. Adenine binding sites of the lectin from lima beans (Phaseolus lunatus). J. Biol. Chem., 1982, 257, 11274.
[PMID: 7118884]
[73]
Roberts, D.D.; Goldstein, I.J. Binding of hydrophobic ligands to plant lectins: titration with arylaminonaphthalenesulfonates. Arch. Biochem. Biophys., 1983, 224(2), 479-484.
[http://dx.doi.org/10.1016/0003-9861(83)90235-7] [PMID: 6870273]
[74]
Yang, D.C.; Gall, W.E.; Edelman, G.M. Rotational correlation time of concanavalin A after interaction with a fluorescent probe. J. Biol. Chem., 1974, 249(21), 7018-7023.
[PMID: 4424709]
[75]
Gegg, C.V.; Roberts, D.D.; Segel, I.H.; Etzler, M.E. Characterization of the adenine binding sites of two Dolichos biflorus lectins. Biochemistry, 1992, 31(30), 6938-6942.
[http://dx.doi.org/10.1021/bi00145a011] [PMID: 1637827]
[76]
Bogoeva, V.P.; Radeva, M.A.; Atanasova, L.Y.; Stoitsova, S.R.; Boteva, R.N. Fluorescence analysis of hormone binding activities of wheat germ agglutinin. Biochim. Biophys. Acta, 2004, 1698(2), 213-218.
[http://dx.doi.org/10.1016/j.bbapap.2003.12.002] [PMID: 15134654]
[77]
Maliarik, M.; Plessas, N.R.; Goldstein, I.J.; Musci, G.; Berliner, L.J. ESR and fluorescence studies on the adenine binding site of lectins using a spin-labeled analogue. Biochemistry, 1989, 28(2), 912-917.
[http://dx.doi.org/10.1021/bi00428a076] [PMID: 2540812]
[78]
Bhanu, K.; Komath, S.S.; Maiya, B.G.; Swamy, M.J. Interaction of porphyrins with concanavalin a and pea lectin Swamy. Curr. Sci., 1997, 73(7), 598-602.
[79]
Komath, S.S.; Bhanu, K.; Maiya, B.G.; Swamy, M.J. Binding of porphyrins by the tumor-specific lectin, jacalin.[Jack fruit (Artocarpus integrifolia) agglutinin] Biosci. Rep., 2000, 20(4), 265-276.
[http://dx.doi.org/10.1023/A:1026440907227] [PMID: 11092249]
[80]
Komath, S.S.; Kenoth, R.; Giribabu, L.; Maiya, B.G.; Swamy, M.J. Fluorescence and absorption spectroscopic studies on the interaction of porphyrins with snake gourd (Trichosanthes anguina) seed lectin. J. Photochem. Photobiol. B, 2000, 55(1), 49-55.
[http://dx.doi.org/10.1016/S1011-1344(00)00026-9] [PMID: 10877067]
[81]
Kenoth, R.; Raghunath Reddy, D.; Maiya, B.G.; Swamy, M.J. Thermodynamic and kinetic analysis of porphyrin binding to Trichosanthes cucumerina seed lectin. Eur. J. Biochem., 2001, 268(21), 5541-5549.
[http://dx.doi.org/10.1046/j.1432-1033.2001.02491.x] [PMID: 11683877]
[82]
Sultan, N.A.; Maiya, B.G.; Swamy, M.J. Thermodynamic analysis of porphyrin binding to Momordica charantia (bitter gourd) lectin. Eur. J. Biochem., 2004, 271(15), 3274-3282.
[http://dx.doi.org/10.1111/j.1432-1033.2004.04261.x] [PMID: 15265047]