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The Galactose-Binding Lectin Isolated from Vatairea macrocarpa Seeds Enhances the Effect of Antibiotics Against Staphylococcus aureus–Resistant Strain

  • Valdenice F. Santos
  • Maria S. Costa
  • Fábia F. Campina
  • Renato R. Rodrigues
  • Ana L. E. Santos
  • Felipe M. Pereira
  • Karla L. R. Batista
  • Rafael C. Silva
  • Raquel O. Pereira
  • Bruno A. M. Rocha
  • Henrique D. M. Coutinho
  • Claudener S. TeixeiraEmail author
Article

Abstract

The use of natural products together with standard antimicrobial drugs has recently received more attention as a strategy to combat infectious diseases caused by multidrug-resistant (MDR) microorganisms. This study aimed to evaluate the capacity of a galactose-binding lectin from Vatairea macrocarpa seeds (VML) to modulate antibiotic activity against standard and MDR Staphylococcus aureus and Escherichia coli bacterial strains. The minimum inhibitory concentration (MIC) obtained for VML against all strains was not clinically relevant (MIC ≥ 1024 μg/mL). However, when VML was combined with the antibacterial drugs gentamicin, norfloxacin and penicillin, a significant increase in antibiotic activity was observed against S. aureus, whereas the combination of VML and norfloxacin presented decreased and, hence, antagonistic antibiotic activity against E. coli. By its inhibition of hemagglutinating activity, gentamicin (MIC = 50 mM) revealed its interaction with the carbohydrate-binding site (CBS) of VML. Using molecular docking, it was found that gentamicin interacts with residues that constitute the CBS of VML with a score of − 120.79 MDS. It is this interaction between the antibiotic and the lectin’s CBS that may be responsible for the enhanced activity of gentamicin in S. aureus. Thus, our results suggest that the VML can be an effective modulating agent against S. aureus. This is the first study to report the effect of lectins as modulators of bacterial sensitivity, and as such, the outcome of this study could lay the groundwork for future research involving the use of lectins and conventional antibiotics against such infectious diseases such as community-acquired methicillin-resistant S. aureus (MRSA).

Keywords

Antimicrobial Gentamicin Protein Agglutinin 

Notes

Acknowledgements

We thank David Martin for English language editing of the manuscript.

Funding Information

This study was partly funded by the Fundação de Amparo à Pesquisa e Desenvolvimento Científico do Maranhão (FAPEMA), Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Finance Code 001, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), referring to the Research Productivity Grants of Bruno Anderson Matias da Rocha and Henrique Douglas Melo Coutinho.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Perl TM (1999) The threat of vancomycin resistance. Am J Med 106:26S–37SCrossRefGoogle Scholar
  2. 2.
    Schito GC (2006) The importance of the development of antibiotic resistance in Staphylococcus aureus. Clin Microbiol Infect 12:3–8CrossRefGoogle Scholar
  3. 3.
    Munita JM, Bayer AS, Arias CA (2015) Evolving resistance among Gram-positive pathogens. Clin Infect Dis 15:48–57CrossRefGoogle Scholar
  4. 4.
    Garcia CP (2003) Resistencia bacteriana en Chile. Rev Chil Infectol 11–23Google Scholar
  5. 5.
    Leite TR, Silva MAPD, Santos ACBD, Coutinho HDM, Duarte AE, Costa JGMD (2017) Antimicrobial, modulatory and chemical analysis of the oil of Croton limae. Pharm Biol 55:2015–2019CrossRefGoogle Scholar
  6. 6.
    Sales DL, Morais-Braga MFB, Santos ATLD, Machado AJT, Araujo-Filho JA, Dias DQ, Cunha FABD, Saraiva RA, Menezes IRA, Coutinho HDM, Costa JGM, Ferreira FS, Alves RRDN, Almeida WO (2017) Antibacterial, modulatory activity of antibiotics and toxicity from Rhinella jimi (Stevaux, 2002) (Anura: Bufonidae) glandular secretions. Biomed Pharmacother 92:554–561CrossRefGoogle Scholar
  7. 7.
    Carneiro RF, Lima-Júnior PHP, Chaves RP, Pereira R, Pereira AL, Vasconcelos MA, Pinheiro U, Teixeira EH, Nagano CS, Sampaio AH (2017) Isolation, biochemical characterization and antibiofilm effect of a lectin from the marine sponge Aplysina lactuca. Int J Biol Macromol 99:213–222CrossRefGoogle Scholar
  8. 8.
    Teixeira EH, Arruda FVS, Nascimento KS, Carneiro VA, Nagano CS, Silva BR, Sampaio AH, Cavada BS (2012) Biological. Applications of plants and algae lectins an overview. In: Chang CF (ed) Carbohydrates - comprehensive studies on glycobiology and glycotechnology. Intech Rijeka, pp 553–558Google Scholar
  9. 9.
    Loh SH, Park JY, Cho EH, Nah SY, Kang YS (2017) Animal lectins: potential receptors for ginseng polysaccharides. J Ginseng Res 41:1–9CrossRefGoogle Scholar
  10. 10.
    Teixeira CS, Assreuy AMS, Osterne VJS, Amorim RMF, Brizeno LAC, Debray H, Nagano CS, Delatorre P, Sampaio AH, Rocha BAM, Cavada BS (2014) Mannose-specific legume lectin from the seeds of Dolichos lablab (FRIL) stimulates inflammatory and hypernociceptive processes in mice. Process Biochem 49:529–534CrossRefGoogle Scholar
  11. 11.
    Sharon N, Lis H (2002) How proteins bind carbohydrates: lessons from legume lectins. J Agric Food Chem 23:6586–6591CrossRefGoogle Scholar
  12. 12.
    Lannoo N, van Damme EJ (2014) Lectin domains at the frontiers of plant defense. Front Plant Sci 5:1–16Google Scholar
  13. 13.
    Dias RO, Machado LS, Migliolo L, Franco OL (2015) Insights into animal and plant lectins with antimicrobial activities. Molecules 5:519–541CrossRefGoogle Scholar
  14. 14.
    Paiva PMG, Gomes FS, Napoleao TH, Sá RA, Correia MTS, Coelho LCB (2010) Antimicrobial activity of secondary metabolites and lectins from plants. In: Vilas AM (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. pp 396–406Google Scholar
  15. 15.
    Costa FO, Lima DCR, Silva ALG (2014) Biologia reprodutiva de Vatairea macrocarpa (Benth.) Ducke (Fabaceae –Faboideae) em uma área de Cerrado no município de Chapadinha, MA, Brasil. Heringeriana 8:1–19Google Scholar
  16. 16.
    Alencar NM, Assreuy AM, Havt A, Benevides RG, de Moura TR, de Sousa RB, Ribeiro RA, Cunha FQ, Cavada BS (2007) Vatairea macrocarpa (Leguminosae) lectin activates cultured macrophages to release chemotactic mediators. Naunyn Schmiedeberg’s Arch Pharmacol 374:275–282CrossRefGoogle Scholar
  17. 17.
    Martins AM, Monteiro AM, Havt A, Barbosa PS, Soares TF, Evangelista JS, de Menezes DB, Fonteles MC, Teixeira EH, Pinto VP, Nascimento KS, Alencar NM, Cavada BS, Monteiro HS (2005) Renal effects induced by the lectin from Vatairea macrocarpa seeds. J Pharm Pharmacol 57:1329–1333CrossRefGoogle Scholar
  18. 18.
    Alencar NM, Assreuy AM, Criddle DN, Souza EP, Soares PM, Havt A, Aragão KS, Bezerra DP, Ribeiro RA, Cavada BS (2004) Vatairea macrocarpa lectin induces paw edema with leukocyte infiltration. Protein Pept Lett 11:195–200CrossRefGoogle Scholar
  19. 19.
    Martínez CR, Chanway CP, Albertini AV, Figueiredo MV, Sampaio AH, Castellon RR, Cavada BS, Lima-Filho JL (2004) The interaction of Vatairea macrocarca and Rhizobium tropici: net H+ efflux stimulus and alteration of extracellular Na+ concentration. FEMS Microbiol Lett 238:17–22CrossRefGoogle Scholar
  20. 20.
    Sousa BL, Silva-Filho JC, Kumar P, Graewert MA, Pereira RI, Cunha RMS, Nascimento KS, Bezerra GA, Delatorre P, Djinovic-Carugo K, Nagano CS, Gruber K, Cavada BS (2016) Structural characterization of a Vatairea macrocarpa lectin in complex with a tumor-associated antigen: a new tool for cancer research. Int J Biochem Cell Biol 72:27–39CrossRefGoogle Scholar
  21. 21.
    Calvete JJ, Santos CF, Mann K, Grangeiro TB, Nimtz M, Urbanke C, Cavada BS (1998) Amino acid sequence, glycan structure, and proteolytic processing of the lectin of Vatairea macrocarpa seeds. FEBS Lett 27:286–292CrossRefGoogle Scholar
  22. 22.
    Laemli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  23. 23.
    Moreira RA, Perrone JC (1977) Purification and partial characterization of a lectin from Phaseolus vulgaris. Plant Physiol 59:783–787CrossRefGoogle Scholar
  24. 24.
    Sousa BL, Silva Filho JC, Kumar P, Pereira RI, Łyskowski A, Rocha BAM, Delatorre P, Bezerra GA, Nagano CS, Gruber K, Cavada BS (2015) High-resolution structure of a new Tn antigen-binding lectin from Vatairea macrocarpa and a comparative analysis of Tn-binding legume lectins. Int J Biochem Cell Biol 59:103–110CrossRefGoogle Scholar
  25. 25.
    Schüttelkopf AW, Van Aalten DMF (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr Sect D 60:1355–1363CrossRefGoogle Scholar
  26. 26.
    Thomsen R, Christensen MH (2006) MolDock: a new technique for highaccuracy molecular docking. J Med Chem 49:3315–3321CrossRefGoogle Scholar
  27. 27.
    Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for crystallography. Acta Crystallogr D Biol Crystallogr 50:760–763CrossRefGoogle Scholar
  28. 28.
    Delano WL (2002) The Pymol Molecular Graphics System. DeLano Scientific, San CarlosGoogle Scholar
  29. 29.
    CLSI–Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Twenty second informational supplement (2012) 9th ed. Document M100–S22Google Scholar
  30. 30.
    Coutinho HDM, Costa JGM, Lima EO, Falcão-Silva VS, Júnior JPS (2009) Herbal therapy associated with antibiotic therapy: potentiation of the antibiotic activity against methicillin-resistant Staphylococcus aureus by Turnera ulmifolia L. BMC Complement Altern Med 8:9–13Google Scholar
  31. 31.
    Carmona-Ribeiro AM, Carrasco LDM (2014) Novel formulations for antimicrobial peptides. Int J Mol Sci 15:18040–18083CrossRefGoogle Scholar
  32. 32.
    Marques DN, Almeida AS, Sousa ARO, Pereira R, Andrade AL, Chaves RP, Carneiro RF, Vasconcelos MA, Nascimento-Neto LGD, Pinheiro U, Videira PA, Teixeira EH, Nagano CS, Sampaio AH (2018) Antibacterial activity of a new lectin isolated from the marine sponge Chondrilla caribensis. Int J Biol Macromol 1:1292–1301CrossRefGoogle Scholar
  33. 33.
    Pereira NLF, Aquino PEA, Júnior JGAS, Cristo JS, Vieira-Filho MA, Moura FF, Ferreira NMN, Silva MKN, Nascimento EM, Correia FMA, Cunha FAB, Boligon AA, Coutinho HDM, Ribeiro-Filho J, Matias EFF, Guedes MIF (2017) Antibacterial activity and antibiotic modulating potential of the essential oil obtained from Eugenia jambolana in association with led lights. J Photochem Photobiol B 174:144–149CrossRefGoogle Scholar
  34. 34.
    Moura RM, Queiroz AFS, Fook JMSLL, Dias ASF, Monteiro NKV, Ribeiro JKC, Moura GE, Macedo LL, Santos EA, Sales MP (2006) CvL, a lectin from the marine sponge Cliona varians: isolation, characterization and its effects on pathogenic bacteria and Leishmania promastigotes. Comp Biochem Physiol A 145:517–523CrossRefGoogle Scholar
  35. 35.
    Schroder HC, Ushijima H, Krasko A, Gamulin V, Thakur NL, DiehlSeifert B, Muller IM, Muller WEG (2003) Emergence and disappearance of an immune molecule, an antimicrobial lectin, in basal metazoa: a tachylectin-related protein in the sponge Suberites domuncula. J Biol Chem 278:32810–32817CrossRefGoogle Scholar
  36. 36.
    Miki T, Holst O, Hardt W (2012) The bactericidal activity of the C-type lectin regiiiβ against gram-negative bacteria involves binding to lipid A. J Biol Chem 287:34844–34855CrossRefGoogle Scholar
  37. 37.
    Purish LM, Asaulenko LG, Abdulina DR, Voychuk SI, Iutynskaya GA (2013) Lectin binding analysis of the biofilm exopolymeric matrix carbohydrate composition of corrosion aggressive bacteria. Appl Biochem Microbiol 49:458–463CrossRefGoogle Scholar
  38. 38.
    Shin WS, Park D, Kim SC, Park HY (2000) Two carbohydrate recognition domains of Hyphantria cunea lectin bind to bacterial lipopolysaccharides through O-specific chain. FEBS Lett 467:70–74CrossRefGoogle Scholar
  39. 39.
    Vasconcelos MA, Arruda FV, Carneiro VA, Silva HC, Nascimento KS, Sampaio AH, Cavada BS, Teixeira EH, Henriques M, Pereira MO (2014) Effect of algae and plant lectins on planktonic growth and biofilm formation in clinically relevant bacteria and yeasts. Biomed Res Int 365272Google Scholar
  40. 40.
    Howden BP, Stinear TP, Allen DL, Johnson PDR, Ward PB, Davies JK (2008) Genomic analysis reveals a point mutation in the two-component sensor gene graS that leads to intermediate vancomycin resistance in clinical Staphylococcus aureus. Antimicrob Agents Chemother 52:3755–3762CrossRefGoogle Scholar
  41. 41.
    Chiu HC, Lee SL, Kapuriya N, Wang D, Chen YR, Yu SL, Kulp SK, Teng LJ, Chen CS (2012) Development of novel antibacterial agents against methicillin-resistant Staphylococcus aureus. Bioorg Med Chem 1:4653–4660CrossRefGoogle Scholar
  42. 42.
    Mingeot-Leclercq MP, Glupczynski Y, Tulkens PM (1999) Aminoglycosides: activity and resistance. Antimicrob Agents Chemother 43:727–737CrossRefGoogle Scholar
  43. 43.
    Horibe T, Matsui H, Tanaka M, Nagai H, Yamaguchi Y, Kato K, Kikuchi M (2004) Gentamicin binds to the lectin site of calreticulin and inhibits its chaperone activity. Biochem Biophys Res Commun 8:281–287CrossRefGoogle Scholar
  44. 44.
    Lum R, Ahmad S, Hong SJ, Chapman DC, Kozlov G, Williams DB (2016) Contributions of the lectin and polypeptide binding sites of calreticulin to its chaperone functions in vitro and in cells. J Biol Chem 9:19631–19641CrossRefGoogle Scholar
  45. 45.
    Danussi C, Coslovi A, Campa C, Mucignat MT, Spessotto P, Uggeri F, Paoletti S, Colombatti A (2009) A newly generated functional antibody identifies Tn antigen as a novel determinant in the cancer cell–lymphatic endothelium interaction. Glycobiology 19:1056–1067CrossRefGoogle Scholar
  46. 46.
    Delatorre P, Silva-Filho JC, Rocha BAM, Santi-Gadelha T, Nóbrega RB, Gadelha CA, Nascimento KS, Nagano CS, Sampaio AH, Cavada BS (2013) Interactions between indole-3-acetic acid (IAA) with a lectin from Canavalia maritima seeds reveal a new function for lectins in plant physiology. Biochimie 95:1697–1703CrossRefGoogle Scholar
  47. 47.
    Shetty KN, Latha VL, Rao RN, Nadimpalli SK, Suguna K (2013) Affinity of a galactose-specific legume lectin from Dolichos lablab to adenine revealed by X-ray cystallography. IUBMB Life 65:633–644CrossRefGoogle Scholar
  48. 48.
    Rocha BAM, Teixeira CS, Silva-Filho JC, Nóbrega RB, Alencar DB, Nascimento KS, Freire VN, Gottfried CJ, Nagano CS, Sampaio AH, Saker-Sampaio S, Cavada BS, Delatorre P (2015) Structural basis of ConM binding with resveratrol, an anti-inflammatory and antioxidant polyphenol. Int J Biol Macromol 72:1136–1142CrossRefGoogle Scholar
  49. 49.
    Pastor RF, Restani P, Di Lorenzo C, Orgiu F, Teissedre PL, Stockley C, Ruf JC, Quini CI, Garcìa Tejedor N, Gargantini R, Aruani C, Prieto S, Murgo M, Videla R, Penissi A, Iermoli RH (2017) Resveratrol, human health and winemaking perspectives. Crit Rev Food Sci Nutr 5:1–19CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Valdenice F. Santos
    • 1
  • Maria S. Costa
    • 2
  • Fábia F. Campina
    • 2
  • Renato R. Rodrigues
    • 1
  • Ana L. E. Santos
    • 1
  • Felipe M. Pereira
    • 1
  • Karla L. R. Batista
    • 1
  • Rafael C. Silva
    • 1
  • Raquel O. Pereira
    • 1
  • Bruno A. M. Rocha
    • 3
  • Henrique D. M. Coutinho
    • 2
  • Claudener S. Teixeira
    • 1
    Email author
  1. 1.Centro de Ciências Agrárias e AmbientaisUniversidade Federal do MaranhãoChapadinhaBrazil
  2. 2.Departamento de Química BiológicaUniversidade Regional do CaririCratoBrazil
  3. 3.Departamento de Bioquímica e Biologia MolecularUniversidade Federal do CearáFortalezaBrazil

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