2,016
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Prospecting in silico antibacterial activity of a peptide from trypsin inhibitor isolated from tamarind seed

, , , , , , , , , ORCID Icon, , & ORCID Icon show all
Pages 67-83 | Received 19 Sep 2022, Accepted 06 Oct 2022, Published online: 28 Oct 2022

References

  • WHO. Infectious diseases. Geneva, Switzerland: WHO; 2020.
  • WHO. The top 10 causes of death. WHO’s global health estimates. Available from: https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death.
  • WHO. World health statistics; 2022. Available from: http://apps.who.int/bookorders.
  • BRAZIL. Outbreaks of food and water transmitted diseases in Brazil; 2022. Available from: https://www.gov.br/saude/pt-br/assuntos/saude-de-a-a-z/d/dtha/arquivos/copy_of_apresentacao-surtos-dtha-2022.pdf.
  • CDC. Centers for disease control and prevention. Causes of food poisoning. Centers for Disease Control and Prevention; 2020. Available from: https://www.cdc.gov/foodsafety/foodborne-germs.html.
  • Michael CA, Dale DH, Labbate M. The antimicrobial resistance crisis: causes, consequences, and management. Front Public Health. 2014;2:145.
  • Nascimento MAS, Oliveira VHS, Felipe AJAC, Piuvezam G, Souza TP, Florentino KSDS, Araújo AHM. Antibacterial action mechanisms and mode of trypsin inhibitors: a systematic review. J Enzyme Inhib Med Chem. 2022;37(1):749–759.
  • WHO. Regulatory situation of herbal medicines: a worldwide review. Geneva, Switzerland: WHO; 1998. p. 45.
  • Liu Q, Meng X, Li Y, Zhao CN, Tang GY, Li HB. Antibacterial and antifungal activities of spices. Int J Mol Sci. 2017;18(6):1283.
  • Mima J, Hayashida M, Fujii T, Narita Y, Hayashi R, Ueda M, Hata Y. Structure of the carboxypeptidase Y inhibitor IC in complex with the cognate proteinase reveals a novel mode of the proteinase–protein inhibitor interaction. J Mol Biol. 2005;346(5):1323–1334.
  • Reyes-Díaz A, Del-Toro-Sánchez CL, Rodríguez-Figueroa JC, Valdéz-Hurtado S, Wong-Corral FJ, Borboa-Flores J, González-Osuna MF, Perez-Perez LM, González-Vega RI. Legume proteins as a promising source of anti-inflammatory peptides. Curr Protein Pept Sci. 2019;20(12):1204–1217.
  • Matos FM, Castro RJS. Insetos comestíveis como potenciais fontes de proteínas para obtenção de peptídeos bioativos. Rev Bras Tecnol Alimentos. 2021;24:1–13.
  • Chaves Filho GP, de Sousa AFG, Câmara RBG, Rocha HAO, de Medeiros SRB, Moreira SMG. Genotoxicity and osteogenic potential of sulfated polysaccharides from Caulerpa prolifera seaweed. Int J Biol Macromol. 2018;114(114):565–571.
  • Carvalho F, Lima V, Costa I, Medeiros A, Serquiz A, Lima M, Serquiz R, Maciel B, Uchôa A, Santos E, et al. A trypsin inhibitor from tamarind reduces food intake and improves inflammatory status in rats with metabolic syndrome regardless of weight loss. Nutrients. 2016;8(10):544–11.
  • Medeiros A. F d, Costa I. d S, Carvalho F. M C d, Kiyota S, Souza B. B P d, Sifuentes DN, Serquiz RP, Maciel BLL, Uchôa AF, Santos EAD, et al. Biochemical characterization of a Kunitz-type inhibitor from Tamarindus indica L. seeds and its efficacy in reducing plasma leptin in an experimental model of obesity. J Enzyme Inhib Med Chem. 2018;33(1):334–348.
  • Costa I, Medeiros A, Carvalho F, Lima V, Serquiz R, Serquiz A, Silbiger V, Bortolin R, Maciel B, Santos E, et al. Satietogenic protein from tamarind seeds decreases food intake, leptin plasma and CCK-1r gene expression in obese wistar rats. Obes Facts. 2018;11(6):440–453.
  • Carvalho FMC, Lima VCO, Costa IS, Luz ABS, Ladd FVL, Serquiz AC, Bortolin RH, Silbiger VN, Maciel BLL, Santos EA, et al. Anti-TNF-α agent tamarind Kunitz trypsin inhibitor improves lipid profile of Wistar rats presenting dyslipidemia and diet-induced obesity regardless of PPAR-γ induction. Nutrients. 2019;11(3):512.
  • Lima VCO, Luz ABS, Amarante M. d S M, Lima MCJS, Carvalho FMC, Figueredo JBS, Santos PPA, Camillo CS, Ladd FVL, Maciel BLL, et al. Tamarind multifunctional protein: safety and anti-inflammatory potential in intestinal mucosa and adipose tissue in a preclinical model of diet-induced obesity. Obes Facts. 2021;14(4):357–369.
  • de Medeiros AF, de Souza BBP, Coutinho LP, Murad AM, Dos Santos PIM, Monteiro N. d K V, Santos EAD, Maciel BLL, de Araújo Morais AH. Structural insights and molecular dynamics into the inhibitory mechanism of a Kunitz-type trypsin inhibitor from Tamarindus indica L. J Enzyme Inhib Med Chem. 2021;36(1):480–490.
  • Bao W, Chen Y, Wang D. Prediction of protein structure classes with flexible neural tree. Biomed Mater Eng. 2014;24(6):3797–3806.
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–685.
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.
  • Mosmann T. Rapid calorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63.
  • Costa R. O d A, Matias LLR, Passos TS, de Queiroz JLC, de Carvalho FMC, Maciel BLL, Uchôa AF, Amado IR, Gonçalves C, Pastrana L, et al. Safety and potential functionality of nanoparticles loaded with a trypsin inhibitor isolated from tamarind seeds. Future Foods. 2020;1–2:100001.
  • He Y, Li Y, Zhao T, Wang Y, Sun C. Ursolic acid inhibits adipogenesis in 3T3-L1 adipocytes through LKB1/AMPK pathway. PLoS One. 2013;8(7):e70135–12.
  • OECD. Test No. 487: In Vitro Mammalian Cell Micronucleus Test. In: OECD Guidelines for the Testing of Chemicals, Section 4. Paris: OECD Publishing; 2010.
  • Fenech M. Cytokinesis-block micronucleus cytome assay. Nat Protoc. 2007;2(5):1084–1104.
  • Brodkorb A, Egger L, Alminger M, Alvito P, Assunção R, Ballance S, Bohn T, Bourlieu-Lacanal C, Boutrou R, Carrière F, et al. INFOGEST static in vitro simulation of gastrointestinal food gigestion. Nat Protoc. 2019;14(4):991–1014.
  • Matias LLR, Costa ROA, Passos TS, Queiroz JLC, Serquiz AC, Maciel BLL, Santos PPA, Camillo CS, Gonçalves C, Amado IR, Pastrana L, et al. Tamarind trypsin inhibitor in chitosan-whey protein nanoparticles reduces fasting blood glucose levels without compromising insulinemia: a preclinical study. Nutrients. 2019;11(11):2770.
  • Schägger H, Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987;166(2):368–379.
  • Kakade ML, Simons N, Liener IE. An evaluation of natural vs. synthetic substrates for measuring the antitryptic activity of soybean samples. Cereal Che. 1969;46:518–526.
  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins M, Appel R, Bairoch A. Protein identification and analysis tools on the ExPASy server. Totowa (NJ): Humana Press; 2005. p. 571–607.
  • WHO, World Cancer Research Fund/American Institute for Cancer Research. Diet, nutrition and physical activity: energy balance and body fatness the determinants of weight gain, overweight and obesity. London: World Cancer Research Fund/American Institute for Cancer Research; 2018.
  • Yang J, Anishchenko I, Park H, Peng Z, Ovchinnikov S, Baker D. Improved protein structure prediction using predicted interresidue orientations. Proc Natl Acad Sci USA. 2020;117(3):1496–1503.
  • Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr. 2010;66(Pt 1):12–21.
  • Gautier R, Douguet D, Antonny B, Drin G. HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics. 2008;24(18):2101–2102.
  • Mukherjee S, Kar RK, Nanga RPR, Mroue KH, Ramamoorthy A, Bhunia A. Accelerated molecular dynamics simulation analysis of MSI-594 in a lipid bilayer. Phys Chem Chem Phys. 2017;19(29):19289–19299.
  • Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC. GROMACS: fast, flexible, and free. J Comput Chem. 2005;26(16):1701–1718.
  • Huang J, Mackerell AD. CHARMM36 all-atom additive protein force field: validation based on comparison to NMR data. J Comput Chem. 2013;34(25):2135–2145.
  • Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 1983;79(2):926–935.
  • Darden T, York D, Pedersen L. Particle mesh Ewald: an N⋅ log (N) method for Ewald sums in large systems. J Chem Phys. 1993;98(12):10089–10092.
  • Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. LINCS: a linear constraint solver for molecular simulations. J Comput Chem. 1997;18(12):1463–1472.
  • Arfken GB, Weber HJ. Mathematical methods for physicists. Cambridge (MA): Academic Press; 1999.
  • Bussi G, Donadio D, Parrinello M. Canonical sampling through velocity rescaling. J Chem Phys. 2007;126(1):014101.
  • Parrinello M, Rahman A. Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys. 1981;52(12):7182–7190.
  • Amorim-Carmo B. Potent and broad-spectrum antimicrobial activity of analogs from the scorpion peptide stigmurin. Int J Mol Sci. 2019;20(3):1–21.
  • Ribeiro LF, Tullman J, Nicholes N, Silva SRB, Vieira DS, Ostermeier M, Ward RJ. A xylose-stimulated xylanase–xylose binding protein chimera created by random nonhomologous recombination. Biotechnol Biofuels. 2016;9(1):119.
  • Silva SB, Pinheiro MP, Fuzo CA, Silva SR, Ferreira TL, Lourenzoni MR, Nonato MC, Vieira DS, Ward RJ. The role of local residue environmental changes in thermostable mutants of the GH11 xylanase from Bacillus subtilis. Int J Biol Macromol. 2017;97:574–584.
  • Minekus M, Alminger M, Alvito P, Ballance S, Bohn T, Bourlieu C, Carrière F, Boutrou R, Corredig M, Dupont D, et al. A standardised static in vitro digestion method suitable for food- an international consensus. Food Funct. 2014;5(6):1113–1124.
  • Ribeiro JAdNC, Serquiz AC, Silva PFdS, Barbosa PBBM, Sampaio TBM, Araújo Junior RFd, Oliveira ASd, Machado RJA, Maciel BLL, Uchôa AF, et al. Trypsin inhibitor from Tamarindus indica L. seeds reduces weight gain and food consumption and increases plasmatic cholecystokinin levels. Clinics. 2015;70(2):136–143.
  • Ali SM, Siddiqui R, Khan NA. Antimicrobial discovery from natural and unusual sources. J Pharm Pharmacol. 2018;70(10):1287–1300.
  • Fogaça MV, Cândido-Bacani PM, Benicio LM, Zapata LM, Cardoso PF, de Oliveira MT, Calvo TR, Varanda EA, Vilegas W, de Syllos Cólus IM. Effects of indirubin and isatin on cell viability, mutagenicity, genotoxicity and BAX/ERCC1 gene expression. Pharm Biol. 2017;55(1):2005–2014.
  • Pellenz NL, Barbisan F, Azzolin VF, Duarte T, Bolignon A, Mastella MH, Teixeira CF, Ribeiro EE, da Cruz IBM, Duarte MMMF. Analysis of in vitro cyto- and genotoxicity of barbatimão extract on human keratinocytes and fibroblasts. Biomed Res Int. 2018;2018:1942451.
  • Lee SB, Lee JS, Wang JH, Kim MY, Choi YH, Lee HD, Son CG. Genotoxicity of water extract from bark-removed Rhus verniciflua stokes. Molecules. 2021;26(4):896.
  • Wu J, Zhang Y, Lv Z, Yu P, Shi W. Safety evaluation of aloe vera soft capsule in acute, subacute toxicity and genotoxicity study. PLOS One. 2021;16(3):e0249356.
  • Spera KD, Figueiredo PA, Santos PCE, Barbosa FC, Alves CP, Dokkedal AL, Saldanha LL, Silva LP, Figueiredo CR, Ferreira PC, et al. Genotoxicity, anti-melanoma and antioxidant activities of Hymenaea courbaril L. seed extract. An Acad Bras Cienc. 2019;91(4):20180446.
  • Li Q, Huang L, Luo Z, Tamer TM. Stability of trypsin inhibitor isolated from potato fruit juice against pH and heating treatment and in vitro gastrointestinal digestion. Food Chem. 2020;328:127152.
  • Kostekli M, Karakaya S. Protease inhibitors in various flours and breads: effect of fermentation, baking and in vitro digestion on trypsin and chymotrypsin inhibitory activities. Food Chem. 2017;224:62–68.
  • Clemente A, Jimenez EC, Marin-Manzano M, Rubio LA. Active Bowman-Birk inhibitors survive gastrointestinal digestion at the terminal ileum of pigs fed chickpea-based diets. J Sci Food Agric. 2008;88(3):513–521.
  • González C, González D, Rommy N, Zúñiga H, Troncoso E. Simulation of human small intestinal digestion of starch using an in vitro system based on a dialysis membrane process. Foods. 2020;9(7):913.
  • Dupont D, Alric M, Blanquet-Diot S, Bornhorst G, Cueva C, Deglaire A, Denis S, Ferrua M, Havenaar R, Lelieveld J, et al. Can dynamic in vitro digestion systems mimic the physiological reality? Crit Rev Food Sci Nutr. 2019;59(10):1546–1562.
  • Maillet N. Rapid peptides generator: fast and efficient in silico protein digestion. NAR Genom Bioinform. 2019;2(1):lqz004.
  • Almeida LHDO, Oliveira CFRD, Rodrigues MDS, Neto SM, Boleti APDA, Tg AE. Adepamycin: design, synthesis and biological properties of a new peptide with antimicrobial properties. Arch Biochem Biophys. 2020;691(0):108487.
  • Abraham P, Sundaram A, R A, V R, George S, Kumar KS. Structure-activity relationship and mode of action of a frog aecreted antibacterial oeptide B1CTcu5 using synthetically and modularly modified or deleted (SMMD). PLOS One. 2015;10(5):e0124210.
  • Miteva M, Andersson M, Karshikoff A, Otting G. Molecular electroporation: aunifying concept for the description of membrane pore formation by antibacterial peptides, exemplified with NK-lysin. FEBS Lett. 1999;462(1–2):155–158.
  • Bahar AA, Ren D. Antimicrobial peptides. Pharmaceuticals. 2013;6(12):1543–1575.
  • Wang C, Shao C, Fang Y, Wang J, Dong N, Shan A. Binding loop of sunflower trypsin inhibitor 1 serves as a design motif for proteolysis-resistant antimicrobial peptides. Acta Biomater. 2021;124:254–269.
  • Yang CH, Chen YC, Peng SY, Tsai APY, Lee TJF, Yen JH, Liou JW. An engineered arginine-rich α-helical antimicrobial peptide exhibits broad-spectrum bactericidal activity against pathogenic bacteria and reduces bacterial infections in mice. Sci Rep. 2018;8(1):14602.