Advertisement

Inflammopharmacology

, Volume 27, Issue 2, pp 373–385 | Cite as

Plantago squarrosa Murray extracts inhibit the growth of some bacterial triggers of autoimmune diseases: GC–MS analysis of an inhibitory extract

  • Elsayed Omer
  • Abdelsamed I. Elshamy
  • Mahmoud Nassar
  • Joseph Shalom
  • Alan White
  • Ian E. CockEmail author
Original Article
  • 79 Downloads

Abstract

Ankylosing spondylitis, multiple sclerosis, rheumatoid arthritis and rheumatic fever are autoimmune inflammatory diseases that may be triggered in genetically susceptible individuals by specific bacterial pathogens. Inhibiting the growth of these bacteria with high antioxidant plant extracts may inhibit the aetiology of these diseases, as well as inhibiting the later phase symptoms. P. squarrosa extracts were analysed for antioxidant activity using a DPPH free radical scavenging assay. Bacterial growth inhibitory activity was evaluated using disc diffusion assays and the activity was quantified by MIC determination. The extracts were screened for toxicity by A. franciscana nauplii assays. The most potent antibacterial extract (ethyl acetate) was analysed by GC–MS headspace profile analysis and compounds were identified with reference to a phytochemical database. All extracts displayed strong DPPH radical scavenging activity. The ethyl acetate extract was particularly potent (IC50 1.4 µg/mL), whilst the other extracts also had significant radical scavenging activity (IC50 values between 11 and 22 µg/mL). Notably, the bacterial growth inhibitory activity of the extracts correlated with their DPPH radical scavenging activity. The ethyl acetate extract, which had the greatest DPPH scavenging activity, generally displayed the most potent bacterial growth inhibitory activity. This extract was particularly potent against P. mirabilis, P. vulgaris and A. baylyi (MIC values of 484, 575 and 880 µg/mL, respectively). It also inhibited P. aeruginosa and S. pyogenes growth, albeit with higher MICs (1600–3700 µg/mL). All other extract–bacteria combinations were either inactive or resulted in mid–low potency inhibition. All extracts were non-toxic in the A. franciscana bioassay (LC50 substantially > 1000 µg/mL). In total, 89 unique mass signals were identified in the P. squarrosa ethyl acetate extract by non-biased GC–MS headspace analysis. A number of compounds which may contribute to the antibacterial activity of this extract have been highlighted.

Keywords

Rheumatoid arthritis Ankylosing spondylitis Multiple sclerosis Proteus mirabilis Acinetobacter baylyi Pseudomonas aeruginosa Molecular mimicry 

Notes

Acknowledgements

Financial support for this work was provided by the Environmental Futures Research Institute, Griffith University, and the National Research Centre, Giza, Egypt.

References

  1. Alataha D, Kapral T, Smolen JS (2003) Toxicity profiles of traditional disease modifying antirheumatic drugs for rheumatoid arthritis. Ann Rheum Dis 62:482–486Google Scholar
  2. Arkhipov A, Sirdaarta J, Rayan P et al (2014) An examination of the antibacterial, antifungal, anti-Giardial and anticancer properties of Kigelia africana fruit extracts. Pharmacogn Commun 4(3):62–76.  https://doi.org/10.5530/pc.2014.3.7 Google Scholar
  3. Beermann C, Wunderli-Allenspach H, Groscurth P et al (2000) Lipoproteins from Borrelia burgdorferi applied in liposomes and presented to dendritic cells induce CD8 + T-lymphocytes in vitro. Cell Immunol 201:124–131Google Scholar
  4. Biggs I, Sirdaarta J, White A et al (2016) GC-MS analysis of frankincense extracts which inhibit the growth of bacterial triggers of selected autoimmune diseases. Pharmacogn Commun 6(1):10–22.  https://doi.org/10.5530/pc.2016.1 Google Scholar
  5. Cheesman MJ, Ilanko A, Blonk B et al (2017) Developing new antimicrobial therapies: are synergistic combinations of plant extracts/compounds with conventional antibiotics the solution? Pharmacogn Rev 11:57–72.  https://doi.org/10.4130/phrev.phrev_21_17 Google Scholar
  6. Cock IE (2013) The phytochemistry and chemotherapeutic potential of Tasmannia lanceolata (Tasmanian pepper): a review. Pharmacogn Commun 3(4):13–25Google Scholar
  7. Cock IE (2014) The early stages of rheumatoid arthritis: new targets for the development of combinational drug therapies. OA Arthritis 2(1):5Google Scholar
  8. Cock IE (2018) Is the pharmaceutical industry’s preoccupation with the monotherapy drug model stifling development of effective new drug therapies? Inflammopharmacol 26(3):861–879.  https://doi.org/10.1007/s10787-018-0488-7 Google Scholar
  9. Cock IE, Cheesman MJ (2018) The potential of plants of the genus Syzugium (Myrtaceae) for the prevention and treatment of arthritic and autoimmune diseases. In: Preedy VR, Watson RR (eds) Neurological disorders and imaging physics, volume 1: application of multiple sclerosis. CRC Press, Baton RougeGoogle Scholar
  10. Cock IE, Kukkonen L (2011) An examination of the medicinal potential of Scaevola spinescens: toxicity, antibacterial, and antiviral activities. Pharmacogn Res 3(2):85–94.  https://doi.org/10.4103/0974-8490.81955 Google Scholar
  11. Cock IE, Ruebhart DR (2009) Comparison of the brine shrimp nauplii bioassay and the ToxScreen-II test for the detection of toxicity associated with Aloe vera (Aloe barbadensis Miller) leaf extract. Pharmacogn Res 1(2):102–108Google Scholar
  12. Crowell PL (1999) Prevention and therapy of cancer by dietary monoterpenes. J Nutr 129(3):775S–877SGoogle Scholar
  13. Drouin EE, Glickstein L, Kwok WW et al (2008) Human homologues of a Borrelia T cell epitope associated with antibiotic-refractory Lyme arthritis. Mol Immunol 45(1):180–189Google Scholar
  14. Ebringer A, Rashid T (2006) Rheumatoid arthritis is an autoimmune disease triggered by Proteus urinary tract infection. Clin Dev Immunol 13(1):41–48Google Scholar
  15. Ebringer A, Cunningham P, Ahmadi K et al (1992) Sequence similarity between HLA-DR1 and DR4 subtypes associated with rheumatoid arthritis and Proteus/Serratia membrane haemolysins. Ann Rheum Dis 51:1245–1246Google Scholar
  16. Hughes LE, Smith PA, Natt RS et al (2003) Cross-reactivity between related sequences found in Acinetobacter sp., Pseudomonas aeruginosa, myelin basic protein and myelin oligodendrocyte glycoprotein in multiple scherosis. J Neuroimmunol 144:105–115Google Scholar
  17. Hutchings A, Cock IE (2018) An interactive antimicrobial activity of Embilica officinalis Gaertn. fruit extracts and conventional antibiotics against some bacterial triggers of autoimmune inflammatory diseases. Pharmacogn J 10(4):654–662Google Scholar
  18. Khatiwora E, Adsul VB, Kulkarm M et al (2012) Antibacterial activity of dibutyl phthalate: a secondary metabolite isolated from Ipomoea carnea stem. J Pharm Res 5(1):150–152Google Scholar
  19. Kollef MH, West S, Davis DR et al (1991) Central and peripheral nervous system demyelination after infection with Mycoplasma pneumoniae. Evidence of an autoimmune process. South Med J 84:1255–1258Google Scholar
  20. Lu XG, Zhan LB, Feng BA et al (2004) Inhibition of growth and metastasis of human gastric cancer implanted in nude mice by d-limonene. World J Gastroenterol 10(14):2140–2144Google Scholar
  21. Mandeville A, Cock IE (2018) Terminalia chebula Retz. fruit extracts inhibit bacterial triggers of some autoimmune diseases and potentiate the activity of tetracycline. Indian J Microbiol 74:25–36.  https://doi.org/10.1007/s12088-018-0754-9 Google Scholar
  22. Omer E, Elshamy AI, El Gendy AN et al (2016) Cakile maritima Scop. extracts inhibit the growth of some bacterial triggers of autoimmune diseases: GC-MS analysis of an inhibitory extract. Pharmacogn J 8(4):361–374.  https://doi.org/10.5530/pj.2016.4.9 Google Scholar
  23. Ruebhart DR, Wickramasinghe W, Cock IE (2009) Protective efficacy of the antioxidants vitamin E and Trolox against Microcystis aeruginosa and microcystin-LR in Artemia franciscana nauplii. J Toxicol Environ Health Part A 72:1567–1575Google Scholar
  24. Salminen A, Lehtonen M, Suuronen T et al (2008) Terpenoids: natural inhibitors of NF-κB signalling with anti-inflammatory and anticancer potential. Cell Mol Life Sci 65(19):2979–2999Google Scholar
  25. Samuelsen AB (2000) The traditional uses, chemical constituents and biological activities of Plantago major L. A review. J Ethnopharmacol 71(1–2):1–21Google Scholar
  26. Sangwan YS, Sangwan S, Jalwal P et al (2011) Mucilages and their pharmaceutical applications: an overview. Pharmacologyonline 2:1265–1271Google Scholar
  27. Shalom J, Cock IE (2018) Terminalia ferdinandiana Exell. fruit and leaf extracts inhibit proliferation and induce apoptosis in selected human cancer cell lines. Nutr Cancer 70(4):579–593Google Scholar
  28. Signorino G, Amaboldi PM, Petzke MM et al (2014) Identification of OppA2 linear epitopes as serodiagnostic markers for Lyme disease. Clin Vaccin Immunol 21(5):704–711Google Scholar
  29. Sirdaarta J, Matthews B, Cock IE (2015a) Kakadu plum fruit extracts inhibit growth of the bacterial triggers of rheumatoid arthritis: identification of stilbene and tannin components. J Funct Foods 17:610–620.  https://doi.org/10.1016/j.jff.2015.06.019 Google Scholar
  30. Sirdaarta J, Matthews B, White A et al (2015b) GC-MS and LC-MS analysis of Kakadu plum fruit extracts displaying inhibitory activity against microbial triggers of multiple sclerosis. Pharmacogn Commun 5(2):100–115.  https://doi.org/10.5530/pc.2015.2.2 Google Scholar
  31. Winnett V, Boyer H, Sirdaarta J et al (2014) The potential of Tasmannia lanceolata as a natural preservative and medicinal agent: antimicrobial activity and toxicity. Pharmacogn Commun 4(1):42–52.  https://doi.org/10.5530/pc.2014.1.7 Google Scholar
  32. Wright MH, Greene AC, Cock IE (2017) Investigating the pharmacognostic potential of Indian Terminalia spp. in the treatment and prevention of yersiniosis. Pharmacogn Commun 7(3):108–113.  https://doi.org/10.5530/pc.2017.3.16 Google Scholar
  33. Zhou JY, Tang FD, Mao GG et al (2004) Effect of a-pinene on nuclear translocation of NF-kB in THP-1 cells. Acta Pharmacol Sin 25(4):480–484Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Medicinal and Aromatic Plants Research DepartmentNational Research CentreDokki, GizaEgypt
  2. 2.Chemistry of Natural Compounds DepartmentNational Research CentreDokki, GizaEgypt
  3. 3.School of Natural Sciences, Nathan CampusGriffith UniversityNathanAustralia
  4. 4.Environmental Futures Research Institute, Nathan CampusGriffith UniversityNathanAustralia

Personalised recommendations