Planta Med 2022; 88(09/10): 753-761
DOI: 10.1055/a-1652-1547
Biological and Pharmacological Activity
Original Papers

More Than Just a Weed: An Exploration of the Antimicrobial Activity of Rumex crispus using a Multivariate Data Analysis Approach

Chantal V. Pelzer
1   Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, Greensboro NC, United States
,
Joëlle Houriet
1   Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, Greensboro NC, United States
,
William J. Crandall
1   Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, Greensboro NC, United States
,
Daniel A. Todd
1   Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, Greensboro NC, United States
,
1   Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, Greensboro NC, United States
,
1   Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, Greensboro NC, United States
2   Department of Pharmaceutical Sciences, University of Illinois at Chicago, Chicago IL, United States
› Author Affiliations
Supported by: National Center for Complementary and Alternative Medicine R15 AT010191
Supported by: National Center for Complementary and Alternative Medicine T32 AT008938
Supported by: National Institute of General Medical Sciences K12GM139186

Abstract

Plants have a long history of use for their medicinal properties. The complexity of botanical extracts presents unique challenges and necessitates the application of innovative approaches to correctly identify and quantify bioactive compounds. For this study, we used untargeted metabolomics to explore the antimicrobial activity of Rumex crispus (yellow dock), a member of the Polygonaceae family used as an herbal remedy for bacterial infections. Ultra-performance liquid chromatography coupled with high resolution mass-spectrometry (UPLC-MS) was used to identify and quantify the known antimicrobial compound emodin. In addition, we used biochemometric approaches to integrate data measuring antimicrobial activity from R. crispus root starting material and fractions against methicillin-resistant Staphylococcus aureus (MRSA) with UPLC-MS data. Our results support the hypothesis that multiple constituents, including the anthraquinone emodin, contribute to the antimicrobial activity of R. crispus against MRSA.

Supporting Information



Publication History

Received: 12 July 2021

Accepted after revision: 15 September 2021

Article published online:
25 October 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Chugh NA, Bali S, Koul A. Integration of botanicals in contemporary medicine: Road blocks, checkpoints and go-ahead signals. Integr Med Res 2018; 7: 109-125
  • 2 Zaller JG. Ecology and non-chemical control of Rumex crispus and R. obtusifolius (Polygonaceae): A review. Weed Res 2004; 44: 414-432
  • 3 Vasas A, Orbán-Gyapai O, Hohmann J. The genus Rumex: Review of traditional uses, phytochemistry and pharmacology. J Ethnopharm 2015; 175: 198-228
  • 4 Wegiera M, Kosikowska U, Malm A, Smolarz HD. Antimicrobial activity of the extracts from fruits of Rumex L. species. Cent Eur J Biol 2011; 6: 1036-1043
  • 5 Yildirim A, Mavi A, Kara AA. Determination of antioxidant and antimicrobial activities of Rumex crispus L. extracts. J Agric Food Chem 2001; 49: 4083-4089
  • 6 Günaydin K, Topçu G, Ion RM. 1, 5-Dihydroxyanthraquinones and an anthrone from roots of Rumex crispus . Nat Prod Lett 2002; 16: 65-70
  • 7 Dong X, Fu J, Yin X, Cao S, Li X, Lin L, Huyiligeqi. Ni J. Emodin: A review of its pharmacology, toxicity and pharmacokinetics. Phytother Res 2016; 30: 1207-1218
  • 8 Izhaki I. Emodin – a secondary metabolite with multiple ecological functions in higher plants. New Phytol 2002; 155: 205-217
  • 9 Orbán-Gyapai O, Liktor-Busa E, Kúsz N, Stefkó D, Urbán E, Hohmann J, Vasas A. Antibacterial screening of Rumex species native to the Carpathian Basin and bioactivity-guided isolation of compounds from Rumex aquaticus . Fitoterapia 2017; 118: 101-106
  • 10 World Health Organization. Antimicrobial Resistance: Global Report on Surveillance. Geneva: World Health Organization; 2014
  • 11 Otto M. Community-associated MRSA: What makes them special?. Int J Med Microbiol 2013; 303: 324-330
  • 12 Rebstock MC, Crooks HM, Controulis J, Bartz QR. Chloramphenicol (Chloromycetin).1IV.1a Chemical Studies. J Am Chem Soc 1949; 71: 2458-2462
  • 13 Zhang W, Chen H, Liu DL, Li H, Luo J, Zhang JH, Li Y, Chen KJ, Tong HF, Lin SZ. Emodin sensitizes the gemcitabine-resistant cell line Bxpc-3/Gem to gemcitabine via downregulation of NF-κB and its regulated targets. Int J Oncol 2013; 42: 1189-1196
  • 14 Caesar LK, Nogo S, Naphen CN, Cech NB. Simplify: A mass spectrometry metabolomics approach to identify additives and synergists from complex mixtures. Anal Chem 2019; 91: 11297-11305
  • 15 Kellogg JJ, Todd DA, Egan JM, Raja HA, Oberlies NH, Kvalheim OM, Cech NB. Biochemometrics for natural products research: Comparison of data analysis approaches and application to identification of bioactive compounds. J Nat Prod 2016; 79: 376-386
  • 16 Kvalheim OM, Brakstad F, Liang Y. Preprocessing of analytical profiles in the presence of homoscedastic or heteroscedastic noise. Anal Chem 1994; 66: 43-51
  • 17 Kvalheim OM, Karstang TV. Interpretation of latent-variable regression models. Chemometr Intell Lab Syst 1989; 7: 39-51
  • 18 Jones DD, Caesar LK, Pelzer CV, Crandall WJ, Jenul C, Todd DA, Horswill AR, Cech NB. Targeted and untargeted analysis of secondary metabolites to monitor growth and quorum sensing inhibition for methicillin-resistant Staphylococcus aureus (MRSA). J Microbiol Met 2020; 176: 106000
  • 19 Kvalheim OM. Interpretation of partial least squares regression models by means of target projection and selectivity ratio plots. J Chemom 2010; 24: 496-504
  • 20 Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TW, Fiehn O, Goodacre R, Griffin JL, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane AN, Lindon JC, Marriott P, Nicholls AW, Reily MD, Thaden JJ, Viant MR. Proposed minimum reporting standards for chemical analysis chemical analysis working group (CAWG) metabolomics standards initiative (MSI). Metabolomics 2007; 3: 211-221
  • 21 Daly SM, Elmore BO, Kavanaugh JS, Triplett KD, Figueroa M, Raja HA, El-Elimat T, Crosby HA, Femling JK, Cech NB, Horswill AR, Oberlies NH, Hall PR. ω-Hydroxyemodin limits Staphylococcus aureus quorum sensing-mediated pathogenesis and inflammation. Antimicrob Agents Chemother 2015; 59: 2223-2235
  • 22 van den Berg AJJ, Labadie RP. The production of acetate derived hydroxyanthraquinones, -dianthrones, -naphthalenes and -benzenes in tissue cultures from Rumex alpinus . Planta Med 1981; 41: 169-173
  • 23 Hariprasad P, Ramakrishnan N. GC-MS analysis of Rumex vesicarius L. Int J Drug Dev Res 2011; 3: 272-279
  • 24 Chen X, Wei L, Pu X, Wang Y, Xu Y. Pharmacokinetics and tissue distribution study of 15 ingredients of Polygonum chinense Linn extract in rats by UHPLC–MS/MS. Biomed Chromatogr 2020; e4975
  • 25 Yang D, Sun G, Zhang A, Fu S, Liu J. Screening and analyzing the potential bioactive components from rhubarb, using a multivariate data processing approach and ultra-high performance liquid chromatography coupled with time-of-flight mass spectrometry. Anal Methods 2015; 7: 650-661
  • 26 Oshio H, Naruse Y, Tsukui M. Quantitative analysis of the purgative components of rhubarb and senna. Chem Pharm Bull 1978; 26: 2458-2464
  • 27 Piola F, Bellvert F, Meiffren G, Rouifed S, Walker V, Comte G, Bertrand C. Invasive Fallopia × bohemica interspecific hybrids display different patterns in secondary metabolites. Écoscience 2013; 20: 230-239
  • 28 Gnonlonfin GJB, Sanni A, Brimer L. Review Scopoletin – A coumarin phytoalexin with medicinal properties. Crit Rev Plant Sci 2012; 31: 47-56
  • 29 Kabir F, Katayama S, Tanji N, Nakamura S. Antimicrobial effects of chlorogenic acid and related compounds. J Korean Soc Appl Biol Chem 2014; 57: 359-365
  • 30 Induli M, Cheloti M, Wasuna A, Wekesa I, Wanjohi JM, Byamukama R, Heydenrich M, Makayoto M, Yenesew A. Naphthoquinones from the roots of Aloe secundiflora . Phytochem Lett 2012; 5: 506-509
  • 31 Smyth T, Ramachandran VN, Smyth WF. A study of the antimicrobial activity of selected naturally occurring and synthetic coumarins. Int J Antimicrob Agents 2009; 33: 421-426
  • 32 Commision Regulation (EU) 2018/468. Official journal of the European Union 2021 (March 18, 2021). Accessed October 5, 2021 at: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32021R0468&qid=1616147010900&from=IT
  • 33 Pluskal T, Castillo S, Villar-Briones A, Oresic M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 2010; 11: 395
  • 34 Kessner D, Chambers M, Burke R, Agus D, Mallick P. ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 2008; 24: 2534-2536
  • 35 Humphries RM, Ambler J, Mitchell SL, Castanheira M, Dingle T, Hindler JA, Koeth L, Sei K. CLSI methods development and standardization working group best practices for evaluation of antimicrobial susceptibility tests. J Clin Microbiol 2018; 56: e01934-17
  • 36 Boles BR, Thoendel M, Roth AJ, Horswill AR. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. Plos One 2010; 5: e10146
  • 37 Demirezer LO, Uzun M. Determination of sun protection factor (SPF) of Rumex crispus and main anthraquinones. Planta Med 2016; 82: P334
  • 38 Demirezer ÖL, Kuruüzüm A. Rapid and simple biological activity screening of some Rumex species; Evaluation of bioguided gractions of R. scutatus and pure compounds. Z Naturforschung C 1997; 52: 665-669
  • 39 Başkan S, Daut-Özdemir A, Günaydın K, Erim FB. Analysis of anthraquinones in Rumex crispus by micellar electrokinetic chromatography. Talanta 2007; 71: 747-750