Abstract
Species of the genus Chuquiraga Juss., Asteraceae, Barnadesioideae, are widely marketed in South America as medicinal plants, despite their relatively uncharacterized phytochemistry. The present study aimed to profile phenolic compounds in commercial samples of three Chuquiraga species (C. jussieui J.F.Gmel., C. spinosa Less., and C. weberbaueri Tovar) from Ecuador and Peru by a high-performance liquid chromatography with diode array detection fingerprinting method combined with multivariate statistical analyses for species classification. From the obtained HPLC fingerprint chromatograms, the traces at 270 nm were selected and submitted to time shifts of peak corrections using the parametric time warping algorithm. Hierarchical clustering analysis, principal components analysis, orthogonal partial least squares discriminant analysis, and k-nearest neighbor measurements were used to evaluate similarities and establish classification models for species discrimination. Based on these analyses, a high percentage of correct classifications (between 83 and 100%) allowed the prediction of the taxonomic identity of unlabeled commercial samples and its geographical origin. Acetophenones (p-hydroxyacetophenone, p-hydroxyacetophenone 4-O-glucoside, p-hydroxyacetophenone 4-O-(6-O-apiosyl)-glucoside), phenylpropanoids (3-O-caffeoylquinic acid, 5-O-caffeoylquinic acid), and flavonoids (quercetin 3-O-rutinoside, quercetin 3-O-glucoronide, kaempferol 3-O-rutinoside) were identified as main constituents of the investigated species.
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17 November 2021
A Correction to this paper has been published: https://doi.org/10.1007/s43450-021-00209-7
References
Alberto MR, Zampini IC, Isla MI (2009) Inhibition of cyclooxygenase activity by standardized hydroalcoholic extracts of four Asteraceae species from the Argentine Puna. Brazilian J Med Biol Res 42:787–790. https://doi.org/10.1590/S0100-879X2009000900003
Arroyo-Acevedo J, Herrera-Calderón O, Chávez-Asmat R, Anampa-Guzmán A, Chumpitaz-Cerrate V, Enciso-Roca E (2017) Protective effect of Chuquiraga spinosa extract on N-methyl-nitrosourea (NMU) induced prostate cancer in rats. Prostate Int 5:47–52. https://doi.org/10.1016/j.prnil.2017.01.005
Beck MA, Häberlein H (1999) Flavonol glycosides from Eschscholzia californica. Phytochemistry 50:329–332. https://doi.org/10.1016/S0031-9422(98)00503-2
Bloemberg TG, Gerretzen J, Wouters HJP, Gloerich, van Dael, Wessels HJCT, van den Heuvel LP, Eilers PHC, Buydens LMC, Wehrens R, (2010) Improved parametric time warping for proteomics. Chemom Intell Lab Syst 104:65–74. https://doi.org/10.1016/j.chemolab.2010.04.008
Bohm BA, Stuessy TF (1995) Flavonoid chemistry of Barnadesioideae (Asteraceae). Syst Bot 20:22–27. http://www.jstor.org/stable/2419629
Bouktaib M, Atmani A, Rolando C (2002) Regio- and stereoselective synthesis of the major metabolite of quercetin, quercetin-3-O-β-D-glucuronide. Tetrahedron Lett 43:6263–6266. https://doi.org/10.1016/S0040-4039(02)01264-9
Bussmann RW, Sharon D, Vandebroek I, Jones A, Revene Z (2007) Health for sale: the medicinal plant markets in Trujillo and Chiclayo. Northern Peru J Ethnobiol Ethnomed 3:37. https://doi.org/10.1186/1746-4269-3-37
Bussmann RW, Glenn A, Meyer K, Kuhlman A, Townesmith A (2010) Herbal mixtures in traditional medicine in Northern Peru. J Ethnobiol Ethnomed 6:10. https://doi.org/10.1186/1746-4269-6-10
Calabria LM, Emerenciano VP, Ferreira MJP, Scotti MT, Marbry TJ (2007) A phylogenetic analysis of tribes of the Asteraceae based on phytochemical data. Nat Prod Commun 2:277–285. https://doi.org/10.1177/1934578X0700200310
Casado R, Landa A, Calvo J, García-Mina JM, Marston A, Hostettmann K, Calvo MI (2011) Anti-inflammatory, antioxidant and antifungal activity of Chuquiraga spinosa. Pharm Biol 49:620–626. https://doi.org/10.3109/13880209.2011.577436
Ccana-Ccapatinta GV, Monge M, Ferreira PL, Da Costa FB (2018) Chemistry and medicinal uses of the subfamily Barnadesioideae (Asteraceae). Phytochem Rev 17:471–489. https://doi.org/10.1007/s11101-017-9544-y
Ccana-Ccapatinta GV, Ferreira PL, Groppo M, Da Costa FB (2019) Caffeic acid ester derivatives and flavonoids of genus Arnaldoa (Asteraceae, Barnadesioideae). Biochem Syst Ecol 86:103911. https://doi.org/10.1016/j.bse.2019.103911
Chagas-Paula DA, Oliveira TB, Faleiro DPV, Oliveira RB, Da Costa FB (2015) Outstanding anti-inflammatory potential of selected Asteraceae species through the potent dual inhibition of cyclooxygenase-1 and 5-lipoxygenase. Planta Med 81:1296–1307. https://doi.org/10.1055/s-0035-1546206
Chaurasia N, Wichtl M (1987) Flavonol glycoside aus Urtica dioica. Planta Med 53:432–434. https://doi.org/10.1055/s-2006-962765
Collins J (1870) Notes on some new little-known vegetable products. Pharm J Trans 11:66–67
Ding H-Y, Lin H-C, Teng C-M, Wu Y-C (2000) Phytochemical and pharmacological studies on Chinese Paeonia species. J Chinese Chem Soc 47:381–388. https://doi.org/10.1002/jccs.200000051
Eilers PHC (2004) Parametric time warping. Anal Chem 76:404–411. https://doi.org/10.1021/ac034800e
Ezcurra C (1985) Revisión del género Chuquiraga (Compositae - Mutisieae). Darwiniana 26:219–284. https://www.jstor.org/stable/23218128
Forino M, Carlo Tenore G, Tartaglione L, Carmela DA, Novellino E, Ciminiello P (2015) (1S,3R,4S,5R)5-O-Caffeoylquinic acid: Isolation, stereo-structure characterization and biological activity. Food Chem 178:306–310. https://doi.org/10.1016/j.foodchem.2015.01.109
Gálvez M, Pastor A (1996) Estudio fitoquímico de la Chuquiraga spinosa. Rev Química 10:133–134
Gerhäuser C, Alt AP, Klimo K et al (2002) Isolation and potential cancer chemopreventive activities of phenolic compounds of beer. Phytochem Rev 1:369–377. https://doi.org/10.1023/A:1026082325529
Gruenstaeudl M, Urtubey E, Jansen RK, Samuel R, Barfuss MHJ, Stuessy TF (2009) Phylogeny of Barnadesioideae (Asteraceae) inferred from DNA sequence data and morphology. Mol Phylogenet Evol 51:572–587. https://doi.org/10.1016/j.ympev.2009.01.023
Han F, Li Y, Zhang X, Song A, Zhang J, Yin R (2016) Comparative study of direct injection analysis and liquid chromatography mass spectrometry for identification of chemical constituents in Kudiezi injection by FT-ICR MS. Int J Mass Spectrom 405:32–38. https://doi.org/10.1016/j.ijms.2016.05.016
Harling G (1991) Compositae-Mutisieae. In: Harling G, Andersson L (eds) Flora of Ecuador. University of Göteborg, Göteborg, pp 1–105
He JW, Yang L, Mu ZQ, Zhu YY, Zhong GY, Liu ZY, Zhou QG, Cheng F (2018) Anti-inflammatory and antioxidant activities of flavonoids from the flowers of Hosta plantaginea. RSC Adv 8:18175–18179. https://doi.org/10.1039/C8RA00443A
Huamantupa I, Cuba M, Urrunaga R, Paz E, Ananya N, Callalli M, Pallqui N, Coasaca H (2012) Riqueza, uso y origen de plantas medicinales expendidas en los mercados de la ciudad del Cusco. Rev Peru Biol 18:283–291
Jeon SH, Chun W, Choi YJ, Kwon YS (2008) Cytotoxic constituents from the bark of Salix hulteni. Arch Pharm Res 31:978–982. https://doi.org/10.1007/s12272-001-1255-9
Landa A, Casado R, Calvo MI (2009) Identification and quantification of flavonoids from Chuquiraga spinosa (Asteraceae). Nat Prod Commun 4:1353–1355. https://doi.org/10.1177/1934578X0900401008
Li X, Liu Z, Zhang XF, Wang LJ, Zheng YN, Yuan CC, Sun GZ (2008) Isolation and characterization of phenolic compounds from the leaves of Salix matsudana. Molecules 13:1530–1537. https://doi.org/10.3390/molecules13081530
Li D, Xu L, Qi J, Yu B (2019) Screening and analysis of cyclooxygenase-2 inhibitors from the complex matrix: a case study to illustrate the important effect of immobilized enzyme activity in magnetic ligand fishing. J Pharm Biomed Anal 175:112795. https://doi.org/10.1016/j.jpba.2019.112795
Madaleno IM (2007) Etno-farmacología en Iberoamérica, una alternativa a la globalización de las prácticas de cura. Cuad Geográficos 41:61–95. https://doi.org/10.30827/cuadgeo.v41i0.1147
Mendiondo ME, Estela Juárez B, Seeligmann P (2000) Flavonoid profiles of some Argentine species of Chuquiraga (Asteraceae). Biochem Syst Ecol 28:283–285. https://doi.org/10.1016/S0305-1978(99)00061-7
Roersch C (1994) Plantas medicinales en el sur andino del Peru. Koenigstein: Koeltz Scientific, Germany
Sagastegui A, Sánchez I (1991) Una nueva especie de Chuquiraga (Asteraceae-Mutisieae) del norte del Perú. Arnaldoa 1:1–4
Senatore F, Nunziata A, D’Agostino M, Feo V (1999) Flavonol glycosides and p-hydroxyacetophenone from Chuquiraga spinosa. Pharm Biol 37:366–368. https://doi.org/10.1076/phbi.37.5.366.6050
Theiler BA, Istvanits S, Zehl M, Marcourt L, Urban E, Caisa LOE, Glasl S (2017) HPTLC Bioautography guided isolation of α-glucosidase inhibiting compounds from Justicia secunda Vahl (Acanthaceae). Phytochem Anal 28:87–92. https://doi.org/10.1002/pca.2651
Wagner H, Bauer R, Melchart D, Xiao PG, Staudinger A (2011) Thin-layer and high performance liquid chromatography of Chinese drugs. In: Chromatographic fingerprint analysis of herbal medicines. Springer-Verlag, Germany, pp 1–1024. https://doi.org/10.1007/978-3-7091-0763-8
Wang M, Li J, Rangarajan M, Shao Y, LaVoie EJ, Huang TC, Ho CT (1998) Antioxidative phenolic compounds from sage (Salvia officinalis). J Agric Food Chem 46:4869–4873. https://doi.org/10.1021/jf980614b
Wehrens R, Bloemberg TG, Eilers PHC (2015) Fast parametric time warping of peak lists. Bioinformatics 31:3063–3065. https://doi.org/10.1093/bioinformatics/btv299
Acknowledgements
The authors express their gratitude to Dr. Ricardo R. da Silva (School of Pharmaceutical Sciences of Ribeirão Preto, USP) for its support in the implementation of PTW script.
Funding
Financial support was provided by the São Paulo Research Foundation (FAPESP) (grant no. 2014/16850–6 and 2014/26866–7), the Coordination for the Improvement of Higher Education Personnel (CAPES: code 001), and the National Council for Scientific and Technological Development (CNPq) for fellowship and funding.
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GVC carried out the experiments and wrote the manuscript; GFP and RC guided the multivariate analyses and revised and corrected the manuscript; MDC helped with the isolation procedures and chromatographic fingerprint data acquisition; PLF, MM, JS, and MG conducted the identification of Chuquiraga species; FBC coordinated the project and was responsible for its final written version. All authors read and approved the final manuscript submission.
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This article is part of a Special Issue to celebrate the 35th anniversary of the Brazilian Journal of Pharmacognosy
This article has been corrected to add an article note and update the size of the chemical structures which are meant to be placed in two columns. This will allow the readers to observe the stereochemistry of the structures. This will allow the readers to observe the stereochemistry of the structures.
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Ccana-Ccapatinta, G.V., Padilla-Gonzalez, G.F., Ferreira, P.L. et al. Phenolic Profiling of Medicinal Species of Chuquiraga, Asteraceae, by HPLC Fingerprinting. Rev. Bras. Farmacogn. 31, 689–697 (2021). https://doi.org/10.1007/s43450-021-00177-y
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DOI: https://doi.org/10.1007/s43450-021-00177-y