Abstract
Achyrocline satureioides (Lam.) DC., Asteraceae, Clinopodium bolivianum Kuntze, Lamiaceae, Rubus urticifolius Poir., Rosaceae, and Tagetes elliptica Sm., Asteraceae, are medicinal South American plants, traditionally used in the form of infusions and decoctions for the treatment of pneumonia. Our research focused on the analysis of their compounds in the aqueous, hexane, and dichloromethane/methanol extracts, using UV, IR, and 1H NMR spectroscopic techniques. Subsequently, based on the initial results, fingerprints were used through the identification of the majoritarian compounds of each extract. Finally, the extracts’ biological activity was determined through cytotoxicity and anti-inflammatory assays (NF-κB inhibition) in MRC-5 and HBEC3-KT cells, while the antioxidant (ABTS•+ inhibition) and antibacterial activities were tested in the Staphylococcus aureus, S. pneumoniae, Haemophilus influenzae, and Legionella pneumophila strains. Chemical analysis allowed us to obtain the first chemical fingerprint of R. urticifolius that confirmed the presence of glycosidic or aglycone compounds in the extracts of A. satureioides, C. bolivianum, and T. elliptica. Regarding cytotoxicity, all aqueous and dichloromethane/methanol extracts showed CC50 > 50 μg/ml (for A. satureioides, this was the most cytotoxic, CC50 52.06 μg/ml in MRC-5 cells). However, all hexane and dichloromethane/methanol extracts had the highest anti-inflammatory activity (for R. urticifolius, IC50 22.88 μg/ml in MRC-5 cells; for R. urticifolius, it also had the highest antioxidant capacity, especially the dichloromethane/methanol extract, with IC50 2.77 μg/ml). Finally, all extracts had the highest antibacterial activity against Gram-positive bacteria (especially the dichloromethane/methanol extract of A. satureioides, with MICs 4.66–10.26 µg/ml). Analyzing chemical and biological results, we can conclude that the dichloromethane/methanol extracts had the most promising pharmacological potential given the synergy of their medium-polarity compounds.
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References
ANMAT (2003) Administración Nacional de Medicamentos, Alimentos y tecnología médica. In: Farmacopea Argentina, 7 edn. ANMAT, Buenos Aires, pp. 2745
Anvisa (2022) Farmacopeia Brasileira, 6 edn, vol II, Agência Nacional de Vigilância Sanitária, Plantas Medicinais. pp. 745
Apaza Ticona L, Tena Pérez V, Serban AM, Alonso Navarro MJ, Rumbero Sánchez Á (2019) Alkamides from Tropaeolum tuberosum inhibit inflammatory response induced by TNF-α and NF-κB. J Ethnopharmacol 235:199–205. https://doi.org/10.1016/j.jep.2019.02.015
Apaza Ticona L, Rumbero Sánchez Á, Sánchez Sánchez-Corral J, Iglesias Moreno P, Ortega Domenech M (2021) Anti-inflammatory, pro-proliferative and antimicrobial potential of the compounds isolated from Daemonorops draco (Willd.) Blume. J Ethnopharmacol 268:113668. https://doi.org/10.1016/j.jep.2020.113668
Arulselvan P, Fard MT, Tan WS, Gothai S, Fakurazi S, Norhaizan ME, Kumar SS (2016) Role of antioxidants and natural products in inflammation. Oxid Med Cell Longev 2016:5276130. https://doi.org/10.1155/2016/5276130
Baronio AM, Galli MC, Posadaz AC, Risso OA, Salusso FA, Suárez DA, Suárez SA, Suyama A, Tavaglia CN, Vianco AM, Walter S (2019) Manual de buenas prácticas para recolección, cultivo y manufactura de marcela: Achyrocline satureioides. UniRío Editora
Berlinck RGS, Proteau PJ (2021) Advancements in natural products research from Central and South America: a virtual issue. J Nat Prod 84:2069. https://doi.org/10.1021/acs.jnatprod.1c00628
Bhavsar A, Zaryczański J, Wasilewska A, Saragoussi D, Devadiga R, Colby C, Bahar E, Wysocki J (2022) Pneumonia hospitalizations of children aged <2 years in Poland before (2013–2016) and after (2017–2018) universal mass vaccination with 10-valent pneumococcal non-typeable Haemophilus influenzae protein D conjugate vaccine. Hum Vaccin Immunother 18:2128566. https://doi.org/10.1080/21645515.2022.2128566
Bianchi SE, Mereilles GdC, Raabe VB, Borges de Souza KC, Bassani VL (2023) Achyrocline satureioides review: from the pharmacochemical diversity to the technological development of products. Fitoterapia 168:105537. https://doi.org/10.1016/j.fitote.2023.105537
Bindu S, Mazumder S, Bandyopadhyay U (2020) Non-steroidal anti-inflammatory drugs (NSAIDs) and organ damage: a current perspective. Biochem Pharmacol 180:114147. https://doi.org/10.1016/j.bcp.2020.114147
Blum U (2019) Simple phenolic acids in solution culture II: Log P, Log D and molecular structure. In: Plant-Plant Allelopathic Interactions III. Springer, Cham, pp 115–153. https://doi.org/10.1007/978-3-030-22098-3_5
Bortolotti A, Troiano C, Bobone S, Konai MM, Ghosh C, Bocchinfuso G, Acharya Y, Santucci V, Bonacorsi S, Di Stefano C, Haldar J, Stella L (2023) Mechanism of lipid bilayer perturbation by bactericidal membrane-active small molecules. Biochim Biophys Acta Biomembr 1865:184079. https://doi.org/10.1016/j.bbamem.2022.184079
Broussalis AM, Ferraro GE, Gurni A, Coussio JD (1988) Phenolic compounds of four Achyrocline species. Biochem Syst Ecol 16:401–402. https://doi.org/10.1016/0305-1978(88)90032-4
Bussmann RW, Glenn A, Sharon D (2010) Antibacterial activity of medicinal plants of Northern Peru –can traditional applications provide leads for modern science? Indian J Tradit Knowl 9:742–753
Carini JP, Leitão GG, Schneider PH, Santos CC, Costa FN, Holzschuh MH, Klamt F, Bassani VL (2015) Isolation of achyrobichalcone from Achyrocline satureioides by high-speed countercurrent chromatography. Curr Pharm Biotechnol 16:66–71. https://doi.org/10.2174/1389201015666141110143019
Carney JR, Kranisky JM, Williamson T, Luo J (2002) Achyrofuran, a new antihyperglycemic dibenzofuran from the South American medicinal plant Achyrocline satureioides. J Nat Prod 65:203–205. https://doi.org/10.1021/np010374l
Casero C, Machín F, Méndez-Álvarez S, Demo M, Ravelo AG, Pérez-Hernández N, Joseph-Nathan P, Estévez-Braun A (2015) Structure and antimicrobial activity of phloroglucinol derivatives from Achyrocline satureioides. J Nat Prod 78:93–102. https://doi.org/10.1021/np500735f
Cerrón-Mercado F, Perez-Alvarez JA, Nolazco-Cama D, Salva-Ruíz B, Tellez-Monzon L, Fernández-López J, Viuda-Martos M (2023) Chemical composition, antioxidant and antibacterial activities of essential oil obtained from Chincho (Tagetes elliptica Sm) leaves grown in the Peruvian Andes. Foods 12:894. https://doi.org/10.3390/foods12040894
Chirinos R, Huamán M, Betalleluz-Pallardel I, Pedreschi R, Campos D (2011) Characterization of phenolic compounds of Inca muña (Clinopodium bolivianum) leaves and the feasibility of their application to improve the oxidative stability of soybean oil during frying. Food Chem 128:711–716. https://doi.org/10.1016/j.foodchem.2011.03.093
Chirinos R, Pedreschi R, Rogez H, Larondelle Y, Campos D (2013) Phenolic compound contents and antioxidant activity in plants with nutritional and/or medicinal properties from the Peruvian Andean region. Ind Crops Prod 47:145–152. https://doi.org/10.1016/j.indcrop.2013.02.025
De Lucca DM, Zalles AJ (1992) Flora medicinal boliviana. Los amigos del libro Cochabamba, Bolivia, pp. 346; 386
De Souza KCB, Schapoval EES, Bassani VL (2002) LC determination of flavonoids: separation of quercetin, luteolin and 3-O-methylquercetin in Achyrocline satureioides preparations. J Pharm Biomed Anal 28:771–777. https://doi.org/10.1016/S0731-7085(01)00693-8
El-Kattan AF, Asbill CS, Kim N, Michniak BB (2001) The effects of terpene enhancers on the percutaneous permeation of drugs with different lipophilicities. Int J Pharm 215:229–240. https://doi.org/10.1007/s00044-014-1241-4
Espinosa NB, Ligarreto GAM, Barrero LSM, Medina CIC (2016) Variabilidad morfológica de variedades nativas de mora (Rubus sp.) en los Andes de Colombia. Rev Colomb Cienc Hortic 10:211–221. https://doi.org/10.17584/rcch.2016v10i2.4755
Fariña E, Daghero H, Bollati-Fogolín M, Boido E, Cantero J, Moncada-Basualto M, Olea-Azar C, Polticelli F, Paulino M (2023) Antioxidant capacity and NF-kB-mediated anti-inflammatory activity of six red Uruguayan grape pomaces. Molecules 28:3909. https://doi.org/10.3390/molecules28093909
Ferreira ECC, Gonçalves TM, Pereira TC, Hasna AA, Oliveira FE, Jorjao AL, Camargo SEA, Oliveira LD, Spalding M (2021) The biocompatibility of Achyrocline satureioides plant extract over human gingival fibroblasts. Res Soc Dev 10:e37610111902. https://doi.org/10.33448/rsd-v10i1.11902
Fukunaga K, Kohli P, Bonnans C, Fredengurgh LE, Levy BD (2005) Cyclooxygenase 2 plays a pivotal role in the resolution of acute lung injury. J Immunol 174:5033–5039. https://doi.org/10.4049/jimmunol.174.8.5033
Golan-Goldhirsh A, Gopas J (2014) Plant derived inhibitors of NF-κB. Phytochem Rev 13:107–121. https://doi.org/10.1007/s11101-013-9293-5
Gonzales GB, Camp JV, Zotti M, Kobayashi V, Grootaert C, Raes K, Smagghe G (2015) Two- and three-dimensional quantitative structure–permeability relationship of flavonoids in Caco-2 cells using stepwise multiple linear regression (SMLR), partial least squares regression (PLSR), and pharmacophore (GALAHAD)-based comparative molecular similarity index analysis (COMSIA). Med Chem Res 24:1696–1706. https://doi.org/10.1007/s00044-014-1241-4
Grassi-Zampieron R, França LV, Carollo VA, Oliveros-Bastidas A, Siquiera JM (2010) Comparative profiles of Achyrocline alata (Kunth) DC. and A. satureioides (Lam.) DC., Astreraceae, applying HPLC-DAD-MS. Rev Bras Farmacogn 20:575–579. https://doi.org/10.1590/S0102-695X2010000400017
Guillouzo A, Guguen-Guillouzo C (2020) Antibiotics-induced oxidative stress. Curr Opin Toxicol 20–21:23–28. https://doi.org/10.1016/j.cotox.2020.03.004
Gupta P, Vasudeva N (2012) Marigold. A potential ornamental plant drug. Hamdard Med 55:45–59
Gupta MP (1995) 270 Plantas Medicinales Iberoamericanas. Presencia Ltda, Bogotá, Colombia, pp 55–57; 328–330
He H, Wunderink RG (2020) Staphylococcus aureus pneumonia in the community. Semin Respir Crit Care Med 41:470–479. https://doi.org/10.1055/s-0040-1709992
Hrelia S, Angeloni C (2020) New mechanisms of action of natural antioxidants in health and disease. Antioxidants 9:344. https://doi.org/10.3390/antiox9040344
Hussein RA, El-Anssary AA (2018) Plants secondary metabolites: the key drivers of the pharmacological actions of medicinal plants. In: Builders PF (ed) Herbal medicine. IntechOpen, pp 11–29. https://doi.org/10.5772/intechopen.76139
Ibrahim IA, Jabbour AA, Abdulmajeed AM, Elhady ME, Almaroai YA, Hashim AM (2022) Adaptive responses of four medicinal plants to high altitude oxidative atresses through the regulation of antioxidants and secondary metabolites. Agronomy 12:3032. https://doi.org/10.3390/agronomy12123032
Ishikawa K, Nakamura T, Matsuo T, Kawai F, Murakami H, Aoki K, Nagasawa T, Uehara Y, Mori N (2022) Clinical presentation of Legionella pneumophila serogroup 1-associated pneumonia and diffuse alveolar hemorrhage: a case report and literature review. Am J Med Case Rep 23:e936309. https://doi.org/10.12659/AJCR.936309
Joray MB, del Rollán MR, Ruiz GM, Palacios SM, Carpinella MC (2011) Antibacterial activity of extracts from plants of central Argentina-isolation of an active principle from Achyrocline satureioides. Planta Med 77:95–100. https://doi.org/10.1055/s-0030-1250133
Kaloga M, Hänsel R, Cybulski EM (1983) Isolation of a Kawapyrone from Achyrocline satureioides. Planta Med 48:103–104. https://doi.org/10.1055/s-2007-969898
Kim GL, Seon SH, Rhee DK (2017) Pneumonia and Streptococcus pneumoniae vaccine. Arch Pharm Res 40:885–893. https://doi.org/10.1007/s12272-017-0933-y
Leicach SR, Chludil HD (2014) Plant secondary metabolites: structure-activity relationships in human health prevention and treatment of common diseases. Stud Nat Prod Chem 42:267–304. https://doi.org/10.1016/B978-0-444-63281-4.00009-4
Lingappan K (2018) NF-κB in oxidative stress. Curr Opin Toxicol 7:81–86. https://doi.org/10.1016/j.cotox.2017.11.002
Lizarraga E, Abdala L (2004) Compuestos fenólicos mayoritarios en Satureja boliviana (Benth.) Briq. (Lamiaceae). Acta Farm Bonaer 23:198–200
Lorenzo D, Atti-Serafini L, Santos AC, Frizzo CD, Paroul N, Paz D, Dellacassa E, Moyna P (2000) Achyrocline satureioides essential oils from southern Brazil and Uruguay. Planta Med 66:476–477. https://doi.org/10.1055/s-2000-8590
Martínez-Busi M, Arredondo F, González D, Echeverry C, Vega-Teijido MA, Carvalho D, Rodríguez-Haralambides A, Rivera F, Dajas F, Abin-Carriquiry JA (2019) Purification, structural elucidation, antioxidant capacity and neuroprotective potential of the main polyphenolic compounds contained in Achyrocline satureioides (Lam) D.C. (Compositae). Bioor Med Chem 27:2579–2591. https://doi.org/10.1016/j.bmc.2019.03.047
Mesquita AAL, Corrêa DDB, de Pádua AP, Guedes MLO, Gottlieb OR (1986) Flavonoids from our Compositae species. Phytochemistry 25:1255–1256. https://doi.org/10.1016/S0031-9422(00)81599-X
Micallef J, Soeiro T, Jonville-Béra AP (2020) Non-steroidal anti-inflammatory drugs, pharmacology, and COVID-19 infection. Therapies 75:305–362. https://doi.org/10.1016/j.therap.2020.05.003
Michel J, Abd Rani NZ, Husain K (2020) A review on the potential use of medicinal plants from Asteraceae and Lamiaceae plant family in cardiovascular diseases. Front Pharmacol 11:484919. https://doi.org/10.3389/fphar.2020.00852
Mohan S, Ajay Krishna MS, Chandramouli M, Keri RS, Patil SA, Ningaiah S, Somappa SB (2023) Antibacterial natural products from microbial and fungal sources: a decade of advances. Mol Divers 27:517–541. https://doi.org/10.1007/s11030-022-10417-5
Mohanty S, Kamolvit W, Zambrana S, Sandström C, Gonzales E, Östenson CG, Brauner, (2017) Extract of Clinopodium bolivianum protects against E. coli invasion of uroepithelial cells. J Ethnopharmacol 198:214–220. https://doi.org/10.1016/j.jep.2017.01.011
Nguelefack TB, Mbakam FHK, Tapondjou LA, Watcho P, Nguelefack-Mbuyo EP, Ponou BK, Kamanyi A, Park HJ (2011) A dimeric triterpenoid glycoside and flavonoid glycosides with free radical-scavenging activity isolated from Rubus rigidus var. camerunensis. Arch Pharm Res 34:543–550. https://doi.org/10.1007/s12272-011-0404-9
Petkova N, Ivanova L, Filova G, Ivanov I, Denev P (2017) Antioxidants and carbohydrate content in infusions and microwave extracts from eight medicinal plants. J Appl Pharm Sci 7:55–61. https://doi.org/10.7324/JAPS.2017.71008
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3
Reinecke MG, Minter DE, Jia Q (1995) Carbon and proton NMR assignments for 6,7-dimethoxycoumarin. Magn Reson Chem 33:757–758. https://doi.org/10.1002/mrc.1260330913
Ruiz Quiroz JR, Salazar Salvatierra ME (2022) Composición química y actividad antibacteriana de los aceites esenciales de Citrus paradisi, Juglans neotropica Diels, Schinus molle y Tagetes elliptica Smith. Rev Soc Quím Perú 87:228–241. https://doi.org/10.37761/rsqp.v87i3.350
Salcedo Ríos MA, Alonso JR (2021) Satureja boliviana (Lamiaceae). An update of “muña blanca” Dominguezia 37:5–12
Salgueiro ACF, Folmer V, da Rosa HS, Costa MT, Boligon AA, Paula FR, Roos DH, Puntel GO (2016) In vitro and in silico antioxidant and toxicological activities of Achyrocline satureioides. J Ethnopharmacol 194:6–14. https://doi.org/10.1016/j.jep.2016.08.048
Simões CM, Schenkel EP, Bauer L, Langeloh A (1988) Pharmacological investigations on Achyrocline satureioides (Lam.) DC., Compositae. J Ethnopharmacol 22:281–293. https://doi.org/10.1016/0378-8741(88)90239-5
Tepe B, Cilkiz M (2016) A pharmacological and phytochemical overview on Satureja. Pharm Biol 54:375–412. https://doi.org/10.3109/13880209.2015.1043560
Thawabteh AM, Swaileh Z, Ammar M, Jaghama W, Yousef M, Karaman RA, Bufo S, Scrano L (2023) Antifungal and antibacterial activities of isolated marine compounds. Toxins 15:93. https://doi.org/10.3390/toxins15020093
Vaishampayan A, Grohmann E (2022) Antimicrobials functioning through ROS-mediated mechanisms: current insights. Microorganisms 10:61. https://doi.org/10.3390/microorganisms10010061
Vega EN, Molina AK, Pereira C, Días MI, Heleno SA, Rodrigues P, Fernandes IP, Barreiro MF, Stojkovic D, Sokovic M, Carocho M, Barreira JCM, Ferreira ICFR, Barros L (2021) Anthocyanins from Rubus fucticosus L. and Morus nigra L. applied as food colorants: a natural alternative. Plants 10:1181. https://doi.org/10.3390/plants10061181
Viturro CI, Molina AC, Heit C, Elechosa MA, Molina AM, Juárez MA (2007) Evaluación de la composición de los aceites esenciales de Satureja boliviana, y S. parvifolia, obtenidos de colectas en Tucumán, Argentina. Bol Latinoam Caribe Pl 6:288–289
Wan J, Wang XJ, Guo N, Wu XY, Xiong J, Zang Y, Jiang CX, Han B, Li J, Hu JF (2021) Highly oxygenated triterpenoids and diterpenoids from Fructus Rubi (Rubus chingii Hu) and their NF-kappa B inhibitory effects. Molecules 26:1911. https://doi.org/10.3390/molecules26071911
Wang S, Zhang D, Zhu J, Liu H, Li B, Huang L, Achyrophenols A-F (2021) Polycyclic polyphenol lactone skeletons and a nor-ursane-type triterpenoid from Achyrocline satureioides. J Org Chem 86:12813–12820. https://doi.org/10.1021/acs.joc.1c01447
WHO (2021) Pneumonia. World Health Organization, https://www.who.int/news-room/fact-sheets/detail/pneumonia. Accessed 30 June, 2022
Zhan X, Chen Z, Chen R, Shen C (2022) Environmental and genetic factors involved in plant protection-associated secondary metabolite biosynthesis pathways. Front Plant Sci 13:877304. https://doi.org/10.3389/fpls.2022.877304
Zhang Y, Chen J, Wang L, Cao J, Xu L (2017) Chemical composition and biological activities of the essential oil from Rubus pungens var. oldhamii. Nat Prod Res 31:1454–1458. https://doi.org/10.1080/14786419.2016.1253076
Zhou R, Yang H, Lu T, Zhao Y, Zheng W (2022) Ultraviolet radiation promotes the production of hispidin polyphenols by medicinal mushroom Inonotus obliquus. Fungal Biol 126:775–785. https://doi.org/10.1016/j.funbio.2022.10.001
Zia-UI-Haq M, Riaz M, De Feo V, Jaafar HZE, Moga M (2014) Rubus fruticosus L.: constituents, biological activities, and health related uses. Mol 19:10998–11029. https://doi.org/10.3390/molecules190810998
Zuo L, Wijegunawardana D (2021) Redox role of ROS and inflammation in pulmonary diseases. In: Wang YX (ed) Lung inflammation in health and disease, volume II Advances in Experimental Medicine and Biology, vol 1304. Springer, Cham. https://doi.org/10.1007/978-3-030-68748-9_11
Acknowledgements
We want to thank Professor Karla Slowing from the Department of Pharmacology, Pharmacognosy and Botany, Faculty of Pharmacy, Complutense University of Madrid for her support in the initial phase of researching these plant species.
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This work was supported by the Fundación de la Universidad Autónoma de Madrid (FUAM).
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BHP and LAT: phytochemical analysis of the extracts; LAT and BHP: biological analysis of the extracts; LAT, BHP, and ARS: writing and editing of the manuscript and the figures. All the authors read and approved the final manuscript.
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Apaza Ticona, L., Hervás Povo, B. & Rumbero Sánchez, Á. Spectroscopical Analysis of Andean Plant Species with Anti-inflammatory, Antioxidant, and Antibacterial Activities. Rev. Bras. Farmacogn. 34, 135–153 (2024). https://doi.org/10.1007/s43450-023-00469-5
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DOI: https://doi.org/10.1007/s43450-023-00469-5