Abstract
Malva parviflora is used as food in the gastronomy of some regions of Mexico and, also, in Mexican traditional medicine for inflammation-related conditions like rheumatoid arthritis. The objective of this work was to evaluate its antiarthritic activity in a mice model. In ICR, female mice were tested the dichloromethane extract (MpD) and fractions MpF4 (extracted with a dichoromethane:methanol system) and MpFphy (a precipitate by acetone:methanol) by using the mono-arthritis with kaolin/carrageenan model. During the treatment, joint inflammation was measured daily, and hyperalgesia was measured using the hot plate test. The treatments diminished both joint inflammation and pain. At the end of the evaluation, the left joint and spleen were extracted for determination of pro- and anti-inflammatory cytokines. The results showed that the MpD, MpF4, and MpFphy treatments modulated the concentration of these proteins. Specifically, MpFphy at 1.0 mg/kg increased IL-4 and IL-10 and decreased IL-17, IL-1β, and TNF-α. GC-MS analysis showed that MpF4 contained a mixture of a total of nine compounds, three of them newly reported for the species. The studies confirmed the presence of five sterols in the MpFphy fraction, including stigmasterol and β-sitosterol. These results confirm the anti-rheumatoid and anti-inflammatory activities of a fraction rich in sterols from Malva parviflora.
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Abbreviations
- RA:
-
Rheumatoid arthritis
- TNF-α:
-
Tumoral necrosis factor
- TGF-β:
-
Transforming growth factor
- MTX:
-
Methotrexate
- PMFS:
-
Phenylmethylsulphonyl fluoride
- IL:
-
Interleukin
- TPA:
-
12-O-Tetradecanoylphorbol-13-acetate
- LK:
-
Left knee
- MpD:
-
Dichloromethane extract from Malva parviflora
- MpF4:
-
Fraction F4 from Malva parviflora
- MpFphy:
-
Sterols fraction from Malva parviflora
References
Adeosun TE, Ogunwande IA, Avoseh ON, Rajj IP, Lawal OA (2017) Composition and anti-inflammatory activity of essential oil of Jatropha curcas. Nat Prod Commun 12:439–440. https://doi.org/10.1177/1934578X1701200333
Afolayan AJ, Aboyade OM, Adedapo AA, Sofidiya MO (2010) Anti-inflammatory and analgesic activity of the methanol extract f Malva parviflora Linn (Malvaceae) in rats. Afr J Biotechnol 9:1225–1229. https://doi.org/10.5897/AJB09.838
Alkabeya HA, Hughes AM, Adams J (2019) Factors associated with hand and upper arm functional disability in people with rheumatoid arthritis: a systematic review. Arthritis Care Res 71:1473–1481 https://www.ncbi.nlm.nih.gov/pubmed/30320976
Argueta A, Cano L, Rodarte M (1994) Atlas de las Plantas de la Medicina Tradicional Mexicana. Instituto Nacional Indigenista, México D.F., pp 943–947
Atolani O, Oguntoye H, Areh ET, Adeyemi ET, Kambizi L (2019) Chemical composition, anti-toxoplasma, cytotoxicity, antioxidant, and anti-inflammatory potentials of Cola gigantea seed oil. Pharm Biol 57:154–160. https://doi.org/10.1080/13880209.2019.1577468
Bouriche H, Mexiti H, Senator A (2010) In Vivo anti-inflammatory and antioxidant effects of Malva parviflora leaf extracts. Acta Hortic 854:23–30 https://www.researchgate.net/publication/283584995_In_vivo_anti-inflammatory_and_antioxidant_effects_of_Malva_parviflora_leaf_extracts
Bouriche H, Meziti H, Senator A, Arnhold J (2011) Anti-inflammatory, free radical-scavenging, and metal-chelating activities of Malva parviflora. Pharm Biol 49:492–496. https://doi.org/10.3109/13880209.2011.558102
Burmester GR, Feist E, Dörner T (2014) Emerging cell and cytokine targets in rheumatoid arthritis. Nat Rev Rheumatol 10:77–88 https://www.ncbi.nlm.nih.gov/pubmed/24217582
Castro-Lara D, Basurto-Peña F, Mera-Ovando L, Bye-Boettler R (2011) Los quelites, tradición milenaria en México. ISBN: 978-607-12-0202-4. Universidad Autónoma Chapingo, Texcoco, Estado de México. http: https://www.gob.mx/cms/uploads/attachment/file/231814/Los_quelites_una_tradicion_milenaria_en_mexico.pdf
Chu J, Wang X, Bi H, Ren M, Wang J (2018) Dihydromyricetin relieves rheumatoid arthritis symptoms and suppresses expression of pro-inflammatory cytokines via the activation of Nrf2 pathway in rheumatoid arthritis model. Int Immunopharmacol 59:174–180. https://doi.org/10.1016/j.intimp.2018.04.001
Davies R, Hyrich K (2018) Biologics registers in rheumatoid arthritis. Medicine 46:243–246. https://doi.org/10.1016/j.mpmed.2018.01.001
dos Reis CM, da Rosa BV, da Rosa GP, do Carmo G, Barassuol LM, Andrade G, Kuhn KR, Farias A, Jahn SL, Kuhn RC (2019) Antifungal and antibacterial activity of extracts produced from Diaporthe schini. J Biotechnol 294:30–37. https://doi.org/10.1016/j.jbiotec.2019.01.022
Eman A-S, Haidy AG, Mohamed E-S, Mohamed MA-D, Abdel NS (2018) Anti-inflammatory and analgesic activities of cupressuflavone from Cupressus macrocarpa: impact on pro-inflammatory mediators. Drug Dev Res 79:22–28. https://doi.org/10.1002/ddr.21417
Espejo EF, Mir D (1994) Differential effects of weekly and daily exposure to the hot plate on the rat’s behavior. Physiol Behav 55:1157–1162. https://doi.org/10.1016/0031-9384(94)90404-9
Feldmann M, Maini SR (2008) Role of cytokines in rheumatoid arthritis: an education in pathophysiology and therapeutics. Immunol Rev 223:7–19. https://doi.org/10.1111/j.1600-065X.2008.00626.x
Fox DA, Gizinski A, Morgan R, Lundy SK (2010) Cell-cell interactions in rheumatoid arthritis synovium. Rheum Dis Clin N Am 36:311–323 https://www.ncbi.nlm.nih.gov/pubmed/20510236
Frisell T, Saevarsdottir S, Askling J (2016) Family history of rheumatoid arthritis: an old concept with new developments. Nat Rev Rheumatol 12:335–343 https://www.ncbi.nlm.nih.gov/pubmed/27098907
Gihan A, Shoubaky E, Mohamed MA-D, Mohamed HM, Essam AS (2016) Isolation and identification of a flavone apigenin from marine red alga Acanthophora spicifera with antinociceptive and anti-inflammatory activities. J Exp Neurosci 10:21–29. https://doi.org/10.4137/JEN.S25096
Hoxha M (2018) A systematic review on the role of eicosanoid pathways in rheumatoid arthritis. Adv Med Sci 63:22–29. https://doi.org/10.1016/j.advms.2017.06.004
Huang B, Chu Z, He W, Qin L (2011) Chemical composition, anti-inflammatory analgesic activities of the petrol ether extract of Pinellia cordata. Afr J Biotechnol 10:11023–11027. https://doi.org/10.5897/AJB11.332
Huhtakangas JA, Veijola J, Turunen S, Karjalainen A, Valkealahti M, Nousiainen T, Yli-Luukko S, Vuolteenaho O, Lehenkari P (2017) Cytokine data obtained from synovial stromal cells of patients with rheumatoid arthritis or osteoarthritis. Data Brief 12:593–602. https://doi.org/10.1016/j.dib.2017.04.041
Kannan K, Ortmann RA, Kimpel D (2005) Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology 12:167–181. https://doi.org/10.1016/j.pathophys.2005.07.011
Lagunas-Herrera H, Tortoriello J, Herrera-Ruiz M, Martínez-Hernández GB, Zamilpa A, Aguilar L, García M, Lombardo-Hearl G, Jiménez-Ferrer E (2019) Acute and chronic antihypertensive effect of fractions, tiliroside and scopoletin from Malva parviflora. Biol Pharm Bull 42:18–25 https://www.ncbi.nlm.nih.gov/pubmed/30606987
Langford DJ, Mogil JS (2008) Pain testing in the laboratory mouse. In: Fish RE, Brown MJ, Danneman PJ, Karas AZ, (Eds.), Anesthesia and Analgesia in Laboratory Animals. Academic Press, pp. 549–560. https://doi.org/10.1016/B978-012373898-1.50027-9
Li L, Wu J, Ting-Han H, Lu-Ping Q (2008) Chemical composition of the essential oil and ether extract from Rhytidium rugosum. Chem Nat Compd 44:797–799. https://doi.org/10.1007/s10600-009-9172-x
Li HJ, Zhang CT, Du H, Xu T, Li Q, Wang P, Fang G, Fan G (2019) Chemical composition of Bawei Longzuan granule and its anti-arthritic activity on collagen-induced arthritis in rats by inhibiting inflammatory responses. Chem Biodivers 16:e1900294. https://doi.org/10.1002/cbdv.201900294
Littlejohn EA, Monrad SU (2018) Early diagnosis and treatment of rheumatoid arthritis. Prim Care 45:237–255. https://doi.org/10.1016/j.pop.2018.02.010
Maddur MS, Miossec P, Kaveri SV, Bayry J (2012) Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol 181:8–18. https://doi.org/10.1016/j.ajpath.2012.03.044
McGonagle D, Watad A, Savic S (2018) Mechanistic immunological based classification of rheumatoid arthritis. Autoimmun Rev 17:1115–1123. https://doi.org/10.1016/j.autrev.2018.06.001
McInnes IB, Schett G (2011) The pathogenesis of rheumatoid arthritis. N Engl J Med 365:2205–2219 https://www.ncbi.nlm.nih.gov/pubmed/22150039
McNamee KE, Alzabin S, Anand JP, Feldmann M, Williams RO, Inglis JJ (2011) IL-17 induces hyperalgesia via TNF-dependent neutrophil infiltration. Pain 152:1838–1845. https://doi.org/10.1016/j.pain.2011.03.035
Milind MM, Eugene K, Jason JM (2016) Preclinical assessment of inflammatory pain. CNS Neurosci Ther 22:88–101. https://doi.org/10.1111/cns.12486
Moreno-Anzúres NE, Marquina S, Alvarez L, Zamilpa A, Castillo-España P, Perea-Arango I, Torres PN, Herrera-Ruiz M, Díaz ER, García JT, Arellano-García J (2017) Acytotoxic and anti-inflammatory campesterol derivative from genetically transformed hairy roots of Lopezia racemosa Cav. (Onagraceae). Molecules 22:118. https://doi.org/10.3390/molecules22010118
Nouran MF, Eman A-S, Mohamed MA-D, Abdel NS (2017) Anti-inflammatory and analgesic activities of Terminalia muelleri Benth. (Combretaceae). Drug Dev Res 78:146–154. https://doi.org/10.1002/ddr.21385
Pan R, Gao XH, Li Y, Xia YF, Dai (2010) Anti-arthritic effect of scopoletin, a coumarin compound occurring in Erycibe obtusifolia Benth stems, is associated decreased angiogenesis in synovium. Fundam Clin Pharmacol 24:477–490. https://doi.org/10.1111/j.1472-8206.2009.00784.x
Plone MA, Emerich DF, Lindner MD (1996) Individual differences in the hot-plate test and effects of habituation on sensitivity to morphine. Pain 66:265–270. https://doi.org/10.1016/0304-3959(96)03048-5
Ramírez-Serrano CE, Jiménez-Ferrer E, Herrera-Ruiz M, Zamilpa A, Vargas-Villa G, Ramírez RJ, Chavarría A, Tortoriello J, Pedraza G, Perez-Martínez L (2019) A Malva parviflora’s fraction prevents the deleterious effects resulting from neuroinflammation. Biomed Pharmacother 118:109349
Rasheed H, Afridi R, Khan AU, Ullah MZ, Khalid S, Atiq A, Ahmed MN, Kim YS, Khan S (2018) Anti-inflammatory, anti-rheumatic and analgesic activities of 2-(5-mercapto-1,3,4-oxadiazol-2-yl)-N-propylbenzenesulphonamide (MOPBS) in rodents. Inflammopharmacology 26:1037–1049. https://doi.org/10.1007/s10787-018-0446-4
Rout SP, Kar DM (2014) Identification of chemical compounds present in different fractions of Annona reticulata L. leaf by using GC-MS. Nat Prod Res 28:1786–1788. https://doi.org/10.1080/14786419.2014.939084
Rzedowski G (2001) Flora fanerogámica del Valle de México. 2da. Edición. Instituto de Ecología y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Pátzcuaro Michoacán
Sakaki H, Matsumiya T, Kusumi A, Imaizumi T, Satoh H, Yoshida H, Satoh K, Kimura H (2004) Interleukin-1beta induces matrix metalloproteinase-1 expression in cultured human gingival fibroblasts: role of cyclooxygenase-2 and prostaglandin E2. Oral Dis 10:87–93. https://doi.org/10.1046/j.1354-523X.2003.00982.x
Salinas-Sánchez DO, Jiménez-Ferrer E, Sánchez-Sánchez V, Zamilpa A, González-Cortazar M, Tortoriello J, Herrera-Ruiz M (2017) Anti-inflammatory activity of polymeric proanthocyanidin from Serjania schiedeana. Molecules 22:863. https://doi.org/10.3390/molecules22060863
Sánchez-Ramón S, López-Longo FJ, Carreño L (2011) Interleukins network in rheumatoid arthritis pathophysiology: beyond proinflammatory cytokines. Reumatol Clín 6:S20–S24. https://doi.org/10.1016/j.reuma.2010.11.010
Shale TL, Stirk WA, van Staden J (2005) Variation in antibacterial and anti-inflammatory activity of different growth forms of Malva parviflora and evidence for synergism of the anti-inflammatory compounds. J Ethnopharmacol 96:325–330. https://doi.org/10.1016/j.jep.2004.09.032
Sluka KA, Bailey K, Bogush J, Olson R, Ricketts A (1998) Treatment with either high or low frequency TENS reduces the secondary hyperalgesia observed after injection of kaolin and carrageenan into the knee joint. Pain 77:97–102 https://insights.ovid.com/article/00006396-199807000-00012
Smith JB, Haynes MK (2002) Rheumatoid arthritis- a molecular understanding. Ann Intern Med 136:908–922 https://annals.org/aim/article-abstract/715345/rheumatoid-arthritis-molecular-understanding
Suh HR, Chung HJ, Park EH, Moon SW, Park SJ, Park CW, Kim YI, Han HC (2016) The effects Chamaecyparis obtusa essential oil pain-related behavior and expression of pro-inflammatory cytokines in carrageenan-induced arthritis in rats. Biosci Biotechnol Biochem 80:203–209. https://doi.org/10.1080/09168451.2015.1075864
Sur B, Kang S, Kim M, Oh S (2019) Inhibition of carrageenan/kaolin-induced arthritis in rats and of inflammatory cytokine expressions in human IL-1β-stimulated fibroblast like synoviocytes by a benzylideneacetophenone derivative. Inflammation 42:928–936. https://doi.org/10.1007/s10753-018-0947-8
World Health Organization, Chronic diseases and health promotion, (2019) (Accessed February 18,2019), https://www.who.int/chp/topics/rheumatic/en/
Zhao CH, Zhao C, Ye HQ, Xi CY, Zou XP, Zhou XH, Hou PP, Zhang TH (2019) Hypolipidemic activity of low-cholesterol ovum oil of Rana chensinensis and phytosterol (stigmasterol) in rats. J Zhejiang Univ Sci B 20:613–616. https://doi.org/10.1631/jzus.B1900018
Zonzini JB, Barros BM, Silva NC, de Morais BC, Sachetto Z, Davitt M, de Paiva ME (2018) Disease-related outcomes influence prevalence of fall in people with rheumatoid arthritis. Ann Phys Rehabil Med 62:84–91. https://doi.org/10.1016/j.rehab.2018.09.003
Author contribution statement
Animal experiments: M-HGB, V-VG, G-AMP; experimental design, statistical analysis: H-RM, J-FE, R-RR; manuscript preparation: H-RM, M-HGB, V-VG, J-FE; chemical analysis: ZA, G-CM; taxonomic preparation: A-FM, F-MM;
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This work was partially financially supported by FIS/IMSS/PROT/G15/1426
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Martínez-Hernández, G.B., Vargas-Villa, G., Jiménez-Ferrer, E. et al. Anti-arthritic and anti- inflammatory effects of extract and fractions of Malva parviflora in a mono- arthritis model induced with kaolin/carrageenan. Naunyn-Schmiedeberg's Arch Pharmacol 393, 1281–1291 (2020). https://doi.org/10.1007/s00210-020-01851-z
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DOI: https://doi.org/10.1007/s00210-020-01851-z