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Planta Med 2024; 90(03): 243-251
DOI: 10.1055/a-2212-0262
Biological and Pharmacological Activity
Original Papers

Polyphenols, Antioxidants, and Wound Healing of Lecythis pisonis Seed Coats

Elisângela Flávia Pimentel
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
,
Bruno Gomes de Oliveira
3   Federal Institute of Espírito Santo, Vila Velha, Brazil
,
Ana Claudia Hertel Pereira 
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
,
Mariana Moreira Figueira
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
,
Danielle Braga Portes
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
,
Rodrigo Scherer
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
,
Fabiana Gomes Ruas
2   Capixaba Institute for Research, Technical Assistance, and Rural Extension, Vitoria, Brazil
,
Wanderson Romão
3   Federal Institute of Espírito Santo, Vila Velha, Brazil
,
Márcio Fronza
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
,
Denise Coutinho Endringer 
1   Pharmaceutical Science Graduate Program, Vila Velha University, Vila Velha, ES, Brazil
› Author AffiliationsThe Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brasil (CNPq), PQ, Fundação Estadual de Amparo à Pesquisa do Estado do Espírito Santo (FAPES), grant number TO # 432665/2016 and #2019/2019, and the Coordination for the Improvement of Higher Education Personnel (Capes), Finance Code 001, are acknowledged for funding this study and fellowship support.
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Abstract

To better use the Lecythis pisonis Cambess. biomass, this study investigates whether Sapucaia seed coats present wound healing properties. We analyzed the antibacterial, antioxidant, and wound healing-promoting potentials, plus cytotoxicity and stimulation of vascular endothelial growth factor-A. The chemical composition was analyzed by positive ion mode electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. A total of 19 compounds were identified, such as proanthocyanidin A1, procyanidins A1, B2, and C1, epigallocatechin, and kaempferol (p-coumaroyl) glycoside. Potent antioxidant strength/index was verified for 2,2-diphenyl-1-picrylhydrazyl radical (IC50 = 0.99 µg/mL) and ferric reducing antioxidant power (IC50 = 1.09 µg/mL). The extract did not present cytotoxicity and promoted significant cell migration and/or proliferation of fibroblasts (p < 0.05). Vascular endothelial growth factor-A was stimulated dose-dependently at 6 µg/mL (167.13 ± 8.30 pg/mL), 12.5 µg/mL (210.3 ± 14.2 pg/mL), and 25 µg/mL (411.6 ± 29.4 pg/mL). Platelet-derived growth factor (PDGF) (0.002 µg/mL) was stimulated at 215.98 pg/mL. Staphylococcus aureus was susceptible to the extract, with a minimum inhibitory concentration of 31.25 µg/mL. The identified compounds benefit the antioxidant activity, promoting hemostasis for the wound healing process, indicating that this extract has the potential for use in dermatological cosmetics.

Key words

Lecythis pisonis Cambess - Lecythidaceae - chemical analysis - wound healing

Supporting Information

    Chemical compounds identified by ESI(+)FT-ICR MS of the ethanolic extract of seed coats from nuts of L. pisonis are available as Supporting Information.

  • Supporting Information


Publication History

Received: 19 January 2023

Accepted after revision: 15 November 2023

Accepted Manuscript online:
16 November 2023

Article published online:
10 January 2024

© 2023. Thieme. All rights reserved.

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  • References

  • 1 Vallilo MI, Tavares M, Aued-Pimentel S, Campos NC, Moita Neto JM. Lecythis pisonis Cambess. Camb. nuts: Oil characterization, fatty acids, and minerals. Food Chem 2009; 66: 197-200
    CrossrefPubMedGoogle Scholar
  • 2 Brandão MS, Pereira SS, Lima DF, Oliveira JPC, Ferreira ELF, Chaves MH, Almeida FRC. Antinociceptive effect of Lecythis pisonis Cambess. Camb. (Lecythidaceae) in models of acute pain in mice. J Ethnopharmacol 2013; 146: 180-186
    CrossrefPubMedGoogle Scholar
  • 3 Silva LL, Gomes BS, Sousa-Neto BP, Oliveira JPC, Ferreira ELF, Chaves MH, Oliveira FA. Effects of Lecythis pisonis Camb. (Lecythidaceae) in a mouse model of pruritus. J Ethnopharmacol 2012; 139: 90-97
    CrossrefPubMedGoogle Scholar
  • 4 Vidal Martins M, Montezano de Carvalho I, Caetano MMM, Toledo RCL, Xavier AA, Queiroz JH. Sapucaia nuts (Lecythis pisonis Cambess.) modulate the hepatic inflammatory and antioxidant metabolism activity in rats fed high-fat diets. African J Biotechnol 2016; 5: 1375-1382
    PubMedGoogle Scholar
  • 5 Ferria T, Cociolia F, Lucab C, Callegaric CV, Morabitod R. Distribution and speciation of selenium in Lecythis ollaria plant. Microchem J 2004; 78: 195-203
    CrossrefPubMedGoogle Scholar
  • 6 Gosain A, DiPietro LA. Aging and wound healing. World J Surg 2004; 8: 321-326
    CrossrefPubMedGoogle Scholar
  • 7 Trinh XT, Long NV, Van Anh LT, Nga PT, Giang NN, Chien PN, Nam SY, Heo CY. A comprehensive review of natural compounds for wound healing: Targeting bioactivity perspective. Int J Mol Sci 2022; 23: 9573
    CrossrefPubMedGoogle Scholar
  • 8 Chow O, Barbul A. Immunonutrition: Role in wound healing and tissue regeneration. Adv Wound Care (New Rochelle) 2014; 1: 46-53
    CrossrefPubMedGoogle Scholar
  • 9 Gonzalez A, Costa T, Andrade Z, Medrado A. Wound healing – A literature review. An Bras Dermatol 2016; 91: 614-620
    CrossrefPubMedGoogle Scholar
  • 10 Boucher JM, Clark RP, Chong DC, Citrin KM, Wylie LA, Bautch VL. Dynamic alterations in decoy VEGF receptor-1 stability regulate angiogenesis. Nat Commun 2017; 8: 15699
    CrossrefPubMedGoogle Scholar
  • 11 Kurahashi T, Fujii J. Roles of antioxidative enzymes in wound healing. J Dev Biol 2015; 3: 57-70
    CrossrefPubMedGoogle Scholar
  • 12 Mohammadinejad R, Shavandi A, Raie DS, Sangeetha J, Soleimani M, Hajibehzad SS, Thangadurai D, Hospet R, Popoola JO, Arzani A, Gómez-Lim MA, Siavash I, Varma RS. Plant molecular farming: Production of metallic nanoparticles and therapeutic proteins using green factories. Green Chem 2019; 21: 1845
    CrossrefPubMedGoogle Scholar
  • 13 Soleimani M, Arzani A, Arzani V, Roberts TH. Phenolic compounds and antimicrobial properties of mint and thyme. J Herb Med 2022; 36: 100604
    CrossrefPubMedGoogle Scholar
  • 14 Chokotho L, Van Hasselt E. The use of tannins in the local treatment of burn wounds – a pilot study. Malawi Med J 2015; 1: 19-20
    PubMedGoogle Scholar
  • 15 Pereira ACH, Ribeiro LO, Pimentel EF, Ruasb FG, Ventura JA, Endringer DC. Stability of a natural-based cream containing Lecythis pisonis extract. J Cosmet Sci 2021; 71: 155-162
    PubMedGoogle Scholar
  • 16 Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal Biochem 1996; 239: 70-76
    CrossrefPubMedGoogle Scholar
  • 17 Aligiannis N, Kalpoutzakis E, Mitaku S, Chinou IB. Composition and antibacterial activity of the essential oils of two Origanum species. J Agric Food Chem 2001; 49: 4168-4170
    CrossrefPubMedGoogle Scholar
  • 18 Marquez A, Serratosa MP, Merida J. Pyranoanthocyanin derived pigments in wine: Structure and formation during winemaking. J Chem 2013; 2013: 1-15
    CrossrefPubMedGoogle Scholar
  • 19 He WJ, Fu ZH, Zeng GZ, Zhang YM, Han HJ, Yan H, Ji CJ, Chu HB, Tan NH. Terpene and lignan glycosides from the twigs and leaves of an endangered conifer, Cathaya argyrophylla . Phytochemistry 2012; 83: 63-69
    CrossrefPubMedGoogle Scholar
  • 20 Huis R, Morreel K, Fliniaux O, Lucau-Danila A, Fénart S, Grec S, Neutelings G, Chabbert B, Mesnard F, Boerjan W, Hawkins S. Natural hypolignification is associated with extensive oligolignol accumulation in flax stems. Plant Physiol 2012; 158: 1893-1915
    CrossrefPubMedGoogle Scholar
  • 21 Nonaka GI, Morimoto S, Kinjo JE, Nohara T, Nishioka I. Tannins and related compounds. L structures of proanthocyanidin A-1 and related compounds. Chem Pharm Bull (Tokyo) 1987; 35: 149-155
    CrossrefPubMedGoogle Scholar
  • 22 De Taeye C, Cibaka MK, Collin S. Occurrence and antioxidant activity of C1 degradation products in Cocoa. Foods 2017; 6: 18
    CrossrefPubMedGoogle Scholar
  • 23 Chen TH, Huang YH, Lin JJ, Liau BC, Wang SY, Wu YC, Jong TT. Cytotoxic lignan esters from Cinnamomum osmophloeum . Planta Med 2010; 76: 613-619
    Article in Thieme ConnectPubMedGoogle Scholar
  • 24 Delcambre A, André Y, Saucier C. Sequencing of red wine proanthocyanidins by UHPLC-ESI-Q-ToF. J Appl Bioanal 2015; 1: 46-54
    CrossrefPubMedGoogle Scholar
  • 25 Wu YQ, Li YA, Lin XF, Liu ZL, Li YU. Phenolic compounds from Anaphalis aureo-punctata . Pharmazie 2002; 58: 833-835
    PubMedGoogle Scholar
  • 26 Kamiya K, Watanabe C, Endang H, Umar M, Satake T. Studies on the constituents of the bark of Parameria laevigata Moldenke. Chem Pharm Bull (Tokyo) 2001; 49: 551-557
    CrossrefPubMedGoogle Scholar
  • 27 Dudek MK, Gliński VB, Davey MH, Sliva D, Kaźmierski S, Gliński JA. Trimeric and tetrameric A-type procyanidins from peanut skins. J Nat Prod 2017; 80: 415-426
    CrossrefPubMedGoogle Scholar
  • 28 Różalska B, Sadowska B, Żuchowski J, Więckowska-Szakiel M, Budzyńska A, Wójcik U, Stochmal A. Phenolic and nonpolar fractions of Elaeagnus rhamnoides (L.) A. Nelson extracts as virulence modulators–In Vitro study on bacteria, fungi, and epithelial cells. Molecules 2018; 23: 1498
    CrossrefPubMedGoogle Scholar
  • 29 Hosny M, Rosazza JPN. Novel isoflavone, cinnamic acid, and triterpenoid glycosides in soybean molasses. J Nat Prod 1999; 62: 853-858
    CrossrefPubMedGoogle Scholar
  • 30 Scherer R, Godoy HT. Antioxidant activity index (AAI) by the 2,2-diphenyl-1-picrylhydrazyl method. Food Chem 2009; 112: 654-658
    CrossrefPubMedGoogle Scholar
  • 31 Çaliş İ, Şatana ME, Yürüker A, Demirdamar R, Alaçam R, Tanker N, Rüegger H, Sticher O. Triterpene saponins from cyclamen mirabile and their biological activities. J Nat Prod 1997; 60: 315-318
    CrossrefPubMedGoogle Scholar
  • 32 Nakashima S, Oda C, Masuda S, Tagashira M, Kanda T. Isolation and structure elucidation of tetrameric procyanidins from unripe apples (Malus pumila cv. Fuji) by NMR spectroscopy. Phytochemistry 2012; 83: 144-152
    CrossrefPubMedGoogle Scholar
  • 33 Rockenbac II, Jungfer E, Ritter C, Santiago-Schübel B, Thiele B, Fett R, Galensa R. Characterization of flavan-3-ols in seeds of grape pomace by CE, HPLC-DAD-MSn and LC ESI-FTICR-MS. Food Res Int 2012; 48: 848-855
    CrossrefPubMedGoogle Scholar
  • 34 Pandey KB, Rizvi SI. Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2009; 2: 270-278
    CrossrefPubMedGoogle Scholar
  • 35 Tanaka T, Matsuo Y, Kouno I. Chemistry of secondary polyphenols produced during processing of tea and selected foods. Int J Mol Sci 2009; 11: 14-40
    CrossrefPubMedGoogle Scholar
  • 36 Plumb GW, De Pascual-Teresa S, Santos-Buelga C, Cheynier V, Williamson G. Antioxidant properties of catechins and proanthocyanidins: Effect of polymerization, galloylation, and glycosylation. Free Radic Res 1998; 29: 351-358
    CrossrefPubMedGoogle Scholar
  • 37 Kamala A, Middha S, Gopinath C, Sindhura H, Karigar C. In vitro antioxidant potentials of Cyperus rotundus L. rhizome extracts and their phytochemical analysis. Pharmacogn Mag 2014; 14: 261
    PubMedGoogle Scholar
  • 38 Kisseih E, Lechtenberg M, Petereit F, Sendker J, Zacharski D, Brandt S, Agyare C, Hensel A. Phytochemical characterization and in vitro wound healing activity of leaf extracts from Combretum mucronatum Schum. & Thonn.: Oligomeric procyanidins as strong inductors of cellular differentiation. J Ethnopharmacol 2015; 174: 628636
    CrossrefPubMedGoogle Scholar
  • 39 Jiao Y, Wang Y, Guo S, Wang G. Glutathione peroxidases as oncotargets. Oncotarget 2017; 8: 80093-80102
    CrossrefPubMedGoogle Scholar
  • 40 Ahmad S, Arshad M, Azam R. Review on methods used to determine antioxidant activity. Jezs 2014; 1: 4146
    PubMedGoogle Scholar
  • 41 Dos Santos C, Vargas Á, Fronza N, Dos Santos JHZ. Structural, textural and morphological characteristics of tannins from Acacia mearnsii encapsulated using sol-gel methods: Applications as antibacterial agents. Colloids Surf B Biointerfaces 2017; 151: 26-33
    CrossrefPubMedGoogle Scholar
  • 42 Li K, Diao Y, Zhang H, Wang S, Zhang Z, Yu B, Huang S, Yang H. Tannin extracts from immature fruits of Terminalia chebula Fructus Retz. promote cutaneous wound healing in rats. BMC Complement Altern Med 2011; 11: 86
    CrossrefPubMedGoogle Scholar
  • 43 Agência Nacional de Vigilância Sanitária. Farmacopeia Brasileira, Vol. 1, 6 ed. Brasília; Brasil: 2019
    Google Scholar
  • 44 Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1993; 65: 55-63
    CrossrefPubMedGoogle Scholar
  • 45 Fronza M, Heinzmann B, Hamburger M, Laufer S, Merfort I. Determination of the wound healing effect of Calendula extracts using the scratch assay with 3T3 fibroblasts. J Ethnopharmacol 2009; 12: 463-467
    CrossrefPubMedGoogle Scholar
  • 46 Goldman E, Green LH. Practical Handbook of Microbiology. 02. Boca Raton: CRC Press; 2008: 1-874 DOI: 10.1201/9781420009330
    CrossrefGoogle Scholar