Planta Med 2017; 83(06): 509-518
DOI: 10.1055/s-0042-117774
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Antiviral Activity of Crude Hydroethanolic Extract from Schinus terebinthifolia against Herpes simplex Virus Type 1

Samara Requena Nocchi
1   Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual de Maringá, Maringá, PR, Brazil
,
Mychelle Vianna Pereira Companhoni
1   Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual de Maringá, Maringá, PR, Brazil
,
João Carlos Palazzo de Mello
1   Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual de Maringá, Maringá, PR, Brazil
3   Departamento de Farmácia, Universidade Estadual de Maringá, Maringá, PR, Brazil
,
Benedito Prado Dias Filho
1   Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual de Maringá, Maringá, PR, Brazil
2   Departamento de Ciências Básicas da Saúde, Universidade Estadual de Maringá, Maringá, PR, Brazil
,
Celso Vataru Nakamura
1   Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual de Maringá, Maringá, PR, Brazil
2   Departamento de Ciências Básicas da Saúde, Universidade Estadual de Maringá, Maringá, PR, Brazil
,
Carlos Alexandre Carollo
4   Laboratório de Produtos Naturais e Espectrometria de Massas (LaPNEM), Centro de Ciências Biológicas e da Saúde (CCBS), Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande, MS, Brazil
,
Denise Brentan Silva
4   Laboratório de Produtos Naturais e Espectrometria de Massas (LaPNEM), Centro de Ciências Biológicas e da Saúde (CCBS), Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande, MS, Brazil
,
Tânia Ueda-Nakamura
1   Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Estadual de Maringá, Maringá, PR, Brazil
2   Departamento de Ciências Básicas da Saúde, Universidade Estadual de Maringá, Maringá, PR, Brazil
› Author Affiliations
Further Information

Publication History

received 29 April 2016
revised 02 September 2016

accepted 15 September 2016

Publication Date:
05 October 2016 (online)

Abstract

Herpes simplex virus infections persist throughout the lifetime of the host and affect more than 80 % of the humans worldwide. The intensive use of available therapeutic drugs has led to undesirable effects, such as drug-resistant strains, prompting the search for new antiherpetic agents. Although diverse bioactivities have been identified in Schinus terebinthifolia, its antiviral activity has not attracted much attention. The present study evaluated the antiherpetic effects of a crude hydroethanolic extract from the stem bark of S. terebinthifolia against Herpes simplex virus type 1 in vitro and in vivo as well as its genotoxicity in bone marrow in mammals and established the chemical composition of the crude hydroethanolic extract based on liquid chromatography-diode array detector-mass spectrometry and MS/MS. The crude hydroethanolic extract inhibited all of the tested Herpes simplex virus type 1 strains in vitro and was effective in the attachment and penetration stages, and showed virucidal activity, which was confirmed by transmission electron microscopy. The micronucleus test showed that the crude hydroethanolic extract had no genotoxic effect at the concentrations tested. The crude hydroethanolic extract afforded protection against lesions that were caused by Herpes simplex virus type 1 in vivo. Liquid chromatography-diode array detector-mass spectrometry and MS/MS identified 25 substances, which are condensed tannins mainly produced by a B-type linkage and prodelphinidin and procyanidin units.

Supporting Information

Chromatographic profiles and total ion chromatograms of the CHE of S. terebinthifolia, as well as the EC50 values of the CHE for different strains are available in Supporting Information.

 
  • References

  • 1 Vilarreal EC. Current and potential therapies for the treatment of herpesvirus infections. Prog Drug Res 2001; 56: 77-120
  • 2 Kukhanova MK, Korovina AN, Kochetkov SN. Human herpes simplex virus: life cycle and development of inhibitors. Biochemistry 2014; 79: 1635-1652
  • 3 Kopp SJ, Ranaivo HR, Wilcox DR, Karaba AH, Wainwright MS, Muller WJ. Herpes simplex virus serotype and entry receptor availability alter CNS disease in a mouse model of neonatal HSV. Pediatr Res 2014; 8: 528-534
  • 4 Cavalher-Machado SC, Rosas EC, Brito FA, Heringe AP, Oliveira RR, Kaplan MAC, Figueiredo MR, Henriques MD. The anti-allergic activity of the acetate fraction of Schinus terebinthifolius leaves in IgE induced mice paw edema and pleurisy. Int Immunopharmacol 2008; 8: 1552-1560
  • 5 Guerra MJM, Barreiro ML, Rodriguez ZM, Rubaiacaba Y. Actividad antimicrobiana de um extracto fluido al 80 % de Schinus terebinthifolius Raddi (copal). Rev Cubana Plant Med 2000; 5: 23-25
  • 6 Soares DGS, Oliveira CB, Leal C, Drumond MRS, Padilha WWN. Atividade antibacteriana in vitro da tintura de aroeira (Schinus terebinthifolius) na descontaminação de escovas dentais contaminadas pelo S. mutans . Pesq Bras Odontoped Clin Integr 2007; 7: 253-257
  • 7 De Lima MR, de Souza Luna J, dos Santos AF, de Andrade MC, SantʼAna AE, Genet JP, Marquez B, Neuville L, Moreau N. Anti-bacterial activity of some Brazilian medicinal plants. J Ethnopharmacol 2006; 105: 137-147
  • 8 Jorge LIF, Markmann BEO. Exame químico e microscópico de Schinus terebinthifolius Raddi (Aroeira). Rev Ciênc Farm (São Paulo) 1996; 17: 139-145
  • 9 Silva RAD. Pharmacopeia dos Estados Unidos do Brasil. 1. ed. São Paulo: Nacional; 1926
  • 10 DiCiaula MC, Lopes GC, Scarminio IS, Mello JCP. Optimization of solvent mixtures for extraction from bark of Schinus terebinthifolius by a statistical mixture-design technique and development of a UV-VIS spectrophotometric method for analysis of total polyphenols in the extract. Quim Nova 2014; 37: 158-163
  • 11 Scalbert A. Antimicrobial properties of tannins. Phytochemistry 1991; 30: 3875-3883
  • 12 Gescher K, Hensel A, Hafezi W, Derksen A, Kuhn J. Oligomeric proanthocyanidins from Rumex acetosa L. inhibit the attachment of herpes simplex virus type-1. Antiviral Res 2011; 89: 9-18
  • 13 Cheng HY, Lin CC, Lin TC. Antiherpes simplex virus type 2 activity of casuarinin from the bark of Terminalia arjuna Linn. Antiviral Res 2002; 55: 447-455
  • 14 Cheng HY, Lin TC, Yang CM, Wang KC, Lin LT, Lin CC. Putranjivain A from Euphorbia jolkini inhibits both virus entry and late stage replication of herpes simplex virus type 2 in vitro . J Antimicrob Chemother 2004; 53: 577-583
  • 15 Hassan STS, Masarcíková R, Berchová K. Bioactive natural products with anti-herpes simplex virus properties. J Pharm Pharmacol 2015; 67: 1325-1336
  • 16 Trentin DS, Silva DB, Frasson AP, Rzhepishevska O, Silva MV, Pulcini EL, James G, Soares GV, Tasca T, Ramstedt M, Giordani RB, Lopes NP, Macedo AJ. Natural green coating inhibits adhesion of clinically important bacteria. Scientific Reports 2015; DOI: 10.1038/srep08287.
  • 17 Mueller-Harvey I, McAllan AB. Tannins: their biochemistry and nutritional properties. Adv Plant Cell Biochem Biotechnol 1992; 1: 151-217
  • 18 Schofield P, Mbugua DM, Pell AN. Analysis of condensed tannins: a review. Anim Feed Sci Technol 2001; 91: 21-40
  • 19 Li HJ, Deinzer ML. Tandem mass spectrometry for sequencing proanthocyanidins. Anal Chem 2007; 79: 1739-1748
  • 20 Jaiswal R, Jayasinghe L, Kuhnert N. Identification and characterization of proanthocyanidins of 16 members of the Rhododendron genus (Ericaceae) by tandem LC–MS. J Mass Spectrom 2012; 47: 502-551
  • 21 Guaratini T, Armelini AI, Ferrari CR, Schefer RR, Placeres Neto A, Navas R, Reigad JB, Silva DB. Application of matrix-assisted laser-desorption/ionization time-of-flight LIFT for identification of cocoa condensed tannins. J Mass Spectrom 2014; 49: 251-255
  • 22 Gu L, Kelm MA, Hammerstone JF, Zhang Z, Beecher G, Holden J, Haytowitz D, Prior RL. Liquid chromatographic/electrospray ionization mass spectrometric studies of proanthocyanidins in foods. J Mass Spectrom 2003; 38: 1272-1280
  • 23 Nocchi SR, Moura-Costa GF, Novello CR, Rodrigues J, Longhini R, Mello JCP, Filho BP, Nakamura CV, Ueda-Nakamura T. In vitro cytotoxicity and anti-herpes simplex virus type 1 activity of hydroethanolic extract, fractions, and isolated compounds from stem bark of Schinus terebinthifolius Raddi. Pharmacogn Mag 2016; 12: 160-164
  • 24 Hong W, Li T, Song Y, Zhang R, Zeng Z, Han S, Zhang X, Wu Y, Li W, Cao Z. Inhibitory activity and mechanism of two scorpion venom peptides against herpes simplex virus type 1. Antiviral Res 2014; 102: 1-10
  • 25 Ruiz AR, De la Torre RA, Alonso N, Villaescusa A, Betancourt J, Vizoso A. Screening of medicinal plants for induction of somatic segregation activity in Aspergillus nidulans . J Ethnopharmacol 1996; 52: 123-127
  • 26 De Carvalho MC, Barca FN, Agnez-Lima LF, de Medeiros SR. Evaluation of mutagenic activity in an extract of pepper tree stem bark (Schinus terebinthifolius Raddi). Environ Mol Mutagen 2003; 42: 185-191
  • 27 Varela-Barca FN, Agnez-Lima LF, de Medeiros SR. Base excision repair pathway is envolved in the repair of lesions generated by flavonoid-enriched fractions of pepper tree (Schinus terebinthifolius Raddi) stem bark. Environ Mol Mutagen 2007; 48: 672-681
  • 28 Brasil. Ministério da Saúde. Anvisa – Agência Nacional de Vigilância Sanitária. Resolução RE No. 90. Guia para a realização de estudos de Toxicidade Pré-Clínica de Fitoterápicos [Guide to the studies of Preclinical Toxicity of Herbal Medicines]. Brasilia: ANVISA; 2004
  • 29 Cheng YW, Lee WW, Li CH, Lee CC, Kang JJ. Genotoxicity of motorcycle exhaust particles in vivo and in vitro . Toxicol Sci 2004; 81: 103-111
  • 30 Winter MJ, Ellis LCJ, Hutchinson TH. Formation of micronuclei in erythrocytes of the fathead minnow (Pimephales promelas) after acute treatment with mitomycin C or cyclophosphamide. Mutat Res 2007; 629: 89-99
  • 31 Herald TJ, Gadgil P, Tilley M. High-throughput micro plate assays for screening flavonoid content and DPPH-scavenging activity in sorghum bran and flour. J Sci Food Agric 2012; 92: 2326-2331
  • 32 Camargo-Filho I, Cortez DAG, Ueda-Nakamura T, Nakamura CV, Filho BP. Antiviral activity and mode of action of a peptide isolated from Sorghum bicolor . Phytomedicine 2008; 15: 202-208
  • 33 Cheng HY, Lin TC, Yang CM, Wang KC, Lin CC. Mechanism of action of the suppression of herpes simplex virus type 2 replication by pterocarnin A. Microbes Infect 2004; 6: 738-744
  • 34 Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58: 621-681
  • 35 Odds FC. Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 2003; 52: 1
  • 36 Cardozo FT, Camelini CM, Mascarello A, Rossi MJ, Nunes RJ, Barardi CRM, Mendonça MM, Simões CMO. Antiherpetic activity of a sulfated polisaccharide from Agaricus brasiliensis mycelia. Antiviral Res 2011; 92: 108-114
  • 37 Costa MA, Ishida K, Kaplum V, Koslyk EDA, Mello JCP, Ueda-Nakamura T, Dias Filho BP, Nakamura CV. Safety evaluation of proanthocyanidin polymer-rich fraction obtained from stem bark of Stryphnodendron adstringens (BARBATIMÃO) for use as a pharmacological agent. Regul Toxicol Pharmacol 2010; 58: 330-335
  • 38 Vilar JB, Ferreira FL, Ferri PH, Guillo LA, Chen Chen L. Assessment of the mutagenic, antimutagenic and cytotoxic activities of ethanolic extract of araticum (Annona crassiflora Mart. 1841) by micronucleus test in mice. Braz J Biol 2008; 68: 141-147
  • 39 Kurokawa M, Nagasaka K, Hirabayashi T, Uyama S, Sato H, Kageyama T, Kadota S, Ohyama H, Hozumi T, Namba T, Shiraki K. Efficacy of traditional herbal medicines in combination with acyclovir against herpes simplex virus type 1 infection in vitro and in vivo . Antiviral Res 1995; 27: 19-37
  • 40 Lipipun V, Kurokawa M, Suttisri R, Taweechotipatr P, Pramyothin P, Hattori M, Shiraki K. Efficacy of Thai medicinal plant extracts against herpes simplex virus type 1 infection in vitro and in vivo . Antiviral Res 2003; 60: 175-180
  • 41 Chunasa T, Phromjai J, Lipipun V, Likhitwitayawuid K, Suzuki M, Pramyothin P, Hattori M, Shiraki K. Anti-herpes simplex virus (HSV-1) activity of oxyresveratrol derived from Thai medicinal plant: mechanism of action and therapeutic efficacy on cutaneous HSV-1 infection in mice. Antiviral Res 2008; 80: 62-70