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DOI: 10.1055/a-0733-7151
Pro-Fibrogenic and Anti-Inflammatory Potential of a Polyphenol-Enriched Fraction from Annona crassiflora in Skin Repair
Publication History
received 23 May 2018
revised 13 August 2018
accepted 03 September 2018
Publication Date:
20 September 2018 (online)
Abstract
A polyphenol-enriched fraction from Annona crassiflora fruit peel (PEF-Ac) containing chlorogenic acid, epi-catechin, procyanidins B2 and C1, quercetin-glucoside, kaempferol, and caffeoyl-glucoside was investigated for its anti-inflammatory, pro-angiogenic, and profibrogenic potential in the healing of cutaneous wounds. Four wounds were performed on the back of C57 mice and the lesions were treated with the vehicle (Vaseline and lanolin) and PEF-Ac at concentrations of 2%, 4%, and 6% for 4 and 7 d. Neutrophils and macrophages activities were evaluated indirectly by the activity of myeloperoxidase and N-acetyl-β-D-glycosaminidase, angiogenesis was evaluated by hemoglobin dosing and vessel count in histological sections, and collagen deposition was assessed from histological sections stained with picrosirius red. PEF-Ac demonstrated anti-inflammatory activity, with reduced activities of neutrophil and macrophage in the cutaneous wounds. In addition, there was an increase in the synthesis of types I and III collagen, as well as in the percentage of wound closure, mainly after 4 d of treatment. On the other hand, PEF-Ac did not present an effective pro-angiogenic activity. A. crassiflora fruit peel showed anti-inflammatory and profibrogenic properties, indicating a promising natural source of bioactive molecules for treatment of cutaneous wounds.
* These authors contributed equally to this manuscript.
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References
- 1 Kanitakis J. Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol 2002; 12: 390-399
- 2 Lindley LE, Stojadinovic O, Pastar I, Tomic-Canic M. Biology and biomarkers for wound healing. Plast Reconstr Surg 2016; 138: 18s-28s
- 3 Wang PH, Huang BS, Horng HC, Yeh CC, Chen YJ. Wound healing. J Chin Med Assoc 2018; 81: 94-101
- 4 Berman B, Maderal A, Raphael B. Keloids and hypertrophic scars: pathophysiology, classification, and treatment. Dermatol Surg 2017; 43 (Suppl. 01) S3-S18
- 5 Estevão LRM, Simões RS, Cassini-Vieira P, Canesso MCC, Barcelos LDS, Rachid MA, Câmara CAGD, Evêncio-Neto J. Schinus terebinthifolius Raddi (Aroeira) leaves oil attenuates inflammatory responses in cutaneous wound healing in mice. Acta Cir Bras 2017; 32: 726-735
- 6 Qian LW, Fourcaudot AB, Yamane K, You T, Chan RK, Leung KP. Exacerbated and prolonged inflammation impairs wound healing and increases scarring. Wound Repair Regen 2016; 24: 26-34
- 7 Duque AP, Pinto Nde C, Mendes Rde F, da Silva JM, Aragao DM, Castanon MC, Scio E. In vivo wound healing activity of gels containing Cecropia pachystachya leaves. J Pharm Pharmacol 2016; 68: 128-138
- 8 Rennert RC, Rodrigues M, Wong VW, Duscher D, Hu M, Maan Z, Sorkin M, Gurtner GC, Longaker MT. Biological therapies for the treatment of cutaneous wounds: phase III and launched therapies. Expert Opin Biol Ther 2013; 13: 1523-1541
- 9 Ricardo LM, Dias BM, Mugge FLB, Leite VV, Brandao MGL. Evidence of traditionality of Brazilian medicinal plants: the case studies of Stryphnodendron adstringens (Mart.) Coville (barbatimao) barks and Copaifera spp. (copaiba) oleoresin in wound healing. J Ethnopharmacol 2018; 219: 319-336
- 10 Działo M, Mierziak J, Korzun U, Preisner M, Szopa J, Kulma A. The potential of plant phenolics in prevention and therapy of skin disorders. Int J Mol Sci 2016; 17: 160
- 11 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
- 12 Justino AB, Pereira MN, Peixoto LG, Vilela DD, Caixeta DC, de Souza AV, Teixeira RR, Silva HCG, de Moura FBR, Moraes IB, Espindola FS. Hepatoprotective properties of a polyphenols-enriched fraction from Annona crassiflora Mart. fruit peel against diabetes-induced oxidative and nitrosative stress. J Agric Food Chem 2017; 65: 4428-4438
- 13 Justino AB, Pereira MN, Vilela DD, Peixoto LG, Martins MM, Teixeira RR, Miranda NC, da Silva NM, de Sousa RMF, de Oliveira A, Espindola FS. Peel of araticum fruit (Annona crassiflora Mart.) as a source of antioxidant compounds with α-amylase, α-glucosidase and glycation inhibitory activities. Bioorg Chem 2016; 69: 167-182
- 14 Takahashi JA, Pereira CR, Pimenta LP, Boaventura MA, Silva LG. Antibacterial activity of eight Brazilian annonaceae plants. Nat Prod Res 2006; 20: 21-26
- 15 Machado AR, Ferreira SR, da Silva Medeiros F, Fujiwara RT, de Souza Filho JD, Pimenta LP. Nematicidal activity of Annona crassiflora leaf extract on Caenorhabditis elegans . Parasit Vectors 2015; 8: 113
- 16 Pereira MN, Justino AB, Martins MM, Peixoto LG, Vilela DD, Santos PS, Teixeira TL, da Silva CV, Goulart LR, Pivatto M, Espindola FS. Stephalagine, an alkaloid with pancreatic lipase inhibitory activity isolated from the fruit peel of Annona crassiflora Mart. Ind Crops Prod 2017; 97: 324-329
- 17 Budovsky A, Yarmolinsky L, Ben-Shabat S. Effect of medicinal plants on wound healing. Wound Repair Regen 2015; 23: 171-183
- 18 Newman DJ, Cragg GM. Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 2016; 79: 629-661
- 19 Li WG, Zhang XY, Wu YJ, Tian X. Anti-inflammatory effect and mechanism of proanthocyanidins from grape seeds. Acta Pharmacol Sin 2001; 22: 1117-1120
- 20 Pastore S, Lulli D, Fidanza P, Potapovich AI, Kostyuk VA, De Luca C, Mikhalʼchik E, Korkina LG. Plant polyphenols regulate chemokine expression and tissue repair in human keratinocytes through interaction with cytoplasmic and nuclear components of epidermal growth factor receptor system. Antioxid Redox Signal 2012; 16: 314-328
- 21 Rocha RS, Kassuya CA, Formagio AS, Mauro Mde O, Andrade-Silva M, Monreal AC, Cunha-Laura AL, Vieira Mdo C, Oliveira RJ. Analysis of the anti-inflammatory and chemopreventive potential and description of the antimutagenic mode of action of the Annona crassiflora methanolic extract. Pharm Biol 2016; 54: 35-47
- 22 da Costa Oliveira C, de Matos NA, de Carvalho Veloso C, Lage GA, Pimenta LPS, Duarte IDG, Romero TRL, Klein A, de Castro Perez A. Anti-inflammatory and antinociceptive properties of the hydroalcoholic fractions from the leaves of Annona crassiflora Mart. in mice. Inflammopharmacology 2018; DOI: 10.1007/s10787-017-0426-0.
- 23 Webster NR, Galley HF. Inflammation and immunity. BJA CEPD Reviews 2003; 3: 54-58
- 24 Eming SA, Brachvogel B, Odorisio T, Koch M. Regulation of angiogenesis: wound healing as a model. Prog Histochem Cytochem 2007; 42: 115-170
- 25 Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 2011; 13: e23
- 26 Steed DL. The role of growth factors in wound healing. Surg Clin North Am 1997; 77: 575-586
- 27 Dovi JV, He LK, DiPietro LA. Accelerated wound closure in neutrophil-depleted mice. J Leukoc Biol 2003; 73: 448-455
- 28 Pierce GF. Inflammation in nonhealing diabetic wounds: the space-time continuum does matter. Am J Pathol 2001; 159: 399-403
- 29 Reish RG, Eriksson E. Scar treatments: preclinical and clinical studies. J Am Coll Surg 2008; 206: 719-730
- 30 Murphy MA, Joyce WP, Condron C, Bouchier-Hayes D. A reduction in serum cytokine levels parallels healing of venous ulcers in patients undergoing compression therapy. Eur J Vasc Endovasc Surg 2002; 23: 349-352
- 31 Liang N, Kitts DD. Role of chlorogenic acids in controlling oxidative and inflammatory stress conditions. Nutrients 2016; 8: 16
- 32 Kulkarni RR, Lee W, Jang TS, Lee J, Kwak S, Park MS, Lee HS, Bae JS, Na M. Caffeoyl glucosides from Nandina domestica inhibit LPS-induced endothelial inflammatory responses. Bioorg Med Chem Lett 2015; 25: 5367-5371
- 33 Borghi SM, Pinho-Ribeiro FA, Fattori V, Bussmann AJC, Vignoli JA, Camilios-Neto D, Casagrande R, Verri WA. Quercetin inhibits peripheral and spinal cord nociceptive mechanisms to reduce intense acute swimming-induced muscle pain in mice. PLoS One 2016; 11: e0162267
- 34 Tonnesen MG, Feng X, Clark RA. Angiogenesis in wound healing. J Investig Dermatol Symp Proc 2000; 5: 40-46
- 35 Galicka A, Nazaruk J. Stimulation of collagen biosynthesis by flavonoid glycosides in skin fibroblasts of osteogenesis imperfecta type I and the potential mechanism of their action. Int J Mol Med 2007; 20: 889-895
- 36 Eckes B, Nischt R, Krieg T. Cell-matrix interactions in dermal repair and scarring. Fibrogenesis Tissue Repair 2010; 3: 4
- 37 Barker TH. The role of ECM proteins and protein fragments in guiding cell behavior in regenerative medicine. Biomaterials 2011; 32: 4211-4214
- 38 Pinto NC, Cassini-Vieira P, Souza-Fagundes EM, Barcelos LS, Castanon MC, Scio E. Pereskia aculeata Miller leaves accelerate excisional wound healing in mice. J Ethnopharmacol 2016; 194: 131-136
- 39 Cassini-Vieira P, Deconte SR, Tomiosso TC, Campos PP, Montenegro Cde F, Selistre-de-Araujo HS, Barcelos LS, Andrade SP, Araujo Fde A. DisBa-01 inhibits angiogenesis, inflammation and fibrogenesis of sponge-induced-fibrovascular tissue in mice. Toxicon 2014; 92: 81-89
- 40 Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982; 78: 206-209
- 41 Bailey PJ. Sponge implants as models. Methods Enzymol 1988; 162: 327-334