Abstract
Pistacia atlantica hulls and Quercus infectoria galls have been used in traditional medicine for treatment of many disorders. In the current study, excision wound model was used for the assessment of wound-healing activity of topical co-administration of hydroethanolic extracts of Pistacia atlantica hulls (P. atlantica) and Quercus infectoria galls (Q. infectoria) in streptozotocin-induced diabetic mice. Four groups of diabetic mouse model were used; control group (received soft yellow paraffin), treated groups P. atlantica 5%; Q. infectoria 5% and Q. infectoria 5% + P. atlantica 5% mixed soft yellow paraffin. Two circular, full-thickness skin wounds with 5 mm diameter were created on the back of each of the mice. During the healing time, wound rate was measured and wound sample was obtained at the end of days 3, 7, and 14 for histopathological evaluation. Moreover, immunohistochemistry staining for GLUT-1 and GPC3 was done. According to the results, topical application of each hydroethanolic extract of pistachio and quercus extract alone and co-administrated together cause improved wound-healing activity in diabetic mice via decrease in inflammation phases with decrease of edema and immune cell migration scores, and proliferation stage with increase in new vessels formation, fibroblast infiltration, collagen synthesis scores, and GLUT-1- and GPC3-positive cells in diabetic mice. These results suggest that the topical application of P. atlantica hulls and Q. infectoria galls hydroethanolic extracts has beneficial effect on full-thickness wound-healing activity in diabetic mice and it might be useful for treating various types of chronic wounds.
Similar content being viewed by others
References
Abu-Al-Basalc MA (2009) In vitro and in vivo anti-microbial effects of Nigella sativa Linn. Seed extracts against clinical isolates from skin wound infections. Am J App Sci 6(8):1440–1445
Akiyama T, Kamimura Firkus C, Takeo S, Shimmi O, Nakato H (2008) Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev Biol 313:408–419
Burant CF, Takeda J, Gould GW, Pendino KJ, Gardner CR, Laskin JD, Laskin DL, Miyata KS, Zhang B, Marcus SL (1993) Structure and function of mammalian facilitative sugar transporters. J Biol Chem 268:19161–19164
Capurro MI, Xu P, Shi W, Li F, Jia A, Filmus J (2008) Glypican-3 inhibits hedgehog signaling during development by competing with patched for hedgehog binding. Dev Cell 14:700–711
Clark LA, Moon RE (1999) Hyperbaric oxygen in the treatment of life-threatening soft-tissue infections. Respir Care Clin N Am 5(2):203–219
Cushman SW, Goodyear LJ, Pilch PF, Ralston E, Galbo H, Ploug T, Kristiansen S, Klip A (1998) Molecular mechanisms involved in GLUT4 translocation in muscle during insulin and contraction stimulation. Adv Exp Med Biol 441:63–71
Dunnill C, Patton T, Brennan J, Barrett J, Dryden M, Cooke J, Leaper D, Georgopoulos NT (2015) Reactive oxygen species (ROS) and wound healing: the functional role of ROS and emerging ROS-modulating technologies for augmentation of the healing process. Inter Wound J. doi:10.1111/iwj.12557
Farahpour MR, Fathollahpour S (2015) Topical co-administration of flaxseed and pistachio ointment promoted wound healing; evidence for histopathological features. Comp Clin Pathol 24(6):1455–1461
Farahpour MR, Mirzakhani N, Doostmohammadi J, Ebrahimzadeh M (2015) Hydroethanolic Pistacia atlantica hulls extract improved wound healing process; evidence for mast cells infiltration, angiogenesis and RNA stability. Inter J Surg 31(17):88–98
Haghdoost F, Baradaran Mahdavi MM, Zandifar A, Sanei MH, Zolfaghari B, Javanmard SH (2013) Pistacia atlantica resin has a dose-dependent effect on angiogenesis and skin burn wound healing in rat. Evid Based Complement Alternat Med 27–33
Haspel HC, Wilk EW, Birnbaum MJ, Cushman SW, Rosen OM (1986) Glucose deprivation and hexose transporter polypeptides of murine fibroblasts. J Biol Chem 261:6778–6789
Hirsch T, Spielmann M, Zuhaili B, Koehler T, Fossum M, Steinau HU, Yao F, Steinstraesser L, Onderdonk AB, Eriksson E (2008) Enhanced susceptibility to infections in a diabetic wound healing model. BMC Surg 8(1):5–9
Hwang JK, Kong TW, Baek NI, Pyun YR (2000) Alpha-glycosidase inhibitory activity of hexagalloylglucose from the galls of Quercus infectoria. Planta Med 66(3):273–274
Jalalpure SS, Patil MB, Alagawadi KR (2002) Wound healing activity of the galls of Quercus infectoria Olivier. J Nat Remed 2(1):54–58
Kaur G, Hamid H, Ali A, Alam MS, Athar M (2004) Anti-inflammatory evaluation of alcoholic extract of galls of Quercus infectoria. J Ethnopharmacol 90(2):285–292
Li WL, Zheng HC, Bukuru J, De Kimpe N (2004) Natural medicines used in the traditional Chinese medical system for therapy of diabetes mellitus. J Ethnopharmacol 92(1):1–21
Lum L, Yao S, Mozer B, Rovescalli A, Von Kessler D, Nirenberg M, Beachy PA (2003) Identification of hedgehog pathway components by RNAi in drosophila cultured cells. Science 299:2039–2045
Moura LI, Dias AM, Suesca E, Casadiegos S, Leal EC, Fontanilla MR, Carvalho L, de Sousa HC, Carvalho E (2014) Neurotensin-loaded collagen dressings reduce inflammation and improve wound healing in diabetic mice. BBA-Mol Basis Dis 1842(1):32–43
Olson AL, Pessin JE (1996) Structure, function, and regulation of the mammalian facilitative glucose transporter gene family. Annu Rev Nutr 16:235–256
Pietrzkowski Z, Mulholland G, Gomella L, Jameson BA, Wernicke D, Baserga R (1993) Inhibition of growth of prostatic cancer cell lines by peptide analogues of insulin-like growth factor 1. Cancer Res 53(5):1102–1106
Pilia G, Hughes-Benzie RM, MacKenzie A, Baybayan P, Chen EY, Huber R, Neri G, Cao A, Forabosco A, Schlessinger D (1996) Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nature Genet 12(3):241–247
Resnicoff M, Abraham D, Yutanawiboonchai W, Rotman HL, Kajstura J, Rubin R, Zoltick P, Baserga R (1995) The insulin-like growth factor I receptor protects tumor cells from apoptosis in vivo. Cancer Res 55(11):2463–2469
Sen CK, Khanna S, Gordillo G, Bagchi D, Bagchi M, Roy S (2002) Oxygen, oxidants, and antioxidants in wound healing. Ann N Y Acad Sci 957(1):239–249
Shehu A, Lu J, Wilson H, Bach DQ, Shipp D, Randeria P, Mirkin C, Paller AS (2013) Cytoplasmic sequestration of keratinocyte GLUT1 by ganglioside GM3 mediates impaired diabetic wound healing. J Invest Dermatol 133:S247–S259
Shen S, Wertheimer E, Sampson SR, Tennenbaum T (2000) Characterization of glucose transport system in keratinocytes: insulin and IGF-1 differentially affect specific transporters. J Invest Dermatol 115:949–954
Silva SY, Rueda LC, Márquez GA, López M, Smith DJ, Calderón CA, Castillo JC, Matute J, Rueda-Clausen CF, Orduz A, Silva FA (2007) Double blind, randomized, placebo controlled clinical trial for the treatment of diabetic foot ulcers, using a nitric oxide releasing patch. PATHON 8(1):26–30
Song HH, Shi W, Xiang Y, Filmus J (2005) The loss of Glypican-3 induces alterations in Wnt signaling. J Biol Chem 280:2116–2125
Takahashi H, Ohara K, Ohmura T, Takahashi R, Zieske JD (2000) Glucose transporter 1 expression in corneal wound repair under high serum glucose level. Jpn J Ophthalmol 44:470–474
Umachigi SP, Jayaveera KN, Kumar CA, Kumar GS, Kumar DK (2008) Studies on wound healing properties of Quercus infectoria. Trop J Pharm Res 7(1):913–919
Acknowledgements
The authors are grateful to Ayande lab for histopathology study and Mohammad Aghaei (Dr) for the preparation of extracts and formulations.
Author information
Authors and Affiliations
Ethics declarations
Ethical approval
All animal experiments strictly complied with the guidelines of the Institutional Animal Ethical Committee no 2015/iau/111.
Funding
This study was the result of a thesis research project and was supported by Author’s own work (grant number 870,064,555).
Conflict of interest
Author A declares that he/she has no conflict of interest. Author B declares that he/she has no conflict of interest.
Rights and permissions
About this article
Cite this article
Bonab, F.S., Farahpour, M.R. Topical co-administration of Pistacia atlantica hull and Quercus infectoria gall hydroethanolic extract improves wound-healing process. Comp Clin Pathol 26, 885–892 (2017). https://doi.org/10.1007/s00580-017-2473-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00580-017-2473-8