Propolis modulates vitronectin, laminin, and heparan sulfate/heparin expression during experimental burn healing

Journal of Zhejiang University: Science B

Volumn 13, Issue 11, 2012, Pages 932-941

  Olczyk, Pawel ^a   Komosinska Vassev, Katarzyna ^a   Winsz Szczotka, Katarzyna ^a   Kozma, Ewa M ^a   Wisowski, Grzegorz ^a   Stojko, Jerzy ^a   Klimek, Katarzyna ^a   Olczyk, Krystyna ^a  

^a MEDICAL UNIVERSITY OF SILESIA   (Poland)

Author keywords

Apitherapeutic agent; Heparan sulfate heparin; Laminin; Silver sulfadiazine; Vitronectin; Wound healing

Indexed keywords

HEPARAN SULFATE; HEPARIN; LAMININ; PROPOLIS; SODIUM CHLORIDE; SULFADIAZINE SILVER; VITRONECTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN; CONTROLLED STUDY; DENSITOMETRY; ELECTROPHORESIS; ENZYME IMMUNOASSAY; EXTRACELLULAR MATRIX; NONHUMAN; PRIORITY JOURNAL; SKIN INJURY; SWINE; WOUND HEALING;

ANIMALS; ANTI-INFECTIVE AGENTS, LOCAL; BURNS; HEPARIN; LAMININ; PROPOLIS; SILVER SULFADIAZINE; SWINE; VITRONECTIN; WOUND HEALING;

SUS SCROFA DOMESTICA;

EID: 84869181715     PISSN: 16731581     EISSN: 18621783     Source Type: Journal    
DOI: 10.1631/jzus.B1100310     Document Type: Article

References (54)

1. Ansorge, S., Reinhold, D., Lendeckel, U., 2003. Propolis and some of its constituents down-regulate DNA synthesis and inflammatory cytokine production but induce TGF-β1 production of human immune cells. Z. Naturforsch. C, 58(7-8):580-589. (Pubitemid 36971463)
2. Beauvais, D.M., Ell, B.J., McWhorter, A.R., Rapraeger, A.C., 2009. Syndecan-1 regulates αvβ3 and αvβ5 integrin activation during angiogenesis and is blocked by synstatin, a novel peptide inhibitor. J. Exp. Med., 206(3):691-705. [doi:10.1084/jem.20081278]
3. Bernards, M.T., Jiang, S., 2008. pH-induced conformation changes of adsorbed vitronectin maximize its bovine aortic endothelial cell binding ability. J. Biomed. Mater. Res. A, 87(2):505-514.
4. Blumenkrantz, N., Asboe-Hansen, G., 1973. New method for quantitative determination of uronic acids. Anal. Biochem., 54(2):484-489. [doi:10.1016/0003-2697(73)90377-1]
5. Brans, T.A., Dutrieux, R.P., Hoekstra, M.J., Kreis, R.W., du Pont, J.S., 1994. Histopathological evaluation of scalds and contact burns in the pig model. Burns, 20:S48-S51. [doi:10.1016/0305-4179(94)90090-6]
6. Chen, Y., Shi-Wen, X., van Beek, J., Kennedy, L., McLeod, M., Renzoni, E.A., Bou-Gharios, G., Wilcox-Adelman, S., Goetinck, P.F., Eastwood, M., et al., 2005. Matrix contraction by dermal fibroblasts requires transforming growth factor-β/activin-linked kinase 5, heparan sulfatecontaining proteoglycans, and MEK/ERK: insights into pathological scarring in chronic fibrotic disease. Am. J. Pathol., 167(6):1699-1711. [doi:10.1016/S0002-9440(10) 61252-7] (Pubitemid 41713321)
7. Costagliola, M., Agrosi, M., 2005. Second-degree burns: a comparative, multicenter, randomized trial of hyaluronic acid plus silver sulfadiazine vs. silver sulfadiazine alone. Curr. Med. Res. Opin., 21(8):1235-1240. [doi:10.1185/030079905X56510] (Pubitemid 41140727)
8. Durbeej, M., 2010. Laminins. Cell Tissue Res., 339(1): 259-268. [doi:10.1007/s00441-009-0838-2]
9. Ekmekçi, O.B., Ekmekçi, H., 2006. Vitronectin in atherosclerotic disease. Clin. Chim. Acta, 368(1-2):77-83. [doi:10.1016/j.cca. 2005.12.015] (Pubitemid 43776027)
10. El-Hadidy, M.R., El-Hadidy, A.R., 2003. Clinical and histological evaluation of acellular allograft dermal matrix in full-thickness burns. Egypt J. Plast. Reconstr. Surg., 27(1):61-72.
11. El Kahi, C.G., Atiyeh, B.S., Abdallah Hajj Hussein, I., Jurjus, R., Dibo, S.A., Jurjus, A., Jurjus, A., 2009. Modulation of wound contracture α-smooth muscle actin and multispecific vitronectin receptor integrin αvβ3 in the rabbit's experimental model. Int. Wound J., 6(3):214-224. [doi:10.1111/j.1742-481X.2009.00597.x]
12. Geberhiwot, T., Wondimu, Z., Salob, S., Pikkarainenc, T., Kortesmaac, J., Tryggvasonc, K., Virtanend, I., Patarroyoa, M., 2000. Chain specificity assignment of monoclonal antibodies to human laminins by using recombinant laminin β1 and γ1 chains. Matrix Biol., 19(2): 163-167. [doi:10.1016/S0945-053X(00)00056-1] (Pubitemid 30332439)
13. Geer, D.J., Swartz, D.D., Andreadis, S.T., 2004. In vivo model of wound healing based on transplanted tissue-engineered skin. Tissue Eng., 10(7):1006-1017. [doi:10.1089/1076 327041887727] (Pubitemid 39223780)
14. Goh, Y.Y., Pal, M., Chong, H.C., Zhu, P., Tan, M.J., Punugu, L., Tan, C.K., Huang, R.L., Sze, S.K., Tang, M.B., et al., 2010. Angiopoietin-like 4 interacts with matrix proteins to modulate wound healing. J. Biol. Chem., 285(43): 32999-33009. [doi:10.1074/jbc.M110.108175]
15. Greenhouse, S.W., Geisser, S., 1959. On methods in the analysis of profile data. Psychometrika, 24(2):95-112. [doi:10.1007/BF02289823]
16. Groah, S.L., Libin, A., Spungen, M., Nguyen, K.L., Woods, E., Nabili, M., Ramella-Roman, J., Barritault, D., 2011. Regenerating matrix-based therapy for chronic wound healing: a prospective within-subject pilot study. Int. Wound J., 8(1):85-95. [doi:10.1111/j.1742-481X.2010. 00748.x]
17. Havran, W.L., Jameson, J.M., 2010. Epidermal T cells and wound healing. J. Immunol., 184(10):5423-5428. [doi:10. 4049/jimmunol.0902733]
18. Hoekstra, M.J., Hupkens, P., Dutrieux, R.P., Bosch, M.M.C., Brans, T.A., Kreis, R.W., 1993. A comparative burn wound model in the New Yorkshire pig for the histopathological evaluation of local therapeutic regimens: silver sulfadiazine cream as a standard. Br. J. Plast. Surg., 46(7):585-589. [doi:10.1016/0007-1226(93)90111-N] (Pubitemid 23324519)
19. Huynh, H., Feldt, L.S., 1970. Conditions under which mean square ratios in repeated measurements designs have exact F-distributions. J. Amer. Statist. Assoc., 65(332): 1582-1589. [doi:10.1080/01621459.1970.10481187]
20. Hyde, C., Hollier, B., Anderson, A., Harkin, D., Upton, Z., 2004. Insulin-like growth factors (IGF) and IGF-binding proteins bound to vitronectin enhance keratinocyte protein synthesis and migration. J. Invest. Dermatol., 122(5): 1198-1206. [doi:10.1111/j.0022-202X.2004.22527.x] (Pubitemid 38651095)
21. Iriyama, S., Hiruma, T., Tsunenaga, M., Amano, S., 2011. Influence of heparan sulfate chains in proteoglycan at the dermal-epidermal junction on epidermal homeostasis. Exp. Dermatol., 20(10):810-814. [doi:10.1111/j.1600-0625. 2011.01330.x]
22. Kikkawa, Y., Takaki, S., Matsuda, Y., Okabe, K., Taniguchi, M., Oomachi, K., Samejima, T., Katagiri, F., Hozumi, K., Nomizu, M., 2010. The influence of tribenoside on expression and deposition of epidermal laminins in Ha-CaT cells. Biol. Pharm. Bull., 33(2):307-310. [doi:10. 1248/bpb.33.307]
23. Koli, K., Lohi, J., Hautanen, A., Keski-Oja, J., 1991. Enhancement of vitronectin expression in human HepG2 hepatoma cells by transforming growth factor-β1. Eur. J. Biochem., 199(2):337-345. [doi:10.1111/j.1432-1033. 1991.tb16129.x]
24. Komosińska-Vassev, K., Winsz-Szczotka, K., Kuznik-Trocha, K., Olczyk, P., Olczyk, K., 2008. Age-related changes of plasma glycosaminoglycans. Clin. Chem. Lab. Med., 46(2):219-224. [doi:10.1515/CCLM.2008.048]
25. Köhling, R., Nischt, R., Vasudevan, A., Ho, M., Weiergräber, M., Schneider, T., Smyth, N., 2006. Nidogen and nidogen-associated basement membrane proteins and neuronal plasticity. Neurodegener. Dis., 3(1-2):56-61. [doi:10.1159/000092094] (Pubitemid 43760369)
26. Liu, T.L., Miao, J.C., Sheng, W.H., Xie, Y.F., Huang, Q., Shan, Y.B., Yang, J.C., 2010. Cytocompatibility of regenerated silk fibroin film: a medical biomaterial applicable to wound healing. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 11(1):10-16. [doi:10.1631/jzus.B0900163]
27. Malavaki, C.J., Theocharis, A.D., Lamari, F.N., Kanakis, I., Tsegenidis, T., Tzanakakis, G.N., Karamanos, N.K., 2011. Heparan sulfate: biological significance, tools for biochemical analysis and structural characterization. Biomed. Chromatogr., 25(1-2):11-20. [doi:10.1002/bmc.1536]
28. Malinda, K.M., Wysocki, A.B., Koblinski, J.E., Kleinman, H.K., Ponce, M.L., 2008. Angiogenic laminin-derived peptides stimulate wound healing. Int. J. Biochem. Cell Biol., 40(12):2771-2780. [doi:10.1016/j.biocel.2008.05.025]
29. McLennan, S.V., Bonner, J., Milne, S., Lo, L., Charlton, A., Kurup, S., Jia, J., Yue, D.K., Twigg, S.M., 2008. The anti-inflammatory agent propolis improves wound healing in a rodent model of experimental diabetes. Wound Rep. Reg., 16(5):706-713. [doi:10.1111/j.1524-475X.2008. 00421.x]
30. Moura, S.A., Ferreira, M.A., Andrade, S.P., Reis, M.L., Noviello, M.D., Cara, D.C., 2011. Brazilian green propolis inhibits inflammatory angiogenesis in a murine sponge model. Evid. Based Complement. Alternat. Med., 2011:182703. [doi:10.1093/ecam/nep197]
31. Natarajan, E., Omobono, J.D.2nd, Guo, Z., Hopkinson, S., Lazar, A.J., Brenn, T., Jones, J.C., Rheinwald, J.G., 2006. A keratinocyte hypermotility/growth-arrest response involving laminin 5 and p16INK4A activated in wound healing and senescence. Am. J. Pathol., 168(6):1821-1837. [doi:10.2353/ajpath.2006.051027] (Pubitemid 43825303)
32. Olczyk, P., Wróblewska-Adamek, I., Stojko, J., Komosińska-Vassev, K., Olczyk, K., 2008. Histopathological evaluation of Propol-T and silver sulfadiazine therapeutic efficacy in burn healing. Farm. Pol., 63(24):1108-1116 (in Polish).
33. Olczyk, P., Komosińska-Vassev, K., Koźma, E.M., Winsz-Szczotka, K., Stojko, J., Klimek, K., Olczyk, K., 2010. Assessment of glucuronosyl epimerization of dermatan sulfate chains in the course of burned wound healing. Bull. Vet. Inst. Pulawy, 54:625-629.
34. Piccard, H., van den Steen, P.E., Opdenakker, G., 2007. Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins. J. Leukoc. Biol., 81(4):870-892. [doi:10.1189/jlb.1006629] (Pubitemid 46495636)
35. Ragbow, R., Seyer, J., Kang, A., 2006. Connective Tissue of the Subendothelium. In: Creager, M.A., Loscalzo, J., Dzau, V.J. (Eds.), Vascular Medicine: A Companion to Braunwald's Heart Disease, 7th Ed. Saunders Elsevier, Philadelphia, p.31-60.
36. Räsänen, K., Vaheri, A., 2010. Proliferation and motility of HaCaT keratinocyte derivatives is enhanced by fibroblast nemosis. Exp. Cell Res., 316(10):1739-1747. [doi:10. 1016/j.yexcr.2010.01.020]
37. Roediger, M., Miosge, N., Gersdorff, N., 2010. Tissue distribution of the laminin β1 and β2 chain during embryonic and fetal human development. J. Mol. Histol., 41(2-3): 177-184. [doi:10.1007/s10735-010-9275-5]
38. Sano, K., Asanuma-Date, K., Arisaka, F., Hattori, S., Ogawa, H., 2007. Changes in glycosylation of vitronectin modulate multimerization and collagen binding during liver regeneration. Glycobiology, 17(7):784-794. [doi:10.1093/glycob/cwm031] (Pubitemid 47050665)
39. Schultz, G.S., Wysocki, A., 2009. Interactions between extracellular matrix and growth factors in wound healing. Wound Rep. Reg., 17(2):153-162. [doi:10.1111/j.1524-475X.2009.00466.x]
40. Scott, J.E., 1960. Aliphatic Ammonium Salts in the Assay of Acidic Polysaccharides from Tissues. In: Glick, D. (Ed.), Methods of Biochemical Analysis. Wiley, New York, p.145-197. [doi:10.1002/9780470110249.ch4]
41. Sforcin, J.M., Bankova, V., 2011. Propolis: is there a potential for the development of new drugs? J. Ethnopharmacol., 133(2):253-260. [doi:10.1016/j.jep.2010.10.032]
42. Slim, G.C., Furneaux, R.H., Yorke, S.C., 1994. A procedure for the analysis of glycosaminoglycan mixtures based on digestion by specific enzymes. Carbohydr. Res., 255: 285-293. [doi:10.1016/S0008-6215(00)90985-6] (Pubitemid 24084979)
43. Sugawara, K., Tsuruta, D., Ishii, M., Jones, J.C., Kobayashi, H., 2008. Laminin-332 and -511 in skin. Exp. Dermatol., 17(6):473-480. [doi:10.1111/j.1600-0625.2008.00721.x] (Pubitemid 351663274)
44. Takasaki, I., Chobanian, A.V., Brecher, P., 1991. Biosynthesis of fibronectin by rabbit aorta. J. Biol. Chem., 266(26): 17686-17694. (Pubitemid 21907992)
45. Teoh, M.L., Fitzgerald, M.P., Oberley, L.W., Domann, F.E., 2009. Overexpression of extracellular superoxide dismutase attenuates heparanase expression and inhibits breast carcinoma cell growth and invasion. Cancer Res., 69(15):6355-6363. [doi:10.1158/0008-5472.CAN-09-1195]
46. Tong, M., Zbinden, M.M., Hekking, I.J., Vermeij, M., Barritault, D., van Neck, J.W., 2008. RGTA OTR 4120, a heparan sulfate proteoglycan mimetic, increases wound breaking strength and vasodilatory capability in healing rat full-thickness excisional wounds. Wound Rep. Reg., 16(2):294-299. [doi:10.1111/j.1524-475X.2008.00368.x] (Pubitemid 351342137)
47. Tuan, T.L., Hwu, P., Ho, W., Yiu, P., Chang, R., Wysocki, A., Benya, P.D., 2008. Adenoviral overexpression and small interfering RNA suppression demonstrate that plasminogen activator inhibitor-1 produces elevated collagen accumulation in normal and keloid fibroblasts. Am. J. Pathol., 173(5):1311-1325. [doi:10.2353/ajpath.2008.080272]
48. Tzu, J., Marinkovich, M.P., 2008. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int. J. Biochem. Cell Biol., 40(2):199-214. [doi:10.1016/j.biocel.2007.07.015] (Pubitemid 350137873)
49. van Amerongen, J.P., Lemmens, A.G., Tonino, G.J.M., 1990. Glycosaminoglycans in Dental Pulp. In: Olgart, I.K. (Ed.), Dynamic Aspects of Dental Pulp: Molecular Biology, Pharmacology and Pathophysiology. Chapman and Hall, London, p.259-276. [doi:10.1007/978-94-009-0421-7-16]
50. Voermans, N.C., Bönnemann, C.G., Huijing, P.A., Hamel, B.C., van Kuppevelt, T.H., de Haan, A., Schalkwijk, J., van Engelen, B.G., Jenniskens, G.J., 2008. Interactions between extracellular matrix and growth factors in wound healing. Neuromuscul. Disord., 18(11):843-856. [doi:10. 1016/j.nmd.2008.05.017]
51. Wang, Z., Xu, Y., Yang, B., Tiruchinapally, G., Sun, B., Liu, R., Dulaney, S., Liu, J., Huang, X., 2010. Preactivationbased, one-ot combinatorial synthesis of heparin-like hexasaccharides for the analysis of heparin-rotein interactions. Chem. Eur. J., 16(28):8365-8375. [doi:10. 1002/chem.201000987]
52. Wegrowski, Y., Milard, A.L., Kotlarz, G., Toulmonde, E., Maquart, F.X., Bernard, J., 2006. Cell surface proteoglycan expression during maturation of human monocytes-derived dendritic cells and macrophages. Clin. Exp. Immunol., 144(3):485-493. [doi:10.1111/j.1365-2249.2006.03059.x] (Pubitemid 43799932)
53. Werner, S., Krieg, T., Smola, H., 2007. Keratinocytefibroblast interactions in wound healing. J. Invest. Dermatol., 127(5):998-1008. [doi:10.1038/sj.jid.5700786] (Pubitemid 46625161)
54. Yildiz, Y., Serter, M., Ek, R.O., Ergin, K., Cecen, S., Demir, E.M., Yenisey, C., 2009. Protective effects of caffeic acid phenethyl ester on intestinal ischemia-reperfusion injury. Dig. Dis. Sci., 54(4):738-744. [doi:10.1007/s10620-008-0405-9]