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Published in: International Journal of Legal Medicine 3/2017

01-05-2017 | Original Article

Detection of RAGE expression and its application to diabetic wound age estimation

Authors: Xin-Yi Ji, Yang Chen, Guang-Hua Ye, Miao-Wu Dong, Ke-Zhi Lin, Jun-Ge Han, Xiang-Ping Feng, Xing-Biao Li, Lin-Sheng Yu, Yan-Yan Fan

Published in: International Journal of Legal Medicine | Issue 3/2017

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Abstract

With the prevalence of diabetes, it is becoming important to analyze the diabetic wound age in forensic practice. The present study investigated the time-dependent expression of receptor for advanced glycation end products (RAGE) during diabetic wound healing in mice and its applicability to wound age determination by immunohistochemistry, double immunofluorescence, and Western blotting. After an incision was created in genetically diabetic db/db mice and control mice, mice were killed at posttraumatic intervals ranging from 6 h to 14 days, followed by the sampling of wound margin. Compared with control mice, diabetic mice showed the delayed wound healing. In control and diabetic wound specimens, RAGE immunoreactivity was observed in a small number of polymorphonuclear cells (PMNs), a number of macrophages, and fibroblasts. Morphometrically, the positive ratios of RAGE in macrophages or fibroblasts considerably increased in diabetic wounds during late repair, which exceeded 60% at 7 and 10 days post-injury. There were no control wound specimens to show a ratio of >60% in macrophages or fibroblasts. By Western blotting analysis, the ratios of RAGE to GAPDH were >1.4 in all diabetic wound samples from 7 to 10 days post-injury, which were >1.8 at 10 days after injury. By comparison, no control wound specimens indicated a ratio of >1.4. In conclusion, the expression of RAGE is upregulated and temporally distributed in macrophages and fibroblasts during diabetic wound healing, which might be closely involved in prolonged inflammation and deficient healing. Moreover, RAGE is promising as a useful marker for diabetic wound age determination.
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Literature
1.
go back to reference Shaw JE, Sicree RA, Zimmet PZ (2010) Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87:4–14CrossRefPubMed Shaw JE, Sicree RA, Zimmet PZ (2010) Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87:4–14CrossRefPubMed
2.
go back to reference Xu Y, Wang L, He J, Bi Y, Li M, Wang T, Wang L, Jiang Y, Dai M, Lu J, Xu M, Li Y, Hu N, Li J, Mi S, Chen CS, Li G, Mu Y, Zhao J, Kong L, Chen J, Lai S, Wang W, Zhao W, Ning G (2013) Prevalence and control of diabetes in Chinese adults. JAMA 310:948–959CrossRefPubMed Xu Y, Wang L, He J, Bi Y, Li M, Wang T, Wang L, Jiang Y, Dai M, Lu J, Xu M, Li Y, Hu N, Li J, Mi S, Chen CS, Li G, Mu Y, Zhao J, Kong L, Chen J, Lai S, Wang W, Zhao W, Ning G (2013) Prevalence and control of diabetes in Chinese adults. JAMA 310:948–959CrossRefPubMed
3.
go back to reference Palmiere C, Sporkert F, Vaucher P, Werner D, Bardy D, Rey F, Lardi C, Brunel C, Augsburger M, Mangin P (2012) Is the formula of Traub still up to date in antemortem blood glucose level estimation? Int J Legal Med 126:407–413CrossRefPubMed Palmiere C, Sporkert F, Vaucher P, Werner D, Bardy D, Rey F, Lardi C, Brunel C, Augsburger M, Mangin P (2012) Is the formula of Traub still up to date in antemortem blood glucose level estimation? Int J Legal Med 126:407–413CrossRefPubMed
4.
go back to reference Hess C, Musshoff F, Madea B (2011) Disorders of glucose metabolism-post mortem analyses in forensic cases: part I. Int J Legal Med 125:163–170CrossRefPubMed Hess C, Musshoff F, Madea B (2011) Disorders of glucose metabolism-post mortem analyses in forensic cases: part I. Int J Legal Med 125:163–170CrossRefPubMed
5.
go back to reference Keltanen T, Nenonen T, Ketola RA, Ojanperä I, Sajantila A, Lindroos K (2015) Post-mortem analysis of lactate concentration in diabetics and metformin poisonings. Int J Legal Med 129:1225–1231CrossRefPubMed Keltanen T, Nenonen T, Ketola RA, Ojanperä I, Sajantila A, Lindroos K (2015) Post-mortem analysis of lactate concentration in diabetics and metformin poisonings. Int J Legal Med 129:1225–1231CrossRefPubMed
6.
go back to reference Hitosugi M, Koseki T, Miyama G, Furukawa S, Morita S (2016) Comparison of the injury severity and medical history of disease-related versus trauma-related bicyclist fatalities. Leg Med (Tokyo) 18:58–61CrossRef Hitosugi M, Koseki T, Miyama G, Furukawa S, Morita S (2016) Comparison of the injury severity and medical history of disease-related versus trauma-related bicyclist fatalities. Leg Med (Tokyo) 18:58–61CrossRef
8.
go back to reference Wetzler C, Kampfer H, Stallmeyer B, Pfeilschifter J, Frank S (2000) Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse prolonged persistence of neutrophils and macrophages during the late phase of repair. J Invest Dermatol 115:245–253CrossRefPubMed Wetzler C, Kampfer H, Stallmeyer B, Pfeilschifter J, Frank S (2000) Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse prolonged persistence of neutrophils and macrophages during the late phase of repair. J Invest Dermatol 115:245–253CrossRefPubMed
9.
go back to reference Khanna S, Biswas S, Shang Y, Collard E, Azad A, Kauh C, Bhasker V, Gordillo GM, Sen CK, Roy S (2010) Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One 5:e9539CrossRefPubMedPubMedCentral Khanna S, Biswas S, Shang Y, Collard E, Azad A, Kauh C, Bhasker V, Gordillo GM, Sen CK, Roy S (2010) Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One 5:e9539CrossRefPubMedPubMedCentral
10.
11.
go back to reference Siqueira MF, Li J, Chehab L, Desta T, Chino T, Krothpali N, Behl Y, Alikhani M, Yang J, Braasch C, Graves DT (2010) Impaired wound healing in mouse models of diabetes is mediated by TNF-alpha dysregulation and associated with enhanced activation of forkhead box O1 (FOXO1). Diabetologia 53:378–388CrossRefPubMed Siqueira MF, Li J, Chehab L, Desta T, Chino T, Krothpali N, Behl Y, Alikhani M, Yang J, Braasch C, Graves DT (2010) Impaired wound healing in mouse models of diabetes is mediated by TNF-alpha dysregulation and associated with enhanced activation of forkhead box O1 (FOXO1). Diabetologia 53:378–388CrossRefPubMed
12.
go back to reference Takamiya M, Saigusa K, Kumagai R, Nakayashiki N, Aoki Y (2005) Studies on mRNA expression of tissue-type plasminogen activator in bruises for wound age estimation. Int J Legal Med 119:16–21CrossRefPubMed Takamiya M, Saigusa K, Kumagai R, Nakayashiki N, Aoki Y (2005) Studies on mRNA expression of tissue-type plasminogen activator in bruises for wound age estimation. Int J Legal Med 119:16–21CrossRefPubMed
14.
go back to reference Takamiya M, Fujita S, Saigusa K, Aoki Y (2008) Simultaneous detection of eight cytokines in human dermal wounds with a multiplex bead-based immunoassay for wound age estimation. Int J Legal Med 122:143–148CrossRefPubMed Takamiya M, Fujita S, Saigusa K, Aoki Y (2008) Simultaneous detection of eight cytokines in human dermal wounds with a multiplex bead-based immunoassay for wound age estimation. Int J Legal Med 122:143–148CrossRefPubMed
15.
go back to reference Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T (2008) Expression of oxygen-regulated protein 150 (ORP150) in skin wound healing and its application for wound age determination. Int J Legal Med 122:409–414CrossRefPubMed Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T (2008) Expression of oxygen-regulated protein 150 (ORP150) in skin wound healing and its application for wound age determination. Int J Legal Med 122:409–414CrossRefPubMed
16.
go back to reference Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T (2009) Detection of fibrocytes in human skin wounds and its application for wound age determination. Int J Legal Med 123:299–304CrossRefPubMed Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T (2009) Detection of fibrocytes in human skin wounds and its application for wound age determination. Int J Legal Med 123:299–304CrossRefPubMed
17.
18.
go back to reference Yu TS, Cheng ZH, Li LQ, Zhao R, Fan YY, Du Y, Ma WX, Guan DW (2010) The cannabinoid receptor type 2 is time-dependently expressed during skeletal muscle wound healing in rats. Int J Legal Med 124:397–404CrossRefPubMed Yu TS, Cheng ZH, Li LQ, Zhao R, Fan YY, Du Y, Ma WX, Guan DW (2010) The cannabinoid receptor type 2 is time-dependently expressed during skeletal muscle wound healing in rats. Int J Legal Med 124:397–404CrossRefPubMed
19.
go back to reference Ma WX, Yu TS, Fan YY, Zhang ST, Ren P, Wang SB, Zhao R, Pi JB, Guan DW (2011) Time-dependent expression and distribution of monoacylglycerol lipase during the skin-incised wound healing in mice. Int J Legal Med 125:549–558CrossRefPubMed Ma WX, Yu TS, Fan YY, Zhang ST, Ren P, Wang SB, Zhao R, Pi JB, Guan DW (2011) Time-dependent expression and distribution of monoacylglycerol lipase during the skin-incised wound healing in mice. Int J Legal Med 125:549–558CrossRefPubMed
20.
go back to reference Ishida Y, Kimura A, Nosaka M, Kuninaka Y, Takayasu T, Eisenmenger W, Kondo T (2012) Immunohistochemical analysis on cyclooxygenase-2 for wound age determination. Int J Legal Med 126:435–440CrossRefPubMed Ishida Y, Kimura A, Nosaka M, Kuninaka Y, Takayasu T, Eisenmenger W, Kondo T (2012) Immunohistochemical analysis on cyclooxygenase-2 for wound age determination. Int J Legal Med 126:435–440CrossRefPubMed
21.
go back to reference Fan YY, Zhang ST, Yu LS, Ye GH, Lin KZ, Wu SZ, Dong MW, Han JG, Feng XP, Li XB (2014) The time-dependent expression of α7nAChR during skeletal muscle wound healing in rats. Int J Legal Med 128:779–786CrossRefPubMed Fan YY, Zhang ST, Yu LS, Ye GH, Lin KZ, Wu SZ, Dong MW, Han JG, Feng XP, Li XB (2014) The time-dependent expression of α7nAChR during skeletal muscle wound healing in rats. Int J Legal Med 128:779–786CrossRefPubMed
22.
go back to reference Ishida Y, Kimura A, Nosaka M, Kuninaka Y, Shimada E, Yamamoto H, Nishiyama K, Inaka S, Takayasu T, Eisenmenger W, Kondo T (2015) Detection of endothelial progenitor cells in human skin wounds and its application for wound age determination. Int J Legal Med 129:1049–1054CrossRefPubMed Ishida Y, Kimura A, Nosaka M, Kuninaka Y, Shimada E, Yamamoto H, Nishiyama K, Inaka S, Takayasu T, Eisenmenger W, Kondo T (2015) Detection of endothelial progenitor cells in human skin wounds and its application for wound age determination. Int J Legal Med 129:1049–1054CrossRefPubMed
23.
go back to reference Ishida Y, Kuninaka Y, Nosaka M, Kimura A, Kawaguchi T, Hama M, Sakamoto S, Shinozaki K, Eisenmenger W, Kondo T (2015) Immunohistochemical analysis on MMP-2 and MMP-9 for wound age determination. Int J Legal Med 129:1043–1048CrossRefPubMed Ishida Y, Kuninaka Y, Nosaka M, Kimura A, Kawaguchi T, Hama M, Sakamoto S, Shinozaki K, Eisenmenger W, Kondo T (2015) Immunohistochemical analysis on MMP-2 and MMP-9 for wound age determination. Int J Legal Med 129:1043–1048CrossRefPubMed
24.
go back to reference Sato T, Iwaki M, Shimogaito N, Wu X, Yamagishi S, Takeuchi M (2006) TAGE (toxic AGEs) theory in diabetic complications. Curr Mol Med 6:351–358CrossRefPubMed Sato T, Iwaki M, Shimogaito N, Wu X, Yamagishi S, Takeuchi M (2006) TAGE (toxic AGEs) theory in diabetic complications. Curr Mol Med 6:351–358CrossRefPubMed
25.
go back to reference Huijberts MS, Schaper NC, Schalkwijk CG (2008) Advanced glycation end products and diabetic foot disease. Diabetes Metab Res Rev 24(Suppl 1):S19–S24CrossRefPubMed Huijberts MS, Schaper NC, Schalkwijk CG (2008) Advanced glycation end products and diabetic foot disease. Diabetes Metab Res Rev 24(Suppl 1):S19–S24CrossRefPubMed
26.
go back to reference Peppa M, Stavroulakis P, Raptis SA (2009) Advanced glycoxidation products and impaired diabetic wound healing. Wound Repair Regen 17:461–472CrossRefPubMed Peppa M, Stavroulakis P, Raptis SA (2009) Advanced glycoxidation products and impaired diabetic wound healing. Wound Repair Regen 17:461–472CrossRefPubMed
27.
go back to reference Roszer T (2011) Inflammation as death or life signal in diabetic fracture healing. Inflamm Res 60:3–10CrossRefPubMed Roszer T (2011) Inflammation as death or life signal in diabetic fracture healing. Inflamm Res 60:3–10CrossRefPubMed
28.
go back to reference Takahashi HK, Mori S, Wake H, Liu K, Yoshino T, Ohashi K, Tanaka N, Shikata K, Makino H, Nishibori M (2009) Advanced glycation end products subspecies-selectively induce adhesion molecule expression and cytokine production in human peripheral blood mononuclear cells. J Pharmacol Exp Ther 330:89–98CrossRefPubMed Takahashi HK, Mori S, Wake H, Liu K, Yoshino T, Ohashi K, Tanaka N, Shikata K, Makino H, Nishibori M (2009) Advanced glycation end products subspecies-selectively induce adhesion molecule expression and cytokine production in human peripheral blood mononuclear cells. J Pharmacol Exp Ther 330:89–98CrossRefPubMed
29.
go back to reference Qin Q, Niu J, Wang Z, Xu W, Qiao Z, Gu Y (2012) Astragalus Membranaceus inhibits inflammation via Phospho-nn38 mitogen-activated protein kinase (MAPK) and nuclear factor (NF)-κB pathways in advanced glycation end product-stimulated macrophages. Int J Mol Sci 13:8379–8387CrossRefPubMedPubMedCentral Qin Q, Niu J, Wang Z, Xu W, Qiao Z, Gu Y (2012) Astragalus Membranaceus inhibits inflammation via Phospho-nn38 mitogen-activated protein kinase (MAPK) and nuclear factor (NF)-κB pathways in advanced glycation end product-stimulated macrophages. Int J Mol Sci 13:8379–8387CrossRefPubMedPubMedCentral
30.
go back to reference Baek GH, Jang YS, Jeong SI, Cha J, Joo M, Shin SW, Ha KT, Jeong HS (2012) Rehmannia glutinosa suppresses inflammatory responses elicited by advanced glycation end products. Inflammation 35:1232–1241CrossRefPubMed Baek GH, Jang YS, Jeong SI, Cha J, Joo M, Shin SW, Ha KT, Jeong HS (2012) Rehmannia glutinosa suppresses inflammatory responses elicited by advanced glycation end products. Inflammation 35:1232–1241CrossRefPubMed
31.
go back to reference Choi HJ, Jang HJ, Chung TW, Jeong SI, Cha J, Choi JY, Han CW, Jang YS, Joo M, Jeong HS, Ha KT (2013) Catalpol suppresses advanced glycation end-products-induced inflammatory responses through inhibition of reactive oxygen species in human monocytic THP-1 cells. Fitoterapia 86:19–28CrossRefPubMed Choi HJ, Jang HJ, Chung TW, Jeong SI, Cha J, Choi JY, Han CW, Jang YS, Joo M, Jeong HS, Ha KT (2013) Catalpol suppresses advanced glycation end-products-induced inflammatory responses through inhibition of reactive oxygen species in human monocytic THP-1 cells. Fitoterapia 86:19–28CrossRefPubMed
32.
go back to reference Dong MW, Li M, Chen J, Fu TT, Lin KZ, Ye GH, Han JG, Feng XP, Li XB, Yu LS, Fan YY (2016) Activation of α7nAChR promotes diabetic wound healing by suppressing AGE-induced TNF-α production. Inflammation 39:687–699CrossRefPubMed Dong MW, Li M, Chen J, Fu TT, Lin KZ, Ye GH, Han JG, Feng XP, Li XB, Yu LS, Fan YY (2016) Activation of α7nAChR promotes diabetic wound healing by suppressing AGE-induced TNF-α production. Inflammation 39:687–699CrossRefPubMed
33.
go back to reference Xu F, Zhang C, Graves DT (2013) Abnormal cell responses and role of TNF-α in impaired diabetic wound healing. Biomed Res Int 2013:754802PubMedPubMedCentral Xu F, Zhang C, Graves DT (2013) Abnormal cell responses and role of TNF-α in impaired diabetic wound healing. Biomed Res Int 2013:754802PubMedPubMedCentral
34.
go back to reference Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, Stern DM, Schmidt AM (2001) Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol 159:513–525CrossRefPubMedPubMedCentral Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, Stern DM, Schmidt AM (2001) Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol 159:513–525CrossRefPubMedPubMedCentral
35.
go back to reference Tian M, Qing C, Niu Y, Dong J, Cao X, Song F, Ji X, Lu S (2016) The relationship between inflammation and impaired wound healing in a diabetic rat burn model. J Burn Care Res 37:e115–e124CrossRefPubMed Tian M, Qing C, Niu Y, Dong J, Cao X, Song F, Ji X, Lu S (2016) The relationship between inflammation and impaired wound healing in a diabetic rat burn model. J Burn Care Res 37:e115–e124CrossRefPubMed
36.
go back to reference Gilbert RE, Thai K, Advani SL, Cummins CL, Kepecs DM, Schroer SA, Woo M, Zhang Y (2015) SIRT1 activation ameliorates hyperglycaemia by inducing a torpor-like state in an obese mouse model of type 2 diabetes. Diabetologia 58:819–827CrossRefPubMed Gilbert RE, Thai K, Advani SL, Cummins CL, Kepecs DM, Schroer SA, Woo M, Zhang Y (2015) SIRT1 activation ameliorates hyperglycaemia by inducing a torpor-like state in an obese mouse model of type 2 diabetes. Diabetologia 58:819–827CrossRefPubMed
37.
go back to reference Kuroda K, Tajima S (2004) HSP47 is a useful marker for skin fibroblasts in formalin-fixed, paraffin-embedded tissue specimens. J Cutan Pathol 31:241–246CrossRefPubMed Kuroda K, Tajima S (2004) HSP47 is a useful marker for skin fibroblasts in formalin-fixed, paraffin-embedded tissue specimens. J Cutan Pathol 31:241–246CrossRefPubMed
38.
go back to reference Yan SF, Ramasamy R, Schmidt AM (2009) Receptor for AGE (RAGE) and its ligands-cast into leading roles in diabetes and the inflammatory response. J Mol Med (Berl) 87:235–247CrossRef Yan SF, Ramasamy R, Schmidt AM (2009) Receptor for AGE (RAGE) and its ligands-cast into leading roles in diabetes and the inflammatory response. J Mol Med (Berl) 87:235–247CrossRef
39.
go back to reference Ramasamy R, Yan SF, Schmidt AM (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243:88–102CrossRefPubMedPubMedCentral Ramasamy R, Yan SF, Schmidt AM (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243:88–102CrossRefPubMedPubMedCentral
40.
go back to reference Sorci G, Riuzzi F, Giambanco I, Donato R (2013) RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta 1833:101–109CrossRefPubMed Sorci G, Riuzzi F, Giambanco I, Donato R (2013) RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta 1833:101–109CrossRefPubMed
41.
go back to reference Litwinoff E, Hurtado Del Pozo C, Ramasamy R, Schmidt AM (2015) Emerging targets for therapeutic development in diabetes and its complications: the RAGE signaling pathway. Clin Pharmacol Ther 98:135–144CrossRefPubMedPubMedCentral Litwinoff E, Hurtado Del Pozo C, Ramasamy R, Schmidt AM (2015) Emerging targets for therapeutic development in diabetes and its complications: the RAGE signaling pathway. Clin Pharmacol Ther 98:135–144CrossRefPubMedPubMedCentral
42.
go back to reference Li J, Schmidt AM (1997) Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J Biol Chem 272:16498–16506CrossRefPubMed Li J, Schmidt AM (1997) Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J Biol Chem 272:16498–16506CrossRefPubMed
43.
go back to reference Schmidt AM, Yan SD, Yan SF, Stern DM (2001) The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108:949–955CrossRefPubMedPubMedCentral Schmidt AM, Yan SD, Yan SF, Stern DM (2001) The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108:949–955CrossRefPubMedPubMedCentral
44.
go back to reference Jin X, Yao T, Zhou Z, Zhu J, Zhang S, Hu W, Shen C (2015) Advanced glycation end products enhance macrophages polarization into M1 phenotype through activating RAGE/NF-κB pathway. Biomed Res Int 2015:732450PubMedPubMedCentral Jin X, Yao T, Zhou Z, Zhu J, Zhang S, Hu W, Shen C (2015) Advanced glycation end products enhance macrophages polarization into M1 phenotype through activating RAGE/NF-κB pathway. Biomed Res Int 2015:732450PubMedPubMedCentral
45.
go back to reference Li DX, Deng TZ, Lv J, Ke J (2014) Advanced glycation end products (AGEs) and their receptor (RAGE) induce apoptosis of periodontal ligament fibroblasts. Braz J Med Biol Res 47:1036–1043CrossRefPubMedPubMedCentral Li DX, Deng TZ, Lv J, Ke J (2014) Advanced glycation end products (AGEs) and their receptor (RAGE) induce apoptosis of periodontal ligament fibroblasts. Braz J Med Biol Res 47:1036–1043CrossRefPubMedPubMedCentral
46.
go back to reference Tian ZL, Jiang SK, Zhang M, Wang M, Li JY, Zhao R, Wang LL, Li SS, Liu M, Zhang MZ, Guan DW (2016) Detection of satellite cells during skeletal muscle wound healing in rats: time-dependent expressions of Pax7 and MyoD in relation to wound age. Int J Legal Med 130:163–172CrossRefPubMed Tian ZL, Jiang SK, Zhang M, Wang M, Li JY, Zhao R, Wang LL, Li SS, Liu M, Zhang MZ, Guan DW (2016) Detection of satellite cells during skeletal muscle wound healing in rats: time-dependent expressions of Pax7 and MyoD in relation to wound age. Int J Legal Med 130:163–172CrossRefPubMed
47.
go back to reference Kimura A, Ishida Y, Nosaka M, Shiraki M, Hama M, Kawaguchi T, Kuninaka Y, Shimada E, Yamamoto H, Takayasu T, Kondo T (2015) Autophagy in skin wounds: a novel marker for vital reactions. Int J Legal Med 129:537–541CrossRefPubMed Kimura A, Ishida Y, Nosaka M, Shiraki M, Hama M, Kawaguchi T, Kuninaka Y, Shimada E, Yamamoto H, Takayasu T, Kondo T (2015) Autophagy in skin wounds: a novel marker for vital reactions. Int J Legal Med 129:537–541CrossRefPubMed
48.
49.
50.
go back to reference Abate M, Schiavone C, Pelotti P, Salini V (2010) Limited joint mobility in diabetes and ageing: recent advances in pathogenesis and therapy. Int J Immunopathol Pharmacol 23:997–1003CrossRefPubMed Abate M, Schiavone C, Pelotti P, Salini V (2010) Limited joint mobility in diabetes and ageing: recent advances in pathogenesis and therapy. Int J Immunopathol Pharmacol 23:997–1003CrossRefPubMed
51.
go back to reference Yan SF, D’Agati V, Schmidt AM, Ramasamy R (2007) Receptor for advanced glycation Endproducts (RAGE): a formidable force in the pathogenesis of the cardiovascular complications of diabetes & aging. Curr Mol Med 7:699–710CrossRefPubMed Yan SF, D’Agati V, Schmidt AM, Ramasamy R (2007) Receptor for advanced glycation Endproducts (RAGE): a formidable force in the pathogenesis of the cardiovascular complications of diabetes & aging. Curr Mol Med 7:699–710CrossRefPubMed
52.
go back to reference Demyanenko IA, Popova EN, Zakharova VV, Ilyinskaya OP, Vasilieva TV, Romashchenko VP, Fedorov AV, Manskikh VN, Skulachev MV, Zinovkin RA, Pletjushkina OY, Skulachev VP, Chernyak BV (2015) Mitochondria-targeted antioxidant SkQ1 improves impaired dermal wound healing in old mice. Aging (Albany NY) 7:475–485CrossRef Demyanenko IA, Popova EN, Zakharova VV, Ilyinskaya OP, Vasilieva TV, Romashchenko VP, Fedorov AV, Manskikh VN, Skulachev MV, Zinovkin RA, Pletjushkina OY, Skulachev VP, Chernyak BV (2015) Mitochondria-targeted antioxidant SkQ1 improves impaired dermal wound healing in old mice. Aging (Albany NY) 7:475–485CrossRef
53.
go back to reference Tsatralis T, Ridiandries A, Robertson S, Vanags LZ, Lam YT, Tan JT, Ng MK, Bursill CA (2016) Reconstituted high-density lipoproteins promote wound repair and blood flow recovery in response to ischemia in aged mice. Lipids Health Dis 15:150CrossRefPubMedPubMedCentral Tsatralis T, Ridiandries A, Robertson S, Vanags LZ, Lam YT, Tan JT, Ng MK, Bursill CA (2016) Reconstituted high-density lipoproteins promote wound repair and blood flow recovery in response to ischemia in aged mice. Lipids Health Dis 15:150CrossRefPubMedPubMedCentral
Metadata
Title
Detection of RAGE expression and its application to diabetic wound age estimation
Authors
Xin-Yi Ji
Yang Chen
Guang-Hua Ye
Miao-Wu Dong
Ke-Zhi Lin
Jun-Ge Han
Xiang-Ping Feng
Xing-Biao Li
Lin-Sheng Yu
Yan-Yan Fan
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Legal Medicine / Issue 3/2017
Print ISSN: 0937-9827
Electronic ISSN: 1437-1596
DOI
https://doi.org/10.1007/s00414-016-1529-7

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