Skip to main content
Top
Published in: International Journal of Legal Medicine 1/2018

01-01-2018 | Original Article

Immunohistochemical analysis on aquaporin-1 and aquaporin-3 in skin wounds from the aspects of wound age determination

Authors: Yuko Ishida, Yumi Kuninaka, Fukumi Furukawa, Akihiko Kimura, Mizuho Nosaka, Mie Fukami, Hiroki Yamamoto, Takashi Kato, Emi Shimada, Satoshi Hata, Tatsunori Takayasu, Wolfgang Eisenmenger, Toshikazu Kondo

Published in: International Journal of Legal Medicine | Issue 1/2018

Login to get access

Abstract

Immunohistochemical investigation of aquaporin (AQP)1 and AQP3 was performed in human skin wounds obtained from forensic autopsy cases. A total of 55 human skin wounds of different postinfliction intervals were collected as follows: group I, 0–3 days (n = 16); II, 4–7 days (n = 11); III, 9–14 days (n = 16); and IV, 17–21 days (n = 12). In uninjured skin samples, AQP1 and AQP3 could be slightly detected in dermal vessels and keratinocytes, respectively. The percentage of AQP1+ vessels and the number of AQP3+ keratinocytes were apparently elevated in accordance with wound ages. The number of AQP3+ keratinocytes was distinctly evident in groups II and III. Morphometrically, both AQP1+ vessel area and AQP3+ cell number were markedly increased in group II, compared with other three groups. With regard to forensic safety, AQP1+ vessel area of over 5% would imply wound ages of 4–12 days. Moreover, the positive area of > 15% would suggest wound age of 7–10 days. Especially, most samples of skin wounds aged 5–10 days except for only one sample (a 10-day-old wound) showed AQP3+ cell number of > 300, and the remaining other samples had that of < 300. Thus, the AQP3+ cell number of > 300 would indicate wound ages of 5–10 days. Collectively, immunohistochemical analyses of AQP1 and AQP3 in human skin wounds would support the objective accuracy of wound age determination.
Literature
1.
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 129:1043–1048PubMed 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 129:1043–1048PubMed
2.
go back to reference Kondo T (2007) Timing of skin wounds. Legal Med (Tokyo) 9:109–114 Kondo T (2007) Timing of skin wounds. Legal Med (Tokyo) 9:109–114
3.
go back to reference Kondo T, Ishida Y (2010) Molecular pathology of wound healing. Forensic Sci Int 203:93–98PubMed Kondo T, Ishida Y (2010) Molecular pathology of wound healing. Forensic Sci Int 203:93–98PubMed
4.
go back to reference Cecchi R (2010) Estimating wound age: looking into the future. Int J Legal Med 124:523–536PubMed Cecchi R (2010) Estimating wound age: looking into the future. Int J Legal Med 124:523–536PubMed
5.
go back to reference Betz P (1994) Histological and enzyme histochemical parameters for the age estimation of human skin wounds. Int J Legal Med 107:60–68PubMed Betz P (1994) Histological and enzyme histochemical parameters for the age estimation of human skin wounds. Int J Legal Med 107:60–68PubMed
6.
go back to reference An JL, Ishida Y, Kimura A, Kondo T (2011) Immunohistochemical examination of intracerebral aquaporin-4 expression and its application for differential diagnosis between freshwater and saltwater drowning. Int J Legal Med 125:59–65PubMed An JL, Ishida Y, Kimura A, Kondo T (2011) Immunohistochemical examination of intracerebral aquaporin-4 expression and its application for differential diagnosis between freshwater and saltwater drowning. Int J Legal Med 125:59–65PubMed
7.
go back to reference Nosaka M, Ishida Y, Kimura A, Kondo T (2010) Immunohistochemical detection of MMP-2 and MMP-9 in a stasis-induced deep vein thrombosis model and its application to thrombus age estimation. Int J Legal Med 124:439–444PubMed Nosaka M, Ishida Y, Kimura A, Kondo T (2010) Immunohistochemical detection of MMP-2 and MMP-9 in a stasis-induced deep vein thrombosis model and its application to thrombus age estimation. Int J Legal Med 124:439–444PubMed
8.
go back to reference Fracasso T, Pfeiffer H, Michaud K, Köhler H, Sauerland C, Schmeling A (2011) Immunohistochemical expression of fibronectin and C5b-9 in the myocardium in cases of carbon monoxide poisoning. Int J Legal Med 125:377–384PubMed Fracasso T, Pfeiffer H, Michaud K, Köhler H, Sauerland C, Schmeling A (2011) Immunohistochemical expression of fibronectin and C5b-9 in the myocardium in cases of carbon monoxide poisoning. Int J Legal Med 125:377–384PubMed
9.
go back to reference Yoshida C, Ishikawa T, Michiue T, Quan L, Maeda H (2011) Postmortem biochemistry and immunohistochemistry of chromogranin A as a stress marker with special regard to fatal hypothermia and hyperthermia. Int J Legal Med 125:11–20PubMed Yoshida C, Ishikawa T, Michiue T, Quan L, Maeda H (2011) Postmortem biochemistry and immunohistochemistry of chromogranin A as a stress marker with special regard to fatal hypothermia and hyperthermia. Int J Legal Med 125:11–20PubMed
10.
go back to reference Bohnert M, Anderson J, Rothschild MA, Böhm J (2010) Immunohistochemical expression of fibronectin in the lungs of fire victims proves intravital reaction in fatal burns. Int J Legal Med 124:583–588PubMed Bohnert M, Anderson J, Rothschild MA, Böhm J (2010) Immunohistochemical expression of fibronectin in the lungs of fire victims proves intravital reaction in fatal burns. Int J Legal Med 124:583–588PubMed
11.
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 126:435–440PubMed 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 126:435–440PubMed
12.
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 123:299–304PubMed 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 123:299–304PubMed
13.
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 122:409–414PubMed 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 122:409–414PubMed
14.
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 129:1049–1054PubMed 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 129:1049–1054PubMed
15.
go back to reference Kondo T, Tanaka J, Ishida Y, Mori R, Takayasu T, Ohshima T (2002) Ubiquitin expression in skin wounds and its application to forensic wound age determination. Int J Legal Med 116:267–272PubMed Kondo T, Tanaka J, Ishida Y, Mori R, Takayasu T, Ohshima T (2002) Ubiquitin expression in skin wounds and its application to forensic wound age determination. Int J Legal Med 116:267–272PubMed
16.
go back to reference Kondo T, Ohshima T, Eisenmenger W (1999) Immunohistochemical and morphometrical study on the temporal expression of interleukin-1α (IL-1α) in human skin wounds for forensic wound age determination. Int J Legal Med 112:249–252PubMed Kondo T, Ohshima T, Eisenmenger W (1999) Immunohistochemical and morphometrical study on the temporal expression of interleukin-1α (IL-1α) in human skin wounds for forensic wound age determination. Int J Legal Med 112:249–252PubMed
17.
go back to reference Hayashi T, Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T (2004) Forensic application of VEGF expression to skin wound age determination. Int J Legal Med 118:320–325PubMed Hayashi T, Ishida Y, Kimura A, Takayasu T, Eisenmenger W, Kondo T (2004) Forensic application of VEGF expression to skin wound age determination. Int J Legal Med 118:320–325PubMed
18.
go back to reference Kondo T, Ohshima T, Mori R, Guan DW, Ohshima K, Eisenmenger W (2002) Immunohistochemical detection of chemokines in human skin wounds and its application to wound age determination. Int J Legal Med 116:87–91PubMed Kondo T, Ohshima T, Mori R, Guan DW, Ohshima K, Eisenmenger W (2002) Immunohistochemical detection of chemokines in human skin wounds and its application to wound age determination. Int J Legal Med 116:87–91PubMed
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 125:549–558PubMed 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 125:549–558PubMed
20.
go back to reference Kondo T, Ohshima T (1996) The dynamics of inflammatory cytokines in the healing process of mouse skin wound: a preliminary study for possible wound age determination. Int J Legal Med 108:231–236PubMed Kondo T, Ohshima T (1996) The dynamics of inflammatory cytokines in the healing process of mouse skin wound: a preliminary study for possible wound age determination. Int J Legal Med 108:231–236PubMed
21.
go back to reference Martin P (1997) Wound healing—aiming for perfect skin regeneration. Science 276:75–81PubMed Martin P (1997) Wound healing—aiming for perfect skin regeneration. Science 276:75–81PubMed
22.
go back to reference Hunt TK, Hopf H, Hussain Z (2000) Physiology of wound healing. Adv Skin Wound Care 13:6–11PubMed Hunt TK, Hopf H, Hussain Z (2000) Physiology of wound healing. Adv Skin Wound Care 13:6–11PubMed
23.
go back to reference Morasso MI, Tomic-Canic M (2005) Epidermal stem cells: the cradle of epidermal determination, differentiation and wound healing. Biol Cell 97:173–183PubMedPubMedCentral Morasso MI, Tomic-Canic M (2005) Epidermal stem cells: the cradle of epidermal determination, differentiation and wound healing. Biol Cell 97:173–183PubMedPubMedCentral
24.
go back to reference Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835–870PubMed Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835–870PubMed
25.
go back to reference Santoro MM, Gaudino G (2005) Cellular and molecular facets of keratinocyte reepithelization during wound healing. Exp Cell Res 304:274–286PubMed Santoro MM, Gaudino G (2005) Cellular and molecular facets of keratinocyte reepithelization during wound healing. Exp Cell Res 304:274–286PubMed
26.
go back to reference Hara-Chikuma M, Verkman AS (2008) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J Mol Med (Berl) 86:221–231 Hara-Chikuma M, Verkman AS (2008) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J Mol Med (Berl) 86:221–231
27.
go back to reference Sebastian R, Chau E, Fillmore P, Matthews J, Price LA, Sidhaye V, Milner SM (2015) Epidermal aquaporin-3 is increased in the cutaneous burn wound. Burns 41:843–847PubMedPubMedCentral Sebastian R, Chau E, Fillmore P, Matthews J, Price LA, Sidhaye V, Milner SM (2015) Epidermal aquaporin-3 is increased in the cutaneous burn wound. Burns 41:843–847PubMedPubMedCentral
28.
go back to reference Boury-Jamot M, Daraspe J, Bonté F, Perrier E, Schnebert S, Dumas M, Verbavatz JM (2009) Skin aquaporins: function in hydration, wound healing, and skin epidermis homeostasis. Handb Exp Pharmacol:205–217 Boury-Jamot M, Daraspe J, Bonté F, Perrier E, Schnebert S, Dumas M, Verbavatz JM (2009) Skin aquaporins: function in hydration, wound healing, and skin epidermis homeostasis. Handb Exp Pharmacol:205–217
29.
go back to reference Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792PubMed Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792PubMed
30.
go back to reference Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS (2005) Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691–5698PubMed Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS (2005) Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691–5698PubMed
31.
go back to reference Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS (2007) Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 21:108–116PubMed Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS (2007) Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 21:108–116PubMed
32.
go back to reference Hara-Chikuma M, Verkman AS (2006) Aquaporin-1 facilitates epithelial cell migration in kidney proximal tubule. J Am Soc Nephrol 17:39–45PubMed Hara-Chikuma M, Verkman AS (2006) Aquaporin-1 facilitates epithelial cell migration in kidney proximal tubule. J Am Soc Nephrol 17:39–45PubMed
33.
go back to reference Hara-Chikuma M, Verkman AS (2008) Roles of aquaporin-3 in the epidermis. J Investig Dermatol 128:2145–2151PubMed Hara-Chikuma M, Verkman AS (2008) Roles of aquaporin-3 in the epidermis. J Investig Dermatol 128:2145–2151PubMed
34.
go back to reference Ishida Y, Gao JL, Murphy PM (2008) Chemokine receptor CX3CR1 mediates skin wound healing by promoting macrophage and fibroblast accumulation and function. J Immunol 180:569–579PubMed Ishida Y, Gao JL, Murphy PM (2008) Chemokine receptor CX3CR1 mediates skin wound healing by promoting macrophage and fibroblast accumulation and function. J Immunol 180:569–579PubMed
35.
go back to reference Rojek A, Praetorius J, Frøkiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327PubMed Rojek A, Praetorius J, Frøkiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327PubMed
36.
go back to reference Verkman AS (2005) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118:3225–3232PubMed Verkman AS (2005) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118:3225–3232PubMed
37.
go back to reference Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporins and cell migration. Pflugers Arch 456:693–700PubMed Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporins and cell migration. Pflugers Arch 456:693–700PubMed
39.
go back to reference Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci U S A 90:7275–7279PubMedPubMedCentral Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci U S A 90:7275–7279PubMedPubMedCentral
40.
go back to reference Hasegawa H, Lian SC, Finkbeiner WE, Verkman AS (1994) Extrarenal tissue distribution of CHIP28 water channels by in situ hybridization and antibody staining. Am J Phys 266:C893–C903 Hasegawa H, Lian SC, Finkbeiner WE, Verkman AS (1994) Extrarenal tissue distribution of CHIP28 water channels by in situ hybridization and antibody staining. Am J Phys 266:C893–C903
41.
go back to reference Verkman AS (2006) Aquaporins in endothelia. Kidney Int 69:1120–1123PubMed Verkman AS (2006) Aquaporins in endothelia. Kidney Int 69:1120–1123PubMed
42.
go back to reference Dolman D, Drndarski S, Abbott NJ, Rattray M (2005) Induction of aquaporin 1 but not aquaporin 4 messenger RNA in rat primary brain microvessel endothelial cells in culture. J Neurochem 93:825–833PubMed Dolman D, Drndarski S, Abbott NJ, Rattray M (2005) Induction of aquaporin 1 but not aquaporin 4 messenger RNA in rat primary brain microvessel endothelial cells in culture. J Neurochem 93:825–833PubMed
43.
go back to reference Agren J, Zelenin S, Håkansson M, Eklöf AC, Aperia A, Nejsum LN, Nielsen S, Sedin G (2003) Transepidermal water loss in developing rats: role of aquaporins in the immature skin. Pediatr Res 53:558–565PubMed Agren J, Zelenin S, Håkansson M, Eklöf AC, Aperia A, Nejsum LN, Nielsen S, Sedin G (2003) Transepidermal water loss in developing rats: role of aquaporins in the immature skin. Pediatr Res 53:558–565PubMed
44.
go back to reference Marchini G, Ståbi B, Kankes K, Lonne-Rahm S, Østergaard M, Nielsen S (2003) AQP1 and AQP3, psoriasin, and nitric oxide synthases 1-3 are inflammatory mediators in erythema toxicum neonatorum. Pediatr Dermatol 20:377–384PubMed Marchini G, Ståbi B, Kankes K, Lonne-Rahm S, Østergaard M, Nielsen S (2003) AQP1 and AQP3, psoriasin, and nitric oxide synthases 1-3 are inflammatory mediators in erythema toxicum neonatorum. Pediatr Dermatol 20:377–384PubMed
45.
go back to reference Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, Verkman AS (1995) Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci 108:2993–3002PubMed Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, Verkman AS (1995) Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci 108:2993–3002PubMed
46.
go back to reference Echevarria M, Windhager EE, Tate SS, Frindt G (1994) Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc Natl Acad Sci U S A 91:10997–11001PubMedPubMedCentral Echevarria M, Windhager EE, Tate SS, Frindt G (1994) Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc Natl Acad Sci U S A 91:10997–11001PubMedPubMedCentral
47.
go back to reference Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T et al (1994) Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc Natl Acad Sci U S A 91:6269–6273PubMedPubMedCentral Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T et al (1994) Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc Natl Acad Sci U S A 91:6269–6273PubMedPubMedCentral
48.
go back to reference Ma T, Frigeri A, Hasegawa H, Verkman AS (1994) Cloning of a water channel homolog expressed in brain meningeal cells and kidney collecting duct that functions as a stilbene-sensitive glycerol transporter. J Biol Chem 269:21845–21849PubMed Ma T, Frigeri A, Hasegawa H, Verkman AS (1994) Cloning of a water channel homolog expressed in brain meningeal cells and kidney collecting duct that functions as a stilbene-sensitive glycerol transporter. J Biol Chem 269:21845–21849PubMed
49.
go back to reference Sugiyama Y, Ota Y, Hara M, Inoue S (2001) Osmotic stress up-regulates aquaporin-3 gene expression in cultured human keratinocytes. Biochim Biophys Acta 1522:82–88PubMed Sugiyama Y, Ota Y, Hara M, Inoue S (2001) Osmotic stress up-regulates aquaporin-3 gene expression in cultured human keratinocytes. Biochim Biophys Acta 1522:82–88PubMed
50.
go back to reference Ma T, Hara M, Sougrat R, Verbavatz JM, Verkman AS (2002) Impaired stratum corneum hydration in mice lacking epidermal water channel aquaporin-3. J Biol Chem 277:17147–17153PubMed Ma T, Hara M, Sougrat R, Verbavatz JM, Verkman AS (2002) Impaired stratum corneum hydration in mice lacking epidermal water channel aquaporin-3. J Biol Chem 277:17147–17153PubMed
51.
go back to reference Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999) Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss. J Histochem Cytochem 47:1275–1286PubMed Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999) Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss. J Histochem Cytochem 47:1275–1286PubMed
52.
go back to reference Sougrat R, Morand M, Gondran C, Barré P, Gobin R, Bonté F, Dumas M, Verbavatz JM (2002) Functional expression of AQP3 in human skin epidermis and reconstructed epidermis. J Investig Dermatol 118:678–685PubMed Sougrat R, Morand M, Gondran C, Barré P, Gobin R, Bonté F, Dumas M, Verbavatz JM (2002) Functional expression of AQP3 in human skin epidermis and reconstructed epidermis. J Investig Dermatol 118:678–685PubMed
53.
go back to reference Hara M, Ma T, Verkman AS (2002) Selectively reduced glycerol in skin of aquaporin-3-deficient mice may account for impaired skin hydration, elasticity, and barrier recovery. J Biol Chem 277:46616–46621PubMed Hara M, Ma T, Verkman AS (2002) Selectively reduced glycerol in skin of aquaporin-3-deficient mice may account for impaired skin hydration, elasticity, and barrier recovery. J Biol Chem 277:46616–46621PubMed
54.
go back to reference Hara-Chikuma M, Takahashi K, Chikuma S, Verkman AS, Miyachi Y (2009) The expression of differentiation markers in aquaporin-3 deficient epidermis. Arch Dermatol Res 301:245–252PubMedPubMedCentral Hara-Chikuma M, Takahashi K, Chikuma S, Verkman AS, Miyachi Y (2009) The expression of differentiation markers in aquaporin-3 deficient epidermis. Arch Dermatol Res 301:245–252PubMedPubMedCentral
55.
go back to reference Levin MH, Verkman AS (2006) Aquaporin-3-dependent cell migration and proliferation during corneal re-epithelialization. Invest Ophthalmol Vis Sci 47:4365–4372PubMed Levin MH, Verkman AS (2006) Aquaporin-3-dependent cell migration and proliferation during corneal re-epithelialization. Invest Ophthalmol Vis Sci 47:4365–4372PubMed
56.
go back to reference Thiagarajah JR, Zhao D, Verkman AS (2007) Impaired enterocyte proliferation in aquaporin-3 deficiency in mouse models of colitis. Gut 56:1529–1535PubMedPubMedCentral Thiagarajah JR, Zhao D, Verkman AS (2007) Impaired enterocyte proliferation in aquaporin-3 deficiency in mouse models of colitis. Gut 56:1529–1535PubMedPubMedCentral
57.
go back to reference Dressler J, Bachmann L, Koch R, Müller E (1999) Estimation of wound age and VCAM-1 in human skin. Int J Legal Med 112:159–162PubMed Dressler J, Bachmann L, Koch R, Müller E (1999) Estimation of wound age and VCAM-1 in human skin. Int J Legal Med 112:159–162PubMed
58.
go back to reference Dressler J, Bachmann L, Koch R, Müller E (1999) Enhanced expression of selectins in human skin wounds. Int J Legal Med 112:39–44 Dressler J, Bachmann L, Koch R, Müller E (1999) Enhanced expression of selectins in human skin wounds. Int J Legal Med 112:39–44
59.
go back to reference Dressler J, Bachmann L, Kasper M, Hauck JG, Müller E (1997) Time dependence of the expression of ICAM-1 (CD 54) in human skin wounds. Int J Legal Med 110:299–304PubMed Dressler J, Bachmann L, Kasper M, Hauck JG, Müller E (1997) Time dependence of the expression of ICAM-1 (CD 54) in human skin wounds. Int J Legal Med 110:299–304PubMed
60.
go back to reference Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967PubMed Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967PubMed
61.
go back to reference Dressler J, Busuttil A, Koch R, Harrison DJ (2001) Sequence of melanocyte migration into human scar tissue. Int J Legal Med 115:61–63PubMed Dressler J, Busuttil A, Koch R, Harrison DJ (2001) Sequence of melanocyte migration into human scar tissue. Int J Legal Med 115:61–63PubMed
Metadata
Title
Immunohistochemical analysis on aquaporin-1 and aquaporin-3 in skin wounds from the aspects of wound age determination
Authors
Yuko Ishida
Yumi Kuninaka
Fukumi Furukawa
Akihiko Kimura
Mizuho Nosaka
Mie Fukami
Hiroki Yamamoto
Takashi Kato
Emi Shimada
Satoshi Hata
Tatsunori Takayasu
Wolfgang Eisenmenger
Toshikazu Kondo
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Legal Medicine / Issue 1/2018
Print ISSN: 0937-9827
Electronic ISSN: 1437-1596
DOI
https://doi.org/10.1007/s00414-017-1725-0

Other articles of this Issue 1/2018

International Journal of Legal Medicine 1/2018 Go to the issue