Aquaporins in Skin.


Journal

Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103

Informations de publication

Date de publication:
2023
Historique:
entrez: 30 1 2023
pubmed: 31 1 2023
medline: 2 2 2023
Statut: ppublish

Résumé

The skin is the largest organ of our body and plays a protective role against the external environment. The skin functions as a mechanical and water permeability barrier, assisting with thermoregulation and defending our body against a variety of stresses such as ultraviolet radiation, microbial infection, physical injuries, and chemical hazards. The structure of the skin consists of three main layers: the hypodermis, the dermis, and the epidermis. Aquaporins (AQPs) are a family of integral membrane proteins whose function is to regulate intracellular fluid hemostasis by facilitating the transportation of water, and in some cases small molecules, across the cell membranes. Up to six different AQPs (AQP1, 3, 5, 7, 9, and 10) are expressed in a variety of cell types in the skin. The AQP family plays an important role in these various locations, contributing to many key functions of the skin including hydration, wound healing, and immune responses. The involvement of different aquaporin family members in skin is discussed.

Identifiants

pubmed: 36717497
doi: 10.1007/978-981-19-7415-1_15
doi:

Substances chimiques

Aquaporins 0
Water 059QF0KO0R

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

211-223

Informations de copyright

© 2023. The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

Références

Slominski AT, Zmijewski MA, Skobowiat C, Zbytek B, Slominski RM, Steketee JD (2012) Sensing the environment: regulation of local and global homeostasis by the skin's neuroendocrine system. Adv Anat Embryol Cell Biol 212:v, vii, 1–115
Verkman AS, Mitra AK (2000) Structure and function of aquaporin water channels. Am J Physiol Renal Physiol 278(1):F13–F28
Boury-Jamot M, Sougrat R, Tailhardat M, Le Varlet B, Bonte F, Dumas M, Verbavatz JM (2006) Expression and function of aquaporins in human skin: is aquaporin-3 just a glycerol transporter? Biochim Biophys Acta 1758(8):1034–1042
Blaydon DC, Lind LK, Plagnol V, Linton KJ, Smith FJ, Wilson NJ, McLean WH, Munro CS, South AP, Leigh IM, O'Toole EA, Lundstrom A, Kelsell DP (2013) Mutations in AQP5, encoding a water-channel protein, cause autosomal-dominant diffuse nonepidermolytic palmoplantar keratoderma. Am J Hum Genet 93(2):330–335
Hara-Chikuma M, Sugiyama Y, Kabashima K, Sohara E, Uchida S, Sasaki S, Inoue S, Miyachi Y (2012) Involvement of aquaporin-7 in the cutaneous primary immune response through modulation of antigen uptake and migration in dendritic cells. FASEB J 26(1):211–218
Patel R, Kevin Heard L, Chen X, Bollag WB (2017) Aquaporins in the skin. Adv Exp Med Biol 969:173–191
Slominski AT, Zmijewski MA, Plonka PM, Szaflarski JP, Paus R (2018) How UV light touches the brain and endocrine system through skin, and why. Endocrinology 159(5):1992–2007
Bollag WB, Aitkens L, White J, Hyndman KA (2020) Aquaporin-3 in the epidermis: more than skin deep. Am J Physiol Cell Physiol 318(6):C1144–C1153
Atkinson SD, McGilligan VE, Liao H, Szeverenyi I, Smith FJ, Moore CB, McLean WH (2011) Development of allele-specific therapeutic siRNA for keratin 5 mutations in epidermolysis bullosa simplex. J Invest Dermatol 131(10):2079–2086
Miller EW, Dickinson BC, Chang CJ (2010) Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci U S A 107(36):15681–15686
Hara-Chikuma M, Chikuma S, Sugiyama Y, Kabashima K, Verkman AS, Inoue S, Miyachi Y (2012) Chemokine-dependent T cell migration requires aquaporin-3-mediated hydrogen peroxide uptake. J Exp Med 209(10):1743–1752
Hara-Chikuma M, Satooka H, Watanabe S, Honda T, Miyachi Y, Watanabe T, Verkman AS (2015) Aquaporin-3-mediated hydrogen peroxide transport is required for NF-kappaB signalling in keratinocytes and development of psoriasis. Nat Commun 6:7454
Hara-Chikuma M, Verkman AS (2008) Roles of aquaporin-3 in the epidermis. J Invest Dermatol 128(9):2145–2151
Marchini G, Stabi B, Kankes K, Lonne-Rahm S, Ostergaard M, Nielsen S (2003) AQP1 and AQP3, psoriasin, and nitric oxide synthases 1-3 are inflammatory mediators in erythema toxicum neonatorum. Pediatr Dermatol 20(5):377–384
Voss KE, Bollag RJ, Fussell N, By C, Sheehan DJ, Bollag WB (2011) Abnormal aquaporin-3 protein expression in hyperproliferative skin disorders. Arch Dermatol Res 303(8):591–600
Garcia N, Gondran C, Menon G, Mur L, Oberto G, Guerif Y, Dal Farra C, Domloge N (2011) Impact of AQP3 inducer treatment on cultured human keratinocytes, ex vivo human skin and volunteers. Int J Cosmet Sci 33(5):432–442
Agren J, Zelenin S, Svensson LB, Nejsum LN, Nielsen S, Aperia A, Sedin G (2010) Antenatal corticosteroids and postnatal fluid restriction produce differential effects on AQP3 expression, water handling, and barrier function in perinatal rat epidermis. Dermatol Res Pract 2010:789729
Jungersted JM, Bomholt J, Bajraktari N, Hansen JS, Klaerke DA, Pedersen PA, Hedfalk K, Nielsen KH, Agner T, Helix-Nielsen C (2013) In vivo studies of aquaporins 3 and 10 in human stratum corneum. Arch Dermatol Res 305(8):699–704
Zheng X, Bollinger Bollag W (2003) Aquaporin 3 colocates with phospholipase d2 in caveolin-rich membrane microdomains and is downregulated upon keratinocyte differentiation. J Invest Dermatol 121(6):1487–1495
Qin H, Zheng X, Zhong X, Shetty AK, Elias PM, Bollag WB (2011) Aquaporin-3 in keratinocytes and skin: its role and interaction with phospholipase D2. Arch Biochem Biophys 508(2):138–143
Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327
Sugiyama Y, Yamazaki K, Kusaka-Kikushima A, Nakahigashi K, Hagiwara H, Miyachi Y (2014) Analysis of aquaporin 9 expression in human epidermis and cultured keratinocytes. FEBS Open Bio 4:611–616
Leitch V, Agre P, King LS (2001) Altered ubiquitination and stability of aquaporin-1 in hypertonic stress. Proc Natl Acad Sci U S A 98(5):2894–2898
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(48):46616–46621
Hara M, Verkman AS (2003) Glycerol replacement corrects defective skin hydration, elasticity, and barrier function in aquaporin-3-deficient mice. Proc Natl Acad Sci U S A 100(12):7360–7365
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(19):17147–17153
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(3):245–252
Hara-Chikuma M, Verkman AS (2008) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J Mol Med (Berl) 86(2):221–231
Hara-Chikuma M, Verkman AS (2008) Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol Cell Biol 28(1):326–332
Nakahigashi K, Kabashima K, Ikoma A, Verkman AS, Miyachi Y, Hara-Chikuma M (2011) Upregulation of aquaporin-3 is involved in keratinocyte proliferation and epidermal hyperplasia. J Invest Dermatol 131(4):865–873
Guo L, Chen H, Li Y, Zhou Q, Sui Y (2013) An aquaporin 3-notch1 axis in keratinocyte differentiation and inflammation. PLoS One 8(11):e80179
Marlar S, Jensen HH, Login FH, Nejsum LN (2017) Aquaporin-3 in Cancer. Int J Mol Sci 18(10):2106
Xie D, Seremwe M, Edwards JG, Podolsky R, Bollag WB (2014) Distinct effects of different phosphatidylglycerol species on mouse keratinocyte proliferation. PLoS One 9(9):e107119
Bollag WB, Xie D, Zheng X, Zhong X (2007) A potential role for the phospholipase D2-aquaporin-3 signaling module in early keratinocyte differentiation: production of a phosphatidylglycerol signaling lipid. J Invest Dermatol 127(12):2823–2831
Choudhary V, Olala LO, Qin H, Helwa I, Pan ZQ, Tsai YY, Frohman MA, Kaddour-Djebbar I, Bollag WB (2015) Aquaporin-3 re-expression induces differentiation in a phospholipase D2-dependent manner in aquaporin-3-knockout mouse keratinocytes. J Invest Dermatol 135(2):499–507
Kim NH, Lee AY (2010) Reduced aquaporin3 expression and survival of keratinocytes in the depigmented epidermis of vitiligo. J Invest Dermatol 130(9):2231–2239
Jiang YJ, Kim P, Lu YF, Feingold KR (2011) PPARgamma activators stimulate aquaporin 3 expression in keratinocytes/epidermis. Exp Dermatol 20(7):595–599
Thrash BR, Menges CW, Pierce RH, McCance DJ (2006) AKT1 provides an essential survival signal required for differentiation and stratification of primary human keratinocytes. J Biol Chem 281(17):12155–12162
Tu CL, Chang W, Bikle DD (2001) The extracellular calcium-sensing receptor is required for calcium-induced differentiation in human keratinocytes. J Biol Chem 276(44):41079–41085
Calautti E, Li J, Saoncella S, Brissette JL, Goetinck PF (2005) Phosphoinositide 3-kinase signaling to Akt promotes keratinocyte differentiation versus death. J Biol Chem 280(38):32856–32865
Lee Y, Je YJ, Lee SS, Li ZJ, Choi DK, Kwon YB, Sohn KC, Im M, Seo YJ, Lee JH (2012) Changes in transepidermal water loss and skin hydration according to expression of aquaporin-3 in psoriasis. Ann Dermatol 24(2):168–174
Zheng X, Ray S, Bollag WB (2003) Modulation of phospholipase D-mediated phosphatidylglycerol formation by differentiating agents in primary mouse epidermal keratinocytes. Biochim Biophys Acta 1643(1–3):25–36
Stroka KM, Jiang H, Chen SH, Tong Z, Wirtz D, Sun SX, Konstantopoulos K (2014) Water permeation drives tumor cell migration in confined microenvironments. Cell 157(3):611–623
Yin Z, Chen W, Yin J, Sun J, Xie Q, Wu M, Zeng F, Ren H (2021) RIPK1 is a negative mediator in aquaporin 1-driven triple-negative breast carcinoma progression and metastasis. NPJ Breast Cancer 7(1):53
Zhou J, Dong Y, Liu J, Ren J, Wu J, Zhu N (2020) AQP5 regulates the proliferation and differentiation of epidermal stem cells in skin aging. Braz J Med Biol Res 53(11):e10009
Song X, Xu A, Pan W, Wallin B, Kivlin R, Lu S, Cao C, Bi Z, Wan Y (2008) Nicotinamide attenuates aquaporin 3 overexpression induced by retinoic acid through inhibition of EGFR/ERK in cultured human skin keratinocytes. Int J Mol Med 22(2):229–236
Hara-Chikuma M, Sohara E, Rai T, Ikawa M, Okabe M, Sasaki S, Uchida S, Verkman AS (2005) Progressive adipocyte hypertrophy in aquaporin-7-deficient mice: adipocyte glycerol permeability as a novel regulator of fat accumulation. J Biol Chem 280(16):15493–15496
Grether-Beck S, Felsner I, Brenden H, Kohne Z, Majora M, Marini A, Jaenicke T, Rodriguez-Martin M, Trullas C, Hupe M, Elias PM, Krutmann J (2012) Urea uptake enhances barrier function and antimicrobial defense in humans by regulating epidermal gene expression. J Invest Dermatol 132(6):1561–1572
Soler DC, Bai X, Ortega L, Pethukova T, Nedorost ST, Popkin DL, Cooper KD, McCormick TS (2015) The key role of aquaporin 3 and aquaporin 10 in the pathogenesis of pompholyx. Med Hypotheses 84(5):498–503
Luo J, Liu X, Liu J, Jiang M, Luo M, Zhao J (2016) Activation of TGF-beta1 by AQP3-mediated H2O2 transport into fibroblasts of a bleomycin-induced mouse model of scleroderma. J Invest Dermatol 136(12):2372–2379
Cao C, Sun Y, Healey S, Bi Z, Hu G, Wan S, Kouttab N, Chu W, Wan Y (2006) EGFR-mediated expression of aquaporin-3 is involved in human skin fibroblast migration. Biochem J 400(2):225–234
Xie H, Liu F, Liu L, Dan J, Luo Y, Yi Y, Chen X, Li J (2013) Protective role of AQP3 in UVA-induced NHSFs apoptosis via Bcl2 up-regulation. Arch Dermatol Res 305(5):397–406
Nejsum LN, Kwon TH, Jensen UB, Fumagalli O, Frokiaer J, Krane CM, Menon AG, King LS, Agre PC, Nielsen S (2002) Functional requirement of aquaporin-5 in plasma membranes of sweat glands. Proc Natl Acad Sci U S A 99(1):511–516
Diao J, Liu J, Wang S, Chang M, Wang X, Guo B, Yu Q, Yan F, Su Y, Wang Y (2019) Sweat gland organoids contribute to cutaneous wound healing and sweat gland regeneration. Cell Death Dis 10(3):238
Inoue R, Sohara E, Rai T, Satoh T, Yokozeki H, Sasaki S, Uchida S (2013) Immunolocalization and translocation of aquaporin-5 water channel in sweat glands. J Dermatol Sci 70(1):26–33
Moniaga CS, Watanabe S, Honda T, Nielsen S, Hara-Chikuma M (2015) Aquaporin-9-expressing neutrophils are required for the establishment of contact hypersensitivity. Sci Rep 5:15319
Maeda N, Funahashi T, Shimomura I (2008) Metabolic impact of adipose and hepatic glycerol channels aquaporin 7 and aquaporin 9. Nat Clin Pract Endocrinol Metab 4(11):627–634
Hibuse T, Maeda N, Funahashi T, Yamamoto K, Nagasawa A, Mizunoya W, Kishida K, Inoue K, Kuriyama H, Nakamura T, Fushiki T, Kihara S, Shimomura I (2005) Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc Natl Acad Sci U S A 102(31):10993–10998
Stenn KS (2001) Insights from the asebia mouse: a molecular sebaceous gland defect leading to cicatricial alopecia. J Cutan Pathol 28(9):445–447
Goldsmith LA (2003) Clinical snippets. J Invest Dermatol 120(2):v
Matsunaga N, Itcho K, Hamamura K, Ikeda E, Ikeyama H, Furuichi Y, Watanabe M, Koyanagi S, Ohdo S (2014) 24-hour rhythm of aquaporin-3 function in the epidermis is regulated by molecular clocks. J Invest Dermatol 134(6):1636–1644
Ikarashi N, Kon R, Kaneko M, Mizukami N, Kusunoki Y, Sugiyama K (2017) Relationship between aging-related skin dryness and aquaporins. Int J Mol Sci 18(7):1559
Schrader A, Siefken W, Kueper T, Breitenbach U, Gatermann C, Sperling G, Biernoth T, Scherner C, Stab F, Wenck H, Wittern KP, Blatt T (2012) Effects of glyceryl glucoside on AQP3 expression, barrier function and hydration of human skin. Skin Pharmacol Physiol 25(4):192–199
Chaudhuri RK, Bojanowski K (2017) Improvement of hydration and epidermal barrier function in human skin by a novel compound isosorbide dicaprylate. Int J Cosmet Sci 39(5):518–526
Li J, Tang H, Hu X, Chen M, Xie H (2010) Aquaporin-3 gene and protein expression in sun-protected human skin decreases with skin ageing. Australas J Dermatol 51(2):106–112
Seleit I, Bakry OA, El Rebey HS, El-Akabawy G, Hamza G (2017) Is aquaporin-3 a determinant factor of intrinsic and extrinsic aging? An Immunohistochemical and morphometric study. Appl Immunohistochem Mol Morphol 25(1):49–57
Ikarashi N, Kaneko M, Watanabe T, Kon R, Yoshino M, Yokoyama T, Tanaka R, Takayama N, Sakai H, Kamei J (2020) Epidermal growth factor receptor tyrosine kinase inhibitor Erlotinib induces dry skin via decreased in aquaporin-3 expression. Biomol Ther 10(4):545
Zhang M, Zeng S, Zhang L, Li H, Chen L, Zhang X, Li X, Lin C, Shu S, Xie S, He Y, Mao X, Peng L, Shi L, Yang L, Tang S, Fu X (2014) Localization of Na(+)-K(+)-ATPase alpha/beta, Na(+)-K(+)-2Cl-cotransporter 1 and aquaporin-5 in human eccrine sweat glands. Acta Histochem 116(8):1374–1381
Xie L, Jin L, Feng J, Lv J (2017) The expression of AQP5 and UTs in the sweat glands of uremic patients. Biomed Res Int 2017:8629783
Stern RS, Nijsten T, Feldman SR, Margolis DJ, Rolstad T (2004) Psoriasis is common, carries a substantial burden even when not extensive, and is associated with widespread treatment dissatisfaction. J Investig Dermatol Symp Proc 9(2):136–139
Zenz R, Eferl R, Kenner L, Florin L, Hummerich L, Mehic D, Scheuch H, Angel P, Tschachler E, Wagner EF (2005) Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 437(7057):369–375
Seleit I, Bakry OA, Al Sharaky D, Ragheb E (2015) Evaluation of aquaporin-3 role in nonmelanoma skin cancer: an immunohistochemical study. Ultrastruct Pathol 39(5):306–317
Soler DC, Young AE, Griffith AD, Fu PF, Cooper KD, McCormick TS, Popkin DL (2017) Overexpression of AQP3 and AQP10 in the skin exacerbates psoriasiform acanthosis. Exp Dermatol 26(10):949–951
Bowcock AM, Shannon W, Du F, Duncan J, Cao K, Aftergut K, Catier J, Fernandez-Vina MA, Menter A (2001) Insights into psoriasis and other inflammatory diseases from large-scale gene expression studies. Hum Mol Genet 10(17):1793–1805
Swindell WR, Xing X, Voorhees JJ, Elder JT, Johnston A, Gudjonsson JE (2014) Integrative RNA-seq and microarray data analysis reveals GC content and gene length biases in the psoriasis transcriptome. Physiol Genomics 46(15):533–546
Choudhary V, Kaddour-Djebbar I, Custer VE, Uaratanawong R, Chen X, Cohen E, Yang R, Ajebo E, Hossack S, Bollag WB (2021) Glycerol improves skin lesion development in the imiquimod mouse model of psoriasis: experimental confirmation of anecdotal reports from patients with psoriasis. Int J Mol Sci 22(16):8749
Esmat S, Zeid OA, Abdel Halim DM, Fawzy MT, Abdel Latif M, Lazarova V, Assaf M (2018) Tissue expression of aquaporin 3 in different sites of vitiligo: an immunohistochemical study. J Eur Acad Dermatol Venereol 32(12):e455–e456
Ikarashi N, Ogiue N, Toyoda E, Kon R, Ishii M, Toda T, Aburada T, Ochiai W, Sugiyama K (2012) Gypsum fibrosum and its major component CaSO4 increase cutaneous aquaporin-3 expression levels. J Ethnopharmacol 139(2):409–413
Osorio G, Zulueta-Dorado T, Gonzalez-Rodriguez P, Bernabeu-Wittel J, Conejo-Mir J, Ramirez-Lorca R, Echevarria M (2019) Expression pattern of aquaporin 1 and aquaporin 3 in melanocytic and nonmelanocytic skin tumors. Am J Clin Pathol 152(4):446–457
Cao X, Yin J, Wang H, Zhao J, Zhang J, Dai L, Zhang J, Jiang H, Lin Z, Yang Y (2014) Mutation in AQP5, encoding aquaporin 5, causes palmoplantar keratoderma Bothnia type. J Invest Dermatol 134(1):284–287
Wada Y, Kusakabe M, Nagai M, Imai Y, Yamanishi K (2019) Japanese case of Bothnian-type palmoplantar keratoderma with a novel missense mutation of p.Trp35Ser in extracellular loop A of aquaporin-5. J Dermatol 46(3):e104–e106
Kroigard AB, Hetland LE, Clemmensen O, Blaydon DC, Hertz JM, Bygum A (2016) The first Danish family reported with an AQP5 mutation presenting diffuse non-epidermolytic palmoplantar keratoderma of Bothnian type, hyperhidrosis and frequent Corynebacterium infections: a case report. BMC Dermatol 16(1):7
Friedman AJ, von Grote EC, Meckfessel MH (2016) Urea: a clinically oriented overview from bench to bedside. J Drugs Dermatol 15(5):633–639
Yamashita T, Asano Y, Saigusa R, Taniguchi T, Nakamura K, Miura S, Toyama T, Takahashi T, Ichimura Y, Hirabayashi M, Yoshizaki A, Miyagaki T, Sugaya M, Sato S (2019) Increased expression of aquaporin-1 in dermal fibroblasts and dermal microvascular endothelial cells possibly contributes to skin fibrosis and edema in patients with systemic sclerosis. J Dermatol Sci 93(1):24–32
Farhadi E, Mahmoudi M, Rahmani F, Yousefi B, Sarafnejad A, Kavosi H, Karimizadeh E, Jamshidi A, Gharibdoost F (2019) Attenuation of aquaporin-3 and epidermal growth factor receptor expression and activation in systemic sclerosis dermal fibroblasts. J Cell Physiol 234(8):12876–12883
Sugimoto T, Huang L, Minematsu T, Yamamoto Y, Asada M, Nakagami G, Akase T, Nagase T, Oe M, Mori T, Sanada H (2013) Impaired aquaporin 3 expression in reepithelialization of cutaneous wound healing in the diabetic rat. Biol Res Nurs 15(3):347–355

Auteurs

Zhuming Yin (Z)

Department of Breast Oncoplastic Surgery, Tianjin Medical University Cancer Institute and Hospital, Tianjin, China.
National Clinical Research Center for Cancer, Tianjin, China.
Key Laboratory of Breast Cancer Prevention and Therapy, Tianjin Medical University, Ministry of Education, Tianjin, China.
Key Laboratory of Cancer Prevention and Therapy, Tianjin, China.
Tianjin's Clinical Research Center for Cancer, Tianjin, China.
Sino-Russian Joint Research Center for Oncoplastic Breast Surgery, Tianjin, China.

Huiwen Ren (H)

Department of Pharmacology, School of Basic Medical Sciences, Tianjin Medical University, Tianjin, China. renhuiwen@tmu.edu.cn.

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Classifications MeSH