Hyaluronan: A key player or just a bystander in skin photoaging?

. 2022 Apr ; 31 (4) : 442-458. [epub] 20211115

Jazyk angličtina Země Dánsko Médium print-electronic

Typ dokumentu časopisecké články, přehledy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34726319

Photoaged skin exhibits signs of inflammation, DNA damage and changes in morphology that are visible at the macroscopic and microscopic levels. Photoaging also affects the extracellular matrix (ECM) including hyaluronan (HA), the main polysaccharide component thereof. HA is a structurally simple but biologically complex molecule that serves as a water-retaining component and provides both a scaffold for a number of the proteins of the ECM and the ligand for cellular receptors. The study provides an overview of the literature concerning the changes in HA amount, size and metabolism, and the potential role of HA in photoaging. We also suggest novel HA contributions to photoaging based on our knowledge of the role of HA in other pathological processes, including the senescence and inflammation-triggered ECM reorganization. Moreover, we discuss potential direct or indirect intervention to mitigate photoaging that targets the hyaluronan metabolism, as well as supplementation.

Zobrazit více v PubMed

Li WH, Wong HK, Serrano J, et al. Topical stabilized retinol treatment induces the expression of HAS genes and HA production in human skin in vitro and in vivo. Arch Dermatol Res. 2017;309(4):275-283.

Kawada C, Kimura M, Masuda Y, Nomura Y. Oral administration of hyaluronan prevents skin dryness and epidermal thickening in ultraviolet irradiated hairless mice. J Photochem Photobiol B. 2015;153:215-221.

Papakonstantinou E, Roth M, Karakiulakis G. Hyaluronic acid: a key molecule in skin aging. Dermatoendocrinol. 2012;4(3):253-258.

Lee DH, Oh JH, Chung JH. Glycosaminoglycan and proteoglycan in skin aging. J. Dermatol. Sci. 2016;83(3):174-181.

McDaniel D, Farris P, Valacchi G. Atmospheric skin aging-Contributors and inhibitors. J Cosmet Dermatol. 2018;17(2):124-137.

Venkatesh S, Maymone MBC, Vashi NA. Aging in skin of color. Clin Dermatol. 2019;37(4):351-357.

Varani J, Schuger L, Dame MK, et al. Reduced fibroblast interaction with intact collagen as a mechanism for depressed collagen synthesis in photodamaged skin. J Invest Dermatol. 2004;122(6):1471-1479.

El-Domyati M, Attia S, Saleh F, et al. Intrinsic aging vs. photoaging: a comparative histopathological, immunohistochemical, and ultrastructural study of skin. Exp Dermatol. 2002;11(5):398-405.

Fernandez-Flores A, Saeb-Lima M. Histopathology of cutaneous aging. Am J Dermatopathol. 2019;41(7):469-479.

Tsuji T. Loss of dermal elastic tissue in solar elastosis. Arch Dermatol. 1980;116(4):474-475.

Sellheyer K. Pathogenesis of solar elastosis: synthesis or degradation? J Cutan Pathol. 2003;30(2):123-127.

Charoenchon N, Rhodes LE, Pilkington SM, Farrar MD, Watson REB. Differential reorganisation of cutaneous elastic fibres: a comparison of the in vivo effects of broadband ultraviolet B versus solar simulated radiation. Photochem Photobiol Sci. 2018;17(7):889-895.

Sherratt MJ, Bayley CP, Reilly SM, Gibbs NK, Griffiths CE, Watson RE. Low-dose ultraviolet radiation selectively degrades chromophore-rich extracellular matrix components. J Pathol. 2010;222(1):32-40.

Uitto J, Ryhanen L, Abraham PA, Perejda AJ. Elastin in diseases. J Invest Dermatol. 1982;79(Suppl 1):160s-168s.

Mhamdi-Ghodbani M, Starzonek C, Degenhardt S, et al. UVB damage response of dermal stem cells as melanocyte precursors compared to keratinocytes, melanocytes, and fibroblasts from human foreskin. J Photochem Photobiol B. 2021;220: 112216.

Delinasios GJ, Karbaschi M, Cooke MS, Young AR. Vitamin E inhibits the UVAI induction of "light" and "dark" cyclobutane pyrimidine dimers, and oxidatively generated DNA damage, in keratinocytes. Sci Rep. 2018;8(1):423.

Battie C, Jitsukawa S, Bernerd F, Del Bino S, Marionnet C, Verschoore M. New insights in photoaging, UVA induced damage and skin types. Exp Dermatol. 2014;23(Suppl 1):7-12.

Cadet J, Douki T, Pouget JP, Ravanat JL. Singlet oxygen DNA damage products: formation and measurement. Methods Enzymol. 2000;319:143-153.

Xu Y, Shao Y, Voorhees JJ, Fisher GJ. Oxidative inhibition of receptor-type protein-tyrosine phosphatase kappa by ultraviolet irradiation activates epidermal growth factor receptor in human keratinocytes. J Biol Chem. 2006;281(37):27389-27397.

Rittie L, Fisher GJ. UV-light-induced signal cascades and skin aging. Ageing Res Rev. 2002;1(4):705-720.

Fisher GJ, Talwar HS, Lin J, et al. Retinoic acid inhibits induction of c-Jun protein by ultraviolet radiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo. J Clin Investig. 1998;101(6):1432-1440.

Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S, Voorhees JJ. Pathophysiology of premature skin aging induced by ultraviolet light. N Engl J Med. 1997;337(20):1419-1428.

Chou YC, Sheu JR, Chung CL, et al. Nuclear-targeted inhibition of NF-kappaB on MMP-9 production by N-2-(4-bromophenyl) ethyl caffeamide in human monocytic cells. Chem Biol Interact. 2010;184(3):403-412.

Jariashvili K, Madhan B, Brodsky B, Kuchava A, Namicheishvili L, Metreveli N. UV damage of collagen: insights from model collagen peptides. Biopolymers. 2012;97(3):189-198.

Varani J, Perone P, Fligiel SE, Fisher GJ, Voorhees JJ. Inhibition of type I procollagen production in photodamage: correlation between presence of high molecular weight collagen fragments and reduced procollagen synthesis. J Invest Dermatol. 2002;119(1):122-129.

Varani J, Spearman D, Perone P, et al. Inhibition of type I procollagen synthesis by damaged collagen in photoaged skin and by collagenase-degraded collagen in vitro. Am J Pathol. 2001;158(3):931-942.

Varani J, Dame MK, Rittie L, et al. Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am J Pathol. 2006;168(6):1861-1868.

Quan T, He T, Kang S, Voorhees JJ, Fisher GJ. Solar ultraviolet irradiation reduces collagen in photoaged human skin by blocking transforming growth factor-beta type II receptor/Smad signaling. Am J Pathol. 2004;165(3):741-751.

Selyanin MA, Boykov PY, Khabarov VN, Polyak F. The history of hyaluronic acid discovery, foundational research and initial use. Hyaluronic Acid. 2015;1-8.

Laurent TC, Fraser JR. Hyaluronan. FASEB J. 1992;6(7):2397-2404.

Huerta Angeles G, Nesporova K. Hyaluronan and its derivatives for ophthalmology: Recent advances and future perspectives. Carbohydr Polym. 2021;259:117697.

West DC, Shaw DM, Lorenz P, Adzick NS, Longaker MT. Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan. Int J Biochem Cell Biol. 1997;29(1):201-210.

Juhlin L. Hyaluronan in skin. J Intern Med. 1997;242(1):61-66.

Frenkel JS. The role of hyaluronan in wound healing. Int Wound J. 2014;11(2):159-163.

Ghersetich I, Lotti T, Campanile G, Grappone C, Dini G. Hyaluronic acid in cutaneous intrinsic aging. Int J Dermatol. 1994;33(2):119-122.

Petrey AC, de la Motte CA. Hyaluronan, a crucial regulator of inflammation. Front Immunol. 2014;5:101.

Pardue EL, Ibrahim S, Ramamurthi A. Role of hyaluronan in angiogenesis and its utility to angiogenic tissue engineering. Organogenesis. 2008;4(4):203-214.

Blundell CD, Almond A, Mahoney DJ, DeAngelis PL, Campbell ID, Day AJ. Towards a structure for a TSG-6.hyaluronan complex by modeling and NMR spectroscopy: insights into other members of the link module superfamily. J Biol Chem. 2005;280(18):18189-18201.

Seyfried NT, McVey GF, Almond A, Mahoney DJ, Dudhia J, Day AJ. Expression and purification of functionally active hyaluronan-binding domains from human cartilage link protein, aggrecan and versican: formation of ternary complexes with defined hyaluronan oligosaccharides. J Biol Chem. 2005;280(7):5435-5448.

Itano N, Sawai T, Yoshida M, et al. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J Biol Chem. 1999;274(35):25085-25092.

Nagaoka A, Yoshida H, Nakamura S, et al. Regulation of hyaluronan (HA) metabolism mediated by HYBID (Hyaluronan-binding protein involved in HA depolymerization, KIAA1199) and HA synthases in growth factor-stimulated fibroblasts. J Biol Chem. 2015;290(52):30910-30923.

Pasonen-Seppanen S, Karvinen S, Torronen K, et al. EGF upregulates, whereas TGF-beta downregulates, the hyaluronan synthases Has2 and Has3 in organotypic keratinocyte cultures: correlations with epidermal proliferation and differentiation. J Invest Dermatol. 2003;120(6):1038-1044.

Sayo T, Sugiyama Y, Takahashi Y, et al. Hyaluronan synthase 3 regulates hyaluronan synthesis in cultured human keratinocytes. J Invest Dermatol. 2002;118(1):43-48.

Sayo T, Sugiyama Y, Inoue S. Lutein, a nonprovitamin A, activates the retinoic acid receptor to induce HAS3-dependent hyaluronan synthesis in keratinocytes. Biosci Biotechnol Biochem. 2013;77(6):1282-1286.

Yoshida H, Nagaoka A, Komiya A, et al. Reduction of hyaluronan and increased expression of HYBID (alias CEMIP and KIAA1199) correlate with clinical symptoms in photoaged skin. Br J Dermatol. 2018;179(1):136-144.

Rauhala L, Hamalainen L, Salonen P, et al. Low dose ultraviolet B irradiation increases hyaluronan synthesis in epidermal keratinocytes via sequential induction of hyaluronan synthases Has1-3 mediated by p38 and Ca2+/calmodulin-dependent protein kinase II (CaMKII) signaling. J Biol Chem. 2013;288(25):17999-18012.

Averbeck M, Gebhardt CA, Voigt S, et al. Differential regulation of hyaluronan metabolism in the epidermal and dermal compartments of human skin by UVB irradiation. J Invest Dermatol. 2007;127(3):687-697.

Kakizaki I, Itano N, Kimata K, et al. Up-regulation of hyaluronan synthase genes in cultured human epidermal keratinocytes by UVB irradiation. Arch Biochem Biophys. 2008;471(1):85-93.

Meyer LJ, Stern R. Age-dependent changes of hyaluronan in human skin. J Invest Dermatol. 1994;102(3):385-389.

Werth BB, Bashir M, Chang L, Werth VP. Ultraviolet irradiation induces the accumulation of chondroitin sulfate, but not other glycosaminoglycans, in human skin. PLoS One. 2011;6(8):e14830.

Iriyama S, Nishikawa S, Hosoi J, Amano S. Basement membrane helps maintain epidermal hyaluronan content. Am J Pathol. 2021;191(6):1010-1019.

Sharma MR, Werth B, Werth VP. Animal models of acute photodamage: comparisons of anatomic, cellular and molecular responses in C57BL/6J, SKH1 and Balb/c mice. Photochem Photobiol. 2011;87(3):690-698.

Calikoglu E, Sorg O, Tran C, et al. UVA and UVB decrease the expression of CD44 and hyaluronate in mouse epidermis, which is counteracted by topical retinoids. Photochem Photobiol. 2006;82(5):1342-1347.

Dai G, Freudenberger T, Zipper P, et al. Chronic ultraviolet B irradiation causes loss of hyaluronic acid from mouse dermis because of down-regulation of hyaluronic acid synthases. Am J Pathol. 2007;171(5):1451-1461.

Fraser JR, Laurent TC, Laurent UB. Hyaluronan: its nature, distribution, functions and turnover. J Intern Med. 1997;242(1):27-33.

Roden L, Campbell P, Fraser JR, Laurent TC, Pertoft H, Thompson JN. Enzymic pathways of hyaluronan catabolism. Ciba Found Symp. 1989;143:60-76; discussion 76-86, 281-285.

Lepperdinger G, Strobl B, Kreil G. HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity. J Biol Chem. 1998;273(35):22466-22470.

Chichibu K, Matsuura T, Shichijo S, Yokoyama MM. Assay of serum hyaluronic acid in clinical application. Clin Chim Acta. 1989;181(3):317-323.

Malaisse J, Evrard C, Feret D, et al. Hyaluronidase-1 Is mainly functional in the upper granular layer, close to the epidermal barrier. J Invest Dermatol. 2015;135(12):3189-3192.

Chowdhury B, Hemming R, Faiyaz S, Triggs-Raine B. Hyaluronidase 2 (HYAL2) is expressed in endothelial cells, as well as some specialized epithelial cells, and is required for normal hyaluronan catabolism. Histochem Cell Biol. 2016;145(1):53-66.

Kurdykowski S, Mine S, Bardey V, et al. Ultraviolet-B irradiation induces differential regulations of hyaluronidase expression and activity in normal human keratinocytes. Photochem Photobiol. 2011;87(5):1105-1112.

Zhang W, Yin G, Zhao H, et al. Secreted KIAA1199 promotes the progression of rheumatoid arthritis by mediating hyaluronic acid degradation in an ANXA1-dependent manner. Cell Death Dis. 2021;12(1):102.

Yoshida H, Nagaoka A, Kusaka-Kikushima A, et al. KIAA1199, a deafness gene of unknown function, is a new hyaluronan binding protein involved in hyaluronan depolymerization. Proc Natl Acad Sci USA. 2013;110(14):5612-5617.

Yoshino Y, Goto M, Hara H, Inoue S. The role and regulation of TMEM2 (transmembrane protein 2) in HYBID (hyaluronan (HA)-binding protein involved in HA depolymerization/ KIAA1199/CEMIP)-mediated HA depolymerization in human skin fibroblasts. Biochem Biophys Res Comm. 2018;505(1):74-80.

Yamamoto H, Tobisawa Y, Inubushi T, Irie F, Ohyama C, Yamaguchi Y. A mammalian homolog of the zebrafish transmembrane protein 2 (TMEM2) is the long-sought-after cell-surface hyaluronidase. J Biol Chem. 2017;292(18):7304-7313.

Yamazaki K, Fukuda K, Matsukawa M, et al. Reactive oxygen species depolymerize hyaluronan: involvement of the hydroxyl radical. Pathophysiology. 2003;9(4):215-220.

Tzellos TG, Klagas I, Vahtsevanos K, et al. Extrinsic ageing in the human skin is associated with alterations in the expression of hyaluronic acid and its metabolizing enzymes. Exp Dermatol. 2009;18(12):1028-1035.

Tobiishi M, Sayo T, Yoshida H, et al. Changes in epidermal hyaluronan metabolism following UVB irradiation. J Dermatol Sci. 2011;64(1):31-38.

Bernstein EF, Fisher LW, Li K, LeBaron RG, Tan EM, Uitto J. Differential expression of the versican and decorin genes in photoaged and sun-protected skin. Comparison by immunohistochemical and northern analyses. Lab Invest. 1995;72(6):662-669.

Terazawa S, Takada M, Sato Y, Nakajima H, Imokawa G. The attenuated secretion of hyaluronan by UVA-exposed human fibroblasts is associated with up- and downregulation of HYBID and HAS2 expression via activated and inactivated signaling of the p38/ATF2 and JAK2/STAT3 cascades. Int J Mol Sci. 2021;22(4):2057.

Weiss JM, Renkl AC, Ahrens T, et al. Activation-dependent modulation of hyaluronate-receptor expression and of hyaluronate-avidity by human monocytes. J Invest Dermatol. 1998;111(2):227-232.

Cyphert JM, Trempus CS, Garantziotis S. Size Matters: Molecular Weight Specificity of Hyaluronan Effects in Cell Biology. Int J Cell Biol. 2015;2015:1-8.

Wang C, Tammi M, Tammi R. Distribution of hyaluronan and its CD44 receptor in the epithelia of human skin appendages. Histochemistry. 1992;98(2):105-112.

Tzellos TG, Sinopidis X, Kyrgidis A, et al. Differential hyaluronan homeostasis and expression of proteoglycans in juvenile and adult human skin. J Dermatol Sci. 2011;61(1):69-72.

Kouvidi K, Berdiaki A, Tzardi M, et al. Receptor for hyaluronic acid- mediated motility (RHAMM) regulates HT1080 fibrosarcoma cell proliferation via a beta-catenin/c-myc signaling axis. Biochem Biophys Acta. 2016;1860(4):814-824.

Samuel SK, Hurta RA, Spearman MA, Wright JA, Turley EA, Greenberg AH. TGF-beta 1 stimulation of cell locomotion utilizes the hyaluronan receptor RHAMM and hyaluronan. J Cell Biol. 1993;123(3):749-758.

Banerji S, Ni J, Wang SX, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol. 1999;144(4):789-801.

Tripp CH, Haid B, Flacher V, et al. The lymph vessel network in mouse skin visualised with antibodies against the hyaluronan receptor LYVE-1. Immunobiology. 2008;213(9-10):715-728.

Matsunaga T, Katayama I, Yokozeki H, Nishioka K. ICAM-1 expression on keratinocytes in mechanically-injured skin of a patient with atopic dermatitis. J Dermatol Sci. 1996;12(3):219-226.

Toussaint O, Medrano EE, von Zglinicki T. Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp Gerontol. 2000;35(8):927-945.

Gorgoulis V, Adams PD, Alimonti A, et al. Cellular senescence: defining a path forward. Cell. 2019;179(4):813-827.

Ogata Y, Yamada T, Hasegawa S, et al. SASP-induced macrophage dysfunction may contribute to accelerated senescent fibroblast accumulation in the dermis. Exp Dermatol. 2021;30(1):84-91.

Yoshioka H, Yamada T, Hasegawa S, et al. Senescent cell removal via JAG1-NOTCH1 signalling in the epidermis. Exp Dermatol. 2021;30(9):1268-1278.

Coppe JP, Patil CK, Rodier F, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 2008;6(12):2853-2868.

Wiley CD, Flynn JM, Morrissey C, et al. Analysis of individual cells identifies cell-to-cell variability following induction of cellular senescence. Aging Cell. 2017;16(5):1043-1050.

Acosta JC, Banito A, Wuestefeld T, et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat Cell Biol. 2013;15(8):978-990.

Kemp MG, Spandau DF, Travers JB. Impact of age and insulin-like growth factor-1 on DNA damage responses in UV-irradiated human skin. Molecules. 2017;22(3):356.

Debacq-Chainiaux F, Leduc C, Verbeke A, Toussaint O. UV, stress and aging. Dermatoendocrinol. 2012;4(3):236-240.

Sha J, Arbesman J, Harter ML. Premature senescence in human melanocytes after exposure to solar UVR: an exosome and UV-miRNA connection. Pigment Cell Melanoma Res. 2020;33(5):671-684.

Wang AS, Ong PF, Chojnowski A, Clavel C, Dreesen O. Loss of lamin B1 is a biomarker to quantify cellular senescence in photoaged skin. Sci Rep. 2017;7(1):15678.

Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA. 1995;92(20):9363-9367.

Ressler S, Bartkova J, Niederegger H, et al. p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell. 2006;5(5):379-389.

Hasova M, Crhak T, Safrankova B, et al. Hyaluronan minimizes effects of UV irradiation on human keratinocytes. Arch Dermatol Res. 2011;303(4):277-284.

Rock K, Tigges J, Sass S, et al. miR-23a-3p causes cellular senescence by targeting hyaluronan synthase 2: possible implication for skin aging. J Invest Dermatol. 2015;135(2):369-377.

Li Y, Liang J, Yang T, et al. Hyaluronan synthase 2 regulates fibroblast senescence in pulmonary fibrosis. Matrix Biol. 2016;55:35-48.

Komori R, Taniguchi M, Ichikawa Y, et al. Ultraviolet A induces endoplasmic reticulum stress response in human dermal fibroblasts. Cell Struct Funct. 2012;37(1):49-53.

Schinzel RT, Higuchi-Sanabria R, Shalem O, et al. The Hyaluronidase, TMEM2, Promotes ER Homeostasis and Longevity Independent of the UPR(ER). Cell. 2019;179(6):1306-1318 e18.

Braude S, Holtze S, Begall S, et al. Surprisingly long survival of premature conclusions about naked mole-rat biology. Biol Rev Camb Philos Soc. 2021;96(2):376-393.

Zhao Y, Tyshkovskiy A, Munoz-Espin D, et al. Naked mole rats can undergo developmental, oncogene-induced and DNA damage-induced cellular senescence. Proc Natl Acad Sci USA. 2018;115(8):1801-1806.

Zhao H, Tanaka T, Mitlitski V, Heeter J, Balazs EA, Darzynkiewicz Z. Protective effect of hyaluronate on oxidative DNA damage in WI-38 and A549 cells. Int J Oncol. 2008;32(6):1159-1167.

Campo GM, Avenoso A, Campo S, D'Ascola A, Ferlazzo AM, Calatroni A. Reduction of DNA fragmentation and hydroxyl radical production by hyaluronic acid and chondroitin-4-sulphate in iron plus ascorbate-induced oxidative stress in fibroblast cultures. Free Radic Res. 2004;38(6):601-611.

Chen Q, Ames BN. Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proc Natl Acad Sci USA. 1994;91(10):4130-4134.

Cirillo N, Vicidomini A, McCullough M, et al. A hyaluronic acid-based compound inhibits fibroblast senescence induced by oxidative stress in vitro and prevents oral mucositis in vivo. J Cell Physiol. 2015;230(7):1421-1429.

Pauloin T, Dutot M, Joly F, Warnet JM, Rat P. High molecular weight hyaluronan decreases UVB-induced apoptosis and inflammation in human epithelial corneal cells. Mol Vis. 2009;15:577-583.

Shen YN, Shin HJ, Joo HY, et al. Inhibition of HAS2 induction enhances the radiosensitivity of cancer cells via persistent DNA damage. Biochem Biophys Res Commun. 2014;443(3):796-801.

Anuja K, Chowdhury AR, Saha A, et al. Radiation-induced DNA damage response and resistance in colorectal cancer stem-like cells. Int J Radiat Biol. 2019;95(6):667-679.

Ma JW, Wang X, Chang L, et al. CD44 collaborates with ERBB2 mediate radiation resistance via p38 phosphorylation and DNA homologous recombination pathway in prostate cancer. Exp Cell Res. 2018;370(1):58-67.

Li M, Sun J, Zhang W, Zhao Y, Zhang S, Zhang S. Drug delivery systems based on CD44-targeted glycosaminoglycans for cancer therapy. Carbohydr Polym. 2021;251:117103.

Lompardia SL, Papademetrio DL, Mascaro M, Alvarez EM, Hajos SE. Human leukemic cell lines synthesize hyaluronan to avoid senescence and resist chemotherapy. Glycobiology. 2013;23(12):1463-1476.

Lompardia S, Diaz M, Pibuel M, et al. Hyaluronan abrogates imatinib-induced senescence in chronic myeloid leukemia cell lines. Sci Rep. 2019;9(1):10930.

Wang Y, Lauer ME, Anand S, Mack JA, Maytin EV. Hyaluronan synthase 2 protects skin fibroblasts against apoptosis induced by environmental stress. J Biol Chem. 2014;289(46):32253-32265.

Kular JK, Basu S, Sharma RI. The extracellular matrix: structure, composition, age-related differences, tools for analysis and applications for tissue engineering. J Tissue Eng. 2014;5:2041731414557112.

Rock K, Grandoch M, Majora M, Krutmann J, Fischer JW. Collagen fragments inhibit hyaluronan synthesis in skin fibroblasts in response to ultraviolet B (UVB): new insights into mechanisms of matrix remodeling. J Biol Chem. 2011;286(20):18268-18276.

Roberts AB, McCune BK, Sporn MB. TGF-beta: regulation of extracellular matrix. Kidney Int. 1992;41(3):557-559.

Quan T, He T, Kang S, Voorhees JJ, Fisher GJ. Ultraviolet irradiation alters transforming growth factor beta/smad pathway in human skin in vivo. J Invest Dermatol. 2002;119(2):499-506.

Callaghan TM, Wilhelm KP. A review of ageing and an examination of clinical methods in the assessment of ageing skin. Part 2: Clinical perspectives and clinical methods in the evaluation of ageing skin. Int J Cosmet Sci. 2008;30(5):323-332.

Bosch R, Philips N, Suarez-Perez JA, et al. Mechanisms of photoaging and cutaneous photocarcinogenesis, and photoprotective strategies with phytochemicals. Antioxidants (Basel). 2015;4(2):248-268.

Athar M, An KP, Morel KD, et al. Ultraviolet B(UVB)-induced cox-2 expression in murine skin: an immunohistochemical study. Biochem Biophys Res Commun. 2001;280(4):1042-1047.

Ruppert SM, Hawn TR, Arrigoni A, Wight TN, Bollyky PL. Tissue integrity signals communicated by high-molecular weight hyaluronan and the resolution of inflammation. Immunol Res. 2014;58(2-3):186-192.

Day AJ, Prestwich GD. Hyaluronan-binding proteins: tying up the giant. J Biol Chem. 2002;277(7):4585-4588.

Day AJ, de la Motte CA. Hyaluronan cross-linking: a protective mechanism in inflammation? Trends Immunol. 2005;26(12):637-643.

Tan KT, McGrouther DA, Day AJ, Milner CM, Bayat A. Characterization of hyaluronan and TSG-6 in skin scarring: differential distribution in keloid scars, normal scars and unscarred skin. J Eur Acad Dermatol Venereol. 2011;25(3):317-327.

Mahoney DJ, Mulloy B, Forster MJ, et al. Characterization of the interaction between tumor necrosis factor-stimulated gene-6 and heparin: implications for the inhibition of plasmin in extracellular matrix microenvironments. J Biol Chem. 2005;280(29):27044-27055.

Szanto S, Bardos T, Gal I, Glant TT, Mikecz K. Enhanced neutrophil extravasation and rapid progression of proteoglycan-induced arthritis in TSG-6-knockout mice. Arthritis Rheum. 2004;50(9):3012-3022.

Rijken F, Kiekens RC, van den Worm E, Lee PL, van Weelden H, Bruijnzeel PL. Pathophysiology of photoaging of human skin: focus on neutrophils. Photochem Photobiol Sci. 2006;5(2):184-189.

Hirakawa S, Fujii S, Kajiya K, Yano K, Detmar M. Vascular endothelial growth factor promotes sensitivity to ultraviolet B-induced cutaneous photodamage. Blood. 2005;105(6):2392-2399.

Ghose S, Biswas S, Datta K, Tyagi RK. Dynamic hyaluronan drives liver endothelial cells towards angiogenesis. BMC Cancer. 2018;18(1):648.

Yoshida H, Okada Y. Role of HYBID (hyaluronan binding protein involved in hyaluronan depolymerization), Alias KIAA1199/CEMIP, in hyaluronan degradation in normal and photoaged skin. Int J Mol Sci. 2019;20(22):5804.

Sato S, Mizutani Y, Yoshino Y, et al. Pro-inflammatory cytokines suppress HYBID (hyaluronan (HA) -binding protein involved in HA depolymerization/KIAA1199/CEMIP) -mediated HA metabolism in human skin fibroblasts. Biochem Biophys Res Commun. 2021;539:77-82.

Kawada C, Kimura M, Masuda Y, Nomura Y. Orally administered hyaluronan affects skin dryness and epidermal thickening in photoaged hairless mice. Biosci Biotechnol Biochem. 2016;80(6):1192-1195.

Yun MK, Lee SJ, Song HJ, et al. protein expression level of skin wrinkle-related factors in hairless mice fed hyaluronic acid. J Med Food. 2017;20(4):420-424.

Balogh L, Polyak A, Mathe D, et al. Absorption, uptake and tissue affinity of high-molecular-weight hyaluronan after oral administration in rats and dogs. J Agric Food Chem. 2008;56(22):10582-10593.

Oe M, Mitsugi K, Odanaka W, et al. Dietary hyaluronic acid migrates into the skin of rats. Scientific World J. 2014;2014:1-8.

Lee B, Lee JH, Lee HS, et al. Glycosaminoglycan degradation-inhibitory lactic acid bacteria ameliorate 2,4,6-trinitrobenzenesulfonic acid-induced colitis in mice. J Microbiol Biotechnol. 2009;19(6):616-621.

Luke HJ, Prehm P. Synthesis and shedding of hyaluronan from plasma membranes of human fibroblasts and metastatic and non-metastatic melanoma cells. Biochem J. 1999;343(Pt 1):71-75.

Kimura M, Maeshima T, Kubota T, Kurihara H, Masuda Y, Nomura Y. Absorption of orally administered hyaluronan. J Med Food. 2016;19(12):1172-1179.

de la Motte CA, Kessler SP. The role of hyaluronan in innate defense responses of the intestine. Int J Cell Biol. 2015;2015:481301.

Di Cerbo A, Laurino C, Palmieri B, Iannitti T. A dietary supplement improves facial photoaging and skin sebum, hydration and tonicity modulating serum fibronectin, neutrophil elastase 2, hyaluronic acid and carbonylated proteins. J Photochem Photobiol B. 2015;144:94-103.

Gollner I, Voss W, von Hehn U, Kammerer S. Ingestion of an oral hyaluronan solution improves skin hydration, wrinkle reduction, elasticity, and skin roughness: results of a clinical study. J Evid Based Complement Altern Med. 2017;22(4):816-823.

Kaya G, Tran C, Sorg O, et al. Hyaluronate fragments reverse skin atrophy by a CD44-dependent mechanism. PLoS Med. 2006;3(12):e493.

Pavicic T, Gauglitz GG, Lersch P, et al. Efficacy of cream-based novel formulations of hyaluronic acid of different molecular weights in anti-wrinkle treatment. J Drugs Dermatol. 2011;10(9):990-1000.

Cui Y, Wang F, Voorhees JJ, Fisher GJ. Rejuvenation of aged human skin by injection of cross-linked hyaluronic acid. Plast Reconstr Surg. 2021;147(1S-2):43S-49S.

Nadra K, Andre M, Marchaud E, et al. A hyaluronic acid-based filler reduces lipolysis in human mature adipocytes and maintains adherence and lipid accumulation of long-term differentiated human preadipocytes. J Cosmet Dermatol. 2021;20(5):1474-1482.

Tolg C, Telmer P, Turley E. Specific sizes of hyaluronan oligosaccharides stimulate fibroblast migration and excisional wound repair. PLoS One. 2014;9(2):e88479.

Ghazi K, Deng-Pichon U, Warnet JM, Rat P. Hyaluronan fragments improve wound healing on in vitro cutaneous model through P2X7 purinoreceptor basal activation: role of molecular weight. PLoS One. 2012;7(11):e48351.

Pasonen-Seppanen SM, Maytin EV, Torronen KJ, et al. All-trans retinoic acid-induced hyaluronan production and hyperplasia are partly mediated by EGFR signaling in epidermal keratinocytes. J Invest Dermatol. 2008;128(4):797-807.

Bjerke DL, Li R, Price JM, et al. The vitamin A ester retinyl propionate has a unique metabolic profile and higher retinoid-related bioactivity over retinol and retinyl palmitate in human skin models. Exp Dermatol. 2021;30(2):226-236.

Patriarca MT, Barbosa de Moraes AR, Nader HB, et al. Hyaluronic acid concentration in postmenopausal facial skin after topical estradiol and genistein treatment: a double-blind, randomized clinical trial of efficacy. Menopause. 2013;20(3):336-341.

Miyazaki K, Hanamizu T, Iizuka R, Chiba K. Genistein and daidzein stimulate hyaluronic acid production in transformed human keratinocyte culture and hairless mouse skin. Skin Pharmacol Appl Skin Physiol. 2002;15(3):175-183.

Nanashima N, Horie K, Maeda H, Tomisawa T, Kitajima M, Nakamura T. Blackcurrant anthocyanins increase the levels of collagen, elastin, and hyaluronic acid in human skin fibroblasts and ovariectomized rats. Nutrients. 2018;10(4):495.

Sugiyama Y, Shimada A, Sayo T, Sakai S, Inoue S. Putative hyaluronan synthase mRNA are expressed in mouse skin and TGF-beta upregulates their expression in cultured human skin cells. J Invest Dermatol. 1998;110(2):116-121.

Kuroda K, Utani A, Hamasaki Y, Shinkai H. Up-regulation of putative hyaluronan synthase mRNA by basic fibroblast growth factor and insulin-like growth factor-1 in human skin fibroblasts. J Dermatol Sci. 2001;26(2):156-160.

Hsu MF, Chiang BH. Stimulating effects of Bacillus subtilis natto-fermented Radix astragali on hyaluronic acid production in human skin cells. J Ethnopharmacol. 2009;125(3):474-481.

Morifuji M. The beneficial role of functional food components in mitigating ultraviolet-induced skin damage. Exp Dermatol. 2019;28(Suppl 1):28-31.

Ohara H, Ichikawa S, Matsumoto H, et al. Collagen-derived dipeptide, proline-hydroxyproline, stimulates cell proliferation and hyaluronic acid synthesis in cultured human dermal fibroblasts. J Dermatol. 2010;37(4):330-338.

Sakai S, Sayo T, Kodama S, Inoue S. N-Methyl-L-serine stimulates hyaluronan production in human skin fibroblasts. Skin Pharmacol Appl Skin Physiol. 1999;12(5):276-283.

Maeda-Sano K, Gotoh M, Morohoshi T, Someya T, Murofushi H, Murakami-Murofushi K. Cyclic phosphatidic acid and lysophosphatidic acid induce hyaluronic acid synthesis via CREB transcription factor regulation in human skin fibroblasts. Biochem Biophys Acta. 2014;1841(9):1256-1263.

Sayo T, Sakai S, Inoue S. Synergistic effect of N-acetylglucosamine and retinoids on hyaluronan production in human keratinocytes. Skin Pharmacol Physiol. 2004;17(2):77-83.

Akazawa Y, Yoshida H, Endo Y, Sugita J, Yakumaru M, Sayo T. 1-Ethyl-beta-N-acetylglucosaminide increases hyaluronan production in human keratinocytes by being converted to N-acetylglucosamine via beta-N-acetylglucosaminidase-dependent manner. Biosci Biotechnol Biochem. 2021;85(6):1433-1440.

Yoshida H, Yamazaki K, Komiya A, et al. Inhibitory effects of Sanguisorba officinalis root extract on HYBID (KIAA1199)-mediated hyaluronan degradation and skin wrinkling. Int J Cosmet Sci. 2019;41(1):12-20.

Yoshida H, Yamazaki K, Komiya A, et al. Inhibition of HYBID (KIAA1199)-mediated hyaluronan degradation and anti-wrinkle effect of Geranium thunbergii extract. J Cosmet Dermatol. 2019;18(4):1052-1060.

Simek M, Nesporova K, Kocurkova A, et al. How the molecular weight affects the in vivo fate of exogenous hyaluronan delivered intravenously: A stable-isotope labelling strategy. Carbohydr Polym. 2021;263:117927.

Achbergerova E, Smejkalova D, Huerta-Angeles G, et al. In vivo monitoring of tumor distribution of hyaluronan polymeric micelles labeled or loaded with near-infrared fluorescence dye. Carbohydr Polym. 2018;198:339-347.

Safrankova B, Hermannova M, Nesporova K, Velebny V, Kubala L. Absence of differences among low, middle, and high molecular weight hyaluronan in activating murine immune cells in vitro. Int J Biol Macromol. 2018;107(Pt A):1-8.

Dong Y, Arif A, Olsson M, et al. Endotoxin free hyaluronan and hyaluronan fragments do not stimulate TNF-alpha, interleukin-12 or upregulate co-stimulatory molecules in dendritic cells or macrophages. Sci Rep. 2016;6:36928.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...