Cell Surface Glycosaminoglycans as Receptors for Adhesion of Candida spp. to Corneal Cells

Esko JD, Kimata K, Lindahl U. Proteoglycans and sulfated glycosaminoglycans. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of glycobiology. Cold Spring Harbor (USA): Cold Spring Harbor Laboratory Press; 2009. EskoJD KimataK LindahlU Proteoglycans and sulfated glycosaminoglycans In: VarkiA CummingsRD EskoJD FreezeHH StanleyP BertozziCR HartGW EtzlerME editors. Essentials of glycobiology Cold Spring Harbor (USA) Cold Spring Harbor Laboratory Press 2009 Search in Google Scholar

Aquino RS, Park PW. Glycosaminoglycans and infection. Front Biosci (Landmark Ed). 2016 Jun 1;21:1260–1277. https://doi.org/10.2741/4455 AquinoRS ParkPW Glycosaminoglycans and infection Front Biosci (Landmark Ed) 2016 Jun 1 21 1260 1277 https://doi.org/10.2741/4455 10.2741/4455 Search in Google Scholar

García B, Merayo-Lloves J, Martin C, Alcalde I, Quirós LM, Vazquez F. Surface proteoglycans as mediators in bacterial pathogens infections. Front Microbiol. 2016a Feb 24;7:220. https://doi.org/10.3389/fmicb.2016.00220 GarcíaB Merayo-LlovesJ MartinC AlcaldeI QuirósLM VazquezF Surface proteoglycans as mediators in bacterial pathogens infections Front Microbiol 2016a Feb 24 7 220 https://doi.org/10.3389/fmicb.2016.00220 10.3389/fmicb.2016.00220 Search in Google Scholar

García B, Merayo-Lloves J, Rodríguez D, Alcalde I, García-Suárez O, Alfonso JF, Baamonde B, Fernández-Vega A, Vazquez F, Quirós LM. Different use of cell surface glycosaminoglycans as adherence receptors to corneal cells by Gram positive and Gram negative pathogens. Front Cell Infect Microbiol. 2016b Nov 30;6:173. https://doi.org/10.3389/fcimb.2016.00173 GarcíaB Merayo-LlovesJ RodríguezD AlcaldeI García-SuárezO AlfonsoJF BaamondeB Fernández-VegaA VazquezF QuirósLM Different use of cell surface glycosaminoglycans as adherence receptors to corneal cells by Gram positive and Gram negative pathogens Front Cell Infect Microbiol 2016b Nov 30 6 173 https://doi.org/10.3389/fcimb.2016.00173 10.3389/fcimb.2016.00173 Search in Google Scholar

Gulati K, Poluri KM. Mechanistic and therapeutic overview of glycosaminoglycans: the unsung heroes of biomolecular signaling. Glycoconj J. 2016 Feb;33(1):1–17. https://doi.org/10.1007/s10719-015-9642-2 GulatiK PoluriKM Mechanistic and therapeutic overview of glycosaminoglycans: the unsung heroes of biomolecular signaling Glycoconj J 2016 Feb 33 1 1 17 https://doi.org/10.1007/s10719-015-9642-2 10.1007/s10719-015-9642-2 Search in Google Scholar

Iozzo R V, Schaefer L. Proteoglycan form and function: A comprehensive nomenclature of proteoglycans. Matrix Biol. 2015 Mar; 42:11–55. https://doi.org/10.1016/j.matbio.2015.02.003 IozzoR V SchaeferL Proteoglycan form and function: A comprehensive nomenclature of proteoglycans Matrix Biol 2015 Mar 42 11 55 https://doi.org/10.1016/j.matbio.2015.02.003 10.1016/j.matbio.2015.02.003 Search in Google Scholar

Kaji T, Kawashima T, Sakamoto M. Rhodamine B inhibition of glycosaminoglycan production by cultured human lip fibroblasts. Toxicol Appl Pharmacol. 1991 Oct;111(1):82–89. https://doi.org/10.1016/0041-008x(91)90136-3 KajiT KawashimaT SakamotoM Rhodamine B inhibition of glycosaminoglycan production by cultured human lip fibroblasts Toxicol Appl Pharmacol 1991 Oct 111 1 82 89 https://doi.org/10.1016/0041-008x(91)90136-3 10.1016/0041-008X(91)90136-3 Search in Google Scholar

Kamhi E, Joo EJ, Dordick JS, Linhardt RJ. Glycosaminoglycans in infectious disease. Biol Rev Camb Philos Soc. 2013 Nov;88(4): 928–943. https://doi.org/10.1111/brv.12034 KamhiE JooEJ DordickJS LinhardtRJ Glycosaminoglycans in infectious disease Biol Rev Camb Philos Soc 2013 Nov 88 4 928 943 https://doi.org/10.1111/brv.12034 10.1111/brv.1203423551941 Search in Google Scholar

Kjellén L, Lindahl U. Proteoglycans: Structures and interactions. Annu Rev Biochem. 1991;60:443–475. https://doi.org/10.1146/annurev.bi.60.070191.002303 KjellénL LindahlU Proteoglycans: Structures and interactions Annu Rev Biochem 1991 60 443 475 https://doi.org/10.1146/annurev.bi.60.070191.002303 10.1146/annurev.bi.60.070191.0023031883201 Search in Google Scholar

Kobayashi M, Ishida K, Matsuo J, Nakamura S, Nagasawa A, Motohashi K, Yao T, Hirai I, Yamamoto Y, Suzuki H, et al. Chlamydophila pneumoniae attachment and infection in low proteoglycan expressing human lymphoid Jurkat cells. Microb Pathog. 2011 Sep; 51(3):209–216. https://doi.org/10.1016/j.micpath.2011.03.010 KobayashiM IshidaK MatsuoJ NakamuraS NagasawaA MotohashiK YaoT HiraiI YamamotoY SuzukiH Chlamydophila pneumoniae attachment and infection in low proteoglycan expressing human lymphoid Jurkat cells Microb Pathog 2011 Sep 51 3 209 216 https://doi.org/10.1016/j.micpath.2011.03.010 10.1016/j.micpath.2011.03.01021511028 Search in Google Scholar

Lakhundi S, Siddiqui R, Khan NA. Pathogenesis of microbial keratitis. Microb Pathog. 2017 Mar;104:97–109. https://doi.org/10.1016/j.micpath.2016.12.013 LakhundiS SiddiquiR KhanNA Pathogenesis of microbial keratitis Microb Pathog 2017 Mar 104 97 109 https://doi.org/10.1016/j.micpath.2016.12.013 10.1016/j.micpath.2016.12.01327998732 Search in Google Scholar

Leong JM, Wang H, Magoun L, Field JA, Morrissey PE, Robbins D, Tatro JB, Coburn J, Parveen N. Different classes of proteoglycans contribute to the attachment of Borrelia burgdorferi to cultured endothelial and brain cells. Infect Immun. 1998 Mar; 66(3): 994–999. https://doi.org/10.1128/IAI.66.3.994-999.1998 LeongJM WangH MagounL FieldJA MorrisseyPE RobbinsD TatroJB CoburnJ ParveenN Different classes of proteoglycans contribute to the attachment of Borrelia burgdorferi to cultured endothelial and brain cells Infect Immun 1998 Mar 66 3 994 999 https://doi.org/10.1128/IAI.66.3.994-999.1998 10.1128/IAI.66.3.994-999.19981080079488387 Search in Google Scholar

Martín C, Lozano-Iturbe V, Girón RM, Vazquez-Espinosa E, Rodriguez D, Merayo-Lloves J, Vazquez F, Quirós LM, García B. Glycosaminoglycans are differentially involved in bacterial binding to healthy and cystic fibrosis lung cells. J Cyst Fibros. 2019 May; 18(3): e19–e25. https://doi.org/10.1016/j.jcf.2018.10.017 MartínC Lozano-IturbeV GirónRM Vazquez-EspinosaE RodriguezD Merayo-LlovesJ VazquezF QuirósLM GarcíaB Glycosaminoglycans are differentially involved in bacterial binding to healthy and cystic fibrosis lung cells J Cyst Fibros 2019 May 18 3 e19 e25 https://doi.org/10.1016/j.jcf.2018.10.017 10.1016/j.jcf.2018.10.01730415947 Search in Google Scholar

Martín R, Martín C, Escobedo S, Suárez JE, Quirós LM. Surface glycosaminoglycans mediate adherence between HeLa cells and Lactobacillus salivarius Lv72. BMC Microbiol. 2013 Sep 17;13:210. https://doi.org/10.1186/1471-2180-13-210 MartínR MartínC EscobedoS SuárezJE QuirósLM Surface glycosaminoglycans mediate adherence between HeLa cells and Lactobacillus salivarius Lv72 BMC Microbiol 2013 Sep 17 13 210 https://doi.org/10.1186/1471-2180-13-210 10.1186/1471-2180-13-210384862024044741 Search in Google Scholar

Mellado F, Rojas T, Cumsille C. [Fungal keratitis: review of diagnosis and treatment] (in Spanish). Arq Bras Oftalmol. 2013 Jan–Feb; 76(1):52–56. https://doi.org/10.1590/s0004-27492013000100016 MelladoF RojasT CumsilleC [Fungal keratitis: review of diagnosis and treatment] (in Spanish) Arq Bras Oftalmol 2013 Jan–Feb 76 1 52 56 https://doi.org/10.1590/s0004-27492013000100016 10.1590/S0004-2749201300010001623812531 Search in Google Scholar

Naglik JR, Moyes DL, Wächtler B, Hube B. Candida albicans interactions with epithelial cells and mucosal immunity. Microbes Infect. 2011 Nov;13(12–13):963–976. https://doi.org/10.1016/j.micinf.2011.06.009 NaglikJR MoyesDL WächtlerB HubeB Candida albicans interactions with epithelial cells and mucosal immunity Microbes Infect 2011 Nov 13 12–13 963 976 https://doi.org/10.1016/j.micinf.2011.06.009 10.1016/j.micinf.2011.06.009318514521801848 Search in Google Scholar

Nikitovic D, Tsatsakis AM, Karamanos NK, Tzanakakis GN. The effects of genistein on the synthesis and distribution of glycosaminoglycans/proteoglycans by two osteosarcoma cell lines depends on tyrosine kinase and the estrogen receptor density. Anticancer Res. 2003 Jan–Feb;23(1A):459–464. NikitovicD TsatsakisAM KaramanosNK TzanakakisGN The effects of genistein on the synthesis and distribution of glycosaminoglycans/proteoglycans by two osteosarcoma cell lines depends on tyrosine kinase and the estrogen receptor density Anticancer Res 2003 Jan–Feb 23 1A 459 464 Search in Google Scholar

Ordiales H, Vázquez-López F, Pevida M, Vázquez-Losada B, Vázquez F, Quirós, LM, Martín C. [Glycosaminoglycans are involved in the adhesion of Candida albicans and Malassezia species to keratinocytes but not to dermal fibroblasts] (in Spanish). Actas Dermo-Sifiliogr. 2021;112(7):619–624. https://doi.org/10.1016/j.ad.2021.02.001 OrdialesH Vázquez-LópezF PevidaM Vázquez-LosadaB VázquezF QuirósLM MartínC [Glycosaminoglycans are involved in the adhesion of Candida albicans and Malassezia species to keratinocytes but not to dermal fibroblasts] (in Spanish) Actas Dermo-Sifiliogr 2021 112 7 619 624 https://doi.org/10.1016/j.ad.2021.02.001 10.1016/j.adengl.2021.05.00234052141 Search in Google Scholar

Piotrowska E, Jakóbkiewicz-Banecka J, Barańska S, Tylki-Szymańska A, Czartoryska B, Wegrzyn A, Wegrzyn G. Genistein-mediated inhibition of glycosaminoglycan synthesis as a basis for gene expression-targeted isoflavone therapy for mucopolysaccharidoses. Eur J Hum Genet. 2006 Jul;14(7):846–852. https://doi.org/10.1038/sj.ejhg.5201623 PiotrowskaE Jakóbkiewicz-BaneckaJ BarańskaS Tylki-SzymańskaA CzartoryskaB WegrzynA WegrzynG Genistein-mediated inhibition of glycosaminoglycan synthesis as a basis for gene expression-targeted isoflavone therapy for mucopolysaccharidoses Eur J Hum Genet 2006 Jul 14 7 846 852 https://doi.org/10.1038/sj.ejhg.5201623 10.1038/sj.ejhg.520162316670689 Search in Google Scholar

Rabenstein DL. Heparin and heparan sulfate: structure and function. Nat Prod Rep. 2002 Jun;19(3):312–331. https://doi.org/10.1039/b100916h RabensteinDL Heparin and heparan sulfate: structure and function Nat Prod Rep 2002 Jun 19 3 312 331 https://doi.org/10.1039/b100916h 10.1039/b100916h12137280 Search in Google Scholar

Rajas O, Quirós LM, Ortega M, Vázquez-Espinosa E, Merayo-Lloves J, Vazquez F, García B. Glycosaminoglycans are involved in bacterial adherence to lung cells. BMC Infect Dis. 2017 May 2; 17(1):319. https://doi.org/10.1186/s12879-017-2418-5 RajasO QuirósLM OrtegaM Vázquez-EspinosaE Merayo-LlovesJ VazquezF GarcíaB Glycosaminoglycans are involved in bacterial adherence to lung cells BMC Infect Dis 2017 May 2 17 1 319 https://doi.org/10.1186/s12879-017-2418-5 10.1186/s12879-017-2418-5541423328464847 Search in Google Scholar

Roberts ALK, Thomas BJ, Wilkinson AS, Fletcher JM, Byers S. Inhibition of glycosaminoglycan synthesis using rhodamine B in a mouse model of mucopolysaccharidosis type IIIA. Pediatr Res. 2006 Sep;60(3):309–314. https://doi.org/10.1203/01.pdr.0000233037.00707.da RobertsALK ThomasBJ WilkinsonAS FletcherJM ByersS Inhibition of glycosaminoglycan synthesis using rhodamine B in a mouse model of mucopolysaccharidosis type IIIA Pediatr Res 2006 Sep 60 3 309 314 https://doi.org/10.1203/01.pdr.0000233037.00707.da 10.1203/01.pdr.0000233037.00707.da16857766 Search in Google Scholar

Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. Candida glabrata, Candida parapsilosis and Candida tropicalis : biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev. 2012 Mar;36(2):288–305. https://doi.org/10.1111/j.1574-6976.2011.00278.x SilvaS NegriM HenriquesM OliveiraR WilliamsDW AzeredoJ Candida glabrata, Candida parapsilosis and Candida tropicalis : biology, epidemiology, pathogenicity and antifungal resistance FEMS Microbiol Rev 2012 Mar 36 2 288 305 https://doi.org/10.1111/j.1574-6976.2011.00278.x 10.1111/j.1574-6976.2011.00278.x21569057 Search in Google Scholar

Thelin MA, Bartolini B, Axelsson J, Gustafsson R, Tykesson E, Pera E, Oldberg Å, Maccarana M, Malmstrom A. Biological functions of iduronic acid in chondroitin/dermatan sulfate. FEBS J. 2013 May;280(10):2431–2446. https://doi.org/10.1111/febs.12214 ThelinMA BartoliniB AxelssonJ GustafssonR TykessonE PeraE OldbergÅ MaccaranaM MalmstromA Biological functions of iduronic acid in chondroitin/dermatan sulfate FEBS J 2013 May 280 10 2431 2446 https://doi.org/10.1111/febs.12214 10.1111/febs.12214371717223441919 Search in Google Scholar

Thomas PA, Kaliamurthy J. Mycotic keratitis: epidemiology, diagnosis and management. Clin Microbiol Infect. 2013 Mar; 19(3): 210–220. https://doi.org/10.1111/1469-0691.12126 ThomasPA KaliamurthyJ Mycotic keratitis: epidemiology, diagnosis and management Clin Microbiol Infect 2013 Mar 19 3 210 220 https://doi.org/10.1111/1469-0691.12126 10.1111/1469-0691.1212623398543 Search in Google Scholar

Tonnaer EL, Hafmans TG, Van Kuppevelt TH, Sanders EA, Verweij PE, Curfs JH. Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes Infect. 2006 Feb;8(2):316–322. https://doi.org/10.1016/j.micinf.2005.06.028 TonnaerEL HafmansTG Van KuppeveltTH SandersEA VerweijPE CurfsJH Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells Microbes Infect 2006 Feb 8 2 316 322 https://doi.org/10.1016/j.micinf.2005.06.028 10.1016/j.micinf.2005.06.02816239116 Search in Google Scholar

Victor XV, Nguyen TK, Ethirajan M, Tran VM, Nguyen KV, Kuberan B. Investigating the elusive mechanism of glycosaminoglycan biosynthesis. J Biol Chem. 2009 Sep 18;284(38):25842–25853. https://doi.org/10.1074/jbc.M109.043208 VictorXV NguyenTK EthirajanM TranVM NguyenKV KuberanB Investigating the elusive mechanism of glycosaminoglycan biosynthesis J Biol Chem 2009 Sep 18 284 38 25842 25853 https://doi.org/10.1074/jbc.M109.043208 10.1074/jbc.M109.043208275798619628873 Search in Google Scholar

Wilson JW, Schurr MJ, LeBlanc CL, Ramamurthy R, Buchanan KL, Nickerson CA. Mechanisms of bacterial pathogenicity. Postgrad Med J. 2002 Apr;78(918):216–224. https://doi.org/10.1136/pmj.78.918.216 WilsonJW SchurrMJ LeBlancCL RamamurthyR BuchananKL NickersonCA Mechanisms of bacterial pathogenicity Postgrad Med J 2002 Apr 78 918 216 224 https://doi.org/10.1136/pmj.78.918.216 10.1136/pmj.78.918.216174232011930024 Search in Google Scholar

Zaretzky FR, Pearce-Pratt R, Phillips DM. Sulfated polyanions block Chlamydia trachomatis infection of cervix-derived human epithelia. Infect Immun. 1995 Sep;63(9):3520–3526. https://doi.org/10.1128/iai.63.9.3520-3526.1995 ZaretzkyFR Pearce-PrattR PhillipsDM Sulfated polyanions block Chlamydia trachomatis infection of cervix-derived human epithelia Infect Immun 1995 Sep 63 9 3520 3526 https://doi.org/10.1128/iai.63.9.3520-3526.1995 10.1128/iai.63.9.3520-3526.19951734877642286 Search in Google Scholar