Vestnik of the Far East Branch of the Russian Academy of SciencesVestnik of the Far East Branch of the Russian Academy of SciencesВестник Дальневосточного отделения Российской академии наук0869-7698The Russian Academy of Sciences67604110.31857/S0869769824030026ISVOGDChemical Sciences. Bioorganic chemistryХимические науки. Биоорганическая химияResearch ArticleFucanases of the 107’th structural family of the marine bacterium Wenyingzhuangia fucanilytica CZ1127TФуканазы 107 структурного семейства морской бактерии Wenyingzhuangia fucanilytica CZ1127Тhttps://orcid.org/0000-0001-9570-7647ZuevaAnastasiya O.ЗуеваАнастасия Олеговна
Russian Federation

Junior Researcher

младший научный сотрудник

a.o.zueva@yandex.ruhttps://orcid.org/0000-0002-3502-5692SilchenkoArtem S.СильченкоАртем Сергеевич
Russian Federation

Candidate of Sciences in Chemistry, Senior Researcher

кандидат химических наук, старший научный сотрудник

artem.silchencko@yandex.ruhttps://orcid.org/0000-0002-5905-2046ErmakovaSvetlana P.ЕрмаковаСветлана Павловна
Russian Federation

Doctor of Sciences in Chemistry, Assistant Professor, Head of the Laboratory

кандидат химических наук, старший научный сотрудник

swetlana_e@mail.ruG.B. Elyakov Pacific Institute of Bioorganic Chemistry, FEB RASТихоокеанский институт биоорганической химии им. Г.Б. Елякова ДВО РАН150620243375628022025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://journals.eco-vector.com/0869-7698/article/view/676041

This work is devoted to a generalization and comparison of the structural organization, physicochemical properties and substrate specificity of four fucanases of glycoside hydrolase family 107 that are part of the fucoidanutilizing cluster of the marine bacterium Wenyingzhuangia fucanilytica CZ1127T. The established differences in the significant characteristics of these enzymes provide new knowledge about the characteristics of fucanases belonging to the GH107 family.

Работа посвящена обобщению и сравнению структурной организации, физико-химических свойств и субстратной специфичности четырех фуканаз 107 семейства гликозидгидролаз, входящих в состав фукоиданутилизирующего кластера морской бактерии Wenyingzhuangia fucanilytica CZ1127Т. Установленные различия в значимых характеристиках этих ферментов дают новые знания об особенностях фуканаз, принадлежащих семейству GH107.

fucanaseGH107 familyfucoidaфуканазасемейство GH107фукоиданAntonio Trincone I. D. Marine glycosyl hydrolases as tool for industrial application. In: Industrial Applications of Glycoside Hydrolases. Springer; 2020. P. 151–166.Antonio Trincone I. D. Marine glycosyl hydrolases as tool for industrial application // Industrial Applications of Glycoside Hydrolases. Springer, 2020. P. 151–166.Pradhan B., Patra S., Nayak R., Behera C., Dash S. R., Nayak S., Sahu B. B., Bhutia S. K., Jena M. Multifunctional role of fucoidan, sulfated polysaccharides in human health and disease: A journey under the sea in pursuit of potent therapeutic agents. Int. J. Biol. Macromol. 2020;164:4263-4278.Pradhan B., Patra S., Nayak R., Behera C., Dash S. R., Nayak S., Sahu B. B., Bhutia S. K., Jena M. Multifunctional role of fucoidan, sulfated polysaccharides in human health and disease: A journey under the sea in pursuit of potent therapeutic agents // Int. J. Biol. Macromol. 2020. Vol. 164. P. 4263–4278.Wang Y., Xing M., Cao Q., Ji A., Liang H., Song S. Biological activities of fucoidan and the factors mediating its therapeutic effects: a review of recent studies. Mar. Drugs. 2019;17(3):183.Wang Y., Xing M., Cao Q., Ji A., Liang H., Song S. Biological activities of fucoidan and the factors mediating its therapeutic effects: a review of recent studies // Mar. Drugs. 2019. Vol. 17, N3. Р. 183.Nagamine T., Nakazato K., Tomioka S., Iha M., Nakajima K. Intestinal absorption of fucoidan extracted from the brown seaweed, Cladosiphon okamuranus. Mar. Drugs. 2014;13(1):48-64.Nagamine T., Nakazato K., Tomioka S., Iha M., Nakajima K. Intestinal absorption of fucoidan extracted from the brown seaweed, Cladosiphon okamuranus // Mar. Drugs. 2014. Vol. 13, N1. P. 48–64.Bai X., Zhang E., Hu B., Liang H., Song S., Ji A. Study on absorption mechanism and tissue distribution of fucoidan. Molecules. 2020;25(5):1087.Bai X., Zhang E., Hu B., Liang H., Song S., Ji A. Study on absorption mechanism and tissue distribution of fucoidan // Molecules. 2020. Vol. 25, N5. P. 1087.Zhu Z., Zhang Q., Chen L., Ren S., Xu P., Tang Y., Luo D. Higher specificity of the activity of low molecular weight fucoidan for thrombin-induced platelet aggregation. Thromb Res. 2010;125(5):419-426.Zhu Z., Zhang Q., Chen L., Ren S., Xu P., Tang Y., Luo D. Higher specificity of the activity of low molecular weight fucoidan for thrombin-induced platelet aggregation // Thromb Res. 2010. Vol. 125, N5. P. 419–426.Jin W. et al. A comparative study of the anticoagulant activities of eleven fucoidans. Carbohydr. Polym. 2013;91(1):1-6.Jin W. et al. A comparative study of the anticoagulant activities of eleven fucoidans // Carbohydr. Polym. 2013. Vol. 91, N1. P. 1–6.Jin W., Zhang Q., Wang J., Zhang W. Structure analysis and anti-tumor and anti-angiogenic activities of sulfated galactofucan extracted from Sargassum thunbergii. Mar. Drugs. 2019;17(1):52.Jin W., Zhang Q., Wang J., Zhang W. Structure analysis and anti-tumor and anti-angiogenic activities of sulfated galactofucan extracted from Sargassum thunbergii // Mar. Drugs. 2019. Vol. 17, N1. Р. 52.Lu J., Shi K. K., Chen S., Wang J., Hassouna A., White L. N., Merien F., Xie M., Kong Q., Li J., Ying T., White W. L., Nie S. Fucoidan extracted from the New Zealand Undaria pinnatifida – physicochemical comparison against five other fucoidans: Unique low molecular weight fraction bioactivity in breast cancer cell lines. Mar. Drugs. 2018;16(12):461.Lu J., Shi K. K., Chen S., Wang J., Hassouna A., White L. N., Merien F., Xie M., Kong Q., Li J., Ying T., White W. L., Nie S. Fucoidan extracted from the New Zealand Undaria pinnatifida – physicochemical comparison against five other fucoidans: Unique low molecular weight fraction bioactivity in breast cancer cell lines // Mar. Drugs. 2018. Vol. 16, N12. P. 461.Mak W., Hamid N., Liu T., Lu J., White W. L. Fucoidan from New Zealand Undaria pinnatifida: monthly variations and determination of antioxidant activities. Carbohydr. Polym. 2013;95(1):606-614.Mak W., Hamid N., Liu T., Lu J., White W. L. Fucoidan from New Zealand Undaria pinnatifida: monthly variations and determination of antioxidant activities // Carbohydr. Polym. 2013. Vol. 95, N1. P.606–614.Zvyagintseva T. N., Shevchenko N. M., Chizhov A. O., Krupnova T. N., Sundukova E. V., Isakov V. V. Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J. Exp. Mar. Biol. Ecol. 2003;294(1):1-13.Zvyagintseva T. N., Shevchenko N. M., Chizhov A. O., Krupnova T. N., Sundukova E. V., Isakov V. V. Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions // J. Exp. Mar. Biol. Ecol. 2003. Vol. 294, N1. P. 1–13.Anastyuk S. D., Shevchenko N. M., Nazarenko E. L., Imbs T. I., Gorbach V. I., Dmitrenok P. S., Zvyagintseva T. N. Structural analysis of a highly sulfated fucan from the brown alga Laminaria cichorioides by tandem MALDI and ESI mass spectrometry. Carbohydr. Res. 2010;345(15):2206-2212.Anastyuk S. D., Shevchenko N. M., Nazarenko E. L., Imbs T. I., Gorbach V. I., Dmitrenok P. S., Zvyagintseva T. N. Structural analysis of a highly sulfated fucan from the brown alga Laminaria cichorioides by tandem MALDI and ESI mass spectrometry // Carbohydr. Res. 2010. Vol. 345, N15. P. 2206–2212.Chen F., Chang Y., Dong S., Xue C. Wenyingzhuangia fucanilytica sp. nov., a sulfated fucan utilizing bacterium isolated from shallow coastal seawater. Int. J. Syst. Evol. Microbiol. 2016;66(9):3270-3275.Chen F., Chang Y., Dong S., Xue C. Wenyingzhuangia fucanilytica sp. nov., a sulfated fucan utilizing bacterium isolated from shallow coastal seawater // Int. J. Syst. Evol. Microbiol. 2016. Vol. 66, N9. P. 3270–3275.Chang Y., Xue C., Tang Q., Li D., Wu X., Wang J. Isolation and characterization of a sea cucumber fucoidan-utilizing marine bacterium. Lett. Appl. Microbiol. 2010;50(3):301-307.Chang Y., Xue C., Tang Q., Li D., Wu X., Wang J. Isolation and characterization of a sea cucumber fucoidan-utilizing marine bacterium // Lett. Appl. Microbiol. 2010. Vol. 50, N3. P. 301–307.Zueva A. O., Silchenko A. S., Rasin A. B., Kusaykin M. I., Usoltseva R. V., Kalinovsky A. I., Kurilenko V. V., Zvyagintseva T. N., Thinh P. D., Ermakova S. P. Expression and biochemical characterization of two recombinant fucoidanases from the marine bacterium Wenyingzhuangia fucanilytica CZ1127T. Int. J. Biol. Macromol. 2020;164:3025-3037.Zueva A. O., Silchenko A. S., Rasin A. B., Kusaykin M. I., Usoltseva R. V., Kalinovsky A. I., Kurilenko V. V., Zvyagintseva T. N., Thinh P. D., Ermakova S. P. Expression and biochemical characterization of two recombinant fucoidanases from the marine bacterium Wenyingzhuangia fucanilytica CZ1127T // Int. J. Biol. Macromol. 2020. Vol. 164. P. 3025–3037.Zueva A. O., Silchenko A. S., Rasin A. B., Malyarenko O. S., Kusaykin M. I., Kalinovsky A. I., Ermakova S. P. Production of high- and low-molecular weight fucoidan fragments with defined sulfation patterns and heightened in vitro anticancer activity against TNBC cells using novel endo-fucanases of the GH107 family. Carbohydr. Polym. 2023;318:121128.Zueva A. O., Silchenko A. S., Rasin A. B., Malyarenko O. S., Kusaykin M. I., Kalinovsky A. I., Ermakova S. P. Production of high- and low-molecular weight fucoidan fragments with defined sulfation patterns and heightened in vitro anticancer activity against TNBC cells using novel endo-fucanases of the GH107 family // Carbohydr. Polym. 2023. Vol. 318. P. 121128.Schultz-Johansen M., Cueff M., Hardouin K., Jam M., Larocque R., Glaring M. A., Hervé C., Czjzek M., Stougaard P. Discovery and screening of novel metagenome-derived GH107 enzymes targeting sulfated fucans from brown algae. FEBS J. 2018;285(22):4281-4295.Schultz-Johansen M., Cueff M., Hardouin K., Jam M., Larocque R., Glaring M. A., Hervé C., Czjzek M., Stougaard P. Discovery and screening of novel metagenome-derived GH107 enzymes targeting sulfated fucans from brown algae // FEBS J. 2018. Vol. 285, N22. P. 4281–4295.Vickers C., Liu F., Abe K., Salama-Alber O., Jenkins M., Springate C. M., Burke J. E., Withers S. G., Boraston A. B. Endo-fucoidan hydrolases from glycoside hydrolase family 107 (GH107) display structural and mechanistic similarities to α-l-fucosidases from GH29. J. Biol. Chem. 2018;293(47):18296-18308.Vickers C., Liu F., Abe K., Salama-Alber O., Jenkins M., Springate C. M., Burke J. E., Withers S. G., Boraston A. B. Endo-fucoidan hydrolases from glycoside hydrolase family 107 (GH107) display structural and mechanistic similarities to α-l-fucosidases from GH29 // J. Biol. Chem. 2018. Vol. 293, N47. P. 18296–18308.Lasica A. M., Ksiazek M., Madej M., Potempa J. The type IX secretion system (T9SS): highlights and recent insights into its structure and function. Front. Cell. Infect. Microbiol. 2017;7:215.Lasica A. M., Ksiazek M., Madej M., Potempa J. The type IX secretion system (T9SS): highlights and recent insights into its structure and function // Front. Cell. Infect. Microbiol. 2017. Vol. 7. P. 215.Silchenko A. S., Rasin A. B., Kusaykin M. I., Kalinovsky A. I., Miansong Z., Changheng L., Malyarenko O. S., Zueva A. O., Zvyagintseva T. N., Ermakova S. P. Structure, enzymatic transformation, anticancer activity of fucoidan and sulphated fucooligosaccharides from Sargassum horneri. Carbohydr. Polym. 2017;175:654-660.Silchenko A. S., Rasin A. B., Kusaykin M. I., Kalinovsky A. I., Miansong Z., Changheng L., Malyarenko O. S., Zueva A. O., Zvyagintseva T. N., Ermakova S. P. Structure, enzymatic transformation, anticancer activity of fucoidan and sulphated fucooligosaccharides from Sargassum horneri // Carbohydr. Polym. 2017. Vol. 175. P. 654–660.Silchenko A. S., Ustyuzhanina N. E., Kusaykin M. I., Krylov V. B., Shashkov A. S., Dmitrenok A. S., Usoltseva R. V., Zueva A. O., Nifantiev N. E., Zvyagintseva T. N. Expression and biochemical characterization and substrate specificity of the fucoidanase from Formosa algae. Glycobiology. 2017;27(3):254-263.Silchenko A. S., Ustyuzhanina N. E., Kusaykin M. I., Krylov V. B., Shashkov A. S., Dmitrenok A. S., Usoltseva R. V., Zueva A. O., Nifantiev N. E., Zvyagintseva T. N. Expression and biochemical characterization and substrate specificity of the fucoidanase from Formosa algae // Glycobiology. 2017. Vol. 27, N 3. P. 254–263.Colin S., Deniaud E., Jam M., Descamps V., Chevolot Y., Kervarec N., Barbeyron T., Yvin J. C., Michel G., Kloareg B. Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans. Glycobiology. 2006;16(11):1021-1032.Colin S., Deniaud E., Jam M., Descamps V., Chevolot Y., Kervarec N., Barbeyron T., Yvin J. C., Michel G., Kloareg B. Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans // Glycobiology. 2006. Vol. 16, N11. P. 1021–1032.Hoppert M. Metalloenzymes. In: Encyclopedia of Earth Sciences Series. Springer; 2011. P. 558–563. Print ISBN9781402092114.Hoppert M. Metalloenzymes // Encyclopedia of Earth Sciences Series. Springer, 2011. P. 558–563. Print ISBN9781402092114.Benkovic S. J. Metal Ion-Activated Enzymes. In: Basolo F. Catalysis Progress in Research. Springer My Copy UK; 1973. P. 43-46.Benkovic S. J. Metal Ion-Activated Enzymes // Basolo F. Catalysis Progress in Research. Springer My Copy UK, 1973. P. 43–46.Liu G., Shen J., Chang Y., Mei X., Chen G., Zhang Y., Xue C. Characterization of an endo-1,3-fucanase from marine bacterium Wenyingzhuangia aestuarii: The first member of a novel glycoside hydrolase family GH174. Carbohydr. Polym. 2023;306. 120591.Liu G., Shen J., Chang Y., Mei X., Chen G., Zhang Y., Xue C. Characterization of an endo-1,3-fucanase from marine bacterium Wenyingzhuangia aestuarii: The first member of a novel glycoside hydrolase family GH174 // Carbohydr. Polym. 2023. Vol. 306. 120591.Qiu Y., Jiang H., Dong Y., Wang Y., Hamouda H. I., Balah M. A., Mao X. Expression and biochemical characterization of a novel fucoidanase from Flavobacterium algicola with the principal product of fucoidan-derived disaccharide. Foods. 2022;11(7):1025.Qiu Y., Jiang H., Dong Y., Wang Y., Hamouda H. I., Balah M. A., Mao X. Expression and biochemical characterization of a novel fucoidanase from Flavobacterium algicola with the principal product of fucoidan-derived disaccharide // Foods. 2022. Vol. 11, N7. P. 1025.Descamps V., Colin S., Lahaye M., Jam M., Richard C., Potin P., Barbeyron T., Yvin J. C., Kloareg B. Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Mar. Biotechnol. 2006;8(1):27-39.Descamps V., Colin S., Lahaye M., Jam M., Richard C., Potin P., Barbeyron T., Yvin J. C., Kloareg B. Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae // Mar. Biotechnol. 2006. Vol. 8, N1. P. 27–39.Furukawa S. I., Fujikawa T., Koga D., Ide A. Purification and some properties of exo-type fucoidanases from Vibrio sp. N-5. Biosci. Biotech. Biochem. 1992;56(11):1829-1834.Furukawa S. I., Fujikawa T., Koga D., Ide A. Purification and some properties of exo-type fucoidanases from Vibrio sp. N-5 // Biosci. Biotech. Biochem. 1992. Vol. 56, N11. P. 1829−1834.Trang V. T.D., Mikkelsen M. D., Vuillemin M., Meier S., Cao H. T.T., Muschiol J., Perna V., Nguyen T. T., Tran V. H.N., Holck J., Van T. T.T., Khanh H. H.N., Meyer A. S. The endo-α (1, 4) specific fucoidanase Fhf2 from Formosa haliotis releases highly sulfated fucoidan oligosaccharides. Front. Plant. Sci. 2022;13:823668.Trang V. T.D., Mikkelsen M. D., Vuillemin M., Meier S., Cao H. T.T., Muschiol J., Perna V., Nguyen T. T., Tran V. H.N., Holck J., Van T. T.T., Khanh H. H.N., Meyer A. S. The endo-α (1, 4) specific fucoidanase Fhf2 from Formosa haliotis releases highly sulfated fucoidan oligosaccharides // Front. Plant. Sci. 2022. Vol. 13. P. 823668.Sakai T., Kawai T., Kato I. Isolation and characterization of a fucoidan-degrading marine bacterial strain and its fucoidanase. Mar. Biotechnol. 2004;6(4):335-346.Sakai T., Kawai T., Kato I. Isolation and characterization of a fucoidan-degrading marine bacterial strain and its fucoidanase // Mar. Biotechnol. 2004. Vol. 6, N4. P. 335–346.Sakai T., Kimura H., Kato I. Purification of sulfated fucoglucuronomannan lyase from bacterial strain of Fucobacter marina and study of appropriate conditions for its enzyme digestion. Mar. Biotechnol. 2003;5:380-387.Sakai T., Kimura H., Kato I. Purification of sulfated fucoglucuronomannan lyase from bacterial strain of Fucobacter marina and study of appropriate conditions for its enzyme digestion // Mar. Biotechnol. 2003. Vol. 5. P. 380−387.Chevolot L., Foucault A., Chaubet F., Kervarec N., Sinquin C., Fisher A. M., Boisson-Vidal C. Further data on the structure of brown seaweed fucans: relationships with anticoagulant activity. Carbohydr. Res. 1999;319(1-4):154-165.Chevolot L., Foucault A., Chaubet F., Kervarec N., Sinquin C., Fisher A. M., Boisson-Vidal C. Further data on the structure of brown seaweed fucans: relationships with anticoagulant activity // Carbohydr. Res. 1999. Vol. 319, N1–4. P. 154–165.Menshova R. V., Shevchenko N. M., Imbs T. I., Zvyagintseva T. N., Malyarenko O. S., Zaporoshets T. S., Besednova N. N., Ermakova S. P. Fucoidans from brown alga Fucus evanescens: Structure and biological activity. Front. Mar. Sci. 2016;3:129.Menshova R. V., Shevchenko N. M., Imbs T. I., Zvyagintseva T. N., Malyarenko O. S., Zaporoshets T. S., Besednova N. N., Ermakova S. P. Fucoidans from brown alga Fucus evanescens: Structure and biological activity // Front. Mar. Sci. 2016. Vol. 3. P. 129.Silchenko A. S., Rasin A. B., Kusaykin M. I., Malyarenko O. S., Shevchenko N. M., Zueva A. O., Kalinovsky A. I., Zvyagintseva T. N., Ermakova S. P. Modification of native fucoidan from Fucus evanescens by recombinant fucoidanase from marine bacteria Formosa algae. Carbohydr. Polym. 2018;193:189-195.Silchenko A. S., Rasin A. B., Kusaykin M. I., Malyarenko O. S., Shevchenko N. M., Zueva A. O., Kalinovsky A. I., Zvyagintseva T. N., Ermakova S. P. Modification of native fucoidan from Fucus evanescens by recombinant fucoidanase from marine bacteria Formosa algae // Carbohydr. Polym. 2018. Vol. 193. P. 189–195.Usoltseva R. V., Shevchenko N. M., Malyarenko O. S., Anastyuk S. D., Kasprik A. E., Zvyagintsev N. V., Ermakova S. P. Fucoidans from brown algae Laminaria longipes and Saccharina cichorioides: Structural characteristics, anticancer and radiosensitizing activity in vitro. Carbohydr. Polym. 2019;221:157-165.Usoltseva R. V., Shevchenko N. M., Malyarenko O. S., Anastyuk S. D., Kasprik A. E., Zvyagintsev N. V., Ermakova S. P. Fucoidans from brown algae Laminaria longipes and Saccharina cichorioides: Structural characteristics, anticancer and radiosensitizing activity in vitro // Carbohydr. Polym. 2019. Vol. 221. P. 157–165.Hemmingson J. A., Falshaw R., Furneaux R. H., Thompson K. Structure and antiviral activity of the galactofucan sulfates extracted from Undaria pinnatifida (Phaeophyta). J. Appl. Phycol. 2006;18(2):185–193.Hemmingson J. A., Falshaw R., Furneaux R. H., Thompson K. Structure and antiviral activity of the galactofucan sulfates extracted from Undaria pinnatifida (Phaeophyta) // J. Appl. Phycol. 2006. Vol. 18, N2. P. 185–193.Chevolot L., Mulloy B., Ratiskol J., Foucault A., Colliec-Jouault S. A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr. Res. 2001;330(4):529-535.Chevolot L., Mulloy B., Ratiskol J., Foucault A., Colliec-Jouault S. A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae // Carbohydr. Res. 2001. Vol. 330, N4. P. 529–535.Cao C., Zhang B., Li C., Huang Q., Fu X., Liu R. H. Structure and in vitro hypoglycemic activity of a homogenous polysaccharide purified from Sargassum pallidum. Food Funct. 2019;10:2828.Cao C., Zhang B., Li C., Huang Q., Fu X., Liu R. H. Structure and in vitro hypoglycemic activity of a homogenous polysaccharide purified from Sargassum pallidum // Food Funct. 2019. Vol. 10. P. 2828.Luo D., Wang Z., Nie K. Structural characterization of a novel polysaccharide from Sargassum thunbergii and its antioxidant and anti-inflammation effects. Plos One. 2019;14(10). e0223198.Luo D., Wang Z., Nie K. Structural characterization of a novel polysaccharide from Sargassum thunbergii and its antioxidant and anti-inflammation effects // PloS One. 2019. Vol. 14. N10. e0223198.Murphy K. J., Merry C. L., Lyon M., Thompson J. E., Roberts I. S., Gallagher J. T. A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase. J. Biol. Chem. 2004;279(26):27239-27245.Murphy K. J., Merry C. L., Lyon M., Thompson J. E., Roberts I. S., Gallagher J. T. A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase // J. Biol. Chem. 2004. Vol. 279, N26. P. 27239–27245.Van Kuppevelt T. H., Oosterhof A., Versteeg E. M., Podhumljak E., Van de Westerlo E. M., Daamen W. F. Sequencing of glycosaminoglycans with potential to interrogate sequence-specific interactions. Sci. Rep. 2017;7(1):1-9.Van Kuppevelt T. H., Oosterhof A., Versteeg E. M., Podhumljak E., Van de Westerlo E. M., Daamen W. F. Sequencing of glycosaminoglycans with potential to interrogate sequence-specific interactions // Sci. Rep. 2017. Vol. 7, N1. P. 1–9.Davies G. J., Wilson K. S., Henrissat B. Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 1997;321(2):557-559.Davies G. J., Wilson K. S., Henrissat B. Nomenclature for sugar-binding subsites in glycosyl hydrolases // Biochem. J. 1997. Vol. 321, N2. P. 557–559.