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Full Critical Review

Glycosaminoglycans as polyelectrolytes: implications in bioactivity and assembly of biomedical devices

ORCID Icon, ORCID Icon & ORCID Icon
Pages 765-795 | Received 04 Oct 2021, Accepted 16 Dec 2021, Published online: 19 Jan 2022

References

  • Barthelat F. Architectured materials in engineering and biology: fabrication, structure, mechanics and performance. Int Mater Rev. 2015;60:413–430. doi:10.1179/1743280415Y.0000000008.
  • Liu WH, Zheng J, Feldman JL, et al. Multivalent interactions drive nucleosome binding and efficient chromatin deacetylation by SIRT6. Nat Commun. 2020;11:5244. doi:10.1038/s41467-020-19018-y.
  • Rood MTM, Spa SJ, Welling MM, et al. Obtaining control of cell surface functionalizations via pre-targeting and supramolecular host guest interactions. Sci Rep. 2017;7:39908. doi:10.1038/srep39908.
  • Villone D, Fritsch A, Koch M, et al. Supramolecular interactions in the dermo-epidermal junction zone: anchoring fibril-collagen VII tightly binds to banded collagen fibrils. J Biol Chem. 2008;283:24506–24513. doi:10.1074/jbc.M802415200.
  • Iqbal N, Khan AS, Asif A, et al. Recent concepts in biodegradable polymers for tissue engineering paradigms: a critical review. Int Mater Rev. 2019;64:91–126. doi:10.1080/09506608.2018.1460943.
  • Schmidt JR, Kliemt S, Preissler C, et al. Osteoblast-released matrix vesicles, regulation of activity and composition by sulfated and non-sulfated glycosaminoglycans. Mol Cell Proteomics. 2016;15:558–572. doi:10.1074/mcp.M115.049718.
  • Soares da Costa D, Reis RL, Pashkuleva I. Sulfation of glycosaminoglycans and its implications in human health and disorders. Annu Rev Biomed Eng. 2017;19:1–26. doi:10.1146/annurev-bioeng-071516-044610.
  • Nguyen T-H, Wesche J, Raschke R, et al. Reactivity of platelet-activating and nonplatelet-activating anti-PF4/heparin antibodies in enzyme immunosorbent assays under different conditions. J Thromb Haemostasis. 2019;17:1113–1119. doi:10.1111/jth.14455.
  • Volpi N, Tarugi P. Influence of chondroitin sulfate charge density, sulfate group position, and molecular mass on Cu2+-mediated oxidation of human Low-density lipoproteins: effect of normal human plasma-derived chondroitin sulfate. J Biochem. 1999;125:297–304. doi:10.1093/oxfordjournals.jbchem.a022286.
  • Lohmann N, Schirmer L, Atallah P, et al. Glycosaminoglycan-based hydrogels capture inflammatory chemokines and rescue defective wound healing in mice. Sci Transl Med. 2017;9:eaai9044. doi:10.1126/scitranslmed.aai9044.
  • Müller E, Pompe T, Freudenberg U, et al. Solvent-assisted micromolding of biohybrid hydrogels to maintain human hematopoietic stem and progenitor cells Ex vivo. Adv Mater. 2017;29:1703489. doi:10.1002/adma.201703489.
  • Terauchi M, Tamura A, Tonegawa A, et al. Polyelectrolyte complexes between polycarboxylates and BMP-2 for enhancing osteogenic differentiation: effect of chemical structure of polycarboxylates. Polymers 2019;11:1327. doi:10.3390/polym11081327.
  • Bergsson G, Reeves EP, McNally P, et al. LL-37 complexation with glycosaminoglycans in cystic fibrosis lungs inhibits antimicrobial activity, which can be restored by hypertonic saline. J Immunol. 2009;183:543–551. doi:10.4049/jimmunol.0803959.
  • Cardin AD, Weintraub HJ. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis. 1989;9:21–32. doi:10.1161/01.ATV.9.1.21.
  • Gandhi NS, Mancera RL. The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des. 2008;72:455–482. doi:10.1111/j.1747-0285.2008.00741.x.
  • Petitou M, van Boeckel CAA. A Synthetic antithrombin III binding pentasaccharide is now a drug! what comes next? Angew Chem Int Ed. 2004;43:3118–3133. doi:10.1002/anie.200300640.
  • Seyrek E, Dubin P. Glycosaminoglycans as polyelectrolytes. Adv Colloid Interface Sci. 2010;158:119–129. doi:10.1016/j.cis.2010.03.001.
  • Hassell JR, Newsome DA, Krachmer JH, et al. Macular corneal dystrophy: failure to synthesize a mature keratan sulfate proteoglycan. Proc Natl Acad Sci USA. 1980;77:3705–3709. doi:10.1073/pnas.77.6.3705.
  • Caterson B, Melrose J. Keratan sulfate, a complex glycosaminoglycan with unique functional capability. Glycobiology. 2018;28:182–206. doi:10.1093/glycob/cwy003.
  • Solakyildirim K. Recent advances in glycosaminoglycan analysis by various mass spectrometry techniques. Anal Bioanal Chem. 2019;411:3731–3741. doi:10.1007/s00216-019-01722-4.
  • Freudenberg U, Liang Y, Kiick KL, et al. Glycosaminoglycan-based biohybrid hydrogels: a sweet and smart choice for multifunctional biomaterials. Adv Mater. 2016;28:8861–8891. doi:10.1002/adma.201601908.
  • Oldenkamp HF, Vela Ramirez JE, Peppas NA. Re-evaluating the importance of carbohydrates as regenerative biomaterials. Regener Biomater. 2018;6:1–12. doi:10.1093/rb/rby023.
  • Morla S. Glycosaminoglycans and glycosaminoglycan mimetics in cancer and inflammation. Int J Mol Sci. 2019;20:1963. doi:10.3390/ijms20081963.
  • Ghiselli G. Drug-mediated regulation of glycosaminoglycan biosynthesis. Med Res Rev. 2017;37:1051–1094. doi:10.1002/med.21429.
  • Taylor SL, Hogwood J, Guo W, et al. By-products of heparin production provide a diverse source of heparin-like and heparan sulfate glycosaminoglycans. Sci Rep. 2019;9:2679. doi:10.1038/s41598-019-39093-6.
  • Capila I, Linhardt RJ. Heparin–protein interactions. Angew Chem Int Ed. 2002;41:390–412. doi:10.1002/1521-3773(20020201)41:3.
  • Chen Y-H, Narimatsu Y, Clausen TM, et al. The GAGOme: a cell-based library of displayed glycosaminoglycans. Nat Methods. 2018;15:881–888. doi:10.1038/s41592-018-0086-z.
  • Teixeira R, Reis RL, Pashkuleva I. Influence of the sulfation degree of glycosaminoglycans on their multilayer assembly with poly-l-lysine. Colloids Surf, B. 2016;145:567–575. doi:10.1016/j.colsurfb.2016.05.069.
  • Pashkuleva I, Reis RL. Sugars: burden or biomaterials of the future? J Mater Chem. 2010;20:8803–8818. doi:10.1039/C0JM01605E.
  • Gama CI, Tully SE, Sotogaku N, et al. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat Chem Biol. 2006;2:467–473. doi:10.1038/nchembio810.
  • Klein DR, Leach FE, Amster IJ, et al. Structural characterization of glycosaminoglycan carbohydrates using ultraviolet photodissociation. Anal Chem. 2019;91:6019–6026. doi:10.1021/acs.analchem.9b00521.
  • Yamada M, Hamaguchi T. The sulfation code for propagation of neurodegeneration. J Biol Chem. 2018;293:10841–10842. doi:10.1074/jbc.H118.003970.
  • Weiss RJ, Esko JD, Tor Y. Targeting heparin and heparan sulfate protein interactions. Org Biomol Chem. 2017;15:5656–5668. doi:10.1039/C7OB01058C.
  • Noti C, Seeberger PH. Synthetic approach to define structure-activity relationship of heparin and heparan sulfate. In: Garg HG, Linhardt RJ, Hales CA, editor. Chemistry and biology of heparin and heparan sulfate. Amsterdam: Elsevier Science; 2005. p. 79–142. Chap. 4
  • Sasisekharan R, Venkataraman G. Heparin and heparan sulfate: biosynthesis, structure and function. Curr Opin Chem Biol. 2000;4:626–631. doi:10.1016/S1367-5931(00)00145-9.
  • Toida T, Yoshida H, Toyoda H, et al. Structural differences and the presence of unsubstituted amino groups in heparan sulphates from different tissues and species. Biochem J. 1997;322:499–506. doi:10.1042/bj3220499.
  • Simon Davis DA, Parish CR. Heparan sulfate: a ubiquitous glycosaminoglycan with multiple roles in immunity. Front Immunol. 2013;4:Article number 470. doi:10.3389/fimmu.2013.00470.
  • Faham S, Hileman RE, Fromm JR, et al. Heparin structure and interactions with basic fibroblast growth factor. Science. 1996;271:1116–1120. doi:10.1126/science.271.5252.1116.
  • Gandhi NS, Mancera RL. Prediction of heparin binding sites in bone morphogenetic proteins (BMPs). Biochim Biophys Acta (BBA) Proteins Proteom. 2012;1824:1374–1381. doi:10.1016/j.bbapap.2012.07.002.
  • Ramdin P, Sheron S. Regulation of interleukin-8 binding and function by heparin and α2-macroglobulin. Clin Exp Allergy. 1998;28:616–624. doi:10.1046/j.1365-2222.1998.00283.x.
  • Zandi N, Mostafavi E, Shokrgozar MA, et al. Biomimetic proteoglycan nanoparticles for growth factor immobilization and delivery. Biomater Sci. 2020;8:1127–1136.
  • Seyrek E, Dubin PL, Henriksen J. Nonspecific electrostatic binding characteristics of the heparin-antithrombin interaction. Biopolymers. 2007;86:249–259. doi:10.1002/bip.20731.
  • Simmons RB, Newton GR, Doctor VM. Effect of sulfated xylans during the interaction of [125I]-thrombin with antithrombin III or heparin cofactor II of human plasma. Eur J Drug Metab Pharmacokinet. 1995;20:73–77. doi:10.1007/BF03192291.
  • Sobczak AIS, Pitt SJ, Stewart AJ. Influence of zinc on glycosaminoglycan neutralisation during coagulation. Metallomics. 2018;10:1180–1190. doi:10.1039/C8MT00159F.
  • Flaumenhaft R, Moscatelli D, Rifkin DB. Heparin and heparan sulfate increase the radius of diffusion and action of basic fibroblast growth factor. J Cell Biol. 1990;111:1651–1659. doi:10.1083/jcb.111.4.1651.
  • Rodgers AL, Jackson GE. Determination of thermodynamic parameters for complexation of calcium and magnesium with chondroitin sulfate isomers using isothermal titration calorimetry: Implications for calcium kidney-stone research. J Cryst Growth. 2017;463:14–18. doi:10.1016/j.jcrysgro.2017.01.056.
  • Hayashida Y, Akama TO, Beecher N, et al. Matrix morphogenesis in cornea is mediated by the modification of keratan sulfate by GlcNAc 6-O-sulfotransferase. Proc Natl Acad Sci USA. 2006;103:13333–13338. doi:10.1073/pnas.0605441103.
  • Littlechild SL, Young RD, Caterson B, et al. Keratan sulfate phenotype in the β-1,3-N-acetylglucosaminyltransferase-7–null mouse cornea. Invest Ophthalmol Visual Sci. 2018;59:1641–1651. doi:10.1167/iovs.17-22716.
  • Amorim S, da Costa DS, Freitas D, et al. Molecular weight of surface immobilized hyaluronic acid influences CD44-mediated binding of gastric cancer cells. Sci Rep. 2018;8:16058. doi:10.1038/s41598-018-34445-0.
  • Carvalho AM, Teixeira R, Novoa-Carballal R, et al. Redox-responsive micellar nanoparticles from glycosaminoglycans for CD44 targeted drug delivery. Biomacromolecules. 2018;19:2991–2999. doi:10.1021/acs.biomac.8b00561.
  • Haskin CL, Fullerton GD, Cameron IL. Molecular basis of articular disk biomechanics: fluid flow and water content in the temporomandibular disk as related to distribution of sulfur. In: Pollack GH, Cameron IL, Wheatley DN, editor. Water and the cell. Dordrecht: Springer; 2006. p. 53–69.
  • Henrotin Y, Mathy M, Sanchez C, et al. Chondroitin sulfate in the treatment of osteoarthritis: from in vitro studies to clinical recommendations. Ther Adv Musculoskeletal Dis. 2010;2:335–348. doi:10.1177/1759720 ( 10383076.
  • Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. 1976;260:808–809. doi:10.1038/260808a0.
  • Niu L-n, Jee SE, Jiao K, et al. Collagen intrafibrillar mineralization as a result of the balance between osmotic equilibrium and electroneutrality. Nat Mater. 2017;16:370–378. doi:10.1038/nmat4789.
  • Maroto M, Fernández-Morales J-C, Padín JF, et al. Chondroitin sulfate, a major component of the perineuronal net, elicits inward currents, cell depolarization, and calcium transients by acting on AMPA and kainate receptors of hippocampal neurons. J Neurochem. 2013;125:205–213. doi:10.1111/jnc.12159.
  • Ajisaka K, Oyanagi Y, Miyazaki T, et al. Effect of the chelation of metal cation on the antioxidant activity of chondroitin sulfates. Biosci Biotechnol Biochem. 2016;80:1179–1185. doi:10.1080/09168451.2016.1141036.
  • Tatara Y, Suto S, Itoh K. Novel roles of glycosaminoglycans in the degradation of type I collagen by cathepsin K. Glycobiology. 2017;27:1089–1098. doi:10.1093/glycob/cwx083.
  • Lim JJ, Temenoff JS. The effect of desulfation of chondroitin sulfate on interactions with positively charged growth factors and upregulation of cartilaginous markers in encapsulated MSCs. Biomaterials. 2013;34:5007–5018. doi:10.1016/j.biomaterials.2013.03.037.
  • Kuboyama K, Fujikawa A, Suzuki R, et al. Role of chondroitin sulfate (CS) modification in the regulation of protein-tyrosine phosphatase receptor type Z (PTPRZ) activity: pleiotrophin-PTPRZ-A signaling is involved in oligodendrocyte differentiation. J Biol Chem. 2016;291:18117–18128. doi:10.1074/jbc.M116.742536.
  • Penc SF, Pomahac B, Winkler T, et al. Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function. J Biol Chem. 1998;273:28116–28121. doi:10.1074/jbc.273.43.28116.
  • Kostoulas G, Hörler D, Naggi A, et al. Electrostatic interactions between human leukocyte elastase and sulfated glycosaminoglycans: physiological implications. Biol Chem. 1997;378:1481. doi:10.1515/bchm.1997.378.12.1481.
  • Griese M, Kappler M, Gaggar A, et al. Inhibition of airway proteases in cystic fibrosis lung disease. Eur Respir J. 2008;32:783–795. doi:10.1183/09031936.00146807.
  • Maurice P, Blaise S, Gayral S, et al. Elastin fragmentation and atherosclerosis progression: the elastokine concept. Trends Cardiovasc Med. 2013;23:211–221. doi:10.1016/j.tcm.2012.12.004.
  • Bartolucci C, Cellai L, Iannelli MA, et al. Inhibition of human leukocyte elastase by chemically and naturally oversulfated galactosaminoglycans. Carbohydr Res. 1995;276:401–408. doi:10.1016/0008-6215(95)00179-W.
  • Fernández JA, Petäjä J, Griffin JH. Dermatan sulfate and LMW heparin enhance the anticoagulant action of activated protein C. Thromb Haemostasis. 1999;82:1462–1468. doi:10.1055/s-0037-1614856.
  • Amorim S, Reis CA, Reis RL, et al. Extracellular matrix mimics using hyaluronan-based biomaterials. Trends Biotechnol. 2021;39:90–104. doi:10.1016/j.tibtech.2020.06.003.
  • Wolf KJ, Kumar S. Hyaluronic acid: incorporating the bio into the material. ACS Biomater Sci Eng. 2019;5:3753–3765. doi:10.1021/acsbiomaterials.8b01268.
  • Amorim S, da Costa D S, Pashkuleva I, et al. Hyaluronic acid of low molecular weight triggers the invasive “hummingbird” phenotype on gastric cancer cells. Adv Biosyst. 2020;4:2000122. doi:10.1002/adbi.202000122.
  • Amorim S, Soares da Costa D, Mereiter S, et al. Multilayer platform to model the bioactivity of hyaluronic acid in gastric cancer. Mater Sci Eng, C. 2021;119:111616. doi:10.1016/j.msec.2020.111616.
  • Lintuluoto M, Horioka Y, Hongo S, et al. Molecular dynamics simulation study on allosteric regulation of CD44-hyaluronan binding as a force sensing mechanism. ACS Omega. 2021;6:8045–8055. doi:10.1021/acsomega.0c05502.
  • Carvalho AM, da Costa D S, Paulo PMR, et al. Co-localization and crosstalk between CD44 and RHAMM depend on hyaluronan presentation. Acta Biomater. 2021;119:114–124. doi:10.1016/j.actbio.2020.10.024.
  • Misra S, Hascall VC, Markwald RR, et al. Interactions between Hyaluronan and its receptors (CD44, RHAMM) regulate the activities of inflammation and cancer. Front Immunol. 2015;6. doi:10.3389/fimmu.2015.00201.
  • Azevedo HS, Pashkuleva I. Biomimetic supramolecular designs for the controlled release of growth factors in bone regeneration. Adv Drug Delivery Rev. 2015;94:63–76. doi:10.1016/j.addr.2015.08.003.
  • Gil ES, Hudson SM. Stimuli-reponsive polymers and their bioconjugates. Prog Polym Sci. 2004;29:1173–1222. doi:10.1016/j.progpolymsci.2004.08.003.
  • Seog J, Dean D, Plaas AHK, et al. Direct measurement of glycosaminoglycan intermolecular interactions via high-resolution force spectroscopy. Macromolecules. 2002;35:5601–5615. doi:10.1021/ma0121621.
  • Lalevée G, David L, Montembault A, et al. Highly stretchable hydrogels from complex coacervation of natural polyelectrolytes. Soft Matter. 2017;13:6594–6605. doi:10.1039/C7SM01215B.
  • Lee H, In B, Mehta PK, et al. Dual role of a fluorescent peptidyl probe based on self-assembly for the detection of heparin and for the inhibition of the heparin-digestive enzyme reaction. ACS Appl Mater Interfaces. 2018;10:2282–2290. doi:10.1021/acsami.7b15411.
  • Remko M, Broer R, Van Duijnen PT. How acidic are monomeric structural units of heparin? Chem Phys Lett. 2013;590:187–191. doi:10.1016/j.cplett.2013.10.062.
  • Wang K, Ren X-W, Cui J-H, et al. Multistimuli responsive supramolecular polymeric nanoparticles formed by calixpyridinium and chondroitin 4-sulfate. ChemistrySelect. 2018;3:2789–2794. doi:10.1002/slct.201800570.
  • Jha PK, Desai PS, Li J, et al. Ph and salt effects on the associative phase separation of oppositely charged polyelectrolytes. Polymers. 2014;6:1414–1436. doi:10.3390/polym6051414.
  • Zhang Y, Cremer PS. Interactions between macromolecules and ions: the Hofmeister series. Curr Opin Chem Biol. 2006;10:658–663. doi:10.1016/j.cbpa.2006.09.020.
  • Follmann HDM, Naves AF, Martins AF, et al. Advanced fibroblast proliferation inhibition for biocompatible coating by electrostatic layer-by-layer assemblies of heparin and chitosan derivatives. J Colloid Interface Sci. 2016;474:9–17. doi:10.1016/j.jcis.2016.04.008.
  • Reisch A, Tirado P, Roger E, et al. Compact saloplastic poly(acrylic acid)/poly(allylamine) complexes: kinetic control over composition, microstructure, and mechanical properties. Adv Funct Mater. 2013;23:673–682. doi:10.1002/adfm.201201413.
  • Costa RR, Soares da Costa D, Reis RL, et al. Bioinspired baroplastic glycosaminoglycan sealants for soft tissues. Acta Biomater. 2019;87:108–117. doi:10.1016/j.actbio.2019.01.040.
  • Boddohi S, Moore N, Johnson PA, et al. Polysaccharide-based polyelectrolyte complex nanoparticles from chitosan, heparin, and hyaluronan. Biomacromolecules. 2009;10:1402–1409. doi:10.1021/bm801513e.
  • Guillot R, Gilde F, Becquart P, et al. The stability of BMP loaded polyelectrolyte multilayer coatings on titanium. Biomaterials. 2013;34:5737–5746. doi:10.1016/j.biomaterials.2013.03.067.
  • Carretero A, da Costa D S, Reis RL, et al. Extracellular matrix-inspired assembly of glycosaminoglycan–collagen fibers. J Mater Chem B. 2017;5:3103–3106. doi:10.1039/C7TB00704C.
  • Picart C, Mutterer J, Richert L, et al. Molecular basis for the explanation of the exponential growth of polyelectrolyte multilayers. Proc Natl Acad Sci USA. 2002;99:12531–5. doi:10.1073/pnas.202486099.
  • Silva C, Carretero A, Soares da Costa D, et al. Design of protein delivery systems by mimicking extracellular mechanisms for protection of growth factors. Acta Biomater. 2017;63:283–293. doi:10.1016/j.actbio.2017.08.042.
  • Hattori T, Kimura K, Seyrek E, et al. Binding of bovine serum albumin to heparin determined by turbidimetric titration and frontal analysis continuous capillary electrophoresis. Anal Biochem. 2001;295:158–167. doi:10.1006/abio.2001.5129.
  • Moerke NJ. Fluorescence polarization (FP) assays for monitoring peptide-protein or nucleic acid-protein binding. Curr Protoc Chem Biol. 2009;1:1–15. doi:10.1002/9780470559277.ch090102.
  • Köhling S, Blaszkiewicz J, Ruiz-Gómez G, et al. Syntheses of defined sulfated oligohyaluronans reveal structural effects, diversity and thermodynamics of GAG–protein binding. Chem Sci. 2019;10:866–878. doi:10.1039/C8SC03649G.
  • Amorim S, Pashkuleva I, Reis CA, et al. Tunable layer-by-layer films containing hyaluronic acid and their interactions with CD44. J Mater Chem B. 2020;8:3880–3885. doi:10.1039/D0TB00407C.
  • Novoa-Carballal R, Carretero A, Pacheco R, et al. Star-like glycosaminoglycans with superior bioactivity assemble with proteins into microfibers. Chem-Eur J. 2018;24:14341–14345. doi:10.1002/chem.201802243.
  • Water JJ, Schack MM, Velazquez-Campoy A, et al. Complex coacervates of hyaluronic acid and lysozyme: effect on protein structure and physical stability. Eur J Pharm Biopharm. 2014;88:325–331. doi:10.1016/j.ejpb.2014.09.001.
  • Crouzier T, Picart C. Ion pairing and hydration in polyelectrolyte multilayer films containing polysaccharides. Biomacromolecules. 2009;10:433–442. doi:10.1021/bm8012378.
  • Boudou T, Crouzier T, Auzély-Velty R, et al. Internal composition versus the mechanical properties of polyelectrolyte multilayer films: the influence of chemical cross-linking. Langmuir. 2009;25:13809–13819. doi:10.1021/la9018663.
  • Li M, Li X, McClements DJ, et al. Physicochemical and functional properties of lactoferrin-hyaluronic acid complexes: effect of non-covalent and covalent interactions. LWT. 2021;151:112121. doi:10.1016/j.lwt.2021.112121.
  • Hsu F-M, Hu M-H, Jiang Y-S, et al. Antibacterial polypeptide/heparin composite hydrogels carrying growth factor for wound healing. Mater Sci Eng, C. 2020;112:110923. doi:10.1016/j.msec.2020.110923.
  • Rodrigues MN, Oliveira MB, Costa RR, et al. Chitosan/chondroitin sulfate membranes produced by polyelectrolyte complexation for cartilage engineering. Biomacromolecules. 2016;17:2178–2188. doi:10.1021/acs.biomac.6b00399.
  • Mohtashamian S, Boddohi S, Hosseinkhani S. Preparation and optimization of self-assembled chondroitin sulfate-nisin nanogel based on quality by design concept. Int J Biol Macromol. 2018;107:2730–2739. doi:10.1016/j.ijbiomac.2017.10.156.
  • Campo GM, Avenoso A, Campo S, et al.. Antioxidant activity of chondroitin sulfate. Adv Pharmacol. 2006;53:417–431. doi:10.1016/S1054-3589(05)53020-5.
  • Marchettini N, Barbucci R, Bonechi C, et al. Structural study of hyaluronic acid oligomers and their complexes with copper in water by NMR and IR and molecular dynamics calculations. Macromol Symp. 1999;138:203–208. doi:10.1002/masy.19991380126.
  • Winter WT, Arnott S. Hyaluronic acid: the role of divalent cations in conformation and packing. J Mol Biol. 1977;117:761–784. doi:10.1016/0022-2836(77)90068-7.
  • Bayraktar H, Akal E, Sarper O, et al. Modeling glycosaminoglycans—hyaluronan, chondroitin, chondroitin sulfate A, chondroitin sulfate C and keratan sulfate. J Mol Struct: Theochem. 2004;683:121–132. doi:10.1016/j.theochem.2004.07.001.
  • Remko M, Van Duijnen PT, Broer R. Effect of metal ions (Li+, Na+, K+, Mg2+ and Ca2+) and water on the conformational changes of glycosidic bonds in heparin oligosaccharides. RSC Adv. 2013;3:9843–9853. doi:10.1039/C3RA40566D.
  • Hunter GK. An ion-exchange mechanism of cartilage calcification. Connect Tissue Res. 1987;16:111–120. doi:10.3109/03008208709001999.
  • He Z, Liu Z, Tian H, et al. Scalable production of core–shell nanoparticles by flash nanocomplexation to enhance mucosal transport for oral delivery of insulin. Nanoscale. 2018;10:3307–3319. doi:10.1039/C7NR08047F.
  • Lallana E, de la Rosa JM R, Tirella A, et al. Chitosan/hyaluronic acid nanoparticles: rational design revisited for RNA delivery. Mol Pharmaceutics. 2017;14:2422–2436. doi:10.1021/acs.molpharmaceut.7b00320.
  • Qiao D, Liu L, Chen Y, et al. Potency of a Scalable nanoparticulate subunit vaccine. Nano Lett. 2018;18:3007–3016. doi:10.1021/acs.nanolett.8b00478.
  • Rasente RY, Imperiale JC, Lázaro-Martínez JM, et al. Dermatan sulfate/chitosan polyelectrolyte complex with potential application in the treatment and diagnosis of vascular disease. Carbohydr Polym. 2016;144:362–370. doi:10.1016/j.carbpol.2016.02.046.
  • Soliman OY, Alameh MG, De Cresenzo G, et al. Efficiency of chitosan/hyaluronan-based mRNA delivery systems In vitro: influence of composition and structure. J Pharm Sci. 2020;109:1581–1593. doi:10.1016/j.xphs.2019.12.020.
  • Zhang J-S, Imai T, Otagiri M. Effects of a cisplatin-chondroitin sulfate A complex in reducing the nephrotoxicity of cisplatin. Arch Toxicol. 2000;74:300–307. doi:10.1007/s002040000124.
  • Zhang J-S, Anraku M, Kadowaki D, et al. Spectroscopic studies of interactions of chondroitin sulfates with cisplatin. Carbohydr Res. 2011;346:631–637. doi:10.1016/j.carres.2011.01.007.
  • Blocher WC, Perry SL. Complex coacervate-based materials for biomedicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017;9:e1442. doi:10.1002/wnan.1442.
  • Andreev M, Prabhu VM, Douglas JF, et al. Complex coacervation in polyelectrolytes from a coarse-grained model. Macromolecules. 2018;51:6717–6723. doi:10.1021/acs.macromol.8b00556.
  • Adhikari S, Leaf MA, Muthukumar M. Polyelectrolyte complex coacervation by electrostatic dipolar interactions. J Chem Phys. 2018;149:163308. doi:10.1063/1.5029268.
  • Lalevée G, Sudre G, Montembault A, et al. Polyelectrolyte complexes via desalting mixtures of hyaluronic acid and chitosan—physicochemical study and structural analysis. Carbohydr Polym. 2016;154:86–95. doi:10.1016/j.carbpol.2016.08.007.
  • Michaeli I, Overbeek JTG, Voorn MJ. Phase separation of polyelectrolyte solutions. J Polym Sci A. 1957;23:443–450. doi:10.1002/pol.1957.1202310337.
  • Overbeek JTG, Voorn MJ. Phase separation in polyelectrolyte solutions. theory of complex coacervation. J Cell Comp Physiol. 1957;49:7–26. doi:10.1002/jcp.1030490404.
  • Gucht J, Spruijt E, Lemmers M, et al. Polyelectrolyte complexes: bulk phases and colloidal systems. J Colloid Interface Sci. 2011;361:407–422. doi:10.1016/j.jcis.2011.05.080.
  • Meng S, Liu Y, Yeo J, et al. Effect of mixed solvents on polyelectrolyte complexes with salt. Colloid Polym Sci. 2020;298:887–894. doi:10.1007/s00396-020-04637-0.
  • Perry SL, Li Y, Priftis D, et al. The effect of salt on the complex coacervation of vinyl polyelectrolytes. Polymers. 2014;6:1756–1772. doi:10.3390/polym6061756.
  • Alkekhia D, Hammond PT, Shukla A. Layer-by-layer biomaterials for drug delivery. Annu Rev Biomed Eng. 2020;22:1–24. doi:10.1146/annurev-bioeng-060418-052350.
  • Antipina MN, Kiryukhin MV, Skirtach AG, et al. Micropackaging via layer-by-layer assembly: microcapsules and microchamber arrays. Int Mater Rev. 2014;59:224–244. doi:10.1179/1743280414Y.0000000030.
  • Costa RR, Mano JF. Polyelectrolyte multilayered assemblies in biomedical technologies. Chem Soc Rev. 2014;43:3453–3479. doi:10.1039/C3CS60393H.
  • Monge C, Almodóvar J, Boudou T, et al. Spatio-temporal control of LbL films for biomedical applications: from 2D to 3D. Adv Healthcare Mater. 2015;4:811–830. doi:10.1002/adhm.201400715.
  • Sui Z, Salloum D, Schlenoff JB. Effect of molecular weight on the construction of polyelectrolyte multilayers:  stripping versus sticking. Langmuir. 2003;19:2491–2495. doi:10.1021/la026531d.
  • Vale AC, Pereira P, Barbosa AM, et al. Antibacterial free-standing polysaccharide composite films inspired by the sea. Int J Biol Macromol. 2019;133:933–944. doi:10.1016/j.ijbiomac.2019.04.102.
  • Lavalle P, Picart C, Mutterer J, et al. Modeling the buildup of polyelectrolyte multilayer films having exponential growth. J Phys Chem B. 2004;108:635–648. doi:10.1021/jp035740j.
  • Picart C, Lavalle P, Hubert P, et al. Buildup mechanism for poly(l-lysine)/hyaluronic acid films onto a solid surface. Langmuir. 2001;17:7414–7424. doi:10.1021/la010848g.
  • Aggarwal N, Altgärde N, Svedhem S, et al. Effect of molecular composition of Heparin and cellulose sulfate on multilayer formation and cell response. Langmuir. 2013;29:13853–13864. doi:10.1021/la4028157.
  • Vikulina AS, Anissimov YG, Singh P, et al. Temperature effect on the build-up of exponentially growing polyelectrolyte multilayers. An exponential-to-linear transition point. Phys Chem Chem Phys. 2016;18:7866–7874. doi:10.1039/C6CP00345A.
  • Amaike M, Senoo Y, Yamamoto H. Sphere, honeycomb, regularly spaced droplet and fiber structures of polyion complexes of chitosan and gellan. Macromol Rapid Commun. 1998;19:287–289. doi:10.1002/(SICI)1521-3927(19980601)19:6.
  • Wan ACA, Cutiongco MFA, Tai BCU, et al. Fibers by interfacial polyelectrolyte complexation – processes, materials and applications. Mater Today. 2016;19:437–450. doi:10.1016/j.mattod.2016.01.017.
  • Toivonen MS, Kurki-Suonio S, Wagermaier W, et al. Interfacial polyelectrolyte complex spinning of cellulose nanofibrils for advanced bicomponent fibers. Biomacromolecules. 2017;18:1293–1301. doi:10.1021/acs.biomac.7b00059.
  • Cui Q, Bell DJ, Rauer SB, et al. Wet-Spinning of biocompatible core–shell polyelectrolyte complex fibers for tissue engineering. Adv Mater Interfaces. 2020;7:2000849. doi:10.1002/admi.202000849.
  • Ohkawa K, Takahashi Y, Yamada M, et al. Polyion complex fiber and capsule formed by self-assembly of chitosan and poly(α,L-glutamic acid) at solution interfaces. Macromol Mater Eng. 2001;286:168–175. doi:10.1002/1439-2054(20010301)286:3.
  • Capito RM, Azevedo HS, Velichko YS, et al. Self-assembly of large and small molecules into hierarchically ordered sacs and membranes. Science. 2008;319:1812–1816. doi:10.1126/science.1154586.
  • Mendes AC, Smith KH, Tejeda-Montes E, et al. Co-assembled and microfabricated bioactive membranes. Adv Funct Mater. 2013;23:430–438. doi:10.1002/adfm.201201065.
  • Iijima K, Tsuji Y, Kuriki I, et al. Control of cell adhesion and proliferation utilizing polysaccharide composite film scaffolds. Colloids Surf, B. 2017;160:228–237. doi:10.1016/j.colsurfb.2017.09.025.
  • Gonzalez-Leon JA, Acar MH, Ryu S-W, et al. Low-temperature processing of ‘baroplastics’ by pressure-induced flow. Nature. 2003;426:424–428. doi:10.1038/nature02140.
  • Lv Z, Qiao J-N, Song Y-N, et al. Baroplastics with robust mechanical properties and reserved processability through hydrogen-bonded interactions. ACS Appl Mater Interfaces. 2019;11:12008–12016. doi:10.1021/acsami.8b20676.
  • Porcel CH, Schlenoff JB. Compact polyelectrolyte complexes: “saloplastic” candidates for biomaterials. Biomacromolecules. 2009;10:2968–2975. doi:10.1021/bm900373c.
  • Huang K-T, Ishihara K, Huang C-J. Polyelectrolyte and antipolyelectrolyte effects for dual salt-responsive interpenetrating network hydrogels. Biomacromolecules. 2019;20:3524–3534. doi:10.1021/acs.biomac.9b00796.
  • Markarian MZ, Hariri HH, Reisch A, et al. A small-angle neutron scattering study of the equilibrium conformation of polyelectrolytes in stoichiometric saloplastic polyelectrolyte complexes. Macromolecules. 2012;45:1016–1024. doi:10.1021/ma2022666.
  • Shamoun RF, Reisch A, Schlenoff JB. Extruded saloplastic polyelectrolyte complexes. Adv Funct Mater. 2012;22:1923–1931. doi:10.1002/adfm.201102787.
  • Yang L, Gao S, Asghar S, et al. Hyaluronic acid/chitosan nanoparticles for delivery of curcuminoid and its in vitro evaluation in glioma cells. Int J Biol Macromol. 2015;72:1391–1401. doi:10.1016/j.ijbiomac.2014.10.039.
  • Lookene A, Chevreuil O, Østergaard P, et al. Interaction of lipoprotein lipase with heparin fragments and with heparan sulfate:  stoichiometry, stabilization, and kinetics. Biochemistry. 1996;35:12155–12163. doi:10.1021/bi960008e.
  • van de Weert M, Andersen MB, Frokjaer S. Complex coacervation of lysozyme and heparin: complex characterization and protein stability. Pharm Res. 2004;21:2354–2359. doi:10.1007/s11095-004-7689-z.
  • Duan H, Donovan M, Hernandez F, et al. Hyaluronic-acid-presenting self-assembled nanoparticles transform a hyaluronidase HYAL1 substrate into an efficient and selective inhibitor. Angew Chem Int Ed. 2020;59:13591–13596. doi:10.1002/anie.202005212.
  • Blachman A, Funez F, Birocco AM, et al. Targeted anti-inflammatory peptide delivery in injured endothelial cells using dermatan sulfate/chitosan nanomaterials. Carbohydr Polym. 2020;230:115610. doi:10.1016/j.carbpol.2019.115610.
  • Tan K, Duquette M, Liu J-h, et al. The structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin. Structure. 2006;14:33–42. doi:10.1016/j.str.2005.09.017.
  • Webb LM, Ehrengruber MU, Clark-Lewis I, et al. Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc Natl Acad Sci USA. 1993;90:7158–7162. doi:10.1073/pnas.90.15.7158.
  • Li W, Johnson DJD, Esmon CT, et al. Structure of the antithrombin–thrombin–heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol. 2004;11:857–862. doi:10.1038/nsmb811.
  • Cardoso MJ, Caridade SG, Costa RR, et al. Enzymatic degradation of polysaccharide-based layer-by-layer structures. Biomacromolecules. 2016;17:1347–1357. doi:10.1021/acs.biomac.5b01742.
  • Novoa-Carballal R, Silva C, Möller S, et al. Tunable nano-carriers from clicked glycosaminoglycan block copolymers. J Mater Chem B. 2014;2:4177–4184. doi:10.1039/C4TB00410H.
  • Volodkin D, Ball V, Schaaf P, et al. Complexation of phosphocholine liposomes with polylysine. stabilization by surface coverage versus aggregation. Biochim Biophys Acta, Biomembr. 2007;1768:280–290. doi:10.1016/j.bbamem.2006.09.015.
  • Ribeiro TG, Chávez-Fumagalli MA, Valadares DG, et al. Novel targeting using nanoparticles: an approach to the development of an effective anti-leishmanial drug-delivery system. Int J Nanomed. 2014;9:877–890. doi:10.2147/IJN.S55678.
  • Danielsen S, Strand S, de Lange Davies C, et al. Glycosaminoglycan destabilization of DNA–chitosan polyplexes for gene delivery depends on chitosan chain length and GAG properties. Biochim Biophys Acta Gen Subj. 2005;1721:44–54. doi:10.1016/j.bbagen.2004.10.011.
  • Moret I, Esteban Peris J, Guillem VM, et al. Stability of PEI–DNA and DOTAP–DNA complexes: effect of alkaline pH, heparin and serum. J Controlled Release. 2001;76:169–181. doi:10.1016/S0168-3659(01)00415-1.
  • Landázuri N, Le Doux JM. Complexation of retroviruses with charged polymers enhances gene transfer by increasing the rate that viruses are delivered to cells. J Gene Med. 2004;6:1304–1319. doi:10.1002/jgm.618.
  • Germershaus O, Lühmann T, Rybak JC, et al. Application of natural and semi-synthetic polymers for the delivery of sensitive drugs. Int Mater Rev. 2015;60:101–131. doi:10.1179/1743280414Y.0000000045.
  • Duceppe N, Tabrizian M. Factors influencing the transfection efficiency of ultra low molecular weight chitosan/hyaluronic acid nanoparticles. Biomaterials. 2009;30:2625–2631. doi:10.1016/j.biomaterials.2009.01.017.
  • Costa-Almeida R, Gasperini L, Borges J, et al. Microengineered multicomponent hydrogel fibers: combining polyelectrolyte complexation and microfluidics. ACS Biomater Sci Eng. 2017;3:1322–1331. doi:10.1021/acsbiomaterials.6b00331.
  • Darby IA, Hewitson TD.. Fibroblast differentiation in wound healing and fibrosis. Int Rev Cytol. 2007: 143–179. doi:10.1016/S0074-7696(07)57004-X.
  • Vishwakarma A, Bhise NS, Evangelista MB, et al. Engineering immunomodulatory biomaterials to tune the inflammatory response. Trends Biotechnol. 2016;34:470–482. doi:10.1016/j.tibtech.2016.03.009.
  • Francesko A, Soares da Costa D, Reis RL, et al. Functional biopolymer-based matrices for modulation of chronic wound enzyme activities. Acta Biomater. 2013;9:5216–5225. doi:10.1016/j.actbio.2012.10.014.
  • Shu M, Long S, Huang Y, et al. High strength and antibacterial polyelectrolyte complex CS/HS hydrogel films for wound healing. Soft Matter. 2019;15:7686–7694. doi:10.1039/C9SM01380F.
  • Francesko A, Ivanova K, Hoyo J, et al. Bottom-up layer-by-layer assembling of antibacterial freestanding nanobiocomposite films. Biomacromolecules. 2018;19:3628–3636. doi:10.1021/acs.biomac.8b00626.
  • Ivanova A, Ivanova K, Hoyo J, et al. Layer-by-layer decorated nanoparticles with tunable antibacterial and antibiofilm properties against both gram-positive and gram-negative bacteria. ACS Appl Mater Interfaces. 2018;10:3314–3323. doi:10.1021/acsami.7b16508.
  • Francesko A, Fernandes MM, Ivanova K, et al. Bacteria-responsive multilayer coatings comprising polycationic nanospheres for bacteria biofilm prevention on urinary catheters. Acta Biomater. 2016;33:203–212. doi:10.1016/j.actbio.2016.01.020.
  • Bertolami CN, Messadi DV. The role of proteoglycans in hard and soft tissue repair. Crit Rev Oral Biol M. 1994;5:311–337. doi:10.1177/10454411940050030601.
  • Hachim D, Whittaker TE, Kim H, et al. Glycosaminoglycan-based biomaterials for growth factor and cytokine delivery: making the right choices. J Controlled Release. 2019;313:131–147. doi:10.1016/j.jconrel.2019.10.018.
  • Salbach J, Rachner TD, Rauner M, et al. Regenerative potential of glycosaminoglycans for skin and bone. J Mol Med. 2012;90:625–635. doi:10.1007/s00109-011-0843-2.
  • Ferreira DS, Marques AP, Reis RL, et al. Hyaluronan and self-assembling peptides as building blocks to reconstruct the extracellular environment in skin tissue. Biomater Sci. 2013;1:952–964. doi:10.1039/C3BM60019J.
  • Radhakrishnan J, Subramanian A, Sethuraman S. Injectable glycosaminoglycan–protein nano-complex in semi-interpenetrating networks: a biphasic hydrogel for hyaline cartilage regeneration. Carbohydr Polym. 2017;175:63–74. doi:10.1016/j.carbpol.2017.07.063.
  • Crouzier T, Szarpak A, Boudou T, et al. Polysaccharide-blend multilayers containing hyaluronan and heparin as a delivery system for rhBMP-2. Small. 2010;6:651–662. doi:10.1002/smll.200901728.
  • Kisiel M, Klar AS, Ventura M, et al. Complexation and sequestration of BMP-2 from an ECM mimetic hyaluronan gel for improved bone formation. PLoS One. 2013;8:e78551. doi:10.1371/journal.pone.0078551.
  • Choi A, Seo KD, Kim DW, et al. Recent advances in engineering microparticles and their nascent utilization in biomedical delivery and diagnostic applications. Lab Chip. 2017;17:591–613. doi:10.1039/C6LC01023G.
  • Fan Y, Wang S, Zhang F. Optical multiplexed bioassays for improved biomedical diagnostics. Angew Chem Int Ed. 2019;58:13208–13219. doi:10.1002/anie.201901964.
  • Siegel G, Malmsten M, Klüßendorf D, et al. A receptor-based biosensor for lipoprotein docking at the endothelial surface and vascular matrix. Biosens Bioelectron. 2001;16:895–904. doi:10.1016/S0956-5663(01)00235-4.
  • Wasik D, Mulchandani A, Yates MV. A heparin-functionalized carbon nanotube-based affinity biosensor for dengue virus. Biosens Bioelectron. 2017;91:811–816. doi:10.1016/j.bios.2017.01.017.
  • Ma SC, Yang VC, Fu B, et al. Electrochemical sensor for heparin: further characterization and bioanalytical applications. Anal Chem. 1993;65:2078–2084. doi:10.1021/ac00063a024.
  • Meng F, Liang W, Sun H, et al. A peptide-based electrochemical biosensor for facile measurement of whole-blood heparin. ChemElectroChem. 2017;4:472–475. doi:10.1002/celc.201600680.
  • Li D, Qin J, Lv J, et al. “Turn on” room-temperature phosphorescent biosensors for detection of hyaluronic acid based on manganese-doped ZnS quantum dots. RSC Adv. 2018;8:2873–2879. doi:10.1039/C7RA11858A.
  • Pu K-Y, Liu B. Conjugated polyelectrolytes as light-up macromolecular probes for heparin sensing. Adv Funct Mater. 2009;19:277–284. doi:10.1002/adfm.200800960.
  • Zheng Z, Geng W-C, Gao J, et al. Differential calixarene receptors create patterns that discriminate glycosaminoglycans. Org Chem Front. 2018;5:2685–2691. doi:10.1039/C8QO00606G.

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