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The Role of Hyaluronic Acid in Tissue Engineering

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Polysaccharides of Microbial Origin

Abstract

Hyaluronic acid (HA) is a glycosaminoglycan that is found in extracellular tissue in many parts of the body. It is a material of increasing importance to biomaterial science and is finding applications in diverse areas ranging from tissue culture scaffolds to cosmetic materials. This chapter considers the recent research on the role of HA in tissue engineering and the importance of HA as an immunomodulatory material. The chemical modifications and processing methods employed to produce HA-modified tissue scaffolds are discussed, thus giving a better understanding of the structure-function-property relationships that influence scaffold performance, tissue growth, and regeneration. The chapter concludes with a vision for the future of HA in tissue-engineered constructs.

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References

  • Abu-Hakmeh A, Kung A, Mintz BR, Kamal S, Cooper JA, Lu XL, et al. Sequential gelation of tyramine-substituted hyaluronic acid hydrogels enhances mechanical integrity and cell viability. Med Biol Eng Comput. 2016;54:1893–902.

    Article  PubMed  Google Scholar 

  • Acharya PS, Majumdar S, Jacob M, Hayden J, Mrass P, Weninger W, et al. Fibroblast migration is mediated by CD44-dependent TGF beta activation. J Cell Sci. 2008;121(Pt 9):1393–402.

    Article  CAS  PubMed  Google Scholar 

  • Ahmadian E, Dizaj SM, Eftekhari A, Dalir E, Vahedi P, Hasanzadeh A, et al. The potential applications of hyaluronic acid hydrogels in biomedicine. Drug Res. 2020;70(1):6–11.

    Article  CAS  Google Scholar 

  • Antich C, de Vicente J, Jiménez G, Chocarro C, Carrillo E, Montañez E, et al. Bio-inspired hydrogel composed of hyaluronic acid and alginate as a potential bioink for 3D bioprinting of articular cartilage engineering constructs. Acta Biomater. 2020;106:114–23.

    Article  CAS  PubMed  Google Scholar 

  • Ardizzoni A, Neglia RG, Baschieri MC, Cermelli C, Caratozzolo M, Righi E, et al. Influence of hyaluronic acid on bacterial and fungal species, including clinically relevant opportunistic pathogens. J Mater Sci Mater Med. 2011;22(10):2329.

    Article  CAS  PubMed  Google Scholar 

  • Asami K, Inagaki A, Imura T, Sekiguchi S, Fujimori K, Masutani H, et al. Thioredoxin-1 attenuates early graft loss after intraportal islet transplantation in mice. PLoS One. 2013;8(8):e70259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Av T, Mohanty S, Dinda AK, Koul V. Fabrication and evaluation of gelatin/hyaluronic acid/chondroitin sulfate/asiatic acid based biopolymeric scaffold for the treatment of second degree burn wounds–Wistar rat model study. Biomed Mater. 2020;15:055016.

    Article  Google Scholar 

  • Bae MS, Ohe JY, Lee JB, Heo DN, Byun W, Bae H, et al. Photo-cured hyaluronic acid-based hydrogels containing growth and differentiation factor 5 (GDF-5) for bone tissue regeneration. Bone. 2014;59:189–98.

    Article  CAS  PubMed  Google Scholar 

  • Baier Leach J, Bivens KA, Patrick CW Jr, Schmidt CE. Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol Bioeng. 2003;82(5):578–89.

    Article  PubMed  CAS  Google Scholar 

  • Bal T, Kepsutlu B, Kizilel S. Characterization of protein release from poly(ethylene glycol) hydrogels with crosslink density gradients. J Biomed Mater Res A. 2014;102(2):487–95.

    Article  PubMed  CAS  Google Scholar 

  • Ballini A, Cantore S, Capodiferro S, Grassi FR. Esterified hyaluronic acid and autologous bone in the surgical correction of the infra-bone defects. Int J Med Sci. 2009;6(2):65–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baranova NS, Nileback E, Haller FM, Briggs DC, Svedhem S, Day AJ, et al. The inflammation-associated protein TSG-6 cross-links hyaluronan via hyaluronan-induced TSG-6 oligomers. J Biol Chem. 2011;286(29):25675–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bautista-Hernandez LA, Gomez-Olivares JL, Buentello-Volante B, Manuel Bautista-de Lucio V. Fibroblasts: the unknown sentinels eliciting immune responses against microorganisms. Eur J Microbiol Immunol. 2017;7(3):151–7.

    Article  CAS  Google Scholar 

  • Bencherif SA, Srinivasan A, Horkay F, Hollinger JO, Matyjaszewski K, Washburn NR. Influence of the degree of methacrylation on hyaluronic acid hydrogels properties. Biomaterials. 2008;29(12):1739–49.

    Article  CAS  PubMed  Google Scholar 

  • Bergman K, Elvingson C, Hilborn J, Svensk G, Bowden T. Hyaluronic acid derivatives prepared in aqueous media by triazine-activated amidation. Biomacromolecules. 2007;8(7):2190–5.

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya M, Wozniak DJ, Stoodley P, Hall-Stoodley L. Prevention and treatment of Staphylococcus aureus biofilms. Expert Rev Anti-Infect Ther. 2015;13(12):1499–516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhowmick S, Scharnweber D, Koul V. Co-cultivation of keratinocyte-human mesenchymal stem cell (hMSC) on sericin loaded electrospun nanofibrous composite scaffold (cationic gelatin/hyaluronan/chondroitin sulfate) stimulates epithelial differentiation in hMSCs: in vitro study. Biomaterials. 2016;88:83–96.

    Article  CAS  PubMed  Google Scholar 

  • Bhowmick S, Thanusha AV, Kumar A, Scharnweber D, Rother S, Koul V. Nanofibrous artificial skin substitute composed of mPEG-PCL grafted gelatin/hyaluronan/chondroitin sulfate/sericin for 2nd degree burn care: in vitro and in vivo study. RSC Adv. 2018;8(30):16420–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blount ZD. The unexhausted potential of E. coli. elife. 2015;4:e05826.

    Article  PubMed Central  Google Scholar 

  • Bulpitt P, Aeschlimann D. New strategy for chemical modification of hyaluronic acid: preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J Biomed Mater Res. 1999;47(2):152–69.

    Article  CAS  PubMed  Google Scholar 

  • Burdick JA, Prestwich GD. Hyaluronic acid hydrogels for biomedical applications. Adv Mater. 2011;23(12):H41–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burdick JA, Chung C, Jia X, Randolph MA, Langer R. Controlled degradation and mechanical behavior of photopolymerized hyaluronic acid networks. Biomacromolecules. 2005;6(1):386–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burnside ER, Bradbury EJ. Manipulating the extracellular matrix and its role in brain and spinal cord plasticity and repair. Neuropathol Appl Neurobiol. 2014;40(1):26–59.

    Article  CAS  PubMed  Google Scholar 

  • Cahill D, Zamboni F, Collins MN. Radiological advances in pancreatic islet transplantation. Acad Radiol. 2019;26(11):1536–43.

    Article  PubMed  Google Scholar 

  • Cankaya ZT, Gurbuz S, Bakirarar B, Kurtis B. Evaluation of the effect of hyaluronic acid application on the vascularization of free gingival graft for both donor and recipient sites with laser Doppler flowmetry: a randomized, examiner-blinded, controlled clinical trial. Int J Periodontics Restorative Dent. 2020;40(2):233–43.

    Article  PubMed  Google Scholar 

  • Cao B, Wang Y, Wen D, Liu W, Wang J, Fan G, et al. A trial of lopinavir–ritonavir in adults hospitalized with severe covid-19. N Engl J Med. 2020;382(19):1787–99.

    Article  PubMed  Google Scholar 

  • Carlson GA, Dragoo JL, Samimi B, Bruckner DA, Bernard GW, Hedrick M, et al. Bacteriostatic properties of biomatrices against common orthopaedic pathogens. Biochem Bioph Res Commun. 2004;321(2):472–8.

    Article  CAS  Google Scholar 

  • Cermelli C, Cuoghi A, Scuri M, Bettua C, Neglia RG, Ardizzoni A, et al. In vitro evaluation of antiviral and virucidal activity of a high molecular weight hyaluronic acid. Virol J. 2011;8(1):141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chanda A, Adhikari J, Ghosh A, Chowdhury SR, Thomas S, Datta P, et al. Electrospun chitosan/polycaprolactone-hyaluronic acid bilayered scaffold for potential wound healing applications. Int J Biol Macromol. 2018;116:774–85.

    Article  CAS  PubMed  Google Scholar 

  • Chen JX, Cao LJ, Shi Y, Wang P, Chen JH. In situ supramolecular hydrogel based on hyaluronic acid and dextran derivatives as cell scaffold. J Biomed Mater Res A. 2016a;104(9):2263–70.

    Google Scholar 

  • Chen SY, He ZH, Xu GJ, Xiao XF. Fabrication of nanofibrous tubular scaffolds for bone tissue engineering. Mater Lett. 2016b;182:289–93.

    Article  CAS  Google Scholar 

  • Choh SY, Cross D, Wang C. Facile synthesis and characterization of disulfide-cross-linked hyaluronic acid hydrogels for protein delivery and cell encapsulation. Biomacromolecules. 2011;12(4):1126–36.

    Article  CAS  PubMed  Google Scholar 

  • Choi SC, Yoo MA, Lee SY, Lee HJ, Son DH, Jung J, et al. Modulation of biomechanical properties of hyaluronic acid hydrogels by crosslinking agents. J Biomed Mater Res A. 2015;103(9):3072–80.

    Article  CAS  PubMed  Google Scholar 

  • Ciccone V, Zazzetta M, Morbidelli L. Comparison of the effect of two hyaluronic acid preparations on fibroblast and endothelial cell functions related to angiogenesis. Cell. 2019;8(12):1479.

    Article  CAS  Google Scholar 

  • Clark CC, Aleman J, Mutkus L, Skardal A. A mechanically robust thixotropic collagen and hyaluronic acid bioink supplemented with gelatin nanoparticles. Bioprinting. 2019;16:e00058.

    Article  Google Scholar 

  • Clegg TE, Caborn D, Mauffrey C. Viscosupplementation with hyaluronic acid in the treatment for cartilage lesions: a review of current evidence and future directions. Eur J Orthop Surg Traumatol. 2013;23:119–24.

    Article  PubMed  Google Scholar 

  • Cohen M, Braun E, Tsalenchuck Y, Panet A, Steiner I. Restrictions that control herpes simplex virus type 1 infection in mouse brain ex vivo. J Gen Virol. 2011;92(10):2383–93.

    Article  CAS  PubMed  Google Scholar 

  • Collins MN, Birkinshaw C. Comparison of the effectiveness of four different crosslinking agents with hyaluronic acid hydrogel films for tisslue-culture applications. J Appl Polym Sci. 2007;104(5):3183–91.

    Article  CAS  Google Scholar 

  • Collins MN, Birkinshaw C. Investigation of the swelling behavior of crosslinked hyaluronic acid films and hydrogels produced using homogeneous reactions. J Appl Polym Sci. 2008;109(2):923–31.

    Article  CAS  Google Scholar 

  • Collins MN, Birkinshaw C. Morphology of crosslinked hyaluronic acid porous hydrogels. J Appl Polym Sci. 2010;120:1040–9.

    Article  CAS  Google Scholar 

  • Collins MN, Birkinshaw C. Hyaluronic acid based scaffolds for tissue engineering-a review. Carbohydr Polym. 2013a;92(2):1262–79.

    Article  CAS  PubMed  Google Scholar 

  • Collins MN, Birkinshaw C. Hyaluronic acid solutions A processing method for efficient chemical modification. J Appl Polym Sci. 2013b;130(1):145–52.

    Article  CAS  Google Scholar 

  • Colson P, Rolain J-M, Lagier J-C, Brouqui P, Raoult D. Chloroquine and hydroxychloroquine as available weapons to fight COVID-19. Int J Antimicrob Agents. 2020;55(4):105932.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conrad TL, Roeder RK. Effects of porogen morphology on the architecture, permeability, and mechanical properties of hydroxyapatite whisker reinforced polyetheretherketone scaffolds. J Mech Behav Biomed Mater. 2020;106:103730.

    Article  CAS  PubMed  Google Scholar 

  • Costantini M, Barbetta A. Gas foaming technologies for 3D scaffold engineering. In: Functional 3D tissue engineering scaffolds. Duxford: Elsevier; 2018. p. 127–49.

    Chapter  Google Scholar 

  • Credi C, De Marco C, Molena E, Nava MM, Raimondi MT, Levi M, et al. Direct photo-patterning of hyaluronic acid baits onto a fouling-release perfluoropolyether surface for selective cancer cell capture and immobilization. Mat Sci Eng C Mater. 2016;62:414–22.

    Article  CAS  Google Scholar 

  • Crescenzi V, Francescangeli A, Capitani D, Mannina L, Renier D, Bellini D. Hyaluronan networking via Ugi’s condensation using lysine as cross-linker diamine. Carbohydr Polym. 2003a;53(3):311–6.

    Article  CAS  Google Scholar 

  • Crescenzi V, Francescangeli A, Taglienti A, Capitani D, Mannina L. Synthesis and partial characterization of hydrogels obtained via glutaraldehyde crosslinking of acetylated chitosan and of hyaluronan derivatives. Biomacromolecules. 2003b;4(4):1045–54.

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Xu H, Zhou S, Zhao T, Liu A, Guo X, et al. Evaluation of angiogenic activities of hyaluronan oligosaccharides of defined minimum size. Life Sci. 2009;85(15–16):573–7.

    Article  CAS  PubMed  Google Scholar 

  • Danishefsky I, Siskovic E. Conversion of carboxyl groups of mucopolysaccharides into amides of amino acid esters. Carbohydr Res. 1971;16(1):199–205.

    Article  CAS  Google Scholar 

  • de Nooy AE, Capitani D, Masci G, Crescenzi V. Ionic polysaccharide hydrogels via the Passerini and Ugi multicomponent condensations: synthesis, behavior and solid-state NMR characterization. Biomacromolecules. 2000;1(2):259–67.

    Article  PubMed  CAS  Google Scholar 

  • del Hoyo-Gallego S, Pérez-Álvarez L, Gómez-Galván F, Lizundia E, Kuritka I, Sedlarik V, et al. Construction of antibacterial poly(ethylene terephthalate) films via layer by layer assembly of chitosan and hyaluronic acid. Carbohydr Polym. 2016;143:35–43.

    Article  PubMed  CAS  Google Scholar 

  • Della Valle F, Romeo A (1997) Crosslinked carboxy polysaccharides. Google Patents

    Google Scholar 

  • Diaz-Gomez L, Concheiro A, Alvarez-Lorenzo C, Garcia-Gonzalez CA. Growth factors delivery from hybrid PCL-starch scaffolds processed using supercritical fluid technology. Carbohydr Polym. 2016;142:282–92.

    Article  CAS  PubMed  Google Scholar 

  • Ding JX, Zhang J, Li JN, Li D, Xiao CS, Xiao HH, et al. Electrospun polymer biomaterials. Prog Polym Sci. 2019;90:1–34.

    Article  CAS  Google Scholar 

  • Drews G, Krippeit-Drews P, Dufer M. Oxidative stress and beta-cell dysfunction. Pflugers Arch - Eur J Physiol. 2010;460(4):703–18.

    Article  CAS  Google Scholar 

  • Eenschooten C, Guillaumie F, Kontogeorgis GM, Stenby EH, Schwach-Abdellaoui K. Preparation and structural characterisation of novel and versatile amphiphilic octenyl succinic anhydride–modified hyaluronic acid derivatives. Carbohydr Polym. 2010;79(3):597–605.

    Article  CAS  Google Scholar 

  • Farrell K, Joshi J, Kothapalli CR. Injectable uncrosslinked biomimetic hydrogels as candidate scaffolds for neural stem cell delivery. J Biomed Mater Res A. 2017;105(3):790–805.

    Article  CAS  PubMed  Google Scholar 

  • Figueira DR, Miguel SP, de Sa KD, Correia IJ. Production and characterization of polycaprolactone- hyaluronic acid/chitosan- zein electrospun bilayer nanofibrous membrane for tissue regeneration. Int J Biol Macromol. 2016;93:1100–10.

    Article  CAS  PubMed  Google Scholar 

  • Follain N, Montanari S, Jeacomine I, Gambarelli S, Vignon MR. Coupling of amines with polyglucuronic acid: evidence for amide bond formation. Carbohydr Polym. 2008;74(3):333–43.

    Article  CAS  Google Scholar 

  • Fuhrmann T, Obermeyer J, Tator CH, Shoichet MS. Click-crosslinked injectable hyaluronic acid hydrogel is safe and biocompatible in the intrathecal space for ultimate use in regenerative strategies of the injured spinal cord. Methods. 2015;84:60–9.

    Article  CAS  PubMed  Google Scholar 

  • Führmann T, Tam RY, Ballarin B, Coles B, Elliott Donaghue I, Van Der Kooy D, et al. Injectable hydrogel promotes early survival of induced pluripotent stem cell-derived oligodendrocytes and attenuates longterm teratoma formation in a spinal cord injury model. Biomaterials. 2016;83:23–36.

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Sun Y, Yang H, Qiu P, Cong Z, Zou Y, et al. A low molecular weight hyaluronic acid derivative accelerates excisional wound healing by modulating pro-inflammation, promoting epithelialization and neovascularization, and remodeling collagen. Int J Mol Sci. 2019;20(15):3722.

    Article  CAS  PubMed Central  Google Scholar 

  • Gaudet AD, Popovich PG. Extracellular matrix regulation of inflammation in the healthy and injured spinal cord. Exp Neurol. 2014;258:24–34.

    Article  CAS  PubMed  Google Scholar 

  • Gautret P, Lagier J-C, Parola P, Hoang VT, Meddeb L, Mailhe M, et al. Hydroxychloroquine and azithromycin as a treatment of COVID-19: results of an open-label non-randomized clinical trial. Int J Antimicrob Agents. 2020;56:105949.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gleadall A, Visscher D, Yang J, Thomas D, Segal J. Review of additive manufactured tissue engineering scaffolds: relationship between geometry and performance. Burns Trauma. 2018;6

    Google Scholar 

  • Godesky MD (2020) Hyaluronic acid-based bioinks for cell-friendly bioprinting. Rutgers University-School of Graduate Studies

    Google Scholar 

  • Gomez-Aristizabal A, Kim KP, Viswanathan S. A systematic study of the effect of different molecular weights of hyaluronic acid on mesenchymal stromal cell-mediated immunomodulation. PLoS One. 2016;11(1):e0147868.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gupta D, Tator CH, Shoichet MS. Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials. 2006;27(11):2370–9.

    Article  CAS  PubMed  Google Scholar 

  • Guzińska K, Kaźmierczak D, Dymel M, Pabjańczyk-Wlazło E, Boguń M. Anti-bacterial materials based on hyaluronic acid: selection of research methodology and analysis of their anti-bacterial properties. Mater Sci Eng C. 2018;93:800–8.

    Article  CAS  Google Scholar 

  • Gwon K, Kim E, Tae G. Heparin-hyaluronic acid hydrogel in support of cellular activities of 3D encapsulated adipose derived stem cells. Acta Biomater. 2017;49:284–95.

    Article  CAS  PubMed  Google Scholar 

  • Hallmann R, Zhang X, Di Russo J, Li L, Song J, Hannocks MJ, et al. The regulation of immune cell trafficking by the extracellular matrix. Curr Opin Cell Biol. 2015;36:54–61.

    Article  CAS  PubMed  Google Scholar 

  • Han CZ, Luo X, Zou D, Li JA, Zhang K, Yang P, et al. Nature-inspired extracellular matrix coating produced by micro-patterned smooth muscle and endothelial cells endows cardiovascular materials with better biocompatibility. Biomater Sci. 2019;7(7):2686–701.

    Article  CAS  PubMed  Google Scholar 

  • Harris LG, Richards RG.Staphylococcus aureus adhesion to different treated titanium surfaces. J Mater Sci Mater Med 2004;15(4):311–4.

    Google Scholar 

  • He Z, Zang H, Zhu L, Huang K, Yi T, Zhang S, et al. An anti-inflammatory peptide and brain-derived neurotrophic factor-modified hyaluronan-methylcellulose hydrogel promotes nerve regeneration in rats with spinal cord injury. Int J Nanomedicine. 2019;14:721–32.

    Article  PubMed  PubMed Central  Google Scholar 

  • Highley CB, Prestwich GD, Burdick JA. Recent advances in hyaluronic acid hydrogels for biomedical applications. Curr Opin Biotechnol. 2016;40:35–40.

    Article  CAS  PubMed  Google Scholar 

  • Hirano K, Sakai S, Ishikawa T, Avci FY, Linhardt RJ, Toida T. Preparation of the methyl ester of hyaluronan and its enzymatic degradation. Carbohydr Res. 2005;340(14):2297–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirayama Y, Yoshimura M, Ozeki Y, Sugawara I, Udagawa T, Mizuno S, et al. Mycobacteria exploit host hyaluronan for efficient extracellular replication. PLoS Pathog. 2009;5(10):e1000643.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ho MT, Teal CJ, Shoichet MS. A hyaluronan/methylcellulose-based hydrogel for local cell and biomolecule delivery to the central nervous system. Brain Res Bull. 2019;148:46–54.

    Article  CAS  PubMed  Google Scholar 

  • Hokmabad VR, Davaran S, Ramazani A, Salehi R. Design and fabrication of porous biodegradable scaffolds: a strategy for tissue engineering. J Biomat Sci Polym E. 2017;28(16):1797–825.

    Article  CAS  Google Scholar 

  • Hu W, Yen Y-T, Singh S, Kao C-L, Wu-Hsieh BA. SARS-CoV regulates immune function-related gene expression in human monocytic cells. Viral Immunol. 2012;25(4):277–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hui E, Gimeno KI, Guan G, Caliari SR (2019) Spatial control of viscoelasticity in phototunable hyaluronic acid hydrogels. BioRxiv 646778

    Google Scholar 

  • Huin-Amargier C, Marchal P, Payan E, Netter P, Dellacherie E. New physically and chemically crosslinked hyaluronate (HA)-based hydrogels for cartilage repair. J Biomed Mater Res A. 2006;76(2):416–24.

    Article  PubMed  CAS  Google Scholar 

  • Ibberson CB, Parlet CP, Kwiecinski J, Crosby HA, Meyerholz DK, Horswill AR. Hyaluronan modulation impacts Staphylococcus aureus biofilm infection. Infect Immun. 2016;84(6):1917–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda K, Yamauchi D, Osamura N, Hagiwara N, Tomita K. Hyaluronic acid prevents peripheral nerve adhesion. Br J Plast Surg. 2003;56(4):342–7.

    Article  CAS  PubMed  Google Scholar 

  • Jeon S, Karkhanechi H, Fang LF, Cheng L, Ono T, Nakamura R, et al. Novel preparation and fundamental characterization of polyamide 6 self-supporting hollow fiber membranes via thermally induced phase separation (TIPS). J Membr Sci. 2018;546:1–14.

    Article  CAS  Google Scholar 

  • Jha AK, Malik MS, Farach-Carson MC, Duncan RL, Jia XQ. Hierarchically structured, hyaluronic acid-based hydrogel matrices via the covalent integration of microgels into macroscopic networks. Soft Matter. 2010;6(20):5045–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jha AK, Tharp KM, Browne S, Ye J, Stahl A, Yeghiazarians Y, et al. Matrix metalloproteinase-13 mediated degradation of hyaluronic acid-based matrices orchestrates stem cell engraftment through vascular integration. Biomaterials. 2016;89:136–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung JT, Kim JF, Wang HH, di Nicolo E, Drioli E, Lee YM. Understanding the non-solvent induced phase separation (NIPS) effect during the fabrication of microporous PVDF membranes via thermally induced phase separation (TIPS). J Membr Sci. 2016;514:250–63.

    Article  CAS  Google Scholar 

  • Kaczmarek B, Sionkowska A, Osyczka AM. The application of chitosan/collagen/hyaluronic acid sponge cross-linked by dialdehyde starch addition as a matrix for calcium phosphate in situ precipitation. Int J Biol Macromol. 2018;107:470–7.

    Article  CAS  PubMed  Google Scholar 

  • Kalam MA. Development of chitosan nanoparticles coated with hyaluronic acid for topical ocular delivery of dexamethasone. Int J Biol Macromol. 2016;89:127–36.

    Article  PubMed  CAS  Google Scholar 

  • Kang L, Jia W, Li M, Wang Q, Wang C, Liu Y, et al. Hyaluronic acid oligosaccharide-modified collagen nanofibers as vascular tissue-engineered scaffold for promoting endothelial cell proliferation. Carbohydr Polym. 2019;223:115106.

    Article  CAS  PubMed  Google Scholar 

  • Kankala RK, Zhang YS, Wang SB, Lee CH, Chen AZ. Supercritical fluid technology: an emphasis on drug delivery and related biomedical applications. Adv Healthc Mater. 2017;6(16):1700433

    Google Scholar 

  • Kenar H, Ozdogan CY, Dumlu C, Doger E, Kose GT, Hasirci V. Microfibrous scaffolds from poly(l-lactide-co-epsilon-caprolactone) blended with xeno-free collagen/hyaluronic acid for improvement of vascularization in tissue engineering applications. Mater Sci Eng C Mater Biol Appl. 2019;97:31–44.

    Article  CAS  PubMed  Google Scholar 

  • Kendall FE, Heidelberger M, Dawson MH. A serologically inactive polysaccharide elaborated by mucoid strains of group a hemolytic streptococcus. J Biol Chem. 1937;118(1):61–9.

    Article  CAS  Google Scholar 

  • Kessler L, Gehrke S, Winnefeld M, Huber B, Hoch E, Walter T, et al. Methacrylated gelatin/hyaluronan-based hydrogels for soft tissue engineering. J Tissue Eng. 2017;8:2041731417744157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khaing ZZ, Milman BD, Vanscoy JE, Seidlits SK, Grill RJ, Schmidt CE. High molecular weight hyaluronic acid limits astrocyte activation and scar formation after spinal cord injury. J Neural Eng. 2011;8:046033.

    Article  PubMed  Google Scholar 

  • Khan R, Aroulmoji V. Hyaluronic acid – hydroxychloroquine conjugate proposed for treatment of COVID-19. Int J Adv Sci Eng. 2020;06:1469–71.

    Article  CAS  Google Scholar 

  • Kheirabadi M, Shi L, Bagheri R, Kabiri K, Hilborn J, Ossipov DA. In situ forming interpenetrating hydrogels of hyaluronic acid hybridized with iron oxide nanoparticles. Biomater Sci. 2015;3(11):1466–74.

    Article  CAS  PubMed  Google Scholar 

  • Kim JF, Kim JH, Lee YM, Drioli E. Thermally induced phase separation and electrospinning methods for emerging membrane applications: a review. AICHE J. 2016;62(2):461–90.

    Article  CAS  Google Scholar 

  • Kim DK, Lee JM, Jeong JY, Park HJ, Lee OJ, Chao J, et al. New fabrication method of silk fibroin plate and screw based on a centrifugal casting technique. J Tissue Eng Regen M. 2018;12(11):2221–9.

    Article  CAS  Google Scholar 

  • Kohi S, Sato N, Koga A, Hirata K, Harunari E, Igarashi Y. Hyaluromycin, a novel hyaluronidase inhibitor attenuates pancreatic cancer cell migration and proliferation. J Oncol. 2016;2016:9063087.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kota DJ, Wiggins LL, Yoon N, Lee RH. TSG-6 produced by hMSCs delays the onset of autoimmune diabetes by suppressing Th1 development and enhancing Tolerogenicity. Diabetes. 2013;62(6):2048–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koul V, Bhowmick S, Thanusha AV. Hydrogels for pharmaceutical applications. In: Handbook of polymers for pharmaceutical technologies, Vol 4: bioactive and compatible synthetic/hybrid polymers. Hoboken: Wiley; 2016. p. 125–44.

    Google Scholar 

  • Kuehl C, Zhang T, Kaminskas LM, Porter CJ, Davies NM, Forrest L, et al. Hyaluronic acid molecular weight determines lung clearance and biodistribution after instillation. Mol Pharm. 2016;13(6):1904–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai JY. Relationship between structure and cytocompatibility of divinyl sulfone cross-linked hyaluronic acid. Carbohydr Polym. 2014;101:203–12.

    Article  CAS  PubMed  Google Scholar 

  • Lai HJ, Kuan CH, Wu HC, Tsai JC, Chen TM, Hsieh DJ, et al. Tailored design of electrospun composite nanofibers with staged release of multiple angiogenic growth factors for chronic wound healing. Acta Biomater. 2014;10(10):4156–66.

    Article  CAS  PubMed  Google Scholar 

  • Larraneta E, Henry M, Irwin NJ, Trotter J, Perminova AA, Donnelly RF. Synthesis and characterization of hyaluronic acid hydrogels crosslinked using a solvent-free process for potential biomedical applications. Carbohydr Polym. 2018;181:1194–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurent TC, Laurent UB, Fraser JRE. The structure and function of hyaluronan: an overview. Immunol Cell Biol. 1996;74:A1–7.

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Park TG. Photo-crosslinkable, biomimetic, and thermo-sensitive pluronic grafted hyaluronic acid copolymers for injectable delivery of chondrocytes. J Biomed Mater Res A. 2009;88A(3):797–806.

    Article  CAS  Google Scholar 

  • Lee DW, Banquy X, Das S, Cadirov N, Jay G, Israelachvili J. Effects of molecular weight of grafted hyaluronic acid on wear initiation. Acta Biomater. 2014;10(5):1817–23.

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Sen A, Bae S, Lee JS, Webb K. Poly(ethylene glycol) diacrylate/hyaluronic acid semi-interpenetrating network compositions for 3-D cell spreading and migration. Acta Biomater. 2015;14:43–52.

    Article  CAS  PubMed  Google Scholar 

  • Lee MC, Kim DK, Lee OJ, Kim JH, Ju HW, Lee JM, et al. Fabrication of silk fibroin film using centrifugal casting technique for corneal tissue engineering. J Biomed Mater Res B. 2016;104(3):508–14.

    Article  CAS  Google Scholar 

  • Lee S, Chung M, Lee SR, Jeon NL. 3D brain angiogenesis model to reconstitute functional human blood-brain barrier in vitro. Biotechnol Bioeng. 2020;117(3):748–62.

    Article  CAS  PubMed  Google Scholar 

  • Lertkiatmongkol P, Liao D, Mei H, Hu Y, Newman PJ. Endothelial functions of platelet/endothelial cell adhesion molecule-1 (CD31). Curr Opin Hematol. 2016;23(3):253–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levene PA, López-Suárez J. Mucins and Mucoids. J Biol Chem. 1918;36(1):105–26.

    Article  CAS  Google Scholar 

  • Li JG, Zhang K, Yang P, Qin W, Li GC, Zhao AS, et al. Human vascular endothelial cell morphology and functional cytokine secretion influenced by different size of HA micro-pattern on titanium substrate. Colloid Surf B. 2013;110:199–207.

    Article  CAS  Google Scholar 

  • Lim HL, Hwang Y, Kar M, Varghese S. Smart hydrogels as functional biomimetic systems. Biomater Sci. 2014;2(5):603–18.

    Article  CAS  PubMed  Google Scholar 

  • Lim DK, Wylie RG, Langer R, Kohane DS. Selective binding of C-6 OH sulfated hyaluronic acid to the angiogenic isoform of VEGF(165). Biomaterials. 2016;77:130–8.

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Ye H, Satkunendrarajah K, Yao GS, Bayon Y, Fehlings MG (2013) A self-assembling peptide reduces glial scarring, attenuates post-traumatic inflammation and promotes neurological recovery following spinal cord injury. Acta Biomater. 9. England: Acta Materialia Inc. Published by Elsevier Ltd, pp 8075–88.

    Google Scholar 

  • Lu HD, Soranno DE, Rodell CB, Kim IL, Burdick JA. Secondary photocrosslinking of injectable shear-thinning dock-and-lock hydrogels. Adv Healthc Mater. 2013;2(7):1028–36.

    Article  CAS  PubMed  Google Scholar 

  • Lu BT, Lu F, Zou YN, Liu JW, Rong B, Li ZQ, et al. In situ reduction of silver nanoparticles by chitosan-L-glutamic acid/hyaluronic acid: enhancing antimicrobial and wound-healing activity. Carbohydr Polym. 2017;173:556–65.

    Article  CAS  PubMed  Google Scholar 

  • Lynch AS, Robertson GT. Bacterial and fungal biofilm infections. Annu Rev Med. 2008;59:415–28.

    Article  CAS  PubMed  Google Scholar 

  • Magnani A, Rappuoli R, Lamponi S, Barbucci R. Novel polysaccharide hydrogels: characterization and properties. Polym Adv Technol. 2000;11(8–12):488–95.

    Article  CAS  Google Scholar 

  • Mahmoodi NM, Mokhtari-Shourijeh Z. Preparation of aminated nanoporous nanofiber by solvent casting/porogen leaching technique and dye adsorption modeling. J Taiwan Inst Chem E. 2016;65:378–89.

    Article  CAS  Google Scholar 

  • Maleki A, Kjøniksen A-L, Nyström B. Characterization of the chemical degradation of hyaluronic acid during chemical gelation in the presence of different cross-linker agents. Carbohydr Res. 2007;342(18):2776–92.

    Article  CAS  PubMed  Google Scholar 

  • Manavitehrani I, Le TYL, Daly S, Wang YW, Maitz PK, Schindeler A, et al. Formation of porous biodegradable scaffolds based on poly(propylene carbonate) using gas foaming technology. Mat Sci Eng C-Mater. 2019;96:824–30.

    Article  CAS  Google Scholar 

  • Maniglio D, Bonani W, Migliaresi C, Motta A. Silk fibroin porous scaffolds by N2O foaming. J Biomat Sci-Polym E. 2018;29(5):491–506.

    Article  CAS  Google Scholar 

  • Markovitsi D, Gustavsson T, Banyasz A. Absorption of UV radiation by DNA: spatial and temporal features. Mutat Res Rev Mutat. 2010;704(1–3):21–8.

    Article  CAS  Google Scholar 

  • Martinez-Ramos C, Doblado LR, Mocholi EL, Alastrue-Agudo A, Petidier MS, Giraldo E, et al. Biohybrids for spinal cord injury repair. J Tissue Eng Regen Med. 2019;13(3):509–21.

    Article  CAS  PubMed  Google Scholar 

  • Maurin M, Raoult D. Use of aminoglycosides in treatment of infections due to intracellular bacteria. Antimicrob Agents Chemother. 2001;45(11):2977–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mealy JE, Rodell CB, Burdick JA. Sustained small molecule delivery from injectable hyaluronic acid hydrogels through host-guest mediated retention. J Mater Chem B Mater Biol Med. 2015;3(40):8010–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet. 2020;395(10229):1033–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meri S, Pangburn MK. Regulation of alternative pathway complement activation by glycosaminoglycans – specificity of the polyanion binding-site on factor-H. Biochem Biophys Res Commun. 1994;198(1):52–9.

    Article  CAS  PubMed  Google Scholar 

  • Meyer K, Palmer JW. The polysaccharide of the vitreous humor. J Biol Chem. 1934;107(3):629–34.

    Article  CAS  Google Scholar 

  • Miguel SP, Figueira DR, Simoes D, Ribeiro MP, Coutinho P, Ferreira P, et al. Electrospun polymeric nanofibres as wound dressings: a review. Colloid Surf B. 2018;169:60–71.

    Article  CAS  Google Scholar 

  • Mong MA, Awkal JA, Marik PE (2020) Accelerated hyaluronan concentration as the primary driver of morbidity and mortality in high-risk COVID-19 patients: with therapeutic introduction of an oral hyaluronan inhibitor in the prevention of “Induced Hyaluronan Storm” Syndrome. medRxiv. 2020.04.19.20071647

    Google Scholar 

  • Monteiro IP, Shukla A, Marques AP, Reis RL, Hammond PT. Spray-assisted layer-by-layer assembly on hyaluronic acid scaffolds for skin tissue engineering. J Biomed Mater Res A. 2015;103(1):330–40.

    Article  PubMed  CAS  Google Scholar 

  • Mothe AJ, Tator CH. Advances in stem cell therapy for spinal cord injury. J Clin Invest. 2012;122(11):3824–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mouser VHM, Levato R, Mensinga A, Dhert WJA, Gawlitta D, Malda J. Bio-ink development for three-dimensional bioprinting of hetero-cellular cartilage constructs. Connect Tissue Res. 2020;61(2):137–51.

    Article  CAS  PubMed  Google Scholar 

  • Movahedi M, Asefnejad A, Rafienia M, Khorasani MT. Potential of novel electrospun core-shell structured polyurethane/starch (hyaluronic acid) nanofibers for skin tissue engineering: in vitro and in vivo evaluation. Int J Biol Macromol. 2020;146:627–37.

    Article  CAS  PubMed  Google Scholar 

  • Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773–85.

    Article  CAS  PubMed  Google Scholar 

  • Nagy N, Kuipers HF, Frymoyer AR, Ishak HD, Bollyky JB, Wight TN, et al. 4-methylumbelliferone treatment and hyaluronan inhibition as a therapeutic strategy in inflammation, autoimmunity, and cancer. Front Immunol. 2015;6:123.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakajima N, Ikada Y. Mechanism of amide formation by carbodiimide for bioconjugation in aqueous media. Bioconjug Chem. 1995;6(1):123–30.

    Article  CAS  PubMed  Google Scholar 

  • Nasreen N, Mohammed KA, Hardwick J, Van Horn RD, Sanders K, Kathuria H, et al. Low molecular weight hyaluronan induces malignant mesothelioma cell (MMC) proliferation and haptotaxis: role of CD44 receptor in MMC proliferation and haptotaxis. Oncol Res. 2002;13(2):71–8.

    CAS  PubMed  Google Scholar 

  • Natividad-Diaz SL, Browne S, Jha AK, Ma Z, Hossainy S, Kurokawa YK, et al. A combined hiPSC-derived endothelial cell and in vitro microfluidic platform for assessing biomaterial-based angiogenesis. Biomaterials. 2019;194:73–83.

    Article  CAS  PubMed  Google Scholar 

  • Ni YL, Tang ZR, Cao WX, Lin H, Fan YJ, Guo LK, et al. Tough and elastic hydrogel of hyaluronic acid and chondroitin sulfate as potential cell scaffold materials. Int J Biol Macromol. 2015;74:367–75.

    Article  CAS  PubMed  Google Scholar 

  • Noh I, Kim N, Tran HN, Lee J, Lee C. 3D printable hyaluronic acid-based hydrogel for its potential application as a bioink in tissue engineering. Biomater Res. 2019;23(1):3.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’brien FJ. Biomaterials & scaffolds for tissue engineering. Mater Today. 2011;14(3):88–95.

    Article  CAS  Google Scholar 

  • Oh EJ, Park K, Kim KS, Kim J, Yang J-A, Kong J-H, et al. Target specific and long-acting delivery of protein, peptide, and nucleotide therapeutics using hyaluronic acid derivatives. J Control Release. 2010;141(1):2–12.

    Article  CAS  PubMed  Google Scholar 

  • Ozgenel GY. Effects of hyaluronic acid on peripheral nerve scarring and regeneration in rats. Microsurgery. 2003;23(6):575–81.

    Article  PubMed  Google Scholar 

  • Palumbo FS, Di Stefano M, Piccionello AP, Fiorica C, Pitarresi G, Pibiri I, et al. Perfluorocarbon functionalized hyaluronic acid derivatives as oxygenating systems for cell culture. RSC Adv. 2014;4(44):22894–901.

    Article  CAS  Google Scholar 

  • Pandey MS, Weigel PH. Hyaluronic acid receptor for endocytosis (HARE)-mediated endocytosis of hyaluronan, heparin, dermatan sulfate, and acetylated low density lipoprotein (AcLDL), but not chondroitin sulfate types A, C, D, or E, activates NF-kappaB-regulated gene expression. J Biol Chem. 2014;289(3):1756–67.

    Article  CAS  PubMed  Google Scholar 

  • Papakonstantinou E, Roth M, Karakiulakis G. Hyaluronic acid: a key molecule in skin aging. Dermato-endocrinol. 2012;4(3):253–8.

    Article  CAS  Google Scholar 

  • Pardue EL, Ibrahim S, Ramamurthi A. Role of hyaluronan in angiogenesis and its utility to angiogenic tissue engineering. Organogenesis. 2008;4(4):203–14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Park KM, Yang JA, Jung H, Yeom J, Park JS, Park KH, et al. In situ supramolecular assembly and modular modification of hyaluronic acid hydrogels for 3D cellular engineering. ACS Nano. 2012a;6(4):2960–8.

    Article  CAS  PubMed  Google Scholar 

  • Park D, Kim Y, Kim H, Kim K, Lee YS, Choe J, et al. Hyaluronic acid promotes angiogenesis by inducing RHAMM-TGFbeta receptor interaction via CD44-PKCdelta. Mol Cell. 2012b;33(6):563–74.

    Article  CAS  Google Scholar 

  • Park JH, Park EJ, Yi HS. Wound healing and anti-inflammatory effects of topical hyaluronic acid injection in surgical-site infection caused by Staphylococcus aureus. Int J Low Extrem Wounds. 2017;16(3):202–7.

    Article  CAS  PubMed  Google Scholar 

  • Pati F, Jang J, Ha DH, Kim SW, Rhie JW, Shim JH, et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun. 2014;5:3935.

    Article  CAS  PubMed  Google Scholar 

  • Patterson RL, Peterson DA, Deinhardt F, Howard F. Rubella and rheumatoid arthritis: hyaluronic acid and susceptibility of cultured rheumatoid synovial cells to viruses. Proc Soc Exp Biol Med. 1975;149(3):594–8.

    Article  CAS  PubMed  Google Scholar 

  • Pereira PAT, Bitencourt CS, Reis MB, Frantz FG, Sorgi CA, Souza COS, et al. Immunomodulatory activity of hyaluronidase is associated with metabolic adaptations during acute inflammation. Inflamm Res. 2020;69(1):105–13.

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Álvarez L, Ruiz-Rubio L, Azua I, Benito V, Bilbao A, Vilas-Vilela JL. Development of multiactive antibacterial multilayers of hyaluronic acid and chitosan onto poly(ethylene terephthalate). Eur Polym J. 2019;112:31–7.

    Article  CAS  Google Scholar 

  • Perng CK, Wang YJ, Tsi CH, Ma H. In vivo angiogenesis effect of porous collagen scaffold with hyaluronic acid oligosaccharides. J Surg Res. 2011;168(1):9–15.

    Article  CAS  PubMed  Google Scholar 

  • Peroglio M, Grad S, Mortisen D, Sprecher CM, Illien-Junger S, Alini M, et al. Injectable thermoreversible hyaluronan-based hydrogels for nucleus pulposus cell encapsulation. Eur Spine J. 2012;21(Suppl 6):S839–49.

    Article  PubMed  Google Scholar 

  • Pescosolido L, Schuurman W, Malda J, Matricardi P, Alhaique F, Coviello T, et al. Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting. Biomacromolecules. 2011;12(5):1831–8.

    Article  CAS  PubMed  Google Scholar 

  • Piperno A, Zagami R, Cordaro A, Pennisi R, Musarra-Pizzo M, Scala A, et al. Exploring the entrapment of antiviral agents in hyaluronic acid-cyclodextrin conjugates. J Incl Phenom Macrocycl Chem. 2019;93(1):33–40.

    Article  CAS  Google Scholar 

  • Pirnazar P, Wolinsky L, Nachnani S, Haake S, Pilloni A, Bernard GW. Bacteriostatic effects of hyaluronic acid. J Periodontol. 1999;70(4):370–4.

    Article  CAS  PubMed  Google Scholar 

  • Poldervaart MT, Goversen B, de Ruijter M, Abbadessa A, Melchels FPW, Oner FC, et al. 3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity. PLoS One. 2017;12(6):e0177628.

    Google Scholar 

  • Porras AM, Sjögren F, Shi L, Ossipov DA, Tenje M (eds) (2016) Photopatterning of hyaluronic acid hydrogels for cell culture scaffolds. 27th micromechanics and microsystems Europe WORKSHOP (MME 2016), Cork, Ireland, August 28–30 2016

    Google Scholar 

  • Portalska KJ, Teixeira LM, Leijten JC, Jin R, van Blitterswijk C, de Boer J, et al. Boosting angiogenesis and functional vascularization in injectable dextran-hyaluronic acid hydrogels by endothelial-like mesenchymal stromal cells. Tissue Eng Part A. 2014;20(3–4):819–29.

    CAS  PubMed  Google Scholar 

  • Poursamar SA, Lehner AN, Azami M, Ebrahimi-Barough S, Samadikuchaksaraei A, Antunes APM. The effects of crosslinkers on physical, mechanical, and cytotoxic properties of gelatin sponge prepared via in-situ gas foaming method as a tissue engineering scaffold. Mat Sci Eng C-Mater. 2016;63:1–9.

    Article  CAS  Google Scholar 

  • Prata JE, Barth TA, Bencherif SA, Washburn NR. Complex fluids based on methacrylated hyaluronic acid. Biomacromolecules. 2010;11(3):769–75.

    Article  CAS  PubMed  Google Scholar 

  • Pravata L, Braud C, Boustta M, El Ghzaoui A, Tømmeraas K, Guillaumie F, et al. New amphiphilic lactic acid oligomer− hyaluronan conjugates: synthesis and physicochemical characterization. Biomacromolecules. 2008;9(1):340–8.

    Article  CAS  PubMed  Google Scholar 

  • Prestwich GD, Marecak DM, Marecek JF, Vercruysse KP, Ziebell MR. Controlled chemical modification of hyaluronic acid: synthesis, applications, and biodegradation of hydrazide derivatives. J Control Release. 1998;53(1–3):93–103.

    Article  CAS  PubMed  Google Scholar 

  • Qiu Y, Hou Y, Sun F, Chen P, Wang D, Mu H, et al. Hyaluronic acid conjugation facilitates clearance of intracellular bacterial infections by streptomycin with neglectable nephrotoxicity. Glycobiology. 2017;27(9):861–7.

    Article  CAS  PubMed  Google Scholar 

  • Ramamurthi A, Vesely I. Smooth muscle cell adhesion on crosslinked hyaluronan gels. J Biomed Mater Res. 2002;60(1):195–205.

    Article  PubMed  CAS  Google Scholar 

  • Ramanan V, Scull MA, Sheahan TP, Rice CM, Bhatia SN. New methods in tissue engineering: improved models for viral infection. Annu Rev Virol. 2014;1:475–99.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramos CM, Bargues MJM, Roca FG, Doblado LR, Sanchez TG, Mir L, et al (2018) Electrical stimulation increases schwann cells proliferation inside hyaluronic acid conduits. 2018 Emf-Med 1st World conference on biomedical applications of electromagnetic fields (Emf-Med 2018)

    Google Scholar 

  • Rao F, Yuan ZP, Li M, Yu F, Fang XX, Jiang BG, et al. Expanded 3D nanofibre sponge scaffolds by gas-foaming technique enhance peripheral nerve regeneration. Artif Cell Nanomed B. 2019;47(1):491–500.

    Article  CAS  Google Scholar 

  • Rey DFV, St-Pierre J-P. Fabrication techniques of tissue engineering scaffolds. In: Handbook of tissue engineering scaffolds, vol. One. San Diego: Elsevier; 2019. p. 109–25.

    Google Scholar 

  • Rodell CB, Kaminski AL, Burdick JA. Rational design of network properties in guest-host assembled and shear-thinning hyaluronic acid hydrogels. Biomacromolecules. 2013;14(11):4125–34.

    Article  CAS  PubMed  Google Scholar 

  • Rodell CB, MacArthur JW, Dorsey SM, Wade RJ, Wang LL, Woo YJ, et al. Shear-thinning supramolecular hydrogels with secondary autonomous covalent crosslinking to modulate viscoelastic properties in vivo. Adv Funct Mater. 2015a;25(4):636–44.

    Article  CAS  PubMed  Google Scholar 

  • Rodell CB, Wade RJ, Purcell BP, Dusaj NN, Burdick JA. Selective proteolytic degradation of guest-host assembled, injectable hyaluronic acid hydrogels. ACS Biomater Sci Eng. 2015b;1(4):277–86.

    Article  CAS  PubMed  Google Scholar 

  • Rodell CB, Highley CB, Chen MH, Dusaj NN, Wang C, Han L, et al. Evolution of hierarchical porous structures in supramolecular guest-host hydrogels. Soft Matter. 2016;12(37):7839–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Perez E, Compan AL, Pradas MM, Martinez-Ramos C. Scaffolds of hyaluronic acid-poly(ethyl acrylate) interpenetrating networks: characterization and in vitro studies. Macromol Biosci. 2016;16(8):1147–57.

    Article  CAS  PubMed  Google Scholar 

  • Rohr RV, Trepp C (1996) High pressure chemical engineering: proceedings of the 3rd International Symposium on High Pressure Chemical Engineering, Zürich, Switzerland, October 7–9, 1996. Elsevier, Amsterdam, New York, xvii, 710 p

    Google Scholar 

  • Romanò CL, De Vecchi E, Bortolin M, Morelli I, Drago L. Hyaluronic acid and its composites as a local antimicrobial/antiadhesive barrier. J Bone Jt Infect. 2017;2(1):63–72.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosales AM, Vega SL, DelRio FW, Burdick JA, Anseth KS. Hydrogels with reversible mechanics to probe dynamic cell microenvironments. Angew Chem Int Ed Eng. 2017;56(40):12132–6.

    Article  CAS  Google Scholar 

  • Rosales AM, Rodell CB, Chen MH, Morrow MG, Anseth KS, Burdick JA. Reversible control of network properties in azobenzene-containing hyaluronic acid-based hydrogels. Bioconjug Chem. 2018;29:905–13.

    Article  CAS  PubMed  Google Scholar 

  • 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):186–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahiner N, Sagbas S, Sahiner M, Ayyala RS. Polyethyleneimine modified poly(hyaluronic acid) particles with controllable antimicrobial and anticancer effects. Carbohydr Polym. 2017;159:29–38.

    Article  CAS  PubMed  Google Scholar 

  • Sakai S, Ohi H, Hotta T, Kamei H, Taya M. Differentiation potential of human adipose stem cells bioprinted with hyaluronic acid/gelatin-based bioink through microextrusion and visible light-initiated crosslinking. Biopolymers. 2018;109(2):e23080.

    Article  CAS  Google Scholar 

  • Schanté CE, Zuber G, Herlin C, Vandamme TF. Chemical modifications of hyaluronic acid for the synthesis of derivatives for a broad range of biomedical applications. Carbohydr Polym. 2011;85(3):469–89.

    Article  CAS  Google Scholar 

  • Schante CE, Zuber G, Herlin C, Vandamme TF. Chemical modifications of hyaluronic acid for the synthesis of derivatives for a broad range of biomedical applications. Carbohydr Polym. 2011;85(3):469–89.

    Article  CAS  Google Scholar 

  • Seidlits SK, Khaing ZZ, Petersen RR, Nickels JD, Vanscoy JE, Shear JB, et al. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials. 2010;31(14):3930–40.

    Article  CAS  PubMed  Google Scholar 

  • Seidlits SK, Liang J, Bierman RD, Sohrabi A, Karam J, Holley SM, et al. Peptide-modified, hyaluronic acid-based hydrogels as a 3D culture platform for neural stem/progenitor cell engineering. J Biomed Mater Res A. 2019;107(4):704–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seon-Lutz M, Couffin AC, Vignoud S, Schlatter G, Hebraud A. Electrospinning in water and in situ crosslinking of hyaluronic acid/cyclodextrin nanofibers: towards wound dressing with controlled drug release. Carbohydr Polym. 2019;207:276–87.

    Article  CAS  PubMed  Google Scholar 

  • Shendi D, Albrecht DR, Jain A. Anti-Fas conjugated hyaluronic acid microsphere gels for neural stem cell delivery. J Biomed Mater Res A. 2017;105(2):608–18.

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Wang Y, Shao C, Huang J, Gan J, Huang X, et al. COVID-19 infection: the perspectives on immune responses. Cell Death Differ. 2020;27(5):1451–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimojo AA, Pires AM, Lichy R, Rodrigues AA, Santana MH. The crosslinking degree controls the mechanical, rheological, and swelling properties of hyaluronic acid microparticles. J Biomed Mater Res A. 2015;103(2):730–7.

    Article  PubMed  CAS  Google Scholar 

  • Silva LP, Pirraco RP, Santos TC, Novoa-Carballal R, Cerqueira MT, Reis RL, et al. Neovascularization induced by the hyaluronic acid-based spongy-like hydrogels degradation products. ACS Appl Mater Interfaces. 2016;8(49):33464–74.

    Article  CAS  PubMed  Google Scholar 

  • Singh I, Lacko CS, Zhao ZY, Schmidt CE, Rinaldi C. Preparation and evaluation of microfluidic magnetic alginate microparticles for magnetically templated hydrogels. J Colloid Interface Sci. 2020;561:647–58.

    Article  CAS  PubMed  Google Scholar 

  • Sloane JA, Batt C, Ma Y, Harris ZM, Trapp B, Vartanian T. Hyaluronan blocks oligodendrocyte progenitor maturation and remyelination through TLR2. Proc Natl Acad Sci U S A. 2010;107(25):11555–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smeds KA, Grinstaff MW. Photocrosslinkable polysaccharides for in situ hydrogel formation. J Biomed Mater Res. 2001;54(1):115–21.

    Article  CAS  PubMed  Google Scholar 

  • Song JE, Kim MJ, Yoon H, Yoo H, Lee YJ, Kim HN, et al. Effect of hyaluronic acid (HA) in a HA/PLGA scaffold on annulus fibrosus regeneration: in vivo tests. Macromol Res. 2013;21(10):1075–82.

    Article  CAS  Google Scholar 

  • Sorokin L. The impact of the extracellular matrix on inflammation. Nat Rev Immunol. 2010;10(10):712–23.

    Article  CAS  PubMed  Google Scholar 

  • Souness A, Zamboni F, Walker GM, Collins MN. Influence of scaffold design on 3D printed cell constructs. J Biomed Mater Res B Appl Biomater. 2018;106(2):533–45.

    Article  CAS  PubMed  Google Scholar 

  • Stern R. Hyaluronan catabolism: a new metabolic pathway. Eur J Cell Biol. 2004;83(7):317–25.

    Article  CAS  PubMed  Google Scholar 

  • Struve J, Maher PC, Li YQ, Kinney S, Fehlings MG, Kuntz C, et al. Disruption of the hyaluronan-based extracellular matrix in spinal cord promotes astrocyte proliferation. Glia. 2005;52(1):16–24.

    Article  PubMed  Google Scholar 

  • Sukowati CHC, Anfuso B, Fiore E, Ie SI, Raseni A, Vascotto F, et al. Hyaluronic acid inhibition by 4-methylumbelliferone reduces the expression of cancer stem cells markers during hepatocarcinogenesis. Sci Rep. 2019;9(1):4026.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun JF, Perry SL, Schiffman JD. Electrospinning nanofibers from chitosan/hyaluronic acid complex coacervates. Biomacromolecules. 2019;20(11):4191–8.

    Article  CAS  PubMed  Google Scholar 

  • Sundaramurthi D, Rauf S, Hauser CAE. 3D bioprinting technology for regenerative medicine applications. Int J Bioprint. 2016;2(2):9–26.

    Article  CAS  Google Scholar 

  • Takahashi A, Suzuki Y, Suhara T, Omichi K, Shimizu A, Hasegawa K, et al. In situ cross-linkable hydrogel of hyaluronan produced via copper-free click chemistry. Biomacromolecules. 2013;14(10):3581–8.

    Article  CAS  PubMed  Google Scholar 

  • Tatara AM. Role of tissue engineering in COVID-19 and future viral outbreaks. Tissue Eng Part A. 2020;26(9–10):468–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thanusha AV, Dinda AK, Koul V. Evaluation of nano hydrogel composite based on gelatin/HA/CS suffused with Asiatic acid/ZnO and CuO nanoparticles for second degree burns. Mat Sci Eng C-Mater. 2018;89:378–86.

    Article  CAS  Google Scholar 

  • Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev. 2016;97:4–27.

    Article  CAS  PubMed  Google Scholar 

  • Thomas RC, Vu P, Modi SP, Chung PE, Landis RC, Khaing ZZ, et al. Sacrificial crystal templated hyaluronic acid hydrogels as biomimetic 3D tissue scaffolds for nerve tissue regeneration. ACS Biomater Sci Eng. 2017;3(7):1451–9.

    Article  CAS  PubMed  Google Scholar 

  • Tiunnikov G, Kostina G, Radaeva I, Bakulina L. Effects of hyaluronic acid preparation on the development of herpetic infection in cell culture. Vopr Virusol. 2002;47:37–9.

    CAS  PubMed  Google Scholar 

  • Tomihata K, Ikada Y. Crosslinking of hyaluronic acid with glutaraldehyde. J Polym Sci A Polym Chem. 1997;35(16):3553–9.

    Article  CAS  Google Scholar 

  • Tommeraas K, Eenschooten C. Aryl/alkyl succinic anhydride-hyaluronan derivatives. Google Patents. 2009.

    Google Scholar 

  • Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4(7):528–39.

    Article  CAS  PubMed  Google Scholar 

  • Uchida K, Otake K, Inoue M, Koike Y, Matsushita K, Tanaka K, et al. Bacteriostatic effects of hyaluronan-based bioresorsable membrane. Surg Sci. 2011;2:6.

    Article  Google Scholar 

  • Valachova K, Banasova M, Topol’ska D, Sasinkova V, Juranek I, Collins MN, et al. Influence of tiopronin, captopril and levamisole therapeutics on the oxidative degradation of hyaluronan. Carbohydr Polym. 2015;134:516–23.

    Article  CAS  PubMed  Google Scholar 

  • Valachova K, Topol’ska D, Mendichi R, Collins MN, Sasinkova V, Soltes L. Hydrogen peroxide generation by the Weissberger biogenic oxidative system during hyaluronan degradation. Carbohydr Polym. 2016;148:189–93.

    Article  CAS  PubMed  Google Scholar 

  • VanEpps JS, Younger JG. Implantable device-related infection. Shock. 2016;46(6):597–608.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vegas AJ, Veiseh O, Doloff JC, Ma M, Tam HH, Bratlie K, et al. Combinatorial hydrogel library enables identification of materials that mitigate the foreign body response in primates. Nat Biotechnol. 2016;34(3):345–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vercruysse KP, Prestwich GD. Hyaluronate derivatives in drug delivery. Crit Rev Ther Drug Carrier Syst. 1998;15(5):43.

    Article  Google Scholar 

  • Wang Y, Han G, Guo B, Huang J. Hyaluronan oligosaccharides promote diabetic wound healing by increasing angiogenesis. Pharmacol Rep. 2016;68(6):1126–32.

    Article  CAS  PubMed  Google Scholar 

  • Wang HH, Jung JT, Kim JF, Kim S, Drioli E, Lee YM. A novel green solvent alternative for polymeric membrane preparation via nonsolvent-induced phase separation (NIPS). J Membr Sci. 2019a;574:44–54.

    Article  CAS  Google Scholar 

  • Wang N, Liu C, Wang X, He T, Li L, Liang X, et al. Hyaluronic acid oligosaccharides improve myocardial function reconstruction and angiogenesis against myocardial infarction by regulation of macrophages. Theranostics. 2019b;9(7):1980–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver JD, Stabler CL. Antioxidant cerium oxide nanoparticle hydrogels for cellular encapsulation. Acta Biomater. 2015;16:136–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber LM, Lopez CG, Anseth KS. The effects of PEG hydrogel crosslinking density on protein diffusion and encapsulated islet survival and function. J Biomed Mater Res A. 2009;90(3):720–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weng L, Gouldstone A, Wu Y, Chen W. Mechanically strong double network photocrosslinked hydrogels from N, N-dimethylacrylamide and glycidyl methacrylated hyaluronan. Biomaterials. 2008;29(14):2153–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West DC, Hampson IN, Arnold F, Kumar S. Angiogenesis induced by degradation products of hyaluronic acid. Science. 1985;228(4705):1324–6.

    Article  CAS  PubMed  Google Scholar 

  • Williams CG, Malik AN, Kim TK, Manson PN, Elisseeff JH. Variable cytocompatibility of six cell lines with photoinitiators used for polymerizing hydrogels and cell encapsulation. Biomaterials. 2005;26(11):1211–8.

    Article  CAS  PubMed  Google Scholar 

  • Wu ZL, Gong JP. Hydrogels with self-assembling ordered structures and their functions. Npg Asia Mater. 2011;3:57–64.

    Article  Google Scholar 

  • Xie Y, Song W, Zhao W, Gao Y, Shang J, Hao P, et al. Application of the sodium hyaluronate-CNTF scaffolds in repairing adult rat spinal cord injury and facilitating neural network formation. Sci China Life Sci. 2018;61(5):559–68.

    Article  CAS  PubMed  Google Scholar 

  • Xu LY, Sheybani N, Yeudall WA, Yang H. The effect of photoinitiators on intracellular AKT signaling pathway in tissue engineering application. Biomater Sci. 2015a;3(2):250–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu KM, Narayanan K, Lee F, Bae KH, Gao SJ, Kurisawa M. Enzyme-mediated hyaluronic acid-tyramine hydrogels for the propagation of human embryonic stem cells in 3D. Acta Biomater. 2015b;24:159–71.

    Article  PubMed  CAS  Google Scholar 

  • Yildirim S, Demirtas TT, Dincer CA, Yildiz N, Karakecili A. Preparation of polycaprolactone/graphene oxide scaffolds: a green route combining supercritial CO2 technology and porogen leaching. J Supercrit Fluids. 2018;133:156–62.

    Article  CAS  Google Scholar 

  • Yin W, Qi X, Zhang Y et al. Advantages of pure platelet-rich plasma compared with leukocyte- and platelet-rich plasma in promoting repair of bone defects. J Transl Med. 2016;14:73. https://doi.org/10.1186/s12967-016-0825-9

  • Yin FQ, Lin LF, Zhan SJ. Preparation and properties of cellulose nanocrystals, gelatin, hyaluronic acid composite hydrogel as wound dressing. J Biomat Sci Polym E. 2019;30(3):190–201.

    Article  CAS  Google Scholar 

  • Zamboni F, Collins MN. Cell based therapeutics in type 1 diabetes mellitus. Int J Pharm. 2017;521(1–2):346–56.

    Article  CAS  PubMed  Google Scholar 

  • Zamboni F, Keays M, Hayes S, Albadarin AB, Walker GM, Kiely PA, et al. Enhanced cell viability in hyaluronic acid coated poly(lactic-co-glycolic acid) porous scaffolds within microfluidic channels. Int J Pharm. 2017;532(1):595–602.

    Article  CAS  PubMed  Google Scholar 

  • Zamboni F, Vieira S, Reis RL, Miguel Oliveira J, Collins MN. The potential of hyaluronic acid in immunoprotection and immunomodulation: chemistry, processing and function. Prog Mater Sci. 2018;97:97–122.

    Article  CAS  Google Scholar 

  • Zamboni F, Ryan E, Culebras M, Collins MN. Labile crosslinked hyaluronic acid via urethane formation using bis(β-isocyanatoethyl) disulphide with tuneable physicochemical and immunomodulatory properties. Carbohydr Polym. 2020;245:116501.

    Article  CAS  PubMed  Google Scholar 

  • Zapotocky V, Pospisilova M, Janouchova K, Svadlak D, Batova J, Sogorkova J, et al. Fabrication of biodegradable textile scaffold based on hydrophobized hyaluronic acid. Int J Biol Macromol. 2017;95:903–9.

    Article  CAS  PubMed  Google Scholar 

  • Zarei-Kheirabadi M, Sadrosadat H, Mohammadshirazi A, Jaberi R, Sorouri F, Khayyatan F, et al. Human embryonic stem cell-derived neural stem cells encapsulated in hyaluronic acid promotes regeneration in a contusion spinal cord injured rat. Int J Biol Macromol. 2020;148:1118–29.

    Article  CAS  PubMed  Google Scholar 

  • Zaviskova K, Tukmachev D, Dubisova J, Vackova I, Hejcl A, Bystronova J, et al. Injectable hydroxyphenyl derivative of hyaluronic acid hydrogel modified with RGD as scaffold for spinal cord injury repair. J Biomed Mater Res A. 2018;106(4):1129–40.

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Wei YT, Tsang KS, Sun CR, Li J, Huang H, et al. Implantation of neural stem cells embedded in hyaluronic acid and collagen composite conduit promotes regeneration in a rabbit facial nerve injury model. J Transl Med. 2008;6

    Google Scholar 

  • Zhang Y, Heher P, Hilborn J, Redl H, Ossipov DA. Hyaluronic acid-fibrin interpenetrating double network hydrogel prepared in situ by orthogonal disulfide cross-linking reaction for biomedical applications. Acta Biomater. 2016;38:23–32.

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Chen S, You RC, Tariq Z, Huang JJ, Li MZ, et al. Silk fibroin/hyaluronic acid porous scaffold for dermal wound healing. Fiber Polym. 2017;18(6):1056–63.

    Article  CAS  Google Scholar 

  • Zhang S, Vijayavenkataraman S, Lu WF, Fuh JYH. A review on the use of computational methods to characterize, design, and optimize tissue engineering scaffolds, with a potential in 3D printing fabrication. J Biomed Mater Res B. 2019;107(5):1329–51.

    Article  CAS  Google Scholar 

  • Zhang Y, Li L, Mu J, Chen J, Feng S, Gao J. Implantation of a functional TEMPO-hydrogel induces recovery from rat spinal cord transection through promoting nerve regeneration and protecting bladder tissue. Biomater Sci. 2020;8(6):1695–701.

    Article  PubMed  Google Scholar 

  • Zoratto N, Matricardi P. Semi-IPNs and IPN-based hydrogels. In: Polymeric gels. San Diego: Elsevier; 2018. p. 91–124.

    Chapter  Google Scholar 

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Acknowledgments

The authors would like to thank the financial support provided by following funding bodies:

Irish Research Council (GOIPG/2015/3577); European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No. 801165, with cofunding through SSPC by its funding body, Science Foundation Ireland, grant no. 112/RC/2275_P2.

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Collins, M.N., Zamboni, F., Serafin, A., Ren, G., Thanusha, A.V., Culebras, M. (2021). The Role of Hyaluronic Acid in Tissue Engineering. In: Oliveira, J., Radhouani, H., Reis, R.L. (eds) Polysaccharides of Microbial Origin. Springer, Cham. https://doi.org/10.1007/978-3-030-35734-4_56-1

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