Microorganism-derived biological macromolecules for tissue engineering
Naser Amini, Peiman Brouki Milan, Vahid Hosseinpour Sarmadi, Bahareh Derakhshanmehr, Ahmad Hivechi, Fateme Khodaei, Masoud Hamidi, Sara Ashraf, Ghazaleh Larijani, Alireza Rezapour
Microorganism-derived biological macromolecules for tissue engineering
According to literature, certain microorganism productions mediate biological effects. However, their beneficial characteristics remain unclear. Nowadays, scientists concentrate on obtaining natural materials from live creatures as new sources to produce innovative smart biomaterials for increasing tissue reconstruction in tissue engineering and regenerative medicine. The present review aims to introduce microorganism-derived biological macromolecules, such as pullulan, alginate, dextran, curdlan, and hyaluronic acid, and their available sources for tissue engineering. Growing evidence indicates that these materials can be used as biological material in scaffolds to enhance regeneration in damaged tissues and contribute to cosmetic and dermatological applications. These natural-based materials are attractive in pharmaceutical, regenerative medicine, and biomedical applications. This study provides a detailed overview of natural-based biomaterials, their chemical and physical properties, and new directions for future research and therapeutic applications.
biological macromolecules / regenerative medicine / tissue engineering / exopolysaccharide / carbohydrate
[1] |
StaudtC, HornH, HempelDC, NeuTR. Volumetric measurements of bacterial cells and extracellular polymeric substance glycoconjugates in biofilms. Biotechnol Bioeng 2004; 88( 5): 585– 592
CrossRef
Google scholar
|
[2] |
NwodoUU, GreenE, OkohAI. Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci 2012; 13( 11): 14002– 14015
CrossRef
Google scholar
|
[3] |
SchmidJ, SieberV, RehmB. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 2015; 6 : 496
CrossRef
Google scholar
|
[4] |
GeeseyG. Microbial exopolymers: ecological and economic considerations. Am Soc Microbiol News 1982; 48 : 9– 14
|
[5] |
PalA, PaulAK. Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J Microbiol 2008; 48( 1): 49– 64
CrossRef
Google scholar
|
[6] |
SutherlandIW. Biotechnology of Microbial Exopolysaccharides. Cambridge, UK: Cambridge University Press, 1990
|
[7] |
RoperMC, GreveLC, LabavitchJM, KirkpatrickBC. Detection and visualization of an exopolysaccharide produced by Xylella fastidiosa in vitro and in planta. Appl Environ Microbiol 2007; 73( 22): 7252– 7258
CrossRef
Google scholar
|
[8] |
AbsalonC, Van DellenK, WatnickPI. A communal bacterial adhesin anchors biofilm and bystander cells to surfaces. PLoS Pathog 2011; 7( 8): e1002210
CrossRef
Google scholar
|
[9] |
NadellCD, BasslerBL. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci USA 2011; 108( 34): 14181– 14185
CrossRef
Google scholar
|
[10] |
MandalAK, SenIK, MaityP, ChattopadhyayS, ChakrabortyR, RoyS, IslamSS. Structural elucidation and biological studies of a novel exopolysaccaride from Klebsiella pneumoniae PB12. Int J Biol Macromol 2015; 79 : 413– 422
CrossRef
Google scholar
|
[11] |
FreitasF, AlvesVD, ReisMA. Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 2011; 29( 8): 388– 398
CrossRef
Google scholar
|
[12] |
OteroA, VincenziniM. Extracellular polysaccharide synthesis by Nostoc strains as affected by N source and light intensity. J Biotechnol 2003; 102( 2): 143– 152
CrossRef
Google scholar
|
[13] |
SutherlandIW. Novel and established applications of microbial polysaccharides. Trends Biotechnol 1998; 16( 1): 41– 46
CrossRef
Google scholar
|
[14] |
RehmBH. Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 2010; 8( 8): 578– 592
CrossRef
Google scholar
|
[15] |
IslamST, LamJS. Synthesis of bacterial polysaccharides via the Wzx/Wzy-dependent pathway. Can J Microbiol 2014; 60( 11): 697– 716
CrossRef
Google scholar
|
[16] |
MoronaR, PurinsL, TociljA, MatteA, CyglerM. Sequence-structure relationships in polysaccharide co-polymerase (PCP) proteins. Trends Biochem Sci 2009; 34( 2): 78– 84
CrossRef
Google scholar
|
[17] |
CuthbertsonL, MainprizeIL, NaismithJH, WhitfieldC. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in gram-negative bacteria. Microbiol Mol Biol Rev 2009; 73( 1): 155– 177
CrossRef
Google scholar
|
[18] |
BakerP, WhitfieldGB, HillPJ, LittleDJ, PestrakMJ, RobinsonH, WozniakDJ, HowellPL. Characterization of the Pseudomonas aeruginosa glycoside hydrolase PslG reveals that its levels are critical for Psl polysaccharide biosynthesis and biofilm formation. J Biol Chem 2015; 290( 47): 28374– 28387
CrossRef
Google scholar
|
[19] |
SchmidJ, SieberV. Enzymatic transformations involved in the biosynthesis of microbial exo-polysaccharides based on the assembly of repeat units. ChemBioChem 2015; 16( 8): 1141– 1147
CrossRef
Google scholar
|
[20] |
WhitneyJC, HowellPL. Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol 2013; 21( 2): 63– 72
CrossRef
Google scholar
|
[21] |
WillisLM, WhitfieldC. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr Res 2013; 378 : 35– 44
CrossRef
Google scholar
|
[22] |
WillisLM, StupakJ, RichardsMR, LowaryTL, LiJ, WhitfieldC. Conserved glycolipid termini in capsular polysaccharides synthesized by ATP-binding cassette transporter-dependent pathways in Gram-negative pathogens. Proc Natl Acad Sci U S A 2013; 110( 19): 7868– 7873
CrossRef
Google scholar
|
[23] |
SchmidJ. Recent insights in microbial exopolysaccharide biosynthesis and engineering strategies. Curr Opin Biotechnol 2018; 53 : 130– 136
CrossRef
Google scholar
|
[24] |
ComteS, GuibaudG, BauduM. Relations between extraction protocols for activated sludge extracellular polymeric substances (EPS) and EPS complexation properties: Part I. Comparison of the efficiency of eight EPS extraction methods. Enzyme Microb Technol 2006; 38( 1-2): 237– 245
CrossRef
Google scholar
|
[25] |
LiuH, FangHH. Extraction of extracellular polymeric substances (EPS) of sludges. J Biotechnol 2002; 95( 3): 249– 256
CrossRef
Google scholar
|
[26] |
ShengGP, YuHQ, YuZ. Extraction of extracellular polymeric substances from the photosynthetic bacterium Rhodopseudomonas acidophila. Appl Microbiol Biotechnol 2005; 67( 1): 125– 130
CrossRef
Google scholar
|
[27] |
NouhaK, KumarRS, BalasubramanianS, TyagiRD. Critical review of EPS production, synthesis and composition for sludge flocculation. J Environ Sci (China) 2018; 66 : 225– 245
CrossRef
Google scholar
|
[28] |
FlemmingHC, WingenderJ. The biofilm matrix. Nat Rev Microbiol 2010; 8( 9): 623– 633
CrossRef
Google scholar
|
[29] |
SpäthR, FlemmingHC, WuertzS. Sorption properties of biofilms. Water Sci Technol 1998; 37( 4-5): 207– 210
CrossRef
Google scholar
|
[30] |
SutherlandI. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology (Reading) 2001; 147( 1): 3– 9
CrossRef
Google scholar
|
[31] |
SutherlandIW. Exopolysaccharides in biofilms, flocs and related structures. Water Sci Technol 2001; 43( 6): 77– 86
CrossRef
Google scholar
|
[32] |
ParkC, NovakJT. Characterization of activated sludge exocellular polymers using several cation-associated extraction methods. Water Res 2007; 41( 8): 1679– 1688
CrossRef
Google scholar
|
[33] |
JoshiPM, JuwarkarAA. In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 2009; 43( 15): 5884– 5889
CrossRef
Google scholar
|
[34] |
HaJ, GélabertA, SpormannAM, BrownGE Jr. Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 2010; 74( 1): 1– 15
CrossRef
Google scholar
|
[35] |
ZhangD, WangJ, PanX. Cadmium sorption by EPSs produced by anaerobic sludge under sulfate-reducing conditions. J Hazard Mater 2006; 138( 3): 589– 593
CrossRef
Google scholar
|
[36] |
PriesterJH, OlsonSG, WebbSM, NeuMP, HersmanLE, HoldenPA. Enhanced exopolymer production and chromium stabilization in Pseudomonas putida unsaturated biofilms. Appl Environ Microbiol 2006; 72( 3): 1988– 1996
CrossRef
Google scholar
|
[37] |
ShengGP, YuHQ, LiXY. Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 2010; 28( 6): 882– 894
CrossRef
Google scholar
|
[38] |
HayID, Ur RehmanZ, MoradaliMF, WangY, RehmBH. Microbial alginate production, modification and its applications. Microb Biotechnol 2013; 6( 6): 637– 650
CrossRef
Google scholar
|
[39] |
SinghRS, SainiGK, KennedyJF. Pullulan: microbial sources, production and applications. Carbohydr Polym 2008; 73( 4): 515– 531
CrossRef
Google scholar
|
[40] |
Díaz-MontesE. Dextran: sources, structures, and properties. Polysaccharides 2021; 2( 3): 554– 565
CrossRef
Google scholar
|
[41] |
SzeJH, BrownlieJC, LoveCA. Biotechnological production of hyaluronic acid: a mini review. 3 Biotech 2016; 6 : 67
CrossRef
Google scholar
|
[42] |
ShodaM, SuganoY. Recent advances in bacterial cellulose production. Biotechnol Bioprocess Eng 2005; 10( 1): 1– 8
CrossRef
Google scholar
|
[43] |
SarwatF, Ul QaderSA, AmanA, AhmedN. Production & characterization of a unique dextran from an indigenous Leuconostoc mesenteroides CMG713. Int J Biol Sci 2008; 4( 6): 379– 386
CrossRef
Google scholar
|
[44] |
MonsanP, BozonnetS, AlbenneC, JouclaG, WillemotRM, Remaud-SiméonM. Homopolysaccharides from lactic acid bacteria. Int Dairy J 2001; 11( 9): 675– 685
CrossRef
Google scholar
|
[45] |
DolsM, Remaud-SimeonM, WillemotRM, VignonM, MonsanP. Characterization of the different dextransucrase activities excreted in glucose, fructose, or sucrose medium by Leuconostoc mesenteroides NRRL B-1299. Appl Environ Microbiol 1998; 64( 4): 1298– 1302
CrossRef
Google scholar
|
[46] |
HisamatsuM, AmemuraA, MatsuoT, MatsudaH, HaradaT. Cyclic (1→2)-β-D-glucan and the octasaccharide repeating-unit of succinoglycan produced by Agrobacterium. Microbiology 1982; 128( 8): 1873– 1879
CrossRef
Google scholar
|
[47] |
SaitoH, MisakiA, HaradaT. A comparison of the structure of curdlan and pachyman. Agric Biol Chem 1968; 32( 10): 1261– 1269
CrossRef
Google scholar
|
[48] |
DhiyaC, BennyIS, GunasekarV, PonnusamiV. A review on development of fermentative production of curdlan. Int J Chemtech Res 2014; 6 : 2769– 2773
|
[49] |
LeathersTD. Biotechnological production and applications of pullulan. Appl Microbiol Biotechnol 2003; 62( 5-6): 468– 473
CrossRef
Google scholar
|
[50] |
U.S
|
[51] |
CzajaW, KrystynowiczA, BieleckiS, BrownRM Jr. Microbial cellulose—the natural power to heal wounds. Biomaterials 2006; 27( 2): 145– 151
CrossRef
Google scholar
|
[52] |
DixonB AbbotP VergerP PascalG DiNoviM. Pullulan. In: Safety Evaluation of Certain Food Additives. Geneva: World Health Organization, 2004: 45– 62
|
[53] |
MeyerK, PalmerJW. The polysaccharide of the vitreous humor. J Biol Chem 1934; 107( 3): 629– 634
CrossRef
Google scholar
|
[54] |
KoganG, SoltésL, SternR, GemeinerP. Hyaluronic acid: a natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol Lett 2007; 29( 1): 17– 25
CrossRef
Google scholar
|
[55] |
CowmanMK, MatsuokaS. Experimental approaches to hyaluronan structure. Carbohydr Res 2005; 340( 5): 791– 809
CrossRef
Google scholar
|
[56] |
RossP, MayerR, BenzimanM. Cellulose biosynthesis and function in bacteria. Microbiol Rev 1991; 55( 1): 35– 58
CrossRef
Google scholar
|
[57] |
JonesD. Crystalline modifications of cellulose. Part V. A crystallographic study of ordered molecular arrangements. J Polym Sci e 1960; 42( 139): 173– 188
CrossRef
Google scholar
|
[58] |
BakhshinejadB, SadeghizadehM. Bacteriophages and development of nanomaterials for neural regeneration. Neural Regen Res 2014; 9( 22): 1955– 1958
CrossRef
Google scholar
|
[59] |
YooSY, KobayashiM, LeePP, LeeSW. Early osteogenic differentiation of mouse preosteoblasts induced by collagen-derived DGEA-peptide on nanofibrous phage tissue matrices. Biomacromolecules 2011; 12( 4): 987– 996
CrossRef
Google scholar
|
[60] |
HoffmanAS. Hydrogels for biomedical applications. Adv Drug Deliv Rev 2012; 64 : 18– 23
CrossRef
Google scholar
|
[61] |
PatelS, KasojuN, BoraU, GoyalA. Structural analysis and biomedical applications of dextran produced by a new isolate Pediococcus pentosaceus screened from biodiversity hot spot Assam. Bioresour Technol 2010; 101( 17): 6852– 6855
CrossRef
Google scholar
|
[62] |
KankeM, TanabeE, KatayamaH, KodaY, YoshitomiH. Application of curdlan to controlled drug delivery. III. Drug release from sustained release suppositories in vitro. Biol Pharm Bull 1995; 18( 8): 1154– 1158
CrossRef
Google scholar
|
[63] |
KankeM, KodaK, KodaY, KatayamaH. Application of curdlan to controlled drug delivery. I. The preparation and evaluation of theophylline-containing curdlan tablets. Pharm Res 1992; 9( 3): 414– 418
CrossRef
Google scholar
|
[64] |
BohnJA, BeMillerJN. (1→3)-β-D-Glucans as biological response modifiers: a review of structure-functional activity relationships. Carbohydr Polym 1995; 28( 1): 3– 14
CrossRef
Google scholar
|
[65] |
WilliamsPA. Renewable Resources for Functional Polymers and Biomaterials: Polysaccharides, Proteins and Polyesters. Cambridge, UK: Royal Society of Chemistry, 2011
|
[66] |
RekhaM, SharmaCP. Pullulan as a promising biomaterial for biomedical applications: a perspective. Trends Biomater Artif Organs 2007; 20 : 116– 121
|
[67] |
DanesePN, PrattLA, KolterR. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 2000; 182( 12): 3593– 3596
CrossRef
Google scholar
|
[68] |
Prigent-CombaretC, VidalO, DorelC, LejeuneP. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 1999; 181( 19): 5993– 6002
CrossRef
Google scholar
|
[69] |
ChristensenGD, SimpsonWA, BisnoAL, BeacheyEH. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 1982; 37( 1): 318– 326
CrossRef
Google scholar
|
[70] |
ChristensenTE, SaxtrupO, HansenTI, KristensenBH, BeckBL, PlesnerT, KroghIM, AndersenV, StrandgaardS. Familial myoglobinuria. A study of muscle and kidney pathophysiology in three brothers. Dan Med Bull 1983; 30( 2): 112– 115
|
[71] |
DavenportDS, MassanariRM, PfallerMA, BaleMJ, StreedSA, HierholzerWJ Jr. Usefulness of a test for slime production as a marker for clinically significant infections with coagulase-negative staphylococci. J Infect Dis 1986; 153( 2): 332– 339
CrossRef
Google scholar
|
[72] |
DruryJL, MooneyDJ. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 2003; 24( 24): 4337– 4351
CrossRef
Google scholar
|
[73] |
GuptaP, VermaniK, GargS. Hydrogels: from controlled release to pH-responsive drug delivery. Drug Discov Today 2002; 7( 10): 569– 579
CrossRef
Google scholar
|
[74] |
LutolfMP, Lauer-FieldsJL, SchmoekelHG, MettersAT, WeberFE, FieldsGB, HubbellJA. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci USA 2003; 100( 9): 5413– 5418
CrossRef
Google scholar
|
[75] |
PeppasNA, HiltJZ, KhademhosseiniA, LangerR. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater 2006; 18( 11): 1345– 1360
CrossRef
Google scholar
|
[76] |
Rezapour-LactoeeA, YeganehH, GharibiR, MilanPB. Enhanced healing of a full-thickness wound by a thermoresponsive dressing utilized for simultaneous transfer and protection of adipose-derived mesenchymal stem cells sheet. J Mater Sci Mater Med 2020; 31( 11): 101
CrossRef
Google scholar
|
[77] |
CutiongcoMF, TanMH, NgMY, Le VisageC, YimEK. Composite pullulan−dextran polysaccharide scaffold with interfacial polyelectrolyte complexation fibers: a platform with enhanced cell interaction and spatial distribution. Acta Biomater 2014; 10( 10): 4410– 4418
CrossRef
Google scholar
|
[78] |
NwodoUU, GreenE, OkohAI. Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci 2012; 13( 11): 14002– 14015
CrossRef
Google scholar
|
[79] |
UnnithanAR, SasikalaAR, MurugesanP, GurusamyM, WuD, ParkCH, KimCS. Electrospun polyurethane-dextran nanofiber mats loaded with estradiol for post-menopausal wound dressing. Int J Biol Macromol 2015; 77 : 1– 8
CrossRef
Google scholar
|
[80] |
LévesqueSG, LimRM, ShoichetMS. Macroporous interconnected dextran scaffolds of controlled porosity for tissue-engineering applications. Biomaterials 2005; 26( 35): 7436– 7446
CrossRef
Google scholar
|
[81] |
LackS, DulongV, PictonL, Le CerfD, CondamineE. High-resolution nuclear magnetic resonance spectroscopy studies of polysaccharides crosslinked by sodium trimetaphosphate: a proposal for the reaction mechanism. Carbohydr Res 2007; 342( 7): 943– 953
CrossRef
Google scholar
|
[82] |
Le VisageC, GournayO, BenguiratN, HamidiS, ChaussumierL, MougenotN, FlandersJA, IsnardR, MichelJB, HatemS, LetourneurD, NorolF. Mesenchymal stem cell delivery into rat infarcted myocardium using a porous polysaccharide-based scaffold: a quantitative comparison with endocardial injection. Tissue Eng Part A 2012; 18( 1-2): 35– 44
CrossRef
Google scholar
|
[83] |
AmedeeJ LetourneurD Le VisageC DerkaouiSM FricainJC CatrosS. Porous polysaccharide scaffold comprising nano-hydroxyapatite and use for bone formation. Google Patents; 2017, Universite Victor Segalen Bordeaux 2 Institut National de la Sante et de la RechercheMedicale INSERM Universite Paris Diderot Paris 7. US20130224277A1
|
[84] |
BanerjeeS, SzepesM, DibbertN, Rios-CamachoJC, KirschningA, GruhI, DrägerG. Dextran-based scaffolds for in-situ hydrogelation: use for next generation of bioartificial cardiac tissues. Carbohydr Polym 2021; 262 : 117924
CrossRef
Google scholar
|
[85] |
NaghiehS, SarkerMD, AbelsethE, ChenX. Indirect 3D bioprinting and characterization of alginate scaffolds for potential nerve tissue engineering applications. J Mech Behav Biomed Mater 2019; 93 : 183– 193
CrossRef
Google scholar
|
[86] |
HivechiA, MilanPB, ModabberiK, AmoupourM, EbrahimzadehK, GholipourAR, SedighiF, AminiN, BahramiSH, RezapourA, HamidiM, DelattreC. Synthesis and characterization of exopolysaccharide encapsulated PCL/gelatin skin substitute for full-thickness wound regeneration. Polymers (Basel) 2021; 13( 6): 854
CrossRef
Google scholar
|
[87] |
CzajaWK, YoungDJ, KaweckiM, BrownRM Jr. The future prospects of microbial cellulose in biomedical applications. Biomacromolecules 2007; 8( 1): 1– 12
CrossRef
Google scholar
|
[88] |
MilanPB AminiN AmoupourM AmadikuchaksaraeiA RezapourA SefatF KargozarS AshtariKh MozafariM. Scaffolds for regeneration of dermo-epidermal skin tissue. Handbook of Tissue Engineering Scaffolds. Volume 2. Elsevier Science, 2019: 193– 209
|
[89] |
SinghRS, KaurN, RanaV, KennedyJF. Pullulan: a novel molecule for biomedical applications. Carbohydr Polym 2017; 171 : 102– 121
CrossRef
Google scholar
|
[90] |
SamoilaI, DinescuS, PircalabioruGG, MarutescuL, FundueanuG, AfloriM, ConstantinM. Pullulan/poly(vinyl alcohol) composite hydrogels for adipose tissue engineering. Materials (Basel) 2019; 12( 19): 3220
CrossRef
Google scholar
|
[91] |
KulkarniN KumarL SorgA. Fast dissolving orally consumable films. Google Patents; 2011, Johnson and Johnson Consumer Inc. US20030206942A1
|
[92] |
ChenF, YuS, LiuB, NiY, YuC, SuY, ZhuX, YuX, ZhouY, YanD. An injectable enzymatically crosslinked carboxymethylated pullulan/chondroitin sulfate hydrogel for cartilage tissue engineering. Sci Rep 2016; 6( 1): 20014
CrossRef
Google scholar
|
[93] |
JinHE, LeeSW. Engineering of M13 bacteriophage for development of tissue engineering materials. Methods Mol Biol 2018; 1776 : 487– 502
CrossRef
Google scholar
|
[94] |
WangJ, WangL, YangM, ZhuY, TomsiaA, MaoC. Untangling the effects of peptide sequences and nanotopographies in a biomimetic niche for directed differentiation of iPSCs by assemblies of genetically engineered viral nanofibers. Nano Lett 2014; 14( 12): 6850– 6856
CrossRef
Google scholar
|
[95] |
ShinYC, LeeJH, JinL, KimMJ, KimC, HongSW, OhJW, HanDW. Cell-adhesive matrices composed of RGD peptide-displaying M13 bacteriophage/poly(lactic-co-glycolic acid) nanofibers beneficial to myoblast differentiation. J Nanosci Nanotechnol 2015; 15( 10): 7907– 7912
CrossRef
Google scholar
|
[96] |
Szot-KarpińskaK, GolecP, LeśniewskiA, PałysB, MarkenF, Niedziółka-Jönsson J, WęgrzynG, Łoś M. Modified filamentous bacteriophage as a scaffold for carbon nanofiber. Bioconjug Chem 2016; 27( 12): 2900– 2910
CrossRef
Google scholar
|
[97] |
AschtgenMS, BrennanCA, NikolakakisK, CohenS, McFall-NgaiM, RubyEG. Insights into flagellar function and mechanism from the squid-vibrio symbiosis. NPJ Biofilms Microbiomes 2019; 5( 1): 32
CrossRef
Google scholar
|
[98] |
LiD, ZhuY, YangT, YangM, MaoC. Bacterial flagella as an osteogenic differentiation nano-promoter. Nanoscale Horiz 2019; 4( 6): 1286– 1292
CrossRef
Google scholar
|
[99] |
LiD, ZhuY, YangT, YangM, MaoC. Genetically engineered flagella form collagen-like ordered structures for inducing stem cell differentiation. iScience 2019; 17 : 277– 287
CrossRef
Google scholar
|
[100] |
ChenY, LongX, LinW, DuB, YinH, LanW, ZhaoD, LiZ, LiJ, LuoF, TanH. Bioactive 3D porous cobalt-doped alginate/waterborne polyurethane scaffolds with a coral reef-like rough surface for nerve tissue engineering application. J Mater Chem B Mater Biol Med 2021; 9( 2): 322– 335
CrossRef
Google scholar
|
[101] |
SajeshKM, JayakumarR, NairSV, ChennazhiKP. Biocompatible conducting chitosan/polypyrrole-alginate composite scaffold for bone tissue engineering. Int J Biol Macromol 2013; 62 : 465– 471
CrossRef
Google scholar
|
[102] |
YangB, YaoF, YeL, HaoT, ZhangY, ZhangL, DongD, FangW, WangY, ZhangX, WangC, LiJ. A conductive PEDOT/alginate porous scaffold as a platform to modulate the biological behaviors of brown adipose-derived stem cells. Biomater Sci 2020; 8( 11): 3173– 3185
CrossRef
Google scholar
|
[103] |
YuanH, ZhengX, LiuW, ZhangH, ShaoJ, YaoJ, MaoC, HuiJ, FanD. A novel bovine serum albumin and sodium alginate hydrogel scaffold doped with hydroxyapatite nanowires for cartilage defects repair. Colloids Surf B Biointerfaces 2020; 192 : 111041
CrossRef
Google scholar
|
[104] |
RashtchianM, HivechiA, BahramiSH, MilanPB, SimorghS. Fabricating alginate/poly(caprolactone) nanofibers with enhanced bio-mechanical properties via cellulose nanocrystal incorporation. Carbohydr Polym 2020; 233 : 115873
CrossRef
Google scholar
|
[105] |
TamimiM, RajabiS, Pezeshki-ModaressM. Cardiac ECM/chitosan/alginate ternary scaffolds for cardiac tissue engineering application. Int J Biol Macromol 2020; 164 : 389– 402
CrossRef
Google scholar
|
[106] |
GhaffariR, Salimi-KenariH, FahimipourF, RabieeSM, AdeliH, DashtimoghadamE. Fabrication and characterization of dextran/nanocrystalline β-tricalcium phosphate nanocomposite hydrogel scaffolds. Int J Biol Macromol 2020; 148 : 434– 448
CrossRef
Google scholar
|
[107] |
Innocenti MaliniR, LesageJ, ToncelliC, FortunatoG, RossiRM, SpanoF. Crosslinking dextran electrospun nanofibers via borate chemistry: proof of concept for wound patches. Eur Polym J 2019; 110 : 276– 282
CrossRef
Google scholar
|
[108] |
MoydeenAM, Ali PadushaMS, AboelfetohEF, Al-DeyabSS, El-NewehyMH. Fabrication of electrospun poly(vinyl alcohol)/dextran nanofibers via emulsion process as drug delivery system: kinetics and in vitro release study. Int J Biol Macromol 2018; 116 : 1250– 1259
CrossRef
Google scholar
|
[109] |
DongY, ZhaoS, LuW, ChenN, ZhuD, LiY. Preparation and characterization of enzymatically cross-linked gelatin/cellulose nanocrystal composite hydrogels. RSC Advances 2021; 11( 18): 10794– 10803
CrossRef
Google scholar
|
[110] |
ZhaoS, EmeryO, WohlhauserA, KoebelMM, AdlhartC, MalfaitWJ. Merging flexibility with superinsulation: machinable, nanofibrous pullulan-silica aerogel composites. Mater Des 2018; 160 : 294– 302
CrossRef
Google scholar
|
[111] |
NosoudiN, OommenAJ, StultzS, JordanM, AldabelS, HohneC, MosserJ, ArchackiB, TurnerA, TurnerP. Electrospinning live cells using gelatin and pullulan. Bioengineering (Basel) 2020; 7( 1): 21
CrossRef
Google scholar
|
[112] |
BarreraJA, TrotsyukAA, MaanZN, BonhamCA, LarsonMR, MittermillerPA, HennD, ChenK, MaysCJ, MittalS, Mermin-BunnellAM, SivarajD, JingS, RodriguesM, KwonSH, NoishikiC, PadmanabhanJ, JiangY, NiuS, InayathullahM, RajadasJ, JanuszykM, GurtnerGC. Adipose-derived stromal cells seeded in pullulan-collagen hydrogels improve healing in murine burns. Tissue Eng Part A 2021; 27( 11-12): 844– 856
CrossRef
Google scholar
|
[113] |
DellaGiustina G, GandinA, BrigoL, PancieraT, GiulittiS, SgarbossaP, D’AlessandroD, TrombiL, DantiS, BrusatinG. Polysaccharide hydrogels for multiscale 3D printing of pullulan scaffolds. Mater Des 2019; 165 : 107566
CrossRef
Google scholar
|
[114] |
DalgicAD, AtilaD, KaratasA, TezcanerA, KeskinD. Diatom shell incorporated PHBV/PCL-pullulan co-electrospun scaffold for bone tissue engineering. Mater Sci Eng C 2019; 100 : 735– 746
CrossRef
Google scholar
|
[115] |
TangS, ChiK, XuH, YongQ, YangJ, CatchmarkJM. A covalently cross-linked hyaluronic acid/bacterial cellulose composite hydrogel for potential biological applications. Carbohydr Polym 2021; 252 : 117123
CrossRef
Google scholar
|
[116] |
YangQ, XieZ, HuJ, LiuY. Hyaluronic acid nanofiber mats loaded with antimicrobial peptide towards wound dressing applications. Mater Sci Eng C 2021; 128 : 112319
CrossRef
Google scholar
|
[117] |
CaiY, JohnsonM, AS, Xu Q, TaiH, WangW. A hybrid injectable and self-healable hydrogel system as 3D cell culture scaffold. Macromol Biosci 2021; 21( 9): e2100079
CrossRef
Google scholar
|
[118] |
LeeAK, LinYH, TsaiCH, ChangWT, LinTL, ShieMY. Digital light processing bioprinted human chondrocyte-laden poly (γ-glutamic acid)/hyaluronic acid bio-ink towards cartilage tissue engineering. Biomedicines 2021; 9( 7): 714
CrossRef
Google scholar
|
[119] |
TarrahiR, KhataeeA, KarimiA, GolizadehM, Ebadi Fard AzarF. Development of a cellulose-based scaffold for sustained delivery of curcumin. Int J Biol Macromol 2021; 183 : 132– 144
CrossRef
Google scholar
|
[120] |
GuoR, LiJ, ChenC, XiaoM, LiaoM, HuY, LiuY, LiD, ZouJ, SunD, TorreV, ZhangQ, ChaiR, TangM. Biomimetic 3D bacterial cellulose-graphene foam hybrid scaffold regulates neural stem cell proliferation and differentiation. Colloids Surf B Biointerfaces 2021; 200 : 111590
CrossRef
Google scholar
|
[121] |
PriyaG, MadhanB, NarendrakumarU, Suresh KumarRV, ManjubalaI. In vitro and in vivo evaluation of carboxymethyl cellulose scaffolds for bone tissue engineering applications. ACS Omega 2021; 6( 2): 1246– 1253
CrossRef
Google scholar
|
[122] |
WahidF, ZhaoXJ, ZhaoXQ, MaXF, XueN, LiuXZ, WangFP, JiaSR, ZhongC. Fabrication of bacterial cellulose-based dressings for promoting infected wound healing. ACS Appl Mater Interfaces 2021; 13( 28): 32716– 32728
CrossRef
Google scholar
|
[123] |
HanY, LiC, CaiQ, BaoX, TangL, AoH, LiuJ, JinM, ZhouY, WanY, LiuZ. Studies on bacterial cellulose/poly(vinyl alcohol) hydrogel composites as tissue-engineered corneal stroma. Biomed Mater 2020; 15( 3): 035022
CrossRef
Google scholar
|
[124] |
Szot-KarpińskaK, LeśniewskiA, Jönsson-Niedziółka M, MarkenF, Niedziółka-Jönsson J. Electrodes modified with bacteriophages and carbon nanofibres for cysteine detection. Sens Actuators B Chem 2019; 287 : 78– 85
CrossRef
Google scholar
|
[125] |
ChengW, ZhangZ, XuR, CaiP, KristensenP, ChenM, HuangY. Incorporation of bacteriophages in polycaprolactone/collagen fibers for antibacterial hemostatic dual-function. J Biomed Mater Res B Appl Biomater 2018; 106( 7): 2588– 2595
CrossRef
Google scholar
|
[126] |
MaY, PacanJC, WangQ, XuY, HuangX, KorenevskyA, SabourPM. Microencapsulation of bacteriophage felix O1 into chitosan-alginate microspheres for oral delivery. Appl Environ Microbiol 2008; 74( 15): 4799– 4805
CrossRef
Google scholar
|
[127] |
LeeJY, ChungWJ, KimG. A mechanically improved virus-based hybrid scaffold for bone tissue regeneration. RSC Advances 2016; 6( 60): 55022– 55032
CrossRef
Google scholar
|
[128] |
GalloN, NasserH, SalvatoreL, NataliML, CampaL, MahmoudM, CapobiancoL, SanninoA, MadaghieleM. Hyaluronic acid for advanced therapies: Promises and challenges. Eur Polym J 2019; 117 : 134– 147
CrossRef
Google scholar
|
[129] |
SunG, KusumaS, GerechtS. Development of a biodegradable, temperature-sensitive dextran-based polymer as a cell-detaching substrate. Macromol Biosci 2012; 12( 1): 21– 28
CrossRef
Google scholar
|
[130] |
CurvelloR, RaghuwanshiVS, GarnierG. Engineering nanocellulose hydrogels for biomedical applications. Adv Colloid Interface Sci 2019; 267 : 47– 61
CrossRef
Google scholar
|
[131] |
SzekalskaM, PuciłowskaA, SzymańskaA, CiosekP, WinnickaK. Alginate: current use and future perspectives in pharmaceutical and biomedical applications. Int J Polym Sci 2016; 2016 : 7697031
CrossRef
Google scholar
|
/
〈 | 〉 |