Injectable Hyaluronic Acid/Poly(<italic style="font-style: italic">γ</italic>-glutamic acid) Hydrogel with Step-by-step Tunable Properties for Soft Tissue Engineering

Xue-Bin Ma; Rong Yang; Kanaparedu P. C. Sekhar; Bo Chi

doi:10.1007/s10118-021-2558-3

Your Location：

Home >

Browse articles >

Injectable Hyaluronic Acid/Poly(γ-glutamic acid) Hydrogel with Step-by-step Tunable Properties for Soft Tissue Engineering

ARTICLE | Updated：2021-04-30

- Injectable Hyaluronic Acid/Poly(γ-glutamic acid) Hydrogel with Step-by-step Tunable Properties for Soft Tissue Engineering
- Chinese Journal of Polymer Science Vol. 39, Issue 8, Pages: 957-965(2021)
- Affiliations：
  
  a.Key Laboratory of Colloid and Interface Chemistry of the Ministry of Education, School of Chemistry and Chemical Engineering, Shandong University, Jinan 250100, China
  b.State Key Laboratory of Materials-Oriented Chemical Engineering, College of Food Science and Light Industry, Nanjing Tech University, Nanjing 211816, China
- Author bio：
  
  chibo@njtech.edu.cn
- Funds：
- DOI：10.1007/s10118-021-2558-3
  CLC：
- Received：02 December 2020，
  
  Revised：2021-1-19，
  
  Accepted：25 January 2021，
  
  Online First：30 April 2021，
  
  Published：18 June 2021
- Accepted：
Scan QR Code
Ma, X. B.; Yang, R.; Sekhar, K. P. C.; Chi, B. Injectable hyaluronic acid/poly(γ-glutamic acid) hydrogel with step-by-step tunable properties for soft tissue engineering. Chinese J. Polym. Sci. 2021, 39, 957–965

Xue-Bin Ma, Rong Yang, Kanaparedu P. C. Sekhar, et al. Injectable Hyaluronic Acid/Poly(γ-glutamic acid) Hydrogel with Step-by-step Tunable Properties for Soft Tissue Engineering[J]. Chinese Journal of Polymer Science, 2021, 39(8): 957-965. DOI: 10.1007/s10118-021-2558-3.
Ma, X. B.; Yang, R.; Sekhar, K. P. C.; Chi, B. Injectable hyaluronic acid/poly(γ-glutamic acid) hydrogel with step-by-step tunable properties for soft tissue engineering. Chinese J. Polym. Sci. 2021, 39, 957–965 DOI： 10.1007/s10118-021-2558-3.

Xue-Bin Ma, Rong Yang, Kanaparedu P. C. Sekhar, et al. Injectable Hyaluronic Acid/Poly(γ-glutamic acid) Hydrogel with Step-by-step Tunable Properties for Soft Tissue Engineering[J]. Chinese Journal of Polymer Science, 2021, 39(8): 957-965. DOI: 10.1007/s10118-021-2558-3. DOI：

摘要

Abstract

Injectable hydrogels as an important class of biomaterials have gained much attention in tissue engineering. However

their crosslinking degree is difficult to be controlled after being injected into body. As we all know

the crosslinking degree strongly influences the physicochemical properties of hydrogels. Therefore

developing an injectable hydrogel with tunable crosslinking degree

in vivo

is important for tissue engineering. Herein

we present a dual crosslinking strategy to prepare injectable hydrogels with step-by-step tunable crosslinking degree using Schiff base reaction and photopolymerization. The developed hyaluronic acid/poly(

-glutamic acid) (HA/

-PGA) hydrogels exhibit step-by-step tunable swelling behavior

enzymatic degradation behavior and mechanical properties. Mechanical performance tests show that the storage moduli of HA/

-PGA hydrogels are all less than 2000 Pa and the compressive moduli are in kilopascal

which have a good match with soft tissue. In addition

NIH 3T3 cells encapsulated in HA/

-PGA hydrogel exhibit a high cell viability

indicating a good cytocompatibility of HA/

-PGA hydrogel. Therefore

the developed HA/

-PGA hydrogel as an injectable biomaterial has a good potential in soft tissue engineering.

关键词

Keywords

references

Pertici, V.; Pin-Barre, C.; Rivera, C.; Pellegrino, C.; Laurin, J.; Gigmes, D.; Trimaille, T. . Degradable and injectable hydrogel for drug delivery in soft tissues . Biomacromolecules , 2019 . 20 149 - 163 . DOI: 10.1021/acs.biomac.8b01242 http://doi.org/10.1021/acs.biomac.8b01242 .

Qu, J.; Zhao, X.; Liang, Y.; Xu, Y.; Ma, P. X.; Guo, B. . Degradable conductive injectable hydrogels as novel antibacterial, anti-oxidant wound dressings for wound healing . Chem. Eng. J. , 2019 . 362 548 - 560 . DOI: 10.1016/j.cej.2019.01.028 http://doi.org/10.1016/j.cej.2019.01.028 .

Jung, Y. S.; Park, W.; Park, H.; Lee, D. K.; Na, K. . Thermo-sensitive injectable hydrogel based on the physical mixing of hyaluronic acid and Pluronic F-127 for sustained NSAID delivery . Carbohydr. Polym. , 2017 . 156 403 - 408 . DOI: 10.1016/j.carbpol.2016.08.068 http://doi.org/10.1016/j.carbpol.2016.08.068 .

Yan, S.; Wang, T.; Feng, L.; Zhu, J.; Zhang, K.; Chen, X.; Cui, L.; Yin, J. . Injectable in situ self-cross-linking hydrogels based on poly(L-glutamic acid) and alginate for cartilage tissue engineering . Biomacromolecules , 2014 . 15 4495 - 4508 . DOI: 10.1021/bm501313t http://doi.org/10.1021/bm501313t .

Fu, S.; Dong, H.; Deng, X.; Zhuo, R.; Zhong, Z. . Injectable hyaluronic acid/poly(ethylene glycol) hydrogels crosslinked via strain-promoted azide-alkyne cycloaddition click reaction . Carbohydr. Polym. , 2017 . 169 332 - 340 . DOI: 10.1016/j.carbpol.2017.04.028 http://doi.org/10.1016/j.carbpol.2017.04.028 .

Yan, S.; Wang, T.; Li, X.; Jian, Y.; Zhang, K.; Li, G.; Yin, J. . Fabrication of injectable hydrogels based on poly(L-glutamic acid) and chitosan . RSC Adv. , 2017 . 7 17005 - 17019 . DOI: 10.1039/C7RA01864A http://doi.org/10.1039/C7RA01864A .

Carvalho, I. C.; Mansur, H. S. . Engineered 3D-scaffolds of photocrosslinked chitosan-gelatin hydrogel hybrids for chronic wound dressings and regeneration . Mater. Sci. Eng. C-Mater. Biol. Appl. , 2017 . 78 690 - 705 . DOI: 10.1016/j.msec.2017.04.126 http://doi.org/10.1016/j.msec.2017.04.126 .

Kang, W.; Bi, B.; Zhuo, R.; Jiang, X. . Photocrosslinked methacrylated carboxymethyl chitin hydrogels with tunable degradation and mechanical behavior . Carbohydr. Polym. , 2017 . 160 18 - 25 . DOI: 10.1016/j.carbpol.2016.12.032 http://doi.org/10.1016/j.carbpol.2016.12.032 .

Bian, L.; Hou, C.; Tous, E.; Rai, R.; Mauck, R. L.; Burdick, J. A. . The influence of hyaluronic acid hydrogel crosslinking density and macromolecular diffusivity on human MSC chondrogenesis and hypertrophy . Biomaterials , 2013 . 34 413 - 421 . DOI: 10.1016/j.biomaterials.2012.09.052 http://doi.org/10.1016/j.biomaterials.2012.09.052 .

Oommen, O. P.; Wang, S.; Kisiel, M.; Sloff, M.; Hilborn, J.; Varghese, O. P. . Smart design of stable extracellular matrix mimetic hydrogel: synthesis, characterization, and in vitro and in vivo evaluation for tissue engineering . Adv. Funct. Mater. , 2013 . 23 1273 - 1280 . DOI: 10.1002/adfm.201201698 http://doi.org/10.1002/adfm.201201698 .

Wei, Z.; Yang, J. H.; Liu, Z. Q.; Xu, F.; Zhou, J. X.; Zrínyi, M.; Osada, Y.; Chen, Y. M. . Novel biocompatible polysaccharide-based self-healing hydrogel . Adv. Funct. Mater. , 2015 . 25 1352 - 1359 . DOI: 10.1002/adfm.201401502 http://doi.org/10.1002/adfm.201401502 .

Pandit, A. H.; Mazumdar, N.; Ahmad, S. . Periodate oxidized hyaluronic acid-based hydrogel scaffolds for tissue engineering applications . Int. J. Biol. Macromol. , 2019 . 137 853 - 869 . DOI: 10.1016/j.ijbiomac.2019.07.014 http://doi.org/10.1016/j.ijbiomac.2019.07.014 .

Ma, X.; Xu, T.; Chen, W.; Qin, H.; Chi, B.; Ye, Z. . Injectable hydrogels based on the hyaluronic acid and poly( γ -glutamic acid) for controlled protein delivery . Carbohydr. Polym. , 2018 . 179 100 - 109 . DOI: 10.1016/j.carbpol.2017.09.071 http://doi.org/10.1016/j.carbpol.2017.09.071 .

Zou, Y. J.; He, S. S.; Du, J. Z. . ε -Poly(L-lysine)-based hydrogels with fast-acting and prolonged antibacterial activities . Chinese J. Polym. Sci. , 2018 . 36 1239 - 1250 . DOI: 10.1007/s10118-018-2156-1 http://doi.org/10.1007/s10118-018-2156-1 .

Duan, J. J.; Zhang, L. N. . Robust and smart hydrogels based on natural polymers . Chinese J. Polym. Sci. , 2017 . 35 1165 - 1180 . DOI: 10.1007/s10118-017-1983-9 http://doi.org/10.1007/s10118-017-1983-9 .

Shi, L.; Zhao, Y.; Xie, Q.; Fan, C.; Hilborn, J.; Dai, J.; Ossipov, D. A. . Moldable hyaluronan hydrogel enabled by dynamic metal-bisphosphonate coordination chemistry for wound healing . Adv. Healthc. Mater. , 2017 . 1700973 .

Bian, S.; He, M.; Sui, J.; Cai, H.; Sun, Y.; Liang, J.; Fan, Y.; Zhang, X. . The self-crosslinking smart hyaluronic acid hydrogels as injectable three-dimensional scaffolds for cells culture . Colloid Surf. B-Biointerfaces , 2016 . 140 392 - 402 . DOI: 10.1016/j.colsurfb.2016.01.008 http://doi.org/10.1016/j.colsurfb.2016.01.008 .

Mohandas, A.; Anisha, B. S.; Chennazhi, K. P.; Jayakumar, R. . Chitosan-hyaluronic acid/VEGF loaded fibrin nanoparticles composite sponges for enhancing angiogenesis in wounds . Colloid Surf. B-Biointerfaces , 2015 . 127 105 - 113 . DOI: 10.1016/j.colsurfb.2015.01.024 http://doi.org/10.1016/j.colsurfb.2015.01.024 .

Hwang, H. D.; Cho, H. J.; Balakrishnan, P.; Chung, C. W.; Yoon, I. S.; Oh, Y. K.; Byun, Y.; Kim, D. D. . Cross-linked hyaluronic acid-based flexible cell delivery system: application for chondrogenic differentiation . Colloid Surf. B-Biointerfaces , 2012 . 91 106 - 113 . DOI: 10.1016/j.colsurfb.2011.10.052 http://doi.org/10.1016/j.colsurfb.2011.10.052 .

Collins, M. N.; Birkinshaw, C. . Hyaluronic acid based scaffolds for tissue engineering−a review . Carbohydr. Polym. , 2013 . 92 1262 - 1279 . DOI: 10.1016/j.carbpol.2012.10.028 http://doi.org/10.1016/j.carbpol.2012.10.028 .

Pescosolido, L.; Schuurman, W.; Malda, J.; Matricardi, P.; Alhaique, F.; Coviello, T.; van, Weeren P. R.; Dhert, W. J.; Hennink, W. E.; Vermonden, T. . Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting . Biomacromolecules , 2011 . 12 1831 - 1838 . DOI: 10.1021/bm200178w http://doi.org/10.1021/bm200178w .

Murphy, S. V.; Skardal, A.; Atala, A. . Evaluation of hydrogels for bio-printing applications . J. Biomed. Mater. Res. Part A , 2013 . 101 272 - 284 . .

Gentilini, C.; Dong, Y.; May, J. R.; Goldoni, S.; Clarke, D. E.; Lee, B. H.; Pashuck, E. T.; Stevens, M. M. . Functionalized poly( γ -glutamic acid) fibrous scaffolds for tissue engineering . Adv. Healthc. Mater. , 2012 . 1 308 - 315 . DOI: 10.1002/adhm.201200036 http://doi.org/10.1002/adhm.201200036 .

Zhang, D.; Feng, X.; Zhou, Z.; Zhang, Y.; Xu, H. . Economical production of poly( γ -glutamic acid) using untreated cane molasses and monosodium glutamate waste liquor by Bacillus subtilis NX-2 . Bioresour. Technol. , 2012 . 114 583 - 588 . DOI: 10.1016/j.biortech.2012.02.114 http://doi.org/10.1016/j.biortech.2012.02.114 .

Clarke, D. E.; Pashuck, E. T.; Bertazzo, S.; Weaver, J. V. M.; Stevens, M. M. . Self-healing, self-assembled β -sheet peptide-poly( γ -glutamic acid) hybrid hydrogels . J. Am. Chem. Soc. , 2017 . 139 7250 - 7255 . DOI: 10.1021/jacs.7b00528 http://doi.org/10.1021/jacs.7b00528 .

Xu, T.; Yang, R.; Ma, X.; Chen, W.; Liu, S.; Liu, X.; Cai, X.; Xu, H.; Chi, B. . Bionic poly( γ -glutamic acid) electrospun fibrous scaffolds for preventing hypertrophic scars . Adv. Healthc. Mater. , 2019 . 1900123 .

Yang, R.; Wang, X.; Liu, S.; Zhang, W.; Wang, P.; Liu, X.; Ren, Y.; Tan, X.; Chi, B. . Bioinspired poly( γ -glutamic acid) hydrogels for enhanced chondrogenesis of bone marrow-derived mesenchymal stem cells . Int. J. Biol. Macromol. , 2020 . 142 332 - 344 . DOI: 10.1016/j.ijbiomac.2019.09.104 http://doi.org/10.1016/j.ijbiomac.2019.09.104 .

Zhuang, H.; Hong, Y.; Gao, J.; Chen, S.; Ma, Y.; Wang, S. . A poly( γ -glutamic acid)-based hydrogel loaded with superoxide dismutase for wound healing . J. Appl. Polym. Sci. , 2015 . 42033 .

Ito, T.; Yeo, Y.; Highley, C. B.; Bellas, E.; Benitez, C. A.; Kohane, D. S. . The prevention of peritoneal adhesions by in situ cross-linking hydrogels of hyaluronic acid and cellulose derivatives . Biomaterials , 2007 . 28 975 - 983 . DOI: 10.1016/j.biomaterials.2006.10.021 http://doi.org/10.1016/j.biomaterials.2006.10.021 .

Huh, H. W.; Zhao, L.; Kim, S. Y. . Biomineralized biomimetic organic/inorganic hybrid hydrogels based on hyaluronic acid and poloxamer . Carbohydr. Polym. , 2015 . 126 130 - 140 . DOI: 10.1016/j.carbpol.2015.03.033 http://doi.org/10.1016/j.carbpol.2015.03.033 .

Li, L.; Wang, N.; Jin, X.; Deng, R.; Nie, S.; Sun, L.; Wu, Q.; Wei, Y.; Gong, C. . Biodegradable and injectable in situ cross-linking chitosan-hyaluronic acid based hydrogels for postoperative adhesion prevention . Biomaterials , 2014 . 35 3903 - 3917 . DOI: 10.1016/j.biomaterials.2014.01.050 http://doi.org/10.1016/j.biomaterials.2014.01.050 .

Li, N. N.; Fu, C. P.; Zhang, L. M. . Using casein and oxidized hyaluronic acid to form biocompatible composite hydrogels for controlled drug release . Mater. Sci. Eng. C-Mater. Biol. Appl. , 2014 . 36 287 - 293 . DOI: 10.1016/j.msec.2013.12.025 http://doi.org/10.1016/j.msec.2013.12.025 .

Dooling, L. J.; Buck, M. E.; Zhang, W. B.; Tirrell, D. A. . Programming molecular association and viscoelastic behavior in protein networks . Adv. Mater. , 2016 . 28 4651 - 4657 . DOI: 10.1002/adma.201506216 http://doi.org/10.1002/adma.201506216 .

Tomer, R.; Dimitrijevic, D.; Florence., A. T . Electrically controlled release of macromolecules from cross–linked hyaluronic acid hydrogels . J. Control. Release , 1995 . 33 405 - 413 . DOI: 10.1016/0168-3659(94)00115-B http://doi.org/10.1016/0168-3659(94)00115-B .

Kunioka, M.; Choi, H. J. . Hydrolytic degradation and mechanical properties of hydrogels prepared from microbial poly(amino acid)s . Polym. Degrad. Stabil. , 1998 . 59 33 - 31 . DOI: 10.1016/S0141-3910(97)00181-X http://doi.org/10.1016/S0141-3910(97)00181-X .

Jeon, O.; Song, S. J.; Lee, K. J.; Park, M. H.; Lee, S. H.; Hahn, S. K.; Kim, S.; Kim, B. S. . Mechanical properties and degradation behaviors of hyaluronic acid hydrogels cross-linked at various cross-linking densities . Carbohydr. Polym. , 2007 . 70 251 - 257 . DOI: 10.1016/j.carbpol.2007.04.002 http://doi.org/10.1016/j.carbpol.2007.04.002 .

Jiao, Y.; Liu, Z.; Zhou, C. . Fabrication and characterization of PLLA-chitosan hybrid scaffolds with improved cell compatibility . J. Biomed. Mater. Res. Part A , 2007 . 80 820 - 825 . .

Yuan, L.; Wu, Y.; Gu, Q. S.; El-Hamshary, H.; El-Newehy, M.; Mo, X. . Injectable photo crosslinked enhanced double-network hydrogels from modified sodium alginate and gelatin . Int. J. Biol. Macromol. , 2017 . 96 569 - 577 . DOI: 10.1016/j.ijbiomac.2016.12.058 http://doi.org/10.1016/j.ijbiomac.2016.12.058 .

Zhao, Y.; Ma, L.; Zeng, R.; Tu, M.; Zhao, J. . Preparation, characterization and protein sorption of photo-crosslinked cell membrane-mimicking chitosan-based hydrogels . Carbohydr. Polym. , 2016 . 151 237 - 244 . DOI: 10.1016/j.carbpol.2016.05.067 http://doi.org/10.1016/j.carbpol.2016.05.067 .

Martínez-Ruvalcaba, A.; Chornet, E.; Rodrigue, D. . Viscoelastic properties of dispersed chitosan/xanthan hydrogels . Carbohydr. Polym. , 2007 . 67 586 - 595 . DOI: 10.1016/j.carbpol.2006.06.033 http://doi.org/10.1016/j.carbpol.2006.06.033 .

Bai, H.; Sheng, K.; Zhang, P.; Li, C.; Shi, G. . Graphene oxide/conducting polymer composite hydrogels . J. Mater. Chem. , 2011 . 21 18653 - 18658 . DOI: 10.1039/c1jm13918e http://doi.org/10.1039/c1jm13918e .

Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. . Matrix elasticity directs stem cell lineage specification . Cell , 2006 . 126 677 - 689 . DOI: 10.1016/j.cell.2006.06.044 http://doi.org/10.1016/j.cell.2006.06.044 .

Bootsma, K.; Fitzgerald, M. M.; Free, B.; Dimbath, E.; Conjerti, J.; Reese, G.; Konkolewicz, D.; Berberich, J. A.; Sparks, J. L. . 3D printing of an interpenetrating network hydrogel material with tunable viscoelastic properties . J. Mech. Behav. Biomed. Mater. , 2017 . 70 84 - 94 . DOI: 10.1016/j.jmbbm.2016.07.020 http://doi.org/10.1016/j.jmbbm.2016.07.020 .

Rose, S. F.; Lewis, A. L.; Hanlon, G. W.; Lloyd, A. W. . Biological responses to cationically charged phosphorylcholine-based materials in vitro . Biomaterials , 2004 . 25 5125 - 5135 . DOI: 10.1016/j.biomaterials.2003.12.016 http://doi.org/10.1016/j.biomaterials.2003.12.016 .

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Amphiphilic Hyaluronic Acids Enhance Sanshool’s Efficacy against Skin Photodamage via Stability Improvement and Cell Cycle Regulation

Polysaccharide-based Hydrogel Formed via In situ Schiff Base Reaction with Contact Lens-like Ocular Surface Coverage for Sustained Ophthalmic Drug Delivery

Study on Hyaluronic Acid-g-lipoic acid Microsphere-based Injectable Hydrogel for Treating Early Knee Osteoarthritis

Topology-regulated Co-assembly of Single Chain Polymer Nanoparticles and Block Copolymers into Hierarchical Micelle@Vesicle Composite Structures

Silk Sericin-inspired Poly-β-homoserine for Protein Protection

Related Author

Yi Yang

Jun-Mei Song

Tian-You Wang

Shu-Wei Wu

Yu-Hang Zhou

Zhi-Peng Gu

Ling-Hong Guo

Xian Jiang

Related Institution

College of Polymer Science and Engineering, State Key Laboratory of Advanced Polymer Materials, Sichuan University

Laboratory of Dermatology, Clinical Institute of Inflammation and Immunology, Frontiers Science Center for Disease-related Molecular Network, West China Hospital

Department of Dermatology, West China Hospital, Sichuan University

Department of Polymer Science and Engineering, Zhejiang University

Shanxi Eye Hospital, Shanxi Medical University

⁰

Injectable Hyaluronic Acid/Poly(γ-glutamic acid) Hydrogel with Step-by-step Tunable Properties for Soft Tissue Engineering

DOI：10.1007/s10118-021-2558-3

摘要

Abstract

关键词

Keywords

references