Injectable Polypeptide Hydrogel as Biomimetic Scaffolds with Tunable Bioactivity and Controllable Cell Adhesion

Biomacromolecules

Volumn 18, Issue 4, 2017, Pages 1411-1418

  Xu, Qinghua ^a   Zhang, Zhen ^a,b   Xiao, Chunsheng ^a   He, Chaoliang ^a   Chen, Xuesi ^a  

^a CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOACTIVITY; BIOMIMETICS; CELL ADHESION; CELLS; COVALENT BONDS; CYTOLOGY; SCAFFOLDS (BIOLOGY);

BIOMEDICAL FIELDS; BIOMIMETIC SCAFFOLDS; CELL MATRIX INTERACTIONS; EXTRACELLULAR MATRICES; INJECTABLE HYDROGELS; MECHANICAL SUPPORT; POLY (LGLUTAMIC ACID); POLYPEPTIDE HYDROGELS;

HYDROGELS;

DISULFIDE; GLUTATHIONE; HORSERADISH PEROXIDASE; HYDROGEN PEROXIDE; POLYPEPTIDE; ARGINYL-GLYCYL-ASPARTIC ACID; BIOMIMETIC MATERIAL; CROSS LINKING REAGENT; HYDROGEL; OLIGOPEPTIDE; POLYGLUTAMIC ACID;

ARTICLE; BIOLOGICAL ACTIVITY; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CHEMICAL BOND; CROSS LINKING; EXTRACELLULAR MATRIX; GELATION; HYDROGEL; IN VITRO STUDY; MOLECULAR WEIGHT; MTT ASSAY; POLYMERIZATION; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RING OPENING; SYNTHESIS; TISSUE SCAFFOLD; ANIMAL; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; FLOW KINETICS; MOUSE; NIH 3T3 CELL LINE; PHARMACOLOGY; SURFACE PROPERTY; TISSUE ENGINEERING;

ANIMALS; BIOMIMETIC MATERIALS; CELL ADHESION; CELL PROLIFERATION; CROSS-LINKING REAGENTS; EXTRACELLULAR MATRIX; GLUTATHIONE; HYDROGELS; MICE; MOLECULAR STRUCTURE; NIH 3T3 CELLS; OLIGOPEPTIDES; POLYGLUTAMIC ACID; RHEOLOGY; SURFACE PROPERTIES; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 85017592756     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.7b00142     Document Type: Article

References (52)

1. Chaudhuri, O.; Gu, L.; Klumpers, D.; Darnell, M.; Bencherif, S. A.; Weaver, J. C.; Huebsch, N.; Lee, H.-p.; Lippens, E.; Duda, G. N.; Mooney, D. J. Hydrogels with tunable stress relaxation regulate stem cell fate and activity Nat. Mater. 2015, 15 ( 3 ) 326-334 10.1038/nmat4489
2. Lau, H. K.; Kiick, K. L. Opportunities for Multicomponent Hybrid Hydrogels in Biomedical Applications Biomacromolecules 2015, 16 ( 1 ) 28-42 10.1021/bm501361c
3. Lowe, S. B.; Tan, V. T. G.; Soeriyadi, A. H.; Davis, T. P.; Gooding, J. J. Synthesis and High-Throughput Processing of Polymeric Hydrogels for 3D Cell Culture Bioconjugate Chem. 2014, 25 ( 9 ) 1581-1601 10.1021/bc500310v
4. Tibbitt, M. W.; Anseth, K. S. Hydrogels as Extracellular Matrix Mimics for 3D Cell Culture Biotechnol. Bioeng. 2009, 103 ( 4 ) 655-663 10.1002/bit.22361
5. Seliktar, D. Designing Cell-Compatible Hydrogels for Biomedical Applications Science 2012, 336 ( 6085 ) 1124-1128 10.1126/science.1214804
6. Yesilyurt, V.; Webber, M. J.; Appel, E. A.; Godwin, C.; Langer, R.; Anderson, D. G. Injectable Self-Healing Glucose-Responsive Hydrogels with pH-Regulated Mechanical Properties Adv. Mater. 2016, 28 ( 1 ) 86-91 10.1002/adma.201502902
7. Duan, J.; Liang, X.; Guo, J.; Zhu, K.; Zhang, L. Ultra-Stretchable and Force-Sensitive Hydrogels Reinforced with Chitosan Microspheres Embedded in Polymer Networks Adv. Mater. 2016, 28 ( 36 ) 8037-8044 10.1002/adma.201602126
8. Kharkar, P. M.; Kiick, K. L.; Kloxin, A. M. Designing degradable hydrogels for orthogonal control of cell microenvironments Chem. Soc. Rev. 2013, 42 ( 17 ) 7335-7372 10.1039/C3CS60040H
9. Lim, H. L.; Hwang, Y.; Kar, M.; Varghese, S. Smart hydrogels as functional biomimetic systems Biomater. Sci. 2014, 2 ( 5 ) 603-618 10.1039/c3bm60288e
10. Tibbitt, M. W.; Rodell, C. B.; Burdick, J. A.; Anseth, K. S. Progress in material design for biomedical applications Proc. Natl. Acad. Sci. U. S. A. 2015, 112 ( 47 ) 14444-14451 10.1073/pnas.1516247112
11. Censi, R.; Di Martino, P.; Vermonden, T.; Hennink, W. E. Hydrogels for protein delivery in tissue engineering J. Controlled Release 2012, 161 ( 2 ) 680-692 10.1016/j.jconrel.2012.03.002
12. Ko, D. Y.; Shinde, U. P.; Yeon, B.; Jeong, B. Recent progress of in situ formed gels for biomedical applications Prog. Polym. Sci. 2013, 38 ( 3-4 ) 672-701 10.1016/j.progpolymsci.2012.08.002
13. Humphrey, J. D.; Dufresne, E. R.; Schwartz, M. A. Mechanotransduction and extracellular matrix homeostasis Nat. Rev. Mol. Cell Biol. 2014, 15 ( 12 ) 802-812 10.1038/nrm3896
14. Rice, J. J.; Martino, M. M.; De Laporte, L.; Tortelli, F.; Briquez, P. S.; Hubbell, J. A. Engineering the Regenerative Microenvironment with Biomaterials Adv. Healthcare Mater. 2013, 2 ( 1 ) 57-71 10.1002/adhm.201200197
15. Zhu, J.; Hu, J.; Marchant, R. E. Biomimetic hydrogels as scaffolds for tissue-engineering applications. In Biomimetic Biomaterials; Ruys, A. J., Eds; Woodhead Publishing: 2013; pp 238-275.
16. DeForest, C. A.; Tirrell, D. A. A photoreversible protein-patterning approach for guiding stem cell fate in three-dimensional gels Nat. Mater. 2015, 14 ( 5 ) 523-531 10.1038/nmat4219
17. Cosgrove, B. D.; Mui, K. L.; Driscoll, T. P.; Caliari, S. R.; Mehta, K. D.; Assoian, R. K.; Burdick, J. A.; Mauck, R. L. N-cadherin adhesive interactions modulate matrix mechanosensing and fate commitment of mesenchymal stem cells Nat. Mater. 2016, 15 ( 12 ) 1297-1306 10.1038/nmat4725
18. Liu, X.; Peng, W.; Wang, Y.; Zhu, M.; Sun, T.; Peng, Q.; Zeng, Y.; Feng, B.; Lu, X.; Weng, J.; Wang, J. Synthesis of an RGD-grafted oxidized sodium alginate-N-succinyl chitosan hydrogel and an in vitro study of endothelial and osteogenic differentiation J. Mater. Chem. B 2013, 1 ( 35 ) 4484-4492 10.1039/c3tb20552e
19. Nuttelman, C. R.; Tripodi, M. C.; Anseth, K. S. Synthetic hydrogel niches that promote hMSC viability Matrix Biol. 2005, 24 ( 3 ) 208-218 10.1016/j.matbio.2005.03.004
20. Kyburz, K. A.; Anseth, K. S. Three-dimensional hMSC motility within peptide-functionalized PEG-based hydrogels of varying adhesivity and crosslinking density Acta Biomater. 2013, 9 ( 5 ) 6381-6392 10.1016/j.actbio.2013.01.026
21. Owen, S. C.; Shoichet, M. S. Design of three-dimensional biomimetic scaffolds J. Biomed. Mater. Res., Part A 2010, 94A ( 4 ) 1321-1331 10.1002/jbm.a.32834
22. Higuchi, A.; Ling, Q.-D.; Hsu, S.-T.; Umezawa, A. Biomimetic Cell Culture Proteins as Extracellular Matrices for Stem Cell Differentiation Chem. Rev. 2012, 112 ( 8 ) 4507-4540 10.1021/cr3000169
23. Ruoslahti, E. RGD and other recognition sequences for integrins Annu. Rev. Cell Dev. Biol. 1996, 12, 697-715 10.1146/annurev.cellbio.12.1.697
24. Bellis, S. L. Advantages of RGD peptides for directing cell association with biomaterials Biomaterials 2011, 32 ( 18 ) 4205-4210 10.1016/j.biomaterials.2011.02.029
25. Lai, Y.; Xie, C.; Zhang, Z.; Lu, W.; Ding, J. Design and synthesis of a potent peptide containing both specific and non-specific cell-adhesion motifs Biomaterials 2010, 31 ( 18 ) 4809-4817 10.1016/j.biomaterials.2010.02.064
26. Hersel, U.; Dahmen, C.; Kessler, H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond Biomaterials 2003, 24 ( 24 ) 4385-4415 10.1016/S0142-9612(03)00343-0
27. Stevens, M. M.; George, J. H. Exploring and engineering the cell surface interface Science 2005, 310 ( 5751 ) 1135-1138 10.1126/science.1106587
28. Guillame-Gentil, O.; Semenov, O.; Roca, A. S.; Groth, T.; Zahn, R.; Voeroes, J.; Zenobi-Wong, M. Engineering the Extracellular Environment: Strategies for Building 2D and 3D Cellular Structures Adv. Mater. 2010, 22 ( 48 ) 5443-5462 10.1002/adma.201001747
29. Lin, L.; Marchant, R. E.; Zhu, J.; Kottke-Marchant, K. Extracellular matrix-mimetic poly(ethylene glycol) hydrogels engineered to regulate smooth muscle cell proliferation in 3-D Acta Biomater. 2014, 10 ( 12 ) 5106-5115 10.1016/j.actbio.2014.08.025
30. Wang, L.-S.; Lee, F.; Lim, J.; Du, C.; Wan, A. C. A.; Lee, S. S.; Kurisawa, M. Enzymatic conjugation of a bioactive peptide into an injectable hyaluronic acid-tyramine hydrogel system to promote the formation of functional vasculature Acta Biomater. 2014, 10 ( 6 ) 2539-2550 10.1016/j.actbio.2014.02.022
31. Lutolf, M. P.; Hubbell, J. A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering Nat. Biotechnol. 2005, 23 ( 1 ) 47-55 10.1038/nbt1055
32. Lutolf, M. P.; Gilbert, P. M.; Blau, H. M. Designing materials to direct stem-cell fate Nature 2009, 462 ( 7272 ) 433-441 10.1038/nature08602
33. Dvir, T.; Timko, B. P.; Kohane, D. S.; Langer, R. Nanotechnological strategies for engineering complex tissues Nat. Nanotechnol. 2011, 6 ( 1 ) 13-22 10.1038/nnano.2010.246
34. Sekiya, I.; Vuoristo, J. T.; Larson, B. L.; Prockop, D. J. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis Proc. Natl. Acad. Sci. U. S. A. 2002, 99 ( 7 ) 4397-4402 10.1073/pnas.052716199
35. Kloxin, A. M.; Kasko, A. M.; Salinas, C. N.; Anseth, K. S. Photodegradable Hydrogels for Dynamic Tuning of Physical and Chemical Properties Science 2009, 324 ( 5923 ) 59-63 10.1126/science.1169494
36. Burdick, J. A.; Murphy, W. L. Moving from static to dynamic complexity in hydrogel design Nat. Commun. 2012, 3, 1269 10.1038/ncomms2271
37. Petersen, S.; Alonso, J. M.; Specht, A.; Duodu, P.; Goeldner, M.; del Campo, A. Phototriggering of cell adhesion by caged cyclic RGD peptides Angew. Chem., Int. Ed. 2008, 47 ( 17 ) 3192-3195 10.1002/anie.200704857
38. Liu, D.; Xie, Y.; Shao, H.; Jiang, X. Using Azobenzene-Embedded Self-Assembled Monolayers To Photochemically Control Cell Adhesion Reversibly Angew. Chem., Int. Ed. 2009, 48 ( 24 ) 4406-4408 10.1002/anie.200901130
39. Li, W.; Wang, J.; Ren, J.; Qu, X. Endogenous signalling control of cell adhesion by using aptamer functionalized biocompatible hydrogel Chem. Sci. 2015, 6 ( 12 ) 6762-6768 10.1039/C5SC02565F
40. Mendes, P. M. Stimuli-responsive surfaces for bio-applications Chem. Soc. Rev. 2008, 37 ( 11 ) 2512-2529 10.1039/b714635n
41. Robertus, J.; Browne, W. R.; Feringa, B. L. Dynamic control over cell adhesive properties using molecular-based surface engineering strategies Chem. Soc. Rev. 2010, 39 ( 1 ) 354-378 10.1039/B906608J
42. Liu, G.-F.; Ji, W.; Wang, W.-L.; Feng, C.-L. Multiresponsive Hydrogel Coassembled from Phenylalanine and Azobenzene Derivatives as 3D Scaffolds for Photoguiding Cell Adhesion and Release ACS Appl. Mater. Interfaces 2015, 7 ( 1 ) 301-307 10.1021/am506202s
43. Xu, Q.; He, C.; Zhang, Z.; Ren, K.; Chen, X. Injectable, Biomolecule-Responsive Polypeptide Hydrogels for Cell Encapsulation and Facile Cell Recovery through Triggered Degradation ACS Appl. Mater. Interfaces 2016, 8 ( 45 ) 30692-30702 10.1021/acsami.6b08292
44. Xu, Q.; He, C.; Ren, K.; Xiao, C.; Chen, X. Thermosensitive Polypeptide Hydrogels as a Platform for ROS-Triggered Cargo Release with Innate Cytoprotective Ability under Oxidative Stress Adv. Healthcare Mater. 2016, 5 ( 15 ) 1979-1990 10.1002/adhm.201600292
45. He, C.; Zhao, C.; Guo, X.; Guo, Z.; Chen, X.; Zhuang, X.; Liu, S.; Jing, X. Novel temperature-and pH-responsive graft copolymers composed of poly(L-glutamic acid) and poly(N-isopropylacrylamide) J. Polym. Sci., Part A: Polym. Chem. 2008, 46 ( 12 ) 4140-4150 10.1002/pola.22760
46. Lelle, M.; Peneva, K. An amino acid-based heterofunctional cross-linking reagent Amino Acids 2014, 46 ( 5 ) 1243-1251 10.1007/s00726-014-1685-3
47. Lelle, M.; Frick, S. U.; Steinbrink, K.; Peneva, K. Novel cleavable cell-penetrating peptidedrug conjugates: synthesis and characterization J. Pept. Sci. 2014, 20 ( 5 ) 323-333 10.1002/psc.2617
48. Graf, N.; Bielenberg, D. R.; Kolishetti, N.; Muus, C.; Banyard, J.; Farokhzad, O. C.; Lippard, S. J. alpha(V)beta(3) Integrin-Targeted PLGA-PEG Nanoparticles for Enhanced Anti-tumor Efficacy of a Pt(IV) Prodrug ACS Nano 2012, 6 ( 5 ) 4530-4539 10.1021/nn301148e
49. Song, W.; Tang, Z.; Zhang, D.; Zhang, Y.; Yu, H.; Li, M.; Lv, S.; Sun, H.; Deng, M.; Chen, X. Anti-tumor efficacy of c(RGDfK)-decorated polypeptide-based micelles co-loaded with docetaxel and cisplatin Biomaterials 2014, 35 ( 9 ) 3005-3014 10.1016/j.biomaterials.2013.12.018
50. Pek, Y. S.; Wan, A. C. A.; Ying, J. Y. The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel Biomaterials 2010, 31 ( 3 ) 385-391 10.1016/j.biomaterials.2009.09.057
51. Ehrbar, M.; Sala, A.; Lienemann, P.; Ranga, A.; Mosiewicz, K.; Bittermann, A.; Rizzi, S. C.; Weber, F. E.; Lutolf, M. P. Elucidating the Role of Matrix Stiffness in 3D Cell Migration and Remodeling Biophys. J. 2011, 100 ( 2 ) 284-293 10.1016/j.bpj.2010.11.082
52. Salinas, C. N.; Anseth, K. S. The influence of the RGD peptide motif and its contextual presentation in PEG gels on human mesenchymal stem cell viability J. Tissue Eng. Regener. Med. 2008, 2 ( 5 ) 296-304 10.1002/term.95