Hydrogel Formation with Enzyme-Responsive Cyclic Peptides.

Enzyme-responsive Hydrogels Injectable Macrocycles Minimally invasive Proteolytic cleavage Self-assembling peptides Steric constraint Tissue engineering

Journal

Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969

Informations de publication

Date de publication:
2022
Historique:
entrez: 1 10 2021
pubmed: 2 10 2021
medline: 6 1 2022
Statut: ppublish

Résumé

Self-assembling peptides (SAPs), which form hydrogels through physical cross-linking of soluble structures, are an intriguing class of materials that have been applied as tissue engineering scaffolds and drug delivery vehicles. For feasible application of these tissue mimetics via minimally invasive delivery, their bulk mechanical properties must be compatible with current delivery strategies. However, injectable SAPs which possess shear-thinning capacity, as well as the ability to reassemble after cessation of shearing can be technically challenging to generate. Many SAPs either clog the high-gauge needle/catheter at high concentration during delivery or are incapable of reassembly following delivery. In this chapter, we provide a detailed protocol for topological control of enzyme-responsive peptide-based hydrogels that enable the user to access both advantages. These materials are formulated as sterically constrained cyclic peptide progelators to temporarily disrupt self-assembly during injection-based delivery, which avoids issues with clogging of needles and catheters as well as nearby vasculature. Proteolytic cleavage by enzymes produced at the target tissue induces progelator linearization and hydrogelation. The scope of this approach is demonstrated by their ability to flow through a catheter without clogging and activated gelation upon exposure to target enzymes.

Identifiants

pubmed: 34596862
doi: 10.1007/978-1-0716-1689-5_23
doi:

Substances chimiques

Hydrogels 0
Peptides, Cyclic 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

427-448

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL139001
Pays : United States

Informations de copyright

© 2022. Springer Science+Business Media, LLC, part of Springer Nature.

Références

Seif-Naraghi SB, Singelyn JM, Salvatore MA, Osborn KG, Wang JJ, Sampat U, Kwan OL, Strachan GM, Wong J, Schup-Magoffin PJ, Braden RL, Bartels K, DeQuach JA, Preul M, Kinsey AM, DeMaria AN, Dib N, Christman KL (2013) Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med 5(173). https://doi.org/10.1126/scitranslmed.3005503
Yu J, Gu Y, Du KT, Mihardja S, Sievers RE, Lee RJ (2009) The effect of injected RGD modified alginate on angiogenesis and left ventricular function in a chronic rat infarct model. Biomaterials 30(5):751–756. https://doi.org/10.1016/j.biomaterials.2008.09.059
doi: 10.1016/j.biomaterials.2008.09.059 pubmed: 19010528
Dorsey SM, McGarvey JR, Wang H, Nikou A, Arama L, Koomalsingh KJ, Kondo N, Gorman JH 3rd, Pilla JJ, Gorman RC, Wenk JF, Burdick JA (2015) MRI evaluation of injectable hyaluronic acid-based hydrogel therapy to limit ventricular remodeling after myocardial infarction. Biomaterials 69:65–75. https://doi.org/10.1016/j.biomaterials.2015.08.011
doi: 10.1016/j.biomaterials.2015.08.011 pubmed: 26280951 pmcid: 4556569
Lee AS, Inayathullah M, Lijkwan MA, Zhao X, Sun W, Park S, Hong WX, Parekh MB, Malkovskiy AV, Lau E, Qin X, Pothineni VR, Sanchez-Freire V, Zhang WY, Kooreman NG, Ebert AD, Chan CKF, Nguyen PK, Rajadas J, Wu JC (2018) Prolonged survival of transplanted stem cells after ischaemic injury via the slow release of pro-survival peptides from a collagen matrix. Nat Biomed Eng 2(2):104–113. https://doi.org/10.1038/s41551-018-0191-4
doi: 10.1038/s41551-018-0191-4 pubmed: 29721363 pmcid: 5927627
Losi P, Briganti E, Magera A, Spiller D, Ristori C, Battolla B, Balderi M, Kull S, Balbarini A, Di Stefano R, Soldani G (2010) Tissue response to poly(ether)urethane-polydimethylsiloxane-fibrin composite scaffolds for controlled delivery of pro-angiogenic growth factors. Biomaterials 31(20):5336–5344. https://doi.org/10.1016/j.biomaterials.2010.03.033
doi: 10.1016/j.biomaterials.2010.03.033 pubmed: 20381861
Prokoph S, Chavakis E, Levental KR, Zieris A, Freudenberg U, Dimmeler S, Werner C (2012) Sustained delivery of SDF-1α from heparin-based hydrogels to attract circulating pro-angiogenic cells. Biomaterials 33(19):4792–4800. https://doi.org/10.1016/j.biomaterials.2012.03.039
doi: 10.1016/j.biomaterials.2012.03.039 pubmed: 22483246
Layman H, Spiga MG, Brooks T, Pham S, Webster KA, Andreopoulos FM (2007) The effect of the controlled release of basic fibroblast growth factor from ionic gelatin-based hydrogels on angiogenesis in a murine critical limb ischemic model. Biomaterials 28(16):2646–2654. https://doi.org/10.1016/j.biomaterials.2007.01.044
doi: 10.1016/j.biomaterials.2007.01.044 pubmed: 17320947 pmcid: 1945227
Fujimoto KL, Ma Z, Nelson DM, Hashizume R, Guan J, Tobita K, Wagner WR (2009) Synthesis, characterization and therapeutic efficacy of a biodegradable, thermoresponsive hydrogel designed for application in chronic infarcted myocardium. Biomaterials 30(26):4357–4368. https://doi.org/10.1016/j.biomaterials.2009.04.055
doi: 10.1016/j.biomaterials.2009.04.055 pubmed: 19487021 pmcid: 2860787
Bastings MM, Koudstaal S, Kieltyka RE, Nakano Y, Pape AC, Feyen DA, van Slochteren FJ, Doevendans PA, Sluijter JP, Meijer EW, Chamuleau SA, Dankers PY (2014) A fast pH-switchable and self-healing supramolecular hydrogel carrier for guided, local catheter injection in the infarcted myocardium. Adv Healthc Mater 3(1):70–78. https://doi.org/10.1002/adhm.201300076
doi: 10.1002/adhm.201300076 pubmed: 23788397
Wang H, Zhang X, Li Y, Ma Y, Zhang Y, Liu Z, Zhou J, Lin Q, Wang Y, Duan C, Wang C (2010) Improved myocardial performance in infarcted rat heart by co-injection of basic fibroblast growth factor with temperature-responsive chitosan hydrogel. J Heart Lung Transplant 29(8):881–887. https://doi.org/10.1016/j.healun.2010.03.016
doi: 10.1016/j.healun.2010.03.016 pubmed: 20466563
Formiga FR, Pelacho B, Garbayo E, Imbuluzqueta I, Díaz-Herráez P, Abizanda G, Gavira JJ, Simón-Yarza T, Albiasu E, Tamayo E, Prósper F, Blanco-Prieto MJ (2014) Controlled delivery of fibroblast growth factor-1 and neuregulin-1 from biodegradable microparticles promotes cardiac repair in a rat myocardial infarction model through activation of endogenous regeneration. J Control Release 173:132–139. https://doi.org/10.1016/j.jconrel.2013.10.034
doi: 10.1016/j.jconrel.2013.10.034 pubmed: 24200746
Suarez SL, Muñoz A, Mitchell A, Braden RL, Luo C, Cochran JR, Almutairi A, Christman KL (2016) Degradable acetalated dextran microparticles for tunable release of an engineered hepatocyte growth factor fragment. ACS Biomater Sci Eng 2(2):197–204. https://doi.org/10.1021/acsbiomaterials.5b00335
doi: 10.1021/acsbiomaterials.5b00335 pubmed: 29333489
Ungerleider JL, Christman KL (2014) Concise review: injectable biomaterials for the treatment of myocardial infarction and peripheral artery disease: translational challenges and progress. Stem Cells Transl Med 3(9):1090–1099. https://doi.org/10.5966/sctm.2014-0049
doi: 10.5966/sctm.2014-0049 pubmed: 25015641 pmcid: 4149304
Hernandez MJ, Christman KL (2017) Designing acellular injectable biomaterial therapeutics for treating myocardial infarction and peripheral artery disease. JACC Basic Transl Sci 2(2):212–226. https://doi.org/10.1016/j.jacbts.2016.11.008
doi: 10.1016/j.jacbts.2016.11.008 pubmed: 29057375 pmcid: 5646282
Portnov T, Shulimzon Tiberiu R, Zilberman M (2017) Injectable hydrogel-based scaffolds for tissue engineering applications. Rev Chem Eng 33. https://doi.org/10.1515/revce-2015-0074
Zhu J, Marchant RE (2011) Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devices 8(5):607–626. https://doi.org/10.1586/erd.11.27
doi: 10.1586/erd.11.27 pubmed: 22026626 pmcid: 3206299
Carlini AS, Adamiak L, Gianneschi NC (2016) Biosynthetic polymers as functional materials. Macromolecules 49(12):4379–4394. https://doi.org/10.1021/acs.macromol.6b00439
doi: 10.1021/acs.macromol.6b00439 pubmed: 27375299 pmcid: 4928144
Chen MH, Wang LL, Chung JJ, Kim Y-H, Atluri P, Burdick JA (2017) Methods to assess shear-thinning hydrogels for application as injectable biomaterials. ACS Biomater Sci Eng 3(12):3146–3160. https://doi.org/10.1021/acsbiomaterials.7b00734
doi: 10.1021/acsbiomaterials.7b00734 pubmed: 29250593 pmcid: 5727472
Yan C, Altunbas A, Yucel T, Nagarkar RP, Schneider JP, Pochan DJ (2010) Injectable solid hydrogel: mechanism of shear-thinning and immediate recovery of injectable β-hairpin peptide hydrogels. Soft Matter 6(20):5143–5156. https://doi.org/10.1039/C0SM00642D
doi: 10.1039/C0SM00642D pubmed: 21566690 pmcid: 3091287
Yuan X, He B, Lv Z, Luo S (2014) Fabrication of self-assembling peptide nanofiber hydrogels for myocardial repair. RSC Adv 4(96):53801–53811. https://doi.org/10.1039/C4RA08582E
doi: 10.1039/C4RA08582E
Ravichandran R, Venugopal JR, Sundarrajan S, Mukherjee S, Ramakrishna S (2012) Minimally invasive cell-seeded biomaterial systems for injectable/epicardial implantation in ischemic heart disease. Int J Nanomedicine 7:5969–5994. https://doi.org/10.2147/IJN.S37575
doi: 10.2147/IJN.S37575 pubmed: 23271906 pmcid: 3526148
Sieminski AL, Semino CE, Gong H, Kamm RD (2008) Primary sequence of ionic self-assembling peptide gels affects endothelial cell adhesion and capillary morphogenesis. J Biomed Mater Res A 87A(2):494–504. https://doi.org/10.1002/jbm.a.31785
doi: 10.1002/jbm.a.31785
Johnson TD, DeQuach JA, Gaetani R, Ungerleider J, Elhag D, Nigam V, Behfar A, Christman KL (2014) Human versus porcine tissue sourcing for an injectable myocardial matrix hydrogel. Biomater Sci 2014:60283D. https://doi.org/10.1039/C3BM60283D
doi: 10.1039/C3BM60283D pubmed: 24634775 pmcid: 3950205
Firth A, Aggeli A, Burke JL, Yang X, Kirkham J (2006) Biomimetic self-assembling peptides as injectable scaffolds for hard tissue engineering. Nanomedicine 1(2):189–199. https://doi.org/10.2217/17435889.1.2.189
doi: 10.2217/17435889.1.2.189 pubmed: 17716108
Sun J, Zheng Q, Wu Y, Liu Y, Guo X, Wu W (2010) Biocompatibility of KLD-12 peptide hydrogel as a scaffold in tissue engineering of intervertebral discs in rabbits. J Huazhong Univ Sci Technolog Med Sci 30(2):173–177
doi: 10.1007/s11596-010-0208-z
Tripathi JK, Pal S, Awasthi B, Kumar A, Tandon A, Mitra K, Chattopadhyay N, Ghosh JK (2015) Variants of self-assembling peptide, KLD-12 that show both rapid fracture healing and antimicrobial properties. Biomaterials 56:92–103. https://doi.org/10.1016/j.biomaterials.2015.03.046
doi: 10.1016/j.biomaterials.2015.03.046 pubmed: 25934283
Carlini AS, Gaetani R, Braden RL, Luo C, Christman KL, Gianneschi NC (2019) Enzyme-responsive progelator cyclic peptides for minimally invasive delivery to the heart post-myocardial infarction. Nat Commun 10(1):1735. https://doi.org/10.1038/s41467-019-09587-y
doi: 10.1038/s41467-019-09587-y pubmed: 30988291 pmcid: 6465301
Carlini AS, Touve MA, Fernández-Caro H, Thompson MP, Cassidy MF, Cao W, Gianneschi NC (2019) UV-responsive cyclic peptide progelator bioinks. Faraday Discuss 219:44–57. https://doi.org/10.1039/C9FD00026G
doi: 10.1039/C9FD00026G pubmed: 31549115 pmcid: 7363176
Bowerman CJ, Nilsson BL (2010) A reductive trigger for peptide self-assembly and hydrogelation. J Am Chem Soc 132(28):9526–9527. https://doi.org/10.1021/ja1025535
doi: 10.1021/ja1025535 pubmed: 20405940
Burke HM, McSweeney L, Scanlan EM (2017) Exploring chemoselective S-to-N acyl transfer reactions in synthesis and chemical biology. Nat Commun 8(1):15655. https://doi.org/10.1038/ncomms15655
doi: 10.1038/ncomms15655 pubmed: 28537277 pmcid: 5458133
Paradís-Bas M, Tulla-Puche J, Albericio F (2016) The road to the synthesis of “difficult peptides”. Chem Soc Rev 45(3):631–654. https://doi.org/10.1039/C5CS00680E
doi: 10.1039/C5CS00680E pubmed: 26612670
Yu H, Xiao Y, Guo H (2012) From spirolactam mixtures to regioisomerically pure 5- and 6-rhodamines: a chemodosimeter-inspired strategy. Org Lett 14(8):2014–2017. https://doi.org/10.1021/ol300523m
doi: 10.1021/ol300523m pubmed: 22471975
Reddy KMB, Kumari YB, Mallikharjunasarma D, Bulliraju K, Sreelatha V, Ananda K (2012) Large scale solid phase synthesis of peptide drugs: use of commercial anion exchange resin as quenching agent for removal of iodine during disulphide bond formation. Int J Pept 2012:323907–323907. https://doi.org/10.1155/2012/323907
doi: 10.1155/2012/323907 pubmed: 23118772 pmcid: 3478740

Auteurs

Andrea S Carlini (AS)

Department of Chemistry, Chemistry of Life Processes Institute, Northwestern University, Evanston, IL, USA.
Department of Materials Science & Engineering, Northwestern University, Evanston, IL, USA.
Department of Biomedical Engineering, Northwestern University, Evanston, IL, USA.
Department of Pharmacology, Northwestern University, Evanston, IL, USA.
International Institute for Nanotechnology, Northwestern University, Evanston, IL, USA.
Simpson Querrey Institute, Northwestern University, Evanston, IL, USA.

Mary F Cassidy (MF)

Department of Chemistry, Chemistry of Life Processes Institute, Northwestern University, Evanston, IL, USA.
Department of Materials Science & Engineering, Northwestern University, Evanston, IL, USA.
Department of Biomedical Engineering, Northwestern University, Evanston, IL, USA.
Department of Pharmacology, Northwestern University, Evanston, IL, USA.
International Institute for Nanotechnology, Northwestern University, Evanston, IL, USA.
Simpson Querrey Institute, Northwestern University, Evanston, IL, USA.

Nathan C Gianneschi (NC)

Department of Chemistry, Chemistry of Life Processes Institute, Northwestern University, Evanston, IL, USA. nathan.gianneschi@northwestern.edu.
Department of Materials Science & Engineering, Northwestern University, Evanston, IL, USA. nathan.gianneschi@northwestern.edu.
Department of Biomedical Engineering, Northwestern University, Evanston, IL, USA. nathan.gianneschi@northwestern.edu.
Department of Pharmacology, Northwestern University, Evanston, IL, USA. nathan.gianneschi@northwestern.edu.
International Institute for Nanotechnology, Northwestern University, Evanston, IL, USA. nathan.gianneschi@northwestern.edu.
Simpson Querrey Institute, Northwestern University, Evanston, IL, USA. nathan.gianneschi@northwestern.edu.

Articles similaires

Organoids Humans Tissue Engineering Coculture Techniques Regenerative Medicine
Animals Osteogenesis Osteoporosis Mesenchymal Stem Cells Humans
Organoids Animals Kidney Mice Humans

Classifications MeSH