Hydrogel Formulation for Biomimetic Fibroblast Cell Culture: Exploring Effects of External Stresses and Cellular Responses

bioscaffolds; fibroblast; gravity-related stress; hydrogels; mechanical stress; parabolic flight; tissue engineering; alginic acid; biomimetic material; hydrogel; macrogol derivative; poly(ethylene glycol)diacrylate; unclassified drug; adaptation; altered gravity; Article; biocompatibility; biomechanics; biomimetics; cell aggregation; cell function; cell stress; cell structure; cell viability; controlled study; fibroblast culture; human; human cell; microgravity; porosity; scanning electron microscopy; space; tissue regeneration; Young modulus; animal; cell culture technique; chemistry; cytology; drug effect; metabolism; mouse; procedures; tissue scaffold; Animals; Biomimetic Materials; Biomimetics; Cell Culture Techniques; Fibroblasts; Humans; Hydrogels; Mice; Stress, Mechanical; Tissue Engineering; Tissue Scaffolds

Abstract :

[en] In the process of tissue engineering, several types of stresses can influence the outcome of tissue regeneration. This outcome can be understood by designing hydrogels that mimic this process and studying how such hydrogel scaffolds and cells behave under a set of stresses. Here, a hydrogel formulation is proposed to create biomimetic scaffolds suitable for fibroblast cell culture. Subsequently, we examine the impact of external stresses on fibroblast cells cultured on both solid and porous hydrogels. These stresses included mechanical tension and altered-gravity conditions experienced during the 83rd parabolic flight campaign conducted by the European Space Agency. This study shows distinct cellular responses characterized by cell aggregation and redistribution in regions of intensified stress concentration. This paper presents a new biomimetic hydrogel that fulfills tissue-engineering requirements in terms of biocompatibility and mechanical stability. Moreover, it contributes to our comprehension of cellular biomechanics under diverse gravitational conditions, shedding light on the dynamic cellular adaptations versus varying stress environments. © 2024 by the authors.

Disciplines :

Materials science & engineering

Author, co-author :

Greco, I.

Machrafi, Hatim ; Université de Liège - ULiège > Département d'astrophysique, géophysique et océanographie (AGO) > Thermodynamique des phénomènes irréversibles

Minetti, C.

Risaliti, C.

Bandini, A.

Cialdai, F.

Monici, M.

Iorio, C.S.

Language :

English

Title :

Hydrogel Formulation for Biomimetic Fibroblast Cell Culture: Exploring Effects of External Stresses and Cellular Responses

Publication date :

2024

Journal title :

International Journal of Molecular Sciences

ISSN :

1661-6596

eISSN :

1422-0067

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.scopus.com/inward/record.uri?eid=2-s2.0-85195827011&doi=10.3390%2fijms25115600&partnerID=40&md5=14bc00891a199e5378380ccf7d86d8e8

Available on ORBi :

since 29 November 2024

Statistics

Number of views

16 (0 by ULiège)

Number of downloads

5 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

publications

supporting

mentioning

contrasting

Smart Citations

Citing PublicationsSupportingMentioningContrasting

View Citations

See how this article has been cited at scite.ai

scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.

Bibliography

Griffith L.G. Naughton G. Tissue Engineering-Current Challenges and Expanding Opportunities Science 2002 295 1009 1014 10.1126/science.1069210 11834815
Chapekar M.S. Tissue Engineering: Challenges and Opportunities J. Biomed. Mater. Res. 2000 53 617 620 10.1002/1097-4636(2000)53:6<617::AID-JBM1>3.0.CO;2-C
El-Sherbiny I.M. Yacoub M.H. Hydrogel scaffolds for tissue engineering: Progress and challenges Glob. Cardiol. Sci. Pract. 2013 2013 38 10.5339/gcsp.2013.38
Drury J.L. Mooney D.J. Hydrogels for tissue engineering: Scaffold design variables and applications Biomaterials 2003 24 4337 4351 10.1016/S0142-9612(03)00340-5 12922147
Pegg D.E. Viability assays for preserved cells, tissues, and organs Cryobiology 1989 26 212 231 10.1016/0011-2240(89)90016-3
Lee K.Y. Mooney D.J. Hydrogels for tissue engineering Chem. Rev. 2001 101 1869 1879 10.1021/cr000108x
Bizzarri M. Monici M. van Loon J.J.W.A. How microgravity affects the biology of living systems Biomed. Res. Int. 2015 2015 863075 10.1155/2015/863075 25667927
Burki T. The final frontier: Health in space Lancet [Internet] 2021 398 199 200 Available online: http://www.thelancet.com/article/S0140673621016445/fulltext (accessed on 13 September 2023) 10.1016/S0140-6736(21)01644-5
Freed L.E. Langer R. Martin I. Pellis N.R. Vunjak-Novakovic G. Tissue engineering of cartilage in space Proc. Natl. Acad. Sci. USA 1997 94 13885 13890 10.1073/pnas.94.25.13885
Babensee J.E. McIntire L.V. Mikos A.G. Growth factor delivery for tissue engineering Pharm. Res. [Internet] 2000 17 497 504 Available online: https://link.springer.com/article/10.1023/A:1007502828372 (accessed on 31 January 2023) 10.1023/A:1007502828372
Whitaker M.J. Quirk R.A. Howdle S.M. Shakesheff K.M. Growth factor release from tissue engineering scaffolds J. Pharm. Pharmacol. [Internet] 2001 53 1427 1437 Available online: https://onlinelibrary.wiley.com/doi/full/10.1211/0022357011777963 (accessed on 31 January 2023) 10.1211/0022357011777963 11732745
Sakiyama-Elbert S.E. Hubbell J.A. Functional Biomaterials: Design of Novel Biomaterials Annu. Rev. Mater. Res. 2001 31 183 201 10.1146/annurev.matsci.31.1.183
Zhu J. Marchant R.E. Design properties of hydrogel tissue engineering scaffolds Expert. Rev. Med. Devices 2011 8 607 626 10.1586/erd.11.27 22026626
Maitra J. Kumar Shukla V. Hydrogels, Cross linking, Gel, Polymer; Hydrogels, Cross linking, Gel, Polymer Am. J. Polym. Sci. [Internet] 2014 2014 25 31 Available online: http://journal.sapub.org/ajps (accessed on 16 May 2024)
Song S.J. Choi J. Park Y.D. Hong S. Lee J.J. Ahn C.B. Choi H. Sun K. Sodium Alginate Hydrogel-Based Bioprinting Using a Novel Multinozzle Bioprinting System Artif. Organs. 2011 35 1132 1136 10.1111/j.1525-1594.2011.01377.x 22097985
Eshel-Green T. Eliyahu S. Avidan-Shlomovich S. Bianco-Peled H. PEGDA hydrogels as a replacement for animal tissues in mucoadhesion testing Int. J. Pharm. 2016 506 25 34 10.1016/j.ijpharm.2016.04.019 27084292
Sun J. Tan H. Alginate-based biomaterials for regenerative medicine applications Materials 2013 6 1285 1309 10.3390/ma6041285 28809210
Tu X. Wang L. Wei J. Wang B. Tang Y. Shi J. Zhang Z. Chen Y. 3D printed PEGDA microstructures for gelatin scaffold integration and neuron differentiation Microelectron. Eng. 2016 158 30 34 10.1016/j.mee.2016.03.007
Laftah W.A. Hashim S. Ibrahim A.N. Polymer hydrogels: A review Polym. Plast. Technol. Eng. 2011 50 1475 1486 10.1080/03602559.2011.593082
Einerson N.J. Stevens K.R. Kao W.J. Synthesis and physicochemical analysis of gelatin-based hydrogels for drug carrier matrices Biomaterials 2003 24 509 523 10.1016/S0142-9612(02)00369-1
Orive G. Tam S.K. Pedraz J.L. Hallé J.P. Biocompatibility of alginate–poly-l-lysine microcapsules for cell therapy Biomaterials 2006 27 3691 3700 10.1016/j.biomaterials.2006.02.048 16574222
Black J. Biological Performance of Materials: Fundamentals of Biocompatibility 4th ed. CRC Press Boca Raton, FL, USA 2005 Available online: https://www.taylorfrancis.com/books/mono/10.1201/9781420057843/biological-performance-materials-jonathan-black-jonathan-black (accessed on 25 January 2023)
Greco I. Miskovic V. Varon C. Marraffa C. Iorio C.S. Printability of Double Network Alginate-Based Hydrogel for 3D Bio-Printed Complex Structures Front. Bioeng. Biotechnol. 2022 10 896166 10.3389/fbioe.2022.896166
Mechanical Stress Influences the Viability and Morphology of Human Parametrial Ligament Fibroblasts [Internet] Available online: https://www.spandidos-publications.com/10.3892/mmr.2016.6052 (accessed on 16 April 2024)
Boccafoschi F. Bosetti M. Gatti S. Cannas M. Dynamic fibroblast cultures: Response to mechanical stretching Cell Adh. Migr. [Internet] 2007 1 124 128 Available online: https://www.tandfonline.com/action/journalInformation?journalCode=kcam20 (accessed on 15 April 2024) 10.4161/cam.1.3.5144 19262127
Cialdai F. Vignali L. Morbidelli L. Colciago A. Celotti F. Santi A. Caselli A. Cirri P. Monici M. Modeled Microgravity Affects Fibroblast Functions Related to Wound Healing Microgravity Sci. Technol. 2017 29 121 132 Available online: http://synthecon.com/pages/rotary (accessed on 10 January 2024) 10.1007/s12217-016-9532-7
Pletser V. Rouquette S. Friedrich U. Clervoy J.F. Gharib T. Gai F. Mora C. The First European Parabolic Flight Campaign with the Airbus A310 ZERO-G Microgravity Sci. Technol. 2016 28 587 601 Available online: https://link.springer.com/article/10.1007/s12217-016-9515-8 (accessed on 1 March 2024) 10.1007/s12217-016-9515-8
Fedeli V. Cucina A. Dinicola S. Fabrizi G. Catizone A. Gesualdi L. Ceccarelli S. Harrath A.H. Alwasel S.H. Ricci G. et al. Microgravity Modifies the Phenotype of Fibroblast and Promotes Remodeling of the Fibroblast–Keratinocyte Interaction in a 3D Co-Culture Model Int. J. Mol. Sci. 2022 23 2163 10.3390/ijms23042163
Ulbrich C. Westphal K. Baatout S. Wehland M. Bauer J. Flick B. Infanger M. Kreutz R. Vadrucci S. Egli M. et al. Effects of Basic Fibroblast Growth Factor on Endothelial Cells Under Conditions of Simulated Microgravity J. Cell Biochem. [Internet] 2008 104 1324 1341 Available online: https://onlinelibrary.wiley.com/doi/10.1002/jcb.21710 (accessed on 10 January 2024) 10.1002/jcb.21710 18253936
Wang Y. Ma M. Wang J. Zhang W. Lu W. Gao Y. Zhang B. Guo Y. Development of a photo-crosslinking, biodegradable GelMA/PEGDA hydrogel for guided bone regeneration materials Materials 2018 11 1345 10.3390/ma11081345 30081450
Liu Y.M. Ma G.S. Zhang D.H. Zhao D.W. Upper bound analysis of rolling force and dog-bone shape via sine function model in vertical rolling J. Mater. Process Technol. 2015 223 91 97 10.1016/j.jmatprotec.2015.03.051
Wang H.Y. Zhao D.W. Zhang D.H. Analysis of Vertical Rolling Force with GM Yield Criterion and Anti-Symmetric Parabola Dog-Bone Shapes Appl. Mech. Mater. 2015 775 34 38 10.4028/www.scientific.net/AMM.775.34
Buken C. Sahana J. Corydon T.J. Melnik D. Bauer J. Wehland M. Krüger M. Balk S. Abuagela N. Infanger M. et al. Morphological and Molecular Changes in Juvenile Normal Human Fibroblasts Exposed to Simulated Microgravity Sci. Rep. 2019 9 11882 10.1038/s41598-019-48378-9
Sherratt M.J. Tissue elasticity and the ageing elastic fibre AGE 2009 31 305 325 10.1007/s11357-009-9103-6 19588272
Ratcliffe A. Tissue engineering of vascular grafts Matrix Biol. 2000 19 353357 10.1016/S0945-053X(00)00080-9
Greco I. Varon C. Iorio C.S. Synthesis and Characterization of a new Alginate-Gelatine Aerogel for Tissue Engineering Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBS Glasgow, UK 11–15 July 2022 Volume 2022 3915 3918
Bonvallet P.P. Culpepper B.K. Bain J.L. Schultz M.J. Thomas S.J. Bellis S.L. Microporous dermal-like electrospun scaffolds promote accelerated skin regeneration Tissue Eng. Part. A 2014 20 2434 2444 10.1089/ten.tea.2013.0645
Giuseppe M.D. Law N. Webb B. AMacrae R. Liew L.J. Sercombe T.B. Dilley R.J. Doyle B.J. Mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting J. Mech. Behav. Biomed. Mater. 2018 79 150 157 10.1016/j.jmbbm.2017.12.018 29304429
Fischer F.G. Dörfel H. Die Polyuronsäuren der Braunalgen (Kohlenhydrate der Algen I) Hoppe Seylers Z. Physiol. Chem. [Internet] 1955 302 186 203 Available online: https://www.degruyter.com/document/doi/10.1515/bchm2.1955.302.1-2.186/html (accessed on 11 March 2024) 10.1515/bchm2.1955.302.1-2.186 13331440
Gacesa P. Enzymic degradation of alginates Int. J. Biochem. 1992 24 545 552 10.1016/0020-711X(92)90325-U 1516726
Lee K.Y. Mooney D.J. Alginate: Properties and biomedical applications Prog. Polym. Sci. 2012 37 106 126 10.1016/j.progpolymsci.2011.06.003 22125349
Xu Q. Pang M. Zhu L. Zhang Y. Feng S. Mechanical properties of silicone rubber composed of diverse vinyl content silicone gums blending Mater. Des. 2010 31 4083 4087 10.1016/j.matdes.2010.04.052
Nassef M.Z. Kopp S. Wehland M. Melnik D. Sahana J. Krüger M. Corydon T.J. Oltmann H. Schmitz B. Schütte A. et al. Real microgravity influences the cytoskeleton and focal adhesions in human breast cancer cells Int. J. Mol. Sci. 2019 20 3156 10.3390/ijms20133156
Vunjak-Novakovic G. Dynamic Hydrogels for Investigating Vascularization Cell Stem Cell [Internet] 2020 27 697 698 10.1016/j.stem.2020.10.009 33157044
Ulbrich C. Wehland M. Pietsch J. Aleshcheva G. Wise P. Van Loon J. Magnusson N. Infanger M. Grosse J. Eilles C. et al. The impact of simulated and real microgravity on bone cells and mesenchymal stem cells Biomed. Res. Int. 2014 2014 928507 10.1155/2014/928507 25110709
Freed L.E. Vunjak-Novakovic G. Microgravity tissue engineering In Vitro Cell Dev. Biol. 1997 133 381 385 10.1007/s11626-997-0009-2 9196897

Name	Provider / Domaine	Expiration	Description
JSESSIONID	Oracle Corporation www.uliege.be	Session	General purpose platform session cookie, used by sites written in JSP. Usually used to maintain an anonymous user session by the server.
CookieScriptConsent	CookieScript .uliege.be	1 year	This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.

Name	Provider / Domaine	Expiration	Description
_pk_id	InnoCraft Ltd .uliege.be	1 year	Used to store a few details about the user such as the unique visitor ID
_pk_ses	InnoCraft Ltd .uliege.be	30 minutes	Short lived cookies used to temporarily store data for the visit
_pk_ref	InnoCraft Ltd .uliege.be	6 months	Used to store the attribution information, the referrer initially used to visit the website