Seaweed cellulose scaffolds derived from green macroalgae for tissue engineering.
Animals
Biocompatible Materials
/ chemistry
Cell Differentiation
Cell Proliferation
Cellulose
/ chemistry
Chlorophyta
/ metabolism
DNA
/ analysis
Ecology
Extracellular Matrix
/ metabolism
Fibroblasts
/ drug effects
Mice
Microscopy, Electron, Scanning
NIH 3T3 Cells
Oxazines
Porosity
Seaweed
Tissue Engineering
/ methods
Tissue Scaffolds
/ chemistry
Ulva
/ metabolism
Xanthenes
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
04 06 2021
04 06 2021
Historique:
received:
04
12
2020
accepted:
17
05
2021
entrez:
5
6
2021
pubmed:
6
6
2021
medline:
16
11
2021
Statut:
epublish
Résumé
Extracellular matrix (ECM) provides structural support for cell growth, attachments and proliferation, which greatly impact cell fate. Marine macroalgae species Ulva sp. and Cladophora sp. were selected for their structural variations, porous and fibrous respectively, and evaluated as alternative ECM candidates. Decellularization-recellularization approach was used to fabricate seaweed cellulose-based scaffolds for in-vitro mammalian cell growth. Both scaffolds were confirmed nontoxic to fibroblasts, indicated by high viability for up to 40 days in culture. Each seaweed cellulose structure demonstrated distinct impact on cell behavior and proliferation rates. The Cladophora sp. scaffold promoted elongated cells spreading along its fibers' axis, and a gradual linear cell growth, while the Ulva sp. porous surface, facilitated rapid cell growth in all directions, reaching saturation at week 3. As such, seaweed-cellulose is an environmentally, biocompatible novel biomaterial, with structural variations that hold a great potential for diverse biomedical applications, while promoting aquaculture and ecological agenda.
Identifiants
pubmed: 34088909
doi: 10.1038/s41598-021-90903-2
pii: 10.1038/s41598-021-90903-2
pmc: PMC8178384
doi:
Substances chimiques
Biocompatible Materials
0
Oxazines
0
Xanthenes
0
resazurin
1FN9YD6968
Cellulose
9004-34-6
DNA
9007-49-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11843Références
Ratner, B. D., Hoffman, A. S., Schoen, F. J. & Lemons, J. E. Biomaterials Science: An Introduction to Materials in Medicine (Elsevier, 2013).
Lanza, R., Langer, R. & Vacanti, J. Principles of Tissue Engineering (Academic Press, 2020).
Hickey, R. J. & Pelling, A. E. Cellulose biomaterials for tissue engineering. Front. Bioeng. Biotechnol. https://doi.org/10.3389/fbioe.2019.00045 (2019).
doi: 10.3389/fbioe.2019.00045
pubmed: 30968018
pmcid: 6438900
Klemm, D., Heublein, B., Fink, H.-P. & Bohn, A. Cellulose: Fascinating biopolymer and sustainable raw material. Angew. Chemie Int. Ed. 44, 3358–3393 (2005).
doi: 10.1002/anie.200460587
Gibson, L. J. The hierarchical structure and mechanics of plant materials. J. R. Soc. Interface 9, 2749–2766 (2012).
pubmed: 22874093
pmcid: 3479918
doi: 10.1098/rsif.2012.0341
Mihranyan, A., Llagostera, A. P., Karmhag, R., Strømme, M. & Ek, R. Moisture sorption by cellulose powders of varying crystallinity. Int. J. Pharm. 269, 433–442 (2004).
pubmed: 14706254
doi: 10.1016/j.ijpharm.2003.09.030
Modulevsky, D. J., Lefebvre, C., Haase, K., Al-Rekabi, Z. & Pelling, A. E. Apple derived cellulose scaffolds for 3D mammalian cell culture. PLoS ONE 9, 97835 (2014).
doi: 10.1371/journal.pone.0097835
Modulevsky, D. J., Cuerrier, C. M. & Pelling, A. E. Biocompatibility of subcutaneously implanted plant-derived cellulose biomaterials. PLoS ONE 11, e0157894 (2016).
pubmed: 27328066
pmcid: 4915699
doi: 10.1371/journal.pone.0157894
Contessi Negrini, N., Toffoletto, N., Farè, S. & Altomare, L. Plant tissues as 3D natural scaffolds for adipose, bone and tendon tissue regeneration. Front. Bioeng. Biotechnol. https://doi.org/10.3389/fbioe.2020.00723 (2020).
doi: 10.3389/fbioe.2020.00723
pubmed: 32714912
pmcid: 7344190
Fu, L., Zhang, J. & Yang, G. Present status and applications of bacterial cellulose-based materials for skin tissue repair. Carbohydr. Polym. 92, 1432–1442 (2013).
pubmed: 23399174
doi: 10.1016/j.carbpol.2012.10.071
Nosar, M. N. et al. Characterization of wet-electrospun cellulose acetate based 3-dimensional scaffolds for skin tissue engineering applications: Influence of cellulose acetate concentration. Cellulose 23, 3239–3248 (2016).
doi: 10.1007/s10570-016-1026-7
Osorio, M. et al. Ex vivo and in vivo biocompatibility assessment (blood and tissue) of three-dimensional bacterial nanocellulose biomaterials for soft tissue implants. Sci. Rep. https://doi.org/10.1038/s41598-019-46918-x (2019).
doi: 10.1038/s41598-019-46918-x
pubmed: 31705004
pmcid: 6841711
Mihranyan, A. Cellulose from cladophorales green algae: From environmental problem to high-tech composite materials albert. Polym. Polym. Compos. 119, 2449–2460 (2011).
Lahaye, M. & Robic, A. Structure and functional properties of Ulvan, a polysaccharide from green seaweeds. Biomacromolecule 8, 1765–1774 (2007).
doi: 10.1021/bm061185q
Chaudhuri, O., Cooper-White, J., Janmey, P. A., Mooney, D. J. & Shenoy, V. B. Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature 584, 535–546 (2020).
pubmed: 32848221
pmcid: 7676152
doi: 10.1038/s41586-020-2612-2
Chemodanov, A., Robin, A. & Golberg, A. Design of marine macroalgae photobioreactor integrated into building to support seagriculture for biorefinery and bioeconomy. Bioresour. Technol. 241, 1084–1093 (2017).
pubmed: 28651325
doi: 10.1016/j.biortech.2017.06.061
Fernand, F. et al. Offshore macroalgae biomass for bioenergy production: Environmental aspects, technological achievements and challenges. Renew. Sustain. Energy Rev. 75, 35–45 (2017).
doi: 10.1016/j.rser.2016.10.046
Kumar, S., Marrero-Berrios, I., Kabat, M. & Berthiaume, F. Recent advances in the use of algal polysaccharides for skin wound healing. Curr. Pharm. Des. 25, 1236–1248 (2019).
pubmed: 31109271
pmcid: 7746437
doi: 10.2174/1381612825666190521120051
Kim, S. K. Marine Biomaterials: Characterization, Isolation and Applications (CRC Press, 2013).
Sudha, P., Gomathi, T. & Kim, S. Ulvan in tissue engineering. In Encyclopedia of Marine Biotechnology (ed. Kim, S.) 1335–1350 (Wiley, 2020).
Madub, K. et al. Green seaweeds ulvan-cellulose scaffolds enhance in vitro cell growth and in vivo angiogenesis for skin tissue engineering. Carbohydr. Polym. 251, 117025 (2021).
pubmed: 33142585
doi: 10.1016/j.carbpol.2020.117025
Zhou, S., Nyholm, L., Strømme, M. & Wang, Z. Cladophora cellulose: Unique biopolymer nanofibrils for emerging energy, environmental, and life science applications. Acc. Chem. Res. 52, 2232–2243 (2019).
pubmed: 31290643
doi: 10.1021/acs.accounts.9b00215
Wahlström, N. et al. Cellulose from the green macroalgae Ulva lactuca: Isolation, characterization, optotracing, and production of cellulose nanofibrils. Cellulose 27, 3707–3725 (2020).
doi: 10.1007/s10570-020-03029-5
Holzinger, A. et al. Desiccation tolerance in the chlorophyte green alga Ulva compressa: Does cell wall architecture contribute to ecological success?. Planta 242, 477–492 (2015).
pubmed: 25896374
pmcid: 4498240
doi: 10.1007/s00425-015-2292-6
ISO/EN10993-5. International Standard ISO 10993-5 Biological evaluation of medical devices: Tests for in vitro cytotoxicity. In Part 5: Tests for Cytotoxicity: In Vitro Methods, vol. 3, 42 (2009).
ISO/EN10993-12. International Standard ISO 10993-12 biological evaluation of medical devices: sample preparation and reference materials. In Part 12: Sample Preparation and Reference Materials (2012).
Hamid, R., Rotshteyn, Y., Rabadi, L., Parikh, R. & Bullock, P. Comparison of alamar blue and MTT assays for high through-put screening. Toxicol. In Vitro 18, 703–710 (2004).
pubmed: 15251189
doi: 10.1016/j.tiv.2004.03.012
López-Álvarez, M., Serra, J., Sánchez, J. M. & de Carlos, A. Marine plants and algae as promising 3D scaffolds for tissue engineering. In Marine Biomaterials: Characterization, Isolation and Applications (ed. Kim, S.-K.) 541–560 (CRC Press, 2013).
dos Santos, F. A., Iulianelli, G. C. V. & Tavares, M. I. B. O. The use of cellulose nanofillers in obtaining polymer nanocomposites: Properties, processing, and applications. Mater. Sci. Appl. 7, 257–294 (2016).
Trivedi, N. et al. An integrated process for the extraction of fuel and chemicals from marine macroalgal biomass. Sci. Rep. 6, 1–8 (2016).
doi: 10.1038/srep30728
Prabhu, M. S., Israel, A., Palatnik, R. R., Zilberman, D. & Golberg, A. Integrated biorefinery process for sustainable fractionation of Ulva ohnoi (Chlorophyta): Process optimization and revenue analysis. J. Appl. Phycol. 32, 2271–2282 (2020).
doi: 10.1007/s10811-020-02044-0
Hughes, J. & McCully, M. E. The use of an optical brightener in the study of plant structure. Biotech. Histochem. 50, 319–329 (1975).
Polikovsky, M. et al. Towards marine biore fi neries: Selective proteins extractions from marine macroalgae Ulva with pulsed electric fi elds. Innov. Food Sci. Emerg. Technol. 37, 194–200 (2016).
doi: 10.1016/j.ifset.2016.03.013
Vesty, E. F., Kessler, R. W., Wichard, T. & Coates, J. C. Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): Comparison with Ulva mutabilis and potential for laboratory culture. Front. Plant Sci. 6, 1–8 (2015).
doi: 10.3389/fpls.2015.00015
Loh, Q. L. & Choong, C. Three-dimensional scaffolds for tissue engineering applications: Role of porosity and pore size. Tissue Eng. B 19, 485–502 (2013).
doi: 10.1089/ten.teb.2012.0437
Owen, S. C. & Shoichet, M. S. Design of three-dimensional biomimetic scaffolds. J. Biomed. Mater. Res. A 94, 1321–1331 (2010).
pubmed: 20597126
Dvir, T., Timko, B. P., Kohane, D. S. & Langer, R. Nanotechnological strategies for engineering complex tissues. Nat. Nanotechnol. 6, 13–22 (2011).
pubmed: 21151110
doi: 10.1038/nnano.2010.246
Prince, E. & Kumacheva, E. Design and applications of man-made biomimetic fibrillar hydrogels. Nat. Rev. Mater. 4, 99–115 (2019).
doi: 10.1038/s41578-018-0077-9
Stevens, M. M. & George, J. H. Exploring and engineering the cell surface interface. Sci. Rev. 310, 1135–1138 (2005).
Mirbagheri, M. et al. Advanced cell culture platforms: A growing quest for emulating natural tissues. Mater. Horiz. 6, 45–71 (2019).
doi: 10.1039/C8MH00803E
Chang, H.-I. & Wang, Y. Cell responses to surface and architecture of tissue engineering scaffolds. In Regenerative Medicine and Tissue Engineering—Cells and Biomaterials (ed. Eberli, D.) 569–588 (IntechOpen, 2011).
Wang, X. et al. The effect of fiber size and pore size on cell proliferation and infiltration in PLLA scaffolds on bone tissue engineering. J. Biomater. Appl. 30, 1545–1551 (2015).
doi: 10.1177/0885328216636320
Reilly, G. C. & Engler, A. J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 43, 55–62 (2010).
pubmed: 19800626
doi: 10.1016/j.jbiomech.2009.09.009
Ranucci, C. S., Kumar, A., Batra, S. P. & Moghe, P. V. Control of hepatocyte function on collagen foams: Sizing matrix pores toward selective induction of 2-D and 3-D cellular morphogenesis. Biomaterials 21, 783–793 (2000).
pubmed: 10721747
doi: 10.1016/S0142-9612(99)00238-0
Mukherjee, P. S. & Satyanarayana, K. G. Structure and properties of some vegetable fibres—Part 1 Sisal fibre. J. Mater. Sci. 19, 3925–3934 (1984).
doi: 10.1007/BF00980755
Rongpipi, S., Ye, D., Gomez, E. D. & Gomez, E. W. Progress and opportunities in the characterization of cellulose—An important regulator of cell wall growth and mechanics. Front. Plant Sci. 9, 1894 (2019).
pubmed: 30881371
pmcid: 6405478
doi: 10.3389/fpls.2018.01894
Kim, S. J., Jang, D. H., Park, W. H. & Min, B. M. Fabrication and characterization of 3-dimensional PLGA nanofiber/microfiber composite scaffolds. Polymer (Guildf). 51, 1320–1327 (2010).
doi: 10.1016/j.polymer.2010.01.025
Hsia, H. C., Nair, M. R., Mintz, R. C. & Corbett, S. A. The fiber diameter of synthetic bioresorbable extracellular matrix influences human fibroblast morphology and fibronectin matrix assembly. Plast. Reconstr. Surg. 127, 2312–2320 (2011).
pubmed: 21617465
pmcid: 3103705
doi: 10.1097/PRS.0b013e3182139fa4
Chen, M., Patra, P. K., Warner, S. B. & Bhowmick, S. Role of fiber diameter in adhesion and proliferation of NIH 3T3 fibroblast on electrospun polycaprolactone scaffolds. Tissue Eng. 13, 579–587 (2007).
pubmed: 17518604
doi: 10.1089/ten.2006.0205
Nimeskern, L. et al. Mechanical evaluation of bacterial nanocellulose as an implant material for ear cartilage replacement. J. Mech. Behav. Biomed. Mater. 22, 12–21 (2013).
pubmed: 23611922
doi: 10.1016/j.jmbbm.2013.03.005
Mondal, S. Preparation, properties and applications of nanocellulosic materials. Carbohyd. Polym. 163, 301–316 (2017).
doi: 10.1016/j.carbpol.2016.12.050
Blakeney, B. A. et al. Cell infiltration and growth in a low density, uncompressed three-dimensional electrospun nanofibrous scaffold. Biomaterials 32, 1583–1590 (2011).
pubmed: 21112625
doi: 10.1016/j.biomaterials.2010.10.056
Zhong, S. et al. An aligned nanofibrous collagen scaffold by electrospinning and its effects on in vitro fibroblast culture. J. Biomed. Mater. Res. Part A 79A, 456–463 (2006).
doi: 10.1002/jbm.a.30870
Teixeira, A. I., Abrams, G. A., Bertics, P. J., Murphy, C. J. & Nealey, P. F. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J. Cell Sci. 116, 1881–1892 (2003).
pubmed: 12692189
doi: 10.1242/jcs.00383
Clark, P., Connolly, P., Curtis, A. S. G., Dow, J. A. T. & Wilkinson, C. D. W. Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108, 635–644 (1990).
pubmed: 2387239
doi: 10.1242/dev.108.4.635
Bettinger, C. J., Langer, R. & Borenstein, J. T. Engineering substrate topography at the micro- and nanoscale to control cell function. Angew. Chem. Int. Ed. 48, 5406–5415 (2009).
doi: 10.1002/anie.200805179
Shelah, O., Wertheimer, S., Haj-Ali, R. & Lesman, A. Coral-derived collagen fibers for engineering aligned tissues. Tissue Eng. A https://doi.org/10.1089/ten.tea.2020.0116 (2020).
doi: 10.1089/ten.tea.2020.0116
Baranes-Zeevi, M., Goder, D. & Zilberman, M. Novel drug-eluting soy-protein structures for wound healing applications. Polym. Adv. Technol. 30, 2523–2538 (2019).
doi: 10.1002/pat.4673
Mikus, J. & Steverding, D. A simple colorimetric method to screen drug cytotoxicity against Leishmania using the dye alamar Blue. Parasitol. Int. 48, 265–269 (2000).
pubmed: 11227767
doi: 10.1016/S1383-5769(99)00020-3
Johansson, U. et al. Assembly of functionalized silk together with cells to obtain proliferative 3D cultures integrated in a network of ECM-like microfibers. Sci. Rep. 9, 1–13 (2019).
doi: 10.1038/s41598-019-42541-y
Gesztelyi, R. et al. The Hill equation and the origin of quantitative pharmacology. Arch. Hist. Exact Sci. 66, 427–438 (2012).
doi: 10.1007/s00407-012-0098-5
Crapo, P. M., Gilbert, T. W. & Badylak, S. F. An overview of tissue and whole organ decellularization processes. Biomaterials 32, 3233–3243 (2011).
pubmed: 21296410
pmcid: 3084613
doi: 10.1016/j.biomaterials.2011.01.057
Charlebois, D. A. & Balázsi, G. Modeling cell population dynamics. In Silico Biol. 13, 21–39 (2018).
doi: 10.3233/ISB-180470