[en] Chemokines such as stromal cell-derived factor-1α (SDF-1α) regulate the migration of cancer cells that can spread from their primary tumor site by migrating up an SDF-1α concentration gradient, facilitating their local invasion and metastasis. Therefore, the implantation of SDF-1α-releasing scaffolds can be a useful strategy to trap cancer cells expressing the CXCR4 receptor. In this work, SDF-1α was encapsulated into poly(lactic-co-glycolic acid) (PLGA)-based nanoparticles and subsequently electrospun with chitosan to produce nanofibrous scaffolds of average fiber diameter of 261 ± 45 nm, intended for trapping glioblastoma (GBM) cells. The encapsulated SDF-1α maintained its biological activity after the electrospinning process as assessed by its capacity to induce the migration of cancer cells. The scaffolds could also provide sustained release of SDF-1α for at least 5 weeks. Using NIH3T3 mouse fibroblasts, human Thp-1 macrophages, and rat primary astrocytes we showed that the scaffolds possessed high cytocompatibility in vitro. Furthermore, a 7-day follow-up of Fischer rats bearing implanted scaffolds demonstrated the absence of adverse effects in vivo. In addition, the nanofibrous structure of the scaffolds provided excellent anchoring sites to support the adhesion of human GBM cells by extension of their pseudopodia. The scaffolds also demonstrated slow degradation kinetics, which may be useful in maximizing the time window for trapping GBM cells. As surgical resection does not permit a complete removal of GBM tumors, our results support the future implantation of these scaffolds into the walls of the resection cavity to evaluate their capacity to attract and trap the residual GBM cells in the brain.
Research Center/Unit :
Complex and Entangled Systems from Atoms to Materials (CESAM) Research Unit Center for Education and Research on Macromolecules (CERM)
Disciplines :
Materials science & engineering Chemistry
Author, co-author :
Molina-Peña, Rodolfo; University of Angers, University of Nantes, CRCINA INSERM, France
Haji Mansor, Muhammad; University of Angers, University of Nantes, CRCINA INSERM, France ; University of Liège (ULiège), Complex and Entangled Systems from Atoms to Materials (CESAM) Research Unit, Center for Education and Research on Macromolecules (CERM), Belgium
Najberg, Mathie; University of Angers, University of Nantes, CRCINA INSERM, France ; University of Santiago de Compostela, Facultad de Farmacia, and Health Research Institute of Santiago de Compostela (IDIS), Spain
Thomassin, Jean-Michel ; University of Liège (ULiège), Complex and Entangled Systems from Atoms to Materials (CESAM) Research Unit, Center for Education and Research on Macromolecules (CERM), Belgium
Gueza, Baya; Univ Angers, Université de Nantes, Inserm, CRCINA, SFR ICAT, F-49000 Angers, France
Alvarez-Lorenzo, Carmen; University of Santiago de Compostela, Facultad de Farmacia, and Health Research Institute of Santiago de Compostela (IDIS), Spain
Garcion, Emmanuel; University of Angers, University of Nantes, CRCINA INSERM, France
Jérôme, Christine ; University of Liège (ULiège), Complex and Entangled Systems from Atoms to Materials (CESAM) Research Unit, Center for Education and Research on Macromolecules (CERM), Belgium
Boury, Frank; University of Angers, University of Nantes, CRCINA INSERM, France
Language :
English
Title :
Nanoparticle-containing electrospun nanofibrous scaffolds for sustained release of SDF-1α.
Publication date :
15 December 2021
Journal title :
International Journal of Pharmaceutics
ISSN :
0378-5173
eISSN :
1873-3476
Publisher :
Elsevier B.V., Netherlands
Volume :
610
Pages :
121205
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
INSERM - French Institute of Health and Medical Research MINECO - Spanish Government. Ministry of Economy, Industry and Competitiveness FEDER - Fonds Européen de Développement Régional PROSTEM BIOREGATE NANOFAR
Funding text :
This work was supported by the “Institut National de la Santé et de la Recherche Médicale” (INSERM), the University of Angers, France; MINECO [SAF2017-83118-R], Agencia Estatal de Investigación (AEI) and Instituto de Salud Carlos III (ISCIII) [ AC19/00067 ] Cofinanciado FEDER, Spain; and FEDER (FMF - Prostem) for the University of Liege (Liege, Belgium). It is also related to the regional programs Bioimplants for Bone Regeneration (BILBO) part of the BIOREGATE Research-Training-Innovation consortium (RFI), and NanoFar + both supported by the French Région Pays-de-la-Loire; LabEx IRON “ Innovative Radiopharmaceuticals in Oncology and Neurology” as part of the French government “Investissements d’Avenir” program; the INCa (Institut National du Cancer ) MARENGO consortium “MicroRNA agonist and antagonist Nanomedicines for Glioblastoma treatment: from molecular programmation to preclinical validation” [Grant PL-BIO 2014-2020 ]; the MuMoFRaT project “Multi-scale Modeling & simulation of the response to hypo-Fractionated Radiotherapy or repeated molecular radiation Therapies” supported by La Région Pays-de-la-Loire and the Cancéropôle Grand-Ouest; and the French National Research Agency (ANR) under the frame of EuroNanoMed III (project GLIOSILK “ Silk-fibroin interventional nano-trap for the treatment of glioblastoma”) [grant ANR-19-ENM3-0003-01 ]. Muhammad Haji Mansor and Mathie Najberg were Ph.D. students involved in the EMJD ( Erasmus Mundus Joint Doctorate) NanoFar program funded by the European Education and Culture Executive Agency (EACEA). Muhammad Haji Mansor and Rodolfo Molina-Pena were PhD fellows from the French “Ministère de l'Enseignement supérieur, de la Recherche et de l’Innovation” (MESRI), while Mathie Najberg received a fellowship from La Région Pays-de-la-Loire.
Almouazen, E., Bourgeois, S., Boussaïd, A., Valot, P., Malleval, C., Fessi, H., Nataf, S., Briançon, S., Development of a nanoparticle-based system for the delivery of retinoic acid into macrophages. Int. J. Pharm. 430:1-2 (2012), 207–215, 10.1016/j.ijpharm.2012.03.025.
Autier, L., Clavreul, A., Cacicedo, M.L., Franconi, F., Sindji, L., Rousseau, A., Perrot, R., Montero-Menei, C.N., Castro, G.R., Menei, P., A new glioblastoma cell trap for implantation after surgical resection. Acta Biomater. 84 (2018), 268–279, 10.1016/j.actbio.2018.11.027.
Balmert, S.C., Zmolek, A.C., Glowacki, A.J., Knab, T.D., Rothstein, S.N., Wokpetah, J.M., Fedorchak, M.V., Little, S.R., Positive charge of “sticky” peptides and proteins impedes release from negatively charged PLGA matrices. J. Mater. Chem. B 3:23 (2015), 4723–4734, 10.1039/C5TB00515A.
Bekard, I., Dunstan, D.E., Electric field induced changes in protein conformation. Soft Matter 10:3 (2014), 431–437, 10.1039/C3SM52653D.
Blakeney, B.A., Tambralli, A., Anderson, J.M., Andukuri, A., Lim, D.-J., Dean, D.R., Jun, H.-W., Cell infiltration and growth in a low density, uncompressed three-dimensional electrospun nanofibrous scaffold. Biomaterials 32:6 (2011), 1583–1590, 10.1016/j.biomaterials.2010.10.056.
Carmo, A.d., Patricio, I., Cruz, M.T., Carvalheiro, H., Oliveira, C.R., Lopes, M.C., CXCL12/CXCR4 promotes motility and proliferation of glioma cells. Cancer Biol. Ther. 9:1 (2010), 56–65, 10.4161/cbt.9.1.10342.
Constantopoulos, A., Antonakakis, K., Matsaniotis, N., Kapsalakis, Z., Spinal Fluid Lysozyme in the Diagnosis of Central Nervous System Tumours. Neurochirurgia 19:04 (1976), 169–171, 10.1055/s-0028-1090407.
Croisier, F., Jérôme, C., Chitosan-based biomaterials for tissue engineering. Eur. Polymer J., Biobased Polymers Related Mater. 49:4 (2013), 780–792, 10.1016/j.eurpolymj.2012.12.009.
Cunha-Reis, C., TuzlaKoglu, K., Baas, E., Yang, Y., Haj, A.E., Reis, R.L., Influence of porosity and fibre diameter on the degradation of chitosan fibre-mesh scaffolds and cell adhesion. J. Mater. Sci. - Mater. Med. 18:2 (2007), 195–200, 10.1007/s10856-006-0681-x.
De La Luz Sierra, M., Yang, F., Narazaki, M., Salvucci, O., Davis, D., Yarchoan, R., Zhang, H.H., Fales, H., Tosato, G., Differential processing of stromal-derived factor-1alpha and stromal-derived factor-1beta explains functional diversity. Blood 103 (2004), 2452–2459, 10.1182/blood-2003-08-2857.
Deng, J., Zou, Z.-M., Zhou, T.-l., Su, Y.-P., Ai, G.-P., Wang, J.-P., Xu, H., Dong, S.-w., Bone marrow mesenchymal stem cells can be mobilized into peripheral blood by G-CSF in vivo and integrate into traumatically injured cerebral tissue. Neurological Sci. 32:4 (2011), 641–651, 10.1007/s10072-011-0608-2.
Dhiman, H.K., Ray, A.R., Panda, A.K., Characterization and evaluation of chitosan matrix for in vitro growth of MCF-7 breast cancer cell lines. Biomaterials 25:21 (2004), 5147–5154, 10.1016/j.biomaterials.2003.12.025.
Dilamian, M., Montazer, M., Masoumi, J., Antimicrobial electrospun membranes of chitosan / poly (ethylene oxide) incorporating poly (hexamethylene biguanide) hydrochloride. Carbohydr. Polym. 94:1 (2013), 364–371, 10.1016/j.carbpol.2013.01.059.
Dong, Y., Xu, C., Wang, J., Wang, M., Wu, Y., Ruan, Y., Determination of degree of substitution for N-acylated chitosan using IR spectra. Sci. China, Ser. B Chem. 44:2 (2001), 216–224, 10.1007/BF02879541.
Du, J., Che, P.-L., Wang, Z.-Y., Aich, U., Yarema, K.J., Designing a binding interface for control of cancer cell adhesion via 3D topography and metabolic oligosaccharide engineering. Biomaterials 32:23 (2011), 5427–5437, 10.1016/j.biomaterials.2011.04.005.
Du, L., Yang, S., Li, W., Li, H., Feng, S., Zeng, R., Yu, B., Xiao, L., Nie, H.Y., Tu, M., Scaffold composed of porous vancomycin-loaded poly(lactide-co-glycolide) microspheres: A controlled-release drug delivery system with shape-memory effect. Mater. Sci. Eng., C 78 (2017), 1172–1178, 10.1016/j.msec.2017.04.099.
Freier, T., Koh, H.S., Kazazian, K., Shoichet, M.S., Controlling cell adhesion and degradation of chitosan films by N-acetylation. Biomaterials 26:29 (2005), 5872–5878, 10.1016/j.biomaterials.2005.02.033.
Frohbergh, M.E., Katsman, A., Botta, G.P., Lazarovici, P., Schauer, C.L., Wegst, U.G.K., Lelkes, P.I., Electrospun hydroxyapatite-containing chitosan nanofibers crosslinked with genipin for bone tissue engineering. Biomaterials 33:36 (2012), 9167–9178, 10.1016/j.biomaterials.2012.09.009.
GENG, X., KWON, O., JANG, J., Electrospinning of chitosan dissolved in concentrated acetic acid solution. Biomaterials 26:27 (2005), 5427–5432, 10.1016/j.biomaterials.2005.01.066.
Gentile, P., Nandagiri, V.K., Pabari, R., Daly, J., Tonda-Turo, C., Ciardelli, G., Ramtoola, Z., Influence of parathyroid hormone-loaded plga nanoparticles in porous scaffolds for bone regeneration. Int. J. Mol. Sci. 16 (2015), 20492–20510, 10.3390/ijms160920492.
Hagemann, C., Anacker, J., Ernestus, R.-I., Vince, G.H., A complete compilation of matrix metalloproteinase expression in human malignant gliomas. World J. Clin. Oncol. 3 (2012), 67–79, 10.5306/wjco.v3.i5.67.
Haji Mansor, M., Najberg, M., Contini, A., Alvarez-Lorenzo, C., Garcion, E., Jérôme, C., Boury, F., Development of a Non-toxic and Non-denaturing Formulation Process for Encapsulation of SDF-1α into PLGA/PEG-PLGA Nanoparticles to Achieve Sustained Release. Eur. J. Pharm. Biopharm. 125 (2018), 38–50, 10.1016/j.ejpb.2017.12.020.
Hamoudeh, M., Salim, H., Barbos, D., Paunoiu, C., Fessi, H., Preparation and characterization of radioactive dirhenium decacarbonyl-loaded PLLA nanoparticles for radionuclide intra-tumoral therapy. Eur. J. Pharm. Biopharm. 67:3 (2007), 597–611, 10.1016/j.ejpb.2007.04.003.
Hassani, L.N., Hindré, F., Beuvier, T., Calvignac, B., Lautram, N., Gibaud, A., Boury, F., Lysozyme encapsulation into nanostructured CaCO3 microparticles using a supercritical CO2 process and comparison with the normal route. J. Mater. Chem. B 1 (2013), 4011–4019, 10.1039/c3tb20467g.
He, Q., Ao, Q., Gong, Y., Zhang, X., Preparation of chitosan films using different neutralizing solutions to improve endothelial cell compatibility. J. Mater. Sci. - Mater. Med. 22:12 (2011), 2791–2802, 10.1007/s10856-011-4444-y.
Hol, W.G.J., The role of the α-helix dipole in protein function and structure. Prog. Biophys. Mol. Biol. 45:3 (1985), 149–195, 10.1016/0079-6107(85)90001-X.
Huang, Z.-M., Zhang, Y.-Z., Kotaki, M., Ramakrishna, S., A review on polymer nanofibers by electrospinning and their applications in nanocomposites. Compos. Sci. Technol. 63:15 (2003), 2223–2253, 10.1016/S0266-3538(03)00178-7.
Jin, F., Zhai, Q., Qiu, L., Meng, H., Zou, D., Wang, Y., Li, Q., Yu, Z., Han, J., Li, Q., Zhou, B., Degradation of BM SDF-1 by MMP-9: The role in G-CSF-induced hematopoietic stem/progenitor cell mobilization. Bone Marrow Transplant 42:9 (2008), 581–588, 10.1038/bmt.2008.222.
Katsura, M., Shoji, F., Okamoto, T., Shimamatsu, S., Hirai, F., Toyokawa, G., Morodomi, Y., Tagawa, T., Oda, Y., Maehara, Y., Correlation between CXCR4/CXCR7/CXCL12 chemokine axis expression and prognosis in lymph-node-positive lung cancer patients. Cancer Sci. 109:1 (2018), 154–165, 10.1111/cas.2018.109.issue-110.1111/cas.13422.
Kessenbrock, K., Plaks, V., Werb, Z., Matrix Metalloproteinases: Regulators of the Tumor Microenvironment. Cell 141:1 (2010), 52–67, 10.1016/j.cell.2010.03.015.
Kim, J., Mori, T., Chen, S.L., Amersi, F.F., Martinez, S.R., Kuo, C., Turner, R.R., Ye, X., Bilchik, A.J., Morton, D.L., Hoon, D.S.B., Chemokine receptor CXCR4 expression in patients with melanoma and colorectal cancer liver metastases and the association with disease outcome. Ann. Surg. 244:1 (2006), 113–120, 10.1097/01.sla.0000217690.65909.9c.
Kitaori, T., Ito, H., Schwarz, E.M., Tsutsumi, R., Yoshitomi, H., Oishi, S., Nakano, M., Fujii, N., Nagasawa, T., Nakamura, T., Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum. 60:3 (2009), 813–823, 10.1002/art.v60:310.1002/art.24330.
Knerlich-Lukoschus, F., Von Der Ropp-Brenner, B., Lucius, R., Mehdorn, H.M., Held-Feindt, J., Chemokine expression in the white matter spinal cord precursor niche after force-defined spinal cord contusion injuries in adult rats. Glia 58 (2010), 916–931, 10.1002/glia.20974.
Kofuku, Y., Yoshiura, C., Ueda, T., Terasawa, H., Hirai, T., Tominaga, S., Hirose, M., Maeda, Y., Takahashi, H., Terashima, Y., Matsushima, K., Shimada, I., Structural basis of the interaction between chemokine stromal cell-derived factor-1/CXCL12 and its G-protein-coupled receptor CXCR4. J. Biol. Chem. 284:50 (2009), 35240–35250, 10.1074/jbc.M109.024851.
Kriegel, C., Kit, K.M., McClements, D.J., Weiss, J., Electrospinning of chitosan – poly (ethylene oxide) blend nanofibers in the presence of micellar surfactant solutions. Polymer 50:1 (2009), 189–200, 10.1016/j.polymer.2008.09.041.
Lee, A.L.Z., Voo, Z.X., Chin, W., Ono, R.J., Yang, C., Gao, S., Hedrick, J.L., Yang, Y.Y., Injectable Coacervate Hydrogel for Delivery of Anticancer Drug-Loaded Nanoparticles in vivo. ACS Appl. Mater. Interfaces 10:16 (2018), 13274–13282, 10.1021/acsami.7b14319.
Lee, Y.H., Lee, J.H., An, I.-G., Kim, C., Lee, D.S., Lee, Y.K., Nam, J.-D., Electrospun dual-porosity structure and biodegradation morphology of Montmorillonite reinforced PLLA nanocomposite scaffolds. Biomaterials 26:16 (2005), 3165–3172, 10.1016/j.biomaterials.2004.08.018.
Ma, G., Liu, Y., Peng, C., Fang, D., He, B., Nie, J., Paclitaxel loaded electrospun porous nanofibers as mat potential application for chemotherapy against prostate cancer. Carbohydr. Polym. 86:2 (2011), 505–512, 10.1016/j.carbpol.2011.04.082.
Marquez-Curtis, L., Jalili, A., Deiteren, K., Shirvaikar, N., Lambeir, A.-M., Janowska-Wieczorek, A., Carboxypeptidase M Expressed by Human Bone Marrow Cells Cleaves the C-Terminal Lysine of Stromal Cell-Derived Factor-1α: Another Player in Hematopoietic Stem/Progenitor Cell Mobilization?. Stem Cells 26:5 (2008), 1211–1220, 10.1634/stemcells.2007-0725.
Martin, L.J., Akhavan, B., Bilek, M.M.M., Electric fields control the orientation of peptides irreversibly immobilized on radical-functionalized surfaces. Nat. Commun. 9 (2018), 357–367, 10.1038/s41467-017-02545-6.
Martínez Rivas, C.J., Tarhini, M., Badri, W., Miladi, K., Greige-Gerges, H., Nazari, Q.A., Galindo Rodríguez, S.A., Román, R.Á., Fessi, H., Elaissari, A., Nanoprecipitation process: From encapsulation to drug delivery. Int. J. Pharm. 532:1 (2017), 66–81, 10.1016/j.ijpharm.2017.08.064.
McCarthy, K.D., de Vellis, J., Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85 (1980), 890–902, 10.1083/jcb.85.3.890.
Milner, R., Edwards, G., Streuli, C., Ffrench-Constant, C., A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. J. Neurosci.: The Off. J. Soc. Neurosci. 16 (1996), 7240–7252, 10.1523/JNEUROSCI.16-22-07240.1996.
Min, B.-M., Lee, S.W., Lim, J.N., You, Y., Lee, T.S., Kang, P.H., Park, W.H., Chitin and chitosan nanofibers: Electrospinning of chitin and deacetylation of chitin nanofibers. Polymer 45:21 (2004), 7137–7142, 10.1016/j.polymer.2004.08.048.
Najberg, M., Haji Mansor, M., Taillé, T., Bouré, C., Molina-Peña, R., Boury, F., Cenis, J.L., Garcion, E., Alvarez-Lorenzo, C., Aerogel sponges of silk fibroin, hyaluronic acid and heparin for soft tissue engineering: Composition-properties relationship. Carbohydr. Polym., 237, 2020, 116107, 10.1016/j.carbpol.2020.116107.
Newman, J., Josephson, A.S., Cacatian, A., Tsang, A., Spinal-fluid lysozyme in the diagnosis of central-nervous-system tumors. Lancet 304 (1974), 756–757, 10.1016/S0140-6736(74)90946-5.
Nicolas, S., Bolzinger, M.-A., Jordheim, L.P., Chevalier, Y., Fessi, H., Almouazen, E., Polymeric nanocapsules as drug carriers for sustained anticancer activity of calcitriol in breast cancer cells. Int. J. Pharm. 550:1-2 (2018), 170–179, 10.1016/j.ijpharm.2018.08.022.
Noriega, S.E., Subramanian, A., Consequences of Neutralization on the Proliferation and Cytoskeletal Organization of Chondrocytes on Chitosan-Based Matrices. Int. J. Carbohydrate Chem. 2011 (2011), 1–13, 10.1155/2011/809743.
O'Boyle, G., Swidenbank, I., Marshall, H., Barker, C.E., Armstrong, J., White, S.A., Fricker, S.P., Plummer, R., Wright, M., Lovat, P.E., Inhibition of CXCR4-CXCL12 chemotaxis in melanoma by AMD11070. Br. J. Cancer 108:8 (2013), 1634–1640, 10.1038/bjc.2013.124.
Ojeda-May, P., Garcia, M.E., Electric field-driven disruption of a native β-sheet protein conformation and generation of a helix-structure. Biophys. J. 99:2 (2010), 595–599, 10.1016/j.bpj.2010.04.040.
Ono, R.J., Lee, A.L.Z., Voo, Z.X., Venkataraman, S., Koh, B.W., Yang, Y.Y., Hedrick, J.L., Biodegradable Strain-Promoted Click Hydrogels for Encapsulation of Drug-Loaded Nanoparticles and Sustained Release of Therapeutics. Biomacromolecules 18:8 (2017), 2277–2285, 10.1021/acs.biomac.7b00377.
Pakravan, M., Heuzey, M.-C., Ajji, A., A fundamental study of chitosan/PEO electrospinning. Polymer 52:21 (2011), 4813–4824, 10.1016/j.polymer.2011.08.034.
Pakulska, M.M., Elliott Donaghue, I., Obermeyer, J.M., Tuladhar, A., McLaughlin, C.K., Shendruk, T.N., Shoichet, M.S., Encapsulation-free controlled release: Electrostatic adsorption eliminates the need for protein encapsulation in PLGA nanoparticles. Sci. Adv. 2 (2016), e1600519–e1600528, 10.1126/sciadv.1600519.
Pardridge, W.M., Drug transport in brain via the cerebrospinal fluid. Fluids Barriers CNS 8 (2011), 7–10, 10.1186/2045-8118-8-7.
Pham, Q.P., Sharma, U., Mikos, A.G., Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng. 12:5 (2006), 1197–1211, 10.1089/ten.2006.12.1197.
Ramakrishna, S., Fujihara, K., Teo, W.-E., Yong, T., Ma, Z., Ramaseshan, R., Electrospun nanofibers: Solving global issues. Mater. Today 9:3 (2006), 40–50, 10.1016/S1369-7021(06)71389-X.
Ratajczak, M.Z., Kucia, M., Reca, R., Majka, M., Janowska-Wieczorek, A., Ratajczak, J., Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells “hide out” in the bone marrow. Leukemia 18:1 (2004), 29–40, 10.1038/sj.leu.2403184.
Ren, D., Yi, H., Wang, W., Ma, X., The enzymatic degradation and swelling properties of chitosan matrices with different degrees of N-acetylation. Carbohydr. Res. 340:15 (2005), 2403–2410, 10.1016/j.carres.2005.07.022.
Rinaudo, M., Pavlov, G., Desbrières, J., Influence of acetic acid concentration on the solubilization of chitosan. Polymer 40:25 (1999), 7029–7032, 10.1016/S0032-3861(99)00056-7.
Ripoll, D.R., Vila, J.A., Scheraga, H.A., On the orientation of the backbone dipoles in native folds. Proc. Natl. Acad. Sci. 102:21 (2005), 7559–7564, 10.1073/pnas.0502754102.
Roccaro, A., Sacco, A., Purschke, W., Moschetta, M., Buchner, K., Maasch, C., Zboralski, D., Zöllner, S., Vonhoff, S., Mishima, Y., Maiso, P., Reagan, M., Lonardi, S., Ungari, M., Facchetti, F., Eulberg, D., Kruschinski, A., Vater, A., Rossi, G., Klussmann, S., Ghobrial, I., SDF-1 inhibition targets the bone marrow niche for cancer therapy. Cell Reports 9:1 (2014), 118–128, 10.1016/j.celrep.2014.08.042.
Saravanan, S., Sareen, N., Abu-El-Rub, E., Ashour, H., Sequiera, G.L., Ammar, H.I., Gopinath, V., Shamaa, A.A., Sayed, S.S.E., Moudgil, M., Vadivelu, J., Dhingra, S., Graphene Oxide-Gold Nanosheets Containing Chitosan Scaffold Improves Ventricular Contractility and Function After Implantation into Infarcted Heart. Sci. Rep., 8, 2018, 15069, 10.1038/s41598-018-33144-0.
Sashiwa, H., Saimoto, H., Shigemasa, Y., Ogawa, R., Tokura, S., Lysozyme susceptibility of partially deacetylated chitin. Int. J. Biol. Macromol. 12:5 (1990), 295–296, 10.1016/0141-8130(90)90016-4.
Séhédic, D., Chourpa, I., Tétaud, C., Griveau, A., Loussouarn, C., Avril, S., Legendre, C., Lepareur, N., Wion, D., Hindré, F., Davodeau, F., Garcion, E., Locoregional Confinement and Major Clinical Benefit of 188 Re-Loaded CXCR4-Targeted Nanocarriers in an Orthotopic Human to Mouse Model of Glioblastoma. Theranostics 7:18 (2017), 4517–4536, 10.7150/thno.19403.
Sobolik, T., Su, Y.-J., Wells, S., Ayers, G.D., Cook, R.S., Richmond, A., Yap, A., CXCR4 drives the metastatic phenotype in breast cancer through induction of CXCR2 and activation of MEK and PI3K pathways. Mol. Biol. Cell 25:5 (2014), 566–582, 10.1091/mbc.e13-07-0360.
Tchemtchoua, V.T., Atanasova, G., Aqil, A., Filée, P., Garbacki, N., Vanhooteghem, O., Deroanne, C., Noël, A., Jérome, C., Nusgens, B., Poumay, Y., Colige, A., Development of a Chitosan Nanofibrillar Scaffold for Skin Repair and Regeneration. Biomacromolecules 12:9 (2011), 3194–3204, 10.1021/bm200680q.
Tomihata, K., Ikada, Y., In vitro and in vivo degradation of films of chitin and its deacetylated derivatives. Biomaterials 18:7 (1997), 567–575, 10.1016/S0142-9612(96)00167-6.
Toschi, F., Lugli, F., Biscarini, F., Zerbetto, F., Effects of Electric Field Stress on a β-Amyloid Peptide. J. Phys. Chem. B 113:1 (2009), 369–376, 10.1021/jp807896g.
Toullec, C., Le Bideau, J., Geoffroy, V., Halgand, B., Buchtova, N., Molina-Peña, R., Garcion, E., Avril, S., Sindji, L., Dube, A., Boury, F., Jérôme, C., Curdlan-Chitosan Electrospun Fibers as Potential Scaffolds for Bone Regeneration. Polymers, 13, 2021, 526, 10.3390/polym13040526.
Tyliszczak, B., Drabczyk, A., Kudłacik-Kramarczyk, S., Bialik-Wąs, K., Sobczak-Kupiec, A., In vitro cytotoxicity of hydrogels based on chitosan and modified with gold nanoparticles. J. Polym. Res., 24, 2017, 153, 10.1007/s10965-017-1315-3.
Vårum, K.M., Myhr, M.M., Hjerde, R.J.N., Smidsrød, O., In vitro degradation rates of partially N-acetylated chitosans in human serum. Carbohydr. Res. 299:1-2 (1997), 99–101, 10.1016/S0008-6215(96)00332-1.
Wada, A., The alpha-helix as an electric macro-dipole. Adv. Biophys. 9 (1976), 1–63.
Wang, M.O., Etheridge, J.M., Thompson, J.A., Vorwald, C.E., Dean, D., Fisher, J.P., Evaluation of the In Vitro Cytotoxicity of Cross-Linked Biomaterial. Biomacromolecules 14 (2013), 1321–1329, 10.1021/bm301962f.
Wang, X., Li, Y., He, X., Chen, S., Zhang, J.Z.H., Effect of strong electric field on the conformational integrity of insulin. J. Phys. Chem. A 118:39 (2014), 8942–8952, 10.1021/jp501051r.
Wolf, K., Te Lindert, M., Krause, M., Alexander, S., Te Riet, J., Willis, A.L., Hoffman, R.M., Figdor, C.G., Weiss, S.J., Friedl, P., Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol. 201 (2013), 1069–1084, 10.1083/jcb.201210152.
Wu, J., Hong, Y.i., Enhancing cell infiltration of electrospun fibrous scaffolds in tissue regeneration. Bioact. Mater. 1:1 (2016), 56–64, 10.1016/j.bioactmat.2016.07.001.
Xia, M., Huang, R., Witt, K.L., Southall, N., Fostel, J., Cho, M.-H., Jadhav, A., Smith, C.S., Inglese, J., Portier, C.J., Tice, R.R., Austin, C.P., Compound Cytotoxicity Profiling Using Quantitative High-Throughput Screening. Environ Health Perspect 116:3 (2008), 284–291, 10.1289/ehp.10727.
Zagzag, D., Esencay, M., Mendez, O., Yee, H., Smirnova, I., Huang, Y., Chiriboga, L., Lukyanov, E., Liu, M., Newcomb, E.W., Hypoxia- and Vascular Endothelial Growth Factor-Induced Stromal Cell-Derived Factor-1α/CXCR4 Expression in Glioblastomas. Am. J. Pathol. 173:2 (2008), 545–560, 10.2353/ajpath.2008.071197.
Zhang, H., Tian, Y., Zhu, Z., Xu, H., Li, X., Zheng, D., Sun, W., Efficient antitumor effect of co-drug-loaded nanoparticles with gelatin hydrogel by local implantation. Sci. Rep. 6 (2016), 1–14, 10.1038/srep26546.
Zhao, W., Yang, R., Experimental Study on Conformational Changes of Lysozyme in Solution Induced by Pulsed Electric Field and Thermal Stresses. J. Phys. Chem. B 114:1 (2010), 503–510, 10.1021/jp9081189.
Zhao, W., Yang, R., Effect of high-intensity pulsed electric fields on the activity, conformation and self-aggregation of pepsin. Food Chem. 114:3 (2009), 777–781, 10.1016/j.foodchem.2008.10.016.
Ziani, K., Henrist, C., Jérôme, C., Aqil, A., Maté, J.I., Cloots, R., Effect of nonionic surfactant and acidity on chitosan nanofibers with different molecular weights. Carbohydr. Polym. 83:2 (2011), 470–476, 10.1016/j.carbpol.2010.08.002.
