journal article·2023Open access

Low-power microwaves: a cell-compatible physical treatment to enhance the mechanical properties of self-assembling peptides

Maria Gessica Ciulla, Amanda Marchini, Jacopo Gazzola, Manuel Sambrotta, Fabrizio Gelain

Nanoscale· Volume 15· Issue 38

Abstract

Biomaterials designed for tissue engineering applications should, among other requirements, mimic the native extracellular matrix (ECM) of the tissues to be regenerated, both in terms of biomimetic and mechanical properties. Ideally, the scaffold stiffness and stress resistance should be tuned for each specific implantation therapy. Self-assembling peptides (SAPs) are promising synthetic bionanomaterials prone to easy multi-functionalization, bestowing biomimetic properties. However, they usually yield soft and fragile hydrogels unsuited for the regeneration of medium-to-hard tissues. For this purpose, chemical cross-linking of SAPs is an option, but it often requires a moderately toxic and expensive chemical compound and/or the presence of specific residues/reactive sites, posing issues for its feasibility and translational potential. In this work, we introduced, characterized by rheology, atomic force microscopy (AFM), Thioflavin-T assay (ThT), and Fourier transform infrared (FT-IR) tests, and optimized (by tuning the power, temperature and treatment time) a novel fast, green and affordable methodology using mild microwave (MW) irradiation to increase the mechanical properties of diverse classes of SAPs. Low-power MWs increase stiffness, resilience, and β-structuration, while high-power MW treatments partially denature the tested SAPs. Our pure-physical methodology does not alter the SAP biomimetic properties (verified via in vitro tests of viability and differentiation of human neural stem cells), is compatible with already seeded cells, and is also synergic with genipin-based cross-linking of SAPs; therefore, it may become the next standard for SAP preparation in tissue engineering applications at hand of all research labs and in clinics.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Supramolecular Self-Assembly in Materials · Polydiacetylene-based materials and applications · Antimicrobial Peptides and Activities

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Institute for Stem-Cell Biology, Regenerative Medicine and Innovative Therapies, IRCCS Casa Sollievo della Sofferenza, 71013 San Giovanni Rotondo, Italy

Center for Nanomedicine and Tissue Engineering (CNTE), ASST Grande Ospedale Metropolitano Niguarda, 20162 Milan, Italy

Department of Biotechnology and Bioscience, University of Milan – Bicocca, 20125 Milan, Italy

Department of Chemistry, Materials and Chemical Engineering “Giulio Natta”, Politecnico di Milano, 20133 Milan, Italy

Funding

Istituto Nazionale per l'Assicurazione Contro Gli Infortuni sul Lavoro · Ministero della Salute

References (91)

Show source-provided references
1. Mazzoni · Front. Bioeng. Biotechnol. · 2021 · 19 · 1
2. Tran · J. Phys.: Conf. Ser. · 2018 · 1082 · 012080
3. Palma · J. Am. Chem. Soc. · 2010 · 132 · 1788010.1021/ja107882e ↗
4. Mandal · Org. Biomol. Chem. · 2014 · 12 · 354410.1039/C4OB00447G ↗
5. Lehn · Proc. Natl. Acad. Sci. U. S. A. · 2002 · 99 · 476310.1073/pnas.072065599 ↗
6. Marsh · Biophys. J. · 2012 · 102 · 107910.1016/j.bpj.2012.01.049 ↗
7. A.Sharma , K.Vaghasiya , R. K.Verma and A. B.Yadav , Chapter 3 - DNA nanostructures: chemistry, self-assembly, and applications , Emerging Applications of Nanoparticles and Architecture Nanostructures , Elsevier Inc. , 2018
8. Levin · Nat. Rev. Chem. · 2020 · 4 · 61510.1038/s41570-020-0215-y ↗
9. Granger · Semin. Cell Dev. Biol. · 2014 · 31 · 2010.1016/j.semcdb.2014.04.011 ↗
10. Kharkar · Chem. Soc. Rev. · 2013 · 42 · 733510.1039/C3CS60040H ↗
11. Wang · Pharmaceutics · 2021 · 13 · 75310.3390/pharmaceutics13050753 ↗
12. Matson · Chem. Commun. · 2011 · 47 · 796210.1039/c1cc12570b ↗
13. Matson · Soft Matter · 2012 · 8 · 358610.1039/c2sm07420f ↗
14. Torchilin · Eur. J. Pharm. Biopharm. · 2009 · 71 · 43110.1016/j.ejpb.2008.09.026 ↗
15. Oren · Biochemistry · 2000 · 39 · 610310.1021/bi992408i ↗
16. Makovitzki · Biochemistry · 2008 · 47 · 1063010.1021/bi8011675 ↗
17. Marchini · Proc. Natl. Acad. Sci. U. S. A. · 2019 · 116 · 748310.1073/pnas.1818392116 ↗
18. Guo · Nanomedicine · 2009 · 5 · 34510.1016/j.nano.2008.12.001 ↗
19. Silva · Science · 2004 · 303 · 135210.1126/science.1093783 ↗
20. Semino · Differentiation · 2003 · 71 · 26210.1046/j.1432-0436.2003.7104503.x ↗
21. Kisiday · J. Biomech. · 2004 · 37 · 59510.1016/j.jbiomech.2003.10.005 ↗
22. Mujeeb · Acta Biomater. · 2013 · 9 · 460910.1016/j.actbio.2012.08.044 ↗
23. Pugliese · Mater. Des. · 2020 · 194 · 10890110.1016/j.matdes.2020.108901 ↗
24. Pugliese · Biomater. Sci. · 2019 · 7 · 7610.1039/C8BM00825F ↗
25. Pugliese · Nano Res. · 2018 · 11 · 58610.1007/s12274-017-1834-6 ↗
26. Ciulla · Nanomaterials · 2022 · 12 · 32010.3390/nano12030320 ↗
27. Pugliese · Int. J. Mol. Sci. · 2020 · 21 · 426110.3390/ijms21124261 ↗
28. Pugliese · Nanoscale Adv. · 2022 · 4 · 44710.1039/D1NA00688F ↗
29. Albuquerque · Molecules · 2021 · 26 · 629310.3390/molecules26206293 ↗
30. de la Hoz · Chem. Soc. Rev. · 2005 · 34 · 16410.1039/B411438H ↗
31. Bose · Synthesis · 2002 · 157810.1055/s-2002-33344 ↗
32. Varma · Tetrahedron · 2002 · 58 · 123510.1016/S0040-4020(01)01216-9 ↗
33. Langa · Electrochem. Soc. · 2000 · 9 · 168
34. D.Bogdal and A.Prociak , Polymer Sci Tech , Gen. Blackwell Pub. , 2007
35. Will · Chem. Ing. Tech. · 2002 · 74 · 105710.1002/1522-2640(20020815)74:8<1057::AID-CITE1057>3.0.CO;2-3 ↗
36. Chen · Sci. Rep. · 2016 · 6 · 3904010.1038/srep39040 ↗
37. Corsaro · Curr. Org. Chem. · 2004 · 8 · 51110.2174/1385272043485828 ↗
38. Zhang · Nat. Mater. · 2010 · 9 · 59410.1038/nmat2778 ↗
39. Kopeček · Biomaterials · 2007 · 28 · 518510.1016/j.biomaterials.2007.07.044 ↗
40. Wichterle · Nature · 1960 · 185 · 11710.1038/185117a0 ↗
41. Kopeček · Polym. Int. · 2007 · 56 · 107810.1002/pi.2253 ↗
42. Xiang · Chem. Eng. J. · 2023 · 460 · 14185210.1016/j.cej.2023.141852 ↗
43. Slaughter · Adv. Mater. · 2009 · 21 · 3210.1002/adma.200802106 ↗
44. Hamidi · Adv. Drug Delivery Rev. · 2008 · 60 · 163810.1016/j.addr.2008.08.002 ↗
45. Narayanaswamy · Molecules · 2019 · 24 · 60310.3390/molecules24030603 ↗
46. Yu · Adv. Funct. Mater. · 2023 · 33 · 221102310.1002/adfm.202211023 ↗
47. Yan · Chem. Soc. Rev. · 2019 · 39 · 352810.1039/b919449p ↗
48. D.Aparna and K. B.Bimal , Microwaves in Chemistry Applications Fundamentals, Methods and Future Trends , Elsevier , 1st edn, 2021
49. Chandrasekaran · Food Res. Int. · 2013 · 52 · 24310.1016/j.foodres.2013.02.033 ↗
50. Mishra · Crit. Rev. Solid State Mater. Sci. · 2016 · 41 · 21710.1080/10408436.2016.1142421 ↗
51. Kłosowski · Catalysts · 2019 · 9 · 75310.3390/catal9090753 ↗
52. C. O.Kappe and A.Stadler , Microwaves in Organic and Medicinal Chemistry , Wiley-VCH , Weinheim , 200510.1002/3527606556 ↗
53. Hettiarachchi · Biomacromolecules · 2012 · 13 · 286810.1021/bm300896r ↗
54. Jiao · Foods · 2021 · 10 · 189210.3390/foods10081892 ↗
55. Cao · Adv. Colloid Interface Sci. · 2019 · 269 · 33410.1016/j.cis.2019.05.002 ↗
56. Shaw · Sci. Rep. · 2021 · 11 · 1400310.1038/s41598-021-93274-w ↗
57. Mishra · Adv Microw. Wirel. Technol. · 2013 · 1 · 410.12966/amwt.05.02.2013 ↗
58. Gelain · Nanoscale · 2012 · 4 · 294610.1039/c2nr30220a ↗
59. Sieminski · J. Biomed. Mater. Res., Part A · 2008 · 87 · 49410.1002/jbm.a.31785 ↗
60. Silva · Nanoscale · 2013 · 5 · 70410.1039/C2NR32656F ↗
61. Sathaye · Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. · 2015 · 7 · 3410.1002/wnan.1299 ↗
62. Zelentsova · Chem. Inf. · 2006 · 3710.1002/chin.200608267 ↗
63. Gelain · Chem. Rev. · 2020 · 120 · 1343410.1021/acs.chemrev.0c00690 ↗
64. Puisto · Eur. Phys. J. E: Soft Matter Biol. Phys. · 2012 · 35 · 110.1140/epje/i2012-12006-1 ↗
65. Belyaev · Eur. J. Oncol. · 2010 · 5
66. Prasanna · Biochem. Biophys. Res. Commun. · 2020 · 534 · 95010.1016/j.bbrc.2020.10.065 ↗
67. Lee · Nanotechnology · 2018 · 29 · 34560410.1088/1361-6528/aac8f4 ↗
68. Ford · ACS Biomater. Sci. Eng. · 2021 · 7 · 417510.1021/acsbiomaterials.1c00589 ↗
69. Xue · Soc. Open Sci. · 2017 · 4 · 16069610.1098/rsos.160696 ↗
70. Jameson · ACS Chem. Neurosci. · 2012 · 3 · 80710.1021/cn300076x ↗
71. Seshadri · Methods Enzymol. · 1999 · 309 · 55910.1016/S0076-6879(99)09038-2 ↗
72. Lee · Sci. Rep. · 2015 · 5 · 1622010.1038/srep16220 ↗
73. Black · Biophys. J. · 2008 · 94 · 191610.1529/biophysj.107.107144 ↗
74. Yan · Chem. Soc. Rev. · 2010 · 39 · 352810.1039/b919449p ↗
75. Song · Korea Aust. Rheol. J. · 2017 · 29 · 28110.1007/s13367-017-0028-9 ↗
76. H.Abé , K.Hayashi and M.Sato , Data Book of Mechanical Properties of Living Cells, Tissues, and Organs , in Blood Vessels , Springer-Verlag, Tokyo , 1996 , ch. 2.2, pp. 25–114
77. Gjorevski · Biophys. J. · 2012 · 103 · 15210.1016/j.bpj.2012.05.048 ↗
78. G. A.Holzapfel and R. W.Ogden , Mechanics of Biological Tissue , Springer , 200610.1007/3-540-31184-X ↗
79. McManus · Nat. Nanotechnol. · 2017 · 12 · 34310.1038/nnano.2016.281 ↗
80. Sun · Int. J. Med. Sci. · 2018 · 15 · 25710.7150/ijms.21620 ↗
81. Yi · Bioact. Mater. · 2022 · 15 · 8210.1016/j.bioactmat.2021.12.005 ↗
82. Pandamooz · Biotechnol. Bioeng. · 2020 · 117 · 30510.1002/bit.27208 ↗
83. Fesenko · Bioelectrochem. Bioenerg. · 1999 · 49 · 2910.1016/S0302-4598(99)00058-6 ↗
84. H. D.Baille , Symposium Proceedings , ed. S. F. Cleary , 2010 , vol. 38 , pp. 728–736
85. Cutz · Lens Eye Toxic. Res. · 1989 · 6 · 729
86. Hendricks · Acc. Chem. Res. · 2017 · 50 · 244010.1021/acs.accounts.7b00297 ↗
87. Ji · ACS Omega · 2020 · 5 · 857210.1021/acsomega.9b04421 ↗
88. Yokoi · Proc. Natl. Acad. Sci. U. S. A. · 2005 · 102 · 841410.1073/pnas.0407843102 ↗
89. Di Rocco · Appl. Spectrosc. · 2001 · 55 · 82210.1366/0003702011952839 ↗
90. Usov · Macromolecules · 2015 · 48 · 126910.1021/ma502264c ↗
91. Raspa · Adv. Funct. Mater. · 2014 · 24 · 631710.1002/adfm.201400956 ↗