EFFECTS OF RIBOSE-INDUCED GLYCATION ON THE ELASTIC MODULUS OF COLLAGEN FIBRILS OBSERVED BY ATOMIC FORCE MICROSCOPY
DOI:
https://doi.org/10.58407/bht.1.24.13Keywords:
glycation, ribose, common digital extensor (CDE), superficial digital flexor (SDF), tendons, atomic force microscopeAbstract
The interplay between diabetes mellitus and the structural integrity of collagen has significant implications for tissue functionality and disease progression.
The aim of this study was to empirically investigate the effects of ribose-induced glycation on the biomechanical properties of collagen fibrils, using atomic force microscopy for precise measurements.
Methodology. We used collagen fibrils from the common digital extensor (CDE) and superficial digital flexor (SDF) tendons of an adult bovine model to mimic the glycation processes that occur in diabetic pathology. The samples underwent controlled glycation by incubation with ribose for 24 hours and 14 days compared to phosphate buffered saline treated controls. A Bioscope Catalyst atomic force microscope (Bruker, USA) was used for all atomic force microscopy imaging in this study.
Scientific novelty. Our results show a marked increase in the elastic modulus of collagen fibrils after ribose treatment, indicating stiffening with glycation. Notably, SDF fibrils showed a greater increase in stiffness after 24 hours of ribose exposure compared to CDE fibrils, suggesting variations in glycation rates relative to fibril anatomy. Statistical analyses confirmed the significance of these findings and provided a model for understanding similar processes in human diabetes.
Conclusions. The different response to glycation observed between CDE and SDF fibrils prompts further investigation into the role of anatomical and structural factors in glycation susceptibility. Identification of tissues at higher risk of glycation-induced damage could lead to the development of targeted prevention strategies for diabetic complications. In addition, the potential for pharmacological intervention to inhibit glycation processes or enhance advanced glycation end products (AGEs) degradation offers a promising avenue for mitigating the progression of diabetes-related complications. The results of this study highlight the potential of ribose-induced changes in collagen as a model for diabetes-related tissue changes and propose a mechanistic framework that could guide the development of interventions aimed at mitigating the effects of collagen-related diabetic complications.
Downloads
References
Adamska, O., Stolarczyk, A., Gondek, A., Maciąg, B., Świderek, J., Czuchaj, P., & Modzelewski, K. (2022). Ligament Alteration in Diabetes Mellitus. Journal of clinical medicine, 11(19), 5719. https://doi.org/10.3390/jcm11195719.
Arseni, L., Lombardi, A., & Orioli, D. (2018). From Structure to Phenotype: Impact of Collagen Alterations on Human Health. International journal of molecular sciences, 19(5), 1407. https://doi.org/10.3390/ijms19051407.
Bai, P., Phua, K., Hardt, T., Cernadas, M., & Brodsky, B. (1992). Glycation alters collagen fibril organization. Connective tissue research, 28(1-2), 1–12. https://doi.org/10.3109/ 03008209209014224.
Baldwin, S. J., Sampson, J., Peacock, C. J., Martin, M. L., Veres, S. P., Lee, J. M., & Kreplak, L. (2020). A new longitudinal variation in the structure of collagen fibrils and its relationship to locations of mechanical damage susceptibility. Journal of the mechanical behavior of biomedical materials, 110, 103849. https://doi.org/10.1016/j.jmbbm.2020.103849.
Banday, M. Z., Sameer, A. S., & Nissar, S. (2020). Pathophysiology of diabetes: An overview. Avicenna journal of medicine, 10(4), 174–188. https://doi.org/10.4103/ajm.ajm_53_20.
Bansode, S., Bashtanova, U., Li, R., Clark, J., Müller, K. H., Puszkarska, A., Goldberga, I., Chetwood, H. H., Reid, D. G., Colwell, L. J., Skepper, J. N., Shanahan, C. M., Schitter, G., Mesquida, P., & Duer, M. J. (2020). Glycation changes molecular organization and charge distribution in type I collagen fibrils. Scientific reports, 10(1), 3397. https://doi.org/10.1038/s41598-020-60250-9.
Birch, H. L. (2007). Tendon matrix composition and turnover in relation to functional requirements. International journal of experimental pathology, 88(4), 241–248. https:// doi.org/10.1111/j.1365-2613.2007.00552.x.
Bondarenko, L. (2019). Diabetes and Collagen: Interrelations. Avicenna Journal of Medical Biochemistry, 7(2), 64-71. https://doi.org/10.34172/ajmb.2019.12.
Breidenbach, A. P., Gilday, S. D., Lalley, A. L., Dyment, N. A., Gooch, C., Shearn, J. T., & Butler, D. L. (2014). Functional tissue engineering of tendon: Establishing biological success criteria for improving tendon repair. Journal of biomechanics, 47(9), 1941–1948. https://doi.org/10.1016/ j.jbiomech.2013.10.023.
Burgess, J. L., Wyant, W. A., Abdo Abujamra, B., Kirsner, R. S., & Jozic, I. (2021). Diabetic Wound-Healing Science. Medicina (Kaunas, Lithuania), 57(10), 1072. https://doi.org/ 10.3390/medicina57101072.
Chaudhuri, J., Bains, Y., Guha, S., Kahn, A., Hall, D., Bose, N., Gugliucci, A., & Kapahi, P. (2018). The Role of Advanced Glycation End Products in Aging and Metabolic Diseases: Bridging Association and Causality. Cell metabolism, 28(3), 337–352. https://doi.org/10.1016/ j.cmet.2018.08.014.
Chen, C. Y., Zhang, J. Q., Li, L., Guo, M. M., He, Y. F., Dong, Y. M., Meng, H., & Yi, F. (2022). Advanced Glycation End Products in the Skin: Molecular Mechanisms, Methods of Measurement, and Inhibitory Pathways. Frontiers in medicine, 9, 837222. https://doi.org/ 10.3389/fmed.2022.837222.
Chilukuri, H., Kulkarni, M. J., & Fernandes, M. (2018). Revisiting amino acids and peptides as anti-glycation agents. MedChemComm, 9(4), 614–624. https://doi.org/10.1039/c7md 00514h.
Cortet, B., Lucas, S., Legroux-Gerot, I., Penel, G., Chauveau, C., & Paccou, J. (2019). Bone disorders associated with diabetes mellitus and its treatments. Joint bone spine, 86(3), 315–320. https://doi.org/10.1016/j.jbspin.2018.08.002.
David, P., Singh, S., & Ankar, R. (2023). A Comprehensive Overview of Skin Complications in Diabetes and Their Prevention. Cureus, 15(5), e38961. https://doi.org/10.7759/cureus. 38961.
Eid, S., Sas, K. M., Abcouwer, S. F., Feldman, E. L., Gardner, T. W., Pennathur, S., & Fort, P. E. (2019). New insights into the mechanisms of diabetic complications: role of lipids and lipid metabolism. Diabetologia, 62(9), 1539–1549. https://doi.org/10.1007/s00125-019-4959-1.
El-Bahy, A. A. Z., Aboulmagd, Y. M., & Zaki, M. (2018). Diabetex: A novel approach for diabetic wound healing. Life sciences, 207, 332–339. https://doi.org/10.1016/j.lfs.2018.06.020.
Farzadfard, A., König, A., Petersen, S. V., Nielsen, J., Vasili, E., Dominguez-Meijide, A., Buell, A. K., Outeiro, T. F., & Otzen, D. E. (2022). Glycation modulates alpha-synuclein fibrillization kinetics: A sweet spot for inhibition. The Journal of biological chemistry, 298(5), 101848. https://doi.org/10.1016/j.jbc.2022.101848.
Fessel, G., Li, Y., Diederich, V., Guizar-Sicairos, M., Schneider, P., Sell, D. R., Monnier, V. M., & Snedeker, J. G. (2014). Advanced glycation end-products reduce collagen molecular sliding to affect collagen fibril damage mechanisms but not stiffness. PloS one, 9(11), e110948. https://doi.org/ 10.1371/journal.pone.0110948.
Fournet, M., Bonté, F., & Desmoulière, A. (2018). Glycation Damage: A Possible Hub for Major Pathophysiological Disorders and Aging. Aging and disease, 9(5), 880–900. https://doi.org/ 10.14336/AD.2017.1121.
Fu, M. X., Wells-Knecht, K. J., Blackledge, J. A., Lyons, T. J., Thorpe, S. R., & Baynes, J. W. (1994). Glycation, glycoxidation, and cross-linking of collagen by glucose. Kinetics, mechanisms, and inhibition of late stages of the Maillard reaction. Diabetes, 43(5), 676–683. https:// doi.org/10.2337/diab.43.5.676.
Gautieri, A., Passini, F. S., Silván, U., Guizar-Sicairos, M., Carimati, G., Volpi, P., Moretti, M., Schoenhuber, H., Redaelli, A., Berli, M., & Snedeker, J. G. (2017). Advanced glycation end-products: Mechanics of aged collagen from molecule to tissue. Matrix biology: journal of the International Society for Matrix Biology, 59, 95–108. https://doi.org/10.1016/j.matbio. 2016.09.001.
Gisbert, V. G., Benaglia, S., Uhlig, M. R., Proksch, R., & Garcia, R. (2021). High-Speed Nanomechanical Mapping of the Early Stages of Collagen Growth by Bimodal Force Microscopy. ACS nano, 15(1), 1850–1857. https://doi.org/10.1021/acsnano.0c10159.
Gkogkolou, P., & Böhm, M. (2012). Advanced glycation end products: Key players in skin aging? Dermato-endocrinology, 4(3), 259–270. https://doi.org/10.4161/derm.22028.
Gsell, K. Y., Veres, S. P., & Kreplak, L. (2023). Single collagen fibrils isolated from high stress and low stress tendons show differing susceptibility to enzymatic degradation by the interstitial collagenase matrix metalloproteinase-1 (MMP-1). Matrix biology plus, 18, 100129. https://doi.org/10.1016/ j.mbplus.2023.100129.
Haase, K., & Pelling, A. E. (2015). Investigating cell mechanics with atomic force microscopy. Journal of the Royal Society, Interface, 12(104), 20140970. https://doi.org/10.1098/ rsif.2014.0970.
Han, B., Nia, H. T., Wang, C., Chandrasekaran, P., Li, Q., Chery, D. R., Li, H., Grodzinsky, A. J., & Han, L. (2017). AFM-Nanomechanical Test: An Interdisciplinary Tool That Links the Understanding of Cartilage and Meniscus Biomechanics, Osteoarthritis Degeneration, and Tissue Engineering. ACS biomaterials science & engineering, 3(9), 2033–2049. https://doi.org/10.1021/ acsbiomaterials.7b00307.
Jahan, H., & Choudhary, M. I. (2015). Glycation, carbonyl stress and AGEs inhibitors: a patent review. Expert opinion on therapeutic patents, 25(11), 1267–1284. https://doi.org/ 10.1517/13543776.2015.1076394.
Jones, M. S., Rivera, M., Puccinelli, C. L., Wang, M. Y., Williams, S. J., & Barber, A. E. (2014). Targeted amino acid supplementation in diabetic foot wounds: pilot data and a review of the literature. Surgical infections, 15(6), 708–712. https://doi.org/10.1089/sur.2013.158.
Kanazawa, I. (2017). Interaction between bone and glucose metabolism [Review]. Endocrine journal, 64(11), 1043–1053. https://doi.org/10.1507/endocrj.EJ17-0323.
Kang, Q., & Yang, C. (2020). Oxidative stress and diabetic retinopathy: Molecular mechanisms, pathogenetic role and therapeutic implications. Redox biology, 37, 101799. https://doi.org/10.1016/j.redox.2020.101799.
Kannus, P. (2000). Structure of the tendon connective tissue. Scandinavian journal of medicine & science in sports, 10(6), 312–320. https://doi.org/10.1034/j.1600-0838.2000.01000 6312.x.
Khalid, M., Petroianu, G., & Adem, A. (2022). Advanced Glycation End Products and Diabetes Mellitus: Mechanisms and Perspectives. Biomolecules, 12(4), 542. https://doi.org/10.3390/ biom12040542.
Kohn, J. C., Lampi, M. C., & Reinhart-King, C. A. (2015). Age-related vascular stiffening: causes and consequences. Frontiers in genetics, 6, 112. https://doi.org/10.3389/fgene.2015.00112.
Kontomaris, S. V., Stylianou, A., & Malamou, A. (2022). Atomic Force Microscopy Nanoin¬dentation Method on Collagen Fibrils. Materials (Basel, Switzerland), 15(7), 2477. https://doi.org/10.3390/ma15072477.
Lee, J. M., & Veres, S. P. (2019). Advanced glycation end-product cross-linking inhibits biomechanical plasticity and characteristic failure morphology of native tendon. Journal of applied physiology (Bethesda, Md.: 1985), 126(4), 832–841. https://doi.org/10.1152/ japplphysiol.00430.2018.
Lee, J., Yun, J. S., & Ko, S. H. (2022). Advanced Glycation End Products and Their Effect on Vascular Complications in Type 2 Diabetes Mellitus. Nutrients, 14(15), 3086. https://doi.org/10.3390/nu14153086.
Liao, H., Zakhaleva, J., & Chen, W. (2009). Cells and tissue interactions with glycated collagen and their relevance to delayed diabetic wound healing. Biomaterials, 30(9), 1689–1696. https://doi.org/10.1016/j.biomaterials.2008.11.038.
Lichtwark, G. A., & Wilson, A. M. (2005). In vivo mechanical properties of the human Achilles tendon during one-legged hopping. The Journal of experimental biology, 208(Pt 24), 4715–4725. https://doi.org/10.1242/jeb.01950.
Liu, J., Pan, S., Wang, X., Liu, Z., & Zhang, Y. (2023). Role of advanced glycation end products in diabetic vascular injury: molecular mechanisms and therapeutic perspectives. European journal of medical research, 28(1), 553. https://doi.org/10.1186/s40001-023-01431-w.
Makarova, N., Lekka, M., Gnanachandran, K., & Sokolov, I. (2023). Mechanical Way To Study Molecular Structure of Pericellular Layer. ACS applied materials & interfaces, 15(30), 35962–35972. https://doi.org/10.1021/acsami.3c06341.
Masenga, S. K., & Kirabo, A. (2023). Hypertensive heart disease: risk factors, complications and mechanisms. Frontiers in cardiovascular medicine, 10, 1205475. https://doi.org/ 10.3389/fcvm.2023.1205475.
Maugis, D., & Barquins, M. (1978). Fracture mechanics and the adherence of viscoelastic bodies. Journal of Physics D: Applied Physics, 11(14), 1989. https://doi.org/10.1088/0022-3727/11/14/011.
McKay, T. B., Priyadarsini, S., & Karamichos, D. (2019). Mechanisms of Collagen Crosslinking in Diabetes and Keratoconus. Cells, 8(10), 1239. https://doi.org/10.3390/cells8101239.
Mendes, A. L., Miot, H. A., & Haddad, V., Junior (2017). Diabetes mellitus and the skin. Anais brasileiros de dermatologia, 92(1), 8–20. https://doi.org/10.1590/abd1806-4841.20175514
Mieczkowski, M., Mrozikiewicz-Rakowska, B., Kowara, M., Kleibert, M., & Czupryniak, L. (2022). The Problem of Wound Healing in Diabetes-From Molecular Pathways to the Design of an Animal Model. International journal of molecular sciences, 23(14), 7930. https:// doi.org/10.3390/ijms23147930.
Monnier, V. M., Bautista, O., Kenny, D., Sell, D. R., Fogarty, J., Dahms, W., Cleary, P. A., Lachin, J., & Genuth, S. (1999). Skin collagen glycation, glycoxidation, and crosslinking are lower in subjects with long-term intensive versus conventional therapy of type 1 diabetes: relevance of glycated collagen products versus HbA1c as markers of diabetic complications. DCCT Skin Collagen Ancillary Study Group. Diabetes Control and Complications Trial. Diabetes, 48(4), 870–880. https://doi.org/10.2337/diabetes.48.4.870.
Mull, V., & Kreplak, L. (2022). Adhesion force microscopy is sensitive to the charge distribution at the surface of single collagen fibrils. Nanoscale advances, 4(22), 4829–4837. https://doi.org/10.1039/d2na00514j.
Murray, C. E., & Coleman, C. M. (2019). Impact of Diabetes Mellitus on Bone Health. International journal of molecular sciences, 20(19), 4873. https://doi.org/10.3390/ijms 20194873.
Napoli, N., Chandran, M., Pierroz, D. D., Abrahamsen, B., Schwartz, A. V., Ferrari, S. L., & IOF Bone and Diabetes Working Group. (2017). Mechanisms of diabetes mellitus-induced bone fragility. Nature reviews. Endocrinology, 13(4), 208–219. https://doi.org/10.1038/nrendo. 2016.153.
Negre-Salvayre, A., Salvayre, R., Augé, N., Pamplona, R., & Portero-Otín, M. (2009). Hyper¬glycemia and glycation in diabetic complications. Antioxidants & redox signaling, 11(12), 3071–3109. https://doi.org/10.1089/ars.2009.2484.
Nichols, A. E. C., Oh, I., & Loiselle, A. E. (2020). Effects of Type II Diabetes Mellitus on Tendon Homeostasis and Healing. Journal of orthopaedic research: official publication of the Orthopaedic Research Society, 38(1), 13–22. https://doi.org/10.1002/jor.24388.
No, Y. J., Castilho, M., Ramaswamy, Y., & Zreiqat, H. (2020). Role of Biomaterials and Controlled Architecture on Tendon/Ligament Repair and Regeneration. Advanced materials (Deerfield Beach, Fla.), 32(18), e1904511. https://doi.org/10.1002/adma.201904511
Onursal, C., Dick, E., Angelidis, I., Schiller, H. B., & Staab-Weijnitz, C. A. (2021). Collagen Biosynthesis, Processing, and Maturation in Lung Ageing. Frontiers in medicine, 8, 593874. https://doi.org/10.3389/fmed.2021.593874.
Palermo, A., D'Onofrio, L., Buzzetti, R., Manfrini, S., & Napoli, N. (2017). Pathophysiology of Bone Fragility in Patients with Diabetes. Calcified tissue international, 100(2), 122–132. https://doi.org/10.1007/s00223-016-0226-3.
Patel, S., Srivastava, S., Singh, M. R., & Singh, D. (2019). Mechanistic insight into diabetic wounds: Pathogenesis, molecular targets and treatment strategies to pace wound healing. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 112, 108615. https://doi.org/10.1016/j.biopha.2019.108615.
Picke, A. K., Campbell, G., Napoli, N., Hofbauer, L. C., & Rauner, M. (2019). Update on the impact of type 2 diabetes mellitus on bone metabolism and material properties. Endocrine connections, 8(3), R55–R70. https://doi.org/10.1530/EC-18-0456.
Poznyak, A. V., Sadykhov, N. K., Kartuesov, A. G., Borisov, E. E., Melnichenko, A. A., Grechko, A. V., & Orekhov, A. N. (2022). Hypertension as a risk factor for atherosclerosis: Cardiovascular risk assessment. Frontiers in cardiovascular medicine, 9, 959285. https://doi.org/10.3389/ fcvm.2022.959285.
Rubin, J., Nambi, V., Chambless, L. E., Steffes, M. W., Juraschek, S. P., Coresh, J., Sharrett, A. R., & Selvin, E. (2012). Hyperglycemia and arterial stiffness: the Atherosclerosis Risk in the Communities study. Atherosclerosis, 225(1), 246–251. https://doi.org/10.1016/ j.atherosclerosis. 2012.09.003.
Saito, M., & Marumo, K. (2015). Effects of Collagen Crosslinking on Bone Material Properties in Health and Disease. Calcified tissue international, 97(3), 242–261. https://doi.org/ 10.1007/s00223-015-9985-5.
San Antonio, J. D., Jacenko, O., Fertala, A., & Orgel, J. P. R. O. (2020). Collagen Structure-Function Mapping Informs Applications for Regenerative Medicine. Bioengineering (Basel, Switzerland), 8(1), 3. https://doi.org/10.3390/bioengineering8010003.
Sarrigiannidis, S. O., Rey, J. M., Dobre, O., González-García, C., Dalby, M. J., & Salmeron-Sanchez, M. (2021). A tough act to follow: collagen hydrogel modifications to improve mechanical and growth factor loading capabilities. Materials today. Bio, 10, 100098. https://doi.org/10.1016/ j.mtbio.2021.100098.
Singh, V. P., Bali, A., Singh, N., & Jaggi, A. S. (2014). Advanced glycation end products and diabetic complications. The Korean journal of physiology & pharmacology: official journal of the Korean Physiological Society and the Korean Society of Pharmacology, 18(1), 1–14. https://doi.org/10.4196/kjpp.2014.18.1.1.
Snedeker, J. G., & Gautieri, A. (2014). The role of collagen crosslinks in ageing and diabetes – the good, the bad, and the ugly. Muscles, ligaments and tendons journal, 4(3), 303–308.
Sternberg, M., Cohen-Forterre, L., & Peyroux, J. (1985). Connective tissue in diabetes mellitus: biochemical alterations of the intercellular matrix with special reference to proteoglycans, collagens and basement membranes. Diabete & metabolisme, 11(1), 27–50.
Stylianou, A., Kontomaris, S. V., Grant, C., & Alexandratou, E. (2019). Atomic Force Microscopy on Biological Materials Related to Pathological Conditions. Scanning, 2019, 8452851. https://doi.org/10.1155/2019/8452851.
Tai, Y., Zhang, Z., Liu, Z., Li, X., Yang, Z., Wang, Z., An, L., Ma, Q., & Su, Y. (2024). D-ribose metabolic disorder and diabetes mellitus. Molecular biology reports, 51(1), 220. https://doi.org/10.1007/s11033-023-09076-y.
Tuttle, K. R., Agarwal, R., Alpers, C. E., Bakris, G. L., Brosius, F. C., Kolkhof, P., & Uribarri, J. (2022). Molecular mechanisms and therapeutic targets for diabetic kidney disease. Kidney international, 102(2), 248–260. https://doi.org/10.1016/j.kint.2022.05.012.
Twarda-Clapa, A., Olczak, A., Białkowska, A. M., & Koziołkiewicz, M. (2022). Advanced Glycation End-Products (AGEs): Formation, Chemistry, Classification, Receptors, and Diseases Related to AGEs. Cells, 11(8), 1312. https://doi.org/10.3390/cells11081312.
Vaidya, R., Lake, S. P., & Zellers, J. A. (2023). Effect of Diabetes on Tendon Structure and Function: Not Limited to Collagen Crosslinking. Journal of diabetes science and technology, 17(1), 89–98. https://doi.org/10.1177/19322968221100842.
Van Putte, L., De Schrijver, S., & Moortgat, P. (2016). The effects of advanced glycation end products (AGEs) on dermal wound healing and scar formation: a systematic review. Scars, burns & healing, 2, 2059513116676828. https://doi.org/10.1177/2059513116676828.
Vithian, K., & Hurel, S. (2010). Microvascular complications: pathophysiology and manage¬ment. Clinical medicine (London, England), 10(5), 505–509. https://doi.org/10.7861/ clinmedicine.10-5-505.
Wilson, A. M., McGuigan, M. P., Su, A., & van Den Bogert, A. J. (2001). Horses damp the spring in their step. Nature, 414(6866), 895–899. https://doi.org/10.1038/414895a.
Wu, B., Fu, Z., Wang, X., Zhou, P., Yang, Q., Jiang, Y., & Zhu, D. (2022). A narrative review of diabetic bone disease: Characteristics, pathogenesis, and treatment. Frontiers in endocrinology, 13, 1052592. https://doi.org/10.3389/fendo.2022.1052592.
Younus, H., & Anwar, S. (2016). Prevention of non-enzymatic glycosylation (glycation): Implication in the treatment of diabetic complication. International journal of health sciences, 10(2), 261–277.
Zgutka, K., Tkacz, M., Tomasiak, P., & Tarnowski, M. (2023). A Role for Advanced Glycation End Products in Molecular Ageing. International journal of molecular sciences, 24(12), 9881. https://doi.org/10.3390/ijms24129881.
Zhang, S., Ju, W., Chen, X., Zhao, Y., Feng, L., Yin, Z., & Chen, X. (2021). Hierarchical ultrastructure: An overview of what is known about tendons and future perspective for tendon engineering. Bioactive materials, 8, 124–139. https://doi.org/10.1016/j.bioactmat. 2021.06.007.
Zheng, W., Li, H., Go, Y., Chan, X. H. F., Huang, Q., & Wu, J. (2022). Research Advances on the Damage Mechanism of Skin Glycation and Related Inhibitors. Nutrients, 14(21), 4588. https://doi.org/10.3390/nu14214588
Zhong, J., Huang, W., & Zhou, H. (2023). Multifunctionality in Nature: Structure-Function Relationships in Biological Materials. Biomimetics (Basel, Switzerland), 8(3), 284. https://doi.org/10.3390/biomimetics8030284.
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Катерина Топчило, Галина Ткаченко
This work is licensed under a Creative Commons Attribution 4.0 International License.
