Microfluidic Synthesis of Ultrasmall Chitosan/Graphene Quantum Dots Particles for Intranasal Delivery in Alzheimer's Disease Treatment
Fariba Mohebichamkhorami
Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
Search for more papers by this authorMehrdad Faizi
Department of Pharmacology and Toxicology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, 19919-53381 Iran
Search for more papers by this authorMatin Mahmoudifard
Department of Industrial and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology, Tehran, 1497716316 Iran
Search for more papers by this authorArman Hajikarim-Hamedani
Faculty of Medicine, Tehran Medical Sciences, Islamic Azad University, Tehran, 1916893813 Iran
Search for more papers by this authorSeyedeh Sarvenaz Mohseni
Department of Pharmacology and Toxicology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, 19919-53381 Iran
Search for more papers by this authorAmirhossein Heidari
Faculty of Medicine, Tehran Medical Sciences, Islamic Azad University, Tehran, 1916893813 Iran
Search for more papers by this authorYekta Ghane
School of Medicine, Tehran University of Medical Sciences, Tehran, 1461884513 Iran
Search for more papers by this authorMona Khoramjouy
Phytochemistry Research Center, Shahid Beheshti University of Medical Sciences, Tehran, 19919-53381 Iran
Search for more papers by this authorMaryam Khayati
Department of Pharmaceutical Nanotechnology, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, 45139-56184 Iran
Pharmaceutical Nanotechnology Research Center, Zanjan University of Medical Sciences, Zanjan, 45139-56184 Iran
Search for more papers by this authorRasoul Ghasemi
Neurophysiology research center and Department of Physiology, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1985717443 Iran
Search for more papers by this authorCorresponding Author
Hakimeh Zali
Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
Medical Nanotechnology and Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
E-mail: [email protected]; [email protected][email protected]
Search for more papers by this authorCorresponding Author
Simzar Hosseinzadeh
Medical Nanotechnology and Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
E-mail: [email protected]; [email protected][email protected]
Search for more papers by this authorCorresponding Author
Ebrahim Mostafavi
Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, 94305 USA
Department of Medicine, Stanford University School of Medicine, Stanford, CA, 94305 USA
E-mail: [email protected]; [email protected][email protected]
Search for more papers by this authorFariba Mohebichamkhorami
Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
Search for more papers by this authorMehrdad Faizi
Department of Pharmacology and Toxicology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, 19919-53381 Iran
Search for more papers by this authorMatin Mahmoudifard
Department of Industrial and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology, Tehran, 1497716316 Iran
Search for more papers by this authorArman Hajikarim-Hamedani
Faculty of Medicine, Tehran Medical Sciences, Islamic Azad University, Tehran, 1916893813 Iran
Search for more papers by this authorSeyedeh Sarvenaz Mohseni
Department of Pharmacology and Toxicology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, 19919-53381 Iran
Search for more papers by this authorAmirhossein Heidari
Faculty of Medicine, Tehran Medical Sciences, Islamic Azad University, Tehran, 1916893813 Iran
Search for more papers by this authorYekta Ghane
School of Medicine, Tehran University of Medical Sciences, Tehran, 1461884513 Iran
Search for more papers by this authorMona Khoramjouy
Phytochemistry Research Center, Shahid Beheshti University of Medical Sciences, Tehran, 19919-53381 Iran
Search for more papers by this authorMaryam Khayati
Department of Pharmaceutical Nanotechnology, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, 45139-56184 Iran
Pharmaceutical Nanotechnology Research Center, Zanjan University of Medical Sciences, Zanjan, 45139-56184 Iran
Search for more papers by this authorRasoul Ghasemi
Neurophysiology research center and Department of Physiology, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1985717443 Iran
Search for more papers by this authorCorresponding Author
Hakimeh Zali
Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
Medical Nanotechnology and Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
E-mail: [email protected]; [email protected][email protected]
Search for more papers by this authorCorresponding Author
Simzar Hosseinzadeh
Medical Nanotechnology and Tissue Engineering Research Center, Shahid Beheshti University of Medical Sciences, Tehran, 1968917313 Iran
E-mail: [email protected]; [email protected][email protected]
Search for more papers by this authorCorresponding Author
Ebrahim Mostafavi
Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, 94305 USA
Department of Medicine, Stanford University School of Medicine, Stanford, CA, 94305 USA
E-mail: [email protected]; [email protected][email protected]
Search for more papers by this authorAbstract
Nanoparticles (NPs) based therapies for Alzheimer's disease (AD) attract interest due to their ability to pass across or bypass the blood-brain barrier. Chitosan (CS) NPs or graphene quantum dots (GQDs) are promising drug carriers with excellent physicochemical and electrical properties. The current study proposes the combination of CS and GQDs in ultrasmall NP form not as drug carriers but as theranostic agents for AD. The microfluidic-based synthesis of the CS/GQD NPs with optimized characteristics makes them ideal for transcellular transfer and brain targeting after intranasal (IN) delivery. The NPs have the ability to enter the cytoplasm of C6 glioma cells in vitro and show dose and time-dependent effects on the viability of the cells. IN administration of the NPs to streptozotocin (STZ) induced AD-like models lead to a significant number of entrances of the treated rats to the target arm in the radial arm water maze (RAWM) test. It shows the positive effect of the NPs on the memory recovery of the treated rats. The NPs are detectable in the brain via in vivo bioimaging due to GQDs as diagnostic markers. The noncytotoxic NPs localize in the myelinated axons of hippocampal neurons. They do not affect the clearance of amyloid β (Aβ) plaques at intercellular space. Moreover, they showed no positive impact on the enhancement of MAP2 and NeuN expression as markers of neural regeneration. The memory improvement in treated AD rats may be due to neuroprotection via the anti-inflammation effect and regulation of the brain tissue microenvironment that needs to be studied.
Conflict of Interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
- 1M. Bilal, M. Barani, F. Sabir, A. Rahdar, G. Z. Kyzas, NanoImpact 2020, 20, 100251.
- 2I. Javed, J. He, A. Kakinen, A. Faridi, W. Yang, T. P. Davis, P. C. Ke, P. Chen, ACS Appl. Mater. Interfaces 2019, 11, 10462.
- 3a) T. T. Nguyen, T. D. Nguyen, T. K. O. Nguyen, T. K. Vo, Biomed. Pharmacother. 2021, 139, 111623; b) S. H. Barage, K. D. Sonawane, Neuropeptides 2015, 52, 1.
- 4J. Trambauer, A. Fukumori, H. Steiner, Curr. Opin. Neurobiol. 2020, 61, 73.
- 5W. M. Pardridge, NeuroRx 2005, 2, 3.
- 6R. E. Becker, N. H. Greig, E. Giacobini, J. Alzheimers Dis. 2008, 15, 303.
- 7F. Khatami, in Neural Regenerative Nanomedicine, Elsevier, New York 2020, pp. 285–297.
10.1016/B978-0-12-820223-4.00009-7 Google Scholar
- 8E. Manek, G. A. Petroianu, Neural Regen Res 2021, 16, 2204.
- 9a) S. Zameer, J. Ali, D. Vohora, A. K. Najmi, M. Akhtar, J. Drug Targeting 2021, 29, 199; b) I. Younes, M. Rinaudo, Mar Drugs 2015, 13, 1133.
- 10A. Kassem, G. M. Ayoub, L. Malaeb, Sci. Total Environ. 2019, 668, 566.
- 11S. Yu, X. Xu, J. Feng, M. Liu, K. Hu, Int. J. Pharm. 2019, 560, 282.
- 12A. Jha, V. Ghormade, H. Kolge, K. M. Paknikar, J. Mater. Chem. B 2019, 7, 3362.
- 13a) K. Tak, R. Sharma, V. Dave, S. Jain, S. Sharma, ACS Chem. Neurosci. 2020, 11, 3741; b) T. Henna, K. Pramod, Mater. Sci. Eng., C 2020, 110, 110651.
- 14E. S. Seven, Y. Zhou, Y. B. Seven, G. S. Mitchell, R. M. Leblanc, FASEB J. 2019, 33, 785.
- 15D. Kim, J. M. Yoo, H. Hwang, J. Lee, S. H. Lee, S. P. Yun, M. J. Park, M. Lee, S. Choi, S. H. Kwon, Nat. Nanotechnol. 2018, 13, 812.
- 16Y. Liu, L.-P. Xu, W. Dai, H. Dong, Y. Wen, X. Zhang, Nanoscale 2015, 7, 19060.
- 17a) N. Shadjou, M. Hasanzadeh, M. Marandi, A. Hasanzadeh, J. Mater. Sci.: Mater. Electron. 2016, 27, 11834; b) G. Perini, V. Palmieri, G. Ciasca, M. De Spirito, M. Papi, Int. J. Mol. Sci. 2020, 21, 3712; c) Z. Niknam, F. Hosseinzadeh, F. Shams, L. Fath-Bayati, G. Nuoroozi, L. Mohammadi Amirabad, F. Mohebichamkhorami, S. Khakpour Naeimi, S. Ghafouri-Fard, H. Zali, J. Biomed. Mater. Res., Part A 2022, 110, 1695.
- 18S. Sharma, N. Singh, E. Nepovimova, J. Korabecny, K. Kuca, M. L. Satnami, K. K. Ghosh, J. Biomol. Struct. Dyn. 2020, 38, 1822.
- 19A. M. Bayoumy, A. Refaat, I. S. Yahia, H. Y. Zahran, H. Elhaes, M. A. Ibrahim, M. Shkir, Opt Quantum Electron 2020, 52, 1.
- 20L. Li, Nanomaterials 2020, 10, 559.
- 21H. Ren, X. Shen, J. Dai, G. Peng, L. Liang, J.-W. Shen, L. Zhang, J. Mol. Liq. 2020, 320, 113453.
- 22Y. Sheng, W. Dai, J. Gao, H. Li, W. Tan, J. Wang, L. Deng, Y. Kong, Mater. Sci. Eng., C 2020, 112, 110888.
- 23M. C. Veronesi, M. Alhamami, S. B. Miedema, Y. Yun, M. Ruiz-Cardozo, M. W. Vannier, Am. J. Nucl. Med. Mol. Imaging 2020, 10, 1.
- 24J. Ahn, J. Ko, S. Lee, J. Yu, Y. Kim, N. L. Jeon, Adv. Drug Delivery Rev. 2018, 128, 29.
- 25A. Francesko, V. F. Cardoso, S. Lanceros-Méndez, in Microfluidics for Pharmaceutical Applications, Elsevier, New York 2019, pp. 3–36.
10.1016/B978-0-12-812659-2.00001-6 Google Scholar
- 26Y. Gao, Q. Ma, J. Cao, Y. Wang, X. Yang, Q. Xu, Q. Liang, Y. Sun, Int. J. Pharm. 2021, 600, 120465.
- 27M. Farahani, F. Moradikhah, I. Shabani, R. K. Soflou, E. Seyedjafari, J. Drug Delivery Sci. Technol. 2021, 61, 102134.
- 28M. Hasanzadeh, N. Shadjou, M. Marandi, J. Nanosci. Nanotechnol. 2017, 17, 4598.
- 29G. Rassu, E. P. Porcu, S. Fancello, A. Obinu, N. Senes, G. Galleri, R. Migheli, E. Gavini, P. Giunchedi, Pharmaceutics 2019, 11, 8.
- 30J. Azevedo, R. Sizilio, M. Brito, A. Costa, M. Serafini, A. Araújo, M. Santos, A. Lira, R. Nunes, J. Therm. Anal. Calorim. 2011, 106, 685.
- 31D. R. Bhumkar, V. B. Pokharkar, AAPS PharmSciTech 2006, 7, E138.
- 32H. Alipanah, M. Farjam, E. Zarenezhad, G. Roozitalab, M. Osanloo, BMC Complement Med Ther 2021, 21, 1.
- 33S. A. Loutfy, H. M. A. El-Din, M. H. Elberry, N. G. Allam, M. Hasanin, A. M. Abdellah, Adv. Nat. Sci. Nanosci. Nanotechnol. 2016, 7, 035008.
10.1088/2043-6262/7/3/035008 Google Scholar
- 34Z. Tian, X. Yao, K. Ma, X. Niu, J. Grothe, Q. Xu, L. Liu, S. Kaskel, Y. Zhu, ACS Omega 2017, 2, 1249.
- 35M. A. Nazeer, E. Yilgör, I. Yilgör, Carbohydr. Polym. 2017, 175, 38.
- 36A. F. Martins, D. M. de Oliveira, A. G. Pereira, A. F. Rubira, E. C. Muniz, Int. J. Biol. Macromol. 2012, 51, 1127.
- 37D. Kumar, S. Dharmendra, M. Jhansee, N. Shrikant, S. Pandey, Int. Res. J. Pharm. 2011, 2, 145.
- 38M. Fernandes Queiroz, K. R. T. Melo, D. A. Sabry, G. L. Sassaki, H. A. O. Rocha, Mar. Drugs 2015, 13, 141.
- 39C. Lustriane, F. M. Dwivany, V. Suendo, M. Reza, J. Plant Biochem. Biotechnol. 2018, 45, 36.
10.5010/JPB.2018.45.1.036 Google Scholar
- 40S. Javanbakht, A. Shaabani, Int. J. Biol. Macromol. 2019, 123, 389.
- 41O. Lv, Y. Tao, Y. Qin, C. Chen, Y. Pan, L. Deng, L. Liu, Y. Kong, Mater. Sci. Eng., C 2016, 67, 478.
- 42N. Bion, J. Saussey, C. Hedouin, T. Seguelong, M. Daturi, Phys. Chem. Chem. Phys. 2001, 3, 4811.
- 43R. Justin, S. Román, D. Chen, K. Tao, X. Geng, R. T. Grant, S. MacNeil, K. Sun, B. Chen, RSC Adv. 2015, 5, 51934.
- 44A. Bonaccorso, T. Musumeci, M. Serapide, R. Pellitteri, I. Uchegbu, G. Puglisi, Colloids Surf., B 2017, 154, 297.
- 45E. F. Ribeiro, T. T. de Barros-Alexandrino, O. B. G. Assis, A. C. Junior, A. Quiles, I. Hernando, V. R. Nicoletti, Carbohydr. Polym. 2020, 250, 116878.
- 46D. Wang, J. F. Chen, L. Dai, Part. Part. Syst. Charact. 2015, 32, 515.
- 47a) D. T. Wiley, P. Webster, A. Gale, M. E. Davis, Proc. Natl. Acad. Sci. USA 2013, 110, 8662; b) O. Ziv-Polat, A. Shahar, I. Levy, H. Skaat, S. Neuman, F. Fregnan, S. Geuna, C. Grothe, K. Haastert-Talini, S. Margel, Biomed Res. Int. 2014, 2014, 267808.
- 48a) A. P. Reddy, J. Ravichandran, N. Carkaci-Salli, Bioch. Biophys. Acta 2020, 1866, 165506; b) F. Mohebichamkhorami, Z. Niknam, M. K. E. Heidarli, R. Ghasemi, S. Hosseinzadeh, S. S. Mohseni, A. Hajikarim-Hamedani, A. Heidari, Y. Ghane, M. Mahmoodifard, Iranian J. Pharma. Res. 2022, 21.
- 49C. Nemeth, A. Fine, A. Fatemi, Adv. Drug Delivery Rev. 2019, 148, 60.
- 50a) D. Ho, J. Zou, X. Chen, A. Munshi, N. M. Smith, V. Agarwal, S. I. Hodgetts, G. W. Plant, A. J. Bakker, A. R. Harvey, ACS Nano 2015, 9, 1767; b) E. Colombo, P. Feyen, M. R. Antognazza, G. Lanzani, F. Benfenati, Front. Neurosci. 2016, 10, 105.
- 51Q. Lyu, L. Peng, X. Hong, T. Fan, J. Li, Y. Cui, H. Zhang, J. Zhao, Biomaterials 2021, 270, 120682.
- 52S. Kaur, P. Manhas, A. Swami, R. Bhandari, K. K. Sharma, R. Jain, R. Kumar, S. K. Pandey, A. Kuhad, R. K. Sharma, Chem. Eng. J. 2018, 346, 630.
- 53L. N. Ramana, L. N. Dinh, V. Agarwal, Nanoscale Adv 2021, 3, 3513.
- 54Y. Decker, E. Németh, R. Schomburg, A. Chemla, L. Fülöp, M. D. Menger, Y. Liu, K. Fassbender, Neurobiol. Aging 2021, 101, 40.
- 55L. Ponto, S. Schultz, M. Jacob, Y. Menda, J. Wemmie, V. Magnotta, Soc. Nuclear Med. 2014, 55, 192.
- 56M. Hoop, F. Mushtaq, C. Hurter, X.-Z. Chen, B. J. Nelson, S. Pané, Nanoscale 2016, 8, 12723.
- 57Q. Gan, T. Wang, C. Cochrane, P. McCarron, Colloids Surf., B 2005, 44, 65.
- 58a) S.-X. Wang, Y.-B. Lu, X.-X. Wang, Y. Wang, Y.-J. Song, X. Wang, M. Nyamgerelt, Neural Regen Res. 2022, 17, 2117; b) Z. Yan, T. Ye, L. Yang, H. Jiang, C. Chen, S. Chen, Y. Qian, C. Fan, Adv. Funct. Mater. 2023, 33, 2211709.
- 59a) S. Khizar, N. Zine, A. Errachid, N. Jaffrezic-Renault, A. Elaissari, Electrophoresis 2022, 43, 819; b) Y. Liu, G. Yang, Y. Hui, S. Ranaweera, C. X. Zhao, Small 2022, 18, 2106580.
- 60N. B. Moghadam, M. Mahmoudifard, M. Karimi, M. Avatefi, J. Mater. Chem. B 2023, 11, 2568.
- 61J. W. Hickey, J. L. Santos, J.-M. Williford, H.-Q. Mao, J. Controlled Release 2015, 219, 536.
- 62G. Viola, C. G. Barracchia, R. Tira, F. Parolini, G. Leo, M. Bellanda, F. Munari, S. Capaldi, M. D'Onofrio, M. Assfalg, Nano Lett. 2022, 22, 8875.
- 63L.-A. Keller, O. Merkel, A. Popp, Drug Delivery Transl. Res. 2021, 12, 735.
- 64M. Mendes, A. Miranda, T. Cova, L. Goncalves, A. J. Almeida, J. J. Sousa, M. L. do Vale, E. F. Marques, A. Pais, C. Vitorino, Eur. J. Pharm. Sci. 2018, 117, 255.
- 65S. Dante, A. Petrelli, E. M. Petrini, R. Marotta, A. Maccione, A. Alabastri, A. Quarta, F. De Donato, T. Ravasenga, A. Sathya, ACS Nano 2017, 11, 6630.
- 66S. K. Jolodar, M. Bigdeli, A. H. Moghaddam, Mini-Rev. Med. Chem. 2021, 21, 1144.
- 67a) A. B. Engin, D. Nikitovic, M. Neagu, P. Henrich-Noack, A. O. Docea, M. I. Shtilman, K. Golokhvast, A. M. Tsatsakis, Part. Fibre Toxicol. 2017, 14, 22; b) R. Rampado, S. Crotti, P. Caliceti, S. Pucciarelli, M. Agostini, Front. Bioeng. Biotechnol. 2020, 8, 166.
- 68M. L. Formica, D. A. Real, M. L. Picchio, E. Catlin, R. F. Donnelly, A. J. Paredes, Appl. Mater. Today 2022, 29, 101631.
- 69R. Augustine, A. Hasan, R. Primavera, R. J. Wilson, A. S. Thakor, B. D. Kevadiya, Mater. Today Commun. 2020, 25, 101692.
- 70N. Hassan, M. Cordero, R. Sierpe, M. Almada, J. Juárez, M. Valdez, A. Riveros, E. Vargas, A. Abou-Hassan, J. Ruso, J. Mater. Chem. B 2018, 6, 5091.
- 71a) M. Ghavami, M. Rezaei, R. Ejtehadi, M. Lotfi, M. A. Shokrgozar, B. Abd Emamy, J. Raush, M. Mahmoudi, ACS Chem. Neurosci. 2013, 4, 375; b) B. Conti, M. Hansen, Cell 2013, 152, 671; c) R. Xiao, B. Zhang, Y. Dong, J. Gong, T. Xu, J. Liu, X. S. Xu, Cell 2013, 152, 806.
- 72H. Amiri, K. Saeidi, P. Borhani, A. Manafirad, M. Ghavami, V. Zerbi, ACS Chem. Neurosci. 2013, 4, 1417.
- 73H. Amiri, L. Bordonali, A. Lascialfari, S. Wan, M. P. Monopoli, I. Lynch, S. Laurent, M. Mahmoudi, Nanoscale 2013, 5, 8656.
- 74a) K. Giannousi, O. Antonoglou, C. Dendrinou-Samara, ACS Chem. Neurosci. 2019, 10, 3796; b) M. Mahmoudi, F. Quinlan-Pluck, M. P. Monopoli, S. Sheibani, H. Vali, K. A. Dawson, I. Lynch, ACS Chem. Neurosci. 2013, 4, 475.
- 75J. Kopeček, Adv. Drug Delivery Rev. 2013, 65, 49.
- 76G. Rassu, E. Soddu, M. Cossu, E. Gavini, P. Giunchedi, A. Dalpiaz, J Drug Deliv Sci Technol 2016, 32, 77.
- 77a) S. Pleskova, E. Mikheeva, E. Gornostaeva, Cell. Mol. Toxicol. Nanopart. 2018, 323; b) M. Nurunnabi, Z. Khatun, K. M. Huh, S. Y. Park, D. Y. Lee, K. J. Cho, Y.-k. Lee, ACS Nano 2013, 7, 6858.
- 78M. C. Biswas, M. T. Islam, P. K. Nandy, M. M. Hossain, ACS Mater. Lett. 2021, 3, 889.
- 79J. Loureiro, S. P. Miguel, I. J. Seabra, M. P. Ribeiro, P. Coutinho, Pharmaceutics 2022, 14, 920.
- 80Y. Ji, Y.-M. Li, J. G. Seo, T.-S. Jang, J. C. Knowles, S. H. Song, J.-H. Lee, Nanomaterials 2021, 11, 1446.
- 81M. Zhang, L. Bai, W. Shang, W. Xie, H. Ma, Y. Fu, D. Fang, H. Sun, L. Fan, M. Han, J. Mater. Chem. 2012, 22, 7461.
- 82W. Shang, X. Zhang, M. Zhang, Z. Fan, Y. Sun, M. Han, L. Fan, Nanoscale 2014, 6, 5799.
- 83X. Yuan, Z. Liu, Z. Guo, Y. Ji, M. Jin, X. Wang, Nanoscale Res. Lett. 2014, 9, 108.
- 84A. Javia, H. Thakkar, J. Microencapsulation 2017, 34, 644.
- 85M. K. Kumawat, M. Thakur, R. B. Gurung, R. Srivastava, Sci. Rep. 2017, 7, 15858.
- 86H. Liu, B. Xie, X. Dong, L. Zhang, Y. Wang, F. Liu, Y. Sun, React. Funct. Polym. 2016, 103, 108.
- 87M. Huang, E. Khor, L.-Y. Lim, Pharm. Res. 2004, 21, 344.
- 88S. Xiao, D. Zhou, P. Luan, B. Gu, L. Feng, S. Fan, W. Liao, W. Fang, L. Yang, E. Tao, Biomaterials 2016, 106, 98.
- 89Z. Zheng, M. Liu, S. Guo, J. Wu, D. Lu, G. Li, S. Liu, X. Wang, D. Kaplan, J. Mater. Chem. B 2015, 3, 6509.
- 90A. B. Siddique, A. K. Pramanick, S. Chatterjee, M. Ray, Sci. Rep. 2018, 8, 9770.
- 91S. Baradaran, A. Hajizadeh Moghaddam, S. Khanjani Jelodar, N. Moradi-Kor, J. Inflamm. Res. 2020, 13, 45.
- 92E. Manek, F. Darvas, G. A. Petroianu, Molecules 2020, 25, 4866.
- 93a) M. Mahmoudifard, M. Soleimani, S. Hatamie, S. Zamanlui, P. Ranjbarvan, M. Vossoughi, S. Hosseinzadeh, Biomed. Mater. 2016, 11, 025006; b) Z. Sun, D. K. James, J. M. Tour, J. Phys. Chem. Lett. 2011, 2, 2425; c) N. Zaaba, K. Foo, U. Hashim, S. Tan, W.-W. Liu, C. Voon, Proc. Eng. 2017, 184, 469.
- 94S. Hosseinzadeh, S. M. Rezayat, A. Giaseddin, A. Aliyan, M. Soleimani, J. Biomater. Appl. 2018, 32, 853.
- 95S. Jeibouei, A. Hojat, E. Mostafavi, A. R. Aref, A. Kalbasi, V. Niazi, M. Ajoudanian, F. Mohammadi, F. Saadati, S. M. Javadi, Sci. Rep. 2022, 12, 7668.
- 96A. Hajizadeh Moghaddam, H. Ahmadnia, S. K. Jelodar, M. Ranjbar, Neurol Res 2020, 42, 477.
- 97a) M. Khoramjouy, N. Naderi, F. Kobarfard, E. Heidarli, M. Faizi, Neurotox Res 2021, 39, 277; b) S. M. Hosseini, A. Golaghaei, E. Nassireslami, N. Naderi, H. G. Pourbadie, M. Rahimzadegan, S. Mohammadi, Acta Neurobiol. Exp. 2019, 79, 73; c) L. E. Chaby, M. J. Sheriff, A. M. Hirrlinger, J. Lim, T. B. Fetherston, V. A. Braithwaite, PLoS One 2015, 10, e0141908.