AccScience Publishing / IJB / Online First / DOI: 10.36922/ijb.3751
RESEARCH ARTICLE

3D-bioprinted model of adult neural stem cell microenvironment in Alzheimer’s disease

Natalia Dall’Agnol Ferreira1,2 Paula Scanavez Ferreira1,2 Cristina Pacheco Soares3 Marimelia Aparecida Porcionatto1,2* Geisa Rodrigues Salles1,2,3*
Show Less
1 Department of Biochemistry, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, Brazil
2 National Institute of Science and Technology in Modeling Human Complex Diseases with 3D Platforms (INCT Model 3D), São Paulo, Brazil
3 Research & Development Institute, Universidade do Vale do Paraíba, São José dos Campos, São Paulo, Brazil
IJB 2024, 10(5), 3751 https://doi.org/10.36922/ijb.3751
Submitted: 24 May 2024 | Accepted: 19 July 2024 | Published: 13 September 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

Neurogenesis plays a major role in neuroplasticity and memory. In adult human and mouse brains, neural stem cells (NSCs) are mainly distributed in two extensively characterized neurogenic niches: the subgranular zone (SGZ) of the hippocampus and the subventricular zone (SVZ) of the lateral ventricles. Impaired neurogenesis is one of the consequences of Alzheimer’s disease (AD), contributing to cognitive decline and progressive memory loss. Developing new in vitro models that resemble this three-dimensional (3D) structure is fundamental for enhancing our understanding of the SVZ neurogenic niche dynamics in AD. Herein, we produced and characterized a 3D-bioprinted model of the adult SVZ neurogenic niche containing amyloid β (Aβ) oligomers, mimicking the NSC microenvironment in AD. In this model, Aβ oligomers induce oxidative stress and reduce the proliferative potential of NSCs, while stimulating neuronal differentiation. We hypothesize that these events are an early attempt of adult NSCs to compensate for neuronal death in AD pathogenesis. Our 3D model simulates the NSC niche physiology, reproducing an early response of NSCs in AD, strengthening the importance of studying the potential of neurogenesis in neurodegeneration.

Keywords
Bioprinting
Neurogenic niche
Alzheimer’s disease
Amyloid beta
Neural stem cells
Subventricular zone
Funding
This study was supported by grants from (i) the São Paulo Research Foundation (FAPESP): Grants 2022/08664-4 (GRS), 2023/08040-3 (NDF), and 2018/12605-8 (MAP); and (ii) the Brazilian National Council for Scientific and Technological Development (CNPq): 406258/2022-8, INCT Model 3D, and 152384/2024-3 (GRS).
Conflict of interest
The authors declare that they have no conflicts of interest. The research was conducted without any commercial or financial relationship.
References
  1. Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, et al. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med. 2019;25(4):554-560. doi: 10.1038/s41591-019-0375-9
  2. Selkoe DJ. Alzheimer’s disease: genes, proteins, and therapy. J Physiol Rev. 2001;81(2):741-766. doi: 10.1152/physrev.2001.81.2.741
  3. Li Puma DD, Piacentini R, Grassi C. Does impairment of adult neurogenesis contribute to pathophysiology of Alzheimer’s disease? A still open question. J Front Mol Neurosci. 2021;13:578211. doi: 10.3389/fnmol.2020.578211
  4. Kim HS, Shin SM, Kim S, Nam Y, Yoo A, Moon M. Relationship between adult subventricular neurogenesis and Alzheimer’s disease: pathologic roles and therapeutic implications. Front Aging Neurosci. 2022;14:1002281. doi: 10.3389/fnagi.2022.1002281
  5. Selkoe DJ. Alzheimer’s disease. Cold Spring Harb Perspect Biol. 2011;3:a004457. doi: 10.1101/cshperspect.a004457
  6. Culig L, Chu X, Bohr VA. Neurogenesis in aging and age-related neurodegenerative diseases. Ageing Res Rev. 2022;78:101636. doi: 10.1016/j.arr.2022.101636
  7. Scopa C, Marrocco F, Latina V, et al. Impaired adult neurogenesis is an early event in Alzheimer’s disease neurodegeneration, mediated by intracellular Aβ oligomers. Cell Death Differ. 2020;27(3):934-948. doi: 10.1038/s41418-019-0409-3
  8. Salles GN, Calió ML, Afewerki S, et al. Prolonged drug-releasing fibers attenuate Alzheimer’s disease-like pathogenesis. ACS Appl Mater Interfaces. 2018;10(43):36693-36702. doi: 10.1021/acsami.8b12649
  9. Salles GN, Calió ML, Hölscher C, Pacheco-Soares C, Porcionatto M, Lobo AO. Neuroprotective and restorative properties of the GLP-1/GIP dual agonist DA-JC1 compared with a GLP-1 single agonist in Alzheimer’s disease. Neuropharmacology. 2020;162:107813. doi: 10.1016/j.neuropharm.2019.107813
  10. Calió ML, Mosini AC, Marinho DS, et al. Leptin enhances adult neurogenesis and reduces pathological features in a transgenic mouse model of Alzheimer’s disease. Neurobiol. Dis. 2021;148:105219. doi: 10.1016/j.nbd.2020.105219
  11. Diaz Brinton R, Ming Wang J. Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer’s disease: allopregnanolone as a proof of concept neurogenic agent. Curr Alzheimer Res. 2006;3(3):185-190. doi: 10.2174/156720506777632817
  12. Sotthibundhu A, Li Q-X, Thangnipon W, Coulson EJ. Aβ1–42 stimulates adult SVZ neurogenesis through the p75 neurotrophin receptor. Neurobiol Aging. 2009;30(12):1975-1985. doi: 10.1016/j.neurobiolaging.2008.02.004
  13. Bernabeu-Zornoza A, Coronel R, Palmer C, Monteagudo M, Zambrano A, Liste I. Physiological and pathological effects of amyloid-β species in neural stem cell biology. Neural Regen Res. 2019;14(12):2035-2042. doi: 10.4103/1673-5374.262571
  14. Walus K, Beyer S, Willerth SM. Three-dimensional bioprinting healthy and diseased models of the brain tissue using stem cells. Curr Opin Biomed Eng. 2020; 14:25-33. doi: 10.1016/j.cobme.2020.03.002
  15. de Melo BAG, Jodat YA, Cruz EM, Benincasa JC, Shin SR, Porcionatto MA. Strategies to use fibrinogen as bioink for 3D bioprinting fibrin-based soft and hard tissues. Acta Biomater. 2020;117:60-76. doi: 10.1016/j.actbio.2020.09.024
  16. de Melo BAG, Benincasa JC, Cruz EM, Maricato JT, Porcionatto MA. 3D culture models to study SARS-CoV-2 infectivity and antiviral candidates: From spheroids to bioprinting. Biomed J. 2021;44(1):31-42. doi: 10.1016/j.bj.2020.11.009
  17. Cruz EM, Machado LS, Zamproni LN, et al. A gelatin methacrylate-based hydrogel as a potential bioink for 3D bioprinting and neuronal differentiation. Pharmaceutics. 2023;15(2):627. doi: 10.3390/pharmaceutics15020627
  18. Knowlton S, Anand S, Shah T, Tasoglu S. Bioprinting for neural tissue engineering. Trends Neurosci. 2018; 41(1):31-46. doi: 10.1016/j.tins.2017.11.001
  19. Cadena M, Ning L, King A, et al. 3D bioprinting of neural tissues. Adv Healthc Mater. 2021;10(15):2001600. doi: 10.1002/adhm.202001600
  20. Parra-Cantu C, Li W, Quiñones-Hinojosa A, Zhang YS. 3D bioprinting of Glioblastoma model. J 3D Print Med. 2020;4(2):113-125. doi: 10.2217/3dp-2019-0027
  21. Gao T, Gillispie GJ, Copus JS, et al. Optimization of gelatin– alginate composite bioink printability using rheological parameters: A systematic approach. Biofabrication. 2018;10(3):034106. doi: 10.1088/1758-5090/aacdc7
  22. Ioannidis K, Angelopoulos I, Gakis G, et al. 3D reconstitution of the neural stem cell niche: connecting the dots. Front Bioeng Biotechnol. 2021;9:705470. doi: 10.3389/fbioe.2021.705470
  23. Centeno EGZ, Cimarosti H, Bithell A. 2D versus 3D human induced pluripotent stem cell-derived cultures for neurodegenerative disease modelling. Mol Neurodegener. 2018;13:1-15. doi: 10.1186/s13024-018-0258-4
  24. Ioannidis K, Danalatos RI, Champeris Tsaniras S, et al. A custom ultra-low-cost 3D bioprinter supports cell growth and differentiation. Front Bioeng Biotechnol. 2020;8:580889. doi: 10.3389/fbioe.2020.580889
  25. Benwood C, Walters-Shumka J, Scheck K, Willerth SM. 3D bioprinting patient-derived induced pluripotent stem cell models of Alzheimer’s disease using a smart bioink. Bioelectron Med. 2023;9(1):10. doi: 10.1186/s42234-023-00112-7
  26. Bovi dos Santos G, de Lima-Vasconcellos TH, Móvio MI, Birbrair A, Del Debbio CB, Kihara AH. New perspectives in stem cell transplantation and associated therapies to treat retinal diseases: from gene editing to 3D bioprinting. Stem Cell Rev Rep. 2024;20(3):722-737. doi: 10.1007/s12015-024-10689-4
  27. Romariz SAA, Sanabria V, da Silva KR, et al. High concentrations of cannabidiol induce neurotoxicity in neurosphere culture system. Neurotox Res. 2024; 42(1):14. doi: 10.1007/s12640-024-00692-5
  28. Fantini V, Bordoni M, Scocozza F, et al. Bioink composition and printing parameters for 3D modeling neural tissue. Cells. 2019;8(8):830. doi: 10.3390/cells8080830
  29. Zhou X, Cui H, Nowicki M, et al. Three-dimensional-bioprinted dopamine-based matrix for promoting neural regeneration. ACS Appl Mater Interfaces. 2018;10(10):8993-9001. doi: 10.1021/acsami.7b18197
  30. Joung D, Truong V, Neitzke CC, et al. 3D printed stem-cell derived neural progenitors generate spinal cord scaffolds. Adv Funct Mater. 2018;28(39):1801850. doi: 10.1002/adfm.201801850
  31. Suslov ON, Kukekov VG, Ignatova TN, Steindler DA. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc Natl Acad Sci USA. 2002;99(22):14506-14511. doi: 10.1073/pnas.212525299
  32. Othman SA, Soon CF, Ma NL, et al. Alginate-gelatin bioink for bioprinting of hela spheroids in alginate-gelatin hexagon shaped scaffolds. Polym Bull. 2021;78:6115-6135. doi: 10.1007/s00289-020-03421-y
  33. Li Z, Huang S, Liu Y, et al. Tuning alginate-gelatin bioink properties by varying solvent and their impact on stem cell behavior. Sci Rep. 2018;8(1):8020. doi: 10.1038/s41598-018-26407-3
  34. Cheng L, Yao B, Hu T, et al. Properties of an alginate-gelatin-based bioink and its potential impact on cell migration, proliferation, and differentiation. Int J Biol Macromol. 2019;135:1107-1113. doi: 10.1016/j.ijbiomac.2019.06.017
  35. Giuseppe MD, Law N, Webb B, et al. Mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting. J Mech Behav Biomed Mater. 2018;79:150-157. doi: 10.1016/j.jmbbm.2017.12.018
  36. Łabowska MB, Cierluk K, Jankowska AM, Kulbacka J, Detyna J, Michalak I. A review on the adaption of alginate-gelatin hydrogels for 3D cultures and bioprinting. Materials (Basel, Switzerland). 2021;14(4):858. doi: 10.3390/ma14040858
  37. Morgan C, Inestrosa NC. Interactions of laminin with the amyloid ß peptide: implications for Alzheimer’s disease. Braz J Med Biol Res. 2001;34:597-601. doi: 10.1590/S0100-879X2001000500006
  38. Bronfman FC, Garrido J, Alvarez A, Morgan C, Inestrosa NC. Laminin inhibits amyloid-beta-peptide fibrillation. Neurosci Lett. 1996;218(3):201-203. doi: 10.1016/s0304-3940(96)13147-5
  39. Rodin S, Kozin SA, Kechko OI, Mitkevich VA, Makarov AA. Aberrant interactions between amyloid-beta and alpha5 laminins as possible driver of neuronal disfunction in Alzheimer’s disease. Biochimie. 2020;174: 44-48. doi: 10.1016/j.biochi.2020.04.011
  40. Zhang Z, Wang J, Song Y, Wang Z, Dong M, Liu L. Disassembly of Alzheimer’s amyloid fibrils by functional upconversion nanoparticles under near-infrared light irradiation. Colloids Surf B Biointerfaces. 2019;181: 341-348. doi: 10.1016/j.colsurfb.2019.05.053
  41. Almenar-Queralt A, Falzone TL, Shen Z, et al. UV irradiation accelerates amyloid precursor protein (APP) processing and disrupts APP axonal transport. J Neurosci. 2014;34(9):3320-3339. doi: 10.1523/jneurosci.1503-13.2014
  42. Measey TJ, Gai F. Light-triggered disassembly of amyloid fibrils. Langmuir. 2012;28(34):12588-12592. doi: 10.1021/la302626d
  43. Gómez-Guillén MC, Giménez B, López-Caballero MEa, Montero MP. Functional and bioactive properties of collagen and gelatin from alternative sources: a review. Food Hydrocolloids. 2011;25(8):1813-1827. doi: 10.1016/j.foodhyd.2011.02.007
  44. Mancha Sánchez E, Gómez-Blanco JC, López Nieto E, et al. Hydrogels for bioprinting: a systematic review of hydrogels synthesis, bioprinting parameters, and bioprinted structures behavior. Front Bioeng Biotechnol. 2020;8:776. doi: 10.3389/fbioe.2020.00776
  45. Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37(1):106-126. doi: 10.1016/j.progpolymsci.2011.06.003
  46. Ishiwata R, Iwasa M. Cellular inertia. Sci Rep. 2021;11(1):23799. doi: 10.1038/s41598-021-02384-y
  47. Derkach SR, Voron’ko NG, Kuchina YA, Kolotova DS. Modified fish gelatin as an alternative to mammalian gelatin in modern food technologies. Polymers. 2020;12(12):3051. doi: 10.3390/polym12123051
  48. Kokol V, Pottathara YB, Mihelčič M, Perše LS. Rheological properties of gelatine hydrogels affected by flow-and horizontally-induced cooling rates during 3D cryo-printing. Colloids Surf A Physicochem Eng Asp. 2021;616:126356. doi: 10.1016/j.colsurfa.2021.126356
  49. Liu S, Yang H, Chen D, et al. Three-dimensional bioprinting sodium alginate/gelatin scaffold combined with neural stem cells and oligodendrocytes markedly promoting nerve regeneration after spinal cord injury. Regen Biomater. 2022;9:rbac038. doi: 10.1093/rb/rbac038
  50. Kaliampakou C, Lagopati N, Pavlatou EA, Charitidis CA. Alginate–gelatin hydrogel scaffolds; an optimization of post-printing treatment for enhanced degradation and swelling behavior. Gels. 2023;9(11):857. doi: 10.3390/gels9110857
  51. Freeman FE, Kelly DJ. Tuning alginate bioink stiffness and composition for controlled growth factor delivery and to spatially direct MSC fate within bioprinted tissues. Sci Rep. 2017;7(1):17042. doi: 10.1038/s41598-017-17286-1
  52. Chung JHY, Naficy S, Yue Z, et al. Bio-ink properties and printability for extrusion printing living cells. Biomater Sci. 2013;1(7):763-773. doi: 10.1039/C3BM00012E
  53. Sonaye SY, Ertugral EG, Kothapalli CR, Sikder P. Extrusion 3D (bio) printing of alginate-gelatin-based composite scaffolds for skeletal muscle tissue engineering. Materials. 2022;15(22):7945. doi: 10.3390/ma15227945
  54. Hazur J, Detsch R, Karakaya E, et al. Improving alginate printability for biofabrication: establishment of a universal and homogeneous pre-crosslinking technique. Biofabrication. 2020;12(4):045004. doi: 10.1088/1758-5090/ab98e5
  55. Kim J, Choi YJ, Gal CW, Sung A, Park H, Yun HS. 142Development of an alginate-gelatin bioink enhancing osteogenic differentiation by gelatin release. Int J Bioprint. 2023;9(2):660. doi: 10.18063/ijb.v9i2.660
  56. Cooke ME, Rosenzweig DH. The rheology of direct and suspended extrusion bioprinting. APL Bioeng. 2021;5(1):011502. doi: 10.1063/5.0031475
  57. Chimene D, Kaunas R, Gaharwar AK. Hydrogel bioink reinforcement for additive manufacturing: a focused review of emerging strategies. Adv Mater. 2020;32(1):e1902026. doi: 10.1002/adma.201902026
  58. Mancha Sánchez E, Gómez-Blanco JC, López Nieto E, et al. Hydrogels for bioprinting: a systematic review of hydrogels synthesis, bioprinting parameters, and bioprinted structures behavior. Front Bioeng Biotechnol. 2020;8:776. doi: 10.3389/fbioe.2020.00776
  59. O’Connell C, Ren J, Pope L, et al. Characterizing bioinks for extrusion bioprinting: printability and rheology. Methods Mol Biol. 2020;2140:111-133. doi: 10.1007/978-1-0716-0520-2_7
  60. Semba JA, Mieloch AA, Tomaszewska E, Cywoniuk P, Rybka JD. Formulation and evaluation of a bioink composed of alginate, gelatin, and nanocellulose for meniscal tissue engineering. Int J Bioprint. 2023;9(1):621. doi: 10.18063/ijb.v9i1.621
  61. Schwab A, Levato R, D’Este M, Piluso S, Eglin D, Malda J. Printability and shape fidelity of bioinks in 3D bioprinting. Chem Rev. 2020;120(19):11028-11055. doi: 10.1021/acs.chemrev.0c00084
  62. Cui R, Li S, Li T, et al. Natural polymer derived hydrogel bioink with enhanced thixotropy improves printability and cellular preservation in 3D bioprinting. J Mater Chem B. 2023;11(17):3907-3918. doi: 10.1039/D2TB02786K
  63. Mouser VH, Melchels FP, Visser J, Dhert WJ, Gawlitta D, Malda J. Yield stress determines bioprintability of hydrogels based on gelatin-methacryloyl and gellan gum for cartilage bioprinting. Biofabrication. 2016;8(3):035003. doi: 10.1088/1758-5090/8/3/035003
  64. Venkata Krishna D, Ravi Sankar M. Persuasive factors on the bioink printability and cell viability in the extrusion-based 3D bioprinting for tissue regeneration applications. Eng Regener. 2023;4(4):396-410. doi: 10.1016/j.engreg.2023.07.002
  65. Herrada-Manchón H, Fernández MA, Aguilar E. Essential guide to hydrogel rheology in extrusion 3D printing: how to measure it and why it matters? Gels. 2023;9(7):517. doi: 10.3390/gels9070517
  66. Tuladhar S, Clark S, Habib A. Tuning shear thinning factors of 3D bio-printable hydrogels using short fiber. Materials (Basel, Switzerland). 2023;16(2):572. doi: 10.3390/ma16020572
  67. Malektaj H, Drozdov AD, deClaville Christiansen JJP. Mechanical properties of alginate hydrogels cross-linked with multivalent cations. Polymers (Basel). 2023;15(14):3012. doi: 10.3390/polym15143012
  68. Łabowska MB, Cierluk K, Jankowska AM, Kulbacka J, Detyna J, Michalak IJM. A review on the adaption of alginate-gelatin hydrogels for 3D cultures and bioprinting. Materials (Basel). 2021;14(4):858. doi: 10.3390/ma14040858
  69. Shams E, Barzad MS, Mohamadnia S, Tavakoli O, Mehrdadfar AJJoBA. A review on alginate-based bioinks, combination with other natural biomaterials and characteristics. J Biomater Appl. 2022;37(2):355-372. doi: 10.1177/08853282221085690
  70. Ioannidis K, Danalatos RI, Champeris Tsaniras S, et al. A custom ultra-low-cost 3D bioprinter supports cell growth and differentiation. Front Bioeng Biotechnol. 2020;8:580889. doi: 10.3389/fbioe.2020.580889
  71. Leonardo M, Prajatelistia E, Judawisastra HJB. Alginate-based bioink for organoid 3D bioprinting: a review. Bioprinting. 2022;28:e00246. doi: 10.1016/j.bprint.2022.e00246
  72. Mondal A, Gebeyehu A, Miranda M, et al. Characterization and printability of Sodium alginate-gelatin hydrogel for bioprinting NSCLC co-culture. Sci Rep. 2019; 9(1):19914. doi: 10.1038/s41598-019-55034-9
  73. Hiller T, Berg J, Elomaa L, et al. Generation of a 3D liver model comprising human extracellular matrix in an alginate/ gelatin-based bioink by extrusion bioprinting for infection and transduction studies. Int J Mol Sci. 2018;19(10):3129. doi: 10.3390/ijms19103129
  74. Di Giuseppe M, Law N, Webb B, et al. Mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting. J Mech Behav Biomed Mater. 2018;79:150-157. doi: 10.1016/j.jmbbm.2017.12.018
  75. Freeman FE, Kelly DJJSr. Tuning alginate bioink stiffness and composition for controlled growth factor delivery and to spatially direct MSC fate within bioprinted tissues. Sci Rep. 2017;7(1):17042. doi: 10.1038/s41598-017-17286-1
  76. Chung JH, Naficy S, Yue Z, et al. Bio-ink properties and printability for extrusion printing living cells. Biomater Sci. 2013;1(7):763-773. doi: 10.1039/C3BM00012E
  77. Maihemuti A, Zhang H, Lin X, et al. 3D-printed fish gelatin scaffolds for cartilage tissue engineering. J Bioact Mater. 2023;26:77-87. doi: 10.1016/j.bioactmat.2023.02.007
  78. Derkach SR, Voron’ko NG, Sokolan NI, Kolotova DS, Kuchina YA. Interactions between gelatin and sodium alginate: UV and FTIR studies. J Dispers Sci Technol. 2020;41(5):690-698. doi: 10.1080/01932691.2019.1611437
  79. Costa HdS, Dias MR. Alginate/bioactive glass beads: synthesis, morphological and compositional changes caused by SBF immersion method. Mater Res. 2021;24(4): e20200587. doi: 10.1590/1980-5373-MR-2020-0587
  80. Vosough F, Barth A. Characterization of homogeneous and heterogeneous amyloid-β42 oligomer preparations with biochemical methods and infrared spectroscopy reveals a correlation between infrared spectrum and oligomer size. ACS Chem Neurosci. 2021;12(3):473-488. doi: 10.1021/acschemneuro.0c00642
  81. Fraser PE, Nguyen JT, Inouye H, et al. Fibril formation by primate, rodent, and Dutch-hemorrhagic analogues of Alzheimer amyloid beta-protein. Biochemistry. 1992;31(44):10716-10723. doi: 10.1021/bi00159a011
  82. Zandomeneghi G, Krebs MR, McCammon MG, Fändrich M. FTIR reveals structural differences between native beta-sheet proteins and amyloid fibrils. Protein Sci. 2004;13(12):3314-3321. doi: 10.1110/ps.041024904
  83. Sarroukh R, Goormaghtigh E, Ruysschaert J-M, Raussens V. ATR-FTIR: A “rejuvenated” tool to investigate amyloid proteins. Biochim Biophys Acta. 2013;1828(10):2328-2338. doi: 10.1016/j.bbamem.2013.04.012
  84. Yankner BA, Duffy LK, Kirschner DA. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science (New York, NY). 1990;250(4978):279-282. doi: 10.1126/science.2218531
  85. Mazur-Kolecka B, Golabek A, Nowicki K, Flory M, Frackowiak J. Amyloid-beta impairs development of neuronal progenitor cells by oxidative mechanisms. Neurobiol Aging. 2006;27(9):1181-1192. doi: 10.1016/j.neurobiolaging.2005.07.006
  86. Wang X, Sun X, Gan D, et al. Bioadhesive and conductive hydrogel-integrated brain-machine interfaces for conformal and immune-evasive contact with brain tissue. Matter. 2022;5(4):1204-1223. doi: 10.1016/j.matt.2022.01.012
  87. Pettikiriarachchi JTS, Parish CL, Shoichet MS, Forsythe JS, Nisbet DR. Biomaterials for brain tissue engineering. Aust J Chem. 2010;63(8):1143-1154. doi: 10.1071/CH10159
  88. Sadeghi A, Afshari E, Hashemi M, Kaplan D, Mozafari M. Brainy biomaterials: latest advances in smart biomaterials to develop the next generation of neural interfaces. Curr Opin Biomed Eng. 2023;25:100420. doi: 10.1016/j.cobme.2022.100420
  89. Bierman‐Duquette RD, Safarians G, Huang J, et al. Engineering tissues of the central nervous system: interfacing conductive biomaterials with neural stem/progenitor cells. Adv Healthc Mater. 2022;11(7):2101577. doi: 10.1002/adhm.202101577
  90. Modulevsky DJ, Cuerrier CM, Pelling AE. Biocompatibility of subcutaneously implanted plant-derived cellulose biomaterials. PloS One. 2016;11(6):e0157894. doi: 10.1371/journal.pone.0157894
  91. Sordini L, Garrudo FFF, Rodrigues CAV, et al. Effect of electrical stimulation conditions on neural stem cells differentiation on cross-linked PEDOT: PSS films. Front Bioeng Biotechnol. 2021;9:591838. doi: 10.3389/fbioe.2021.591838
  92. Kaur G, Adhikari R, Cass P, Bown M, Gunatillake P. Electrically conductive polymers and composites for biomedical applications. RSC Adv. 2015;5(47):37553-37567. doi: 10.1039/C5RA01851J
  93. Jensen JB, Parmar M. Strengths and limitations of the neurosphere culture system. Mol Neurobiol. 2006;34(3): 153-161. doi: 10.1385/mn:34:3:153
  94. Simpson LW, Szeto GL, Boukari H, Good TA, Leach JB. Collagen hydrogel confinement of Amyloid-β (Aβ) accelerates aggregation and reduces cytotoxic effects. Acta Biomater. 2020;112:164-173. doi: 10.1016/j.actbio.2020.05.030
  95. Li YE, Jodat YA, Samanipour R, et al. Toward a neurospheroid niche model: optimizing embedded 3D bioprinting for fabrication of neurospheroid brain-like co-culture constructs. Biofabrication. 2020;13:015014. doi: 10.1088/1758-5090/abc1be
  96. Sears NA, Seshadri DR, Dhavalikar PS, Cosgriff-Hernandez E. A review of three-dimensional printing in tissue engineering. Tissue Eng Part B Rev. 2016;22(4):298-310. doi: 10.1089/ten.TEB.2015.0464
  97. Pillat MM, Ayupe AC, Juvenal G, et al. Differentiated embryonic neurospheres from familial Alzheimer’s disease model show innate immune and glial cell responses. Stem Cell Rev Rep. 2023;19(6):1800-1811. doi: 10.1007/s12015-023-10542-0
  98. Gaugler J, James B, Johnson T, et al. Alzheimer’s disease facts and figures. Alzheimers Dement. 2022;18(4):700-789. doi: 10.1002/alz.12638
  99. Andrade-Guerrero J, Santiago-Balmaseda A, Jeronimo- Aguilar P, et al. Alzheimer’s disease: an updated overview of its genetics. Int J Mol Sci. 2023;24(4):3754. doi: 10.3390/ijms24043754
  100. Esteve D, Molina-Navarro MM, Giraldo E, et al. Adult neural stem cell migration is impaired in a mouse model of Alzheimer’s disease. Mol Neurobiol. 2022;59(2): 1168-1182. doi: 10.1007/s12035-021-02620-6
  101. Choi YJ, Park J, Lee SH. Size-controllable networked neurospheres as a 3D neuronal tissue model for Alzheimer’s disease studies. Biomaterials. 2013;34(12):2938-2946. doi: 10.1016/j.biomaterials.2013.01.038
  102. Bernabeu-Zornoza A, Coronel R, Palmer C, Martín A, López-Alonso V, Liste I. Neurogenesis is increased in human neural stem cells by Aβ40 peptide. Int J Mol Sci. 2022;23(10):5820. doi: 10.3390/ijms23105820
  103. Cheignon C, Tomas M, Bonnefont-Rousselot D, Faller P, Hureau C, Collin F. Oxidative stress and the amyloid beta peptide in Alzheimer’s disease. Redox Biol. 2018;14:450-464. doi: 10.1016/j.redox.2017.10.014
  104. Li F, Gong Q, Dong H, Shi J. Resveratrol, a neuroprotective supplement for Alzheimer’s disease. Curr Pharm Des. 2012;18(1):27-33. doi: 10.2174/138161212798919075
  105. Chiang MC, Nicol CJB, Lin CH, Chen SJ, Yen C, Huang RN. Nanogold induces anti-inflammation against oxidative stress induced in human neural stem cells exposed to amyloid-beta peptide. Neurochem Int. 2021;145:104992. doi: 10.1016/j.neuint.2021.104992
  106. Walton NM, Shin R, Tajinda K, et al. Adult neurogenesis transiently generates oxidative stress. PloS One. 2012;7(4):e35264. doi: 10.1371/journal.pone.0035264
  107. Pérez Estrada C, Covacu R, Sankavaram SR, Svensson M, Brundin L. Oxidative stress increases neurogenesis and oligodendrogenesis in adult neural progenitor cells. Stem Cells Dev. 2014;23(19):2311-2327. doi: 10.1089/scd.2013.0452
  108. Madhavan L, Ourednik V, Ourednik J. Grafted neural stem cells shield the host environment from oxidative stress. Ann NY Acad Sci. 2005;1049:185-188. doi: 10.1196/annals.1334.017
  109. Fonseca MB, Solá S, Xavier JM, Dionísio PA, Rodrigues CM. Amyloid β peptides promote autophagy-dependent differentiation of mouse neural stem cells: Aβ-mediated neural differentiation. Mol Neurobiol. 2013;48(3):829-840. doi: 10.1007/s12035-013-8471-1
  110. Vázquez P, Arroba AI, Cecconi F, de la Rosa EJ, Boya P, de Pablo F. Atg5 and Ambra1 differentially modulate neurogenesis in neural stem cells. Autophagy. 2012;8(2):187-199. doi: 10.4161/auto.8.2.18535
  111. López-Toledano MA, Shelanski ML. Neurogenic effect of beta-amyloid peptide in the development of neural stem cells. J Neurosc. 2004;24(23):5439-5444. doi: 10.1523/jneurosci.0974-04.2004
  112. Bernabeu-Zornoza A, Coronel R, Palmer C, et al. Aβ42 peptide promotes proliferation and gliogenesis in human neural stem cells. Mol Neurobiol. 2019;56(6):4023-4036. doi: 10.1007/s12035-018-1355-7
  113. Baglietto-Vargas D, Sánchez-Mejias E, Navarro V, et al. Dual roles of Aβ in proliferative processes in an amyloidogenic model of Alzheimer’s disease. Sci Rep. 2017;7(1):10085. doi: 10.1038/s41598-017-10353-7
  114. Micci MA, Krishnan B, Bishop E, et al. Hippocampal stem cells promotes synaptic resistance to the dysfunctional impact of amyloid beta oligomers via secreted exosomes. Mol Neurodegener. 2019;14(1):25. doi: 10.1186/s13024-019-0322-8
  115. Wander CM, Song J. The neurogenic niche in Alzheimer’s disease. Neurosci Lett. 2021;762:136109. doi: 10.1016/j.neulet.2021.136109
  116. Jin K, Peel AL, Mao XO, et al. Increased hippocampal neurogenesis in Alzheimer’s disease. Proc Natl Acad Sci USA. 2004;101(1):343-347. doi: 10.1073/pnas.2634794100
  117. Porayette P, Gallego MJ, Kaltcheva MM, Bowen RL, Vadakkadath Meethal S, Atwood CS. Differential processing of amyloid-beta precursor protein directs human embryonic stem cell proliferation and differentiation into neuronal precursor cells. J Biol Chem. 2009;284(35): 23806-23817. doi: 10.1074/jbc.M109.026328
  118. Matta R, Gonzalez AL. Engineered biomimetic neural stem cell niche. Curr Stem Cell Rep. 2019;5(3):109-114. doi: 10.1007/s40778-019-00161-2

 

 

 

 

 

 



Share
Back to top
International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing