Biomaterials Translational ›› 2024, Vol. 5 ›› Issue (4): 355-371.doi: 10.12336/biomatertransl.2024.04.003
• REVIEW • Previous Articles Next Articles
Ruiqi Huang1,2, Yanjing Zhu1,2,3, Haokun Chen1,2, Liqun Yu1,2, Zhibo Liu1, Yuchen Liu1, Zhaojie Wang1,2, Xiaolie He1,2, Li Yang1,2, Xu Xu1,2, Yuxin Bai1,2, Bairu Chen1, Rongrong Zhu1,2,3,*()
Received:
2024-09-29
Revised:
2024-10-20
Accepted:
2024-10-24
Online:
2024-11-14
Published:
2024-12-28
Contact:
Rongrong Zhu, rrzhu@tongji.edu.cn.Huang, R.; Zhu, Y.; Chen, H.; Yu, L.; Liu, Z.; Liu, Y.; Wang, Z.; He, X.; Yang, L.; Xu, X.; Bai, Y.; Chen, B.; Zhu, R. Progress in spinal cord organoid research: advancing understanding of neural development, disease modelling, and regenerative medicine. Biomater Transl. 2024, 5(4), 355-371.
Figure 1. The developmental axes of the spinal cord are orchestrated through precise signalling gradients. (A) The A–P axis is patterned by the intersecting gradients of RA and FGF8/GDF11. (B) The D–V axis is established by the opposing gradients of BMP/Wnt and Shh. (C) The M–L axis arises from the radial migration and differentiation of neural progenitors, resulting in the formation of the gray and white matter of the spinal cord. Created with BioRender.com and Adobe Illustrator 2024. A–P: anterior–posterior; BMP: bone morphogenetic protein; D–V: dorsal–ventral; dl: dorsal interneuron; FGF: fibroblast growth factor; FP: floor plate; GDF: growth differentiation factor; M–L: medial–lateral; MN: motor neuron; pMN: motor neuron progenitor; pd: progenitor domain; RA: retinoic acid; RP: floor plate; Shh: sonic hedgehog.
Figure 2. Generation of myelinoids and their application in disease research. (A) Schematic protocol for the generation of myelinoids. (B) Application of myelinoids in studying human myelin biology. (C, D) Distribution and quantification of myelin within myelinoids at various stages of cultivation. Scale bars: 250 μm. (E) Immunofluorescence staining analysis of oligodendrocyte morphology within MI–12 myelinoids. Scale bar: 25 μm. (F) Transmission electron microscopy images of myelinated axons within myelinoids. Scale bars: 1 μm (F1 and F2), 500 nm (F3). (G, H) Application of myelinoids in modelling disordered myelinated axon organisation caused by Nfasc155?/? mutation. Scale bars: 2 μm. Reprinted from James et al.40 ANK–G: ankyrin–G; CASPR: contactin–associated protein–like 2; CNP: 2′,3′–cyclic nucleotide 3′ phosphodiesterase; IGF: insulin like growth factor; iPSCs: induced pluripotent stem cells; MBP: myelin basic protein; MI: myelin induction; Nfasc155: neurofascin–155; pan–Nfasc: pan–neurofascin; PDGF: platelet–derived growth factor; RA: retinoic acid; Shh: sonic hedgehog; SMADi: small mothers against decapentaplegic (Smad) inhibitors; SOX: SRY–box transcription factor; T3: triiodothyronine.
Figure 3. Different models for the research of spinal cord related disorders. Mono layer cultured neural cells can represent heterotypic cellular interactions, with short experimental period; Neural spheroids are 3D unpattern neural progenitor cells; SCOs can represent developmental characteristics of neural tube, and contains several types of neural cells; Animal models have the interaction of multi–system and vasculature, represent high complexity of physiological. Created with BioRender.com. 3D: three–dimensional; A–P: anterior–posterior; D–V: dorsal–ventral; SCOs: spinal cord organoids.
Figure 4. Construction of SCOs and their application in disease modelling. SCOs derived from iPSCs or NSCs, are cultivated using neurogenic induction molecules or bioengineering approaches. These organoids provide a robust model system for the study of a spectrum of spinal cord pathologies. Their utility extends to the elucidation of disease mechanisms and the high–throughput screening of therapeutic small molecules, underscoring their pivotal role in advancing spinal cord research. Created with BioRender.com. iPSC: induced pluripotent stem cells; NSC: neural stem cell; SCOs: spinal cord organoids.
Type of SCOs | Model establishment method | Disease modelling/phenotypes gained | Reference |
---|---|---|---|
nf–hSCOs | CoCl2 simulation | The hypoxic and hypoglycaemic conditions of fetal spinal cord. | |
hSCOs | VPA treatment | Neurodevelopmental defects, impaired expression of tight junction proteins ZO1 and ZO2 can be detected | |
hSCOs | FUS–KO | Impaired motor neuron development | |
SCOs | VPA and carbamazepine treatment | Dose–dependent effect of antiepileptic drugs on neurotube closure defects | |
hSCOs | iPSCs from MEALAS patients | MEALAS modelling, including phenotypes of delayed motor neuron development and axonal growth defects | |
NMOs | iPSCs with C9orf72 mutation from ALS patients | ALS modelling, including phenotypes of muscular dystrophy and loss of Schwann cells | |
hSCOs | EV–D68 infection | Viral–induced neurological disorders, including structural disruption and cellular apoptosis | |
SCOs | iPSCs from patients with SMA | Early state of SMA, including developmental bias towards mesodermal progenitors and muscle cells | |
SCO–on–chip | Modulating nociceptive molecules treatment | Pain research |
Table 1. Applications of SCOs in disease modelling
Type of SCOs | Model establishment method | Disease modelling/phenotypes gained | Reference |
---|---|---|---|
nf–hSCOs | CoCl2 simulation | The hypoxic and hypoglycaemic conditions of fetal spinal cord. | |
hSCOs | VPA treatment | Neurodevelopmental defects, impaired expression of tight junction proteins ZO1 and ZO2 can be detected | |
hSCOs | FUS–KO | Impaired motor neuron development | |
SCOs | VPA and carbamazepine treatment | Dose–dependent effect of antiepileptic drugs on neurotube closure defects | |
hSCOs | iPSCs from MEALAS patients | MEALAS modelling, including phenotypes of delayed motor neuron development and axonal growth defects | |
NMOs | iPSCs with C9orf72 mutation from ALS patients | ALS modelling, including phenotypes of muscular dystrophy and loss of Schwann cells | |
hSCOs | EV–D68 infection | Viral–induced neurological disorders, including structural disruption and cellular apoptosis | |
SCOs | iPSCs from patients with SMA | Early state of SMA, including developmental bias towards mesodermal progenitors and muscle cells | |
SCO–on–chip | Modulating nociceptive molecules treatment | Pain research |
Type | Material | Cell | Application | Advancement/insight | Reference |
---|---|---|---|---|---|
Hydrogel | Alginate | iPSCs | ALS SCOs model with a TDP43 (G298S) mutation | Produce a xeno–free and fully defined 3D culture condition for organoid generation | |
Nanogel | HA | PC12 cells | Applied for the encapsulation on individual neuronal cell | Controlling the permeability of TNF–α, inhibit apoptosis under adverse conditions | |
ECM hydrogel | Decellularised brain ECM | iPSCs | Advance the development of SCOs | SCOs generated more mature neurons, and exhibit higher levels of markers for multiple compartments of the native spinal cord | |
ECM hydrogel | Decellularised spinal cord ECM | NPCs | Act as a delivery vehicle for NPCs and organoids in SCI models | The ECM derived from neonatal rabbit spinal cord tissue has superior potential to promote the proliferation, migration, and differentiation of neural progenitors | |
ECM hydrogel | Decellularised placenta–derived ECM | iPSCs | Accelerate the developmental process of SCOs | SCOs derived more mature cellular phenotypes, can be applied in future personalised medicine | |
PCSM–Matrigel@SAG | Chitosan microspheres combined with Matrigel | iPSCs | Spatially regulate the concentration distribution of Shh signal | Generate the D–V–like cytoarchitecture with domain–specific progenitors and neurons. | |
Bioink | Gelatin cross–linked by mTG | BC– and iPSC–derived neural cells | 3D printing | The 3D bioprinted scaffold is suitable for the survival and differentiation of human neural cells | |
Scaffold material | Collagen sponge | NSCs and OPCs | Bioengineer the spinal cord–like structure | Act as scaffolds for SCLT with white matter and gray matter–like structure |
Table 2. Biomaterials applied in generation of SCOs
Type | Material | Cell | Application | Advancement/insight | Reference |
---|---|---|---|---|---|
Hydrogel | Alginate | iPSCs | ALS SCOs model with a TDP43 (G298S) mutation | Produce a xeno–free and fully defined 3D culture condition for organoid generation | |
Nanogel | HA | PC12 cells | Applied for the encapsulation on individual neuronal cell | Controlling the permeability of TNF–α, inhibit apoptosis under adverse conditions | |
ECM hydrogel | Decellularised brain ECM | iPSCs | Advance the development of SCOs | SCOs generated more mature neurons, and exhibit higher levels of markers for multiple compartments of the native spinal cord | |
ECM hydrogel | Decellularised spinal cord ECM | NPCs | Act as a delivery vehicle for NPCs and organoids in SCI models | The ECM derived from neonatal rabbit spinal cord tissue has superior potential to promote the proliferation, migration, and differentiation of neural progenitors | |
ECM hydrogel | Decellularised placenta–derived ECM | iPSCs | Accelerate the developmental process of SCOs | SCOs derived more mature cellular phenotypes, can be applied in future personalised medicine | |
PCSM–Matrigel@SAG | Chitosan microspheres combined with Matrigel | iPSCs | Spatially regulate the concentration distribution of Shh signal | Generate the D–V–like cytoarchitecture with domain–specific progenitors and neurons. | |
Bioink | Gelatin cross–linked by mTG | BC– and iPSC–derived neural cells | 3D printing | The 3D bioprinted scaffold is suitable for the survival and differentiation of human neural cells | |
Scaffold material | Collagen sponge | NSCs and OPCs | Bioengineer the spinal cord–like structure | Act as scaffolds for SCLT with white matter and gray matter–like structure |
Figure 5. Decellularised ECM hydrogels, derived from sources such as rat brain tissue, neonatal rabbit spinal cord tissue, and human placental tissue, are increasingly utilised in the construction of SCOs. These hydrogels enhance the maturation and functionality of neural cells within SCOs, presenting a significant advancement for research into pathogenic genes and the screening of small molecule therapeutics. Created with BioRender.com. ECM: extracellular matrix; SCOs: spinal cord organoids.
Figure 6. Assembly methodology of the SCLT and its application in SCI. (A) Fabrication of engineered hydrogels and assembly with OPCs and NSCs. (B–D) Brightfield morphology of SCLT and cellular morphology revealed by HE staining. The arrows indicate the GMLT and WMLT structure in SCLT. Scale bars: 500 μm (B–D), 40 μm (D1, D2). (E, F) SEM appearance of SCLT after 14 days of culture. The arrows indicate the cell bodies in SCLT. Scale bar: 500 μm (E) and 5 μm (F). (G, H) Improvement in hindlimb motor function in rats post–SCLT transplantation. The arrows indicate the different postures of the hind limbs while in motion in each treatment group. (I) Significant enhancement in MEP in animals following SCLT transplantation, indicating neural conductivity recovery. *P < 0.05, vs. Nor group; #P < 0.05, vs. SCLT group; &P < 0.05, vs. SF group. Reprinted from Lai et al.81 BBB: Basso–Beattie–Bresnahan; CNTF: ciliary neurotrophic factor; GFP; green fluorescent protein; GMLT: gray matter like tissue; Hoe: Hoechst; MBP: myelin basic protein; MEP: motor evoked potential; Nor: normal; NT–3: neurotrophin–3; NSC: neural stem cell; OPCs: oligodendrocyte precursor cells; SCI: spinal cord injury; SCLT: spinal cord like tissue; SEM: scanning electron microscopy; SF: scaffold; WMLT: white matter like tissue.
Figure 7. Schematic representation of the process for obtaining microfluidic neural tube–like structure utilising micropatterning and microfluidic techniques. By simulating the morphogen gradients in the body, the cell fate of organoids–on–chip is regulated, leading to the development of organoids that mimic early neural tube morphogenesis, including the acquisition of NC cells. Created with BioRender.com. A–P: anterior–posterior; BMP: bone morphogenetic protein; D–V: dorsal–ventral; FGF: fibroblast growth factor; FP: floor plate; iPSC: induced pluripotent stem cell; NC: neural crest; RA: retinoic acid; RP: roof plate; SHH: sonic hedgehog.
Figure 8. Method for obtaining assembloids and their applications. By integrating COs, SCOs, and MNSs derived from hiPSCs, cotico–motor assembloids are generated. Stimulation of the COs module within the assembloid can receive muscle contraction signals detected on the MNSs. Assembloids are utilizable for investigating neuromuscular signal transmission and the pathological mechanisms of related diseases. Created with BioRender.com. COs: cortical organoids; hiPSCs: human induced pluripotent stem cells; MNSs: motor neuron spheroids; SCOs: spinal cord organoids; Stim: stimulation.
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