Adult stem cells from different germ layers applied in peripheral nerve injury repair

doi:10.12307/2025.067

Abstract

Abstract: BACKGROUND: Adult stem cell therapy is one of the research hotspots in the field of peripheral nerve injury repair and regeneration. With excellent properties of mesenchymal stem cells such as high acquisition rate, wide source, and rapid proliferation, mesoderm have been regarded as the ideal source of adult stem cells, while ectoderm-derived adult stem cells, especially neural crest stem cells, have certain neurogenic properties and attract more and more attention from researchers.
OBJECTIVE: To mainly review the role and mechanism of multifunctional adult stem cells from ectoderm and mesoderm in peripheral nerve injury repair and regeneration, so as to explore the research progress and application prospect of adult stem cells from different sources and discuss the potential application value of adult stem cell therapy and the problems to be solved in connection with clinical studies.
METHODS: The first author searched the relevant articles published from December 2001 to February 2024 in PubMed and SinoMed by computer in February 2024. The Chinese and English search terms were “ectodermal stem cells, mesenchymal stem cells, peripheral nerve injury, repair, regeneration.” Finally, 69 articles were included and analyzed.
RESULTS AND CONCLUSION: (1) Ectodermal adult stem cells have excellent differentiation and regeneration potential, especially epidermal neural crest stems cells, olfactory stem cells, and dental ectomesenchymal stem cells, which have certain neurogenic properties and can express neural specific markers in vitro. However, relevant clinical research needs to be accumulated. (2) There are many types of adult stem cells derived from mesoderm, which are easy to obtain and purify. Among them, the efficacy and safety of bone marrow mesenchymal stem cells and umbilical cord mesenchymal stem cells in the repair of peripheral nerve injury are supported by clinical trials; that is, they can improve sensory and motor nerve conduction and there are no complications and obvious adverse reactions in follow-up. The acquisition of bone marrow mesenchymal stem cells needs invasive surgery and requires the patient to match the donor bone marrow type, which limit the application to some extent. Although umbilical cord mesenchymal stem cells do not require invasive harvesting, their isolation is difficult and phenotypically unstable. (3) Adult stem cells derived from endoderm often fail to grow in vitro, so the possibility of clinical application is low. (4) In conclusion, bone marrow mesenchymal stem cells are still the first choice for adult stem cell therapy in the treatment of peripheral nerve injury, which is suitable for cases without surgical contraindications and meeting the matching requirements, followed by umbilical cord mesenchymal stem cells supplemented by improved isolation methods and advanced phenotypic stability strategies. (5) Dental ectomesenchymal stem cells and adipose-derived mesenchymal stem cells have high application potential and need to be further tested in clinical trials. Other adult stem cells derived from ectodermal and mesodermal layers have significant advantages in animal and cell experimental studies due to their excellent properties.

Key words: adult stem cell, peripheral nerve injury, hair follicle neural crest stem cell, olfactory stem cell, dental ectomesenchymal stem cell, bone marrow mesenchymal stem cell, umbilical cord-derived mesenchymal stem cell, amniotic fluid-derived mesenchymal stem cell, skin-derived stem cell, muscle-derived mesenchymal stem cell

CLC Number:

Zheng Jiachen, Yang Entong, Zhu Yizhou, Liu Fang. Adult stem cells from different germ layers applied in peripheral nerve injury repair[J]. Chinese Journal of Tissue Engineering Research, 2025, 29(19): 4102-4110.

Figures/Tables 7

2.1 外胚层来源成体干细胞胚胎三胚层分化过程中，在脊索的诱导下，相应的外胚层细胞增生，分化形成表皮及附属器和神经系统。当神经沟闭合为神经管时，神经板外侧缘的细胞迁移至神经管背外侧形成2条纵行细胞索，即神经嵴。神经嵴又称“第四胚层”，是周围神经系统的原基，具有很强的迁移能力，可分化为多种特定的细胞和组织。 2.1.1 毛囊神经嵴干细胞起源于胚胎神经嵴，表达巢蛋白(Nestin)、Sox10和未成熟的神经嵴细胞标志物，具有定向分化为神经元、平滑肌细胞、施万细胞、黑素细胞和软骨细胞的能力[10]。研究表明，毛囊神经嵴干细胞可促进周围神经损伤的修复，并可能通过定向分化、调节相关细胞因子分泌等多种机制发挥作用，见图3。LIN等[11]认为其作用机制是定向分化为施万细胞后促进轴索及髓鞘形成，而HU等[12]发现毛囊神经嵴干细胞能促进神经营养因子、血管生长因子以及金属蛋白酶的分泌。唐笠等[13]以静脉导管桥接SD大鼠面神经干缺损，探究毛囊表皮神经嵴干细胞(epidermal neural crest stem cells，EPI-NCSCs)对面神经损伤的调节作用，发现术后毛囊EPI-NCSCs组的肿瘤坏死因子α表达水平显著降低，而白细胞介素4表达水平和面神经功能评分显著增高，表明毛囊EPI-NCSCs对面神经损伤修复早期局部肿瘤坏死因子α和白细胞介素4表达具有调节作用，能促进面神经功能和形态恢复。可见毛囊EPI-NCSCs能通过调节细胞因子水平促进周围神经损伤后轴突的生长和神经功能恢复。最新研究显示，PAN等[14]提取毛囊EPI-NCSCs来源的外泌体促进面神经功能恢复，结果表明其外泌体有助于脱细胞同种异体神经移植物修复面神经缺损，并有可能在临床上取代自体移植疗法。"

ROCHE等[15]将嗅干细胞与双相胶原神经导管结合，治疗大鼠坐骨神经缺损，发现嗅干细胞可促进神经电生理功能和组织学结构的恢复。ESAKI等[16]应用嗅干细胞治疗小鼠面神经压榨伤，发现其有助于促进面部麻痹康复，并增强神经再生能力。ENTEZARI等[20]研究发现，嗅干细胞相比脂肪间充质干细胞和施万细胞，具有更显著的分裂活性和增殖速度；同时，嗅干细胞可表达施万细胞标志物(SOX10，p75，S100，GFAP和MBP)并分泌神经营养因子(脑源性神经营养因子和神经生长因子)，提示嗅干细胞能够自发分化为施万细胞样细胞表型并通过分泌神经营养因子促进神经突生长。嗅干细胞易于从嗅黏膜活检中获得，且风险较低，可以作为组织工程神经的种子细胞，用于基础乃至临床试验的研究。 2.1.3 牙外胚层干细胞包括牙髓干细胞、脱落乳牙干细胞、根尖乳头干细胞和牙周韧带干细胞等，其与神经嵴干细胞有着相同的起源，具有神经源性。目前对牙髓干细胞的研究较为全面[21-26]，见图4。牙髓干细胞可在体外分化为施万细胞，表达多种早期神经细胞标志物并释放生长因子，促进体内血管形成、促进神经生长以及髓鞘形成和轴突再生[27]。体内移植的牙髓干细胞可能同时发挥多种作用，如牙髓干细胞通过向施万细胞前体细胞分化并分泌神经营养因子3和脑源性神经营养因子等促进坐骨神经再生和再髓鞘化[28]。PEREIRA等[29]将脱落乳牙干细胞注入聚乙醇酸导管，治疗大鼠面神经缺损，发现脱落乳牙干细胞同样可以在体内分化为施万细胞，促进神经再生。可见牙外胚层干细胞不仅具有多能分化潜力，还展现出很好的再生能力，为其应用于周围神经损伤修复提供了依据。"

DARADKA等[30]发现在犬面神经损伤、移植自体隐静脉模型中，骨髓间充质干细胞注射组的神经功能恢复、粘连减少程度以及胶原沉积程度均有显著性改善。叶放等[31]将骨髓间充质干细胞注入大鼠坐骨神经3 mm缺损模型，观察各项指标发现，注射骨髓间充质干细胞所产生的细胞外基质，相较于施万细胞、皮肤前体细胞分化的施万细胞和成纤维细胞，能为神经功能恢复提供更为有利的微环境，同时减少炎症反应的发生[36]。LI等[37]研究显示，骨髓间充质干细胞来源外泌体在大鼠坐骨神经损伤模型中可促进M2巨噬细胞极化、轴突再生和重建，加速轴突功能恢复。最新研究发现，骨髓间充质干细胞可通过靶向miR-449a调控核转录因子κB信号通路，从而减轻周围神经损伤的炎症反应，修复神经损伤[34]。相比于神经干细胞以及施万细胞，骨髓间充质干细胞取材更为便捷，体外扩增能力较强，在伦理学中具有较强优势，是目前研究的热点。 2.2.2 脂肪来源间充质干细胞脂肪在人体内含量丰富，且提取纯化后的脂肪间充质干细胞纯度高、活性好、扩增能力强，具有分化为施万细胞样细胞(SC like cells，SCLCs)和抑制炎症反应的能力，成为临床治疗与再生医学应用的理想种子细胞。近年来，研究者们不断探究脂肪来源间充质干细胞在神经再生领域的作用机制，见图5。研究显示，该干细胞向神经分化后由长梭形转变为类圆形胞体，延伸出突起，并表达神经细胞特异性蛋白NSE和Nestin[38]。移植至损伤部位的脂肪来源间充质干细胞可受施万细胞产生的外泌体诱导而向其分化[39]，并通过诱导神经营养因子及生长因子的旁分泌，促进损伤部位施万细胞的生理作用。YAL??N等[40]研究发现脂肪来源间充质干细胞可增加受损神经syndecan-1和热休克蛋白70水平，显著改善功能恢复和促进神经再生，其产生的外泌体可通过内含的miRNA-26b下调Kpna水平，以抑制施万细胞自噬作用，促进坐骨神经损伤修复[41]。工程化细胞技术同样得到应用，HSU等[42]以基因编辑的方式多路径激活脂肪来源间充质干细胞，延长神经因子的作用时间，促进大鼠坐骨神经再生。脂肪来源间充质干细胞获得率高、体外大量扩增所耗费的成本低，在所有非神经源性干细胞中更具吸引力，因此更有可能广泛应用于临床，促进周围神经损伤修复与再生。"

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