Chinese Journal of Tissue Engineering Research ›› 2022, Vol. 26 ›› Issue (25): 4046-4051.doi: 10.12307/2022.412
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Wang Kang1, Zhi Xiaodong1, 2, Wang Wei1, 2, 3
Received:
2021-02-20
Accepted:
2021-03-24
Online:
2022-09-08
Published:
2022-01-26
Contact:
Wang Wei, MD, Chief physician, Professor, Department of Orthopedics, First Affiliated Hospital of Jinzhou Medical University, Jinzhou 121000, Liaoning Province, China; Liaoning Key Laboratory of Medical Tissue Engineering, Jinzhou 121000, Liaoning Province, China; Institute of Orthopedics, Jinzhou Medical University, Jinzhou 121000, Liaoning Province, China
About author:
Wang Kang, Master candidate, Department of Orthopedics, First Affiliated Hospital of Jinzhou Medical University, Jinzhou 121000, Liaoning Province, China
Zhi Xiaodong, MD, Chief physician, Department of Orthopedics, First Affiliated Hospital of Jinzhou Medical University, Jinzhou 121000, Liaoning Province, China; Liaoning Key Laboratory of Medical Tissue Engineering, Jinzhou 121000, Liaoning Province, China
Wang Kang and Zhi Xiaodong contributed equally to this article.
Supported by:
CLC Number:
Wang Kang, Zhi Xiaodong, Wang Wei. Effect and mechanism of human amniotic epithelial cells on nerve injury repair[J]. Chinese Journal of Tissue Engineering Research, 2022, 26(25): 4046-4051.
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2.1 文献筛选 初检文献7 838篇,去除重复文献3 459篇,通过阅读文题、摘要排除无关文献3 866篇,阅读全文,排除不符合纳入标准的文献453篇,最终纳入60篇文献。 2.2 简要回顾:人羊膜上皮细胞促进损伤修复的研究现状 人羊膜上皮细胞是一类处于胚胎干细胞和成体干细胞过渡阶段的特殊干/祖细胞。人羊膜上皮细胞基因具有良好的稳定性,移植入异种动物体内不易形成畸胎瘤[13]。人羊膜上皮细胞还表达间充质干细胞的数种表面标志和基因产物,如CD44、CD49e、CD73、CD105、CD166、STRO-1,提示人羊膜上皮细胞可向多种组织细胞分化[10,14]。因此,人羊膜上皮细胞被广泛用作细胞疗法或组织再生疗法的理想种子细胞。尽管大多数研究结果尚未应用于临床领域,但已在多种疾病模型中获得了初步结果。近年来,陆续报道了自体或异体移植的人羊膜上皮细胞,在不同的诱导分化条件下可对创伤组织进行修复,其机制可能是人羊膜上皮细胞通过产生多种细胞生长因子、血管调节细胞因子、抗菌肽和抗炎因子,调控细胞的增殖、迁移或抑制细胞的凋亡、介导免疫反应等途径加速伤口愈合[15-17]。研究发现,人羊膜上皮细胞可下调T辅助17细胞(helper T cell-17,Th-17)和上调T调节细胞(regulatory T cell,Treg),来调节T细胞亚群的平衡,抑制单核细胞趋化蛋白1、白细胞介素17和干扰素γ水平,上调血管生成素、表皮生长因子来改善局部细胞因子环境,还可增加血管内皮生长因子、增殖细胞核抗原的表达,改善局部微环境血供,促进腺体分泌,抑制组织粘连[18-19]。有学者研究证实人羊膜上皮细胞能通过介导转化生长因子β1或miR-34a-5p促进成骨细胞增殖分化和迁移,这一研究进一步完善了人羊膜上皮细胞局部调节创伤修复的基本机制[20]。另外,将人羊膜上皮细胞应用到CCl4诱导的肝损伤小鼠模型中,发现人羊膜上皮细胞能分泌肝细胞生长因子、转化生长因子β、白细胞介素10等多种细胞活性因子营养受损肝细胞[21],而在饮食诱导的非酒精性脂肪肝疾病模型中,人羊膜上皮细胞可显著降低pSMAD 2/3信号传导以及活化的肝星状细胞和肝巨噬细胞的数量,并调控基质金属蛋白酶的表达,以此改善肝脏炎症和纤维化[22]。LIU等[23]发现人羊膜上皮细胞通过Wnt/β-catenin途径调节端粒酶活性及上调β-连环蛋白和T细胞因子4表达水平,降低人角膜内皮细胞凋亡率,并促进其增殖。 综上,人羊膜上皮细胞已成功应用于转化医学、组织工程、临床治疗等方面,对肝脏疾病、肿瘤、骨质疏松、心肌梗死、卵巢早衰等疾病具有较为明显的治疗效果,在组织损伤修复和再造方面具有重要应用潜力。 2.3 人羊膜上皮细胞对神经损伤修复的作用"
2.3.1 人羊膜上皮细胞的神经生物学特性 人羊膜上皮细胞表达神经细胞特异性标记蛋白,包括胶质纤维酸性蛋白、微管相关蛋白、波形蛋白、神经纤维丝、髓鞘碱性蛋白和半乳糖脑苷脂等,表明人羊膜上皮细胞本身具有神经细胞和神经前体细胞的生物学特性[11,14]。人羊膜上皮细胞可通过分泌神经营养因子促进神经系统发育,分泌诸如胶质细胞源性神经营养因子、表皮生长因子、转化生长因子β等细胞生长因子,具有营养神经细胞、促进轴突再生及轴突髓鞘化的功能,可使神经细胞免受毒素损害。另外,人羊膜上皮细胞可合成释放表达酪氨酸羟化酶、多巴胺β脱氢酶和多巴胺、乙酰胆碱、去甲肾上腺素等神经递质参与神经电活动[24-25]。基于人羊膜上皮细胞的神经生物学特性,有望作为神经系统疾病新的细胞来源。 2.3.2 人羊膜上皮细胞调控细胞间的信息交流和营养因子表达促进轴突生长 在神经系统损伤修复过程中,miRNA介导的信息交换是一种重要的细胞间通讯方式,影响着包括神经发育、细胞存活、突触重排、神经细胞-胶质细胞相互作用和外泌体传递细胞信息等生理过程[26-27]。目前已发现在神经变性时,轴突或神经末梢有大量影响细胞骨架组织的miRNA,如miR-124、miR-9、miR-212 、miR-221、 miR-145、miR-29a等,调节轴突生长和巨噬细胞迁移、囊泡介导的细胞信息交流、细胞黏附和细胞凋亡负调控,是神经胶质细胞对神经损伤反应的重要调控因子[28-29]。人羊膜上皮细胞可通过miR-128-3p靶向调节JAG1表达来阻止Notch途径激活,从而减少神经细胞的数量并增加神经胶质细胞的数量[30]。人羊膜上皮细胞还可在神经损伤时调控miR-141的表达,促进脑源性神经营养因子、多巴胺转运蛋白和5-羟色胺的表达增加,而且与脑源性神经营养因子直接或间接相互作用的蛋白质表达水平也明显提高,这些蛋白可刺激多巴胺能神经细胞样细胞轴突再生[31]。CHOI等[32]研究表明人羊膜上皮细胞可通过介导miR-410抑制作用促进视网膜神经细胞的再生,其机制是miRNA直接靶向并抑制人分泌型卷曲相关蛋白2的表达。这些研究有力地证明了人羊膜上皮细胞衍生的miRNAs促进了神经细胞的增殖、分化和迁移,能进一步加速伤口愈合。总之,人羊膜上皮细胞衍生miRNAs在创伤修复方面具有广阔的临床应用前景,是未来创新生物医学工程研究的热点,结合靶向性miRNAs的组织/器官重建的先进策略,将有助于开发治疗各种临床神经功能障碍的未来疗法。 另外,人羊膜上皮细胞移植能阻止神经元进一步死亡,这种作用与人羊膜上皮细胞表达神经保护性因子有关,如胶质细胞源性神经营养因子、脑源性神经营养因子、神经生长因子和神经鞘胚素。在受损的神经组织中进行外源性神经生长因子补充,有助于神经组织的再生与功能恢复[33]。研究表明,人羊膜上皮细胞能分泌大量神经营养因子,含有大量脑源性神经营养因子、神经营养因子3、睫状神经营养因子、胶质细胞源性神经营养因子和神经生长因子,对感觉神经细胞和运动神经细胞的存活有明显作用,其中睫状神经营养因子是促进细胞体发育的主要因素,而胶质细胞源性神经营养因子对神经突生长、感觉神经细胞和运动神经细胞的伸长具有最强大的作用,神经营养因子3对神经突起生长的影响大于对迁移的影响,而脑源性神经营养因子本身对迁移和神经突起的生长没有影响,当脑源性神经营养因子与神经营养因子3结合时,能对迁移和神经突起的生长产生协同作用[34-36]。脑源性神经营养因子和神经营养因子3协同提高螺旋神经节的存活率,因此同时暴露于这两种化合物中产生的反应比预期的单独效应更大,这一研究进一步揭示了人羊膜上皮细胞介导周围神经损伤修复的机制[37]。另外,人羊膜上皮细胞可差异性分泌神经营养因子,FENG等[37]将人羊膜上皮细胞和许旺细胞在含有脑脊液的培养基中共培养,结果神经生长因子、脑源性神经营养因子和胶质细胞源性神经营养因子的表达都能明显提高,其中分泌的神经生长因子水平比脑源性神经营养因子高4倍,而胶质细胞源性神经营养因子较神经生长因子高3倍,提示有可能实现人为合理地对人羊膜上皮细胞分泌的营养因子含量进行调节,以此对不同神经细胞类型进行精准化治疗。ZHOU等[38]也证实将人羊膜上皮细胞移植到阿尔茨海默病小鼠体内30 d后,被整合到大脑中,且分泌各种细胞生长因子提供良好修复微环境,以支持神经细胞的再生,明显增加乙酰胆碱水平和海马胆碱能神经突的数量,显著改善了阿尔茨海默症小鼠的空间记忆缺陷。人羊膜上皮细胞对于miRNA和细胞生长因子的分泌调节功能提示可以利用基因工程技术控制人羊膜上皮细胞目标基因表达,靶向分泌适宜的细胞因子,从而获得更好的神经损伤修复效果。人羊膜上皮细胞可作为特异性靶向细胞生长因子的封装细胞用于治疗帕金森病或痴呆等神经退行性疾病。人羊膜上皮细胞可能是治疗神经系统疾病的最有价值的候选细胞之一,这为开发用于组织修复的生物制剂提供了新的方法。 2.3.3 人羊膜上皮细胞调节神经再生炎症反应 神经损伤导致远端神经残端的轴突解离,失神经支配的许旺细胞募集巨噬细胞、中性粒细胞、单核细胞等免疫炎症细胞和产生趋化因子、蛋白酶和氧化代谢产物等细胞活性物质到损伤部位,共同参与调节免疫炎症的动态平衡,影响相应信号通路的激活和细胞的增殖分化、迁移[39-40]。适当的神经炎症水平是神经损伤功能修复的重要部分,但是当神经炎症反应过度且持续发生时,将会引起免疫炎症细胞持续激活,引起神经细胞的变性和退化,甚至导致局部微血管内皮细胞损伤[41]。对中枢神经系统和外周神经系统轴突再生的比较分析表明,外周神经系统轴突的再生效率高于中枢神经系统,这在一定程度上是由于外周神经系统损伤时巨噬细胞清除受损神经远端细胞轴突和髓鞘碎片的能力更强以及肿瘤坏死因子α、白细胞介素1β、白细胞介素2、白细胞介素6和干扰素等炎性细胞因子调节效率较高[42-43]。因此,神经炎症反应的表达程度对于神经细胞的再生尤为重要。人羊膜上皮细胞本身具有较低的免疫原性,实际上,它们可引发先天性和适应性免疫系统细胞的抑制,从而降低这种反应,而不是引起免疫反应,且在免疫调节中的作用似乎是多因素的,其特征在于抑制促炎性细胞因子,调节中性粒细胞和巨噬细胞募集和分泌抑制其趋化活性的因子[44]。ROH等[45]研究发现人羊膜上皮细胞移植显著降低NMDA受体NR1亚基磷酸化(pNR1)的表达,能明显减轻脊髓损伤诱导的机械性异常性疼痛,能减少炎症因子干扰素γ和肿瘤坏死因子的释放,通过抑制 T淋巴细胞增殖,减少促炎症细胞因子白细胞介素1α和白细胞介素1β的表达,具有免疫调节的作用,可分泌Fas配体、转化生长因子β、巨噬细胞迁移抑制因子等免疫炎症抑制因子,能抑制中性粒细胞和巨噬细胞的趋化活性,还可通过上调调节性T细胞抑制免疫性炎症反应和小胶质细胞的激活,明显增加白细胞介素2、白细胞介素10水平,诱导T细胞凋亡途径参与免疫耐受。另有研究表明,人羊膜上皮细胞移植入枫糖浆尿病大鼠体内后,脑病变区炎症应明显改善,大鼠不对称旋转行为得到好转[46]。由此可见,人羊膜上皮细胞具有很强的免疫调节作用,在损伤的中枢神经系统能够通过诱导免疫耐受以及高表达调节性T细胞,降低炎症反应导致的组织损伤,有利于损伤中枢神经组织的恢复,避免瘢痕形成,对神经功能的改善起到了至关重要的作用。人羊膜上皮细胞表达的多种细胞因子具有免疫炎症调节作用,改善了神经再生微环境,提示人羊膜上皮细胞可能有希望作为减轻神经炎症基因介导的载体,成为神经损伤后局部免疫炎症调节的重要方法之一。 2.3.4 人羊膜上皮细胞参与调控细胞分化、增殖、凋亡过程 人羊膜上皮细胞具有多向分化潜能,表达多能干细胞的分子标志物,包括SSEA-4,OCT-4,SOX-9等,可在特定环境下向神经样细胞和神经胶质细胞分化,还可诱导间充质干细胞向神经细胞分化[9]。将人羊膜上皮细胞与神经干细胞共培养可促进神经干细胞的分化,且主要向神经细胞分化,神经干细胞克隆的分化细胞总数、分化为神经细胞的百分率及神经细胞初级突起长度明显提高,提示人羊膜上皮细胞为神经干细胞提供促进其分化及存活的适宜微环境[35]。人羊膜上皮细胞还可促进缺氧缺血性脑损伤大鼠脑皮质自身神经干细胞增殖,移植后可迁移到缺血部位,并选择性进入脑缺血坏死区,促进与坏死区功能相关部位的神经细胞或神经胶质细胞成活,与坏死区部位功能无关的神经细胞或神经胶质细胞随时间延长消失[38]。人羊膜上皮细胞的条件培养基可诱导脐血间充质干细胞向多巴胺能神经细胞样细胞分化,在人羊膜上皮细胞条件培养基中培养后,来自脐血间充质干细胞的多巴胺能神经细胞样细胞的比例显著增加,这主要由多巴胺转运蛋白、酪氨酸羟化酶、Nurr1和Pitx3的表达上调所促进,另外,人羊膜上皮细胞释放的多效生长因子与其他神经营养因子产生协同作用,参与脐血间充质干细胞向多巴胺能神经细胞样细胞的分化[47]。人羊膜上皮细胞还能在诱导因素的刺激下分化为神经细胞、星形胶质细胞取代受损伤或死亡的细胞,NIKNEJAD等[48]利用成纤维细胞生长因子8和音猬因子共同处理细胞,成功诱导人羊膜上皮细胞永久表达多巴胺能神经细胞样细胞性状,并利用其协同效应,高表达酪氨酸羟化酶、多巴胺转运蛋白、Pax2、Lmx1b和En1,这一研究为人羊膜上皮细胞成为帕金森病细胞替代治疗的候选药物进一步奠定了基础。某些因素影响着干细胞在神经退行性疾病中的治疗效率,如移植神经元在宿主组织中的转移和整合程度,以及轴突伸展达到靶区的距离。突触可以反映神经元网络的功能状态,因此需要进一步研究证明分化的功能性多巴胺能神经元的突触形成过程和突触释放神经递质类型。OKAWA等[49]在体外将人羊膜上皮细胞移植到成年沙鼠的海马体中,细胞选择性迁移到神经细胞死亡的CA1锥体层,在缺血区域中转化为神经细胞样细胞,以类似于CA1锥体神经细胞的方式存活。另一方面,周围神经损伤修复依赖于一个适宜神经再生的微环境,而这个微环境是由许旺细胞提供的。因此,改造损伤修复的微环境,目前已成为促进周围神经再生的重要策略之一。 在体外通过人羊膜上皮细胞与许旺细胞间接共培养,可诱导人羊膜上皮细胞分化为许旺细胞,且神经生长因子、脑源性神经营养因子和胶质细胞源性神经营养因子的表达上调。人羊膜上皮细胞能够分化为多种神经元细胞替代损伤的神经元,并且可作为种子细胞定向分化为所需的神经元细胞,同时能够促进神经轴突生长,这为人羊膜上皮细胞用于神经损伤提供了可靠的依据。因此,利用人羊膜上皮细胞的干细胞特性,将其作为供体细胞用于神经损伤移植具有良好的治疗潜力且不会产生法律或道德问题。 2.3.5 人羊膜上皮细胞抑制神经内瘢痕形成 神经修复的过程极为缓慢,易导致胶原纤维增生,使神经吻合口处形成瘢痕,阻碍再生轴突的延伸并导致神经外膜与周围组织形成粘连,压迫血管而影响神经血运[50]。在神经损伤早期,转化生长因子β1介导的胶原合成增加伴Ⅰ型前胶原mRNA水平提高,转化生长因子β1信号被激活,促进成纤维细胞的增殖,这些增殖的成纤维细胞可分泌Ⅳ型胶原、层粘连蛋白、纤维连结瘢痕蛋白在损伤区域中心而形成纤维化瘢痕[51]。人羊膜上皮细胞能显著减少神经瘢痕粘连的复发,还可释放抗炎细胞因子白细胞介素10支持神经组织的无瘢痕愈合,并可能防止轴切细胞死亡或吸引新侧枝芽的生长[52]。WANG等[53]将人羊膜上皮细胞应用于脊髓损伤修复,发现人羊膜上皮细胞植入脊髓损伤大鼠模型中能够明显减少胶质瘢痕的形成,且将人羊膜上皮细胞和支架材料组成的复合物移植于神经缺损处,利用支架材料出色的生物相容性确保移植的细胞具有三维多孔生长能力,提高细胞生长的表面积,促进细胞的黏附、固定和繁殖,能进一步减少神经吻合口瘢痕的形成,机制可能是人羊膜上皮细胞通过刺激基质金属蛋白酶1的表达,部分消除细胞外基质的沉积,促进成纤维细胞的迁移和增殖。另外,人羊膜上皮细胞还可通过转化生长因子β1调节胶原合成,在周围神经损伤修复中影响间质组织内胶原纤维和弹力纤维等成分的渗出,改善神经损伤后应力松弛,并有助于损伤神经张力的衰减和蠕变特性的恢复[54]。 基于人羊膜上皮细胞的细胞治疗方法能有效防止再生轴突延伸过程中神经组织形成粘连,避免压迫微血管而影响神经血运,丰富和发展了神经损伤修复的研究。相信随着细胞分子学技术的发展,人羊膜上皮细胞预防瘢痕形成机制将进一步阐明,结合神经组织工程、基因疗法和中医药疗法等治疗手段,将实现更有效地预防神经瘢痕,从而促进神经损伤恢复。 2.3.6 人羊膜上皮细胞介导神经再生中的血管再生 血管生成和血管重塑是神经损伤后功能恢复的重要环节,微循环血供不足将无法维持神经再生微环境的稳定,神经细胞胞体与其轴突之间的物质和信息传递会出现中断,导致神经纤维的轴浆运输发生障碍,相关神经细胞胞体发生逆行性变性乃至死亡[55-56]。另外,局部血供不足会导致神经胶质细胞分泌血管活性因子减少,进一步加重血液神经屏障的紊乱。GUAN等[57]研究证明人羊膜上皮细胞也可能具有分化为内皮细胞的能力,可以在不同条件下使组织血管化,能整合到裸鼠子宫内膜癌的血管结构中,减轻了肿瘤血管生成的失调,提高了肿瘤血管灌注的效率。在神经系统中,人羊膜上皮细胞可能通过选择性地向受损大脑的缺血区域迁移,分泌各种营养和血管生成因子,产生促进血管生成反应所需的适当细胞因子环境,刺激血管生成。如LEBRETON等[58]研究发现具有抗炎和再生特性的人羊膜上皮细胞在体外对缺氧损伤组织有明显的促进血管再生作用,可表达促血管生成细胞活性因子,例如血管内皮生长因子、碱性成纤维细胞生长因子、骨形态发生蛋白2、血管生成素和白细胞介素6,在周围神经损伤局部移植人羊膜上皮细胞也可诱导缺血组织中的循环干细胞或祖细胞归巢定植,可显著增加损伤组织血流灌注和毛细血管密度,有效参与血运重建与恢复。因此,人羊膜上皮细胞可能对于神经微循环血供的恢复具有重大意义。然而,人羊膜上皮细胞对神经损伤血管修复的作用机制并未得到完全揭示,因此,有必要进行进一步的研究以更明确探究人羊膜上皮细胞的促微循环血管再生的作用。 2.4 人羊膜上皮细胞在神经损伤修复中的优势和挑战 人羊膜上皮细胞具有强大的组织修复再生和保护能力,其旁分泌机制对神经修复过程有着重要的积极影响,参与细胞间通讯并维持局部微环境的动态平衡,促进轴突成长和髓鞘化。人羊膜上皮细胞与各种间充质干细胞相比,人羊膜上皮细胞发育上更原始,扩增能力更强,特别是人羊膜上皮细胞的来源广、成本低、可控性强等众多优势,能够避免生物安全、来源缺乏、免疫排斥和伦理争论等问题。目前已经发现其治疗帕金森病、脊髓损伤、周围神经损伤等神经系统疾病,取得了肯定的成绩,但是许多人羊膜上皮细胞的基础研究仍然有待深入[10,13]。例如:①移植人羊膜上皮细胞之后,人羊膜上皮细胞诱导分化的神经样细胞是否能够与宿主神经细胞形成新的神经环路,起到恢复神经功能的作用;②人羊膜上皮细胞的批量制备工艺规程、质控体系有待规范;③胚胎不同时期的人羊膜上皮细胞中生长因子的种类和含量是否存在差异;④人羊膜上皮细胞疗效评价体系等有待规范;⑤不同解剖位置的人羊膜上皮细胞修复效果是否不同;⑥人羊膜上皮细胞传代次数是否对其分泌物质的种类与含量以及对神经修复效果有影响;⑦人羊膜上皮细胞修复周围神经损伤与中枢神经系统损伤的效果是否有差异。另外,人羊膜上皮细胞与神经组织工程导管、基因治疗等方法高效结合的精准靶向治疗也需进一步探索。因此,需要大量工作来克服上述困难与挑战,以实现人羊膜上皮细胞早日广泛应用于临床研究中。"
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