Chinese Journal of Tissue Engineering Research ›› 2021, Vol. 25 ›› Issue (20): 3232-3238.doi: 10.3969/j.issn.2095-4344.3141
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Li Shang1, 2, 3, Huang Xiang1, 2, 3, Chen Ming1, 2, 3, Lei Mingxing2, 3, Cheng Shi4, Zhang Licheng2, 3, Yin Pengbin2, 3, Tang Peifu2, 3
Received:
2020-06-10
Revised:
2020-06-16
Accepted:
2020-07-29
Online:
2021-07-18
Published:
2021-01-18
Contact:
Tang Peifu, MD, Professor, Department of Orthopedics, First Medical Center of Chinese PLA General Hospital, Beijing 100853, China; National Orthopedics and Sports Rehabilitation Clinical Research Center, Beijing 100853, China
About author:
Li Shang, Master candidate, Physician, Medical College of Chinese PLA, Beijing 100853, China; Department of Orthopedics, First Medical Center of Chinese PLA General Hospital, Beijing 100853, China; National Orthopedics and Sports Rehabilitation Clinical Research Center, Beijing 100853, China
Supported by:
CLC Number:
Li Shang, Huang Xiang, Chen Ming, Lei Mingxing, Cheng Shi, Zhang Licheng, Yin Pengbin, Tang Peifu. Semaphorin 3A is expected to be a new target for the repair of skeletal muscle injury[J]. Chinese Journal of Tissue Engineering Research, 2021, 25(20): 3232-3238.
2.1 Sema3A的结构及其受体 Sema3A是信号蛋白家族中的第三类成员之一,是脊椎动物特有的分泌型信号蛋白,其氨基末端均含有约500个氨基酸残基组成的发挥主要生物学功能的胞外保守序列——SEMA结构域[14]。此外,Sema3A还含有免疫球蛋白样(immunoglobulin-like,Ig) 结构域,富含半胱氨酸的丛状蛋白-信号蛋白-整联蛋白结构域及羧基末端等氨基酸序列等[14]。 Sema3A能够与神经纤毛蛋白 (neuropilin,Nrp)和丛状蛋白组成的共刺激复合受体结合,通过与不同的神经纤毛蛋白和丛状蛋白组合成的受体复合物结合,Sema3A可介导多种不同的生理过程[15]。神经纤毛蛋白家族包含神经纤毛蛋白1、神经纤毛蛋白2两名成员,两者具有相似的蛋白结构。神经纤毛蛋白的胞外区与跨膜区主要介导神经纤毛蛋白与SEMA结构域、血管内皮生长因子及丛状蛋白的结合,并促进神经纤毛蛋白二聚体形成。胞内区连接胞外信号并通过其末端氨基酸残基构成的丝氨酸-谷氨酸-丙氨酸(SEA)序列转导胞内信号[16]。丛状蛋白根据其结构特性分为4个亚组(A,B,C,D),其胞外氨基末端是与信号蛋白结合的SEMA结构域,与之相邻的是3个丛状蛋白-信号蛋白-整联蛋白结构域和3个免疫球蛋白-丛状蛋白-转录因子结构域;在其胞内结构中含有2个GTP酶激活蛋白结构域[17]。 2.2 Sema3A调控骨骼肌再生的作用机制 2009年, TATSUMI等[18]发现成年大鼠下肢的卫星细胞在早期分化阶段上调Sema3A表达;HENNINGSEN等[19]使用C2C12成肌细胞也观察到类似结果。骨骼肌在发生机械损伤后可见Sema3A表达显著升高[18],为降低骨骼肌内神经及血管等组织在相应受损后Sema3A表达改变对观察结果的影响,有研究者使用蛇毒细胞毒素损伤小鼠下肢肌肉组织后同样观察到Sema3A在卫星细胞的表达显著上升[20-21]。这些发现提示,Sema3A与卫星细胞、骨骼肌损伤之间存在紧密联系。WOKKE等[22]在对人肋间外肌的研究中观察到,卫星细胞计数在神经肌肉接头处升高约20倍;另有文献表明,超过80%的卫星细胞集中于毛细血管21 μm范围内[23],这提示卫星细胞与肌内神经、血管网络与之间存在密切联系,近年来对Sema3A的研究进一步印证了这一观点。 2.2.1 Sema3A对卫星细胞增殖与分化的调控 卫星细胞是具有自我更新能力的异质性干细胞群体,正常生理条件下多保持静息状态,仅维持必需的细胞自我更新。骨骼肌发生损伤时静息的卫星细胞被激活,在多种调控机制的协调下增殖、迁移至损伤部位并进一步分化为成肌细胞。成肌细胞可与受损部位的肌细胞融合形成肌管进而组装为新的多核肌纤维[24]。研究表明,骨骼肌具有活跃的分泌功能并以自分泌、旁分泌及内分泌等形式调控机体许多生理过程[25],而卫星细胞位于肌纤维膜与基底膜之间,其再生能力与贮存微环境的稳态受到骨骼肌分泌因子的直接调控[26]。现今,骨骼肌分泌因子对骨骼肌再生修复的影响,特别是对卫星细胞的精细调控机制正受到广泛关注[27],明确Sema3A作为自分泌因子如何影响卫星细胞的生物学行为与功能具有重要意义。 Sema3A可促进卫星细胞增殖。在卫星细胞来源的成肌细胞中使用Sema3A-siRNA转染以降低Sema3A表达后,可观察到细胞Pax7和Myf5的转录和分泌水平显著降低,且细胞增殖水平显著低于对照组;相应的,成肌细胞过表达Sema3A则出现Pax7、Myf5的表达升高,成肌细胞的增殖水平提高,但肌细胞分化标记MyoD的表达和分泌水平在细胞进入分化阶段前未表现出统计学差异[28]。有研究显示,Pax7可通过与Myf5的启动子结合以激活其表达[29],Sema3A或在通过Pax7调节卫星细胞增殖能力的同时,间接影响Myf5表达,进而调控卫星细胞再生[30]。 卫星细胞的自我更新、增殖和分化间的平衡对于骨骼肌再生同样至关重要,卫星细胞若过度增殖而分化受到抑制将损害成熟肌纤维再生,而反之则可造成卫星细胞池“枯竭”同样使修复受损[31]。尚未激活的静息卫星细胞通常处于高度极化状态,其在肌纤维侧与基底膜侧分别具有不同的蛋白表达模式[32],卫星细胞两侧的基底膜和肌纤维膜的分泌模式也有所不同,从而进一步以极性微环境的形式参与形成卫星细胞内部的微环境[33]。基于上述结构基础,卫星细胞的分裂模式可在对称分裂或不对称分裂之间进行变化,卫星细胞的自我更新与分化得以维持协调,从而支持其完整的损伤修复功能[34]。 Sema3A对成肌细胞分化具有调控作用。成肌细胞转染Sema3A-siRNA后,实验组内增殖细胞(Pax7+/MyoD+)显著少于对照组,且分化细胞(Pax7-/MyoD+)出现早于对照组;72 h后成肌细胞逐渐融合,实验组中分化细胞占比低于对照组,MyoD+细胞和肌球蛋白重链(myosin heavy chain,MyHC)表达均较对照组减少,在72 h的观察中自我更新细胞(Pax7+/MyoD-)所占组分未见明显变化[28]。依据上述实验结果,Sema3A低表达削弱了成肌细胞分化能力,但上述现象同样可能由于Pax7表达随Sema3A的下调而减少,使卫星细胞自我更新及增殖受损,成肌细胞提前进入分化阶段,从而导致“卫星细胞池”存量不足,最终表现为卫星细胞修复骨骼肌损伤能力下降。 卫星细胞在Sema3A-siRNA转染后的再生过程中出现大量胞核及胞质显著增大的Pax7-/MyoD-细胞表型,这在对照组中始终未曾出现[28],或与细胞衰老有关。既往研究提示,处于衰老状态的细胞通常具有增大的细胞核和细胞质区域,而“衰老细胞”较正常细胞的功能有显著差异[35];Sema3A的表达及分泌随年龄增长而升高,且这一增龄性改变已被发现与骨骼、中枢神经等组织的疾病病程中存在密切联系[36-37]。Sema3A的表达是否可以减少或逆转Pax7-/MyoD-表型卫星细胞的出现,此表型卫星细胞的细胞命运和表型特征及其与Sema3A之间的联系值得进一步探索。 2.2.2 Sema3A对肌纤维类型的调控作用 骨骼肌纤维类型的构成与骨骼肌的收缩功能、代谢特征、抗疲劳等特性和疾病易感程度密切相关,不同肌纤维类型的特化和其生理特性支持着其生物学功能的发挥[38]。骨骼肌损伤后,特定肌群再生的纤维类型分布是否与其承担的收缩及代谢等特性相适应,对于骨骼肌功能恢复的程度至关重要[13]。 研究表明,Sema3A促进Ⅰ型肌纤维合成,并发挥抑制Ⅱ型肌纤维合成作用。在体内实验中,卫星细胞Sema3A特异性敲除的成年小鼠下肢骨骼肌被蛇毒细胞毒素损伤后,于再生修复的腓肠肌中观察到Ⅰ型肌纤维所占比例、Ⅰ型MyHC及肌红蛋白表达显著减少,Ⅱb型肌纤维所占比例及Ⅱb型MyHC表达显著升高,且肌管平均直径高于对照组,再生的骨骼肌具有更大的最大收缩力,但收缩耐受能力下降[39]。体外细胞实验使用Sema3A-siRNA转染分化阶段的成肌细胞后观察到MyHC的表达总量及成肌细胞融合指数均未见显著差异,但其中Ⅰ型MyHC的表达下调并伴有融合指数下降,相反Ⅱa、Ⅱx型MyHC表达增加并伴有融合指数上升,肌管平均直径增加,Ⅱb型MyHC未见显著差异[39]。 肌细胞生成素是介导Sema3A调控肌纤维类型分布的重要下游因子。肌细胞生成素对于Ⅰ型肌纤维的合成十分重要,在体内、外实验中从比目鱼肌(以氧化型慢肌纤维为主)分离获取的卫星细胞比趾长伸肌(以酵解型快肌纤维为主)来源的卫星细胞具有更高的肌细胞生成素表达[40-41]。对从趾长伸肌及比目鱼肌中获取的卫星细胞在早期分化阶段分别给予外源性成纤维细胞生长因子2或肝细胞生长因子处理后,比目鱼肌来源的卫星细胞呈现更高的Sema3A表达及分泌水平[42]。外源性给予Sema3A可上调卫星细胞肌细胞生成素表达,而使用Sema3A-siRNA转染细胞后,肌细胞生成素表达则随Sema3A减少而下降[39,42]。值得注意的是,单独抑制肌细胞生成素表达只出现Ⅰ型MyHC表达下降,但并不伴有Ⅱ型MyHC表达的上升,这表明或存在其他通路介导Sema3A对肌纤维类型的调控。通过siRNA转染进一步分别明确了受体通路功能,结果表明:神经纤毛蛋白2-丛状蛋白A3受体通路主要介导了Sema3A对骨骼肌类型分布的主要调控功能,而神经纤毛蛋白1、丛状蛋白A1、丛状蛋白A2或构成拮抗其主要功能的受体通路[39]。 最新研究发现,Sema3A可抑制扭曲蛋白2阳性(Twist2+, Tw2+)骨骼肌前体细胞与Ⅰ、Ⅱa型肌纤维融合,间接调控肌纤维类型的构成。不同于Pax7+卫星细胞存贮于肌纤维膜与基底膜之间,Tw2+骨骼肌前体细胞常贮于肌纤维基底膜外间质,是一类可与Ⅱb、Ⅱx型肌纤维融合的特异性前体细胞[43]。LI等[44]发现相比于Pax7+卫星细胞,转录因子Twist2可提高Sema3A受体神经纤毛蛋白1的表达,且Sema3A在Ⅰ、Ⅱa型肌纤维具有较高表达。在条带迁移实验及多种转基因条件下的细胞融合实验中,Sema3A作为排斥因子使Tw2+骨骼肌前体细胞无法成为再生来源与Ⅰ、Ⅱa型肌纤维相融合,而由于Ⅱb型肌纤维缺少Sema3A表达故Tw2+细胞可特异性补充至Ⅱb型肌纤维[44]。以上现象的发现使Sema3A在骨骼肌再生过程中发挥了类似于其在神经系统中所为人熟知的排斥效应。这一趋化作用主要由Sema3A-Nrp1受体途径介导实现,而在此过程中丛状蛋白等共受体如何参与这一生理现象目前尚未明确。既往研究表明,成人比目鱼肌通常比胫骨前肌或趾长伸肌贮有更多的卫星细胞数量,且在同一肌肉中Ⅰ型肌纤维常较Ⅱ型肌纤维有更多附着的卫星细胞;在机体衰老时骨骼肌的Ⅱb型纤维可发生特异性萎缩、Ⅰ型肌纤维所占比例增加[22,26]。这些差异反映了卫星细胞在不同肌纤维上的内在异质性,这是否同Sema3A的增龄性变化及Tw2+骨骼肌前体细胞针对特异性纤维类型的补充存在直接联系值得进一步探究。 2.2.3 Sema3A对骨骼肌损伤局部组织环境再生的调控 骨骼肌损伤常伴随局部骨骼、神经纤维及血管的损伤,其整体再生水平最终决定骨骼肌收缩及代谢等功能的恢复,现已有许多研究通过组织工程学手段将神经及血管组织内组分与骨骼肌再生相结合进行探索[45]。研究表明Sema3A对骨、血管及神经纤维等组织的功能和再生同样具有显著的调控能力。 骨骼肌附着于骨骼,两者共同组成了机体运动系统的主要部分。骨组织存在由破骨细胞及成骨细胞维持的骨吸收与骨形成的之间动态平衡,并籍此保持其质量和功能的稳定[46]。Sema3A可与破骨前体细胞膜上神经纤毛蛋白1 结合,抑制核因子κB受体活化因子配体通路下游分子的激活,进而抑制破骨细胞分化,此外Sema3A与神经纤毛蛋白1结合可抑制巨噬细胞集落刺激因子对骨髓源性破骨前体细胞迁移的趋化作用,减少骨质破坏[47]。Sema3A也可通过与成骨细胞神经纤毛蛋白1结合后上调Rac1的表达,促进使β连环蛋白在胞核内聚集,从而促进成骨细胞分化,促进骨形成[48];与此同时,Sema3A可通过调节骨内感觉神经的分布间接影响骨质平衡,发挥骨保护作用[49]。Sema3A表达在骨骼肌损伤早期的快速上调促进了骨组织重建,这加强了骨骼肌再生的结构支撑,从而促进机体运动功能的恢复。 骨骼肌内血管及神经纤维的结构与功能的完整对骨骼肌功能至关重要,骨骼肌损伤后,Sema3A以相似的模式调控神经纤维与肌内血管网络对再生骨骼肌的重新支配。运动神经末梢与再生肌纤维的突触后膜之间连接的重建在骨骼肌功能恢复中不可或缺,卫星细胞的Sema3A分泌水平在损伤早期上调,作为轴突排斥因子延迟神经纤维末端对损伤肌纤维的支配,而在损伤修复后期转化生长因子β下调Sema3A的表达,或可促使运动神经生长并诱导其重新附着至再生肌纤维[13,50];相似的是,Sema3A可通过抑制血管内皮整合素活性、作用于血管内皮生长因子受体或抑制血管内皮生长因子165与神经纤毛蛋白1相结合等多种方式,使血管内皮细胞增殖、迁移和存活受损,抑制血管生成,而当Sema3A表达下调时,其对血管再生的抑制作用被解除[51]。骨骼肌损伤后血管及神经纤维短暂的再生延迟可能削弱了早期修复阶段骨骼肌运动功能的恢复,但或可在损伤局部带来潜在的“制动”效应,从而降低了早期修复过程中局部能量消耗,减少了结构恢复尚不完整时骨骼肌剧烈收缩可能造成的二次损伤。且另有研究表明,在骨骼肌损伤早期给予血管内皮生长因子局部治疗可促进肌内血管重建,但多为无法支持骨骼肌功能恢复的“随机血管”,反而限制骨骼肌修复[45]。在Sema3A表达受调控的降低后,神经及血管组织对新生肌纤维的再支配可促进骨骼肌结构重建和代谢等功能的恢复。在骨骼肌修复过程中Sema3A以时间特异性方式精密调控局部血管与神经纤维的协调再支配,但机体内环境十分复杂,Sema3A对骨骼肌损伤局部血管及神经再生的内在调节机制还需要进一步探索。 Sema3A可通过上调血管内皮钙黏蛋白磷酸化以增加局部血管通透性[9],从而协助炎细胞及循环祖细胞的募集[45]。骨骼肌损伤后M1、M2型巨噬细胞和中性粒细胞等炎症细胞浸润损伤部位并贯穿骨骼肌再生全程,多种炎症细胞以时间特异性的方式参与坏死组织清除、卫星细胞的募集与激活并协调促进肌纤维再生[52-53],但当前对于Sema3A如何调节骨骼肌损伤后炎细胞募集及巨噬细胞类型的转变尚不明确,对此的进一步探索可加深对Sema3A调控骨骼肌损后修复的理解。 2.3 Sema3A表达受局部生长因子调控 骨骼肌中Sema3A的基础分泌使其具有协调肌内血管网络分布和骨骼肌神经支配的潜力,但在骨骼肌损伤后,卫星细胞的Sema3A表达水平在多种生长因子的调控下呈现时间特异性,这种特性对于骨骼肌损伤后的炎症反应、肌纤维再生、血管及神经网络再支配的协调具有重要作用。目前已经发现肝细胞生长因子、成纤维细胞生长因子2和转化生长因子β在骨骼肌损伤后再生过程中对Sema3A的表达发挥突出调控作用[20]。 肝细胞生长因子由肝细胞、脾脏、巨噬细胞、卫星细胞等多种细胞分泌,在骨骼肌损伤后局部浓度显著升高。肝细胞生长因子可诱导静止的卫星细胞激活、促进卫星细胞增殖并抑制分化,对C2C12成肌细胞有趋化作用,是参与骨骼肌再生过程中的重要分子信号[54]。研究发现,肝细胞生长因子以浓度依赖性和时间特异性的方式促进成肌细胞Sema3A表达和分泌,可达生理水平8倍;在卫星细胞培养中早期给予肝细胞生长因子处理并不影响Sema3A的表达,而在成肌细胞的早期分化阶段给予外源性肝细胞生长因子,可观察到Sema3A表达显著上调[55-56]。 成纤维细胞生长因子2可促进骨骼肌增殖,现已广泛应用于肌细胞培养,研究发现成纤维细胞生长因子2在骨骼肌损伤后2-8 d分泌水平显著升高[57]。成纤维细胞生长因子2上调卫星细胞的Sema3A表达和分泌也存在剂量与时间的依赖性,且与肝细胞生长因子处理得到的结果非常相似,但并未发现两者可协同促进Sema3A表达[58]。目前研究显示,在卫星细胞培养中,除表皮生长因子可小幅提升Sema3A表达水平,胰岛素样生长因子1、血小板衍生生长因子及转铁蛋白等对骨骼肌再生有促进作用的生长因子对Sema3A在卫星细胞的表达未见显著调节作用,这些结果更突出了肝细胞生长因子及成纤维细胞生长因子2在骨骼肌再生中的重要促进作用[20]。 转化生长因子β2、转化生长因子β3可显著抑制Sema3A的表达。在模拟骨骼肌机械损伤的体内实验中,转化生长因子β3的分泌水平在骨骼肌损伤12 d后升高,并可下调Sema3A表达水平,进一步实验表明,在培养过程中分别加入转化生长因子β2、转化生长因子β3均可阻断肝细胞生长因子、成纤维细胞生长因子2对Sema3A表达的促进作用,对卫星细胞Sema3A表达具有强力抑制作用[20]。上述生长因子在骨骼肌损伤后不同阶段的差异性表达,共同参与形成了Sema3A表达随时间变化的特征。 此外,体内实验表明骨骼肌损伤后Sema3A最高表达水平约为对照组的16倍,远高于肝细胞生长因子或成纤维细胞生长因子2处理组的升高水平(8倍),这表明体内或有其他尚未发现的可显著调节Sema3A表达的机制存在[20,59]。如前所述,血管内皮生长因子是一类可促进血管内皮细胞增殖及迁移等作用的生长因子,也是促进骨骼肌内血管生成的介导因子之一[60],与Sema3A存在密切联系。现如今,骨骼肌微血管、血管内皮生长因子和卫星细胞间的密切联系正在不断被发现[61],然而血管内皮生长因子对于卫星细胞Sema3A的表达是否存在调节,其是否作为竞争性配体与Sema3A共同协调骨骼肌发育及再生尚不明确。 "
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