Effects of the pretreatment of human umbilical cord mesenchymal stem cells with tumor necrosis factor-α and interleukin-1β on the healing of ischemic wounds in rats
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摘要:
目的 探讨肿瘤坏死因子α（TNF-α）和白细胞介素-1β（IL-1β）预处理人脐带间充质干细胞（hUMSC）对大鼠缺血创面愈合的影响。 方法 该研究为实验研究。收集2022年12月—2023年4月在遵义医科大学附属医院接受剖宫产的3名22~35岁产妇分娩的健康足月新生儿脐带组织,分离hUMSC,进行划痕试验后,按随机数字表法（分组方法下同）分为用终质量浓度均为20 ng/mL的TNF-α和 IL-1β预处理的预处理组及常规培养的对照组,计算划痕后8、16、32 h细胞迁移率（样本数为3）。取5只9周龄雄性SD大鼠,在背部构建面积为11.0 cm×2.5 cm的双蒂皮瓣,在皮瓣上构建2个直径0.6 cm的缺血创面,在背部正常皮肤上构建2个直径0.6 cm的非缺血创面,计算2种创面建模后6、12、18 d愈合率,确定该缺血创面模型可靠性。另取15只9周龄雄性SD大鼠,同前制备缺血创面模型,分为预处理hUMSC组、常规hUMSC组及磷酸盐缓冲液（PBS）组,每组5只,分别于创缘注射同前预处理的hUMSC、常规培养的hUMSC及PBS。计算注射后3、6、9、12 d创面愈合率；注射后12 d,取创面组织,行苏木精-伊红染色后观察创面上皮化程度,行Masson染色后观察创面组织中胶原纤维形成情况,行免疫荧光染色检测创面组织中血管数量及精氨酸酶-1（Arg1）、诱导型一氧化氮合酶（iNOS）阳性细胞数。 结果 划痕后16、32 h,预处理组细胞迁移率均明显高于对照组（Z值分别为-2.61、-2.61,P<0.05）。建模后6、12、18 d,大鼠非缺血创面愈合率均明显高于缺血创面（Z值分别为2.61、2.79、2.79,P<0.05）。注射后6、9、12 d,预处理hUMSC组大鼠创面愈合率分别为6.83%（3.13%,12.22%）、66.83%（60.09%,95.68%）、96.98%（91.67%,99.80%）,均明显高于PBS组的1.54%（0.30%,3.47%）、1.54%（0.60%,5.90%）、3.08%（0.90%,7.64%）,Z值分别为7.60、9.40、10.00,P<0.05。注射后9 d,预处理hUMSC组大鼠创面愈合率明显高于常规hUMSC组的5.86%（4.72%,8.12%）,Z=5.60,P<0.05。注射后12 d,预处理hUMSC组大鼠创面已基本完成上皮化,创面组织中胶原纤维形成情况明显优于常规hUMSC组和PBS组。注射后12 d,预处理hUMSC组大鼠创面组织中血管数量和Arg1阳性细胞数均明显多于常规hUMSC组和PBS组（P<0.05）,常规hUMSC组大鼠创面组织中血管数量和Arg1阳性细胞数均明显多于PBS组（P<0.05）；预处理hUMSC组大鼠创面组织中iNOS阳性细胞数明显少于常规hUMSC组和PBS组（P值均<0.05）,常规hUMSC组大鼠创面组织中iNOS阳性细胞数明显少于PBS组（P<0.05）。 结论 TNF-α和IL-1β预处理可增强hUMSC的迁移能力、免疫调节能力和促血管生成能力,从而促进大鼠缺血创面愈合。 Abstract:Objective To investigate the effects of the pretreatment of human umbilical cord mesenchymal stem cells (hUMSCs) with tumor necrosis factor-α (TNF-α) and interleukin-1β (IL-1β) on the healing of ischemic wounds in rats. Methods This study was an experimental research. The umbilical cord tissue was collected from three healthy full-term neonates delivered by cesarean section from delivery women aged 22-35 years in the Affiliated Hospital of Zunyi Medical University between December 2022 and April 2023. The hUMSCs were isolated, and after the scratch test, the cells were divided into pretreatment group pretreated with TNF-α and IL-1β of both final mass concentrations of 20 ng/mL and control group cultured conventionally according to the random number table method (the same grouping method below). The cell migration rates were calculated at 8, 16, and 32 h after scratch, with sample size of 3. Five 9-week-old male Sprague-Dawley (SD) rats were used to construct a bipedicled flap with an area of 11.0 cm×2.5 cm on the back, two ischemic wounds with diameter of 0.6 cm were created on the flaps, and two non-ischemic wounds with diameter of 0.6 cm were created on normal dorsal skin. The wound healing rates were calculated at 6, 12, and 18 d after modeling to validate the reliability of the ischemic wound model. Another 15 male SD rats aged 9 weeks were subjected to the same ischemic wound model as above and divided into pretreated hUMSC group, conventional hUMSC group, and phosphate-buffered saline (PBS) group, with 5 rats in each group, which were respectively injected with pretreated hUMSCs as before, conventionally cultured hUMSCs, and PBS at the wound margin. The wound healing rates were calculated at 3, 6, 9, and 12 d after injection. At 12 d after injection, the wound tissue was collected for hematoxylin-eosin staining to assess epithelialization of wounds, for Masson staining to observe collagen fiber formation in wound tissue, and for immunofluorescence staining to detect the number of blood vessels, arginase-1 (Arg1)-positive cells, and inducible nitric oxide synthase (iNOS)-positive cells in wound tissue. Results At 16 and 32 h after scratch, the cell migration rates in pretreatment group were significantly higher than those in control group (with Z values of -2.61 and -2.61, respectively, P<0.05). At 6, 12, and 18 d after modeling, the healing rates of non-ischemic wounds of rats were significantly higher than those of ischemic wounds (with Z values of 2.61, 2.79, and 2.79, respectively, P<0.05). At 6, 9, and 12 d after injection, the wound healing rates in pretreated hUMSC group of rats were 6.83% (3.13%, 12.22%), 66.83% (60.09%, 95.68%), and 96.98% (91.67%, 99.80%), respectively, which were significantly higher than 1.54% (0.30%, 3.47%), 1.54% (0.60%, 5.90%), and 3.08% (0.90%, 7.64%) in PBS group (with Z values of 7.60, 9.40, and 10.00, respectively, P<0.05). At 9 d after injection, the wound healing rate in pretreated hUMSC group of rats was significantly higher than 5.86% (4.72%, 8.12%) in conventional hUMSC group (Z=5.60, P<0.05). At 12 d after injection, the wound epithelialization basically completed in pretreated hUMSC group of rats, and the collagen fiber formation in wound tissue was markedly better than that in conventional hUMSC group and PBS group. At 12 d after injection, the number of blood vessels and Arg1-positive cells in wound tissue in pretreated hUMSC group of rats was significantly more than that in conventional hUMSC group and PBS group (P<0.05), and the number of blood vessels and Arg1-positive cells in wound tissue in conventional hUMSC group of rats was significantly more than that in PBS group (P<0.05); the number of iNOS-positive cells in pretreated hUMSC group of rats was significantly less than that in conventional hUMSC group and PBS group (with both P values <0.05), and the number of iNOS-positive cells in conventional hUMSC group of rats was significantly less than that in PBS group (P<0.05). Conclusions The pretreatment of hUMSCs with TNF-α and IL-1β can enhance the abilities of migration, immunomodulation, and promoting angiogenesis of the cells, thereby promoting the healing of ischemic wounds. -
参考文献
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图 1 大鼠背部缺血创面的构建。1A.设计以脊柱正中线为纵轴的长方形皮瓣及缺血创面（皮瓣上的创面）、非缺血创面（皮瓣外的创面）；1B.构建双蒂皮瓣和缺血创面并在皮瓣下放置无菌硅胶板；1C.缝合皮肤与硅胶板后即刻
图 2 2组人脐带间充质干细胞划痕后各时间点迁移情况。2A、2B、2C、2D.分别为预处理组细胞划痕后0（即刻）、8、16、32 h的划痕情况,划痕面积逐渐缩小；2E、2F、2G、2H.分别为对照组细胞划痕后0、8、16、32 h的划痕情况,划痕面积逐渐缩小,图2A和2B划痕面积分别与图2E、2F相近,图2C、2D划痕面积分别明显小于图2G、2H
注：预处理组细胞用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β处理,对照组细胞进行常规培养
图 3 大鼠缺血创面和非缺血创面建模后各时间点愈合情况。3A、3B、3C、3D.分别为建模后0（即刻）、6、12、18 d创面愈合情况,图3B中非缺血创面面积小于缺血创面,图3C、3D中非缺血创面已完全愈合而缺血创面未完全愈合
注：于双蒂皮瓣上构建的创面为缺血创面,于皮瓣周围正常皮肤构建的创面为非缺血创面
图 4 大鼠缺血创面和非缺血创面建模后18 d的组织学变化。4A、4B.分别为非缺血创面和缺血创面上皮化情况,图4A创面上皮化情况明显好于图4B 苏木精-伊红×4；4C、4D.分别为非缺血创面和缺血创面胶原纤维形成情况,图4C创面胶原纤维形成明显多于图4D Masson×4
注：于双蒂皮瓣上构建的创面为缺血创面,于皮瓣周围正常皮肤处构建的创面为非缺血创面
图 5 3组大鼠注射后各时间点缺血创面愈合情况。5A、5B、5C.分别为预处理hUMSC组、常规hUMSC组、PBS组注射后9 d创面愈合情况,图5A创面面积明显小于图5B、5C；5D、5E、5F.分别为预处理hUMSC组、常规hUMSC组、PBS组注射后12 d创面愈合情况,图5D创面面积明显小于图5E、5F
注：hUMSC为人脐带间充质干细胞,PBS为磷酸盐缓冲液；于预处理hUMSC组大鼠创缘注射用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β预处理的hUMSC,于常规hUMSC组大鼠创缘注射常规培养的hUMSC,于PBS组大鼠创缘注射PBS
图 6 3组大鼠注射后12 d缺血创面上皮化情况及胶原纤维新生情况。6A、6B、6C.分别为预处理hUMSC组、常规hUMSC组、PBS组,图6A创面上皮化情况明显优于图6B、6C 苏木精-伊红×4；6D、6E、6F.分别为预处理hUMSC组、常规hUMSC组、PBS组,图6D创面组织中新生胶原纤维数量明显多于图6E、6F Masson×4
注：hUMSC为人脐带间充质干细胞,PBS为磷酸盐缓冲液；于预处理hUMSC组大鼠创缘注射用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β预处理的hUMSC,于常规hUMSC组大鼠创缘注射常规培养的hUMSC,于PBS组大鼠创缘注射PBS
图 7 3组大鼠注射后12 d缺血创面组织中血管形成及巨噬细胞极化情况 Alexa Fluor 488-4',6-二脒基-2-苯基吲哚×400。7A、7B、7C.分别为预处理hUMSC组、常规hUMSC组和PBS组创面组织中血管形成情况,图7A中血管数量多于图7B、7C；7D、7E、7F.分别为预处理hUMSC组、常规hUMSC组和PBS组创面组织中Arg1阳性细胞,图7D中Arg1阳性细胞数多于图7E、7F；7G、7H、7I.分别为预处理hUMSC组、常规hUMSC组和PBS组创面组织中iNOS阳性细胞,图7G中 iNOS阳性细胞数少于图7H、7I
注：hUMSC为人脐带间充质干细胞,PBS为磷酸盐缓冲液,Arg1为精氨酸酶-1,iNOS为诱导型一氧化氮合酶；于预处理hUMSC组大鼠创缘注射用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β预处理的hUMSC,于常规hUMSC组大鼠创缘注射常规培养的hUMSC,于PBS组大鼠创缘注射PBS
Table 1. 2组人脐带间充质干细胞划痕后各时间点迁移率比较[%,M（Q1,Q3）]
组别 样本数 8 h 16 h 32 h 预处理组 5 28.41（23.35,31.72） 63.60（54.31,64.35） 94.70（92.48,95.41） 对照组 5 24.31（22.05,26.50） 43.27（40.27,45.13） 79.25（77.28,81.17） Z值 -2.19 -2.61 -2.61 P值 0.030 0.009 0.009 注：预处理组细胞用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β处理,对照组细胞进行常规培养 
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Table 2. 大鼠缺血创面和非缺血创面建模后各时间点愈合率比较[%,M（Q1,Q3）]
创面类型 样本数 6 d 12 d 18 d 缺血创面 5 8.24（2.38,10.08） 20.62（12.53,24.24） 35.97（21.77,53.44） 非缺血创面 5 64.15（33.32,71.31） 100.00（100.00,100.00） 100.00（100.00,100.00） Z值 2.61 2.79 2.79 P值 0.009 0.005 0.005 注：于双蒂皮瓣上构建的创面为缺血创面,于皮瓣周围正常皮肤构建的创面为非缺血创面
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Table 3. 3组大鼠注射后各时间点缺血创面愈合率比较[%,M（Q1,Q3）]
组别 样本数 3 d 6 d 9 d 12 d 预处理hUMSC组 5 1.75（0.04,9.61） 6.83（3.13,12.22） 66.83（60.09,95.68） 96.98（91.67,99.80） 常规hUMSC组 5 0.37（0.28,0.79） 3.35（1.73,5.32） 5.86（4.72,8.12） 47.01（35.83,54.62） PBS组 5 0.31（0.28,0.37） 1.54（0.30,3.47） 1.54（0.60,5.90） 3.08（0.90,7.64） H值 3.26 7.28 11.18 12.50 P值 0.196 0.026 0.004 0.002 Z1值 — 3.20 5.60 5.00 P1值 — 0.258 0.048 0.077 Z2值 — 7.60 9.40 10.00 P2值 — 0.007 <0.001 <0.001 Z3值 — 4.40 3.80 5.00 P3值 — 0.120 0.179 0.077 注：hUMSC为人脐带间充质干细胞,PBS为磷酸盐缓冲液；于预处理hUMSC组大鼠创缘注射用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β预处理的hUMSC,于常规hUMSC组大鼠创缘注射常规培养的hUMSC,于PBS组大鼠创缘注射PBS；Z1值、P1值及Z2值、P2值分别为预处理hUMSC组和常规hUMSC组、PBS组各时间点比较所得,Z3值、P3值为常规hUMSC组与PBS组比较所得；“—”表示无此项
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Table 4. 3组大鼠注射后12 d缺血创面组织中血管数量及Arg1和iNOS阳性细胞数比较（
组别 样本数 血管数量（根） Arg1阳性细胞数（个） iNOS阳性细胞数（个） 预处理hUMSC组 5 16.2±3.0 210±23 37±7 常规hUMSC组 5 11.0±2.3 88±10 101±11 PBS组 5 5.4±2.3 34±6 139±9 F值 22.44 184.40 157.90 P值 <0.001 <0.001 <0.001 P1值 <0.001 <0.001 <0.001 P2值 <0.001 <0.001 <0.001 P3值 <0.001 <0.001 <0.001 注：hUMSC为人脐带间充质干细胞,PBS为磷酸盐缓冲液,Arg1为精氨酸酶-1,iNOS为诱导型一氧化氮合酶；于预处理hUMSC组大鼠创缘注射用终质量浓度均为20 ng/mL的肿瘤坏死因子α和白细胞介素-1β预处理的hUMSC,于常规hUMSC组大鼠创缘注射常规培养的hUMSC,于PBS组大鼠创缘注射PBS；P1值、P2值分别为预处理hUMSC组和常规hUMSC组、PBS组各指标比较所得,P3值为常规hUMSC组与PBS组各指标比较所得
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