Zhou KQ,Su YJ,Jia CY.Reliability study on establishing a rat tuberculosis wound model using Bacillus Calmette-Guérin[J].Chin J Burns,2021,37(8):793-796.DOI: 10.3760/cma.j.cn501120-20200531-00290.
Citation: Tang XY,Liu CY,Chu GP,et al.Effects of porcine urinary bladder matrix on motility and polarization of bone marrow-derived macrophages in mice[J].Chin J Burns Wounds,2023,39(1):25-34.DOI: 10.3760/cma.j.cn501225-20220516-00187.

Effects of porcine urinary bladder matrix on motility and polarization of bone marrow-derived macrophages in mice

doi: 10.3760/cma.j.cn501225-20220516-00187
Funds:

Clinical Frontier Technology Program of Social Development of Science and Technology Agency of Jiangsu Province of China BE2018626

Cultivation Plan of "Double Hundred" Medical Youth Tip-Top Professionals Program of Wuxi City HB2020050

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  •   Objective  To explore the effects of porcine urinary bladder matrix (UBM) on the motility and polarization of bone marrow-derived macrophages in mice, so as to provide evidence for the rational selection of stent in clinical wound repair.  Methods  The method of experimental research was used. The microstructure of porcine UBM and absorbable dressing was observed under scanning electron microscope. Polyacrylamide gel electrophoresis was used to observe the protein distribution of the two stent extracts. The primary macrophages were induced from bone marrow-derived cells isolated from six 6-8-week-old male C57BL/6J mice (mouse age, sex, and strain, the same below) and identified. Three batches of macrophages were divided into porcine UBM extract group and absorbable dressing extract group. The cells in each group were cultured with Dulbecco's modified Eagle medium/F12 medium containing the corresponding extracts. The cell migration rate was detected and calculated on 1, 3, and 7 d after scratching by scratch test. The number of migrated cells at 12 and 24 h of culture was detected by Transwell experiment. The percentages of CD206 and CD86 positive cells at 24 h of culture was detected by flow cytometer. The numbers of sample in the above cell experiments were all 3. An incision was prepared on the left and right back of twelve mice, respectively. The left incision of each mouse was included in porcine UBM group and the right incision was included in absorbable dressing group, and the corresponding stents were implanted into the incisions respectively. On post operation day (POD) 7 and 14, the number of inflammatory cells infiltrated in the stent was detected by hematoxylin-eosin staining; the number of F4/80, transforming growth factor-β1 (TGF-β1), vascular endothelial growth factor (VEGF), and matrix metalloprotein-9 (MMP-9) positive cells and type Ⅰ collagen deposition in stents were observed by immunohistochemistry; the percentages of F4/80, CD86, and CD206 positive cells were observed by immunofluorescence staining. The numbers of sample in the above animal experiments were all 6. Data were statistically analyzed with analysis of variance for factorial design, analysis of variance for repeated measurement, and independent sample t test.  Results  Porcine UBM has a dense basement membrane structure on one side and porous propria containing a fibrous structures on the other. Both sides of the absorbable dressing had three-dimensional porous structure. In the molecular weight range of (50-70)×103, multiple non-type Ⅰ collagen bands appeared in the lanes of porcine UBM extract, while no obvious bands appeared in the lanes of absorbable dressing extract. It had been identified that mouse bone marrow-derived cells had been successfully induced into macrophages. The cell migration rates in porcine UBM extract group were significantly higher than those in absorbable dressing extract group on 1, 3, and 7 d after scratching (with t values of 15.31, 19.76, and 20.58, respectively, P<0.05). The numbers of migrated cells in porcine UBM extract group were significantly more than those in absorbable dressing extract group at 12 and 24 h of culture (with t values of 12.20 and 33.26, respectively, P<0.05). At 24 h of culture, the percentage of CD86 positive cells in porcine UBM extract group ((1.27±0.19)%) was significantly lower than (7.34±0.14)% in absorbable dressing extract group (t=17.03, P<0.05);the percentage of CD206 positive cells in porcine UBM extract group was (73.4±0.7)%, significantly higher than (32.2±0.5)% in absorbable dressing extract group (t=119.10, P<0.05). On POD 7 and 14, the numbers of inflammatory cells infiltrated in the stents in porcine UBM group was significantly more than those in absorbable dressing group (with t values of 6.58 and 10.70, respectively, P<0.05). On POD 7 and 14, the numbers of F4/80, TGF-β1, VEGF, and MMP-9 positive cells in the stents in porcine UBM group were significantly more than those in absorbable dressing group (with t values of 46.11, 40.69, 13.90, 14.15, 19.79, 32.93, 12.16, and 13.21, respectively, P<0.05); type Ⅰ collagen deposition in the stents in porcine UBM group was more pronounced than that in absorbable dressing group; the percentages of CD206 positive cells in the stents in porcine UBM group were significantly higher than those in absorbable dressing group (with t values of 5.05 and 4.13, respectively, P<0.05), while the percentages of CD86 positive cells were significantly lower than those in absorbable dressing group (with t values of 20.90 and 19.64, respectively, P<0.05), and more M2-type macrophages were seen in the stents in porcine UBM group and more M1-type macrophages were seen in the stents in absorbable dressing group.  Conclusions  Porcine UBM can enhance macrophage motility, induce M2 polarization and paracrine function, create a microenvironment containing growth factors such as TGF-β1 and MMP-9 tissue remodeling molecules, and promote tissue regeneration and extracellular matrix remodeling in mice.

     

  • 结核病是全世界十大死亡病因之一1。我国报告的肺外结核占结核病总数的5%2。在肺外结核中,约50%以上患者伴病灶周围软组织的损害,这些损害最终破溃形成“结核性创面”3。结核性创面具有多变的临床表现,仍是发展中国家常见的皮肤病之一4。结核性创面发病早期因临床表现缺乏特异性,因此该类患者常延迟就诊5;加之创面细菌培养阳性率低,造成了较高的漏诊率及误诊率6;创面常伴潜行的皮下隧道,对治疗造成了一定的困难3。目前结核性创面的发病机制尚不清楚,同时缺乏特效的治疗手段7, 8,与目前没有成熟的动物模型有关。因此,对动物模型的研究显得尤为重要。为了给深入研究结核性创面提供稳定可行的动物模型,本课题组使用牛分枝杆菌减毒株(BCG)对SD大鼠进行了结核性创面模型的构建并取得初步结果。

    本实验研究遵循山西医科大学和国家有关实验动物管理和使用的相关规定。

    15只健康无特殊病原体(SPF)级6周龄雄性SD大鼠,体重(200±20)g,由山西医科大学实验动物中心提供,许可证号:SCXK(晋)2015-0001。BCG购于美国ATCC菌株保存中心,Middlebrook OADC增菌液、Middlebrook 7H9培养基购于美国BD公司,弗氏完全佐剂购于美国Sigma公司,石碳酸品红染液、亚甲蓝复染液、苏木精染液购于北京索莱宝生物科技有限公司,伊红购于西亚化学科技(山东)有限公司。EclipseCi-L型光学显微镜购于日本尼康仪器有限公司。

    将-80 ℃冻存的BCG置于冰上,在室温中消融。在生物安全柜中将BCG加入预先添加OADC增菌液的7H9培养液中,置于37 ℃恒温摇床(转速80次/min)培养至菌落形成,通过测菌液吸光度值9的方法计数细菌浓度,分装成浓度为1×107CFU/mL BCG菌液备用。

    将15只大鼠在适宜洁净的饲养间适应性饲养3周,按照随机数字表法分为感染组(12只)和正常对照组(3只)。感染组大鼠背部皮下隧道样注射弗氏完全佐剂0.2 mL,3周后皮下注射BCG菌液0.2 mL,建立大鼠结核性创面模型。正常对照组大鼠未经任何处理。

    1.4.1   大体观察

    分别于感染第8、15、32、43天,大体观察感染组大鼠注射部位皮肤情况并拍照。

    1.4.2   局部组织情况

    分别于感染第8、15、32、43天大体观察后,用颈椎脱臼法处死感染组3只大鼠,取注射部位皮肤组织,体积分数10%甲醛固定24 h后进行包埋。正常对照组正常喂养3周后同前处死,取对应组织进行固定包埋(方法同前)。取正常对照组及感染组大鼠各时间点石蜡组织进行切片(厚度约4 μm),行常规HE染色,400倍光学显微镜下观察细胞排列、坏死及炎症等情况。取感染第43天感染组大鼠石蜡组织同前进行切片,石碳酸品红染液室温染色30 min,冲洗至液体呈无色。滴加亚甲蓝复染液,室温染色1 min,冲洗至液体呈无色。行常规脱水、透明、封片,于600倍和1 000倍光学显微镜下观察组织中细菌分布情况。

    感染组大鼠感染第8天,可见注射部位皮肤稍隆起、皮下形成脓肿,见图1A。随着感染时间的延长,脓肿物体积逐渐增大。感染第15天,注射部位皮肤明显隆起、皮下脓肿较感染第8天时明显增大,见图1B。感染第32天,注射部位隆起的脓肿出现破溃、脓肿表面呈火山口样外观,破溃处可见脓性分泌物,见图1C。感染第43天,脓肿破溃处无愈合倾向,脓肿较感染第32天增大,见图1D。感染第43天时完整切除脓肿,挤压脓肿物可见长条形类似乳酪状脓性分泌物由皮肤破溃处溢出,见图1E, 1H

    1  感染组大鼠感染不同时间点注射部位皮肤组织形成的病灶表现。1A.感染第8天,注射部位皮肤稍隆起(→);1B.感染第15天,注射部位皮下脓肿较图1A明显(→);1C.感染第32天,注射部位隆起的脓肿出现破溃;1D.感染第43天,脓肿破溃处无愈合倾向;1E~1H.感染第43天,创面脓性分泌物经挤压由感染灶内不断溢出的过程

    正常大鼠皮肤组织细胞排列规律,未见炎症细胞浸润,见图2A。感染组大鼠感染第8天,可见细胞分布杂乱、大量聚集、细胞核呈融合趋势,见图2B。感染第15天,可见肉芽肿形成、炎症细胞呈同心圆状排列,见图2C。感染第32天,肉芽肿数量增多,在细菌聚集区域可见大量细胞被破坏,见图2D。感染第43天,细胞排列疏松,部分细胞坏死,见图2E。对感染第43天的组织行抗酸染色,可见组织内存在大量细菌,细菌在组织内呈团簇样聚集(图3A),高倍镜下可以看到大量呈杆状的细菌菌体聚集在病灶中(图3B)。

    2  感染组大鼠感染不同时间点注射部位皮肤组织与正常对照组大鼠对应皮肤组织形态学观察 苏木精-伊红×400。2A.正常对照组大鼠组织细胞排列规律;2B.感染组大鼠感染第8天,细胞分布杂乱、细胞大量聚集;2C.感染组大鼠感染第15天,可见肉芽肿形成(→);2D.感染组大鼠感染第32天,肉芽肿数量增多(→);2E.感染组大鼠感染第43天,细胞排列疏松,部分细胞坏死(→)
    3  感染组大鼠感染第43天注射部位皮肤组织抗酸染色结果。3A.细菌(红色)在组织内呈团簇样聚集 石碳酸品红×600;3B.大量呈杆状的细菌菌体聚集在病灶中 石碳酸品红×1 000

    早期,研究者为了寻找实验条件有限时肺结核研究的替代模型,使用结核杆菌建立了动物皮肤液化和坏死模型10, 11。随着临床对结核性创面的重视,目前研究的皮肤结核动物有兔子、小鼠、大鼠、斑马鱼、猴等12, 13, 14, 15, 16,本研究团队也针对结核性创面进行了动物实验的探索12, 13, 14。Zhang等17使用兔模型评价了不同分枝杆菌的毒力,BCG活菌较H37Ra或耻垢分枝杆菌活菌诱导的病灶面积明显扩大,经过灭活的BCG依然比灭活的H37Ra或耻垢分枝杆菌诱导肉芽肿更明显。兔体型较大、需占用大量饲养空间、实验操作不方便,斑马鱼虽然饲养方便但形成创面所需时间较长。高剂量BCG活菌(5×106 CFU)可引起兔皮肤组织液化和溃疡18,中剂量BCG活菌(5×104 CFU)可诱发兔皮肤组织形成肉芽肿17。本研究既要使大鼠皮肤形成破溃,又要探索使用较低的接种浓度保障安全性,故选用了2×106 CFU的接种量,更低的接种浓度能否引起大鼠皮肤破溃还需要进一步研究。BCG活菌引起兔皮肤结核在11 d左右达到高峰并形成液化19,经灭活的BCG引起的兔皮肤结核在35 d后病变缓慢消退并愈合17,有研究将42 d20或56 d21作为动物皮肤结核取材的最长时间,而海分枝杆菌引起斑马鱼结核创面形成的平均时间为59 d14。本研究最长的观察时间为感染后第43天,未观察到自愈倾向,更长时间的观察有待于进一步研究。

    因结核杆菌标准毒株H37Rv对实验条件要求较高,更多研究者选择BCG作为动物实验1822和细胞实验23中模拟结核菌感染的病原体,使用低毒性的BCG可以最大限度地保障实验环境及人员的安全。大鼠饲养方便,容易获得,实验试剂供应充足,大小适中便于实验操作和观察。本研究团队前期使用BCG活菌成功建立了大鼠皮肤结核模型13,证实使用大鼠作为结核创面模型的可行性,在此基础上进行了多次建模实验,每只大鼠均可稳定地形成局部脓肿并最终破溃。前期研究显示BCG菌(1×107CFU)引起的大鼠结核创面在感染第15天仍有局部红肿13,提示局部红肿的急性炎症表现可能与接种菌量较大有关,为了建立更接近于临床的慢性结核性创面模型,本研究使用较低的接种剂量(2×106 CFU)和隧道样注射方法,在第32天可以形成结核性创面破溃表现。该方法更容易形成局部脓肿、局部炎症反应轻,更符合慢性病灶的特点。该动物模型外观符合结核性创面的临床表现,感染第8天可见注射部位皮下脓肿形成、脓腔内可见黄绿色的黏稠脓液;感染第15天皮下脓肿较前明显增大;感染第32天脓肿出现破溃,破溃后脓肿断层剖面可见皮下形成脓性隧道与外界相通;感染第43天,脓肿破溃处未见愈合倾向。该动物模型符合结核性创面的实验室诊断标准,镜下可见感染灶部位有炎性浸润及多核巨细胞,对其组织进行抗酸染色,结果为阳性。

    综上所述,本研究选用了BCG对大鼠进行建模,具有安全性、可重复性、稳定性、可控性、可靠性及对疾病的代表性,为后续研究提供了稳定的动物模型实验平台,探索使用更小接种菌量和更短的感染时间可以有效缩短研究周期、提高科研效率,这可能成为今后结核性创面动物模型的研究趋势。

    本研究的不足之处:因实验条件所限,未对该模型进行深入的细胞及分子生物水平研究。本研究采用建模动物的清洁级为SPF级,针对不同免疫状态下动物建模后的表现以及BCG是否会引起动物其他系统的播散性感染,有待进一步研究。

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