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West China Journal of Stomatology logoLink to West China Journal of Stomatology
. 2020 Oct;38(5):576–582. [Article in Chinese] doi: 10.7518/hxkq.2020.05.018

韦荣球菌与口腔疾病的研究进展

Research progress in the relationship between Veillonella and oral diseases

罗 瑜雪 1, 孙 蔓琳 1, 施 培磊 1, 刘 盼 1, 陈 艺尹 1, 彭 显 1,
Editor: 张 玉楠1
PMCID: PMC7573782  PMID: 33085245

Abstract

韦荣球菌是口腔生物膜的早期定植菌之一,高丰度分布于口腔微生态中。目前在口腔中已检出7种韦荣球菌,其在不同部位、不同患者口腔中存在分布差异。近年来研究发现,韦荣球菌与口腔疾病的关系密切,韦荣球菌有助于变异链球菌的黏附且能分解链球菌代谢产生的乳酸,是被公认的致龋因素之一;韦荣球菌为牙龈卟啉单胞菌提供黏附位点,并可通过促进免疫反应参与牙周病的发生发展;韦荣球菌脂多糖的致病性及代谢产生H2S也与牙髓及根尖周病、口臭等相关。韦荣球菌与疾病的相关性已有研究进行阐释,与相关致病菌的作用机制也有一定进展,但其影响口腔疾病发生发展的分子机制仍不明确,本文就韦荣球菌与龋病、牙周病等口腔感染性疾病的研究进展作一综述。

Keywords: 韦荣球菌, 龋病, 牙周病, 口腔疾病


1898年,法国微生物学家Veillon和Zuber从人的感染阑尾中首次分离出一种革兰阴性专性厌氧球菌,1933年,Prévot将之命名为“Veillonella parvula”,之后韦荣球菌属下的各韦荣球菌种被科学家们陆续分离得到。韦荣球菌属是口腔微生态的重要成员之一,除了口腔,韦荣球菌也存在于人类上呼吸道、肠道和阴道等位置。有研究[1]显示,健康成人唾液、牙菌斑中韦荣球菌丰度仅次于链球菌。目前报道过的韦荣球菌共有14种,其中有7种可从人口腔中分离得到:小韦荣菌(Veillonella parvulaV. parvula)、殊异韦荣菌(Veillonella disparV. dispar)、非典型韦荣菌(Veillonella atypicaV. atypica)、Veillonella rogosaeVeillonella denticariosiVeillonella tobetsuensisVeillonella infantium[2][5]。由于具有相似的生化特性和表型特征,韦荣球菌种类的鉴别目前主要是基于16S rDNA、dnaK、rpoB和gltA等基因的差异[6][7]。在人口腔中,韦荣球菌主要分布于唾液、舌黏膜及颊黏膜、牙龈及龈沟,不同种韦荣球菌的分布存在一定差异。Doel等[8]分析样本后发现了V. atypica的检出率为舌面>唾液>牙菌斑,V. dispar的检出率为舌面>唾液,V. parvula在牙菌斑中检出率最高。V. dispar主要在口腔卫生指标良好或社会经济地位高者口腔内检出[9]V. parvula在儿童中检出最频繁,而严重的早发性孩童期龋齿与V. atypica有关[10];牙周袋中V. parvula的检出率比在牙龈沟中更高,与慢性牙周炎有关[11]。地区、年龄、吸烟、饮食、口腔卫生及患病情况等影响因素也会造成菌种分布的差异[12][14]。韦荣球菌不能代谢碳水化合物和多元醇,但能利用短链有机酸,特别是利用乳酸作为能源,转化为酸性较弱的乙酸和丙酸。口腔韦荣球菌因其代谢乳酸可降低pH的特性曾被认为是防龋的益生菌,后多项研究[15][16]表明,口腔韦荣球菌与龋病密切相关,可协同变异链球菌(Streptococcus mutansS. mutans)致龋。除此之外,口腔韦荣球菌与牙髓、根尖周感染以及慢性牙周炎等口腔疾病也有一定关系。因此,韦荣球菌属在口腔微生态中的作用及其与口腔疾病的相关性不容忽视。

1. 韦荣球菌与龋病

龋病是在以细菌为主的多种因素影响下,牙体硬组织发生慢性进行性破坏的一种疾病,链球菌属为常见的致龋微生物之一。链球菌可分解碳水化合物产酸,使牙面局部pH下降造成脱矿而致龋,因此能利用其他细菌产生的乳酸而减少牙脱矿的韦荣球菌与龋病的关系值得探讨。

1.1. 韦荣球菌与龋病相关性的研究

关于韦荣球菌属在龋病与非龋病人群口腔中的分布情况仍存在争议。有关于根面龋、乳牙龋等的研究[10],[17]认为,韦荣球菌属在龋病组中的丰度和检出率高于无龋组,是龋病的优势菌之一;然而有研究[18][19]则得出相反结论,也有实验[20][21]证明,其丰度无显著差别。Tanner等[21]则发现,V. parvula在严重儿童龋的样本中检出率显著高于无龋组,而V. dispar在无龋组的检出率显著高于严重儿童龋组。综上,近来的研究[22]更倾向于认为,韦荣球菌属在龋病发生发展中有重要作用,其与链球菌属在生物膜形成过程中的形态结构、生长代谢、细菌间共聚集及其他黏附现象、环境因素等方面的相互作用不可忽视。Guggenheim等[23]观察到在生物膜形成过程中,V. dispar发生了形态上的转变,由在整个生物膜中稀疏散布的单个球菌和大多数小球状小菌落,到不存在单细胞且大多数小菌落是细长细胞桥连接而成的大扁圆结构。Kara等[24]发现,S. mutansV. parvula双菌种生物膜中的细菌会聚集成距离小于1.2 µm的空间排列。在口腔内唾液流动的环境中,链球菌的黏附为韦荣球菌提供了位点,当链球菌不存在,韦荣球菌则不能附着并生长[25]。许多研究[15],[25][26]也通过链球菌与韦荣球菌的双菌种生物模型反复验证了,韦荣球菌的存在能促进S. mutans、戈登链球菌(Streptococcus gordoniiS. gordonii)及唾液链球菌(Streptococcus salivariusS. salivarius)生物膜的形成,而与口腔链球菌(Streptococcus oralisS. oralis)及血链球菌(Streptococcus sanguinisS. sanguinis)的生长无关甚至抑制。

1.2. 韦荣球菌与链球菌的相互作用

S. mutansS. gordonii、韦荣球菌这3种菌种的相互作用涉及多个层面(图1)。S. gordonii可以通过产生H2O2抑制S. mutans的生长,而S. mutans产生细菌素抑制S. gordonii[27]V. parvula参与的生物膜形成则能减少H2O2S. mutans的抑制[28],Zhou等[29]V. parvula PK1910的过氧化氢酶基因(catA)整合到V. atypica OK5,证实了catA基因产物能保护具核梭杆菌在S. gordonii产生的H2O2环境下生长的猜想。Liu等[27]通过向S. mutansS. gordonii双菌种模型中加入V. parvulaS. mutans生长速率和最终生物量的增加证明了V. parvula能平衡两者的竞争。链球菌发酵碳水化合物产生的有机酸可作为韦荣球菌的碳源,V. disparV. atypica是口腔中硝酸盐还原细菌的重要组成部分[30],有助于硝酸盐转化成抑制龋洞中产酸细菌生长的还原产物[31]V. atypica PK1910与相对分子质量为4.5×104的蛋白有关的黏附素、V. atypica OK5的表面蛋白血凝素(hemagglutinin,Hag)1,S. gordonii的表面黏附素Hsa均可介导两者的属间共聚集[32][34],而V. tobetsuensis产生的环状二肽会抑制S. gordonii生物膜的形成[35],Egland等[36]和Johnson等[37]则观察到S. gordoniiV. atypica PK1910之间有特异性可扩散信号传导现象,由于转录因子CcpA的诱导作用,V. atypica使S. gordonii的α-淀粉酶amyB基因的淀粉酶产物活性增加,促进糖原水解,提高碳水化合物利用率和乳酸生成量,有助于细菌生长。

图 1. S. mutansS. gordonii、韦荣球菌的相互作用.

图 1

Fig 1 The internaction between S. mutans, S. gordonii and Veillonella

2. 韦荣球菌与牙周病

牙周病是发生在牙的支持组织的疾病,主要临床症状是牙龈出血、牙槽骨吸收、牙周袋形成、牙齿松动,牙菌斑生物膜是牙周病的一个最重要致病因素,牙周病是牙菌斑微生态失衡使牙周致病菌成为优势菌群的结果。较牙周健康人群来说,牙周病患者口腔中韦荣球菌丰度显著增高[38]

2.1. 韦荣球菌直接参与牙周病的进展

通过调节中性粒细胞[39]等免疫细胞的功能及炎症介质反应[40],微生物可影响牙周炎的发生发展。Hirschfeld等[41]通过研究人外周血中性粒细胞对19种牙周菌斑优势菌的反应发现,牙周炎组织损伤可能是由牙菌斑诱导的细胞外活性氧释放过多引起的,活性氧虽然有助于微生物的杀灭,但其却并不能区分病原体和宿主组织。研究还提示,中性粒细胞在牙周细菌刺激下,会促进细胞外、细胞内和超氧化物释放,且具有物种特异性,与其他微生物相比,V. parvula能刺激更高水平的中性粒细胞胞外杀菌网络和活性氧的释放。Ji等[42]在研究非牙周致病菌与牙周致病菌对牙龈上皮细胞先天免疫应答的影响中发现,作为非牙周致病菌的V. atypica可显著诱导牙龈上皮细胞产生一种在炎症或感染状态下才产生的广谱抗菌肽,即人β防御素-3(human beta defensin-3,HBD-3)。此外,韦荣球菌具有强毒性内毒素,可能通过引起非特性免疫反应参与牙周病的进展[43],其脂多糖(lipopolysaccharide,LPS)也被证明可通过介导前列腺素E2生成而促进骨的吸收[44]

2.2. 韦荣球菌协同牙龈卟啉单胞菌影响牙周病的发生发展

韦荣球菌作为“桥接菌”,附着于早期定植菌后,吸附中、晚期定植菌。牙龈卟啉单胞菌(Porphyromonas gingivalisP. gingivalis)是公认的牙周致病菌[45],也是晚期定植菌,韦荣球菌与P. gingivalis在形成生物膜过程中的协同作用[46]与二者间的黏附密切相关。一方面,韦荣球菌可为P. gingivalis提供黏附位点。Zhou等[34]研究发现V. atypica表面存在一种蛋白Hag1,可以介导韦荣球菌与P. gingivalis的黏附。Hag1是韦荣球菌第一个被证实的表面蛋白,为目前已知最大的Hag基因。Hag1可以介导韦荣球菌与一些早期定植菌如S. gordonii等的聚集,以及晚期定植菌如P. gingivalis等的黏附[47]。Hag1基因位于单基因操纵子上,编码蛋白为三聚体自转运蛋白,由头、颈、体、膜锚定域4部分组成,头部形成浅口袋形的受体结合域,颈部具有弹性连接头部与体部,体部借锚定域锚定在外膜上(图2A)。Eke等[48]曾得到韦荣球菌与P. gingivalis的黏附受乳糖、半乳糖抑制的结论,由此推断其黏附机制包括糖结合作用,且可能受菌种、菌液的密度标准、加入乳糖的顺序、加入乳糖的量、允许两菌反应的时间长度影响。Zhou等[34]发现,乳糖、半乳糖处理对V. atypicaP. gingivalis的黏附无影响。Park等[49]研究表明,血清型、菌株特异性的黏附在口腔菌群间十分常见,即韦荣球菌、P. gingivalis不同亚型之间的相互黏附均有差异,可分为乳糖敏感性及非乳糖敏感型。S. gordonii通过唾液酸结合性蛋白(sialic acid-binding adhesin,Hsa)与韦荣球菌表面蛋白Hag1结合黏附[33][34]P. gingivalis表面与Hag1的结合受体仍未知,而胎球蛋白能够在一定程度上抑制韦荣球菌与P. gingivalis的黏附,证明其黏附机制中包括唾液酸结合作用(图2B)。

图 2. V. atypicaS. gordoniiP. gingivalis的相互作用.

图 2

Fig 2 The internaction between V. atypica, S. gordonii and P. gingivalis

A:Hag1基因编码的蛋白结构;B:V. atypicaS. gordoniiP. gingivalis的结合黏附模型,S. gordonii代谢碳水化合物产生的乳酸为V. atypica提供碳源,V. atypica合成的氯化血红素促进P. gingivalis的生长,S. gordonii通过唾液酸结合性蛋白Hsa与V. atypica表面蛋白Hag1结合黏附,而P. gingivalis表面与Hag1的结合受体仍未知。

另一方面,韦荣球菌可以为P. gingivalis提供营养来源。Zhou等[50]V. atypica的细胞裂解液中检测到氯化血红素及其相关产物,表明存在氯化血红素生物合成途径,他们还证明了韦荣球菌通过提供P. gingivalis生长所必需的氯化血红素促进其生长,P. gingivalis又可使韦荣球菌的氯化血红素合成表达上调。在组成成分不包含氯化血红素的培养基中无法存活的P. gingivalis,加入灭活氯化血红素合成基因的V. atypica后数量可倍增,说明韦荣球菌还可通过其他途径促进P. gingivalis生长,亟待进一步研究。此外,V. parvula对四环素等牙周炎常用抗菌药物具有天生抗性[51],生物膜中韦荣球菌的存在降低其对抗菌素的敏感性。

3. 韦荣球菌与其他口腔疾病

牙髓和根尖周病变中频繁检出韦荣球菌[52],多为V. parvula,韦荣球菌致病性可能与其产生的LPS有关,LPS能够激活机体的补体系统[53],持续释放促炎症因子。对于其引起根尖周病变的免疫潜力方面,有研究发现,V. parvula蛋白和LPS均对巨噬细胞和淋巴细胞具有免疫调节作用,能显著增强人外周血单核细胞迁移活性[54],且V. parvula产生的LPS是人外周血单个核细胞产生细胞因子的弱刺激因子[55]。牙髓及根尖周感染通常为混合感染,韦荣球菌和其他细菌之间的相互作用也不容忽视,V. parvula能够产维生素K2供卟啉单胞菌属和普雷沃菌属利用[56]。此外,V. parvula在与牙密螺旋体的共培养中能够促进其生长[57]

口臭的主要来源是口腔内细菌代谢产生的H2S等含硫化合物,该过程受到口腔环境因素pH和乳酸的调节。韦荣球菌可通过分解L-半胱氨酸产H2S[58],Washio等[59]的研究发现,口腔中脱落细胞中的主要蛋白质——角蛋白,可以作为L-半胱氨酸在口腔中的来源,而位于细胞质中的多种酶参与了其代谢过程,而关于韦荣球菌产生H2S的具体酶和通路仍不明确;他们还发现,乳酸的存在可以通过激活L-半胱氨酸降解前的过程,如细胞膜上L-半胱氨酸的摄取,来显著提高韦荣球菌静息细胞H2S生成量,并且在pH=6~7时,H2S生成量较高,pH=5时,H2S生成量较低。已有研究[60]证明,由产碱韦荣球菌(Veillonella alcalescens)产生的膜泡具有对谷氨酸和丝氨酸的摄取活性,并伴有乳酸作为电子供体参与电子传递系统。韦荣球菌是否可通过类似的系统影响H2S的产生还有待进一步研究。

4. 韦荣球菌分子机制的研究进展

韦荣球菌曾经由于基因改造、遗传操作的困难,是人类口腔微生物群中最普遍但研究最少的微生物之一。而Liu等[61]通过电穿孔成功将靶向突变引入到V. parvula PK1910的染色体中,第一次验证了韦荣球菌的可转化性。但是转化效率较低,因此,他们又基于韦荣球菌的内源质粒构建了第一个大肠杆菌-韦荣球菌穿梭载体,开发了第一个遗传可转化菌株V. atypica OK5[62],并测定了完整基因组序列[63]。但是在下游基因不产生极性效应的情况下,单交叉诱变系统不能在多基因操纵子中产生突变,因此,他们再次利用V. atypica建立了第一个反向无标记诱变系统[64],这样的遗传转化系统不仅可以用于基因缺失研究,还可以用于插入序列。由于通过电穿孔的等位基因交换突变已经被证实是无效的,Knapp等[65]验证了V. parvula菌株等位基因置换突变的自然转化能力较常见。Zhou等[33][34]利用该遗传可转化菌株V. atypica OK5鉴定出Hag1黏附素参与韦荣球菌与链球菌、P. gingivalis和人体颊细胞的分子识别、共聚集过程;并证明了存在促进牙周病原体生长的血红素生物合成途径[50];证实了韦荣球菌的catA基因产物过氧化氢酶能保护具核梭杆菌等其他细菌在H2O2环境的生长[29]。韦荣球菌遗传转化系统的建立为韦荣球菌在口腔生物膜形成中的桥接作用及疾病防治的研究提供新的思路,有利于深入了解人类口腔生物膜的生态学。

5. 总结

综上所述,韦荣球菌与龋病、牙周病、牙髓及根尖周病、口臭等口腔疾病存在相关性,但在分子水平上的具体机制仍不够清楚。龋病方面,早期认为可利用乳酸减少牙脱矿的韦荣球菌有防龋作用,尽管针对龋病患者口腔韦荣球菌的分布情况仍无统一定论,但目前研究更倾向于认可韦荣球菌在致龋过程中发挥重要作用,由于其与链球菌属间的共聚集和黏附、并能促进形成生物膜,以及在代谢方面有协同生长作用,而其与链球菌的具体黏附方式及促进链球菌生物膜形成的机制尚不清楚。牙周病方面,韦荣球菌通过调节免疫反应中的中性粒细胞和释放活性氧、为牙周致病菌提供黏附位点和营养来源参与牙周病的进展,但与P. gingivalis表面的结合位点仍不明确,也需要进一步研究促进P. gingivalis生长的其他代谢途径。口腔疾病是多种微生物、多因素共同作用的结果,目前韦荣球菌与致病菌在某些方面的协同关系已被证实,其在分子水平上影响口腔疾病的具体机制、是否促进疾病发生发展仍需要进一步研究。

Funding Statement

[基金项目] 国家自然科学基金(81700963);四川省科技计划项目(2018JY0561)

Supported by: The National Natural Science Foundation of China (81700963); Sichuan Science and Technology Program (2018JY0561).

Footnotes

利益冲突声明:作者声明本文无利益冲突。

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