Nett Jeniel, Lincoln Leslie, Marchillo Karen, Massey Randall, Holoyda Kathleen, Hoff Brian, VanHandel Michelle, Andes David
Department of Medicine, University of Wisconsin Electron Microscopy Facility, Madison 53792, USA.
Antimicrob Agents Chemother. 2007 Feb;51(2):510-20. doi: 10.1128/AAC.01056-06. Epub 2006 Nov 27.
Biofilms are microbial communities, embedded in a polymeric matrix, growing attached to a surface. Nearly all device-associated infections involve growth in the biofilm life style. Biofilm communities have characteristic architecture and distinct phenotypic properties. The most clinically important phenotype involves extraordinary resistance to antimicrobial therapy, making biofilm infections very difficulty to cure without device removal. The current studies examine drug resistance in Candida albicans biofilms. Similar to previous reports, we observed marked fluconazole and amphotericin B resistance in a C. albicans biofilm both in vitro and in vivo. We identified biofilm-associated cell wall architectural changes and increased beta-1,3 glucan content in C. albicans cell walls from a biofilm compared to planktonic organisms. Elevated beta-1,3 glucan levels were also found in the surrounding biofilm milieu and as part of the matrix both from in vitro and in vivo biofilm models. We thus investigated the possible contribution of beta-glucans to antimicrobial resistance in Candida albicans biofilms. Initial studies examined the ability of cell wall and cell supernatant from biofilm and planktonic C. albicans to bind fluconazole. The cell walls from both environmental conditions bound fluconazole; however, four- to fivefold more compound was bound to the biofilm cell walls. Culture supernatant from the biofilm, but not planktonic cells, bound a measurable amount of this antifungal agent. We next investigated the effect of enzymatic modification of beta-1,3 glucans on biofilm cell viability and the susceptibility of biofilm cells to fluconazole and amphotericin B. We observed a dose-dependent killing of in vitro biofilm cells in the presence of three different beta-glucanase preparations. These same concentrations had no impact on planktonic cell viability. beta-1,3 Glucanase markedly enhanced the activity of both fluconazole and amphotericin B. These observations were corroborated with an in vivo biofilm model. Exogenous biofilm matrix and commercial beta-1,3 glucan reduced the activity of fluconazole against planktonic C. albicans in vitro. In sum, the current investigation identified glucan changes associated with C. albicans biofilm cells, demonstrated preferential binding of these biofilm cell components to antifungals, and showed a positive impact of the modification of biofilm beta-1,3 glucans on drug susceptibility. These results provide indirect evidence suggesting a role for glucans in biofilm resistance and present a strong rationale for further molecular dissection of this resistance mechanism to identify new drug targets to treat biofilm infections.
生物膜是嵌入聚合基质中的微生物群落,附着于表面生长。几乎所有与器械相关的感染都涉及生物膜生活方式下的生长。生物膜群落具有独特的结构和明显的表型特性。临床上最重要的表型是对抗菌治疗具有非凡的抗性,这使得在不拔除器械的情况下生物膜感染很难治愈。目前的研究检测了白色念珠菌生物膜中的耐药性。与之前的报道相似,我们在体外和体内均观察到白色念珠菌生物膜对氟康唑和两性霉素B具有显著抗性。我们发现,与浮游生物相比,生物膜中白色念珠菌的细胞壁结构发生了与生物膜相关的变化,且β-1,3-葡聚糖含量增加。在体外和体内生物膜模型中,生物膜周围环境以及作为基质一部分的区域也发现了升高的β-1,3-葡聚糖水平。因此,我们研究了β-葡聚糖对白色念珠菌生物膜抗菌抗性的可能作用。初步研究检测了生物膜和浮游白色念珠菌的细胞壁及细胞上清液结合氟康唑的能力。两种环境条件下的细胞壁均能结合氟康唑;然而,生物膜细胞壁结合的化合物量是浮游细胞细胞壁的四到五倍。生物膜的培养上清液(而非浮游细胞的上清液)能结合可测量量的这种抗真菌剂。接下来,我们研究了β-1,3-葡聚糖的酶促修饰对生物膜细胞活力以及生物膜细胞对氟康唑和两性霉素B敏感性的影响。我们观察到在三种不同的β-葡聚糖酶制剂存在的情况下,体外生物膜细胞出现剂量依赖性死亡。相同浓度对浮游细胞活力没有影响。β-1,3-葡聚糖酶显著增强了氟康唑和两性霉素B的活性。这些观察结果在体内生物膜模型中得到了证实。外源性生物膜基质和市售β-1,3-葡聚糖在体外降低了氟康唑对浮游白色念珠菌的活性。总之,当前的研究确定了与白色念珠菌生物膜细胞相关的葡聚糖变化,证明了这些生物膜细胞成分与抗真菌剂的优先结合,并表明生物膜β-1,3-葡聚糖的修饰对药物敏感性有积极影响。这些结果提供了间接证据,表明葡聚糖在生物膜抗性中发挥作用,并为进一步从分子层面剖析这种抗性机制以确定治疗生物膜感染的新药物靶点提供了有力的理论依据。