Deng Lingquan, Bensing Barbara A, Thamadilok Supaporn, Yu Hai, Lau Kam, Chen Xi, Ruhl Stefan, Sullam Paul M, Varki Ajit
Glycobiology Research and Training Center, Departments of Medicine and Cellular & Molecular Medicine, University of California, San Diego, San Diego, California, United States of America.
Department of Medicine, San Francisco Veterans Affairs Medical Center and the University of California, San Francisco, San Francisco, California, United States of America.
PLoS Pathog. 2014 Dec 4;10(12):e1004540. doi: 10.1371/journal.ppat.1004540. eCollection 2014 Dec.
Damaged cardiac valves attract blood-borne bacteria, and infective endocarditis is often caused by viridans group streptococci. While such bacteria use multiple adhesins to maintain their normal oral commensal state, recognition of platelet sialoglycans provides an intermediary for binding to damaged valvular endocardium. We use a customized sialoglycan microarray to explore the varied binding properties of phylogenetically related serine-rich repeat adhesins, the GspB, Hsa, and SrpA homologs from Streptococcus gordonii and Streptococcus sanguinis species, which belong to a highly conserved family of glycoproteins that contribute to virulence for a broad range of Gram-positive pathogens. Binding profiles of recombinant soluble homologs containing novel sialic acid-recognizing Siglec-like domains correlate well with binding of corresponding whole bacteria to arrays. These bacteria show multiple modes of glycan, protein, or divalent cation-dependent binding to synthetic glycoconjugates and isolated glycoproteins in vitro. However, endogenous asialoglycan-recognizing clearance receptors are known to ensure that only fully sialylated glycans dominate in the endovascular system, wherein we find these particular streptococci become primarily dependent on their Siglec-like adhesins for glycan-mediated recognition events. Remarkably, despite an excess of alternate sialoglycan ligands in cellular and soluble blood components, these adhesins selectively target intact bacteria to sialylated ligands on platelets, within human whole blood. These preferred interactions are inhibited by corresponding recombinant soluble adhesins, which also preferentially recognize platelets. Our data indicate that circulating platelets may act as inadvertent Trojan horse carriers of oral streptococci to the site of damaged endocardium, and provide an explanation why it is that among innumerable microbes that gain occasional access to the bloodstream, certain viridans group streptococci have a selective advantage in colonizing damaged cardiac valves and cause infective endocarditis.
受损的心脏瓣膜会吸引血源细菌,感染性心内膜炎通常由草绿色链球菌引起。虽然这类细菌利用多种黏附素来维持其正常的口腔共生状态,但对血小板唾液酸聚糖的识别为其与受损瓣膜心内膜的结合提供了媒介。我们使用定制的唾液酸聚糖微阵列来探究来自戈登链球菌和血链球菌的系统发育相关的富含丝氨酸重复黏附素(GspB、Hsa和SrpA同源物)的不同结合特性,这些黏附素属于一个高度保守的糖蛋白家族,对多种革兰氏阳性病原体的毒力有贡献。含有新型唾液酸识别Siglec样结构域的重组可溶性同源物的结合谱与相应全细菌与阵列的结合情况密切相关。这些细菌在体外对合成糖缀合物和分离的糖蛋白表现出多种聚糖、蛋白质或二价阳离子依赖性结合模式。然而,已知内源性去唾液酸聚糖识别清除受体可确保只有完全唾液酸化的聚糖在血管内系统中占主导地位,而我们发现这些特定的链球菌在聚糖介导的识别事件中主要依赖其Siglec样黏附素。值得注意的是,尽管细胞和可溶性血液成分中存在过量的替代唾液酸聚糖配体,但这些黏附素在人全血中选择性地将完整细菌靶向血小板上的唾液酸化配体。这些优先相互作用被相应的重组可溶性黏附素抑制,后者也优先识别血小板。我们的数据表明,循环血小板可能作为口腔链球菌无意中的特洛伊木马载体将其运送至受损心内膜部位,并解释了为什么在偶尔进入血液的无数微生物中,某些草绿色链球菌在定植受损心脏瓣膜并引起感染性心内膜炎方面具有选择性优势。