Manzo Giorgia, Scorciapino Mariano A, Wadhwani Parvesh, Bürck Jochen, Montaldo Nicola Pietro, Pintus Manuela, Sanna Roberta, Casu Mariano, Giuliani Andrea, Pirri Giovanna, Luca Vincenzo, Ulrich Anne S, Rinaldi Andrea C
Department of Chemical and Geological Sciences, University of Cagliari, Cittadella Universitaria, I-09042 Monserrato (CA), Italy.
Institute of Biological Interfaces (IBG-2), Karlsruhe Institute of Technology (KIT), POB 3640, 76021 Karlsruhe, Germany.
PLoS One. 2015 Jan 24;10(1):e0116379. doi: 10.1371/journal.pone.0116379. eCollection 2015.
SB056 is a novel semi-synthetic antimicrobial peptide with a dimeric dendrimer scaffold. Active against both Gram-negative and -positive bacteria, its mechanism has been attributed to a disruption of bacterial membranes. The branched peptide was shown to assume a β-stranded conformation in a lipidic environment. Here, we report on a rational modification of the original, empirically derived linear peptide sequence [WKKIRVRLSA-NH2, SB056-lin]. We interchanged the first two residues [KWKIRVRLSA-NH2, β-SB056-lin] to enhance the amphipathic profile, in the hope that a more regular β-strand would lead to a better antimicrobial performance. MIC values confirmed that an enhanced amphiphilic profile indeed significantly increases activity against both Gram-positive and -negative strains. The membrane binding affinity of both peptides, measured by tryptophan fluorescence, increased with an increasing ratio of negatively charged/zwitterionic lipids. Remarkably, β-SB056-lin showed considerable binding even to purely zwitterionic membranes, unlike the original sequence, indicating that besides electrostatic attraction also the amphipathicity of the peptide structure plays a fundamental role in binding, by stabilizing the bound state. Synchrotron radiation circular dichroism and solid-state 19F-NMR were used to characterize and compare the conformation and mobility of the membrane bound peptides. Both SB056-lin and β-SB056-lin adopt a β-stranded conformation upon binding POPC vesicles, but the former maintains an intrinsic structural disorder that also affects its aggregation tendency. Upon introducing some anionic POPG into the POPC matrix, the sequence-optimized β-SB056-lin forms well-ordered β-strands once electro-neutrality is approached, and it aggregates into more extended β-sheets as the concentration of anionic lipids in the bilayer is raised. The enhanced antimicrobial activity of the analogue correlates with the formation of these extended β-sheets, which also leads to a dramatic alteration of membrane integrity as shown by 31P-NMR. These findings are generally relevant for the design and optimization of other membrane-active antimicrobial peptides that can fold into amphipathic β-strands.
SB056是一种具有二聚体树枝状支架的新型半合成抗菌肽。它对革兰氏阴性菌和阳性菌均有活性,其作用机制被认为是破坏细菌膜。研究表明,这种分支肽在脂质环境中呈现β链构象。在此,我们报道了对最初通过经验推导得到的线性肽序列[WKKIRVRLSA-NH2,SB056-lin]进行的合理修饰。我们交换了前两个残基[KWKIRVRLSA-NH2,β-SB056-lin]以增强两亲性,希望更规则的β链能带来更好的抗菌性能。最低抑菌浓度(MIC)值证实,增强的两亲性确实显著提高了对革兰氏阳性菌和阴性菌菌株的活性。通过色氨酸荧光测量,两种肽的膜结合亲和力都随着带负电荷/两性离子脂质比例的增加而增加。值得注意的是,与原始序列不同,β-SB056-lin即使对纯两性离子膜也表现出相当强的结合能力,这表明除了静电吸引外,肽结构的两亲性在结合过程中也起着重要作用,通过稳定结合状态。同步辐射圆二色光谱和固态19F-核磁共振被用于表征和比较膜结合肽段的构象和流动性。SB056-lin和β-SB056-lin在结合1-棕榈酰-2-油酰-sn-甘油-3-磷酸胆碱(POPC)囊泡时均呈现β链构象,但前者保持着内在的结构无序性,这也影响了其聚集倾向。在将一些阴离子型1-棕榈酰-2-油酰-sn-甘油-3-磷酸甘油(POPG)引入POPC基质后,序列优化后的β-SB056-lin一旦接近电中性就会形成排列有序的β链,并且随着双层中阴离子脂质浓度的升高,它会聚集形成更伸展的β片层。类似物增强的抗菌活性与这些伸展的β片层的形成相关,31P-核磁共振显示这也导致了膜完整性的显著改变。这些发现对于设计和优化其他能够折叠成两亲性β链的膜活性抗菌肽具有普遍意义。