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Dermatophytic Defensin with Antiinfective Potential

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Dermatophytic Defensin with Antiinfective Potential Dermatophytic defensin with antiinfective potential Shunyi Zhua,1, Bin Gaoa, Peta J. Harveyb, and David J. Craikb aGroup of Animal Innate Immunity, State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, 100101 Beijing, China; and bInstitute for Molecular Bioscience, University of Queensland, Brisbane Queensland 4072, Australia Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved April 6, 2012 (received for review January 25, 2012) Fungi are a newly emerging source of peptide antibiotics with micasin) from the dermatophytic fungus Microsporum canis using therapeutic potential. Here, we report 17 new fungal defensin-like the synthetic peptide. Our results show that fungal genomes are a peptide (fDLP) genes and the detailed characterization of a corre- source of antiinfective therapeutic agents that can be rapidly sponding synthetic fDLP (micasin) from a dermatophyte in terms characterized by an integrated computational and experimental of its structure, activity and therapeutic potential. NMR analysis approach. The potential applications of dermatophytes in devel- showed that synthetic micasin adopts a “hallmark” cysteine- oping drugs against skin-derived bacterial infections (e.g., Staphy- stablized α-helical and β-sheet fold. It was active on both Gram- lococcus aureus and P. aeruginosa) are highlighted. positive and Gram-negtive bacteria, and importantly it killed two clinical isolates of methicillin-resistant Staphylococcus aureus Results and the opportunistic pathogen Pseudomonas aeruginosa at low Fungal Genomes Are a New Source of Defensin-Like Peptides. From micromolar concentrations. Micasin killed approximately 100% of recently sequenced fungal genomes, we identified 17 DLP genes. treated bacteria within 3 h through a membrane nondisruptive These DLPs can be grouped into four different families based mechanism of action, and showed extremely low hemolysis and on their sequence similarity, three of which are classified into high serum stability. Consistent with these functional properties, known families (fDEF1, fDEF2 and fDEF5) (12) (Fig. 1). In micasin increases survival in mice infected by the pathogenic comparison with fDEF1, fDEF2 has a smaller, less anionic pro- bacteria in a peritonitis model. Our work represents a valuable peptide, whereas the precursors of fDEF5 and the family fDEF7 approach to explore novel peptide antibiotics from a large resource lack a propeptide. Peptides in fDEF7 have a unique structural of fungal genomes. characteristic in that their amino-termini are longer and rich in histidine compared with other DLPs. ascomycota ∣ methicillin-resistant Staphylococcus aureus ∣ plectasin ∣ The fDEF1 members belong to ancient invertebrate-type mouse peritonitis model defensins (AITDs) (12) and they all originated from Pezizomy- cota (Ascomycota) classified into three genera: Ajellomyces, ntimicrobial peptides (AMPs), typically 12–80 amino acids in Arthroderma, and Trichophyton (Table S1). Species derived from Asize, are key effectors of innate immunity in multicellular the latter two genera belong to dermatophytic fungi. The mature organisms (1). They comprise the first line of defense to rapidly DLPs share 30% to 60% sequence identity with plectasin, and clear pathogens in the early stage of infection through a multi- they all carry net positive charges from þ1.2 to þ5.2 at physio- target mode of action, which may serve to prevent or delay evolu- logical pH (Fig. 1A), providing a possibility to bind polyanionic tion of microbial resistance. Their diverse action modes include bacterial membranes by electrostatic interaction. Despite the disruption of membrane integrity, impairment of nucleic acid overall net positive charge nature, these peptides have a net ne- and protein synthesis, inhibition of chaperone-assisted protein gatively charged N-terminal loop (n-loop), as in the case of folding, interruption of cell-wall biosynthesis pathway, and even plectasin. Aside from six conserved cysteines, the fDEF1 family targeting of membrane biogenesis (2–4). Some vertebrate AMPs has three identical residues (Ser17, Gly19, and Gly23, numbered (e.g., human cathelicidins and defensins) have also evolved a mul- according to micasin) whose conservation is across the alignment. tifunctional, immunomodulatory ability in bridging the innate The fDEF2 members belong to classical invertebrate-type defen- and adaptive immune systems (5). sins (CITDs) (Fig. 1B). However, unlike other known CITDs The unique properties of AMPs make them attractive candi- (12), these fungal CITDs carry net charges of −0.6 to −4.8,a dates for the development of antiinfective drugs with reduced characteristic previously observed in the tick scasin-type defen- risk of resistance (1, 6), especially when used in combination. To sins (13). Except labisin in Basidiomycota (Agaricomycotina), date, some such peptides and their derivatives are in clinical trials a sister group to the Ascomycota, all other members come from – (7 9; however, they have proven difficult to reach the market as Ascomycota (Pezizomycotina). Analysis of exon-intron structures systemic (parenteral and oral) therapeutics owing to limitations of the newly discovered DLPs revealed that despite low sequence including nonspecific toxicity, suboptimal efficacy, and lability similarity among families 1, 2, and 7, some of them share a con- to serum proteolysis (7, 8). Studies have shown that when systemi- served phase-0 intron within the α-helical region (Fig. 1), suggest- cally applied, some mammalian AMPs produce side effects, ing common ancestral origin for these DLP families. probably due to their immunomodulatory properties interfering with the normal immune network and inducing an exacerbating inflammatory response. Turning to nonmammalian sources of Author contributions: S.Z. designed research; S.Z., B.G., P.J.H., and D.J.C. performed research; S.Z., B.G., P.J.H., and D.J.C. analyzed data; and S.Z., P.J.H., and D.J.C. wrote AMPs offers the potential to develop new classes of antimicrobial SCIENCES agents. Plectasin, the first defensin isolated from the saprophytic the paper. Conflict of interest statement: Based on this work, a patent application (“Novel fungus Pseudoplectania nigrella (Ascomycota: Pezizomycota), is APPLIED BIOLOGICAL fungus-derived antiinfective defensins”) has been filed. of particular interest as it selectively targets Gram-positive bac- teria with particular activity against Streptococcus pneumoniae This article is a PNAS Direct Submission. (10). Its lack of induction of the inflammatory cytokine interleu- Data deposition: The sequences reported in this paper have been deposited in the GenBank database (http://www.ncbi.nlm.nih.gov/) [accession nos. JN014007 (micasin) and kin-8 (IL-8) has also been confirmed (11). Following its discov- JN014008 (micasin-1)]. The atomic coordinates of micasin have been deposited in the ery, plectasin-related peptides in fungi have also been reported Protein Data Bank, www.pdb.org (PDB ID code 2LR5) recently using bioinformatics approaches (12). 1To whom correspondence should be addressed. E-mail: [email protected]. Here, we describe 17 fungal defensin-like peptide (DLP) genes This article contains supporting information online at www.pnas.org/lookup/suppl/ and the detailed characterization of a DLP (herein referred to as doi:10.1073/pnas.1201263109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1201263109 PNAS ∣ May 29, 2012 ∣ vol. 109 ∣ no. 22 ∣ 8495–8500 Downloaded by guest on September 29, 2021 A Fig. 1. Multiple sequence alignment of fungal DLP fa- milies. (A) fDLP1; (B)fDLP2;(C) fDLP5; (D)fDLP7.Signalpep- tides, propeptides, and ma- ture peptides are boxed in black, red, and green, respec- tively. Cysteines are shadowed in yellow; basic and acidic resi- dues are shown in blue and red, respectively. The pairing pattern of the three disulfide B bridges and secondary struc- tural elements (cylinder: α-he- lix; arrow: β-strand) were extracted from the coordi- nates of plectasin (Protein Data Bank entry 1ZFU). HRR, histidine-rich region. Introns are indicated by arrows or small boxes. a, peptide size; b, identity to plectasin; c,net C charges, estimated at pH 7.0 using protein calculation V3.3 (http://www.scripps.edu/ ~cdputnam/protcalc.html). D Sequences described pre- viously (10, 12) are indicated by an asterisk. M. canis DLPs. M. canis is the only species whose genome encodes (4061.68 Da) calculated from its primary sequence, indicating two DLPs (micasin and micasin-1) with low sequence similarity. that six hydrogen atoms in the cysteines of the reduced peptide These two DLPs are functional genes, as evidenced by cDNA have been removed when three disulfide bridges are formed. cloning (Fig. 2A; Fig. S1). In a Neighbor-Joining (NJ) tree, We then studied the structural features of micasin by circular micasin-1 is separated as a single clade with a large distance from dichroism and found that it displayed a minimum at 208 nm micasin, whereas micasin and other members constitute another and a maximum at 198 nm (Fig. 2D), demonstrating that it has orthologous clade (Fig. 2B), suggesting that these two M. canis folded into a native-like conformation similar to other peptides DLPs originated by an early gene duplication preceding specia- with a cysteine-stabilized α-helical and β-sheet (CSαβ) fold (14). tion of Pezizomycotina. In the subsequent evolution, the ortho- logue of this gene lost
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