{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T08:23:49Z","timestamp":1785313429569,"version":"3.55.0"},"reference-count":64,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T00:00:00Z","timestamp":1704672000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>Cryptococcosis and cryptococcal meningitis, caused by <jats:italic>Cryptococcus neoformans<\/jats:italic> infections, lead to approximately 180,000 deaths per year, primarily in developing countries. Individuals with compromised immune systems, e.g., due to HIV infection (AIDS) or chemotherapy, are particularly vulnerable. Conventional treatment options are often limited and can cause severe side effects. Therefore, this study aimed to investigate the antifungal effect of insect-derived proline-rich antimicrobial peptides (PrAMPs) against <jats:italic>C. neoformans<\/jats:italic>. These peptides are known for their low toxicity and their high efficacy in murine infection models, making them a promising alternative for treatment.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A preliminary screening of the minimal inhibitory concentrations (MICs) of 20 AMPs, including the well-known PrAMPs Onc112, Api137, and Chex1Arg20 as well as the cathelicidin CRAMP against the <jats:italic>C. neoformans<\/jats:italic> strains 1841, H99, and KN99\u03b1 revealed promising results, with MICs as low as 1.6\u2009\u03bcmol\/L. Subsequent investigations of selected peptides, determining their influence on fungal colony-forming units, confirmed their strong activity. The antifungal activity was affected by factors such as peptide net charge and sequence, with stronger effects at higher net charges probably due to better intracellular uptake confirmed by confocal laser scanning microscopy. Inactive scrambled peptides suggest a specific intracellular target, although scanning electron microscopy showed that PrAMPs also damaged the cell exterior for a low proportion of the cells. Possible pore formation could facilitate entry into the cytosol.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2023.1328890","type":"journal-article","created":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T05:40:20Z","timestamp":1704692420000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Evaluation of proline-rich antimicrobial peptides as potential lead structures for novel antimycotics against Cryptococcus neoformans"],"prefix":"10.3389","volume":"14","author":[{"given":"Alexandra","family":"Brakel","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Grochow","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefanie","family":"Fritsche","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Knappe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andor","family":"Krizsan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simone A.","family":"Fietz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gottfried","family":"Alber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ralf","family":"Hoffmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Uwe","family":"M\u00fcller","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,1,8]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"2055","DOI":"10.1016\/j.peptides.2004.08.004","article-title":"Antimicrobial activity of Bac7 fragments against drug-resistant clinical isolates","volume":"25","author":"Benincasa","year":"2004","journal-title":"Peptides"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1128\/AAC.01923-12","article-title":"Novel apidaecin 1b analogs with superior serum stabilities for treatment of infections by gram-negative pathogens","volume":"57","author":"Berthold","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"39","DOI":"10.3389\/fcell.2016.00039","article-title":"N-terminal Ile-Orn- and Trp-Orn-motif repeats enhance membrane interaction and increase the antimicrobial activity of Apidaecins against Pseudomonas aeruginosa","volume":"4","author":"Bluhm","year":"2016","journal-title":"Front. Cell Dev. Biol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"3","DOI":"10.3390\/jof3040057","article-title":"Global and multi-National Prevalence of fungal diseases-estimate precision","volume":"3","author":"Bongomin","year":"2017","journal-title":"J Fungi (Basel)"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"798006","DOI":"10.3389\/fchem.2022.798006","article-title":"Functional effects of ARV-1502 analogs against bacterial Hsp70 and implications for antimicrobial activity","volume":"10","author":"Brakel","year":"","journal-title":"Front. Chem."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"23","DOI":"10.3390\/ijms23063150","article-title":"Influence of substitutions in the binding motif of proline-rich antimicrobial peptide ARV-1502 on 70S ribosome binding and antimicrobial activity","volume":"23","author":"Brakel","year":"","journal-title":"Int. J. Mol. Sci."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"753","DOI":"10.3389\/fchem.2019.00753","article-title":"Quantitation of a novel engineered anti-infective host defense peptide, ARV-1502: pharmacokinetic study of different doses in rats and dogs","volume":"7","author":"Brakel","year":"2019","journal-title":"Front. Chem."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"165rv13","DOI":"10.1126\/scitranslmed.3004404","article-title":"Hidden killers: human fungal infections","volume":"4","author":"Brown","year":"2012","journal-title":"Sci. Transl. Med."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1080\/13693780600735452","article-title":"Role of birds of prey as carriers and spreaders of Cryptococcus neoformans and other zoonotic yeasts","volume":"44","author":"Cafarchia","year":"2006","journal-title":"Med. Mycol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"822","DOI":"10.1080\/21505594.2018.1431087","article-title":"The capsule of Cryptococcus neoformans","volume":"10","author":"Casadevall","year":"2019","journal-title":"Virulence"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"354","DOI":"10.1016\/S1369-5274(00)00103-X","article-title":"Melanin and virulence in Cryptococcus neoformans","volume":"3","author":"Casadevall","year":"2000","journal-title":"Curr. Opin. Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"746006","DOI":"10.3389\/fmicb.2021.746006","article-title":"A novel antimicrobial peptide Sparamosin26-54 from the mud crab Scylla paramamosain showing potent antifungal activity against Cryptococcus neoformans","volume":"12","author":"Chen","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1066","DOI":"10.1016\/j.bbamem.2012.12.013","article-title":"Structural and functional studies on a proline-rich peptide isolated from swine saliva endowed with antifungal activity towards Cryptococcus neoformans","volume":"1828","author":"Conti","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1021\/cb300063v","article-title":"Api88 is a novel antibacterial designer peptide to treat systemic infections with multidrug-resistant gram-negative pathogens","volume":"7","author":"Czihal","year":"2012","journal-title":"ACS Chem. Biol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1724","DOI":"10.1016\/j.bpj.2016.08.032","article-title":"Mode of action of a designed antimicrobial peptide: high potency against Cryptococcus neoformans","volume":"111","author":"Datta","year":"2016","journal-title":"Biophys. J."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"4994","DOI":"10.1128\/IAI.66.10.4994-5000.1998","article-title":"Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans","volume":"66","author":"Decken","year":"1998","journal-title":"Infect. Immun."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1414","DOI":"10.1126\/science.aaa6097","article-title":"Infectious disease. How to bolster the antifungal pipeline","volume":"347","author":"Denning","year":"2015","journal-title":"Science"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1016\/j.tim.2010.02.004","article-title":"Therapy for fungal diseases: opportunities and priorities","volume":"18","author":"Denning","year":"2010","journal-title":"Trends Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"2052","DOI":"10.1038\/s41467-023-37573-y","article-title":"A host defense peptide mimetic, brilacidin, potentiates caspofungin antifungal activity against human pathogenic fungi","volume":"14","author":"Dos Reis","year":"2023","journal-title":"Nat. Commun."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1038\/s41579-022-00720-1","article-title":"Tackling the emerging threat of antifungal resistance to human health","volume":"20","author":"Fisher","year":"2022","journal-title":"Nat. Rev. Microbiol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1128\/mBio.00449-20","article-title":"Threats posed by the fungal kingdom to humans, wildlife, and agriculture","volume":"11","author":"Fisher","year":"2020","journal-title":"MBio"},{"key":"ref22","first-page":"599","article-title":"Absence of in vitro innate immunomodulation by insect-derived short proline-rich antimicrobial peptides points to direct antibacterial action in vivo","volume-title":"J. Pept. 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Rep."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/j.ejps.2018.01.017","article-title":"Amphotericin B-albumin conjugates: synthesis, toxicity and anti-fungal activity","volume":"115","author":"Gurudevan","year":"2018","journal-title":"Eur. J. Pharm. Sci."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"5194","DOI":"10.1128\/AAC.00585-12","article-title":"Intracellular toxicity of proline-rich antimicrobial peptides shuttled into mammalian cells by the cell-penetrating peptide penetratin","volume":"56","author":"Hansen","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1128\/CMR.8.4.462","article-title":"New and emerging yeast pathogens","volume":"8","author":"Hazen","year":"1995","journal-title":"Clin. Microbiol. 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Chem."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"e202100609","DOI":"10.1002\/cbic.202100609","article-title":"Effect of amino acid substitutions on 70S ribosomal binding, cellular uptake, and antimicrobial activity of Oncocin Onc112","volume":"23","author":"Kolano","year":"2021","journal-title":"Chembiochem"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.jgar.2020.12.012","article-title":"Proline-rich antimicrobial peptide Api137 is bactericidal in porcine blood infected ex vivo with a porcine or human Klebsiella pneumoniae strain","volume":"24","author":"Krieger","year":"2021","journal-title":"J Glob Antimicrob Resist"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"5992","DOI":"10.1128\/AAC.01307-15","article-title":"Influence of the yjiL-mdtM gene cluster on the antibacterial activity of proline-rich antimicrobial peptides overcoming Escherichia coli resistance induced by the missing SbmA transporter system","volume":"59","author":"Krizsan","year":"","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"2304","DOI":"10.1002\/cbic.201500375","article-title":"Short proline-rich antimicrobial peptides inhibit either the bacterial 70S ribosome or the assembly of its large 50S subunit","volume":"16","author":"Krizsan","year":"","journal-title":"Chembiochem"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"12236","DOI":"10.1002\/anie.201407145","article-title":"Insect-derived proline-rich antimicrobial peptides kill bacteria by inhibiting bacterial protein translation at the 70S ribosome","volume":"53","author":"Krizsan","year":"2014","journal-title":"Angew. Chem."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"2439","DOI":"10.1002\/bit.27092","article-title":"Identification and elucidation of proline-rich antimicrobial peptides with enhanced potency and delivery","volume":"116","author":"Lai","year":"2019","journal-title":"Biotechnol. Bioeng."},{"key":"ref42","first-page":"305","article-title":"Fungicidal effect of indolicidin and its interaction with phospholipid membranes","volume-title":"Biochem. Biophys. Res. Commun.","author":"Lee","year":"2003"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"26","DOI":"10.3390\/molecules26113438","article-title":"Activity and mechanism of action of antifungal peptides from microorganisms: a review","volume":"26","author":"Li","year":"2021","journal-title":"Molecules"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1146\/annurev.micro.60.080805.142102","article-title":"The biology of the Cryptococcus neoformans species complex","volume":"60","author":"Lin","year":"2006","journal-title":"Annu. Rev. Microbiol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"241","DOI":"10.2174\/1386207053764576","article-title":"Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics","volume":"8","author":"Lohner","year":"2005","journal-title":"Comb. Chem. High Throughput Screen."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"3365","DOI":"10.1128\/JCM.39.9.3365-3367.2001","article-title":"Cryptococcus neoformans var. neoformans (serotype D) strains are more susceptible to heat than C. neoformans var. grubii (serotype a) strains","volume":"39","author":"Martinez","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1111\/j.1365-2958.2007.05903.x","article-title":"Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides","volume":"66","author":"Mattiuzzo","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"e2202368","DOI":"10.1002\/adhm.202202368","article-title":"In vitro properties and pharmacokinetics of temporarily PEGylated Onc72 prodrugs","volume":"12","author":"Mohammed","year":"2023","journal-title":"Adv. Healthc. Mater."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3390\/jof7040260","article-title":"Associations between Cryptococcus genotypes, phenotypes, and clinical parameters of human disease: a review","volume":"7","author":"Montoya","year":"2021","journal-title":"J Fungi (Basel)"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"1207","DOI":"10.1016\/j.jaad.2021.11.065","article-title":"Antimicrobials and resistance part II: antifungals, antivirals, and antiparasitics","volume":"86","author":"Muhaj","year":"2022","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1007\/s40265-022-01757-5","article-title":"Treatment of Cryptococcal meningitis: how have we got Here and where are we going?","volume":"82","author":"Ngan","year":"2022","journal-title":"Drugs"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"3519","DOI":"10.1128\/AAC.00545-06","article-title":"Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds","volume":"50","author":"Nosanchuk","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1128\/CMR.00001-12","article-title":"The Cryptococcus neoformans capsule: a sword and a shield","volume":"25","author":"O'Meara","year":"2012","journal-title":"Clin. Microbiol. Rev."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"368","DOI":"10.2174\/09298665113206660107","article-title":"In vivo activity of optimized apidaecin and oncocin peptides against a multiresistant, KPC-producing Klebsiella pneumoniae strain","volume":"21","author":"Ostorhazi","year":"2014","journal-title":"Protein Pept. Lett."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1097\/QAD.0b013e328322ffac","article-title":"Estimation of the current global burden of cryptococcal meningitis among persons living with HIV\/AIDS","volume":"23","author":"Park","year":"2009","journal-title":"AIDS"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"9824","DOI":"10.1038\/s41598-018-27813-3","article-title":"Genetic factors and genotype-environment interactions contribute to variation in melanin production in the fungal pathogen Cryptococcus neoformans","volume":"8","author":"Samarasinghe","year":"2018","journal-title":"Sci. Rep."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"15","DOI":"10.3389\/fchem.2017.00015","article-title":"In vivo efficacy and pharmacokinetics of optimized Apidaecin analogs","volume":"5","author":"Schmidt","year":"2017","journal-title":"Front. Chem."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"1003","DOI":"10.1093\/jac\/dkv454","article-title":"Pharmacokinetics and in vivo efficacy of optimized oncocin derivatives","volume":"71","author":"Schmidt","year":"2016","journal-title":"J. Antimicrob. Chemother."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"w14281","DOI":"10.4414\/smw.2016.14281","article-title":"Common invasive fungal diseases: an overview of invasive candidiasis, aspergillosis, cryptococcosis, and pneumocystis pneumonia","volume":"146","author":"Schmiedel","year":"2016","journal-title":"Swiss Med. Wkly."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"2429","DOI":"10.1093\/nar\/gkv1545","article-title":"Structure of the mammalian antimicrobial peptide Bac7(1-16) bound within the exit tunnel of a bacterial ribosome","volume":"44","author":"Seefeldt","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1038\/nsmb.3034","article-title":"The proline-rich antimicrobial peptide Onc112 inhibits translation by blocking and destabilizing the initiation complex","volume":"22","author":"Seefeldt","year":"2015","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"28","DOI":"10.3390\/molecules28010087","article-title":"Ring-modified histidine-containing cationic short peptides exhibit Anticryptococcal activity by cellular disruption","volume":"28","author":"Sharma","year":"2022","journal-title":"Molecules"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"6607","DOI":"10.1021\/acs.jmedchem.7b00481","article-title":"Discovery of a membrane-active, ring-modified histidine containing ultrashort amphiphilic peptide that exhibits potent inhibition of Cryptococcus neoformans","volume":"60","author":"Sharma","year":"2017","journal-title":"J. Med. Chem."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"649875","DOI":"10.3389\/fcell.2021.649875","article-title":"Membrane-interacting antifungal peptides","volume":"9","author":"Struyfs","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1111\/j.1574-6968.1998.tb12896.x","article-title":"Mechanism of antimicrobial action of indolicidin","volume":"160","author":"Subbalakshmi","year":"1998","journal-title":"FEMS Microbiol. 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