Autophagic-related cell death of Trypanosoma brucei induced by bacteriocin AS-48

Marta Martínez-García1, Jean-Mathieu Bart2,3, Jenny Campos-Salinas1, Eva Valdivia4, Manuel Martínez-Bueno4, Elena González-Rey1, Miguel Navarro1, Mercedes Maqueda4, Rubén Cebrián4, José M. Pérez-Victoria1
1Instituto de Parasitología y Biomedicina “López-Neyra”, CSIC (IPBLN-CSIC), PTS Granada, Granada, Spain
2Centro Nacional de Medicina Tropical. Instituto de Salud Carlos III, Madrid, Spain
3UMR INTERTRYP, Institut de Recherche pour le Développement, Montpellier, France
4Departamento de Microbiología, Facultad de Ciencias, Universidad de Granada, Spain

Tài liệu tham khảo

Abengózar, 2017, Enterocin AS-48 as evidence for the use of bacteriocins as new leishmanicidal agents, Antimicrob. Agents Chemother., 61, 10.1128/AAC.02288-16 Allen, 2003, Clathrin-mediated endocytosis is essential in Trypanosoma brucei, EMBO J., 22, 4991, 10.1093/emboj/cdg481 Alsford, 2012, High-throughput decoding of antitrypanosomal drug efficacy and resistance, Nature, 482, 232, 10.1038/nature10771 Alsford, 2013, Receptor-mediated endocytosis for drug delivery in African trypanosomes: fulfilling Paul Ehrlich's vision of chemotherapy, Trends Parasitol., 29, 207, 10.1016/j.pt.2013.03.004 Ananou, 2008, Optimization of enterocin AS-48 production on a whey-based substrate, Int. Dairy J., 18, 923, 10.1016/j.idairyj.2008.02.001 Bakunova, 2009, Structure-activity study of pentamidine analogues as antiprotozoal agents, J. Med. Chem., 52, 2016, 10.1021/jm801547t Barrett, 2007, Human African trypanosomiasis: pharmacological re-engagement with a neglected disease, Br. J. Pharmacol., 152, 1155, 10.1038/sj.bjp.0707354 Bart, 2015, Localization of serum resistance-associated protein in Trypanosoma brucei rhodesiense and transgenic Trypanosoma brucei brucei, Cell Microbiol., 17, 1523, 10.1111/cmi.12454 Belmonte-Reche, 2016, Tyrosol and hydroxytyrosol derivatives as antitrypanosomal and antileishmanial agents, Eur. J. Med. Chem., 119, 132, 10.1016/j.ejmech.2016.04.047 Cabello-Donayre, 2016, Trypanosomatid parasites rescue heme from endocytosed hemoglobin through lysosomal HRG transporters, Mol. Microbiol., 101, 895, 10.1111/mmi.13430 Carvalho, 2015, The oral antimalarial drug Tafenoquine shows activity against Trypanosoma brucei, Antimicrob. Agents Chemother., 59, 6151, 10.1128/AAC.00879-15 Castillo-Acosta, 2013, Carbohydrate-binding agents act as potent trypanocidals that elicit modifications in VSG glycosylation and reduced virulence in Trypanosoma brucei, Mol. Microbiol., 90, 665, 10.1111/mmi.12359 Cebrián, 2012, Characterization of functional, safety, and probiotic properties of Enterococcus faecalis UGRA10, a new AS-48-producer strain, Food Microbiol., 30, 59, 10.1016/j.fm.2011.12.002 Cross, 1984, Release and purification of Trypanosoma brucei variant surface glycoprotein, J. Cell. Biochem., 24, 79, 10.1002/jcb.240240107 Cullen, 2017, A brief review of drug discovery research for Human African Trypanosomiasis, Curr. Med. Chem., 10.2174/0929867324666170120160034 David Barry, 2001, Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite, Adv. Parasitol., 49, 1, 10.1016/S0065-308X(01)49037-3 De Rycker, 2013, Comparison of a high-throughput high-content intracellular Leishmania donovani assay with an axenic amastigote assay, Antimicrob. Agents Chemother., 57, 2913, 10.1128/AAC.02398-12 Delgado, 2008, Neuropeptides kill African trypanosomes by targeting intracellular compartments and inducing autophagic-like cell death, Cell Death Differ., 16, 406, 10.1038/cdd.2008.161 Dezfuli, 2006, Effects of experimental terbuthylazine exposure on the cells of Dicentrarchus labrax (L.), Chemosphere, 64, 1684, 10.1016/j.chemosphere.2006.01.023 Engstler, 2004, Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei, J. Cell Sci., 117, 1105, 10.1242/jcs.00938 Field, 2009, The trypanosome flagellar pocket, Nat. Rev. Microbiol., 7, 775, 10.1038/nrmicro2221 Gonzalez-Rey, 2006, VIP: an agent with license to kill infective parasites, Ann. N. Y. Acad. Sci., 1070, 303, 10.1196/annals.1317.032 Gonzalez-Rey, 2007, Therapeutic effect of urocortin on collagen-induced arthritis by down-regulation of inflammatory and Th1 responses and induction of regulatory T cells, Arthritis Rheum., 56, 531, 10.1002/art.22394 Grande Burgos, 2014, The cyclic antibacterial peptide enterocin AS-48: isolation, mode of action, and possible food applications, Int. J. Mol. Sci., 15, 22706, 10.3390/ijms151222706 Greene, 2016, Trypanosome lytic Factor-1 initiates oxidation-stimulated osmotic lysis of Trypanosoma brucei brucei, J. Biol. Chem., 291, 3063, 10.1074/jbc.M115.680371 Haines, 2003, Cationic antimicrobial peptide killing of african Trypanosomes and Sodalis glossinidius, a bacterial symbiont of the insect vector of sleeping sickness, Vector Borne Zoonotic Dis., 3, 175, 10.1089/153036603322662165 Harrington, 2011, Antimicrobial peptide killing of african Trypanosomes, Parasite Immunol., 33, 461, 10.1111/j.1365-3024.2011.01294.x Hu, 2006, Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans, Mol. Microbiol., 60, 1194, 10.1111/j.1365-2958.2006.05180.x Hu, 2005, An antimicrobial peptide with trypanocidal activity characterized from Glossina morsitans morsitans, Insect Biochem. Mol. Biol., 35, 105, 10.1016/j.ibmb.2004.10.007 Ishiyama, 2009, In vitro and in vivo antitrypanosomal activities of three peptide antibiotics: leucinostatin A and B, alamethicin I and tsushimycin, J. Antibiot. (Tokyo), 62, 303, 10.1038/ja.2009.32 Jenssen, 2006, Peptide antimicrobial agents, Clin. Microbiol. Rev., 19, 491, 10.1128/CMR.00056-05 Lanz, 1997, Use of FITC as a fluorescent probe for intracellular pH measurement, J. Fluoresc., 7, 317, 10.1023/A:1022586127784 Li, 2012, A role of autophagy in Trypanosoma brucei cell death, Cell Microbiol., 14, 1242, 10.1111/j.1462-5822.2012.01795.x Luque-Ortega, 2012, Defeating Leishmania resistance to miltefosine (hexadecylphosphocholine) by peptide-mediated drug smuggling: a proof of mechanism for trypanosomatid chemotherapy, J. Control. Release Off. J. Control. Release Soc., 161, 835, 10.1016/j.jconrel.2012.05.023 Maqueda, 2004, Peptide AS-48: prototype of a new class of cyclic bacteriocins, Curr. Protein Pept. Sci., 5, 399, 10.2174/1389203043379567 Maqueda, 1993, Neutralizing antibodies against the peptide antibiotic AS-48: immunocytological studies, Antimicrob. Agents Chemother., 37, 148, 10.1128/AAC.37.1.148 McGwire, 2003, Killing of african Trypanosomes by antimicrobial peptides, J. Infect. Dis., 188, 146, 10.1086/375747 Mendoza, 1999, Antilisterial activity of peptide AS-48 and study of changes induced in the cell envelope properties of an AS-48-adapted strain of Listeria monocytogenes, Appl. Environ. Microbiol., 65, 618, 10.1128/AEM.65.2.618-625.1999 Montalban-Lopez, 2011, Are bacteriocins Underexploited? NOVEL applications for OLD antimicrobials, Curr. Pharm. Biotechnol, 12, 1205, 10.2174/138920111796117364 Morgan, 2001, Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei, J. Cell Sci., 114, 2605, 10.1242/jcs.114.14.2605 Natesan, 2007, Activation of endocytosis as an adaptation to the mammalian host by Trypanosomes, Eukaryot. Cell, 6, 2029, 10.1128/EC.00213-07 Navarro, 1996, DNA rearrangements associated with multiple consecutive directed antigenic switches in Trypanosoma brucei, Mol. Cell Biol., 16, 3615, 10.1128/MCB.16.7.3615 Pal, 2002, Differential endocytic functions of Trypanosoma brucei Rab5 isoforms reveal a glycosylphosphatidylinositol-specific endosomal pathway, J. Biol. Chem., 277, 9529, 10.1074/jbc.M110055200 Pérez-Victoria, 2006, Combination of suboptimal doses of inhibitors Targeting different domains of LtrMDR1 efficiently overcomes resistance of Leishmania spp. to miltefosine by inhibiting drug efflux, Antimicrob. Agents Chemother., 50, 3102, 10.1128/AAC.00423-06 Pham, 2017, Novel 1,2-dihydroquinazolin-2-ones: design, synthesis, and biological evaluation against Trypanosoma brucei, Bioorg. Med. Chem. Lett, 27, 3629, 10.1016/j.bmcl.2017.07.032 Proto, 2014, Tracking autophagy during proliferation and differentiation of Trypanosoma brucei, Microb. Cell Graz Austria, 1, 9, 10.15698/mic2014.01.120 Ramu, 2015, Bacteriocins and Their applications in food preservation, Crit. Rev. Food Sci. Nutr., 0 Räz, 1997, The Alamar Blue assay to determine drug sensitivity of African trypanosomes (T.b. rhodesiense and T.b. gambiense) in vitro, Acta Trop., 68, 139, 10.1016/S0001-706X(97)00079-X Reinhardt, 2008 Riley, 2002, Bacteriocins: evolution, ecology, and application, Annu. Rev. Microbiol., 56, 117, 10.1146/annurev.micro.56.012302.161024 Rycker, 2012, A static-cidal assay for Trypanosoma brucei to aid hit prioritisation for progression into drug discovery programmes, PLoS Neglected Trop. Dis., 6, e1932, 10.1371/journal.pntd.0001932 Sánchez-Barrena, 2003, Structure of bacteriocin AS-48: from soluble state to membrane bound state, J. Mol. Biol., 334, 541, 10.1016/j.jmb.2003.09.060 Sánchez-Fernández, 2015, Antileishmanial activity of sp2-iminosugar derivatives, RSC Adv., 5, 21812, 10.1039/C5RA02627J Sánchez-Hidalgo, 2011, AS-48 bacteriocin: close to perfection, Cell. Mol. Life Sci., 68, 2845, 10.1007/s00018-011-0724-4 Souto-Padrón, 1990, The surface charge of trypanosomatids of the genus Trypanosoma, Mem. Inst. Oswaldo Cruz, 85, 215, 10.1590/S0074-02761990000200013 Uzcátegui, 2007, Antiproliferative effect of dihydroxyacetone on Trypanosoma brucei bloodstream forms: cell cycle progression, subcellular alterations, and cell death, Antimicrob. Agents Chemother., 51, 3960, 10.1128/AAC.00423-07 Vanhollebeke, 2008, A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans, Science, 320, 677, 10.1126/science.1156296 Vreysen, 2013, Tsetse flies: Their biology and control using area-wide integrated pest management approaches, J. Invertebr. Pathol., 112, S15, 10.1016/j.jip.2012.07.026 Welburn, 2009, Controlling sleeping sickness – a review, Parasitology, 136, 1943, 10.1017/S0031182009006416 Wirtz, 1999, A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei, Mol. Biochem. Parasitol., 99, 89, 10.1016/S0166-6851(99)00002-X Yeaman, 2001, Sec6/8 complexes on trans-Golgi network and plasma membrane regulate late stages of exocytosis in mammalian cells, J. Cell Biol., 155, 593, 10.1083/jcb.200107088