Eating the brain - A multidisciplinary study provides new insights into the mechanisms underlying the cytopathogenicity of Naegleria fowleri

Malych, Ronald; Folgosa, Filipe; Pilátová, Jana; Mikeš, Libor; Dohnálek, Vít; Mach, Jan; Matějková, Magdaléna; Kopecký, Vladimír; Doležal, Pavel; Sutak, Robert; Lamb, ed., Tracey J.

doi:10.1371/journal.ppat.1012995

Eating the brain - A multidisciplinary study provides new insights into the mechanisms underlying the cytopathogenicity of Naegleria fowleri

Journal Article · Mon Mar 17 00:00:00 EDT 2025 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1012995· OSTI ID:2545949

Malych, Ronald; Folgosa, Filipe; Pilátová, Jana; Mikeš, Libor; Dohnálek, Vít; Mach, Jan; Matějková, Magdaléna; Kopecký, Vladimír; Doležal, Pavel; ; Lamb, ed., Tracey J.

Naegleria fowleri , the causative agent of primary amoebic meningoencephalitis (PAM), requires increased research attention due to its high lethality and the potential for increased incidence as a result of global warming. The aim of this study was to investigate the interactions between N. fowleri and host cells in order to elucidate the mechanisms underlying the pathogenicity of this amoeba. A co-culture system comprising human fibrosarcoma cells was established to study both contact-dependent and contact-independent cytopathogenicity. Proteomic analyses of the amoebas exposed to human cell cultures or passaged through mouse brain were used to identify novel virulence factors. Our results indicate that actin dynamics, regulated by Arp2/3 and Src kinase, play a considerable role in ingestion of host cells by amoebae. We have identified three promising candidate virulence factors, namely lysozyme, cystatin and hemerythrin, which may be critical in facilitating N. fowleri evasion of host defenses, migration to the brain and induction of a lethal infection. Long-term co-culture secretome analysis revealed an increase in protease secretion, which enhances N. fowleri cytopathogenicity. Raman microspectroscopy revealed significant metabolic differences between axenic and brain-isolated amoebae, particularly in lipid storage and utilization. Taken together, our findings provide important new insights into the pathogenic mechanisms of N. fowleri and highlight potential targets for therapeutic intervention against PAM.

View Journal Article

Sponsoring Organization:: USDOE

OSTI ID:: 2545949

Alternate ID(s):: OSTI ID: 2531136

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 3 Vol. 21; ISSN 1553-7374

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

References (79)

The MPO system participates actively in the formation of an oxidative environment produced by neutrophils and activates the antioxidant mechanism of Naegleria fowleri Flores-Huerta, Nadia; Pacheco-Yépez, Judith; Sánchez-Monroy, Virginia Journal of Leukocyte Biology, Vol. 108, Issue 3 https://doi.org/10.1002/JLB.4MA0520-565RR	journal	June 2020
Influence of ligand binding on structure and thermostability of human α₁-acid glycoprotein Kopecký, Vladimír; Ettrich, Rüdiger; Pazderka, Tomáš Journal of Molecular Recognition, Vol. 29, Issue 2 https://doi.org/10.1002/jmr.2496	journal	September 2015
Raman spectroscopy of proteins: a review: Raman spectroscopy of proteins Rygula, A.; Majzner, K.; Marzec, K. M. Journal of Raman Spectroscopy, Vol. 44, Issue 8 https://doi.org/10.1002/jrs.4335	journal	July 2013
Raman spectroscopy of lipids: a review: Raman spectroscopy of lipids Czamara, K.; Majzner, K.; Pacia, M. Z. Journal of Raman Spectroscopy, Vol. 46, Issue 1 https://doi.org/10.1002/jrs.4607	journal	December 2014
UCSF ChimeraX: Tools for structure building and analysis Meng, Elaine C.; Goddard, Thomas D.; Pettersen, Eric F. Protein Science, Vol. 32, Issue 11 https://doi.org/10.1002/pro.4792	journal	October 2023
Naegleria fowleri: Characterization of a Secreted Histolytic Cysteine Protease Aldape, K.; Huizinga, H.; Bouvier, J. Experimental Parasitology, Vol. 78, Issue 2 https://doi.org/10.1006/expr.1994.1023	journal	March 1994
Differences between Naegleria fowleri and Naegleria gruberi in expression of mannose and fucose glycoconjugates Cervantes-Sandoval, Isaac; Jesús Serrano-Luna, José; Pacheco-Yépez, Judith Parasitology Research, Vol. 106, Issue 3 https://doi.org/10.1007/s00436-010-1727-z	journal	January 2010
The Nf-actin gene is an important factor for food-cup formation and cytotoxicity of pathogenic Naegleria fowleri Sohn, Hae-Jin; Kim, Jong-Hyun; Shin, Myeong-Heon Parasitology Research, Vol. 106, Issue 4 https://doi.org/10.1007/s00436-010-1760-y	journal	February 2010
Naegleria fowleri glycoconjugates with residues of α-d-mannose are involved in adherence of trophozoites to mouse nasal mucosa Carrasco-Yepez, Maricela; Campos-Rodriguez, Rafael; Godinez-Victoria, Marycarmen Parasitology Research, Vol. 112, Issue 10 https://doi.org/10.1007/s00436-013-3549-2	journal	August 2013
Role of cathepsin B of Naegleria fowleri during primary amebic meningoencephalitis Rodríguez-Mera, Itzel Berenice; Carrasco-Yépez, María Maricela; Vásquez-Moctezuma, Ismael Parasitology Research, Vol. 121, Issue 11 https://doi.org/10.1007/s00436-022-07660-y	journal	September 2022
Structure/function correlations over binuclear non-heme iron active sites Solomon, Edward I.; Park, Kiyoung JBIC Journal of Biological Inorganic Chemistry, Vol. 21, Issue 5-6 https://doi.org/10.1007/s00775-016-1372-9	journal	July 2016
Activated macrophages demonstrate direct cytotoxicity, antibody-dependent cellular cytotoxicity, and enhanced binding of Naegleria fowleri amoebae Cleary, S. F.; Marciano-Cabral, F. Cellular Immunology, Vol. 98, Issue 1 https://doi.org/10.1016/0008-8749(86)90273-X	journal	March 1986
Structure of myohemerythrin in the azidomet state at resolution Sheriff, Steven; Hendrickson, Wayne A.; Smith, Janet L. Journal of Molecular Biology, Vol. 197, Issue 2 https://doi.org/10.1016/0022-2836(87)90124-0	journal	September 1987
Structures of deoxy and oxy hemerythrin at 2.0 Å resolution Holmes, Margaret A.; Le Trong, Isolde; Turley, Stewart Journal of Molecular Biology, Vol. 218, Issue 3 https://doi.org/10.1016/0022-2836(91)90703-9	journal	April 1991
Principles of structure, bonding, and reactivity for metal nitrosyl complexes Enemark, J. H.; Feltham, R. D. Coordination Chemistry Reviews, Vol. 13, Issue 4 https://doi.org/10.1016/S0010-8545(00)80259-3	journal	September 1974
Purification and characterization of a potent bactericidal and membrane active protein from the granules of human polymorphonuclear leukocytes. Weiss, J.; Elsbach, P.; Olsson, I. Journal of Biological Chemistry, Vol. 253, Issue 8 https://doi.org/10.1016/S0021-9258(17)40872-6	journal	April 1978
Quantitative Interpretation of Multifrequency Multimode EPR Spectra of Metal Containing Proteins, Enzymes, and Biomimetic Complexes Petasis, Doros T.; Hendrich, Michael P. Methods in Enzymology https://doi.org/10.1016/bs.mie.2015.06.025	book	January 2015
Structural and dynamic changes of the serum response element and the core domain of serum response factor induced by their association Štěpánek, Josef; Kopecký, Vladimír; Mezzetti, Alberto Biochemical and Biophysical Research Communications, Vol. 391, Issue 1 https://doi.org/10.1016/j.bbrc.2009.11.032	journal	January 2010
Lipids Are the Preferred Substrate of the Protist Naegleria gruberi, Relative of a Human Brain Pathogen Bexkens, Michiel L.; Zimorski, Verena; Sarink, Maarten J. Cell Reports, Vol. 25, Issue 3 https://doi.org/10.1016/j.celrep.2018.09.055	journal	October 2018
Iron economy in Naegleria gruberi reflects its metabolic flexibility Mach, Jan; Bíla, Jarmila; Ženíšková, Kateřina International Journal for Parasitology, Vol. 48, Issue 9-10 https://doi.org/10.1016/j.ijpara.2018.03.005	journal	August 2018
The hemerythrin-like diiron protein from Mycobacterium kansasii is a nitric oxide peroxidase Ma, Zhongxin; Holland, Ashley A.; Szlamkowicz, Ilana Journal of Biological Chemistry, Vol. 298, Issue 3 https://doi.org/10.1016/j.jbc.2022.101696	journal	March 2022
The bacteriohemerythrin from Methylococcus capsulatus (Bath): Crystal structures reveal that Leu114 regulates a water tunnel Chen, Kelvin H. -C.; Chuankhayan, Phimonphan; Wu, Hsin-Hui Journal of Inorganic Biochemistry, Vol. 150 https://doi.org/10.1016/j.jinorgbio.2015.04.001	journal	September 2015
A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core Zimmermann, Lukas; Stephens, Andrew; Nam, Seung-Zin Journal of Molecular Biology, Vol. 430, Issue 15 https://doi.org/10.1016/j.jmb.2017.12.007	journal	July 2018
Gene silencing of nfa1 affects the in vitro cytotoxicity of Naegleria fowleri in murine macrophages Jung, Suk-Yul; Kim, Jong-Hyun; Song, Kyoung-Ju Molecular and Biochemical Parasitology, Vol. 165, Issue 1 https://doi.org/10.1016/j.molbiopara.2009.01.007	journal	May 2009
Cathepsin K generates enkephalin from β-endorphin: A new mechanism with possible relevance for schizophrenia Lendeckel, Uwe; Kähne, Thilo; Ten Have, Sara Neurochemistry International, Vol. 54, Issue 7 https://doi.org/10.1016/j.neuint.2009.01.011	journal	June 2009
Analysis of Bacteriophage–Host Interaction by Raman Tweezers Pilát, Zdeněk; Jonáš, Alexandr; Pilátová, Jana Analytical Chemistry, Vol. 92, Issue 18 https://doi.org/10.1021/acs.analchem.0c01963	journal	August 2020
Raman Spectroscopy: A Tool for Molecular Fingerprinting of Brain Cancer Murugappan, Sivasubramanian; Tofail, Syed A. M.; Thorat, Nanasaheb D. ACS Omega, Vol. 8, Issue 31 https://doi.org/10.1021/acsomega.3c01848	journal	July 2023
Reversible Dioxygen Binding to Hemerythrin. 1. Electronic Structures of Deoxy- and Oxyhemerythrin Brunold, Thomas C.; Solomon, Edward I. Journal of the American Chemical Society, Vol. 121, Issue 36 https://doi.org/10.1021/ja990334s	journal	August 1999
Spectroscopic Characterization of a Diferric Mycobacterial Hemerythrin-Like Protein with Unprecedented Reactivity toward Nitric Oxide Albert, Therese; Moënne-Loccoz, Pierre Journal of the American Chemical Society, Vol. 144, Issue 38 https://doi.org/10.1021/jacs.2c07113	journal	September 2022
Predominant Release of Lysosomal Enzymes by Newborn Rat Microglia After LPS Treatment Revealed by Proteomic Studies Liu, Jun; Hong, Zhen; Ding, Jianqing Journal of Proteome Research, Vol. 7, Issue 5 https://doi.org/10.1021/pr7007779	journal	April 2008
Cathepsin L Acutely Alters Microvessel Integrity within the Neurovascular Unit during Focal Cerebral Ischemia Gu, Yu-Huan; Kanazawa, Masato; Hung, Stephanie Y. Journal of Cerebral Blood Flow & Metabolism, Vol. 35, Issue 11 https://doi.org/10.1038/jcbfm.2015.170	journal	July 2015
Trogocytosis by Entamoeba histolytica contributes to cell killing and tissue invasion Ralston, Katherine S.; Solga, Michael D.; Mackey-Lawrence, Nicole M. Nature, Vol. 508, Issue 7497 https://doi.org/10.1038/nature13242	journal	April 2014
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
The Perseus computational platform for comprehensive analysis of (prote)omics data Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel Nature Methods, Vol. 13, Issue 9 https://doi.org/10.1038/nmeth.3901	journal	June 2016
Revisiting biocrystallization: purine crystalline inclusions are widespread in eukaryotes Pilátová, Jana; Pánek, Tomáš; Oborník, Miroslav The ISME Journal, Vol. 16, Issue 9 https://doi.org/10.1038/s41396-022-01264-1	journal	June 2022
AGC family kinase 1 participates in trogocytosis but not in phagocytosis in Entamoeba histolytica No authors listed Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00199-y	journal	July 2017
Accurate structure prediction of biomolecular interactions with AlphaFold 3 Abramson, Josh; Adler, Jonas; Dunger, Jack Nature, Vol. 630, Issue 8016 https://doi.org/10.1038/s41586-024-07487-w	journal	May 2024
VolcaNoseR is a web app for creating, exploring, labeling and sharing volcano plots Goedhart, Joachim; Luijsterburg, Martijn S. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-76603-3	journal	November 2020
Cathepsin K: a cysteine protease with unique kinin-degrading properties Godat, Emmanuel; Lecaille, Fabien; Desmazes, Claire Biochemical Journal, Vol. 383, Issue 3 https://doi.org/10.1042/BJ20040864	journal	October 2004
Monitoring the RNA distribution in human embryonic stem cells using Raman micro-spectroscopy and fluorescence imaging Falamas, A.; Kalra, S.; Chis, V. AIP Conference Proceedings https://doi.org/10.1063/1.4833693	conference	January 2013
Guanine, a high-capacity and rapid-turnover nitrogen reserve in microalgal cells Mojzeš, Peter; Gao, Lu; Ismagulova, Tatiana Proceedings of the National Academy of Sciences, Vol. 117, Issue 51 https://doi.org/10.1073/pnas.2005460117	journal	December 2020
Pore-forming Polypeptides of the Pathogenic Protozoon Naegleria fowleri Herbst, Rosa; Ott, Claudia; Jacobs, Thomas Journal of Biological Chemistry, Vol. 277, Issue 25 https://doi.org/10.1074/jbc.M201475200	journal	June 2002
Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ Cox, Jürgen; Hein, Marco Y.; Luber, Christian A. Molecular & Cellular Proteomics, Vol. 13, Issue 9 https://doi.org/10.1074/mcp.M113.031591	journal	June 2014
Raman Spectroscopy of Biological Tissues Movasaghi, Zanyar; Rehman, Shazza; Rehman, Ihtesham U. Applied Spectroscopy Reviews, Vol. 42, Issue 5 https://doi.org/10.1080/05704920701551530	journal	September 2007
Conserved actin machinery drives microtubule-independent motility and phagocytosis in Naegleria Velle, Katrina B.; Fritz-Laylin, Lillian K. Journal of Cell Biology, Vol. 219, Issue 11 https://doi.org/10.1083/jcb.202007158	journal	September 2020
The Tyrosine Kinase Activity of c-Src Regulates Actin Dynamics and Organization of Podosomes in Osteoclasts Destaing, Olivier; Sanjay, Archana; Itzstein, Cecile Molecular Biology of the Cell, Vol. 19, Issue 1 https://doi.org/10.1091/mbc.e07-03-0227	journal	January 2008
The response of Naegleria gruberi to oxidative stress Malych, Ronald; Füssy, Zoltán; Ženíšková, Kateřina Metallomics, Vol. 14, Issue 3 https://doi.org/10.1093/mtomcs/mfac009	journal	February 2022
The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences Perez-Riverol, Yasset; Bai, Jingwen; Bandla, Chakradhar Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab1038	journal	November 2021
Polymorphism of human telomeric quadruplex structure controlled by DNA concentration: a Raman study Palacký, Jan; Vorlíčková, Michaela; Kejnovská, Iva Nucleic Acids Research, Vol. 41, Issue 2 https://doi.org/10.1093/nar/gks1135	journal	November 2012
Expression of matrix metalloproteinases in Naegleria fowleri and their role in invasion of the central nervous system Lam, Charlton; Jamerson, Melissa; Cabral, Guy Microbiology, Vol. 163, Issue 10 https://doi.org/10.1099/mic.0.000537	journal	October 2017
Pathogenic Naegleria fowleri and non-pathogenic Naegleria lovaniensis exhibit differential adhesion to, and invasion of, extracellular matrix proteins Jamerson, Melissa; da Rocha-Azevedo, Bruno; Cabral, Guy A. Microbiology, Vol. 158, Issue 3 https://doi.org/10.1099/mic.0.055020-0	journal	March 2012
Disruption of MDCK cell tight junctions by the free-living amoeba Naegleria fowleri Shibayama, Mineko; Martínez-Castillo, Moisés; Silva-Olivares, Angélica Microbiology, Vol. 159, Issue Pt_2 https://doi.org/10.1099/mic.0.063255-0	journal	February 2013
The flavodiiron protein from Syntrophomonas wolfei has five domains and acts both as an NADH:O₂ or an NADH:H₂O₂ oxidoreductase Martins, Maria C.; Alves, Catarina M.; Teixeira, Miguel The FEBS Journal, Vol. 291, Issue 6 https://doi.org/10.1111/febs.17040	journal	January 2024
The Interaction of Naegleria fowleri Amoebae with Murine Macrophage Cell Lines Fischer‐Stenger, Krista; Cabral, Guy A.; Marciano‐Cabral, Francine The Journal of Protozoology, Vol. 37, Issue 3 https://doi.org/10.1111/j.1550-7408.1990.tb01122.x	journal	May 1990
Isolation of a Unique Membrane Protein from Naegleria fowleri RÉVeiller, Fabienne L.; Suh, Sang‐Jin; Sullivan, Karen Journal of Eukaryotic Microbiology, Vol. 48, Issue 6 https://doi.org/10.1111/j.1550-7408.2001.tb00208.x	journal	November 2001
A Biochemical Comparison of Proteases from Pathogenic Naegleria fowleri and Non‐Pathogenic Naegleria gruberi Serrano‐Luna, JesÚS; Cervantes‐Sandoval, Isaac; Tsutsumi, Victor Journal of Eukaryotic Microbiology, Vol. 54, Issue 5 https://doi.org/10.1111/j.1550-7408.2007.00280.x	journal	September 2007
Identification of Peptidases in Highly Pathogenic vs. Weakly Pathogenic Naegleria fowleri Amebae Vyas, Ishan K.; Jamerson, Melissa; Cabral, Guy A. Journal of Eukaryotic Microbiology, Vol. 62, Issue 1 https://doi.org/10.1111/jeu.12152	journal	August 2014
An In Vitro Model of the Blood–Brain Barrier: Naegleria fowleri Affects the Tight Junction Proteins and Activates the Microvascular Endothelial Cells Coronado‐Velázquez, Daniel; Betanzos, Abigail; Serrano‐Luna, Jesús Journal of Eukaryotic Microbiology, Vol. 65, Issue 6 https://doi.org/10.1111/jeu.12522	journal	April 2018
The Arctic Cylindrocystis (Zygnematophyceae, Streptophyta) Green Algae are Genetically and Morphologically Diverse and Exhibit Effective Accumulation of Polyphosphate Barcytė, Dovilė; Pilátová, Jana; Mojzeš, Peter Journal of Phycology, Vol. 56, Issue 1 https://doi.org/10.1111/jpy.12931	journal	November 2019
Mouse neutrophils release extracellular traps in response to Naegleria fowleri Carrasco‐Yepez, Maria Maricela; Contis‐Montes de Oca, Arturo; Campos‐Rodriguez, Rafael Parasite Immunology, Vol. 41, Issue 2 https://doi.org/10.1111/pim.12610	journal	January 2019
The arginine-dependent cytolytic mechanism plays a role in destruction of Naegleria fowleri amoebae by activated macrophages Fischer-Stenger, K.; Marciano-Cabral, F. Infection and Immunity, Vol. 60, Issue 12 https://doi.org/10.1128/iai.60.12.5126-5131.1992	journal	December 1992
Comparative Genomic and Transcriptomic Analysis of Naegleria fowleri Clinical and Environmental Isolates Joseph, Sandeep J.; Park, Subin; Kelley, Alyssa mSphere, Vol. 6, Issue 4 https://doi.org/10.1128/mSphere.00637-21	journal	August 2021
Massive Accumulation of Strontium and Barium in Diplonemid Protists Pilátová, Jana; Tashyreva, Daria; Týč, Jiří mBio, Vol. 14, Issue 1 https://doi.org/10.1128/mbio.03279-22	journal	February 2023
Raman Spectroscopy of Blood and Blood Components Atkins, Chad G.; Buckley, Kevin; Blades, Michael W. Applied Spectroscopy, Vol. 71, Issue 5 https://doi.org/10.1177/0003702816686593	journal	April 2017
Capture of plasma membrane fragments from target cells by trogocytosis requires signaling in T cells but not in B cells Aucher, Anne; Magdeleine, Eddy; Joly, Etienne Blood, Vol. 111, Issue 12 https://doi.org/10.1182/blood-2008-01-134155	journal	June 2008
Genomics and transcriptomics yields a system-level view of the biology of the pathogen Naegleria fowleri Herman, Emily K.; Greninger, Alex; van der Giezen, Mark BMC Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12915-021-01078-1	journal	July 2021
Fowlerstefin, a cysteine protease inhibitor of Naegleria fowleri, induces inflammatory responses in BV-2 microglial cells in vitro Thái, Thị Lam; Kang, Jung-Mi; Lê, Hương Giang Parasites & Vectors, Vol. 13, Issue 1 https://doi.org/10.1186/s13071-020-3909-6	journal	January 2020
Adaptive iron utilization compensates for the lack of an inducible uptake system in Naegleria fowleri and represents a potential target for therapeutic intervention Arbon, Dominik; Ženíšková, Kateřina; Mach, Jan https://doi.org/10.1371/journal.pntd.0007759	preprint	June 2020
Src Kinases Regulate De Novo Actin Polymerization during Exocytosis in Neuroendocrine Chromaffin Cells Olivares, María José; González-Jamett, Arlek M.; Guerra, María José PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0099001	journal	June 2014
EhNPC1 and EhNPC2 Proteins Participate in Trafficking of Exogenous Cholesterol in Entamoeba histolytica Trophozoites: Relevance for Phagocytosis Bolaños, Jeni; Betanzos, Abigail; Javier-Reyna, Rosario PLOS Pathogens, Vol. 12, Issue 12 https://doi.org/10.1371/journal.ppat.1006089	journal	December 2016
First evidence of free-living Naegleria species in recreational lakes of Alberta, Canada Dey, Rafik; Dlusskaya, Elena; Oloroso, Mariem Journal of Water and Health, Vol. 21, Issue 3 https://doi.org/10.2166/wh.2023.325	journal	February 2023
Nf-GH, a Glycosidase Secreted by Naegleria Fowleri , Causes Mucin Degradation: An in Vitro and in Vivo Study Martínez-Castillo, Moisés; Cárdenas-Guerra, Rosa Elena; Arroyo, Rossana Future Microbiology, Vol. 12, Issue 9 https://doi.org/10.2217/fmb-2016-0230	journal	June 2017
Enhancement of Virulence of Naegleria fowleri by Growth in Vero-Cell Cultures John, David T.; John, Rebecca A. The Journal of Parasitology, Vol. 80, Issue 1 https://doi.org/10.2307/3283359	journal	February 1994
Geographic Range of Recreational Water-Associated Primary Amebic Meningoencephalitis, United States, 1978–2018 Gharpure, Radhika; Gleason, Michelle; Salah, Zainab Emerging Infectious Diseases, Vol. 27, Issue 1 https://doi.org/10.3201/eid2701.202119	journal	January 2021
Bactericidal/Permeability-Increasing Protein Preeminently Mediates Clearance of Pseudomonas aeruginosa In Vivo via CD18-Dependent Phagocytosis Theprungsirikul, Jomkuan; Skopelja-Gardner, Sladjana; Burns, Ashley S. Frontiers in Immunology, Vol. 12 https://doi.org/10.3389/fimmu.2021.659523	journal	April 2021
Characterization of the extracellular vesicles, ultrastructural morphology, and intercellular interactions of multiple clinical isolates of the brain-eating amoeba, Naegleria fowleri Russell, A. Cassiopeia; Bush, Peter; Grigorean, Gabriela Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1264348	journal	September 2023
Naegleria fowleri Cathepsin B Induces a Pro-Inflammatory Immune Response in BV-2 Microglial Cells via NF-κB and AP-1 Dependent-MAPK Signaling Pathway Lê, Hương Giang; Kang, Jung-Mi; Võ, Tuấn Cường International Journal of Molecular Sciences, Vol. 23, Issue 15 https://doi.org/10.3390/ijms23158388	journal	July 2022
A Novel Cysteine Protease Inhibitor of Naegleria fowleri That Is Specifically Expressed during Encystation and at Mature Cysts Lê, Hương Giang; Ham, A-Jeong; Kang, Jung-Mi Pathogens, Vol. 10, Issue 4 https://doi.org/10.3390/pathogens10040388	journal	March 2021
Extracellular Vesicles from Naegleria fowleri Induce IL-8 Response in THP-1 Macrophage Lertjuthaporn, Sakaorat; Somkird, Jinjuta; Lekmanee, Kittima Pathogens, Vol. 11, Issue 6 https://doi.org/10.3390/pathogens11060632	journal	May 2022

Similar Records

Occurrence and pathogenicity of Naegleria fowleri in artificially heated waters

Journal Article · Mon Feb 28 23:00:00 EST 1983 · Appl. Environ. Microbiol.; (United States) · OSTI ID:5683452

Effect of thermal additions on the density and distribution of thermophilic amoebae and pathogenic Naegleria fowleri in a newly created cooling lake

Journal Article · Tue Feb 28 23:00:00 EST 1989 · Applied and Environmental Microbiology; (USA) · OSTI ID:5099015

Eating the brain - A multidisciplinary study provides new insights into the mechanisms underlying the cytopathogenicity of Naegleria fowleri

Citation Formats

References (79)

Similar Records

Related Subjects