-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Step-Wise Loss of Bacterial Flagellar Torsion Confers Progressive Phagocytic Evasion
Phagocytosis of bacteria by innate immune cells is a primary method of bacterial clearance during infection. However, the mechanisms by which the host cell recognizes bacteria and consequentially initiates phagocytosis are largely unclear. Previous studies of the bacterium Pseudomonas aeruginosa have indicated that bacterial flagella and flagellar motility play an important role in colonization of the host and, importantly, that loss of flagellar motility enables phagocytic evasion. Here we use molecular, cellular, and genetic methods to provide the first formal evidence that phagocytic cells recognize bacterial motility rather than flagella and initiate phagocytosis in response to this motility. We demonstrate that deletion of genes coding for the flagellar stator complex, which results in non-swimming bacteria that retain an initial flagellar structure, confers resistance to phagocytic binding and ingestion in several species of the gamma proteobacterial group of Gram-negative bacteria, indicative of a shared strategy for phagocytic evasion. Furthermore, we show for the first time that susceptibility to phagocytosis in swimming bacteria is proportional to mot gene function and, consequently, flagellar rotation since complementary genetically - and biochemically-modulated incremental decreases in flagellar motility result in corresponding and proportional phagocytic evasion. These findings identify that phagocytic cells respond to flagellar movement, which represents a novel mechanism for non-opsonized phagocytic recognition of pathogenic bacteria.
Vyšlo v časopise: Step-Wise Loss of Bacterial Flagellar Torsion Confers Progressive Phagocytic Evasion. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002253
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002253Souhrn
Phagocytosis of bacteria by innate immune cells is a primary method of bacterial clearance during infection. However, the mechanisms by which the host cell recognizes bacteria and consequentially initiates phagocytosis are largely unclear. Previous studies of the bacterium Pseudomonas aeruginosa have indicated that bacterial flagella and flagellar motility play an important role in colonization of the host and, importantly, that loss of flagellar motility enables phagocytic evasion. Here we use molecular, cellular, and genetic methods to provide the first formal evidence that phagocytic cells recognize bacterial motility rather than flagella and initiate phagocytosis in response to this motility. We demonstrate that deletion of genes coding for the flagellar stator complex, which results in non-swimming bacteria that retain an initial flagellar structure, confers resistance to phagocytic binding and ingestion in several species of the gamma proteobacterial group of Gram-negative bacteria, indicative of a shared strategy for phagocytic evasion. Furthermore, we show for the first time that susceptibility to phagocytosis in swimming bacteria is proportional to mot gene function and, consequently, flagellar rotation since complementary genetically - and biochemically-modulated incremental decreases in flagellar motility result in corresponding and proportional phagocytic evasion. These findings identify that phagocytic cells respond to flagellar movement, which represents a novel mechanism for non-opsonized phagocytic recognition of pathogenic bacteria.
Zdroje
1. AkiraSUematsuSTakeuchiO 2006 Pathogen recognition and innate immunity. Cell 124 783 801
2. LyczakJBCannonCLPierGB 2000 Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2 1051 1060
3. LyczakJBCannonCLPierGB 2002 Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15 194 222
4. AmielELovewellRRO'TooleGAHoganDABerwinB 2010 Pseudomonas aeruginosa evasion of phagocytosis is mediated by loss of swimming motility and is independent of flagellum expression. Infect Immun 78 2937 2945
5. BalloyVVermaAKuraviSSi-TaharMChignardM 2007 The role of flagellin versus motility in acute lung disease caused by Pseudomonas aeruginosa. J Infect Dis 196 289 296
6. LuzarMAThomassenMJMontieTC 1985 Flagella and motility alterations in Pseudomonas aeruginosa strains from patients with cystic fibrosis: relationship to patient clinical condition. Infect Immun 50 577 582
7. MahenthiralingamECampbellMESpeertDP 1994 Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun 62 596 605
8. MahenthiralingamESpeertDP 1995 Nonopsonic phagocytosis of Pseudomonas aeruginosa by macrophages and polymorphonuclear leukocytes requires the presence of the bacterial flagellum. Infect Immun 63 4519 4523
9. ToutainCMZegansMEO'TooleGA 2005 Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J. Bacteriol 187 771 777
10. TerashimaHKojimaSHommaM 2008 Flagellar motility in bacteria structure and function of flagellar motor. Int Rev Cell Mol Biol 270 39 85
11. DeRosierDJ 1998 The turn of the screw: the bacterial flagellar motor. Cell 93 17 20
12. MartinezRMDharmasenaMNKirnTJTaylorRK 2009 Characterization of two outer membrane proteins, FlgO and FlgP, that influence vibrio cholerae motility. J Bacteriol 191 5669 5679
13. BraunTFPSGullyJBEmpeyJCVan WaySPutnamA 1999 Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli. J Bacteriol 181 3542 3551
14. DoyleTBHawkinsACMcCarterLL 2004 The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol 186 6341 6350
15. GosinkKKHaseCC 2000 Requirements for conversion of the Na(+)-driven flagellar motor of Vibrio cholerae to the H(+)-driven motor of Escherichia coli. J Bacteriol 182 4234 4240
16. PrittBO'BrienLWinnW 2007 Mucoid Pseudomonas in cystic fibrosis. Am J Clin Pathol 128 32 34
17. OhmanDEChakrabartyAM 1981 Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect Immun 33 142 148
18. HulbertRRTaylorRK 2002 Mechanism of ToxT-dependent transcriptional activation at the Vibrio cholerae tcpA promoter. J Bacteriol 184 5533 5544
19. StonehouseEKovacikovaGTaylorRKSkorupskiK 2008 Integration host factor positively regulates virulence gene expression in Vibrio cholerae. J Bacteriol 190 4736 4748
20. SunDXMekalanosJJTaylorRK 1990 Antibodies directed against the toxin-coregulated pilus isolated from Vibrio cholerae provide protection in the infant mouse experimental cholera model. J Infect Dis 161 1231 1236
21. SantosLRodriguesDLiraMOliveiraRReal OliveiraME 2007 The effect of octylglucoside and sodium cholate in Staphylococcus epidermidis and Pseudomonas aeruginosa adhesion to soft contact lenses. Optom Vis Sci 84 429 434
22. KandaETatsutaTSuzukiTTaguchiFNaitoK 2010 Two flagellar stators and their roles in motility and virulence in Pseudomonas syringae pv. tabaci 6605. Mol Genet Genomics
23. KojimaSYamamotoKKawagishiIHommaM 1999 The polar flagellar motor of Vibrio cholerae is driven by an Na+ motive force. J Bacteriol 181 1927 1930
24. AroraSKRitchingsBWAlmiraECLorySRamphalR 1998 The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect Immun 66 1000 1007
25. AttridgeSRRowleyD 1983 The role of the flagellum in the adherence of Vibrio cholerae. J Infect Dis 147 864 872
26. GironJATorresAGFreerEKaperJB 2002 The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44 361 379
27. BirukovKGShirinskyVPStepanovaOVTkachukVAHahnAW 1995 Stretch affects phenotype and proliferation of vascular smooth muscle cells. Mol Cell Biochem 144 131 139
28. FingerEBPuriKDAlonRLawrenceMBvon AndrianUH 1996 Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature 379 266 269
29. DrakeDMontieTC 1988 Flagella, motility and invasive virulence of Pseudomonas aeruginosa. J Gen Microbiol 134 43 52
30. FreterRJonesGW 1976 Adhesive properties of Vibrio cholerae: nature of the interaction with intact mucosal surfaces. Infect Immun 14 246 256
31. PierGBMeluleniGGoldbergJB 1995 Clearance of Pseudomonas aeruginosa from the murine gastrointestinal tract is effectively mediated by O-antigen-specific circulating antibodies. Infect Immun 63 2818 2825
32. SiitonenANurminenM 1992 Bacterial motility is a colonization factor in experimental urinary tract infection. Infect Immun 60 3918 3920
33. InabaKInabaMDeguchiMHagiKYasumizuR 1993 Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class II-negative progenitor in mouse bone marrow. Proc Natl Acad Sci U S A 90 3038 3042
34. BloembergGVO'TooleGALugtenbergBJJKolterR 1997 Green fluorescent protein as a marker for Pseudomonas spp. Appl Environ Microbiol 63 4543 4551
35. MacFerrinKDTerranovaMPSchreiberSLVerdineGL 1990 Overproduction and dissection of proteins by the expression-cassette polymerase chain reaction. Proc Natl Acad Sci U S A 87 1937 1941
36. DuncanMJLiGShinJSCarsonJLAbrahamSN 2004 Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem 279 18944 18951
37. R Development Core Team 2009 R: A Language and Environment for Statistical Computing. http://www.R-project.org
38. GentlemanR 2005 Bioinformatics and computational biology solutions using R and Bioconductor, in Statistics for biology and health. Vol. xix New york Springer Science+Business Media 473
39. GentlemanRCCareyVJBatesDMBolstadBDettlingM 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 R80
40. BolstadBMIrizarryRAAstrandMSpeedTP 2003 A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19 185 193
41. IrizarryRABolstadBMCollinFCopeLMBHobbs 2003 Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31 e15
42. BengtssonHSimpsonKBullardJHansenK 2008 aroma.affymetrix: A generic framework in R for analyzing small to very large Affymetrix data sets in bounded memory, in Technical Report #745, Department of Statistics, University of California, Berkeley
43. WilsonCLMillerCJ 2005 Simpleaffy: a BioConductor package for Affymetrix Quality Control and data analysis. Bioinformatics 21 3683 3685
44. ParmanCHallingCGentlemanR 2005 affyQCReport: QC Report Generation for affyBatch objects
45. BatesDMoechlerMDaiB 2008 lme4: Linear mixed-effects models using S4 classes
Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek Hostile Takeover by : Reorganization of Parasite and Host Cell Membranes during Liver Stage EgressČlánek A Trigger Enzyme in : Impact of the Glycerophosphodiesterase GlpQ on Virulence and Gene ExpressionČlánek An EGF-like Protein Forms a Complex with PfRh5 and Is Required for Invasion of Human Erythrocytes byČlánek Th2-polarised PrP-specific Transgenic T-cells Confer Partial Protection against Murine ScrapieČlánek Alterations in the Transcriptome during Infection with West Nile, Dengue and Yellow Fever Viruses
Článok vyšiel v časopisePLOS Pathogens
Najčítanejšie tento týždeň
2011 Číslo 9- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
-
Všetky články tohto čísla
- Unconventional Repertoire Profile Is Imprinted during Acute Chikungunya Infection for Natural Killer Cells Polarization toward Cytotoxicity
- Envelope Deglycosylation Enhances Antigenicity of HIV-1 gp41 Epitopes for Both Broad Neutralizing Antibodies and Their Unmutated Ancestor Antibodies
- Co-opts GBF1 and CERT to Acquire Host Sphingomyelin for Distinct Roles during Intracellular Development
- Nrf2, a PPARγ Alternative Pathway to Promote CD36 Expression on Inflammatory Macrophages: Implication for Malaria
- Robust Antigen Specific Th17 T Cell Response to Group A Streptococcus Is Dependent on IL-6 and Intranasal Route of Infection
- Targeting of a Chlamydial Protease Impedes Intracellular Bacterial Growth
- The Protease Cruzain Mediates Immune Evasion
- High-Resolution Phenotypic Profiling Defines Genes Essential for Mycobacterial Growth and Cholesterol Catabolism
- Plague and Climate: Scales Matter
- Exhausted CD8 T Cells Downregulate the IL-18 Receptor and Become Unresponsive to Inflammatory Cytokines and Bacterial Co-infections
- Maturation-Induced Cloaking of Neutralization Epitopes on HIV-1 Particles
- Murine Gamma-herpesvirus Immortalization of Fetal Liver-Derived B Cells Requires both the Viral Cyclin D Homolog and Latency-Associated Nuclear Antigen
- Rapid and Efficient Clearance of Blood-borne Virus by Liver Sinusoidal Endothelium
- Hostile Takeover by : Reorganization of Parasite and Host Cell Membranes during Liver Stage Egress
- A Trigger Enzyme in : Impact of the Glycerophosphodiesterase GlpQ on Virulence and Gene Expression
- Strain Specific Resistance to Murine Scrapie Associated with a Naturally Occurring Human Prion Protein Polymorphism at Residue 171
- Development of a Transformation System for : Restoration of Glycogen Biosynthesis by Acquisition of a Plasmid Shuttle Vector
- Monalysin, a Novel -Pore-Forming Toxin from the Pathogen Contributes to Host Intestinal Damage and Lethality
- Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts
- BC2L-C Is a Super Lectin with Dual Specificity and Proinflammatory Activity
- Expression of the RAE-1 Family of Stimulatory NK-Cell Ligands Requires Activation of the PI3K Pathway during Viral Infection and Transformation
- Structure of the Vesicular Stomatitis Virus N-P Complex
- HSV Infection Induces Production of ROS, which Potentiate Signaling from Pattern Recognition Receptors: Role for S-glutathionylation of TRAF3 and 6
- The Human Papillomavirus E6 Oncogene Represses a Cell Adhesion Pathway and Disrupts Focal Adhesion through Degradation of TAp63β upon Transformation
- Analysis of Behavior and Trafficking of Dendritic Cells within the Brain during Toxoplasmic Encephalitis
- Exposure to the Viral By-Product dsRNA or Coxsackievirus B5 Triggers Pancreatic Beta Cell Apoptosis via a Bim / Mcl-1 Imbalance
- Multidrug Resistant 2009 A/H1N1 Influenza Clinical Isolate with a Neuraminidase I223R Mutation Retains Its Virulence and Transmissibility in Ferrets
- Structure of Herpes Simplex Virus Glycoprotein D Bound to the Human Receptor Nectin-1
- Step-Wise Loss of Bacterial Flagellar Torsion Confers Progressive Phagocytic Evasion
- Complex Recombination Patterns Arising during Geminivirus Coinfections Preserve and Demarcate Biologically Important Intra-Genome Interaction Networks
- An EGF-like Protein Forms a Complex with PfRh5 and Is Required for Invasion of Human Erythrocytes by
- Non-Lytic, Actin-Based Exit of Intracellular Parasites from Intestinal Cells
- The Fecal Viral Flora of Wild Rodents
- The General Transcriptional Repressor Tup1 Is Required for Dimorphism and Virulence in a Fungal Plant Pathogen
- Interferon Regulatory Factor-1 (IRF-1) Shapes Both Innate and CD8 T Cell Immune Responses against West Nile Virus Infection
- A Small Non-Coding RNA Facilitates Bacterial Invasion and Intracellular Replication by Modulating the Expression of Virulence Factors
- Evaluating the Sensitivity of to Biotin Deprivation Using Regulated Gene Expression
- The Motility of a Human Parasite, , Is Regulated by a Novel Lysine Methyltransferase
- Phosphodiesterase-4 Inhibition Alters Gene Expression and Improves Isoniazid – Mediated Clearance of in Rabbit Lungs
- Restoration of IFNγR Subunit Assembly, IFNγ Signaling and Parasite Clearance in Infected Macrophages: Role of Membrane Cholesterol
- Protease ROM1 Is Important for Proper Formation of the Parasitophorous Vacuole
- The Regulated Secretory Pathway in CD4 T cells Contributes to Human Immunodeficiency Virus Type-1 Cell-to-Cell Spread at the Virological Synapse
- Rerouting of Host Lipids by Bacteria: Are You CERTain You Need a Vesicle?
- Transmission Characteristics of the 2009 H1N1 Influenza Pandemic: Comparison of 8 Southern Hemisphere Countries
- Th2-polarised PrP-specific Transgenic T-cells Confer Partial Protection against Murine Scrapie
- Sequential Bottlenecks Drive Viral Evolution in Early Acute Hepatitis C Virus Infection
- Genomic Insights into the Origin of Parasitism in the Emerging Plant Pathogen
- Genomic and Proteomic Analyses of the Fungus Provide Insights into Nematode-Trap Formation
- Influenza Virus Ribonucleoprotein Complexes Gain Preferential Access to Cellular Export Machinery through Chromatin Targeting
- Alterations in the Transcriptome during Infection with West Nile, Dengue and Yellow Fever Viruses
- Protease-Sensitive Conformers in Broad Spectrum of Distinct PrP Structures in Sporadic Creutzfeldt-Jakob Disease Are Indicator of Progression Rate
- Vaccinia Virus Protein C6 Is a Virulence Factor that Binds TBK-1 Adaptor Proteins and Inhibits Activation of IRF3 and IRF7
- c-di-AMP Is a New Second Messenger in with a Role in Controlling Cell Size and Envelope Stress
- Structural and Functional Studies on the Interaction of GspC and GspD in the Type II Secretion System
- APOBEC3A Is a Specific Inhibitor of the Early Phases of HIV-1 Infection in Myeloid Cells
- Impairment of Immunoproteasome Function by β5i/LMP7 Subunit Deficiency Results in Severe Enterovirus Myocarditis
- HTLV-1 Propels Thymic Human T Cell Development in “Human Immune System” Rag2 gamma c Mice
- Tri6 Is a Global Transcription Regulator in the Phytopathogen
- Exploiting and Subverting Tor Signaling in the Pathogenesis of Fungi, Parasites, and Viruses
- The Next Opportunity in Anti-Malaria Drug Discovery: The Liver Stage
- Significant Effects of Antiretroviral Therapy on Global Gene Expression in Brain Tissues of Patients with HIV-1-Associated Neurocognitive Disorders
- Inhibition of Competence Development, Horizontal Gene Transfer and Virulence in by a Modified Competence Stimulating Peptide
- A Novel Metal Transporter Mediating Manganese Export (MntX) Regulates the Mn to Fe Intracellular Ratio and Virulence
- Rhoptry Kinase ROP16 Activates STAT3 and STAT6 Resulting in Cytokine Inhibition and Arginase-1-Dependent Growth Control
- Hsp90 Governs Dispersion and Drug Resistance of Fungal Biofilms
- Secretion of Genome-Free Hepatitis B Virus – Single Strand Blocking Model for Virion Morphogenesis of Para-retrovirus
- A Viral Ubiquitin Ligase Has Substrate Preferential SUMO Targeted Ubiquitin Ligase Activity that Counteracts Intrinsic Antiviral Defence
- Membrane Remodeling by the Double-Barrel Scaffolding Protein of Poxvirus
- A Diverse Population of Molecular Type VGIII in Southern Californian HIV/AIDS Patients
- Disruption of TLR3 Signaling Due to Cleavage of TRIF by the Hepatitis A Virus Protease-Polymerase Processing Intermediate, 3CD
- Quantitative Analyses Reveal Calcium-dependent Phosphorylation Sites and Identifies a Novel Component of the Invasion Motor Complex
- Discovery of the First Insect Nidovirus, a Missing Evolutionary Link in the Emergence of the Largest RNA Virus Genomes
- Old World Arenaviruses Enter the Host Cell via the Multivesicular Body and Depend on the Endosomal Sorting Complex Required for Transport
- Exploits a Unique Repertoire of Type IV Secretion System Components for Pilus Assembly at the Bacteria-Host Cell Interface
- Recurrent Signature Patterns in HIV-1 B Clade Envelope Glycoproteins Associated with either Early or Chronic Infections
- PLOS Pathogens
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- HTLV-1 Propels Thymic Human T Cell Development in “Human Immune System” Rag2 gamma c Mice
- Hostile Takeover by : Reorganization of Parasite and Host Cell Membranes during Liver Stage Egress
- Exploiting and Subverting Tor Signaling in the Pathogenesis of Fungi, Parasites, and Viruses
- A Viral Ubiquitin Ligase Has Substrate Preferential SUMO Targeted Ubiquitin Ligase Activity that Counteracts Intrinsic Antiviral Defence
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy