-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Utilize Host Actin for Efficient Maternal Transmission in
The world’s most common intracellular infection, Wolbachia pipientis, infects 40% of insect species and is currently used to prevent transmission of Dengue by mosquitoes. The bacterium targets the germline of insects, where it is faithfully transmitted to the developing oocyte and the next generation. Here we identify host cytoskeletal proteins required by Wolbachia in order to be efficiently transmitted between Drosophila melanogaster generations. We show that after only two generations in a phenotypically wild type, heterozygous mutant fly, Wolbachia infections are cleared or reduced in titer. Characterization of the mutants suggests that Wolbachia is sensitive to the regulation of actin in the ovary and that actin may be used by Wolbachia to both target and proliferate within host tissues and to be faithfully, maternally transmitted.
Vyšlo v časopise: Utilize Host Actin for Efficient Maternal Transmission in. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004798
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004798Souhrn
The world’s most common intracellular infection, Wolbachia pipientis, infects 40% of insect species and is currently used to prevent transmission of Dengue by mosquitoes. The bacterium targets the germline of insects, where it is faithfully transmitted to the developing oocyte and the next generation. Here we identify host cytoskeletal proteins required by Wolbachia in order to be efficiently transmitted between Drosophila melanogaster generations. We show that after only two generations in a phenotypically wild type, heterozygous mutant fly, Wolbachia infections are cleared or reduced in titer. Characterization of the mutants suggests that Wolbachia is sensitive to the regulation of actin in the ovary and that actin may be used by Wolbachia to both target and proliferate within host tissues and to be faithfully, maternally transmitted.
Zdroje
1. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6 : 741–751. doi: 10.1038/nrmicro1969 18794912
2. Zug R, Hammerstein P (2012) Still a host of hosts for wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7: e38544. doi: 10.1371/journal.pone.0038544 22685581
3. Hoerauf A, Specht S, Buttner M, Pfarr K, Mand S, et al. (2008) Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Medical Microbiology and Immunology 197 : 295–311. 17999080
4. Taylor MJ, Bandi C, Hoerauf AM, Lazdins J (2000) Wolbachia bacteria of filarial nematodes: A target for control? Parasitology Today 16 : 179–180. 10782070
5. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu GJ, Pyke AT, et al. (2009) A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium. Cell 139 : 1268–1278. doi: 10.1016/j.cell.2009.11.042 20064373
6. Turley AP, Moreira LA, O'Neill SL, McGraw EA (2009) Wolbachia Infection Reduces Blood-Feeding Success in the Dengue Fever Mosquito, Aedes aegypti. Plos Neglected Tropical Diseases 3(9):e516. doi: 10.1371/journal.pntd.0000516 19753103
7. LePage D, Bordenstein SR (2013) Wolbachia: Can we save lives with a great pandemic? Trends Parasitol 29 : 385–393. doi: 10.1016/j.pt.2013.06.003 23845310
8. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139 : 1268–1278. doi: 10.1016/j.cell.2009.11.042 20064373
9. Kittayapong P, Baisley KJ, Sharpe RG, Baimai V, O'Neill SL (2002) Maternal transmission efficiency of Wolbachia superinfections in Aedes albopictus populations in Thailand. Am J Trop Med Hyg 66 : 103–107. 12135258
10. Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140 : 1319–1338. 7498773
11. McGraw EA, Merritt DJ, Droller JN, O'Neill SL (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 99 : 2918–2923. 11880639
12. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5: e114. 17439303
13. Perrot-Minnot MJ, Werren JH (1999) Wolbachia infection and incompatibility dynamics in experimental selection lines. Journal of Evolutionary Biology 12 : 272–282.
14. Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol 70 : 5366–5372. 15345422
15. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, et al. (2005) Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1: e14. 16228015
16. Serbus LR, Sullivan W (2007) A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog 3: e190. 18085821
17. Albertson R, Casper-Lindley C, Cao J, Tram U, Sullivan W (2009) Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue. J Cell Sci 122 : 4570–4583. doi: 10.1242/jcs.054981 19934219
18. Toomey ME, Panaram K, Fast EM, Beatty C, Frydman HM (2013) Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection. Proc Natl Acad Sci U S A 110 : 10788–10793. doi: 10.1073/pnas.1301524110 23744038
19. Landmann F, Bain O, Martin C, Uni S, Taylor MJ, et al. (2012) Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biol Open 1 : 536–547. doi: 10.1242/bio.2012737 23213446
20. Melnikow E, Xu S, Liu J, Bell AJ, Ghedin E, et al. (2013) A potential role for the interaction of Wolbachia surface proteins with the Brugia malayi glycolytic enzymes and cytoskeleton in maintenance of endosymbiosis. PLoS Negl Trop Dis 7: e2151. doi: 10.1371/journal.pntd.0002151 23593519
21. Fischer K, Beatty WL, Weil GJ, Fischer PU (2014) High pressure freezing/freeze substitution fixation improves the ultrastructural assessment of Wolbachia endosymbiont—filarial nematode host interaction. PLoS One 9:e86383. doi: 10.1371/journal.pone.0086383 24466066
22. Verheyen EM, Cooley L (1994) Profilin Mutations Disrupt Multiple Actin-Dependent Processes during Drosophila Development. Development 120 : 717–728. 7600952
23. Cooley L, Verheyen E, Ayers K (1992) chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69 : 173–184. 1339308
24. Bakken AH (1973) A cytological and genetic study of oogenesis in Drosophila melanogaster. Dev Biol 33 : 100–122. 4363796
25. Cook RK, Christensen SJ, Deal JA, Coburn RA, Deal ME, et al. (2012) The generation of chromosomal deletions to provide extensive coverage and subdivision of the Drosophila melanogaster genome. Genome Biol 13: R21. doi: 10.1186/gb-2012-13-3-r21 22445104
26. Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, et al. (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334 : 990–992. doi: 10.1126/science.1209609 22021671
27. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8 : 405–407. doi: 10.1038/nmeth.1592 21460824
28. Verheyen E, Cooley L (1994) Looking at Oogenesis. Methods in Cell Biology, Vol 44 44 : 545–561. 7707970
29. Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA, et al. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology 72 : 7098–7110. 16936055
30. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: e(45).
31. Frydman HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441 : 509–512. 16724067
32. Shields AR, Spence AC, Yamashita YM, Davies EL, Fuller MT (2014) The actin-binding protein profilin is required for germline stem cell maintenance and germ cell enclosure by somatic cyst cells. Development 141 : 73–82. doi: 10.1242/dev.101931 24346697
33. Gonczy P, DiNardo S (1996) The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis. Development 122 : 2437–2447. 8756289
34. Genty LM, Bouchon D, Raimond M, Bertaux J (2014) Wolbachia infect ovaries in the course of their maturation: last minute passengers and priority travellers? PLoS One 9: e94577. doi: 10.1371/journal.pone.0094577 24722673
35. Robinson DN, Cooley L (1997) Genetic analysis of the actin cytoskeleton in the Drosophila ovary. Annual Review of Cell and Developmental Biology 13 : 147–170. 9442871
36. Castrillon DH, Gonczy P, Alexander S, Rawson R, Eberhart CG, et al. (1993) Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135 : 489–505. 8244010
37. Matova N, Cooley L (1998) Quail, a Drosophila villin-like protein, bundles actin filaments in apoptotic nurse cells. Molecular Biology of the Cell 9 : 18A–18A.
38. Matova N, Foley K, Cooley L (1998) Death and actin dynamics during Drosophila egg chamber development. Molecular Biology of the Cell 9 : 382A–382A.
39. Mahajanmiklos S, Cooley L (1994) The Villin-Like Protein Encoded by the Drosophila Quail Gene Is Required for Actin Bundle Assembly during Oogenesis. Cell 78 : 291–301. 8044841
40. Matova N, Mahajan-Miklos S, Mooseker MS, Cooley L (1999) Drosophila Quail, a villin-related protein, bundles actin filaments in apoptotic nurse cells. Development 126 : 5645–5657. 10572041
41. Manseau L, Calley J, Phan H (1996) Profilin is required for posterior patterning of the Drosophila oocyte. Development 122 : 2109–2116. 8681792
42. Hadfield SJ, Axton JM (1999) Reproduction—Germ cells colonized by endosymbiotic bacteria. Nature 402 : 482–482. 10591206
43. Kose H, Karr TL (1995) Organization of Wolbachia-Pipientis in the Drosophila Fertilized Egg and Embryo Revealed by an Anti-Wolbachia Monoclonal-Antibody. Mechanisms of Development 51 : 275–288. 7547474
44. Miller WJ, Riegler M (2006) Evolutionary dynamics of wAu-Like Wolbachia variants in neotropical Drosophila spp. Applied and Environmental Microbiology 72 : 826–835. 16391124
45. Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353 : 440–442. 1896086
46. Hamm CA, Begun DJ, Vo A, Smith CC, Saelao P, et al. (2014) Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella. Mol Ecol.
47. Carrington LB, Lipkowitz JR, Hoffmann AA, Turelli M (2011) A re-examination of Wolbachia-induced cytoplasmic incompatibility in California Drosophila simulans. PLoS One 6: e22565. doi: 10.1371/journal.pone.0022565 21799900
48. Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou WG, et al. (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochemistry and Molecular Biology 29 : 153–160. 10196738
49. Newton IL, Sheehan KB (2014) Passage of Wolbachia through mutant Drosophila melanogaster induces phenotypic and genomic changes. Appl Environ Microbiol.
50. Baum B, Perrimon N (2001) Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat Cell Biol 3 : 883–890. 11584269
51. Gouin E, Gantelet H, Egile C, Lasa I, Ohayon H, et al. (1999) A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112 (Pt 11): 1697–1708. 10318762
Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek Relay of Herpes Simplex Virus between Langerhans Cells and Dermal Dendritic Cells in Human SkinČlánek Does the Arthropod Microbiota Impact the Establishment of Vector-Borne Diseases in Mammalian Hosts?Článek The Ebola Epidemic Crystallizes the Potential of Passive Antibody Therapy for Infectious DiseasesČlánek Hepatitis D Virus Infection of Mice Expressing Human Sodium Taurocholate Co-transporting PolypeptideČlánek A Redox Regulatory System Critical for Mycobacterial Survival in Macrophages and Biofilm Development
Článok vyšiel v časopisePLOS Pathogens
Najčítanejšie tento týždeň
2015 Číslo 4- 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
- Pathogens as Biological Weapons of Invasive Species
- Selection and Spread of Artemisinin-Resistant Alleles in Thailand Prior to the Global Artemisinin Resistance Containment Campaign
- Endopeptidase-Mediated Beta Lactam Tolerance
- Prospective Large-Scale Field Study Generates Predictive Model Identifying Major Contributors to Colony Losses
- Relay of Herpes Simplex Virus between Langerhans Cells and Dermal Dendritic Cells in Human Skin
- Structural Determinants of Phenotypic Diversity and Replication Rate of Human Prions
- Sigma Factor SigB Is Crucial to Mediate Adaptation during Chronic Infections
- EphrinA2 Receptor (EphA2) Is an Invasion and Intracellular Signaling Receptor for
- Toxin-Induced Necroptosis Is a Major Mechanism of Lung Damage
- Heterologous Expression in Remodeled . : A Platform for Monoaminergic Agonist Identification and Anthelmintic Screening
- Novel Disease Susceptibility Factors for Fungal Necrotrophic Pathogens in Arabidopsis
- Interleukin 21 Signaling in B Cells Is Required for Efficient Establishment of Murine Gammaherpesvirus Latency
- Phosphorylation at the Homotypic Interface Regulates Nucleoprotein Oligomerization and Assembly of the Influenza Virus Replication Machinery
- Human Papillomaviruses Activate and Recruit SMC1 Cohesin Proteins for the Differentiation-Dependent Life Cycle through Association with CTCF Insulators
- Ubiquitous Promoter-Localization of Essential Virulence Regulators in
- TGF-β Suppression of HBV RNA through AID-Dependent Recruitment of an RNA Exosome Complex
- The Immune Adaptor ADAP Regulates Reciprocal TGF-β1-Integrin Crosstalk to Protect from Influenza Virus Infection
- Antagonism of miR-328 Increases the Antimicrobial Function of Macrophages and Neutrophils and Rapid Clearance of Non-typeable (NTHi) from Infected Lung
- The Epigenetic Regulator G9a Mediates Tolerance to RNA Virus Infection in
- Does the Arthropod Microbiota Impact the Establishment of Vector-Borne Diseases in Mammalian Hosts?
- Hantaan Virus Infection Induces Both Th1 and ThGranzyme B+ Cell Immune Responses That Associated with Viral Control and Clinical Outcome in Humans
- Viral Inhibition of the Transporter Associated with Antigen Processing (TAP): A Striking Example of Functional Convergent Evolution
- Plasma Membrane Profiling Defines an Expanded Class of Cell Surface Proteins Selectively Targeted for Degradation by HCMV US2 in Cooperation with UL141
- Optineurin Regulates the Interferon Response in a Cell Cycle-Dependent Manner
- IFIT1 Differentially Interferes with Translation and Replication of Alphavirus Genomes and Promotes Induction of Type I Interferon
- The EBNA3 Family of Epstein-Barr Virus Nuclear Proteins Associates with the USP46/USP12 Deubiquitination Complexes to Regulate Lymphoblastoid Cell Line Growth
- Hepatitis C Virus RNA Replication Depends on Specific and -Acting Activities of Viral Nonstructural Proteins
- A Neuron-Specific Antiviral Mechanism Prevents Lethal Flaviviral Infection of Mosquitoes
- The Aspartate-Less Receiver (ALR) Domains: Distribution, Structure and Function
- Global Genome and Transcriptome Analyses of Epidemic Isolate 98-06 Uncover Novel Effectors and Pathogenicity-Related Genes, Revealing Gene Gain and Lose Dynamics in Genome Evolution
- The Ebola Epidemic Crystallizes the Potential of Passive Antibody Therapy for Infectious Diseases
- Ebola Virus Entry: A Curious and Complex Series of Events
- Conserved Spirosomes Suggest a Single Type of Transformation Pilus in Competence
- Spatial Structure, Transmission Modes and the Evolution of Viral Exploitation Strategies
- Bacterial Cooperation Causes Systematic Errors in Pathogen Risk Assessment due to the Failure of the Independent Action Hypothesis
- Transgenic Fatal Familial Insomnia Mice Indicate Prion Infectivity-Independent Mechanisms of Pathogenesis and Phenotypic Expression of Disease
- Cerebrospinal Fluid Cytokine Profiles Predict Risk of Early Mortality and Immune Reconstitution Inflammatory Syndrome in HIV-Associated Cryptococcal Meningitis
- Utilize Host Actin for Efficient Maternal Transmission in
- Borna Disease Virus Phosphoprotein Impairs the Developmental Program Controlling Neurogenesis and Reduces Human GABAergic Neurogenesis
- An Effector Peptide Family Required for Toll-Mediated Immunity
- Hepatitis D Virus Infection of Mice Expressing Human Sodium Taurocholate Co-transporting Polypeptide
- A Redox Regulatory System Critical for Mycobacterial Survival in Macrophages and Biofilm Development
- Quadruple Quorum-Sensing Inputs Control Virulence and Maintain System Robustness
- Leukocyte-Derived IFN-α/β and Epithelial IFN-λ Constitute a Compartmentalized Mucosal Defense System that Restricts Enteric Virus Infections
- A Strategy for O-Glycoproteomics of Enveloped Viruses—the O-Glycoproteome of Herpes Simplex Virus Type 1
- Macrocyclic Lactones Differ in Interaction with Recombinant P-Glycoprotein 9 of the Parasitic Nematode and Ketoconazole in a Yeast Growth Assay
- Neofunctionalization of the α1,2fucosyltransferase Paralogue in Leporids Contributes to Glycan Polymorphism and Resistance to Rabbit Hemorrhagic Disease Virus
- The Extracytoplasmic Linker Peptide of the Sensor Protein SaeS Tunes the Kinase Activity Required for Staphylococcal Virulence in Response to Host Signals
- Murine CMV-Induced Hearing Loss Is Associated with Inner Ear Inflammation and Loss of Spiral Ganglia Neurons
- Dual miRNA Targeting Restricts Host Range and Attenuates Neurovirulence of Flaviviruses
- GATA-Dependent Glutaminolysis Drives Appressorium Formation in by Suppressing TOR Inhibition of cAMP/PKA Signaling
- Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Infection
- Genetic Analysis Using an Isogenic Mating Pair of Identifies Azole Resistance Genes and Lack of Locus’s Role in Virulence
- A Temporal Gate for Viral Enhancers to Co-opt Toll-Like-Receptor Transcriptional Activation Pathways upon Acute Infection
- Neutrophil Recruitment to Lymph Nodes Limits Local Humoral Response to
- PLOS Pathogens
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Toxin-Induced Necroptosis Is a Major Mechanism of Lung Damage
- Transgenic Fatal Familial Insomnia Mice Indicate Prion Infectivity-Independent Mechanisms of Pathogenesis and Phenotypic Expression of Disease
- Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Infection
- EphrinA2 Receptor (EphA2) Is an Invasion and Intracellular Signaling Receptor for
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