A Cyclic GMP Signalling Module That Regulates Gliding Motility in a Malaria Parasite
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{"title"=>"A cyclic GMP signalling module that regulates gliding motility in a malaria parasite", "type"=>"journal", "authors"=>[{"first_name"=>"Robert W.", "last_name"=>"Moon", "scopus_author_id"=>"9635670600"}, {"first_name"=>"Cathy J.", "last_name"=>"Taylor", "scopus_author_id"=>"56328827700"}, {"first_name"=>"Claudia", "last_name"=>"Bex", "scopus_author_id"=>"57189181869"}, {"first_name"=>"Rebecca", "last_name"=>"Schepers", "scopus_author_id"=>"20735608700"}, {"first_name"=>"David", "last_name"=>"Goulding", "scopus_author_id"=>"7003436963"}, {"first_name"=>"Chris J.", "last_name"=>"Janse", "scopus_author_id"=>"7005097427"}, {"first_name"=>"Andrew P.", "last_name"=>"Waters", "scopus_author_id"=>"7101758887"}, {"first_name"=>"David A.", "last_name"=>"Baker", "scopus_author_id"=>"7404141194"}, {"first_name"=>"Oliver", "last_name"=>"Billker", "scopus_author_id"=>"6602301142"}], "year"=>2009, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-70349666538", "sgr"=>"70349666538", "pui"=>"355378744", "isbn"=>"1553-7374 (Electronic)", "pmid"=>"19779564", "doi"=>"10.1371/journal.ppat.1000599"}, "id"=>"4e10379a-bc8a-3f69-82da-965be7a65e42", "abstract"=>"The ookinete is a motile stage in the malaria life cycle which forms in the mosquito blood meal from the zygote. Ookinetes use an acto-myosin motor to glide towards and penetrate the midgut wall to establish infection in the vector. The regulation of gliding motility is poorly understood. Through genetic interaction studies we here describe a signalling module that identifies guanosine 3', 5'-cyclic monophosphate (cGMP) as an important second messenger regulating ookinete differentiation and motility. In ookinetes lacking the cyclic nucleotide degrading phosphodiesterase delta (PDEdelta), unregulated signalling through cGMP results in rounding up of the normally banana-shaped cells. This phenotype is suppressed in a double mutant additionally lacking guanylyl cyclase beta (GCbeta), showing that in ookinetes GCbeta is an important source for cGMP, and that PDEdelta is the relevant cGMP degrading enzyme. Inhibition of the cGMP-dependent protein kinase, PKG, blocks gliding, whereas enhanced signalling through cGMP restores normal gliding speed in a mutant lacking calcium dependent protein kinase 3, suggesting at least a partial overlap between calcium and cGMP dependent pathways. These data demonstrate an important function for signalling through cGMP, and most likely PKG, in dynamically regulating ookinete gliding during the transmission of malaria to the mosquito.", "link"=>"http://www.mendeley.com/research/cyclic-gmp-signalling-module-regulates-gliding-motility-malaria-parasite", "reader_count"=>83, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>35, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>35, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>61, "Medicine and Dentistry"=>4, "Business, Management and Accounting"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>4, "Social Sciences"=>1, "Immunology and Microbiology"=>3, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>4}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>61}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>2, "United Kingdom"=>2, "Germany"=>1}, "group_count"=>1}

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  • {"files"=>["https://ndownloader.figshare.com/files/882777"], "description"=>"<p>(A) Conversion rate to mature ookinetes was scored for 22 h cultures, to which Cmpd 1 or vehicle had been added from 3 hours of culture. (B) Southern blot analysis comparing genotypes of three <i>pdeδ gcβ</i> double knockout clones (<i>p/g</i> cl. 3–5) obtained from a cross to the parental mutants and wild type. Genomic DNA was digested and probed as for single mutants (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat-1000599-g002\" target=\"_blank\">Figs. 2</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat-1000599-g005\" target=\"_blank\">5</a>). Effect of <i>pdeδ gcβ</i> double mutant (C), and pde<i>δ</i> cdpk3 double mutant (F) on conversion to morphologically mature ookinetes in 22-hour cultures. (D) Effect of <i>pdeδ gcβ</i> double mutant on average gliding speed in Matrigel™. (E) Three parasite clones obtained from the <i>pdeδ</i> and <i>cdpk3</i> genetic cross (<i>p/c</i>) were genotyped by Southern hybridization, along with wild type and parental clones. To examine disruption/deletion of the targeted locus genomic DNA was digested and probed as in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat-1000599-g005\" target=\"_blank\">Fig. 5</a> for <i>pdeδ</i>, or as described previously (Siden-Kiamos <i>et al.</i>, 2006) for <i>cdpk3</i>. In the left panel a 4.3 kb band is recognised by a 5' probe in <i>Eco</i>RI-digested DNA in wild type and appearance of a larger 5.8 kb fragment is diagnostic of <i>pdeδ</i> deletion. In the right panel a 3 kb and a 0.9 kb fragment recognised in <i>Eco</i>RI/<i>Hin</i>dIII digested DNA by a <i>cdpk3</i>-specific probe indicate an intact <i>cdpk3</i> locus only in wild type and <i>pdeδ</i>, and there absence indicates deletion of <i>cdpk3</i> in all other clones (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat.1000599.s003\" target=\"_blank\">Figure S2 G</a>). (G) Effect of the <i>pdeδ cdpk3</i> double mutant on average gliding speed of individual, morphologically mature ookinetes after 15–18 hour of culture. Statistical analysis was done by two-tailed t-test), p≤0.02 (A, C, D, F and G). For all graphs error bars show standard deviations in 3 biological replicates, * = significantly greater than <i>pdeδ</i>. Φ = significantly less than wild type. Ψ = significantly greater speed than <i>cdpk3</i> ookinetes.</p>", "links"=>[], "tags"=>["phenotype", "cmpd", "epistatic", "interactions"], "article_id"=>553229, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000599.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Suppression_of_the_pde_948_phenotype_by_Cmpd_1_and_epistatic_interactions_in_pde_948_gc_946_and_pde_948_cdpk3_double_mutants_/553229", "title"=>"Suppression of the <i>pdeδ</i> phenotype by Cmpd 1 and epistatic interactions in <i>pdeδ gcβ</i> and <i>pdeδ cdpk3</i> double mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-09-25 00:53:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/882418"], "description"=>"<p>(A) Male gamete formation (exflagellation), (B) macrogamete-to-mature ookinete conversion rate (determined as % of “banana”-shaped cells stained with female-derived cell specific antibody) and (C) average oocysts numbers on midguts dissected 10 days post infection were compared. Data were from 3 independent experiments and error bars show standard deviations. (D) Giemsa-stained blood films illustrating normal stages of ookinete differentiation and aberrant forms additionally present in <i>pdeδ</i> ookinete cultures. Scale bars indicate 2 µm. (E) Ookinete stages as a percentage of the total number of female derived cells on Giemsa-stained blood films. Slides were prepared from <i>in vitro</i> cultures at the times indicated. Error bars represent standard deviations in three biological replicates. (F) Forward motility and (G) rotation speed of <i>pdeδ</i> and wild type ookinetes as a function of cell length from 15–22 hour <i>in vitro</i> cultures were determined using the Matrigel™ motility assay. Forward speed was averaged over 10 minutes. The rotational component of ookinete motility was determined as (number of turns×circumference at widest point) and averaged over 10 min. Best fit and correlation coefficient r are given for <i>pdeδ</i> ookinetes only. Examples of motility of <i>pdeδ</i> ookinetes with normal, stumpy and round morphology are shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat.1000599.s008\" target=\"_blank\">Videos S3</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat.1000599.s009\" target=\"_blank\">S4</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat.1000599.s010\" target=\"_blank\">S5</a>.</p>", "links"=>[], "tags"=>["ookinete", "morphology", "parasite"], "article_id"=>552873, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000599.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PDE_948_is_essential_for_normal_ookinete_morphology_and_parasite_transmission_to_the_mosquito_/552873", "title"=>"PDEδ is essential for normal ookinete morphology and parasite transmission to the mosquito.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-09-25 00:47:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/882936"], "description"=>"<p>20–21 days after injection with mutant and wild type ookinetes, salivary glands were dissected and sporozoites were quantified, or mosquitoes were allowed to feed on naïve mice. * Number of mosquitoes dissected. Ψ Number of mosquitoes fed.</p>", "links"=>[], "tags"=>["numbers", "infectivity", "ookinete", "injected"], "article_id"=>553384, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000599.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sporozoite_numbers_and_infectivity_in_ookinete_injected_mosquitoes_/553384", "title"=>"Sporozoite numbers and infectivity in ookinete injected mosquitoes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-09-25 00:56:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/882306"], "description"=>"<p>(A) Male gamete formation (exflagellation), (B) macrogamete-to-mature ookinete conversion rate (determined as % of “banana”-shaped cells stained with female-derived cell specific antibody) and (C) average oocysts numbers on midguts dissected 10 days post infection were compared. Data were from 3 independent experiments and error bars show standard deviations. Different gliding speeds of wild type (D) and <i>gcβ</i> (E) ookinetes in Matrigel™ is illustrated with representative frames from time lapse videos (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat.1000599.s006\" target=\"_blank\">Videos S1</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000599#ppat.1000599.s007\" target=\"_blank\">S2</a>). The black arrow marks the apical end of the ookinete and scale bar denotes 10 µm. (F) Speed of individual ookinetes (diamonds) from 24 h cultures, measured over a 10 min period in 3 mutants compared to wild type. The thick black lines denote mean. (G) Impact of Cmpd 1 on gliding of wild type ookinetes. * = significantly different, Student's T-test, p≤0.01.</p>", "links"=>[], "tags"=>["ookinete", "motility", "parasite"], "article_id"=>552752, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000599.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GC_946_is_essential_for_ookinete_motility_and_parasite_transmission_to_the_mosquito_/552752", "title"=>"GCβ is essential for ookinete motility and parasite transmission to the mosquito.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-09-25 00:45:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/882567"], "description"=>"<p>(A) Sagittal section through wild type ookinete. (B). Detail of wild type apical complex. (C) Detail of <i>pdeδ</i> apical complex. (D) Detail of <i>pdeδ</i> subpellicular microtubules in transverse section (detail of F). (E) Detail of <i>pdeδ</i> IMC (detail of F). (F). Sagittal section of whole “round” form <i>pdeδ</i> ookinete. Arrows point to interruptions in the IMC (C, E and F). Scale bars denote 500 nm in all images. Abbreviations: ApC; Apical Complex, Co; Collar, Cr; Crystalloid, Pg; Pigment Vacuole, IMC; Inner Membrane Complex, Mi; Micronemes, MTL; Subpellicular Microtubules in Longitudinal Section, MTT; Subpellicular Microtubules in Traverse Section, Nu; Nucleus, OM; Outer Pellicle Membrane.</p>", "links"=>[], "tags"=>["electron", "micrographs"], "article_id"=>553020, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000599.g003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transmission_electron_micrographs_of_wild_type_A_B_and_pde_948_C_F_ookinetes_/553020", "title"=>"Transmission electron micrographs of wild type (A, B) and <i>pdeδ</i> (C–F) ookinetes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-09-25 00:50:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/882695"], "description"=>"<p>cGMP-PDE (A) and cAMP-PDE (B) activity was measured in membrane fractions from various purified parasite stages in wild type and <i>pdeδ</i> parasites. (C) Total intracellular cGMP concentration was measured in 24 h paramagnetic bead-purified ookinetes. For all datasets the graphs show the mean of three independently purified samples in each case, with error bars indicating standard deviations.</p>", "links"=>[], "tags"=>["cell biology/cell signaling", "cell biology/morphogenesis and cell biology", "microbiology/parasitology"], "article_id"=>553145, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000599.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Biochemical_analysis_of_pde_948_and_gc_946_mutants_/553145", "title"=>"Biochemical analysis of <i>pdeδ</i> and <i>gcβ</i> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-09-25 00:52:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/437783", "https://ndownloader.figshare.com/files/437817", "https://ndownloader.figshare.com/files/437848", "https://ndownloader.figshare.com/files/437875", "https://ndownloader.figshare.com/files/437893", "https://ndownloader.figshare.com/files/437913", "https://ndownloader.figshare.com/files/437947", "https://ndownloader.figshare.com/files/437980", "https://ndownloader.figshare.com/files/438014", "https://ndownloader.figshare.com/files/438044"], "description"=>"<div><p>The ookinete is a motile stage in the malaria life cycle which forms in the mosquito blood meal from the zygote. Ookinetes use an acto-myosin motor to glide towards and penetrate the midgut wall to establish infection in the vector. The regulation of gliding motility is poorly understood. Through genetic interaction studies we here describe a signalling module that identifies guanosine 3′, 5′-cyclic monophosphate (cGMP) as an important second messenger regulating ookinete differentiation and motility. In ookinetes lacking the cyclic nucleotide degrading phosphodiesterase δ (PDEδ), unregulated signalling through cGMP results in rounding up of the normally banana-shaped cells. This phenotype is suppressed in a double mutant additionally lacking guanylyl cyclase β (GCβ), showing that in ookinetes GCβ is an important source for cGMP, and that PDEδ is the relevant cGMP degrading enzyme. Inhibition of the cGMP-dependent protein kinase, PKG, blocks gliding, whereas enhanced signalling through cGMP restores normal gliding speed in a mutant lacking calcium dependent protein kinase 3, suggesting at least a partial overlap between calcium and cGMP dependent pathways. These data demonstrate an important function for signalling through cGMP, and most likely PKG, in dynamically regulating ookinete gliding during the transmission of malaria to the mosquito.</p></div>", "links"=>[], "tags"=>["cyclic", "gmp", "signalling", "module", "regulates", "gliding", "motility", "malaria", "parasite"], "article_id"=>146300, "categories"=>["Microbiology", "Cell Biology"], "users"=>["Robert W. Moon", "Cathy J. Taylor", "Claudia Bex", "Rebecca Schepers", "David Goulding", "Chris J. Janse", "Andrew P. Waters", "David A. Baker", "Oliver Billker"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000599.s001", "https://dx.doi.org/10.1371/journal.ppat.1000599.s002", "https://dx.doi.org/10.1371/journal.ppat.1000599.s003", "https://dx.doi.org/10.1371/journal.ppat.1000599.s004", "https://dx.doi.org/10.1371/journal.ppat.1000599.s005", "https://dx.doi.org/10.1371/journal.ppat.1000599.s006", "https://dx.doi.org/10.1371/journal.ppat.1000599.s007", "https://dx.doi.org/10.1371/journal.ppat.1000599.s008", "https://dx.doi.org/10.1371/journal.ppat.1000599.s009", "https://dx.doi.org/10.1371/journal.ppat.1000599.s010"], "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Cyclic_GMP_Signalling_Module_That_Regulates_Gliding_Motility_in_a_Malaria_Parasite/146300", "title"=>"A Cyclic GMP Signalling Module That Regulates Gliding Motility in a Malaria Parasite", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-09-25 01:45:00"}

PMC Usage Stats | Further Information

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Relative Metric

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