The Interaction between a Sexually Transferred Steroid Hormone and a Female Protein Regulates Oogenesis in the Malaria Mosquito Anopheles gambiae
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{"title"=>"The Interaction between a Sexually Transferred Steroid Hormone and a Female Protein Regulates Oogenesis in the Malaria Mosquito Anopheles gambiae", "type"=>"journal", "authors"=>[{"first_name"=>"Francesco", "last_name"=>"Baldini", "scopus_author_id"=>"35620058000"}, {"first_name"=>"Paolo", "last_name"=>"Gabrieli", "scopus_author_id"=>"25932069400"}, {"first_name"=>"Adam", "last_name"=>"South", "scopus_author_id"=>"24172929900"}, {"first_name"=>"Clarissa", "last_name"=>"Valim", "scopus_author_id"=>"8872362100"}, {"first_name"=>"Francesca", "last_name"=>"Mancini", "scopus_author_id"=>"55905968800"}, {"first_name"=>"Flaminia", "last_name"=>"Catteruccia", "scopus_author_id"=>"6603287350"}], "year"=>2013, "source"=>"PLoS Biology", "identifiers"=>{"issn"=>"15449173", "scopus"=>"2-s2.0-84886634315", "pui"=>"370141418", "doi"=>"10.1371/journal.pbio.1001695", "isbn"=>"1545-7885", "sgr"=>"84886634315", "pmid"=>"24204210"}, "id"=>"c1a3cd4a-a819-35ec-97d0-973569f7f990", "abstract"=>"Molecular interactions between male and female factors during mating profoundly affect the reproductive behavior and physiology of female insects. In natural populations of the malaria mosquito Anopheles gambiae, blood-fed females direct nutritional resources towards oogenesis only when inseminated. Here we show that the mating-dependent pathway of egg development in these mosquitoes is regulated by the interaction between the steroid hormone 20-hydroxy-ecdysone (20E) transferred by males during copulation and a female Mating-Induced Stimulator of Oogenesis (MISO) protein. RNAi silencing of MISO abolishes the increase in oogenesis caused by mating in blood-fed females, causes a delay in oocyte development, and impairs the function of male-transferred 20E. Co-immunoprecipitation experiments show that MISO and 20E interact in the female reproductive tract. Moreover MISO expression after mating is induced by 20E via the Ecdysone Receptor, demonstrating a close cooperation between the two factors. Male-transferred 20E therefore acts as a mating signal that females translate into an increased investment in egg development via a MISO-dependent pathway. The identification of this male-female reproductive interaction offers novel opportunities for the control of mosquito populations that transmit malaria.", "link"=>"http://www.mendeley.com/research/interaction-between-sexually-transferred-steroid-hormone-female-protein-regulates-oogenesis-malaria", "reader_count"=>91, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>23, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>6, "Lecturer"=>3, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>23, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>6, "Lecturer"=>3, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>7, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>66, "Medicine and Dentistry"=>3, "Neuroscience"=>2, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>2, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>66}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>4}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>3, "Senegal"=>1, "Tanzania"=>1, "Brazil"=>1, "United Kingdom"=>2, "France"=>1, "Bulgaria"=>1, "Portugal"=>1, "Germany"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1260278"], "description"=>"<p>(A) Mated females injected with ds<i>RNA</i> were blood fed and allowed to lay eggs 3 d post-blood-feeding for 4 nights. Control females (ds<i>LacZ</i>) laid on average 82.5 eggs, while ds<i>MISO</i> oviposited a statistically significant lower number of eggs (65.4). The data are representative of three independent replicates. (B) Virgin or mated females injected with ds<i>RNA</i> were blood fed, and eggs developed inside the ovaries were counted 3 d post-blood-feeding without allowing oviposition. Mated ds<i>LacZ</i> produced on average 77.8 eggs, while virgin ds<i>LacZ</i> and mated ds<i>MISO</i> produced a statistically significant lower number of eggs (62.3 and 60.4, respectively). The data are representative of six independent replicates.</p>", "links"=>[], "tags"=>["knockdown", "decreases", "virgin"], "article_id"=>834090, "categories"=>["Biological Sciences"], "users"=>["Francesco Baldini", "Paolo Gabrieli", "Adam South", "Clarissa Valim", "Francesca Mancini", "Flaminia Catteruccia"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001695.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MISO_knockdown_decreases_egg_production_to_virgin_levels_/834090", "title"=>"<i>MISO</i> knockdown decreases egg production to virgin levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-29 02:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1260283"], "description"=>"<p>(A and B) Immunofluorescence experiments on ovaries dissected from virgin and mated ds<i>LacZ</i> and mated ds<i>MISO</i> females stained with the lipid-binding reagent Nile-Red (red) at 24 h (A) and 60 h (B) post-blood-feeding. Asterisks in ds<i>MISO</i> and ds<i>LacZ</i> virgin ovaries indicate undeveloped primary follicles. Cell nuclei are labeled with DAPI (blue). Scale bar: 200 µm. (C) qRT-PCR of <i>Lp</i> and <i>Vg</i> from the fat body of virgin and mated ds<i>LacZ</i> and mated ds<i>MISO</i> females 24 h after blood feeding (BF). Expression levels (shown in logarithmic scale) were normalized to the housekeeping gene <i>RpL19</i>. The box-and-whisker diagrams represent five replicates of pools of 6–10 tissues.</p>", "links"=>[], "tags"=>["alters", "lipid", "transporter", "oocytes"], "article_id"=>834095, "categories"=>["Biological Sciences"], "users"=>["Francesco Baldini", "Paolo Gabrieli", "Adam South", "Clarissa Valim", "Francesca Mancini", "Flaminia Catteruccia"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001695.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MISO_silencing_alters_the_expression_of_the_lipid_transporter_Lipophorin_in_developing_oocytes_after_blood_feeding_/834095", "title"=>"<i>MISO</i> silencing alters the expression of the lipid transporter <i>Lipophorin</i> in developing oocytes after blood feeding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-29 02:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1260284"], "description"=>"<p>(A) <i>In vitro</i> ovarian ecdysteroid secretion before and 18 h after a blood meal in virgin and mated ds<i>LacZ</i> and mated ds<i>MISO</i>. Graph shows data from eight individual ovaries. Data are represented as mean ± SEM. Means with the same letter are not significantly different (<i>p</i>>0.05). (B) Changes over time in the geometric mean of the ecdysteroid titer (natural logarithm) of ds<i>LacZ</i> (black solid line with circles) and ds<i>MISO</i> (green dashed line with triangles) females at 5 time points after mating (0.5, 6, 12, 18, and 24 hpm) with the mean trajectories estimated in regression mixed models (dashed and dotted lines). Nine replicates were performed using a pool of three atria each. (C) qRT-PCR of 5 20E-responsive genes (<i>Vg</i>, <i>Lp</i>, <i>EcR</i>, <i>HR3</i>, and <i>USP</i>) in ds<i>MISO</i> and ds<i>LacZ</i> females at different time points (0, 6, 12, 18 h) after mating. The levels of <i>MISO</i> after ds<i>MISO</i> injections are also shown. Four independent replicates were performed using a pool of 5–10 female abdomens. Expression was normalized to the housekeeping gene <i>RpL19</i>. Data are represented as mean ± SEM. One or two asterisks represent <i>p</i><0.05 and <i>p</i><0.001, respectively.</p>", "links"=>[], "tags"=>["atrial", "20e", "titers", "activation", "20e-responsive", "genes"], "article_id"=>834096, "categories"=>["Biological Sciences"], "users"=>["Francesco Baldini", "Paolo Gabrieli", "Adam South", "Clarissa Valim", "Francesca Mancini", "Flaminia Catteruccia"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001695.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MISO_silencing_affects_atrial_20E_titers_and_reduces_the_activation_of_20E_responsive_genes_after_mating_/834096", "title"=>"<i>MISO</i> silencing affects atrial 20E titers and reduces the activation of 20E-responsive genes after mating.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-29 02:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1260291"], "description"=>"<p>(A) Western blot under native nondenaturing gel condition using anti-20E and anti-MISO antibodies on atria of virgin or mated (8 hpm) females. Left and right arrowheads indicate 20E and MISO positive bands, respectively. (B) Co-immunoprecipitation of MISO and 20E in atria of virgin or mated (8 hpm) females. The anti-MISO immunoprecipitation (IP) was quantified with anti-20E ELISA. Mated atria showed a mean of 0.68 ng, while in virgin atria no 20E was detected. Three experiments were performed using a pool of 50 atria each, one-third used for the IP (upper panel) and two-thirds for the ELISA (lower panel). Data are represented as mean ± SEM. (C) <i>MISO</i> expression in atria dissected from females previously injected in the hemolymph with three 10-fold dilutions of 20E in ethanol (10% v/v) (starting from 2.5 µg of 20E per mosquito). Ethanol (10% v/v) and water-soluble cholesterol (0.25 µg/mosquito) were used as controls. Expression levels were measured 24 h after injection or mating, and were normalized to <i>RpL19</i> and then to virgin levels in each replicate. A minimum of three replicates were performed for each condition. Data are represented as mean ± SEM. (D) qRT-PCR of <i>MISO</i> and <i>Vg</i> in females injected with ds<i>EcR</i>, analyzed at 6, 24, and 72 hpm. Expression levels (shown in logarithmic scale as fold changes relative to age-matched virgins) were normalized to the housekeeping gene <i>RpL19</i>. The analysis was performed in four replicates on pools of 5–10 female lower reproductive tracts. Data are represented as mean ± SEM. The asterisk indicates <i>p</i><0.05.</p>", "links"=>[], "tags"=>["induced", "interacts", "20e"], "article_id"=>834098, "categories"=>["Biological Sciences"], "users"=>["Francesco Baldini", "Paolo Gabrieli", "Adam South", "Clarissa Valim", "Francesca Mancini", "Flaminia Catteruccia"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001695.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MISO_is_induced_by_and_interacts_with_20E_in_the_female_atrium_/834098", "title"=>"MISO is induced by and interacts with 20E in the female atrium.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-29 02:48:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/1260297", "https://ndownloader.figshare.com/files/1260298", "https://ndownloader.figshare.com/files/1260299", "https://ndownloader.figshare.com/files/1260300", "https://ndownloader.figshare.com/files/1260301", "https://ndownloader.figshare.com/files/1260302", "https://ndownloader.figshare.com/files/1260303"], "description"=>"<div><p>Molecular interactions between male and female factors during mating profoundly affect the reproductive behavior and physiology of female insects. In natural populations of the malaria mosquito <i>Anopheles gambiae</i>, blood-fed females direct nutritional resources towards oogenesis only when inseminated. Here we show that the mating-dependent pathway of egg development in these mosquitoes is regulated by the interaction between the steroid hormone 20-hydroxy-ecdysone (20E) transferred by males during copulation and a female <i>Mating-Induced Stimulator of Oogenesis</i> (<i>MISO</i>) protein. RNAi silencing of <i>MISO</i> abolishes the increase in oogenesis caused by mating in blood-fed females, causes a delay in oocyte development, and impairs the function of male-transferred 20E. Co-immunoprecipitation experiments show that MISO and 20E interact in the female reproductive tract. Moreover <i>MISO</i> expression after mating is induced by 20E via the <i>Ecdysone Receptor</i>, demonstrating a close cooperation between the two factors. Male-transferred 20E therefore acts as a mating signal that females translate into an increased investment in egg development via a MISO-dependent pathway. The identification of this male–female reproductive interaction offers novel opportunities for the control of mosquito populations that transmit malaria.</p></div>", "links"=>[], "tags"=>["steroid", "regulates", "oogenesis", "malaria", "mosquito"], "article_id"=>834104, "categories"=>["Biological Sciences"], "users"=>["Francesco Baldini", "Paolo Gabrieli", "Adam South", "Clarissa Valim", "Francesca Mancini", "Flaminia Catteruccia"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001695.s001", "https://dx.doi.org/10.1371/journal.pbio.1001695.s002", "https://dx.doi.org/10.1371/journal.pbio.1001695.s003", "https://dx.doi.org/10.1371/journal.pbio.1001695.s004", "https://dx.doi.org/10.1371/journal.pbio.1001695.s005", "https://dx.doi.org/10.1371/journal.pbio.1001695.s006", "https://dx.doi.org/10.1371/journal.pbio.1001695.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Interaction_between_a_Sexually_Transferred_Steroid_Hormone_and_a_Female_Protein_Regulates_Oogenesis_in_the_Malaria_Mosquito_Anopheles_gambiae_/834104", "title"=>"The Interaction between a Sexually Transferred Steroid Hormone and a Female Protein Regulates Oogenesis in the Malaria Mosquito <i>Anopheles gambiae</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-10-29 02:48:59"}

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Relative Metric

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