The Mosquito Melanization Response Is Implicated in Defense against the Entomopathogenic Fungus Beauveria bassiana
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{"title"=>"The Mosquito Melanization Response Is Implicated in Defense against the Entomopathogenic Fungus Beauveria bassiana", "type"=>"journal", "authors"=>[{"first_name"=>"Hassan", "last_name"=>"Yassine", "scopus_author_id"=>"27568248900"}, {"first_name"=>"Layla", "last_name"=>"Kamareddine", "scopus_author_id"=>"55375439700"}, {"first_name"=>"Mike A.", "last_name"=>"Osta", "scopus_author_id"=>"7801551625"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"sgr"=>"84870827106", "issn"=>"15537366", "scopus"=>"2-s2.0-84870827106", "pmid"=>"23166497", "pui"=>"366234358", "isbn"=>"1553-7366", "arxiv"=>"1003.3921v1", "doi"=>"10.1371/journal.ppat.1003029"}, "id"=>"be774581-4e5c-3425-b913-02ec8a230dc5", "abstract"=>"Mosquito immunity studies have focused mainly on characterizing immune effector mechanisms elicited against parasites, bacteria and more recently, viruses. However, those elicited against entomopathogenic fungi remain poorly understood, despite the ubiquitous nature of these microorganisms and their unique invasion route that bypasses the midgut epithelium, an important immune tissue and physical barrier. Here, we used the malaria vector Anopheles gambiae as a model to investigate the role of melanization, a potent immune effector mechanism of arthropods, in mosquito defense against the entomopathogenic fungus Beauveria bassiana, using in vivo functional genetic analysis and confocal microscopy. The temporal monitoring of fungal growth in mosquitoes injected with B. bassiana conidia showed that melanin eventually formed on all stages, including conidia, germ tubes and hyphae, except the single cell hyphal bodies. Nevertheless, melanin rarely aborted the growth of any of these stages and the mycelium continued growing despite being melanized. Silencing TEP1 and CLIPA8, key positive regulators of Plasmodium and bacterial melanization in A. gambiae, abolished completely melanin formation on hyphae but not on germinating conidia or germ tubes. The detection of a layer of hemocytes surrounding germinating conidia but not hyphae suggested that melanization of early fungal stages is cell-mediated while that of late stages is a humoral response dependent on TEP1 and CLIPA8. Microscopic analysis revealed specific association of TEP1 with surfaces of hyphae and the requirement of both, TEP1 and CLIPA8, for recruiting phenoloxidase to these surfaces. Finally, fungal proliferation was more rapid in TEP1 and CLIPA8 knockdown mosquitoes which exhibited increased sensitivity to natural B. bassiana infections than controls. In sum, the mosquito melanization response retards significantly B. bassiana growth and dissemination, a finding that may be exploited to design transgenic fungi with more potent bio-control activities against mosquitoes.", "link"=>"http://www.mendeley.com/research/mosquito-melanization-response-implicated-defense-against-entomopathogenic-fungus-beauveria-bassiana", "reader_count"=>87, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>19, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>31, "Student > Postgraduate"=>4, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>19, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>31, "Student > Postgraduate"=>4, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>13, "Agricultural and Biological Sciences"=>63, "Medicine and Dentistry"=>1, "Design"=>1, "Social Sciences"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>63}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "United Kingdom"=>2, "Malaysia"=>1, "France"=>1, "Peru"=>1, "Germany"=>2}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/542842"], "description"=>"<p><i>LacZ</i>, <i>TEP1</i> and <i>CLIPA8</i> kd adult female <i>A. gambiae</i> mosquitoes were challenged with <i>B. bassiana</i> (strain 80.2) either by (A) bringing the mosquitoes in contact with a lawn of conidia on fungal PDA plates or (B) by spraying mosquitoes with a suspension of 1×10<sup>8</sup> conidia/ml. Dead mosquitoes were counted daily over the indicated period. Graphs represent percent survival as calculated by the Kaplan-Meier method for one representative experiment of each treatment. Statistical significance was calculated by the log rank test. Survival curves were considered to be significantly different if <i>P</i><0.05. (C) <i>B. bassiana</i> infected <i>CLIPA8</i> and <i>TEP1</i> kd mosquitoes contained significantly more hyphal body colony forming units (cfu) than infected <i>LacZ</i> kd controls. Here, mosquitoes were challenged by spraying with <i>B. bassiana</i> strain 80.2 at a suspension of 5×10<sup>7</sup> conidia/ml and batches of two mosquitoes each were collected four days later, surface sterilized, grinded and serial dilutions plated on <i>B. bassiana</i> selective medium. Each circle represents mean hyphal body cfu per mosquito per batch. Medians are indicated with horizontal lines and were 0, 15 and 50 for <i>LacZ</i>, <i>CLIPA8</i> and <i>TEP1</i> kd mosquitoes, respectively. The numbers of batches (N) processed per genotype are indicated. Statistical significance was calculated using the Mann-Whitney test; medians were considered significant if <i>P</i><0.05. Results are from two independent biological experiments involving different batches of mosquitoes and fungal conidia.</p>", "links"=>[], "tags"=>["kd", "mosquitoes"], "article_id"=>213344, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g007", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CLIPA8_and_TEP1_kd_mosquitoes_are_more_sensitive_to_B_bassiana_infections_/213344", "title"=>"<i>CLIPA8</i> and <i>TEP1</i> kd mosquitoes are more sensitive to <i>B. bassiana</i> infections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:55:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/542477"], "description"=>"<p>Mosquito abdomens were dissected from (A) <i>LacZ</i>, (B) <i>CLIPA8</i> and (C) <i>TEP1</i> kd mosquitoes at 48 h post-injection of each with 200 conidia of GFP-expressing <i>B. bassiana</i> and stained with PPO6 antibody. Shown are Bright field (Bf) and fluorescence (Fl) images of confocal sections, and Z projections (Z-proj) of whole stacks. (A) An abdomen from <i>LacZ</i> kd mosquitoes at 100× magnification showed uniform PPO staining along an established hypha (Aiii, filled arrowhead) elaborating new hyphae and hyphal bodies. Note that melanin was barely detectable on this hyphal surface (Ai, open arrowhead) despite its intense PPO staining. A strong PPO signal was also observed at the branching points of the established hypha (Aii and Aiii, arrows with filled heads). The hyphal bodies detected were not labelled with PPO (Aii and Aiii, arrows with open heads). Shown also are PPO-expressing hemocytes (Aii and Aiii, open arrowheads). (B) <i>CLIPA8</i> and (C) <i>TEP1</i> kd mosquito abdomens at 40× magnification showing the absence of PPO and hence melanin from hyphal surfaces despite the extensive mycelial growth in these genotypes; melanin formation (Bi and Ci, open arrowheads) and PPO staining (Bii–iii and Cii–iii, open arrowheads) were restricted only to the base of the mycelium from which hyphae emerged. PPO6 (red), <i>B. bassiana</i>-GFP (green) and nuclei (blue). All scale bars are 50 µm.</p>", "links"=>[], "tags"=>["recruitment", "hyphae", "requires", "tep1"], "article_id"=>212973, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PPO_recruitment_to_hyphae_requires_TEP1_and_CLIPA8_/212973", "title"=>"PPO recruitment to hyphae requires TEP1 and CLIPA8.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:49:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/289679", "https://ndownloader.figshare.com/files/289712"], "description"=>"<div><p>Mosquito immunity studies have focused mainly on characterizing immune effector mechanisms elicited against parasites, bacteria and more recently, viruses. However, those elicited against entomopathogenic fungi remain poorly understood, despite the ubiquitous nature of these microorganisms and their unique invasion route that bypasses the midgut epithelium, an important immune tissue and physical barrier. Here, we used the malaria vector <em>Anopheles gambiae</em> as a model to investigate the role of melanization, a potent immune effector mechanism of arthropods, in mosquito defense against the entomopathogenic fungus <em>Beauveria bassiana</em>, using <em>in vivo</em> functional genetic analysis and confocal microscopy. The temporal monitoring of fungal growth in mosquitoes injected with <em>B. bassiana</em> conidia showed that melanin eventually formed on all stages, including conidia, germ tubes and hyphae, except the single cell hyphal bodies. Nevertheless, melanin rarely aborted the growth of any of these stages and the mycelium continued growing despite being melanized. Silencing <em>TEP1</em> and <em>CLIPA8</em>, key positive regulators of <em>Plasmodium</em> and bacterial melanization in <em>A. gambiae</em>, abolished completely melanin formation on hyphae but not on germinating conidia or germ tubes. The detection of a layer of hemocytes surrounding germinating conidia but not hyphae suggested that melanization of early fungal stages is cell-mediated while that of late stages is a humoral response dependent on TEP1 and CLIPA8. Microscopic analysis revealed specific association of TEP1 with surfaces of hyphae and the requirement of both, TEP1 and CLIPA8, for recruiting phenoloxidase to these surfaces. Finally, fungal proliferation was more rapid in <em>TEP1</em> and <em>CLIPA8</em> knockdown mosquitoes which exhibited increased sensitivity to natural <em>B. bassiana</em> infections than controls. In sum, the mosquito melanization response retards significantly <em>B. bassiana</em> growth and dissemination, a finding that may be exploited to design transgenic fungi with more potent bio-control activities against mosquitoes.</p> </div>", "links"=>[], "tags"=>["mosquito", "melanization", "implicated", "entomopathogenic", "fungus"], "article_id"=>117045, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003029.s001", "https://dx.doi.org/10.1371/journal.ppat.1003029.s002"], "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Mosquito_Melanization_Response_Is_Implicated_in_Defense_against_the_Entomopathogenic_Fungus_Beauveria_bassiana__/117045", "title"=>"The Mosquito Melanization Response Is Implicated in Defense against the Entomopathogenic Fungus <em>Beauveria bassiana</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-11-15 01:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/542708"], "description"=>"<p>(A) <i>LacZ</i> (control) and (B) <i>TEP1</i> kd mosquitoes were injected each with 200 conidia of GFP-expressing <i>B. bassiana</i>. Abdomens were dissected 48 h later and immunostained with TEP1 antibody. Shown are bright field (Bf) and merged bright field and red channel (Bf+red) confocal sections and Z projections (Z-proj) of whole stacks. (A) In control mosquitoes TEP1 staining was observed on established hyphae (Aii, filled arrowheads), young branching hyphae (Aii and Aiii, open arrowheads) and hyphal bodies (Aiii, inset and filled arrowhead). Most TEP1-stained hyphae did not exhibit melanin formation at that time point (compare Ai and Aii), except in rare cases where TEP1 signal overlapped with a thin layer of melanin (Ai and Aii, arrows with open heads). TEP1 was not detected on heavily melanized hyphal surfaces probably because it was masked by melanin (Ai and Aii, arrows with filled heads). (B) TEP1 staining of hyphae was completely abolished in <i>TEP1</i> kd mosquitoes (compare Aii with Bii, and Aiii with Biii). Consequently, melanin did not form over these hyphal surfaces but was present only on early fungal stages including germinating spores and germ tubes (Bi, open arrowheads). Note the abundance of hyphal bodies in <i>TEP1</i> kd (Biii, arrows) compared to controls. TEP1 (red) GFP-expressing <i>B. bassiana</i> (green), nuclei (blue). All scale bars are 50 µm.</p>", "links"=>[], "tags"=>["localizes", "hyphae", "hyphal"], "article_id"=>213204, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g006", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TEP1_localizes_to_hyphae_and_hyphal_bodies_/213204", "title"=>"TEP1 localizes to hyphae and hyphal bodies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:53:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/542381"], "description"=>"<p>Phenoloxidase (PO) enzymatic activity [detected as absorbance at 492 nm, OD<sub>492</sub>, after conversion of L-3,4-dihydroxyphenylalanine (L-DOPA)], was measured in hemolymph extracted from (A) <i>CLIPA8</i> and (B) <i>TEP1</i> kd mosquitoes and compared to that in <i>LacZ</i> kd controls at the indicated time points after challenging mosquitoes by spraying with a <i>B. bassiana</i> (strain 80.2) suspension containing 1×10<sup>8</sup> conidia/ml. The graphs show PO activity measured at 50 min after addition of L-DOPA. Means were calculated from two independent biological experiments performed using different batches of mosquitoes and fungal conidia. Error bars represent the standard error of the mean. Statistical analysis was performed using the Student's t-test and differences were considered to be statistically significant if <i>P</i><0.05 (indicated by an asterisk).</p>", "links"=>[], "tags"=>["kd", "abolished", "po", "triggered", "fungal"], "article_id"=>212879, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CLIPA8_and_TEP1_kd_abolished_PO_activity_triggered_during_late_but_not_early_fungal_infection_/212879", "title"=>"<i>CLIPA8</i> and <i>TEP1</i> kd abolished PO activity triggered during late but not early fungal infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:47:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/542025"], "description"=>"<p>Merged fluorescent and bright field images of abdomens dissected from mosquitoes at (A) 1 hr, (B) 6 h, (C) 12 h, (D) 24 h and (E and F) 48 h following the injection of each with 200 conidia of GFP-expressing <i>B. bassiana</i>. (A) Conidia were rapidly melanized (arrow) 1 h post-injection (pi); few non-melanized conidia were detected at that time point (arrowhead). (B) All conidia were melanized at 6 h pi. (C) An enlarged conidium germinating within the melanotic capsule (arrowhead) at 12 h pi. (D) A germ tube breaking through the melanin coat at 24 h pi (arrowhead) and another elongating with concomitant melanin formation around its wall (arrow). (E) Partially melanized hypha in a mycelium at 48 h pi showing absence of melanin at the apical part (arrowhead) and presence of a thick melanin coat around the basal part (arrow) (F) A low magnification image showing extensive melanization of hyphae (arrowheads) in the growing mycelium at 48 h pi, with few GFP-expressing, non-melanized hyphae detected (arrow). h, hour; GFP-expressing <i>B. bassiana</i> (Green). Scale bars are 10 µm in A–E and 50 µm in F.</p>", "links"=>[], "tags"=>["melanization"], "article_id"=>212522, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mosquito_melanization_response_to_B_bassiana_developmental_stages_/212522", "title"=>"Mosquito melanization response to <i>B. bassiana</i> developmental stages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:42:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/542159"], "description"=>"<p>(A) Western blot analysis showing CLIPA8 and TEP1 depletion in the hemolymph four days after silencing their corresponding genes by RNAi. <i>Left</i>, arrowhead indicates full-length TEP1 (TEP1-F) and asterisk denote the cleaved form of TEP1 (TEP1-C); <i>Right</i>, arrowhead indicates full length CLIPA8. PPO6 and SRPN3 were used as loading controls. (B) Abdomens dissected from <i>LacZ</i> kd mosquitoes at 48 h post-injection of 200 conidia of GFP-expressing <i>B. bassiana</i> (Green), show intense melanization of hyphae (arrowheads) (C and D) Absence of melanin around hyphae in <i>CLIPA8</i> and <i>TEP1</i> kd mosquitoes, respectively. Note, however, the strong melanization associated with the base of the mycelium in each of these genotypes (arrows). Scale bars are 100 µm.</p>", "links"=>[], "tags"=>["clipa8", "melanization"], "article_id"=>212655, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TEP1_and_CLIPA8_are_required_for_the_melanization_of_hyphae_/212655", "title"=>"TEP1 and CLIPA8 are required for the melanization of hyphae.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:44:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/542271"], "description"=>"<p>Abdomens were dissected at (A) 12 and (B) 48 h post-injection of each mosquito with 200 conidia of GFP-expressing <i>B. bassiana</i> and immunostained with α-PPO6 antibody. Shown are bright field (Bf), fluorescence (Fl), and merged bright field and fluorescence (Merge) images of confocal sections. (A) PPO staining of a germinating conidium. A conidium germinating despite being melanized (Ai, open arrowhead) exhibited an enlarged size compared to a nearby non-germinating spore (Ai, filled arrowhead). A cellular layer of hemocytes surrounding the germinating conidium (Aii and Aiii, arrows). These hemocytes exhibited no or faint PPO signal (Aii, open arrowhead). A hemocyte expressing PPO (Aii and Aiii, filled arrowhead) was resting on top of the cells that surrounded the germinating conidium. (B) PPO staining of hyphae. The apical parts of hyphal filaments exhibited a thin melanin coat (Bi, arrows) but strong PPO signal (Bii and Biii, arrowheads). The absence of hemocytes around these hyphae inform a humoral melanotic response. PPO6 (red), GFP-expressing <i>B. bassiana</i> (green), nuclei (blue). All scale bars are 20 µm.</p>", "links"=>[], "tags"=>["triggered", "cellular", "humoral", "melanotic", "responses"], "article_id"=>212767, "categories"=>["Microbiology"], "users"=>["Hassan Yassine", "Layla Kamareddine", "Mike A. Osta"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003029.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_B_bassiana_infection_triggered_cellular_and_humoral_melanotic_responses_in_the_mosquito_/212767", "title"=>"<i>B. bassiana</i> infection triggered cellular and humoral melanotic responses in the mosquito.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:46:07"}

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