Transferrin-mediated iron sequestration suggests a novel therapeutic strategy for controlling Nosema disease in the honey bee, Apis mellifera
Nosemosis C, a Nosema disease caused by microsporidia parasite Nosema ceranae, is a significant disease burden of the European honey bee Apis mellifera which is one of the most economically important insect pollinators. Nevertheless, there is no effective treatment currently available for Nosema dis...
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| creator | Rodríguez-García, Cristina Heerman, Matthew C Cook, Steven C Evans, Jay D DeGrandi-Hoffman, Gloria Banmeke, Olubukola Zhang, Yi Huang, Shaokang Hamilton, Michele Chen, Yan Ping |
| description | Nosemosis C, a Nosema disease caused by microsporidia parasite Nosema ceranae, is a significant disease burden of the European honey bee Apis mellifera which is one of the most economically important insect pollinators. Nevertheless, there is no effective treatment currently available for Nosema disease and the disease mechanisms underlying the pathological effects of N. ceranae infection in honey bees are poorly understood. Iron is an essential nutrient for growth and survival of hosts and pathogens alike. The iron tug-of-war between host and pathogen is a central battlefield at the host-pathogen interface which determines the outcome of an infection, however, has not been explored in honey bees. To fill the gap, we conducted a study to investigate the impact of N. ceranae infection on iron homeostasis in honey bees. The expression of transferrin, an iron binding and transporting protein that is one of the key players of iron homeostasis, in response to N. ceranae infection was analysed. Furthermore, the functional roles of transferrin in iron homeostasis and honey bee host immunity were characterized using an RNA interference (RNAi)-based method. The results showed that N. ceranae infection causes iron deficiency and upregulation of the A. mellifera transferrin (AmTsf) mRNA in honey bees, implying that higher expression of AmTsf allows N. ceranae to scavenge more iron from the host for its proliferation and survival. The suppressed expression levels of AmTsf via RNAi could lead to reduced N. ceranae transcription activity, alleviated iron loss, enhanced immunity, and improved survival of the infected bees. The intriguing multifunctionality of transferrin illustrated in this study is a significant contribution to the existing body of literature concerning iron homeostasis in insects. The uncovered functional role of transferrin on iron homeostasis, pathogen growth and honey bee's ability to mount immune responses may hold the key for the development of novel strategies to treat or prevent diseases in honey bees. |
| doi_str_mv | 10.1371/journal.ppat.1009270 |
| format | Article |
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Nevertheless, there is no effective treatment currently available for Nosema disease and the disease mechanisms underlying the pathological effects of N. ceranae infection in honey bees are poorly understood. Iron is an essential nutrient for growth and survival of hosts and pathogens alike. The iron tug-of-war between host and pathogen is a central battlefield at the host-pathogen interface which determines the outcome of an infection, however, has not been explored in honey bees. To fill the gap, we conducted a study to investigate the impact of N. ceranae infection on iron homeostasis in honey bees. The expression of transferrin, an iron binding and transporting protein that is one of the key players of iron homeostasis, in response to N. ceranae infection was analysed. Furthermore, the functional roles of transferrin in iron homeostasis and honey bee host immunity were characterized using an RNA interference (RNAi)-based method. The results showed that N. ceranae infection causes iron deficiency and upregulation of the A. mellifera transferrin (AmTsf) mRNA in honey bees, implying that higher expression of AmTsf allows N. ceranae to scavenge more iron from the host for its proliferation and survival. The suppressed expression levels of AmTsf via RNAi could lead to reduced N. ceranae transcription activity, alleviated iron loss, enhanced immunity, and improved survival of the infected bees. The intriguing multifunctionality of transferrin illustrated in this study is a significant contribution to the existing body of literature concerning iron homeostasis in insects. 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Nevertheless, there is no effective treatment currently available for Nosema disease and the disease mechanisms underlying the pathological effects of N. ceranae infection in honey bees are poorly understood. Iron is an essential nutrient for growth and survival of hosts and pathogens alike. The iron tug-of-war between host and pathogen is a central battlefield at the host-pathogen interface which determines the outcome of an infection, however, has not been explored in honey bees. To fill the gap, we conducted a study to investigate the impact of N. ceranae infection on iron homeostasis in honey bees. The expression of transferrin, an iron binding and transporting protein that is one of the key players of iron homeostasis, in response to N. ceranae infection was analysed. Furthermore, the functional roles of transferrin in iron homeostasis and honey bee host immunity were characterized using an RNA interference (RNAi)-based method. The results showed that N. ceranae infection causes iron deficiency and upregulation of the A. mellifera transferrin (AmTsf) mRNA in honey bees, implying that higher expression of AmTsf allows N. ceranae to scavenge more iron from the host for its proliferation and survival. The suppressed expression levels of AmTsf via RNAi could lead to reduced N. ceranae transcription activity, alleviated iron loss, enhanced immunity, and improved survival of the infected bees. The intriguing multifunctionality of transferrin illustrated in this study is a significant contribution to the existing body of literature concerning iron homeostasis in insects. The uncovered functional role of transferrin on iron homeostasis, pathogen growth and honey bee's ability to mount immune responses may hold the key for the development of novel strategies to treat or prevent diseases in honey bees.</description><subject>Agricultural production</subject><subject>Antibiotics</subject><subject>Apis mellifera</subject><subject>Apoptosis</subject><subject>Aquatic insects</subject><subject>Bees</subject><subject>Biology and Life Sciences</subject><subject>Catalysis</subject><subject>Cell death</subject><subject>Deoxyribonucleic acid</subject><subject>Diptera</subject><subject>Disease</subject><subject>Disease control</subject><subject>DNA</subject><subject>DNA damage</subject><subject>Food contamination & poisoning</subject><subject>Free radicals</subject><subject>Fruit flies</subject><subject>Genes</subject><subject>Genomes</subject><subject>Homology</subject><subject>Honey</subject><subject>Hydroxyl 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iron sequestration suggests a novel therapeutic strategy for controlling Nosema disease in the honey bee, Apis mellifera</title><author>Rodríguez-García, Cristina ; Heerman, Matthew C ; Cook, Steven C ; Evans, Jay D ; DeGrandi-Hoffman, Gloria ; Banmeke, Olubukola ; Zhang, Yi ; Huang, Shaokang ; Hamilton, Michele ; Chen, Yan Ping</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c592t-a76419c480cc66c11a5e75a08a5c3dd18b41c8cf6cd67dfe4b433825a91c35963</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Agricultural production</topic><topic>Antibiotics</topic><topic>Apis mellifera</topic><topic>Apoptosis</topic><topic>Aquatic insects</topic><topic>Bees</topic><topic>Biology and Life Sciences</topic><topic>Catalysis</topic><topic>Cell death</topic><topic>Deoxyribonucleic acid</topic><topic>Diptera</topic><topic>Disease</topic><topic>Disease 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Nevertheless, there is no effective treatment currently available for Nosema disease and the disease mechanisms underlying the pathological effects of N. ceranae infection in honey bees are poorly understood. Iron is an essential nutrient for growth and survival of hosts and pathogens alike. The iron tug-of-war between host and pathogen is a central battlefield at the host-pathogen interface which determines the outcome of an infection, however, has not been explored in honey bees. To fill the gap, we conducted a study to investigate the impact of N. ceranae infection on iron homeostasis in honey bees. The expression of transferrin, an iron binding and transporting protein that is one of the key players of iron homeostasis, in response to N. ceranae infection was analysed. Furthermore, the functional roles of transferrin in iron homeostasis and honey bee host immunity were characterized using an RNA interference (RNAi)-based method. The results showed that N. ceranae infection causes iron deficiency and upregulation of the A. mellifera transferrin (AmTsf) mRNA in honey bees, implying that higher expression of AmTsf allows N. ceranae to scavenge more iron from the host for its proliferation and survival. The suppressed expression levels of AmTsf via RNAi could lead to reduced N. ceranae transcription activity, alleviated iron loss, enhanced immunity, and improved survival of the infected bees. The intriguing multifunctionality of transferrin illustrated in this study is a significant contribution to the existing body of literature concerning iron homeostasis in insects. The uncovered functional role of transferrin on iron homeostasis, pathogen growth and honey bee's ability to mount immune responses may hold the key for the development of novel strategies to treat or prevent diseases in honey bees.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33600478</pmid><doi>10.1371/journal.ppat.1009270</doi><orcidid>https://orcid.org/0000-0002-3078-2926</orcidid><orcidid>https://orcid.org/0000-0002-5224-1100</orcidid><orcidid>https://orcid.org/0000-0003-2156-5548</orcidid><orcidid>https://orcid.org/0000-0003-4927-1402</orcidid><orcidid>https://orcid.org/0000-0002-0036-4651</orcidid><orcidid>https://orcid.org/0000-0002-0257-2745</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Agricultural production Antibiotics Apis mellifera Apoptosis Aquatic insects Bees Biology and Life Sciences Catalysis Cell death Deoxyribonucleic acid Diptera Disease Disease control DNA DNA damage Food contamination & poisoning Free radicals Fruit flies Genes Genomes Homology Honey Hydroxyl radicals Hymenoptera Immune response Infections Innate immunity Insects Iron Lepidoptera Lipids Mammals Metabolism Mosquitoes Nosema Oxidative stress Parasites Pathogens Physiology Protein transport Proteins Redox potential Silkworms Species Toxicity Transferrin Transferrins |
| title | Transferrin-mediated iron sequestration suggests a novel therapeutic strategy for controlling Nosema disease in the honey bee, Apis mellifera |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-11T07%3A00%3A39IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Transferrin-mediated%20iron%20sequestration%20suggests%20a%20novel%20therapeutic%20strategy%20for%20controlling%20Nosema%20disease%20in%20the%20honey%20bee,%20Apis%20mellifera&rft.jtitle=PLoS%20pathogens&rft.au=Rodr%C3%ADguez-Garc%C3%ADa,%20Cristina&rft.date=2021-02-01&rft.volume=17&rft.issue=2&rft.spage=e1009270&rft.epage=e1009270&rft.pages=e1009270-e1009270&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1009270&rft_dat=%3Cproquest_plos_%3E2491952705%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2501883504&rft_id=info:pmid/33600478&rft_doaj_id=oai_doaj_org_article_bae068109b4c431fbd8a54c61f6a1fcb&rfr_iscdi=true |