Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera
Melanization, an important insect defense mechanism, is mediated by clip-domain serine protease (cSP) cascades and is regulated by serpins. Here we show that proteolytic activation of prophenoloxidase (PPO) and PO-catalyzed melanization kill the baculovirus in vitro. Our quantitative proteomics and...
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| creator | Yuan, Chuanfei Xing, Longsheng Wang, Manli Wang, Xi Yin, Mengyi Wang, Qianran Hu, Zhihong Zou, Zhen |
| description | Melanization, an important insect defense mechanism, is mediated by clip-domain serine protease (cSP) cascades and is regulated by serpins. Here we show that proteolytic activation of prophenoloxidase (PPO) and PO-catalyzed melanization kill the baculovirus in vitro. Our quantitative proteomics and biochemical experiments revealed that baculovirus infection of the cotton bollworm, Helicoverpa armigera, reduced levels of most cascade members in the host hemolymph and PO activity. By contrast, serpin-9 and serpin-5 were sequentially upregulated after the viral infection. The H. armigera serpin-5 and serpin-9 regulate melanization by directly inhibiting their target proteases cSP4 and cSP6, respectively and cSP6 activates PPO purified from hemolymph. Furthermore, serpin-5/9-depleted insects exhibited high PO activities and showed resistance to baculovirus infection. Together, our results characterize a part of the melanization cascade in H. armigera, and suggest that natural insect virus baculovirus has evolved a distinct strategy to suppress the host immune system. |
| doi_str_mv | 10.1371/journal.ppat.1006645 |
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Here we show that proteolytic activation of prophenoloxidase (PPO) and PO-catalyzed melanization kill the baculovirus in vitro. Our quantitative proteomics and biochemical experiments revealed that baculovirus infection of the cotton bollworm, Helicoverpa armigera, reduced levels of most cascade members in the host hemolymph and PO activity. By contrast, serpin-9 and serpin-5 were sequentially upregulated after the viral infection. The H. armigera serpin-5 and serpin-9 regulate melanization by directly inhibiting their target proteases cSP4 and cSP6, respectively and cSP6 activates PPO purified from hemolymph. Furthermore, serpin-5/9-depleted insects exhibited high PO activities and showed resistance to baculovirus infection. Together, our results characterize a part of the melanization cascade in H. armigera, and suggest that natural insect virus baculovirus has evolved a distinct strategy to suppress the host immune system.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1006645</identifier><identifier>PMID: 28953952</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence - genetics ; Animals ; Antibiotics ; Bacteria ; Baculoviridae ; Baculovirus ; Baculoviruses ; Biology and Life Sciences ; Biopesticides ; Cascades ; Corn earworm ; Cotton ; Funding ; Health aspects ; Helicoverpa armigera ; Hemolymph ; Hemolymph - metabolism ; Immune system ; Infection ; Infections ; Insect Proteins - metabolism ; Insects ; Laboratories ; Manduca - metabolism ; Manduca sexta ; Medicine and Health Sciences ; Melanin ; Melanization ; MicroRNAs ; Peptide Hydrolases - metabolism ; Phenols ; Prophenoloxidase ; Proteins ; Proteolysis ; Proteomics ; R&D ; Research & development ; Research and Analysis Methods ; Serine ; Serine proteinase ; Serine proteinase inhibitors ; Serpins ; Serpins - metabolism ; Software ; Viral infections ; Virology ; Viruses ; Zoology</subject><ispartof>PLoS pathogens, 2017-09, Vol.13 (9), p.e1006645-e1006645</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog13(9): e1006645. https://doi.org/10.1371/journal.ppat.1006645</rights><rights>2017 Yuan et al 2017 Yuan et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . 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Here we show that proteolytic activation of prophenoloxidase (PPO) and PO-catalyzed melanization kill the baculovirus in vitro. Our quantitative proteomics and biochemical experiments revealed that baculovirus infection of the cotton bollworm, Helicoverpa armigera, reduced levels of most cascade members in the host hemolymph and PO activity. By contrast, serpin-9 and serpin-5 were sequentially upregulated after the viral infection. The H. armigera serpin-5 and serpin-9 regulate melanization by directly inhibiting their target proteases cSP4 and cSP6, respectively and cSP6 activates PPO purified from hemolymph. Furthermore, serpin-5/9-depleted insects exhibited high PO activities and showed resistance to baculovirus infection. Together, our results characterize a part of the melanization cascade in H. armigera, and suggest that natural insect virus baculovirus has evolved a distinct strategy to suppress the host immune system.</description><subject>Amino Acid Sequence - genetics</subject><subject>Animals</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Baculoviridae</subject><subject>Baculovirus</subject><subject>Baculoviruses</subject><subject>Biology and Life Sciences</subject><subject>Biopesticides</subject><subject>Cascades</subject><subject>Corn earworm</subject><subject>Cotton</subject><subject>Funding</subject><subject>Health aspects</subject><subject>Helicoverpa armigera</subject><subject>Hemolymph</subject><subject>Hemolymph - metabolism</subject><subject>Immune system</subject><subject>Infection</subject><subject>Infections</subject><subject>Insect Proteins - metabolism</subject><subject>Insects</subject><subject>Laboratories</subject><subject>Manduca - metabolism</subject><subject>Manduca sexta</subject><subject>Medicine and Health Sciences</subject><subject>Melanin</subject><subject>Melanization</subject><subject>MicroRNAs</subject><subject>Peptide Hydrolases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yuan, Chuanfei</au><au>Xing, Longsheng</au><au>Wang, Manli</au><au>Wang, Xi</au><au>Yin, Mengyi</au><au>Wang, Qianran</au><au>Hu, Zhihong</au><au>Zou, Zhen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2017-09-01</date><risdate>2017</risdate><volume>13</volume><issue>9</issue><spage>e1006645</spage><epage>e1006645</epage><pages>e1006645-e1006645</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Melanization, an important insect defense mechanism, is mediated by clip-domain serine protease (cSP) cascades and is regulated by serpins. Here we show that proteolytic activation of prophenoloxidase (PPO) and PO-catalyzed melanization kill the baculovirus in vitro. Our quantitative proteomics and biochemical experiments revealed that baculovirus infection of the cotton bollworm, Helicoverpa armigera, reduced levels of most cascade members in the host hemolymph and PO activity. By contrast, serpin-9 and serpin-5 were sequentially upregulated after the viral infection. The H. armigera serpin-5 and serpin-9 regulate melanization by directly inhibiting their target proteases cSP4 and cSP6, respectively and cSP6 activates PPO purified from hemolymph. Furthermore, serpin-5/9-depleted insects exhibited high PO activities and showed resistance to baculovirus infection. Together, our results characterize a part of the melanization cascade in H. armigera, and suggest that natural insect virus baculovirus has evolved a distinct strategy to suppress the host immune system.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28953952</pmid><doi>10.1371/journal.ppat.1006645</doi><orcidid>https://orcid.org/0000-0003-3550-7656</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Sequence - genetics Animals Antibiotics Bacteria Baculoviridae Baculovirus Baculoviruses Biology and Life Sciences Biopesticides Cascades Corn earworm Cotton Funding Health aspects Helicoverpa armigera Hemolymph Hemolymph - metabolism Immune system Infection Infections Insect Proteins - metabolism Insects Laboratories Manduca - metabolism Manduca sexta Medicine and Health Sciences Melanin Melanization MicroRNAs Peptide Hydrolases - metabolism Phenols Prophenoloxidase Proteins Proteolysis Proteomics R&D Research & development Research and Analysis Methods Serine Serine proteinase Serine proteinase inhibitors Serpins Serpins - metabolism Software Viral infections Virology Viruses Zoology |
| title | Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera |
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