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Anopheles Salivary Gland Architecture Shapes Plasmodium Sporozoite Availability for Transmission
sporozoites (SPZs) must traverse the mosquito salivary glands (SGs) to reach a new vertebrate host and continue the malaria disease cycle. Although SGs can harbor thousands of sporozoites, only 10 to 100 are deposited into a host during probing. To determine how the SGs might function as a bottlenec...
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description | sporozoites (SPZs) must traverse the mosquito salivary glands (SGs) to reach a new vertebrate host and continue the malaria disease cycle. Although SGs can harbor thousands of sporozoites, only 10 to 100 are deposited into a host during probing. To determine how the SGs might function as a bottleneck in SPZ transmission, we have characterized
SGs infected with the rodent malaria parasite
using immunofluorescence confocal microscopy. Our analyses corroborate findings from previous electron microscopy studies and provide new insights into the invasion process. We identified sites of SPZ accumulation within SGs across a range of infection intensities. Although SPZs were most often seen in the distal lateral SG lobes, they were also observed in the medial and proximal lateral lobes. Most parasites were associated with either the basement membrane or secretory cavities. SPZs accumulated at physical barriers, including fused salivary ducts and extensions of the chitinous salivary duct wall into the distal lumen. SPZs were observed only rarely within salivary ducts. SPZs appeared to contact each other in many different quantities, not just in the previously described large bundles. Within parasite bundles, all of the SPZs were oriented in the same direction. We found that moderate levels of infection did not necessarily correlate with major SG disruptions or abundant SG cell death. Altogether, our findings suggest that SG architecture largely acts as a barrier to SPZ transmission.
Malaria continues to have a devastating impact on human health. With growing resistance to insecticides and antimalarial drugs, as well as climate change predictions indicating expansion of vector territories, the impact of malaria is likely to increase. Additional insights regarding pathogen migration through vector mosquitoes are needed to develop novel methods to prevent transmission to new hosts. Pathogens, including the microbes that cause malaria, must invade the salivary glands (SGs) for transmission. Since SG traversal is required for parasite transmission, SGs are ideal targets for transmission-blocking strategies. The work presented here highlights the role that mosquito SG architecture plays in limiting parasite traversal, revealing how the SG transmission bottleneck is imposed. Further, our data provide unprecedented detail about SG-sporozoite interactions and gland-to-gland variation not provided in previous studies. |
doi_str_mv | 10.1128/mBio.01238-19 |
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SGs infected with the rodent malaria parasite
using immunofluorescence confocal microscopy. Our analyses corroborate findings from previous electron microscopy studies and provide new insights into the invasion process. We identified sites of SPZ accumulation within SGs across a range of infection intensities. Although SPZs were most often seen in the distal lateral SG lobes, they were also observed in the medial and proximal lateral lobes. Most parasites were associated with either the basement membrane or secretory cavities. SPZs accumulated at physical barriers, including fused salivary ducts and extensions of the chitinous salivary duct wall into the distal lumen. SPZs were observed only rarely within salivary ducts. SPZs appeared to contact each other in many different quantities, not just in the previously described large bundles. Within parasite bundles, all of the SPZs were oriented in the same direction. We found that moderate levels of infection did not necessarily correlate with major SG disruptions or abundant SG cell death. Altogether, our findings suggest that SG architecture largely acts as a barrier to SPZ transmission.
Malaria continues to have a devastating impact on human health. With growing resistance to insecticides and antimalarial drugs, as well as climate change predictions indicating expansion of vector territories, the impact of malaria is likely to increase. Additional insights regarding pathogen migration through vector mosquitoes are needed to develop novel methods to prevent transmission to new hosts. Pathogens, including the microbes that cause malaria, must invade the salivary glands (SGs) for transmission. Since SG traversal is required for parasite transmission, SGs are ideal targets for transmission-blocking strategies. The work presented here highlights the role that mosquito SG architecture plays in limiting parasite traversal, revealing how the SG transmission bottleneck is imposed. Further, our data provide unprecedented detail about SG-sporozoite interactions and gland-to-gland variation not provided in previous studies.</description><identifier>ISSN: 2161-2129</identifier><identifier>EISSN: 2150-7511</identifier><identifier>DOI: 10.1128/mBio.01238-19</identifier><identifier>PMID: 31387905</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Animals ; Anopheles - parasitology ; Anopheles - physiology ; Female ; Host-Microbe Biology ; Humans ; Malaria - parasitology ; Malaria - transmission ; Male ; Mice ; Mosquito Vectors - parasitology ; Mosquito Vectors - physiology ; Plasmodium berghei - growth & development ; Plasmodium berghei - physiology ; Salivary Glands - parasitology ; Sporozoites - growth & development ; Sporozoites - physiology</subject><ispartof>mBio, 2019-08, Vol.10 (4)</ispartof><rights>Copyright © 2019 Wells and Andrew.</rights><rights>Copyright © 2019 Wells and Andrew. 2019 Wells and Andrew</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c387t-3a8703e3af0047f28b02bf453452bed199e1cd2c622839fb12c935f5cbe21a5e3</citedby><cites>FETCH-LOGICAL-c387t-3a8703e3af0047f28b02bf453452bed199e1cd2c622839fb12c935f5cbe21a5e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6686039/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6686039/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31387905$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Miller, Louis H.</contributor><creatorcontrib>Wells, Michael B</creatorcontrib><creatorcontrib>Andrew, Deborah J</creatorcontrib><title>Anopheles Salivary Gland Architecture Shapes Plasmodium Sporozoite Availability for Transmission</title><title>mBio</title><addtitle>mBio</addtitle><description>sporozoites (SPZs) must traverse the mosquito salivary glands (SGs) to reach a new vertebrate host and continue the malaria disease cycle. Although SGs can harbor thousands of sporozoites, only 10 to 100 are deposited into a host during probing. To determine how the SGs might function as a bottleneck in SPZ transmission, we have characterized
SGs infected with the rodent malaria parasite
using immunofluorescence confocal microscopy. Our analyses corroborate findings from previous electron microscopy studies and provide new insights into the invasion process. We identified sites of SPZ accumulation within SGs across a range of infection intensities. Although SPZs were most often seen in the distal lateral SG lobes, they were also observed in the medial and proximal lateral lobes. Most parasites were associated with either the basement membrane or secretory cavities. SPZs accumulated at physical barriers, including fused salivary ducts and extensions of the chitinous salivary duct wall into the distal lumen. SPZs were observed only rarely within salivary ducts. SPZs appeared to contact each other in many different quantities, not just in the previously described large bundles. Within parasite bundles, all of the SPZs were oriented in the same direction. We found that moderate levels of infection did not necessarily correlate with major SG disruptions or abundant SG cell death. Altogether, our findings suggest that SG architecture largely acts as a barrier to SPZ transmission.
Malaria continues to have a devastating impact on human health. With growing resistance to insecticides and antimalarial drugs, as well as climate change predictions indicating expansion of vector territories, the impact of malaria is likely to increase. Additional insights regarding pathogen migration through vector mosquitoes are needed to develop novel methods to prevent transmission to new hosts. Pathogens, including the microbes that cause malaria, must invade the salivary glands (SGs) for transmission. Since SG traversal is required for parasite transmission, SGs are ideal targets for transmission-blocking strategies. The work presented here highlights the role that mosquito SG architecture plays in limiting parasite traversal, revealing how the SG transmission bottleneck is imposed. Further, our data provide unprecedented detail about SG-sporozoite interactions and gland-to-gland variation not provided in previous studies.</description><subject>Animals</subject><subject>Anopheles - parasitology</subject><subject>Anopheles - physiology</subject><subject>Female</subject><subject>Host-Microbe Biology</subject><subject>Humans</subject><subject>Malaria - parasitology</subject><subject>Malaria - transmission</subject><subject>Male</subject><subject>Mice</subject><subject>Mosquito Vectors - parasitology</subject><subject>Mosquito Vectors - physiology</subject><subject>Plasmodium berghei - growth & development</subject><subject>Plasmodium berghei - physiology</subject><subject>Salivary Glands - parasitology</subject><subject>Sporozoites - growth & development</subject><subject>Sporozoites - physiology</subject><issn>2161-2129</issn><issn>2150-7511</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNpVkN9LwzAQx4Mobsw9-ir9BzpzyfojL8IcOgVBYfM5pmliI2lTkm4w_3pbp0Pv5Q7ue9-7-yB0CXgGQPLr-ta4GQZC8xjYCRoTSHCcJQCnQ51CTICwEZqG8IH7oBRyis_RiALNM4aTMXpbNK6tlFUhWgtrdsLvo5UVTRktvKxMp2S39SpaV6LtJS9WhNqVZltH69Z59-l6RbTYCWNFYazp9pF2Ptp40YTahGBcc4HOtLBBTX_yBL3e322WD_HT8-pxuXiKZX9KF1ORZ5gqKjTG80yTvMCk0POEzhNSqBIYUyBLIlNCcsp0AUQymuhEFoqASBSdoJuDb7stalVK1XReWN56U_c_cScM_99pTMXf3Y6naZ5iynqD-GAgvQvBK32cBcwH2nygzb9pcxj0V38XHtW_bOkXfNF-TQ</recordid><startdate>20190806</startdate><enddate>20190806</enddate><creator>Wells, Michael B</creator><creator>Andrew, Deborah J</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope></search><sort><creationdate>20190806</creationdate><title>Anopheles Salivary Gland Architecture Shapes Plasmodium Sporozoite Availability for Transmission</title><author>Wells, Michael B ; Andrew, Deborah J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c387t-3a8703e3af0047f28b02bf453452bed199e1cd2c622839fb12c935f5cbe21a5e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Anopheles - parasitology</topic><topic>Anopheles - physiology</topic><topic>Female</topic><topic>Host-Microbe Biology</topic><topic>Humans</topic><topic>Malaria - parasitology</topic><topic>Malaria - transmission</topic><topic>Male</topic><topic>Mice</topic><topic>Mosquito Vectors - parasitology</topic><topic>Mosquito Vectors - physiology</topic><topic>Plasmodium berghei - growth & development</topic><topic>Plasmodium berghei - physiology</topic><topic>Salivary Glands - parasitology</topic><topic>Sporozoites - growth & development</topic><topic>Sporozoites - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wells, Michael B</creatorcontrib><creatorcontrib>Andrew, Deborah J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>mBio</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wells, Michael B</au><au>Andrew, Deborah J</au><au>Miller, Louis H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Anopheles Salivary Gland Architecture Shapes Plasmodium Sporozoite Availability for Transmission</atitle><jtitle>mBio</jtitle><addtitle>mBio</addtitle><date>2019-08-06</date><risdate>2019</risdate><volume>10</volume><issue>4</issue><issn>2161-2129</issn><eissn>2150-7511</eissn><abstract>sporozoites (SPZs) must traverse the mosquito salivary glands (SGs) to reach a new vertebrate host and continue the malaria disease cycle. Although SGs can harbor thousands of sporozoites, only 10 to 100 are deposited into a host during probing. To determine how the SGs might function as a bottleneck in SPZ transmission, we have characterized
SGs infected with the rodent malaria parasite
using immunofluorescence confocal microscopy. Our analyses corroborate findings from previous electron microscopy studies and provide new insights into the invasion process. We identified sites of SPZ accumulation within SGs across a range of infection intensities. Although SPZs were most often seen in the distal lateral SG lobes, they were also observed in the medial and proximal lateral lobes. Most parasites were associated with either the basement membrane or secretory cavities. SPZs accumulated at physical barriers, including fused salivary ducts and extensions of the chitinous salivary duct wall into the distal lumen. SPZs were observed only rarely within salivary ducts. SPZs appeared to contact each other in many different quantities, not just in the previously described large bundles. Within parasite bundles, all of the SPZs were oriented in the same direction. We found that moderate levels of infection did not necessarily correlate with major SG disruptions or abundant SG cell death. Altogether, our findings suggest that SG architecture largely acts as a barrier to SPZ transmission.
Malaria continues to have a devastating impact on human health. With growing resistance to insecticides and antimalarial drugs, as well as climate change predictions indicating expansion of vector territories, the impact of malaria is likely to increase. Additional insights regarding pathogen migration through vector mosquitoes are needed to develop novel methods to prevent transmission to new hosts. Pathogens, including the microbes that cause malaria, must invade the salivary glands (SGs) for transmission. Since SG traversal is required for parasite transmission, SGs are ideal targets for transmission-blocking strategies. The work presented here highlights the role that mosquito SG architecture plays in limiting parasite traversal, revealing how the SG transmission bottleneck is imposed. Further, our data provide unprecedented detail about SG-sporozoite interactions and gland-to-gland variation not provided in previous studies.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>31387905</pmid><doi>10.1128/mBio.01238-19</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Anopheles - parasitology Anopheles - physiology Female Host-Microbe Biology Humans Malaria - parasitology Malaria - transmission Male Mice Mosquito Vectors - parasitology Mosquito Vectors - physiology Plasmodium berghei - growth & development Plasmodium berghei - physiology Salivary Glands - parasitology Sporozoites - growth & development Sporozoites - physiology |
title | Anopheles Salivary Gland Architecture Shapes Plasmodium Sporozoite Availability for Transmission |
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