Oxidative Reactions Catalyzed by Hydrogen Peroxide Produced by Streptococcus pneumoniae and Other Streptococci Cause the Release and Degradation of Heme from Hemoglobin
Streptococcus pneumoniae (Spn) strains cause pneumonia that kills millions every year worldwide. Spn produces Ply, a hemolysin that lyses erythrocytes releasing hemoglobin, and also produces the pro-oxidant hydrogen peroxide (Spn-H O ) during growth. The hallmark of the pathophysiology of hemolytic...
Gespeichert in:
| Veröffentlicht in: | Infection and immunity 2022-12, Vol.90 (12), p.e0047122 |
|---|---|
| Hauptverfasser: | , , , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | |
|---|---|
| container_issue | 12 |
| container_start_page | e0047122 |
| container_title | Infection and immunity |
| container_volume | 90 |
| creator | Alibayov, Babek Scasny, Anna Khan, Faidad Creel, Aidan Smith, Perriann Vidal, Ana G Jop Fitisemanu, Fa'alataitaua M Padilla-Benavides, Teresita Weiser, Jeffrey N Vidal, Jorge E |
| description | Streptococcus pneumoniae (Spn) strains cause pneumonia that kills millions every year worldwide. Spn produces Ply, a hemolysin that lyses erythrocytes releasing hemoglobin, and also produces the pro-oxidant hydrogen peroxide (Spn-H
O
) during growth. The hallmark of the pathophysiology of hemolytic diseases is the oxidation of hemoglobin, but oxidative reactions catalyzed by Spn-H
O
have been poorly studied. We characterized the oxidation of hemoglobin by Spn-H
O
. We prepared a series of single-mutant (Δ
or Δ
), double-mutant (Δ
Δ
), and complemented strains in TIGR4, D39, and EF3030. We then utilized an
model with oxyhemoglobin to demonstrate that oxyhemoglobin was oxidized rapidly, within 30 min of incubation, by Spn-H
O
to methemoglobin and that the main source of Spn-H
O
was pyruvate oxidase (SpxB). Moreover, extended incubation caused the release and the degradation of heme. We then assessed oxidation of hemoglobin and heme degradation by other bacterial inhabitants of the respiratory tract. All hydrogen peroxide-producing streptococci tested caused the oxidation of hemoglobin and heme degradation, whereas bacterial species that produce |
| doi_str_mv | 10.1128/iai.00471-22 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9753736</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2738493918</sourcerecordid><originalsourceid>FETCH-LOGICAL-a418t-c345e37a00816003e4a446ae275517eaf571d68bc7a50a012f3928393fa1841a3</originalsourceid><addsrcrecordid>eNp1kUtv1DAURi0EokNhxxp5CRIpfibOBqkaHoNUaSoea-uOczN1ldiDnVQMv4ifiYcpVVmw8uMenXvtj5DnnJ1xLswbD_6MMdXwSogHZMFZayqthXhIFozxtmp13ZyQJzlfl6NSyjwmJ7JWrOVcL8iv9Q_fweRvkH5GcJOPIdMlTDDsf2JHN3u62ncpbjHQS0yxwEgvU-xmd6x-mRLupuiic3Omu4DzGIMHpBA6up6uMN1HfFHPGWm5L-0GhHwE3-E2wWGMGGjs6QpHpH2K42EXt0Pc-PCUPOphyPjsdj0l3z68_7pcVRfrj5-W5xcVKG6mykmlUTbAmOE1YxIVKFUDikZr3iD0uuFdbTauAc2AcdHLVhjZyh64URzkKXl79O7mzYidwzAlGOwu-RHS3kbw9t9K8Fd2G29s22jZyLoIXt4KUvw-Y57s6LPDYYCAcc5WNNKoVrbcFPT1EXUp5pywv2vDmT2Ea0u49k-4VoiCvzrikEdhr-OcQvmJ_7Ev7j_jTvw3efkbypWwnA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2738493918</pqid></control><display><type>article</type><title>Oxidative Reactions Catalyzed by Hydrogen Peroxide Produced by Streptococcus pneumoniae and Other Streptococci Cause the Release and Degradation of Heme from Hemoglobin</title><source>American Society for Microbiology</source><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Alibayov, Babek ; Scasny, Anna ; Khan, Faidad ; Creel, Aidan ; Smith, Perriann ; Vidal, Ana G Jop ; Fitisemanu, Fa'alataitaua M ; Padilla-Benavides, Teresita ; Weiser, Jeffrey N ; Vidal, Jorge E</creator><contributor>Bäumler, Andreas J.</contributor><creatorcontrib>Alibayov, Babek ; Scasny, Anna ; Khan, Faidad ; Creel, Aidan ; Smith, Perriann ; Vidal, Ana G Jop ; Fitisemanu, Fa'alataitaua M ; Padilla-Benavides, Teresita ; Weiser, Jeffrey N ; Vidal, Jorge E ; Bäumler, Andreas J.</creatorcontrib><description>Streptococcus pneumoniae (Spn) strains cause pneumonia that kills millions every year worldwide. Spn produces Ply, a hemolysin that lyses erythrocytes releasing hemoglobin, and also produces the pro-oxidant hydrogen peroxide (Spn-H
O
) during growth. The hallmark of the pathophysiology of hemolytic diseases is the oxidation of hemoglobin, but oxidative reactions catalyzed by Spn-H
O
have been poorly studied. We characterized the oxidation of hemoglobin by Spn-H
O
. We prepared a series of single-mutant (Δ
or Δ
), double-mutant (Δ
Δ
), and complemented strains in TIGR4, D39, and EF3030. We then utilized an
model with oxyhemoglobin to demonstrate that oxyhemoglobin was oxidized rapidly, within 30 min of incubation, by Spn-H
O
to methemoglobin and that the main source of Spn-H
O
was pyruvate oxidase (SpxB). Moreover, extended incubation caused the release and the degradation of heme. We then assessed oxidation of hemoglobin and heme degradation by other bacterial inhabitants of the respiratory tract. All hydrogen peroxide-producing streptococci tested caused the oxidation of hemoglobin and heme degradation, whereas bacterial species that produce <1 μM H
O
neither oxidized hemoglobin nor degraded heme. An
bacteremia model confirmed that oxidation of hemoglobin and heme degradation occurred concurrently with hemoglobin that was released from erythrocytes by Ply. Finally, gene expression studies demonstrated that heme, but not red blood cells or hemoglobin, induced upregulated transcription of the
gene. Oxidation of hemoglobin may be important for pathogenesis and for the symbiosis of hydrogen peroxide-producing bacteria with other species by providing nutrients such as iron.</description><identifier>ISSN: 0019-9567</identifier><identifier>ISSN: 1098-5522</identifier><identifier>EISSN: 1098-5522</identifier><identifier>DOI: 10.1128/iai.00471-22</identifier><identifier>PMID: 36409115</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Bacteriology ; Catalysis ; Heme - metabolism ; Hemoglobins - metabolism ; Hydrogen Peroxide - pharmacology ; Molecular Pathogenesis ; Oxidation-Reduction ; Oxidative Stress ; Oxyhemoglobins - metabolism ; Streptococcus - metabolism ; Streptococcus pneumoniae - genetics ; Streptococcus pneumoniae - metabolism</subject><ispartof>Infection and immunity, 2022-12, Vol.90 (12), p.e0047122</ispartof><rights>Copyright © 2022 American Society for Microbiology.</rights><rights>Copyright © 2022 American Society for Microbiology. 2022 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a418t-c345e37a00816003e4a446ae275517eaf571d68bc7a50a012f3928393fa1841a3</citedby><cites>FETCH-LOGICAL-a418t-c345e37a00816003e4a446ae275517eaf571d68bc7a50a012f3928393fa1841a3</cites><orcidid>0000-0001-7168-8090 ; 0000-0003-0573-5658</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/iai.00471-22$$EPDF$$P50$$Gasm2$$H</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/iai.00471-22$$EHTML$$P50$$Gasm2$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3186,27922,27923,52749,52750,52751,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36409115$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bäumler, Andreas J.</contributor><creatorcontrib>Alibayov, Babek</creatorcontrib><creatorcontrib>Scasny, Anna</creatorcontrib><creatorcontrib>Khan, Faidad</creatorcontrib><creatorcontrib>Creel, Aidan</creatorcontrib><creatorcontrib>Smith, Perriann</creatorcontrib><creatorcontrib>Vidal, Ana G Jop</creatorcontrib><creatorcontrib>Fitisemanu, Fa'alataitaua M</creatorcontrib><creatorcontrib>Padilla-Benavides, Teresita</creatorcontrib><creatorcontrib>Weiser, Jeffrey N</creatorcontrib><creatorcontrib>Vidal, Jorge E</creatorcontrib><title>Oxidative Reactions Catalyzed by Hydrogen Peroxide Produced by Streptococcus pneumoniae and Other Streptococci Cause the Release and Degradation of Heme from Hemoglobin</title><title>Infection and immunity</title><addtitle>Infect Immun</addtitle><addtitle>Infect Immun</addtitle><description>Streptococcus pneumoniae (Spn) strains cause pneumonia that kills millions every year worldwide. Spn produces Ply, a hemolysin that lyses erythrocytes releasing hemoglobin, and also produces the pro-oxidant hydrogen peroxide (Spn-H
O
) during growth. The hallmark of the pathophysiology of hemolytic diseases is the oxidation of hemoglobin, but oxidative reactions catalyzed by Spn-H
O
have been poorly studied. We characterized the oxidation of hemoglobin by Spn-H
O
. We prepared a series of single-mutant (Δ
or Δ
), double-mutant (Δ
Δ
), and complemented strains in TIGR4, D39, and EF3030. We then utilized an
model with oxyhemoglobin to demonstrate that oxyhemoglobin was oxidized rapidly, within 30 min of incubation, by Spn-H
O
to methemoglobin and that the main source of Spn-H
O
was pyruvate oxidase (SpxB). Moreover, extended incubation caused the release and the degradation of heme. We then assessed oxidation of hemoglobin and heme degradation by other bacterial inhabitants of the respiratory tract. All hydrogen peroxide-producing streptococci tested caused the oxidation of hemoglobin and heme degradation, whereas bacterial species that produce <1 μM H
O
neither oxidized hemoglobin nor degraded heme. An
bacteremia model confirmed that oxidation of hemoglobin and heme degradation occurred concurrently with hemoglobin that was released from erythrocytes by Ply. Finally, gene expression studies demonstrated that heme, but not red blood cells or hemoglobin, induced upregulated transcription of the
gene. Oxidation of hemoglobin may be important for pathogenesis and for the symbiosis of hydrogen peroxide-producing bacteria with other species by providing nutrients such as iron.</description><subject>Bacteriology</subject><subject>Catalysis</subject><subject>Heme - metabolism</subject><subject>Hemoglobins - metabolism</subject><subject>Hydrogen Peroxide - pharmacology</subject><subject>Molecular Pathogenesis</subject><subject>Oxidation-Reduction</subject><subject>Oxidative Stress</subject><subject>Oxyhemoglobins - metabolism</subject><subject>Streptococcus - metabolism</subject><subject>Streptococcus pneumoniae - genetics</subject><subject>Streptococcus pneumoniae - metabolism</subject><issn>0019-9567</issn><issn>1098-5522</issn><issn>1098-5522</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUtv1DAURi0EokNhxxp5CRIpfibOBqkaHoNUaSoea-uOczN1ldiDnVQMv4ifiYcpVVmw8uMenXvtj5DnnJ1xLswbD_6MMdXwSogHZMFZayqthXhIFozxtmp13ZyQJzlfl6NSyjwmJ7JWrOVcL8iv9Q_fweRvkH5GcJOPIdMlTDDsf2JHN3u62ncpbjHQS0yxwEgvU-xmd6x-mRLupuiic3Omu4DzGIMHpBA6up6uMN1HfFHPGWm5L-0GhHwE3-E2wWGMGGjs6QpHpH2K42EXt0Pc-PCUPOphyPjsdj0l3z68_7pcVRfrj5-W5xcVKG6mykmlUTbAmOE1YxIVKFUDikZr3iD0uuFdbTauAc2AcdHLVhjZyh64URzkKXl79O7mzYidwzAlGOwu-RHS3kbw9t9K8Fd2G29s22jZyLoIXt4KUvw-Y57s6LPDYYCAcc5WNNKoVrbcFPT1EXUp5pywv2vDmT2Ea0u49k-4VoiCvzrikEdhr-OcQvmJ_7Ev7j_jTvw3efkbypWwnA</recordid><startdate>20221215</startdate><enddate>20221215</enddate><creator>Alibayov, Babek</creator><creator>Scasny, Anna</creator><creator>Khan, Faidad</creator><creator>Creel, Aidan</creator><creator>Smith, Perriann</creator><creator>Vidal, Ana G Jop</creator><creator>Fitisemanu, Fa'alataitaua M</creator><creator>Padilla-Benavides, Teresita</creator><creator>Weiser, Jeffrey N</creator><creator>Vidal, Jorge E</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7168-8090</orcidid><orcidid>https://orcid.org/0000-0003-0573-5658</orcidid></search><sort><creationdate>20221215</creationdate><title>Oxidative Reactions Catalyzed by Hydrogen Peroxide Produced by Streptococcus pneumoniae and Other Streptococci Cause the Release and Degradation of Heme from Hemoglobin</title><author>Alibayov, Babek ; Scasny, Anna ; Khan, Faidad ; Creel, Aidan ; Smith, Perriann ; Vidal, Ana G Jop ; Fitisemanu, Fa'alataitaua M ; Padilla-Benavides, Teresita ; Weiser, Jeffrey N ; Vidal, Jorge E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a418t-c345e37a00816003e4a446ae275517eaf571d68bc7a50a012f3928393fa1841a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Bacteriology</topic><topic>Catalysis</topic><topic>Heme - metabolism</topic><topic>Hemoglobins - metabolism</topic><topic>Hydrogen Peroxide - pharmacology</topic><topic>Molecular Pathogenesis</topic><topic>Oxidation-Reduction</topic><topic>Oxidative Stress</topic><topic>Oxyhemoglobins - metabolism</topic><topic>Streptococcus - metabolism</topic><topic>Streptococcus pneumoniae - genetics</topic><topic>Streptococcus pneumoniae - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Alibayov, Babek</creatorcontrib><creatorcontrib>Scasny, Anna</creatorcontrib><creatorcontrib>Khan, Faidad</creatorcontrib><creatorcontrib>Creel, Aidan</creatorcontrib><creatorcontrib>Smith, Perriann</creatorcontrib><creatorcontrib>Vidal, Ana G Jop</creatorcontrib><creatorcontrib>Fitisemanu, Fa'alataitaua M</creatorcontrib><creatorcontrib>Padilla-Benavides, Teresita</creatorcontrib><creatorcontrib>Weiser, Jeffrey N</creatorcontrib><creatorcontrib>Vidal, Jorge E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Infection and immunity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Alibayov, Babek</au><au>Scasny, Anna</au><au>Khan, Faidad</au><au>Creel, Aidan</au><au>Smith, Perriann</au><au>Vidal, Ana G Jop</au><au>Fitisemanu, Fa'alataitaua M</au><au>Padilla-Benavides, Teresita</au><au>Weiser, Jeffrey N</au><au>Vidal, Jorge E</au><au>Bäumler, Andreas J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oxidative Reactions Catalyzed by Hydrogen Peroxide Produced by Streptococcus pneumoniae and Other Streptococci Cause the Release and Degradation of Heme from Hemoglobin</atitle><jtitle>Infection and immunity</jtitle><stitle>Infect Immun</stitle><addtitle>Infect Immun</addtitle><date>2022-12-15</date><risdate>2022</risdate><volume>90</volume><issue>12</issue><spage>e0047122</spage><pages>e0047122-</pages><issn>0019-9567</issn><issn>1098-5522</issn><eissn>1098-5522</eissn><abstract>Streptococcus pneumoniae (Spn) strains cause pneumonia that kills millions every year worldwide. Spn produces Ply, a hemolysin that lyses erythrocytes releasing hemoglobin, and also produces the pro-oxidant hydrogen peroxide (Spn-H
O
) during growth. The hallmark of the pathophysiology of hemolytic diseases is the oxidation of hemoglobin, but oxidative reactions catalyzed by Spn-H
O
have been poorly studied. We characterized the oxidation of hemoglobin by Spn-H
O
. We prepared a series of single-mutant (Δ
or Δ
), double-mutant (Δ
Δ
), and complemented strains in TIGR4, D39, and EF3030. We then utilized an
model with oxyhemoglobin to demonstrate that oxyhemoglobin was oxidized rapidly, within 30 min of incubation, by Spn-H
O
to methemoglobin and that the main source of Spn-H
O
was pyruvate oxidase (SpxB). Moreover, extended incubation caused the release and the degradation of heme. We then assessed oxidation of hemoglobin and heme degradation by other bacterial inhabitants of the respiratory tract. All hydrogen peroxide-producing streptococci tested caused the oxidation of hemoglobin and heme degradation, whereas bacterial species that produce <1 μM H
O
neither oxidized hemoglobin nor degraded heme. An
bacteremia model confirmed that oxidation of hemoglobin and heme degradation occurred concurrently with hemoglobin that was released from erythrocytes by Ply. Finally, gene expression studies demonstrated that heme, but not red blood cells or hemoglobin, induced upregulated transcription of the
gene. Oxidation of hemoglobin may be important for pathogenesis and for the symbiosis of hydrogen peroxide-producing bacteria with other species by providing nutrients such as iron.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>36409115</pmid><doi>10.1128/iai.00471-22</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-7168-8090</orcidid><orcidid>https://orcid.org/0000-0003-0573-5658</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0019-9567 |
| ispartof | Infection and immunity, 2022-12, Vol.90 (12), p.e0047122 |
| issn | 0019-9567 1098-5522 1098-5522 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9753736 |
| source | American Society for Microbiology; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Bacteriology Catalysis Heme - metabolism Hemoglobins - metabolism Hydrogen Peroxide - pharmacology Molecular Pathogenesis Oxidation-Reduction Oxidative Stress Oxyhemoglobins - metabolism Streptococcus - metabolism Streptococcus pneumoniae - genetics Streptococcus pneumoniae - metabolism |
| title | Oxidative Reactions Catalyzed by Hydrogen Peroxide Produced by Streptococcus pneumoniae and Other Streptococci Cause the Release and Degradation of Heme from Hemoglobin |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-09T15%3A02%3A48IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Oxidative%20Reactions%20Catalyzed%20by%20Hydrogen%20Peroxide%20Produced%20by%20Streptococcus%20pneumoniae%20and%20Other%20Streptococci%20Cause%20the%20Release%20and%20Degradation%20of%20Heme%20from%20Hemoglobin&rft.jtitle=Infection%20and%20immunity&rft.au=Alibayov,%20Babek&rft.date=2022-12-15&rft.volume=90&rft.issue=12&rft.spage=e0047122&rft.pages=e0047122-&rft.issn=0019-9567&rft.eissn=1098-5522&rft_id=info:doi/10.1128/iai.00471-22&rft_dat=%3Cproquest_pubme%3E2738493918%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2738493918&rft_id=info:pmid/36409115&rfr_iscdi=true |