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Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae
Streptococcus pneumoniae undergoes spontaneous phase variation between a transparent and an opaque colony phenotype, the latter being more virulent in a murine model of sepsis. Opaque pneumococci have previously been shown to express lower amounts of C polysaccharide (cell wall teichoic acid) and in...
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Published in: | Infection and immunity 1999-05, Vol.67 (5), p.2327-2333 |
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description | Streptococcus pneumoniae undergoes spontaneous phase variation between a transparent and an opaque colony phenotype, the latter being more virulent in a murine model of sepsis. Opaque pneumococci have previously been shown to express lower amounts of C polysaccharide (cell wall teichoic acid) and in this study were shown to have a higher content of capsular polysaccharide by immunoelectron microscopy. This report then examined the relationship between expression of these two cell surface carbohydrate structures and their relative contribution to the increased virulence of opaque variants. Comparison of genetically related strains showed that the differential content of capsular polysaccharide did not affect the amount of teichoic acid as measured by a capture enzyme-linked immunosorbent assay (ELISA). In contrast, when the teichoic acid structure was altered by replacing choline in the growth medium with structural analogs, the quantity of capsular polysaccharide as measured by a capture ELISA was decreased, demonstrating a linkage in the expression of the two surface carbohydrate structures. A standardized assay was used to assess the relative contribution of cell surface carbohydrates to opsonophagocytosis. The opaque variants required 1.2- to 30-fold more immune human serum to achieve 50% opsonophagocytic killing than did related transparent variants (types 6B and 9V). The opsonophagocytic titer was proportional to the quantity of capsular polysaccharide rather than teichoic acid. The major factor in binding of the opsonin, C-reactive protein (CRP), was also the amount of capsular polysaccharide rather than the teichoic acid ligand. Only for the transparent variant (type 6B), which bound more CRP, was there enhanced opsonophagocytic killing in the presence of this serum protein. Increased expression of capsular polysaccharide, therefore, appeared to be the major factor in the decreased opsonophagocytic killing of opaque pneumococci. |
doi_str_mv | 10.1128/IAI.67.5.2327-2333.1999 |
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O ; ROMERO-STEINER, S ; SØRENSEN, U. B. S ; BLOM, J ; CARVALHO, M ; BARNARD, S ; CARLONE, G ; WEISER, J. N</creator><contributor>Tuomanen, E. I.</contributor><creatorcontrib>KIM, J. O ; ROMERO-STEINER, S ; SØRENSEN, U. B. S ; BLOM, J ; CARVALHO, M ; BARNARD, S ; CARLONE, G ; WEISER, J. N ; Tuomanen, E. I.</creatorcontrib><description>Streptococcus pneumoniae undergoes spontaneous phase variation between a transparent and an opaque colony phenotype, the latter being more virulent in a murine model of sepsis. Opaque pneumococci have previously been shown to express lower amounts of C polysaccharide (cell wall teichoic acid) and in this study were shown to have a higher content of capsular polysaccharide by immunoelectron microscopy. This report then examined the relationship between expression of these two cell surface carbohydrate structures and their relative contribution to the increased virulence of opaque variants. Comparison of genetically related strains showed that the differential content of capsular polysaccharide did not affect the amount of teichoic acid as measured by a capture enzyme-linked immunosorbent assay (ELISA). In contrast, when the teichoic acid structure was altered by replacing choline in the growth medium with structural analogs, the quantity of capsular polysaccharide as measured by a capture ELISA was decreased, demonstrating a linkage in the expression of the two surface carbohydrate structures. A standardized assay was used to assess the relative contribution of cell surface carbohydrates to opsonophagocytosis. The opaque variants required 1.2- to 30-fold more immune human serum to achieve 50% opsonophagocytic killing than did related transparent variants (types 6B and 9V). The opsonophagocytic titer was proportional to the quantity of capsular polysaccharide rather than teichoic acid. The major factor in binding of the opsonin, C-reactive protein (CRP), was also the amount of capsular polysaccharide rather than the teichoic acid ligand. Only for the transparent variant (type 6B), which bound more CRP, was there enhanced opsonophagocytic killing in the presence of this serum protein. Increased expression of capsular polysaccharide, therefore, appeared to be the major factor in the decreased opsonophagocytic killing of opaque pneumococci.</description><identifier>ISSN: 0019-9567</identifier><identifier>EISSN: 1098-5522</identifier><identifier>DOI: 10.1128/IAI.67.5.2327-2333.1999</identifier><identifier>PMID: 10225891</identifier><identifier>CODEN: INFIBR</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>Animals ; Antibodies, Bacterial ; Bacteriology ; Biological and medical sciences ; C-Reactive Protein - metabolism ; Carbohydrates - immunology ; Cell Membrane - immunology ; Fundamental and applied biological sciences. Psychology ; Genetic Variation ; HL-60 Cells ; Humans ; Mice ; Microbiology ; Microscopy, Immunoelectron ; Molecular and Cellular Pathogenesis ; Opsonin Proteins ; Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains ; Phagocytosis ; Phenotype ; Polysaccharides, Bacterial - immunology ; Streptococcus pneumoniae - immunology ; Streptococcus pneumoniae - pathogenicity ; Streptococcus pneumoniae - ultrastructure ; Teichoic Acids - immunology ; Virulence - immunology</subject><ispartof>Infection and immunity, 1999-05, Vol.67 (5), p.2327-2333</ispartof><rights>1999 INIST-CNRS</rights><rights>Copyright © 1999, American Society for Microbiology 1999</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c446t-918d4c820ddfb0e7060e6fc56ac0e306f34a81c93e8c86ade7a4737f69be0b5d3</citedby><cites>FETCH-LOGICAL-c446t-918d4c820ddfb0e7060e6fc56ac0e306f34a81c93e8c86ade7a4737f69be0b5d3</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/PMC115974/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC115974/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=1802295$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10225891$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Tuomanen, E. I.</contributor><creatorcontrib>KIM, J. O</creatorcontrib><creatorcontrib>ROMERO-STEINER, S</creatorcontrib><creatorcontrib>SØRENSEN, U. B. S</creatorcontrib><creatorcontrib>BLOM, J</creatorcontrib><creatorcontrib>CARVALHO, M</creatorcontrib><creatorcontrib>BARNARD, S</creatorcontrib><creatorcontrib>CARLONE, G</creatorcontrib><creatorcontrib>WEISER, J. N</creatorcontrib><title>Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae</title><title>Infection and immunity</title><addtitle>Infect Immun</addtitle><description>Streptococcus pneumoniae undergoes spontaneous phase variation between a transparent and an opaque colony phenotype, the latter being more virulent in a murine model of sepsis. Opaque pneumococci have previously been shown to express lower amounts of C polysaccharide (cell wall teichoic acid) and in this study were shown to have a higher content of capsular polysaccharide by immunoelectron microscopy. This report then examined the relationship between expression of these two cell surface carbohydrate structures and their relative contribution to the increased virulence of opaque variants. Comparison of genetically related strains showed that the differential content of capsular polysaccharide did not affect the amount of teichoic acid as measured by a capture enzyme-linked immunosorbent assay (ELISA). In contrast, when the teichoic acid structure was altered by replacing choline in the growth medium with structural analogs, the quantity of capsular polysaccharide as measured by a capture ELISA was decreased, demonstrating a linkage in the expression of the two surface carbohydrate structures. A standardized assay was used to assess the relative contribution of cell surface carbohydrates to opsonophagocytosis. The opaque variants required 1.2- to 30-fold more immune human serum to achieve 50% opsonophagocytic killing than did related transparent variants (types 6B and 9V). The opsonophagocytic titer was proportional to the quantity of capsular polysaccharide rather than teichoic acid. The major factor in binding of the opsonin, C-reactive protein (CRP), was also the amount of capsular polysaccharide rather than the teichoic acid ligand. Only for the transparent variant (type 6B), which bound more CRP, was there enhanced opsonophagocytic killing in the presence of this serum protein. Increased expression of capsular polysaccharide, therefore, appeared to be the major factor in the decreased opsonophagocytic killing of opaque pneumococci.</description><subject>Animals</subject><subject>Antibodies, Bacterial</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>C-Reactive Protein - metabolism</subject><subject>Carbohydrates - immunology</subject><subject>Cell Membrane - immunology</subject><subject>Fundamental and applied biological sciences. 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S</creatorcontrib><creatorcontrib>BLOM, J</creatorcontrib><creatorcontrib>CARVALHO, M</creatorcontrib><creatorcontrib>BARNARD, S</creatorcontrib><creatorcontrib>CARLONE, G</creatorcontrib><creatorcontrib>WEISER, J. N</creatorcontrib><collection>Pascal-Francis</collection><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>KIM, J. O</au><au>ROMERO-STEINER, S</au><au>SØRENSEN, U. B. S</au><au>BLOM, J</au><au>CARVALHO, M</au><au>BARNARD, S</au><au>CARLONE, G</au><au>WEISER, J. N</au><au>Tuomanen, E. I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae</atitle><jtitle>Infection and immunity</jtitle><addtitle>Infect Immun</addtitle><date>1999-05-01</date><risdate>1999</risdate><volume>67</volume><issue>5</issue><spage>2327</spage><epage>2333</epage><pages>2327-2333</pages><issn>0019-9567</issn><eissn>1098-5522</eissn><coden>INFIBR</coden><abstract>Streptococcus pneumoniae undergoes spontaneous phase variation between a transparent and an opaque colony phenotype, the latter being more virulent in a murine model of sepsis. Opaque pneumococci have previously been shown to express lower amounts of C polysaccharide (cell wall teichoic acid) and in this study were shown to have a higher content of capsular polysaccharide by immunoelectron microscopy. This report then examined the relationship between expression of these two cell surface carbohydrate structures and their relative contribution to the increased virulence of opaque variants. Comparison of genetically related strains showed that the differential content of capsular polysaccharide did not affect the amount of teichoic acid as measured by a capture enzyme-linked immunosorbent assay (ELISA). In contrast, when the teichoic acid structure was altered by replacing choline in the growth medium with structural analogs, the quantity of capsular polysaccharide as measured by a capture ELISA was decreased, demonstrating a linkage in the expression of the two surface carbohydrate structures. A standardized assay was used to assess the relative contribution of cell surface carbohydrates to opsonophagocytosis. The opaque variants required 1.2- to 30-fold more immune human serum to achieve 50% opsonophagocytic killing than did related transparent variants (types 6B and 9V). The opsonophagocytic titer was proportional to the quantity of capsular polysaccharide rather than teichoic acid. The major factor in binding of the opsonin, C-reactive protein (CRP), was also the amount of capsular polysaccharide rather than the teichoic acid ligand. Only for the transparent variant (type 6B), which bound more CRP, was there enhanced opsonophagocytic killing in the presence of this serum protein. Increased expression of capsular polysaccharide, therefore, appeared to be the major factor in the decreased opsonophagocytic killing of opaque pneumococci.</abstract><cop>Washington, DC</cop><pub>American Society for Microbiology</pub><pmid>10225891</pmid><doi>10.1128/IAI.67.5.2327-2333.1999</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Antibodies, Bacterial Bacteriology Biological and medical sciences C-Reactive Protein - metabolism Carbohydrates - immunology Cell Membrane - immunology Fundamental and applied biological sciences. Psychology Genetic Variation HL-60 Cells Humans Mice Microbiology Microscopy, Immunoelectron Molecular and Cellular Pathogenesis Opsonin Proteins Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains Phagocytosis Phenotype Polysaccharides, Bacterial - immunology Streptococcus pneumoniae - immunology Streptococcus pneumoniae - pathogenicity Streptococcus pneumoniae - ultrastructure Teichoic Acids - immunology Virulence - immunology |
title | Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae |
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