Home LiteratureArticle Details
PMID: 8606082 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Cell growth rate regulates expression of group B Streptococcus type III capsular polysaccharide.

Infection and immunity ·Vol. 64 ·No. 4 ·1996-04-00 ·Pages 1220-6

Paoletti LC, Ross RA, Johnson KD

Abstract

The capsular polysaccharide (CPS) of group B streptococci (GBS) is an important virulence factor that also serves to protect cells from nonspecific host defense mechanisms. Expression of CPS by GBS, as with other encapsulated bacterial pathogens, is not constitutive but varies during growth in vitro and in primary cultures isolated from different sites of infection. Despite this understanding, little is known about regulation of this surface-expressed carbohydrate antigen in GBS. Here we report that expression of type III CPS by GBS strain M781 grown in continuous culture with a modified chemically defined medium is regulated by growth rate. Cells in steady state at mass doubling times (tds) of 0.8, 1.4, and 1.6 h expressed an average of sixfold more cell-associated CPS than did cells held at tds of 2.3 and 11 h. Strain M781 grown at a td of 1.4 h repeatedly produced more type III CPS than those held at a td of 11.0 h, even when limited for glucose, pyridoxamine, or thiamine. In our studies, > or = 93% of the total CPS expressed by strain M781 was cell associated. Strain M781 grown at a td of 11.0 h (i.e., lowered CPS expression) was susceptible to in vitro complement-mediated opsonophagocytosis and killing by human peripheral blood leukocytes, whereas cells grown at a td of 1.4 h (i.e., higher CPS expression) were not killed unless type III CPS-specific antibody was present. Factors that allow GBS to asymptomatically colonize women yet cause invasive infection to both mother and infant are poorly understood. Our results shed new light on parameters that regulate the pathogenic potential of GBS and may also serve as a way to discern more fully the genetics and biochemistry of GBS capsule synthesis.

MeSH Terms
Animals Female Humans Hydrogen-Ion Concentration Phagocytosis Polysaccharides, Bacterial/biosynthesis,chemistry,immunology Rabbits Streptococcus agalactiae/growth & development,metabolism
Chemicals
Polysaccharides, Bacterial streptococcal polysaccharide type III group B
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Paoletti L C
Channing Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, 02115, USA.
Ross R A
Johnson K D
References (44)
44 references, click to expand
  1. Quantitative relationship between capsular content and killing of K1-encapsulated Escherichia coli.
    Infect Immun. 1988 Oct;56(10):2723-30 PMID: 3047064
  2. Capsular polysaccharide regulates neutrophil complement receptor interactions with type III group B streptococci.
    Infect Immun. 1993 Jul;61(7):2866-71 PMID: 8514389
  3. Lysis and protoplast formation of group B streptococci by mutanolysin.
    Infect Immun. 1980 Jun;28(3):1033-7 PMID: 6995317
  4. Properties of high and low density subpopulations of group B streptococci: enhanced virulence of the low density variant.
    Microb Pathog. 1988 Nov;5(5):345-55 PMID: 3070266
  5. Adherence of Streptococcus agalactiae to synchronously growing human cell monolayers without lipoteichoic acid involvement.
    Infect Immun. 1988 Feb;56(2):505-12 PMID: 2828238
  6. Structure of native polysaccharide antigens of type Ia and type Ib group B Streptococcus.
    Biochemistry. 1983 Mar 1;22(5):1258-64 PMID: 6838851
  7. Loss of capsule expression by Haemophilus influenzae type b results in enhanced adherence to and invasion of human cells.
    Infect Immun. 1991 Apr;59(4):1325-33 PMID: 1672302
  8. Structural determination of the capsular polysaccharide antigen of type II group B Streptococcus.
    J Biol Chem. 1983 Feb 10;258(3):1793-8 PMID: 6337145
  9. Identification of a high-virulence clone of type III Streptococcus agalactiae (group B Streptococcus) causing invasive neonatal disease.
    Proc Natl Acad Sci U S A. 1989 Jun;86(12):4731-5 PMID: 2660146
  10. Conformational aspects critical to the immunospecificity of the type III group B streptococcal polysaccharide.
    Biochemistry. 1981 Aug 4;20(16):4511-8 PMID: 6170311
  11. Immunogenicity in animals of a polysaccharide-protein conjugate vaccine against type III group B Streptococcus.
    J Clin Invest. 1990 Nov;86(5):1428-33 PMID: 2243123
  12. Adherence of isolates of Neisseria meningitidis from patients and carriers to human buccal epithelial cells.
    J Infect Dis. 1980 Oct;142(4):556-68 PMID: 6108344
  13. Role of hydrophobic surface proteins in mediating adherence of group B streptococci to epithelial cells.
    J Gen Microbiol. 1992 Jun;138(6):1237-42 PMID: 1527495
  14. Transposon mutagenesis of type III group B Streptococcus: correlation of capsule expression with virulence.
    Proc Natl Acad Sci U S A. 1987 Oct;84(20):7208-12 PMID: 2823254
  15. Definition of a bacterial virulence factor: sialylation of the group B streptococcal capsule.
    Proc Natl Acad Sci U S A. 1989 Nov;86(22):8983-7 PMID: 2554337
  16. Structural determination and immunochemical characterization of the type V group B Streptococcus capsular polysaccharide.
    J Biol Chem. 1991 Apr 15;266(11):6714-9 PMID: 2016287
  17. Weighing technique for determining bacterial dry mass based on rate of moisture uptake.
    Appl Environ Microbiol. 1983 Aug;46(2):506-8 PMID: 16346373
  18. Biosynthesis of microbial exopolysaccharides.
    Adv Microb Physiol. 1982;23:79-150 PMID: 6180610
  19. Capsular sialic acid prevents activation of the alternative complement pathway by type III, group B streptococci.
    J Immunol. 1982 Mar;128(3):1278-83 PMID: 7035562
  20. Respiratory epithelial cell invasion by group B streptococci.
    Infect Immun. 1992 Dec;60(12):5157-63 PMID: 1452349
  21. Stimulation of protective antibodies against type Ia and Ib group B streptococci by a type Ia polysaccharide-tetanus toxoid conjugate vaccine.
    Infect Immun. 1993 Nov;61(11):4760-6 PMID: 8406875
  22. Continuous culture studies on the synthesis of capsular polysaccharide by Klebsiella pneumoniae K1.
    J Appl Bacteriol. 1994 May;76(5):424-30 PMID: 8005831
  23. Molecular analysis of a region of the group B streptococcus chromosome involved in type III capsule expression.
    Infect Immun. 1989 Oct;57(10):3058-65 PMID: 2550369
  24. Growth characteristics of group A streptococci in a new chemically defined medium.
    Infect Immun. 1980 Feb;27(2):444-8 PMID: 6991416
  25. Effects of chain length on the immunogenicity in rabbits of group B Streptococcus type III oligosaccharide-tetanus toxoid conjugates.
    J Clin Invest. 1992 Jan;89(1):203-9 PMID: 1729272
  26. Structure and immunochemistry of an oligosaccharide repeating unit of the capsular polysaccharide of type III group B Streptococcus. A revised structure for the type III group B streptococcal polysaccharide antigen.
    J Biol Chem. 1987 Jun 15;262(17):8262-7 PMID: 3298228
  27. Biosynthetic capacity for type-specific antigen synthesis determines the virulence of serotype III strains of group B streptococci.
    Infect Immun. 1984 May;44(2):217-21 PMID: 6370860
  28. Establishment of exponential growth after a nutritional shift-up in Escherichia coli B/r: accumulation of deoxyribonucleic acid, ribonucleic acid, and protein.
    J Bacteriol. 1977 Feb;129(2):1020-33 PMID: 320174
  29. Structural determination and serology of the native polysaccharide antigen of type-III group B Streptococcus.
    Can J Biochem. 1980 Feb;58(2):112-20 PMID: 6155983
  30. Identification of cpsD, a gene essential for type III capsule expression in group B streptococci.
    Mol Microbiol. 1993 May;8(5):843-55 PMID: 8355611
  31. Effect of type III group B streptococcal capsular polysaccharide on invasion of respiratory epithelial cells.
    Infect Immun. 1993 Nov;61(11):4835-41 PMID: 8406885
  32. Prevention of C3 deposition by capsular polysaccharide is a virulence mechanism of type III group B streptococci.
    Infect Immun. 1992 Oct;60(10):3986-93 PMID: 1398910
  33. Group B, type III streptococcal cell wall: composition and structural aspects revealed through endo-N-acetylmuramidase-catalyzed hydrolysis.
    Infect Immun. 1982 Feb;35(2):572-81 PMID: 7035367
  34. The role of specific antibody in alternative complement pathway-mediated opsonophagocytosis of type III, group B Streptococcus.
    J Exp Med. 1980 May 1;151(5):1275-87 PMID: 6989947
  35. Epidemiology of group B streptococcal disease. Risk factors, prevention strategies, and vaccine development.
    Epidemiol Rev. 1994;16(2):374-402 PMID: 7713185
  36. Very slow growth of Escherichia coli.
    J Bacteriol. 1979 Aug;139(2):625-38 PMID: 378981
  37. Correlation between the production of extracellular substances by type III group B streptococcal strains and virulence in a mouse model.
    Infect Immun. 1981 Nov;34(2):448-54 PMID: 7030959
  38. Antigenic specificity of opsonophagocytic antibodies in rabbit anti-sera to group B streptococci.
    J Immunol. 1977 Feb;118(2):673-8 PMID: 65433
  39. Role of cellular lipoteichoic acids in mediating adherence of serotype III strains of group B streptococci to human embryonic, fetal, and adult epithelial cells.
    Infect Immun. 1984 Feb;43(2):523-30 PMID: 6363289
  40. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  41. Biosynthesis of exopolysaccharide by Pseudomonas aeruginosa.
    J Bacteriol. 1978 May;134(2):418-22 PMID: 96088
  42. Production of fimbrial adhesins K99 and F41 by enterotoxigenic Escherichia coli as a function of growth-rate domain.
    Infect Immun. 1985 Jul;49(1):159-63 PMID: 2861163
  43. Influence of growth temperature of Escherichia coli on K1 capsular antigen production and resistance to opsonization.
    Infect Immun. 1983 Mar;39(3):1136-41 PMID: 6341228
  44. Factors influencing release of type III antigens by group B streptococci.
    Infect Immun. 1981 Feb;31(2):615-23 PMID: 7012015
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1996-04-00
Pages
1220-6
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC173907
Subset
IM
Grants
NIAID NIH HHS · AI-25125 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com