Home LiteratureArticle Details
PMID: 10811914 Published · ppublish English Journal Article

Highly reduced protection against Streptococcus pneumoniae after deletion of a single heavy chain gene in mouse.

Mi QS, Zhou L, Schulze DH, Fischer RT, Lustig A, Rezanka LJ, Donovan DM, Longo DL, Kenny JJ

Abstract

Phosphocholine (PC) is the immunodominant epitope found on the surface of Streptococcus pneumoniae (SPn). T15-idiotype Abs, whose heavy (H) chain variable region is encoded by the V1 gene, are dominant in the anti-PC response in adult mice and protect mice from lethal pneumococcal infection. The ability of anti-PC Abs using H chains other than the V1 H chain to protect against pneumococcal infection remains controversial. We generated V1(-/-) knockout mice to determine whether protective anti-PC Abs could be produced in the absence of the V1 gene. No anti-PC Abs were produced in V1(-/-) mice immunized with avirulent SPn; however, PC-BSA binding Abs were induced after immunization with PC-keyhole limpet hemocyanin but at significantly lower levels than those in wild-type mice. These Abs provided poor protection against virulent SPn; thus, <25% of V1(-/-) mice survived challenge with 10(4) bacteria as compared with 100% survival of V1(+/+) mice. The anti-PC Abs in V1(-/-) mice were heteroclitic, binding to nitrophenyl-PC better than to PC. None of nine hybridomas produced from V1(-/-) mice provided passive protection. However, the V1(-/-) mice produced normal amounts of Ab to SPn proteins that can partially protect mice against SPn. These data indicate that the V1 gene is critical for the production of anti-PC Abs providing optimum protection against infection with SPn, and the V1(-/-) mice could be useful in unmasking epitopes other than the immunodominant PC epitope on SPn capable of providing cross protection.

MeSH Terms
Animals Antibodies, Bacterial/biosynthesis,genetics,immunology Antibodies, Monoclonal/genetics,immunology Antigens, Bacterial/immunology Bacterial Vaccines/immunology Cross Reactions Gene Deletion Genes, Immunoglobulin Hemocyanins/immunology Hybridomas/immunology Immunity, Innate/genetics Immunodominant Epitopes/immunology Immunoglobulin Heavy Chains/genetics Mice Mice, Knockout Phosphorylcholine/immunology Streptococcus pneumoniae/immunology Vaccination Virulence
Chemicals
Antibodies, Bacterial Antibodies, Monoclonal Antigens, Bacterial Bacterial Vaccines Immunodominant Epitopes Immunoglobulin Heavy Chains Phosphorylcholine Hemocyanins keyhole-limpet hemocyanin
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Mi Q S
Laboratory of Immunology, B Cell Development Section, Gerontology Research Center, National Institute on Aging, National Institutes of Health, 5600 Nathan Shock Drive, Baltimore, MD 21224, USA.
Zhou L
Schulze D H
Fischer R T
Lustig A
Rezanka L J
Donovan D M
Longo D L
Kenny J J
References (44)
44 references, click to expand
  1. Antigen-binding myeloma proteins in mice.
    Ann N Y Acad Sci. 1971 Dec 31;190:306-21 PMID: 4109640
  2. Subpopulations of antibodies to phosphocholine in human serum.
    J Immunol. 1984 Mar;132(3):1323-8 PMID: 6693768
  3. Clonal restriction of the immune response to phosphorylcholine.
    Nature. 1974 Jan 4;247(5435):55-7 PMID: 4128785
  4. The monoclonal anti-phosphorylcholine antibody response in several murine strains: genetic implications of a diverse repertoire.
    J Exp Med. 1977 Apr 1;145(4):876-91 PMID: 67172
  5. The "patchy" immunodeficiency of CBA/N mice.
    Eur J Immunol. 1977 Oct;7(10):749-51 PMID: 338312
  6. Rat anti-T15 monoclonal antibodies with specificity for VH- and VH-VL epitopes.
    Mol Immunol. 1984 Oct;21(10):961-7 PMID: 6209566
  7. Genetic control of the susceptibility to pneumococcal infection.
    Curr Top Microbiol Immunol. 1986;124:103-20 PMID: 3086036
  8. Natural and vaccine-related immunity to Streptococcus pneumoniae.
    J Infect Dis. 1986 Aug;154(2):245-56 PMID: 3722865
  9. Inefficacy of pneumococcal vaccine in a high-risk population.
    Am J Med. 1987 Sep;83(3):425-30 PMID: 3661581
  10. Inhibition of self-binding antibodies (autobodies) by a VH-derived peptide.
    Science. 1988 May 20;240(4855):1034-6 PMID: 3368787
  11. Age-dependent IgG subclass distribution of phosphocholine antibodies in humans.
    APMIS. 1988 Oct;96(10):901-5 PMID: 3190913
  12. Phosphorylcholine antibodies in pulmonary infection.
    Med Microbiol Immunol. 1990;179(4):205-14 PMID: 2263226
  13. Receptor-mediated elimination of phosphocholine-specific B cells in x-linked immune-deficient mice.
    J Immunol. 1991 Apr 15;146(8):2568-77 PMID: 1901880
  14. A mouse monoclonal antibody specific for an allotypic determinant of the Igha allele of murine IgM: genetic and functional analysis of Igh-6a epitopes using anti-IgM monoclonal antibodies.
    Hybridoma. 1991 Feb;10(1):121-35 PMID: 1709612
  15. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene.
    Cell. 1991 Jun 28;65(7):1153-63 PMID: 2065352
  16. Human anti-phosphorylcholine antibodies share idiotopes and are self-binding.
    J Clin Invest. 1991 Aug;88(2):476-82 PMID: 1864959
  17. Repertoire diversity of antibody response to bacterial antigens in aged mice. II. Phosphorylcholine-antibody in young and aged mice differ in both VH/VL gene repertoire and in specificity.
    J Immunol. 1991 Oct 15;147(8):2750-5 PMID: 1918989
  18. The protective efficacy of polyvalent pneumococcal polysaccharide vaccine.
    N Engl J Med. 1991 Nov 21;325(21):1453-60 PMID: 1944423
  19. Mouse antibody to phosphocholine can protect mice from infection with mouse-virulent human isolates of Streptococcus pneumoniae.
    Infect Immun. 1992 May;60(5):1957-62 PMID: 1563788
  20. A study of autologous anti-idiotypic antibody-forming cells in mice of different ages and genetic backgrounds.
    Cell Immunol. 1992 Oct 15;144(2):332-46 PMID: 1394446
  21. Antigen binding and idiotype analysis of antibodies obtained after electroporation of heavy and light chain genes encoding phosphocholine-specific antibodies: a model for T15-idiotype dominance.
    J Exp Med. 1992 Dec 1;176(6):1637-43 PMID: 1460422
  22. Repertoire diversity of antibody response to bacterial antigens in aged mice. III. Phosphorylcholine antibody from young and aged mice differ in structure and protective activity against infection with Streptococcus pneumoniae.
    J Immunol. 1993 Jan 15;150(2):543-9 PMID: 8419487
  23. Antibodies against pneumococcal C-polysaccharide are not protective.
    Microb Pathog. 1993 Apr;14(4):299-305 PMID: 8326853
  24. Repertoire diversity of antibody response to bacterial antigens in aged mice. IV. Study of VH and VL gene utilization in splenic antibody foci by in situ hybridization.
    J Immunol. 1994 Mar 1;152(5):2214-21 PMID: 8133035
  25. Induction of phosphocholine-specific antibodies in X-linked immune deficient mice: in vivo protection against a Streptococcus pneumoniae challenge.
    Int Immunol. 1994 Apr;6(4):561-8 PMID: 8018596
  26. A novel phosphocholine antigen protects both normal and X-linked immune deficient mice against Streptococcus pneumoniae. Comparison of the 6-O-phosphocholine hydroxyhexanoate-conjugate with other phosphocholine-containing vaccines.
    J Immunol. 1995 Apr 1;154(7):3373-82 PMID: 7897220
  27. Pathogenesis of pneumococcal infection.
    N Engl J Med. 1995 May 11;332(19):1280-4 PMID: 7708073
  28. Enhancement and destruction of antibody function by somatic mutation: unequal occurrence is controlled by V gene combinatorial associations.
    EMBO J. 1995 Jun 15;14(12):2784-94 PMID: 7796805
  29. Cross-reactive antibodies have both protective and pathogenic potential.
    J Immunol. 1995 Jul 15;155(2):967-73 PMID: 7608572
  30. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor.
    Nature. 1995 Oct 5;377(6548):435-8 PMID: 7566121
  31. Antibody protection in aging: influence of idiotypic repertoire and antibody binding activity to a bacterial antigen.
    Exp Mol Pathol. 1995 Apr;62(2):99-108 PMID: 8549700
  32. Sequence changes at the V-D junction of the VH1 heavy chain of anti-phosphocholine antibodies alter binding to and protection against Streptococcus pneumoniae.
    Int Immunol. 1997 May;9(5):665-77 PMID: 9184912
  33. Immunologic epitope, gene, and immunity involved in pneumococcal glycoconjugate.
    Crit Rev Microbiol. 1997;23(2):121-42 PMID: 9226111
  34. Impaired antibody response to pneumococcal capsular polysaccharides and phosphorylcholine in adult patients with a history of bacteremic pneumococcal infection.
    Clin Infect Dis. 1997 Sep;25(3):654-60 PMID: 9314455
  35. Age-related changes in antibody repertoire: contribution from T cells.
    Immunol Rev. 1997 Dec;160:55-62 PMID: 9476665
  36. Recent developments in bacterial conjugate vaccines.
    J Med Microbiol. 1998 Jul;47(7):563-7 PMID: 9839559
  37. Idiotype-specific neonatal suppression of phosphorylcholine-responsive B cells.
    Eur J Immunol. 1977 Dec;7(12):876-81 PMID: 75802
  38. Pneumococcal polysaccharide immunization in infants and children.
    Pediatrics. 1978 Nov;62(5):721-7 PMID: 31592
  39. Clonal nature of the immune response to phosphocholine. VII. Evidence throughout inbred mice for molecular similarities among antibodies bearing the T15 idiotype.
    J Immunol. 1980 Aug;125(2):551-8 PMID: 7391569
  40. A single VH gene segment encodes the immune response to phosphorylcholine: somatic mutation is correlated with the class of the antibody.
    Cell. 1981 Jul;25(1):59-66 PMID: 6791833
  41. Immunologic memory to phosphorylcholine. II. PC-KLH induces two antibody populations that dominate different isotypes.
    J Immunol. 1982 Feb;128(2):702-6 PMID: 7054294
  42. Protection of mice from infection with Streptococcus pneumoniae by anti-phosphocholine antibody.
    Infect Immun. 1982 Apr;36(1):184-8 PMID: 7076292
  43. Epidemiological studies of Streptococcus pneumoniae in infants: development of antibody to phosphocholine.
    J Clin Microbiol. 1983 Nov;18(5):1102-7 PMID: 6643664
  44. Specific inhibition of plaque formation to phosphorylcholine by antibody against antibody.
    Science. 1972 Jun 2;176(4038):1027-9 PMID: 4113485
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-05-23
Pages
6031-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC18553
Subset
IM
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