Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1996 Nov;64(11):4694–4699. doi: 10.1128/iai.64.11.4694-4699.1996

No apparent influence of immunoglobulins on indigenous oral and intestinal microbiota of mice.

H Marcotte 1, M C Lavoie 1
PMCID: PMC174433  PMID: 8890227

Abstract

The role of secretory immunoglobulin A (sIgA) in the control of the indigenous microbiota is not well understood. In this study, we compared the oral and intestinal microbiota of transgenic B-cell-deficient (microMT) mice with their heterozygous (microMT/+) normal littermates. The levels of salivary IgA and serum IgA and IgG were normal in microMT/+ mice, while no immunoglobulins were detected in microMT/microMT mice. The acquisition and proportions of the different species of the oral and intestinal indigenous bacterial populations were not significantly different between the two groups of mice. Our results thus suggest that secretory IgA does not play a major role in the regulation of the indigenous microbiota of mice.

Full Text

The Full Text of this article is available as a PDF (409.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albanese C. T., Smith S. D., Watkins S., Kurkchubasche A., Simmons R. L., Rowe M. I. Effect of secretory IgA on transepithelial passage of bacteria across the intact ileum in vitro. J Am Coll Surg. 1994 Dec;179(6):679–688. [PubMed] [Google Scholar]
  2. Arnold R. R., Cole M. F., Prince S., McGhee J. R. Secretory IgM antibodies to Streptococcus mutans in subjects with selective IgA deficiency. Clin Immunol Immunopathol. 1977 Nov;8(3):475–486. doi: 10.1016/0090-1229(77)90011-3. [DOI] [PubMed] [Google Scholar]
  3. Berg R. D. Mechanisms confining indigenous bacteria to the gastrointestinal tract. Am J Clin Nutr. 1980 Nov;33(11 Suppl):2472–2484. doi: 10.1093/ajcn/33.11.2472. [DOI] [PubMed] [Google Scholar]
  4. Berg R. D., Savage D. C. Immune responses of specific pathogen-free and gnotobiotic mice to antigens of indigenous and nonindigenous microorganisms. Infect Immun. 1975 Feb;11(2):320–329. doi: 10.1128/iai.11.2.320-329.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brandtzaeg P., Fjellanger I., Gjeruldsen S. T. Adsorption of immunolgobulin A onto oral bacteria in vivo. J Bacteriol. 1968 Jul;96(1):242–249. doi: 10.1128/jb.96.1.242-249.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brandtzaeg P. Molecular and cellular aspects of the secretory immunoglobulin system. APMIS. 1995 Jan;103(1):1–19. doi: 10.1111/j.1699-0463.1995.tb01073.x. [DOI] [PubMed] [Google Scholar]
  7. Bratthall D., Gibbons R. J. Changing agglutination activities of salivary immunoglobulin A preparations against oral streptococci. Infect Immun. 1975 Mar;11(3):603–606. doi: 10.1128/iai.11.3.603-606.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown L. R., Mackler B. F., Levy B. M., Wright T. E., Handler S. F., Moylan J. S., Perkins D. H., Keene H. J. Comparison of the plaque microflora in immunodeficient and immunocompetent dental patients. J Dent Res. 1979 Dec;58(12):2344–2352. doi: 10.1177/00220345790580120301. [DOI] [PubMed] [Google Scholar]
  9. Brown W. R., Savage D. C., Dubois R. S., Alp M. H., Mallory A., Kern F., Jr Intestinal microflora of immunoglobulin-deficient and normal human subjects. Gastroenterology. 1972 Jun;62(6):1143–1152. [PubMed] [Google Scholar]
  10. Cole M. F., Arnold R. R., Rhodes M. J., McGhee J. R. Immune dysfunction and dental caries: a preliminary report. J Dent Res. 1977 Mar;56(3):198–204. doi: 10.1177/00220345770560030201. [DOI] [PubMed] [Google Scholar]
  11. DUBOS R., SCHAEDLER R. W., COSTELLO R., HOET P. INDIGENOUS, NORMAL, AND AUTOCHTHONOUS FLORA OF THE GASTROINTESTINAL TRACT. J Exp Med. 1965 Jul 1;122:67–76. doi: 10.1084/jem.122.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Davis C. P., McAllister J. S., Savage D. C. Microbial colonization of the intestinal epithelium in suckling mice. Infect Immun. 1973 Apr;7(4):666–672. doi: 10.1128/iai.7.4.666-672.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Deslauriers N., Seguin J., Trudel L. Differential recognition of oral indigenous bacteria by salivary immunoglobulins A and G. Microbiol Immunol. 1987;31(3):199–209. doi: 10.1111/j.1348-0421.1987.tb03084.x. [DOI] [PubMed] [Google Scholar]
  14. Duchmann R., Kaiser I., Hermann E., Mayet W., Ewe K., Meyer zum Büschenfelde K. H. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD) Clin Exp Immunol. 1995 Dec;102(3):448–455. doi: 10.1111/j.1365-2249.1995.tb03836.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Freter R., Stauffer E., Cleven D., Holdeman L. V., Moore W. E. Continuous-flow cultures as in vitro models of the ecology of large intestinal flora. Infect Immun. 1983 Feb;39(2):666–675. doi: 10.1128/iai.39.2.666-675.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gleeson M., Cripps A. W., Clancy R. L., Hensley M. J., Dobson A. J., Firman D. W. Breast feeding conditions a differential developmental pattern of mucosal immunity. Clin Exp Immunol. 1986 Oct;66(1):216–222. [PMC free article] [PubMed] [Google Scholar]
  17. Hanson L. A., Ahlstedt S., Andersson B., Carlsson B., Fällström S. P., Mellander L., Porras O., Söderström T., Edén C. S. Protective factors in milk and the development of the immune system. Pediatrics. 1985 Jan;75(1 Pt 2):172–176. [PubMed] [Google Scholar]
  18. Harris M. A., Reddy C. A., Carter G. R. Anaerobic bacteria from the large intestine of mice. Appl Environ Microbiol. 1976 Jun;31(6):907–912. doi: 10.1128/aem.31.6.907-912.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hersh T., Floch M. H., Binder H. J., Conn H. O., Prizont R., Spiro H. M. Disturbance of the jejunal and colonic bacterial flora in immunoglobulin deficiencies. Am J Clin Nutr. 1970 Dec;23(12):1595–1601. doi: 10.1093/ajcn/23.12.1595. [DOI] [PubMed] [Google Scholar]
  20. Hohwy J., Kilian M. Clonal diversity of the Streptococcus mitis biovar 1 population in the human oral cavity and pharynx. Oral Microbiol Immunol. 1995 Feb;10(1):19–25. doi: 10.1111/j.1399-302x.1995.tb00113.x. [DOI] [PubMed] [Google Scholar]
  21. Kitamura D., Roes J., Kühn R., Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 1991 Apr 4;350(6317):423–426. doi: 10.1038/350423a0. [DOI] [PubMed] [Google Scholar]
  22. Kramer D. R., Cebra J. J. Early appearance of "natural" mucosal IgA responses and germinal centers in suckling mice developing in the absence of maternal antibodies. J Immunol. 1995 Mar 1;154(5):2051–2062. [PubMed] [Google Scholar]
  23. Lee S. F. Active release of bound antibody by Streptococcus mutans. Infect Immun. 1995 May;63(5):1940–1946. doi: 10.1128/iai.63.5.1940-1946.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Legler D. W., McGhee J. R., Lynch D. P., Mestecky J. F., Schaefer M. E., Carson J., Bradley E. L., Jr Immunodeficiency disease and dental caries in man. Arch Oral Biol. 1981;26(11):905–910. doi: 10.1016/0003-9969(81)90150-3. [DOI] [PubMed] [Google Scholar]
  25. Loesche W. J., Hockett R. N., Syed S. A. The predominant cultivable flora of tooth surface plaque removed from institutionalized subjects. Arch Oral Biol. 1972 Sep;17(9):1311–1325. doi: 10.1016/0003-9969(72)90164-1. [DOI] [PubMed] [Google Scholar]
  26. Lopatin D. E., Blackburn E. Avidity and titer of immunoglobulin G subclasses to Porphyromonas gingivalis in adult periodontitis patients. Oral Microbiol Immunol. 1992 Dec;7(6):332–337. doi: 10.1111/j.1399-302x.1992.tb00632.x. [DOI] [PubMed] [Google Scholar]
  27. MacDonald T. T. Breakdown of tolerance to the intestinal bacterial flora in inflammatory bowel disease (IBD) Clin Exp Immunol. 1995 Dec;102(3):445–447. doi: 10.1111/j.1365-2249.1995.tb03835.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Marcotte H., Lavoie M. C. Evaluation of mouse salivary IgA directed against indigenous oral bacteria. J Immunoassay. 1993 Mar-Jun;14(1-2):63–81. doi: 10.1080/15321819308019841. [DOI] [PubMed] [Google Scholar]
  29. Marcotte H., Levesque D., Delanay K., Bourgeault A., de la Durantaye R., Brochu S., Lavoie M. C. Pneumocystis carinii infection in transgenic B cell-deficient mice. J Infect Dis. 1996 Apr;173(4):1034–1037. doi: 10.1093/infdis/173.4.1034. [DOI] [PubMed] [Google Scholar]
  30. Marcotte H., Rodrigue L., Coulombe C., Goyette N., Lavoie M. C. Colonization of the oral cavity of mice by an unidentified streptococcus. Oral Microbiol Immunol. 1995 Jun;10(3):168–174. doi: 10.1111/j.1399-302x.1995.tb00138.x. [DOI] [PubMed] [Google Scholar]
  31. Marcotte H., Rodrigue L., Gamache M., Lavoie M. C. Immunization against the oral indigenous bacteria of the BALB/c mouse. Adv Exp Med Biol. 1995;371B:1173–1176. [PubMed] [Google Scholar]
  32. McLoughlin G. A., Hede J. E., Temple J. G., Bradley J., Chapman D. M., McFarland J. The role of IgA in the prevention of bacterial colonization of the jejunum in the vagotomized subject. Br J Surg. 1978 Jun;65(6):435–437. doi: 10.1002/bjs.1800650619. [DOI] [PubMed] [Google Scholar]
  33. Michalek S. M., Childers N. K. Development and outlook for a caries vaccine. Crit Rev Oral Biol Med. 1990;1(1):37–54. doi: 10.1177/10454411900010010401. [DOI] [PubMed] [Google Scholar]
  34. Moore W. E., Holdeman L. V., Cato E. P., Good I. J., Smith E. P., Ranney R. R., Palcanis K. G. Variation in periodontal floras. Infect Immun. 1984 Dec;46(3):720–726. doi: 10.1128/iai.46.3.720-726.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Moore W. E., Holdeman L. V., Smibert R. M., Good I. J., Burmeister J. A., Palcanis K. G., Ranney R. R. Bacteriology of experimental gingivitis in young adult humans. Infect Immun. 1982 Nov;38(2):651–667. doi: 10.1128/iai.38.2.651-667.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Norhagen G. E., Engström P. E., Hammarström L., Smith C. I., Nord C. E. Oral and intestinal microflora in individuals with different immunoglobulin deficiencies. Eur J Clin Microbiol Infect Dis. 1990 Aug;9(8):631–633. doi: 10.1007/BF01967224. [DOI] [PubMed] [Google Scholar]
  37. Pignata C., Budillon G., Monaco G., Nani E., Cuomo R., Parrilli G., Ciccimarra F. Jejunal bacterial overgrowth and intestinal permeability in children with immunodeficiency syndromes. Gut. 1990 Aug;31(8):879–882. doi: 10.1136/gut.31.8.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Riviere G. R., Wagoner M. A., Freeman I. L. Chronic peroral immunization of conventional laboratory rats with mutans streptococci leads to stable acquired suppression of salivary antibodies. Oral Microbiol Immunol. 1992 Jun;7(3):137–141. doi: 10.1111/j.1399-302x.1992.tb00526.x. [DOI] [PubMed] [Google Scholar]
  39. Robertson P. B., Mackler B. F., Wright T. E., Levy B. M. Periodontal status of patients with abnormalities of the immune system. II. Observations over a 2-year period. J Periodontol. 1980 Feb;51(2):70–73. doi: 10.1902/jop.1980.51.2.70. [DOI] [PubMed] [Google Scholar]
  40. Rölla G., Ciardi J. E., Bowen W. H. Identification of IgA, IgG, lysozyme, albumin, alpha-amylase and glucosyltransferase in the protein layer adsorbed to hydroxyapatite from whole saliva. Scand J Dent Res. 1983 Jun;91(3):186–190. doi: 10.1111/j.1600-0722.1983.tb00800.x. [DOI] [PubMed] [Google Scholar]
  41. SCHAEDLER R. W., DUBOS R. J. The fecal flora of various strains of mice. Its bearing on their susceptibility to endotoxin. J Exp Med. 1962 Jun 1;115:1149–1160. doi: 10.1084/jem.115.6.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Savage D. C. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–133. doi: 10.1146/annurev.mi.31.100177.000543. [DOI] [PubMed] [Google Scholar]
  43. Shroff K. E., Meslin K., Cebra J. J. Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut. Infect Immun. 1995 Oct;63(10):3904–3913. doi: 10.1128/iai.63.10.3904-3913.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tancrède C. Role of human microflora in health and disease. Eur J Clin Microbiol Infect Dis. 1992 Nov;11(11):1012–1015. doi: 10.1007/BF01967791. [DOI] [PubMed] [Google Scholar]
  45. Tannock G. W., Savage D. C. Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun. 1974 Mar;9(3):591–598. doi: 10.1128/iai.9.3.591-598.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Trudel L., St-Amand L., Bareil M., Cardinal P., Lavoie M. C. Bacteriology of the oral cavity of BALB/c mice. Can J Microbiol. 1986 Aug;32(8):673–678. doi: 10.1139/m86-124. [DOI] [PubMed] [Google Scholar]
  47. Van Saene H. K., Van der Waaij D. A novel technique for detecting IgA coated potentially pathogenic microorganisms in the human intestine. J Immunol Methods. 1979;30(1):87–96. doi: 10.1016/0022-1759(79)90276-x. [DOI] [PubMed] [Google Scholar]
  48. Williams R. C., Gibbons R. J. Inhibition of bacterial adherence by secretory immunoglobulin A: a mechanism of antigen disposal. Science. 1972 Aug 25;177(4050):697–699. doi: 10.1126/science.177.4050.697. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES