Skip to main content
SpringerLink
Log in

The effect of type-1 fimbrial immunization on gut pathophysiological response in rats infected with Salmonella enterica subsp. enterica serovar Typhimurium

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

The pathophysiological mechanism of Salmonella enterica subsp. enterica serovar Typhimurium (Salmonella typhimurium) induced gastroenteritis is controlled by interplay of various cell signaling events. Adherence of this organism through type-1 fimbriae is known to be a vital prerequisite for the establishment of infection. In the present investigation male albino Wistar rats were immunized with purified type-1 fimbriae and challenged intragastrically with S. typhimurium. Electrolyte transport and level of different second messengers were studied in four different groups of animals. Transepithelial fluxes of Na+ and Cl− revealed absorption in immunized-challenged group as observed in case of control and immunized group while secretion was observed in infected group. Ca2+ and 3-0-methyl-D-glucose fluxes did not show any change. Significant increase in the level of intracellular Ca2+, cAMP, membrane form of protein kinase C, prostaglandins, NADPH oxidase, glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase, total oxygen free radicals, reactive nitrogen intermediates, citrulline and lipid peroxidation was found in the infected group. However, in the immunized-challenged group, the values of all the parameters were found to be same as that of control as well as immunized groups. Na+, K+-ATPase and calmodulin levels were found to be unaltered in all the groups of animals. Thus, the immunization with type-1 fimbriae has been found to be quite effective leading to the prevention of multiple physiologic derangements in isolated ileal cells suggesting the protective role of the fimbriae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Ispahani P, Slack RC: Enteric fever and other extraintestinal salmonellosis in University Hospital, Nottingham, UK, between 1980 and 1997. Eur J Clin Microbiol Infect Dis 19: 679–87, 2000

    Article  CAS  PubMed  Google Scholar 

  2. Darwin HK, Miller VL: Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin Microb Rev 12: 405–428, 1999

    CAS  Google Scholar 

  3. Clegg S, Swenson DL: Salmonella fimbriae, In: P. Klemm (ed), Fimbriae: Adhesion, Genetics, Biogenesis and Vaccines. CRC Press, Inc., Boca Raton, Florida, 1994, pp. 105–113

    Google Scholar 

  4. Lindquist BL, Lebenthal E, Lee PC, Stinson MW, Merrick FM: Adherence of Salmonella typhimurium to small intestinal enterocytes of the rat. Infect Immun 55: 3044–3050, 1987

    CAS  PubMed  Google Scholar 

  5. Soderlind O, Olsson E, Smyth CJ, Mollby R: Effect of parenteral vaccination of dams on intestinal Escherichia coli in piglets with diarrhoea. Infect Immun 36: 900–906, 1982

    CAS  PubMed  Google Scholar 

  6. Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS, Burlein J, Barren P, Koenig S, Leath S, Jones CH, Hultgren SJ: Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276: 607–611, 1997

    Article  CAS  PubMed  Google Scholar 

  7. Ascon MA, Hone DM, Walters N, Pascarl DW: Oral immunization with a Salmonella typhimurium vaccine vector expressing recombinant enterotoxigenic E. coli K99 fimbriae elicits elevated antibody titers for protective immunity. Infect Immun 66: 5470–5476, 1998

    CAS  PubMed  Google Scholar 

  8. Li W, Watari S, Iwasaki T, Kodama H: Suppresion of Salmonella enterica erovar Enteridis excretion by intraocular vaccination with fimbriae proteins incorporated in liposomes. Dev Comp Immunol 28: 29–38, 2004

    Article  PubMed  Google Scholar 

  9. Barbou EK, Bejjani NE, Daghir NJ, Faroon OM, Bouljihad M, Spasojevic R et~al.: Induction of early immunopotentiation of fimbriae of Salmonella enteritidis administering thymulin and zinc to SE-vaccinated chicken breeders: Relationship and protection. J Vet Med Sci 62:1139–1143, 2000

    Article  CAS  PubMed  Google Scholar 

  10. Li X, Mobley HL: Vaccines for proteus mirabilis in urinary tract infection. Int J Antimicrob Agents 19: 461–465, 2002

    Article  CAS  PubMed  Google Scholar 

  11. Khurana S, Ganguly NK, Khullar M, Panigrahi D, Walia BNS: Studies on mechanisms of Salmonella typhimurium enterotoxin-mediated diarrhoea. Biochem Biophys Acta 1097: 171–176, 1991

    CAS  PubMed  Google Scholar 

  12. Basu S, Sarkar M, Mandal C: A single step purification of a sialic acid binding lectin (Achatinin H) from Achatina fulica snail. Mol Cell Biochem 71:149–157, 1986

    Article  CAS  PubMed  Google Scholar 

  13. Ghosh S, Mittal A, Ganguly NK: Purification and characterization of distinct type of mannose sensitive fimbriae from Salmonella typhimurium. FEMS Microbiol Lett 115: 229–234, 1994

    Article  CAS  PubMed  Google Scholar 

  14. Laemmli UK: Cleavage of structural proteins during the assembly of bacteriophage T4. Nature 227: 680–685, 1970

    CAS  PubMed  Google Scholar 

  15. Zhang T, Stanley SL Jr: Oral immunization with an attenuated strain of Salmonella typhimurium expressing the serine-rich Entamoeba histolytica protein induces an antiamebic immune response and protects gerbils from amebic liver abscess. Infect Immun 64: 1526–1531, 1996

    CAS  PubMed  Google Scholar 

  16. Donowitz M, Wicks J, Madara JL, Sharp GWG: Studies on role of calmodulin in Ca2+ regulation of rabbit ileal Na+ and Cl- transport. Am J Physiol 248: G726–G740, 1985

    CAS  PubMed  Google Scholar 

  17. Ouchterlony O: Diffusion in gel methods for immunological analysis II. In: P. Kallos, B.H. Waksman (eds). Progress in Allergy. Vol VI, Basel, Karger, 1962, pp. 30–154

  18. Wild GE, Murray D: Changes in Na+, K+-ATPase, sodium ion and glucose transport in isolated enterocytes in an experimental model malabsorption. Dig Dis Sci 34: 739–744, 1989

    Article  Google Scholar 

  19. Pinkus LM: Separation and use of enterocytes. Methods Enzymol 77: 154–162, 1981

    CAS  PubMed  Google Scholar 

  20. Quigley JP, Gotterer GS: Distribution of (Na+, K+) stimulated ATPase activity in rat intestinal mucosa. Biochim Biophys Acta 173: 456–468, 1969

    CAS  PubMed  Google Scholar 

  21. Pace JL, Galan JE: Measurement of free intracellular calcium levels in epithelial cells as consequence of bacterial invasion. Methods Enzymol 236: 482–485, 1994

    CAS  PubMed  Google Scholar 

  22. Howe CL, Mousekar MS, Graves TA: Brush border calmodulin: A major component of the isolated micovillar core. J Cell Biol 85: 916–923, 1980

    Article  CAS  PubMed  Google Scholar 

  23. Wallace RW, Tallant EA, Cheung WY: Assay of calmodulin by Ca2+ dependent phosphodiesterase. Methods Enzymol 102: 39–47, 1983

    CAS  PubMed  Google Scholar 

  24. Thomas KH, Susan MT, Judith MC, Richard RC: Protein kinase C inhibitors inhibit primary (1–0) but not secondary (1–1) or cloned cytotoxic T lymphocytes. Biochem Biophys Res Commun 154: 1280–1286, 1988

    Article  PubMed  Google Scholar 

  25. Jafe BM, Behrman HR, Parker CW: Radioimmunoassay measurement of prostaglandins E, A and F in human plasma. J Clin Invest 52: 398–404, 1973

    PubMed  Google Scholar 

  26. Davies MDJ, Parrot DMV: Preparation and purification of lympocytes from the epithelium and lamina propria of murine small intestine Gut 22: 481–488, 1981

    CAS  PubMed  Google Scholar 

  27. Bhatnagar R, Rudiger S, Martin E, Decker K: Superoxide release by zymosan stimulated rat kupffer cells in vitro. Eur J Biochem 119: 171–175, 1981

    CAS  PubMed  Google Scholar 

  28. Babior BM, Cohen HJ. Measurement of neutrophil function: Phagocytosis, degranulation, the respiratory burst and bacterial killing. In: M.J. Chine (ed) Leukocyte Function. Churchill Livingstone, New York, 1981

    Google Scholar 

  29. Cheung K, Archibaid AC, Robinson MF: Luminol-dependent chemiluminescence produced by neutrophils stimulated by immune complexes. Aust J Exp Biol Med Sci 62: 403–419, 1984

    CAS  PubMed  Google Scholar 

  30. Green LC, Wagner DA, Glogowski J, Skipper Pl, Wishnok J, Tannenbau SR: Analysis of nitrate, nitrite and 15N nitrate in biological fluids. Anal Biochem 126: 131–158, 1982

    CAS  PubMed  Google Scholar 

  31. Boyde TRC, Rahmatullah M: Calorimetric determination of citrulline. Anal Biochem 107: 424–431, 1980

    CAS  PubMed  Google Scholar 

  32. Utley HG, Bernheim F, Hochstein P: Effect of sulphydryl reagents on peroxidation in microsomes. Arch Biochem Biophys 118: 29–32, 1967

    CAS  Google Scholar 

  33. Paranchych W, Frost LS: The physiology and biochemistry of pili. Adv Microb Physiol 29: 53–114, 1988

    CAS  PubMed  Google Scholar 

  34. Powell DW, Plotkin GR, Maenza RM, Solberg LI, Catlin DH, Formal SB: Experimental diarrhoea: Intestinal water and electrolyte transport in rat Salmonella enterocolitis Gastroenterol 60: 1053–1064, 1971

    CAS  Google Scholar 

  35. Binder HJ: Absorption and secretion of water and electrolytes by small and large intestine. In: M. Steisenger, J.S. Fordtran. (eds) Gastrointestinal Disease, Pathophysiology, Diagnosis and Management. WB Saunders Company, Philadelphia, 1989, pp. 1022–1044

    Google Scholar 

  36. Schafer JA, Williams JC Jr: Transport of metabolic substrates by proximal nephron. Ann Rev Physiol 77: 103–125, 1985

    Google Scholar 

  37. Zemelman BV, Walker WA, Chu SW: Expression and developmental regulation of Na+ K+-ATPase in rat small intestine. J Clin Invest 90: 1010–1012, 1992

    Google Scholar 

  38. Zimmerman TW, Dobins JW, Binder HJ: Role of calcium in the regulation of colonic secretion in rat. Am J Physiol 244: G552–G560, 1983

    CAS  PubMed  Google Scholar 

  39. Pace J, Hayman MJ, Galan JE: Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72: 505–514, 1993

    CAS  PubMed  Google Scholar 

  40. Peterson JW, Molina NC, Houston CW, Fader RC: Elevated cAMP in intestinal epithelial cells during experimental {Cholera} and Salmonellosis. Toxicon 21: 761–775, 1983

    CAS  PubMed  Google Scholar 

  41. Caleraro V, Choisi E, Greco R, Spina AM, Gione A, Quagliualo L, Servillo L, Balestreiri C, Illiano G: Role of calcium in chloride secretion mediated by cAMP pathway activation in rabbit distal colon mucosa. Am J Physiol 264: G252–G260, 1993

    PubMed  Google Scholar 

  42. Fondacaro JD, Henderson LS: Evidence for protein kinase C as a regulator of intestinal electrolyte transport. Am J Physiol 249: G422–G426, 1985

    CAS  PubMed  Google Scholar 

  43. Henderson LS, Naselsky D, Fondacaro JD: Calcium and cyclic nucleotide dependent phosphorylation of intestinal microvillus membranes. Federation Proc 44: 704, 1985

    Google Scholar 

  44. Calderaro V, Giovane A, Simone DE, Camussi G, Rossiello R, Quagliuolo L, Servillo L, Tauone W, Giordano C and Balestrieri C: Arachidonic acid metabolites and chloride secretion in rabbit distal colonic mucosa. Am J Physiol 261: G443–G450, 1991

    CAS  PubMed  Google Scholar 

  45. Bueno L, Fargeas MK, Fioramonti JF, Primi MP: Central control of intestinal motility by prostaglandins: A mediator of the actions of several peptides in rats and dogs. Gastroenterol 88: 1888–1894, 1985

    CAS  Google Scholar 

  46. Beckman JS, Beckman TW, Chen J, Marshell PA, Freeman BA: Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620–1625, 1990

    CAS  PubMed  Google Scholar 

  47. Segal AW, Abo A: The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem Sci 18: 43–47, 1993

    CAS  PubMed  Google Scholar 

  48. Klebanoff SJ: Reactive nitrogen intermediates and antimicrobial activity: Role of nitrite. Free Radic Biol Med 14: 351–360, 1993

    CAS  PubMed  Google Scholar 

  49. Stuehr DJ, Marletta MA: Mammalian nitrite biosynthesis. Mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc Natl Acad Sci USA 82: 7738–7742, 1985

    CAS  PubMed  Google Scholar 

  50. Cunha FQ, Assreuy J, Moncada S, Liew Y: Phagocytosis and induction of nitric oxide synthase in murine macrophages. Immunol 79: 408–411, 1993

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Experimental Medicine and Biotechnology, Postgraduate Institute of Medical Education and Research, Chandigarh, India

    Amrisha Verma, Sulagna Basu, Sujata Ghosh (Dr.) & S. Majumdar

  2. Indian Council of Medical Resarch, New Delhi, India

    N. K. Ganguly

  3. Department of Experimental Medicine and Biotechnology, Postgraduate Institute of Medical Education and Research, Chandigarh, 160 012, India

    Sujata Ghosh (Dr.)

Authors
  1. Amrisha Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sulagna Basu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sujata Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Majumdar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. K. Ganguly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sujata Ghosh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verma, A., Basu, S., Ghosh, S. et al. The effect of type-1 fimbrial immunization on gut pathophysiological response in rats infected with Salmonella enterica subsp. enterica serovar Typhimurium. Mol Cell Biochem 273, 127–135 (2005). https://doi.org/10.1007/s11010-005-8160-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-005-8160-0

Keywords

Search

Navigation