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Volume 62, Issue 1

Modulation of the immuno-coagulative response in a pneumococcal infection in malnourished mice nasally treated with Free

Abstract

We studied the systemic effects of the intranasal administration of on the immuno-coagulative response in pneumoccocal infection in immunocompromised mice. Weaned mice consumed a protein-free diet (PFD) for 21 days and were therefore malnourished. Malnourished mice were fed a balanced conventional diet (BCD) for 7 days (BCD group) or a BCD for 7 days with nasal administration of viable on days 6 and 7 (BCD+LcN group). The malnourished control mice (MNC) received a PFD, whereas the well-nourished control mice (WNC) continually consumed a BCD. At the end of the treatment period, the mice were infected with . At different times after infection, we analysed the following parameters: global coagulation system, activation of coagulation, coagulation inhibitors, platelet count, leukocyte count and myeloperoxidase (MPO) activity, total proteins, albumin and acute phase proteins (APPs). The MNC group showed greater impairment in the coagulation tests and an increase in the positive APPs. These parameters were normalized by the treatment. However, the number of leukocytes, decreased by malnutrition, was improved only by the administration of . After infection, the BCD+LcN group showed similar results to those of the WNC group for most of the haemostatic parameters. The BCD+LcN group did not show significant variations in the prothrombin time or in the level of anticoagulant protein C, but showed higher levels of fibrinogen, platelets, albumin, leukocytes and MPO activity compared with the different experimental groups. The intranasal administration of was effective in modulating the pro-inflammatory aspects of coagulation without affecting coagulation itself.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
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2013-01-01
2024-04-26
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References

  1. Agüero G., Villena J., Racedo S., Haro C., Alvarez S. 2006; Beneficial immunomodulatory activity of Lactobacillus casei in malnourished mice pneumonia: effect on inflammation and coagulation. Nutrition 22:810–819 [View Article][PubMed]
     [Google Scholar]
  2. Alvarez S., Villena J., Racedo S., Salva S., Agüero G. 2007; Malnutrition, probiotics and respiratory infections. In Research Advances in Nutrition pp. 9–23 Kerala, India: G. R. Network;
     [Google Scholar]
  3. Alvarez S., Villena J., Salva S. 2009; Humoral immunity against respiratory pathogens: can lactic acid bacteria improve it?. In Research Advances in Infection and Immunity pp. 1–19 Kerala, India: G. R. Network;
     [Google Scholar]
  4. Alves-Filho J. C. 2005; Toll-like receptors on platelets: the key for disseminated intravascular coagulation in sepsis?. Thromb Res 115:537–538 [View Article][PubMed]
     [Google Scholar]
  5. Anthony R., el-Omar E., Lappin D. F., MacSween R. N., Whaley K. 1989; Regulation of hepatic synthesis of C3 and C4 during the acute-phase response in the rat. Eur J Immunol 19:1405–1412 [View Article][PubMed]
     [Google Scholar]
  6. Beutler B., Poltorak A. 2001; Sepsis and evolution of the innate immune response. Crit Care Med 29:Suppl.S2–S6 [View Article][PubMed]
     [Google Scholar]
  7. Busso N., Chobaz-Péclat V., Hamilton J., Spee P., Wagtmann N., So A. 2008; Essential role of platelet activation via protease activated receptor 4 in tissue factor-initiated inflammation. Arthritis Res Ther 10:R42 [View Article][PubMed]
     [Google Scholar]
  8. Choi G., Vlaar A. P., Schouten M., Van’t Veer C., van der Poll T., Levi M., Schultz M. J. 2007; Natural anticoagulants limit lipopolysaccharide-induced pulmonary coagulation but not inflammation. Eur Respir J 30:423–428 [View Article][PubMed]
     [Google Scholar]
  9. Cox D., Kerrigan S. W., Watson S. P. 2011; Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation. J Thromb Haemost 9:1097–1107 [View Article][PubMed]
     [Google Scholar]
  10. Cross M. L. 2002; Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunol Med Microbiol 34:245–253 [View Article][PubMed]
     [Google Scholar]
  11. Dacie J., Lewis S. 1995; Basic haematological techniques. In Practical Haematology pp. 49–82 Edinburgh: Churchill Livingstone;
     [Google Scholar]
  12. Dogi C. A., Galdeano C. M., Perdigón G. 2008; Gut immune stimulation by non pathogenic Gram(+) and Gram(−) bacteria. Comparison with a probiotic strain. Cytokine 41:223–231 [View Article][PubMed]
     [Google Scholar]
  13. FAO/WHO 2001 Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria Geneva, Switzerland: World Health Organization; Available at http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf
     [Google Scholar]
  14. Fleck A. 1989; Clinical and nutritional aspects of changes in acute-phase proteins during inflammation. Proc Nutr Soc 48:347–354 [View Article][PubMed]
     [Google Scholar]
  15. Fournier T., Medjoubi-N N., Porquet D. 2000; Alpha-1-acid glycoprotein. Biochim Biophys Acta 1482:157–171 [View Article][PubMed]
     [Google Scholar]
  16. Gaggìa F., Mattarelli P., Biavati B. 2010; Probiotics and prebiotics in animal feeding for safe food production. Int J Food Microbiol 141:Suppl. 1S15–S28 [View Article][PubMed]
     [Google Scholar]
  17. Galdeano C. M., de Moreno de LeBlanc A., Vinderola G., Bonet M. E., Perdigón G. 2007; Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clin Vaccine Immunol 14:485–492 [View Article][PubMed]
     [Google Scholar]
  18. Gill H. S., Rutherfurd K. J., Prasad J., Gopal P. K. 2000; Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83:167–176 [View Article][PubMed]
     [Google Scholar]
  19. González Naranjo L. A., Molina Restrepo J. F. 2010; Laboratory evaluation of inflammation. Revista Colombiana de Reumatología 17:35–47 (in Spanish) [CrossRef]
     [Google Scholar]
  20. Griesshammer M., Bangerter M., Sauer T., Wennauer R., Bergmann L., Heimpel H. 1999; Aetiology and clinical significance of thrombocytosis: analysis of 732 patients with an elevated platelet count. J Intern Med 245:295–300 [View Article][PubMed]
     [Google Scholar]
  21. Haro C., Villena J., Zelaya H., Alvarez S., Agüero G. 2009; Lactobacillus casei modulates the inflammation-coagulation interaction in a pneumococcal pneumonia experimental model. J Inflamm (Lond) 6:28 [View Article][PubMed]
     [Google Scholar]
  22. Janeway C. A. Jr, Medzhitov R. 1998; Introduction: the role of innate immunity in the adaptive immune response. Semin Immunol 10:349–350 [View Article][PubMed]
     [Google Scholar]
  23. Kaplow L. S. 1965; Simplified myeloperoxidase stain using benzidine dihydrochloride. Blood 26:215–219[PubMed]
     [Google Scholar]
  24. Kaysen G. A., Chertow G. M., Adhikarla R., Young B., Ronco C., Levin N. W. 2001; Inflammation and dietary protein intake exert competing effects on serum albumin and creatinine in hemodialysis patients. Kidney Int 60:333–340 [View Article][PubMed]
     [Google Scholar]
  25. Kiyono H., Fukuyama S. 2004; NALT- versus Peyer’s-patch-mediated mucosal immunity. Nat Rev Immunol 4:699–710 [View Article][PubMed]
     [Google Scholar]
  26. Knapp S., Hareng L., Rijneveld A. W., Bresser P., van der Zee J. S., Florquin S., Hartung T., van der Poll T. 2004; Activation of neutrophils and inhibition of the proinflammatory cytokine response by endogenous granulocyte colony-stimulating factor in murine pneumococcal pneumonia. J Infect Dis 189:1506–1515 [View Article][PubMed]
     [Google Scholar]
  27. Komatsu W., Mawatari K., Miura Y., Yagasaki K. 2007; Restoration by dietary glutamine of reduced tumor necrosis factor production in a low-protein-diet-fed rat model. Biosci Biotechnol Biochem 71:352–357 [View Article][PubMed]
     [Google Scholar]
  28. Konecny F. A. 2010; Review of cellular and molecular pathways linking thrombosis and innate immune system during sepsis. J Res Med Sci 15:348–358[PubMed]
     [Google Scholar]
  29. Levi M., van der Poll T., Büller H. R. 2004; Bidirectional relation between inflammation and coagulation. Circulation 109:2698–2704 [View Article][PubMed]
     [Google Scholar]
  30. Ling P. R., Smith R. J., Kie S., Boyce P., Bistrian B. R. 2004; Effects of protein malnutrition on IL-6-mediated signaling in the liver and the systemic acute-phase response in rats. Am J Physiol Regul Integr Comp Physiol 287:R801–R808 [View Article][PubMed]
     [Google Scholar]
  31. Loof T. G., Schmidt O., Herwald H., Theopold U. 2011; Coagulation systems of invertebrates and vertebrates and their roles in innate immunity: the same side of two coins?. J Innate Immun 3:34–40 [View Article][PubMed]
     [Google Scholar]
  32. Luchtefeld M., Preuss C., Rühle F., Bogalle E. P., Sietmann A., Figura S., Müller W., Grote K., Schieffer B., Stoll M. 2011; Gp130-dependent release of acute phase proteins is linked to the activation of innate immune signaling pathways. PLoS ONE 6:e19427 [View Article][PubMed]
     [Google Scholar]
  33. Ménard S., Candalh C., Bambou J. C., Terpend K., Cerf-Bensussan N., Heyman M. 2004; Lactic acid bacteria secrete metabolites retaining anti-inflammatory properties after intestinal transport. Gut 53:821–828 [View Article][PubMed]
     [Google Scholar]
  34. Morlese J. F., Forrester T., Jahoor F. 1998; Acute-phase protein response to infection in severe malnutrition. Am J Physiol 275:E112–E117[PubMed]
     [Google Scholar]
  35. O’Neill L. A., Bowie A. G. 2007; The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353–364 [View Article][PubMed]
     [Google Scholar]
  36. Ogra P. L., Faden H., Welliver R. C. 2001; Vaccination strategies for mucosal immune responses. Clin Microbiol Rev 14:430–445 [View Article][PubMed]
     [Google Scholar]
  37. Pawlinski R., Mackman N. 2010; Cellular sources of tissue factor in endotoxemia and sepsis. Thromb Res 125:Suppl. 1S70–S73 [View Article][PubMed]
     [Google Scholar]
  38. Perdigón G., Maldonado Galdeano C., Valdez J. C., Medici M. 2002; Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56:Suppl. 4S21–S26 [View Article][PubMed]
     [Google Scholar]
  39. Racedo S., Villena J., Medina M., Agüero G., Rodríguez V., Alvarez S. 2006; Lactobacillus casei administration reduces lung injuries in a Streptococcus pneumoniae infection in mice. Microbes Infect 8:2359–2366 [View Article][PubMed]
     [Google Scholar]
  40. Reitsma P. H., Branger J., Van Den Blink B., Weijer S., Van Der Poll T., Meijers J. C. 2003; Procoagulant protein levels are differentially increased during human endotoxemia. J Thromb Haemost 1:1019–1023 [View Article][PubMed]
     [Google Scholar]
  41. Rittirsch D., Flierl M. A., Ward P. A. 2008; Harmful molecular mechanisms in sepsis. Nat Rev Immunol 8:776–787 [View Article][PubMed]
     [Google Scholar]
  42. Sakamoto M., Ishii S., Nishioka K., Shimada K. 1981; Level of complement activity and components C1, C4, C2, and C3 in complement response to bacterial challenge in malnourished rats. Infect Immun 32:553–556[PubMed]
     [Google Scholar]
  43. Salva S., Villena J., Racedo S., Alvarez S., Agüero G. 2008; Lactobacillus casei addition to a repletion diet-induced early normalisation of cytokine profils during a pneumococcal infection in malnourished mice. Food Agric Immunol 19:195–211 [View Article]
     [Google Scholar]
  44. Sampietro T., Bigazzi F., Dal Pino B., Rossi G., Chella E., Lusso S., Puntoni M., Tuoni M., Bionda A. 2004; Up regulation of C3, C4, and soluble intercellular adhesion molecule-1 co-expresses with high sensitivity C reactive protein in familial hypoalphalipoproteinaemia: further evidence of inflammatory activation. Heart 90:1438–1442 [View Article][PubMed]
     [Google Scholar]
  45. Savino W. 2002; The thymus gland is a target in malnutrition. Eur J Clin Nutr 56:Suppl. 3S46–S49 [View Article][PubMed]
     [Google Scholar]
  46. Scrimshaw N. S., SanGiovanni J. P. 1997; Synergism of nutrition, infection, and immunity: an overview. Am J Clin Nutr 66:464S–477S[PubMed]
     [Google Scholar]
  47. Shils M. E., Olson J. A., Shike M., Ross C. A. 1999 Modern Nutrition in Health and Disease Philadelphia: Lippincott Williams and Wilkins;
     [Google Scholar]
  48. Su S. J., Yeh T. M. 1996; Effects of alpha 1-acid glycoprotein on tissue factor expression and tumor necrosis factor secretion in human monocytes. Immunopharmacology 34:139–145 [View Article][PubMed]
     [Google Scholar]
  49. van Gils J. M., Zwaginga J. J., Hordijk P. L. 2009; Molecular and functional interactions among monocytes, platelets, and endothelial cells and their relevance for cardiovascular diseases. J Leukoc Biol 85:195–204 [View Article][PubMed]
     [Google Scholar]
  50. Villena J., Racedo S., Agüero G., Bru E., Medina M., Alvarez S. 2005; Lactobacillus casei improves resistance to pneumococcal respiratory infection in malnourished mice. J Nutr 135:1462–1469[PubMed]
     [Google Scholar]
  51. Villena J., Barbieri N., Salva S., Herrera M., Alvarez S. 2009; Enhanced immune response to pneumococcal infection in malnourished mice nasally treated with heat-killed Lactobacillus casei . Microbiol Immunol 53:636–646 [View Article][PubMed]
     [Google Scholar]
  52. Vizoso Pinto M. G., Rodriguez Gómez M., Seifert S., Watzl B., Holzapfel W. H., Franz C. M. A. P. 2009; Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol 133:86–93 [View Article][PubMed]
     [Google Scholar]
  53. Weyrich A. S., Zimmerman G. A. 2004; Platelets: signaling cells in the immune continuum. Trends Immunol 25:489–495 [View Article][PubMed]
     [Google Scholar]
  54. Yuksel M., Okajima K., Uchiba M., Horiuchi S., Okabe H. 2002; Activated protein C inhibits lipopolysaccharide-induced tumor necrosis factor-alpha production by inhibiting activation of both nuclear factor-kappa B and activator protein-1 in human monocytes. Thromb Haemost 88:267–273[PubMed]
     [Google Scholar]
  55. Zelaya H., Haro C., Laiño J., Alvarez S., Agüero G. 2011a; Coagulation activation in an experimental pneumonia model in malnourished mice. Can J Physiol Pharmacol 89:41–49 [View Article][PubMed]
     [Google Scholar]
  56. Zelaya H., Laiño J., Haro C., Agüero G. 2011b Haemostatic alterations in infected malnourished mice: effect of nasal treatment with Lactobacillus casei (Abstract). XXVIII Annual Scientific Meeting, Tucuman Biology Association. Tucumán, Argentina
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Modulation of the immuno-coagulative response in a pneumococcal infection in malnourished mice nasally treated with Lactobacillus casei
J. Med. Microbiol. 62, 145 (2013); https://doi.org/10.1099/jmm.0.045526-0
/content/journal/jmm/10.1099/jmm.0.045526-0
/content/journal/jmm/10.1099/jmm.0.045526-0
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