Immunobiotic lactobacilli reduce viral-associated pulmonary damage through the modulation of inflammation-coagulation interactions

International Immunopharmacology

Volumn 19, Issue 1, 2014, Pages 161-173

  Zelaya, Hortensia ^a,b,c   Tsukida, Kohichiro ^d   Chiba, Eriko ^d   Marranzino, Gabriela ^a,b   Alvarez, Susana ^a,b,c   Kitazawa, Haruki ^d   Agüero, Graciela ^a,c   Villena, Julio ^a,b,d  

^a Immunobiotics Research Group   (Argentina)

^b CENTRO DE REFERENCIA PARA LACTOBACILOS CERELA CONICET   (Argentina)

^c UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

IL 10; Inflammation Coagulation; Influenza virus; Lactobacillus rhamnosus CRL1505; Poly(I:C); Respiratory syncytial virus; TLR3

Indexed keywords

IL-10; INFLAMMATION-COAGULATION; INFLUENZA VIRUS; LACTOBACILLUS RHAMNOSUS CRL1505; POLY(I:C); RESPIRATORY SYNCYTIAL VIRUS; TLR3;

ANIMALS; ANTITHROMBIN III; BLOOD COAGULATION; BRONCHOALVEOLAR LAVAGE FLUID; CERCOPITHECUS AETHIOPS; CYTOKINES; DOGS; IMMUNOLOGIC FACTORS; INFLUENZAVIRUS A; LACTOBACILLUS RHAMNOSUS; LEUKOCYTE COUNT; MADIN DARBY CANINE KIDNEY CELLS; MALE; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; PEPTIDE HYDROLASES; PNEUMONIA; POLY I-C; PROBIOTICS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VERO CELLS;

EID: 84893745384     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2013.12.020     Document Type: Article

References (46)

1. F.L. Visseren, J.J. Bouwman, K.P. Bouter, R.J. Diepersloot, P.H. de Groot, and D.W. Erkelens Procoagulant activity of endothelial cells after infection with respiratory viruses Thromb Haemost 84 2000 319 324 (Pubitemid 30601481)
2. J.J. Bouwman, F.L. Visseren, M.C. Bosch, K.P. Bouter, and R.J. Diepersloot Procoagulant and inflammatory response of virus-infected monocytes Eur J Clin Invest 32 2002 759 766 (Pubitemid 35334972)
3. T.T. Keller, K.F. van der Sluijs, M.D. de Kruif, V.E. Gerdes, J.C. Meijers, and S. Florquin et al. Effects on coagulation and fibrinolysis induced by influenza in mice with a reduced capacity to generate activated protein C and a deficiency in plasminogen activator inhibitor type 1 Circ Res 99 2006 1261 1269 (Pubitemid 44808663)
4. M. Schouten, J.D. de Boer, K.F. van der Sluijs, J.J. Roelofs, C. van't Veer, and M. Levi et al. Impact of endogenous protein C on pulmonary coagulation and injury during lethal H1N1 influenza in mice Am J Respir Cell Mol Biol 45 2011 789 794
5. F. Zare, M. Magnusson, L.N. Mollers, T. Jin, A. Tarkowski, and M. Bokarewa Single-stranded polyinosinic acid oligonucleotides trigger leukocyte production of proteins belonging to fibrinolytic and coagulation cascades J Leukoc Biol 84 2008 741 747
6. L. Smeeth, S.L. Thomas, A.J. Hall, R. Hubbard, P. Farrington, and P. Vallance Risk of myocardial infarction and stroke after acute infection or vaccination N Engl J Med 351 2004 2611 2618 (Pubitemid 39628582)
7. C.R. Meier, S.S. Jick, L.E. Derby, C. Vasilakis, and H. Jick Acute respiratory-tract infections and risk of first-time acute myocardial infarction Lancet 351 1998 1467 1471 (Pubitemid 28227037)
8. V.A. Londhe, J.A. Belperio, M.P. Keane, M.D. Burdick, Y.Y. Xue, and R.M. Strieter CXCR2 is critical for dsRNA-induced lung injury: relevance to viral lung infection J Inflamm (Lond) 2 2005 4
9. N.C. Stowell, J. Seideman, H.A. Raymond, K.A. Smalley, R.J. Lamb, and D.D. Egenolf et al. Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice Respir Res 10 2009 43
10. A. Shibamiya, K. Hersemeyer, T. Schmidt Woll, D. Sedding, J.M. Daniel, and S. Bauer et al. A key role for Toll-like receptor-3 in disrupting the hemostasis balance on endothelial cells Blood 113 2009 714 722
11. J. Villena, S. Salva, N. Barbieri, and S. Alvarez Immunobiotics for the prevention of bacterial and viral respiratory infections H. Kitazawa, J. Villena, S. Alvarez, Probiotics: immunobiotics and immunogenics 2013 Science Publishers, CRC Press, Taylor & Francis Group company 128 168
12. S. Alvarez, J. Villena, M. Tohno, S. Salva, and H. Kitazawa Modulation of innate immunity by lactic acid bacteria: impact on host response to infections Curr Res Immunol 3 2009 87 126
13. J. Villena, E. Chiba, Y. Tomosada, S. Salva, G. Marranzino, and H. Kitazawa et al. Orally administered Lactobacillus rhamnosus modulates the respiratory immune response triggered by the viral pathogen-associated molecular pattern poly(I:C) BMC Immunol 13 2012 53
14. Y. Tomosada, E. Chiba, H. Zelaya, T. Takahashi, K. Tsukida, and H. Kitazawa et al. Nasally administered Lactobacillus rhamnosus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection BMC Immunol 14 2013 40
15. E. Chiba, Y. Tomosada, M.G. Vizoso-Pinto, S. Salva, T. Takahashi, and K. Tsukida et al. Immunobiotic Lactobacillus rhamnosus improves resistance of infant mice against respiratory syncytial virus infection Int Immunopharmacol 17 2013 373 382
16. C. Haro, J. Villena, H. Zelaya, S. Alvarez, and G. Agüero Lactobacillus casei modulates the inflammation-coagulation interaction in a pneumococcal pneumonia experimental model J Inflamm (Lond) 6 2009 28
17. H. Zelaya, C. Haro, J. Laiño, S. Alvarez, and G. Aguero Inflammation-Hemostasis relationship in infected malnourished mice: modulatory effect of Lactobacillus casei CRL 431 Inflamm Res 61 2012 775 785
18. H. Zelaya, J. Laiño, C. Haro, S. Alvarez, and G. Aguero Modulation of the immuno-coagulative response in a pneumococcal infection in malnourished mice nasally treated with Lactobacillus casei J Med Microbiol 62 2013 145 154
19. H. Zelaya, J. Laiño, J. Villena, S. Alvarez, and G. Aguero Lactobacillus rhamnosus CRL1505 beneficially modulates the immuno-coagulative response after pneumococcal infection in immunocompromised malnourished mice Can J Microbiol 59 2013 684 693
20. S. Salva, J. Villena, and S. Alvarez Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections Int J Food Microbiol 141 2010 82 89
21. S. Salva, M. Nunez, J. Villena, A. Ramon, G. Font, and S. Alvarez Development of a fermented goats' milk containing Lactobacillus rhamnosus: in vivo study of health benefits J Sci Food Agric 91 2011 2355 2362
22. J. Dacie, and S. Lewis Dacie y Lewis. Hematología Práctica 10th ed. 2008 Elsevier España
23. S. Kaplow Simplified myeloperoxidase stain using benzidine dihydrochloride Blood 26 1965 215
24. G. Agüero, J. Villena, S. Racedo, C. Haro, and S. Alvarez Beneficial immunomodulatory activity of Lactobacillus casei in malnourished mice pneumonia: effect on inflammation and coagulation Nutrition 22 2006 810 819 (Pubitemid 43947497)
25. L. Kordich, and A. Blanco Fundamentos para el manejo práctico en el laboratorio de hemostasia. Grupo CAHT Segunda Edición ed. 2012 Federación Bioquímica de la Provincia de Buenos Aires Buenos Aires
26. G. Perdigon, C. Maldonado Galdeano, J.C. Valdez, and M. Medici Interaction of lactic acid bacteria with the gut immune system Eur J Clin Nutr 56 Suppl. 4 2002 S21 S26
27. M.R. Murawski, G.N. Bowen, A.M. Cerny, L.J. Anderson, L.M. Haynes, and R.A. Tripp et al. Respiratory syncytial virus activates innate immunity through Toll-like receptor 2 J Virol 83 2009 1492 1500
28. R. Sawai, K. Kuroda, T. Shibata, R. Gomyou, K. Osawa, and K. Shimizu Anti-influenza virus activity of Chaenomeles sinensis J Ethnopharmacol 118 2008 108 112
29. S. Takeda, M. Takeshita, Y. Kikuchi, B. Dashnyam, S. Kawahara, and H. Yoshida et al. Efficacy of oral administration of heat-killed probiotics from Mongolian dairy products against influenza infection in mice: alleviation of influenza infection by its immunomodulatory activity through intestinal immunity Int Immunopharmacol 11 2011 1976 1983
30. T. Kawai, and S. Akira Toll-like receptor and RIG-I-like receptor signaling Ann N Y Acad Sci 1143 2008 1 20
31. S.M. Bueno, P.A. Gonzalez, C.A. Riedel, L.J. Carreno, A.E. Vasquez, and A.M. Kalergis Local cytokine response upon respiratory syncytial virus infection Immunol Lett 136 2011 122 129
32. B.D. Rudd, J.J. Smit, R.A. Flavell, L. Alexopoulou, M.A. Schaller, and A. Gruber et al. Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection J Immunol 176 2006 1937 1942 (Pubitemid 43134339)
33. R. Le Goffic, V. Balloy, M. Lagranderie, L. Alexopoulou, N. Escriou, and R. Flavell et al. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia PLoS Pathog 2 2006 e53
34. L. Gitlin, W. Barchet, S. Gilfillan, M. Cella, B. Beutler, and R.A. Flavell et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus Proc Natl Acad Sci U S A 103 2006 8459 8464 (Pubitemid 43838477)
35. T. Wang, T. Town, L. Alexopoulou, J.F. Anderson, E. Fikrig, and R.A. Flavell Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis Nat Med 10 2004 1366 1373 (Pubitemid 40022719)
36. D.M. Hwang, D.W. Chamberlain, S.M. Poutanen, D.E. Low, S.L. Asa, and J. Butany Pulmonary pathology of severe acute respiratory syndrome in Toronto Mod Pathol 18 2005 1 10 (Pubitemid 40128088)
37. Y. Muramoto, H. Ozaki, A. Takada, C.H. Park, Y. Sunden, and T. Umemura et al. Highly pathogenic H5N1 influenza virus causes coagulopathy in chickens Microbiol Immunol 50 2006 73 81 (Pubitemid 43142971)
38. J. Sun, A. Cardani, A.K. Sharma, V.E. Laubach, R.S. Jack, and W. Muller et al. Autocrine regulation of pulmonary inflammation by effector T-cell derived IL-10 during infection with respiratory syncytial virus PLoS Pathog 7 2011 e1002173
39. Y. Becker Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy - a review Virus Genes 33 2006 235 252 (Pubitemid 44401431)
40. B.S. Graham, T.R. Johnson, and R.S. Peebles Immune-mediated disease pathogenesis in respiratory syncytial virus infection Immunopharmacology 48 2000 237 247
41. M.L. Moore, D.C. Newcomb, V.V. Parekh, L. Van Kaer, R.D. Collins, and W. Zhou et al. STAT1 negatively regulates lung basophil IL-4 expression induced by respiratory syncytial virus infection J Immunol 183 2009 2016 2026
42. S. Poitevin, E. Cochery-Nouvellon, A. Dupont, and P. Nguyen Monocyte IL-10 produced in response to lipopolysaccharide modulates thrombin generation by inhibiting tissue factor expression and release of active tissue factor-bound microparticles Thromb Haemost 97 2007 598 607 (Pubitemid 46592938)
43. S. Ben-Hadj-Khalifa, P. Nguyen, T. Mahjoub, and N. Hezard Anticoagulant properties of the anti-inflammatory cytokine IL-10 in a factor Xa-activated human monocyte model Eur Cytokine Netw 23 2012 87 92
44. L. Smeeth, C. Cook, S. Thomas, A.J. Hall, R. Hubbard, and P. Vallance Risk of deep vein thrombosis and pulmonary embolism after acute infection in a community setting Lancet 367 2006 1075 1079
45. C.T. Esmon Crosstalk between inflammation and thrombosis Maturitas 47 2004 305 314 (Pubitemid 38520117)
46. M. van Wissen, T.T. Keller, E.C. van Gorp, V.E. Gerdes, J.C. Meijers, and G.J. van Doornum et al. Acute respiratory tract infection leads to procoagulant changes in human subjects J Thromb Haemost 9 2011 1432 1434