Are the immunomodulatory properties of Lactobacillus rhamnosus CRL1505 peptidoglycan common for all Lactobacilli during respiratory infection in malnourished mice?

PLoS ONE

Volumn 13, Issue 3, 2018, Pages

  Kolling, Yanina ^a   Salva, Susana ^a   Villena, Julio ^a   Alvarez, Susana ^a,b  

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

^b UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; PROBIOTIC AGENT; BACTERIUM ANTIBODY; CYTOKINE; IMMUNOLOGIC FACTOR; PEPTIDOGLYCAN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; HUMORAL IMMUNITY; IMMUNOMODULATION; INNATE IMMUNITY; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; LYMPHOCYTE COUNT; MALE; MALNUTRITION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PNEUMOCOCCAL INFECTION; RESPIRATORY TRACT INFECTION; TH1 TH2 BALANCE; ANIMAL; BACTEREMIA; BLOOD; BRONCHOALVEOLAR LAVAGE FLUID; CELLULAR IMMUNITY; COMPLICATION; CYTOLOGY; DIET THERAPY; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; IMMUNOTHERAPY; INTRANASAL DRUG ADMINISTRATION; LEUKOCYTE COUNT; LUNG; MICROBIOLOGY; PATHOLOGY; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PHYSIOLOGY; PROCEDURES; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE;

ADAPTIVE IMMUNITY; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, BACTERIAL; BACTEREMIA; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; IMMUNITY, CELLULAR; IMMUNOCOMPROMISED HOST; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; LEUKOCYTE COUNT; LUNG; MACROPHAGES, PERITONEAL; MALE; MALNUTRITION; MICE; PEPTIDOGLYCAN; PHAGOCYTOSIS; PNEUMONIA, PNEUMOCOCCAL; PROBIOTICS; STREPTOCOCCUS PNEUMONIAE;

EID: 85043477429     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0194034     Document Type: Article

References (49)

1. Kitazawa H, Tohno M, Shimosato T, Saito T. Development of molecular immunoassay system for probi-otics via toll-like receptors based on food immunology. Anim Sci J. 2008; 79: 11–21. https://doi.org/10.1111/j.1740-0929.2007.00492.x
2. Zelaya H, Alvarez S, Kitazawa H, Villena J. Respiratory Antiviral Immunity and Immunobiotics: Beneficial Effects on Inflammation-Coagulation Interaction during Influenza Virus Infection. Front Immunol. 2016; 7: 633. https://doi.org/10.3389/fimmu.2016.00633 PMID: 28066442
3. Villena J, Vizoso-Pinto MG, Kitazawa H. Intestinal Innate Antiviral Immunity and Immunobiotics: Beneficial Effects against Rotavirus Infection. Front Immunol. 2016; 7: 563. https://doi.org/10.3389/fimmu.2016.00563 PMID: 27994593
4. Lebeer S, Vanderleyden J, De Keersmaecker SCJ. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol. 2010; 8: 171–184. https://doi.org/10.1038/nrmicro2297 PMID: 20157338
5. Matsuguchi T, Takagi A, Matsuzaki T, Nagaoka M, Ishikawa K, Yokokura T, et al. Lipoteichoic acids from Lactobacillus strains elicit strong tumor necrosis factor alpha-inducing activities in macrophages through Toll-like receptor 2. Clin Diagn Lab Immunol. 2003; 10: 259–66. Available: http://www.ncbi.nlm.nih.gov/pubmed/12626452 https://doi.org/10.1128/CDLI.10.2.259-266.2003 PMID: 12626452
6. Dalpke A, Frey M, Morath S, Hartung T, Heeg K. Interaction of Lipoteichoic Acid and CpG-DNA During Activation of Innate Immune Cells. Immunobiology. 2002; 206: 392–407. https://doi.org/10.1078/0171-2985-00189 PMID: 12437070
7. Rachmilewitz D, Karmeli F, Takabayashi K, Hayashi T, Leider-Trejo L, Lee J, et al. Immunostimulatory DNA ameliorates experimental and spontaneous murine colitis. Gastroenterology. 2002; 122: 1428–41. Available: http://www.ncbi.nlm.nih.gov/pubmed/11984528 PMID: 11984528
8. Villena J, Racedo S, Aguero G, Bru E, Medina M, Alvarez S. Lactobacillus casei Improves Resistance to Pneumococcal Respiratory Infection in Malnourished Mice. J Nutr. 2005; 135: 1462–9. Available: http://www.ncbi.nlm.nih.gov/pubmed/15930453 PMID: 15930453
9. Salva S, Villena J, Racedo S, Alvarez S, Aguero G. Lactobacillus casei addition to a repletion diet-induced early normalisation of cytokine profils during a pneumococcal infection in malnourished mice. Food Agric Immunol. 2008; 19: 195–211. https://doi.org/10.1080/09540100802247243
10. Barbieri N, Villena J, Herrera M, Salva S, Alvarez S. Nasally Administered Lactobacillus rhamnosus Accelerate the Recovery of Humoral Immunity in B Lymphocyte-Deficient Malnourished Mice. J Nutr. 2013; 143: 227–235. https://doi.org/10.3945/jn.112.165811 PMID: 23269656
11. Herrera M, Salva S, Villena J, Barbieri N, Marranzino G, Alvarez S. Dietary supplementation with Lactobacilli improves emergency granulopoiesis in protein-malnourished mice and enhances respiratory innate immune response. PLoS One. 2014; 9. https://doi.org/10.1371/journal.pone.0090227 PMID: 24691464
12. Barbieri N, Villena J, Herrera M, Salva S, Alvarez S. Lactobacillus rhamnosus CRL1505 nasal administration improves recovery of T-cell mediated immunity against pneumococcal infection in malnourished mice. Benef Microbes. 2017;
13. Salva S, Nuñez M, Villena J, Ramón A, Font G, Alvarez S. Development of a fermented goats’ milk containing Lactobacillus rhamnosus: In vivo study of health benefits. J Sci Food Agric. 2011; 91: 2355–2362. https://doi.org/10.1002/jsfa.4467 PMID: 21604277
14. Villena J, Barbieri N, Salva S, Herrera M, Alvarez S. Enhanced immune response to pneumococcal infection in malnourished mice nasally treated with heat-killed Lactobacillus casei. Microbiol Immunol. 2009; 53: 636–646. https://doi.org/10.1111/j.1348-0421.2009.00171.x PMID: 19903264
15. Kolling Y, Salva S, Villena J, Marranzino G, Alvarez S. Non-viable immunobiotic Lactobacillus rhamnosus CRL1505 and its peptidoglycan improve systemic and respiratory innate immune response during recovery of immunocompromised-malnourished mice. Int Immunopharmacol. Elsevier B.V.; 2015; 25. https://doi.org/10.1016/j.intimp.2015.02.006 PMID: 25744605
16. Markowicz C, Kubiak P, Grajek W, Schmidt MT. Inactivation of Lactobacillus rhamnosus GG by fixation modifies its probiotic properties. Can J Microbiol. 2016; 62: 72–82. https://doi.org/10.1139/cjm-2015-0249 PMID: 26634746
17. Shida K, Kiyoshima-Shibata J, Kaji R, Nagaoka M, Nanno M. Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology. 2009; 128. https://doi.org/10.1111/j.13652567.2009.03095.x PMID: 19740347
18. Villena J, Chiba E, Tomosada Y, Salva S, Marranzino G, Kitazawa H, et al. Orally administered Lactobacillus rhamnosus modulates the respiratory immune response triggered by the viral pathogen-associated molecular pattern poly(I:C). BMC Immunol. BMC Immunology; 2012; 13: 53. https://doi.org/10.1186/1471-2172-13-53 PMID: 22989047
19. Racedo S, Villena J, Medina M, Agero G, Rodrguez V, Alvarez S. Lactobacillus casei administration reduces lung injuries in a Streptococcus pneumoniae infection in mice. Microbes Infect. 2006; 8: 2359–2366. https://doi.org/10.1016/j.micinf.2006.04.022 PMID: 16904925
20. Brouwer N, Dolman KM, van Houdt M, Sta M, Roos D, Kuijpers TW. Mannose-binding lectin (MBL) facilitates opsonophagocytosis of yeasts but not of bacteria despite MBL binding. J Immunol. 2008; 180: 4124–4132. https://doi.org/10.4049/jimmunol.180.6.4124 PMID: 18322223
21. Overweg K, Kerr A, Sluijter M, Jackson MH, Mitchell TJ, De Jong APJM, et al. The putative proteinase maturation protein A of Streptococcus pneumoniae is a conserved surface protein with potential to elicit protective immune responses. Infect Immun. 2000; 68: 4180–4188. https://doi.org/10.1128/IAI.68.7.4180–4188.2000 PMID: 10858235
22. Salva S, Merino MC, Agüero G, Gruppi A, Alvarez S. Dietary Supplementation with Probiotics Improves Hematopoiesis in Malnourished Mice. Ansari AA, editor. PLoS One. 2012; 7: e31171. https://doi.org/10.1371/journal.pone.0031171 PMID: 22347448
23. Levine AP, Segal AW. The NADPH Oxidase and Microbial Killing by Neutrophils, With a Particular Emphasis on the Proposed Antimicrobial Role of Myeloperoxidase within the Phagocytic Vacuole. Microbiol Spectr. 2016; 4: 1–14. https://doi.org/10.1128/microbiolspec.MCHD-0018-2015 PMID: 27726789
24. Kirby AC, Beattie L, Maroof A, van Rooijen N, Kaye PM. SIGNR1-negative red pulp macrophages protect against acute streptococcal sepsis after Leishmania donovani-induced loss of marginal zone macrophages. Am J Pathol. 2009; 175: 1107–15. https://doi.org/10.2353/ajpath.2009.090258 PMID: 19644016
25. Villena J, Salva S, Núñez M, Corzo J, Tolaba R, Faedda J, et al. Probiotics for Everyone! The Novel Immunobiotic Lactobacillus rhamnosus CRL1505 and the Beginning of Social Probiotic Programs in Argentina. Int J Biotechnol Wellness Ind. 2012; 1: 189–198.
26. Salva S, Villena J, Alvarez S. Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: Impact on intestinal and respiratory infections. Int J Food Microbiol. Elsevier B.V.; 2010; 141: 82–89. https://doi.org/10.1016/j.ijfoodmicro.2010.03.013 PMID: 20395002
27. Passera M, Pellicioli I, Corbellini S, Corno M, Vailati F, Bonanomi E, et al. Lactobacillus casei subsp. rhamnosus septicaemia in three patients of the paediatric intensive care unit. J Hosp Infect. 2016; 94: 361–362. https://doi.org/10.1016/j.jhin.2016.09.018 PMID: 28029469
28. Rodriguez A V, Baigorí MD, Alvarez S, Castro GR, Oliver G. Phosphatidylinositol-specific phospholi-pase C activity in Lactobacillus rhamnosus with capacity to translocate. FEMS Microbiol Lett. 2001; 204: 33–8. Available: http://www.ncbi.nlm.nih.gov/pubmed/11682174 PMID: 11682174
29. Tomosada Y, Chiba E, Zelaya H, Takahashi T, Tsukida K, Kitazawa H, et al. Nasally administered Lactobacillus rhamnosus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection. BMC Immunol. 2013; 14: 40. https://doi.org/10.1186/1471-2172-14-40 PMID: 23947615
30. Aktas B, De Wolfe TJ, Safdar N, Darien BJ, Steele JL. The Impact of Lactobacillus casei on the Composition of the Cecal Microbiota and Innate Immune System Is Strain Specific. Cappello F, editor. PLoS One. 2016; 11: e0156374. https://doi.org/10.1371/journal.pone.0156374 PMID: 27244133
31. Jensen H, Drømtorp SM, Axelsson L, Grimmer S. Immunomodulation of monocytes by probiotic and selected lactic Acid bacteria. Probiotics Antimicrob Proteins. 2015; 7: 14–23. https://doi.org/10.1007/s12602-014-9174-2 PMID: 25331988
32. Gwyer Findlay E, Hussell T. Macrophage-mediated inflammation and disease: a focus on the lung. Mediators Inflamm. 2012; 2012: 140937. https://doi.org/10.1155/2012/140937 PMID: 23304058
33. Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol. Nature Publishing Group; 2014; 14: 81–93. https://doi.org/10.1038/nri3600 PMID: 24445666
34. Aberdein JD, Cole J, Bewley MA, Marriott HM, Dockrell DH. Alveolar macrophages in pulmonary host defence the unrecognized role of apoptosis as a mechanism of intracellular bacterial killing. Clin Exp Immunol. Wiley-Blackwell; 2013; 174: 193–202. https://doi.org/10.1111/cei.12170 PMID: 23841514
35. Blok DC, Van Lieshout MHP, Hoogendijk AJ, Florquin S, De Boer OJ, Garlanda C, et al. Single immuno-globulin interleukin-1 receptor-related molecule impairs host defense during pneumonia and sepsis caused by streptococcus pneumoniae. J Innate Immun. 2014; 6: 542–552. https://doi.org/10.1159/000358239 PMID: 24556793
36. Karmakar M, Katsnelson M, Malak HA, Greene NG, Howell SJ, Hise AG, et al. Neutrophil IL-1β processing induced by pneumolysin is mediated by the NLRP3/ASC inflammasome and caspase-1 activation, and is dependent on K+ efflux. J Immunol. 2015; 194: 1–18. https://doi.org/10.4049/jimmunol.1401624 PMID: 25609842
37. Das R, LaRose MI, Hergott CB, Leng L, Bucala R, Weiser JN. Macrophage migration inhibitory factor promotes clearance of pneumococcal colonization. J Immunol. 2014; 193: 764–72. https://doi.org/10.4049/jimmunol.1400133 PMID: 24928996
38. Aslam A, Chapel H, Ogg G. Direct ex-vivo evaluation of pneumococcal specific T-cells in healthy adults. Borrow R, editor. PLoS One. 2011; 6: e25367. https://doi.org/10.1371/journal.pone.0025367 PMID: 22039412
39. Goldblatt D, Hussain M, Andrews N, Ashton L, Virta C, Melegaro A, et al. Antibody responses to naso-pharyngeal carriage of Streptococcus pneumoniae in adults: a longitudinal household study. J Infect Dis. 2005; 192: 387–93. https://doi.org/10.1086/431524 PMID: 15995951
40. Savino W, Dardenne M. Nutritional imbalances and infections affect the thymus: consequences on T-cell-mediated immune responses. Proc Nutr Soc. 2010; 69: 636–643. https://doi.org/10.1017/S0029665110002545 PMID: 20860857
41. Bandera A, Ferrario G, Saresella M, Marventano I, Soria A, Zanini F, et al. CD4+ T cell depletion, immune activation and increased production of regulatory T cells in the thymus of HIV-infected individuals. Ndhlovu LC, editor. PLoS One. 2010; 5: e10788. https://doi.org/10.1371/journal.pone.0010788PMID: 20520721
42. Malley R, Trzcinski K, Srivastava A, Thompson CM, Anderson PW, Lipsitch M. CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc Natl Acad Sci U S A. 2005; 102: 4848–53. https://doi.org/10.1073/pnas.0501254102 PMID: 15781870
43. Kiyono H, Fukuyama S. Nalt- versus peyer’s-patch-mediated mucosal immunity. Nat Rev Immunol. 2004; 4: 699–710. https://doi.org/10.1038/nri1439 PMID: 15343369
44. Shimosato T, Tomida K, Otani H. Effect of Lactobacillus pentosus ONRIC b0240 on Intestinal IgA Production in Mice Fed Differing Levels of Protein. J Agric Food Chem. 2011; 59: 2646–2651. https://doi.org/10.1021/jf104240d PMID: 21361374
45. Peñaloza HF, Nieto PA, Muñoz-Durango N, Salazar-Echegarai FJ, Torres J, Parga MJ, et al. Interleukin-10 plays a key role in the modulation of neutrophils recruitment and lung inflammation during infection by Streptococcus pneumoniae. Immunology. Wiley-Blackwell; 2015; 146: 100–12. https://doi.org/10.1111/imm.12486 PMID: 26032199
46. Sharma SK, Roumanes D, Almudevar A, Mosmann TR, Pichichero ME. CD4+ T-cell responses among adults and young children in response to Streptococcus pneumoniae and Haemophilus influenzae vaccine candidate protein antigens. Vaccine. 2013; 31: 3090–7. https://doi.org/10.1016/j.vaccine.2013.03.060 PMID: 23632305
47. Marranzino G, Villena J, Salva S, Alvarez S. Stimulation of macrophages by immunobiotic Lactobacillus strains: influence beyond the intestinal tract. Microbiol Immunol. 2012; 56: 771–781. https://doi.org/10.1111/j.1348-0421.2012.00495.x PMID: 22846065
48. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci. 2011; 108: 5354–5359. https://doi.org/10.1073/pnas.1019378108 PMID: 21402903
49. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med. 2010; 16: 228–231. https://doi.org/10.1038/nm.2087 PMID: 20081863