The role of beneficial bacteria wall elasticity in regulating innate immune response

EPMA Journal

Volumn 6, Issue 1, 2015, Pages

  Mokrozub, Viktoria V ^a   Lazarenko, Liudmyla M ^a   Sichel, Liubov M ^b   Babenko, Lidia P ^a   Lytvyn, Petro M ^c   Demchenko, Olga M ^d   Melnichenko, Yulia O ^a   Boyko, Nadiya V ^a   Biavati, Bruno ^e   Di Gioia, Diana ^e   Bubnov, Rostyslav V ^a,f   Spivak, Mykola Ya ^a,d  

^a ZABOLOTNY INSTITUTE OF MICROBIOLOGY AND VIROLOGY   (Ukraine)

^b Pure Research Products LLC   (United States)

^c INSTITUTE OF SEMICONDUCTOR PHYSICS   (Ukraine)

^d LCL Diaprof   (Ukraine)

^e UNIVERSITY OF BOLOGNA   (Italy)

^f Clinical Hospital Pheophania of State Affairs Department   (Ukraine)

Author keywords

and personalized medicine; Atomic force microscopy; Bifidobacterium; Cancer; Cell wall elasticity; Cytokines; Dietary biomarkers; Fecal microbiota transplantation; Gut microbiota; Gut brain axis; Healthy diet; Immune disorders; Lactobacillus; Macrophages; Microbiome; nitrosative stress; Nutrition; Oxidative; Pattern recognition receptors; Predictive; preventive

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; NITRIC OXIDE; PROBIOTIC AGENT;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ELASTICITY; HOST PATHOGEN INTERACTION; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSTIMULATION; IN VITRO STUDY; INNATE IMMUNITY; LACTIC ACID BACTERIUM; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; MACROPHAGE ACTIVATION; MACROPHAGE CULTURE; MACROPHAGE FUNCTION; MOUSE; NITROGEN METABOLISM; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; RIGIDITY; SPECIES DIFFERENCE;

EID: 84934991355     PISSN: 18785077     EISSN: 18785085     Source Type: Journal    
DOI: 10.1186/s13167-015-0035-1     Document Type: Article

References (70)

1. Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol. 2011;12(1):5-9. doi: 10.1038/ni0111-5 .
2. Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989;299:1259-60.
3. Toh ZQ, Anzela A, Tang ML, Licciardi PV. Probiotic therapy as a novel approach for allergic disease. Front Pharmacol. 2012;3:171.
4. Wills-Karp M, Santeliz J, Karp CL. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol. 2001;1:69-75.
5. Nemcová R. Criteria for selection of lactobacilli for probiotic use. Vet Med (Praha). 1997;42(1):19-27.
6. Polak-Berecka M, Waśko A, Paduch R, Skrzypek T, Sroka-Bartnicka A. The effect of cell surface components on adhesion ability of Lactobacillus rhamnosus. Antonie Van Leeuwenhoek. 2014;106(4):751-62. doi: 10.1007/s10482-014-0245-x .
7. Zeuthen LH, Fink LN, Frøkiaer H. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells. Immunology. 2008;124(4):489-502. doi: 10.1111/j.1365-2567.2007.02800.x .
8. Bron PA, van Baarlen P, Kleerebezem M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol. 2012;10(1):66-78.
9. Sánchez B, Schmitter JM, Urdaci MC. Identification of novel proteins secreted by Lactobacillus rhamnosus GG grown in de Mann-Rogosa-Sharpe broth. Lett Appl Microbiol. 2009;48(5):618-22. doi: 10.1111/j.1472-765X.2009.02579.x .
10. Sánchez B, Schmitter JM, Urdaci MC. Identification of novel proteins secreted by Lactobacillus plantarum that bind to mucin and fibronectin. J Mol Microbiol Biotechnol. 2009;17(3):158-62. doi: 10.1159/000233579 .
11. Dijkstra AJ, Keck W. Peptidoglycan as a barrier to transenvelope transport. J Bacteriol. 1996;178(19):5555-62.
12. Deepika G, Green RJ, Frazier RA, Charalampopoulos D. Effect of growth time on the surface and adhesion properties of Lactobacillus rhamnosus GG. J Appl Microbiol. 2009;107(4):1230-40.
13. Deepika G, Karunakaran E, Hurley CR, Biggs CA, Charalampopoulos D. Influence of fermentation conditions on the surface properties and adhesion of Lactobacillus rhamnosus GG. Microb Cell Fact. 2012;11:116.
14. Dziarski R, Gupta D. Staphylococcus aureus peptidoglycan is a Toll-like receptor 2 activator: a reevaluation. Infect Immun. 2005;73:5212-6.
15. Travassos LH, Girardin SE, Philpott DJ, Blanot D, Nahori MA, Werts C, et al. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep. 2004;5:1000-6.
16. Volz T, Nega M, Buschmann J, Kaesler S, Guenova E, Peschel A, et al. Natural Staphylococcus aureus-derived peptidoglycan fragments activate NOD2 and act as potent co-stimulators of the innate immune system exclusively in the presence of TLR signals. FASEB J. 2010;24:4089-102.
17. Asong J, Wolfert MA, Maiti KK, Miller D, Boons GJ. Binding and cellular activation studies reveal that Toll-like receptor 2 can differentially recognize peptidoglycan from Gram-positive and Gram-negative bacteria. J Biol Chem. 2009;284:8643-53.
18. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335-76.
19. Maliničová L, Piknová M, Pristaš P, Javorský P. Peptidoglycan hydrolases as novel tool for anti-enterococcal therapy. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. The Formatex Microbiology Book Series. 2010, Volume, 1. Access mode: http://www.formatex.info/microbiology2/463-472.pdf Accessed 5 May 2015.
20. Ruas-Madiedo P, Gueimonde M, Margolles A, delos Reyes-Gavilán CG, Salminen SJ. Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. Food Prot. 2006;69(8):2011-5.
21. Sengupta R, Altermann E, Anderson RC, McNabb WC, Moughan PJ, Roy NC. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators Inflamm. 2013;2013:237921.
22. Mohamadzadeh M, Pfeiler EA, Brown JB, Zadeh M, Gramarossa M, Managlia E, et al. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4623-30.
23. Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P. The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek. 1999;76(1-4):159-84.
24. Wells JM. mmunomodulatory mechanisms of lactobacilli. Microb Cell Fact. 2011;10 Suppl 1:S17.
25. Chapot-Chartier MP, Kulakauskas S. Cell wall structure and function in lactic acid bacteria. Microb Cell Fact. 2014;13 Suppl 1:S9.
26. Derkx PM, Janzen T, Sørensen KI, Christensen JE, Stuer-Lauridsen B, Johansen E. The art of strain improvement of industrial lactic acid bacteria without the use of recombinant DNAtechnology. Microb Cell Fact. 2014;13 Suppl 1:S5. doi: 10.1186/1475-2859-13-S1-S5 .
27. de Goffau MC, Luopajärvi K, Knip M, Ilonen J, Ruohtula T, Härkönen T, et al. Fecal microbiota composition differs between children with β-cell autoimmunity and those without. Diabetes. 2013;62(4):1238-44. doi: 10.2337/db12-0526 .
28. West CE, Renz H, Jenmalm MC, Kozyrskyj AL, Allen KJ, Vuillermin P, et al. The gut microbiota and inflammatory noncommunicable diseases: associations and potentials for gutmicrobiota therapies. J Allergy Clin Immunol. 2015;135(1):3-13. doi: 10.1016/j.jaci.2014.11.012 . quiz 14.
29. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, et al. The extracellular biology of the lactobacilli. FEMS Microbiol Rev. 2010;34(2):199-230. doi: 10.1111/j.1574-6976.2010.00208.x .
30. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, et al. Enhanced anti-inflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoicacids. Proc Natl Acad Sci U S A. 2005;102(29):10321-6.
31. Wyckoff TJ, Taylor JA, Salama NR. Beyond growth: novel functions for bacterial cell wall hydrolases. Trends Microbiol. 2012;20(11):540-7. doi: 10.1016/j.tim.2012.08.003 .
32. MiragliadelGiudice M, De Luca MG. The role of probiotics in the clinical management of food allergy and atopic dermatitis. J Clin Gastroenterol. 2004;38(6 Suppl):S84-5.
33. Pinto MV, Rodriguez Gómez M, Seifert S, Watzl B, Holzapfe WH, Franz C. Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol. 2009;133(1-2):86-93.
34. Tymoshok NO, Lazarenko LM, Bubnov RV, Shynkarenko LN, Babenko LP, Mokrozub VV, et al. New aspects the regulation of immune response through balance Th1/Th2 cytokines. EPMA J. 2014;5 Suppl 1:A134.
35. Dabbagh K, Lewis DB. Toll-like receptors and T-helper-1/T-helper-2 responses. Curr Opin Infect Dis. 2003;16(3):199-204.
36. 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(2):259-66.
37. Vinderola G, Matar C, Perdigon G. Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: involvement of Toll-like receptors. Clin Diagn Lab Immunol. 2005;12(9):1075-84.
38. Shida K, Kiyoshima-Shibata J, Nagaoka M, Watanabe K, Nanno M. Induction of interleukin-12 by Lactobacillus strains having a rigid cell wall resistant to intracellular. digestion. J Dairy Sci. 2006;89(9):3306-17.
39. Yasuda E, Serata M, Sako T. Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl Environ Microbiol. 2008;74(15):4746-55.
40. Butt HJ, Cappella B, Kappl M. Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep. 2005;59(1):1-152.
41. Schaer-Zammaretti P, Ubbink J. Imaging of lactic acid bacteria with AFM-elasticity and adhesion maps and their relationship to biological and structural data. Ultramicroscopy. 2003;97(1-4):199-208.
42. Reznikov O. The problem of ethics in carrying out of experimental medical and biological research on animals. Bulletin of the National Academy of Sciences of Ukraine. 2001;1:5-7.
43. Alonso JL, Goldmann WH. Feeling the forces: atomic force microscopy in cell biology. Life Sci. 2003;72(23):2553-60.
44. Metelska VA, Tumanova NG. Screening-method of determining the level of nitric oxide metabolites in blood serum. Clinical and laboratory diagnostics. 2005;6:15-8.
45. Grachev MP. Definition of bactericidal power of alveolar macrophages with NBT-test. JMEI. 1984;2:87-8.
46. Vinckier A, Semenza G. Measuring elasticity of biological materials by atomic force microscopy. FEBS Lett. 1998;430(1-2):12-6.
47. Babenko LP, Lazarenko LM, Shynkarenko LM, Mokrozub VV, Pidgorskyi VS, Spivak MJ. The effect of Lacto- and Bifidobacteria in monoculture on the vaginal microflora in norm and in cases of intravaginal staphylococcosis. Mikrobiol Z. 2013;75(3):46-55.
48. Popova P, Guencheva G, Davidkova G, Bogdanov A, Pacelli E, Opalchenova G, et al. Stimulating effect of DEODAN (an oral preparation from Lactobacillus bulgaricus LB 51) on monocites/macrophages and host resistance to experimental infections. Int J Immunopharmacol. 1993;15(1):25-37.
49. Perdigon G, de Macias ME, Alvarez S, Oliver G, de Ruiz Holgado AA. Effect of perorally administered lactobacilli on macrophage activation in mice. Infect Immun. 1986;53(2):404-10.
50. Kim DW, Cho SB, Yun CH, Jeong HY, Chung WT, Choi CW, et al. Induction of cytokines and nitric oxide in murine macrophages stimulated with enzymatically digested lactobacillus strains. J Microbiol. 2007;45(5):373-8.
51. Schär-Zammaretti P, Ubbink J. The cell wall of lactic acid bacteria: surface constituents and macromolecular conformations. Biophys J. 2003;85(6):4076-92.
52. Ruas-Madiedo P, Hugenholtz J, Zoon P. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. J Dairy Sci. 2003;86(2):407-23.
53. Spivak M, Pidhorskyy V, Shynkarenko, L. Gorchakov V, Starovoitova S, Lazarenko L, Timoshok N: Lactobacillus casei IMV B-7280 strain-inductor of the late interferon and macrophages activator. Patent Ukraine N 93133. IPC (2011.01) C12N 1/20 C12R 1/23 (2006.01) A61K 35/74 (2006.01), issued 10.01.2011, (Bull. N 1).
54. Spivak M, Pidhorskyy V, Shynkarenko, L. Gorchakov V, Starovoitova S, Lazarenko L, Timoshok N: Lactobacillus acidophilus IMV B-7279 strain-inductor of the I type endogenous interferon Patent Ukraine N 93132. IPC (2011.01) C12N 1/20 C12R 1/23 (2006.01) A61K 35/74 (2006.01), issued 10.01.2011, (Bull. N 1).
55. Liu CF, Tseng KC, Chiang SS, Lee BH, Hsu WH, Pan TM. Immunomodulatory and antioxidant potential of Lactobacillus exopolysaccharides. J Sci Food Agric. 2011;91(12):2284-91.
56. Tejada-Simon MV, Pestka JJ. Proinflammatory cytokine and nitric oxide induction in murine macrophages by cell wall and cytoplasmic extracts of lactic acid bacteria. J Food Prot. 1999;62(12):1435-44.
57. Cross ML, Ganner A, Teilab D, Fray LM. Patterns of cytokine induction by gram- positive and gram-negative probiotic bacteria. FEMS Immunol Med Microbiol. 2004;42(2):173-80.
58. Murata K, Tomosada Y, Villena J, Chiba E, Shimazu T, Aso H, et al. Bifidobacterium breve MCC-117 induces tolerance in porcine intestinal epithelial cells: study of the mechanisms involved in the immunoregulatory effect. Biosci Microbiota Food Health. 2014;33(1):1-10.
59. You J, Dong H, Mann ER, Knight SC, Yaqoob P. Probiotic modulation of dendritic cell function is influenced by ageing. Immunobiology. 2014;219(2):138-48.
60. Adams CA. The probiotic paradox: live and dead cells are biological response modifiers. Nutr Res Rev. 2010;23(1):37-46. doi: 10.1017/S0954422410000090 .
61. Reid G. The importance of guidelines in the development and application of probiotics. Curr Pharm Des. 2005;11:11-6.
62. Marzorati M, Possemiers S, Verstraete W. The use of the SHIME-related technology platform to assess the efficacy of pre- and probiotics. Agro Food Ind Hi-Tech. 2009;20:S50-3.
63. Obataya I, Nakamura C, Han S, Nakamura N, Miyake J. Nanoscale operation of a living cell using an atomic force microscope with a nanoneedle. Nano Lett. 2005;5(1):27-30.
64. Golubnitschaja O, Costigliola V. EPMA. EPMA summit 2014 under the auspices of the presidency of Italy in the EU: professional statements. EPMA J. 2015;6:4.
65. Zijlstra S, Gunawan J, Freytag C, Burchert W. Synthesis and evaluation of fluorine-18 labelled compounds for imaging of bacterial infections with pet. Appl Radiat Isot. 2006;64(7):802-7.
66. Wang H, Machtaler S, Bettinger T, Lutz AM, Luong R, Bussat P, et al. Molecular imaging of inflammation in inflammatory bowel disease with a clinically translatable dual-selectin-targeted US contrast agent: comparison with FDG PET/CT in a mouse model. Radiology. 2013;267(3):818-29.
67. Karunatilaka KS, Cameron EA, Martens EC, Koropatkin NM, Biteen JS. Superresolution imaging captures carbohydrate utilization dynamics in human gut symbionts. MBio. 2014;5(6), e02172. doi: 10.1128/mBio.02172-14 .
68. Blow N. In vivo molecular imaging: the inside job. Nat Methods. 2009;6(6):465-9.
69. Honka H, Mäkinen J, Hannukainen JC, Tarkia M, Oikonen V, Teräs M, et al. Validation of [18F] fluorodeoxyglucose and positron emission tomography (PET) for the measurement of intestinal metabolism in pigs, and evidence of intestinal insulin resistance in patients with morbid obesity. Diabetologia. 2013;56(4):893-900.
70. Ding S, Chi MM, Scull BP, Rigby R, Schwerbrock NM, Magness S, et al. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One. 2010;5(8):e12191.