1887
  1. Home
  2. Publications
  3. Journal of Medical Microbiology
  4. Volume 64, Issue 12
  5. Article

f Probiotic attributes, antioxidant, anti-inflammatory and neuromodulatory effects of CFR 3003: and evidence

HTML
146.73 Kb
PDF
658.30 Kb
  • Authors: G. Divyashri1​ ,2​ ,  G. Krishna3​ ,  Muralidhara3​ , S. G. Prapulla2​
    • VIEW AFFILIATIONS
    • 1​ 1​ Academy of Scientific and Innovative Research (AcSIR), New Delhi, India 2​ 2​ Microbiology and Fermentation Technology Department, CSIR-Central Food Technological Research Institute (CFTRI), Karnataka, Mysore 570 020, India 3​ 3​ Biochemistry and Nutrition Department, CSIR-Central Food Technological Research Institute (CFTRI), Karnataka, Mysore 570 020, India
  • S. G. Prapulla [email protected]
  • First Published Online: 01 December 2015, Journal of Medical Microbiology 64: 1527-1540, doi: 10.1099/jmm.0.000184
  • Subject: Prevention and Therapy
  • Received:
  • Accepted:
  • Cover date:
Preview this:
Free Preview thumbnail Magnify
Zoom in
Zoomout

Probiotic attributes, antioxidant, anti-inflammatory and neuromodulatory effects of CFR 3003: and evidence, Page 1 of 1

| /docserver/preview/fulltext/jmm/64/12/1527_jmm000184-1.gif

  • Accumulating evidence suggests that probiotic bacteria play a vital role in modulating various aspects integral to the health and well-being of humans. In the present study, probiotic attributes and the antioxidant, anti-inflammatory and neuromodulatory potential of CFR 3003 were investigated by employing suitable model systems. exhibited robust resistance to gastrointestinal stress conditions as it could withstand acid stress at pH 1.5, 2 and 3. The bacterium also survived at a bile salt concentration of 0.45 %, and better tolerance was observed towards pepsin and trypsin. produced lactic acid as a major metabolic product, followed by butyric acid. Lyophilized cell-free supernatant (LCS) of exhibited significant antioxidant capacity evaluated against 1,1-diphenyl-2-picryl-hydrazyl, ascorbate auto-oxidation, oxygen radical absorbance and reducing power. Interestingly, , GG MTCC 1408 and LCS showed a significant anti-inflammatory effect by negatively modulating TNF-α production and upregulating IL-10 levels in LPS-stimulated macrophage cell lines. In an mice model, the propensity of probiotic supplements to modulate endogenous oxidative markers and redox status in brain regions was assessed. Young mice provided with oral supplements (daily for 28 days) of and exhibited diminished oxidative markers in the brain and enhanced activities of antioxidant enzymes with a concomitant increase in γ-aminobutyric acid and dopamine levels. Collectively, our findings clearly suggest the propensity of these bacteria to protect against tissue damage mediated through free radicals and inflammatory cytokines. Although the underlying molecular mechanisms need further studies, it is tempting to speculate that probiotics confer a neuroprotective advantage against oxidative damage-mediated neurodegenerative conditions.

  • Abbreviations:
    AChE acetylcholine esterase
    CAT catalase
    DA dopamine
    DCF 2′,7′-dichlorofluorescein
    DPPH 1,1-diphenyl-2-picryl-hydrazyl
    GABA γ-aminobutyric acid
    GSH glutathione
    GST glutathione -transferase
    LCS lyophilized cell-free supernatant
    ORAC oxygen radical absorbance capacity
    ROS reactive oxygen species
    TCA trichloroacetic acid
    TE Trolox equivalent

© 2015 The Authors | Published by the Microbiology Society

  • Aebi H. . ( 1984;). Catalase in vitro. Methods Enzymol 105: 121––126 [CrossRef] [PubMed].
     [Google Scholar]
  • Afify A.E.M.R. , Romeilah R. M. , Sultan S. I. M. , Hussein M. M. . ( 2012;). Antioxidant activity and biological evaluations of probiotic bacteria strains. Int J Acad Res Part A 4: 131––139.[CrossRef]
    [Google Scholar]
  • Ahire J. J. , Mokashe N. U. , Patil H. J. , Chaudhari B. L. . ( 2013;). Antioxidative potential of folate producing probiotic Lactobacillus helveticus CD6. J Food Sci Technol 50: 26––34 [CrossRef] [PubMed].
     [Google Scholar]
  • Andersen J. K. . ( 2004;). Oxidative stress in neurodegeneration: cause or consequence?. Nat Med 10: S18––S25 [CrossRef] [PubMed].
     [Google Scholar]
  • Araújo T. F. , Ferreira C. . ( 2013;). The genus Enterococcus as probiotic: safety concerns. Braz Arch Biol Technol 56: 457––466 [CrossRef].
     [Google Scholar]
  • Balish E. , Warner T. . ( 2002;). Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 160: 2253––2257 [CrossRef] [PubMed].
     [Google Scholar]
  • Benyacoub J. , Czarnecki-Maulden G. L. , Cavadini C. , Sauthier T. , Anderson R. E. , Schiffrin E. J. , Weid T. . ( 2003;). Supplementation of food with Enterococcus faecium (SF68) stimulates immune functions in young dogs.. J Nutr 133 1158––1162.
     [Google Scholar]
  • Bhardwaj A. , Kapila S. , Mani J. , Malik R. K. . ( 2009;). Comparison of susceptibility to opsonic killing by in vitro human immune response of Enterococcus strains isolated from dairy products, clinical samples and probiotic preparation. Int J Food Microbiol 128: 513––515 [CrossRef] [PubMed].
     [Google Scholar]
  • Bravo J. A. , Forsythe P. , Chew M. V. , Escaravage E. , Savignac H. M. , Dinan T. G. , Bienenstock J. , Cryan J. F. . ( 2011;). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 108: 16050––16055 [CrossRef] [PubMed].
     [Google Scholar]
  • Brestoff J. R. , Artis D. . ( 2013;). Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 14: 676––684 [CrossRef] [PubMed].
     [Google Scholar]
  • Calabrese V. , Cornelius C. , Dinkova-Kostova A. T. , Iavicoli I. , Di Paola R. , Koverech A. , Cuzzocrea S. , Rizzarelli E. , Calabrese E. J. . ( 2012;). Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochim Biophys Acta 1822: 753––783 [CrossRef] [PubMed].
     [Google Scholar]
  • Cao G. , Prior R. L. . ( 1999;). Measurement of oxygen radical absorbance capacity in biological samples. Methods Enzymol 299: 50––62 [CrossRef] [PubMed].
     [Google Scholar]
  • Caradonna L. , Amati L. , Magrone T. , Pellegrino N. M. , Jirillo E. , Caccavo D. . ( 2000;). Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 6: 205––214 [PubMed].
     [Google Scholar]
  • Carasi P. , Díaz M. , Racedo S. M. , de Antoni G. , Urdaci M. C. , de Los M. , Serradell A. . ( 2014;) Safety characterization and antimicrobial properties of kefir-isolated Lactobacillus kefiri . BioMed Res Int 2014: [CrossRef] [PubMed].
     [Google Scholar]
  • Chen S. , Fu Y. , Liu L. L. , Gao W. , Liu Y. L. , Fei S. H. , Tan Y. , Zou K. F. . ( 2014;). Live combined Bacillus subtilis and Enterococcus faecium ameliorate murine experimental colitis by immunosuppression. Int J Inflamm 2014: 878054 [CrossRef] [PubMed].
     [Google Scholar]
  • Cryan J. F. , Dinan T. G. . ( 2012;). Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13: 701––712 [CrossRef] [PubMed].
     [Google Scholar]
  • Cummings J. H. , Branch W. J. . ( 1982;). Postulated mechanisms whereby fibre may protect against large bowel cancer. . In Dietary Fiber in Health and Disease, pp. 313––325. Edited by Vahouney G. V. , Kritchevsky D. . New York: Plenum Press; [CrossRef].
     [Google Scholar]
  • Dalle-Donne I. , Scaloni A. , Giustarini D. , Cavarra E. , Tell G. , Lungarella G. , Colombo R. , Rossi R. , Milzani A. . ( 2005;). Proteins as biomarkers of oxidative/nitrosative stress in diseases: the contribution of redox proteomics. Mass Spectrom Rev 24: 55––99 [CrossRef] [PubMed].
     [Google Scholar]
  • Dalpiaz A. , Filosa R. , de Caprariis P. , Conte G. , Bortolotti F. , Biondi C. , Scatturin A. , Prasad P. D. , Pavan B. . ( 2007;). Molecular mechanism involved in the transport of a prodrug dopamine glycosyl conjugate. Int J Pharm 336: 133––139 [CrossRef] [PubMed].
     [Google Scholar]
  • Desbonnet L. , Garrett L. , Clarke G. , Bienenstock J. , Dinan T. G. . ( 2008;). The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 43: 164––174 [CrossRef] [PubMed].
     [Google Scholar]
  • Diaz Heijtz R. , Wang S. , Anuar F. , Qian Y. , Björkholm B. , Samuelsson A. , Hibberd M. L. , Forssberg H. , Pettersson S. . ( 2011;). Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 108: 3047––3052 [CrossRef] [PubMed].
     [Google Scholar]
  • Divyashri G. , Prapulla S. G. . ( 2015a;). An insight into kinetics and thermodynamics of gamma-aminobutyric acid production by Enterococcus faecium CFR 3003 in batch fermentation. Ann Microbiol 65: 1109––1118 [CrossRef].
     [Google Scholar]
  • Divyashri G. , Prapulla S. G. . ( 2015b;). Mass transfer characterization of gamma-aminobutyric acid production by Enterococcus faecium CFR 3003: encapsulation improves its survival under simulated gastro-intestinal conditions. Bioprocess Biosyst Eng 38: 569––574 [CrossRef] [PubMed].
     [Google Scholar]
  • Dixit G. , Samarth D. , Tale V. , Bhadekar R. . ( 2013;). Comparitive studies on potential probiotic characteristics of Lactobacillus acidophilus strains. EurAsian J BioSci 7: 1––9 [CrossRef].
     [Google Scholar]
  • Ellman G. L. , Courtney K. D. , Andres V. Jr , Feather-Stone R. M. . ( 1961;). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88––95 [CrossRef] [PubMed].
     [Google Scholar]
  • Flohé L. , Günzler W. A. . ( 1984;). Assays of glutathione peroxidase. Methods Enzymol 105: 114––121 [CrossRef] [PubMed].
     [Google Scholar]
  • Foulquié Moreno M. R. , Sarantinopoulos P. , Tsakalidou E. , De Vuyst L. . ( 2006;). The role and application of enterococci in food and health. Int J Food Microbiol 106: 1––24 [CrossRef] [PubMed].
     [Google Scholar]
  • Franz C.M.A.P. , Huch M. , Abriouel H. , Holzapfel W. , Gálvez A. . ( 2011;). Enterococci as probiotics and their implications in food safety. Int J Food Microbiol 151: 125––140 [CrossRef] [PubMed].
     [Google Scholar]
  • Gaggia F. , Mattarelli P. , Biavati B. . ( 2010;). Probiotics and prebiotics in animal feeding for safe food production. Int J Food Microbiol 141: S15––S28.[CrossRef]
    [Google Scholar]
  • Gagnon M. , Savard P. , Rivière A. , LaPointe G. , Roy D. . ( 2015;). Bioaccessible antioxidants in milk fermented by Bifidobacterium longum subsp. longum strains. BioMed Res Int 2015: [CrossRef] [PubMed].
     [Google Scholar]
  • Gangaraju D. , Murty V. R. , Prapulla S. G. . ( 2014;). Probiotic-mediated biotransformation of monosodium glutamate to γ-aminobutyric acid: differential production in complex and minimal media and kinetic modelling. Ann Microbiol 64: 229––237 [CrossRef].
     [Google Scholar]
  • Gardner H. W. . ( 1975;). Decomposition of linoleic acid hydroperoxides. Enzymic reactions compared with nonenzymic. J Agric Food Chem 23: 129––136 [CrossRef] [PubMed].
     [Google Scholar]
  • Giraffa G. . ( 2003;). Functionality of enterococci in dairy products. Int J Food Microbiol 88: 215––222 [CrossRef] [PubMed].
     [Google Scholar]
  • Gokul K. , Muralidhara . ( 2014;). Oral supplements of aqueous extract of tomato seeds alleviate motor abnormality, oxidative impairments and neurotoxicity induced by rotenone in mice: relevance to Parkinson's disease. Neurochem Res 39: 1382––1394 [CrossRef] [PubMed].
     [Google Scholar]
  • Hosamani R. , Krishna G. , Muralidhara . , ( 2014;).[PubMed] Standardized Bacopa monnieri extract ameliorates acute paraquat-induced oxidative stress, and neurotoxicity in prepubertal mice brain. Nutr Neurosci [CrossRef] [Epub ahead of print].
     [Google Scholar]
  • Huang D. , Ou B. , Hampsch-Woodill M. , Flanagan J. A. , Prior R. L. . ( 2002;). High-throughput assay of oxygen radical absorbance capacity (ORAC) using a multichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format. J Agric Food Chem 50: 4437––4444 [CrossRef] [PubMed].
     [Google Scholar]
  • Ishibashi N. , Yamazaki S. . ( 2001;). Probiotics and safety. Am J Clin Nutr 73: (Suppl.), 465S––470S [PubMed].
     [Google Scholar]
  • Kiffin R. , Bandyopadhyay U. , Cuervo A. M. . ( 2006;). Oxidative stress and autophagy. Antioxid Redox Signal 8: 152––162 [CrossRef] [PubMed].
     [Google Scholar]
  • Lei M. , Dai X. , Liu M. . ( 2014;). Biological characteristics and safety examination of five enterococcal strains from probiotic products. J Food Saf 35: 324––335 [CrossRef].
     [Google Scholar]
  • Levine R. L. , Garland D. , Oliver C. N. , Amici A. , Climent I. , Lenz A. G. , Ahn B. W. , Shaltiel S. , Stadtman E. R. . ( 1990;). Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186: 464––478 [CrossRef] [PubMed].
     [Google Scholar]
  • Lewenstein A. , Frigerio G. , Moroni M. . ( 1979;). Biological properties of SF68, a new approach for the treatment of diarrhoeal diseases. Curr Ther Res 26: 967––981.
     [Google Scholar]
  • Lin M. Y. , Yen C. L. . ( 1999;). Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47: 1460––1466 [CrossRef] [PubMed].
     [Google Scholar]
  • Litteljohn D. , Mangano E. N. , Hayley S. . ( 2008;). Cyclooxygenase-2 deficiency modifies the neurochemical effects, motor impairment and co-morbid anxiety provoked by paraquat administration in mice. Eur J Neurosci 28: 707––716 [CrossRef] [PubMed].
     [Google Scholar]
  • Lorea Baroja M. , Kirjavainen P. V. , Hekmat S. , Reid G. . ( 2007;). Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin Exp Immunol 149: 470––479 [CrossRef] [PubMed].
     [Google Scholar]
  • Lowry O. H. , Rosebrough N. J. , Farr A. L. , Randall R. J. . ( 1951;). Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265––275 [PubMed].
     [Google Scholar]
  • Lyte M. . ( 2011;). Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. BioEssays 33: 574––581 [CrossRef] [PubMed].
     [Google Scholar]
  • Messaoudi M. , Lalonde R. , Violle N. , Javelot H. , Desor D. , Nejdi A. , Bisson J.-F. , Rougeot C. , Pichelin M. , other authors . ( 2011;). Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 105: 755––764 [CrossRef] [PubMed].
     [Google Scholar]
  • Mokrasch L. C. , Teschke E. J. . ( 1984;). Glutathione content of cultured cells and rodent brain regions: a specific fluorometric assay. Anal Biochem 140: 506––509 [CrossRef] [PubMed].
     [Google Scholar]
  • Moreadith R. W. , Fiskum G. . ( 1984;). Isolation of mitochondria from ascites tumor cells permeabilized with digitonin. Anal Biochem 137: 360––367 [CrossRef] [PubMed].
     [Google Scholar]
  • O'Mahony L. , McCarthy J. , Kelly P. , Hurley G. , Luo F. , Chen K. , O'Sullivan G. C. , Kiely B. , Collins J. K. , other authors . ( 2005;). Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128: 541––551 [CrossRef] [PubMed].
     [Google Scholar]
  • Okada Y. , Tsuzuki Y. , Hokari R. , Komoto S. , Kurihara C. , Kawaguchi A. , Nagao S. , Miura S. . ( 2009;). Anti-inflammatory effects of the genus Bifidobacterium on macrophages by modification of phospho-IκB and SOCS gene expression. Int J Exp Pathol 90: 131––140 [CrossRef] [PubMed].
     [Google Scholar]
  • Petrof E. O. . ( 2009;). Probiotics and gastrointestinal disease: clinical evidence and basic science. Antiinflamm Antiallergy Agents Med Chem 8: 260––269 [CrossRef] [PubMed].
     [Google Scholar]
  • Pieniz S. , Andreazza R. , Anghinoni T. , Camargo F. , Brandelli A. . ( 2014;). Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Contr 37: 251––256 [CrossRef].
     [Google Scholar]
  • Playne M. . ( 1994;). Probiotic foods. J Food Aust 46: 362.
     [Google Scholar]
  • Ramalakshmi K. , Rao L. J. M. , Takano-Ishikawa Y. , Goto M. . ( 2009;). Bioactivities of low-grade green coffee and spent coffee in different in vitro model systems. Food Chem 115: 79––85 [CrossRef].
     [Google Scholar]
  • Savignac H. M. , Kiely B. , Dinan T. G. , Cryan J. F. . ( 2014;). Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 26: 1615––1627 [CrossRef] [PubMed].
     [Google Scholar]
  • Stecher B. , Hardt W. D. . ( 2008;). The role of microbiota in infectious disease. Trends Microbiol 16: 107––114 [CrossRef] [PubMed].
     [Google Scholar]
  • Sun P. , Wang J. , Jiang Y. . ( 2010;). Effect of Enterococcus faecium (SF68) on immune function in mice. Food Chem 123: 63––68 [CrossRef].
     [Google Scholar]
  • Szabó I. , Wieler L. H. , Tedin K. , Scharek-Tedin L. , Taras D. , Hensel A. , Appel B. , Nöckler K. . ( 2009;). Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica serovar Typhimurium DT104 infection in a porcine animal infection model. Appl Environ Microbiol 75: 2621––2628 [CrossRef] [PubMed].
     [Google Scholar]
  • Tan Q. , Xu H. , Aguilar Z. P. , Peng S. , Dong S. , Wang B. , Li P. , Chen T. , Xu F. , Wei H. . ( 2013;). Safety assessment and probiotic evaluation of Enterococcus faecium YF5 isolated from sourdough. J Food Sci 78: M587––M593 [CrossRef] [PubMed].
     [Google Scholar]
  • Tsai S. Y. , Huang S. J. , Mau J. L. . ( 2006;). Antioxidant properties of hot water extracts from Agrocybe cylindracea. Food Chem 98: 670––677 [CrossRef].
     [Google Scholar]
  • Woo J. Y. , Gu W. , Kim K. A. , Jang S. E. , Han M. J. , Kim D. H. . ( 2014;). Lactobacillus pentosus var. plantarum C29 ameliorates memory impairment and inflammaging in a d-galactose-induced accelerated aging mouse model. Anaerobe 27: 22––26 [CrossRef] [PubMed].
     [Google Scholar]
  • Wu M.-H. , Pan T.-M. , Wu Y.-J. , Chang S.-J. , Chang M.-S. , Hu C.-Y. . ( 2010;). Exopolysaccharide activities from probiotic bifidobacterium: immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int J Food Microbiol 144: 104––110 [CrossRef] [PubMed].
     [Google Scholar]
  • Wunderlich P. F. , Braun L. , Fumagalli I. , D'Apuzzo V. , Heim F. , Karly M. , Lodi R. , Politta G. , Vonbank F. , Zeltner L. . ( 1989;). Double-blind report on the efficacy of lactic acid-producing Enterococcus SF68 in the prevention of antibiotic-associated diarrhoea and in the treatment of acute diarrhoea. J Int Med Res 17: 333––338 [PubMed].
     [Google Scholar]
http://sgm.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000184
Loading

Supplementary Data

 Data loading....

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000184
2015-12-01
2019-05-21
Loading full text...

Full text loading...

/deliver/fulltext/jmm/64/12/1527.html?itemId=/content/journal/jmm/10.1099/jmm.0.000184&mimeType=html&fmt=ahah

Author and Article Information

 Figure data loading....

Footnotes:

Validated antibodies in this article

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error