Skip to main content
    • Aa
    • Aa
  • Access
  • Cited by 34
  • Cited by
    This article has been cited by the following publications. This list is generated based on data provided by CrossRef.

    Das, Jugal Kishore Mahapatra, Rajani Kanta Patro, Shubhransu Goswami, Chandan Suar, Mrutyunjay and Ferreira, Cälia 2016. Lactobacillus acidophilusbinds to MUC3 component of cultured intestinal epithelial cells with highest affinity. FEMS Microbiology Letters, Vol. 363, Issue. 8, p. fnw050.

    Gleeson, Michael Bishop, Nicolette C. and Struszczak, Lauren 2016. Effects of Lactobacillus casei Shirota ingestion on common cold infection and herpes virus antibodies in endurance athletes: a placebo-controlled, randomized trial. European Journal of Applied Physiology, Vol. 116, Issue. 8, p. 1555.

    Hessenberger, S. Schatzmayr, G. and Teichmann, K. 2016. In vitro inhibition of Eimeria tenella sporozoite invasion into host cells by probiotics. Veterinary Parasitology, Vol. 229, p. 93.

    Kalyuzhin, O. V. Afanasyev, S. S. and Bykov, A. S. 2016. Oral probiotics as anti-infectious immune response stimulators in the respiratory tract. Terapevticheskii arkhiv, Vol. 88, Issue. 5, p. 118.

    Le Bourgot, Cindy Ferret-Bernard, Stéphanie Blat, Sophie Apper, Emmanuelle and Le Huërou-Luron, Isabelle 2016. Short-chain fructooligosaccharide supplementation during gestation and lactation or after weaning differentially impacts pig growth and IgA response to influenza vaccination. Journal of Functional Foods, Vol. 24, p. 307.

    Rosa, Damiana D. Grześkowiak, Łukasz M. Ferreira, Célia L. L. F. Fonseca, Ana Carolina M. Reis, Sandra A. Dias, Mariana M. Siqueira, Nathane P. Silva, Leticia L. Neves, Clóvis A. Oliveira, Leandro L. Machado, Alessandra B. F. and Peluzio, Maria do Carmo G. 2016. Kefir reduces insulin resistance and inflammatory cytokine expression in an animal model of metabolic syndrome. Food Funct., Vol. 7, Issue. 8, p. 3390.

    Thysen, Anna Hammerich Rasmussen, Morten Arendt Kreiner-Møller, Eskil Larsen, Jeppe Madura Følsgaard, Nilofar Vahman Bønnelykke, Klaus Stokholm, Jakob Bisgaard, Hans and Brix, Susanne 2016. Season of birth shapes neonatal immune function. Journal of Allergy and Clinical Immunology, Vol. 137, Issue. 4, p. 1238.

    van den Nieuwboer, Maurits van Hemert, Saskia Claassen, Eric and de Vos, Willem M. 2016. Lactobacillus plantarumWCFS1 and its host interaction: a dozen years after the genome. Microbial Biotechnology, Vol. 9, Issue. 4, p. 452.

    Watters, C. Fleming, D. Bishop, D. and Rumbaugh, K.P. 2016. Host-Microbe Interactions.

    Bordalo Tonucci, Livia Dos Santos, Karina Olbrich Ferreira, Celia Lucia De Luces Fortes Ribeiro, Sonia Machado Rocha De Oliveira, Leandro Licursi and Martino, Hercia Stampini Duarte 2015. Clinical Application of Probiotics in Diabetes Mellitus: Therapeutics and New Perspectives. Critical Reviews in Food Science and Nutrition, p. 00.

    Carasi, P. Racedo, S. M. Jacquot, C. Romanin, D. E. Serradell, M. A. and Urdaci, M. C. 2015. Impact of Kefir DerivedLactobacillus kefirion the Mucosal Immune Response and Gut Microbiota. Journal of Immunology Research, Vol. 2015, p. 1.

    Jorjão, Adeline Lacerda Oliveira, Felipe Eduardo de Leão, Mariella Vieira Pereira Carvalho, Cláudio Antonio Talge Jorge, Antonio Olavo Cardoso and Oliveira, Luciane Dias de 2015. Live and Heat-KilledLactobacillus rhamnosusATCC 7469 May Induce Modulatory Cytokines Profiles on Macrophages RAW 264.7. The Scientific World Journal, Vol. 2015, p. 1.

    Ladda, Boonyarut Theparee, Talent Chimchang, Juntana Tanasupawat, Somboon and Taweechotipatr, Malai 2015. In vitro modulation of tumor necrosis factor α production in THP-1 cells by lactic acid bacteria isolated from healthy human infants. Anaerobe, Vol. 33, p. 109.

    Lovegrove, J. A. Commane, D. M. Jackson, K. G. Karani, V. Kennedy, O. B. Kuhnle, G. G. Spencer, J. P. E. Wagstaff, C. and Yaqoob, P. 2015. The Hugh Sinclair Unit of Human Nutrition - 20 years of research 1995-2015. Nutrition Bulletin, Vol. 40, Issue. 4, p. 303.

    Nawaz, M. Ma, C. Basra, M.A.R Wang, J. and Xu, J. 2015. Amelioration of ovalbumin induced allergic symptoms in Balb/c mice by potentially probiotic strains of lactobacilli. Beneficial Microbes, Vol. 6, Issue. 5, p. 669.

    Patel, Seema Shukla, Rishikesh and Goyal, Arun 2015. Probiotics in valorization of innate immunity across various animal models. Journal of Functional Foods, Vol. 14, p. 549.

    Spaiser, Samuel J. Culpepper, Tyler Nieves, Carmelo Ukhanova, Maria Mai, Volker Percival, Susan S. Christman, Mary C. and Langkamp-Henken, Bobbi 2015. Lactobacillus gasseriKS-13,Bifidobacterium bifidumG9-1, andBifidobacterium longumMM-2 Ingestion Induces a Less Inflammatory Cytokine Profile and a Potentially Beneficial Shift in Gut Microbiota in Older Adults: A Randomized, Double-Blind, Placebo-Controlled, Crossover Study. Journal of the American College of Nutrition, Vol. 34, Issue. 6, p. 459.

    Christoffersen, Trine Eker Hult, Lene Therese Olsen Kuczkowska, Katarzyna Moe, Kim Marius Skeie, Siv Lea, Tor and Kleiveland, Charlotte Ramstad 2014. In Vitro Comparison of the Effects of Probiotic, Commensal and Pathogenic Strains on Macrophage Polarization. Probiotics and Antimicrobial Proteins, Vol. 6, Issue. 1, p. 1.

    Dimitrijevic, Rajna Ivanovic, Nevena Mathiesen, Geir Petrusic, Vladimir Zivkovic, Irena Djordjevic, Brizita and Dimitrijevic, Ljiljana 2014. Effects of Lactobacillus rhamnosus LA68 on the immune system of C57BL/6 mice upon oral administration. Journal of Dairy Research, Vol. 81, Issue. 02, p. 202.

    Ghadimi, Darab Njeru, Patrisio Njiru Guigas, Claudia Farghaly, Mohammed Hassan Fölster-Holst, Regina Geis, Arnold de Vrese, Michael Schrezenmeir, Jürgen and Heller, Knut J. 2014. Molecular identification of potential Th1/Th2 responses-modulating bacterial genes using suppression subtractive DNA hybridization. Immunobiology, Vol. 219, Issue. 3, p. 208.


Comparative effects of six probiotic strains on immune function in vitro

  • Honglin Dong (a1), Ian Rowland (a1) and Parveen Yaqoob (a1)
  • DOI:
  • Published online: 07 November 2011

There is considerable interest in the strain specificity of immune modulation by probiotics. The present study compared the immunomodulatory properties of six probiotic strains of different species and two genera in a human peripheral blood mononuclear cell (PBMC) model in vitro. Live cells of lactobacilli (Lactobacillus casei Shirota, L. rhamnosus GG, L. plantarum NCIMB 8826 and L. reuteri NCIMB 11951) and bifidobacteria (Bifidobacterium longum SP 07/3 and B. bifidum MF 20/5) were individually incubated with PBMC from seven healthy subjects for 24 h. Probiotic strains increased the proportion of CD69+ on lymphocytes, T cells, T cell subsets and natural killer (NK) cells, and increased the proportion of CD25+, mainly on lymphocytes and NK cells. The effects on activation marker expression did not appear to be strain specific. NK cell activity was significantly increased by all six strains, without any significant difference between strains. Probiotic strains increased production of IL-1β, IL-6, IL-10, TNF-α, granulocyte-macrophage colony-stimulating factor and macrophage inflammatory protein 1α to different extents, but had no effect on the production of IL-2, IL-4, IL-5 or TNF-β. The cytokines that showed strain-specific modulation included IL-10, interferon-γ, TNF-α, IL-12p70, IL-6 and monocyte chemotactic protein-1. The Lactobacillus strains tended to promote T helper 1 cytokines, whereas bifidobacterial strains tended to produce a more anti-inflammatory profile. The results suggest that there was limited evidence of strain-specific effects of probiotics with respect to T cell and NK cell activation or NK cell activity, whereas production of some cytokines was differentially influenced by probiotic strains.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Comparative effects of six probiotic strains on immune function in vitro
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Comparative effects of six probiotic strains on immune function in vitro
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Comparative effects of six probiotic strains on immune function in vitro
      Available formats
Corresponding author
*Corresponding author: P. Yaqoob, fax +44 118 931 0080, email
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

1E Isolauri , S Salminen & AC Ouwehand (2004) Probiotics. Best Pract Res Clin Gastroenterol 18, 299313.

2RD Sleator & C Hill (2008) New frontiers in probiotic research. Lett Appl Microbiol 46, 143147.

3D Paineau , D Carcano , G Leyer , (2008) Effects of seven potential probiotic strains on specific immune responses in healthy adults: a double-blind, randomized, controlled trial. FEMS Immunol Med Microbiol 53, 107113.

4ML Cross , A Ganner , D Teilab , (2004) Patterns of cytokine induction by gram-positive and gram-negative probiotic bacteria. FEMS Immunol Med Microbiol 42, 173180.

5D Ghadimi , R Folster-Holst , M de Vrese , (2008) Effects of probiotic bacteria and their genomic DNA on T(H)1/T(H)2-cytokine production by peripheral blood mononuclear cells (PBMCs) of healthy and allergic subjects. Immunobiology 213, 677692.

6U Helwig , KM Lammers , F Rizzello , (2006) Lactobacilli, bifidobacteria and E. coli Nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World J Gastroenterol 12, 59785986.

7M Medina , E Izquierdo , S Ennahar , (2007) Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol 150, 531538.

8K Shida , T Suzuki , J Kiyoshima-Shibata , (2006) Essential roles of monocytes in stimulating human peripheral blood mononuclear cells with Lactobacillus casei to produce cytokines and augment natural killer cell activity. Clin Vaccine Immunol 13, 9971003.

9D Haller , S Blum , C Bode , (2000) Activation of human peripheral blood mononuclear cells by nonpathogenic bacteria in vitro: evidence of NK cells as primary targets. Infect Immun 68, 752759.

10LN Fink , LH Zeuthen , HR Christensen , (2007) Distinct gut-derived lactic acid bacteria elicit divergent dendritic cell-mediated NK cell responses. Int Immunol 19, 13191327.

11AM Castellazzi , C Valsecchi , L Montagna , (2007) In vitro activation of mononuclear cells by two probiotics: Lactobacillus paracasei I 1688, Lactobacillus salivarius I 1794, and their mixture (PSMIX). Immunol Invest 36, 413421.

14P Kankaanpaa , Y Sutas , S Salminen , (2003) Homogenates derived from probiotic bacteria provide down-regulatory signals for peripheral blood mononuclear cells. Food Chem 83, 269277.

15LH Zeuthen , HR Christensen & H Frokiaer (2006) Lactic acid bacteria inducing a weak interleukin-12 and tumor necrosis factor alpha response in human dendritic cells inhibit strongly stimulating lactic acid bacteria but act synergistically with gram-negative bacteria. Clin Vaccine Immunol 13, 365375.

16S Salminen , MC Collado , E Isolauri , (2009) Microbial–host interactions: selecting the right probiotics and prebiotics for infants. Nestle Nutr Workshop Ser Pediatr Program 64, 201217.

17P Lopez , M Gueimonde , A Margolles , (2010) Distinct Bifidobacterium strains drive different immune responses in vitro. Int J Food Microbiol 138, 157165.

19C Hessle , LA Hanson & AE Wold (1999) Lactobacilli from human gastrointestinal mucosa are strong stimulators of IL-12 production. Clin Exp Immunol 116, 276282.

20L Drago , L Nicola , E Iemoli , (2010) Strain-dependent release of cytokines modulated by Lactobacillus salivarius human isolates in an in vitro model. BMC Res Notes 3, 4448.

21B Foligne , S Nutten , C Grangette , (2007) Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 13, 236243.

22G Mastrangeli , S Corinti , C Butteroni , (2009) Effects of live and inactivated VSL#3 probiotic preparations in the modulation of in vitro and in vivo allergen-induced Th2 responses. Int Arch Allergy Immunol 150, 133143.

23AE Flinterman , EF Knol , AG van Ieperen-Van Dijk , (2007) Probiotics have a different immunomodulatory potential in vitro versus ex vivo upon oral administration in children with food allergy. Int Arch Allergy Immunol 143, 237244.

24RA Kekkonen , N Lummela , H Karjalainen , (2008) Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14, 20292036.

25IM Rea , SE McNerlan & HD Alexander (1999) CD69, CD25, and HLA-DR activation antigen expression on CD3+ lymphocytes and relationship to serum TNF-alpha, IFN-gamma, and sIL-2R levels in aging. Exp Gerontol 34, 7993.

26AL Meyer , M Micksche , I Herbacek , (2006) Daily intake of probiotic as well as conventional yogurt has a stimulating effect on cellular immunity in young healthy women. Ann Nutr Metab 50, 282289.

27TB Ozkan , E Sahin , G Erdemir , (2007) Effect of Saccharomyces boulardii in children with acute gastroenteritis and its relationship to the immune response. J Int Med Res 35, 201212.

28M de Vrese , P Winkler , P Rautenberg , (2005) Effect of Lactobacillus gasseri PA 16/8, Bifidobacterium longum SP 07/3, B. bifidum MF 20/5 on common cold episodes: a double blind, randomized, controlled trial. Clin Nutr 24, 481491.

29P Garciapenarrubia , FT Koster , RO Kelley , (1989) Antibacterial activity of human natural-killer cells. J Exp Med 169, 99113.

30M Olivares , MP Diaz-Ropero , S Sierra , (2007) Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 23, 254260.

31D Bunout , G Barrera , S Hirsch , (2004) Effects of a nutritional supplement on the immune response and cytokine production in free-living Chilean elderly. J Parenter Enter Nutr 28, 348354.

33S Spanhaak , R Havenaar & G Schaafsma (1998) The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur J Clin Nutr 52, 899907.

34AJ Cox , DB Pyne , PU Saunders , (2010) Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. Br J Sports Med 44, 222226.

35H Ishikawa , I Akedo , T Otani , (2005) Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int J Cancer 116, 762767.

37M Kalliomaki , JM Antoine , U Herz , (2010) Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of allergic diseases by probiotics. J Nutr 140, 713S721S.

38CT Weaver , LE Harrington , PR Mangan , (2006) Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24, 677688.

39VK Singh , S Mehrotra & SS Agarwal (1999) The paradigm of Th1 and Th2 cytokines – its relevance to autoimmunity and allergy. Immunol Res 20, 147161.

40AT Borchers , C Selmi , FJ Meyers , (2009) Probiotics and immunity. J Gastroenterol 44, 2646.

41RA Kekkonen , E Kajasto , M Miettinen , (2008) Probiotic Leuconostoc mesenteroides ssp cremoris and Streptococcus thermophilus induce IL-12 and IFN-gamma production. World J Gastroenterol 14, 11921203.

42HM Timmerman , LEM Niers , BU Ridwan , (2007) Design of a multispecies probiotic mixture to prevent infectious complications in critically ill patients. Clin Nutr 26, 450459.

43YM Vissers , J Snel , PF Zuurendonk , (2010) Differential effects of Lactobacillus acidophilus and Lactobacillus plantarum strains on cytokine induction in human peripheral blood mononuclear cells. FEMS Immunol Med Microbiol 59, 6070.

45C Hessle , B Andersson & AE Wold (2000) Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL-12) while gram-negative bacteria preferentially stimulate IL-10 production. Infect Immun 68, 35813586.

46AL Hart , K Lammers , P Brigidi , (2004) Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53, 16021609.

47KM Lammers , P Brigidi , B Vitali , (2003) Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol Med Microbiol 38, 165172.

48LEM Niers , HM Timmerman , GT Rijkers , (2005) Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin Exp Allergy 35, 14811489.

49GE Ji (2009) Probiotics in primary prevention of atopic dermatitis. In Food Factors for Health Promotion, pp. 117128. Basel: Karger.

50RL Clancy & G Pang (2007) Probiotics – industry myth or a practical reality? J Am Coll Nutr 26, 691S694S.

51R Kaji , J Kiyoshima-Shibata , M Nagaoka , (2010) Bacterial teichoic acids reverse predominant IL-12 production induced by certain Lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J Immunol 184, 35053513.

52K Ivory , SJ Chambers , C Pin , (2008) Oral delivery of Lactobacillus casei Shirota modifies allergen-induced immune responses in allergic rhinitis. Clin Exp Allergy 38, 12821289.

53T Shima , K Fukushima , H Setoyama , (2008) Differential effects of two probiotic strains with different bacteriological properties on intestinal gene expression, with special reference to indigenous bacteria. FEMS Immunol Med Microbiol 52, 6977.

54T Kobayashi , I Kato , M Nanno , (2010) Oral administration of probiotic bacteria, Lactobacillus casei and Bifidobacterium breve, does not exacerbate neurological symptoms in experimental autoimmune encephalomyelitis. Immunopharmacol Immunotoxicol 32, 116124.

56JA Pena & J Versalovic (2003) Lactobacillus rhamnosus GG decreases TNF-alpha production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol 5, 277285.

57T Pessi , Y Sutas , H Hurme , (2000) Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy 30, 18041808.

58E Isolauri , T Arvola , Y Sutas , (2000) Probiotics in the management of atopic eczema. Clin Exp Allergy 30, 16041610.

59M Kalliomaki , S Salminen , H Arvilommi , (2001) Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357, 10761079.

60M Viljanen , E Savilahti , T Haahtela , (2005) Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 60, 494500.

61K Kukkonen , M Kuitunen , T Haahtela , (2010) High intestinal IgA associates with reduced risk of IgE-associated allergic diseases. Pediatr Allergy Immunol 21, 6773.

62JD de Jonge , J Ezendam , LMJ Knippels , (2008) Lactobacillus casei Shirota does not decrease the food allergic response to peanut extract in Brown Norway rats. Toxicology 249, 140145.

63MV Kopp , I Hennemuth , A Heinzmann , (2008) Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics 121, E850E856.

64CE Rose , SSJ Sung & SM Fu (2003) Significant involvement of CCL2 (MCP-1) in inflammatory disorders of the lung. Microcirculation 10, 273288.

65A Steensberg , CP Fischer , C Keller , (2003) IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab 285, E433E437.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *