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Intestinal immunity of rats with colon cancer is modulated by oligofructose-enriched inulin combined with Lactobacillus rhamnosus and Bifidobacterium lactis

Published online by Cambridge University Press:  09 March 2007

Monika Roller
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, 76131, Karlsruhe, Germany
Angelo Pietro Femia
Affiliation:
Department of Pharmacology, University of Florence, 6 Viale Pieraccini, 50139, Florence, Italy
Giovanna Caderni
Affiliation:
Department of Pharmacology, University of Florence, 6 Viale Pieraccini, 50139, Florence, Italy
Gerhard Rechkemmer
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, 76131, Karlsruhe, Germany
Bernhard Watzl*
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, 76131, Karlsruhe, Germany
*
*Corresponding author: Dr Bernhard Watzl, fax +49 721 6625 400, email, bernhard.watzl@bfe.uni-karlsruhe.de
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Abstract

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Probiotics (PRO) are known to modulate immunity in animals and human subjects and to inhibit colon carcinogenesis in experimental models, but the effects of synbiotics (SYN) are not well understood. Therefore, the effects of PRO (Lactobacillus rhamnosus GG and Bifidobacterium lactis Bb12), PRE (inulin-based enriched with oligofructose, 100g/kg) and SYN (combination of PRO and PRE) on the immune system of rats were investigated in the azoxymethane (AOM)-induced colon cancer model. After 33 weeks, rats with and without AOM treatment were killed and immune cells were isolated from spleen, mesenterial lymph nodes (MLN) and Peyer's patches (PP). AOM treatment significantly reduced natural killer (NK) cell-like cytotoxicity in control rats and in PRO- and PRE-supplemented rats. SYN supplementation prevented the AOM-induced suppression of NK cell-like cytotoxicity in PP compared with control rats (P<0·01). SYN and PRE supplementation stimulated IL-10 production in PP in these rats (P<0·01) and in MLN of rats not treated with AOM (P<0·05). Interferon-γ production in PP was decreased by PRO supplementation (PRO and SYN groups combined; P<0·05). Proliferative responsiveness of lymphocytes (PP) from AOM-treated rats was suppressed in SYN-supplemented rats (P<0·01). Overall, SYN supplementation in carcinogen-treated rats primarily modulated immune functions in the PP, coinciding with a reduced number of colon tumours. PRE and PRO provided in combination as SYN may contribute to the suppression of colon carcinogenesis by modulating the gut-associated lymphoid tissue.

Type
Review Article
Copyright
Copyright © The Nutrition Society 2004

References

Aattouri, N, Bouras, M, Tome, D, Marcos, A & Lemonnier, D (2002) Oral ingestion of lactic-acid bacteria by rats increases lymphocyte proliferation and interferon-γ production. Br J Nutr 87, 367373.CrossRefGoogle Scholar
Altmann, GG & Lala, PK (1994) Initiated stem cells in murine intestinal carcinogenesis: prolonged survival, control by NK cells, and progression. Int J Cancer 59, 569579.CrossRefGoogle ScholarPubMed
American, Institute & of, Nutrition (1977) Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. J Nutr 107, 13401348.Google Scholar
Barone, J, Hebert, JR & Reddy, MM (1989) Dietary fat and natural-killer-cell activity. Am J Clin Nutr 50, 861867.CrossRefGoogle Scholar
Baten, A, Ullah, A, Tomazic, VJ & Shamsuddin, AM (1989) Inositol-phosphate-induced enhancement of natural killer cell activity correlates with tumor suppression. Carcinogenesis 10, 15951598.CrossRefGoogle ScholarPubMed
Cavaglieri, CR, Nishiyama, A, Fernandes, LC, Curi, R, Miles, EA & Calder, PC (2003) Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes. Life Sci 73, 16831690.CrossRefGoogle ScholarPubMed
Chang, L, Gusewitch, GA, Chritton, DBW, Folz, JC, Lebeck, NK, Nehlsen-Cannarella, SL (1993) Rapid flow cytometric assay for the assessment of natural killer cell activity. J Immunol Methods 166, 4554.CrossRefGoogle ScholarPubMed
Cooper, MA, Fehniger, TA & Caligiuri, MA (2001) The biology of human natural killer-cell subsets. Trends Immunol 22, 633640.CrossRefGoogle ScholarPubMed
Cross, ML (2002) Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunol Med Microbiol 34, 245253.CrossRefGoogle ScholarPubMed
De Roos, NM & Katan, MB (2000) Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: a review of papers published between 1988 and 1998. Am J Clin Nutr 71, 405411.CrossRefGoogle ScholarPubMed
Erdman, SE, Rao, VP, Poutahidis, T, Ihrig, MM, Ge, Z, Feng, Y, Tomczak, M, Rogers, AB, Horwitz, BH & Fox, JG (2003) CD4 + CD25 + regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res 63, 60426050.Google ScholarPubMed
Exon, JH & South, EH (2003) Effects of sphingomyelin on aberrant colonic crypt foci development, colon crypt cell proliferation and immune function in an aging rat tumor model. Food Chem Toxicol 41, 471476.CrossRefGoogle Scholar
Femia, AP, Luceri, C, Dolara, P, Giannini, A, Biggeri, A, Salvadori, M, Clune, Y, Collins, KJ, Paglierani, M & Caderni, G (2002) Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogenesis 23, 19531960.CrossRefGoogle ScholarPubMed
Gill, HS & Cross, ML (2002) Probiotics and immune function Nutrition and Immune Function 251272 [PC Calder, CJ Field CJ Gill, editors] Wallingford, Oxon CAB InternationalCrossRefGoogle Scholar
Gill, HS, Rutherfurd, KJ & Cross, ML (2001) Dietary probiotic supplementation enhances natural killer cell activity in the elderly: an investigation of age-related immunological changes. J Clin Immunol 21, 264271.CrossRefGoogle ScholarPubMed
Gill, HS, Rutherfurd, KJ, Prasad, J & Gopal, PK (2000) Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83, 167176.CrossRefGoogle ScholarPubMed
Greenwald, P, Clifford, CK & Milner, JA (2001) Diet and cancer prevention. Eur J Cancer 37, 948965.CrossRefGoogle ScholarPubMed
Hosono, A, Ozawa, A, Kato, R, Ohnishi, Y, Nakanishi, Y, Kimura, T & Nakamura, R (2003) Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer's patch cells. Biosci Biotechnol Biochem 67, 758764.CrossRefGoogle ScholarPubMed
Imai, K, Matsuyama, S, Miyake, S, Suga, K & Nakachi, K (2000) Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356, 17951799.CrossRefGoogle ScholarPubMed
Kelly-Quagliana, KA, Nelson, PD & Buddington, RK (2003) Dietary oligofructose and inulin modulate immune functions in mice. Nutr Res 23, 257267.CrossRefGoogle Scholar
MacDonald, TT & Monteleone, G (2001) IL-12 and Th1 immune responses in human Peyer's patches. Trends Immunol 22, 244247.CrossRefGoogle ScholarPubMed
McIntosh, GH, Royle, PJ & Playne, MJ (1999) A probiotic strain of L. acidophilus reduces DMH-induced large intestinal tumors in male Sprague-Dawley rats. Nutr Cancer 35, 153159.CrossRefGoogle ScholarPubMed
Manhart, N, Spittler, A, Bergmeister, H, Mittlböck, M & Roth, E (2003) Influence of fructooligosaccharides on Peyer's patch lymphocyte numbers in healthy and endotoxemic mice. Nutrition 19, 657660.CrossRefGoogle ScholarPubMed
Murosaki, S, Muroyama, K, Yamamoto, Y, Kusaka, H, Liu, T & Yoshika, Y (1999) Immunopotentiating activity of nigerooligosaccharides for the T helper 1-like immune response in mice. Biosci Biotechnol Biochem 63, 373378.CrossRefGoogle Scholar
Murosaki, S, Muroyama, K, Yamamoto, Y, Liu, T & Yoshika, Y (2002) Nigerooligosaccharides augments natural killer activity of hepatic mononuclear cells in mice. Int Immunopharmacol 2, 151159.CrossRefGoogle Scholar
Nagura, T, Hachimura, S, Hashiguchi, M, Ueda, Y, Kanno, T, Kikuchi, H, Sayama, K & Kaminogawa, S (2002) Suppressive effect of dietary raffinose on T-helper 2 cell-mediated immunity. Br J Nutr 88, 421426.CrossRefGoogle ScholarPubMed
Pierre, F, Perrin, P, Champ, M, Bornet, F, Meflah, K & Menanteau, J (1997) Short-chain fructo-oligosaccharides reduce the occurrence of colon tumors and develop gut-associated lymphoid tissue in Min mice. Cancer Res 57, 225228.Google ScholarPubMed
Pool-Zobel, BL, van Loo, J, Rowland, IR & Roberfroid, MB (2002) Experimental evidences on the potential of prebiotic fructans to reduce the risk of colon cancer. Brit J Nutr 87, Suppl. 2S273S281.CrossRefGoogle ScholarPubMed
Reddy, BS (1998) Prevention of colon cancer by pre- and probiotics: evidence from laboratory studies. Br J Nutr 80, Suppl. 7S219S223.CrossRefGoogle ScholarPubMed
Reddy, BS (1999) Possible mechanisms by which pro- and prebiotics influence colon carcinogenesis and tumor growth. J Nutr 129, 1478S1482SSuppl. 7.CrossRefGoogle ScholarPubMed
Roller, M, Rechkemmer, G & Watzl, B (2004) Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr 134, 153156.CrossRefGoogle ScholarPubMed
Säemann, MD, Böhmig, GA, Österreicher, CH, Burtscher, H, Parolini, O, Diakos, C, Stöckl, J, Hörl, WH & Zlabinger, GJ (2000) Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J 14, 23802382.CrossRefGoogle ScholarPubMed
Schley, PD & Field, CJ (2002) The immuno-enhancing effects of dietary fibres and prebiotics. Br J Nutr 87, Suppl. 2S221S230.CrossRefGoogle Scholar
Sekine, K, Ushida, Y, Kuhara, T, Iigo, M, Baba-Toriyama, H, Moore, MA, Murakoshi, M, Satomi, Y, Nishino, H & Kakizoe, T (1997) Inhibition of initiation and early stage development of aberrant crypt foci and enhanced natural killer activity in male rats administered bovine lactoferrin concomitantly with azoxymethane. Cancer Lett 121, 211216.CrossRefGoogle ScholarPubMed
Singh, J, Rivenson, A, Tomita, M, Shimamura, S, Ishibashi, N & Reddy, BS (1997) Bifidobacterium longum, a lactic acid-producing intestinal bacterium, inhibits colon cancer and modulates the intermediate biomarkers of colon cancer. Carcinogenesis 18, 833841.CrossRefGoogle ScholarPubMed
Smyth, MJ, Godfrey, DI & Trapani, JA (2001) A fresh look at tumor immunosurveillance and immunotherapy. Nat Immunol 2, 293299.CrossRefGoogle Scholar
Takagi, A, Matsuzaki, T, Sato, M, Nomoto, K, Morotomi, M & Yokokura, T (2001) Enhancement of natural killer cytotoxicity delayed murine carcinogenesis by a probiotic microorganism. Carcinogenesis 22, 599605.CrossRefGoogle ScholarPubMed
Tartter, PI, Steinberg, B, Barron, DM & Martinelli, G (1987) The prognostic significance of natural killer cytotoxicity in patients with colorectal cancer. Arch Surg 122, 12641268.CrossRefGoogle ScholarPubMed
Teitelbaum, JE & Walker, WA (2002) Nutritional impact of pre- and probiotics as protective gastrointestinal organisms. Annu Rev Nutr 22, 107138.CrossRefGoogle ScholarPubMed
Tejada-Simon, MV, Ustunol, Z & Pestka, JJ (1999) Effects of lactic acid bacteria ingestion on basal cytokine mRNA and immunoglobulin levels in the mouse. J Food Protect 62, 287291.CrossRefGoogle ScholarPubMed
Trinchieri, G (1995) Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu Rev Immunol 13, 251276.CrossRefGoogle ScholarPubMed
Van Loo, J, Cummings, JH, Delzenne, N, Englyst, HN, Franck, A, Hopkins, MJ, Kok, N, Macfarlane, GT, Newton, DF & Quigley, ME (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). Br J Nutr 81, 121132.Google ScholarPubMed
Verghese, M, Rao, DR, Chawan, CB, Williams, LL & Shackelford, L (2002) Dietary inulin suppresses azoxymethane-induced aberrant crypt foci and colon tumors at the promotion stage in young Fisher 344 rats. J Nutr 132, 28092813.CrossRefGoogle ScholarPubMed
Watzl, B, Neudecker, C, Hänsch, GM, Rechkemmer, G, Pool-Zobel, BL (1999) Short-term moderate aflatoxin B 1 exposure has only minor effects on the gut-associated lymphoid tissue of Brown Norway rats. Toxicology 138, 93102.CrossRefGoogle ScholarPubMed
Wollowski, I, Rechkemmer, G, Pool-Zobel, BL (2001) Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr 73, 451S455S.CrossRefGoogle ScholarPubMed