Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine

British Journal of Nutrition

Volumn 99, Issue 3, 2008, Pages 472-480

  Tako, Elad ^a   Glahn, R P ^a   Welch, R M ^a   Lei, X ^a   Yasuda, K ^a   Miller, D D ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Intestinal gene expression; Inulin; Iron; Microbiota

Indexed keywords

BACTERIAL DNA; BINDING PROTEIN; CYTOCHROME B5 REDUCTASE; DNA 16S; FERRITIN; FERROPORTIN 1; INULIN; MUCIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PREBIOTIC AGENT; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ARTICLE; BIFIDOBACTERIUM; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; FERRITIN BLOOD LEVEL; GENE EXPRESSION; GENETIC CODE; INSULIN BLOOD LEVEL; INTESTINE FLORA; IRON BLOOD LEVEL; LACTOBACILLUS; MICROBIAL DIVERSITY; NONHUMAN; NUTRITIONAL VALUE; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN SECRETION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROBE; SEQUENCE ANALYSIS; TISSUE REACTION;

ANIMAL NUTRITION PHYSIOLOGY; ANIMALS; BACTERIA; CATION TRANSPORT PROTEINS; CECUM; COLON; CYTOCHROME B GROUP; DIET; DIETARY CARBOHYDRATES; ENTEROCYTES; GENE EXPRESSION REGULATION; GROWTH; HEMOGLOBINS; INTESTINE, SMALL; INULIN; IRON; IRON-BINDING PROTEINS; MUCINS; RNA, MESSENGER; SUS SCROFA;

ANIMALIA; BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; CICHORIUM INTYBUS; LACTOBACILLUS; SUIDAE; TRITICUM AESTIVUM; ZEA MAYS;

EID: 38949198681     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114507825128     Document Type: Article

References (74)

1. Collins JF (2006) Gene chip analyses reveal differential genetic responses to iron deficiency in rat duodenum and jejunum. Biol Res 39, 25-37.
2. Mackenzie B & Garrick MD (2005) Iron imports. II. Iron uptake at the apical membrane in the intestine. Am J Physiol 299, G981-G986.
3. McKie AT, Marciani P, Rolfs A, et al. (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell Biol 5, 299-309.
4. Latunde-Dada GO, Van der Westhuizen J, Vulpe CD, Anderson GJ, Simpson RJ & McKie AT (2002) Molecular and functional roles of duodenal cytochrome B (Dcytb) in iron metabolism. Blood Cells Mol. Dis 29, 356-360.
5. Takeuchi K, Bjarnason I, Laftah AH, Latunde-Dada GO, Simpson RJ & McKie AT (2005) Expression of iron absorption genes in mouse large intestine Scand J Gastroenterol 40, 169-177.
6. van Loo J, Coussement P, de Leenheer L, Hoebregs H & Smits G (1995) On the presence of inulin and oligofructose as natural ingedients in the Western diet. Crit Rev Food Sci Nutr 35, 525-552.
7. Bougle D, Vaghefi-Vaezzadeh N, Roland N, Bouvard G, Arhan P, Bureau F, Neuville D & Maubois JL (2002) Influence of short-chain fatty acids on iron absorplion by proximal colon. Scand J Gastroenterol 37, 1008-1011.
8. Bosscher D, Van Caillie-Bertrand M, Van Cauwenbergh R & Deelstra H (2003) Availabilities of calcium, iron, and zinc from dairy infant formulas is affected by soluble dietary fibers and modified starch fractions. Nutrition 19, 641-645.
9. van den Heuvel EG, Muys T, van Dokkum W & Schaafsma G (1999) Oligofructose stimulates calcium absorption in adolescents. Am J Clin Nutr 69, 544-548.
10. Scholz-Ahrens KE & Schrezenmeir J (2002) Inulin, oligofructose and mineral metabolism - experimental data and mechanism. Br J Nutr 87, Suppl. 2, S179-S186.
11. Ohta A, Motohashi Y, Sakai K, Hirayama M, Adaohi T & Sakuma K (1998) Dietary fructooligosaccharides increase calcium absorption and levels of mucosal calbindin-D9k in the large intestine of gastrectomized rats. Scand J Gastroenterol 33; 1062-1068.
12. Yasuda K, Roneker KR, Miller DD, Welch RM & Lei XG (2006) Supplemental dietary inulin affects bioavailability of iron present in corn and soybean meal to young pigs. J Nutr 136, 3033-3038.
13. Ellegard L, Andersson H & Bosaeus I (1997) Inulin and oligofructose do not influence the absorption of cholesterol, or the excretion of cholesterol, Ca, Mg, Zn, Fe, or bile acids but increases energy excretion in ileostomy subjects. Eur J Clin Nutr 51, 1-5.
14. Gibson GR, Beatty ER, Wang X & Cummings JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975-982.
15. Bakker-Zierikzee AM, Alles MS, Knol J, Kok FJ, Tolboom JJ & Bindels JG (2005) Effects of infant formula containing a mixture of galacto- and fructo-oligosaccharides or viable Bifidobacterium animalis on the intestinal microflora during the first 4 months of life. Br J Nutr 94, 783-790.
16. Yang SC, Chen JY, Shang HF, Cheng TY, Tsou SC & Chen JR (2005) Effect of synbiotics on intestinal microflora and digestive enzyme activities in rats. World J Gastroenterol 11, 7413-7417.
17. Broekaert IJ & Walker WA (2006) Probiotics as flourishing benefactors for the human body. Gastroenterol Nurs 29, 26-34.
18. Cummings JH, Pomare EW, Branch WJ, Naylor CP & Macfarlane GT (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 1221-1227.
19. Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri E, Moreau MC, Roberfroid M & Rowland I (1998) Functional food science and gastrointestinal physiology and function. Br J Nutr 80, Suppl. 1, S147-S171.
20. 2) by intestinal bacteria and their role in maintaining coagulation homeostasis. Prog Food Nutr Sci 16, 307-343.
21. Hopkins MJ & Macfarlane GT (2003) Nondigestible oligosaccharides enhance bacterial colonization resistance against Clostridium difficile in vitro. Appl Environ Microbiol 69, 1920-1927.
22. Collins MD & Gibson GR (1999) Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 69, l012S-1057S.
23. Zhu XY, Zhong T, Pandya Y & Joerger RD (2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl Environ Microbiol 68, 124-137.
24. Smirnov A, Perez R, Amit-Romach E, Sklan D & Uni Z (2005) Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. J Nutr 135, 187-192.
25. Apajalahti JH, Kettunen H, Kettunen A, Holben WE, Nurminen PH, Rautonen N & Mutanen M (2002) Culture-independent microbial community analysis reveals that inulin in the diet primarily affects previously unknown bacteria in the mouse cecum. Appl Environ Microbiol 68, 4986-4995.
26. de Wiele TV, Boon N, Possemiers S, Jacobs H & Verstraete W (2004) Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem. Fetal Diagn Ther 51, 143-153.
27. Nelson KE, Thonney ML, Woolston TK, Zinder SH & Pell AN (1998) Phenotypic and phylogenetic characterization of ruminal tannin-tolerant bacteria. Appl Environ Microbiol 64, 3824-3830.
28. Harmsen HJ, Gibson GR, Elfferich P, Raangs GC, Wildeboer-Veloo AC, Argaiz A, Roberfroid MB & Welling GW (2000) Comparison of viable cell counts and fluorescence in situ hybridization using specific rRNA-based probes for the quantification of human fecal bacteria. FEMS Microbiol Lett 183, 125-129.
29. Kleessen B, Hartmann L & Blaut M (2003) Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. Br J Nutr 89, 597-606.
30. Subcommittee on Swine Nutrition, Committee on Animal Nutrition & National Research Council (1998) Nutrition Requirements of Swine, 10th ed. Washington, DC: National Academy Press.
31. Eppard P, Bauman D, Bitman J, Wood D, Akers R & House W (1985) Effect of dose of bovine growth hormone on milk composition: α-lactalbumin, fatty acids, and mineral elements. J Dairy Sci 68, 3047-3054.
32. Sharp P, Tandy S, Yamaji S, Tennant J, Williams M & Singh Srai SK (2002) Rapid regulation of divalent metal transporter (DMT1) protein but not mRNA expression by non-haem iron in human intestinal Caco-2 cells. FEBS Lett 510, 71-76.
33. McKie AT, Barrow D, Latunde-Dada GO, et al. (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291, 1755-1759.
34. Lagendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH & Welling GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 3069-3075.
35. Amit-Romach E, Sklan D & Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci 83, 1095-1098.
36. Ludwiczek S, Theurl I, Artner-Dworzak E, Chorney M, & Weiss G (2004) Duodenal HFE expression and hepcidin levels determine body iron homeosteostasis: Modulation by genetic diversity and dietary iron availability. J Mol Med 82, 373-3821.
37. Collins JF, Franck CA, Kowdley KV & Ghishan FK (2005) Identification of differentially expressed genes in response to dietary iron deprivation in rat duodenum. Am J Gastroenterol 288, G964-G971.
38. Anderson GJ (2001) Ironing out disease: Inherited disorders of iron homeostasis. IUBMB Life 51, 11-17.
39. Tandy S, Williams M, Leggett A, Lopez-Jimenez M, Dedes M, Ramesh B, Srai SK & Sharp P (2000) Nramp2 expression is associated with pH-dependent iron uptake across the apical membrane of human intestinal Caco-2 cells. J Biol Chem 275, 1023-1029.
40. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL & Hediger MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388 482-488.
41. Fleming MD & Andrews NC (1998) Mammalian iron transport: An unexpected link between metal homeostasis and host defense. J Lab Clin Med 132, 464-468.
42. Coudray C, Bellanger J, Castiglia-Delavaud C, Remesy C, Vermorel M & Rayssignuier Y (1997) Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc, in healthy young men. Eur J Clin Nutr 51, 375-380.
43. Raschka L & Daniel H (2005) Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats. Bone 37, 728-735.
44. Yeh KY, Yeh M, Watkin JA, Rodriguez-Paris J & Glass J (2000) Dietary iron induces rapid changes in rat intestinal divalent metal transporter expression. Am J Physiol 279, G1070-G1079.
45. Sreedhar B & Nair KM (2005) Modulation of aconitase, metallothionein, and oxidative stress in zinc-deficient rat intestine during zinc and iron repletion. Free Radic Biol Med 39, 999-1008.
46. Nzeusseu A, Dienst D, Haufroid V, Depresseux G, Devogelaer JP & Manicourt DH (2006) Inulin and fructo-oligosaccharides differ in their ability to enhance the density of cancellous and cortical bone in the axial and peripheral skeleton of growing rats. Bone 38, 394-399.
47. Staun M & Jarnum S (1988) Measurement of the 10,000-molecular weight calcium-binding protein in small-intestinal biopsy specimens from patients with malabsorption syndromes: Scand J Gastroenterol 23 827-832.
48. Ohta A, Motohashi Y, Ohtsuki M, Hirayama M, Adachi T & Sakuma K (1998) Dietary fructooligosaccharides change the concentration of calbindin-D9k differently in the mucosa of the small and large intestine of rats. J Nutr 128, 934-939.
49. Hoverstad T & Bjorneklett A (1984) Short-chain fatty acids and bowel functions in man. Scand J Gastroenterol 19, 1059-1065.
50. Hoverstad T, Bjorneklett A, Midtvedt T, Fausa O & Bohmer T (1984) Short-chain fatty acids in the proximal gastrointestinal tract of healthy subjects. Scand J Gastroenterol 19, 1053-1058.
51. Hoverstad T, Fausa O, Bjorneklett A & Bohmer T (1994) Short-chain fatty acids in the normal human feces. Scand J Gastroenterol 19, 375-381.
52. Cummings JH & Macfarlane GT (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70 443-459.
53. Tzortzis G, Goulas AK, Gee JM & Gibson GR (2005) A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J Nutr 135, 1726-1731.
54. Mentschel, J & Claus R (2003) Increased butyrate formation in the pig colon by feeding raw potato starch leads to a reduction of colonocyte apoptosis and a shift to the stem cell compartment. Metabolism 52, 1400-1405.
55. Ruppin H, Bar-Meir S, Soergel KH, Wood CM & Schmitt MG Jr (1980) Absorption of short-chain fatty acids by the colon. Gastroenterology 78, 1500-1507.
56. Livesey G (1995) The impact of complex carbohydrates on energy balance. Eur J Clin Nutr 49, Suppl. 3, S89-S96.
57. Cummings JH & Englyst HN (1987) Fermentation in the human large intestine and the available substrates. Am J Clin Nutr 45, 1243-1255.
58. Kolida S, Tuohy K & Gibson GR (2002) Prebiotic effects of inulin and oligofructose. Br J Nutr 87, Suppl. 2, S193-S197.
59. Bouhnik Y, Attar A, Joly FA, Riottot M, Dyard F & Flourie B (2004) Lactulose ingestion increases faecal bifidobacterial counts: A randomised double-blind study in healthy humans. Eur J Clin Nutr 58, 462-466.
60. Bouhnik Y, Raskine L, Simoneau G, Vicaut E, Neut C, Flourie B, Brouns F & Bornet FR (2004) The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: A double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. Am J Clin Nutr 80, 1658-1664.
61. Nilsson U & Bjorck I (1988) Availability of cereal fructans and inulin in the rat intestinal tract. J Nutr 118, 1482-1486.
62. Molly K, Vande Woestyne M & Verstraete W (1993) Development of a 5-step multi-chamber reactor as a simulation of the human intestinal microbial ecosystem. Appl Microbiol Biotechnol 39, 254-258.
63. Wang X & Gibson GR (1993) Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol 75, 373-380.
64. Heid CA, Stevens J, Livak KJ & Williams PM (1996) Real time quantitative PCR. Genome Res 6, 986-994.
65. Boon N, Goris J, De Vos P, Verstraete W & Top EM (2000) Bioaugmentation of activated sludge by an indigenous 3-chloroaniline-degrading Comamonas testosteroni strain, 12gfp. Appl. Environ Microbiol 66, 2906-2913.
66. Uehara M, Ohta A, Sakai & Suzuki Watanabe S & Adlercreutz H (2001) Dietary fructooligosaccharides modify intestinal bioavailability of a single dose of genistein and daidzein and affect their urinary excretion and kinetics in blood of rats. J Nutr 131, 787-795.
67. Daly K, Cuff MA, Fung F & Shirazi-Beechey SP (2605) The importance of colonic butyrate transport to the regulation of genes associated wi4i colonic tissue homoeostasis. Biochem Soc Trans 33, 733-731.
68. Hass R, Busche R, Luciano L, Reale E & Engelhardt WV (1997).Lack of butyrate is associated with induction of Bax and subsequent apoptosis in the proximal colon of guinea pig. Gastroenterology 112, 875-881.
69. Gaudier E, Jarry A, Blottiere HM, de Coppet P, Buisine MP, Aubert IP, Laboisse C, Cherbut C Hoebler C (2004) Butyrate specifically modulates MUC gene exprpssign in intestinal epithelial cells deprived of glucose. Am J Physiol 287, G1168-G1174.
70. Simovich M, Hainsworth LN, Fields PA, -Umbreit JN & Conrad ME (2003) Localization of the iron transport proteins mobilferrin and DMT-1 in the duodenum: The surprising role of mucin. Am J Hematol 74, 32-45.
71. Wang RF, Cao WW & Cemiglia CE (1996) PCR detection and quantification of predominant anaerobic bacteria in human and animal fecal samples, Appl Environ Microbiol 62, 1242-1247.
72. Candarian U, Furer B, Hofelein C, Meyer R, Jermini M & Luthy J (1991) Detection of Escherichia coli and identification of enterotoxigenic strains by primer-directed enzymatic amplification of specific DNA sequences. Int J Food Microbiol 12, 339-351.
73. Denis M,.Refregier-Petton J, Laisney MJ, Ermel G & Salvat G (2001) Campylobacter contamination in french chicken production from farm to consumers Use of PCR assay for detection and identification of Campylobacter jejunic and Camp. coli. J Appl Microbiol 91 255-267.
74. Langendijk PS, Schut F, Jansen J, Raangs GC, Kamphius GR, Wilkinson MH & Welling GW (1995) Quantitive fluorescence in situ hybridization of bifidobacterium spp. with genus specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 3069-3075.