High-protein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: The increased luminal bulk connection

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 307, Issue 4, 2014, Pages

  Liu, Xinxin ^a   Blouin, Jean Marc ^a   Santacruz, Arlette ^b   Lan, Annaïg ^a   Andriamihaja, Mireille ^a   Wilkanowicz, Sabina ^b   Benetti, Pierre Henri ^a   Tomé, Daniel ^a   Sanz, Yolanda ^b   Blachier, François ^a   Davila, Anne Marie ^a  

^a AGROPARISTECH   (France)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

Metabolism; Microbiota; Protein; SCFA; Transport

Indexed keywords

ALCOHOL; BUTYRIC ACID; FATTY ACID; FORMIC ACID; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; SUCCINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CECUM; CLOSTRIDIUM; CLOSTRIDIUM COCCOIDES; CLOSTRIDIUM LEPTUM; COLON; COLON FLORA; CONTROLLED STUDY; FAECALIBACTERIUM PRAUSNITZII; LARGE INTESTINE; MALE; MICROFLORA; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN DIET; RAT; WEIGHT REDUCTION;

METABOLISM; MICROBIOTA; PROTEIN; SCFA; TRANSPORT;

ANIMALS; BUTYRATES; CECUM; CLOSTRIDIUM; COLON; DIETARY PROTEINS; ENERGY METABOLISM; EPITHELIAL CELLS; FATTY ACIDS; GASTROINTESTINAL CONTENTS; INTESTINE, LARGE; MALE; MICROBIOTA; RATS; RATS, WISTAR;

EID: 84907954053     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00400.2013     Document Type: Article

References (75)

1. Andriamihaja M, Chaumontet C, Tome D, Blachier F. Butyrate metabolism in human colon carcinoma cells: implications concerning its growth-inhibitory effect. J Cell Physiol 218: 58-65, 2009.
2. Archer SYJJ, Kim HJ, Ma Q, Mou H, Dasety V, Meng S, Hodin RA. The histone deacetylase inhibitor butyrate down regulates cyclin B1 gene expression via p21/WAF-1-dependent mechanism in human colon cancer cells. Am J Physiol Gastrointest Liver Physiol 289: G696-G703, 2005.
3. Bach Knudsen KE, Serena A, Canibe N, Juntunen KS. New insight into butyrate metabolism. Proc Nutr Soc 62: 81-86, 2003.
4. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66: 1654-1661, 2000.
5. Barker HA. Amino acid degradation by anaerobic bacteria. Annu Rev Biochem 50: 23-40, 1981.
6. Binder HJ. Role of colonic short-chain fatty acid transport in diarrhea. Annu Rev Physiol 72: 297-313, 2010.
7. Binder HJ, Sangan P, Rajendran VM. Physiological and molecular studies of colonic H, K-ATPase. Semin Nephrol 19: 405-414, 1999.
8. Blachier F, Mariotti F, Huneau JF, Tome D. Effects of amino acidderived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33: 547-562, 2007.
9. Boren J, Lee WN, Bassilian S, Centelles JJ, Lim S, Ahmed S, Boros LG, Cascante M. The stable isotope-based dynamic metabolic profile of butyrate-induced HT29 cell differentiation. J Biol Chem 278: 28395-28402, 2003.
10. Borthakur A, Saksena S, Gill RK, Alrefai WA, Ramaswamy K, Dudeja PK. Regulation of monocarboxylate transporter 1 (MCT1) promoter by butyrate in human intestinal epithelial cells: involvement of NF-kappaB pathway. J Cell Biochem 103: 1452-1463, 2008.
11. Buyse M, Sitaraman SV, Liu X, Bado A, Merlin D. Luminal leptin enhances CD147/MCT-1-mediated uptake of butyrate in the human intestinal cell line Caco2-BBE. J Biol Chem 277: 28182-28190, 2002.
12. Cano PG, Santacruz A, Trejo FM, Sanz Y. Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet fed mice. Obesity (Silver Spring) 21: 2310-2321, 2013.
13. Chacko A, Cummings JH. Nitrogen losses from the human small bowel: obligatory losses and the effect of physical form of food. Gut 29: 809-815, 1988.
14. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
15. Cuff M, Dyer J, Jones M, Shirazi-Beechey S. The human colonic monocarboxylate transporter Isoform 1: its potential importance to colonic tissue homeostasis. Gastroenterology 128: 676-686, 2005.
16. Cuff MA, Lambert DW, Shirazi-Beechey SP. Substrate-induced regulation of the human colonic monocarboxylate transporter, MCT1. J Physiol 539: 361-371, 2002.
17. Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70: 443-459, 1991.
18. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28: 1221-1227, 1987.
19. Darcy-Vrillon B, Morel MT, Cherbuy C, Bernard F, Posho L, Blachier F, Meslin JC, Duee PH. Metabolic characteristics of pig colonocytes after adaptation to a high fiber diet. J Nutr 123: 234-243, 1993.
20. Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell 48: 612-626, 2012.
21. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science 308: 1635-1638, 2005.
22. Elsden SR, Hilton MG. Volatile acid production from threonine, valine, leucine and isoleucine by clostridia. Arch Microbiol 117: 165-172, 1978.
23. Evenepoel P, Claus D, Geypens B, Hiele M, Geboes K, Rutgeerts P, Ghoos Y. Amount and fate of egg protein escaping assimilation in the small intestine of humans. Am J Physiol Gastrointest Liver Physiol 277: G935-G943, 1999.
24. Fromentin G, Darcel N, Chaumontet C, Marsset-Baglieri A, Nadkarni N, Tome D. Peripheral and central mechanisms involved in the control of food intake by dietary amino acids and proteins. Nutr Res Rev 25: 29-39, 2012.
25. Gaudichon C, Bos C, Morens C, Petzke KJ, Mariotti F, Everwand J, Benamouzig R, Dare S, Tome D, Metges CC. Ileal losses of nitrogen and amino acids in humans and their importance to the assessment of amino acid requirements. Gastroenterology 123: 50-59, 2002.
26. Genell S, Gustafsson BE, Ohlsson K. Quantitation of active pancreatic endopeptidases in the intestinal contents of germfree and conventional rats. Scand J Gastroenterol 11: 757-762, 1976.
27. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125: 1401-1412, 1995.
28. Gibson GR, Willems A, Reading S, Collins MD. Fermentation of non-digestible oligosaccharides by human colonic bacteria. Proc Nutr Soc 55: 899-912, 1996.
29. Gibson JA, Sladen GE, Dawson AM. Protein absorption and ammonia production: the effects of dietary protein and removal of the colon. Br J Nutr 35: 61-65, 1976.
30. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. Metagenomic analysis of the human distal gut microbiome. Science 312: 1355-1359, 2006.
31. Goubern M, Andriamihaja M, Nubel T, Blachier F, Bouillaud F. Sulfide, the first inorganic substrate for human cells. FASEB J 21: 1699-1706, 2007.
32. Gustafsson BE. The physiological importance of the colonic microflora. Scand J Gastroenterol Suppl 77: 117-131, 1982.
33. He T, Priebe MG, Harmsen HJ, Stellaard F, Sun X, Welling GW, Vonk RJ. Colonic fermentation may play a role in lactose intolerance in humans. J Nutr 136: 58-63, 2006.
34. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132: 1012-1017, 2002.
35. Hooda S, Boler BM, Serao MC, Brulc JM, Staeger MA, Boileau TW, Dowd SE, Fahey GC Jr, Swanson KS. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. J Nutr 142: 1259-1265, 2012.
36. Johnstone AM. Safety and efficacy of high-protein diets for weight loss. Proc Nutr Soc 71: 339-349, 2012.
37. Kabeerdoss J, Devi RS, Mary RR, Ramakrishna BS. Faecal microbiota composition in vegetarians: comparison with omnivores in a cohort of young women in southern India. Br J Nutr 108: 953-957, 2012.
38. Klenk J, Nagel G, Ulmer H, Strasak A, Concin H, Diem G, Rapp K. Body mass index and mortality: results of a cohort of 184,697 adults in Austria. Eur J Epidemiol 24: 83-91, 2009.
39. Kristensen NB, Pierzynowski SG, Danfaer A. Net portal appearance of volatile fatty acids in sheep intraruminally infused with mixtures of acetate, propionate, isobutyrate, butyrate, and valerate. J Anim Sci 78: 1372-1379, 2000.
40. Lecona E, Olmo N, Turnay J, Santiago-Gomez A, Lopez de Silanes I, Gorospe M, Lizarbe MA. Kinetic analysis of butyrate transport in human colon adenocarcinoma cells reveals two different carrier-mediated mechanisms. Biochem J 409: 311-320, 2008.
41. Leschelle X, Goubern M, Andriamihaja M, Blottiere HM, Couplan E, Gonzalez-Barroso MD, Petit C, Pagniez A, Chaumontet C, Mignotte B, Bouillaud F, Blachier F. Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim Biophys Acta 1725: 201-212, 2005.
42. Livesey G, Elia M. Estimation of energy expenditure, net carbohydrate utilization, and net fat oxidation and synthesis by indirect calorimetry: evaluation of errors with special reference to the detailed composition of fuels. Am J Clin Nutr 47: 608-628, 1988.
43. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294: 1-8, 2009.
44. Macfarlane GT. Microbiological Aspects of the Production of Short-Chain Fatty Acids in the Large Bowel. Cambridge, UK: Cambridge Univ Press, 1995, p. 87-105.
45. Macfarlane GT, Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 95: 50-60, 2012.
46. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc 62: 67-72, 2003.
47. Malinen E, Rinttila T, Kajander K, Matto J, Kassinen A, Krogius L, Saarela M, Korpela R, Palva A. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 100: 373-382, 2005.
48. Martinez-Medina M, Denizot J, Dreux N, Robin F, Billard E, Bonnet R, Darfeuille-Michaud A, Barnich N. Western diet induces dysbiosis with increased E coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut 63: 116-124, 2014.
49. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R. Development of 16S rRNA-genetargeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68: 5445-5451, 2002.
50. Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 70: 7220-7228, 2004.
51. Miner-Williams W, Deglaire A, Benamouzig R, Fuller MF, Tome D, Moughan PJ. Endogenous proteins in terminal ileal digesta of adult subjects fed a casein-based diet. Am J Clin Nutr 96: 508-515, 2012.
52. Mouille B, Robert V, Blachier F. Adaptative increase of ornithine production and decrease of ammonia metabolism in rat colonocytes after hyperproteic diet ingestion. Am J Physiol Gastrointest Liver Physiol 287: G344-G351, 2004.
53. Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res 11: 5573-5585, 2012.
54. Potten CS, Grant HK. The relationship between ionizing radiationinduced apoptosis and stem cells in the small and large intestine. Br J Cancer 78: 993-1003, 1998.
55. Rasmussen HS, Holtug K, Mortensen PB. Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scand J Gastroenterol 23: 178-182, 1988.
56. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951, 1993.
57. Ritzhaupt A, Wood IS, Ellis A, Hosie KB, Shirazi-Beechey SP. Identification and characterization of a monocarboxylate transporter 513: 719-732, 1998.
58. Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83: 424-429, 1982.
59. Santacruz A, Collado MC, Garcia-Valdes L, Segura MT, Martin-Lagos JA, Anjos T, Marti-Romero M, Lopez RM, Florido J, Campoy C, Sanz Y. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 104: 83-92, 2010.
60. Sanz Y, Sanchez E, Marzotto M, Calabuig M, Torriani S, Dellaglio F. Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol 51: 562-568, 2007.
61. Schwarz J, Tome D, Baars A, Hooiveld GJ, Muller M. Dietary protein affects gene expression and prevents lipid accumulation in the liver in mice. PLoS One 7: e47303, 2012.
62. Siavoshian S, Blottiere HM, Cherbut C, Galmiche JP. Butyrate stimulates cyclin D and p21 and inhibits cyclin-dependent kinase 2 expression in HT-29 colonic epithelial cells. Biochem Biophys Res Commun 232: 169-172, 1997.
63. Singh B, Halestrap AP, Paraskeva C. Butyrate can act as a stimulator of growth or inducer of apoptosis in human colonic epithelial cell lines depending on the presence of alternative energy sources. Carcinogenesis 18: 1265-1270, 1997.
64. Smiddy FG, Gregory SD, Smith IB, Goligher JC. Faecal loss of fluid, electrolytes, and nitrogen in colitis before and after ileostomy. Lancet 1: 14-19, 1960.
65. Smith JG, Yokoyama WH, German JB. Butyric acid from the diet: actions at the level of gene expression. Crit Rev Food Sci Nutr 38: 259-297, 1998.
66. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105: 16731-16736, 2008.
67. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Dore J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15: 1183-1189, 2009.
68. Tothmeresz B. Comparison of different methods for diversity ordering. J Veg Sci 283-290, 1995.
69. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ. Dominant and dietresponsive groups of bacteria within the human colonic microbiota. ISME J 5: 220-230, 2011.
70. Walter J, Tannock GW, Tilsala-Timisjarvi A, Rodtong S, Loach DM, Munro K, Alatossava T. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl Environ Microbiol 66: 297-303, 2000.
71. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324: 1076-1080, 2009.
72. Westerterp-Plantenga MS, Nieuwenhuizen A, Tome D, Soenen S, Westerterp KR. Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr 29: 21-41, 2009.
73. Wilson AJ, Gibson PR. Short-chain fatty acids promote the migration of colonic epithelial cells in vitro. Gastroenterology 113: 487-496, 1997.
74. Wolffram S, Badertscher M, Scharrer E. Carrier-mediated transport is involved in mucosal succinate uptake by rat large intestine. Exp Physiol 79: 215-226, 1994.
75. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD. Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108, 2011.