Recent advances in transport of water-soluble vitamins in organs of the digestive system: A focus on the colon and the pancreas

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 305, Issue 9, 2013, Pages

  Said, Hamid M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA LONG BEACH HEALTHCARE SYSTEM   (United States)

Author keywords

Biotin; Colon; Folate; Niacin; Pancreas; Pyridoxine; Riboflavin; Thiamine; Transport

Indexed keywords

BIOTIN; NICOTINAMIDE; NICOTINIC ACID; THIAMINE; UNCLASSIFIED DRUG; VITAMIN; WATER SOLUBLE VITAMIN;

COLON; DIET SUPPLEMENTATION; GASTROINTESTINAL ABSORPTION; HUMAN; INTESTINE FLORA; NONHUMAN; PANCREAS; PRIORITY JOURNAL; REVIEW;

BIOTIN; COLON; FOLATE; NIACIN; PANCREAS; PYRIDOXINE; RIBOFLAVIN; THIAMINE; TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; COLON; HUMANS; INTESTINAL ABSORPTION; PANCREAS; SOLUBILITY; VITAMINS; WATER;

EID: 84887012548     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00231.2013     Document Type: Review

References (110)

1. Alexander B. The chemical determination of thiamine and cocarboxylase in biological material. J Biol Chem 151: 455-465, 1943.
2. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoetendal EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Doré J; MetaHIT Consortium, Antolín M, Artiguenave F, Blottiere HM, Almeida M, Brechot C, Cara C, Chervaux C, Cultrone A, Delorme C, Denariaz G, Dervyn R, Foerstner KU, Friss C, van de Guchte M, Guedon E, Haimet F, Huber W, van Hylckama-Vlieg J, Jamet A, Juste C, Kaci G, Knol J, Lakhdari O, Layec S, Le Roux K, Maguin E, Mérieux A, Melo Minardi R, M'rini C, Muller J, Oozeer R, Parkhill J, Renault P, Rescigno M, Sanchez N, Sunagawa S, Torrejon A, Turner K, Vandemeulebrouck G, Varela E, Winogradsky Y, Zeller G, Weissenbach J, Ehrlich SD, Bork P. Enterotypes of the human gut microbiome. Nature 473: 174-180, 2011.
3. Ashokkumar B, Kumar JS, Hecht GA, Said HM. Enteropathogenic Escherichia coli inhibits intestinal vitamin B1 (thiamine) uptake: studies with human-derived intestinal epithelial Caco-2 cells. Am J Physiol Gastrointest Liver Physiol 297: G825-G833, 2009.
4. Auer IO, Ziemer E, Sommer H. Immune status in Crohn's disease. V. Decreased in vitro natural killer cell activity in peripheral blood. Clin Exp Immunol 42: 41-49, 1980.
5. Aufreiter S, Kim JH, O'Connor DL. Dietary oligosaccharides increase colonic weight and the amount but not concentration of bacterially synthesized folate in the colon of piglets. J Nutr 141: 366-372, 2011.
6. Bahn A, Hagos Y, Reuter S, Balen D, Brzica H, Krick W, Burckhardt BC, Sabolic I, Burckhardt G. Identification of a new urate and high affinity nicotinate transporter, hOAT10 (SLC22A13). J Biol Chem 283: 16332-16341, 2008.
7. Balaghi M, Wager C. Folate deficiency inhibits pancreatic amylase secretion in rats. Am J Clin Nutr 61: 90-96, 1995.
8. Balaghi M, Wagner C. Methyl group metabolism in the pancreas of folate deficient rats. J Nutr 122: 1391-1396, 1992.
9. Balaghi M, Horne DW, Woodward SC, Wagner C. Pancreatic onecarbon metabolism in rats. Am J Clin Nutr 58: 198-203, 1993.
10. Balamurugan K, Ortiz A, Said HM. Biotin uptake by human intestinal and liver epithelial cells: role of the SMVT system. Am J Physiol Gastrointest Liver Physiol 285: G73-G77, 2003.
11. Barrow BJ, Ortiz-Reyes R, O'Riordan MA, Pretlow TP. In situ localization of enzymes and mucin in normal rat colon embedded in plastic. Histochem J 21: 289-295, 1989.
12. Berdanier CD. Trace minerals. Adv Nutr Micronutr 183-219, 1998.
13. Bettendorff L, Goessens G, Sluse F, Wins P, Bureau M, Laschet J, Grisar T. Thiamine deficiency in cultured neuroblastoma cells: effect on mitochondrial function and peripheral benzodiazepine receptors. J Neurochem 64: 2013-2021, 1995.
14. Betz Al Ren XD, Ennis SR, Hultquist DE. Riboflavin reduces edema in focal cerebral ischemia. Acta Neurochir Suppl (Wien) 60: 314-317, 1944.
15. Black S, McKibbin JM, Elvehjem CA. Use of sulfaguanidine in nutrition experiments. Proc Soc Exp Biol Med 47:308-310, 1941.
16. Bowman BB, Rosenberg IH. Biotin absorption by distal rat intestine. J Nutr 117: 2121-2126, 1987.
17. Calingasan N, Chun W, Park L, Uchida K, Gibson GE. Oxidative stress is associated with region-specific neuronal death during thiamine deficiency. J Neuropathol Exp Neurol 58: 946-958, 1999.
18. Chernobilsky B, Tsou KC. Adenocarcinoma, adenomas and polyps of the colon. Histochemical study. Cancer 21: 165-177, 1968.
19. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O'Sullivan O, Fitzgerald GF, Deane J, O'Connor M, Harnedy N, O'Connor K, O'Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O'Toole PW. Gut microbiota composition correlates with diet and health in the elderly. Nature 488: 178-184, 2012.
20. Coates ME, Ford JE, Harrison GF. Intestinal synthesis of vitamins of the B complex in chicks. Br J Nutr 22: 493-500, 1968.
21. Cobianchi L, Fornoni A, Pileggi A, Molano RD, Sanabria NY, Gonzalez-Quintana J, Bocca N, Marzorati S, Zahr E, Hogan AR, Ricordi C, Inverardi L. Riboflavin inhibits IL-6 expression and p38 activation in islet cells. Cell Transplant 17: 559-566, 2008.
22. Cooper EA. On the protective and curative properties of certain foodstuffs against polyneuritis induced in birds by a diet of polished rice: part II. J Hygiene 14: 12-22, 1914.
23. Cravo ML, Mason JB, Selhub J, Rosenberg IH. Use of deoxyuridine suppression test to evaluate localized folate deficiency in rat colonic epithelium. Am J Clin Nutr 53: 1450-1454, 1991.
24. Dawson I, Pryse-Davies J. The distribution of certain enzyme systems in the normal human gastrointestinal tract. Gastroenterology 44: 745-760, 1963.
25. Dethlefsen L, Huse S, Sogin M, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6: e280, 2008.
26. Diaz GA, Banikazemi M, Oishi K, Desnick RJ, Gelb BD. Mutations in a new gene encoding a thiamine transporter cause thiamine-responsive megaloblastic anaemia syndrome. Nat Genet 22: 309-312, 1999.
27. Dudeja PK, Kode A, Alnounou M, Tyagi S, Torania S, Subramanian VS, Said HM. Mechanism of folate transport across the human colonic basolateral membrane. Am J Physiol Gastrointest Liver Physiol 281: G54-G60, 2001.
28. Dudeja PK, Torania SA, Said HM. Evidence for the existence of an electroneutral, pH-dependent, DIDS-sensitive carrier-mediated folate uptake mechanism in the human colonic luminal membrane vesicles. Am J Physiol Gastrointest Liver Physiol 272: G1408-G1415, 1997.
29. Dutta B, Huang W, Molero M, Kekuda R, Leibach FH, Devoe LD, Ganapathy V, Prasad PD. Cloning of the human thiamine transporter, a member of the folate transporter family. J Biol Chem 45: 31925-31929, 1999.
30. Fernandez-Banares F, Abad-Lacruz A, Xiol X. Vitamin status in patients with inflammatory bowel disease. Am J Gastroenterol 84: 744-748, 1989.
31. Flachowsky G. Niacin in dairy and beef cattle nutrition. Arch Anim Nutr 43: 195-213, 1993.
32. Fleming JC, Tartaglini E, Steinkamp MP, Schorderet DF, Cohen N, Neufeld EJ. The gene mutated in thiamine-responsive anaemia with diabetes and deafness (TRMA) encodes a functional thiamine transporter. Nat Genet 22: 305-308, 1999.
33. Ghosal A, Said HM. Mechanism and regulation of vitamin B2 (riboflavin) uptake by mouse and human pancreatic B-cells/islets: physiological and molecular aspects. Am J Physiol Gastrointest Liver Physiol 303: G1052-G1058, 2012.
34. Ghosal A, Lambrecht N, Subramanya SB, Kapadia R, Said HM. Conditional knockout of the Slc5a6 gene in mouse intestine impairs biotin absorption. Am J Physiol Gastrointest Liver Physiol 304: G64-G71, 2013.
35. Greensberger NJ, Toskes PP. Acute and chronic pancreatic. In: Harrison's Principles of Internal Medicine, edited by Kasper DL. New York: McGraw-Hill, 2005.
36. Gurerrant NB, Dutcher RA, Brown RA. Further studies concerning formation of B vitamins in digestive tract of rat. J Nutr 13: 305-315, 1937.
37. Hashimoto T, Perlot T, Rehman A, Trichereau J, Ishiguro H, Paolino M, Sigl V, Hanada T, Hanada R, Lipinski S, Wild B, Camargo SM, Singer D, Andreas R, Kuba K, Fukamizu A, Schreiber S, Clevers H, Verrey F, Rosenstiel P, Penninger JM. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 487: 477-481, 2012.
38. Iinuma S. Synthesis of riboflavin by intestinal bacteria. J Vitaminol (Kyoto) 10: 6-13, 1955.
39. Iinuma S. Synthesis of riboflavin by intestinal bacteria. J Vitamin 2: 6-13, 1955.
40. Kasper H. Vitamin absorption in the colon. Am J Protocol 21: 341-345, 1970.
41. Keagy PM, Oace SM. Folic acid utilization from high fiber diets in rats. J Nutr 114: 1252-1259, 1984.
42. Kono S, Miyajima H, Yoshida K, Togawa A, Shirakawa K, Suzuki H. Mutations in thiamine-transporter gene and Wernickes-like encephalopathy. N Engl J Med 360: 1792-1794, 2009.
43. Kornberg A, Daft FS, Sebrell WH. Production and treatment of granulocytopenia and anemia in rats fed sulfonamides in purified diets. Science 98: 20-22, 1944.
44. Krause LJ, Forsberg CW, O'Connor DL. Feeding human milk to rats increases Bifidobacterium in the cecum and colon which correlates with enhanced folate status. J Nutr 126: 1505-1511, 1996.
45. Kubisch CH, Gukovsky I, Lugea A, Pandol SJ, Kuick R, Misek DE, Hanash SM, Logsdon CD. Long-term ethanol consumption alters pancreatic gene expression in rats: a possible connection to pancreatic injury. Pancreas 33: 66-76, 2006.
46. Kumar CK, Moyer MP, Dudeja PK, Said HM. A protein-tyrosine kinase regulated, pH-dependent carrier-mediated uptake system for folate by human normal colonic epithelial cell line NCM 460. J Biol Chem 272: 6226-6231, 1997.
47. Kumar JS, Subramanian VS, Kapadia R, Kashyap ML, Said HM. Mammalian colonocytes possess a carrier-mediated mechanism for uptake of vitamin B3 (niacin): studies utilizing human and mouse colonic preparations. Am J Physiol Gastrointest Liver Physiol 305: G207-G213, 2013.
48. Lashner BA, Heidenreich PA, Su GL, Kane SV, Hanauer SB. The effect of folate supplementation on the incidence of dysplasia and cancer in chronic ulcerative colitis: a case control study. Gastroenterology 97: 255-259, 1989.
49. Longnecker DS. Abnormal methyl metabolism in pancreatic toxicity and diabetes. J Nutr 132: 2373S-2376S, 2002.
50. Lu Z, Karne S, Kolodecik T, Gorelick FS. Alcohols enhance caeruleininduced zymogen activation in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 282: G501-G507, 2002.
51. Mandel H, Berant M, Hazani A, Naveh Y. Thiamine-dependent beriberi in the "thiamine-responsive anemia syndrome. " N Engl J Med 311: 836-838, 1984.
52. Matherly LH, Hou Z. Structure and function of the reduced folate carrier: a paradigm of a major facilitator superfamily mammalian nutrient transporter. Vitam Horm 79: 145-184, 2008.
53. Mee L, Nabokina SM, Sekar VT, Subramanian VS, Maedler K, Said HM. Pancreatic beta cells and islets take up thiamine by a regulated carrier-mediated process: studies using mice and human pancreatic preparations. Am J Physiol Gastrointest Liver Physiol 297: G197-G206, 2009.
54. Mitchell HK, Isbell ER. Intestinal Bacterial Synthesis as a Source of B Vitamins for the Rat. Austin, TX: University of Texas, 1942, p. 125-134.
55. Mock DM. Biotin. In: Handbook of Vitamins, edited by Zempleni J, McCormick DB, Suttie JW. New York: CRC, 2006, p. 361-377.
56. Nabokina SM, Said HM. A high affinity and specific carrier-mediated mechanism for uptake of thiamine pyrophosphate by human colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 303: G389-G395, 2012.
57. Nabokina SM, Subramanian VS, Said HM. Association of PDZcontaining protein PDZD11 with the human sodium dependent multivitamin transporter gene. Am J Physiol Cell Physiol 280: C548-C555, 2001.
58. Najjar VA, Holt LE. The biosynthesis of thiamine in man and its implication in human nutrition. JAMA 123: 683-684, 1943.
59. Neufeld EJ, Fleming JC, Tartaglini E, Steinkamp MP. Thiamineresponsive megaloblastic anemia syndrome: a disorder of high-affinity thiamine transport. Blood Cells Mol Dis 27: 135-138, 2001.
60. O'Sullivan MG, Thornton G, O'Sullivan GC, Collins JK. Probiotic bacteria: myth or reality? Food Sci Technol 3: 309-314, 1992.
61. Okabe N, Fujita K, Yao T. Immunological studies on Crohn's disease. III. Defective natural killer activity. J Clin Lab Immunol 17: 143-146, 1985.
62. Okabe N, Urabe K, Fujita K, Yamamoto T, Yao T, Doi S. Biotin effects in Crohn's disease. Dig Dis Sci 33: 1495-1496, 1988.
63. Portari GV, Marchini JS, Vannucchi H, Jordao AA. Antioxidant effect of thiamine on acutely alcoholized rats and lack of efficacy using thiamine or glucose to reduce blood alcohol content. Basic Clin Pharmacol Toxicol 103: 482-486, 2008.
64. Prasannan KG, Sundaresan R, Venkatesan K. Thiamine deficiency and protein secretion by pancreatic slices in vitro. Experientia 33: 169-170, 1977.
65. Rajgopal A, Edmondson A, Goldman D, Zhao R. SLC19A3 encodes a second thiamine transporter ThTr2. Biochim Biophys Acta 1537: 175-178, 2001.
66. Rathanaswami P, Pourany A, Sundaresan R. Effects of thiamine deficiency on the secretion of insulin and the metabolism of glucose in isolated rat pancreatic islets. Biochem Int 25: 577-583, 1991.
67. Reidling JC, Lambrecht N, Kassir M, Said HM. Impaired intestinal vitamin B1 (thiamine) uptake in thiamine transporter-2-deficient mice. Gastroenterology 138: 1802-1809, 2010.
68. Rindi G, Laforenza U. Thiamine intestinal transport and related issues: recent aspects. Proc Soc Exp Biol Med 224: 246-255, 2000.
69. Rindi G, Patrini C, Laforenza U, Mandel H, Berant M, Viana MB, Poggi V, Zarra AN. Further studies on erythrocytes: thiamine transport and phosphorylation in seven patients with thiamine-responsive megaloblastic anaemia. J Inherit Metab Dis 17: 667-667, 1994.
70. Rong N, Selhub J, Goldin BR, Rosenberg IH. Bacterially synthesized folate in rat large intestine is incorporated into host tissue folyl polyglutamates. J Nutr 121: 1955-1959, 1991.
71. Said HM, Ross C. Riboflavin. In: Modern Nutrition in Health and Disease (11th ed.), edited by Ross C, Caballero B, Cousins RJ, Tucker KL, Ziegler TR. Philadelphia, PA: Lippincott Williams & Wilkins, 2011, p. 325-330.
72. Said HM, Balamurugan K, Subramanian VS, Marchant JS. Expression and functional contribution of hTHTR-2 in thiamine absorption in human intestine. Am J Physiol Gastrointest Liver Physiol 286: G491-G498, 2004.
73. Said HM, Mee L, Sekar VT, Ashokkumar B, Pandol SJ. Mechanism and regulation of folate uptake by pancreatic acinar cells: effect of chronic alcohol consumption. Am J Physiol Gastrointest Liver Physiol 298: G985-G993, 2010.
74. Said HM, Ortiz A, McCloud E, Dyer D, Moyer MP, Rubin S. Biotin uptake by the human colonic epithelial cells NCM460: a carrier-mediated process shared with pantothenic acid. Am J Physiol Cell Physiol 275: C1365-C1371, 1998.
75. Said HM, Ortiz A, Moyer MP, Yanagawa N. Riboflavin uptake by human-derived colonic epithelial NCM460 cells. Am J Physiol Cell Physiol 278: C270-C276, 2000.
76. Said HM, Ortiz A, Subramanian VS, Neufeld EJ, Moyer MP, Dudeja PK. Mechanism of thiamine uptake by human coloncytes: studies with cultured colonic epithelial cell line NCM460. Am J Physiol Gastrointest Liver Physiol 281: G144-G150, 2001.
77. Saito N, Kimura M, Kuchiba A, Itokawa Y. Blood thiamine levels in outpatients with diabetes mellitus. J Nutr Sci Vitaminol (Tokyo) 33: 421-430, 1987.
78. Salaspuro M. Bacteriocolonic pathway for ethanol oxidation: characteristics and implications. Ann Med 28: 195-200, 1996.
79. Segal I, Ou TL, Demetriou A, Paterson A, Hale M, Lerios M. Rectal manifestations of pellagra. Int J Colorectal Dis 1: 238-243, 1986.
80. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC, Frazer DM, Anderson GJ, Vulpe CD, Simpson RJ, McKie AT. Identification of an intestinal heme transporter. Cell 122: 789-801, 2005.
81. Singh M. Effect of thiamine deficiency on pancreatic acinar cell function. Am J Clin Nutr 36: 500-504, 1982.
82. Singleton CK, Martin PR. Molecular mechanisms of thiamine utilization. Curr Mol Med 1: 197-207, 2001.
83. Sorell MF, Frank O, Thomsom AD. Absorption of vitamins from the large intestine. Nutr Res Int 3: 143-48, 1971.
84. Srinivasan P, Subramanian VS, Said HM. Effect of chronic alcohol feeding on physiological and molecular parameters of thiamine uptake by pancreatic acinar cells of transgenic reporter mice carrying the human SLC19A2 and SLC19A3 promoters (Abstract). FASEB J 27: 722, 2013.
85. Stolzenberg-Solomon RZ, Albanes D, Nieto FJ, Hartman TJ, Tangrea JA, Rautalahti M, Sehlub J, Virtamo J, Taylor PR. Pancreatic cancer risk and nutrition-related methyl-group availability indicators in male smokers. J Natl Cancer Inst 91: 535-541, 1999.
86. Stratigos JD, Katsambas A. Pellagra: a still existing disease. Br J Dermatol 96: 99-106, 1977.
87. Subramanian VS, Marchant JS, Said HM. Targeting and trafficking of the human thiamine transporter-2 in epithelial cells. J Biol Chem 281: 5233-5245, 2006.
88. Subramanian VS, Marchant JS, Boulware MJ, Ma TY, Said HM. Membrane targeting and intracellular trafficking of the human sodiumdependent multivitamin transporter in polarized epithelial cells. Am J Physiol Cell Physiol 296: C663-C671, 2009.
89. Subramanian VS, Marchant JS, Parker I, Said HM. Cell biology of the human thiamine transporter-1 (htHTR1): intracellular trafficking and membrane targeting mechanisms. J Biol Chem 278: 3976-3984, 2003.
90. Subramanian VS, Rapp L, Marchant JS, Said HM. Role of cysteine residues in cell surface expression of the human riboflavin transporter-2 (hRFT2) in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 301: G100-G109, 2011.
91. Subramanian VS, Subramanya SB, Said HM. Relative contribution of THTR-1 and THTR-2 in thiamine uptake by pancreatic acinar cells: studies utilizing Slc19a2 and Slc19a3 knockout mouse models. Am J Physiol Gastrointest Liver Physiol 302: G572-G578, 2012.
92. Subramanian VS, Subramanya SB, Ghosal A, Said HM. Chronic alcohol feeding inhibits physiological and molecular parameters of intestinal and renal riboflavin transport. Am J Physiol Cell Physiol 305: C539-C546, 2013.
93. Subramanian VS, Subramanya SB, Rapp L, Marchant JS, Ma TY, Said HM. Differential expression of human riboflavin transporters-1,-2, and-3 in polarized epithelia: a key role for hRFT-2 in intestinal riboflavin uptake. Biochim Biophys Acta 1808: 3016-3021, 2011.
94. Subramanya SB, Subramanian VS, Said HM. Chronic alcohol consumption and intestinal thiamine absorption: effects on physiological and molecular parameters of the uptake process. Am J Physiol Gastrointest Liver Physiol 299: G23-G31, 2010.
95. Subramanya SB, Subramanian VS, Kumar JS, Hoiness R, Said HM. Inhibition of intestinal biotin absorption by chronic alcohol feeding: cellular and molecular mechanisms. Am J Physiol Gastrointest Liver Physiol 300: G494-G501, 2011.
96. Subramanya SB, Subramanian VS, Sekar VT, Said HM. Thiamine uptake by pancreatic acinar cells: effect of chronic alcohol feeding/exposure. Am J Physiol Gastrointest Liver Physiol 301: G896-G904, 2011.
97. Tallaksen CM, Bell H, Bohmer T. Thiamine and thiamine phosphate ester deficiency assessed by high performance liquid chromatography in four clinical cases of Werincke encephalopathy. Alcohol Clin Exp Res 17: 712-716, 1993.
98. Tallaksen CM, Bohmer T, Bell H. Blood serum thiamine and thiamine phosphate esters concentrations in patients with alcohol dependence syndrome before and after thiamine treatment. Alcohol Clin Exp Res 16: 320-325, 1992.
99. Thoma C, Green TJ, Ferguson LR. Citrus pectin and oligofructose improve folate status and lower serum total homocysteine in rats. Int J Vitam Nutr Res 73: 403-409, 2003.
100. Todd K, Butterworth R. Early microglial response in experimental thiamine deficiency: an immunohistochemical analysis. Glia 25: 190-198, 1999.
101. Walker A. Say hello to our little friends. Nat Rev Microbiol 5: 572-573, 2007.
102. Walzem RL, Clifford AJ. Folate deficiency in rats fed diets containing free amino acids or intact proteins. J Nutr 118: 1089-1096, 1988.
103. Wrong OM, Edmonds CJ, Chadwich VS. Vitamins in the Large Intestine: Its Role in Mammmlian Nutrition and Homeostasis. New York: Wiley, 1981, p. 157-166.
104. Yadav PK, Chen C, Lui Z. Potential role of NK cells in the pathogenesis of inflammatory bowel disease. J Biomed Biotechnol 2011: 348530, 2011.
105. Yamamoto S, Inoue K, Ohta KY, Fukatsu R, Maeda JY, Yoshida Y, Yuasa H. Identification and functional characterization of rat riboflavin transporter 2. J Biochem 145: 437-443, 2009.
106. Yeo EJ, Wagner C. Tissue distribution of glycine N-methyltransferase, a major folate binding protein of liver. Proc Natl Acad Sci USA 91: 210-214, 1994.
107. Yonezawa A, Masuda S, Katsura T, Inui K. Identification and functional characterization of a novel human and rat riboflavin transporter, RRT1. Am J Physiol Cell Physiol 295: C632-C641, 2008.
108. Zempleni J, Mock DM. Uptake and metabolism of biotin by human peripheral blood mononuclear cells. Am J Physiol Cell Physiol 275: C382-C388, 1998.
109. Zhao R, Matherly LH, Goldman ID. Membrane transporters and folate homeostatis: intestinal absorption and transport into systemic compartments and tissues. Exp Rev Mol Med 11: 1-27, 2009.
110. Zoetenal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC, Troost FJ, Bork P, Wels M, de Vos WM, Kleerebezem M. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6: 1415-1426, 2012.