Enteropathogenic Escherichia coli inhibits intestinal vitamin B1 (thiamin) uptake: Studies with human-derived intestinal epithelial Caco-2 cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 4, 2009, Pages

  Ashokkumar, Balasubramaniem ^a,b   Kumar, Jeyan S ^b   Hecht, Gail A ^c   Said, Hamid M ^a,b  

^a VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

hTHTR 1; hTHTR 2; Thiamin transport

Indexed keywords

MESSENGER RNA; PROTEIN SLC19A2; PROTEIN SLC19A3; THIAMIN TRANSPORTER 1; THIAMIN TRANSPORTER 2; THIAMINE; UNCLASSIFIED DRUG; VITAMIN BINDING PROTEIN; CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN; SLC19A2 PROTEIN, HUMAN; SLC19A3 PROTEIN, HUMAN;

ARTICLE; CELL STRAIN CACO 2; CELL SURFACE; CONTROLLED STUDY; DRUG UPTAKE; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; GENE MUTATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; INTESTINE EPITHELIUM CELL; NUTRIENT UPTAKE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; VITAMIN SUPPLEMENTATION; CACO 2 CELL LINE; CELL MEMBRANE; DOWN REGULATION; EPITHELIUM CELL; ESCHERICHIA COLI; GENETIC TRANSFECTION; GENETICS; INTESTINE MUCOSA; KINETICS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MUTATION; PATHOGENICITY; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CACO-2 CELLS; CELL MEMBRANE; DOWN-REGULATION; EPITHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; INTESTINAL MUCOSA; KINETICS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL VIABILITY; MUTATION; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; THIAMINE; TRANSFECTION;

EID: 70349728495     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00250.2009     Document Type: Article

References (41)

1. Babei-Jadidi R, Karachalias N, Ahmed N, Battah S, Thornalley PJ. Prevention of incipient diabetic nephropathy by high-dose thiamine and benfotiamine. Diabetes 52: 2110-2120, 2003. (Pubitemid 36919806)
2. Berdanier CD. Micronutrients. In: Advanced Nutrition. Boca Raton, FL: CRC, 1998.
3. Borthakur A, Gill RK, Hodges K, Ramaswamy K, Hecht G, Dudeja PK. Enteropathogenic Escherichia coli inhibits butyrate uptake in Caco-2 cells by altering the apical membrane MCT1 level. Am J Physiol Gastrointest Liver Physiol 290: G30-G35, 2006.
4. Calingasan NY, Chun WJ, Park LC, Uchida K, Gibson GE. Oxidative stress is associated with region-specific neuronal death during thiamine deficiency. J Neuropathol Exp Neurol 58: 946-958, 1999. (Pubitemid 29441923)
5. Collington GK, Booth IW, Knutton S. Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection. Gut 42: 200-207, 1998. (Pubitemid 28212174)
6. Dean P, Maresca M, Schuller S, Phillips AD, Kenny B. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc Natl Acad Sci USA 103: 1876-1881, 2006.
7. 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. (Pubitemid 29297262)
8. Donnenberg MS, Kaper JB. Enteropathogenic E coli. Infect Immun 60: 3953-3961, 1992.
9. Dudeja PK, Tyagi S, Kavilaveettil RJ, Gill R, Said HM. Mechanism of thiamin uptake by human jejunal brush-border membrane vesicles. Am J Physiol Cell Physiol 281: C786-C792, 2001. (Pubitemid 32880882)
10. Fagundes U, Andrade J. Acute diarrhea and malnutrition: lethality risk in hospitalized infants. J Am Coll Nutr 18: 303-308, 1999. (Pubitemid 29377189)
11. Fagundes U, Scaletsky IC. The gut at war: the consequences of enteropathogenic Escherichia coli infection as a factor of diarrhea and malnutrition. Sao Paulo Med J 118: 21-29, 2000.
12. Fleming JC, Tartaglini E, Steinkamp MP, Schorderet DF, Cohen N, Neufeld EJ. The gene mutated in thiamine-responsive anemia with diabetes and deafness (TRMA) encodes a functional thiamine transporter. Nat Genet 22: 305-308, 1999. (Pubitemid 29297261)
13. Frederikse PH, Farnsworth P, Zigler JS Jr. Thiamin deficiency in vivo produces fiber cell degeneration in mouse lenses. Biochem Biophys Res Commun 258: 703-707, 1999. (Pubitemid 29290333)
14. Gauthier A, Puente JL, Finlay BB. Secretion of the enteropathogenic E. coli type III secretion system requires components of the type III apparatus for assembly and localization. Infect Immun 71: 3310-3319, 2003. (Pubitemid 36637557)
15. Gill RK, Borthakur A, Hodges K, Turner JR, Clayburgh DR, Saksena S, Zaheer A, Ramaswamy K, Hecht G, Dudeja PK. Mechanism underlying inhibition of intestinal apical Cl/OH exchange following infection with enteropathogenic E. coli. J Clin Invest 117: 428-437, 2007. (Pubitemid 46203971)
16. Guerrant RL, Oriá RB, Moore SR, Oriá MOB, Lima AAM. Malnutrition as an enteric infectious disease with long-term effects on child development. Nutr Rev 66: 487-505, 2008.
17. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, Neumaier M, Bergfeld R, Giardino I, Brownlee M. Benfotiamine blocks three major pathways of hyperglycemia damage and prevents experimental diabetic retinopathy. Nat Med 9: 294-299, 2003. (Pubitemid 36362784)
18. + exchange isoform activities by enteropathogenic E. coli in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 287: G370-G378, 2004.
19. - secretion from intestinal epithelia by upregulation galanin-1 receptor expression. J Clin Invest 104: 253-262, 1999.
20. Kenny B, Jepson M. Targeting of an EPEC effector protein to host mitochondria. Cell Microbiol 2: 579-590, 2000.
21. Laforenza U, Patrini C, Alvisi C, Faelli A, Licandro A, Rindi G. Thiamine uptake in human intestinal biopsy specimens including observations from a patient with acute thiamine deficiency. Am J Clin Nutr 66: 320-326, 1997. (Pubitemid 27360330)
22. Levine MM, Edelman R. Enteropathogenic Escherichia coli of classic serotypes associated with infant diarrhea: epidemiology and pathogenesis. Epidemiol Rev 6: 31-51, 1984. (Pubitemid 14024788)
23. Matsushima K, MacManus JP, Hakim AM. Apoptosis is restricted to the thalamus in thiamin-deficient rats. Neuroreport 8: 867-870, 1997. (Pubitemid 27152136)
24. McDaniel TK, Kaper JB. A cloned pathogenicity island from enteropathogenic E. coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 23: 399-407, 1997.
25. McNamara BP, Koutsouris A, O'Connell CB, Nougayrede JP, Donnenberg MS, Hecht G. Translocated EspF protein from enteropathogenic E. coli disrupts host intestinal barrier function. J Clin Invest 107: 621-629, 2001. (Pubitemid 32205183)
26. Nabokina SM, Said HM. Characterization of the 5′-regulatory region of the human thiamin transporter SLC19A3: in vitro and in vivo studies. Am J Physiol Gastrointest Liver Physiol 287: G822-G829, 2004.
27. Nguyen HTT, Dalmasso G, Yan Y, Powell K, Bhatt S, Kalman D, Gewirtz AT, Sitaraman SV, Merlin D. Pathogenic bacteria transcriptionally induce colonic PepT1 expression - an implication in modulating bacterial-epithelial interaction (Abstract). Gastroenterology 136: A-87, 2009.
28. Reidling JC, Subramanian VS, Dudeja PK, Said HM. Expression and promoter analysis of SLC19A2 in the human intestine. Biochim Biophys Acta 1561: 180-187, 2002. (Pubitemid 34454785)
29. Rindi G, Laforenza U. Thiamin intestinal transport and related issues: recent aspects. Proc Soc Exp Biol Med 224: 246-255, 2000. (Pubitemid 30643502)
30. Said HM, Balamurugan K, Subramanian VS, Marchant JS. Expression and functional contribution of hTHTR-2 in thiamin absorption in human intestine. Am J Physiol Gastrointest Liver Physiol 286: G491-G498, 2004. (Pubitemid 38250322)
31. Said HM, Ortiz A, Kumar C, Chatterjee N, Dudeja P, Rubin S. Transport of thiamine in the human intestine: mechanism and regulation in an intestinal epithelial cell model Caco-2. Am J Physiol Cell Physiol 277: C645-C651, 1999. (Pubitemid 29525903)
32. Spitz J, Yuhan R, Koutsouris C, Blatt C, Alverdy J, Hecht G. Enteropathogenic Escherichia coli adherence to intestinal epithelial monolayers diminishes barrier function. Am J Physiol Gastrointest Liver Physiol 268: G374-G379, 1995.
33. Stagg AR, Fleming JC, Baker MA, Sakamoto M, Cohen N, Neufeld EJ. Defective high-affinity thiamin transporters lead to cell death in thiamin-responsive megaloblastic anemia syndrome fibroblasts. J Clin Invest 103: 723-729, 1999. (Pubitemid 29122426)
34. Subramanian VS, Marchant JS, Parker I, Said HM. Cell biology of the human thiamin transporter-1 (hTHTR1): intracellular trafficking and membrane targeting. J Biol Chem 278: 3976-3984, 2003. (Pubitemid 36801129)
35. Subramanian VS, Marchant JS, Said HM. Targeting and trafficking of the human thiamin transporter-2 (hTHTR2) in epithelial cells. J Biol Chem 281: 5233-5245, 2006. (Pubitemid 43847788)
36. Todd K, Butterworth RF. Mechanisms of selective neuronal cell death due to thiamine deficiency. Ann NY Acad Sci 893: 404-411, 1999. (Pubitemid 30038116)
37. Tomson FL, Viswanathan VK, Kanack K, Kanteti RP, Straub KV, Menet M, Kaper JB, Hecht G. Enteropathogenic Escherichia coli EspG disrupts microtubules and in conjunction with Orf3 enhances perturbation of the tight junction barrier. Mol Microbiol 56: 447-464, 2005. (Pubitemid 40516783)
38. Tu X, Nisan I, Yona C, Hanski E, Rosenshine I. EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic E. coli. Mol Microbiol 47: 595-606, 2003. (Pubitemid 36114973)
39. Victor M, Adams RD, Collins GH. The Wernicke-Korsakoff Syndrome and Related Neurological Disorders Due to Alcoholism and Malnutrition. Philadelphia, PA: Davis, 1989.
40. Zimnicka AM, Maryon EB, Kaplan JH. Human copper transporter hCTR1 mediates basolateral uptake of copper into enterocytes: implications for copper homeostasis. J Biol Chem 282: 26471-26480, 2007.
41. Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 Zo-2 and PKC redistribution in tight junction and epithelial barrier repair. Cell Microbiol 9: 804-816, 2007.