Long-term selenium deficiency increases the pathogenicity of a Citrobacter rodentium infection in mice

Biological Trace Element Research

Volumn 144, Issue 1-3, 2011, Pages 965-982

  Smith, Allen D ^a   Cheung, Lumei ^a   Botero, Sebastian ^a,b  

^a BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

C.rodentium; Inflammation; Pathogenesis; Selenium

Indexed keywords

CARBONATE DEHYDRATASE IV; GLUTATHIONE PEROXIDASE; SELENIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; BODY WEIGHT; CELL INFILTRATION; CHEMOKINE GENE; CITROBACTER RODENTIUM; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE GENE; DIARRHEA; DIET RESTRICTION; DISEASE ASSOCIATION; DISEASE DURATION; ENTEROBACTERIACEAE INFECTION; ENZYME ACTIVITY; GENE; GENE EXPRESSION REGULATION; IMMUNOREACTIVITY; INFLAMMATORY CELL; MALE; MOUSE; NONHUMAN; SELENIUM DEFICIENCY; SPLEEN;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TRANSLOCATION; BODY WEIGHT; CITROBACTER RODENTIUM; COLON; DIET; DISEASE RESISTANCE; DNA, COMPLEMENTARY; ENTEROBACTERIACEAE INFECTIONS; GASTROINTESTINAL TRACT; GENE EXPRESSION; GLUTATHIONE PEROXIDASE; LIVER; MALE; MICE; MICE, INBRED C57BL; ORGAN SIZE; RNA; SELENIUM; SPLEEN;

BACTERIA (MICROORGANISMS); CITROBACTER RODENTIUM; ESCHERICHIA COLI; MUS;

EID: 84155165686     PISSN: 01634984     EISSN: 15590720     Source Type: Journal    
DOI: 10.1007/s12011-011-9071-4     Document Type: Article

References (72)

1. Gobert AP, Wilson KT, Martin C (2005) Cellular responses to attaching and effacing bacteria: activation and implication of the innate immune system. Arch Immunol Ther Exp (Warsz) 53:234-244 (Pubitemid 41059744)
2. Petty NK, Bulgin R, Crepin VF et al (2010) The Citrobacter rodentium genome sequence reveals convergent evolution with human pathogenic Escherichia coli. J Bacteriol 192:525-538
3. MacDonald TT, Frankel G, Dougan G et al (2003) Host defences to Citrobacter rodentium. Int J Med Microbiol 293:87-93 (Pubitemid 36534600)
4. Vallance BA, Deng W, Jacobson K et al (2003) Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect Immun 71:3443-3453 (Pubitemid 36637573)
5. Wiles S, Clare S, Harker J et al (2004) Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 6:963-972 (Pubitemid 39255609)
6. Symonds EL, Riedel CU, O'Mahony D et al (2009) Involvement of T helper type 17 and regulatory T cell activity in Citrobacter rodentium invasion and inflammatory damage. Clin Exp Immunol 157:148-154
7. Higgins LM, Frankel G, Connerton I et al (1999) Role of bacterial intimin in colonic hyperplasia and inflammation. Science 285:588-591
8. Higgins LM, Frankel G, Douce G et al (1999) Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect Immun 67:3031-3039 (Pubitemid 29244725)
9. Gobert AP, Cheng Y, Akhtar M et al (2004) Protective role of arginase in a mouse model of colitis. J Immunol 173:2109-2117 (Pubitemid 38971649)
10. Zheng Y, Valdez PA, Danilenko DM et al (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14:282-289 (Pubitemid 351347912)
11. Simmons CP, Goncalves NS, Ghaem-Maghami M et al (2002) Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-gamma. J Immunol 168:1804-1812 (Pubitemid 34135780)
12. Ishigame H, Kakuta S, Nagai T et al (2009) Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30:108-119
13. Mangan PR, Harrington LE, O'Quinn DB et al (2006) Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441:231-234
14. Simmons CP, Clare S, Ghaem-Maghami M et al (2003) Central role for B lymphocytes and CD4+ T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect Immun 71:5077-5086 (Pubitemid 37070750)
15. Bry L, Brenner MB (2004) Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J Immunol 172:433-441 (Pubitemid 38020498)
16. Forstrom JW, Zakowski JJ, Tappel AL (1978) Identification of the catalytic site of rat liver glutathione peroxidase as selenocysteine. Biochemistry 17:2639-2644 (Pubitemid 8363379)
17. Tamura T, Stadtman TC (1996) A new selenoprotein from human lung adenocarcinoma cells: purification, properties, and thioredoxin reductase activity. Proc Natl Acad Sci USA 93:1006-1011 (Pubitemid 26054364)
18. Kiremidjian-Schumacher L, Roy M, Wishe HI et al (1994) Supplementation with selenium and human immune cell functions. II. Effect on cytotoxic lymphocytes and natural killer cells. Biol Trace Elem Res 41:115-127 (Pubitemid 24228274)
19. Sakaguchi S, Iizuka Y, Furusawa S et al (2000) Roles of selenium in endotoxin-induced lipid peroxidation in the rats liver and in nitric oxide production in J774A.1 cells. Toxicol Lett 118:69-77 (Pubitemid 32008396)
20. Beck MA, Matthews CC (2000) Micronutrients and host resistance to viral infection. Proc Nutr Soc 59:581-585 (Pubitemid 32002989)
21. Baker SS, Cohen HJ (1983) Altered oxidative metabolism in selenium-deficient rat granulocytes. J Immunol 130:2856-2860 (Pubitemid 13107719)
22. Serfass RE, Ganther HE (1975) Defective microbicidal activity in glutathione peroxidase-deficient neutrophils of selenium-deficient rats. Nature 255:640-641
23. Kim SH, Johnson VJ, Shin TY et al (2004) Selenium attenuates lipopolysaccharide-induced oxidative stress responses through modulation of p38 MAPK and NF-kappaB signaling pathways. Exp Biol Med (Maywood) 229:203-213 (Pubitemid 38146564)
24. Maehira F, Miyagi I, Eguchi Y (2003) Selenium regulates transcription factor NF-kappaB activation during the acute phase reaction. Clin Chim Acta 334:163-171 (Pubitemid 36836071)
25. Smith A, Madden KB, Yeung KJ et al (2005) Deficiencies in selenium and/or vitamin E lower the resistance of mice to Heligmosomoides polygyrus infections. J Nutr 135:830-836 (Pubitemid 40464113)
26. Au Yeung KJ, Smith A, Zhao A et al (2005) Impact of vitamin E or selenium deficiency on nematodeinduced alterations in murine intestinal function. Exp Parasitol 109:201-208 (Pubitemid 40332319)
27. Smith AD, Botero S, Shea-Donohue T et al (2011) The pathogenicity of an enteric Citrobacter rodentium infection is enhanced by deficiencies in the antioxidants selenium and vitamin E. Infect Immun 79:1471-1478
28. Beck MA, Kolbeck PC, Rohr LH et al (1994) Vitamin E deficiency intensifies the myocardial injury of coxsackievirus B3 infection of mice. J Nutr 124:345-358 (Pubitemid 24096485)
29. Levander OA (1985) Considerations on the assessment of selenium status. Fed Proc 44:2579-2583 (Pubitemid 15017059)
30. Smith AD, Morris VC, Levander OA (2001) Rapid determination of glutathione peroxidase and thioredoxin reductase activities using a 96-well microplate format: comparison to standard cuvette-based assays. Int J Vitam Nutr Res 71:87-92 (Pubitemid 32205808)
31. Solano-Aguilar GI, Zarlenga D, Beshah E et al (2002) Limited effect of recombinant porcine interleukin-12 on porcine lymphocytes due to a low level of IL-12 beta2 receptor. Vet Immunol Immunopathol 89:133-148 (Pubitemid 35292286)
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408 (Pubitemid 34164012)
33. Shea-Donohue T, Thomas K, Cody MJ et al (2008) Mice deficient in the CXCR2 ligand, CXCL1 (KC/GRO-alpha), exhibit increased susceptibility to dextran sodium sulfate (DSS)-induced colitis. Innate Immun 14:117-124
34. Kramer M, Weldon PJ, Carroll JF (2009) Composite scores for concurrent behaviours constructed using canonical discriminant analysis. Anim Behav 77:763-768
35. Saedi MS, Smith CG, Frampton J et al (1988) Effect of selenium status on mRNA levels for glutathione peroxidase in rat liver. Biochem Biophys Res Commun 153:855-861
36. Hoglund P, Haila S, Socha J et al (1996) Mutations of the down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat Genet 14:316-319
37. Guttman JA, Samji FN, Li Y et al (2007) Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell Microbiol 9:131-141 (Pubitemid 44896840)
38. Borenshtein D, Nambiar PR, Groff EB et al (2007) Development of fatal colitis in FVB mice infected with Citrobacter rodentium. Infect Immun 75:3271-3281 (Pubitemid 47040928)
39. Borenshtein D, Fry RC, Groff EB et al (2008) Diarrhea as a cause of mortality in a mouse model of infectious colitis. Genome Biol 9:R122
40. Borenshtein D, Schlieper KA, Rickman BH et al (2009) Decreased expression of colonic Slc26a3 and carbonic anhydrase iv as a cause of fatal infectious diarrhea in mice. Infect Immun 77:3639-3650
41. Lee HS, Csallany AS (1994) The influence of vitamin E and selenium on lipid peroxidation and aldehyde dehydrogenase activity in rat liver and tissue. Lipids 29:345-350 (Pubitemid 24149948)
42. Moseley RH, Hoglund P, Wu GD et al (1999) Downregulated in adenoma gene encodes a chloride transporter defective in congenital chloride diarrhea. Am J Physiol 276:G185-G192 (Pubitemid 29063615)
43. Holmberg C, Perheentupa J, Launiala K (1975) Colonic electrolyte transport in health and in congenital chloride diarrhea. J Clin Invest 56:302-310
44. Charney AN, Dagher PC (1996) Acid-base effects on colonic electrolyte transport revisited. Gastroenterology 111:1358-1368 (Pubitemid 26362262)
45. Saksena S, Singla A, Goyal S et al (2010) Mechanisms of transcriptional modulation of the human anion exchanger SLC26A3 gene expression by IFN-{gamma}. Am J Physiol Gastrointest Liver Physiol 298: G159-G166
46. Choi AM, Knobil K, Otterbein SL et al (1996) Oxidant stress responses in influenza virus pneumonia: gene expression and transcription factor activation. Am J Physiol 271:L383-L391
47. Schreck R, Rieber P, Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10:2247-2258 (Pubitemid 21905698)
48. Nguyen T, Sherratt PJ, Pickett CB (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 43:233-260 (Pubitemid 37372641)
49. Makropoulos V, Bruning T, Schulze-Osthoff K (1996) Selenium-mediated inhibition of transcription factor NF-kappa B and HIV-1 LTR promoter activity. Arch Toxicol 70:277-283
50. 2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 12:2005-2015 (Pubitemid 23157717)
51. Khan MA, Ma C, Knodler LA et al (2006) Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect Immun 74:2522-2536 (Pubitemid 43672959)
52. Wang Y, Xiang GS, Kourouma F et al (2006) Citrobacter rodentium-induced NF-kappaB activation in hyperproliferating colonic epithelia: role of p65 (Ser536) phosphorylation. Br J Pharmacol 148:814-824 (Pubitemid 44079411)
53. Sunde RA, Thompson BM, Palm MD et al (1997) Selenium regulation of selenium-dependent glutathione peroxidases in animals and transfected CHO cells. Biomed Environ Sci 10:346-355 (Pubitemid 127472098)
54. Hill KE, McCollum GW, Boeglin ME et al (1997) Thioredoxin reductase activity is decreased by selenium deficiency. Biochem Biophys Res Commun 234:293-295 (Pubitemid 27243893)
55. Cheng W, Fu YX, Porres JM et al (1999) Selenium-dependent cellular glutathione peroxidase protects mice against a pro-oxidant-induced oxidation of NADPH, NADH, lipids, and protein. FASEB J 13:1467-1475 (Pubitemid 29382514)
56. Esworthy RS, Aranda R, Martin MG et al (2001) Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol 281:G848-G855
57. Esworthy RS, Binder SW, Doroshow JH et al (2003) Microflora trigger colitis in mice deficient in selenium-dependent glutathione peroxidase and induce Gpx2 gene expression. Biol Chem 384:597-607 (Pubitemid 36609175)
58. Esworthy RS, Yang L, Frankel PH et al (2005) Epithelium-specific glutathione peroxidase, Gpx2, is involved in the prevention of intestinal inflammation in selenium-deficient mice. J Nutr 135:740-745 (Pubitemid 40464097)
59. Banning A, Deubel S, Kluth D et al (2005) The GI-GPx gene is a target for Nrf2. Mol Cell Biol 25:4914-4923 (Pubitemid 40781093)
60. 2? Eur J Gastroenterol Hepatol 20:555-560 (Pubitemid 351667896)
61. Goncalves NS, Ghaem-Maghami M, Monteleone G et al (2001) Critical role for tumor necrosis factor alpha in controlling the number of lumenal pathogenic bacteria and immunopathology in infectious colitis. Infect Immun 69:6651-6659 (Pubitemid 32995420)
62. Curtis MM, Way SS (2009) Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126:177-185
63. El-behi M, Rostami A, Ciric B (2010) Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 5:189-197
64. Ma HL, Liang S, Li J et al (2008) IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J Clin Invest 118:597-607 (Pubitemid 351206549)
65. Kreymborg K, Etzensperger R, Dumoutier L et al (2007) IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. J Immunol 179:8098-8104
66. Sugimoto K, Ogawa A, Mizoguchi E et al (2008) IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 118:534-544 (Pubitemid 351206544)
67. Schmechel S, Konrad A, Diegelmann J et al (2008) Linking genetic susceptibility to Crohn's disease with Th17 cell function: IL-22 serum levels are increased in Crohn's disease and correlate with disease activity and IL23R genotype status. Inflamm Bowel Dis 14:204-212 (Pubitemid 351288041)
68. Sonnenberg GF, Nair MG, Kirn TJ et al (2010) Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J Exp Med 207:1293-1305
69. Dann SM, Spehlmann ME, Hammond DC et al (2008) IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol 180:6816-6826
70. Kitamura K, Nakamoto Y, Kaneko S et al (2004) Pivotal roles of interleukin-6 in transmural inflammation in murine T cell transfer colitis. J Leukoc Biol 76:1111-1117 (Pubitemid 39602946)
71. Yamamoto M, Yoshizaki K, Kishimoto T et al (2000) IL-6 is required for the development of Th1 cellmediated murine colitis. J Immunol 164:4878-4882 (Pubitemid 30238092)
72. Mitsuyama K, Sata M, Rose-John S (2006) Interleukin-6 trans-signaling in inflammatory bowel disease. Cytokine Growth Factor Rev 17:451-461 (Pubitemid 44793118)