Selenium status alters the immune response and expulsion of adult heligmosomoides bakeri worms in mice

Infection and Immunity

Volumn 81, Issue 7, 2013, Pages 2546-2553

  Smith, Allen D ^a   Cheung, Lumei ^a   Beshah, Ethiopia ^a   Shea Donohue, Terez ^b   Urban, Joseph F ^a  

^a BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTHELMINTIC AGENT; GLUTATHIONE PEROXIDASE; SELENIUM;

ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; CYST; ENZYME ACTIVITY; GENE EXPRESSION; HELIGMOSOMOIDES; HELIGMOSOMOIDES BAKERI; HELIGMOSOMOIDES BAKERI INFECTION; IMMUNE RESPONSE; INOCULATION; LARVA; MALE; MOUSE; NONHUMAN; PARASITE; PARASITOSIS; PRIORITY JOURNAL; SELENIUM DEFICIENCY; SMALL INTESTINE; TH2 CELL; WORM EXPULSION;

EID: 84879424636     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01047-12     Document Type: Article

References (54)

1. Combs GF, Jr. 2001. Selenium in global food systems. Br. J. Nutr. 85:517- 547.
2. Rannem T, Ladefoged K, Hylander E, Hegnhoj J, Staun M. 1998. Selenium depletion in patients with gastrointestinal diseases: are there any predictive factors? Scand. J. Gastroenterol. 33:1057-1061.
3. Andoh A, Hirashima M, Maeda H, Hata K, Inatomi O, Tsujikawa T, Sasaki M, Takahashi K, Fujiyama Y. 2005. Serum selenoprotein-P levels in patients with inflammatory bowel disease. Nutrition 21:574-579.
4. Forceville X, Vitoux D, Gauzit R, Combes A, Lahilaire P, Chappuis P. 1998. Selenium, systemic immune response syndrome, sepsis, and outcome in critically ill patients. Crit. Care Med. 26:1536-1544.
5. Sakr Y, Reinhart K, Bloos F, Marx G, Russwurm S, Bauer M, Brunkhorst F. 2007. Time course and relationship between plasma selenium concentrations, systemic inflammatory response, sepsis, and multiorgan failure. Br. J. Anaesth. 98:775-784.
6. Angstwurm MW, Engelmann L, Zimmermann T, Lehmann C, Spes CH, Abel P, Strauss R, Meier-Hellmann A, Insel R, Radke J, Schuttler J, Gartner R. 2007. Selenium in Intensive Care (SIC): results of a prospective randomized, placebo-controlled, multiple-center study in patients with severe systemic inflammatory response syndrome, sepsis, and septic shock. Crit. Care Med. 35:118-126.
7. Manzanares W, Biestro A, Torre MH, Galusso F, Facchin G, Hardy G. 2011. High-dose selenium reduces ventilator-associated pneumonia and illness severity in critically ill patients with systemic inflammation. Intensive Care Med.
8. Kiremidjian-Schumacher L, Roy M, Wishe HI, Cohen MW, Stotzky G. 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.
9. Sakaguchi S, Iizuka Y, Furusawa S, Tanaka Y, Takayanagi M, Takayanagi Y. 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.
10. Kim IY, Stadtman TC. 1997. Inhibition of NF-kappaB DNA binding and nitric oxide induction in human T cells and lung adenocarcinoma cells by selenite treatment. Proc. Natl. Acad. Sci. U. S. A. 94:12904-12907.
11. Kim SH, Johnson VJ, Shin TY, Sharma RP. 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.
12. 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.
13. Baker SS, Cohen HJ. 1983. Altered oxidative metabolism in seleniumdeficient rat granulocytes. J. Immunol. 130:2856-2860.
14. Serfass RE, Ganther HE. 1975. Defective microbicidal activity in glutathione peroxidase-deficient neutrophils of selenium-deficient rats. Nature 255:640-641.
15. Beck MA, Matthews CC. 2000. Micronutrients and host resistance to viral infection. Proc. Nutr. Soc. 59:581-585.
16. Smith AD, Cheung L, Botero S. 2011. Long-term selenium deficiency increases the pathogenicity of a Citrobacter rodentium infection in mice. Biol. Trace Elem Res. 144:965-982.
17. Al-Shammari S, Khoja T, El-Khwasky F, Gad A. 2001. Intestinal parasitic diseases in Riyadh, Saudi Arabia: prevalence, sociodemographic and environmental associates. Trop. Med. Int. Health 6:184-189.
18. Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM. 2002. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359:564- 571.
19. Rodriguez L, Cervantes E, Ortiz R. 2011. Malnutrition and gastrointestinal and respiratory infections in children: a public health problem. Int. J. Environ. Res. Public Health 8:1174-1205.
20. Ing R, Su Z, Scott ME, Koski KG. 2000. Suppressed T helper 2 immunity and prolonged survival of a nematode parasite in protein-malnourished mice. Proc. Natl. Acad. Sci. U. S. A. 97:7078-7083.
21. Scott ME, Koski KG. 2000. Zinc deficiency impairs immune responses against parasitic nematode infections at intestinal and systemic sites. J. Nutr. 130:1412S-1420S.
22. Koski KG, Su Z, Scott ME. 1999. Energy deficits suppress both systemic and gut immunity during infection. Biochem. Biophys. Res. Commun. 264:796-801.
23. Patel N, Kreider T, Urban JF, Jr, Gause WC. 2009. Characterisation of effector mechanisms at the host:parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int. J. Parasitol. 39:13-21.
24. Anthony RM, Urban JF, Jr, Alem F, Hamed HA, Rozo CT, Boucher JL, Van Rooijen N, Gause WC. 2006. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12:955-960.
25. Herbert DR, Yang JQ, Hogan SP, Groschwitz K, Khodoun M, Munitz A, Orekov T, Perkins C, Wang Q, Brombacher F, Urban JF, Jr, Rothenberg ME, Finkelman FD. 2009. Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection. J. Exp. Med. 206:2947-2957.
26. Au Yeung KJ, Smith A, Zhao A, Madden KB, Elfrey J, Sullivan C, Levander O, Urban JF, Shea-Donohue T. 2005. Impact of vitamin E or selenium deficiency on nematode-induced alterations in murine intestinal function. Exp. Parasitol. 109:201-208.
27. Smith A, Madden KB, Yeung KJ, Zhao A, Elfrey J, Finkelman F, Levander O, Shea-Donohue T, Urban JF, Jr. 2005. Deficiencies in selenium and/or vitamin E lower the resistance of mice to Heligmosomoides polygyrus infections. J. Nutr. 135:830-836.
28. Beck MA, Kolbeck PC, Rohr LH, Shi Q, Morris VC, Levander OA. 1994. Vitamin E deficiency intensifies the myocardial injury of coxsackievirus B3 infection of mice. J. Nutr. 124:345-358.
29. Behnke J, Harris PD. 2010. Heligmosomoides bakeri: a new name for an old worm? Trends Parasitol. 26:524-529.
30. Persson L. 1974. A modified Baermann apparatus for the recovery of infective nematode larvae from herbage and manure. Zentralbl. Veterinarmed. B 21:483-488.
31. Liu Q, Kreider T, Bowdridge S, Liu Z, Song Y, Gaydo AG, Urban JF, Jr, Gause WC. 2010. B cells have distinct roles in host protection against different nematode parasites. J. Immunol. 184:5213-5223.
32. Dawson HD, Beshah E, Nishi S, Solano-Aguilar G, Morimoto M, Zhao A, Madden KB, Ledbetter TK, Dubey JP, Shea-Donohue T, Lunney JK, Urban JF, Jr. 2005. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect. Immun. 73:1116-1128.
33. 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.
34. 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.
35. Kangas L, Gronroos M, Nieminen AL. 1984. Bioluminescence of cellular ATP: a new method for evaluating cytotoxic agents in vitro. Med. Biol. 62:338-343.
36. Ishiwata K, Watanabe N. 2007. Nippostrongylus brasiliensis: reversibility of reduced-energy status associated with the course of expulsion from the small intestine in rats. Exp. Parasitol. 117:80-86.
37. Shea-Donohue T, Urban JF, Jr. 2004. Gastrointestinal parasite and host interactions. Curr. Opin. Gastroenterol. 20:3-9.
38. McCoy KD, Stoel M, Stettler R, Merky P, Fink K, Senn BM, Schaer C,Massacand J, Odermatt B, Oettgen HC, Zinkernagel RM, Bos NA, Hengartner H, Macpherson AJ, Harris NL. 2008. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4:362-373.
39. Forstrom JW, Zakowski JJ, Tappel AL. 1978. Identification of the catalytic site of rat liver glutathione peroxidase as selenocysteine. Biochemistry 17:2639-2644.
40. Tamura T, Stadtman TC. 1996. A new selenoprotein from human lung adenocarcinoma cells: purification, properties, and thioredoxin reductase activity. Proc. Natl. Acad. Sci. U. S. A. 93:1006-1011.
41. Dong L, Wang SJ, Camoretti-Mercado B, Li HJ, Chen M, Bi WX. 2008. FIZZ1 plays a crucial role in early stage airway remodeling of OVAinduced asthma. J. Asthma 45:648-653.
42. Chen F, Liu Z, Wu W, Rozo C, Bowdridge S, Millman A, Van Rooijen N, Urban JF, Jr, Wynn TA, Gause WC. 2012. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 18:260-266.
43. Beck MA, Nelson HK, Shi Q, Van Dael P, Schiffrin EJ, Blum S, Barclay D, Levander OA. 2001. Selenium deficiency increases the pathology of an influenza virus infection. FASEB J. 15:1481-1483.
44. Beck MA, Kolbeck PC, Shi Q, Rohr LH, Morris VC, Levander OA. 1994. Increased virulence of a human enterovirus (coxsackievirus B3) in selenium-deficient mice. J. Infect. Dis. 170:351-357.
45. Brigelius-Flohe R, Muller C, Menard J, Florian S, Schmehl K, Wingler K. 2001. Functions of GI-GPx: lessons from selenium-dependent expression and intracellular localization. Biofactors 14:101-106.
46. Esworthy RS, Ho YS, Chu FF. 1997. The Gpx1 gene encodes mitochondrial glutathione peroxidase in the mouse liver. Arch. Biochem. Biophys. 340:59-63.
47. Esworthy RS, Swiderek KM, Ho YS, Chu FF. 1998. Selenium-dependent glutathione peroxidase-GI is a major glutathione peroxidase activity in the mucosal epithelium of rodent intestine. Biochim. Biophys. Acta 1381: 213-226.
48. Wingler K, Bocher M, Flohe L, Kollmus H, Brigelius-Flohe R. 1999. mRNA stability and selenocysteine insertion sequence efficiency rank gastrointestinal glutathione peroxidase high in the hierarchy of selenoproteins. Eur. J. Biochem. 259:149-157.
49. Brophy PM, Ben-Smith A, Brown A, Behnke JM, Pritchard DI. 1995. Differential expression of glutathione S-transferase (GST) by adult Heligmosomoides polygyrus during primary infection in fast and slow responding hosts. Int. J. Parasitol. 25:641-645.
50. Hoffmann FW, Hashimoto AC, Shafer LA, Dow S, Berry MJ, Hoffmann PR. 2010. Dietary selenium modulates activation and differentiation of CD4_ T cells in mice through a mechanism involving cellular free thiols. J. Nutr. 140:1155-1161.
51. Shrimali RK, Irons RD, Carlson BA, Sano Y, Gladyshev VN, Park JM, Hatfield DL. 2008. Selenoproteins mediate T cell immunity through an antioxidant mechanism. J. Biol. Chem. 283:20181-20185.
52. Carlson BA, Yoo MH, Sano Y, Sengupta A, Kim JY, Irons R, Gladyshev VN, Hatfield DL, Park JM. 2009. Selenoproteins regulate macrophage invasiveness and extracellular matrix-related gene expression. BMC Immunol. 10:57.
53. Monick MM, Samavati L, Butler NS, Mohning M, Powers LS, Yarovinsky T, Spitz DR, Hunninghake GW. 2003. Intracellular thiols contribute to Th2 function via a positive role in IL-4 production. J. Immunol. 171: 5107-5115.
54. Nelson SM, Lei X, Prabhu KS. 2011. Selenium levels affect the IL-4-induced expression of alternative activation markers in murine macrophages. J. Nutr. 141:1754-1761.