Chloride secretion induced by rotavirus is oxidative stress-dependent and inhibited by Saccharomyces boulardii in human enterocytes

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Buccigrossi, Vittoria ^a   Laudiero, Gabriella ^a   Russo, Carla ^a   Miele, Erasmo ^a   Sofia, Morena ^a   Monini, Marina ^b   Ruggeri, Franco Maria ^b   Guarino, Alfredo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CHLORIDE; GLUTATHIONE DISULFIDE; GLUTATHIONE SYNTHASE; NONSTRUCTURAL PROTEIN 4; PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE; ANTIOXIDANT; GLUTATHIONE; GLYCOPROTEIN; NS28 PROTEIN, ROTAVIRUS; TOXIN; VIRUS PROTEIN;

ANTIOXIDANT ACTIVITY; ARTICLE; CHILD; CHLORIDE SECRETION; CONTROLLED STUDY; ELECTROLYTE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTESTINE BIOPSY; INTESTINE CELL; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; ROTAVIRUS; ROTAVIRUS INFECTION; SACCHAROMYCES BOULARDII; CACO 2 CELL LINE; INTESTINE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SACCHAROMYCES; TUMOR CELL LINE; VIROLOGY;

ACETYLCYSTEINE; ANTIOXIDANTS; CACO-2 CELLS; CELL LINE, TUMOR; CHLORIDES; ENTEROCYTES; GLUTATHIONE; GLYCOPROTEINS; HUMANS; INTESTINES; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; ROTAVIRUS; ROTAVIRUS INFECTIONS; SACCHAROMYCES; TOXINS, BIOLOGICAL; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84903398974     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099830     Document Type: Article

References (36)

1. Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, et al. (2009) Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200: S9-S15. Available: http://www.ncbi.nlm.nih.gov/pubmed/19817620. Accessed 2 September 2011.
2. Albano F, Bruzzese E, Bella A, Cascio A, Titone L, et al. (2007) Rotavirus and not age determines gastroenteritis severity in children: a hospital-based study. Eur J Pediatr 166: 241-247. Available: http://www.ncbi.nlm.nih.gov/pubmed/16941130. Accessed 5 September 2012.
3. Forster J, Guarino A, Parez N, Moraga F, Román E, et al. (2009) Hospital-based surveillance to estimate the burden of rotavirus gastroenteritis among European children younger than 5 years of age. Pediatrics 123: e393-400. Available: http://www.ncbi.nlm.nih.gov/pubmed/19254975. Accessed 6 November 2011.
4. Parashar UD, Gibson CJ, Bresee JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12: 304-306. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3373114&tool= pmcentrez&rendertype=abstract. Accessed 26 July 2012.
5. Tanaka G, Faruque ASG, Luby SP, Malek MA, Glass RI, et al. (2007) Deaths from rotavirus disease in Bangladeshi children: estimates from hospital-based surveillance. Pediatr Infect Dis J 26: 1014-1018. Available: http://www.ncbi.nlm.nih.gov/pubmed/17984808. Accessed 6 September 2012.
6. Guarino A, Winter H, Sandhu B, Quak SH, Lanata C (2012) Acute gastroenteritis disease: Report of the FISPGHAN Working Group. J Pediatr Gastroenterol Nutr 55: 621-626. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 22983379. Accessed 4 February 2013.
7. Hagbom M, Sharma S, Lundgren O, Svensson L (2012) Towards a human rotavirus disease model. Curr Opin Virol 2: 408-418. Available: http://www.ncbi.nlm.nih.gov/pubmed/22722079. Accessed 24 July 2012.
8. Field M (2003) Intestinal ion transport and the pathophysiology of diarrhea. J Clin Invest 111: 931-943. doi:10.1172/JCI200318326.Worldwide.
9. De Marco G, Bracale I, Buccigrossi V, Bruzzese E, Canani RB, et al. (2009) Rotavirus induces a biphasic enterotoxic and cytotoxic response in human-derived intestinal enterocytes, which is inhibited by human immunoglobulins. J Infect Dis 200: 813-819. Available: http://www.ncbi.nlm.nih. gov/pubmed/19604044. Accessed 5 August 2011.
10. Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK (1996) Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 272: 101-104. Available: http://www.ncbi.nlm.nih.gov/pubmed/8600515. Accessed 6 September 2012.
11. Ousingsawat J, Mirza M, Tian Y, Roussa E, Schreiber R, et al. (2011) Rotavirus toxin NSP4 induces diarrhea by activation of TMEM16A and inhibition of Na+ absorption. Pflügers Arch Eur J Physiol 461: 579-589. Available: http://www.ncbi.nlm.nih.gov/pubmed/21399895. Accessed 30 June 2011.
12. Grisham MB, Gaginella TS, von Ritter C, Tamai H, Be RM, et al. (1990) Effects of neutrophil-derived oxidants on intestinal permeability, electrolyte transport, and epithelial cell viability. Inflammation 14: 531-542. Available: http://www.ncbi.nlm.nih.gov/pubmed/2174408. Accessed 3 February 2012.
13. Tamai H, Gaginella TS, Kachur JF, Musch MW, Chang EB (1992) Ca-mediated stimulation of Cl secretion by reactive oxygen metabolites in human colonic T84 cells. J Clin Invest 89: 301-307. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=442848&tool=pmcentrez&rendertype=abstract.
14. Nguyen TD, Canada AT (1994) Modulation of human colonic T84 cell secretion by hydrogen peroxide. Biochem Pharmacol 47: 403-410. Available: http://www.ncbi.nlm.nih.gov/pubmed/8304984. Accessed 3 February 2012.
15. Hosakote YM, Liu T, Castro SM, Garofalo RP, Casola A (2009) Respiratory syncytial virus induces oxidative stress by modulating antioxidant enzymes. Am J Respir Cell Mol Biol 41: 348-357. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=2742754&tool=pmcentrez&rendertype=abstract. Accessed 16 November 2011.
16. Ivanov A V, Smirnova O a, Ivanova ON, Masalova O V, Kochetkov SN, et al. (2011) Hepatitis C virus proteins activate NRF2/ARE pathway by distinct ROS-dependent and independent mechanisms in HUH7 cells. PLoS One 6: e24957. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 3172309&tool=pmcentrez&rendertype=abstract. Accessed 16 November 2011.
17. Agrawal L, Louboutin J-P, Reyes B a S, Van Bockstaele EJ, Strayer DS (2011) HIV-1 Tat neurotoxicity: A model of acute and chronic exposure, and neuroprotection by gene delivery of antioxidant enzymes. Neurobiol Dis: 1-14. Available: http://www.ncbi.nlm.nih.gov/pubmed/22036626. Accessed 16 November 2011.
18. Sodhi CP, Katyal R, Rana SV, Attri S S V. (1996) Study of oxidative-stress in rotavirus infected infant mice. Indian J Med Res 104: 245-249. (Pubitemid 26377269)
19. Gac M, Bigda J, Vahlenkamp TW (2010) Increased mitochondrial superoxide dismutase expression and lowered production of reactive oxygen species during rotavirus infection. Virology 404: 293-303. Available: http://www.ncbi.nlm.nih. gov/pubmed/20538313. Accessed 23 September 2011.
20. Corrêa NBO, Penna FJ, Lima FMLS, Nicoli JR, Filho L a P (2011) Treatment of Acute Diarrhea With Saccharomyces boulardii in Infants. J Pediatr Gastroenterol Nutr 53: 497-501. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 21734600. Accessed 16 November 2011.
21. Pieścik-Lech M, Shamir R, Guarino A, Szajewska H (2013) Review article: the management of acute gastroenteritis in children. Aliment Pharmacol Ther 37: 289-303. Available: http://www.ncbi.nlm.nih.gov/pubmed/23190209. Accessed 10 January 2013.
22. Guarino A, Lo Vecchio A, Canani RB (2009) Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol 25: 18-23. Available: http://www.ncbi.nlm.nih.gov/pubmed/19114770. Accessed 13 August 2012.
23. Pothoulakis C (2009) Review article: Anti-inflammatory mechanisms of action of Saccharomyces boulardii. Aliment Pharmacol Ther 30: 826-833. doi:10.1111/j.1365-2036.2009.04102.x.Review.
24. Buts J-P, De Keyser N (2010) Transduction pathways regulating the trophic effects of Saccharomyces boulardii in rat intestinal mucosa. Scand J Gastroenterol 45: 175-185. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 19958054. Accessed 23 September 2011.
25. Chen X, Kokkotou EG, Mustafa N, Bhaskar KR, Sougioultzis S, et al. (2006) Saccharomyces boulardii Inhibits ERK1/2 Mitogen-activated Protein Kinase Activation Both in Vitro and in Vivo and Protects against Clostridium difficile Toxin. J Biol Chem 281: 24449-24454. doi:10.1074/jbc.M605200200. (Pubitemid 44274218)
26. Rooj AK, Kimura Y, Buddington RK (2010) Metabolites produced by probiotic Lactobacilli rapidly increase glucose uptake by Caco-2 cells. BMC Microbiol 10: 16. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2835675&tool=pmcentrez&rendertype=abstract. Accessed 7 March 2013.
27. Tsilingiri K, Barbosa T, Penna G, Caprioli F, Sonzogni A, et al. (2012) Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex-vivo organ culture model. Gut 61: 1007-1015. Available: http://www.ncbi.nlm.nih.gov/pubmed/22301383. Accessed 19 November 2012.
28. Buccigrossi V, Laudiero G, Nicastro E, Miele E, Esposito F, et al. (2011) The HIV-1 Transactivator Factor (Tat) Induces Enterocyte Apoptosis through a Redox-Mediated Mechanism. PLoS One 6: e29436. Available: http://www. pubmedcentral.nih.gov/articlerender.fcgi?artid=3246489&tool= pmcentrez&rendertype=abstract. Accessed 8 February 2012.
29. Allen S, John S, Tara F, Jessica G, Paula D (2001) A kinetic microassay for glutathione in cells plated on 96-well microtiter plates. Methods cell Sci 22: 305-312. (Pubitemid 32926956)
30. Canani RB, Cirillo P, Mallardo G, Buccigrossi V, Secondo A, et al. (2003) Effects of HIV-1 Tat protein on ion secretion and on cell proliferation in human intestinal epithelial cells. Gastroenterology 124: 368-376. Available: http://www.ncbi.nlm.nih.gov/pubmed/12557143. Accessed 5 August 2011.
31. Lorrot M, Vasseur M (2007) How do the rotavirus NSP4 and bacterial enterotoxins lead differently to diarrhea? Virol J 4: 31. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1839081&tool= pmcentrez&rendertype=abstract. Accessed 7 September 2012.
32. Schultheiss G, Hennig B, Diener M (2008) Sites of action of hydrogen peroxide on ion transport across rat distal colon. Br J Pharmacol 154: 991-1000. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2451038&tool=pmcentrez&rendertype=abstract. Accessed 3 February 2012.
33. Morris AP, Scott JK, Ball JM, Zeng CQ, Wanda K, et al. (1999) NSP4 elicits age-dependent diarrhea and Ca2+- mediated I-influx into intestinal crypts of CF mice. Am J Physiol Gastrointest Liver Physiol 277: G431-G444. (Pubitemid 29415071)
34. Guarino A, Lo Vecchio A, Berni Canani R (2009) Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol 25: 18-23.
35. Dylag M, Szajewska H, Sko A (2007) Meta-analysis: Saccharomyces boulardii for treating acute diarrhoea in children. Aliment Pharmacol Ther: 257-264. doi:10.1111/j.1365-2036.2006.03202. x.
36. Tsilingiri K, Rescigno M (2013) Postbiotics: what else? Benef Microbes 4: 101-107. Available: http://www.ncbi.nlm.nih.gov/pubmed/23271068. Accessed 7 March 2013.