Porcine small intestinal epithelial cell line (IPEC-J2) of rotavirus infection as a new model for the study of innate immune responses to rotaviruses and probiotics

Viral Immunology

Volumn 23, Issue 2, 2010, Pages 135-149

  Liu, Fangning ^a,b   Li, Guohua ^b   Wen, Ke ^b   Bui, Tammy ^b   Cao, Dianjun ^b   Zhang, Yanming ^a   Yuan, Lijuan ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MUCIN 3; PROBIOTIC AGENT; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL LINE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOMODULATION; INNATE IMMUNITY; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS RHAMNOSUS; NONHUMAN; ROTAVIRUS; ROTAVIRUS INFECTION; SMALL INTESTINE MUCOSA; SWINE; VIRUS REPLICATION;

ANIMALS; CELL LINE; IMMUNITY, INNATE; INTERLEUKIN-6; INTESTINAL MUCOSA; MUCIN-3; PROBIOTICS; ROTAVIRUS; ROTAVIRUS INFECTIONS; SWINE; TOLL-LIKE RECEPTOR 2; VIRUS REPLICATION;

HUMAN ROTAVIRUS A; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS RHAMNOSUS; PORCINE ROTAVIRUS; ROTAVIRUS; SUID HERPESVIRUS 1; SUS;

EID: 77953925122     PISSN: 08828245     EISSN: None     Source Type: Journal    
DOI: 10.1089/vim.2009.0088     Document Type: Article

References (69)

1. Arce C, Ramirez-Boo M, Lucena C, and Garrido JJ: Innate immune activation of swine intestinal epithelial cell lines (IPEC-J2 and IPI-2I) in response to LPS from Salmonella typhimurium. Comp Immunol Microbiol Infect Dis.doi: 10.1016=j.cimid.2008.1008.1003.
2. Azevedo MS, Yuan L, Pouly S, Gonzales AM, Jeong KI, Nguyen TV, and Saif LJ: Cytokine responses in gnotobiotic pigs after infection with virulent or attenuated human rotavirus. J Virol 2006;80:372-382.
3. Azim T, Zaki MH, Podder G, et al.: Rotavirus-specific subclass antibody and cytokine responses in Bangladeshi children with rotavirus diarrhoea. J Med Virol 2003;69: 286-295.
4. Bohl EH, Theil KW, and Saif LJ: Isolation and serotyping of porcine rotaviruses and antigenic comparison with other rotaviruses. J Clin Microbiol 1984;19:105-111.
5. Borchers AT, Selmi C, Meyers FJ, Keen CL, and Gershwin ME: Probiotics and immunity. J Gastroenterol 2009; 44:26-46.
6. Boshuizen JA, Reimerink JH, Korteland-Van Male AM, et al.: Homeostasis and function of goblet cells during rotavirus infection in mice. Virology 2005;337:210-221.
7. Boshuizen JA, Reimerink JH, and Korteland-Van Male AM, et al.: Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol 2003;77:13005-13016.
8. Botic T, Klingberg TD, Weingartl H, and Cencic A: A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol 2007;115: 227-234.
9. Brown DR, and Price LD: Characterization of Salmonella enterica serovar Typhimurium DT104 invasion in an epithelial cell line (IPEC J2) from porcine small intestine. Vet Microbiol 2007;120:328-333.
10. Burkey TE, Skjolaas KA, Dritz SS, and Minton JE: Expression of porcine Toll-like receptor 2, 4 and 9 gene transcripts in the presence of lipopolysaccharide and Salmonella enterica serovars Typhimurium and Choleraesuis. Vet Immunol Immunopathol 2009;130:96-101.
11. Caballero-Franco C, Keller K, De Simone C, and Chadee K: The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 2007;292:G315-G322.
12. Cario E: Barrier-protective function of intestinal epithelial Toll-like receptor 2. Mucosal Immunol 2008;1(Suppl 1): S62-S66.
13. Cario E, Gerken G, and Podolsky DK: Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 2007;132:1359-1374.
14. Chang SK, Dohrman AF, Basbaum CB, et al.: Localization of mucin (MUC2 and MUC3) messenger RNA and peptide expression in human normal intestine and colon cancer. Gastroenterology 1994;107:28-36.
15. Chen CC, Baylor M, and Bass DM: Murine intestinal mucins inhibit rotavirus infection. Gastroenterology 1993;105:84-92.
16. Choi CH, Kim TI, Lee SK, Yang KM, and Kim WH: Effect of Lactobacillus GG and conditioned media on IL-1beta-induced IL-8 production in Caco-2 cells. Scand J Gastroenterol 2008;43:938-947.
17. De Vrese M, and Schrezenmeir J: Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 2008;111:1-66.
18. Didierlaurent A, Sirard JC, Kraehenbuhl JP, and Neutra MR: How the gut senses its content. Cell Microbiol 2002;4:61-72.
19. Ewaschuk JB, Backer JL, Churchill TA, Obermeier F, Krause DO, and Madsen KL: Surface expression of Toll-like receptor 9 is upregulated on intestinal epithelial cells in response to pathogenic bacterial DNA. Infect Immun 2007;75:2572-2579.
20. Guandalini S: Probiotics for children: use in diarrhea. J Clin Gastroenterol 2006;40:244-248.
21. Guandalini S: Probiotics for children with diarrhea: an update. J Clin Gastroenterol 2008;42(Suppl 2):S53-S57.
22. Guandalini S, Pensabene L, Zikri MA, et al.: Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediatr Gastroenterol Nutr 2000;30:54-60.
23. Guarino A, Canani RB, Spagnuolo MI, Albano F, and Di Benedetto L: Oral bacterial therapy reduces the duration of symptoms and of viral excretion in children with mild diarrhea. J Pediatr Gastroenterol Nutr 1997;25:516-519.
24. Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, and Koivula T: A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 1991;88:90-97.
25. Jiang B, Snipes-Magaldi L, Dennehy P, et al.: Cytokines as mediators for or effectors against rotavirus disease in children. Clin Diagn Lab Immunol 2003;10:995-1001.
26. Jorgenson RL, Young SL, Lesmeister MJ, Lyddon TD, and Misfeldt ML: Human endometrial epithelial cells cyclically express Toll-like receptor 3 (TLR3) and exhibit TLR3- dependent responses to dsRNA. Hum Immunol 2005;66: 469-482.
27. Koh SY, George S, Brozel V, Moxley R, Francis D, and Kaushik RS: Porcine intestinal epithelial cell lines as a new in vitro model for studying adherence and pathogenesis of enterotoxigenic Escherichia coli. Vet Microbiol 2008;130: 191-197.
28. Kopp E, and Medzhitov R: Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 2003;15:396-401.
29. Kumagai Y, Takeuchi O, and Akira S: TLR9 as a key receptor for the recognition of DNA. Adv Drug Deliv Rev 2008;60: 795-804.
30. Lan JG, Cruickshank SM, Singh JC, Farrar M, Lodge JP, Felsburg PJ, and Carding SR: Different cytokine response of primary colonic epithelial cells to commensal bacteria. World J Gastroenterol 2005;11:3375-3384.
31. Lievin-Le Moal V, and Servin AL: The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clin Microbiol Rev 2006;19:315-337.
32. Mack DR, Ahrne S, Hyde L, Wei S, and Hollingsworth MA: Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 2003;52:827-833.
33. Mack DR, Michail S, Wei S, McDougall L, and Hollingsworth MA: Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol 1999;276:G941-G950.
34. Madsen K, Cornish A, Soper P, et al.: Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 2001;121:580-591.
35. Manta S, Agelis G, Botic T, Cencic A, and Komiotis D: Fluoro-ketopyranosyl nucleosides: synthesis and biological evaluation of 3-fluoro-2-keto-beta-D-glucopyranosyl derivatives of N4-benzoyl cytosine. Bioorg Med Chem 2007; 15:980-987.
36. Mariani V, Palermo S, Fiorentini S, Lanubile A, and Giuffra E: Gene expression study of two widely used pig intestinal epithelial cell lines: IPEC-J2 and IPI-2I. Vet Immunol Immunopathol. doi:10.1016=j.vetimm.2009.1004. 1006.
37. Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, and Coran AG: Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int 2002;18:586-590.
38. Moncada DM, Kammanadiminti SJ, and Chadee K: Mucin and Toll-like receptors in host defense against intestinal parasites. Trends Parasitol 2003;19:305-311.
39. Moue M, Tohno M, Shimazu T, Kido T, Aso H, Saito T, and Kitazawa H: Toll-like receptor 4 and cytokine expression involved in functional immune response in an originally established porcine intestinal epitheliocyte cell line. Biochim Biophys Acta 2008;1780:134-144.
40. Netea MG, Van Der Meer JW, and Kullberg BJ: Toll-like receptors as an escape mechanism from the host defense. Trends Microbiol 2004;12:484-488.
41. Oswald IP: Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet Res 2006;37: 359-368.
42. Parashar UD, Gibson CJ, Bresse JS, and Glass RI: Rotavirus and severe childhood diarrhea. Emerg Infect Dis 2006;12: 304-306.
43. Pedersen G, Andresen L, Matthiessen MW, Rask-Madsen J, and Brynskov J: Expression of Toll-like receptor 9 and response to bacterial CpG oligodeoxynucleotides in human intestinal epithelium. Clin Exp Immunol 2005;141:298-306.
44. Pelto L, Isolauri E, Lilius EM, Nuutila J, and Salminen S: Probiotic bacteria down-regulate the milk-induced inflammatory response in milk-hypersensitive subjects but have an immunostimulatory effect in healthy subjects. Clin Exp Allergy 1998;28:1474-1479.
45. Rollo EE, Kumar KP, Reich NC, et al.: The epithelial cell response to rotavirus infection. J Immunol 1999;163:4442-4452.
46. Rosenfeldt V, Michaelsen K, Jakobsen M, et al.: Effect of probiotic Lactobacillus strains in young children hospitalized with acute diarrhea. Pediatr Infect Dis J 2002;21:411-416.
47. Sanders ME, and Klaenhammer TR: Invited review: the scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. J Dairy Sci 2001;84:319-331.
48. Sato A, Iizuka M, Nakagomi O, et al.: Rotavirus doublestranded RNA induces apoptosis and diminishes wound repair in rat intestinal epithelial cells. J Gastroenterol Hepatol 2006;21:521-530.
49. Schierack P, Nordhoff, M, Pollmann M, et al.: Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem Cell Biol 2006;125:293-305.
50. Sheth R, Anderson J, Sato T, et al.: Rotavirus stimulates IL-8 secretion from cultured epithelial cells. Virology 1996;221: 251-259.
51. Skjolaas KA, Burkey TE, Dritz SS, and Minton JE: Effects of Salmonella enterica serovar Typhimurium, or serovar Choleraesuis, Lactobacillus reuteri and Bacillus licheniformis on chemokine and cytokine expression in the swine jejunal epithelial cell line, IPEC-J2. Vet Immunol Immunopathol 2007;115:299-308.
52. Taima K, Imaizumi T, Yamashita K, et al.: Expression of IP- 10=CXCL10 is upregulated by double-stranded RNA in BEAS- 2B bronchial epithelial cells. Respiration 2006;73:360-364.
53. Teran CG, Teran-Escalera CN, and Villarroel P: Nitazoxanide vs. probiotics for the treatment of acute rotavirus diarrhea in children: a randomized, single-blind, controlled trial in Bolivian children. Int J Infect Dis 2009;13:518-523.
54. Uematsu S, and Akira S: Toll-like receptors and Type I interferons. J Biol Chem 2007;282:15319-15323.
55. Vercammen E, Staal J, and Beyaert R: Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin Microbiol Rev 2008;21:13-25.
56. Vijay-Kumar M, Gentsch JR, Kaiser WJ, Borregaard N, Offermann MK, Neish AS, and Gewirtz AT: Protein kinase R mediates intestinal epithelial gene remodeling in response to double-stranded RNA and live rotavirus. J Immunol 2005;174:6322-6331.
57. Vizoso Pinto MG, Rodriguez Gomez M, Seifert S, Watzl B, Holzapfel WH, and Franz CM: Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol 2009;133:86-93.
58. Ward LA, Rosen BI, Yuan L, and Saif LJ: Pathogenesis of an attenuated and a virulent strain of group A human rotavirus in neonatal gnotobiotic pigs. J Gen Virol 1996;77 (Pt 7):1431-1441.
59. Watson JL, and McKay DM: The immunophysiological impact of bacterial CpG DNA on the gut. Clin Chim Acta 2006;364:1-11.
60. Weiss AA, Babyatsky MW, Ogata S, Chen A, and Itzkowitz SH: Expression of MUC2 and MUC3 mRNA in human normal, malignant, and inflammatory intestinal tissues. J Histochem Cytochem 1996;44:1161-1166.
61. Wen K, Azevedo MS, Gonzalez A, et al.: Toll-like receptor and innate cytokine responses induced by lactobacilli colonization and human rotavirus infection in gnotobiotic pigs. Vet Immunol Immunopathol 2009;127:304-315.
62. Yolken RH, Ojeh C, Khatri I., Sajjan U, and Forstner JF: Intestinal mucins inhibit rotavirus replication in an oligosaccharide- dependent manner. J Infect Dis 1994;169:1002-1006.
63. Yuan L, and Saif LJ: Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model. Vet Immunol Immunopathol 2002;87:147-160.
64. Zeuthen LH, Christensen HR, and Frokiaer H: Lactic acid bacteria inducing a weak interleukin-12 and tumor necrosis factor alpha response in human dendritic cells inhibit strongly stimulating lactic acid bacteria but act synergistically with gram-negative bacteria. Clin Vaccine Immunol 2006;13:365-375.
65. Zhang L, Li N, Caicedo R, and Neu J: Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factoralpha- induced interleukin-8 production in Caco-2 cells. J Nutr 2005;135:1752-1756.
66. Zhang L, Li N, Des Robert C, Fang M, Liboni K, McMahon R, Caicedo RA, and Neu J: Lactobacillus rhamnosus GG decreases lipopolysaccharide-induced systemic inflammation in a gastrostomy-fed infant rat model. J Pediatr Gastroenterol Nutr 2006;42:545-552.
67. Zhang L, Xu YQ, Liu HY, Lai T, Ma JL, Wang JF, and Zhu YH: Evaluation of Lactobacillus rhamnosus GG using an Escherichia coli K88 model of piglet diarrhoea: Effects on diarrhoea incidence, faecal microflora and immune responses. Vet Microbiol 141:142-148.
68. Zhang W, Azevedo MS, Wen K, et al.: Probiotic Lactobacillus acidophilus enhances the immunogenicity of an oral rotavirus vaccine in gnotobiotic pigs. Vaccine 2008;26:3655-3661.
69. Zhou R, Wei H, Sun R, and Tian Z: Recognition of doublestranded RNA by TLR3 induces severe small intestinal injury in mice. J Immunol 2007;178:4548-4556.