Immunomodulation of Gut-Associated Lymphoid Tissue: Current Perspectives

REFERENCES

• C. Czerkinsky, F. Anjuere, J.R. McGhee, . Mucosal immunity and tolerance: Relevance to vaccine development. Immunol Rev 170: 197–222, 1999.
   PubMed Web of Science ®Google Scholar
• S. Fagarasan and T. Honjo. Intestinal IgA synthesis: Regulation of front line body defences. Nat Rev Immunol 3: 63–72, 2003.
   PubMed Web of Science ®Google Scholar
• R. Jerry, R. McGhee, J. Kunisawa, and H. Kimono. Gut lymphocyte migration: We are halfway ‘home’. Trends Immunol 28: 150–153, 2007.
   PubMed Web of Science ®Google Scholar
• J.D. Clements, N.M. Hartzog, and F.L. Lyon. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine 6: 269–277, 1988.
   PubMed Web of Science ®Google Scholar
• C.O. Elson. Cholera toxin and its subunits as potential oral adjuvants. Immunol Today 146: 29–33, 1989.
   Google Scholar
• N. Lycke, T. Tsuji, and J. Holmgren. The adjuvant effect of Vibrio cholerae and Escherichia coli heat-labile enterotoxins is linked to their ADP-ribosyltransferase activity. Eur J Immunol 22: 2277–2281, 1992.
   PubMed Web of Science ®Google Scholar
• J. Xu-Amano, H. Kiyono, and R.J. Jackson. Helper T cell subsets for immunoglobulin A responses: Oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J Exp Med 178: 1309–1320, 1993.
   PubMed Web of Science ®Google Scholar
• C.J. O'Neal, M.G. Jobling, R.K. Holmes, and W.G. Hol. Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309: 1093–1096, 2005.
   PubMed Web of Science ®Google Scholar
• N. Lycke and J. Holmgren. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 59: 301–308, 1986.
   PubMed Web of Science ®Google Scholar
• T. Tsuji, T. Inoue, A. Miyama, . A single amino acid substitution in the A subunit of Escherichia coli enterotoxin results in a loss of its toxic activity. J Biol Chem 265: 22520–22525, 1990.
   PubMed Web of Science ®Google Scholar
• N. Lycke, T. Tsuji, and J. Holmgren. The adjuvant effect of Vibrio cholerae and Escherichia coli heat-labile enterotoxins is linked to their ADP-ribosyltransferase activity. Eur J Immunol 22: 2277–2281, 1992.
   PubMed Web of Science ®Google Scholar
• K. Komase, S.-I. Tamura, K. Matsuo, . Mutants of Escherichia coli heat-labile enterotoxin as an adjuvant for nasal influenza vaccine. Vaccine 16: 248–254, 1998.
   PubMed Web of Science ®Google Scholar
• G. Douce, C. Turcotte, I. Cropley, . Mutants of Escherichia coli heat-labile toxin lacking ADP-ribosyltransferase activity act as nontoxic, mucosal adjuvants. Proc Natl Acad Sci U S A 92: 1644–1648, 1995.
   PubMed Web of Science ®Google Scholar
• B.L. Dickinson and J.D. Clements. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect Immun 63: 1617–1623, 1995.
   PubMed Web of Science ®Google Scholar
• S. Yamamoto, Y. Takeda, M. Yamamoto, . Mutants in the ADP-ribosyltransferase cleft of cholera toxin lack diarrheagenicity but retain adjuvanticity. J Exp Med 185: 1203–1210, 1997.
   PubMed Web of Science ®Google Scholar
• S. Yamamoto, H. Kiyono, M. Yamamoto, . A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc Natl Acad Sci USA 94: 5267–5272, 1997.
   PubMed Web of Science ®Google Scholar
• A. McI. Mowat, A. M. Donachie, S. Jägewall, . CTA1-DD-immune stimulating complexes: A novel, rationally designed combined mucosal vaccine adjuvant effective with nanogram doses of antigen. J Immunol 167: 3398–3405, 2007.
   Google Scholar
• A. McI. Mowat, R.E. Smith, A.M. Donachie, . Oral vaccination with immune stimulating complexes. Immunol Lett 65: 133–140, 1999.
   PubMed Web of Science ®Google Scholar
• A. Aguila, A.M. Donachie, M. Peyre, . Induction of protective and mucosal immunity against diphtheria by an immune stimulating complex (ISCOMS) based vaccine. Vaccine 24: 5201–5210, 2006.
   PubMed Web of Science ®Google Scholar
• H.-X. Suna, Y. Xiea, and Y.-P. Yec. ISCOMs and ISCOMATRIX™. Vaccine 2009 May 28. [Epub ahead of print].
   Web of Science ®Google Scholar
• W.T. McBurney, D.G. Lendemans, J. Myschik, . In vivo activity of cationic immune stimulating complexes (PLUSCOMs). Vaccine 26: 4549–4556, 2008.
   PubMed Web of Science ®Google Scholar
• A.M. Krieg, T. Wu, R. Weeratna, . Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs. Proc Natl Acad Sci USA 95: 12631–12636, 1998.
   PubMed Web of Science ®Google Scholar
• A.M. Krieg. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20: 709–760, 2002.
   PubMed Web of Science ®Google Scholar
• S. Raghavan, J. Nyström, M. Fredriksson, . Orally administered CpG oligodeoxynucleotide induces production of CXC and CC chemokines in the gastric mucosa and suppresses bacterial colonization in a mouse model of Helicobacter pylori infection. Infect Immunol 72: 1842–1853, 2004.
   Web of Science ®Google Scholar
• F. Obermeier, N. Dunger, U.G. Strauch, . Contrasting activity of cytosin--guanosin dinucleotide oligonucleotides in mice with experimental colitis. Clin Exp Immunol 134: 217–224, 2003.
   PubMed Web of Science ®Google Scholar
• S.H. Blaas, M. Stieber-Gunckel, W. Falk, . CpG-oligodeoxynucleotides stimulate immunoglobulin A secretion in intestinal mucosal B cells. Clin Exp Immunol 155: 534–540, 2009.
   PubMedGoogle Scholar
• C.F. Huang, C.C. Wang, T.C. Wu, . Neonatal sublingual vaccination with Salmonella proteins and adjuvant cholera toxin or CpG oligodeoxynucleotides induces mucosal and systemic immunity in mice. J Pediatr Gastroenterol Nutr 46: 262–271, 2008.
   PubMed Web of Science ®Google Scholar
• C.M. Galdeanoand and G. Perdigón. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 13: 219–226, 2006.
   PubMedGoogle Scholar
• C. Hessle, L.A. Hanson, and A.E. Wold. Lactobacilli from human gastrointestinal mucosa are strong stimulators of IL-12 production. Clin Exp Immunol 116: 276–282, 1999.
   PubMed Web of Science ®Google Scholar
• C. Hessle, B. Andersson, and A.E. Wold. Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL-12) while Gram-negative bacteria preferentially stimulate IL-10 production. Infect Immun 68: 3581–3586, 2000.
   PubMed Web of Science ®Google Scholar
• D. Haller, S. Blum, C. Bode, . Activation of human peripheral blood mononuclear cell by nonpathogenic bacteria in vitro: Evidence of NK cells as primary targets. Infect Immun 68: 752–759, 2000.
   PubMed Web of Science ®Google Scholar
• M. Mohamadzadeh, S. Olson, W.V. Kalina, . Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci 102: 2880–2885, 2005.
   PubMed Web of Science ®Google Scholar
• R. D'Arienzo, F. Maurano, D. Luongo, . Adjuvant effect of Lactobacillus casei in a mouse model of gluten sensitivity. Imm Lett 119: 78–83, 2008.
   PubMed Web of Science ®Google Scholar
• A. Kajikawa, E. Satoh, R.J. Leer, . Intragastric immunization with recombinant Lactobacillus casei expressing flagellar antigen confers antibody-independent protective immunity against Salmonella enterica serovar Enteritidis. Vaccine 25: 3599–3605, 2007.
   PubMed Web of Science ®Google Scholar
• I. Bergerot, C. Ploix, and J. Petersen. A cholera toxoid--insulin conjugate as an oral vaccine against spontaneous autoimmune diabetes. Proc Natl Acad Sci U S A 94: 4610–4614, 1997.
   PubMed Web of Science ®Google Scholar
• A. Tarkowski, J.-B. Sun, R. Holmdahl, . Treatment of experimental autoimmune arthritis by nasal administration of a type II collagen--cholera toxoid conjugate vaccine. Arthritis Rheum 42: 1628–1634, 1999.
   PubMed Web of Science ®Google Scholar
• J.-B. Sun, B.-G. Xiao, M. Lindblad, . Oral administration of cholera toxin B subunit conjugated to myelin basic protein protects against experimental autoimmune encephalomyelitis by inducing transforming growth factor-β-secreting cells and suppressing chemokine expression. Int Immunol 12: 1449–1457, 2000.
   PubMed Web of Science ®Google Scholar
• C. Rask, J. Holmgren, M. Fredriksson, . Prolonged oral treatment with low doses of allergen conjugated to cholera toxin B subunit suppresses immunoglobulin E antibody responses in sensitized mice. Clin Exp Allergy 30: 1024–1032, 2000.
   PubMed Web of Science ®Google Scholar
• M.P. Matousek, J.G. Nedrud, and C.V. Harding. Distinct effects of recombinant cholera toxin B subunit and holotoxin on different stages of class II MHC antigen processing and presentation by macrophages. J Immunol 156: 4137–4145, 1996.
   PubMed Web of Science ®Google Scholar
• M.L. Francis, J. Ryan, M.G. Jobling, . Cyclic AMP-independent effects of cholera toxin on B cell activation. II. Binding of ganglioside GM1 induces B cell activation. J Immunol 148: 1999–2005, 1992.
   PubMed Web of Science ®Google Scholar
• T.K. Li and B.S. Fox. Cholera toxin B subunit binding to an antigen-presenting cell directly co-stimulates cytokine production from a T cell clone. Int Immunol 8: 1849–1856, 1996.
   PubMed Web of Science ®Google Scholar
• C.P. Simmons, M. Ghaem-Magami, L. Petrovska, . Immunomodulation using bacterial enterotoxins. Scand J Immunol 53: 218–226, 2001.
   PubMed Web of Science ®Google Scholar
• N.A. Williams, T.R. Hirst, and T.O. Nashar. Immune modulation by the cholera-like enterotoxins: From adjuvant to therapeutic. Immunol Today 20: 95–101, 1999.
   PubMedGoogle Scholar
• J.B. Sun, C.F. Flach, C. Czerkinsky, and J. Holmgren. B lymphocytes promote expansion of regulatory T cells in oral tolerance: Powerful induction by antigen coupled to cholera toxin B subunit. J Immunol 181: 8278–8287, 2008.
   PubMed Web of Science ®Google Scholar
• M. Stanford, T. Whittall, A. Bergmeier, . Oral tolerization with peptide 336–351 linked to cholera toxin B subunit in preventing relapses of uveitis in Behcet's disease. Clin Exp Immunol 137: 201–208, 2004.
   PubMed Web of Science ®Google Scholar
• P.A. Phipps, M.R. Stanford, J.-B. Sun, B.G. Xiao, . Prevention of mucosally induced uveitis with a HSP60 derived peptide linked to cholera toxin B subunit. Eur J Immunol 33: 224–232, 2003.
   PubMed Web of Science ®Google Scholar
• R. Medzhitov and C. Janeway, Jr. The toll receptor family and microbial recognition. Trends Microbiol 8: 452–456, 2000.
   PubMed Web of Science ®Google Scholar
• W. Chen, W. Jin, N. Hardegen, . Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198: 1875–1886, 2003.
   PubMed Web of Science ®Google Scholar
• B.L. Kelsall and W. Strober. Dendritic cells of the gastrointestinal tract. Springer Semin Immunopathol 18: 409–420, 1997.
   PubMed Web of Science ®Google Scholar
• A.M. Mowat, A.M. Donachie, L.A. Parker, . The role of dendritic cells in regulating mucosal immunity and tolerance. Novartis Found Symp 252: 291–305, 2003.
   PubMedGoogle Scholar
• B.L. Kelsall, C.A. Biron, O. Sharma, and P.M. Kaye. Dendritic cells at the host-pathogen interface. Nat Immunol 3: 699–702, 2002.
   PubMed Web of Science ®Google Scholar
• D. Rachmilewitz, K. Katakura, F. Karmeli, . Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 126: 520–528, 2004.
   PubMed Web of Science ®Google Scholar
• C.B. Maassen, J.D. Laman, C. van Holten-Neelen, . Reduced experimental autoimmune encephalomyelitis after intranasal and oral administration of recombinant lactobacilli expressing myelin antigens. Vaccine 21: 4685–4693, 2003.
   PubMed Web of Science ®Google Scholar
• M.G. Roncarolo, S. Gregori, M. Battaglia, . Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 212: 28–50, 2006.
   PubMed Web of Science ®Google Scholar
• M.G. Roncarolo and M. Battaglia. Regulatory T cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat Rev Immunol 7: 585–598, 2007.
   PubMed Web of Science ®Google Scholar
• K.R. Groschwitz and S.P. Hogan. Intestinal barrier function: Molecular regulation and disease pathogenesis. J Allergy Clin Immunol 124: 3–20, 2009.
   PubMed Web of Science ®Google Scholar
• M.G. Buell and R.K. Harding. Proinflammatory effects of local abdominal irradiation on rat gastrointestinal tract. Dig Dis Sci 34: 390–399, 1989.
   PubMed Web of Science ®Google Scholar
• R. El Asmar, P. Panigrahi, P. Bamford, . Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology 123: 1607–1615, 2002.
   PubMed Web of Science ®Google Scholar
• R.J. Shulman, R.J. Schanler, C. Lau, . Early feeding, antenatal glucocorticoids, and human milk decrease intestinal permeability in preterm infants. Pediatr Res 44: 519–523, 1998.
   PubMed Web of Science ®Google Scholar
• T. Damci, I. Nuhoglu, G. Devranoglu, . Increased intestinal permeability as a cause of fluctuating postprandial blood glucose levels in Type 1 diabetic patients. Eur J Clin Invest 33: 397–401, 2003.
   PubMed Web of Science ®Google Scholar
• M. Secondulfo, D. Iafusco, R. Carratu, . Ultrastructural mucosal alterations and increased intestinal permeability in non-celiac, type I diabetic patients. Dig Liver Dis 36: 35–45, 2004.
   PubMedGoogle Scholar
• J.B. Meddings, J. Jarand, S.J. Urbanski, . Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am J Physiol 276: G951–G957, 1999.
   PubMed Web of Science ®Google Scholar
• M. Di Pierro, R. Lu, S. Uzzau, . Zonula occludens toxin structure-function analysis. Identification of the fragment biologically active on tight junctions and of the zonulin receptor binding domain. J Biol Chem 276: 19160–19165, 2001.
   PubMed Web of Science ®Google Scholar
• T. Watts, I. Berti, A. Sapone, . Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci U S A 102: 2916–2921, 2005.
   PubMed Web of Science ®Google Scholar
• L.M. Sollid. Coeliac disease: Dissecting a complex inflammatory disorder. Nat Rev Immunol 2: 647–655, 2002.
   PubMed Web of Science ®Google Scholar
• E. Nilsen, F.L. Jahnsen, K.E. Lundin, . Gluten induces an intestinal cytokine response strongly dominated by interferon gamma in patients with celiac disease. Gastroenterology 115: 551–563, 1998.
   PubMed Web of Science ®Google Scholar
• D. Branski, A. Fasano, and R. Troncone. Latest developments in the pathogenesis and treatment of celiac disease. J Pediatr 149: 295–300, 2006.
   PubMed Web of Science ®Google Scholar
• C. Gianfrani, S. Auricchio, and R. Troncone. Adaptive and innate immune responses in celiac disease. Immunol Lett 99: 141–145, 2005.
   PubMed Web of Science ®Google Scholar
• G. Forsberg, O. Hernell, S. Melgar, . Paradoxical coexpression of proinflammatory and down-regulatory cytokines in intestinal T cells in childhood celiac disease. Gastroenterology 123: 667–678, 2002.
   PubMed Web of Science ®Google Scholar
• C. Gianfrani, M.K. Levings, C. Sartirana, . Gliadin-specific type 1 regulatory T cells from the intestinal mucosa of treated celiac patients inhibit pathogenic T cells. J Immunol 177: 4178–4186, 2006.
   PubMed Web of Science ®Google Scholar
• V. Salvati, G. Mazzarella, C. Gianfrani, . Recombinant human IL-10 suppresses gliadin-dependent T cell activation in ex vivo cultured celiac intestinal mucosa. Gut 54: 46–53, 2005.
   PubMed Web of Science ®Google Scholar
• A. Fasano, T. Not, W. Wang, . Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet 355: 1518–1519, 2000.
   PubMed Web of Science ®Google Scholar
• P.J. Ciclitira, M.W. Johnson, D.H. Dewar, and H.J. Ellis. The pathogenesis of celiac disease. Mol Aspects Med 26: 421–458, 2005.
   PubMedGoogle Scholar
• D.R. Clayburgh, L. Shen, J.R. Turner. A porous defense: The leaky epithelial barrier in intestinal disease. Lab Invest 84: 282–291, 2004.
   PubMed Web of Science ®Google Scholar
• B.M. Paterson, K.M. Lammers, M.C. Arrieta, . The safety, tolerance, pharmacokinetic, and pharmacodynamic effects of single doses of AT-1001 in coeliac disease subjects: A proof of concept study. Aliment Pharmacol Ther 26: 757–766, 2007.
   PubMed Web of Science ®Google Scholar
• F. Hausch, L. Shan, N.A. Santiago, . Intestinal digestive resistance of immunodominant gliadin peptides. Am J Physiol Gastrointest Liver Physiol 283: G996–G1003, 2002.
   PubMed Web of Science ®Google Scholar
• L. Shan, O. Molberg, I. Parrot, . Structural basis for gluten intolerance in celiac sprue. Science 297: 2275–2279, 2002.
   PubMed Web of Science ®Google Scholar
• T. Marti, O. Molberg, Q. Li, . Prolyl endopeptidase-mediated destruction of T cell epitopes in whole gluten: Chemical and immunological characterization. J Pharmacol Exp Ther 312: 19–26, 2005.
   PubMed Web of Science ®Google Scholar
• N. Cerf-Bensussan, T. Matysiak-Budnik, C. Cellier, and M. Heyman. Oral proteases: A new approach to managing coeliac disease. Gut 56: 157–160, 2007.
   PubMed Web of Science ®Google Scholar
• L. Polgar. Prolyl endopeptidase catalysis. A physical rather than a chemical step is rate-limiting. Biochem J 283: 647–648, 1992.
   PubMed Web of Science ®Google Scholar
• C. Mitea, R. Havenaar, J. Wouter Drijfhout, . Efficient degradation of gluten by a prolyl endoprotease in a gastrointestinal model: Implications for coeliac disease. Gut 57: 25–32, 2008.
   PubMed Web of Science ®Google Scholar
• C. Gianfrani, R.A. Siciliano, A.M. Facchiano, . Transamidation inhibits the intestinal immune response to gliadin in vitro. Gastroenterology 133: 780–789, 2007.
   PubMed Web of Science ®Google Scholar