Antigen sampling in the fish intestine

Developmental & Comparative Immunology - Tập 64 - Trang 138-149 - 2016
Guro Løkka1, Erling Olaf Koppang1
1Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine and Biosciences, Norwegian University of Life Sciences, Ullevålsveien 72, 0454 Oslo, Norway

Tóm tắt

Từ khóa


Tài liệu tham khảo

Abad, 1987, A comparative immunocytochemical study of the gastro-entero-pancreatic (GEP) endocrine system in a stomachless and a stomach-containing teleost, Gen. Comp. Endocrinol., 66, 123, 10.1016/0016-6480(87)90357-1

Abbate, 2012, Morphology of the European sea bass (Dicentrarchus labrax) tongue, Microsc. Res. Tech., 75, 643, 10.1002/jemt.21105

Adelmann, 2008, Development of an oral vaccine for immunisation of rainbow trout (Oncorhynchus mykiss) against viral haemorrhagic septicaemia, Vaccine, 26, 837, 10.1016/j.vaccine.2007.11.065

Adomako, 2012, Oral DNA vaccination of rainbow trout, Oncorhynchus mykiss (Walbaum), against infectious haematopoietic necrosis virus using PLGA [Poly(D,L-Lactic-Co-Glycolic Acid)] nanoparticles, J. Fish. Dis., 35, 203, 10.1111/j.1365-2761.2011.01338.x

Amthauer, 2001, Horseradish peroxidase binding to intestinal brush-border membranes of Cyprinus carpio. Identification of a putative receptor, J. Cell. Biochem., 80, 274, 10.1002/1097-4644(20010201)80:2<274::AID-JCB170>3.0.CO;2-A

Azad, 2000, Uptake and processing of biofilm and free-cell vaccines of Aeromonas hydrophila in Indian major carps and common carp following oral vaccination-antigen localization by a monoclonal antibody, Dis. Aquat. Organ., 43, 103, 10.3354/dao043103

Bakke-McKellep, 2007, Histological, digestive, metabolic, hormonal and some immune factor responses in Atlantic salmon, Salmo salar L., fed genetically modified soybeans, J. Fish. Dis., 30, 65, 10.1111/j.1365-2761.2007.00782.x

Ballesteros, 2013, The pyloric caeca area is a major site for IgM+ and IgT+ B cell recruitment in response to oral vaccination in rainbow trout, PLoS One, 8, e66118, 10.1371/journal.pone.0066118

Bockman, 1971, Fine structural analysis of pinocytosis in lymphoid follicle-associated epithelium in chick bursa and rabbit appendix, Fed. Proc. Fed. Am. Soc. Exp. Biol., 30, 511

Bockman, 1973, Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer's patches. An electron microscopic study, Am. J. Anat., 136, 455, 10.1002/aja.1001360406

Bockman, 1983, The role of epithelial cells in gut-associated immune reactivity, Ann. N.Y. Acad. Sci., 409, 129, 10.1111/j.1749-6632.1983.tb26864.x

Borghesi, 1999, Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer's patch, Lab. Investig., 79, 1393

Buddington, 2000, Digestive system, 379

Buddington, 1997, The intestines of carnivorous fish: structure and functions and the relations with diet, Acta Physiol. Scand. Suppl., 638, 67

Cain, 2011, Barrier function and immunology, 112

Casadei, 2009, Characterization of three novel β-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss), Mol. Immunol., 46, 3358, 10.1016/j.molimm.2009.07.018

Cerovic, 2014, Intestinal macrophages and dendritic cells: what's the difference?, Trends Immunol., 35, 270, 10.1016/j.it.2014.04.003

Chen, 2014, Augmentation of the antibody response of Atlantic salmon by oral administration of alginate-encapsulated IPNV antigens, PLoS One, 9, e109337, 10.1371/journal.pone.0109337

Chen, 2015, IPNV antigen uptake and distribution in Atlantic salmon following oral administration, Viruses, 7, 2507, 10.3390/v7052507

Cheroutre, 2011, The light and dark sides of intestinal intraepithelial lymphocytes, Nat. Rev. Immunol., 11, 445, 10.1038/nri3007

Companjen, 2006, Improved uptake of plant-derived LTB-linked proteins in carp gut and induction of specific humoral immune responses upon infeed delivery, Fish. Shellfish Immunol., 21, 251, 10.1016/j.fsi.2005.12.001

Dalmo, 1995, Microspheres as antigen carriers: studies on intestinal absorption and tissue localization of polystyrene microspheres in Atlantic salmon, Salmo salar L, J. Fish. Dis., 18, 87, 10.1111/j.1365-2761.1995.tb01270.x

Danilova, 2005, The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z, Nat. Immunol, 6, 295, 10.1038/ni1166

Davidson, 1994, A preliminary investigation into the phenomenon of oral tolerance in rainbow trout (Oncorhynchus mykiss, Walbaum, 1792), Fish. Shellfish Immunol., 4, 141, 10.1006/fsim.1994.1012

Davina, 1982, Effect of oral vaccination of Vibrio bacterin on the intestine of cyprinid fish, Dev. Comp. Immunol., 2, 157

De Santa Barbara, 2003, Development and differentiation of the intestinal epithelium, Cell Mol. Life Sci., 60, 1322, 10.1007/s00018-003-2289-3

Farache, 2013, Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense, Immunol. Cell Biol., 91, 232, 10.1038/icb.2012.79

Fuglem, 2010, Antigen-sampling cells in the salmonid intestinal epithelium, Dev. Comp. Immunol., 34, 768, 10.1016/j.dci.2010.02.007

Fujino, 1987, Studies on uptake of rabbit's immunoglobulin into the columnar epithelial cells in the gut of rainbow trout Salmo gairdneri, Bull. Jpn. Soc. Sci. Fish., 53, 367, 10.2331/suisan.53.367

Gauthier, 1972, The relationship of ultrastructural and cytochemical features to absorptive activity in the goldfish intestine, Anat. Rec., 172, 675, 10.1002/ar.1091720408

Georgopoulou, 1986, Local immunological response in the posterior intestinal segment of the rainbow trout after oral administration of macromolecules, Dev. Comp. Immunol., 10, 529, 10.1016/0145-305X(86)90174-6

Georgopoulou, 1985, Macromolecular absorption of proteins by epithelial cells of the posterior intestinal segment and their intracellular digestion in the rainbow trout. Ultrastructural and biochemical study, Biol. Cell, 53, 269

Georgopoulou, 1986, Immunological demonstration of intestinal absorption and digestion of protein macromolecules in the trout (Salmo gairdneri), Cell Tissue Res., 245, 387, 10.1007/BF00213946

Georgopoulou, 1988, Absorption of intact proteins by the intestinal epithelium of trout, Salmo gairdneri. A luminescence enzyme immunoassay and cytochemical study, Cell Tissue Res., 251, 145, 10.1007/BF00215459

Glimcher, 1992, Sequences and factors: a guide to MHC class-II transcription, Annu. Rev. Immunol., 10, 13, 10.1146/annurev.iy.10.040192.000305

Goto, 2013, Intestinal epithelial cells as mediators of the commensal-host immune crosstalk, Immunol. Cell Biol., 91, 204, 10.1038/icb.2012.80

Grisez, 1996, Mode of infection and spread of Vibrio anguillarum in turbot Scopthalmus maximus larvae after oral challenge through live feed, Dis. Aquat. Organ, 26, 181, 10.3354/dao026181

Guttvik, 2002, Oral administration of lipopolysaccharide to Atlantic salmon (Salmo salar L.) fry. Uptake, distribution, influence on growth and immune stimulation, Aquaculture, 214, 35, 10.1016/S0044-8486(02)00358-7

Hansen, 1992, Effect of different holding regimens on the intestinal microflora of herring (Clupea harengus) larvae, Appl. Environ. Microbiol., 58, 461, 10.1128/aem.58.2.461-470.1992

Harder, 1975, 128

Hart, 1987

Hart, 1988, Gut immunology in fish: a review, Dev. Comp. Immunol., 12, 453, 10.1016/0145-305X(88)90065-1

Hase, 2009, Uptake through glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response, Nature, 462, 226, 10.1038/nature08529

Hellberg, 2000, The anatomy of the oesophagus, stomach and intestine in common wolffish (Anarhichas lupus L.): a basis for diagnostic work and research, Acta Vet. Scand., 41, 283, 10.1186/BF03549637

Hellberg, 2013, Mast cells in common wolffish Anarhichas lupus L.: ontogeny, distribution and association with lymphatic vessels, Fish Shellfish Immunol., 35, 1769, 10.1016/j.fsi.2013.08.031

Hershberg, 2000, Antigen processing and presentation by intestinal epithelial cells - polarity and complexity, Immunol. Today, 21, 123, 10.1016/S0167-5699(99)01575-3

Holmgren, 2005, Mucosal immunity and vaccines, Nat. Med., 11, S45, 10.1038/nm1213

Howe, 2014, The uptake of soluble and particulate antigens by epithelial cells in the mouse small intestine, PLoS One, 9, e86656, 10.1371/journal.pone.0086656

Iida, 1985, Intracellular transport of horseradish peroxidase in the absorptive cells of goldfish hindgut in vitro, with special reference to the cytoplasmic tubules, Cell Tissue Res., 240, 553, 10.1007/BF00216344

Iida, 1986, The endosome-lysosome system in the absorptive cells of goldfish hindgut, Cell Tissue Res., 243, 449, 10.1007/BF00251064

Inami, 2009, Immunological differences in intestine and rectum of Atlantic cod (Gadus morhua L.), Fish. Shellfish Immunol., 26, 751, 10.1016/j.fsi.2009.03.007

Ishikawa, 2007, Curriculum vitae of intestinal intraepithelial T cells: their developmental and behavioral characteristics, Immunol. Rev., 215, 154, 10.1111/j.1600-065X.2006.00473.x

Jakobsson, 2015, The composition of the gut microbiota shapes the colon mucus barrier, EMBO Rep., 16, 164, 10.15252/embr.201439263

Jang, 2004, Intestinal villous M cells: an antigen entry site in the mucosal epithelium, Proc. Natl. Acad. Sci. U. S. A., 101, 6110, 10.1073/pnas.0400969101

Jenkins, 1991, Enhanced enteric uptake of human gamma globulin by Quil-A saponin in Oreochromis mossambicus, Fish. Shellfish Immunol., 1, 279, 10.1016/S1050-4648(05)80066-X

Jeurissen, 1985, Uptake of particulate and soluble antigens in the small intestines of the rat, Cell Biol. Int. Rep., 9, 523, 10.1016/0309-1651(85)90010-4

Jin, 2015, Atlantic salmon carries a range of novel O-glycan structures differentially localized on skin and intestinal mucins, J. Proteome Res., 14, 3239, 10.1021/acs.jproteome.5b00232

Joosten, 1996, Anal immunisation of carp and rainbow trout with different fractions of a Vibrio anguillarum bacterin, Fish. Shellfish Immunol., 6, 541, 10.1006/fsim.1996.0051

Joosten, 1997, Oral vaccination of fish against Vibrio anguillarum using alginate microparticles, Fish. Shellfish Immunol., 7, 471, 10.1006/fsim.1997.0100

Kapoor, 1975, The alimentary canal and digestion in teleosts, Adv. Mar. Biol., 13, 109, 10.1016/S0065-2881(08)60281-3

Khimmakthong, 2013, Tissue specific uptake of inactivated and live Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss): visualization by immunohistochemistry and in situ hybridization, Microb. Pathog., 59−60, 33, 10.1016/j.micpath.2013.03.001

Koppang, 1998, Expression of insulin-like growth factor-I in the gastrointestinal tract of Atlantic salmon (Salmo salar L.), Fish. Physiol. Biochem., 18, 165, 10.1023/A:1007771102755

Koppang, 2003, Production of rabbit antisera against recombinant MHC class II beta chain and identification of immunoreactive cells in Atlantic salmon (Salmo salar), Fish. Shellfish Immunol., 14, 115, 10.1006/fsim.2002.0424

Koppang, 2010, Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue, J. Anat., 217, 728

Kraehenbuhl, 2000, Epithelial M cells: differentiation and function, Annu. Rev. Cell Dev. Biol., 16, 301, 10.1146/annurev.cellbio.16.1.301

Kyd, 2008, Functional differences between M cells and enterocytes in sampling luminal antigens, Vaccine, 26, 6221, 10.1016/j.vaccine.2008.09.061

Langille, 1985, Protein and lipid absorption in the intestinal mucosa of adult lampreys (Petromyzon marinus L.) following induced feeding, Can. J. Zool., 63, 691, 10.1139/z85-099

Le Bail, 1989, Intestinal transfer of growth hormone into the circulatory system of the rainbow trout, Salmo gairdneri: interference by granule cells, J. Exp. Zool., 251, 101, 10.1002/jez.1402510112

Li, 2006, B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities, Nat. Immunol., 7, 1116, 10.1038/ni1389

Lin, 2000, Use of a lipid-emulsion carrier for immunisation of dab (Limanda limanda) by bath and oral routes: an assessment of systemic and mucosal antibody responses, Aquaculture, 181, 11, 10.1016/S0044-8486(99)00218-5

Løkka, 2013, Intestinal morphology of the wild Atlantic salmon (Salmo salar), J. Morphol., 274, 859, 10.1002/jmor.20142

Løkka, 2014, Immune parameters in the intestine of wild and reared unvaccinated and vaccinated Atlantic salmon (Salmo salar L.), Dev. Comp. Immunol., 47, 6, 10.1016/j.dci.2014.06.009

Løkka, 2014, Uptake of yeast cells in the Atlantic salmon (Salmo salar L.) intestine, Dev. Comp. Immunol., 47, 77, 10.1016/j.dci.2014.07.005

Lugton, 1999, Mucosa-associated lymphoid tissues as sites for uptake, carriage and excretion of tubercle bacilli and other pathogenic mycobacteria, Immunol. Cell Biol., 77, 364, 10.1046/j.1440-1711.1999.00836.x

Mahida, 1997, Migration of human intestinal lamina propria lymphocytes, macrophages and eosinophils following the loss of surface epithelial cells, Clin. Exp. Immunol., 109, 377, 10.1046/j.1365-2249.1997.4481346.x

McDole, 2012, Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine, Nature, 483, 345, 10.1038/nature10863

McGuckin, 2011, Mucin dynamics and enteric pathogens, Nat. Rev. Micro, 9, 265, 10.1038/nrmicro2538

McLean, 1990, Absorption of bioactive proteins by the gastrointestinal tract of fish: a review, J. Aquat. Anim. Health, 2, 1, 10.1577/1548-8667(1990)002<0001:AOBPBT>2.3.CO;2

McLean, 1999, Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts, Aquaculture, 177, 231, 10.1016/S0044-8486(99)00087-3

Menard, 2010, Multiple facets of intestinal permeability and epithelial handling of dietary antigens, Mucosal Immunol., 3, 247, 10.1038/mi.2010.5

Merrifield, 2009, Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum), J. Fish. Dis., 32, 755, 10.1111/j.1365-2761.2009.01052.x

Mestecky, 1994, Common mucosal immune system and strategies for the development of vaccines effective at the mucosal surfaces, 357

Mowat, 1997, The anatomical basis of intestinal immunity, Immunol. Rev., 156, 145, 10.1111/j.1600-065X.1997.tb00966.x

Nelson, 1985, Tissue location of Vibrio bacterin delivered by intraperitoneal injection, immersion and oral routes to Salmo gairdneri, Fish. Pathol., 19, 263, 10.3147/jsfp.19.263

Neuhaus, 2007, Biochemical and histochemical effects of perorally applied endotoxin on intestinal mucin glycoproteins of the common carp Cyprinus carpio, Dis. Aquat. Organ, 77, 17, 10.3354/dao01836

Neuhaus, 2007, Biochemical and histochemical study on the intestinal mucosa of the common carp Cyprinus carpio L., with special consideration of mucin glycoproteins, J. Fish. Biol., 70, 1523, 10.1111/j.1095-8649.2007.01438.x

Neumann, 2001, Antimicrobial mechanisms of fish phagocytes and their role in host defense, Dev. Comp. Immunol., 25, 807, 10.1016/S0145-305X(01)00037-4

Neutra, 2001, Collaboration of epithelial cells with organized mucosal lymphoid tissues, Nat. Immunol., 2, 1004, 10.1038/ni1101-1004

Noaillac-Depeyre, 1973, Absorption of protein macromolecules by the enterocytes of the carp (Cyprinus carpio L.). Ultrastructural and cytochemical study, Z. Zellforsch. Mikrosk. Anat., 146, 525, 10.1007/BF02347181

Noaillac-Depeyre, 1976, Electron microscopic study on gut epithelium of the tench (Tinca tinca L.) with respect to its absorptive functions, Tissue Cell, 8, 511, 10.1016/0040-8166(76)90010-0

Noaillac-Depeyre, 1979, Structure and function of the intestinal epithelial cells in the perch (Perca fluviatillis L.), Anat. Rec., 195, 621, 10.1002/ar.1091950405

O'Donnell, 1994, Uptake and fate of orally administered bacterial lipopolysaccharide in brown trout (Salmo trutta), Fish. Shellfish Immunol., 4, 285, 10.1006/fsim.1994.1025

O'Donnell, 1996, The uptake of human gamma globulin incorporated into poly (D,L-lactide-co-glycolide) microparticles following oral intubation in Atlantic salmon, Salmo salar L., Fish. Shellfish Immunol., 6, 507, 10.1006/fsim.1996.0048

Ohtani, 2015, Global 3D imaging of Yersinia ruckeri bacterin uptake in rainbow Trout fry, PLoS One, 10, 10.1371/journal.pone.0117263

Olafsen, 1992, Intact antigen uptake in intestinal epithelial cells of marine fish larvae, J. Fish. Biol., 40, 141, 10.1111/j.1095-8649.1992.tb02562.x

Øverland, 2010, Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.), Fish. Shellfish Immunol., 28, 193, 10.1016/j.fsi.2009.10.021

Owen, 1974, Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles, Gastroenterology, 66, 189, 10.1016/S0016-5085(74)80102-2

Owen, 1978, Antigen processing structures of the mammalian intestinal tract: a SEM study of lymphoepithelial organs, Scanning Electron Microsc., 2, 367

Pabst, 2012, Oral tolerance to food protein, Mucosal Immunol., 5, 232, 10.1038/mi.2012.4

Parham, 2009, 289

Parham, 2009, 71

Petrie, 2006, Evidence of particulate uptake by the gut of Atlantic salmon (Salmo salar L.), Fish. Shellfish Immunol., 20, 660, 10.1016/j.fsi.2005.07.006

Quentel, 1997, Antigen uptake and immune responses after oral vaccination, Dev. Biol. Stand., 90, 69

Ringø, 2001, Epithelium-associated bacteria in the gastrointestinal tract of Arctic charr (Salvelinus alpinus L.). An electron microscopical study, J. Appl. Microbiol., 90, 294, 10.1046/j.1365-2672.2001.01246.x

Ringø, 2011, Use of immunostimulants and nucleotides in aquaculture: a review, J. Mar. Sci. Res. Dev., 1

Rodrigues, 2006, Production and characterisation of alginate microparticles incorporating Aeromonas hydrophila designed for fish oral vaccination, Process Biochem., 41, 638, 10.1016/j.procbio.2005.08.010

Romarheim, 2013, Prevention of soya-induced enteritis in Atlantic salmon (Salmo salar) by bacteria grown on natural gas is dose dependent and related to epithelial MHC II reactivity and CD8α+ intraepithelial lymphocytes, Br. J. Nutr., 109, 1062, 10.1017/S0007114512002899

Rombout, 2014, Mucosal vaccination of fish, 56

Rombout, 1984, Immunohistochemical localization of (neuro)peptide hormones in endocrine cells and nerves of the gut of a stomachless teleost fish, Barbus conchonius (Cyprinidae), Cell Tissue Res., 237, 57, 10.1007/BF00229200

Rombout, 1989, Immunological importance of the second gut segment of carp. I. Uptake and processing of antigens by epithelial cells and macrophages, J. Fish. Biol., 35, 13, 10.1111/j.1095-8649.1989.tb03388.x

Rombout, 1985, Uptake and transport of intact macromolecules in the intestinal epithelium of carp (Cyprinus carpio L.) and the possible immunological implications, Cell Tissue Res., 239, 519, 10.1007/BF00219230

Rombout, 1986, Immunization of carp (Cyprinus carpio) with a Vibrio anguillarum bacterin: indications for a common mucosal immune system, Dev. Comp. Immunol., 10, 341, 10.1016/0145-305X(86)90024-8

Rombout, 1986, Immunocytochemical identification and localization of peptide hormones in the gastro-entero-pancreatic (GEP) endocrine system of the mouse and a stomachless fish, Barbus conchonius, Histochemistry, 84, 471, 10.1007/BF00482980

Rombout, 1989, Immunological importance of the second gut segment in carp. III. Systemic and/or mucosal immune responses after immunization with a soluble or particulate antigen, J. Fish. Biol., 35, 179, 10.1111/j.1095-8649.1989.tb02967.x

Rombout, 2011, Teleost intestinal immunology, Fish. Shellfish Immunol., 31, 616, 10.1016/j.fsi.2010.09.001

Rombout, 2014, Adaptive immune responses at mucosal surfaces of teleost fish, Fish. Shellfish Immunol., 40, 634, 10.1016/j.fsi.2014.08.020

Salinas, 2015, Fish mucosal immunity: intestine, 135

Salinas, 2011, Mucosal immunoglobulins and B cells of teleost fish, Dev. Comp. Immunol., 35, 1346, 10.1016/j.dci.2011.11.009

Sansonetti, 2004, War and peace at mucosal surfaces, Nat. Rev. Immunol., 4, 953, 10.1038/nri1499

Schroers, 2009, Changes of intestinal mucus glycoproteins after peroral application of Aeromonas hydrophila to common carp (Cyprinus carpio), Aquaculture, 288, 184, 10.1016/j.aquaculture.2008.12.013

Silverthorn, 2001, 602

Smith, 2005, Intestinal macrophages: unique effector cells of the innate immune system, Immunol. Rev., 206, 149, 10.1111/j.0105-2896.2005.00288.x

Smith, 2013, 55

Stroband, 1977, Growth and diet dependant structural adaptations of the digestive tract in juvenile grass carp (Ctenopharyngodon idella, Val.), J. Fish. Biol., 11, 167, 10.1111/j.1095-8649.1977.tb04110.x

Stroband, 1981, The development of the stomach in Clarias lazera and the intestinal absorption of protein macromolecules, Cell Tissue Res., 215, 397, 10.1007/BF00239123

Stroband, 1981, Localization of protein absorption during transport of food in the intestine of the grasscarp, Ctenopharyngodon idella (Val.), J. Exp. Zool., 218, 149, 10.1002/jez.1402180207

Strugnell, 2010, The role of secretory antibodies in infection immunity, Nat. Rev. Microbiol., 8, 656, 10.1038/nrmicro2384

Swan, 2008, Identification of a localized mucosal immune response in rainbow trout, Oncorhynchus mykiss (Walbaum), following immunization with a protein-hapten antigen, J. Fish. Dis., 31, 383, 10.1111/j.1365-2761.2008.00918.x

Tian, 2008, The formulation and immunisation of oral poly(DL-lactide-co-glycolide) microcapsules containing a plasmid vaccine against lymphocystis disease virus in Japanese flounder (Paralichthys olivaceus), Int. Immunopharmacol., 8, 900, 10.1016/j.intimp.2008.02.006

Turner, 2009, Intestinal mucosal barrier function in health and disease, Nat. Rev. Immunol., 9, 799, 10.1038/nri2653

Urán, 2008, Soybean meal-induced uptake block in Atlantic salmon Salmo salar distal enterocytes, J. Fish. Biol., 73, 2571, 10.1111/j.1095-8649.2008.02091.x

Valdenegro-Vega, 2013, Effect of immunization route on mucosal and systemic immune response in Atlantic salmon (Salmo salar), Vet. Immunol. Immunopathol., 151, 113, 10.1016/j.vetimm.2012.10.010

van der Marel, 2014, Differences between intestinal segments and soybean meal−induced changes in intestinal mucus composition of common carp Cyprinus carpio L., Aquac. Nutr., 20, 12, 10.1111/anu.12041

Vervarcke, 2005, Mucosal response in African catfish after administration of Vibrio anguillarum O2 antigens via different routes, Fish. Shellfish Immunol., 18, 125, 10.1016/j.fsi.2004.06.004

Vigneulle, 1991, Uptake of Vibrio anguillarum bacterin in the posterior intestine of rainbow trout Oncorhynchus mykiss, sea bass Dicentrarchus labrax and turbot Scophthalmus maximus after oral administration and anal intubation, Dis. Aquat. Organ, 11, 85, 10.3354/dao011085

Villumsen, 2014, Oral and anal vaccination confers full protection against enteric redmouth disease (ERM) in rainbow trout, PLoS One, 9, e93845, 10.1371/journal.pone.0093845

Wallace, 2005, Intestinal growth and differentiation in zebrafish, Mech. Dev., 122, 157, 10.1016/j.mod.2004.10.009

Watanabe, 1981, Ingestion of horseradish peroxidase by the intestinal cells in larvae and juveniles of some teleosts, Bull. Jpn. Soc. Sci. Fish., 47, 1299, 10.2331/suisan.47.1299

Watanabe, 1984, An ultrastructural study of intracellular digestion of horseradish peroxidase by the rectal epithelium cells in larvae of a freshwater cottid fish Cottus nozawae, Bull. Jpn. Soc. Sci. Fish., 50, 409, 10.2331/suisan.50.409

Winkelbach, 2015, Differences in IgY gut absorption in gastric rainbow trout (Oncorhynchus mykiss) and agastric common carp (Cyprinus carpio) assessed in vivo and in vitro, Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 167, 58, 10.1016/j.cbpc.2014.09.001

Young, 2006, 263

Zapata, 2000, Phylogeny of lower vertebrates and their immunological structures, Curr. Top. Microbiol. Immunol., 248, 67

Zhang, 2010, IgT, a primitive immunoglobulin class specialized in mucosal immunity, Nat. Immunol., 11, 827, 10.1038/ni.1913

Zhang, 2015, The intestinal epithelium as guardian of gut barrier integrity, Cell. Microbiol., 10.1111/cmi.12501