Intestinal barrier of carp (Cyprinus carpio L.) during a cyprinid herpesvirus 3-infection: Molecular identification and regulation of the mRNA expression of claudin encoding genes

Fish and Shellfish Immunology

Volumn 34, Issue 1, 2013, Pages 305-314

  Syakuri, Hamdan ^a,d   Adamek, Mikołaj ^a   Brogden, Graham ^a   Rakus, Krzysztof Ł ^b,e   Matras, Marek ^c   Irnazarow, Ilgiz ^b   Steinhagen, Dieter ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b Polish Academy of Sciences   (Poland)

^c NATIONAL VETERINARY RESEARCH INSTITUTE   (Poland)

^d JENDERAL SOEDIRMAN UNIVERSITY   (Indonesia)

^e UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Barrier intestine; Claudin gene; Cyprinid herpesvirus 3; Cyprinus carpio; Koi herpesvirus

Indexed keywords

CYPRINIDAE; CYPRINUS CARPIO; HERPESVIRIDAE; KOI HERPESVIRUS; VERTEBRATA;

EID: 84871611577     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2012.11.010     Document Type: Article

References (81)

1. FAO Cultured aquatic species information Programme Cyprinus carpio (Linnaeus, 1758) 2011, Food and Agriculture Organization of the United Nations.
2. Ahmed M., Lorica M.H. Improving developing country food security through aquaculture development-lessons from Asia. Food Policy 2002, 27:125-141.
3. Liao I.C., Chao N.H. Aquaculture and food crisis: opportunities and constraints. Asia Pacific Journal of Clinical Nutrition 2009, 18:564-569.
4. Hedrick R.P., Gilad O., Yun S., Spangenberg J.V., Marty G.D., Nordhausen R.W., et al. A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. Journal of Aquatic Animal Health 2000, 12:44-57.
5. Pikarsky E., Ronen A., Abramowitz J., Levavi-Sivan B., Hutoran M., Shapira Y., et al. Pathogenesis of acute viral disease induced in fish by carp interstitial nephritis and gill necrosis virus. Journal of Virology 2004, 78:9544-9551.
6. Waltzek T.B., Kelley G.O., Stone D.M., Way K., Hanson L., Fukuda H., et al. Koi herpesvirus represents a third cyprinid herpesvirus (CyHV-3) in the family Herpesviridae. Journal of General Virology 2005, 86:1659-1667.
7. Bretzinger A., Fisher-Scherl T., Oumouna M., Hoffmann R., Truyen U. Mass mortalities in koi carp, Cyprinus carpio, associated with gill and skin disease. Bulletin of the European Association of Fish Pathologist 1999, 19:182-185.
8. Neukirch M., Böttcher K., Bunnajirakul S. Isolation of a virus from koi with altered gills. Bulletin of the European Association of Fish Pathologist 1999, 19:221-224.
9. Walster C.I. Clinical observations of severe mortalities in koi carp, Cyprinus carpio, with gill disease. Fish Veterinary Journal 1999, 3:54-58.
10. Gray W.L., Mullis L., LaPatra S.E., Groff J.M., Goodwin A. Detection of koi herpesvirus DNA in tissues of infected fish. Journal of Fish Diseases 2002, 25:171-178.
11. Ishioka T., Yoshizumi M., Izumi S., Suzuki K., Suzuki H., Kozawa K., et al. Detection and sequence analysis of DNA polymerase and major envelope protein genes in koi herpesviruses derived from Cyprinus carpio in Gunma prefecture, Japan. Veterinary Microbiology 2005, 110:27-33.
12. Sunarto A., Rukyani A., Itami T. Indonesian experience on the outbreak of koi herpesvirus in koi and carp (Cyprinus carpio). Bulletin of Fisheries Research Agency Supplement 2005, 2:15-21.
13. Cheng L., Chen C.Y., Tsai M.A., Wang P.C., Hsu J.P., Chern R.S., et al. Koi herpesvirus epizootic in cultured carp and koi, Cyprinus carpio L., in Taiwan. Journal of Fish Diseases 2011, 34:547-554.
14. Gilad O., Yun S., Zagmutt-Vergara F.J., Leutenegger C.M., Bercovier H., Hedrick R.P. Concentrations of a koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Diseases of Aquatic Organisms 2004, 60:179-187.
15. Gibson J.S., Ellory J.C., Cossins A.R. Temperature acclimation of intestinal Na+ transport in the carp (Cyprinus carpio L.). The Journal of Experimental Biology 1985, 114:355-364.
16. Eveloff J., Field M., Kinne R., Murer H. Sodium-cotransport systems in intestine and kidney of the winter flounder. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 1980, 135:175-182.
17. Sire M.F., Vernier J.M. Intestinal absorption of protein in teleost fish. Comparative Biochemistry and Physiology Part A: Physiology 1992, 103:771-781.
18. Hart S., Wrathmell A.B., Harris J.E., Grayson T.H. Gut immunology in fish: a review. Developmental & Comparative Immunology 1988, 12:453-480.
19. Groschwitz K.R., Hogan S.P. Intestinal barrier function: molecular regulation and disease pathogenesis. Journal of Allergy and Clinical Immunology 2009, 124:3-20.
20. Rombout J.H.W.M., Abelli L., Picchietti S., Scapigliati G., Kiron V. Teleost intestinal immunology. Fish & Shellfish Immunology 2011, 31:616-626.
21. Jutfelt F., Sundh H., Glette J., Mellander L., Thrandur Björnsson B., Sundell K. The involvement of Aeromonas salmonicida virulence factors in bacterial translocation across the rainbow trout, Oncorhynchus mykiss (Walbaum), intestine. Journal of Fish Diseases 2008, 31:141-151.
22. Ringø E., Myklebust R., Mayhew T.M., Olsen R.E. Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 2007, 268:251-264.
23. Will C., Fromm M., Muller D. Claudin tight junction proteins: novel aspects in paracellular transport. Peritoneal Dialysis International 2008, 28:577-584.
24. Heiskala M., Peterson P.A., Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2001, 2:92-98.
25. Van Itallie C.M., Anderson J.M. Claudins and epithelial paracellular transport. Annual Review of Physiology 2006, 68:403-429.
26. Lal-Nag M., Morin P. The claudins. Genome Biology 2009, 10:235.
27. Mineta K., Yamamoto Y., Yamazaki Y., Tanaka H., Tada Y., Saito K., et al. Predicted expansion of the claudin multigene family. FEBS Letters 2011, 585:606-612.
28. Kollmar R., Nakamura S.K., Kappler J.A., Hudspeth A.J. Expression and phylogeny of claudins in vertebrate primordia. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:10196-10201.
29. Loh Y.H., Christoffels A., Brenner S., Hunziker W., Venkatesh B. Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Research 2004, 14:1248-1257.
30. Bagherie-Lachidan M., Wright S.I., Kelly S.P. Claudin-3 tight junction proteins in Tetraodon nigroviridis: cloning, tissue-specific expression, and a role in hydromineral balance. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2008, 294:R1638-R1647.
31. Tipsmark C.K., Kiilerich P., Nilsen T.O., Ebbesson L.O.E., Stefansson S.O., Madsen S.S. Branchial expression patterns of claudin isoforms in Atlantic salmon during seawater acclimation and smoltification. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2008, 294:R1563-R1574.
32. Tipsmark C.K., Luckenbach J.A., Madsen S.S., Kiilerich P., Borski R.J. Osmoregulation and expression of ion transport proteins and putative claudins in the gill of Southern Flounder (Paralichthys lethostigma). Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2008, 150:265-273.
33. Chasiotis H., Kelly S.P. Effect of cortisol on permeability and tight junction protein transcript abundance in primary cultured gill epithelia from stenohaline goldfish and euryhaline trout. General and Comparative Endocrinology 2011, 172:494-504.
34. Sandbichler A.M., Egg M., Schwerte T., Pelster B. Claudin 28b and F-actin are involved in rainbow trout gill pavement cell tight junction remodeling under osmotic stress. Journal of Experimental Biology 2011, 214:1473-1487.
35. Poritz L.S., Harris L.R., Kelly A.A., Koltun W.A. Increase in the tight junction protein claudin-1 in intestinal inflammation. Digestive Disease and Sciences 2011, 56:2802-2809.
36. Prasad S., Mingrino R., Kaukinen K., Hayes K.L., Powell R.M., MacDonald T.T., et al. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Laboratory Investigation 2005, 85:1139-1162.
37. Berkes J., Viswanathan V.K., Savkovic S.D., Hecht G. Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation. Gut 2003, 52:439-451.
38. Guttman J.A., Finlay B.B. Tight junctions as targets of infectious agents. Biochimica et Biophysica Acta (BBA) - Biomembranes 2009, 1788:832-841.
39. Nava P., López S., Arias C.F., Islas S., González-Mariscal L. The rotavirus surface protein VP8 modulates the gate and fence function of tight junctions in epithelial cells. Journal of Cell Science 2004, 117:5509-5519.
40. Medigeshi G.R., Hirsch A.J., Brien J.D., Uhrlaub J.L., Mason P.W., Wiley C., et al. West Nile virus capsid degradation of claudin proteins disrupts epithelial barrier function. Journal of Virology 2009, 83:6125-6134.
41. Katahira J., Sugiyama H., Inouei N., Horiguchi Y., Matsuda M., Sugimoto N. Clostridium perfringens enterotoxin utilizes two structurally related membrane proteins as functional receptors in vivo. The Journal of Biological Chemistry 1997, 272:26652-26658.
42. Sonoda N., Furuse M., Sasaki H., Yonemura S., Katahira J., Horiguchi Y., et al. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. The Journal of Cell Biology 1999, 147:195-204.
43. Olsen R.E., Sundell K., Mayhew T.M., Myklebust R., Ringø E. Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 2005, 250:480-495.
44. Negenborn J. Klinisch-chemische parameter im Blut und Urin von Karpfen unter infection mit dem Koi Herpesvirus. Thesis of Dr. Med. Vet. at University of Veterinary Medicine Hannover, Hannover; 2009, p. 129.
45. Rakus K.Ł., Irnazarow I., Adamek Ma, Palmeira L., Kawana Y., Hirono I., et al. Gene expression analysis of common carp (Cyprinus carpio L.) lines during cyprinid herpesvirus 3 infection yields insights into differential immune responses. Developmental & Comparative Immunology 2012, 37:65-76.
46. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols 1999, 365-386.
47. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. Journal of Molecular Biology 1990, 215:403-410.
48. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research 2003, 31:3784-3788.
49. Pagni M., Ioannidis V., Cerutti L., Zahn-Zabal M., Jongeneel C.V., Falquet L. MyHits: a new interactive resource for protein annotation and domain identification. Nucleic Acids Research 2004, 32:W332-W335.
50. Pagni M., Ioannidis V., Cerutti L., Zahn-Zabal M., Jongeneel C.V., Hau J., et al. MyHits: improvements to an interactive resource for analyzing protein sequences. Nucleic Acids Research 2007, 35:W433-W437.
51. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
52. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 2003, 52:696-704.
53. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 2004, 32:1792-1797.
54. Anisimova M., Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 2006, 55:539-552.
55. Chevenet F., Brun C., Banuls A.L., Jacq B., Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 2006, 7:439.
56. Dereeper A., Audic S., Claverie J.M., Blanc G. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evolutionary Biology 2010, 10:8.
57. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 2008, 36:W465-W469.
58. van der Marel M., Adamek M., Gonzalez S.F., Frost P., Rombout J.H.W.M., Wiegertjes G.F., et al. Molecular cloning and expression of two β-defensin and two mucin genes in common carp (Cyprinus carpio L.) and their up-regulation after β-glucan feeding. Fish & Shellfish Immunology 2012, 32:494-501.
59. Adamek M., Rakus K.L., Chyb J., Brogden G., Huebner A., Irnazarow I., et al. Interferon type I responses to virus infections in carp cells: in vitro studies on cyprinid herpesvirus 3 and Rhabdovirus carpio infections. Fish & Shellfish Immunology 2012, 33:482-493.
60. Forlenza M., Dias J.D.A.D.C., Veselý T., Pokorová D., Savelkoul H.F.J., Wiegertjes G.F. Transcription of signal-3 cytokines, IL-12 and IFNαβ, coincides with the timing of CD8αβ up-regulation during viral infection of common carp (Cyprinus carpio L. Molecular Immunology 2008, 45:1531-1547.
61. Urán P.A., Gonçalves A.A., Taverne-Thiele J.J., Schrama J.W., Verreth J.A.J., Rombout J.H.W.M. Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish & Shellfish Immunology 2008, 25:751-760.
62. Furuse M., Fujita K., Hiiragi T., Fujimoto K., Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. The Journal of Cell Biology 1998, 141:1539-1550.
63. Morita K., Furuse M., Fujimoto K., Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:511-516.
64. Tipsmark C.K., Sørensen K.J., Hulgard K., Madsen S.S. Claudin-15 and -25b expression in the intestinal tract of Atlantic salmon in response to seawater acclimation, smoltification and hormone treatment. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2010, 155:361-370.
65. Holmes J.L., Van Itallie C.M., Rasmussen J.E., Anderson J.M. Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expression Patterns 2006, 6:581-588.
66. Jutfelt F. Barrier function of the gut. Encyclopedia of fish physiology: from genome to environment 2011, Academic Press. A.P. Farrell (Ed.).
67. Robbins R.A., Grisham M.B. Nitric oxide. The International Journal of Biochemistry & Cell Biology 1997, 29:857-860.
68. Evans M.J., von Hahn T., Tscherne D.M., Syder A.J., Panis M., Wolk B., et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007, 446:801-805.
69. Meertens L., Bertaux C., Cukierman L., Cormier E., Lavillette D., Cosset F.-L., et al. The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. The Journal of Virology 2008, 82:3555-3560.
70. Shinozaki A., Ushiku T., Morikawa T., Hino R., Sakatani T., Uozaki H., et al. Epstein-barr virus-associated gastric carcinoma: a distinct carcinoma of gastric phenotype by claudin expression profiling. Journal of Histochemistry Cytochemistry 2009, 57:775-785.
71. András I.E., Toborek M. HIV-1-induced alterations of claudin-5 expression at the blood-brain barrier level. Methods in Molecular Biology 2011, 762:355-370.
72. Schulzke J.D., Ploeger S., Amasheh M., Fromm A., Zeissig S., Troeger H., et al. Epithelial tight junctions in intestinal inflammation. Annals of the New York Academy of Sciences 2009, 1165:294-300.
73. Banan A., Fields J.Z., Decker H., Zhang Y., Keshavarzian A. Nitric oxide and its metabolites mediate ethanol-induced microtubule disruption and intestinal barrier dysfunction. The Journal of Pharmacology and Experimental Therapeutics 2000, 294:997-1008.
74. Banan A., Fields J.Z., Zhang Y., Keshavarzian A. iNOS upregulation mediates oxidant-induced disruption of F-actin and barrier of intestinal monolayers. American Journal of Physiology Gastrointestinal and Liver Physiology 2001, 280:G1234-G1246.
75. Takizawa Y., Kishimoto H., Kitazato T., Tomita M., Hayashi M. Effects of nitric oxide on mucosal barrier dysfunction during early phase of intestinal ischemia/reperfusion. European Journal of Pharmaceutical Sciences 2011, 42:246-252.
76. Amasheh S., Fromm M., Günzel D. Claudins of intestine and nephron - a correlation of molecular tight junction structure and barrier function. Acta Physiologica 2011, 201:133-140.
77. Tipsmark C.K., Baltzegar D.A., Ozden O., Grubb B.J., Borski R.J. Salinity regulates claudin mRNA and protein expression in the teleost gill. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2008, 294:R1004-R1014.
78. Clelland E.S., Bui P., Bagherie-Lachidan M., Kelly S.P. Spatial and salinity-induced alterations in claudin-3 isoform mRNA along the gastrointestinal tract of the pufferfish Tetraodon nigroviridis. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2010, 155:154-163.
79. Loretz C.A., Chris M.W., Shuttleworth T.J. Electrophysiology of ion transport in teleost intestinal cells. Fish physiology 1995, Academic Press, p. 25-56.
80. Sundell K., Jutfelt F., ãgustsson T., Olsen R.-E., Sandblom E., Hansen T., et al. Intestinal transport mechanisms and plasma cortisol levels during normal and out-of-season parr-smolt transformation of Atlantic salmon, Salmo salar. Aquaculture 2003, 222:265-285.
81. Tipsmark C.K., Madsen S.S. Tricellulin, occludin and claudin-3 expression in salmon intestine and kidney during salinity adaptation. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2012, 162:378-385.