Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization

Bibliographic Details
Format: Restricted Document
_version_ 1860797393942872064
building INTELEK Repository
collection Online Access
collectionurl https://intelek.unisza.edu.my/intelek/pages/search.php?search=!collection407072
date 2015-11-25 14:33:16
format Restricted Document
id 12539
institution UniSZA
internalnotes [1] Costello MJ. The global economic cost of sea lice to the salmonid farmingindustry. J Fish Dis 2009;32:115e8. [2] Torrissen O, Jones S, Asche F, Guttormsen A, Skilbrei OT, Nilsen F, et al. Salmonlice - impact on wild salmonids and salmon aquaculture. J Fish Dis 2013;36:171e94. [3] Costello MJ. How sea lice from salmon farms may cause wild salmonid de-clines in Europe and North America and be a threat to fishes elsewhere. Proc RSoc B-Biol Sci 2009;276:3385e94. [4] Krkosek M, Ford JS, Morton A, Lele S, Myers RA, Lewis MA. Declining wildsalmon populations in relation to parasites from farm salmon. Science2007;318:1772e5. [5] Heuch PA, Parsons A, Boxaspen K. Diel vertical migration ea possible host-finding mechanism in salmon louse (Lepeophtheirus salmonis) Copepodids.Can J Fish Aquat Sci 1995;52:681e9. [6] Heuch PA, Karlsen HE. Detection of infrasonic water oscillations by copepo-dids of Lepeophtheirus salmonis (Copepoda: Caligida). J Plankton Res 1997;19:735e47. [7] Bron JE, Sommerville C, Rae GH. Aspects of the behaviour of copepodid larvaeof the salmon louse Lepeophtheirus salmonis (Krøyer, 1837). In: Boxshall GA,Defaye D, editors. Pathogens of wild and farmed fish: sea lice. 1st ed. NewYork: Ellis Horwood; 1993. p. 125e42. [8] Bailey RJE, Birkett MA, Ingvarsdottir A, Mordue AJ, Mordue W, O'Shea B, et al.The role of semiochemicals in host location and non-host avoidance bysalmon louse (Lepeophtheirus salmonis) copepodids. Can J Fish Aquat Sci2006;63:448e56. [9] Mordue (Luntz) AJ, Birkett MA. A review of host finding behaviour in theparasitic sea louse, Lepeophtheirus salmonis (Caligidae: Copepoda). J Fish Dis2009;32:3e13. [10] Regnier FE. Semiochemicals estructure and function. Biol Reprod 1971;4:309e26. [11] Burks RL, Lodge DM. Cued in: advances and opportunities in freshwaterchemical ecology. J Chem Ecol 2002;28:1901e17. [12] Devine GJ, Ingvarsdottir A, Mordue W, Pike AW, Pickett J, Duce I, et al. Salmonlice, Lepeophtheirus salmonis, exhibit specific chemotactic responses to semi-ochemicals originating from the salmonid, Salmo salar. J Chem Ecol 2000;26:1833e47. [13] Ingvarsdottir A, Birkett MA, Duce I, Genna RL, Mordue W, Pickett JA, et al.Semiochemical strategies for sea louse control: host location cues. Pest ManagSci 2002;58:537e45. [14] Yamaguti S. Part 2: Caligoida, I. In: Yamaguti S, editor. Parasitic copepods fromfishes of Japan. Kyoto: published by the author; 1936. p. 22. [15] Dojiri M, Ho JS. Systematics of the caligidae, copepods parasitic on marinefishes. Brill; 2013. [16] Nagasawa K, Uyeno D, Tang D. A checklist of copepods of the genus Caligus(Siphonostomatoida, Caligidae) from fishes in Japanese waters (1927e2010).Bull Biogeogr Soc Jpn 2010;65:103e22. [17] Ohtsuka S, Takami I, Maran BAV, Ogawa K, Shimono T, Fujita Y, et al. Devel-opmental stages and growth of Pseudocaligus fugu Yamaguti, 1936 (Copepoda:Siphonostomatoida: Caligidae) host-specific to puffer. J Nat Hist 2009;43:1779e804. [18] Aparicio S, Chapman J, Stupka E, Putnam N, Chia J, Dehal P, et al. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Sci-ence 2002;297:1301e10. [19] Kai W, Kikuchi K, Tohari S, Chew AK, Tay A, Fujiwara A, et al. Integration of thegenetic map and genome assembly of fugu facilitates insights into distinctfeatures of genome evolution in teleosts and mammals. Genome Biol Evol2011;3:424e42. [20] Takashima F, Hibiya T. An atlas of fish histology: normal and pathologicalfeatures. 2nd ed. Tokyo: Kodansha; 1995. [21] Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, et al.Suppression subtractive hybridization: a method for generating differentiallyregulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci U S A1996;93:6025e30. [22] Gurskaya NG, Diatchenko L, Chenchik A, Siebert PD, Khaspekov GL,Lukyanov KA, et al. Equalizing cDNA subtraction based on selective sup-pression of polymerase chain reaction: cloning of Jurkat cell transcriptsinduced by phytohemaglutinin and phorbol 12-myristate 13-acetate. AnalBiochem 1996;240:90e7. [23] Zhi-Liang H, Bao J, Reecy JM. CateGOrizer: a web-based program to batchanalyze gene ontology classification categories. Online J Bioinforma 2008;9:108e12. [24] Chaisson KE, Hallem EA. Chemosensory behaviors of parasites. Trends Para-sitol 2012;28:427e36. [25] Buchmann K, Lindenstrøm T. Interactions between monogenean parasites andtheir fish hosts. Int J Parasitol 2002;32:309e19. [26] Yoshinaga T, Nagakura T, Ogawa K, Wakabayashi H. Attachment-inducingcapacities of fish tissue extracts on oncomiracidia of Neobenedenia girellae(Monogenea, Capsalidae). J Parasitol 2000;86:214e9. [27] Ohashi H, Umeda N, Hirazawa N, Ozaki Y, Miura C, Miura T. Purification andidentification of a glycoprotein that induces the attachment of oncomiracidiaof Neobenedenia girellae (Monogenea, Capsalidae). Int J Parasitol 2007;37:1483e90. [28] Kato K, Takegawa Y, Ralston KS, Gilchrist CA, Hamano S, Petri Jr WA, et al.Sialic acid-dependent attachment of mucins from three mouse strains toEntamoeba histolytica. Biochem Biophys Res Commun 2013;436:252e8. [29] Tasumi S, Vasta GR. A galectin of unique domain organization from hemocytesof the eastern oyster (Crassostrea virginica) is a receptor for the protistanparasite Perkinsus marinus. J Immunol 2007;179:3086e98. [30] Vasta GR. Roles of galectins in infection. Nat Rev Microbiol 2009;7:424e38. [31] Vasta GR. Galectins as pattern recognition receptors: structure, function, andevolution. Adv Exp Med Biol 2012;946:21e36. [32] Diatchenko L, Lukyanov S, Lau YFC, Siebert PD. Suppression subtractive hy-bridization: a versatile method for identifying differentially expressed genes.Methods Enzymol 1999;303:349e80. [33] Murphy G, Nagase H. Progress in matrix metalloproteinase research. Mol AspMed 2008;29:290e308. [34] Kawasaki K, Suzuki T. Molecular evolution of matrix metalloproteinase 20. EurJ Oral Sci 2011;119:247e53. [35] Tadiso TM, Krasnov A, Skugor S, Afanasyev S, Hordvik I, Nilsen F. Geneexpression analyses of immune responses in Atlantic salmon during earlystages of infection by salmon louse (Lepeophtheirus salmonis) revealed bi-phasic responses coinciding with the copepod-chalimus transition. BMC Ge-nomics 2011;12:141. http://dx.doi.org/10.1186/1471-2164-12-141. [36] Krasnov A, Skugor S, Todorcevic M, Glover KA, Nilsen F. Gene expression inAtlantic salmon skin in response to infection with the parasitic copepodLepeophtheirus salmonis, cortisol implant, and their combination. BMC Geno-mics 2012;13:130. http://dx.doi.org/10.1186/1471-2164-13-130. [37] Adolph KW. The zebrafish thrombospondin 3 and 4 genes (thbs3 and thbs4):cDNA and protein structure. DNA Seq 2002;13:277e85. [38] Hynes RO, Yamada KM. Fibronectins emultifunctional modular glycopro-teins. J Cell Biol 1982;95:369e77. [39] Boxshall GA, Halsey SH. An introduction to copepod diversity. 1st ed. London:Ray Society; 2004. [40] Karplus I. Symbiosis in fishes: the biology of interspecific partnerships. 1st ed.Chichester: Wiley; 2014. [41] Ismail N, Ohtsuka S, Maran BAV, Tasumi S, Zaleha K, Yamashita H. Completelife cycle of a pennellid Peniculus minuticaudae Shiino, 1956 (Copepoda:Siphonostomatoida) infecting cultured threadsail filefish, Stephanolepis cir-rhifer. Parasite 2013;20:42. [42] Cui J, Liu S, Zhang B, Wang H, Sun H, Song S, et al. Transciptome analysis of thegill and swimbladder of Takifugu rubripes by RNA-Seq. Plos One 2014;9.e85505.S. Tasumi et al. / Fish & Shellfish Immunology 44 (2015) 356e364364
originalfilename 6846-01-FH02-FBIM-15-04186.jpg
person norman
recordtype oai_dc
resourceurl https://intelek.unisza.edu.my/intelek/pages/view.php?ref=12539
spelling 12539 https://intelek.unisza.edu.my/intelek/pages/view.php?ref=12539 https://intelek.unisza.edu.my/intelek/pages/search.php?search=!collection407072 Restricted Document Article Journal image/jpeg inches 96 96 norman 1417 61 61 723 2015-11-25 14:33:16 1417x723 6846-01-FH02-FBIM-15-04186.jpg UniSZA Private Access Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization Fish and Shellfish Immunology Caligus fugu is a parasitic copepod specific to the tetraodontid genus Takifugu including the commercially important Takifugu rubripes. Despite the rapid accumulation of knowledge on other aspects of its biology, the host and settlement-site recognition mechanisms of this parasite are not yet well understood. Since the infective copepodid stage shows preferential site selection in attaching to the fins, we considered it likely that the copepodid recognizes chemical cues released or leaking from the fins, and/or transmembrane protein present on the fins. To isolate molecules potentially related to attachment site specificity, we applied suppression subtractive hybridization (SSH) PCR by identifying genes expressed more highly in pectoral fins of T. rubripes than in the body surface skin. We sequenced plasmid DNA from 392 clones in a SSH library. The number of non-redundant sequences was 276, which included 135 sequences located on 117 annotated genes and 141 located in positions where no genes had been annotated. We characterized those annotated genes on the basis of gene ontology terms, and found that 46 of the identified genes encode secreted proteins, enzymes or membrane proteins. Among them nine showed higher expression in the pectoral fins than in the skin. These could be candidate genes for involvement in behavioral mechanisms related to the site specificity shown by the infective copepodids of C. fugu. 44 1 Academic Press Academic Press 356-364 [1] Costello MJ. The global economic cost of sea lice to the salmonid farmingindustry. J Fish Dis 2009;32:115e8. [2] Torrissen O, Jones S, Asche F, Guttormsen A, Skilbrei OT, Nilsen F, et al. Salmonlice - impact on wild salmonids and salmon aquaculture. J Fish Dis 2013;36:171e94. [3] Costello MJ. How sea lice from salmon farms may cause wild salmonid de-clines in Europe and North America and be a threat to fishes elsewhere. Proc RSoc B-Biol Sci 2009;276:3385e94. [4] Krkosek M, Ford JS, Morton A, Lele S, Myers RA, Lewis MA. Declining wildsalmon populations in relation to parasites from farm salmon. Science2007;318:1772e5. [5] Heuch PA, Parsons A, Boxaspen K. Diel vertical migration ea possible host-finding mechanism in salmon louse (Lepeophtheirus salmonis) Copepodids.Can J Fish Aquat Sci 1995;52:681e9. [6] Heuch PA, Karlsen HE. Detection of infrasonic water oscillations by copepo-dids of Lepeophtheirus salmonis (Copepoda: Caligida). J Plankton Res 1997;19:735e47. [7] Bron JE, Sommerville C, Rae GH. Aspects of the behaviour of copepodid larvaeof the salmon louse Lepeophtheirus salmonis (Krøyer, 1837). In: Boxshall GA,Defaye D, editors. Pathogens of wild and farmed fish: sea lice. 1st ed. NewYork: Ellis Horwood; 1993. p. 125e42. [8] Bailey RJE, Birkett MA, Ingvarsdottir A, Mordue AJ, Mordue W, O'Shea B, et al.The role of semiochemicals in host location and non-host avoidance bysalmon louse (Lepeophtheirus salmonis) copepodids. Can J Fish Aquat Sci2006;63:448e56. [9] Mordue (Luntz) AJ, Birkett MA. A review of host finding behaviour in theparasitic sea louse, Lepeophtheirus salmonis (Caligidae: Copepoda). J Fish Dis2009;32:3e13. [10] Regnier FE. Semiochemicals estructure and function. Biol Reprod 1971;4:309e26. [11] Burks RL, Lodge DM. Cued in: advances and opportunities in freshwaterchemical ecology. J Chem Ecol 2002;28:1901e17. [12] Devine GJ, Ingvarsdottir A, Mordue W, Pike AW, Pickett J, Duce I, et al. Salmonlice, Lepeophtheirus salmonis, exhibit specific chemotactic responses to semi-ochemicals originating from the salmonid, Salmo salar. J Chem Ecol 2000;26:1833e47. [13] Ingvarsdottir A, Birkett MA, Duce I, Genna RL, Mordue W, Pickett JA, et al.Semiochemical strategies for sea louse control: host location cues. Pest ManagSci 2002;58:537e45. [14] Yamaguti S. Part 2: Caligoida, I. In: Yamaguti S, editor. Parasitic copepods fromfishes of Japan. Kyoto: published by the author; 1936. p. 22. [15] Dojiri M, Ho JS. Systematics of the caligidae, copepods parasitic on marinefishes. Brill; 2013. [16] Nagasawa K, Uyeno D, Tang D. A checklist of copepods of the genus Caligus(Siphonostomatoida, Caligidae) from fishes in Japanese waters (1927e2010).Bull Biogeogr Soc Jpn 2010;65:103e22. [17] Ohtsuka S, Takami I, Maran BAV, Ogawa K, Shimono T, Fujita Y, et al. Devel-opmental stages and growth of Pseudocaligus fugu Yamaguti, 1936 (Copepoda:Siphonostomatoida: Caligidae) host-specific to puffer. J Nat Hist 2009;43:1779e804. [18] Aparicio S, Chapman J, Stupka E, Putnam N, Chia J, Dehal P, et al. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Sci-ence 2002;297:1301e10. [19] Kai W, Kikuchi K, Tohari S, Chew AK, Tay A, Fujiwara A, et al. Integration of thegenetic map and genome assembly of fugu facilitates insights into distinctfeatures of genome evolution in teleosts and mammals. Genome Biol Evol2011;3:424e42. [20] Takashima F, Hibiya T. An atlas of fish histology: normal and pathologicalfeatures. 2nd ed. Tokyo: Kodansha; 1995. [21] Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, et al.Suppression subtractive hybridization: a method for generating differentiallyregulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci U S A1996;93:6025e30. [22] Gurskaya NG, Diatchenko L, Chenchik A, Siebert PD, Khaspekov GL,Lukyanov KA, et al. Equalizing cDNA subtraction based on selective sup-pression of polymerase chain reaction: cloning of Jurkat cell transcriptsinduced by phytohemaglutinin and phorbol 12-myristate 13-acetate. AnalBiochem 1996;240:90e7. [23] Zhi-Liang H, Bao J, Reecy JM. CateGOrizer: a web-based program to batchanalyze gene ontology classification categories. Online J Bioinforma 2008;9:108e12. [24] Chaisson KE, Hallem EA. Chemosensory behaviors of parasites. Trends Para-sitol 2012;28:427e36. [25] Buchmann K, Lindenstrøm T. Interactions between monogenean parasites andtheir fish hosts. Int J Parasitol 2002;32:309e19. [26] Yoshinaga T, Nagakura T, Ogawa K, Wakabayashi H. Attachment-inducingcapacities of fish tissue extracts on oncomiracidia of Neobenedenia girellae(Monogenea, Capsalidae). J Parasitol 2000;86:214e9. [27] Ohashi H, Umeda N, Hirazawa N, Ozaki Y, Miura C, Miura T. Purification andidentification of a glycoprotein that induces the attachment of oncomiracidiaof Neobenedenia girellae (Monogenea, Capsalidae). Int J Parasitol 2007;37:1483e90. [28] Kato K, Takegawa Y, Ralston KS, Gilchrist CA, Hamano S, Petri Jr WA, et al.Sialic acid-dependent attachment of mucins from three mouse strains toEntamoeba histolytica. Biochem Biophys Res Commun 2013;436:252e8. [29] Tasumi S, Vasta GR. A galectin of unique domain organization from hemocytesof the eastern oyster (Crassostrea virginica) is a receptor for the protistanparasite Perkinsus marinus. J Immunol 2007;179:3086e98. [30] Vasta GR. Roles of galectins in infection. Nat Rev Microbiol 2009;7:424e38. [31] Vasta GR. Galectins as pattern recognition receptors: structure, function, andevolution. Adv Exp Med Biol 2012;946:21e36. [32] Diatchenko L, Lukyanov S, Lau YFC, Siebert PD. Suppression subtractive hy-bridization: a versatile method for identifying differentially expressed genes.Methods Enzymol 1999;303:349e80. [33] Murphy G, Nagase H. Progress in matrix metalloproteinase research. Mol AspMed 2008;29:290e308. [34] Kawasaki K, Suzuki T. Molecular evolution of matrix metalloproteinase 20. EurJ Oral Sci 2011;119:247e53. [35] Tadiso TM, Krasnov A, Skugor S, Afanasyev S, Hordvik I, Nilsen F. Geneexpression analyses of immune responses in Atlantic salmon during earlystages of infection by salmon louse (Lepeophtheirus salmonis) revealed bi-phasic responses coinciding with the copepod-chalimus transition. BMC Ge-nomics 2011;12:141. http://dx.doi.org/10.1186/1471-2164-12-141. [36] Krasnov A, Skugor S, Todorcevic M, Glover KA, Nilsen F. Gene expression inAtlantic salmon skin in response to infection with the parasitic copepodLepeophtheirus salmonis, cortisol implant, and their combination. BMC Geno-mics 2012;13:130. http://dx.doi.org/10.1186/1471-2164-13-130. [37] Adolph KW. The zebrafish thrombospondin 3 and 4 genes (thbs3 and thbs4):cDNA and protein structure. DNA Seq 2002;13:277e85. [38] Hynes RO, Yamada KM. Fibronectins emultifunctional modular glycopro-teins. J Cell Biol 1982;95:369e77. [39] Boxshall GA, Halsey SH. An introduction to copepod diversity. 1st ed. London:Ray Society; 2004. [40] Karplus I. Symbiosis in fishes: the biology of interspecific partnerships. 1st ed.Chichester: Wiley; 2014. [41] Ismail N, Ohtsuka S, Maran BAV, Tasumi S, Zaleha K, Yamashita H. Completelife cycle of a pennellid Peniculus minuticaudae Shiino, 1956 (Copepoda:Siphonostomatoida) infecting cultured threadsail filefish, Stephanolepis cir-rhifer. Parasite 2013;20:42. [42] Cui J, Liu S, Zhang B, Wang H, Sun H, Song S, et al. Transciptome analysis of thegill and swimbladder of Takifugu rubripes by RNA-Seq. Plos One 2014;9.e85505.S. Tasumi et al. / Fish & Shellfish Immunology 44 (2015) 356e364364
spellingShingle Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization
summary Caligus fugu is a parasitic copepod specific to the tetraodontid genus Takifugu including the commercially important Takifugu rubripes. Despite the rapid accumulation of knowledge on other aspects of its biology, the host and settlement-site recognition mechanisms of this parasite are not yet well understood. Since the infective copepodid stage shows preferential site selection in attaching to the fins, we considered it likely that the copepodid recognizes chemical cues released or leaking from the fins, and/or transmembrane protein present on the fins. To isolate molecules potentially related to attachment site specificity, we applied suppression subtractive hybridization (SSH) PCR by identifying genes expressed more highly in pectoral fins of T. rubripes than in the body surface skin. We sequenced plasmid DNA from 392 clones in a SSH library. The number of non-redundant sequences was 276, which included 135 sequences located on 117 annotated genes and 141 located in positions where no genes had been annotated. We characterized those annotated genes on the basis of gene ontology terms, and found that 46 of the identified genes encode secreted proteins, enzymes or membrane proteins. Among them nine showed higher expression in the pectoral fins than in the skin. These could be candidate genes for involvement in behavioral mechanisms related to the site specificity shown by the infective copepodids of C. fugu.
title Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization
title_full Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization
title_fullStr Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization
title_full_unstemmed Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization
title_short Screening of candidate genes encoding proteins expressed in pectoral fins of fugu Takifugu rubripes, in relation to habitat site of parasitic copepod Caligus fugu, using suppression subtractive hybridization
title_sort screening of candidate genes encoding proteins expressed in pectoral fins of fugu takifugu rubripes, in relation to habitat site of parasitic copepod caligus fugu, using suppression subtractive hybridization