Abstract
Toll-like receptors (TLRs) are responsible for the recognition of specific pathogen-associated molecular patterns and consequently activate signal pathways leading to inflammatory and interferon responses. The region surrounding several TLRs was previously found to be associated with resistance to specific disease. Hence, we determined the location of 11 TLRs in Japanese flounder (Paralichthys olivaceus) using polymorphic microsatellite markers. TLR1 and TLR3 were located on linkage group (LG) 21 and 7, respectively. Membrane TLR5 and soluble TLR5 were mapped to LG22. TLR7 and TLR8 were mapped to LG3. TLR9 was found on LG1 and TLR14 and TLR21 were located on the same linkage group, LG10. TLR22 was found on LG8. Interestingly, TLR2 was mapped with the previously reported Poli9-8TUF microsatellite marker which is tightly associated with lymphocystis virus disease resistance. Therefore, TLR2 is a candidate gene for resistance to lymphocystis disease. These results imply that the location of a TLR associated with a particular disease may be valuable for the research on the relationship between host immune response and disease resistance.
Similar content being viewed by others
References
Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511
Aravalli RN, Hu SX, Rowen TN, Palmquist JM, Lokensgard JR (2005) Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J Immunol 175:4189–4193
Bell JK, Mullen GED, Leifer CA, Mazzoni A, Davies DR, Segal DM (2003) Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol 24:528–533
Castaño-Sánchez C, Fuji K, Ozaki A, Hasegawa O, Sakamoto T, Morishima K, Nakayama I, Fujiwara A, Okamoto H, Hayashida K, Tagami M, Kawai J, Hayashizaki Y, Okamoto N (2010) A second generation genetic linkage map of Japanese flounder (Paralichthys olivaceus). BMC Genomics 11:554
Chistiakov DA, Hellemans B, Haley CS, Law AS, Tsigenopoulos CS, Kotoulas G, Bertotto D, Libertini A, Volckaert FA (2005) A microsatellite linkage map of the European sea bass Dicentrarchus labrax L. Genetics 170:1821–1826
Coimbra MRM, Kobayashi K, Koretsugu S, Hasegawa O, Ohara E, Ozaki A, Sakamoto T, Naruse K, Okamoto N (2003) A genetic linkage map of Japanese flounder, Paralichthys olivaceus. Aquaculture 220:203–218
Du X, Poltorak A, Wei Y, Beutler B (2000) Three novel mammalian toll-like receptors: gene structure, expression, and evolution. Eur Cytokine Netw 11:362–371
Fuji K, Kobayashi K, Hasegawa O, Coimbra MRM, Sakamoto T, Okamoto N (2006) Identification of a single major genetic locus controlling the resistance to lymphocystis disease in Japanese flounder (Paralichthys olivaceus). Aquaculture 254:203–210
Fuji K, Hasegawa O, Honda K, Kumasaka K, Sakamoto T, Okamoto N (2007) Marker-assisted breeding of a lymphocystis disease-resistant Japanese flounder (Paralichthys olivaceus). Aquaculture 272:291–295
Hirono I, Takami M, Miyata M, Miyazaki T, Han HJ, Takano T, Endo M, Aoki T (2004) Characterization of gene structure and expression of two toll-like receptors from Japanese flounder, Paralichthys olivaceus. Immunogenetics 56:38–46
Hu J, Bumstead N, Barrow P, Sebastiani G, Olien L, Morgan K, Malo D (1997) Resistance to salmonellosis in the chicken is linked to NRAMP1 and TNC. Genome Res 7:693–704
Hwang SD, Asahi T, Kondo H, Hirono I, Aoki T (2010a) Molecular cloning and expression study on Toll-like receptor 5 paralogs in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 29:630–638
Hwang SD, Kondo H, Hirono I, Aoki T (2010b) Molecular cloning and characterization of Toll-like receptor 14 in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 30:425–429
Jaari S, Li MH, Merilä J (2009) A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus): insight into avian genome evolution. BMC Genomics 10:1
Jault C, Pichon L, Chluba J (2004) Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol Immunol 40:759–771
Johnson NA, Vallejo RL, Silverstein JT, Welch TJ, Wiens GD, Hallerman EM, Palti Y (2008) Suggestive association of major histocompatibility IB genetic markers with resistance to bacterial cold water disease in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 10:429–437
Katagiri T, Asakawa S, Hirono I, Aoki T, Shimizu N (2000) Genomic bacterial artificial chromosome library of the Japanese flounder, Paralichthys olivaceus. Mar Biotechnol 2:571–576
Kocher TD, Lee WJ, Sobolewska H, Penman D, McAndrew B (1998) A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148:1225–1232
Koshimizu E, Strüssmann CA, Okamoto N, Fukuda H, Sakamoto T (2010) Construction of a genetic map and development of DNA markers linked to the sex-determining locus in the Patagonian pejerrey (Odontesthes hatcheri). Mar Biotechnol 12:8–13
Lallias D, Gomez-Raya L, Haley CS, Arzul I, Heurtebise S, Beaumont AR, Boudry P, Lapègue S (2009) Combining two-stage testing and interval mapping strategies to detect QTL for resistance to bonamiosis in the European flat oyster Ostrea edulis. Mar Biotechnol 11:570–584
Lee BY, Lee WJ, Streelman JT, Carleton KL, Howe AE, Hulata G, Slettan A, Stern JE, Terai Y, Kocher TD (2005) A second-generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170:237–244
Leveque G, Forgetta V, Morroll S, Smith AL, Bumstead N, Barrow P, Loredo-Osti JC, Morgan K, Malo D (2003) Allelic variation in TLR4 is linked susceptibility to Salmonella enteric serovar Typhimurium infection in chickens. Infect Immun 71:1116–1124
Li L, Guo X (2004) AFLP-based genetic linkage maps of the pacific oyster Crassostrea gigas Thunberg. Mar Biotechnol 6:26–36
Liao X, Ma HY, Xu GB, Shao CW, Tian YS, Ji XS, Yang JF, Chen SL (2009) Construction of a genetic linkage map and mapping of a female-specific DNA marker in half-smooth tongue sole (Cynoglossus semilaevis). Mar Biotechnol 11:699–709
Liu Z, Karsi A, Li P, Cao D, Dunham R (2003) An AFLP-based genetic linkage map of channel catfish (Ictalurus punctatus) constructed by using an interspecific hybrid resource family. Genetics 165:687–694
Liu X, Liu X, Guo X, Gao Q, Zhao H, Zhang G (2006) A preliminary genetic linkage map of the Pacific abalone Haliotis discus hannai Ino. Mar Biotechnol 8:386–397
Liu F, Shao Z, Zhang H, Liu J, Wang X, Duan D (2010) QTL mapping for frond length and width in Laminaria japonica aresch (Laminarales, Phaeophyta) using AFLP and SSR markers. Mar Biotechnol 12:386–394
Manly KF, Olson JM (1999) Overview of QTL mapping software and introduction to Map Manager Qt. Mamm Genome 10:327–334
McConnell SK, Beynon C, Leamon J, Skibinski DO (2000) Microsatellite marker based genetic linkage maps of Oreochromis aureus and O. niloticus (Cichlidae): extensive linkage group segment homologies revealed. Anim Genet 31:214–218
Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1:135–145
Meehan D, Xu Z, Zuniga G, Alcivar-Warren A (2003) High frequency and large number of polymorphic microsatellites in cultured shrimp, Penaeus (Litopenaeus) vannamei [Crustacea:Decapoda]. Mar Biotechnol 5:311–330
Morrison LA (2004) The Toll of herpes simplex virus infection. Trends Microbiol 12:353–356
Oshiumi H, Tsujita T, Shida K, Matsumoto M, Ikeo K, Seya T (2003) Prediction of the prototype of the human Toll-like receptor gene family from the pufferfish, Fugu rubripes, genome. Immunogenetics 54:791–800
Palti Y, Rodriguez MF, Vallejo RL, Rexroad CE III (2006) Mapping of Toll-like receptor genes in rainbow trout. Anim Genet 37:597–598
Palti Y, Gahr SA, Purcell MK, Hadidi S, Rexroad CE III, Wiens GD (2010a) Identification, characterization and genetic mapping of TLR7, TLR8a1 and TLR8a2 genes in rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 34:219–233
Palti Y, Rodriguez MF, Gahr SA, Purcell MK, Rexroad CE III, Wiens GD (2010b) Identification, characterization and genetic mapping of TLR1 loci in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 28:918–926
Rebl A, Siegl E, Köllner B, Fischer U, Seyfert HM (2007) Characterization of twin toll-like receptors from rainbow trout (Oncorhynchus mykiss): evolutionary relationship and induced expression by Aeromonas salmonicida salmonicida. Dev Comp Immunol 31:499–510
Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A 102:9577–9582
Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345
Sebastiani G, Olien L, Gauthier S, Skamene E, Morgan K, Gros P, Malo D (1998) Mapping of genetic modulators of natural resistance to infection with Salmonella typhimurium in wild-derived mice. Genomics 47:180–186
Sebastiani G, Leveque G, Larivierè L, Laroche L, Skamene E, Gros P, Malo D (2000) Cloning and characterization of the murine Toll-like receptor 5 (Tlr5) gene: sequence and mRNA expression studies in Salmonella-susceptible MOLF/Ei mice. Genomics 64:230–240
Sekino M, Kobayashi T, Hara M (2006) Segregation and linkage analysis of 75 novel microsatellite DNA markers in pair crosses of Japanese abalone (Haliotis discus hannai) using the 5′-tailed primer method. Mar Biotechnol 8:453–466
Sørensen LN, Reinert LS, Malmgaard L, Bartholdy C, Thomsen AR, Paludan SR (2008) TLR2 and TLR9 synergistically control herpes simplex virus infection in the brain. J Immunol 181:8604–8612
Takano T, Kondo H, Hirono I, Endo M, Saito-Taki T, Aoki T (2007) Molecular cloning and characterization of Toll-like receptor 9 in Japanese flounder, Paralichthys olivaceus. Mol Immunol 44:1845–1853
Takano T, Hwang SD, Kondo H, Hirono I, Aoki T, Sano M (2010) Evidence of molecular Toll-like receptor mechanisms in teleosts. Fish Pathol 45:1–16
Takeda K, Kasho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376
Tsoi S, Park KC, Kay HH, O’Brien TJ, Podor E, Sun G, Douglas SE, Brown LL, Johnson SC (2006) Identification of a transcript encoding a soluble form of toll-like receptor 5 (TLR5) in Atlantic salmon during Aeromonas salmonicida infection. Vet Immunol Immunopathol 109:183–187
Tsujita T, Tsukada H, Nakao M, Oshiumi H, Matsumoto M, Seya T (2004) Sensing bacterial flagellin by membrane and soluble orthologs of Toll-like receptor 5 in rainbow trout (Oncorhynchus mykiss). J Biol Chem 279:48588–48597
Voorrips RE (2002) Mapchart: software for the graphical presentation of linkage maps and QTLs. J Heredity 93:77–78
Waldbieser GC, Bosworth BG, Nonneman DJ, Wolters WR (2001) A microsatellite-based genetic linkage map for channel catfish, Ictalurus punctatus. Genetics 158:727–734
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hwang, S.D., Fuji, K., Takano, T. et al. Linkage Mapping of Toll-Like Receptors (TLRs) in Japanese Flounder, Paralichthys olivaceus . Mar Biotechnol 13, 1086–1091 (2011). https://doi.org/10.1007/s10126-011-9371-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-011-9371-x