The fish gill, as one of the mucosal barriers, plays an important role in mucosal immune response. The fish swimbladder functions for regulating buoyancy. The fish swimbladder has long been postulated as a homologous organ of the tetrapod lung, but the molecular evidence is scarce. In order to provide new information that is complementary to gill immune genes, initiate new research directions concerning the genetic basis of the gill immune response and understand the molecular function of swimbladder as well as its relationship with lungs, transcriptome analysis of the fugu Takifugu rubripes gill and swimbladder was carried out by RNA-Seq. Approximately 55,061,524 and 44,736,850 raw sequence reads from gill and swimbladder were generated, respectively. Gene ontology (GO) and KEGG pathway analysis revealed diverse biological functions and processes. Transcriptome comparison between gill and swimbladder resulted in 3,790 differentially expressed genes, of which 1,520 were up-regulated in the swimbladder while 2,270 were down-regulated. In addition, 406 up regulated isoforms and 296 down regulated isoforms were observed in swimbladder in comparison to gill. By the gene enrichment analysis, the three immune-related pathways and 32 immune-related genes in gill were identified. In swimbladder, five pathways including 43 swimbladder-enriched genes were identified. This work should set the foundation for studying immune-related genes for the mucosal immunity and provide genomic resources to study the relatedness of the fish swimbladder and mammalian lung.
References
[1]
Cerutti A, Chen K, Chorny A (2011) Immunoglobulin responses at the mucosal interface. Annu Rev Immunol 29: 273–293.
[2]
Dickerson H, Clark T (1998) Ichthyophthirius multifiliis: a model of cutaneous infection and immunity in fishes. Immunol Rev 22: 465–474.
[3]
Lu C, Ling F, Ji J, Kang YJ, Wang GX (2013) Expression of immune-related genes in goldfish gills induced by Dactylogyrus intermedius infections. Fish Shellfish Immunol 34: 372–377.
[4]
Su JG, Zhu ZY, Wang YP (2008) Up-regulating expressions of toll-like receptor 3 and Mx genes in gills by grass CARP reovirus in rare minnow, Gobiocypris rayus. Acta Hydrobiologica Sinica 32: 728–734.
[5]
Yang M, Wang K, Chen H, Li S (2006) Cloning and sequence analysis of hepcidin-like antimicrobial peptide gene from gill of Japanese seabass(Lateolabrax japonicus). Journal of Oceanography in Taiwan Strait 25: 330–335.
[6]
Yang C, Su J, Peng L, Dong J (2011) Cloning and characterization of grass carp (Ctenopharyngodon idella)Toll-like receptor 9. Journal of Fisheries of China 35: 641–649.
[7]
Beck BH, Farmer BD, Straus DL, Li C, Peatman E (2012) Putative roles for a rhamnose binding lectin in Flavobacterium columnare pathogenesis in channel catfish Ictalurus punctatus. Fish Shellfish Immunol 33: 1008–1015.
[8]
Sun F, Peatman E, Li C, Liu S, Jiang Y, et al. (2012) Transcriptomic signatures of attachment, NF-κB suppression and IFN stimulation in the catfish gills following columnaris bacterial infection. Dev Comp Immunol 38: 169–180.
[9]
Perry SF, Sander M (2004) Reconstructing the evolution of the respiratory apparatus in tetrapods. Respir Physiol Neurobiol 144: 125–139.
[10]
Winata CL, Korzh S, Kondrychyn I, Zheng W, Korzh V, et al. (2009) Development of zebrafish swimbladder: The requirement of Hedgehog signaling in specification and organization of the three tissue layers. Dev Biol 331: 222–236.
[11]
Yin A, Korzh V, Gong Z (2012) Perturbation of zebrafish swimbladder development by enhancing Wnt signaling in Wifl morphants. Biochim Biophys Acta 1823: 236–244.
[12]
Winata CL, Korzh S, Kondrychyn I, Korzh V, Gong Z (2010) The role of vasculature and blood circulation in zebrafish swimbladder development. BMC Dev Biol 10: 3.
[13]
Zheng W, Wang Z, Collins JE, Andrews RM, Stemple D, et al. (2011) Comparative transcriptome analyses indicate molecular homology of zebrafish swimbladder and mammalian lung. PLoS One 6(8): e24019.
[14]
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool fortranscriptomics. Nat Rev Genet 10: 57–63.
[15]
Anisimov SV (2008) Serial Analysis of Gene Expression (SAGE): 13 years of application in research. Curr Pharm Biotechnol 9: 338–350.
[16]
Liu S, Wang X, Sun F, Zhang J, Feng J, et al. (2013) RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding and degradation in response to heat stress in catfish. Physiol Genomics 45: 462–476.
[17]
Liu S, Zhang Y, Zhou Z, Waldbieser G, Sun F, et al. (2012) Efficient assembly and annotation of the transcriptome of catfish by RNA-Seq analysis of a doubled haploid homozygote. BMC Genomics 13: 595.
[18]
Liu S, Zhou Z, Lu J, Sun F, Wang S, et al. (2011) Generation of genome-scale gene-associated SNPs in catfish for the construction of a high-density SNP array. BMC Genomics 12: 53.
[19]
Owen R (1846) Lectures on Comparative Anatomy and Physiology of the Vertebrate Animals. London: Longman, Brown, Green, and Longmans.
[20]
Perry SF, Wilson RJ, Straus C, Harris MB, Remmers JE (2001) Which came first, the lung or the breath? Comp Biochem Physiol A Mol Integr Physiol 129: 37–47.
[21]
Oshiumi H, Tsujita T, Shida K, Matsumoto M, Ikeo K, et al. (2003) (2003) Prediction of the prototype of the human Toll-like receptor gene family from the pufferfish, Fugu rubripes, genome. Immunogenetics 54: 791–800.
[22]
Jault C, Pichon L, Chluba J (2004) Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol Immunol 40: 759–571.
[23]
Brocker C, Thompson D, Matsumoto A, Nebert DW, Vasiliou V (2010) Evolutionary divergence and functions of the human interleukin (IL) gene family. Human Genomics 5: 30–55.
[24]
Dong W, Shao J, Xing L (2006) Identification and characterization of an interleukin2 homologue in fugu, Fugu rubripes, based on comparative genomics. Journal of Zhejiang University (Science Edition) 33: 688–694.
[25]
Zou J, Clark MS, Secombes CJ (2003) Characterisation, expression and promoter analysis of an interleukin 10 homologue in the puffer fish, Fugu rubripes. Immunogenetics 55: 325–335.
[26]
Yoshiura Y, Kiryu I, Fujiwara A, Suetake H, Suzuki Y, et al. (2003) Identification and characterization of Fugu orthologues of mammalian interleukin-12 subunits. Immunogenetics 55: 296–306.
[27]
Bird S, Zou J, Kono T, Sakai M, Dijkstra JM, et al. (2005) Characterisation and expression analysis of interleukin 2 (IL-2) and IL-21 homologues in the Japanese pufferfish, Fugu rubripes, following their discovery by synteny. Immunogenetics 56: 909–923.
[28]
Bird S, Zou J, Savan R, Sakai M, Woo J, et al. (2005) Characterisation and expression analysis of an interleukin 6 homologue in the Japanese pufferfish, Fugu rubripes. Dev Comp Immunol 29: 775–789.
[29]
Kono T, Bird S, Sonoda K, Savan R, Secombes CJ, et al. (2008) Characterization and expression analysis of an interleukin-7 homologue in the Japanese pufferfish, Takifugu rubripes. FEBS J 275: 1213–1226.
[30]
Korenaga H, Kono T, Sakai M (2010) Isolation of seven IL-17 family genes from the Japanese pufferfish Takifugu rubripes. Fish Shellfish Immunol 28: 809–818.
[31]
Bei JX, Suetake H, Araki K, Kikuchi K, Yoshiura Y, et al. (2006) Two interleukin (IL)-15 homologues in fish from two distinct origins. Mol Immunol 43: 860–859.
[32]
Arena A, Merendino RA, Bonina L, Iannello D, Stassi G, et al. (2000) Role of IL-15 on monocytic resistance to human herpesvirus 6 infection. New Microbiol 23: 105–112.
[33]
Wang T, Holland JW, Carrington A, Zou J, Secombes CJ (2007) Molecular and functional characterization of IL-15 in rainbow trout Oncorhynchus mykiss: a potent inducer of IFN-gamma expression in spleen leukocytes. JImmunol 179: 1475–1488.
[34]
Gunimaladevi I, Savan R, Sato K, Yamaguchi R, Sakai M (2007) Characterization of an interleukin-15 like (IL-15L) gene from zebrafish (Danio rerio). Fish Shellfish Immunol 22: 351–362.
[35]
Fang W, Xiang LX, Shao JZ, Wen Y, Chen SY (2006) Identification and characterization of an interleukin-15 homologue from Tetraodon nigroviridis. Comp Biochem Physiol B Biochem Mol Biol 143: 335–343.
[36]
Mélik-Parsadaniantz S, Rostène W (2008) Chemokines and neuromodulation. Journal of Neuroimmunology 198: 62–68.
[37]
Vicari AP, Figueroa DJ, Hedrick JA, Foster JS, Singh KP, et al. (1997) TECK: a novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development. Immunity 7: 291–301.
[38]
Li J, Xiong T, Xiao R, Xiong A, Chen J, et al.. (2013) Anti-CCL25 Antibody Prolongs Skin Allograft Survival by Blocking CCR9 Expression and Impairing Splenic T-Cell Function. Arch Immunol Ther Exp (Warsz). doi 10.1007/s00005-013-0223-4.
[39]
Lee HS, Kim HR, Lee EH, Jang MH, Kim SB, et al. (2012) Characterization of CCR9 expression and thymus-expressed chemokine responsiveness of the murine thymus, spleen and mesenteric lymph node. Immunobiology 217: 402–411.
[40]
Long Q, Quint E, Lin S, Ekker M (2000) The zebrafish scyba gene encodes a novel CXC-type chemokine with distinctive expression patterns in the vestibulo-acoustic system during embryogenesis. Mech Dev. 97: 183–186.
[41]
Liu Y, Chang MX, Wu SG, Nie P (2009) Characterization of C-C chemokine receptor subfamily in teleost fish. Mol Immunol 46: 498–504.
[42]
DeVries ME, Kelvin AA, Xu L, Ran L, Robinson J, et al. (2006) Defining the origins and evolution of the chemokine/chemokine receptor system. J Immunol 176: 401–415.
[43]
Lu IN, Chiang BL, Lou KL, Huang PT, Yao CC, et al. (2012) Cloning, expression and characterization of CCL21 and CCL25 chemokines in zebrafish. Dev. Comp. Immunol 38: 203–214.
[44]
Chong SW, Nguyet LM, Jiang YJ, Korzh V (2007) The chemokine Sdf-1 and its receptor Cxcr4 are required for formation of muscle in zebrafish. BMC Dev Biol 7: 54.
[45]
Daniels GD, Zou J, Charlemagne J, Partula S, Cunningham C, et al. (1999) Cloning of two chemokine receptor homologs (CXC-R4 and CC-R7) in rainbow trout Oncorhynchus mykiss. J Leukoc Biol 65: 684–690.
[46]
Fujiki K, Shin DH, Nakao M, Yano T (1999) Molecular cloning of carp (Cyprinus carpio) CC chemokine, CXC chemokine receptors, allograft inflammatory factor-1, and natural killer cell enhancing factor by use of suppression subtractive hybridization. Immunogenetics 49: 909–914.
[47]
Alabyev BY, Najakshin AM, Mechetina LV, Taranin AV (2000) Cloning of a CXCR4 homolog in chondrostean fish and characterization of the CXCR4-specific structural features. Dev Comp Immunol 24: 765–770.
[48]
Goostrey A, Jones G, Secombes CJ (2005) Isolation and characterization of CXC receptor genes in a range of elasmobranches. Dev Comp Immunol 29: 229–242.
[49]
Chong SW, Emelyanov A, Gong Z, Korzh V (2001) Expression pattern of two zebrafish genes, cxcr4a and cxcr4b. Mech Dev 109: 347–354.
[50]
Wang F, Daugherty B, Keise LL, Wei Z, Foley JP, et al. (2003) Heterogeneity of claudin expression by alveolar epithelial cells. Am J Respir Cell Mol Biol 29: 62–70.
[51]
Van Itallie C, Rahner C, Anderson JM (2001) Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J Clin Invest 107: 1319–1327.
[52]
Coyne CB, Gambling TM, Boucher RC, Carson JL, Johnson LG (2003) Role of claudin interactions in airway tight junctional permeability. Am J Physiol Lung Cell Mol Physiol 285: L1166–1178.
[53]
Yin A, Korzh V, Gong Z (2012) Perturbation of zebrafish swimbladder development by enhancing Wnt signaling in Wif1 morphants. Biochim Biophys Acta 1823: 236–244.
[54]
Yin A, Korzh V, Winata CL, Korzh V, Gong Z (2011) Wnt signaling is required for early development of zebrafish swimbladder. PloS One 6: e18431.
[55]
De Langhe SP, Sala FG, Del Moral PM, Fairbanks TJ, Yamada KM, et al. (2005) Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev. Biol 277: 316–331.
[56]
Mucenski ML, Wert SE, Nation JM, Loudy DE, Huelsken J, et al. (2003) beta-Catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J. Biol. Chem 278: 40231–40238.
[57]
Shu W, Jiang YQ, Lu MM, Morrisey EE (2002) Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129: 4831–4842.
[58]
Dean CH, Miller LA, Smith AN, Dufort D, Lang RA, et al. (2005) Canonical Wnt signaling negatively regulates branching morphogenesis of the lung and lacrimal gland. Dev. Biol 286: 270–286.
[59]
Rajagopal J, Carroll TJ, Guseh JS, Bores SA, Blank LJ, et al. (2008) Wnt7b stimulates embryonic lung growth by coordinately inceasing the replication of epithelium and mesenchyme. Development 135: 1625–1634.
[60]
Boucherat O, Chakir J, Jeannotte L (2012) The loss of Hoxa5 function promotes Notch-dependent goblet cell metaplasia in lung airways. Biol Open 1: 677–91.
[61]
Fu JH, Xue XD, Pan L, Xu W (2008) Expression of HoxB5 mRNA and their effect on lung development in premature rats with hyperoxia-induced chronic lung disease. Zhonghua Er Ke Za Zhi 46: 540–543.
[62]
Calvo R, West J, Franklin W, Erickson P, Bemis L, et al. (2000) Altered HOX and WNT7A expression in human lung cancer. Proc Natl Acad Sci U S A 97: 12776–12781.
[63]
Grier DG, Thompson A, Lappin TR, Halliday HL (2009) Quantification of Hox and surfactant protein-B transcription during murine lung development. Neonatology 96: 50–60.
[64]
Scheper GE, Bullejios M, Hosking BM, Koopman P (2000) Cloning and characterisation of the Sry-related transcription factor gene Sox8. Nucleic Acids Res 28: 1473–1480.
[65]
Xia X, Zhao J, Du Q, Chang Z (2010) Isolation and expression of two distinct Sox8 genes in mudloach (Misgurnus anguillicaudatus). Biochem Genet 49: 161–176.
[66]
Xia X, Zhao J, Du Q, Chang Z (2010) cDNA cloning and expression analysis of two distinct Sox8 genes in Paramisgurnus dabryanus (Cypriniformes). J Genet. 89: 183–92.
[67]
Clarke RL, Yzaguirre AD, Yashiro-Ohtani Y, Bondue A, Blanpain C, et al. (2013) The expression of Sox17 identifies and regulates haemogenic endothelium. Nat Cell Biol. 15: 502–510.
[68]
Chan TM, Chao CH, Wang HD, Yu YJ, Yuh CH (2009) Functional analysis of the evolutionarily conserved cis-regulatory elements on the sox17 gene in zebrafish. Dev Biol. 326: 456–70.
[69]
Kobayashi D, Jindo T, Naruse K, Takeda H (2006) Development of the endoderm and gut in medaka, Oryzias latipes. Dev Growth Differ. 48: 283–295.
[70]
Lange AW, Keiser AR, Wells JM, Zorn AM, Whitsett JA (2009) Sox17 promotes cell cycle progression and inhibits tgf-beta/smad3 signaling to initiate progenitor cell behavior in the respiratory epithelium. PLoS One 4: e5711.
[71]
Park J, Zhang JJ, Moro A, Kushida M, Wegner M, et al. (2010) Regulation of Sox9 by sonic hedgehog (shh) is essential for patterning and formation of tracheal cartilage. Dev Dyn 239: 514–526.
[72]
Park KS, Wells JM, Zorn AM, Wert SE, Whitsett JA (2006) Sox17 influences the differentiation of respiratory epithelial cells. Dev Biol 294: 192–202.
[73]
Tompkins DH, Besnard V, Lange AW, Keiser AR, Wert SE, et al. (2011) Sox2 activates cell proliferation and differentiation in the respiratory epithelium. Am J Respir Cell Mol Biol 45: 101–110.
[74]
Sock E, Rettig SD, Enderich J, Bosl MR, Tamm ER, et al. (2004) Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol Cell Biol 24: 6635–6644.
[75]
Park KS, Wells JM, Zorn AM, Wert SE, Laubach VE, et al. (2006) Transdifferentiation of ciliated cells during repair of the respiratory epithelium. Am J Respir Cell Mol Biol 34: 151–157.
[76]
Yin D, Jia Y, Yu Y, Brock MV, Herman JG, et al. (2012) Sox17 methylation inhibits its antagonism of wnt signaling pathway in lung cancer. Discovery Med. 14: 33–40.
[77]
Seguin CA, Draper JS, Nagy A, Rossant J (2008) Establishment of endoderm progenitors by Sox transcription factor expression in human embryonic stem cells. Cell Stem Cell 3: 182–195.
[78]
Kim I, Saunders TL, Morrison SJ (2007) Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 130: 470–483.
[79]
Matsui T, Kanai-Azuma M, Hara K, Matoba S, Hiramatsu R, et al. (2006) Redundant roles of Sox17 and Sox18 in postnatal angiogenesis in mice. J Cell Sci 119: 3513–3526.
[80]
Sakamoto Y, Hara K, Kanai-Azuma M, Matsui T, Miura Y, et al. (2007) Redundant roles of Sox17 and Sox18 in early cardiovascular development of mouse embryos. Biochem. Biophys. Res. Commun. 360: 539–544.
[81]
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.
[82]
Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595.
[83]
Ramskold D, Wang ET, Burge CB, Sandberg R (2009) An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol 5: e1000598.
[84]
Wang L, Feng Z, Wang X, Zhang X (2009) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136–138.
[85]
Wang Z, Gerstein M, Snyder M (2009) RNA-seq: A revolutionary tool for transcriptomics. Nat Rev Genet 10(1): 57–63.
Trapnell C, Williams BA, Pertea G, Mortazavi AM, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28(5): 511–515.
[88]
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7(3): 562–578.
[89]
Merico D, Isserlin R, Stueker O, Emili A, Bader GD (2010) Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS ONE 5(11): e13984.
