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Characterization and molecular evolution of claudin genes in the Pungitius sinensis

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Abstract

Claudins are a family of integrated membrane-bound proteins involving in paracellular tightness, barrier forming, ion permeability, and substrate selection at tight junctions of chordate epithelial and endothelial cells. Here, 39 putative claudin genes were identified in the Pungitius sinensis based on the high throughput RNA-seq. Conservative motif distribution in each group suggested functional relevance. Divergence of duplicated genes implied the species’ adaptation to the environment. In addition, selective pressure analyses identified one site, which may accelerate functional divergence in this protein family. Pesticides cause environmental pollution and have a serious impact on aquatic organisms when entering the water. The expression pattern of most claudin genes was affected by organophosphorus pesticide, indicating that they may be involved in the immune regulation of organisms and the detoxification of xenobiotics. Protein–protein network analyses also exhibited 439 interactions, which implied the functional diversity. It will provide some references for the functional study on claudin genes.

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Abbreviations

HMM:

Hidden Markov model

JTT:

Jones–Taylor–Thornton

Ka:

Non-synonymous rate of nucleotide substitution

Ks:

Synonymous rate of nucleotide substitution

ML:

Maximum likelihood

NJ:

Neighbor-joining

OP:

Organophosphorus pesticide

TJ:

Tight junction

TM:

Transmembrane helixe

References

  • Abdelilah-Seyfried S (2010) Claudin-5a in developing zebrafish brain barriers: another brick in the wall. BioEssays 32(9):768–776

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2012) Differential expression of RNA-Seq data at the gene level–the DESeq package, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany

  • Angelow S, Ahlstrom R, Yu AS (2018) Biology of claudins. Am. J. Physiol. Renal Physiol. 295(4):F867–876

    Article  CAS  Google Scholar 

  • Bagherie-Lachidan M, Wright SI, Kelly SP (2008) Claudin-3 tight junction proteins in Tetraodon nigroviridis: cloning, tissue-specific expression, and a role in hydromineral balance. Am J Physiol Regul Integr Comp Physiol 294(5):R1638–1647

    Article  CAS  PubMed  Google Scholar 

  • Bagherie-Lachidan M, Wright SI, Kelly SP (2009) Claudin-8 and -27 tight junction proteins in puffer fish Tetraodon nigroviridis acclimated to freshwater and seawater. J Comp Physiol B 179(4):419–431

    Article  CAS  PubMed  Google Scholar 

  • Bagnat M, Cheung ID, Mostov KE, Stainier DY (2007) Genetic control of single lumen formation in the zebrafish gut. Nat Cell Biol 9(8):954–960

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltzegar DA, Reading BJ, Brune ES, Borski RJ (2013) Phylogenetic revision of the claudin gene family. Mar Genomics 11:17–26

    Article  PubMed  Google Scholar 

  • Bossus MC, Madsen SS, Tipsmark CK (2015) Functional dynamics of claudin expression in Japanese medaka (Oryzias latipes): Response to environmental salinity. Comp Biochem Physiol A Mol Integr Physiol 187:74–85

    Article  CAS  PubMed  Google Scholar 

  • Bui P, Kelly SP (2014) Claudin-6, -10d and -10e contribute to seawater acclimation in the euryhaline puffer fish Tetraodon nigroviridis. J Exp Biol 217(Pt 10):1758–1767

    PubMed  Google Scholar 

  • Cao J, Lv Y (2016) Evolutionary analysis of the jacalin-related lectin family genes in 11 fishes. Fish Shellfish Immunol 56:543–553

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Tan X (2018) Comparative analysis of the tetraspanin gene family in six teleost fishes. Fish Shellfish Immunol 82:432–441

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Cheng X (2019) Transcriptome-based identification and molecular evolution of the Cytochrome P450 genes and expression profiling under dimethoate treatment in Amur stickleback (Pungitius sinensis). Animals 9:873

    Article  PubMed Central  Google Scholar 

  • Cao J, Shi F (2019) Comparative analysis of the aquaporin gene family in 12 fish species. Animals 9:233

    Article  PubMed Central  Google Scholar 

  • Cao J, Wang B, Tan X (2019) Transcriptomic responses of the clam Meretrix meretrix to the organophosphorus pesticide (dimethoate). Ecotoxicology 28:539–549

    Article  CAS  PubMed  Google Scholar 

  • Capriotti E, Fariselli P, Casadio R (2005) I-Mutant2.0: predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Res 33:W306–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chasiotis H, Kolosov D, Kelly SP (2012) Permeability properties of the teleost gill epithelium under ion-poor conditions. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302(6):R727–R739

    Article  CAS  PubMed  Google Scholar 

  • Cheung ID, Bagnat M, Ma TP et al (2012) Regulation of intrahepatic biliary duct morphogenesis by Claudin 15-like b. Dev. Biol. 361(1):68–78

    Article  CAS  PubMed  Google Scholar 

  • Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM (2002) Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol 283(1):C142–147

    Article  CAS  PubMed  Google Scholar 

  • Deretic V (2010) Autophagy in infection. Curr Opin Cell Biol 22(2):252–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Díaz-Resendiz KJ, Toledo-Ibarra GA, Girón-Pérez MI (2015) Modulation of immune response by organophosphorus pesticides: fishes as a potential model in immunotoxicology. J Immunol Res 2015:213836

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinf 5:113

    Article  CAS  Google Scholar 

  • Engelund MB, Madsen SS (2011) The role of aquaporins in the kidney of euryhaline teleosts. Front Physiol 2:51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85(1):97–177

    Article  CAS  PubMed  Google Scholar 

  • FAO (Food and Agriculture Organization) (2016) FAO yearbook. Fishery and Aquaculture Statistics. 2014/FAO annuaire, FAO, Rome

  • Fast MD, Sims DE, Burka JF, Mustafa A, Ross NW (2002) Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout, coho and Atlantic salmon. Comp Biochem Physiol A Mol Integr Physiol 132(3):645–657

    Article  CAS  PubMed  Google Scholar 

  • Force A, Lynch M, Pickett FB et al (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45

    Article  CAS  PubMed  Google Scholar 

  • Furuse M, Sasaki H, Tsukita S (1999) Manner of interaction of heterogeneous claudin species within and between tight junction strands. J Cell Biol 147(4):891–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gauberg J, Kolosov D, Kelly SP (2017) Claudin tight junction proteins in rainbow trout (Oncorhynchus mykiss) skin: spatial response to elevated cortisol levels. Gen Comp Endocrinol 240:214–226

    Article  CAS  PubMed  Google Scholar 

  • González-Mariscal L, Tapia R, Chamorro D (2008) Crosstalk of tight junction components with signaling pathways. Biochim Biophys Acta 1778(3):729–756

    Article  PubMed  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gui L, Zhang P, Liang X, Su M, Wu D, Zhang J (2016) Adaptive responses to osmotic stress in kidney-derived cell lines from Scatophagus argus, a euryhaline fish. Gene 583(2):134–140

    Article  CAS  PubMed  Google Scholar 

  • Günzel D, Yu AS (2013) Claudins and the modulation of tight junction permeability. Physiol Rev 93(2):525–569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hamazaki Y, Itoh M, Sasaki H, Furuse M, Tsukita S (2002) Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem 277(1):455–461

    Article  CAS  PubMed  Google Scholar 

  • Harrison PM, Hegyi H, Balasubramanian S et al (2002) Molecular fossils in the human genome: identification and analysis of the pseudogenes in chromosomes 21 and 22. Genome Res 12(2):272–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hay ED (1995) An overview of epithelio-mesenchymal transformation. Acta Anat 154(1):8–20

    Article  CAS  PubMed  Google Scholar 

  • Heiskala M, Peterson PA, Yang Y (2001) The roles of claudin superfamily proteins in paracellular transport. Traffic 2(2):93–98

    Article  CAS  PubMed  Google Scholar 

  • Hou Z, Cao J (2016) Comparative study of the P2X gene family in animals and plants. Purinergic Signal 12:269–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes AL, Ota T, Nei M (1990) Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. Mol Biol Evol 7(6):515–524

    CAS  PubMed  Google Scholar 

  • Itoh M, Furuse M, Morita K et al (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147(6):1351–1363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolosov D, Kelly SP (2016) Dietary salt loading and ion-poor water exposure provide insight into the molecular physiology of the rainbow trout gill epithelium tight junction complex. J Comp Physiol B 186(6):739–757

    Article  CAS  PubMed  Google Scholar 

  • Kolosov D, Kelly SP (2017) Claudin-8d is a cortisol-responsive barrier protein in the gill epithelium of trout. J Mol Endocrinol 59(3):299–310

    Article  CAS  PubMed  Google Scholar 

  • Kolosov D, Kelly SP (2020) C-type natriuretic peptide regulates the molecular components of the rainbow trout gill epithelium tight junction complex. Peptides 124:170211

    Article  CAS  PubMed  Google Scholar 

  • Kolosov D, Bui P, Chasiotis H, Kelly SP (2013) Claudins in teleost fishes. Tissue Barriers 1(3):e25391

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolosov D, Chasiotis H, Kelly SP (2014) Tight junction protein gene expression patterns and changes in transcript abundance during development of model fish gill epithelia. J Exp Biol 217(Pt 10):1667–1681

    PubMed  Google Scholar 

  • Kolosov D, Donini A, Kelly SP (2017) Claudin-31 contributes to corticosteroid-induced alterations in the barrier properties of the gill epithelium. Mol Cell Endocrinol 439:457–466

    Article  CAS  PubMed  Google Scholar 

  • Kolosov D, Bui P, Wilkie MP, Kelly SP (2020) Claudins of sea lamprey (Petromyzon marinus)—organ-specific expression and transcriptional responses to water of varying ion content. J Fish Biol 96(3):768–781

    Article  CAS  PubMed  Google Scholar 

  • Kumai Y, Bahubeshi A, Steele S, Perry SF (2011) Strategies for maintaining Na+ balance in zebrafish (Danio rerio) during prolonged exposure to acidic water. Comp Biochem Physiol A Mol Integr Physiol 160(1):52–62

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwong TC (2002) Organophosphate pesticides: biochemistry and clinical toxicology. Ther Drug Monit 24:144–149

    Article  CAS  PubMed  Google Scholar 

  • Kwong RW, Kumai Y, Perry SF (2013) Evidence for a role of tight junctions in regulating sodium permeability in zebrafish (Danio rerio) acclimated to ion-poor water. J Comp Physiol B 183(2):203–213

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lignot JH, Trilles JP, Charmantier G (1997) Effect of an organophosphorus insecticide, fenitrothion, on survival and osmoregulation of various developmental stages of the shrimp Penaeus japonicus (Vrustacea: Decapoda). Mar Biol 128:307–316

    Article  CAS  Google Scholar 

  • Lim IK (2006) TIS21 (/BTG2/PC3) as a link between ageing and cancer: cell cycle regulator and endogenous cell death molecule. J Cancer Res Clin Oncol 132(7):417–426

    Article  CAS  PubMed  Google Scholar 

  • Loh YH, Christoffels A, Brenner S, Hunziker W, Venkatesh B (2004) Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Res 14(7):1248–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Z, Ding L, Lu Q, Chen YH (2013) Claudins in intestines: distribution and functional significance in health and diseases. Tissue Barriers 1(3):e24978

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch M (2002) Genomics. Gene duplication and evolution. Science 297(5583):945–947

    Article  CAS  PubMed  Google Scholar 

  • Makino T, Takaishi M, Morohashi M, Huh NH (2001) Hornerin, a novel profilaggrin-like protein and differentiation-specific marker isolated from mouse skin. J Biol Chem 276(50):47445–47452

    Article  CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Derbyshire MK, Gonzales NR et al (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–226

    Article  CAS  PubMed  Google Scholar 

  • Markov AG, Aschenbach JR, Amasheh S (2015) Claudin clusters as determinants of epithelial barrier function. IUBMB Life 67(1):29–35

    Article  CAS  PubMed  Google Scholar 

  • Marshall WS, Breves JP, Doohan EM et al (2018) claudin-10 isoform expression and cation selectivity change with salinity in salt-secreting epithelia of Fundulus heteroclitus. J Exp Biol 221(Pt 1):jeb168906

    PubMed  Google Scholar 

  • Maryoung LA, Lavado R, Schlenk D (2014) Impacts of hypersaline acclimation on the acute toxicity of the organophosphate chlorpyrifos to salmonids. Aquat Toxicol 152:284–290

    Article  CAS  PubMed  Google Scholar 

  • McKiernan E, McDermott EW, Evoy D, Crown J, Duffy MJ (2011) The role of S100 genes in breast cancer progression. Tumour Biol 32(3):441–450

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin J, Padfield PJ, Burt JP, O'Neill CA (2004) Ochratoxin A increases permeability through tight junctions by removal of specific claudin isoforms. Am J Physiol Cell Physiol 287(5):C1412–1417

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto T, Momoi A, Kato K et al (2009) Generation of transgenic medaka expressing claudin7-EGFP for imaging of tight junctions in living medaka embryos. Cell Tissue Res 335(2):465–471

    Article  CAS  PubMed  Google Scholar 

  • Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3(6):542–545

    Article  CAS  PubMed  Google Scholar 

  • Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140(3):313–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morita K, Furuse M, Fujimoto K, Tsukita S (1999) Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci U S A 96(2):511–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piontek J, Winkler L, Wolburg H et al (2008) Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 22(1):146–158

    Article  CAS  PubMed  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY et al (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–301

    Article  CAS  PubMed  Google Scholar 

  • Rauta PR, Nayak B, Das S (2012) Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunol Lett 148(1):23–33

    Article  CAS  PubMed  Google Scholar 

  • Roberts A (2013) Ambiguous fragment assignment for high-throughput sequencing experiments, Ph.D. Thesis. University of California, Berkeley, CA, USA. Fall 2013. https://escholarship.org/uc/item/7zx1s4hr

  • Robinson PJ, Rhodes D (2006) Structure of the '30 nm' chromatin fibre: a key role for the linker histone. Curr Opin Struct Biol 16(3):336–343

    Article  CAS  PubMed  Google Scholar 

  • Rollins DA, Coppo M, Rogatsky I (2015) Minireview: nuclear receptor coregulators of the p160 family: insights into inflammation and metabolism. Mol Endocrinol 29(4):502–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandbichler AM, Egg M, Schwerte T, Pelster B (2011) Claudin 28b and F-actin are involved in rainbow trout gill pavement cell tight junction remodeling under osmotic stress. J Exp Biol 214(Pt 9):1473–1487

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui M, Sheikh H, Tran C, Bruce AE (2010) The tight junction component Claudin E is required for zebrafish epiboly. Dev Dyn 239(2):715–722

    Article  CAS  PubMed  Google Scholar 

  • Soma T, Chiba H, Kato-Mori Y et al (2004) Thr(207) of claudin-5 is involved in size-selective loosening of the endothelial barrier by cyclic AMP. Exp Cell Res 300(1):202–212

    Article  CAS  PubMed  Google Scholar 

  • Stern A, Doron-Faigenboim A, Erez E et al (2007) Selecton 2007: Advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res 35:W506–511

    Article  PubMed  PubMed Central  Google Scholar 

  • Studencka M, Konzer A, Moneron G et al (2012) Novel roles of Caenorhabditis elegans heterochromatin protein HP1 and linker histone in the regulation of innate immune gene expression. Mol Cell Biol 32(2):251–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki H, Tani K, Tamura A, Tsukita S, Fujiyoshi Y (2015) Model for the architecture of claudin-based paracellular ion channels through tight junctions. J Mol Biol 427(2):291–297

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–452

    Article  CAS  PubMed  Google Scholar 

  • Tacon AGJ, Metian M (2013) Fish Matters: importance of aquatic foods in human and global food supply. Rev Fish Sci 21(1):1–17

    Article  CAS  Google Scholar 

  • Tipsmark CK, Madsen SS (2012) Tricellulin, occludin and claudin-3 expression in salmon intestine and kidney during salinity adaptation. Comp Biochem Physiol A Mol Integr Physiol 162(4):378–385

    Article  CAS  PubMed  Google Scholar 

  • Tipsmark CK, Luckenbach JA, Madsen SS, Kiilerich P, Borski RJ (2008) Osmoregulation and expression of ion transport proteins and putative claudins in the gill of southern flounder (Paralichthys lethostigma). Comp Biochem Physiol A Mol Integr Physiol 150(3):265–273

    Article  PubMed  CAS  Google Scholar 

  • Tipsmark CK, Sørensen KJ, Hulgard K, Madsen SS (2010) Claudin-15 and -25b expression in the intestinal tract of Atlantic salmon in response to seawater acclimation, smoltification and hormone treatment. Comp Biochem Physiol A Mol Integr Physiol 155(3):361–370

    Article  PubMed  CAS  Google Scholar 

  • Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2(4):285–293

    Article  CAS  PubMed  Google Scholar 

  • Van Itallie CM, Colegio OR, Anderson JM (2004) The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability. J Membr Biol 199(1):29–38

    Article  PubMed  CAS  Google Scholar 

  • Van Itallie CM, Tietgens AJ, LoGrande K et al (2012) Phosphorylation of claudin-2 on serine 208 promotes membrane retention and reduces trafficking to lysosomes. J Cell Sci 125(Pt 20):4902–4912

    PubMed  PubMed Central  Google Scholar 

  • van Meer G, Gumbiner B, Simons K (1986) The tight junction does not allow lipid molecules to diffuse from one epithelial cell to the next. Nature 322(6080):639–641

    Article  PubMed  Google Scholar 

  • Wen H, Watry DD, Marcondes MC, Fox HS (2004) Selective decrease in paracellular conductance of tight junctions: role of the first extracellular domain of claudin-5. Mol Cell Biol 24(19):8408–8417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkins MR, Gasteiger E, Bairoch A et al (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552

    CAS  PubMed  Google Scholar 

  • Xu F, Ye YT, Cai CF, Wu P, Song L, Liu M, Yao LJ, Dong JJ, Huang YW, Gong Z, Qin J, Song L (2014) Observation of the middle intestinal tight junction structure, cloning and studying tissue distribution of the four Claudin genes of the grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem 40(6):1783–1792

    Article  CAS  PubMed  Google Scholar 

  • Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39:306–314

    Article  CAS  PubMed  Google Scholar 

  • Yeh SP, Sung TG, Chang CC, Chen W, Kuo CM (2005) Effects of an organophosphorus insecticide, trichlorfon, on hematological parameters of the giant freshwater prawn, Macrobrachium rosenbergii (de Man). Aquaculture 243:383–392

    Article  CAS  Google Scholar 

  • Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13:1402–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95(7):3708–3713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The research was funded by Jiangsu University “Youth Backbone Teacher Training Project”.

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The research was funded by Jiangsu University “Youth Backbone Teacher Training Project”.

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  1. Institute of Life Sciences, Jiangsu University, Zhenjiang, 212013, China

    Jun Cao & Xiuzhu Cheng

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  1. Jun Cao
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Conceptualization was carried out by J.C.; Methodology was carried out by J.C. and X.C.; Validation was done by J.C.; Formal analysis was done by J.C. Resources were carried out by J.C. and X.C.; Writing—original draft preparation was done by J.C.; Writing—review and editing was done by J.C. and X.C.; Project administration was done by J.C.; Funding acquisition was carried out by J.C.

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Correspondence to Jun Cao.

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360_2020_1301_MOESM1_ESM.ppt

Fig. S1. Motif and variation patterns among claudin proteins. The height of a letter indicates its Motif and variation patterns among claudin proteins. (PPT 322 kb)

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Cao, J., Cheng, X. Characterization and molecular evolution of claudin genes in the Pungitius sinensis. J Comp Physiol B 190, 749–759 (2020). https://doi.org/10.1007/s00360-020-01301-5

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