Transcriptional Identification of Related Proteins in the Immune System of the Crayfish Procambarus clarkii
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Transcriptional Identification of Related Proteins in the Immune System of the Crayfish
3.2. Components Identified Related to the Coagulation and Melanization Immune Pathway
3.3. Pattern Recognition Receptor and Apoptosis Components Identified in Crayfish
3.4. Complement Pathway Components Identified in Crayfish
3.5. Endocytic Route Components Identified in Crayfish
3.6. Anti-Microbial Peptides Identified in Crayfish
3.7. Toll, Immune Deficiency Pathway, and Ubiquitin-Proteasome System Components Identified in Crayfish
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Vioque-Fernández, A.; de Almeida, E.A.; López-Barea, J. Esterases as pesticide biomarkers in crayfish (Procambarus clarkii, Crustacea): Tissue distribution, sensitivity to model compounds and recovery from inactivation. Comp. Biochem. Physiol. C 2007, 145, 404–412. [Google Scholar] [CrossRef] [PubMed]
- Hofkin, B.V.; Hofinger, D.M.; Koech, D.K.; Loker, E.S. Predation of Biomphalaria and non-target molluscs by the crayfish Procambarus clarkii: Implications for the biological control of schistosomiasis. Ann. Trop. Med. Parasitol. 1992, 86, 663–670. [Google Scholar] [CrossRef] [PubMed]
- Gherardi, F.; Acquistapace, P. Invasive crayfish in Europe: The impact of Procambarus clarkii on the littoral community of a Mediterranean lake. Freshw. Biol. 2007, 52, 1249–1259. [Google Scholar] [CrossRef]
- Mikles, D.L.; Hui, J.H. Neocaridina denticulate: A decapod crustaceas model for functional genomics. Integr. Comp. Biol. 2015, 55, 891–897. [Google Scholar] [CrossRef] [PubMed]
- The State of World Fisheries and Aquaculture 2016. Available online: http://www.fao.org/3/a-i5555e.pdf (accessed on 7 May 2018).
- Blom, J.; Ottaviani, E. Immune-Neuroendocrine Interactions: Evolution, Ecology, and Susceptibility to Illness. Med. Sci. Monit. Basic Res. 2017, 23, 362–367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, F.; Wei, J.; Li, Q.; Jiang, R.; Yu, N.; Qin, J.; Chen, L. Effects of perfluorooctane sulfonate on the immune responses and expression of immune-related genes in Chinese mitten-handed crab Eriocheir sinensis. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2015, 172, 13–18. [Google Scholar] [CrossRef] [PubMed]
- Robinson, G.E.; Hackett, K.J.; Purcell-Miramontes, M.; Brown, S.J.; Evans, J.D.; Goldsmith, M.R.; Lawson, D.; Okamuro, J.; Robertson, H.M.; Schneider, D.J. Creating a buzz about insect genomes. Science 2011, 331, 1386. [Google Scholar] [CrossRef] [PubMed]
- Sequenced Arthropod Genomes. Available online: http://i5k.github.io/arthropod_genomes_at_ncbi (accessed on 20 May 2018).
- Colbourne, J.K.; Pfrender, M.E.; Gilbert, D.; Thomas, W.K.; Tucker, A.; Oakley, T.H.; Tokishita, S.; Aerts, A.; Arnold, G.J.; Basu, M.K.; et al. The Ecoresponsive Genome of Daphnia pulex. Science 2011, 331, 555–561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- MacTaggart, S.J.; Conlon, C.; Colbourne, J.K.; Blaxter, M.L.; Little, T.J. The components of the Daphnia pulex immune system as revealed by complete genome sequencing. BMC Genom. 2009, 10, 175. [Google Scholar] [CrossRef] [PubMed]
- Clark, K.F.; Greenwood, S.J. Next-Generation Sequencing and the Crustacean Immune System: The Need for Alternatives in Immune Gene Annotation. Integr. Comp. Biol. 2016, 56, 1113–1130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, J.A.; Wang, Z. Next-generation transcriptome assembly. Nat. Rev. Genet. 2011, 12, 671–682. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manfrin, C.; Tom, M.; De Moro, G.; Gerdol, M.; Giulianini, P.G.; Pallavicini, A. The eyestalk transcriptome of red swamp crayfish Procambarus clarkii. Gene 2015, 557, 28–34. [Google Scholar] [CrossRef] [PubMed]
- Society for Neuroscience Policies on The Use of Animals and Humans in Research. Available online: https://www.sfn.org/advocacy/policy-positions/policies-on-the-use-of-animals-and-humans-in-research (accessed on 13 May 2017).
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef] [PubMed]
- Haas, B.J.; Papanicolaou, A.; Yassour, M.; Grabherr, M.; Blood, P.D.; Bowden, J.; Couger, M.B.; Eccles, D.; Li, B.; Lieber, M.; et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013, 8, 1494–1512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Afgan, E.; Baker, D.; van den Beek, M.; Blankenberg, D.; Bouvier, D.; Čech, M.; Chilton, J.; Clements, D.; Coraor, N.; Eberhard, C.; et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res. 2016, 44, W537–W544. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [PubMed]
- ExPASy. Available online: http://web.expasy.org/traslate/ (accessed on 1 February 2018).
- Basic Local Alignment Search Tool. Available online: http://www.ncbi.nlm.nih.gov/blast (accessed on 1 February 2018).
- GenBank. Available online: http://www.ncbi.nlm.nih.gov/Genbank/index.html (accessed on 1 February 2018).
- Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673–4680. [Google Scholar] [CrossRef] [PubMed]
- Prosite Database of Protein Domains, Families and Functional Sites. Available online: https://prosite.expasy.org/ (accessed on 1 February 2018).
- UniprotKB/Swiss-Prot Database. Available online: http://www.uniprot.org/blast/uniprot (accessed on 1 February 2018).
- Cerenius, L.; Jiravanichpaisal, P.; Liu, H.-P.; Söderhäll, I. Crustacean immunity. In Invertebrate Inmunnity; Soderhal, K., Ed.; Landes Bioscience and Springer Science and Business Media: New York, NY, USA, 2010; Volume 708, pp. 239–281. [Google Scholar]
- Li, F.; Xiang, J. Signaling pathways regulating innate immune responses in shrimp. Fish Shellfish Immunol. 2013, 34, 973–980. [Google Scholar] [CrossRef] [PubMed]
- Cerenius, L.; Söderhäll, K. Crayfish immunity. Recent findings. Dev. Comp. Immunol. 2018, 80, 94–98. [Google Scholar] [CrossRef] [PubMed]
- Söderhäll, I. Crustacean hematopoiesis. Dev. Comp. Immunol. 2016, 58, 129–141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, R.Y.; Shen, K.L.; Chen, Z.; Fan, W.W.; Xie, X.L.; Meng, C.; Chang, X.J.; Zheng, L.B.; Jeswin, J.; Li, C.H.; et al. White spot syndrome virus entry is dependent on multiple endocytic routes and strongly facilitated by Cq-GABARAP in a CME-dependent manner. Sci. Rep. 2016, 6, 28694. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, F.; Xiang, J. Recent advances in researches on the innate immunity of shrimp in China. Dev. Comp. Immunol. 2013, 39, 11–26. [Google Scholar] [CrossRef] [PubMed]
- Tassanakajon, A.; Somboonwiwat, K.; Supungul, P.; Tang, S. Discovery of immune molecules and their crucial functions in shrimp immunity. Fish Shellfish Immunol. 2013, 34, 954–967. [Google Scholar] [CrossRef] [PubMed]
- Aspán, A.; Huang, T.S.; Cerenius, L.; Söderhäll, K. cDNA cloning of prophenoloxidase from the freshwater crayfish Pacifastacus leniusculus and its activation. Proc. Natl. Acad. Sci. USA 1995, 92, 939–943. [Google Scholar] [CrossRef] [PubMed]
- Söderhäll, K.; Cerenius, L. Role of prophenoloxidase-activating system in invertebrate immunity. Curr. Opin. Immunol. 1998, 10, 23–28. [Google Scholar] [CrossRef]
- Cerenius, L.; Söderhäll, K. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 2004, 198, 116–126. [Google Scholar] [CrossRef] [PubMed]
- Cerenius, L.; Lee, B.L.; Söderhäll, K. The proPO-system: Pros and cons for its role in invertebrate immunity. Trends Immunol. 2008, 29, 263–271. [Google Scholar] [CrossRef] [PubMed]
- Iwanaga, S.; Lee, B.L. Recent advances in the innate immunity of invertebrate animals. BMB Rep. 2005, 38, 128–150. [Google Scholar] [CrossRef]
- Li, Y.H.; Zheng, F.L.; Chen, H.Q.; Wang, H.Z.; Wang, L.Q.; Xu, D.P. Cloning and Sequence Analysis of Prophenoloxidase from Haemocytes of the Red Swamp Crayfish, Procambarus clarkii. Agric. Sci. China 2009, 8, 369–379. [Google Scholar] [CrossRef]
- Sritunyalucksana, K.; Cerenius, L.; Söderhäll, K. Molecular cloning and characterization of prophenoloxidase in the black tiger shrimp, Penaeus monodon. Dev. Comp. Immunol. 1999, 23, 179–186. [Google Scholar] [CrossRef]
- Ai, H.S.; Liao, J.X.; Huang, X.D.; Yin, Z.X.; Weng, S.P.; Zhao, Z.Y.; Li, S.D.; Yu, X.Q.; He, J.G. A novel prophenoloxidase 2 exists in shrimp hemocytes. Dev. Comp. Immunol. 2009, 33, 59–68. [Google Scholar] [CrossRef] [PubMed]
- Genbank: ACJ31817.1. Available online: https://www.ncbi.nlm.nih.gov/protein/212552195 (accessed on 10 February 2018).
- Amparyup, P.; Charoensapsri, W.; Tassanakajon, A. Two prophenoloxidases are important for the survival of Vibrio harveyi challenged shrimp Penaeus monodon. Dev. Comp. Immunol. 2009, 33, 247–256. [Google Scholar] [CrossRef] [PubMed]
- Wang, R.; Liang, Z.; Hal, M.; Söderhäll, K. A transglutaminase involved in the coagulation system of the freshwater crayfish, Pacifastacus leniusculus. Tissue localisation and cDNA cloning. Fish Shellfish Immunol. 2001, 11, 623–637. [Google Scholar] [CrossRef] [PubMed]
- Chen, M.Y.; Hu, K.Y.; Huang, C.C.; Song, Y.L. More than one type of transglutaminase in invertebrates? A second type of transglutaminase is involved in shrimp coagulation. Dev. Comp. Immunol. 2005, 29, 1003–1016. [Google Scholar] [CrossRef] [PubMed]
- Liang, Z.; Sottrup-Jensen, L.; Aspán, A.; Hall, M.; Söderhäll, K. Pacifastin, a novel 155-kDa heterodimeric proteinase inhibitor containing a unique transferrin chain. Proc. Natl. Acad. Sci. USA 1997, 94, 6682–6687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ponprateep, S.; Vatanavicharn, T.; Lo, C.F.; Tassanakajon, A.; Rimphanitchayakit, V. Alpha-2-macroglobulin is a modulator of prophenoloxidase system in pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol. 2017, 62, 68–74. [Google Scholar] [CrossRef] [PubMed]
- Hall, M.; Wang, R.; van Antwerpen, R.; Sottrup-Jensen, L.; Söderhäll, K. The crayfish plasma clotting protein: A vitellogenin-related protein responsible for clot formation in crustacean blood. Proc. Natl. Acad. Sci. USA 1999, 96, 1965–1970. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cheng, W.; Tsai, I.H.; Huang, C.J.; Chiang, P.C.; Cheng, C.H.; Yeh, M.S. Cloning and characterization of hemolymph clottable proteins of kuruma prawn (Marsupenaeus japonicus) and white shrimp (Litopenaeus vannamei). Dev. Comp. Immunol. 2008, 32, 265–274. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.; Gillen, C.M.; Wheatly, M.G. Cloning and characterization of a calmodulin gene (CaM) in crayfish Procambarus clarkii and expression during molting. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009, 152, 216–225. [Google Scholar] [CrossRef] [PubMed]
- Ameri, K.; Harris, A.L. Activating transcription factor 4. Int. J. Biochem. Cell Biol. 2008, 40, 14–21. [Google Scholar] [CrossRef] [PubMed]
- Lan, J.F.; Zhao, L.J.; Wei, S.; Wang, Y.; Lin, L.; Li, X.C. PcToll2 positively regulates the expression of antimicrobial peptides by promoting PcATF4 translocation into the nucleus. Fish Shellfish Immunol. 2016, 58, 59–66. [Google Scholar] [CrossRef] [PubMed]
- Huang, Y.; Li, T.; Jin, M.; Yin, S.; Hui, K.M.; Ren, Q. Newly identified PcToll4 regulates antimicrobial peptide expression in intestine of red swamp crayfish Procambarus clarkii. Gene 2017, 610, 140–147. [Google Scholar] [CrossRef] [PubMed]
- Smith, V.J.; Dyrynda, E.A. Antimicrobial proteins: From old proteins, new tricks. Mol. Immunol. 2015, 68, 383–398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, A.J.; Gao, L.; Wang, X.W.; Zhao, X.F.; Wang, J.X. SUMO-Conjugating enzyme E2 UBC9 mediates viral immediate-Early Protein SUMOylation in crayfish to facilitate reproduction of white spot syndrome virus. J. Virol. 2013, 87, 636–647. [Google Scholar] [CrossRef] [PubMed]
- Götze, S.; Saborowski, R.; Martínez-Cruz, O.; Muhlia-Almazán, A.; Sánchez-Paz, A. Proteasome properties of hemocytes differ between the whiteleg shrimp Penaeus vannamei and the brown shrimp Crangon crangon (Crustacea, Decapoda). Cell Stress Chaperones 2017, 22, 879–891. [Google Scholar] [CrossRef] [PubMed]
- Kanayama, H.O.; Tamura, T.; Ugai, S.; Kagawa, S.; Tanahashi, N.; Yoshimura, T.; Tanaka, K.; Ichihara, A. Demonstration that a human 26S proteolytic complex consists of a proteasome and multiple associated protein components and hydrolyzes ATP and ubiquitin-ligated proteins by closely linked mechanisms. Eur. J. Biochem. 1992, 206, 567–578. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dzik, J.M. The ancestry and cumulative evolution of immune reactions. Acta Biochim. Pol. 2010, 57, 443–466. [Google Scholar] [PubMed]
- Cerenius, L.; Söderhäll, K. Variable immune molecules in invertebrates. J. Exp. Biol. 2013, 216, 4313–4319. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nappi, A.J.; Ottaviani, E. Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 2000, 22, 469–480. [Google Scholar] [CrossRef]
- Song, Y.L.; Li, C.Y. Shrimp immune system-special focus on penaeidin. J. Mar. Sci. Technol. 2014, 22, 1–8. [Google Scholar]
- Shen, H.; Hu, Y.; Ma, Y.; Zhou, X.; Xu, Z.; Shui, Y.; Li, C.; Xu, P.; Sun, X. In-depth transcriptome analysis of the red swamp crayfish Procambarus clarkii. PLoS ONE 2014, 9, e110548. [Google Scholar] [CrossRef] [PubMed]
- Ou, J.; Li, Y.; Ding, Z.; Xiu, Y.; Wu, T.; Du, J.; Li, W.; Zhu, H.; Ren, Q.; Gu, W.; et al. Transcriptome-wide identification and characterization of the Procambarus clarkii microRNAs potentially related to immunity against Spiroplasma eriocheiris infection. Fish Shellfish Immunol. 2013, 35, 607–617. [Google Scholar] [CrossRef] [PubMed]
- Du, Z.Q. Comparative transcriptome analysis reveals three potential antiviral signaling pathways in lymph organ tissue of the red swamp crayfish, Procambarus clarkii. Genet. Mol. Res. 2016, 15. [Google Scholar] [CrossRef] [PubMed]
- Jiang, H.; Xing, Z.; Lu, W.; Qian, Z.; Yu, H.; Li, J. Transcriptome analysis of red swamp crayfish Procambarus clarkii reveals genes involved in gonadal development. PLoS ONE 2014, 9, e105122. [Google Scholar]
- Munro, S.; Pelham, H.R.B. A C-terminal signal prevents secretion of luminal ER proteins. Cell 1987, 48, 899–907. [Google Scholar] [CrossRef]
- Pelham, H.R.B. The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem. Sci. 1990, 15, 483–486. [Google Scholar] [CrossRef]
- Genbank: AGZ84432.1. Available online: https://www.ncbi.nlm.nih.gov/protein/AGZ84432.1 (accessed on 15 February 2018).
- Genbank: AEB54630.1. Available online: https://www.ncbi.nlm.nih.gov/protein/AEB54630.1 (accessed on 2 March 2018).
- Shi, X.Z.; Zhang, R.R.; Jia, Y.P.; Zhao, X.F.; Yu, X.Q.; Wang, J.X. Identification and molecular characterization of a Spatzle-like protein from Chinese shrimp (Fenneropenaeus chinensis). Fish Shellfish Immunol. 2009, 27, 610–617. [Google Scholar] [CrossRef] [PubMed]
- Lima, P.C.; Harris, J.O.; Cook, M. Exploring RNAi as a therapeutic strategy for controlling disease in aquaculture. Fish Shellfish Immunol. 2013, 34, 729. [Google Scholar] [CrossRef] [PubMed]
- Itsathitphaisarn, O.; Thitamadee, S.; Weerachatyanukul, W.; Sritunyalucksana, K. Potential of RNAi applications to control viral diseases of farmed shrimp. J. Invertebr. Pathol. 2017, 147, 76. [Google Scholar] [CrossRef] [PubMed]
Name | Nucleotides | Homology (aa) | Id GenBank | Function |
---|---|---|---|---|
Beta-1,3-glucan-binding protein precursor | 10,743 | Astacus astacus 3070/3607 (85%) | KY974279 | Involved in recognition of invading microorganisms. Binds specifically to beta-1,3-glucan and activates the phenoloxidase cascade. |
Transglutaminase | 2178 | Pacifastacus leniusculus 688/766 (90%) | MF385053 | Enzyme of clotting system |
Clotting protein precursor | 5127 | Pacifastacus leniusculus 1257/1725 (73%) | MG452709 | Forms stable clots in the presence of calcium. |
Laccase-10-like | 2814 | Hyalella azteca 262/656 (40%) | MG452692 | Multicopper oxidases, oxidizes many different types of phenols and diamines. |
Laccase-1-like | 2043 | Bombus impatiens 280/645 (43%) | MG452693 | Laccases act on phenols and similar molecules |
Alpha-2-macroglobulin-like isoform 3 | 4659 | Pacifastacus leniusculus 1312/1606 (82%) | MG452688 | A2M-like proteins can inhibit all four classes of proteinases by a ‘trapping’ mechanism. |
Fibrinogen | 2031 | Daphnia magna 121/223 (54%) | MG452685 | Fibrinogen, the principal protein of vertebrate blood clotting. |
Pacifastin heavy chain precursor | 3897 | Pacifastacus leniusculus 805/917 (88%) | MG452696 | Participates in the control of the prophenoloxidase (ProPo) system |
Pacifastin light chain-like serine proteinase inhibitor | 3405 | Litopenaeus vannamei 249/637 (39%) | MG452697 | |
Masquerade -like serine proteinase (cMasII) | 1110 | Pacifastacus leniusculus 320/369 (87%) | MG452712 | Participates in the ProPo system. The N-terminal region exhibited in vitro antimicrobial activity against Gram-positive bacteria |
Hemocytin-like | 1455 | Hyalella azteca 151/374 (40%) | MG452718 | Adhesive protein and relates to hemostasis or encapsulation of foreign substances for self-defense |
Prophenoloxidase | 1377 | Procambarus clarkii 220/249 (88%) | MH156427 | The terminal component of the so-called proPO activating system. This is a copper-containing oxidase that functions in the formation of pigments such as melanins and other polyphenolic compounds. |
Flocculation protein FLO11-like | 1857 | Hyalella azteca 142/300 (40%) | MG976887 | Cell wall protein that participates in adhesive cell-cell interactions during yeast flocculation, a reversible, asexual, and Ca2+-dependent process in which cells adhere to form aggregates (flocs) consisting of thousands of cells. |
Tyrosine-protein kinase Fer | 2619 | Hyalella azteca 673/909 (74%) | KY974273 | Plays a role in leukocyte recruitment and diapedesis in response to bacterial lipopolysaccharide (LPS). |
Techylectin-5B-like | 858 | Hyalella azteca] 166/245 (68%) | MG976886 | Lectin involved in innate immunity. Agglutinates all types of human erythrocytes, Gram-positive, and -negative bacteria. Has a stronger agglutinating activity towards Gram-negative bacteria than -positive bacteria. Specifically recognizes acetyl group-containing substances on agglutinated cells. |
Integrin | 2430 | Litopenaeus vannamei 671/811 (83%) | MF140473 | Integrins are cell adhesion molecules that mediate cell extracellular matrix and cell-cell interactions. They contain both alpha and beta subunits. |
Name | Nucleotides | Homology (aa) | Id GenBank | Function |
---|---|---|---|---|
Heat shock protein 70 kDa (hsp70) | 1914 | Procambarus clarkii 635/638 (99%) | MH156459 | The organisms respond to heat shock or other environmental stresses by inducing synthesis of proteins collectively known as heat-shock proteins |
Heat shock protein 70 kDa cognate 3 | 1962 | Cherax cainii 627/654 (96%) | MG910465 | |
Heat shock protein 70 kDa isoform 1 | 1962 | Astacus astacus 646/658 (98%) | MG910466 | |
Heat shock protein 70 kDa isoform 2 | 1971 | Philodina roseola 554/607 (91%) | MG910467 | |
Heat shock protein 84 kDa | 2208 | Philodina roseola 707/737 (96%) | MG910468 | |
Heat shock protein 90 kDa | 2190 | Cherax destructor 708/740 (96%) | MG910469 | |
Small heat shock protein | 552 | Cherax destructor 178/184 (97%) | MG910470 | Small heat shock proteins acting as chaperones that can protect other proteins against heat-induced denaturation and aggregation. |
Glycogen synthase kinase 3 beta (GSK3beta) | 1230 | Litopenaeus vannamei 403/410 (98%) | KY974307 | Probably regulates NF-kappa-B (NFKB1) at the transcriptional level and is required for the NF-kappa-B-mediated anti-apoptotic response to TNF-alpha (TNF/TNFA). |
Tax1 binding protein | 2838 | Scylla serrata 418/1027 (41%) | MG976888 | Inhibits TNF-induced apoptosis by mediating TNFAIP3 anti-apoptotic activity. Degraded by caspase-3-like family proteins upon TNF-induced apoptosis. May also play a role in the pro-inflammatory cytokine IL-1 signaling cascade. |
Tumor necrosis factor (TNF) | 1524 | Metanephrops japonicus 248/516 (48%) | MG452707 | TNF-related apoptosis inducing ligand (TRAIL) |
Tumor Necrosis Factor Super Family (TNFSF) | 1476 | Litopenaeus vannamei 258/496 (52%) | MG452708 | TNF-related apoptosis inducing ligand (TRAIL) Membrane receptor involved in phagocytosis by macrophages and astrocytes of apoptotic cells. Receptor for C1q, an eat-me signal, that binds phosphatidylserine expressed on the surface of apoptotic cells |
Multiple epidermal growth factor-like domains protein 10-like | 917 | Saccoglossus kowalevskii 62/232 (27%) | MH156433 | TNF-related apoptosis inducing ligand (TRAIL) Membrane receptor involved in phagocytosis by macrophages and astrocytes of apoptotic cells. Receptor for C1q, an eat-me signal, that binds phosphatidylserine expressed on the surface of apoptotic cells. Regulates osteoblast maturation by controlling TGF-beta bioavailability and calibrating TGF-beta and bone morphogenetic protein (BMP) levels, respectively. |
Fibrillin 2 | 5139 | Hyalella azteca 1241/1725 (72%) | MG910478 | |
Calmodulin | 447 | Procambarus clarkii 148/149 (99%) | MG910474 | Calmodulin mediates control of many enzymes, ion channels, aquaporins, and other proteins by Ca2+. |
Stabilin 2 | 2010 | Lingula anatine 167/493 (34%) | MH492359 | Phosphatidylserine receptor that enhances the engulfment of apoptotic cells. Binds to both Gram-positive and -negative bacteria and may play a role in defense against bacterial infection. |
Name | Nucleotides | Homology (aa) | Id GenBank | Function |
---|---|---|---|---|
C-type lectin | 687 | Litopenaeus vannamei 68/147 (46%) | MG452686 | Protein domains homologous to the carbohydrate-recognition domains (CRDs) of the C-type lectins. |
C-type lectin | 930 | Portunus trituberculatus 141/213 (66%) | MG452687 | C-type lectin (CTL) or carbohydrate-recognition domain (CRD). |
Galactose-specific lectin nattectin-like | 567 | Hyalella azteca 42/119 (35%) | MG910471 | Exhibits hemagglutination activity (minimum hemagglutination concentration = 2.5 µg/well) in a calcium-independent fashion. Has remarkable pro-inflammatory activity, inducing neutrophil mobilization in mice. |
Ras-related protein Rab-11A-like | 642 | Penaeus monodon 210/214 (98%) | KY974298 | The small Guanosine Triphosphatase or GTPases Rab are key regulators of intracellular membrane trafficking. Regulates the recycling of receptor of Fc region of monomeric Ig G (FCGRT) to basolateral membranes. |
Casein kinase I | 987 | Hyalella azteca 284/307 (93%) | MF062030 | Probably involved in lymphocyte physiology. |
Activating transcription factor 4 | 1293 | Procambarus clarkii 430/431 (99%) | MG976885 | ATF4 regulates the expression of genes involved in oxidative stress [51]. |
Dual oxidase 2-like | 1407 | Hyalella azteca 333/472 (71%) | MF688645 | Generates hydrogen peroxide, required for the activity of Thyroid Peroxidase (TPO) and Lactoperoxidase (LPO) Plays a role in thyroid hormones synthesis and lactoperoxidase-mediated antimicrobial defense at the surface of mucosa. |
Polypeptide N-acetilgalactosaminyltransferase 2 | 1659 | Zootermopsis nevadensis 272/549 (50%) | MG910472 | Probably involved in O-linked glycosylation of the immunoglobulin A1 (IgA1) hinge region |
Angiopoietin-related protein 2-like | 1446 | Hyalella azteca 140/239 (59%) | MG452689 | ANGPTL2 has a role also in angiogenesis, in tissue repair. |
Thrombospondin-1 | 2859 | Zootermopsis nevadensis 356/845 (42%) | MG452690 | Adhesive glycoprotein that mediates cell-to-cell and cell-to-matrix interactions. |
Angiopoietin-2-like | 1983 | Hyalella azteca 242/490 (49%) | MG452694 | Binds to TEK/TIE2, competing for the ANGPT1 binding site, and modulating ANGPT1 signaling. |
Wiskott-Aldrich Syndrome protein (WASp) family member 3 isoform X1 | 1175 | Zootermopsis nevadensis 131/292 (45%) | MG452710 | WASp is required for various functions in myeloid and lymphoid immune cells |
Wiskott-Aldrich syndrome protein family member 3-like | 1143 | Hyalella azteca 163/243 (67%) | MG452711 | |
B-cell receptor-associated protein 31-like | 690 | Hyalella azteca 136/230 (59%) | MG452713 | Functions as a chaperone protein. |
B-cell differentiation antigen CD72 | 672 | Vicugna pacos 51/192 (27%) | MG452715 | Plays a role in B-cell proliferation and differentiation. |
CD109 antigen-like | 5160 | Crassostrea gigas 148/706 (21%) | MG452716 | Modulates negative TGFB1 signaling in keratinocytes. |
Vascular endothelial growth factor 2 | 1173 | Litopenaeus vannamei 172/334 (51%) | MG452717 | Growth factor active in angiogenesis, vasculogenesis, and endothelial cell growth. |
Peroxidasin homolog | 1392 | Hyalella azteca 229/323 (71%) | MG910475 | Plays a role in extracellular matrix consolidation, phagocytosis, and defense. Contains the IG-like domain profile. |
Name | Nucleotides | Homology (aa) | Id GenBank | Function |
---|---|---|---|---|
Beta-Tubulin 1 | 1353 | Daphnia pulex 403/451 (89%) | MG910477 | Tubulin is the major constituents of microtubules. It binds two moles of GTP, one at an exchangeable site on the beta chain and one at a non-exchangeable site on the alpha chain. |
Actin, cytoplasmic 1 | 1128 | P. tepidariorum 360/376 (96%) | MG910479 | Actins are highly conserved proteins that are involved in various types of cell motility and are ubiquitously expressed in all eukaryotic cells. |
Clathrin | 4206 | F. chinensis 1383/1402 (99%) | KY974296 | Participates in the internalization of viruses. |
Gamma-aminobutyric acid receptor-associated protein GABARAP | 357 | C. quadricarinatus 117/119 (98%) | MG910480 | Participates in the formation of autophagosomes. |
Sortilin-related receptor-like | 3348 | Hyalella azteca 491/1176 (42%) | MF279130 | Likely to be a multifunctional endocytic receptor that may be implicated in the uptake of lipoproteins and of proteases. |
Cathepsin A | 1458 | Eriocheir sinensis 348/453 (77%) | MG452720 | Enclosed within lysosomes, participates in innate immune system. |
Endoplasmin | 2355 | Penaeus monodon 612/722 (85%) | MG452719 | Molecular chaperone that functions in the processing and transport of secreted proteins. |
Name | Nucleotides | Homology (aa) | Id Genbank | Function |
---|---|---|---|---|
ALF12 | 1314 | Procambarus clarkii 44/101 (44%) | MH538268 | May bind to bacterial LPS and thus specifically inhibit LPS-mediated activation of hemolymph coagulation. It has a strong antibacterial effect, particularly on the growth of Gram-negative bacteria. |
Crustin 2 | 330 | Procambarus clarkii 110/110 (100%) | MG976884 | Crustins act primarily against Gram-positive bacteria, although some have also been reported to kill Gram-negatives [52] |
Crustin 2 isoform 1 | 267 | Procambarus clarkii 89/89 (100%) | MH492354 | |
Lysozyme-like | 456 | Procambarus clarkii 71/149 (48%) | MG976883 | Has bacteriolytic activity. May play a role in digestion and in host defense mechanisms against invading microbes |
Lysosome-associated membrane glycoprotein 1-like | 990 | Hyalella azteca 92/245 (38%) | MG452714 | LAMP are integral membrane proteins, specific to lysosomes, and their exact biological function is not yet clear. |
Name | Nucleotides | Homology (aa) | Id GenBank | Function |
---|---|---|---|---|
Toll-like receptor 3 | 1902 | Hyalella azteca 320/522 (61%) | MG452691 | Toll type receptors recognize molecular patterns expressed by a broad spectrum of infectious agents. |
Sequestosome-1 | 1014 | Lingula anatina 83/225 (37%) | MG452705 | May regulate the activation of NFKB1 by TNF-alpha, nerve growth factor (NGF), and interleukin-1. May regulate signaling cascades through ubiquitination. |
Ubiquitin-activating enzyme E1 | 3114 | Eriocheir sinensis 866/1014 (85%) | MG452698 | Activates ubiquitin by first adenylating with Adenosine Triphosphate (ATP) its C-terminal glycine residue |
Ubiquitin-conjugating enzyme E2 UBC9 | 480 | Procambarus clarkii 159/160 (99%) | MG452699 | Catalyzes covalent attachment of ubiquitin to target proteins. |
Ubiquitin conjugating enzyme-3 | 495 | Eriocheir sinensis 165/165 (100%) | MG452700 | Accepts ubiquitin from an E2 ubiquitin-conjugating enzyme in the form of a thioester and then directly transfers ubiquitin to targeted substrates |
E3 ubiquitin-protein ligase UBR5 | 1092 | Zootermopsis nevadensis 283/382 (74%) | MG452701 | |
Ubiquitin-protein ligase E3A | 1128 | Stegodyphus mimosarum 275/376 (73%) | MG452702 | |
Ubiquitin carboxyl-terminal hydrolase 7-like | 2631 | Hyalella azteca 705/904 (78%) | MG452703 | Deubiquitinating enzymes |
Proteasome subunit beta type-3 | 615 | Hyalella azteca 165/204 (81%) | MG910481 | Associated with two 19S regulatory particles, forms the 26S proteasome and thus participates in the ATP-dependent degradation of ubiquitinated proteins. |
26S Proteasome non-ATPase regulatory subunit 2-like | 2166 | Hyalella azteca 578/732 (79%) | MG910482 | Component of the 26S proteasome, a multiprotein complex involved in the ATP-dependent degradation of ubiquitinated proteins. |
26S Proteasome non-ATPase regulatory subunit 3-like | 1497 | Camponotus floridanus 330/504 (65%) | MG910483 | |
26S Proteasome non-ATPase regulatory subunit 4-like | 1320 | Fopius arisanus 258/440 (59%) | MG910484 | |
26S Protease regulatory subunit 7-like | 510 | Hyalella azteca 149/170 (88%) | MG910485 | |
Papain family cysteine protease | 798 | Tetrahymena thermophila SB210 138/269 (51%) | MH156429 | Papain-like cysteine proteinase: plays a role in inhibition of interferon-activated JAK/STAT signal transduction by mediating ubiquitination and subsequent proteasomal degradation of host KPNA1. |
Leucine-rich repeats and immunoglobulin-like domains protein 1 | 1428 | Hyalella azteca 228/454 (50%) | MG976882 | Acts as a negative feedback regulator of signaling by tyrosine receptor kinases through a mechanism that involves enhancement of receptor ubiquitination and accelerated intracellular degradation. |
Large proline-rich protein BAG6 | 1086 | Zootermopsis nevadensis 114/369 (31%) | MG976889 | BAG6 is also required for selective ubiquitin-mediated degradation of defective nascent chain polypeptides by the proteasome. In this context, it may participate in production of antigenic peptides and play a role in antigen presentation in the immune response |
Chitin binding-like protein | 591 | Fenneropenaeus chinensis 65/189 (34%) | MF688647 | Binds chitin but does not hydrolyze it; has no detectable protease or staphylolytic activity. |
NF-kB Transcription factor Relish | 1842 | Procambarus clarkii 580/581 (99%) | MG910473 | The endpoint of a series of signal transduction events initiated by a vast array of stimuli related to many biological processes such as inflammation, immunity, differentiation, cell growth, tumorigenesis, and apoptosis. |
Transforming growth factor-beta-induced protein ig-h3-like | 1470 | Cryptotermes secundus 143/492 (29%) | MG910476 | Plays a role in cell adhesion. May play a role in cell-collagen interactions. |
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Calderón-Rosete, G.; González-Barrios, J.A.; Lara-Lozano, M.; Piña-Leyva, C.; Rodríguez-Sosa, L. Transcriptional Identification of Related Proteins in the Immune System of the Crayfish Procambarus clarkii. High-Throughput 2018, 7, 26. https://doi.org/10.3390/ht7030026
Calderón-Rosete G, González-Barrios JA, Lara-Lozano M, Piña-Leyva C, Rodríguez-Sosa L. Transcriptional Identification of Related Proteins in the Immune System of the Crayfish Procambarus clarkii. High-Throughput. 2018; 7(3):26. https://doi.org/10.3390/ht7030026
Chicago/Turabian StyleCalderón-Rosete, Gabina, Juan Antonio González-Barrios, Manuel Lara-Lozano, Celia Piña-Leyva, and Leonardo Rodríguez-Sosa. 2018. "Transcriptional Identification of Related Proteins in the Immune System of the Crayfish Procambarus clarkii" High-Throughput 7, no. 3: 26. https://doi.org/10.3390/ht7030026