Genomic and phylogenetic analysis of choriolysins, and biological activity of hatching liquid in the flatfish Senegalese sole

English version

Autoři: Carlos Carballo ^aff001; Evangelia G. Chronopoulou ^aff002; Sophia Letsiou ^aff003; Eleni Spanidi ^aff003; Konstantinos Gardikis ^aff003; Nikolaos E. Labrou ^aff002; Manuel Manchado ^aff001
Působiště autorů: IFAPA Centro El Toruño, Junta de Andalucía, El Puerto de Santa María, Spain ^aff001; Laboratory of Enzyme Technology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, Athens, Greece ^aff002; Research and Development Department, APIVITA S.A., Athens, Greece ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225666

Souhrn

The hatching enzymes or choriolysins are key proteases in fish life cycle controlling the release of larvae to surrounding environment that have been suggested as target for novel biotechnological uses. Due to the large amounts of eggs released by the flatfish Solea senegalensis, during the spawning season, the hatching liquid properties and choriolysin-encoding genes were investigated in this species. A genomic analysis identified four putative genes referred to as SseHCEa, SseHCEb, SseLCE and SseHE. The phylogenetic analysis classified these paralogs into two clades, the clade I containing SseHCE paralogs and the clade II containing two well-supported subclades named as HE and LCE. The two SseHCE paralogs were intron-less and both genes were tandemly arrayed very close in the genome. The synteny and gene rearrangement identified in the flatfish lineage indicated that the duplication of these two paralogs occurred recently and they are under divergent evolution. The genes SseHE and SseLCE were structured in 8 exons and 7 introns and the synteny was conserved in teleosts. Expression studies confirmed that the four genes were expressed in the hatching gland cells and they migrate co-ordinately from the head to around the yolk sac close to the hatch with specific temporal and intensity expression profiles. Although the mRNA levels of the four genes peaked in the hours previous to larval hatching, the SseHCE and SseLCE paralogs kept a longer expression than SseHE after hatching. These expression patterns were consistent even when larvae were incubated at different temperatures that modified hatching times. The analysis of hatching-liquid using SDS-PAGE and zymography analyses of hatching liquid identified a major band of expected choriolysin size. The optimal pH for protease activity was 8.5 and inhibition assays using EDTA demonstrated that most of the activity in the hatching liquid was due to metalloproteases with Ca²⁺ ions acting as the most effective metal to restore the activity. All these data provide new clues about the choriolysin evolution and function in flatfish with impact in the aquaculture and the blue cosmetic industry.

Klíčová slova:

Embryos – Enzyme structure – Gene expression – Introns – Larvae – Phylogenetic analysis – Proteases – Structural genomics

Zdroje

1. Semenova SA, Rudenskaia GN. The astacin family of metalloproteinases. Biomed Khim. 2008;54(5):531–54. doi: 10.1134/S199075080901003X 19105396.

2. Bond JS. Proteases: History, discovery, and roles in health and disease. J Biol Chem. 2019;294(5):1643–51. doi: 10.1074/jbc.TM118.004156 30710012; PubMed Central PMCID: PMC6364759.

3. Bond JS, Beynon RJ. The astacin family of metalloendopeptidases. Protein Sci. 1995;4(7):1247–61. doi: 10.1002/pro.5560040701 7670368; PubMed Central PMCID: PMC2143163.

4. Sano K, Kawaguchi M, Watanabe S, Yasumasu S. Neofunctionalization of a duplicate hatching enzyme gene during the evolution of teleost fishes. BMC Evol Biol. 2014;14:221. doi: 10.1186/s12862-014-0221-0 25326699; PubMed Central PMCID: PMC4219043.

5. Kawaguchi M, Hiroi J, Miya M, Nishida M, Iuchi I, Yasumasu S. Intron-loss evolution of hatching enzyme genes in Teleostei. BMC Evol Biol. 2010;10:260. doi: 10.1186/1471-2148-10-260 20796321; PubMed Central PMCID: PMC2939575.

6. Kawaguchi M, Takahashi H, Takehana Y, Naruse K, Nishida M, Yasumasu S. Sub-functionalization of duplicated genes in the evolution of nine-spined stickleback hatching enzyme. J Exp Zool B Mol Dev Evol. 2013;320(3):140–50. doi: 10.1002/jez.b.22490 23554322.

7. Nagasawa T, Kawaguchi M, Yano T, Isoyama S, Yasumasu S, Okabe M. Translocation of promoter-conserved hatching enzyme genes with intron-loss provides a new insight in the role of retrocopy during teleostean evolution. Sci Rep. 2019;9(1):2448. doi: 10.1038/s41598-019-38693-6 30792427; PubMed Central PMCID: PMC6385490.

8. Kawaguchi M, Sano K, Yoshizaki N, Shimizu D, Fujinami Y, Noda T, et al. Comparison of hatching mode in pelagic and demersal eggs of two closely related species in the order pleuronectiformes. Zoolog Sci. 2014;31(11):709–15. doi: 10.2108/zs140018 25366152

9. Chakraborty T, Mohapatra S, Tobayama M, Ohta K, Ryu YW, Kazeto Y, et al. Hatching enzymes disrupt aberrant gonadal degeneration by the autophagy/apoptosis cell fate decision. Sci Rep. 2017;7(1):3183. doi: 10.1038/s41598-017-03314-7 28600501; PubMed Central PMCID: PMC5466654.

10. Inohaya K, Yasumasu S, Araki K, Naruse K, Yamazaki K, Yasumasu I, et al. Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common [corrected]. Dev Growth Differ. 1997;39(2):191–7. doi: 10.1046/j.1440-169x.1997.t01-1-00007.x 9108332.

11. Kawaguchi M, Fujita H, Yoshizaki N, Hiroi J, Okouchi H, Nagakura Y, et al. Different hatching strategies in embryos of two species, pacific herring Clupea pallasii and Japanese anchovy Engraulis japonicus, that belong to the same order Clupeiformes, and their environmental adaptation. J Exp Zool B Mol Dev Evol. 2009;312(2):95–107. doi: 10.1002/jez.b.21247 19025965.

12. Helvik JV, Oppen-Berntsen DO, Walther BT. The hatching mechanism in Atlantic halibut (Hippoglossus hippoglossus). Int J Dev Biol. 1991;35(1):9–16. 1868003.

13. Manchado M, Planas JV, Cousin X, Rebordinos L, Claros MG. Current status in other finfish species: Description of current genomic resources for the gilthead seabream (Sparus aurata) and soles (Solea senegalensis and Solea solea). In: MacKenzie SA, Jentoft S, editors. Genomics in aquaculture. Cambridge, MA, USA: Elsevier; 2016. p. 195–221.

14. Cerda J, Manchado M. Advances in genomics for flatfish aquaculture. Genes Nutr. 2013;8(1):5–17. doi: 10.1007/s12263-012-0312-8 22903900; PubMed Central PMCID: PMC3534989.

15. Anguís V, Cañavate JP. Spawning of captive Senegal sole (Solea senegalensis) under a naturally fluctuating temperature regime. Aquaculture. 2005;243:133–45. doi: 10.1016/j.aquaculture.2004.09.026

16. Carballo C, Firmino J, Anjos L, Santos S, Power DM, Manchado M. Short- and long-term effects on growth and expression patterns in response to incubation temperatures in Senegalese sole. Aquaculture. 2018;495:222–31. doi: 10.1016/j.aquaculture.2018.05.043

17. Campos C, Valente LM, Conceiçao LE, Engrola S, Sousa V, Rocha E, et al. Incubation temperature induces changes in muscle cellularity and gene expression in Senegalese sole (Solea senegalensis). Gene. 2013;516(2):209–17. doi: 10.1016/j.gene.2012.12.074 23291415.

18. Campos C, Valente L, Conceiçao L, Engrola S, Fernandes J. Temperature affects methylation of the myogenin putative promoter, its expression and muscle cellularity in Senegalese sole larvae. Epigenetics. 2013;8(4). doi: 10.4161/epi.24178 23538611.

19. Alparslan L, Sekeroglu N, Kijjoa N. The potential of marine resources in cosmetics. Curr Pers MAPs. 2018;2:53–66.

20. Roman-Padilla J, Rodriguez-Rua A, Claros MG, Hachero-Cruzado I, Manchado M. Genomic characterization and expression analysis of four apolipoprotein A-IV paralogs in Senegalese sole (Solea senegalensis Kaup). Comp Biochem Physiol B Biochem Mol Biol. 2016;191:84–98. doi: 10.1016/j.cbpb.2015.09.010 26453798.

21. Firmino J, Carballo C, Armesto P, Campinho MA, Power DM, Manchado M. Phylogeny, expression patterns and regulation of DNA Methyltransferases in early development of the flatfish, Solea senegalensis. BMC Dev Biol. 2017;17(1):11. doi: 10.1186/s12861-017-0154-0 28716037; PubMed Central PMCID: PMC5513168.

22. Benzekri H, Armesto P, Cousin X, Rovira M, Crespo D, Merlo MA, et al. De novo assembly, characterization and functional annotation of Senegalese sole (Solea senegalensis) and common sole (Solea solea) transcriptomes: integration in a database and design of a microarray. BMC Genomics. 2014;15:952. doi: 10.1186/1471-2164-15-952 25366320; PubMed Central PMCID: PMC4232633.

23. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. doi: 10.1093/molbev/msu300 25371430; PubMed Central PMCID: PMC4271533.

24. Minh BQ, Nguyen MA, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 2013;30(5):1188–95. doi: 10.1093/molbev/mst024 23418397; PubMed Central PMCID: PMC3670741.

25. Campinho MA, Silva N, Martins GG, Anjos L, Florindo C, Roman-Padilla J, et al. A thyroid hormone regulated asymmetric responsive centre is correlated with eye migration during flatfish metamorphosis. Sci Rep. 2018;8(1):12267. doi: 10.1038/s41598-018-29957-8 30115956; PubMed Central PMCID: PMC6095868.

26. Boglino A, Ponce M, Cousin X, Gisbert E, Manchado M. Transcriptional regulation of genes involved in retinoic acid metabolism in Senegalese sole larvae. Comp Biochem Physiol B Biochem Mol Biol. 2017;203:35–46. doi: 10.1016/j.cbpb.2016.08.007 27619487.

27. Infante C, Matsuoka MP, Asensio E, Cañavate JP, Reith M, Manchado M. Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol Biol. 2008;9:28. doi: 10.1186/1471-2199-9-28 18325098; PubMed Central PMCID: PMC2275743.

28. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54. doi: 10.1006/abio.1976.9999 942051.

29. Charney J, Tomarelli RM. A colorimetric method for the determination of the proteolytic activity of duodenal juice. J Biol Chem. 1947;171(2):501–5. 20272088.

30. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–5. doi: 10.1038/227680a0 5432063.

31. Fernandez-Resa P, Mira E, Quesada AR. Enhanced detection of casein zymography of matrix metalloproteinases. Anal Biochem. 1995;224(1):434–5. doi: 10.1006/abio.1995.1063 7710105.

32. Carballo C, Chronopoulou EG, Letsiou S, Maya C, Labrou NE, Infante C, et al. Antioxidant capacity and immunomodulatory effects of a chrysolaminarin-enriched extract in Senegalese sole. Fish Shellfish Immunol. 2018;82:1–8. doi: 10.1016/j.fsi.2018.07.052 30064015.

33. Letsiou S, Kalliampakou K, Gardikis K, Mantecon L, Infante C, Chatzikonstantinou M, et al. Skin protective effects of Nannochloropsis gaditana extract on H2O2-stressed human dermal fibroblasts. Front Mar Sci. 2017;4:221. doi: 10.3389/fmars.2017.00221

34. Stahlberg A, Aman P, Ridell B, Mostad P, Kubista M. Quantitative real-time PCR method for detection of B-lymphocyte monoclonality by comparison of kappa and lambda immunoglobulin light chain expression. Clin Chem. 2003;49(1):51–9. doi: 10.1373/49.1.51 12507960.

35. Kawaguchi M, Yasumasu S, Hiroi J, Naruse K, Suzuki T, Iuchi I. Analysis of the exon-intron structures of fish, amphibian, bird and mammalian hatching enzyme genes, with special reference to the intron loss evolution of hatching enzyme genes in Teleostei. Gene. 2007;392(1–2):77–88. doi: 10.1016/j.gene.2006.11.012 17222522.

36. Kawaguchi M, Yasumasu S, Hiroi J, Naruse K, Inoue M, Iuchi I. Evolution of teleostean hatching enzyme genes and their paralogous genes. Dev Genes Evol. 2006;216(12):769–84. doi: 10.1007/s00427-006-0104-5 17016731.

37. Nagasawa T, Kawaguchi M, Sano K, Yasumasu S. Sturgeon hatching enzyme and the mechanism of egg envelope digestion: Insight into changes in the mechanism of egg envelope digestion during the evolution of ray-finned fish. J Exp Zool B Mol Dev Evol. 2015;324(8):720–32. doi: 10.1002/jez.b.22660 26514945.

38. Ferraresso S, Bonaldo A, Parma L, Cinotti S, Massi P, Bargelloni L, et al. Exploring the larval transcriptome of the common sole (Solea solea L.). BMC Genomics. 2013;14:315. doi: 10.1186/1471-2164-14-315 23663263; PubMed Central PMCID: PMC3659078.

39. DiMichele L, Taylor M, Singleton R. The hatching enzyme of Fundulus heteroclitus. J Exp Zool. 1981;216:133–40.

40. Yasumasu S, Iuchi I, Yamagami K. Purification and partial characterization of high choriolytic enzyme (HCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J Biochem. 1989;105(2):204–11. doi: 10.1093/oxfordjournals.jbchem.a122640 2656664.

41. Yasumasu S, Iuchi I, Yamagami K. Isolation and some properties of low choriolytic enzyme (LCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J Biochem. 1989;105(2):212–8. doi: 10.1093/oxfordjournals.jbchem.a122641 2656665.

42. Shi ZP, Fan TJ, Cong RS, Wang XF, Sun WJ, Yang LL. Purification and characterization of hatching enzyme from flounder Paralichthys olivaceus. Fish Physiol Biochem. 2006;32(1):35–42. doi: 10.1007/s10695-005-5250-6 20035476.

43. Lun HM, Mak CH, Ko RC. Characterization and cloning of metallo-proteinase in the excretory/secretory products of the infective-stage larva of Trichinella spiralis. Parasitol Res. 2003;90(1):27–37. doi: 10.1007/s00436-002-0815-0 12743801.

Genomic and phylogenetic analysis of choriolysins, and biological activity of hatching liquid in the flatfish Senegalese sole

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií