DOI QR코드

DOI QR Code

Molecular cloning of metal-responsive transcription factor-1 (MTF-1) and transcriptional responses to metal and heat stresses in Pacific abalone, Haliotis discus hannai

  • Lee, Sang Yoon (Department of Marine Bio-Materials & Aquaculture, Pukyong National University) ;
  • Nam, Yoon Kwon (Department of Marine Bio-Materials & Aquaculture, Pukyong National University)
  • Received : 2017.01.23
  • Accepted : 2017.06.05
  • Published : 2017.07.31

Abstract

Background: Metal-responsive transcription factor-1 (MTF-1) is a key transcriptional regulator playing crucial roles in metal homeostasis and cellular adaptation to diverse oxidative stresses. In order to understand cellular pathways associated with metal regulation and stress responses in Pacific abalone (Haliotis discus hannai), this study was aimed to isolate the genetic determinant of abalone MTF-1 and to examine its expression characteristics under basal and experimentally stimulated conditions. Results: The abalone MTF-1 shared conserved features in zinc-finger DNA binding domain with its orthologs; however, it represented a non-conservative shape in presumed transactivation domain region with the lack of typical motifs for nuclear export signal (NES) and Cys-cluster. Abalone MTF-1 promoter exhibited various transcription factor binding motifs that would be potentially related with metal regulation, stress responses, and development. The highest messenger RNA (mRNA) expression level of MTF-1 was observed in the testes, and MTF-1 transcripts were detected during the entire period of embryonic and early ontogenic developments. Abalone MTF-1 was found to be Cd inducible and highly modulated by heat shock treatment. Conclusion: Abalone MTF-1 possesses a non-consensus structure of activation domains and represents distinct features for its activation mechanism in response to metal overload and heat stress. The activation mechanism of abalone MTF-1 might include both indirect zinc sensing and direct de novo synthesis of transcripts. Taken together, results from this study could be a useful basis for future researches on stress physiology of this abalone species, particularly with regard to heavy metal detoxification and thermal adaptation.

Keywords

References

  1. Attig H, Kamel N, Sforzini S, Dagnino A, Jamel J, Boussetta H, Viarengo A, Banni M. Effects of thermal stress and nickel exposure on biomarkers responses in Mytilus galloprovincialis (Lam). Mar Environ Res. 2014;94:65-71. https://doi.org/10.1016/j.marenvres.2013.12.006
  2. Auf der Maur A, Belser T, Wang Y, Gunes C, Lichtlen P, Georgiev O, Schaffner W. Characterization of the mouse gene for the heavy metal-responsive transcription factor MTF-1. Cell Stress Chaperones. 2000;5:196-206. https://doi.org/10.1379/1466-1268(2000)005<0196:COTMGF>2.0.CO;2
  3. Banni M, Hajer A, Sforzini S, Oliveri C, Boussetta H, Viarengo A. Transcriptional expression levels and biochemical markers of oxidative stress in Mytilus galloprovincialis exposed to nickel and heat stress. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 2014;160:23-9. https://doi.org/10.1016/j.cbpc.2013.11.005
  4. Bi Y, Lin GX, Millecchia L, Ma Q. Superinduction of metallothionein I by inhibition of protein synthesis: role of a labile repressor in MTF-1 mediated gene transcription. J Biochem Mol Toxicol. 2006;20:57-68. https://doi.org/10.1002/jbt.20116
  5. Bittel DC, Smirnova IV, Andrews GK. Functional heterogeneity in the zinc fingers of metalloregulatory protein metal response element-binding transcription factor-1. J Biol Chem. 2000;275:37194-201. https://doi.org/10.1074/jbc.M003863200
  6. Chen X, Chu M, Giedroc DP. MRE-Binding transcription factor-1: weak zinc-binding finger domains 5 and 6 modulate the structure, affinity, and specificity of the metal-response element complex. Biochemistry. 1999;38:12915-25. https://doi.org/10.1021/bi9913000
  7. Chen W-Y, John JAC, Lin C-H, Chang C-Y. Molecular cloning and developmental expression of zinc finger transcription factor MTF-1 gene in zebrafish, Danio rerio. Biochem Biophys Res Commun. 2002;291:798-805. https://doi.org/10.1006/bbrc.2002.6517
  8. Chen W, John JAC, Lin C, Chang C. Expression pattern of metallothionein, MTF-1 nuclear translocation, and its dna-binding activity in zebrafish (Danio rerio) induced by zinc and cadmium. Environ Toxicol Chem. 2007;26:110-7. https://doi.org/10.1897/06-153R.1
  9. Cheuk WK, Chan PC-Y, Chan KM. Cytotoxicities and induction of metallothionein (MT) and metal regulatory element (MRE)-binding transcription factor-1 (MTF-1) messenger RNA levels in the zebrafish (Danio rerio) ZFL and SJD cell lines after exposure to various metal ions. Aquat Toxicol. 2008;89:103-12. https://doi.org/10.1016/j.aquatox.2008.06.006
  10. Cheung AP-L, Au CY-M, Chan WW-L, Chan KM. Characterization and localization of metal-responsive-element-binding transcription factors from tilapia. Aquat Toxicol. 2010;99:42-55. https://doi.org/10.1016/j.aquatox.2010.03.017
  11. Cho YS, Lee SY, Bang IC, Kim DS, Nam YK. Genomic organization and mRNA expression of manganese superoxide dismutase (Mn-SOD) from Hemibarbus mylodon (Teleostei, Cypriniformes). Fish Shellfish Immunol. 2009;27:571-6. https://doi.org/10.1016/j.fsi.2009.07.003
  12. De SK, Enders GC, Andrews GK. High levels of metallothionein messenger RNAs in male germ cells of the adult mouse. Mol Endocrinol. 1991;5:628-36. https://doi.org/10.1210/mend-5-5-628
  13. Dube A, Harrisson J-F, Saint-Gelais G, Seguin C. Hypoxia acts through multiple signaling pathways to induce metallothionein transactivation by the metal-responsive transcription factor-1 (MTF-1). Biochem Cell Biol. 2011;89:562-77. https://doi.org/10.1139/o11-063
  14. Ferencz A, Hermesz E. Identification and characterization of two mtf-1 genes in common carp. Comp Biochem Physiol C Toxicol Pharmacol. 2008;148:238-43. https://doi.org/10.1016/j.cbpc.2008.06.001
  15. Ferencz A, Hermesz E. Identification of a splice variant of the metal-responsive transcription factor MTF-1 in common carp. Comp Biochem Physiol C Toxicol Pharmacol. 2009;150:113-7. https://doi.org/10.1016/j.cbpc.2009.03.006
  16. Giedroc DP, Chen X, Apuy JL. Metal response element (MRE)-binding transcription factor-1 (MTF-1): structure, function, and regulation. Antioxid Redox Signal. 2001;3:577-96. https://doi.org/10.1089/15230860152542943
  17. Gunes C, Heuchel R, Georgiev O, Muller K-H, Lichtlen P, Bluthmann H, Marino S, Aguzzi A, Schaffner W. Embryonic lethality and liver degeneration in mice lacking the metal-responsive transcriptional activator MTF-1. EMBO J. 1998;17:2846-54. https://doi.org/10.1093/emboj/17.10.2846
  18. Gunther V, Lindert U, Schaffner W. The taste of heavy metals: Gene regulation by MTF-1. Biochim Biophys Acta, Mol Cell Res. 2012a;1823:1416-25. https://doi.org/10.1016/j.bbamcr.2012.01.005
  19. Gunther V, Davis AM, Georgiev O, Schaffner W. A conserved cysteine cluster, essential for transcriptional activity, mediates homodimerization of human metal-responsive transcription factor-1 (MTF-1). Biochim Biophys Acta, Mol Cell Res. 2012b;1823:476-83. https://doi.org/10.1016/j.bbamcr.2011.10.006
  20. Hahn ME, Karchner SI, Evans BR, Franks DG, Merson RR, Lapseritis JM. Unexpected diversity of aryl hydrocarbon receptors in non-mammalian vertebrates: insights from comparative genomics. J Exp Zool A Ecol Genet Physiol. 2006;305:693-706.
  21. Jackson DP, Joshi AD, Elferink CJ. Ah receptor pathway intricacies; signaling through diverse protein partners and DNA-motifs. Toxicol Res. 2015;4:1143-58. https://doi.org/10.1039/C4TX00236A
  22. Jarque S, Prats E, Olivares A, Casado M, Ramon M, Pina B. Seasonal variations of gene expression biomarkers in Mytilus galloprovincialis cultured populations: temperature, oxidative stress and reproductive cycle as major modulators. Sci Total Environ. 2014;499:363-72. https://doi.org/10.1016/j.scitotenv.2014.08.064
  23. Jenny MJ, Warr GW, Ringwood AH, Baltzegar DA, Chapman RW. Regulation of metallothionein genes in the American oyster (Crassostrea virginica): ontogeny and differential expression in response to different stressors. Gene. 2006;379:156-65. https://doi.org/10.1016/j.gene.2006.05.004
  24. Kang J, Lee YG, Jeong DU, Lee JS, Choi YH, Shin YK. Effect of abalone farming on sediment geochemistry in the Shallow Sea near Wando, South Korea. Ocean Sci J. 2015;50:669-82. https://doi.org/10.1007/s12601-015-0061-x
  25. Kim K-Y, Lee SY, Cho YS, Bang IC, Kim KH, Kim DS, Nam YK. Molecular characterization and mRNA expression during metal exposure and thermal stress of copper/zinc-and manganese-superoxide dismutases in disk abalone, Haliotis discus discus. Fish Shellfish Immunol. 2007;23:1043-59. https://doi.org/10.1016/j.fsi.2007.04.010
  26. Laity JH, Andrews GK. Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch Biochem Biophys. 2007;463:201-10. https://doi.org/10.1016/j.abb.2007.03.019
  27. Lee SY, Nam YK. Transcriptional responses of metallothionein gene to different stress factors in Pacific abalone (Haliotis discus hannai). Fish Shellfish Immunol. 2016a;58:530-41. https://doi.org/10.1016/j.fsi.2016.09.030
  28. Lee SY, Nam YK. Evaluation of reference genes for RT-qPCR study in abalone Haliotis discus hannai during heavy metal overload stress. Fish Aquat Sci. 2016b;19:21. https://doi.org/10.1186/s41240-016-0022-z
  29. Li Y, Kimura T, Laity JH, Andrews GK. The zinc-sensing mechanism of mouse MTF-1 involves linker peptides between the zinc fingers. Mol Cell Biol. 2006;26:5580-7. https://doi.org/10.1128/MCB.00471-06
  30. Li Y, Kimura T, Huyck RW, Laity JH, Andrews GK. Zinc-induced formation of a coactivator complex containing the zinc-sensing transcription factor MTF-1, p300/CBP, and Sp1. Mol Cell Biol. 2008;28:4275-84. https://doi.org/10.1128/MCB.00369-08
  31. Lichtlen P, Schaffner W. Putting its fingers on stressful situations: the heavy metal-regulatory transcription factor MTF-1. BioEssays. 2001;23:1010-7. https://doi.org/10.1002/bies.1146
  32. Lichtlen P, Wang Y, Belser T, Georgiev O, Certa U, Sack R, Schaffner W. Target gene search for the metal-responsive transcription factor MTF-1. Nucleic Acids Res. 2001;29:1514-23. https://doi.org/10.1093/nar/29.7.1514
  33. Mao H, Wang D-H, Yang W-X. The involvement of metallothionein in the development of aquatic invertebrate. Aquat Toxicol. 2012;110:208-13.
  34. Meng J, Zhang L, Li L, Li C, Wang T, Zhang G. Transcription factor CgMTF-1 regulates CgZnT1 and CgMT expression in Pacific oyster (Crassostrea gigas) under zinc stress. Aquat Toxicol. 2015;165:179-88. https://doi.org/10.1016/j.aquatox.2015.05.023
  35. Negri A, Oliveri C, Sforzini S, Mignione F, Viarengo A, Banni M. Transcriptional response of the mussel Mytilus galloprovincialis (Lam.) following exposure to heat stress and copper. PLoS One. 2013;8:e66802. https://doi.org/10.1371/journal.pone.0066802
  36. O'Shields B, McArthur AG, Holowiecki A, Kamper M, Tapley J, Jenny MJ. Inhibition of endogenous MTF-1 signaling in zebrafish embryos identifies novel roles for MTF-1 in development. Biochim Biophys Acta, Mol Cell Res. 2014;1843:1818-33. https://doi.org/10.1016/j.bbamcr.2014.04.015
  37. Park C-J, Kim SY. Abalone aquaculture in Korea. J Shellfish Res. 2013;32:17-9. https://doi.org/10.2983/035.032.0104
  38. Qiu J, Liu Y, Yu M, Pang Z, Chen W, Xu Z. Identification and functional characterization of MRE-binding transcription factor (MTF) in Crassostrea gigas and its conserved role in metal-induced response. Mol Biol Rep. 2013;40:3321-31. https://doi.org/10.1007/s11033-012-2407-0
  39. Roesijadi G, Hansen KM, Unger ME. Cadmium-induced metallothionein expression during embryonic and early larval development of the mollusc Crassostrea virginica. Toxicol Appl Pharmacol. 1996;140:356-63. https://doi.org/10.1006/taap.1996.0231
  40. Saydam N, Georgiev O, Nakano MY, Greber UF, Schaffner W. Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals. J Biol Chem. 2001;276:25487-95. https://doi.org/10.1074/jbc.M009154200
  41. Saydam N, Steiner F, Georgiev O, Schaffner W. Heat and heavy metal stress synergize to mediate transcriptional hyperactivation by metal-responsive transcription factor MTF-1. J Biol Chem. 2003;278:31879-83. https://doi.org/10.1074/jbc.M302138200
  42. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101-8. https://doi.org/10.1038/nprot.2008.73
  43. Smirnova IV, Bittel DC, Ravindra R, Jiang H, Andrews GK. Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J Biol Chem. 2000;275:9377-84. https://doi.org/10.1074/jbc.275.13.9377
  44. Stoytcheva ZR, Vladimirov V, Douet V, Stoychev I, Berry MJ. Metal transcription factor-1 regulation via MREs in the transcribed regions of selenoprotein H and other metal-responsive genes. Biochim Biophys Acta, Gen Subj. 2010;1800:416-24. https://doi.org/10.1016/j.bbagen.2009.11.003
  45. Uenishi R, Gong P, Suzuki K, Koizumi S. Cross talk of heat shock and heavy metal regulatory pathways. Biochem Biophys Res Commun. 2006;341:1072-7. https://doi.org/10.1016/j.bbrc.2006.01.066
  46. Wang Y, Wimmer U, Lichtlen P, Inderbitzin D, Stieger B, Meier PJ, Hunziker L, Stallmach T, Forrer R, Rulicke T, Georgiev O, Schaffner W. Metal-responsive transcription factor-1 (MTF-1) is essential for embryonic liver development and heavy metal detoxification in the adult liver. FASEB J. 2004;18:1071-9. https://doi.org/10.1096/fj.03-1282com
  47. Zhang B, Egli D, Georgiev O, Schaffner W. The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Mol Cell Biol. 2001;21:4505-14. https://doi.org/10.1128/MCB.21.14.4505-4514.2001

Cited by

  1. Characterization of testis-specific serine/threonine kinase 1-like (TSSK1-like) gene and expression patterns in diploid and triploid Pacific abalone (Haliotis discus hannai; Gastropoda; Mollusca) male vol.14, pp.12, 2017, https://doi.org/10.1371/journal.pone.0226022