Skip to main content
Log in

Molecular and immune response characterizations of a novel Bax inhibitor-1 gene in pufferfish, Takifugu obscurus

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Apoptosis plays a crucial role in many biological processes, including development, cellular homeostasis, and immune responses. Bax inhibitor-1 (BI-1) is an anti-apoptotic protein that protects cells from endoplasmic reticulum stress-induced apoptosis. In this study, a BI-1 gene from the pufferfish Takifugu obscurus (Pf-BI-1) was identified and characterized. The full length of Pf-BI-1 cDNA was 1387 bp, including a 5′-UTR of 82 bp, a 3′-UTR of 591 bp containing a poly-(A) tail, and an open reading frame (ORF) of 714 bp that encodes a polypeptide of 237 amino acids. Pf-BI-1 was ubiquitously expressed in various tissues, with the highest expression levels in the blood, brain, and gill. The expression of Pf-BI-1 was up-regulated in a time-dependent manner after heat shock stress, ammonia stress, and bacterial challenge. Intracellular localization revealed that Pf-BI-1 was primarily localized in the cell cytoplasm. Furthermore, over-expression of Pf-BI-1 could active NF-кB reporter genes in HeLa cells. These results indicated that Pf-BI-1 may be involved in the apoptosis and immunity process against ambient stressors in pufferfish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adams JM, Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281:1322–1326

    Article  CAS  PubMed  Google Scholar 

  • Baichwal VR, Baeuerle PA (1997) Apoptosis: activate NF-κB or die? Curr Biol 7:94–96

    Article  Google Scholar 

  • Bailly-Maitre B, Fondevila C, Kaldas F, Droin N, Luciano F, Ricci JE (2006) Cytoprotective gene bi-1 is required for intrinsic protection from endoplasmic reticulum stress and ischemia-reperfusion injury. Proc Natl Acad Sci 103:2809–2814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D (1995) Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature 376:167–170

    Article  CAS  PubMed  Google Scholar 

  • Bentires-Alj M, Dejardin E, Viatour P, Lint CV, Froesch B, Reed JC, Merville MP, Bours V (2001) Inhibition of the NF-кB transcription factor increases Bax expression in cancer cell lines. Oncogene 20:2805–2813

    Article  CAS  PubMed  Google Scholar 

  • Chae HJ, Ke N, Kim HR, Chen S, Godzik A, Dickman M, Reed JC (2003) Evolutionarily conserved cytoprotection provided by Bax inhibitor-1 homologs from animals, plants, and yeast. Gene 24:101–113

    Article  Google Scholar 

  • Chae HJ, Kim HR, Xu C, Bailly-Maitre B, Krajewska M, Krajewski S (2004) BI-1 regulates an apoptosis pathway linked to endoplasmic reticulum stress. Mol Cell 15:355–366

    Article  CAS  PubMed  Google Scholar 

  • Cheng CH, Yang FF, Liao SA, Miao YT, Ye CX, Wang AL (2015) Effect of acute ammonia exposure on expression of GH/IGF axis genes GHR1, GHR2 and IGF-1 in pufferfish (Takifugu obscurus). Fish Physiol Biochem 41:495–507

    Article  CAS  PubMed  Google Scholar 

  • Du ZQ, Lan JF, Weng YD, Zhao XF, Wang JX (2013) BAX inhibitor-1 silencing suppresses white spot syndrome virus replication in red swamp crayfish, Procambarus clarkia. Fish Shellfish Immunol 35:46–53

    Article  PubMed  Google Scholar 

  • Er E, Oliver L, Cartron PF, Juin P, Manon S, Vallette FM (2006) Mitochondria as the target of the pro-apoptotic protein Bax. Biochim Biophys Acta 1757:1301–1311

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Fernández JC (2014) Functions of the C-terminal domains of apoptosis-related proteins of the Bcl-2 family. Chem Phys Lipids 183:77–90

    Article  PubMed  Google Scholar 

  • Halliwell B (1999) Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free Radic Res 31:261–272

    Article  CAS  PubMed  Google Scholar 

  • Henke N, Lisak DA, Schneider L, Habicht J, Pergande M, Methner A (2011) The ancient cell death suppressor BAX inhibitor-1. Cell Calcium 50:251–260

    Article  CAS  PubMed  Google Scholar 

  • Hückelhoven R (2004) BAX inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 9:299–307

    Article  PubMed  Google Scholar 

  • Isbat M, Zeba N, Kim SR, Hong CB (2009) A BAX inhibitor-1 gene in Capsicum annuum is induced under various abiotic stresses and endows multi-tolerance in transgenic tobacco. J Plant Physiol 166:1685–1693

    Article  CAS  PubMed  Google Scholar 

  • Jeon K, Lim H, Kim JH, Han D, Lee ER, Yang GM (2012) Bax inhibitor-1 enhances survival and neuronal differentiation of embryonic stem cells via differential regulation of mitogen-activated protein kinases activities. Biochim Biophys Acta 1823:2190–2200

    Article  CAS  PubMed  Google Scholar 

  • Kim HR, Lee GH, Ha KC, Ahn T, Moon JY, Lee BJ (2008) Bax inhibitor-1 is a pH-dependent regulator of Ca2+ channel activity in the endoplasmic reticulum. J Biol Chem 283:15946–15955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirkin V, Joos S, Zörnig M (2004) The role of Bcl-2 family members in tumorigenesis. Biochim Biophys Acta 1644:229–249

    Article  CAS  PubMed  Google Scholar 

  • Lee GH, Kim HK, Chae SW, Kim DS, Ha KC, Cuddy M (2007) Bax inhibitor-1 regulates endoplasmic reticulum stress-associated reactive oxygen species and heme oxygenase-1 expression. J Biol Chem 282:18–28

    Google Scholar 

  • Lee GH, Kim HR, Chae HJ (2012) Bax inhibitor-1 regulates the expression of P450 2E1 through enhanced lysosome activity. Int J Biochem Cell Biol 44:600–611

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo SW, Xie FX, Liu Y, Wang WN (2015) Characterization and expression analysis of Calmodulin (CaM) in orange-spotted grouper (Epinephelus coioides) in response to Vibrio alginolyticus challenge. Ecotoxicology 10:645–651

    Google Scholar 

  • Meier P, Finch A, Evan G (2000) Apoptosis in development. Nature 407:796–801

    Article  CAS  PubMed  Google Scholar 

  • Oshima R, Yoshinaga K, Ihara-Ohori Y, Fukuda R, Ohta A, Uchimiya H, Kawai-Yamada M (2007) The Bax lnhibitor-1 needs a functional electron transport chain for cell death suppression. FEBS Lett 581:4627–4632

    Article  CAS  PubMed  Google Scholar 

  • Qu FF, Xiang ZM, Wang FX, Zhang Y, Tong Y, Li J, Zhang YH, Yu ZN (2015) A novel molluscan Fos gene with immune defense function identified in the Hong Kong oyster, Crassostrea hongkongensis. Dev Comp Immunol 51:194–201

    Article  CAS  PubMed  Google Scholar 

  • Solem ST, Jørgensen JB, Robertsen B (1995) Stimulation of respiratory burst and phagocytic activity in Atlantic salmon (Salmo salar L.) macrophages by lipopolysaccharide. Fish Shellfish Immunol 5:475–491

    Article  Google Scholar 

  • Xiang YL, Yang CC, Ke YZ, Mei HZ, Hai QL, Hsiang FK, Xin Z (2010) Overexpression of Bax inhibitor-1 (BI-1) induces cell transformation in NIH3T3 cells. Cell Biol Int 34:1099–1104

    Article  Google Scholar 

  • Xu Q, Reed JC (1998) Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell 1:337–346

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Kwon KB, Park JW, Chae HJ, Park BH (2009) Bax inhibitor-1 overexpression reduces the suppressive effect of calcium mobilizing agent on adipogenesis. Int J Biochem Cell Biol 41:1739–1745

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Xiao JF, Yang YH, Bi CW, Qing L, Tan WZ (2015) Ss-Bi1encodes a putative BAX inhibitor-1 protein that is required for full virulence of Sclerotinia sclerotiorum. Physiol Mol Plant Pathol 90:115–122

    Article  CAS  Google Scholar 

  • Yue Y, Zhou Z, Wang LL, Wang MQ, Song SL (2014) A conserved zinc finger transcription factor GATA involving in the hemocyte production of scallopchlamys farreri. Fish Shellfish Immunol 39:125–135

    Article  CAS  PubMed  Google Scholar 

  • Zong WX, Edelstein LC, Chen C, Bash J, Gélinas C (1999) The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNFα-induced apoptosis. Genes Dev 13:382–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by Hainan Applied Technology Research and Development and Demonstration Projects (ZDXM2015025), the China Postdoctoral Science Foundation (2012M511829), the Science and Technology Innovation of Higher School Guangdong Province (cxzd114). Special Funds for Fish Diseases of Guangdong province (2015-352 and 2016-302), Marine Fisheries Technology and Industry Development Special Projects of Guangdong Province (A201501B14), Marine Fisheries Science and Technology Extension Projectsof Guangdong Province (B201601-11), Science and technology Projects of Guangdong Province (2014B040404057).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to An-Li Wang or Zhi-Xun Guo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, CH., Luo, SW., Wang, AL. et al. Molecular and immune response characterizations of a novel Bax inhibitor-1 gene in pufferfish, Takifugu obscurus . Fish Physiol Biochem 43, 965–975 (2017). https://doi.org/10.1007/s10695-016-0337-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0337-9

Keywords

Navigation