Skip to main content
Log in

Ecl1 is a zinc-binding protein involved in the zinc-limitation-dependent extension of chronological life span in fission yeast

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Overexpression of Ecl1-family genes (ecl1 +, ecl2 +, and ecl3 +) results in the extension of the chronological life span in Schizosaccharomyces pombe. However, the mechanism for this extension has not been defined clearly. Ecl1-family proteins consist of approximately 80 amino acids, and four cysteine residues are conserved in their N-terminal domains. This study focused on the Ecl1 protein, mutating its cysteine residues sequentially to confirm their importance. As a result, all mutated Ecl1 proteins nearly lost the function to extend the chronological life span, suggesting that these four cysteine residues are essential for the Ecl1 protein. Utilizing ICP-AES (inductively coupled plasma atomic emission spectroscopy) analysis, we found that wild-type Ecl1 proteins contain zinc, while cysteine-mutated Ecl1 proteins do not. We also analyzed the effect of environmental zinc on the chronological life span. We found that zinc limitation extends the chronological life span, and this extension depends on the Ecl1-family proteins.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andreini C, Bertini I (2012) A bioinformatics view of zinc enzymes. J Inorg Biochem 111:150–156

    Article  CAS  PubMed  Google Scholar 

  • Azuma K, Ohtsuka H, Mita S, Murakami H, Aiba H (2009) Identification and characterization of an Ecl1-family gene in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 73:2787–2789

    Article  CAS  PubMed  Google Scholar 

  • Boch A, Trampczynska A, Simm C, Taudte N, Krämer U, Clemens S (2008) Loss of Zhf and the tightly regulated zinc-uptake system SpZrt1 in Schizosaccharomyces pombe reveals the delicacy of cellular zinc balance. FEMS Yeast Res 8:883–896

    Article  CAS  PubMed  Google Scholar 

  • Choi S, Bird AJ (2014) Zinc’ing sensibly: controlling zinc homeostasis at the transcriptional level. Metallomics 6:1198–1215

    Article  CAS  PubMed  Google Scholar 

  • Dainty SJ, Kennedy CA, Watt S, Bähler J, Whitehall SK (2008) Response of Schizosaccharomyces pombe to zinc deficiency. Eukaryot Cell 7:454–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabrizio P, Longo VD (2003) The chronological lifespan of. Saccharomyces Cerevisiae Aging Cell 2:73–81

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Oshiro T, Fujita Y, Kubota S, Naito C, Ohtsuka H, Murakami H, Aiba H (2010) Pma1, a P-type proton ATPase, is a determinant of chronological lifespan in fission yeast. J Biol Chem 285:34616–34620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar J, Barhydt T, Awasthi A, Lithgow GJ, Killilea DW, Kapahi P (2016) Zinc levels modulate lifespan through multiple longevity pathway in Caenorhabditis elegans. PLoS One 11:e0153513

    Article  PubMed  PubMed Central  Google Scholar 

  • Kyba M, Brock HW (1998) The SAM domain of polyhomeotic, RAE28, and Scm mediates specific interactions through conserved residues. Dev Genet 22:74–84

    Article  CAS  PubMed  Google Scholar 

  • Laity JH, Lee BM, Wright PE (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Struct Biol 11:39–46

    Article  CAS  PubMed  Google Scholar 

  • Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795–823

    Article  CAS  PubMed  Google Scholar 

  • Nagano Y, Furuhashi H, Inaba T, Sasaki Y (2001) A novel class of plant-specific zinc-dependent DNA-binding protein that binds to A/T-rich DNA sequences. Nucleic Acids Res 29:4097–4105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohtsuka H, Ogawa Y, Mizuno H, Mita S, Aiba H (2009) Identification of Ecl family genes that extend chronological lifespan in fission yeast. Biosci Biotechnol Biochem 73:885–889

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka H, Azuma K, Kubota S, Murakami H, Giga-Hama Y, Tohda H, Aiba H (2012) Chronological lifespan extension by Ecl1 family proteins depends on Prr1 response regulator in fission yeast. Genes Cells 17:39–52

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka H, Ogawa S, Kawamura H, Sakai E, Ichinose K, Murakami H, Aiba H (2013) Screening for long-lived genes identifies Oga1, a guanine-quadruplex associated protein that affects the chronological lifespan of the fission yeast Schizosaccharomyces pombe. Mol Genet Genomics 288:285–295

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka H, Ishida M, Naito C, Murakami H, Aiba H (2015) Sexual development of Schizosaccharomyces pombe is induced by zinc or iron limitation through Ecl1 family genes. Mol Genet Genomics 290:173–185

    Article  CAS  PubMed  Google Scholar 

  • Oshiro T, Aiba H, Mizuno T (2003) A defect in a fatty acyl-CoA synthetase gene, lcf1 +, results in a decrease in viability after entry into the stationary phase in fission yeast. Mol Genet Genomics 269:437–442

    Article  CAS  PubMed  Google Scholar 

  • Reuscher S, Isuzugawa K, Kawachi M, Oikawa A, Shiratake K (2014) Comprehensive element analysis of fruit flesh from European pear ‘La France’ and its giant fruit bud mutant indicates specific roles for B and Ca in fruit development. Sci Hortic 176:255–260

    Article  CAS  Google Scholar 

  • Roux AE, Chartrand P, Ferbeyre G, Rokeach LA (2010) Fission yeast and other yeasts as emergent models to unravel cellular aging in eukaryotes. J Gerontol A Biol Sci Med Sci 65:1–8

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Drs. M. Kawachi and M. Maeshima (Nagoya University, Japan) for support of ICP-AES analysis. This work was supported by MEXT KAKENHI Grant No. 23119002 (to HA), a Grant-in-Aid for Young Scientists (B) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to HO) and a Grant-in-Aid for Scientific Research (C) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to HO). TS was supported by Grant-in-Aid for JSPS Research Fellow from Japan Society for the Promotion of Science (JSPS). Part of this work was also supported by Institute for Fermentation, Osaka and the Asahi Glass Foundation [to HA].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hirofumi Aiba.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 23 KB)

Supplementary material 2 (DOCX 12 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shimasaki, T., Ohtsuka, H., Naito, C. et al. Ecl1 is a zinc-binding protein involved in the zinc-limitation-dependent extension of chronological life span in fission yeast. Mol Genet Genomics 292, 475–481 (2017). https://doi.org/10.1007/s00438-016-1285-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-016-1285-x

Keywords

Navigation