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Research article

References

  1. Roxstrom-Lindquist K, Faye I. 2001. The Drosophila gene Yippee r eveals a n ovel f amily of p utative zinc-binding proteins highly conserved among eukaryotes. Insect Mol. Biol. 10: 77-86.
    Pubmed CrossRef
  2. Hosono K, Sasaki T, Minoshima S, Shimizu N. 2004. Identification and characterization of a novel gene family YPEL in a wide spectrum of eukaryotic species. Gene 340: 31-43.
    Pubmed CrossRef
  3. Hosono K, Noda S, Shimizu A, Nakanishi N, Ohtsubo M, Shimizu N, Minoshima S. 2010. YPEL5 protein of the YPEL gene family is involved in the cell cycle progression by interacting with two distinct proteins RanBPM and RanBP10. Genomics 96: 102-111.
    Pubmed CrossRef
  4. Baker SJ. 2 003. Small unstable a poptotic p rotein, an apoptosis-associated protein, suppresses proliferation of myeloid cells. Cancer Res. 63: 705-712.
    Pubmed
  5. Kelley KD, Miller KR, Todd A, Kelley AR, Tuttle R, Berberich SJ. 2010. YPEL3, a p53-regulated gene that induces cellular senescence. Cancer Res. 70: 3566-3575.
    Pubmed PMC CrossRef
  6. Berberich SJ, Todd A, Tuttle R. 2011. Why YPEL3 represents a novel tumor suppressor. Front. Biosci. 16: 1746-1751.
    CrossRef
  7. Tuttle R, Simon M, Hitch DC, Maiorano JN, Hellan M, Ouellette J, et al. 2011. Senescence-associated gene YPEL3 is downregulated in human colon tumors. Ann. Surg. Oncol. 18: 1791-1796.
    Pubmed CrossRef
  8. Scherens B, el Bakkoury M, Vierendeels F, Dubois E, Messenguy F. 1993. Sequencing and functional analysis of a 32,560 bp segment on the left arm of yeast chromosome II. Identification of 26 open reading frames, including the KIP1 and SEC17 genes. Yeast 9: 1355-1371.
    Pubmed CrossRef
  9. Giaever G, Nislow C. 2014. The yeast deletion collection: a decade of functional genomics. Genetics 197: 451-465.
    Pubmed PMC CrossRef
  10. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
    Pubmed CrossRef
  11. Brown JA, Sherlock G, Myers CL, Burrows NM, Deng C, Wu HI, et al. 2006. Global analysis of gene function in yeast by quantitative phenotypic profiling. Mol. Syst. Biol. 2:2006.0001.
  12. Botstein D, Fink GR. 2011. Yeast: an experimental organism for 21st century biology. Genetics 189: 695-704.
    Pubmed PMC CrossRef
  13. Karathia H, Vilaprinyo E, Sorribas A, Alves R. 2011. Saccharomyces cerevisiae as a model organism: a comparative study. PLoS One 6: e16015.
    Pubmed PMC CrossRef
  14. Jun DY, Park HW, Kim YH. 2007. Expression of Yippee-like 5 (YPEL5) gene during activation of human peripheral T lymphocytes by immobilized anti-CD3. J. Life Sci. 17: 16411648.
    CrossRef
  15. Jun D Y, Kim M K, K im YH. 1996. R abbit antibody r aised against murine cyclin D3 protein overexpressed in bacterial system. J. Microbiol. Biotechnol. 6: 474-491.
  16. Belinchon MM, Flores CL, Gancedo JM. 2004. Sampling Saccharomyces cerevisiae cells by rapid filtration improves the yield of mRNAs. FEMS Yeast Res. 4: 751-756.
    Pubmed CrossRef
  17. Gietz D, St Jean A, Woods RA, Schiestl RH. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425-1425.
    Pubmed PMC CrossRef
  18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
    Pubmed CrossRef
  19. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  20. Kim SM, Park HS, Jun DY, Woo HJ, Woo MH, Yang CH, Kim YH. 2009. Mollugin induces apoptosis in human Jurkat T cells through endoplasmic reticulum stress-mediated activation of JNK and caspase-12 and subsequent activation of mitochondria-dependent caspase cascade regulated by Bcl-xL. Toxicol. Appl. Pharmacol. 241: 210-220.
    Pubmed CrossRef
  21. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, et al. 1991. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregateforming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88:3671-3675.
    Pubmed PMC CrossRef
  22. Morris EJ, Geller HM. 1996. Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I:evidence for cell cycle-independent toxicity. J. Cell Biol. 134:757-770.
    CrossRef
  23. Ribeiro GF, Côrte-Real M, Johansson B. 2006. Characterization of DNA damage in yeast apoptosis induced by hydrogen peroxide, acetic acid, and hyperosmotic shock. Mol. Biol. Cell 17: 4584-4591.
    Pubmed PMC CrossRef
  24. Ochs K, Sobol RW, Wilson SH, Kaina B. 1999. Cells deficient in DNA polymerase beta are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res. 59: 1544-1551.
    Pubmed
  25. Guaragnella N, Zdralević M, Antonacci L, Passarella S, Marra E, Giannattasio S. 2012. The role of mitochondria in yeast programmed cell death. Front. Oncol. 2: 70.
    Pubmed PMC CrossRef
  26. Jarrett SG, Novak M, Dabernat S, Daniel JY, Mellon I, Zhang Q, et al. 2012. Metastasis suppressor NM23-H1 promotes repair of UV-induced DNA damage and suppresses UVinduced melanoma genesis. Cancer Res. 72: 133-143.
    Pubmed PMC CrossRef
  27. Yang M, Jarrett SG, Craven R, Kaetzel DM. 2009. YNK1, the yeast homolog of human metastasis suppressor NM23, is required for repair of UV radiation- and etoposide-induced DNA damage. Mutat. Res. 660: 74-78.
    Pubmed PMC CrossRef
  28. Ligr M, Madeo F, Frohlich E, Hilt W, Frohlich KU, Wolf DH. 1998. Mammalian Bax triggers apoptotic changes in yeast. FEBS Lett. 30: 61-65.
    CrossRef
  29. Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Frohlich KU. 2004. Apoptosis in yeast. Curr. Opin. Microbiol. 7: 655-660.
    Pubmed CrossRef
  30. Mazzoni C, Falcone C. 2008. Caspase-dependent apoptosis in yeast. Biochim. Biophys. Acta 1783: 1320-1327.
    Pubmed CrossRef
  31. Pereira C, Silva RD, Saraiva L, Johansson B, Sousa MJ, Corte-Real M. 2008. Mitochondria-dependent apoptosis in yeast. Biochim. Biophys. Acta 1783: 1286-1302.
    Pubmed CrossRef
  32. Adams JM. 2003. Ways of dying: multiple pathways to apoptosis. Genes Dev. 17: 2481-2495.
    Pubmed CrossRef
  33. Del Carratore R, Della Croce C, Simili M, Taccini E, Scavuzzo M, Sbrana S. 2002. Cell cycle and morphological alterations as indicative of apoptosis promoted by UV irradiation in S. cerevisiae. Mutat. Res. 513: 183-191.
    CrossRef
  34. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV. 2011. Metacaspases. Cell Death Differ. 18:1279-1288.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(3): 633-643

Published online March 28, 2017 https://doi.org/10.4014/jmb.1610.10045

Copyright © The Korean Society for Microbiology and Biotechnology.

Pro-Apoptotic Role of the Human YPEL5 Gene Identified by Functional Complementation of a Yeast moh1Δ Mutation

Ji Young Lee 1, Do Youn Jun 1, Ju Eun Park 1, Gi Hyun Kwon 1, Jong-Sik Kim 2 and Young Ho Kim 1*

1Laboratory of Immunobiology, School of Life Science and Biotechnology, College of Natural Sciences, Kyungpook National University, Daegu 41566, Republic of Korea, 2Department of Biological Sciences, Andong National University, Andong 36729, Republic of Korea

Received: October 18, 2016; Accepted: February 6, 2017

Abstract

To examine the pro-apoptotic role of the human ortholog (YPEL5) of the Drosophila Yippee
protein, the cell viability of Saccharomyces cerevisiae mutant strain with deleted MOH1, the
yeast ortholog, was compared with that of the wild-type (WT)-MOH1 strain after exposure to
different apoptogenic stimulants, including UV irradiation, methyl methanesulfonate (MMS),
camptothecin (CPT), heat shock, and hyperosmotic shock. The moh1Δ mutant exhibited
enhanced cell viability compared with the WT-MOH1 strain when treated with lethal UV
irradiation, 1.8 mM MMS, 100 μM CPT, heat shock at 50°C, or 1.2 M KCl. At the same time, the
level of Moh1 protein was commonly up-regulated in the WT-MOH1 strain as was that of
Ynk1 protein, which is known as a marker for DNA damage. Although the enhanced UV
resistance of the moh1Δ mutant largely disappeared following transformation with the yeast
MOH1 gene or one of the human YPEL1-YPEL5 genes, the transformant bearing pYES2-
YPEL5 was more sensitive to lethal UV irradiation and its UV sensitivity was similar to that of
the WT-MOH1 strain. Under these conditions, the UV irradiation-induced apoptotic events,
such as FITC-Annexin V stainability, mitochondrial membrane potential (Δψm) loss, and
metacaspase activation, occurred to a much lesser extent in the moh1Δ mutant compared with
the WT-MOH1 strain and the mutant strain bearing pYES2-MOH1 or pYES2-YPEL5. These
results demonstrate the functional conservation between yeast Moh1 and human YPEL5, and
their involvement in mitochondria-dependent apoptosis induced by DNA damage.

Keywords: DNA damage, Drosophila Yippee, Apoptosis, metacaspase, S. cerevisiae MOH1, human YPEL5

References

  1. Roxstrom-Lindquist K, Faye I. 2001. The Drosophila gene Yippee r eveals a n ovel f amily of p utative zinc-binding proteins highly conserved among eukaryotes. Insect Mol. Biol. 10: 77-86.
    Pubmed CrossRef
  2. Hosono K, Sasaki T, Minoshima S, Shimizu N. 2004. Identification and characterization of a novel gene family YPEL in a wide spectrum of eukaryotic species. Gene 340: 31-43.
    Pubmed CrossRef
  3. Hosono K, Noda S, Shimizu A, Nakanishi N, Ohtsubo M, Shimizu N, Minoshima S. 2010. YPEL5 protein of the YPEL gene family is involved in the cell cycle progression by interacting with two distinct proteins RanBPM and RanBP10. Genomics 96: 102-111.
    Pubmed CrossRef
  4. Baker SJ. 2 003. Small unstable a poptotic p rotein, an apoptosis-associated protein, suppresses proliferation of myeloid cells. Cancer Res. 63: 705-712.
    Pubmed
  5. Kelley KD, Miller KR, Todd A, Kelley AR, Tuttle R, Berberich SJ. 2010. YPEL3, a p53-regulated gene that induces cellular senescence. Cancer Res. 70: 3566-3575.
    Pubmed KoreaMed CrossRef
  6. Berberich SJ, Todd A, Tuttle R. 2011. Why YPEL3 represents a novel tumor suppressor. Front. Biosci. 16: 1746-1751.
    CrossRef
  7. Tuttle R, Simon M, Hitch DC, Maiorano JN, Hellan M, Ouellette J, et al. 2011. Senescence-associated gene YPEL3 is downregulated in human colon tumors. Ann. Surg. Oncol. 18: 1791-1796.
    Pubmed CrossRef
  8. Scherens B, el Bakkoury M, Vierendeels F, Dubois E, Messenguy F. 1993. Sequencing and functional analysis of a 32,560 bp segment on the left arm of yeast chromosome II. Identification of 26 open reading frames, including the KIP1 and SEC17 genes. Yeast 9: 1355-1371.
    Pubmed CrossRef
  9. Giaever G, Nislow C. 2014. The yeast deletion collection: a decade of functional genomics. Genetics 197: 451-465.
    Pubmed KoreaMed CrossRef
  10. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
    Pubmed CrossRef
  11. Brown JA, Sherlock G, Myers CL, Burrows NM, Deng C, Wu HI, et al. 2006. Global analysis of gene function in yeast by quantitative phenotypic profiling. Mol. Syst. Biol. 2:2006.0001.
  12. Botstein D, Fink GR. 2011. Yeast: an experimental organism for 21st century biology. Genetics 189: 695-704.
    Pubmed KoreaMed CrossRef
  13. Karathia H, Vilaprinyo E, Sorribas A, Alves R. 2011. Saccharomyces cerevisiae as a model organism: a comparative study. PLoS One 6: e16015.
    Pubmed KoreaMed CrossRef
  14. Jun DY, Park HW, Kim YH. 2007. Expression of Yippee-like 5 (YPEL5) gene during activation of human peripheral T lymphocytes by immobilized anti-CD3. J. Life Sci. 17: 16411648.
    CrossRef
  15. Jun D Y, Kim M K, K im YH. 1996. R abbit antibody r aised against murine cyclin D3 protein overexpressed in bacterial system. J. Microbiol. Biotechnol. 6: 474-491.
  16. Belinchon MM, Flores CL, Gancedo JM. 2004. Sampling Saccharomyces cerevisiae cells by rapid filtration improves the yield of mRNAs. FEMS Yeast Res. 4: 751-756.
    Pubmed CrossRef
  17. Gietz D, St Jean A, Woods RA, Schiestl RH. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425-1425.
    Pubmed KoreaMed CrossRef
  18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
    Pubmed CrossRef
  19. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  20. Kim SM, Park HS, Jun DY, Woo HJ, Woo MH, Yang CH, Kim YH. 2009. Mollugin induces apoptosis in human Jurkat T cells through endoplasmic reticulum stress-mediated activation of JNK and caspase-12 and subsequent activation of mitochondria-dependent caspase cascade regulated by Bcl-xL. Toxicol. Appl. Pharmacol. 241: 210-220.
    Pubmed CrossRef
  21. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, et al. 1991. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregateforming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88:3671-3675.
    Pubmed KoreaMed CrossRef
  22. Morris EJ, Geller HM. 1996. Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I:evidence for cell cycle-independent toxicity. J. Cell Biol. 134:757-770.
    CrossRef
  23. Ribeiro GF, Côrte-Real M, Johansson B. 2006. Characterization of DNA damage in yeast apoptosis induced by hydrogen peroxide, acetic acid, and hyperosmotic shock. Mol. Biol. Cell 17: 4584-4591.
    Pubmed KoreaMed CrossRef
  24. Ochs K, Sobol RW, Wilson SH, Kaina B. 1999. Cells deficient in DNA polymerase beta are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res. 59: 1544-1551.
    Pubmed
  25. Guaragnella N, Zdralević M, Antonacci L, Passarella S, Marra E, Giannattasio S. 2012. The role of mitochondria in yeast programmed cell death. Front. Oncol. 2: 70.
    Pubmed KoreaMed CrossRef
  26. Jarrett SG, Novak M, Dabernat S, Daniel JY, Mellon I, Zhang Q, et al. 2012. Metastasis suppressor NM23-H1 promotes repair of UV-induced DNA damage and suppresses UVinduced melanoma genesis. Cancer Res. 72: 133-143.
    Pubmed KoreaMed CrossRef
  27. Yang M, Jarrett SG, Craven R, Kaetzel DM. 2009. YNK1, the yeast homolog of human metastasis suppressor NM23, is required for repair of UV radiation- and etoposide-induced DNA damage. Mutat. Res. 660: 74-78.
    Pubmed KoreaMed CrossRef
  28. Ligr M, Madeo F, Frohlich E, Hilt W, Frohlich KU, Wolf DH. 1998. Mammalian Bax triggers apoptotic changes in yeast. FEBS Lett. 30: 61-65.
    CrossRef
  29. Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Frohlich KU. 2004. Apoptosis in yeast. Curr. Opin. Microbiol. 7: 655-660.
    Pubmed CrossRef
  30. Mazzoni C, Falcone C. 2008. Caspase-dependent apoptosis in yeast. Biochim. Biophys. Acta 1783: 1320-1327.
    Pubmed CrossRef
  31. Pereira C, Silva RD, Saraiva L, Johansson B, Sousa MJ, Corte-Real M. 2008. Mitochondria-dependent apoptosis in yeast. Biochim. Biophys. Acta 1783: 1286-1302.
    Pubmed CrossRef
  32. Adams JM. 2003. Ways of dying: multiple pathways to apoptosis. Genes Dev. 17: 2481-2495.
    Pubmed CrossRef
  33. Del Carratore R, Della Croce C, Simili M, Taccini E, Scavuzzo M, Sbrana S. 2002. Cell cycle and morphological alterations as indicative of apoptosis promoted by UV irradiation in S. cerevisiae. Mutat. Res. 513: 183-191.
    CrossRef
  34. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV. 2011. Metacaspases. Cell Death Differ. 18:1279-1288.
    Pubmed KoreaMed CrossRef