Table of Contents
International Journal of Proteomics
Volume 2016 (2016), Article ID 8302423, 12 pages
http://dx.doi.org/10.1155/2016/8302423
Research Article

Label-Free Proteomic Analysis of Flavohemoglobin Deleted Strain of Saccharomyces cerevisiae

1Department of Biochemistry, University of Calcutta, 35, Ballygunge Circular Road, Kolkata, West Bengal 700 019, India
2Waters India Pvt. Ltd., Bangalore 560 058, India

Received 17 September 2015; Revised 8 December 2015; Accepted 16 December 2015

Academic Editor: Christian Huck

Copyright © 2016 Chiranjit Panja et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Hardison, “Hemoglobins from bacteria to man: evolution of different patterns of gene expression,” Journal of Experimental Biology, vol. 201, no. 8, pp. 1099–1117, 1998. View at Google Scholar · View at Scopus
  2. H. Zhu and A. F. Riggs, “Yeast flavohemoglobin is an ancient protein related to globins and a reductase family,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 11, pp. 5015–5019, 1992. View at Publisher · View at Google Scholar · View at Scopus
  3. R. K. Poole and M. N. Hughes, “New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress,” Molecular Microbiology, vol. 36, no. 4, pp. 775–783, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Liu, M. Zeng, A. Hausladen, J. Heitman, and J. S. Stamler, “Protection from nitrosative stress by yeast flavohemoglobin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4672–4676, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Membrillo-Hernández, M. D. Coopamah, M. F. Anjum et al., “The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a ‘nitric oxide releaser,’ and paraquat and is essential for transcriptional responses to oxidative stress,” The Journal of Biological Chemistry, vol. 274, no. 2, pp. 748–754, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. P. R. Gardner, A. M. Gardner, L. A. Martin, and A. L. Salzman, “Nitric oxide dioxygenase: an enzymic function for flavohemoglobin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 18, pp. 10378–10383, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Hausladen, A. J. Gow, and J. S. Stamler, “Nitrosative stress: metabolic pathway involving the flavohemoglobin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 24, pp. 14100–14105, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. R. K. Poole, M. F. Anjum, J. Membrillo-Hernández, S. O. Kim, M. N. Hughes, and V. Stewart, “Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12,” Journal of Bacteriology, vol. 178, no. 18, pp. 5487–5492, 1996. View at Google Scholar · View at Scopus
  9. J. Membrillo-Hernandez, M. D. Coopamah, A. Channa, M. N. Hughes, and R. K. Poole, “A novel mechanism for upregulation of the Escherichia coli K-12 hmp (flavohaemoglobin) gene by the ‘NO releaser’, S-nitrosoglutathione: nitrosation of homocysteine and modulation of MetR binding to the glyA-hmp intergenic region,” Molecular Microbiology, vol. 29, no. 4, pp. 1101–1112, 1998. View at Publisher · View at Google Scholar
  10. M. J. Crawford and D. E. Goldberg, “Role for the Salmonella flavohemoglobin in protection from nitric oxide,” The Journal of Biological Chemistry, vol. 273, no. 20, pp. 12543–12547, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. T. M. Stevanin, R. K. Poole, E. A. G. Demoncheaux, and R. C. Read, “Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages,” Infection and Immunity, vol. 70, no. 8, pp. 4399–4405, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. I.-S. Bang, L. Liu, A. Vazquez-Torres, M.-L. Crouch, J. S. Stamler, and F. C. Fang, “Maintenance of nitric oxide and redox homeostasis by the Salmonella flavohemoglobin Hmp,” The Journal of Biological Chemistry, vol. 281, no. 38, pp. 28039–28047, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Keilin and A. Tissieres, “Hemoglobin in certain strains of yeast Saccharomyces cerevisiae,” Biochemical Journal, vol. 57, pp. 29–30, 1954. View at Google Scholar
  14. A. Lewinska and G. Bartosz, “Yeast flavohemoglobin protects against nitrosative stress and controls ferric reductase activity,” Redox Report, vol. 11, no. 5, pp. 231–239, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. B. S. Hromatka, S. M. Noble, and A. D. Johnson, “Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence,” Molecular Biology of the Cell, vol. 16, no. 10, pp. 4814–4826, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. M. J. Crawford, D. R. Sherman, and D. E. Goldberg, “Regulation of Saccharomyces cerevisiae flavohemoglobin gene expression,” The Journal of Biological Chemistry, vol. 270, no. 12, pp. 6991–6996, 1995. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Lacelle, M. Kumano, K. Kurita, K. Yamane, P. Zuber, and M. M. Nakano, “Oxygen-controlled regulation of the flavohemoglobin gene in Bacillus subtilis,” Journal of Bacteriology, vol. 178, no. 13, pp. 3803–3808, 1996. View at Google Scholar · View at Scopus
  18. N. Cassanova, K. M. O'Brien, B. T. Stahl, T. McClure, and R. O. Poyton, “Yeast flavohemoglobin, a nitric oxide oxidoreductase, is located in both the cytosol and the mitochondrial matrix: effects of respiration, anoxia, and the mitochondrial genome on its intracellular level and distribution,” The Journal of Biological Chemistry, vol. 280, no. 9, pp. 7645–7653, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. X.-J. Zhao, D. Raitt, P. V. Burke, A. S. Clewell, K. E. Kwast, and R. O. Poyton, “Function and expression of flavohemoglobin in Saccharomyces cerevisiae. Evidence for a role in the oxidative stress response,” Journal of Biological Chemistry, vol. 271, no. 41, pp. 25131–25138, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Buisson and R. Labbe-Bois, “Flavohemoglobin expression and function in Saccharomyces cerevisiae. No relationship with respiration and complex response to oxidative stress,” The Journal of Biological Chemistry, vol. 273, no. 16, pp. 9527–9533, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Bhattacharjee, U. Majumdar, D. Maity et al., “Characterizing the effect of nitrosative stress in Saccharomyces cerevisiae,” Archives of Biochemistry and Biophysics, vol. 496, no. 2, pp. 109–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Bhattacharjee, U. Majumdar, D. Maity et al., “In vivo protein tyrosine nitration in S. cerevisiae: identification of tyrosine-nitrated proteins in mitochondria,” Biochemical and Biophysical Research Communications, vol. 388, no. 3, pp. 612–617, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Panja and S. Ghosh, “Detection of in vivo protein tyrosine nitration in petite mutant of Saccharomyces cerevisiae: consequence of its formation and significance,” Biochemical and Biophysical Research Communications, vol. 451, no. 4, pp. 529–534, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Sahoo, A. Bhattacharjee, U. Majumdar, S. S. Ray, T. Dutta, and S. Ghosh, “A novel role of catalase in detoxification of peroxynitrite in S. cerevisiae,” Biochemical and Biophysical Research Communications, vol. 385, no. 4, pp. 507–511, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  26. J. C. Silva, M. V. Gorenstein, G.-Z. Li, J. P. C. Vissers, and S. J. Geromanos, “Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition,” Molecular and Cellular Proteomics, vol. 5, no. 1, pp. 144–156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. Z. Shen, P. Li, R.-J. Ni et al., “Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening,” Molecular and Cellular Proteomics, vol. 8, no. 11, pp. 2443–2460, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. W. da Huang, B. T. Sherman, and R. A. Lempicki, “Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources,” Nature Protocols, vol. 4, no. 1, pp. 44–57, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. D. W. Huang, B. T. Sherman, and R. A. Lempicki, “Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists,” Nucleic Acids Research, vol. 37, no. 1, pp. 1–13, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Schlicker, F. S. Domingues, J. Rahnenführer, and T. Lengauer, “A new measure for functional similarity of gene products based on Gene Ontology,” BMC Bioinformatics, vol. 7, article 302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Supek, M. Bošnjak, N. Škunca, and T. Šmuc, “Revigo summarizes and visualizes long lists of gene ontology terms,” PLoS ONE, vol. 6, no. 7, Article ID e21800, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Franceschini, D. Szklarczyk, S. Frankild et al., “STRING v9.1: protein-protein interaction networks, with increased coverage and integration,” Nucleic Acids Research, vol. 41, no. 1, pp. D808–D815, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. S. D. Hooper and P. Bork, “Medusa: a simple tool for interaction graph analysis,” Bioinformatics, vol. 21, no. 24, pp. 4432–4433, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. S. O. Kim, Y. Orii, D. Lloyd, M. N. Hughes, and R. K. Poole, “Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide,” FEBS Letters, vol. 445, no. 2-3, pp. 389–394, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Horan, I. Bourges, and B. Meunier, “Transcriptional response to nitrosative stress in Saccharomyces cerevisiae,” Yeast, vol. 23, no. 7, pp. 519–535, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. X. Duan, J. Yang, B. Ren, G. Tan, and H. Ding, “Reactivity of nitric oxide with the (4Fe-4S) cluster of dihydroxyacid dehydratase from Escherichia coli,” Biochemical Journal, vol. 417, no. 3, pp. 783–789, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. J. K. Bhattacharjee, “α-Aminoadipate pathway for the biosynthesis of lysine in lower eukaryotes,” Critical reviews in microbiology, vol. 12, no. 2, pp. 131–151, 1985. View at Publisher · View at Google Scholar · View at Scopus
  38. T. M. Zabriskie and M. D. Jackson, “Lysine biosynthesis and metabolism in fungi,” Natural Product Reports, vol. 17, no. 1, pp. 85–97, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Quezada, A. Marín-Hernández, D. Aguilar et al., “The Lys20 homocitrate synthase isoform exerts most of the flux control over the lysine synthesis pathway in Saccharomyces cerevisiae,” Molecular Microbiology, vol. 82, no. 3, pp. 578–590, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. W. E. Karsten, Z. L. Reyes, K. D. Bobyk, P. F. Cook, and L. Chooback, “Mechanism of the aromatic aminotransferase encoded by the Aro8 gene from Saccharomyces cerevisiae,” Archives of Biochemistry and Biophysics, vol. 516, no. 1, pp. 67–74, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. D. R. Hyduke, L. R. Jarboe, L. M. Tran, K. J. Y. Chou, and J. C. Liao, “Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 20, pp. 8484–8489, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. A. R. Richardson, E. C. Payne, N. Younger et al., “Multiple targets of nitric oxide in the tricarboxylic acid cycle of Salmonella enterica serovar typhimurium,” Cell Host and Microbe, vol. 10, no. 1, pp. 33–43, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. S. M. Brown, R. Upadhya, J. D. Shoemaker, and J. K. Lodge, “Isocitrate dehydrogenase is important for nitrosative stress resistance in Cryptococcus neoformans, but oxidative stress resistance is not dependent on glucose-6-phosphate dehydrogenase,” Eukaryotic Cell, vol. 9, no. 6, pp. 971–980, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. T. A. Missall, M. E. Pusateri, M. J. Donlin, K. T. Chambers, J. A. Corbett, and J. K. Lodge, “Posttranslational, translational, and transcriptional responses to nitric oxide stress in Cryptococcus neoformans: implications for virulence,” Eukaryotic Cell, vol. 5, no. 3, pp. 518–529, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Quezada, A. Marín-Hernández, R. Arreguín-Espinosa, F. D. Rumjanek, R. Moreno-Sánchez, and E. Saavedra, “The 2-oxoglutarate supply exerts significant control on the lysine synthesis flux in Saccharomyces cerevisiae,” FEBS Journal, vol. 280, no. 22, pp. 5737–5749, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Parsyan, Y. Svitkin, D. Shahbazian et al., “MRNA helicases: the tacticians of translational control,” Nature Reviews Molecular Cell Biology, vol. 12, no. 4, pp. 235–245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Linder and P. P. Slonimski, “An essential yeast protein, encoded by duplicated genes TIF1 and TIF2 and homologous to the mammalian translation initiation factor eIF-4A, can suppress a mitochondrial missense mutation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 7, pp. 2286–2290, 1989. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. V. Svitkin, A. Pause, A. Haghighat et al., “The requirement for eukaryotic initiation factor 4A.elF4A; in translation is in direct proportion to the degree of mRNA 5 secondary structure,” RNA, vol. 7, no. 3, pp. 382–394, 2001. View at Publisher · View at Google Scholar
  49. Y. Sakasegawa, N. S. Hachiya, S. Tsukita, and K. Kaneko, “Ecm10p localizes in yeast mitochondrial nucleoids and its overexpression induces extensive mitochondrial DNA aggregations,” Biochemical and Biophysical Research Communications, vol. 309, no. 1, pp. 217–221, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. R.-F. Mao, V. Rubio, H. Chen, L. Bai, O. C. Mansour, and Z.-Z. Shi, “OLA1 protects cells in heat shock by stabilizing HSP70,” Cell Death and Disease, vol. 4, article e491, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Zhang, V. Rubio, M. W. Lieberman, and Z.-Z. Shi, “OLA1, an Obg-like ATPase, suppresses antioxidant response via nontranscriptional mechanisms,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 36, pp. 15356–15361, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Wenk, Q. Ba, V. Erichsen et al., “A universally conserved ATPase regulates the oxidative stress response in Escherichia coli,” The Journal of Biological Chemistry, vol. 287, no. 52, pp. 43585–43598, 2012. View at Publisher · View at Google Scholar · View at Scopus