The effect of deletions of genes encoding Pho3p and Bgl2p on the polyphosphate level, stress adaptation and attachment of these proteins in Saccharomyces cerevisiae cell wall

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Толық мәтін

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Аннотация

Inorganic polyphosphates (polyP), according to literature data, are involved in the regulatory processes of molecular complex of the Saccharomyces cerevisiae cell wall (CW). The aim of the work was to reveal relationship between polyP, acid phosphatase Pho3p, and the major CW protein, glucanosyl transglycosylase Bgl2p, which is the main glucan-remodelling enzyme with amyloid properties. It has been shown that the yeast cells with deletion of the PHO3 gene contain more high molecular alkali-soluble polyP and are also more resistant to exposure to alkali and manganese ions compared to the wild type strain. This suggests that Pho3p is responsible for hydrolysis of the high molecular polyP on the surface of yeast cells, and these polyP belong to the stress resistance factors. The S. cerevisiae strain with deletion of the BGL2 gene is similar to the Δpho3 strain both in the level of high molecular alkali-soluble polyP and in the increased resistance to alkali and manganese. Comparative analysis of the CW proteins demonstrated correlation between the extractability of the acid phosphatase and Bgl2p, and also revealed a change in the mode of Bgl2p attachment to the CW of the strain lacking Pho3p. It has been suggested that Bgl2p and Pho3p are able to form a metabolon or its parts that connects biogenesis of the main structural polymer of the CW, glucan, and catabolism of an important regulatory polymer, polyphosphates.

Авторлар туралы

T. Kalebina

Lomonosov Moscow State University, Faculty of Biology

Email: kalebina@gmail.com
119234 Moscow, Russia

E. Kulakovskaya

Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”, Skryabin Institute of Biochemistry and Physiology of Microorganisms

Email: kalebina@gmail.com
142290 Pushchino, Russia

V. Rekstina

Lomonosov Moscow State University, Faculty of Biology

Email: kalebina@gmail.com
119234 Moscow, Russia

L. Trilisenko

Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”, Skryabin Institute of Biochemistry and Physiology of Microorganisms

Email: kalebina@gmail.com
142290 Pushchino, Russia

R. Ziganshin

Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: kalebina@gmail.com
117997 Moscow, Russia

N. Marmiy

Institute of Mitoengineering, Lomonosov Moscow State University

Email: kalebina@gmail.com
119992 Moscow, Russia

D. Esipov

Lomonosov Moscow State University, Faculty of Biology

Email: kalebina@gmail.com
119234 Moscow, Russia

T. Kulakovskaya

Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”, Skryabin Institute of Biochemistry and Physiology of Microorganisms

Email: kalebina@gmail.com
142290 Pushchino, Russia

Әдебиет тізімі

  1. Sanz, A. B., García, R., Rodríguez-Peña, J. M., and Arroyo, J. (2017) The CWI Pathway: regulation of the transcriptional adaptive response to cell wall stress in yeast, J. Fungi (Basel), 4, 1, doi: 10.3390/jof4010001.
  2. Huang, C., Zhao, F., Lin, Y., Zheng, S., Liang, S., and Han, S. (2018) RNA-Seq analysis of global transcriptomic changes suggests a roles for the MAPK pathway and carbon metabolism in cell wall maintenance in a Saccharomyces cerevisiae FKS1 mutant, Biochem. Biophys. Res. Commun., 500, 603-608, doi: 10.1016/j.bbrc.2018.04.113.
  3. Liu, L., and Levin, D. E. (2018) Intracellular mechanism by which genotoxic stress activates yeast SAPK Mpk1, Mol. Biol. Cell, 29, 2898-2909, doi: 10.1091/mbc.E18-07-0441.
  4. Molon, M., Woznicka, O., and Zebrowski, J. (2018) Cell wall biosynthesis impairment affects the budding lifespan of the Saccharomyces cerevisiae yeast, Biogerontology, 19, 67-79, doi: 10.1007/s10522-017-9740-6.
  5. Davì, V., Chevalier, L., Guo, H., Tanimoto, H., Barrett, K., Couturier, E., Boudaoud, A., and Minc, N. (2019) Systematic mapping of cell wall mechanics in the regulation of cell morphogenesis, Proc. Natl. Acad. Sci. USA, 116, 13833-13838, doi: 10.1073/pnas.1820455116.
  6. Willaert, R. G. (2018) Adhesins of yeasts: protein structure and interactions, J. Fungi (Basel), 4, 119, doi: 10.3390/jof4040119.
  7. Kalebina, T. S., Plotnikova, T. A., Gorkovskii, A. A., Selyakh, I. O., Galzitskaya, O. V., Bezsonov, E. E., Gellissen, G., and Kulaev, I. S. (2008) Amyloid-like properties of Saccharomyces cerevisiae cell wall glucantransferase Bgl2p: prediction and experimental evidences, Prion, 2, 91-96, doi: 10.4161/pri.2.2.6645.
  8. Bezsonov, E. E., Groenning, M., Galzitskaya, O. V., Gorkovskii, A. A., Semisotnov, G. V., Selyakh, I. O., Ziganshin, R. H., Rekstina, V. V., Kudryashova, I. B., Kuznetsov, S. A., Kulaev, I. S., and Kalebina, T. S. (2013) Amyloidogenic peptides of yeast cell wall glucantransferase Bgl2p as a model for the investigation of its pH-dependent fibril formation, Prion, 7, 175-184, doi: 10.4161/pri.22992.
  9. Mouyna, I., Hartl, L., and Latgé, J. P. (2013) β-1,3-glucan modifying enzymes in Aspergillus fumigatus, Front. Microbiol., 4, 81, doi: 10.3389/fmicb.2013.00081.
  10. Блинникова Е. И., Мирющенко Ф. Л., Шабалин Ю. А., Егоров С. Н. (2002) Везикулярный транспорт внеклеточных кислых фосфатаз у дрожжей Saccharomyces cerevisiae, Биохимия, 67, 580-586.
  11. Калебина Т. С., Егоров С. Н., Арбатский Н. П., Безсонов Е. Е., Горковский А. А., Кулаев И. С. (2008) О роли высокомолекулярных полифосфатов в активации глюкантрансферазы Bgl2p из клеточной стенки дрожжей Saccharomyces cerevisiae, Докл. Акад Наук, 420, 695-699.
  12. Weimberg, R., and Orton, W. L. (1964) Evidence for an exocellular site for the acid phosphatase of Saccharomyces mellis, J. Bacteriol., 88, 1743-1152, doi: 10.1128/jb.88.6.1743-1754.1964.
  13. Кулаев И. С., Крашенинников И. А., Кокурина И. А. (1966) О локализации неорганических полифосфатов и нуклеотидов у Neurospora crassa, Биохимия, 31, 850-858.
  14. Tijssen, J. P. F., Beekes, H. W., and Van Steveninck, J. (1982) Localization of polyphosphate in Saccharomyces fragilis, as revealed by 4′6-diamidino-2-phenylindole fluorescence, Biochem. Biophys. Acta, 721, 394-398. doi: 10.1016/0167-4889(82)90094-5.
  15. Вагабов В. М., Чемоданова О. В., Кулаев И. С. (1990) Влияние неорганических полифосфатов на величину отрицательного заряда клеточной оболочки дрожжей, Докл. АН СССР, 313, 989-992.
  16. Ivanov, A. J., Vagabov, V. M., Fomchenkov, V. M., and Kulaev, I. S. (1996) Study of the influence of polyphosphates of cell envelope on the sensitivity of yeast Saccharomyces carlsbergensis to the cytyl-3-methylammonium bromide, Microbiologiia, 65, 611-616.
  17. Кулаев И. С., Вагабов В. М., Циоменко А. Б. (1972) О корреляции накопления полисахаридов клеточной стенки и некоторых фракций высокомолекулярных полифосфатов у дрожжей, Докл. АН СССР, 204, 734-736.
  18. Циоменко А. Б., Аугустин И., Вагабов В. М., Кулаев И. С. (1974) О взаимосвязи обмена неорганических полифосфатов и маннана у дрожжей, Докл. АН СССР, 215, 478-480.
  19. Шабалин Ю. А., Вагабов В. М., Кулаев И. С. (1979) О механизме сопряжения биосинтеза высокомолекулярных полифосфатов и маннана у дрожжей Saccharomyces carlsbergensis, Докл. АН СССР, 249, 243-246.
  20. Шабалин Ю. А., Вагабов В. М., Кулаев И. С. (1985) Долихилдифосфатманноза: интермедиат биосинтеза гликопротеинов у дрожжей? Докл. АН СССР, 283, 720-723.
  21. Zvonarev, A. N., Crowley, D. E., Ryazanova, L. P., Lichko, L. P., Rusakova, T. G., Kulakovskaya, T. V., and Dmitriev, V. V. (2017) Cell wall canals formed upon growth of Candida maltosa in the presence of hexadecane are associated with polyphosphates, FEMS Yeast Res., 17, fox026, doi: 10.1093/femsyr/fox026.
  22. Oshima, Y. (1997) The phosphatase system in Saccharomyces cerevisiae, Gen. Genet. Syst., 72, 323-334, doi: 10.1266/ggs.72.323.
  23. Secco, D., Wang, C., Shou, H., and Whelan, J. (2012) Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins, FEBS Lett., 586, 289-295, doi: 10.1016/j.febslet.2012.01.036.
  24. Yadav, K. K., Singh, N., and Rajasekharan, R. (2016) Responses to phosphate deprivation in yeast cells, Curr. Genet., 62, 301-307, doi: 10.1007/s00294-015-0544-4.
  25. Eskes, E., Deprez, M. A., Wilms, T., and Winderickx, J. (2018) pH homeostasis in yeast; the phosphate perspective, Curr. Genet., 64, 155-161, doi: 10.1007/s00294-017-0743-2.
  26. Nosaka, K., Kaneko, Y., Nishimura, H., and Iwashima, A. (1989) A possible role for acid phosphatase with thiamin-binding activity encoded by PHO3 in yeast, FEMS Microbiol. Lett., 51, 55-59, doi: 10.1016/0378-1097(89)90077-3.
  27. Nosaka, K. (1990) High affinity of acid phosphatase encoded by PHO3 gene in Saccharomyces cerevisiae for thiamin phosphates, Biochim. Biophys. Acta., 1037, 147-54, doi: 10.1016/0167-4838(90)90160-h.
  28. Kennedy, E. J., Pillus, L., and Ghosh, G. (2005) Pho5p and newly identified nucleotide pyrophosphatases/phosphodiesterases regulate extracellular nucleotide phosphate metabolism in Saccharomyces cerevisiae, Eukaryot. Cell, 4, 1892-1901, doi: 10.1128/EC.4.11.1892-1901.2005.
  29. Andreeva, N., Ledova, L., Ryasanova, L., Kulakovskaya, T., and Eldarov, M. (2019) The acid phosphatase Pho5 of Saccharomyces cerevisiae is not involved in polyphosphate breakdown, Folia Microbiol. (Praha), 64, 867-873, doi: 10.1007/s12223-019-00702-6.
  30. Рекстина В. В., Безсонов Е. Е. (2012) Влияние неорганических полифосфатов на конформацию пептида АК187-196 глюкантрасферазы Bgl2p - амилоида клеточной стенки Saccharomyces cerevisiae. "Ломоносов-2012": МАКС Пресс, Москва, с. 191.
  31. Rekstina, V. V., Sabirzyanova, T. A., Sabirzyanov, F. A., Adzhubei, A. A., Tkachev, Y. V., Kudryashova, I. B., Snalina, N. E., Bykova, A. A., Alessenko, A. V., Ziganshin, R. H., Kuznetsov, S. A., and Kalebina, T. S. (2020) The post-translational modifications, localization, and mode of attachment of non-covalently bound glucanosyltransglycosylases of yeast cell wall as a key to understanding their functioning, Int. J. Mol. Sci., 21, 8304, doi: 10.3390/ijms21218304.
  32. Sherman, F. (2002) Getting started with yeast, Methods Enzymol., 350, 3-41, doi: 10.1016/s0076-687950954-x.
  33. Gietz, R. D., Schiestl, R. H., Willems, A. R., and Woods, R. A. (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure, Yeast, 11, 355-360, doi: 10.1002/yea.320110408.
  34. Gietz, R. D., and Schiestl, R. H. (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method, Nat. Protoc., 2, 31-34, doi: 10.1038/nprot.2007.13.
  35. Вагабов В. М., Трилисенко Л. В., Кулаев И. С. (2000) Зависимость длины цепи неорганических полифосфатов от содержания ортофосфата в среде у дрожжей, Биохимия, 65, 414-420.
  36. Vagabov, V. M., Trilisenko, L. V., Kulakovskaya, T. V., and Kulaev, I. S. (2008) Effect of a carbon source on polyphosphate accumulation in Saccharomyces cerevisiae, FEMS Yeast Res., 8, 877-882, doi: 10.1111/j.1567-1364.2008.00420.x.
  37. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage, Nature, 227, 680-685, doi: 10.1038/227680a0.
  38. Mruk, D. D., and Cheng, C. Y. (2011) Enhanced chemiluminescence (ECL) for routine immunoblotting, Spermatogenesis, 1, 121-122, doi: 10.4161/spmg.1.2.16606.
  39. Kulak, N. A., Pichler, G., Paron, I., Nagaraj, N., and Mann, M. (2014) Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells, Nat. Methods, 3, 319-324, doi: 10.1038/nmeth.2834.
  40. Sherman, F., Fink, G. R., and Hicks, J. B. (1986) Methods in Yeast Genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor Press, New York.
  41. Kulaev, I. S. (1979) The Biochemistry of Inorganic Polyphosphates, 1st Edn, Wiley.
  42. Andreeva, N., Ryazanova, L., Dmitriev, V., Kulakovskaya, T., and Kulaev, I. (2013) Adaptation of Saccharomyces cerevisiae to toxic manganese concentration triggers changes in inorganic polyphosphates, FEMS Yeast Res., 13, 463-470, doi: 10.1111/1567-1364.12049.
  43. Andreeva, N., Ryazanova, L., Dmitriev, V., Kulakovskaya, T., and Kulaev, I. (2014) Cytoplasmic inorganic polyphosphate participates in the heavy metal tolerance of Cryptococcus humicola, Folia Microbiol. (Praha), 59, 381-389, doi: 10.1007/s12223-014-0310-x.
  44. Trilisenko, L. V., Kulakovskaya, E. V., and Kulakovskaya, T. V. (2017) The cadmium tolerance in Saccharomyces cerevisiae depends on inorganic polyphosphate, J. Basic Microbiol., 57, 982-986, doi: 10.1002/jobm.201700257.
  45. Gerasimaitė, R., and Mayer, A. (2016) Enzymes of yeast polyphosphate metabolism: structure, enzymology and biological roles, Biochem. Soc. Trans., 44, 234-239, doi: 10.1042/BST20150213.
  46. Mundt, J. M., Hah, S. S., Sumbad, R. A., Schramm, V., and Henderson, P. T. (2008) Incorporation of extracellular 8-oxodG into DNA and RNA requires purine nucleoside phosphorylase in MCF-7 cells, Nucleic Acids Res., 36, 228-236, doi: 10.1093/nar/gkm1032.
  47. Doi, K., and Uetsuka, K. (2011) Mechanisms of mycotoxin-induced neurotoxicity through oxidative stress-associated pathways, Int. J. Mol. Sci., 12, 5213-5237, doi: 10.3390/ijms12085213.
  48. Hajam, Y. A., Rani, R., Ganie, S. Y., Sheikh, T. A., Javaid, D., Qadri, S. S., Pramodh, S., Alsulimani, A., Alkhanani, M. F., Harakeh, S., Hussain, A., Haque, S., and Reshi, M. S. (2022) Oxidative stress in human pathology and aging: molecular mechanisms and perspectives, Cells, 11, 552, doi: 10.3390/cells11030552.
  49. Shan, X., Chang, Y., and Lin, C. G. (2007) Messenger RNA oxidation is an early event preceding cell death and causes reduced protein expression, FASEB J., 21, 2753-2764, doi: 10.1096/fj.07-8200com.
  50. Tanaka, M., Chock, P. B., and Stadtman, E. R. (2007) Oxidized messenger RNA induces translation errors, Proc. Natl. Acad. Sci. USA, 104, 66-71, doi: 10.1073/pnas.0609737104.
  51. Nunomura, A., Honda, K., Takeda, A., Hirai, K., Zhu, X., Smith, M. A., and Perry, G. (2006) Oxidative damage to RNA in neurodegenerative diseases, J. Biomed. Biotechnol., 2006, 82323, doi: 10.1155/JBB/2006/82323.
  52. Martinet, W., de Meyer, G. R. Y., Herman, A. G., and Kockx, M. M. (2004) Reactive oxygen species induce RNA damage in human atherosclerosis, Eur. J. Clin. Invest., 34, 323-327, doi: 10.1111/j.1365-2362.2004.01343.x.
  53. Liu, M., Gong, X., Alluri, R. K., Wu, J., Sablo, T., and Li, Z. (2012) Characterization of RNA damage under oxidative stress in Escherichia coli, Biol. Chem., 393, 123-132, doi: 10.1515/hsz-2011-0247.
  54. Nakatsu, Y., and Sekiguchi, M. (2006) Oxidative Damage to Nucleotide: Consequences and Preventive Mechanisms, in Oxidative Stress, Disease and Cancer (Singh, K. K., ed.) Imperial College Press, London, pp. 221-252.
  55. Kanazawa, K., Sakamoto, M., Kanazawa, K., Ishigaki, Y., Aihara, Y., Hashimoto, T., and Mizuno, M. (2016) Lipid peroxides as endogenous oxidants forming 8-oxo-guanosine and lipid soluble antioxidants as suppressing agents, J. Clin. Biochem. Nutr., 59, 16-24, doi: 10.3164/jcbn.15-122.
  56. Estevez, M., Valesyan, S., Jora, M., Limbach, P. A., and Addepalli, B. (2021) Oxidative damage to RNA is altered by the presence of interacting proteins or modified nucleosides, Front. Mol. Biosci., 8, 697149, doi: 10.3389/fmolb.2021.697149.
  57. Jones, D. P. (2008) Radical-free biology of oxidative stress, Am. J. Physiol. Cell. Physiol., 295, C849-868, doi: 10.1152/ajpcell.00283.2008.
  58. Егоров С. Н., Семенова И. Н., Максимов В. Н. (2000) Взаимное влияние инвертазы и кислой фосфатазы дрожжей Saccharomyces cerevisiae на их секрецию в среду культивирования, Микробиология (Москва), 69, 34-37.
  59. Горковский А.А. (2009) Выявление и частичная характеристика белков клеточной стенки дрожжей Saccharomyces cerevisiae, обладающих свойствами амилоидов. Дис. канд. биол. наук. ИБФМ, Пущино.
  60. Kalebina, T. S., Laurinavichiute, D. K., Packeiser, A. N., Morenkov, O. S., Ter-Avanesyan, M. D., and Kulaev, I.S. (2002) Correct GPI-anchor synthesis is required for the incorporation of endoglucanase/glucanosyltransferase Bgl2p into the Saccharomyces cerevisiae cell wall, FEMS Microbiol. Lett., 210, 81-85, doi: 10.1111/j.1574-6968.2002.tb11163.x.
  61. Basu, A., Chaudhuri, P., Malakar, D., and Ghosh, A. K. (2007) Co-purification of glucanase with acid trehalase-invertase aggregate in Saccharomyces cerevisiae, Biotechnol. Lett., 30, 299-304, doi: 10.1007/s10529-007-9535-y.

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