STRATEGY OF PROGRAMMED CELL DEATH IN PROKARYOTES

Cover Page


Cite item

Full Text

Abstract

Programmed cell death (PCD) was first studied in eukaryotic organisms. This system also operates in the development life cycle of prokaryotes. The system PCD in microorganisms is activated a wide range of signals in response to the stresses associated with adverse environmental conditions or exposure to antibacterial agents. The results of numerous studies in the past decade allow considering the system PCD in prokaryotes as an evolutionary conservation of the species. These results significantly expanded understanding of the role of PCD in microorganisms and opened a number of important areas of research of the morphological and molecular genetic approaches to the study of death strategies for the survival in bacterial populations. The purpose of the review is to summarize the morphological and molecular genetic characteristics of PCD in prokaryotes which are real manifestations of the mechanisms of this phenomenon. 

About the authors

B. G. Andrukov

690087, Russian Federation, Vladivostok, Selskaya str., 1, Somov Research Institute of Epidemiology and Microbiology, Siberian Branch of RAMS.

Author for correspondence.
Email: andrukov_bg@mail.ru

PhD, MD (Medicine), Leading Researcher, Laboratory of Molecular Epidemiology and Microbiology, Somov Research Institute of Epidemiology and Microbiology, Siberian Branch of RAMS, Vladivostok, Russian Federation;

Russian Federation

L. M. Somova

690087, Russian Federation, Vladivostok, Selskaya str., 1, Somov Research Institute of Epidemiology and Microbiology, Siberian Branch of RAMS.

Email: fake@neicon.ru

PhD, MD (Medicine), Professor, Director of Somov Research Institute of Epidemiology and Microbiology, Siberian Branch of RAMS, Vladivostok, Russian Federation;

Russian Federation

N. F. Timchenko

690087, Russian Federation, Vladivostok, Selskaya str., 1, Somov Research Institute of Epidemiology and Microbiology, Siberian Branch of RAMS.

Email: fake@neicon.ru

PhD, MD (Medicine), Professor, Leading Researcher, Laboratory of Molecular Epidemiology
and Microbiology, Somov Research Institute of Epidemiology and Microbiology, Siberian Branch of RAMS, Vladivostok, Russian Federation.

Russian Federation

References

  1. Абатуров А.Е., Волосовец А.П., Юлиш Е.И. Роль NOD-подобных рецепторов в рекогниции патоген-ассоциированных молекулярных структур инфекционных патогенных агентов и развитии воспаления. Здоровье ребенка (Украина). 2013. Т. 47, No 4. С. 7–13. [Abaturov A.E., Volosovets A.P., Yulish E.I. The role of NOD-like receptor in recognition of pathogenassociated molecular structures of infectious pathogens and the development of inflammation. Zdorov’e rebenka (Ukraina) = Child Health (Ukraine), 2013, vol. 47, no. 4, pp. 7–13. (In Russ.)]
  2. Андрюков Б.Г., Тимченко Н.Ф. Апоптоз-модулирующие стратегии детерминант патогенности иерсиний // Здоровье. Медицинская экология. Наука. 2015. Т. 59, No 1. С. 29–40. [Andryukov B.G., Timchenko N.F. Apoptosis-modulating strategy determinants of virulence of Yersinia. Zdorov’e. Meditsinskaya ekologiya. Nauka = Health. Medical ecology. Science, 2015, vol. 59, no. 1, pp. 29–40. (In Russ.)]
  3. Сомова Л.М., Бузолева Л.С., Исаченко А.С., Сомов Г.П. Адаптивные ультраструктурные изменения бактерий Yersinia pseudotuberculosis при обитании в почве // Журнал микробиологии, эпидемиологии и иммунобиологии. 2006. No 3. С. 36–40. [Somova L.M., Buzoleva L.S., Isachenko A.S., Somov G.P. Adaptive ultrastructural changes Yersinia pseudotuberculosis at habitation in soil. Zhurnal mikrobiologii, epidemiologii i immunobiologii = Journal of Microbiology, Epidemiology and Immunobiology, 2006, no. 3, pp. 36–40. (In Russ.)]
  4. Сомова Л.М., Бузолева Л.С., Плехова Н.Г. Ультраструктура патогенных бактерий в разных экологических условиях. Владивосток: Медицина ДВ, 2009. 200 с. [Somova L.M., Buzoleva L.S., Plekhova N.G. Ul’trastruktura patogennykh bakterii v raznykh ekologicheskikh usloviyakh [Ultrastructure of pathogenic bacteria in different ecological conditions]. Vladivostok: Far East Medicine, 2009, 200 p.]
  5. Ackermann S., Hiller S., Osswald H., Lösle M., Grenz A., Hambrock A. 17beta-estradiol modulates apoptosis in pancreatic betacells by specific involvement of the sulfonylurea receptor (SUR) isoform SUR1. J. Biol. Chem., 2009, vol. 284, no. 8, pp. 4905–4913.
  6. Adler E., Barak I., Stragier P. Bacillus subtilis locus encoding a killer protein and its antidote. J. Bacteriol., 2001, vol. 183, pp. 3574–3581.
  7. Aguiló N., Marinova D., Martín C., Pardo J. ESX-1-induced apoptosis during mycobacterial infection: to be or not to be, that is the question. Front Cell Infect. Microbiol., 2013, vol. 3, pp. 80–88.
  8. Bos J., Yakhnina A.A., Gitai Z. BapE DNA endonuclease induces an apoptotic-like response to DNA damage in Caulobacter. Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 18096–18101.
  9. Buts L., Lah J., Dao-Thi M.-H., Wyns L., Loris R. Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci., 2005, vol. 30, no. 12, pp. 672–679.
  10. Camacho D.M., Kohanski M.A., Callura J.M., Collins J.J. Antibiotic-induced bacterial cell death exhibits physiological and biochemical hallmarks of apoptosis. Mol. Cell, 2012, vol. 46, no. 5, pp. 561–572.
  11. Camougrand N., Kissová I., Velours G., Manon S. Uth1p: a yeast mitochondrial protein at the crossroads of stress, degradation and cell death. FEMS Yeast Res., 2004, vol. 5, no. 2, pp. 133–140.
  12. Carmona-Gutierrez D., Eisenberg T., Buttner S., Meisinger C., Kroemer G., Madeo F. Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ., 2010, vol. 17, no. 5, pp. 763–773.
  13. Cellini L., Robuffo I., Maraldi N.M., Donelli G. Searching the point of no return in Helicobacter pylori life: necrosis and/or programmed death? J. Appl. Microbiol., 2001, vol. 90, pp. 727–732.
  14. Chatterjee I., Neumayer D., Herrmann M. Senescence of staphylococci: using functional genomics to unravel the roles of ClpC ATPase during late stationary phase. Int. J. Med. Microbiol., 2010, vol. 300, no. 2–3, pp. 130–136.
  15. Chaumorcel M., Lussignol M., Mouna L., Cavignac Y., Fahie K., Cotte-Laffitte J., Geballe A., Brune W., Beau I., Codogno P., Esclatine A. The human cytomegalovirus protein TRS1 inhibits autophagy via its interaction with Beclin 1. J. Virol., 2012, vol. 86, no. 5, pp. 2571–2584.
  16. Christensen M.E., Jansen E.S., Sanchez W., Waterhouse N.J. Flow cytometry based assays for the measurement of apoptosisassociated mitochondrial membrane depolarisation and cytochrome c release. Methods, 2013, vol. 61, no. 2, pp. 138–145.
  17. Christensen S.K., Pedersen K., Hansen F.G., Gerdes K. Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J. Mol. Biol., 2003, vol. 332, pp. 809–819.
  18. D’Amelio M., Sheng M., Cecconi F. Caspase-3 in the central nervous system: beyond apoptosis. Trends Neurosci., 2012, vol. 35, no. 11, pp. 700–709.
  19. Danelishvili L., Bermudez L.E. Analysis of pyroptosis in bacterial infection. Methods Mol. Biol., 2013, vol. 1004, pp. 67–73.
  20. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell, 2004, vol. 116, no. 2, pp. 205–219.
  21. Declercq W., Vanden-Berghe T., Vandenabeele P. RIP kinases at the crossroads of cell death and survival. Cell, 2009, vol. 138, no. 2, pp. 229–232.
  22. De la Cruz M. A., Zhao W., Farenc C., Gimenez G., Raoult D., Cambillau C., Gorvel J.-P., Méresse S. A toxin-antitoxin module of Salmonella promotes virulence in mice. PLOS pathogens, 2013, vol. 9, no. 12, p. e1003827.
  23. Deleo V. Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis (London), 2004, vol. 9, pp. 399–413.
  24. Denton D., Aung-Htut M.T., Kumar S., Baehrecke E.H. Developmentally programmed cell death in Drosophila. Biochim. Biophys. Acta, 2013, vol. 1833, no. 12, pp. 3499–3506.
  25. Denton D., Chang T.K., Nicolson S., Shravage B., Simin R., Baehrecke E.H., Kumar S. Relationship between growth arrest and autophagy in midgut programmed cell death in Drosophila. Cell Death Differ., 2012, vol. 19, no. 8, pp. 1299–1307.
  26. Dunin-Horkawicz S., Kopec K.O., Lupas A.N. Prokaryotic ancestry of eukaryotic protein networks mediating innate immunity and apoptosis. J. Mol. Biol., 2014, vol. 426, no. 7, pp.1568–1582.
  27. Dwyer D.J., Kohanski M.A., Hayete B., Collins J.J. Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol. Syst. Biol., 2007, vol. 3, p. 91.
  28. Eckardt J., Lorek M., Zimmer G. The fusion protein of respiratory syncytial virus triggers p53-dependent apoptosis. J. Virol., 2008, vol. 82, no. 7, pp. 3236–3249.
  29. Engelberg-Kulka H., Amitai S., Reches M., Sat B., Hazan R. Bacterial programmed cell death as a target for antibiotics. Trends Microbiol., 2004, vol. 12, рр. 66–71.
  30. Engelberg-Kulka H., Kolodkin-Gal I., Amitai S., Hazan R. Bacterial programmed cell death and multicellular behavior in bacteria. PLOS Genet., 2006, vol. 2, no. 10, p. e135.
  31. Erental A., Idith Sh.I., Engelberg-Kulka H. Two programmed cell death systems in Escherichia coli: an apoptotic-like dеath is inhibited by the mazEF-mediated death pathway. PLOS Biology, 2012, vol. 10, no. 3, p. e1001281.
  32. Fineran P.C., Blower T.R., Foulds I.J., Humphreys D.P., Lilley K.S. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 894–899.
  33. Fink S.L., Cookson B.T. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol., 2006, vol. 8, no. 11, pp. 1812–1825.
  34. Fu Z., Tamber S., Memmi G., Donegan N.P. Cheung A.L. Overexpression of MazFsa in Staphylococcus aureus induces bacteriostasis by selectively targeting mRNAs for cleavage. J. Bacteriol. 2012, vol. 191, pp. 2051–2059.
  35. Galluzzi L., Kepp O., Krautwald S., Kroemer G., Linkermann A. Molecular mechanisms of regulated necrosis. Semin. Cell Dev. Biol., 2014, vol. 35, pp. 24–32.
  36. Gautam S., Sharma A. Rapid cell death in Xanthomonas campestris pv. glycines. J. Gen. Appl. Microbiol., 2002, vol. 48, no. 2, pp. 67–76.
  37. Gertz S., Engelmann S., Schmid R., Ohlsen K., Hacker J., Hecker M. Regulation of σB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains. Mol. Gen. Genet., 1999, vol. 261, pp. 558–566.
  38. Giansanti V., Torriglia A., Scovassi A.I. Conversation between apoptosis and autophagy: «Is it your turn or mine?». Apoptosis, 2011, vol. 16, no. 4, pp. 321–333.
  39. Godoy V.G., Jarosz D.F., Walker F.L., Simmons L.A., Walker G. Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression. EMBO J., 2006, vol. 25, pp. 868–879.
  40. Gómez-Fernández J.C. Functions of the C-terminal domains of apoptosis-related proteins of the Bcl-2 family. Chem. Phys. Lipids, 2014, vol. 183, pp. 77–90.
  41. Goulard C., Langrand S., Chauvaux S. Yersinia pestis chromosome encodes active addiction toxins. J. Bacteriol., 2010, vol. 192, no. 14, pp. 3669–3677.
  42. Green D.R., Oberst A., Dillon C.P., Weinlich R., Salvesen G.S. RIPK-dependent necrosis and its regulation by caspases: a mystery in five acts. Mol. Cell, 2011, vol. 44, no. 1, pp. 9–16.
  43. Guilhelmelli F., Vilela N., Albuquerque P., Derengowski L.D., Silva-Pereira I., Kyaw C.M. Antibiotic development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance. Front Microbiol., 2013, vol. 4, 353 p.
  44. Guiral S., Mitchell T.J., Martin B., Claverys J.P. Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc. Natl. Acad. Sci. USA, 2005, vol. 14, pp. 8710–8715.
  45. Han K.D., Ahn D.H., Lee S.A., Min Y.H., Kwon A.R., Ahn H.C., Lee B.J. Identification of chromosomal HP0892-HP0893 toxin-antitoxin proteins in Helicobacter pylori and structural elucidation of their protein-protein interaction. J. Biol. Chem., 2013, vol. 288, no. 8, pp. 6004–6013.
  46. Hayes F. Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science, 2003, vol. 301, pp. 1496–1499.
  47. Hayes F., Van Melderen L. Toxins-antitoxins: diversity, evolution and function. Crit. Rev. Biochem. Mol. Biol., 2011, vol. 46, no. 5, pp. 386–408.
  48. Hazan R., Sat B., Engelberg-Kulka H. Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol., 2004, vol. 186, pp. 3663–3669.
  49. Hotchkiss R.S., Strasser A., McDunn J.E., Swanson P.E. Cell death in disease: mechanisms and emerging therapeutic concepts. N. Engl. J. Med., 2009, vol. 361, pp. 1570–1583.
  50. Kamat P.K., Kalani A., Kyles P., Tyagi S.C., Tyagi N. Autophagy of Mitochondria: A promising therapeutic target for neurodegenerative disease. Cell Biochem. Biophys., 2014, vol. 70, no. 2, pp. 707–719.
  51. Kang J., Pervaiz S. Crosstalk between Bcl-2 family and Ras family small GTPases: potential cell fate regulation? Front Oncol., 2013, vol. 2, 206 p.
  52. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Brit. J. Cancer, 1972, vol. 26, pp. 239–257.
  53. Klionsky D.J., Codogno P. The mechanism and physiological function of macroautophagy. J. Innate Immun., 2013, vol. 5, no. 5, pp. 427–433.
  54. Kolodkin-Gal I., Sat B., Keshet A., Engelberg-Kulka H. The communication factor EDF and the toxin-antitoxin module mazEF determine the mode of action of antibiotics. PLOS Biol., 2008, vol. 16, no. 6, p. e319.
  55. Koonin E.V., Aravind L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ., 2002, vol. 9, no. 4, pp. 394–404.
  56. Labbé K., Saleh M. Cell death in the host response to infection. Cell Death Differ., 2008, vol. 15, no. 9, pp. 1339–1349.
  57. Leplae R., Geeraerts D., Hallez R., Guglielmini J., Drèze P. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Research, 2011, vol. 39, pp. 5513–5525.
  58. Lewis K. Programmed death in bacteria. Microbiol. Mol. Biol. Rev., 2002, vol. 64, pp. 503–514.
  59. Loewith R., Hall M.N. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics, 2011, vol. 189, no. 4, pp. 1177–1201.
  60. Ludovico P. Overeating yeast display fatty acid-induced necrotic cell death. Cell Cycle, 2010, vol. 9, no. 15, 2929 p.
  61. Makarova K.S., Wolf Y.I., Koonin E.V. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct., 2009, vol. 4, pp. 11–19.
  62. Manteca A., Fernandez M., Sanchez J. Cytological and biochemical evidence for an early cell dismantling event in surface cultures of Streptomyces antibioticus. Res. Microbiol., 2006, vol. 157, no. 2, pp. 143–152.
  63. Marino G., Niso-Santano M., Baehrecke E.H., Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nature Rev. Mol. Cell Biol., 2014, vol. 15, pp. 81–94.
  64. Marino M.L., Pellegrini P., Di Lernia G., Djavaheri-Mergny M., Brnjic S., Zhang X., Hägg M., Linder S., Fais S., Codogno P., De Milito A. Autophagy is a protective mechanism for human melanoma cells under acidic stress. J. Biol. Chem., 2012, vol. 287, no. 36, pp. 30664–30676.
  65. Masuda H., Tan Q., Awano N., Wu K.P., Inouye M. YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol. Microbiol., 2012, vol. 84, pp. 979–989.
  66. Mavrianos J., Berkow E.L., Desai C., Pandey A., Batish M., Rabadi M.J., Barker K.S., Pain D., Rogers P.D., Eugenin E.A., Chauhan N. Mitochondrial two-component signaling systems in Candida albicans. Eukaryot. Cell, 2013, vol. 12, no. 6, pp. 913–922.
  67. Nancy A. Eukaryote programmed cell death in plants: a role for mitochondrial-associated hexokinases. Plant Cell, 2006, vol. 18, pp. 2097–2099.
  68. Nariya H., Inouye M. MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell, 2008, vol. 32, pp. 55–66.
  69. Nolle N., Schuster C.F., Bertram R. Two paralogous yefM-yoeB loci from Staphylococcus equorum encode functional toxinantitoxin systems. Microbiology, 2013, vol. 159, no. 8, pp. 1575–1585.
  70. Norton J.P., Mulvey M.A. Toxin-antitoxin systems are important for niche-specific colonization and stress resistance of uropathogenic Escherichia coli. PLOS Pathog., 2012, vol. 8, p. e1002954.
  71. Nyström T. Nonculturable bacteria: programmed survival forms or cells at death’s door? Bioessays, 2003, vol. 25, pp. 204–211.
  72. Pandey D.P., Gerdes K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Research, 2005, vol. 33, pp. 966–976.
  73. Park J.H., Yamaguchi Y., Inouye M. Bacillus subtilis MazF-bs (EndoA) is a UACAU-specific mRNA interferase. FEBS Lett., 2011, vol. 585, pp. 2526–2532.
  74. Pedersen K., Christensen S.K., Gerdes K. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol. Microbiol., 2002, vol. 45, pp. 501–510.
  75. Port U., Brovkin V., Claussen M. The influence of vegetation dynamics on anthropogenic climate change. Earth Syst. Dynam., 2012, vol. 3, pp. 233–243.
  76. Ramage H.R., Connolly L.E., Cox J.S. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLOS Genet., 2009, vol. 5, p. e1000767.
  77. Ramisetty B.C., Natarajan B., Santhosh R.S. MazEF-mediated programmed cell death in bacteria: «What is this?». Crit. Rev. Microbiol., 2015, vol. 41, no. 1, pp. 89–100.
  78. Rice K.C., Bayles K.W. Molecular control of bacterial death and lysis. Microbiol. Mol. Biol. Rev., 2008, vol. 72, pp. 85–109.
  79. Robertson C.L., Scafidi S., McKenna M.C., Fiskum G. Mitochondrial mechanisms of cell death and neuroprotection in pediatric ischemic and traumatic brain injury. Exp. Neurol., 2009, vol. 218, no. 2, pp. 371–380.
  80. Rostovtseva T.K., Tan W., Colombini M. On the role of VDAC in apoptosis: fact and fiction. J. Bioenerg. Biomembr., 2005, vol. 37, pp. 129–142.
  81. Rothenbacher F.P. Clostridium difficile MazF toxin exhibits selective, not global, mRNA cleavage. J. Bacteriol., 2012, vol. 194, pp. 3464–3474.
  82. Ryter S.W., Mizumura K., Choi A.M. The impact of autophagy on cell death modalities. Int. J. Cell. Biol., 2014, vol. 2014, p. е502676.
  83. Samejima K., Earnshaw W.C. Trashing the genome: the role of nucleases during apoptosis. Nat. Rev. Mol. Cell. Biol., 2005, vol. 6, no. 9, pp. 677–688.
  84. Shamas-Din A., Brahmbhatt H., Leber B., Andrews D.W. BH3-only proteins: orchestrators of apoptosis. Biochim. Biophys. Acta, 2011, vol. 1813, no. 4, pp. 508–520.
  85. Shemarova I.V. Phosphoinositide signaling in unicellular eukarуotes. Crit. Rev. Microbiol., 2007, vol. 33, pp. 141–156.
  86. Søgaard-Andersen L., Yang Z. Programmed cell death: role for MazF and MrpC in Myxococcus multicellular development. Curr. Biol., 2008, vol. 18, pp. 337–339.
  87. Tait S.W., Green D.R. Mitochondrial regulation of cell death. Cold Spring Harb. Perspect. Biol., 2013, vol. 5, no. 9, p. a008706.
  88. Tanouchi Y., Lee A.J., Meredith H., You L. Programmed cell death in bacteria and implications for antibiotic therapy. Trends Microbiol., 2013, vol. 21, no. 6, рр. 265–270.
  89. Ulukaya E., Acilan C., Yilmaz Y. Apoptosis: why and how does it occur in biology? Cell. Biochem. Funct., 2011, vol. 29, no. 6, pp. 468–480.
  90. Van Loo G., Saelens X., Van Gurp M., MacFarlane M., Martin S.J., Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ., 2002, vol. 9, pp. 1031–1042.
  91. Wang X., Lord D.M., Cheng H.Y., Osbourne D.O., Hong S.H. A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol., 2012, vol. 8, pp. 855–861.
  92. Wardhawan S., Gautam S., Sharma A. Involvement of proline oxidase (PutA) in programmed cell death of Xanthomonas. PLOS One, 2014, vol. 9, no. 5, p. e96423.
  93. Weely H., Yoshida R., Kudoh S., Hasegawa K., Niimori-Kita K., Ito T. Regulator of calcineurin 1-1L protects cardiomyocytes against hypoxia-induced apoptosis via mitophagy. Trends Microbiol., 2010, vol. 13, pp. 169–182.
  94. Williams K., Gokulan K., Shelman D., Akiyama T., Khan A., Khare S. Cytotoxic mechanism of cytolethal distending toxin in nontyphoidal salmonella serovar (Salmonella javiana) during macrophage infection. DNA Cell Biol., 2015, vol. 34, no. 2, рр. 113–124.
  95. Wu W., Liu P., Li J. Necroptosis: an emerging form of programmed cell death. Crit. Rev. Oncol. Hematol., 2012, vol. 82, no. 3, pp. 249–258.
  96. Wu Y.C., Wang X., Xue D. Methods for studying programmed cell death in C. elegans. Methods Cell. Biol., 2012, vol. 10, pp. 295–320.
  97. Yagüe P., López-García M.T., Rioseras B., Sánchez J.A. Pre-sporulation stages of Streptomyces differentiation: state-of-the-art and future perspectives. FEMS Microbiol. Lett., 2013, vol. 342, no. 2, pp. 79–88.
  98. Yamaguchi Y., Park J.H., Inouye M. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet., 2011, vol. 45, pp. 61–79.
  99. Yuan J., Kroemer G. Alternative cell death mechanisms in development and beyond. Genes Dev., 2010, vol. 24, pp. 2592–2602.
  100. Zorzini V., Buts L., Sleutel M., Garcia-Pino A., Talavera A. Structural and biophysical characterization of Staphylococcus aureus SaMazF shows conservation of functional dynamics. Nucleic Acids Research, 2014, vol. 42, no. 10, pp. 6709–6725.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2015 Andrukov B.G., Somova L.M., Timchenko N.F.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies