microbeПроблемы особо опасных инфекцийProblems of Particularly Dangerous Infections0370-10692658-719XRussian Research Anti-Plague Institute “Microbe”10.21055/0370-1069-2009-4(102)-54-59microbe-962Research ArticleМИКРОБИОЛОГИЯ, ИММУНОЛОГИЯ, ПАТОГЕНЕЗMICROBIOLOGY, IMMUNOLOGY, PATHOGENESISМежклеточная коммуникация quorum sensing у патогенных бактерий рода YersiniaIntercellular Communication Quorum Sensing in Pathogenic Bacteria of the Genus YersiniaКуклеваЛ. М.KouklevaL. M.microbe@san.ruЕрошенкоГ. А.EroshenkoG. A.noemail@neicon.ruРоссийский научно-исследовательский противочумный институт «Микроб»РоссияRussian Research Anti-Plague Institute MicrobeRussian Federation20092008200904(102)5459Copyright © Куклева Л.М., Ерошенко Г.А., 20092009Куклева Л.М., Ерошенко Г.А.Koukleva L.M., Eroshenko G.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://journal.microbe.ru/jour/article/view/962

В обзоре рассмотрены ключевые элементы системы quorum sensing у грамотрицательных бактерий, а также суммированы имеющиеся в литературе данные об особенностях функционирования системы межклеточной коммуникации у трех патогенных иерсиний - Yersinia enterocolitica, Y. pseudotuberculosis и Y. pestis.

The present review considered key elements of quorum sensing system of gram-negative bacteria and summarized the existing literature data on functioning features of intercellular communication system in three pathogenic Yersinia -Yersinia enterocolitica, Y. pseudotuberculosis and Y. pestis.

патогенные иерсиниисистема межклеточной коммуникациисигнальные молекулывоздействие quorum sensing на жизнедеятельность и вирулентные свойстваpathogenic Yersiniaintercellular communication systemsignal moleculesquorum sensing effect upon housekeeping and virulent propertiesReferencesИльина Т.С., Романова ЮМ., Гинцбург А.Л. Биопленка как способ существования бактерий в окружающей среде и организме хозяина: феномен, генетический контроль и системы регуляции их развития. Генетика. 2004; 40(11):1-12.Ильина Т.С., Романова ЮМ., Гинцбург А.Л. Биопленка как способ существования бактерий в окружающей среде и организме хозяина: феномен, генетический контроль и системы регуляции их развития. Генетика. 2004; 40(11):1-12.Ильина Т.С. Романова ЮМ., Гинцбург А.Л Системы коммуникаций у бактерий и их роль в патогенезе. Мол. генет., микробиол. и вирусол. 2006; 3:22-9.Ильина Т.С. Романова ЮМ., Гинцбург А.Л Системы коммуникаций у бактерий и их роль в патогенезе. Мол. генет., микробиол. и вирусол. 2006; 3:22-9.Atkinson S., Throup J., Stewart G., Williams P. A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol. Microbiol. 1999; 33:1267-77.Atkinson S., Throup J., Stewart G., Williams P. A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol. Microbiol. 1999; 33:1267-77.Atkinson S., Chang C., Sockett R. et al. Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J. Bacteriol. 2006; 188:1451-61.Atkinson S., Chang C., Sockett R. et al. Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J. Bacteriol. 2006; 188:1451-61.Atkinson S., Sockett R., Camara M., Williams P. Quorum sensing and lifestyle of Yersinia. Curr. Issues Mol. Biol. 2006; 8(1):1-10.Atkinson S., Sockett R., Camara M., Williams P. Quorum sensing and lifestyle of Yersinia. Curr. Issues Mol. Biol. 2006; 8(1):1-10.Atkinson S., Chang C., Patrick H. et al. Functional interplay between the Yersinia pseudotuberculosis YpsRI and YtbRI quorum sensing systems modulates swimming motility by controlling expression of flhDC and fliA. Mol. Microbiol. 2008; 69(1):137-51.Atkinson S., Chang C., Patrick H. et al. Functional interplay between the Yersinia pseudotuberculosis YpsRI and YtbRI quorum sensing systems modulates swimming motility by controlling expression of flhDC and fliA. Mol. Microbiol. 2008; 69(1):137-51.Bassler B. Small talk. Cell-to-cell communication in bacteria. Cell. 2002; 109(4):421-4.Bassler B. Small talk. Cell-to-cell communication in bacteria. Cell. 2002; 109(4):421-4.Bobrov A., Bearden S., Fetherston J. et al. Functional quorum sensing systems affect biofilm formation and protein expression in Yersinia pestis. Adv. Exp. Med. Biol. 2007; 603:178-97.Bobrov A., Bearden S., Fetherston J. et al. Functional quorum sensing systems affect biofilm formation and protein expression in Yersinia pestis. Adv. Exp. Med. Biol. 2007; 603:178-97.Chen Z., Li B., Zhang J. et al. Quorum sensing affects virulence-associated proteins FI, LcrV, KatY and pH6 etc of Yersinia pestis as revealed by protein microarray-based antibody profiling. Microbes Infect. 2006; 8( 9-10):2501-8.Chen Z., Li B., Zhang J. et al. Quorum sensing affects virulence-associated proteins FI, LcrV, KatY and pH6 etc of Yersinia pestis as revealed by protein microarray-based antibody profiling. Microbes Infect. 2006; 8( 9-10):2501-8.Deng W., Burland V., Plunkett G. et al. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 2002; 184:4601-11.Deng W., Burland V., Plunkett G. et al. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 2002; 184:4601-11.Egland K., Greenberg E. Quorum sensing in Vibrio fischeri: elements of the luxI promoter. Mol. Microbiol. 1999; 31:1197-204.Egland K., Greenberg E. Quorum sensing in Vibrio fischeri: elements of the luxI promoter. Mol. Microbiol. 1999; 31:1197-204.Fukua W., Winans S., Greenberg E. Quorum sensing in bacteria: the LuxR LuxI family of cell density responsive transcriptional regulators. J. Bacteriol. 1994; 176:269-75.Fukua W., Winans S., Greenberg E. Quorum sensing in bacteria: the LuxR LuxI family of cell density responsive transcriptional regulators. J. Bacteriol. 1994; 176:269-75.Fukua W.,Winans S., Greenberg E. Census and consensus in bacterial ecosystems: the LuxR LuxI family of quorum sensing transcriptional regulators. A. Rev. Microbiol. 1996; 50:727-51.Fukua W.,Winans S., Greenberg E. Census and consensus in bacterial ecosystems: the LuxR LuxI family of quorum sensing transcriptional regulators. A. Rev. Microbiol. 1996; 50:727-51.Fukua C., Parsek M., Greenberg E. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 2001; 35:439-68.Fukua C., Parsek M., Greenberg E. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 2001; 35:439-68.Gelhaus H., Rozak D., Nierman W. et al. Exogenous Yersinia pestis quorum sensing molecules N-octanoyl-homoserine lactone and N-(3-oxooctanoyl)-homoserine lactone regulate the LcrV virulence factor. Microb. Pathog. 2009; 46(5):283-7.Gelhaus H., Rozak D., Nierman W. et al. Exogenous Yersinia pestis quorum sensing molecules N-octanoyl-homoserine lactone and N-(3-oxooctanoyl)-homoserine lactone regulate the LcrV virulence factor. Microb. Pathog. 2009; 46(5):283-7.Girón J., Torres A., Freer E., Kaper J. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 2002; 44(2):361-79.Girón J., Torres A., Freer E., Kaper J. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 2002; 44(2):361-79.Gonzalez J., Keshavan N. Messing with bacterial quorum sensing. Microbiol. Mol. Biol. Rev. 2006; 70:859-75.Gonzalez J., Keshavan N. Messing with bacterial quorum sensing. Microbiol. Mol. Biol. Rev. 2006; 70:859-75.Jacobi C., Bach A., Eberi L. et al. Detection of N-(3-oxohexanoyl)-L-homoserine lactone in mice, infected with Yersinia enterocolitica serotype 0:8. Infect. Immun. 2003; 71:6624-6.Jacobi C., Bach A., Eberi L. et al. Detection of N-(3-oxohexanoyl)-L-homoserine lactone in mice, infected with Yersinia enterocolitica serotype 0:8. Infect. Immun. 2003; 71:6624-6.Kievit T., Iglewsky B. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 2000; 68(9):4839-49.Kievit T., Iglewsky B. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 2000; 68(9):4839-49.Kim T., Young B., Young G. Effect of flagellar mutations on Yersinia enterocolitica biofilm formation. Appl. Environ. Microbiol. 2008; 74(17):5466-74.Kim T., Young B., Young G. Effect of flagellar mutations on Yersinia enterocolitica biofilm formation. Appl. Environ. Microbiol. 2008; 74(17):5466-74.Kirwan J., Gould T., Schweizer H. et al. Quorum sensing signal synthesis by Yersinia pestis acyl-homoserine lactone synthase YspI. J. Bacteriol. 2006; 188(2):784-8.Kirwan J., Gould T., Schweizer H. et al. Quorum sensing signal synthesis by Yersinia pestis acyl-homoserine lactone synthase YspI. J. Bacteriol. 2006; 188(2):784-8.Lemon K., Higgins D., Kolter R. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J. Bacteriol. 2007; 189:4418-24.Lemon K., Higgins D., Kolter R. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J. Bacteriol. 2007; 189:4418-24.Lerat E., Moran N. The Evolutionary history of quorum-sensing systems in Bacteria. Mol. Biol. Evol. 2004; 21(5):903-13.Lerat E., Moran N. The Evolutionary history of quorum-sensing systems in Bacteria. Mol. Biol. Evol. 2004; 21(5):903-13.Lazdunski A., Ventre I., Sturgis J. Regulatory circuits and communication in Gram-negative bacteria. Nat. Rev. Microbiol. 2004; 2:581-92.Lazdunski A., Ventre I., Sturgis J. Regulatory circuits and communication in Gram-negative bacteria. Nat. Rev. Microbiol. 2004; 2:581-92.McLean R.J., Pierson L.S. 3rd, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. J. Microbiol. Methods. 2004; 58:351-60.McLean R.J., Pierson L.S. 3rd, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. J. Microbiol. Methods. 2004; 58:351-60.Miller M., Bassler B. Quorum sensing in bacteria. Annu. Rev. Microbiol. 2001; 55:165-99.Miller M., Bassler B. Quorum sensing in bacteria. Annu. Rev. Microbiol. 2001; 55:165-99.Morton M., Garmory H., Perkins S. et al. A Salmonella enterica serovar Typhi vaccine expressing Yersinia pestis F1 antigen on its surface provides protection against plague in mice. Vaccine. 2004; 22:2524-32.Morton M., Garmory H., Perkins S. et al. A Salmonella enterica serovar Typhi vaccine expressing Yersinia pestis F1 antigen on its surface provides protection against plague in mice. Vaccine. 2004; 22:2524-32.Nasser W., Reverchon S. New insights into the regulatory mechanisms of the LuxR family of quorum sensing regulators. Anal. Bioanal. Chem. 2007; 387:381-90.Nasser W., Reverchon S. New insights into the regulatory mechanisms of the LuxR family of quorum sensing regulators. Anal. Bioanal. Chem. 2007; 387:381-90.Ortori C., Atkinson S., Chhabra S. et al. Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal. Bioanal. Chem. 2007; 387:497-511.Ortori C., Atkinson S., Chhabra S. et al. Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal. Bioanal. Chem. 2007; 387:497-511.Parsek M., Val D., Hanzelka B. Acyl homoserine-lactone quorum-sensing signal generation. PNAS. 1999; 96:4360-5.Parsek M., Val D., Hanzelka B. Acyl homoserine-lactone quorum-sensing signal generation. PNAS. 1999; 96:4360-5.Pearson J., Van Delden C., Iglewski B. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 1999; 181:1203-10.Pearson J., Van Delden C., Iglewski B. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 1999; 181:1203-10.Popat R, Crusz S., Diggle S. The social behaviours of bacterial pathogens. British Medical Bulletin. 2008; 87:63-75.Popat R, Crusz S., Diggle S. The social behaviours of bacterial pathogens. British Medical Bulletin. 2008; 87:63-75.Qin Y., Luo Z., Smyth A. , et al. Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm. EMBO J. 2000; 19(19):5212-21.Qin Y., Luo Z., Smyth A. , et al. Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm. EMBO J. 2000; 19(19):5212-21.Salmond G., Bycroft B., Srewart G., Williams P. The bacterial "enigma": cracking the code of cell-cell communication. Mol. Microbiol. 1995; 16:615-24.Salmond G., Bycroft B., Srewart G., Williams P. The bacterial "enigma": cracking the code of cell-cell communication. Mol. Microbiol. 1995; 16:615-24.Schuster M., Urbanowski M., Greenberg E. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc. Natl. Acad. Sci. USA. 2004; 101(45):15833-9.Schuster M., Urbanowski M., Greenberg E. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc. Natl. Acad. Sci. USA. 2004; 101(45):15833-9.Smith R., Harris S., Phipps R., Iglewski B. The Pseudomonas aeruginosa quorum sensing signal molecule, N-(3-oxododecanoyl)-L-homoserine lactone contributes to virulence and induces inflammation in vivo. J. Bacteriol. 2002; 184:1132-9.Smith R., Harris S., Phipps R., Iglewski B. The Pseudomonas aeruginosa quorum sensing signal molecule, N-(3-oxododecanoyl)-L-homoserine lactone contributes to virulence and induces inflammation in vivo. J. Bacteriol. 2002; 184:1132-9.Smith R., Iglewski B. Pseudomonas aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 2003; 6(1):56-60.Smith R., Iglewski B. Pseudomonas aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 2003; 6(1):56-60.Swift S., Isherwood K., Atkinson S. et al. Quorum sensing in Aeromonas and Yersinia. In: England R., Hobbs G., Bainton N., Roberts D. Microbial signaling and communication. Society for general microbiology symposium 57. Cambridge, 1999. P. 85-104.Swift S., Isherwood K., Atkinson S. et al. Quorum sensing in Aeromonas and Yersinia. In: England R., Hobbs G., Bainton N., Roberts D. Microbial signaling and communication. Society for general microbiology symposium 57. Cambridge, 1999. P. 85-104.Swift S., Downie J., Whitehead N. et al. Quorum sensing as a population density dependent determinant of bacterial physiology. Adv. Microb. Physiol. 2001; 45:199-270.Swift S., Downie J., Whitehead N. et al. Quorum sensing as a population density dependent determinant of bacterial physiology. Adv. Microb. Physiol. 2001; 45:199-270.Taga M., Bassler B. Chemical communication among bacteria. PNAS. 2003; 100(Suppl. 2):14549-54.Taga M., Bassler B. Chemical communication among bacteria. PNAS. 2003; 100(Suppl. 2):14549-54.Throup J., Camara M., Briggs G. et al. Characterization of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two quorum sensing signal molecules. Mol. Microbiol. 1995; 17:345-56.Throup J., Camara M., Briggs G. et al. Characterization of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two quorum sensing signal molecules. Mol. Microbiol. 1995; 17:345-56.Urbanowski M., Lostroh C., Greenberg E. Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J. Bacteriol. 2004; 186(3):631-7.Urbanowski M., Lostroh C., Greenberg E. Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J. Bacteriol. 2004; 186(3):631-7.Wang Y., Ding L, Hu Y. et al. The flhDC gene affects motility and biofilm formation in Yersinia pseudotuberculosis. Sci. China C. Life Sci. 2007; 50(6):814-21.Wang Y., Ding L, Hu Y. et al. The flhDC gene affects motility and biofilm formation in Yersinia pseudotuberculosis. Sci. China C. Life Sci. 2007; 50(6):814-21.Watson W., Minogue T., Val D. et al. Structural basis and specificity of acyl homoserine lactone signal production in bacterial quorum sensing. Mol. Cell. 2002; 9:685-94.Watson W., Minogue T., Val D. et al. Structural basis and specificity of acyl homoserine lactone signal production in bacterial quorum sensing. Mol. Cell. 2002; 9:685-94.Whitehead N., Barnard A., Slater H. et al. Quorum sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 2001; 25:365-404.Whitehead N., Barnard A., Slater H. et al. Quorum sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 2001; 25:365-404.Williams P., Camara M., Hardman A. et al. Quorum sensing and the population-dependent control of virulence. Phil. Trans. R. Soc. Lond. B. 2000; 355:667-80.Williams P., Camara M., Hardman A. et al. Quorum sensing and the population-dependent control of virulence. Phil. Trans. R. Soc. Lond. B. 2000; 355:667-80.Winzer K., Hardie K., Williams P. LuxS and autoinducer-2: their contribution to quorum sensing and metabolism in bacteria. Adv. Appl. Microbiol. 2003; 53:291-396.Winzer K., Hardie K., Williams P. LuxS and autoinducer-2: their contribution to quorum sensing and metabolism in bacteria. Adv. Appl. Microbiol. 2003; 53:291-396.Yates E., Philipp B., Buckley C. et al. N-acylhomoserine lactones undergo lactonolysis on pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 2002; 70:5635-46.Yates E., Philipp B., Buckley C. et al. N-acylhomoserine lactones undergo lactonolysis on pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 2002; 70:5635-46.Young G., Badger J., Miller V. Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect. Immun. 2000; 68:4323-6.Young G., Badger J., Miller V. Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect. Immun. 2000; 68:4323-6.

The authors declare that there are no conflicts of interest present.