An extracellular bacterial pathogen modulates host metabolism to regulate its own sensing and proliferation

Cell

Volumn 156, Issue 1-2, 2014, Pages 97-108

  Baruch, Moshe ^a   Belotserkovsky, Ilia ^a   Hertzog, Baruch B ^a   Ravins, Miriam ^a   Dov, Eran ^a   McIver, Kevin S ^b   Le Breton, Yoann S ^b   Zhou, Yiting ^c   Chen, Catherine Youting ^c   Hanski, Emanuel ^a,c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b University of Maryland   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINASE; ASPARTATE AMMONIA LIGASE; STREPTOLYSIN; TOXIN; ALANINE; ASPARAGINE; ASPARTIC ACID; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; GLUTAMIC ACID; PROLINE; TRANSCRIPTOME;

ARTICLE; BACTEREMIA; BACTERIAL GENE; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC CELL; GENE LOCUS; GROUP A STREPTOCOCCAL INFECTION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUORUM SENSING; STREPTOCOCCUS GROUP A; UPREGULATION; A549 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL DEATH; CONTROLLED STUDY; EMBRYO; ENZYME SYNTHESIS; EX VIVO STUDY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HELA CELL LINE; HEMOLYSIS; HOST; HOST CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; L929 CELL LINE; MICROBIAL METABOLISM; MOUSE; NECROPTOSIS; QUANTITATIVE ANALYSIS; RNA SEQUENCE; START CODON; TANDEM MASS SPECTROMETRY; THERAPY EFFECT;

ANIMALS; ASPARAGINE; ASPARTATE-AMMONIA LIGASE; BACTEREMIA; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; HELA CELLS; HUMANS; MALE; MICE; MICE, INBRED BALB C; QUORUM SENSING; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS);

EID: 84892724315     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.12.007     Document Type: Article

References (59)

1. I.P. Barbosa-Tessmann, C. Chen, C. Zhong, S.M. Schuster, H.S. Nick, and M.S. Kilberg Activation of the unfolded protein response pathway induces human asparagine synthetase gene expression J. Biol. Chem. 274 1999 31139 31144
2. I. Belotserkovsky, M. Baruch, A. Peer, E. Dov, M. Ravins, I. Mishalian, M. Persky, Y. Smith, and E. Hanski Functional analysis of the quorum-sensing streptococcal invasion locus (sil) PLoS Pathog. 5 2009 e1000651
3. S.A. Brown, K.L. Palmer, and M. Whiteley Revisiting the host as a growth medium Nat. Rev. Microbiol. 6 2008 657 666
4. J.R. Carapetis, A.C. Steer, E.K. Mulholland, and M. Weber The global burden of group A streptococcal diseases Lancet Infect. Dis. 5 2005 685 694
5. M.A. Chaussee, E.A. Callegari, and M.S. Chaussee Rgg regulates growth phase-dependent expression of proteins associated with secondary metabolism and stress in Streptococcus pyogenes J. Bacteriol. 186 2004 7091 7099
6. S.T. Christensen, J. Chemnitz, E.M. Straarup, K. Kristiansen, D.N. Wheatley, and L. Rasmussen Staurosporine-induced cell death in Tetrahymena thermophila has mixed characteristics of both apoptotic and autophagic degeneration Cell Biol. Int. 22 1998 591 598
7. H.S. Courtney, D.L. Hasty, and J.B. Dale Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci Ann. Med. 34 2002 77 87
8. M.W. Cunningham Pathogenesis of group A streptococcal infections Clin. Microbiol. Rev. 13 2000 470 511
9. C. Cywes Bentley, A. Hakansson, J. Christianson, and M.R. Wessels Extracellular group A Streptococcus induces keratinocyte apoptosis by dysregulating calcium signalling Cell. Microbiol. 7 2005 945 955
10. V. Datta, S.M. Myskowski, L.A. Kwinn, D.N. Chiem, N. Varki, R.G. Kansal, M. Kotb, and V. Nizet Mutational analysis of the group A streptococcal operon encoding streptolysin S and its virulence role in invasive infection Mol. Microbiol. 56 2005 681 695
11. A. Degterev, J. Hitomi, M. Germscheid, I.L. Ch'en, O. Korkina, X. Teng, D. Abbott, G.D. Cuny, C. Yuan, and G. Wagner et al. Identification of RIP1 kinase as a specific cellular target of necrostatins Nat. Chem. Biol. 4 2008 313 321
12. Z.A. Dunai, G. Imre, G. Barna, T. Korcsmaros, I. Petak, P.I. Bauer, and R. Mihalik Staurosporine induces necroptotic cell death under caspase-compromised conditions in U937 cells PLoS ONE 7 2012 e41945
13. A. Gjymishka, N. Su, and M.S. Kilberg Transcriptional induction of the human asparagine synthetase gene during the unfolded protein response does not require the ATF6 and IRE1/XBP1 arms of the pathway Biochem. J. 417 2009 695 703
14. G.D. Glekas, R.M. Foster, J.R. Cates, J.A. Estrella, M.J. Wawrzyniak, C.V. Rao, and G.W. Ordal A PAS domain binds asparagine in the chemotaxis receptor McpB in Bacillus subtilis J. Biol. Chem. 285 2010 1870 1878
15. O. Goldmann, I. Sastalla, M. Wos-Oxley, M. Rohde, and E. Medina Streptococcus pyogenes induces oncosis in macrophages through the activation of an inflammatory programmed cell death pathway Cell. Microbiol. 11 2009 138 155
16. C. Hidalgo-Grass, M. Ravins, M. Dan-Goor, J. Jaffe, A.E. Moses, and E. Hanski A locus of group A Streptococcus involved in invasive disease and DNA transfer Mol. Microbiol. 46 2002 87 99
17. C. Hidalgo-Grass, M. Dan-Goor, A. Maly, Y. Eran, L.A. Kwinn, V. Nizet, M. Ravins, J. Jaffe, A. Peyser, A.E. Moses, and E. Hanski Effect of a bacterial pheromone peptide on host chemokine degradation in group A streptococcal necrotising soft-tissue infections Lancet 363 2004 696 703
18. C. Hidalgo-Grass, I. Mishalian, M. Dan-Goor, I. Belotserkovsky, Y. Eran, V. Nizet, A. Peled, and E. Hanski A streptococcal protease that degrades CXC chemokines and impairs bacterial clearance from infected tissues EMBO J. 25 2006 4628 4637
19. S.J. Jackson, A.C. Steer, and H. Campbell Systematic Review: Estimation of global burden of non-suppurative sequelae of upper respiratory tract infection: rheumatic fever and post-streptococcal glomerulonephritis Trop. Med. Int. Health 16 2011 2 11
20. C.C. Kietzman, and M.G. Caparon Distinct time-resolved roles for two catabolite-sensing pathways during Streptococcus pyogenes infection Infect. Immun. 79 2011 812 821
21. T.L. Kinkel, and K.S. McIver CcpA-mediated repression of streptolysin S expression and virulence in the group A streptococcus Infect. Immun. 76 2008 3451 3463
22. T.V. Leday, K.M. Gold, T.L. Kinkel, S.A. Roberts, J.R. Scott, and K.S. McIver TrxR, a new CovR-repressed response regulator that activates the Mga virulence regulon in group A Streptococcus Infect. Immun. 76 2008 4659 4668
23. A. Lepoutre, A. Doloy, P. Bidet, A. Leblond, A. Perrocheau, E. Bingen, P. Trieu-Cuot, A. Bouvet, C. Poyart, D. Lévy-Bruhl Microbiologists of the Epibac Network Epidemiology of invasive Streptococcus pyogenes infections in France in 2007 J. Clin. Microbiol. 49 2011 4094 4100
24. J.N. Lin, L.L. Chang, C.H. Lai, H.H. Lin, and Y.H. Chen Clinical and molecular characteristics of invasive and noninvasive skin and soft tissue infections caused by group A Streptococcus J. Clin. Microbiol. 49 2011 3632 3637
25. P.G. Maamary, N.L. Ben Zakour, J.N. Cole, A. Hollands, R.K. Aziz, T.C. Barnett, A.J. Cork, A. Henningham, M. Sanderson-Smith, and J.D. McArthur et al. Tracing the evolutionary history of the pandemic group A streptococcal M1T1 clone FASEB J. 26 2012 4675 4684
26. H. Malke, K. Steiner, W.M. McShan, and J.J. Ferretti Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA Int. J. Med. Microbiol. 296 2006 259 275
27. E. Medina, O. Goldmann, M. Rohde, A. Lengeling, and G.S. Chhatwal Genetic control of susceptibility to group A streptococcal infection in mice J. Infect. Dis. 184 2001 846 852
28. T. Miyoshi-Akiyama, D. Takamatsu, M. Koyanagi, J. Zhao, K. Imanishi, and T. Uchiyama Cytocidal effect of Streptococcus pyogenes on mouse neutrophils in vivo and the critical role of streptolysin S J. Infect. Dis. 192 2005 107 116
29. E.M. Molloy, P.D. Cotter, C. Hill, D.A. Mitchell, and R.P. Ross Streptolysin S-like virulence factors: the continuing sagA Nat. Rev. Microbiol. 9 2011 670 681
30. A.E. Moses, M.R. Wessels, K. Zalcman, S. Albertí, S. Natanson-Yaron, T. Menes, and E. Hanski Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A Streptococcus Infect. Immun. 65 1997 64 71
31. I. Nakagawa, A. Amano, N. Mizushima, A. Yamamoto, H. Yamaguchi, T. Kamimoto, A. Nara, J. Funao, M. Nakata, and K. Tsuda et al. Autophagy defends cells against invading group A Streptococcus Science 306 2004 1037 1040
32. V. Nizet Streptococcal beta-hemolysins: genetics and role in disease pathogenesis Trends Microbiol. 10 2002 575 580
33. V. Nizet, B. Beall, D.J. Bast, V. Datta, L. Kilburn, D.E. Low, and J.C. De Azavedo Genetic locus for streptolysin S production by group A streptococcus Infect. Immun. 68 2000 4245 4254
34. A. Norrby-Teglund, M.P. Muller, A. Mcgeer, B.S. Gan, V. Guru, J. Bohnen, P. Thulin, and D.E. Low Successful management of severe group A streptococcal soft tissue infections using an aggressive medical regimen including intravenous polyspecific immunoglobulin together with a conservative surgical approach Scand. J. Infect. Dis. 37 2005 166 172
35. I. Ofek, D. Zafriri, J. Goldhar, and B.I. Eisenstein Inability of toxin inhibitors to neutralize enhanced toxicity caused by bacteria adherent to tissue culture cells Infect. Immun. 58 1990 3737 3742
36. V. Ozeri, I. Rosenshine, A. Ben-Ze'Ev, G.M. Bokoch, T.S. Jou, and E. Hanski De novo formation of focal complex-like structures in host cells by invading Streptococci Mol. Microbiol. 41 2001 561 573
37. M. Palmer The family of thiol-activated, cholesterol-binding cytolysins Toxicon 39 2001 1681 1689
38. C.H. Pui, L.L. Robison, and A.T. Look Acute lymphoblastic leukaemia Lancet 371 2008 1030 1043
39. P. Rice, I. Longden, and A. Bleasby EMBOSS: the European Molecular Biology Open Software Suite Trends Genet. 16 2000 276 277
40. N. Ruiz, B. Wang, A. Pentland, and M. Caparon Streptolysin O and adherence synergistically modulate proinflammatory responses of keratinocytes to group A streptococci Mol. Microbiol. 27 1998 337 346
41. S.A. Shelburne, R.J. Olsen, B. Suber, P. Sahasrabhojane, P. Sumby, R.G. Brennan, and J.M. Musser A combination of independent transcriptional regulators shapes bacterial virulence gene expression during infection PLoS Pathog. 6 2010 e1000817
42. D.M. Short, I.D. Heron, J.L. Birse-Archbold, L.E. Kerr, J. Sharkey, and J. McCulloch Apoptosis induced by staurosporine alters chaperone and endoplasmic reticulum proteins: Identification by quantitative proteomics Proteomics 7 2007 3085 3096
43. J. Söding Protein homology detection by HMM-HMM comparison Bioinformatics 21 2005 951 960
44. A.M. Timmer, J.C. Timmer, M.A. Pence, L.C. Hsu, M. Ghochani, T.G. Frey, M. Karin, G.S. Salvesen, and V. Nizet Streptolysin O promotes group A Streptococcus immune evasion by accelerated macrophage apoptosis J. Biol. Chem. 284 2009 862 871
45. P. Vandenabeele, L. Galluzzi, T. Vanden Berghe, and G. Kroemer Molecular mechanisms of necroptosis: an ordered cellular explosion Nat. Rev. Mol. Cell. Biol. 11 2010 700 714
46. C.E. White, and S.C. Winans Cell-cell communication in the plant pathogen Agrobacterium tumefaciens Philos. Trans. R. Soc. Lond. B Biol. Sci. 362 2007 1135 1148
47. S. Wu, and Y. Zhang LOMETS: a local meta-threading-server for protein structure prediction Nucleic Acids Res. 35 2007 3375 3382
48. Y.T. Wu, H.L. Tan, Q. Huang, X.J. Sun, X. Zhu, and H.M. Shen zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFα mediated by the PKC-MAPKs-AP-1 pathway Cell Death Differ. 18 2011 26 37
49. X. Xue, J.H. Piao, A. Nakajima, S. Sakon-Komazawa, Y. Kojima, K. Mori, H. Yagita, K. Okumura, H. Harding, and H. Nakano Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha J. Biol. Chem. 280 2005 33917 33925
50. Y. Zhang I-TASSER server for protein 3D structure prediction BMC Bioinformatics 9 2008 40
51. Y. Eran, Y. Getter, M. Baruch, I. Belotserkovsky, G. Padalon, I. Mishalian, A. Podbielski, B. Kreikemeyer, and E. Hanski Transcriptional regulation of the sil locus by the SilCR signalling peptide and its implications on group A streptococcus virulence Mol. Microbiol. 63 2007 1209 1222
52. G.D. Glekas, J.R. Cates, T.M. Cohen, C.V. Rao, and G.W. Ordal Site-specific methylation in Bacillus subtilis chemotaxis: effect of covalent modifications to the chemotaxis receptor McpB Microbiology 157 2011 56 65
53. J. Perez-Casal, M.G. Caparon, and J.R. Scott Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems J. Bacteriol. 173 1991 2617 2624
54. M. Ravins, J. Jaffe, E. Hanski, I. Shetzigovski, S. Natanson-Yaron, and A.E. Moses Characterization of a mouse-passaged, highly encapsulated variant of group A streptococcus in in vitro and in vivo studies J. Infect. Dis. 182 2000 1702 1711
55. D.J. Savic, W.M. McShan, and J.J. Ferretti Autonomous expression of the slo gene of the bicistronic nga-slo operon of Streptococcus pyogenes Infect. Immun. 70 2002 2730 2733
56. I.N. Shindyalov, and P.E. Bourne Protein structure alignment by incremental combinatorial extension (CE) of the optimal path Protein Eng. 11 1998 739 747
57. A. Sturn, J. Quackenbush, and Z. Trajanoski Genesis: cluster analysis of microarray data Bioinformatics 18 2002 207 208
58. Y.Q. Zhang, S.X. Ren, H.L. Li, Y.X. Wang, G. Fu, J. Yang, Z.Q. Qin, Y.G. Miao, W.Y. Wang, and R.S. Chen et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228) Mol. Microbiol. 49 2003 1577 1593
59. M.Y. Zhou, and C.E. Gomez-Sanchez Universal TA cloning Curr. Issues Mol. Biol. 2 2000 1 7