Polyphosphate kinase 1 is required for the pathogenesis process of meningitic Escherichia coli K1 (RS218)

Future Microbiology

Volumn 7, Issue 3, 2012, Pages 411-423

  Peng, Liang ^a   Luo, Wen Ying ^a   Zhao, Tie ^a   Wan, Cheng Song ^a   Jiang, Yong ^a   Chi, Feng ^b   Zhao, Wei ^a   Cao, Hong ^a   Huang, Sheng He ^a,b  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

Author keywords

brain microvascular endothelial cell; Escherichia coli K1; meningitis; polyphosphate; polyphosphate kinase 1; stationary phase

Indexed keywords

INTERLEUKIN 1BETA; MESSENGER RNA; PHOSPHOTRANSFERASE; POLYPHOSPHATE; POLYPHOSPHATE KINASE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL MENINGITIS; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DISEASE COURSE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI K1 STRAIN E44; ESCHERICHIA COLI K1 STRAIN RS218; FRAMESHIFT MUTATION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MICROVASCULAR ENDOTHELIAL CELL; NEWBORN; NONHUMAN; OSMOTIC STRESS; PATHOGENESIS; PRIORITY JOURNAL; RAT;

ANIMALS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MALE; MENINGITIS, ESCHERICHIA COLI; PHOSPHOTRANSFERASES (PHOSPHATE GROUP ACCEPTOR); POLYPHOSPHATES; RATS; RATS, SPRAGUE-DAWLEY; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; RATTUS;

EID: 84863250274     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.12.3     Document Type: Article

References (41)

1. Kim BY, Kang J, Kim KS. Invasion processes of pathogenic Escherichia coli. Int. J. Med. Microbiol. 295(6-7), 463-470 (2005).
2. Grandgirard D, Leib SL. Strategies to prevent neuronal damage in paediatric bacterial meningitis. Curr. Opin. Pediatr. 18(2), 112-118 (2006).
3. Huang SH, Jong AY. Cellular mechanisms of microbial proteins contributing to invasion of the blood-brain barrier. Cell. Microbiol. 3(5), 277-287 (2001).
4. Huang SH, Stins MF, Kim KS. Bacterial penetration across the blood-brain barrier during the development of neonatal meningitis. Microbes Infect. 2(10), 1237-1244 (2000).
5. Xie Y, Kim KJ, Kim KS. Current concepts on Escherichia coli K1 translocation of the blood-brain barrier. FEMS Immunol. Med. Microbiol. 42(3), 271-279 (2004).
6. Kim KS. Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat. Rev. Neurosci. 4(5), 376-385 (2003). Excellent review for understanding the pathogenesis of bacterial meningitis.
7. Wang Y, Kim KS. Effect of rpoS mutations on stress-resistance and invasion of brain microvascular endothelial cells in Escherichia coli K1. FEMS Microbiol. Lett. 182(2), 241-247 (2000). Pioneering work suggesting that there is a loss-of-function mutation in the rpoS gene of Escherichia coli K1 strain RS218, which can not be complemented by the wild-type rpoS gene.
8. Rao NN, Kornberg A. Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J. Bacteriol. 178(5), 1394-1400 (1996).
9. Ogawa N, Tzeng CM, Fraley CD, Kornberg A. Inorganic polyphosphate in Vibrio cholerae: genetic, biochemical, and physiologic features. J. Bacteriol. 182(23), 6687-6693 (2000).
10. Rashid MH, Rumbaugh K, Passador L et al. Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 97(17), 9636-9641 (2000).
11. Kim KS, Rao NN, Fraley CD, Kornberg A. Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc. Natl Acad. Sci. USA 99(11), 7675-7680 (2002).
12. Shiba T, Tsutsumi K, Yano H et al. Inorganic polyphosphate and the induction of rpoS expression. Proc. Natl Acad. Sci. USA 94(21), 11210-11215 (1997).
13. Smith AH, Blevins JS, Bachlani GN, Yang XF, Norgard MV. Evidence that RpoS (sigmaS) in Borrelia burgdorferi is controlled directly by RpoN (sigma54/sigmaN). J. Bacteriol. 189(5), 2139-2144 (2007).
14. Bhagwat AA, Tan J, Sharma M et al. Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl. Environ. Microbiol. 72(7), 4978-4986 (2006).
15. Chi F, Wang Y, Gallaher TK, Wu CH, Jong A, Huang SH. Identification of IbeR as a stationary-phase regulator in meningitic Escherichia coli K1 that carries a loss-of-function mutation in rpoS. J. Biomed. Biotechnol. 2009, 520283 (2009). Demonstrates that IbeR is a novel RpoS-like regulator contributing to the stationary phase regulation in E.coli K1.
16. Huang SH, Chen YH, Kong G et al. A novel genetic island of meningitic Escherichia coli K1 containing the ibeA invasion gene (GimA): functional annotation and carbon-source-regulated invasion of human brain microvascular endothelial cells. Funct. Integr. Genomics 1(5), 312-322 (2001).
17. Cortes MAM, Gibon J, Chanteloup NK, Moulin-Schouleur M, Gilot P, Germon P. Inactivation of ibeA and ibeT results in decreased expression of type 1 fimbriae in extraintestinal pathogenic Escherichia coli strain BEN2908▽. Infect. Immun. 76(9), 4129-4136 (2008). Evidence that the ibeA gene is involved in regulating the expression of type 1 fimbriae in pathogenic E. coli.
18. Wang Y. The function of OmpA in Escherichia coli. Biochem. Biophys. Res. Commun. 292, 396-401 (2002).
19. Zou Y, He L, Chi F, Jong A, Huang SH. Involvement of Escherichia coli K1 ibeT in bacterial adhesion that is associated with the entry into human brain microvascular endothelial cells. Med. Microbiol. Immunol. 197(4), 337-344 (2008).
20. Zhang K, Zhao WD, Li Q et al. Tentative identification of glycerol dehydrogenase as Escherichia coli K1 virulence factor cglD and its involvement in the pathogenesis of experimental neonatal meningitis. Med. Microbiol. Immunol. 198(3), 195-204 (2009).
21. Candon HL, Allan BJ, Fraley CD, Gaynor EC. Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J. Bacteriol. 189(22), 8099-8108 (2007). Evidence that polyphosphate kinase 1 is a pathogenesis determinant in some bacteria.
22. Silby MW, Nicoll JS, Levy SB. Requirement of polyphosphate by Pseudomonas fluorescens Pf0-1 for competitive fitness and heat tolerance in laboratory media and sterile soil▽. Appl. Environ. Microbiol. 75(12), 3872-3881 (2009).
23. Stinsa MF, Badgera J, Kim KS. Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb. Pathog. 30, 19-28 (2001).
24. Huang SH, He L, Zhou Y, Wu CH, Jong A. Lactobacillus rhamnosus GG suppresses meningitic E. coli K1 penetration across human intestinal epithelial cells in vitro and protects neonatal rats against experimental hematogenous meningitis. Int. J. Microbiol. 2009, 647862 (2009).
25. Huang SH, Wan ZS, Chen YH, Jong AY, Kim KS. Further characterization of Escherichia coli brain microvascular endothelial cell invasion gene ibeA by deletion, complementation, and protein expression. J. Infect. Dis. 183(7), 1071-1078 (2001).
26. Huang SH, Wass C, Fu Q, Prasadarao NV, Stins M, Kim KS. Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect. Immun. 63(11), 4470-4475 (1995).
27. Hill VT, Townsend SM, Arias RS et al. TraJ-dependent Escherichia coli K1 interactions with professional phagocytes are important for early systemic dissemination of infection in the neonatal rat. Infect. Immun. 72(1), 478-488 (2004).
28. Yepes M, Sandkvist M, Moore EG et al. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest. 112(10), 1553-1540 (2003).
29. Chi F, Wang L, Zheng X et al. Meningitic Escherichia coli K1 penetration and neutrophil transmigration across the blood-brain barrier are modulated by alpha7 nicotinic receptor. PLoS One 6(9), E25016 (2011).
30. Carey CM, Kostrzynska M, Thompson S. Escherichia coli O157:H7 stress and virulence gene expression on Romaine lettuce using comparative real-time PCR. J. Microbiol. Methods 77(2), 235-242 (2009).
31. Jiao J, Cao H, Chen XW, Zhou MJ, Liu ZH, Ding ZH. Downregulation of HBx mRNA in HepG2.2.15 cells by small interfering RNA. Eur. J. Gastroenterol. Hepatol. 19(12), 1114-1118 (2007).
32. Metkar S, Awasthi S, Denamur E et al. Role of CD14 in responses to clinical isolates of Escherichia coli: effects of K1 capsule expression. Infect. Immun. 75(11), 5415-5424 (2007).
33. Tang YJ, Zhou FW, Luo ZQ et al. Multiple therapeutic effects of adjunctive baicalin therapy in experimental bacterial meningitis. Inflammation 33(3), 180-188 (2010).
34. Tzeng CM, Kornberg A. Polyphosphate kinase is highly conserved in many bacterial pathogens. Mol. Microbiol. 29(1), 381-382 (1998).
35. Brown MR, Kornberg A. The long and short of it - polyphosphate, PPK and bacterial survival. Trends Biochem. Sci. 33(6), 284-290 (2008). Elaborated on the biological function of polyphosphate kinase in bacteria.
36. Ishige K, Zhang H, Kornberg A. Polyphosphate kinase (PPK2), a potent, polyphosphate-driven generator of GTP. Proc. Natl Acad. Sci. USA 99(26), 16684-16688 (2002).
37. Gangaiah D, Liu Z, Arcos J et al. Polyphosphate kinase 2: a novel determinant of stress responses and pathogenesis in Campylobacter jejuni. PLoS One 5(8), E12142 (2010).
38. Brown MR, Kornberg A. Inorganic polyphosphate in the origin and survival of species. Proc. Natl Acad. Sci. USA 101(46), 16085-16087 (2004).
39. Notley-McRobb L, King T, Ferenci T. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J. Bacteriol. 184(3), 806-811 (2002).
40. King T, Ishihama A, Kori A, Ferenci T. A regulatory trade-off as a source of strain variation in the species Escherichia coli. J. Bacteriol. 186(17), 5614-5620 (2004).
41. Cheng Y, Sun B. Polyphosphate kinase affects oxidative stress response by modulating cAMP receptor protein and rpoS expression in Salmonella typhimurium. J. Microbiol. Biotechnol. 19(12), 1527-1535 (2009).