Outer and inner membrane proteins compose an arginine-agmatine exchange system in Chlamydophila pneumoniae

Journal of Bacteriology

Volumn 190, Issue 22, 2008, Pages 7431-7440

  Smith, Conor B ^a   Graham, David E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGMATINE; ARGININE; CADAVERINE; LYSINE; MEMBRANE PROTEIN; ORNITHINE; PORIN;

ARTICLE; BACTERIAL CELL; CELL SURVIVAL; CHEMICAL ANALYSIS; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; CYTOPLASM; DECARBOXYLATION; ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION;

AGMATINE; ARGININE; BACTERIAL PROTEINS; BLOTTING, WESTERN; CARBOXY-LYASES; CENTRIFUGATION, DENSITY GRADIENT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; MUTATION; PHYLOGENY; PROTEIN TRANSPORT; TANDEM MASS SPECTROMETRY;

CHLAMYDIAE; CHLAMYDOPHILA PNEUMONIAE; ESCHERICHIA COLI;

EID: 55549105754     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00652-08     Document Type: Article

References (53)

1. Adewoye, L. O., L. Tschetter, J. O'Neil, and E. A. Worobec. 1998. Channel specificity and secondary structure of the glucose-inducible porins of Pseudomonas spp. J. Bioenerg. Biomembr. 30:257-267.
2. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
3. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462.
4. Chaturvedi, R., M. Asim, N. D. Lewis, H. M. S. Algood, T. L. Cover, P. Y. Kim, and K. T. Wilson. 2007. L-Arginine availability regulates inducible nitric oxide synthase-dependent host defense against Helicobacter pylori. Infect. Immun. 75:4305-4315.
5. Cunin, R., N. Glansdorff, A. Pierard, and V. Stalon. 1986. Biosynthesis and metabolism of arginine in bacteria. Microbiol. Mol. Biol. Rev. 50:314-352.
6. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
7. Dautry-Varsat, A., A. Subtil, and T. Hackstadt. 2005. Recent insights into the mechanisms of Chlamydia entry. Cell. Microbiol. 7:1714-1722.
8. Dupont, M., C. E. James, J. Chevalier, and J.-M. Pagès. 2007. An early response to environmental stress involves regulation of OmpX and OmpF, two enterobacterial outer membrane pore-forming proteins. Antimicrob. Agents Chemother. 51:3190-3198.
9. Ekman, M. R., J. T. Grayston, R. Visakorpi, M. Kleemola, C. C. Kuo, and P. Saikku. 1993. An epidemic of infections due to Chlamydia pneumoniae in military conscripts. Clin. Infect. Dis. 17:420-425.
10. Fang, Y., L. Kolmakova-Partensky, and C. Miller. 2007. A bacterial arginineagmatine exchange transporter involved in extreme acid resistance. J. Biol. Chem. 282:176-182.
11. Fields, K. A., and T. Hackstadt. 2002. The chlamydial inclusion: escape from the endocytic pathway. Annu. Rev. Cell Dev. Biol. 18:221-245.
12. Giles, T. N., and D. E. Graham. 2007. Characterization of an acid-dependent arginine decarboxylase enzyme from Chlamydophila pneumoniae. J. Bacteriol. 189:7376-7383.
13. Giles, T. N., and D. E. Graham. 2008. Crenarchaeal arginine decarboxylase evolved from an S-adenosylmethionine decarboxylase enzyme. J. Biol. Chem. 283:25829-25838.
14. Gobert, A. P., D. J. McGee, M. Akhtar, G. L. Mendz, J. C. Newton, Y. Cheng, H. L. T. Mobley, and K. T. Wilson. 2001. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc. Natl. Acad. Sci. USA 98:13844-13849.
15. Gong, S., H. Richard, and J. W. Foster. 2003. YjdE (AdiC) is the arginine: agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J. Bacteriol. 185:4402-4409.
16. Graham, D. E., and H. K. Huse. 2008. Methanogens with pseudomurein use diaminopimelate aminotransferase in lysine biosynthesis. FEBS Lett. 582: 1369-1374.
17. Graham, D. E., H. Xu, and R. H. White. 2002. Methanococcus jannaschii uses a pyruvoyl-dependent arginine decarboxylase in polyamine biosynthesis. J. Biol. Chem. 277:23500-23507.
18. Grieshaber, S., J. A. Swanson, and T. Hackstadt. 2002. Determination of the physical environment within the Chlamydia trachomatis inclusion using ionselective ratiometric probes. Cell. Microbiol. 4:273-283.
19. Hancock, R. E. W., and F. S. L. Brinkman. 2002. Function of Pseudomonas porins in uptake and efflux. Annu. Rev. Microbiol. 56:17-38.
20. Iyer, R. K., C. Williams, and C. Miller. 2003. Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J. Bacteriol. 185:6556-6561.
21. Jack, D. L., I. T. Paulsen, and M. H. Saier. 2000. The amino acid/polyamine/ organocation (APC) superfamily of transporters specific for amino acids, polyamines and organocations. Microbiology 146:1797-1814.
22. Kakishima, K., A. Shiratsuchi, A. Taoka, Y. Nakanishi, and Y. Fukumori. 2007. Participation of nitric oxide reductase in survival of Pseudomonas aeruginosa in LPS-activated macrophages. Biochem. Biophys. Res. Commun. 355:587-591.
23. Kalman, S., W. Mitchell, R. Marathe, C. Lammel, J. Fan, R. W. Hyman, L. Olinger, J. Grimwood, R. W. Davis, and R. S. Stephens. 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21:385-389.
24. Karunakaran, K. P., J. Rey-Ladino, N. Stoynov, K. Berg, C. Shen, X. Jiang, B. R. Gabel, H. Yu, L. J. Foster, and R. C. Brunham. 2008. Immunoproteomic discovery of novel T-cell antigens from the obligate intracellular pathogen Chlamydia. J. Immunol. 180:2459-2465.
25. Kashiwagi, K., S. Shibuya, H. Tomitori, A. Kuraishi, and K. Igarashi. 1997. Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J. Biol. Chem. 272:6318-6323.
26. Kieboom, J., and T. Abee. 2006. Arginine-dependent acid resistance in Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:5650-5653.
27. Krogh, A., B. Larsson, G. von Heijne, and E. L. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
28. Kubo, A., and R. S. Stephens. 2001. Substrate-specific diffusion of select dicarboxylates through Chlamydia trachomatis PorB. Microbiology 147:3135-3140.
29. Lee, J., H. Ryu, R. J. Ferrante, S. M. Morris, Jr., and R. R. Ratan. 2003. Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. Proc. Natl. Acad. Sci. USA 100:4843-4848.
30. Lin, J., I. S. Lee, J. Frey, J. L. Slonczewski, and J. W. Foster. 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J. Bacteriol. 177:4097-4104.
31. Marani, P., S. Wagner, L. Baars, P. Genevaux, J.-W. De Gier, I. Nilsson, R. Casadio, and G. Von Heijne. 2006. New Escherichia coli outer membrane proteins identified through prediction and experimental verification. Protein Sci. 15:884-889.
32. March, P. E., and M. Inouye. 1985. GTP-binding membrane protein of Escherichia coli with sequence homology to initiation factor 2 and elongation factors Tu and G. Proc. Natl. Acad. Sci. USA 82:7500-7504.
33. McClarty, G. 1999. Chlamydial metabolism as inferred from the complete genome sequence, p. 69-100. In R. S. Stephens (ed.), Chlamydia: intracellular biology, pathogenesis, and immunity. American Society for Microbiology, Washington, DC.
34. Morris, D. R., and A. B. Pardee. 1966. Multiple pathways of putrescine biosynthesis in Escherichia coli. J. Biol. Chem. 241:3129-3135.
35. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Mol. Biol. Rev. 55:143-190.
36. Nicholson, T. L., L. Olinger, K. Chong, G. Schoolnik, and R. S. Stephens. 2003. Global stage-specific gene regulation during the developmental cycle of Chlamydia trachomatis. J. Bacteriol. 185:3179-3189.
37. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593-656.
38. Notredame, C., D. G. Higgins, and J. Heringa. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302:205-217.
39. Pautsch, A., J. Vogt, K. Model, C. Siebold, and G. E. Schulz. 1999. Strategy for membrane protein crystallization exemplified with OmpA and OmpX. Proteins Struct. Funct. Genet. 34:167-172.
40. Qin, Y., N. Polacek, O. Vesper, E. Staub, E. Einfeldt, D. N. Wilson, and K. H. Nierhaus. 2006. The highly conserved LepA is a ribosomal elongation factor that back-translocates the ribosome. Cell 127:721-733.
41. Read, T. D., R. C. Brunham, C. Shen, S. R. Gill, J. F. Heidelberg, O. White, E. K. Hickey, J. Peterson, T. Utterback, K. Berry, S. Bass, K. Linher, J. Weidman, H. Khouri, B. Craven, C. Bowman, R. Dodson, M. Gwinn, W. Nelson, R. DeBoy, J. Kolonay, G. McClarty, S. L. Salzberg, J. Eisen, and C. M. Fraser. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397-1406.
42. Recsei, P. A., W. M. Moore, and E. E. Snell. 1983. Pyruvoyl-dependent histidine decarboxylases from Clostridium perfringens and Lactobacillus buchneri. Comparative structures and properties. J. Biol. Chem. 258:439-444.
43. Richard, H., and J. W. Foster. 2004. Escherichia coli glutamate- and argininedependent acid resistance systems increase internal pH and reverse transmembrane potential. J. Bacteriol. 186:6032-6041.
44. Samartzidou, H., and A. H. Delcour. 1999. Excretion of endogenous cadaverine leads to a decrease in porin-mediated outer membrane permeability. J. Bacteriol. 181:791-798.
45. Samartzidou, H., M. Mehrazin, Z. Xu, M. J. Benedik, and A. H. Delcour. 2003. Cadaverine inhibition of porin plays a role in cell survival at acidic pH. J. Bacteriol. 185:13-19.
46. Schaumburg, C. S., and M. Tan. 2006. Arginine-dependent gene regulation via the ArgR repressor is species specific in Chlamydia. J. Bacteriol. 188:919-927.
47. Schramm, N., C. R. Bagnell, and P. B. Wyrick. 1996. Vesicles containing Chlamydia trachomatis serovar L2 remain above pH 6 within HEC-1B cells. Infect. Immun. 64:1208-1214.
48. Scidmore, M. A. 2006. Chlamydial exploitation of host signaling, cytoskeletal, and membrane trafficking pathways, p. 255-295. In P. M. Bavoil and P. B. Wyrick (ed.), Chlamydia: genomics and pathogenesis. Horizon Bioscience, Norfolk, United Kingdom.
49. Soda, K., T. Yorifuji, and K. Ogata. 1967. Occurrence of arginine racemase in bacterial extract. Biochim. Biophys. Acta 146:606-608.
50. Thomson, N. R., M. T. G. Holden, C. Carder, N. Lennard, S. J. Lockey, P. Marsh, P. Skipp, C. D. O'Connor, I. Goodhead, H. Norbertzcak, B. Harris, D. Ormond, R. Rance, M. A. Quail, J. Parkhill, R. S. Stephens, and I. N. Clarke. 2008. Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18:161-171.
51. Verhoogt, H. J., H. Smit, T. Abee, M. Gamper, A. J. Driessen, D. Haas, and W. N. Konings. 1992. arcD, the first gene of the arc operon for anaerobic arginine catabolism in Pseudomonas aeruginosa, encodes an arginine-ornithine exchanger. J. Bacteriol. 174:1568-1573.
52. Vogel, H. J., and D. M. Bonner. 1956. Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218:97-106.
53. Ward, A., N. M. Sanderson, J. O'Reilly, N. G. Rutherford, B. Poolman, and P. J. G. Henderston. 2000. The amplified expression, identification, purification, assay, and properties of hexahistidine-tagged bacterial membrane transport proteins, p. 141-166. In S. A. Baldwin (ed.), Membrane transport: a practical approach. Oxford University Press, New York, NY.