The phtc-phtd locus equips legionella pneumophila for thymidine salvage and replication in macrophages

Infection and Immunity

Volumn 82, Issue 2, 2014, Pages 720-730

  Fonseca, Maris V ^a,b   Sauer, John Demian ^a,c   Crepin, Sebastien ^a   Byrne, Brenda ^a   Swanson, Michele S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b MONROE COMMUNITY COLLEGE   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLOXURIDINE; NUCLEOSIDE TRANSPORTER; PROTEIN PHTC; PROTEIN PHTD; THYMIDINE; THYMIDINE KINASE; THYMIDINE PHOSPHATE; THYMIDYLATE SYNTHASE; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM CULTURE; BACTERIUM MUTANT; ESCHERICHIA COLI; FEMALE; GENE LOCUS; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION;

ANIMALS; CELLS, CULTURED; CULTURE MEDIA; FEMALE; GENE DELETION; LEGIONELLA PNEUMOPHILA; MACROPHAGES; MEMBRANE TRANSPORT PROTEINS; MICE; MICROBIAL VIABILITY; THYMIDINE;

EID: 84892972592     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01043-13     Document Type: Article

References (54)

1. Fields BS, Benson RF, Besser RE. 2002. Legionella and legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15:506-526. http: //dx.doi.org/10.1128/CMR.15.3.506-526.2002.
2. Snelling W, Moore J, McKenna J, Lecky D, Dooley J. 2006. Bacterialprotozoa interactions; an update on the role these phenomena play towards human illness. Microbes Infect. 8:578-587. http://dx.doi.org/10 .1016/j.micinf.2005.09.001.
3. Sauer JD, Bachman MA, Swanson MS. 2005. The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. Proc. Natl. Acad. Sci. U. S. A. 102:9924-9929. http://dx.doi.org/10.1073/pnas.0502767102.
4. Chen DE, Podell S, Sauer JD, Swanson MS, Saier MH, Jr. 2008. The phagosomal nutrient transporter (Pht) family. Microbiology 154:42-53. http://dx.doi.org/10.1099/mic.0.2007/010611-0.
5. Degtyar E, Zusman T, Ehrilich M, Segal G. 2009. A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria. Cell. Microbiol. 11:1219-1235. http://dx.doi.org/10.1111/j.1462-5822.2009.01328.x.
6. Isberg RR, O'Connor TJ, Heidtman M. 2009. The Legionella pneumophila replication vacuole: making a cozy niche inside host cells. Nat. Rev. Microbiol. 7:13-24. http://dx.doi.org/10.1038/nrmicro1967.
7. Gillespie JJ, Ammerman NC, Dreher-Lesnick SM, Rahman MS, Worley MJ, Setubal JC, Sobral BS, Azad AF. 2009. An anomalous type IV secretion system in Rickettsia is evolutionarily conserved. PLoS One 4:e4833. http://dx.doi.org/10.1371/journal.pone.0004833.
8. Horwitz MA. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158:1319-1331. http://dx.doi.org/10.1084/jem.158.4.1319.
9. Swanson MS, Isberg RR. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
10. Byrne B, Swanson MS. 1998. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect. Immun. 66:3029-3034.
11. Garduno RA, Garduno E, Hiltz M, Hoffman PS. 2002. Intracellular growth of Legionella pneumophila gives rise to a differentiated form dissimilar to stationary-phase forms. Infect. Immun. 70:6273-6283. http: //dx.doi.org/10.1128/IAI.70.11.6273-6283.2002.
12. Faulkner G, Berk SG, Garduno E, Ortiz-Jimenez MA, Garduno RA. 2008. Passage through Tetrahymena tropicalis triggers a rapid morphological differentiation in Legionella pneumophila. J. Bacteriol. 190:7728-7738. http://dx.doi.org/10.1128/JB.00751-08.
13. Hammer BK, Swanson MS. 1999. Coordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 33:721-731. http://dx.doi.org/10.1046/j.1365-2958.1999.01519.x.
14. Dalebroux ZD, Edwards RL, Swanson MS. 2009. SpoT governs Legionella pneumophila differentiation in host macrophages. Mol. Microbiol. 71:640-658. http://dx.doi.org/10.1111/j.1365-2958.2008.06555.x.
15. Edwards RL, Dalebroux ZD, Swanson MS. 2009. Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. Mol. Microbiol. 71:1190-1204. http://dx.doi.org/10.1111/j.1365-2958.2008 .06593.x.
16. Ristroph JD, Hedlund KW, Gowda S. 1981. Chemically defined medium for Legionella pneumophila growth. J. Clin. Microbiol. 13:115-119.
17. Wieland H, Ullrich S, Lang F, Neumeister B. 2005. Intracellular multiplication of Legionella pneumophila depends on host cell amino acid transporter SLC1A5. Mol. Microbiol. 55:1528-1537. http://dx.doi.org/10.1111 /j.1365-2958.2005.04490.x.
18. Ewann F, Hoffman PS. 2006. Cysteine metabolism in Legionella pneumophila: characterization of an L-cystine-utilizing mutant. Appl. Environ. Microbiol. 72:3993-4000. http://dx.doi.org/10.1128/AEM.00684-06.
19. Sauer JD. 2006. Contribution of the Pht transporters to nutrient acquisition and differentiation of intracellular Legionella pneumophila. PhD thesis. University of Michigan, Ann Arbor, MI.
20. Berger KH, Isberg RR. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:7-19. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01092.x.
21. Davis RW, Botstein D, Roth JR. 1980. Advanced bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Vogel HJ, Bonner DM. 1956. Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218:97-106.
23. Neidhardt FC, Bloch PL, Smith DF. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
24. Molofsky AB, Shetron-Rama LM, Swanson MS. 2005. Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect. Immun. 73:5720-5734. http://dx.doi.org/10.1128/IAI.73.9.5720-5734.2005.
25. Martinez E, Bartolome B, de la Cruz F. 1988. pACYC184-derived cloning vectors containing the multiple cloning site and lacZ alpha reporter gene of pUC8/9 and pUC18/19 plasmids. Gene 68:159-162. http: //dx.doi.org/10.1016/0378-1119(88)90608-7.
26. Marra A, Blander SJ, Horwitz MA, Shuman HA. 1992. Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc. Natl. Acad. Sci. U. S. A. 89:9607-9611. http: //dx.doi.org/10.1073/pnas.89.20.9607.
27. Sexton JA, Vogel JP. 2004. Regulation of hypercompetence in Legionella pneumophila. J. Bacteriol. 186:3814-3825. http://dx.doi.org/10.1128/JB .186.12.3814-3825.2004.
28. Neuhard J, Kelin R. 1996. Biosynthesis and conversions of pyrimidines, p 580-599. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), EcoSal-Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC.
29. McKeown M, Kahn M, Hanawalt P. 1976. Thymidine uptake and utilization in Escherichia coli: a new gene controlling nucleoside transport. J. Bacteriol. 126:814-822.
30. Mollgaard H, Neuhard J. 1983. Biosynthesis of deoxythymidine triphosphate, p 149-199. In Munch-Petersen A (ed), Metabolism of nucleotides, nucleosides and nucleobases in microorganisms. Academic Press, Inc., London, United Kingdom.
31. Bachman MA, Swanson MS. 2004. Genetic evidence that Legionella pneumophila RpoS modulates expression of the transmission phenotype in both the exponential phase and the stationary phase. Infect. Immun. 72: 2468-2476. http://dx.doi.org/10.1128/IAI.72.5.2468-2476.2004.
32. Summers WC, Raksin P. 1993. A method for selection of mutations at the tdk locus in Escherichia coli. J. Bacteriol. 175:6049-6051.
33. Orchard SS, Goodrich-Blair H. 2005. An encoded N-terminal extension results in low levels of heterologous protein production in Escherichia coli. Microb. Cell Fact. 4:22. http://dx.doi.org/10.1186/1475-2859-4-22.
34. Norholm MH, Dandanell G. 2001. Specificity and topology of the Escherichia coli xanthosine permease, a representative of the NHS subfamily of the major facilitator superfamily. J. Bacteriol. 183:4900-4904. http://dx .doi.org/10.1128/JB.183.16.4900-4904.2001.
35. Munch-Petersen A, Mygind B. 1983. Transport of nucleic acid precursors, p 259-305. In Munch-Petersen A (ed), Metabolism of nucleotides, nucleosides and nucleobases in microorganisms. Academic Press, Inc., London, United Kingdom.
36. Craig JE, Zhang Y, Gallagher MP. 1994. Cloning of the nupC gene of Escherichia coli encoding a nucleoside transport system, and identification of an adjacent insertion element, IS 186. Mol. Microbiol. 11:1159-1168. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00392.x.
37. Patching SG, Baldwin SA, Baldwin AD, Young JD, Gallagher MP, Henderson PJ, Herbert RB. 2005. The nucleoside transport proteins, NupC and NupG, from Escherichia coli: specific structural motifs necessary for the binding of ligands. Org. Biomol. Chem. 3:462-470. http://dx .doi.org/10.1039/b414739a.
38. Pine L, George JR, Reeves MW, Harrell WK. 1979. Development of a chemically defined liquid medium for growth of Legionella pneumophila. J. Clin. Microbiol. 9:615-626.
39. Reeves MW, Pine L, Hutner SH, George JR, Harrell WK. 1981. Metal requirements of Legionella pneumophila. J. Clin. Microbiol. 13:688-695.
40. Tesh MJ, Miller RD. 1983. Arginine biosynthesis in Legionella pneumophila: absence of N-acetylglutamate synthetase. Can. J. Microbiol. 29: 1230-1233. http://dx.doi.org/10.1139/m83-190.
41. Hoffman PS. 2008. Microbial physiology, p 113-132. In Hoffman P, Friedman H, BendinelliM(ed), Legionella pneumophila: pathogenesis and immunity. Springer Publishing Corp., New York, NY.
42. Seol W, Shatkin AJ. 1991. Escherichia coli kgtP encodes an alphaketoglutarate transporter. Proc. Natl. Acad. Sci. U. S. A. 88:3802-3806. http://dx.doi.org/10.1073/pnas.88.9.3802.
43. Hammer-Jespersen K, Munch-Petersen A, Schwartz M, Nygaard P. 1971. Induction of enzymes involved in the catabolism of deoxyribonucleosides and ribonucleosides in Escherichia coli K 12. Eur. J. Biochem. 19:533-538. http://dx.doi.org/10.1111/j.1432-1033.1971.tb01345.x.
44. Jensen KF, Dandanell G, Hove-Jensen B, Willemoes M. 2008. Nucleotides, nucleosides, and nucleobases. EcoSal Plus 2008. http://dx.doi.org/10 .1128/ecosalplus.3.6.2.
45. Jung B, Florchinger M, Kunz HH, Traub M, Wartenberg R, Jeblick W, Neuhaus HE, Mohlmann T. 2009. Uridine-ribohydrolase is a key regulator in the uridine degradation pathway of arabidopsis. Plant Cell 21: 876-891. http://dx.doi.org/10.1105/tpc.108.062612.
46. Weiss B. 2007. The deoxycytidine pathway for thymidylate synthesis in Escherichia coli. J. Bacteriol. 189:7922-7926. http://dx.doi.org/10.1128/JB .00461-07.
47. Barner HD, Cohen SS. 1954. The induction of thymine synthesis by T2 infection of a thymine requiring mutant of Escherichia coli. J. Bacteriol. 68:80-88.
48. Cohen SS, Barner HD. 1954. Studies on unbalanced growth in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 40:885-893. http://dx.doi.org/10.1073 /pnas.40.10.885.
49. Ahmad SI, Kirk SH, Eisenstark A. 1998. Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 52:591-625. http://dx.doi.org/10.1146/annurev.micro.52.1.591.
50. Molofsky AB, Swanson MS. 2004. Differentiate to thrive: Lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40. http://dx .doi.org/10.1111/j.1365-2958.2004.04129.x.
51. Nakayama K, Kusano K, Irino N, Nakayama H. 1994. Thymine starvation-induced structural changes in Escherichia coli DNA. Detection by pulsed field gel electrophoresis and evidence for involvement of homologous recombination. J. Mol. Biol. 243:611-620. http://dx.doi.org/10.1016 /0022-2836(94)90036-1.
52. Kuong KJ, Kuzminov A. 2012. Disintegration of nascent replication bubbles during thymine starvation triggers RecA-and RecBCDdependent replication origin destruction. J. Biol. Chem. 287:23958-23970. http://dx.doi.org/10.1074/jbc.M112.359687.
53. Bartolome B, Jubete Y, Martinez E, de la Cruz F. 1991. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene 102:75-78. http://dx.doi.org/10 .1016/0378-1119(91)90541-I.
54. Weiss B, Wang L. 1994. De novo synthesis of thymidylate via deoxycytidine in dcd (dCTP deaminase) mutants of Escherichia coli. J. Bacteriol. 176:2194-2199.