Ehrlichia chaffeensis proliferation begins with NtrY/NtrX and PutA/GlnA upregulation and CtrA degradation induced by proline and glutamine uptake

mBio

Volumn 5, Issue 6, 2014, Pages

  Cheng, Zhihui ^a   Lin, Mingqun ^a   Rikihisa, Yasuko ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; DNA BINDING PROTEIN CTRA; GLNA PROTEIN; GLUTAMINE; NTRX PROTEIN; NTRY PROTEIN; PROLINE; PUTA PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CELL DIVISION; CONTROLLED STUDY; EHRLICHIA CHAFFEENSIS; ESCHERICHIA COLI; GENE ACTIVATION; GENE EXPRESSION REGULATION; GLNA GENE; NONHUMAN; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PUTA GENE; SIGNAL TRANSDUCTION; UPREGULATION; CELL LINE; DRUG EFFECTS; GENE REGULATORY NETWORK; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; MONOCYTE;

BACTERIA (MICROORGANISMS); EHRLICHIA CHAFFEENSIS; ESCHERICHIA COLI; EUKARYOTA; RICKETTSIA; RICKETTSIALES;

CELL LINE; DNA-BINDING PROTEINS; EHRLICHIA CHAFFEENSIS; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GLUTAMINE; HUMANS; MONOCYTES; PROLINE; PROTEOLYSIS; UP-REGULATION;

EID: 84920913770     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02141-14     Document Type: Article

References (64)

1. Adams DA, Jajosky RA, Ajani U, Kriseman J, Sharp P, Onwen DH, Schley AW, Anderson WJ, Grigoryan A, Aranas AE, Wodajo MS, Abellera JP, Centers for Disease Control and Prevention. 2014. Summary of notifiable diseases—United States, 2012. MMWR Morb. Mortal. Wkly. Rep. 61:1-121.
2. Olano JP, Walker DH. 2002. Human ehrlichioses. Med. Clin. North Am. 86:375-392. http://dx.doi.org/10.1016/S0025-7125(03)00093-2.
3. Paddock CD, Childs JE. 2003. Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin. Microbiol. Rev. 16:37-64. http://dx.doi.org/10.1128/CMR.16.1.37-64.2003.
4. Rohmer L, Hocquet D, Miller SI. 2011. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol. 19:341-348. http://dx.doi.org/10.1016/j.tim.2011.04.003.
5. Dunning Hotopp JC, Lin M, Madupu R, Crabtree J, Angiuoli SV, Eisen JA, Seshadri R, Ren Q, Wu M, Utterback TR, Smith S, Lewis M, Khouri H, Zhang C, Niu H, Lin Q, Ohashi N, Zhi N, Nelson W, Brinkac LM, Dodson RJ, Rosovitz MJ, Sundaram J, Daugherty SC, Davidsen T, Durkin AS, Gwinn M, Haft DH, Selengut JD, Sullivan SA, Zafar N, Zhou L, Benahmed F, Forberger H, Halpin R, Mulligan S, Robinson J, White O, Rikihisa Y, Tettelin H, Tettelin H. 2006. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet. 2:e21. http://dx.doi.org/10.1371/journal.pgen.0020021.
6. Leigh JA, Dodsworth JA. 2007. Nitrogen regulation in bacteria and archaea. Annu. Rev. Microbiol. 61:349-377. http://dx.doi.org/10.1146/annurev.micro.61.080706.093409.
7. Brown ED, Wood JM. 1992. Redesigned purification yields a fully functional PutA protein dimer from Escherichia coli. J. Biol. Chem. 267: 13086-13092.
8. Colombo G, Villafranca JJ. 1986. Amino acid sequence of Escherichia coli glutamine synthetase deduced from theDNAnucleotide sequence. J. Biol. Chem. 261:10587-10591.
9. Miller RE, Stadtman ER. 1972. Glutamate synthase from Escherichia coli. An iron-sulfide flavoprotein. J. Biol. Chem. 247:7407-7419.
10. Zhou Y, Larson JD, Bottoms CA, Arturo EC, Henzl MT, Jenkins JL, Nix JC, Becker DF, Tanner JJ. 2008. Structural basis of the transcriptional regulation of the proline utilization regulon by multifunctional PutA. J. Mol. Biol. 381:174-188. http://dx.doi.org/10.1016/j.jmb.2008.05.084.
11. Hervás AB, Canosa I, Little R, Dixon R, Santero E. 2009. NtrCdependent regulatory network for nitrogen assimilation in Pseudomonas putida. J. Bacteriol. 191:6123-6135. http://dx.doi.org/10.1128/JB.00744-09.
12. Cheng Z, Kumagai Y, Lin M, Zhang C, Rikihisa Y. 2006. Intra-leukocyte expression of two-component systems in Ehrlichia chaffeensis and Anaplasma phagocytophilum and effects of the histidine kinase inhibitor closantel. Cell. Microbiol. 8:1241-1252. http://dx.doi.org/10.1111/j.1462-5822.2006.00704.x.
13. Assumpção MC, de Souza EM, Yates MG, de Oliveira Pedrosa F, Benelli EM. 2007. Purification and characterisation of Azospirillum brasilense N-truncated NtrX protein. Protein Expr. Purif. 53:302-308. http://dx.doi.org/10.1016/j.pep.2007.01.003.
14. Carrica MDC, Fernandez I, Martí MA, Paris G, Goldbaum FA. 2012. The NtrY/X two-component system of Brucella spp. acts as a redox sensor and regulates the expression of nitrogen respiration enzymes. Mol. Microbiol. 85:39-50. http://dx.doi.org/10.1111/j.1365-2958.2012.08095.x.
15. Drepper T, Wiethaus J, Giaourakis D, Gross S, Schubert B, Vogt M, Wiencek Y, McEwan AG, Masepohl B. 2006. Cross-talk towards the response regulator NtrC controlling nitrogen metabolism in Rhodobacter capsulatus. FEMS Microbiol. Lett. 258:250-256. http://dx.doi.org/10.1111/j.1574-6968.2006.00228.x.
16. Ishida ML, Assumpção MC, Machado HB, Benelli EM, Souza EM, Pedrosa FO. 2002. Identification and characterization of the twocomponent NtrY/NtrX regulatory system in Azospirillum brasilense. Braz. J. Med. Biol. Res. 35:651-661. http://dx.doi.org/10.1590/S0100-879X2002000600004.
17. Kumagai Y, Cheng Z, Lin M, Rikihisa Y. 2006. Biochemical activities of three pairs of Ehrlichia chaffeensis two-component regulatory system proteins involved in inhibition of lysosomal fusion. Infect. Immun. 74: 5014-5022. http://dx.doi.org/10.1128/IAI.00735-06.
18. Bergström J, Fürst P, Norée LO, Vinnars E. 1974. Intracellular free amino acid concentration in human muscle tissue. J. Appl. Physiol. 36: 693-697.
19. Cheng Z, Miura K, Popov VL, Kumagai Y, Rikihisa Y. 2011. Insights into the CtrA regulon in development of stress resistance in obligatory intracellular pathogen Ehrlichia chaffeensis. Mol. Microbiol. 82: 1217-1234. http://dx.doi.org/10.1111/j.1365-2958.2011.07885.x.
20. Gorbatyuk B, Marczynski GT. 2005. Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol. Microbiol. 55:1233-1245. http://dx.doi.org/10.1111/j.1365-2958.2004.04459.x.
21. Menzel R, Roth J. 1981. Enzymatic properties of the purified PutA protein from Salmonella Typhimurium. J. Biol. Chem. 256:9762-9766.
22. Keuntje B, Masepohl B, Klipp W. 1995. Expression of the putA gene encoding proline dehydrogenase from Rhodobacter capsulatus is independent of NtrC regulation but requires an Lrp-like activator protein. J. Bacteriol. 177:6432-6439.
23. Cho K, Winans SC. 1996. The putA gene of Agrobacterium tumefaciens is transcriptionally activated in response to proline by an Lrp-like protein and is not autoregulated. Mol. Microbiol. 22:1025-1033. http://dx.doi.org/10.1046/j.1365-2958.1996.01524.x.
24. Soto MJ, Jiménez-Zurdo JI, van Dillewijn P, Toro N. 2000. Sinorhizobium meliloti putA gene regulation: a new model within the family Rhizobiaceae. J. Bacteriol. 182:1935-1941. http://dx.doi.org/10.1128/JB.182.7.1935-1941.2000.
25. Menzel R, Roth J. 1981. Regulation of the genes for proline utilization in Salmonella Typhimurium: autogenous repression by the putA gene product. J. Mol. Biol. 148:21-44. http://dx.doi.org/10.1016/0022-2836(81)90233-3.
26. Zhou Y, Zhu W, Bellur PS, Rewinkel D, Becker DF. 2008. Direct linking of metabolism and gene expression in the proline utilization A protein from Escherichia coli. Amino Acids 35:711-718. http://dx.doi.org/10.1007/s00726-008-0053-6.
27. Wood JM. 1981. Genetics of L-proline utilization in Escherichia coli. J. Bacteriol. 146:895-901.
28. van Rooyen JM, Abratt VR, Sewell BT. 2006. Three-dimensional structure of a type III glutamine synthetase by single-particle reconstruction. J. Mol. Biol. 361:796-810. http://dx.doi.org/10.1016/j.jmb.2006.06.026.
29. Shatters RG, Kahn ML. 1989. Glutamine synthetase II in Rhizobium: reexamination of the proposed horizontal transfer of DNA from eukaryotes to prokaryotes. J. Mol. Evol. 29:422-428. http://dx.doi.org/10.1007/BF02602912.
30. Eisenberg D, Gill HS, Pfluegl GM, Rotstein SH. 2000. Structurefunction relationships of glutamine synthetases. Biochim. Biophys. Acta 1477:122-145. http://dx.doi.org/10.1016/S0167-4838(99)00270-8.
31. Burroughs AM, Balaji S, Iyer LM, Aravind L. 2007. Small but versatile: the extraordinary functional and structural diversity of the beta-grasp fold. Biol. Direct 2:18. http://dx.doi.org/10.1186/1745-6150-2-18.
32. Li X, Liu T, Wu Y, Zhao G, Zhou Z. 2010. Derepressive effect of NH4_ on hydrogen production by deleting the glnA1 gene in Rhodobacter spha-eroides. Biotechnol. Bioeng. 106:564-572. http://dx.doi.org/10.1002/bit.22722.
33. Manning JM, Moore S, Rowe WB, Meister A. 1969. Identification of L-methionine S-sulfoximine as the diastereoisomer of L-methionine SRsulfoximine that inhibits glutamine synthetase. Biochemistry 8:2681-2685. http://dx.doi.org/10.1021/bi00834a066.
34. Weisbrod RE, Meister A. 1973. Studies on glutamine synthetase from Escherichia coli. Formation of pyrrolidone carboxylate and inhibition by methionine sulfoximine. J. Biol. Chem. 248:3997-4002.
35. Harth G, Horwitz MA. 1999. An inhibitor of exported Mycobacterium tuberculosis glutamine synthetase selectively blocks the growth of pathogenic mycobacteria in axenic culture and in human monocytes: extracellular proteins as potential novel drug targets. J. Exp. Med. 189:1425-1436. http://dx.doi.org/10.1084/jem.189.9.1425.
36. Aspedon A, Groisman EA. 1996. The antibacterial action of protamine: evidence for disruption of cytoplasmic membrane energization in Salmonella Typhimurium. Microbiology 142(12):3389-3397. http://dx.doi.org/10.1099/13500872-142-12-3389.
37. Deutch CE. 2011. L-Proline nutrition and catabolism in Staphylococcus saprophyticus. Antonie Van Leeuwenhoek 99:781-793. http://dx.doi.org/10.1007/s10482-011-9552-7.
38. Albrecht J, Doliǹska M, Hilgier W, Lipkowski AW, Nowacki J. 2000. Modulation of glutamine uptake and phosphate-activated glutaminase activity in rat brain mitochondria by amino acids and their synthetic analogues. Neurochem. Int. 36:341-347. http://dx.doi.org/10.1016/S0197-0186(99)00142-4.
39. Pawlowski K, Klosse U, de Bruijn FJ. 1991. Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Mol. Gen. Genet. 231:124-138. http://dx.doi.org/10.1007/BF00293830.
40. Lin M, Kikuchi T, Brewer HM, Norbeck AD, Rikihisa Y. 2011. Global proteomic analysis of two tick-borne emerging zoonotic agents: Anaplasma phagocytophilum and Ehrlichia chaffeensis. Front. Microbiol. 2:24. http://dx.doi.org/10.3389/fmicb.2011.00024.
41. Cullen PJ, Bowman WC, Kranz RG. 1996. In vitro reconstitution and characterization of the Rhodobacter capsulatus NtrB and NtrC twocomponent system. J. Biol. Chem. 271:6530-6536. http://dx.doi.org/10.1074/jbc.271.11.6530.
42. Quon KC, Marczynski GT, Shapiro L. 1996. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84: 83-93. http://dx.doi.org/10.1016/S0092-8674(00)80995-2.
43. Hallez R, Bellefontaine AF, Letesson JJ, De Bolle X. 2004. Morphological and functional asymmetry in alpha-proteobacteria. Trends Microbiol. 12:361-365. http://dx.doi.org/10.1016/j.tim.2004.06.002.
44. Lin M, Zhu MX, Rikihisa Y. 2002. Rapid activation of protein tyrosine kinase and phospholipase C-gamma2 and increase in cytosolic free calcium are required by Ehrlichia chaffeensis for internalization and growth in THP-1 cells. Infect. Immun. 70:889-898. http://dx.doi.org/10.1128/IAI.70.2.889-898.2002.
45. Tullius MV, Harth G, Horwitz MA. 2003. Glutamine synthetase GlnA1 is essential for growth of Mycobacterium tuberculosis in human THP-1 macrophages and guinea pigs. Infect. Immun. 71:3927-3936. http://dx.doi.org/10.1128/IAI.71.7.3927-3936.2003.
46. Harth G, Maslesa-Galic´ S, Tullius MV, Horwitz MA. 2005. All four Mycobacterium tuberculosis glnA genes encode glutamine synthetase activities but only GlnA1 is abundantly expressed and essential for bacterial homeostasis. Mol. Microbiol. 58:1157-1172. http://dx.doi.org/10.1111/j.1365-2958.2005.04899.x.
47. Weiss E, Dasch GA, Kang YH, Westfall HN. 1988. Substrate utilization by Ehrlichia sennetsu and Ehrlichia risticii separated from host constituents by Renografin gradient centrifugation. J. Bacteriol. 170:5012-5017.
48. Messick JB, Rikihisa Y. 1993. Characterization of Ehrlichia risticii binding, internalization, and proliferation in host cells by flow cytometry. Infect. Immun. 61:3803-3810.
49. Williams JC, Weiss E. 1978. Energy metabolism of Rickettsia typhi: pools of adenine nucleotides and energy charge in the presence and absence of glutamate. J. Bacteriol. 134:884-892.
50. Allan I, Pearce JH. 1983. Differential amino acid utilization by Chlamydia psittaci (strain guinea pig inclusion conjunctivitis) and its regulatory effect on chlamydial growth. J. Gen. Microbiol. 129:1991-2000.
51. Josemans AI, Zweygarth E. 2002. Amino acid content of cell cultures infected with Cowdria ruminantium propagated in a protein-free medium. Ann. N. Y. Acad. Sci. 969:141-146. http://dx.doi.org/10.1111/j.1749-6632.2002.tb04366.x.
52. Gregor J, Zeller T, Balzer A, Haberzettl K, Klug G. 2007. Bacterial regulatory networks include direct contact of response regulator proteins: interaction of RegA and NtrX in Rhodobacter capsulatus. J. Mol. Microbiol. Biotechnol. 13:126-139. http://dx.doi.org/10.1159/000103604.
53. Kamberov ES, Atkinson MR, Feng J, Chandran P, Ninfa AJ. 1994. Sensory components controlling bacterial nitrogen assimilation. Cell. Mol. Biol. Res. 40:175-191.
54. Laub MT, Chen SL, Shapiro L, McAdams HH. 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc. Natl. Acad. Sci. U. S. A. 99:4632-4637. http://dx.doi.org/10.1073/pnas.062065699.
55. Skerker JM, Laub MT. 2004. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat. Rev. Microbiol. 2:325-337. http://dx.doi.org/10.1038/nrmicro864.
56. Mohan Kumar D, Yamaguchi M, Miura K, Lin M, Los M, Coy JF, Rikihisa Y. 2013. Ehrlichia chaffeensis uses its surface protein EtpE to bind GPI-anchored protein DNase X and trigger entry into mammalian cells. PLoS Pathog. 9: e1003666. http://dx.doi.org/10.1371/journal.ppat.1003666.
57. Dawson JE, Anderson BE, Fishbein DB, Sanchez JL, Goldsmith CS, Wilson KH, Duntley CW. 1991. Isolation and characterization of an Ehrlichia sp. from a patient diagnosed with human ehrlichiosis. J. Clin. Microbiol. 29:2741-2745.
58. Sambrook J, Pollack R. 1974. Basic methodology for cell culture—cell transformation. Methods Enzymol. 32:583-592. http://dx.doi.org/10.1016/0076-6879(74)32058-7.
59. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. http://dx.doi.org/10.1016/0378-1119(89)90358-2.
60. Hosted TJ, Rochefort DA, Benson DR. 1993. Close linkage of genes encoding glutamine synthetases I and II in Frankia alni CpI1. J. Bacteriol. 175:3679-3684.
61. Cheng Z, Wang X, Rikihisa Y. 2008. Regulation of type IV secretion apparatus genes during Ehrlichia chaffeensis intracellular development by a previously unidentified protein. J. Bacteriol. 190:2096-2105. http://dx.doi.org/10.1128/JB.01813-07.
62. Rikihisa Y, Zhang Y, Park J. 1994. Inhibition of infection of macrophages with Ehrlichia risticii by cytochalasins, monodansylcadaverine, and taxol. Infect. Immun. 62:5126-5132.
63. Kenney LJ, Bauer MD, Silhavy TJ. 1995. Phosphorylation-dependent conformational changes in OmpR, an osmoregulatory DNA-binding protein of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 92:8866-8870. http://dx.doi.org/10.1073/pnas.92.19.8866.
64. Wang X, Kikuchi T, Rikihisa Y. 2007. Proteomic identification of a novel Anaplasma phagocytophilum DNA binding protein that regulates a putative transcription factor. J. Bacteriol. 189:4880-4886. http://dx.doi.org/10.1128/JB.00318-07.