Cyclic dimeric GMP signaling regulates intracellular aggregation, sessility, and growth of Ehrlichia chaffeensis

Infection and Immunity

Volumn 79, Issue 10, 2011, Pages 3905-3912

  Kumagai, Yumi ^a,c   Matsuo, Junji ^a   Cheng, Zhihui ^a   Hayakawa, Yoshihiro ^b   Rikihisa, Yasuko ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b AICHI INSTITUTE OF TECHNOLOGY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 O DI(TERT BUTYLDIMETHYSILYL) C DI GMP; CYCLIC DIMERIC GMP; CYCLIC GMP; CYCLIC GMP DERIVATIVE; MATRIX PROTEIN; PLEC PROTEIN; PLED PROTEIN; SERINE PROTEINASE INHIBITOR; TRP120 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; CELL AGGREGATION; CELL FUNCTION; CELL ISOLATION; CELL MATURATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; EHRLICHIA CHAFFEENSIS; HOST CELL; MORULA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; SHAM PROCEDURE; UPREGULATION;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CELL LINE; CYCLIC GMP; DIMERIZATION; EHRLICHIA CHAFFEENSIS; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INCLUSION BODIES; MONOCYTES; PHOSPHORUS-OXYGEN LYASES; PROTEIN KINASES; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 80855127776     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05320-11     Document Type: Article

References (44)

1. Aldridge, P., and U. Jenal. 1999. Cell cycle-dependent degradation of a flagellar motor component requires a novel-type response regulator. Mol. Microbiol. 32:379-391.
2. Barnewall, R. E., Y. Rikihisa, and E. H. Lee. 1997. Ehrlichia chaffeensis inclusions are early endosomes which selectively accumulate transferrin receptor. Infect. Immun. 65:1455-1461.
3. Cheng, Z., Y. Kumagai, M. Lin, C. Zhang, and Y. Rikihisa. 2006. Intraleukocyte expression of two-component systems in Ehrlichia chaffeensis and Anaplasma phagocytophilum and effects of the histidine kinase inhibitor closantel. Cell Microbiol. 8:1241-1252.
4. Cheng, Z., X. Wang, and Y. Rikihisa. 2008. Regulation of type IV secretion apparatus genes during Ehrlichia chaffeensis intracellular development by a previously unidentified protein. J. Bacteriol. 190:2096-2105.
5. Christen, B., et al. 2006. Allosteric control of cyclic di-GMP signaling. J. Biol. Chem. 281:32015-32024.
6. Christen, M., et al. 2007. DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc. Natl. Acad. Sci. U. S. A. 104:4112-4117.
7. Curtis, P. D., and Y. V. Brun. 2010. Getting in the loop: regulation of development in Caulobacter crescentus. Microbiol. Mol. Biol. Rev. 74:13-41.
8. Demma, L. J., R. C. Holman, J. H. McQuiston, J. W. Krebs, and D. L. Swerdlow. 2006. Human monocytic ehrlichiosis and human granulocytic anaplasmosis in the United States, 2001-2002. Ann. N. Y. Acad. Sci. 1078:118-119.
9. Duerig, A., et al. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23:93-104.
10. Fang, X., and M. Gomelsky. 2010. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol. Microbiol. 76:1295-1305.
11. Gouin, E., et al. 1999. A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J. Cell Sci. 112:1697-1708.
12. Haglund, C. M., J. E. Choe, C. T. Skau, D. R. Kovar, and M. D. Welch. 2010. Rickettsia Sca2 is a bacterial formin-like mediator of actin-based motility. Nat. Cell Biol. 12:1057-1063.
13. Hecht, G. B., and A. Newton. 1995. Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus. J. Bacteriol. 177:6223-6229.
14. Heinzen, R. A., T. Hackstadt, and J. E. Samuel. 1999. Developmental biology of Coxiella burnettii. Trends Microbiol. 7:149-154.
15. Hengge, R. 2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7:263-273.
16. Huang, H., et al. 2008. Proteomic analysis of and immune responses to Ehrlichia chaffeensis lipoproteins. Infect. Immun. 76:3405-3414.
17. Jenal, U. 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol. 7:185-191.
18. Jenal, U., and J. Malone. 2006. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40:385-407.
19. Kulasakara, H., et al. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U. S. A. 103:2839-2844.
20. Kumagai, Y., Z. Cheng, M. Lin, and Y. Rikihisa. 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.
21. Kumagai, Y., H. Huang, and Y. Rikihisa. 2008. Expression and porin activity of P28 and OMP-1F during intracellular Ehrlichia chaffeensis development. J. Bacteriol. 190:3597-3605.
22. Kumagai, Y., J. Matsuo, Y. Hayakawa, and Y. Rikihisa. 2010. Cyclic di-GMP signaling regulates invasion by Ehrlichia chaffeensis of human monocytes. J. Bacteriol. 192:4122-4133.
23. Lai, T. H., Y. Kumagai, M. Hyodo, Y. Hayakawa, and Y. Rikihisa. 2009. The Anaplasma phagocytophilum PleC histidine kinase and PleD diguanylate cyclase two-component system and role of cyclic Di-GMP in host cell infection. J. Bacteriol. 191:693-700.
24. McWhirter, S. M., et al. 2009. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 206:1899-1911.
25. Miura, K., and Y. Rikihisa. 2009. Liver transcriptome profiles associated with strain-specific Ehrlichia chaffeensis-induced hepatitis in SCID mice. Infect. Immun. 77:245-254.
26. Mott, J., R. E. Barnewall, and Y. Rikihisa. 1999. Human granulocytic ehrlichiosis agent and Ehrlichia chaffeensis reside in different cytoplasmic compartments in HL-60 cells. Infect. Immun. 67:1368-1378.
27. Moulder, J. W. 1985. Comparative biology of intracellular parasitism. Microbiol. Rev. 49:298-337.
28. Paddock, C. D., and J. E. Childs. 2003. Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin. Microbiol. Rev. 16:37-64.
29. Paul, R., et al. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-727.
30. Popov, V. L., X. Yu, and D. H. Walker. 2000. The 120 kDa outer membrane protein of Ehrlichia chaffeensis: preferential expression on dense-core cells and gene expression in Escherichia coli associated with attachment and entry. Microb. Pathog. 28:71-80.
31. Qiu, D., V. M. Eisinger, D. W. Rowen, and H. D. Yu. 2007. Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 104:8107-8112.
32. Rikihisa, Y. 1991. The tribe Ehrlichieae and ehrlichial diseases. Clin. Microbiol. Rev. 4:286-308.
33. Römling, U. 2005. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol. Life Sci. 62:1234-1246.
34. Römling, U. 2009. Cyclic di-GMP (c-Di-GMP) goes into host cells-c-Di-GMP signaling in the obligate intracellular pathogen Anaplasma phagocytophilum. J. Bacteriol. 191:683-686.
35. Römling, U., and D. Amikam. 2006. Cyclic di-GMP as a second messenger. Curr. Opin. Microbiol. 9:218-228.
36. Römling, U., M. Gomelsky, and M. Y. Galperin. 2005. c-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57:629-639.
37. Ryder, C., M. Byrd, and D. J. Wozniak. 2007. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr. Opin. Microbiol. 10:644-648.
38. Ryjenkov, D. A., R. Simm, U. Romling, and M. Gomelsky. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem. 281:30310-30314.
39. Solano, C., et al. 2009. Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc. Natl. Acad. Sci. U. S. A. 106:7997-8002.
40. Tamayo, R., J. T. Pratt, and A. Camilli. 2007. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu. Rev. Microbiol. 61:7997-8002.
41. Thomas, S., V. L. Popov, and D. H. Walker. 2010. Exit mechanisms of the intracellular bacterium Ehrlichia. PLoS One 5:e15775.
42. Van Kirk, L. S., S. F. Hayes, and R. A. Heinzen. 2000. Ultrastructure of Rickettsia rickettsii actin tails and localization of cytoskeletal proteins. Infect. Immun. 68:4706-4713.
43. Zhang, J. Z., V. L. Popov, S. Gao, D. H. Walker, and X. J. Yu. 2007. The developmental cycle of Ehrlichia chaffeensis in vertebrate cells. Cell Microbiol. 9:610-618.
44. Zhang, Y., N. Ohashi, E. H. Lee, A. Tamura, and Y. Rikihisa. 1997. Ehrlichia sennetsu groE operon and antigenic properties of the GroEL homolog. FEMS Immunol. Med. Microbiol. 18:39-46.