Ehrlichia moonlighting effectors and interkingdom interactions with the mononuclear phagocyte

Microbes and Infection

Volumn 15, Issue 14-15, 2013, Pages 1005-1016

  Dunphy, Paige Selvy ^a   Luo, Tian ^a   McBride, Jere W ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Effector; Ehrlichia; Human monocytotropic ehrlichiosis; Moonlighting protein; Nucleomodulin; Post translational modification; Tandem repeat protein; Type 1 secretion system; Zoonosis

Indexed keywords

ANKYRIN; BACTERIAL PROTEIN; NUCLEOMODULIN; TANDEM REPEAT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL SURVIVAL; EHRLICHIA CHAFFEENSIS; EPIGENETICS; EUKARYOTE; GENE EXPRESSION; GRAM NEGATIVE BACTERIUM; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; MOLECULAR INTERACTION; MONONUCLEAR PHAGOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TYPE I SECRETION SYSTEM; TYPE IV SECRETION SYSTEM;

ANAPLASMATACEAE; EHRLICHIA; EHRLICHIA CHAFFEENSIS; EUKARYOTA; MAMMALIA; NEGIBACTERIA;

EFFECTOR; EHRLICHIA; HUMAN MONOCYTOTROPIC EHRLICHIOSIS; MOONLIGHTING PROTEIN; NUCLEOMODULIN; POST TRANSLATIONAL MODIFICATION; TANDEM REPEAT PROTEIN; TYPE 1 SECRETION SYSTEM; ZOONOSIS;

ANIMALS; ANKYRINS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL NUCLEUS; EHRLICHIA; EHRLICHIOSIS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SPACE; PHAGOCYTES; PROTEIN BINDING; PROTEIN TRANSPORT; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84889079800     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2013.09.011     Document Type: Article

References (66)

1. Anderson B.E., Dawson J.E., Jones D.C., Wilson K.H. Ehrlichia chaffeensis, a new species associated with human ehrlichiosis. J. Clin. Microbiol. 1991, 29:2838-2842.
2. Olano J.P., Walker D.H. Human ehrlichioses. Med. Clin. North Am. 2002, 86:375-392.
3. Olano J.P., Masters E., Hogrefe W., Walker D.H. Human monocytotropic ehrlichiosis, Missouri. Emerg. Infect. Dis. 2003, 9:1579-1586.
4. Paddock C.D., Sumner J.W., Shore G.M., Bartley D.C., Elie R.C., McQuade J.G., Martin C.R., Goldsmith C.S., Childs J.E. Isolation and characterization of Ehrlichia chaffeensis strains from patients with fatal ehrlichiosis. J. Clin. Microbiol. 1997, 35:2496-2502.
5. Ewing S.A., Dawson J.E., Kocan A.A., Barker R.W., Warner C.K., Panciera R.J., Fox J.C., Kocan K.M., Blouin E.F. Experimental transmission of Ehrlichia chaffeensis (Rickettsiales: Ehrlichieae) among white-tailed deer by Amblyomma americanum (Acari: Ixodidae). J. Med. Entomol. 1995, 32:368-374.
6. Ismail N., Bloch K.C., McBride J.W. Human ehrlichiosis and anaplasmosis. Clin. Lab. Med. 2010, 30:261-292.
7. Dumler J.S., Barbet A.F., Bekker C.P., Dasch G.A., Palmer G.H., Ray S.C., Rikihisa Y., Rurangirwa F.R. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and 'HGE agent' as subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 2001, 51:2145-2165.
8. Zhang J.Z., Popov V.L., Gao S., Walker D.H., Yu X.J. The developmental cycle of Ehrlichia chaffeensis in vertebrate cells. Cell Microbiol. 2007, 9:610-618.
9. Zhang J.Z., Sinha M., Luxon B.A., Yu X.J. Survival strategy of obligately intracellular Ehrlichia chaffeensis: novel modulation of immune response and host cell cycles. Infect. Immun. 2004, 72:498-507.
10. Rikihisa Y. Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells. Nat. Rev. Microbiol. 2010, 8:328-339.
11. McBride J.W., Walker D.H. Molecular and cellular pathobiology of Ehrlichia infection: targets for new therapeutics and immunomodulation strategies. Expert Rev. Mol. Med. 2011, 13:e3.
12. Mansueto P., Vitale G., Cascio A., Seidita A., Pepe I., Carroccio A., di Rosa S., Rini G.B., Cillari E., Walker D.H. New insight into immunity and immunopathology of Rickettsial diseases. Clin. Dev. Immunol. 2012, 2012:967852.
13. Zhang J.Z., McBride J.W., Yu X.J. L-selectin and E-selectin expressed on monocytes mediating Ehrlichia chaffeensis attachment onto host cells. FEMS Microbiol. Lett. 2003, 227:303-309.
14. Lin M., Rikihisa Y. Obligatory intracellular parasitism by Ehrlichia chaffeensis and Anaplasma phagocytophilum involves caveolae and glycosylphosphatidylinositol-anchored proteins. Cell Microbiol. 2003, 5:809-820.
15. Kumar D.M., Yamaguchi M., Miura K., Lin M., Los M., Coy J.F., Rikihisa Y. Ehrlichia chaffeensis uses its surface protein EtpE to bind GPI-anchored protein DNase X and trigger entry into mammalian cells. PloS Path. 2013, 9:e1003666.
16. Popov V.L., Yu X., Walker D.H. The 120kDa 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. 2000, 28:71-80.
17. Kumagai Y., Matsuo J., Hayakawa Y., Rikihisa Y. Cyclic di-GMP signaling regulates invasion by Ehrlichia chaffeensis of human monocytes. J. Bacteriol. 2010, 192:4122-4133.
18. Lin M., Zhu M.X., Rikihisa Y. 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. 2002, 70:889-898.
19. Barnewall R.E., Rikihisa Y., Lee E.H. Ehrlichia chaffeensis inclusions are early endosomes which selectively accumulate transferrin receptor. Infect. Immun. 1997, 65:1455-1461.
20. Dedonder S.E., Cheng C., Willard L.H., Boyle D.L., Ganta R.R. Transmission electron microscopy reveals distinct macrophage- and tick cell-specific morphological stages of Ehrlichia chaffeensis. PloS One 2012, 7:e36749.
21. Thomas S., Popov V.L., Walker D.H. Exit mechanisms of the intracellular bacterium Ehrlichia. PloS One 2010, 5:e15775.
22. Lin M., Rikihisa Y. Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid A biosynthesis and incorporate cholesterol for their survival. Infect. Immun. 2003, 71:5324-5331.
23. Hotopp J.C.L.M., Madupu R., Crabtree J., Angiuoli S.V., Eisen J.A., Seshadri R., Ren Q., Wu M., Utterback T.R., Smith S., Lewis M., Khouri H., Zhang C., Niu H., Lin Q., Ohashi N., Zhi N., Nelson W., Brinkac L.M., Dodson R.J., Rosovitz M.J., Sundaram J., Daugherty S.C., Davidsen T., Durkin A.S., Gwinn M., Haft D.H., Selengut J.D., Sullivan S.A., Zafar N., Zhou L., Benahmed F., Forberger H., Halpin R., Mulligan S., Robinson J., White O., Rikihisa Y., Tettelin H. Comparative genomics of emerging human ehrlichiosis agents. PloS Genet. 2006, e21.
24. Kuriakose J.A., Miyashiro S., Luo T., Zhu B., McBride J.W. Ehrlichia chaffeensis transcriptome in mammalian and arthropod hosts reveals differential gene expression and post transcriptional regulation. PloS One 2011, 6:e24136.
25. Ellison D.W., Clark T.R., Sturdevant D.E., Virtaneva K., Hackstadt T. Limited transcriptional responses of Rickettsia rickettsii exposed to environmental stimuli. PloS One 2009, 4:e5612.
26. Luo T., McBride J.W. Ehrlichia chaffeensis TRP32 interacts with host cell targets that influence intracellular survival. Infect. Immun. 2012, 80:2297-2306.
27. Wakeel A., Kuriakose J.A., McBride J.W. An Ehrlichia chaffeensis tandem repeat protein interacts with multiple host targets involved in cell signaling, transcriptional regulation, and vesicle trafficking. Infect. Immun. 2009, 77:1734-1745.
28. Kumagai Y., Huang H., Rikihisa Y. Expression and porin activity of P28 and OMP-1F during intracellular Ehrlichia chaffeensis development. J. Bacteriol. 2008, 190:3597-3605.
29. Kumagai Y., Cheng Z., Lin M., Rikihisa Y. Biochemical activities of three pairs of Ehrlichia chaffeensis two-component regulatory system proteins involved in inhibition of lysosomal fusion. Infect. Immun. 2006, 74:5014-5022.
30. Cheng Z., Kumagai Y., Lin M., Zhang C., Rikihisa Y. Intra-leukocyte expression of two-component systems in Ehrlichia chaffeensis and Anaplasma phagocytophilum and effects of the histidine kinase inhibitor closantel. Cell Microbiol. 2006, 8:1241-1252.
31. Cheng Z., Miura K., Popov V.L., Kumagai Y., Rikihisa Y. Insights into the CtrA regulon in development of stress resistance in obligatory intracellular pathogen Ehrlichia chaffeensis. Mol. Microbiol. 2011, 82:1217-1234.
32. Bao W., Kumagai Y., Niu H., Yamaguchi M., Miura K., Rikihisa Y. Four VirB6 paralogs and VirB9 are expressed and interact in Ehrlichia chaffeensis-containing vacuoles. J. Bacteriol. 2009, 191:278-286.
33. Rikihisa Y., Lin M., Niu H., Cheng Z. Type IV secretion system of Anaplasma phagocytophilum and Ehrlichia chaffeensis. Ann. N.Y. Acad. Sci. 2009, 1166:106-111.
34. Cheng Z., Wang X., Rikihisa Y. Regulation of type IV secretion apparatus genes during Ehrlichia chaffeensis intracellular development by a previously unidentified protein. J. Bacteriol. 2008, 190:2096-2105.
35. Liu H., Bao W., Lin M., Niu H., Rikihisa Y. Ehrlichia type IV secretion effector ECH0825 is translocated to mitochondria and curbs ROS and apoptosis by upregulating host MnSOD. Cell Microbiol. 2012, 14:1037-1050.
36. Delepelaire P. Type I secretion in gram-negative bacteria. Biochim. Biophys. Acta 2004, 1694:149-161.
37. Holland I.B., Schmitt L., Young J. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol. Membr. Biol. 2005, 22:29-39.
38. Wakeel A., den Dulk-Ras A., Hooykaas P.J., McBride J.W. Ehrlichia chaffeensis tandem repeat proteins and Ank200 are type 1 secretion system substrates related to the repeats-in-toxin exoprotein family. Front. Cell. Infect. Microbiol. 2011, 1:22.
39. McBride J.W., Comer J.E., Walker D.H. Novel immunoreactive glycoprotein orthologs of Ehrlichia spp. Ann. N.Y. Acad. Sci. 2003, 990:678-684.
40. McBride J.W., Corstvet R.E., Gaunt S.D., Boudreaux C., Guedry T., Walker D.H. Kinetics of antibody response to Ehrlichia canis immunoreactive proteins. Infect. Immun. 2003, 71:2516-2524.
41. Kuriakose J.A., Zhang X., Luo T., McBride J.W. Molecular basis of antibody mediated immunity against Ehrlichia chaffeensis involves species-specific linear epitopes in tandem repeat proteins. Microbes Infect. Inst. Pasteur 2012, 14:1054-1063.
42. Wakeel A., Zhang X., McBride J.W. Mass spectrometric analysis of Ehrlichia chaffeensis tandem repeat proteins reveals evidence of phosphorylation and absence of glycosylation. PloS One 2010, 5:e9552.
43. McBride J.W., Zhang X., Wakeel A., Kuriakose J.A. Tyrosine-phosphorylated Ehrlichia chaffeensis and Ehrlichia canis tandem repeat orthologs contain a major continuous cross-reactive antibody epitope in lysine-rich repeats. Infect. Immun. 2011, 79:3178-3187.
44. Doyle C.K., Nethery K.A., Popov V.L., McBride J.W. Differentially expressed and secreted major immunoreactive protein orthologs of Ehrlichia canis and E. chaffeensis elicit early antibody responses to epitopes on glycosylated tandem repeats. Infect. Immun. 2006, 74:711-720.
45. Luo T., Zhang X., Wakeel A., Popov V.L., McBride J.W. A variable-length PCR target protein of Ehrlichia chaffeensis contains major species-specific antibody epitopes in acidic serine-rich tandem repeats. Infect. Immun. 2008, 76:1572-1580.
46. Luo T., Zhang X., McBride J.W. Major species-specific antibody epitopes of the Ehrlichia chaffeensis p120 and E. canis p140 orthologs in surface-exposed tandem repeat regions. Clin. Vaccine Immunol. CVI 2009, 16:982-990.
47. Luo T., Zhang X., Nicholson W.L., Zhu B., McBride J.W. Molecular characterization of antibody epitopes of Ehrlichia chaffeensis ankyrin protein 200 and tandem repeat protein 47 and evaluation of synthetic immunodeterminants for serodiagnosis of human monocytotropic ehrlichiosis. Clin. Vaccine Immunol. CVI 2010, 17:87-97.
48. Zhu B., Kuriakose J.A., Luo T., Ballesteros E., Gupta S., Fofanov Y., McBride J.W. Ehrlichia chaffeensis TRP120 binds a G+C-rich motif in host cell DNA and exhibits eukaryotic transcriptional activator function. Infect. Immun. 2011, 79:4370-4381.
49. Huang H., Lin M., Wang X., Kikuchi T., Mottaz H., Norbeck A., Rikihisa Y. Proteomic analysis of and immune responses to Ehrlichia chaffeensis lipoproteins. Infect. Immun. 2008, 76:3405-3414.
50. Dunphy P.S., Luo T., McBride J.W. Host Post Translational Modification Pathways Mediate Nuclear Translocation of Ehrlichia Chaffeensis Type 1 Secreted Effectors 2013, American Society of Rickettsiology Annual Meeting.
51. Dunphy P.S., Luo T., McBride J.W. Ehrlichia Type 1 Secreted Effectors Exploit Host SUMO Pathways 2013, American Society of Microbiology General Meeting.
52. Nethery K.A., Doyle C.K., Zhang X., McBride J.W. Ehrlichia canis gp200 contains dominant species-specific antibody epitopes in terminal acidic domains. Infect. Immun. 2007, 75:4900-4908.
53. Zhu B., Nethery K.A., Kuriakose J.A., Wakeel A., Zhang X., McBride J.W. Nuclear translocated Ehrlichia chaffeensis ankyrin protein interacts with a specific adenine-rich motif of host promoter and intronic Alu elements. Infect. Immun. 2009, 77:4243-4255.
54. Luo T., Kuriakose J.A., Zhu B., Wakeel A., McBride J.W. Ehrlichia chaffeensis TRP120 interacts with a diverse array of eukaryotic proteins involved in transcription, signaling, and cytoskeleton organization. Infect. Immun. 2011, 79:4382-4391.
55. Junco S.E., Wang R., Gaipa J.C., Taylor A.B., Schirf V., Gearhart M.D., Bardwell V.J., Demeler B., Hart P.J., Kim C.A. Structure of the polycomb group protein PCGF1 in complex with BCOR reveals basis for binding selectivity of PCGF homologs. Structure 2013, 21:665-671.
56. Bazzocchi C., Comazzi S., Santoni R., Bandi C., Genchi C., Mortarino M. Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunol. 2007, 29:73-79.
57. Xiong Q., Bao W., Ge Y., Rikihisa Y. Ehrlichia ewingii infection delays spontaneous neutrophil apoptosis through stabilization of mitochondria. J. Infect. Dis. 2008, 197:1110-1118.
58. Kajikawa S., Nakayama H., Suzuki M., Takashima A., Murayama O., Nishihara M., Takahashi M., Doi K. Increased expression of rat ribosomal protein L4 mRNA in 5-azacytidine-treated PC12 cells prior to apoptosis. Biochem. Biophy. Res. Commun. 1998, 252:220-224.
59. Donati G., Thomas G. Apoptosis in pluripotent stem cells: RPL11 strikes again. Cell Cycle 2012, 11:840.
60. Yang S.B., Chen X., Wu B.Y., Wang M.W., Cai C.H., Cho D.B., Chong J., Li P., Tang S.G., Yang P.C. Immunoglobulin kappa and immunoglobulin lambda are required for expression of the anti-apoptotic molecule Bcl-xL in human colorectal cancer tissue. Scand. J. Gastroenterol. 2009, 44:1443-1451.
61. Bierne H., Hamon M., Cossart P. Epigenetics and bacterial infections. Cold Spring Harbor Perspect. Med. 2012, 2:a010272.
62. Voytas D.F., Joung J.K. Plant science. DNA binding made easy. Science 2009, 326:1491-1492.
63. Rennoll-Bankert K.E., Dumler J.S. Lessons from Anaplasma phagocytophilum: chromatin remodeling by bacterial effectors. Infect. Disord. Drug Targets 2012, 12:380-387.
64. Bierne H., Cossart P. When bacteria target the nucleus: the emerging family of nucleomodulins. Cell Microbiol. 2012, 14:622-633.
65. Medvedeva Y.A., Fridman M.V., Oparina N.J., Malko D.B., Ermakova E.O., Kulakovskiy I.V., Heinzel A., Makeev V.J. Intergenic, gene terminal, and intragenic CpG islands in the human genome. BMC Genomics 2010, 11:48.
66. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011, 25:1010-1022.