Structure of the type IV secretion system in different strains of Anaplasma phagocytophilum

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Al Khedery, Basima ^a   Lundgren, Anna M ^a   Stuen, Snorre ^b   Granquist, Erik G ^b   Munderloh, Ulrike G ^c   Nelson, Curtis M ^c   Alleman, A Rick ^a   Mahan, Suman M ^d   Barbet, Anthony F ^a  

^a University of Florida College of Veterinary Medicine   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c UNIVERSITY OF MINNESOTA   (United States)

^d ZOETIS   (United States)

Author keywords

Anaplasma; Comparative genomics; phagocytophilum; Rickettsiales; T4SS

Indexed keywords

BACTERIAL PROTEIN; UNCLASSIFIED DRUG; VIRB10 PROTEIN; VIRB11 PROTEIN; VIRB3 PROTEIN; VIRB4 PROTEIN; VIRB6 PROTEIN; VIRB7 PROTEIN; VIRB8 PROTEIN; VIRB9 PROTEIN;

ANAPLASMA PHAGOCYTOPHILUM; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; GENE DUPLICATION; GENE LOCUS; GENE STRUCTURE; GENETIC VARIABILITY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; STRUCTURE ANALYSIS; TYPE IV SECRETION SYSTEM; VIRB2 GENE; VIRB6 4 GENE; VIRB6 GENE;

AMINO ACID SEQUENCE; ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE; DOGS; GENETIC LOCI; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PERIPLASM; PROTEIN SUBUNITS; SPECIES SPECIFICITY;

ANAPLASMA; ANAPLASMA PHAGOCYTOPHILUM; ANIMALIA; BACTERIA (MICROORGANISMS); CANIS FAMILIARIS; EQUIDAE; IXODIDA; MAMMALIA; RICKETTSIALES; RODENTIA; VIR;

EID: 84870061216     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-678     Document Type: Article

References (55)

1. Dumler JS, Choi KS, Garcia-Garcia JC, Barat NS, Scorpio DG, Garyu JW, et al. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis 2005, 11:1828-1834. 10.3201/eid1112.050898, 3367650, 16485466.
2. Jin H, Wei F, Liu Q, Qian J. Epidemiology and control of human granulocytic anaplasmosis: a systematic review. Vector Borne Zoonotic Dis 2012, 12:269-274. 10.1089/vbz.2011.0753, 22217177.
3. Bakken JS, Dumler JS. Clinical diagnosis and treatment of human granulocytotropic anaplasmosis. Ann N Y Acad Sci 2006, 1078:236-247. 10.1196/annals.1374.042, 17114714.
4. Dahlgren FS, Mandel EJ, Krebs JW, Massung RF, McQuiston JH. Increasing incidence of Ehrlichia chaffeensis and Anaplasma phagocytophilum in the United States, 2000-2007. Am J Trop Med Hyg 2011, 85:124-131. 10.4269/ajtmh.2011.10-0613, 3122356, 21734137.
5. Weil AA, Baron EL, Brown CM, Drapkin MS. Clinical findings and diagnosis in human granulocytic anaplasmosis: a case series from Massachusetts. Mayo Clin Proc 2012, 87:233-239. 10.1016/j.mayocp.2011.09.008, 3498394, 22386178.
6. Li H, Zhou Y, Wang W, Guo D, Huang S, Jie S. The clinical characteristics and outcomes of patients with human granulocytic anaplasmosis in China. Int J Infect Dis 2011, 15:e859-e866. 10.1016/j.ijid.2011.09.008, 22015246.
7. Eberts MD, Beall MJ, Stillman BA, Chandrashekar R, Breitschwerdt EB. Typical and atypical manifestations of Anaplasma phagocytophilum infection in dogs. J Am Anim Hosp Assoc 2011, 47:e86-e94. 10.5326/JAAHA-MS-5578, 22058372.
8. Bowman D, Little SE, Lorentzen L, Shields J, Sullivan MP, Carlin EP. Prevalence and geographic distribution of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis, and Anaplasma phagocytophilum in dogs in the United States: results of a national clinic-based serologic survey. Vet Parasitol 2009, 160:138-148. 10.1016/j.vetpar.2008.10.093, 19150176.
9. Foley J, Nieto NC, Madigan J, Sykes J. Possible differential host tropism in Anaplasma phagocytophilum strains in the Western United States. Ann N Y Acad Sci 2008, 1149:94-97. 10.1196/annals.1428.066, 19120182.
10. Foley JE, Nieto NC, Massung R, Barbet A, Madigan J, Brown RN. Distinct ecologically relevant strains of Anaplasma phagocytophilum. Emerg Infect Dis 2009, 15:842-843. 10.3201/eid1505.081502, 2687023, 19402993.
11. Massung RF, Mather TN, Priestley RA, Levin ML. Transmission efficiency of the AP-variant 1 strain of Anaplasma phagocytophila. Ann N Y Acad Sci 2003, 990:75-79. 10.1111/j.1749-6632.2003.tb07340.x, 12860603.
12. Massung RF, Priestley RA, Miller NJ, Mather TN, Levin ML. Inability of a variant strain of Anaplasma phagocytophilum to infect mice. J Infect Dis 2003, 188:1757-1763. 10.1086/379725, 14639548.
13. Massung RF, Courtney JW, Hiratzka SL, Pitzer VE, Smith G, Dryden RL. Anaplasma phagocytophilum in white-tailed deer. Emerg Infect Dis 2005, 11:1604-1606. 10.3201/eid1110.041329, 3366735, 16318705.
14. Stuen S. Anaplasma phagocytophilum - the most widespread tick-borne infection in animals in Europe. Vet Res Commun 2007, 31(Suppl 1):79-84.
15. Dunning Hotopp JC, Lin M, Madupu R, Crabtree J, Angiuoli SV, Eisen J, et al. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2006, 2:e21. 10.1371/journal.pgen.0020021, 1366493, 16482227.
16. Rikihisa Y, Lin M, Niu H. Type IV secretion in the obligatory intracellular bacterium Anaplasma phagocytophilum. Cell Microbiol 2010, 12:1213-1221. 10.1111/j.1462-5822.2010.01500.x, 20670295.
17. Waksman G, Fronzes R. Molecular architecture of bacterial type IV secretion systems. Trends Biochem Sci 2010, 35:691-698. 10.1016/j.tibs.2010.06.002, 20621482.
18. Niu H, Rikihisa Y, Yamaguchi M, Ohashi N. Differential expression of VirB9 and VirB6 during the life cycle of Anaplasma phagocytophilum in human leucocytes is associated with differential binding and avoidance of lysosome pathway. Cell Microbiol 2006, 8:523-534. 10.1111/j.1462-5822.2005.00643.x, 16469062.
19. Ge Y, Rikihisa Y. Identification of novel surface proteins of Anaplasma phagocytophilum by affinity purification and proteomics. J Bacteriol 2007, 189:7819-7828. 10.1128/JB.00866-07, 2168727, 17766422.
20. Alvarez-Martinez CE, Christie PJ. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 2009, 73:775-808. 2786583, 19946141.
21. Lopez JE, Palmer GH, Brayton KA, Dark MJ, Leach SE, Brown WC. Immunogenicity of Anaplasma marginale type IV secretion system proteins in a protective outer membrane vaccine. Infect Immun 2007, 75:2333-2342. 10.1128/IAI.00061-07, 1865776, 17339347.
22. Morse K, Norimine J, Palmer GH, Sutten EL, Baszler TV, Brown WC. Association and evidence for linked recognition of type IV secretion system proteins VirB9-1, VirB9-2, and VirB10 in Anaplasma marginale. Infect Immun 2012, 80:215-227. 10.1128/IAI.05798-11, 3255688, 22038917.
23. Morse K, Norimine J, Hope JC, Brown WC. Breadth of the CD4(+) T cell response to Anaplasma marginale VirB9-1, VirB9-2 and VirB10 and MHC class II DR and DQ restriction elements. Immunogenetics 2012, 64:507-523. 10.1007/s00251-012-0606-4, 22361828.
24. Araujo FR, Costa CM, Ramos CA, Farias TA, Souza II, Melo ES, et al. IgG and IgG2 antibodies from cattle naturally infected with Anaplasma marginale recognize the recombinant vaccine candidate antigens VirB9, VirB10, and elongation factor-Tu. Mem Inst Oswaldo Cruz 2008, 103:186-190. 10.1590/S0074-02762008000200010, 18425271.
25. Sutten EL, Norimine J, Beare PA, Heinzen RA, Lopez JE, Morse K, et al. Anaplasma marginale type IV secretion system proteins VirB2, VirB7, VirB11, and VirD4 are immunogenic components of a protective bacterial membrane vaccine. Infect Immun 2010, 78:1314-1325. 10.1128/IAI.01207-09, 2825951, 20065028.
26. Dark MJ, Al-Khedery B, Barbet AF. Multistrain genome analysis identifies candidate vaccine antigens of Anaplasma marginale. Vaccine 2011, 29:4923-4932. 10.1016/j.vaccine.2011.04.131, 3133685, 21596083.
27. Park J, Kim KJ, Choi KS, Grab DJ, Dumler JS. Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cell Microbiol 2004, 6:743-751. 10.1111/j.1462-5822.2004.00400.x, 15236641.
28. Garcia-Garcia JC, Rennoll-Bankert KE, Pelly S, Milstone AM, Dumler JS. Silencing of host cell CYBB gene expression by the nuclear effector AnkA of the intracellular pathogen Anaplasma phagocytophilum. Infect Immun 2009, 77:2385-2391. 10.1128/IAI.00023-09, 2687357, 19307214.
29. Niu H, Kozjak-Pavlovic V, Rudel T, Rikihisa Y. Anaplasma phagocytophilum Ats-1 is imported into host cell mitochondria and interferes with apoptosis induction. PLoS Pathog 2010, 6:e1000774. 10.1371/journal.ppat.1000774, 2824752, 20174550.
30. Gillespie JJ, Brayton KA, Williams KP, Diaz MA, Brown WC, Azad AF, Sobral BW. Phylogenomics reveals a diverse Rickettsiales type IV secretion system. Infect Immun 2010, 78:1809-1823. 10.1128/IAI.01384-09, 2863512, 20176788.
31. Ohashi N, Zhi N, Lin Q, Rikihisa Y. Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect Immun 2002, 70:2128-2138. 10.1128/IAI.70.4.2128-2138.2002, 127848, 11895979.
32. Berger BR, Christie PJ. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J Bacteriol 1994, 176:3646-3660. 205554, 8206843.
33. Yuan Q, Carle A, Gao C, Sivanesan D, Aly KA, Hoppner C, et al. Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J Biol Chem 2005, 280:26349-26359. 10.1074/jbc.M502347200, 15901731.
34. Judd PK, Kumar RB, Das A. Spatial location and requirements for the assembly of the Agrobacterium tumefaciens type IV secretion apparatus. Proc Natl Acad Sci USA 2005, 102:11498-11503. 10.1073/pnas.0505290102, 1183602, 16076948.
35. Kumar RB, Xie YH, Das A. Subcellular localization of the Agrobacterium tumefaciens T-DNA transport pore proteins: VirB8 is essential for the assembly of the transport pore. Mol Microbiol 2000, 36:608-617.
36. Cascales E, Christie PJ. Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc Natl Acad Sci USA 2004, 101:17228-17233. 10.1073/pnas.0405843101, 535377, 15569944.
37. Rances E, Voronin D, Tran-Van V, Mavingui P. Genetic and functional characterization of the type IV secretion system in Wolbachia. J Bacteriol 2008, 190:5020-5030. 10.1128/JB.00377-08, 2447017, 18502862.
38. Anderson LB, Hertzel AV, Das A. Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc Natl Acad Sci USA 1996, 93:8889-8894. 10.1073/pnas.93.17.8889, 38564, 8799123.
39. Spudich GM, Fernandez D, Zhou XR, Christie PJ. Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci USA 1996, 93:7512-7517. 10.1073/pnas.93.15.7512, 38776, 8755505.
40. Bayliss R, Harris R, Coutte L, Monier A, Fronzes R, Christie PJ, et al. NMR structure of a complex between the VirB9/VirB7 interaction domains of the pKM101 type IV secretion system. Proc Natl Acad Sci USA 2007, 104:1673-1678. 10.1073/pnas.0609535104, 1785264, 17244707.
41. Ge Y, Rikihisa Y. Surface-exposed proteins of Ehrlichia chaffeensis. Infect Immun 2007, 75:3833-3841. 10.1128/IAI.00188-07, 1951975, 17517859.
42. Meeus PF, Brayton KA, Palmer GH, Barbet AF. Conservation of a gene conversion mechanism in two distantly related paralogues of Anaplasma marginale. Mol Microbiol 2003, 47:633-643. 10.1046/j.1365-2958.2003.03331.x, 12535066.
43. Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC, et al. 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. 10.1099/00207713-51-6-2145, 11760958.
44. Gribble DH. Equine ehrlichiosis. J Am Vet Med Assoc 1969, 155:462-469.
45. Johnson RC, Kodner C, Jarnefeld J, Eck DK, Xu Y. Agents of human anaplasmosis and Lyme disease at Camp Ripley, Minnesota. Vector Borne Zoonotic Dis 2011, 11:1529-1534. 10.1089/vbz.2011.0633, 3231789, 21867420.
46. Munderloh UG, Jauron SD, Fingerle V, Leitritz L, Hayes SF, Hautman JM, et al. Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. J Clin Microbiol 1999, 37:2518-2524. 85271, 10405394.
47. Massung RF, Levin ML, Munderloh UG, Silverman DJ, Lynch MJ, Gaywee JK, Kurtti TJ. Isolation and propagation of the Ap-Variant 1 strain of Anaplasma phagocytophilum in a tick cell line. J Clin Microbiol 2007, 45:2138-2143. 10.1128/JCM.00478-07, 1932999, 17475757.
48. Granquist EG, Bardsen K, Bergstrom K, Stuen S. Variant and individual dependent nature of persistent Anaplasma phagocytophilum infection. Acta Vet Scand 2010, 52:25. 10.1186/1751-0147-52-25, 2859769, 20398321.
49. Felsheim RF, Herron MJ, Nelson CM, Burkhardt NY, Barbet AF, Kurtti TJ, Munderloh UG. Transformation of Anaplasma phagocytophilum. BMC Biotechnol 2006, 6:42. 10.1186/1472-6750-6-42, 1635035, 17076894.
50. Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 2008, 9:286-298. 10.1093/bib/bbn013, 18372315.
51. Goodstadt L, Ponting CP. CHROMA: consensus-based colouring of multiple alignments for publication. Bioinformatics 2001, 17:845-846. 10.1093/bioinformatics/17.9.845, 11590103.
52. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992, 8:275-282.
53. Hopp TP, Woods KR. A computer program for predicting protein antigenic determinants. Mol Immunol 1983, 20:483-489. 10.1016/0161-5890(83)90029-9, 6191210.
54. Hopp TP. Use of hydrophilicity plotting procedures to identify protein antigenic segments and other interaction sites. Methods Enzymol 1989, 178:571-585.
55. Goecks J, Nekrutenko A, Taylor J. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. 10.1186/gb-2010-11-8-r86, 2945788, 20738864.