Anaplasma marginale major surface protein 1a: A marker of strain diversity with implications for control of bovine anaplasmosis

Ticks and Tick-borne Diseases

Volumn 6, Issue 3, 2015, Pages 205-210

  Cabezas Cruz, Alejandro ^a,b   de la Fuente, José ^b,c  

^a UNIV LILLE   (France)

^b INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^c OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

A. marginale; Control; Genetic diversity; Molecular diagnostics

Indexed keywords

BACTERIAL PROTEIN; BIOLOGICAL MARKER; EPITOPE; MAJOR SURFACE PROTEIN 1A; UNCLASSIFIED DRUG; ADHESIN; MAJOR SURFACE PROTEIN 1A, ANAPLASMA; OUTER MEMBRANE PROTEIN;

ANAPLASMA MARGINALE; ANAPLASMOSIS; BACTERIAL GENE; BACTERIAL STRAIN; EPITOPE MAPPING; GENETIC CODE; GENETIC VARIABILITY; HOUSEKEEPING GENE; INFECTION CONTROL; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; SEQUENCE ANALYSIS; SHORT SURVEY; STRAIN IDENTIFICATION; TANDEM REPEAT; TAXONOMY; AMINO ACID SEQUENCE; ANIMAL; BOVINE; CATTLE DISEASES; CLASSIFICATION; GENETIC VARIATION; GENETICS; GENOTYPE; METABOLISM; MICROBIOLOGY; TICK;

ANAPLASMA MARGINALE; BACTERIA (MICROORGANISMS); BOS; BOVINAE; IXODIDA;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; ANAPLASMA MARGINALE; ANAPLASMOSIS; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CATTLE; CATTLE DISEASES; GENETIC VARIATION; GENOTYPE; PHYLOGENY; TICKS;

EID: 84928207062     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2015.03.007     Document Type: Short Survey

References (53)

1. Allred D.R., McGuire T.C., Palmer G.H., Leib S.R., Harkins T.M., McElwain T.F., Barbet A.F. Molecular basis for surface antigen size polymorphisms and conservation of a neutralization-sensitive epitope in Anaplasma marginale. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:3220-3224.
2. Almazán C., Medrano C., Ortiz M., de la Fuente J. Genetic diversity of Anaplasma marginale strains from an outbreak of bovine anaplasmosis in an endemic area. Vet. Parasitol. 2008, 158:103-109.
3. 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.
4. Brown W.C., McGuire T.C., Mwangi W., Kegerreis K.A., Macmillan H., Lewin H.A., Palmer G.H. Major histocompatibility complex class II DR-restricted memory CD4(+) T lymphocytes recognize conserved immunodominant epitopes of Anaplasma marginale major surface protein 1a. Infect. Immun. 2002, 70:521-532.
5. Cabezas-Cruz A., Passos L.M.F., Lis K., Kenneil R., Valdés J.J., Ferrolho J., Tonk M., Pohl A.E., Grubhoffer L., Zweygarth E., Shkap V., Ribeiro M.F.B., Estrada-Peña A., Kocan K.M., de la Fuente J. Functional and immunological relevance of Anaplasma marginale major surface protein 1a sequence and structural analysis. PLOS ONE 2013, 8:e65243.
6. Cabezas-Cruz A., Zweygarth E., Ribeiro M.F.B., da Silveira A.G.J., de la Fuente J., Grubhoffer L., Valdés J.J., Passos M.F.L. New species of Ehrlichia isolated from Rhipicephalus (Boophilus) microplus shows an ortholog of the E. canis major immunogenic glycoprotein gp36 with a new sequence of tandem repeats. Parasites Vectors 2012, 5:291.
7. Canales M., Almazán C., Pérez de la Lastra J.M., de la Fuente J. Anaplasma marginale major surface protein 1a directs cell surface display of tick BM95 immunogenic peptides on Escherichia coli. J. Biotechnol. 2008, 135:326-332.
8. Chan J.Z., Halachev M.R., Loman N.J., Constantinidou C., Pallen M.J. Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol. 2012, 12:302.
9. Cohan F.M., Perry E.B. A systematics for discovering the fundamental units of bacterial diversity. Curr. Biol. 2007, 17:373-386.
10. de la Fuente J., Van Den Bussche R.A., Prado T., Kocan K.M. Anaplasma marginale major surface protein 1a genotypes evolved under positive selection pressure but are not markers for geographic strains. J. Clin. Microbiol. 2003, 41:1609-1616.
11. de la Fuente J., Garcia-Garcia J.C., Barbet A.F., Blouin E.F., Kocan K.M. Adhesion of outer membrane proteins containing tandem repeats of Anaplasma and Ehrlichia species (Rickettsiales: Anaplasmataceae) to tick cells. Vet. Microbiol. 2004, 98:313-322.
12. de la Fuente J., Ruybal P., Mtshali M.S., Naranjo V., Shuqing Li., Mangold A.J., Rodríguez S.D., Jiménez R., Vicente J., Moretta R., Torina A., Almazán C., Mbati P.M., Torioni de Echaide S., Farber M., Rosario-Cruz R., Gortazar C., Kocan K.M. Analysis of world strains of Anaplasma marginale using major surface protein 1a repeat sequences. Vet. Microbiol. 2007, 119:382-390.
13. 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.
14. 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.
15. Estrada-Peña A., Naranjo V., Acevedo-Whitehouse K., Mangold A., Kocan K., de la Fuente J. Phylogeographic analysis reveals association of tick-borne pathogen, Anaplasma marginale, MSP1α sequences with ecological traits affecting tick vector performance. BMC Biol. 2009, 57:1-13.
16. Fournier P.E., Roux V., Raoult D. Phylogenetic analysis of spotted fever group rickettsiae by study of the outer surface protein rOmpA. Int. J. Syst. Bacteriol. 1998, 48:839-849.
17. Garcia-Garcia J.C., de la Fuente J., Kocan K.M., Blouin E.F., Halbur T., Onet V.C., Saliki J.T. Mapping of B-cell epitopes in the N-terminal repeated peptides of Anaplasma marginale major surface protein 1a and characterization of the humoral immune response of cattle immunized with recombinant and whole organism antigens. Vet. Immunol. Immunopathol. 2004, 98:137-151.
18. Hsieh Y.C., Lee C.C., Tsang C.L., Chung Y.T. Detection and characterization of four novel genotypes of Ehrlichia canis from dogs. Vet. Microbiol. 2010, 146:70-75.
19. Inokuma H., Brouqui P., Drancourt M., Raoult D. Citrate synthase gene sequence: a new tool for phylogenetic analysis and identification of Ehrlichia. J. Clin. Microbiol. 2001, 39:3031-3039.
20. Kuttler K.L., Zaugg J.L., Johnson L.W. Serologic and clinical responses of premunized, vaccinated, and previously infected cattle to challenge exposure by two different Anaplasma marginale isolates. Am. J. Vet. Res. 1984, 45:2223-2226.
21. Lawrence J.G., Ochman H. Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9413-9417.
22. Lee J.H., Park H.S., Jang W.J., Koh S.E., Kim J.M., Shim S.K., Park M.Y., Kim Y.W., Kim B.J., Kook Y.H., Park K.H., Lee S.H. Differentiation of rickettsiae by groEL gene analysis. J. Clin. Microbiol. 2003, 41:2952-2960.
23. Lew A.E., Gale K.R., Minchin C.M., Shkap V., de Waal D.T. Phylogenetic analysis of the erythrocytic Anaplasma species based on 16S rDNA and GroEL (HSP60) sequences of A. marginale, A. centrale, and A. ovis and the specific detection of A. centrale vaccine strain. Vet. Microbiol. 2003, 92:145-160.
24. Massey S.E., Churbanov A., Rastogi S., Liberles D.A. Characterizing positive and negative selection and their phylogenetic effects. Gene 2008, 418:22-26.
25. Merhej V., Raoult D. Rickettsial evolution in the light of comparative genomics. Biol. Rev. Camb. Philos. Soc. 2011, 86:379-405.
26. Mutshembele A.M., Cabezas-Cruz A., Mtshali M.S., Thekisoe O.M.M., Galindo R.C., de la Fuente J. Epidemiology and evolution of genetic variability of Anaplasma marginale in South Africa. Ticks Tick Borne Dis. 2014, 5:624-631.
27. Jiménez-Ocampo R., Vega y Murguía C.A., Rojas-Ramírez E.E., García-Ortiz M.A., Preciado de la Torre J.F., Rosario-Cruz R., Rodríguez-Camarillo S.D. Genetic diversity of the msp1a gene variable region and msp4 gene of Anaplasma marginale strains from Mexico. Rev. Mex. Cienc. Pecu. 2012, 3:373-387.
28. Ødegaard F. How many species of arthropods? Erwin's estimate revised. Biol. J. Linn. Soc. 2000, 71:583-597.
29. Palmer G.H., Barbet A.F., Davis W.C., McGuire T.C. Immunization with an isolate-common surface protein protects cattle against anaplasmosis. Science 1986, 231:1299-1302.
30. Palmer G.H., Waghela S.D., Barbet A.F., Davis W.C., McGuire T.C. Characterization of a neutralization-sensitive epitope on the Am 105 surface protein of Anaplasma marginale. Int. J. Parasitol. 1987, 17:1279-1285.
31. Palmer G.H., Rurangirwa F.R., McElwain T.F. Strain composition of the ehrlichia Anaplasma marginale within persistently infected cattle, a mammalian reservoir for tick transmission. J. Clin. Microbiol. 2001, 39:631-635.
32. Palmer G.H., Brayton K.A. Antigenic variation and transmission fitness as drivers of bacterial strain structure. Cell. Microbiol. 2013, 15:1969-1975.
33. Pohl A.E., Cabezas-Cruz A., Ribeiro M.F.B., Silveira J.A.G., Silaghi C., Pfister K., Passos L.M.F. Detection of genetic diversity of Anaplasma marginale isolates in Minas Gerais, Brazil. Rev. Bras. Parasitol. Vet. 2013, 22:1-7.
34. Rosselló-Mora R., Amann R. The species concept for prokaryotes. FEMS Microbiol. Rev. 2001, 25:39-67.
35. Ruybal P., Moretta R., Perez A., Petrigh R., Zimmer P., Alcaraz E., Echaide I., Torioni de Echaide S., Kocan K.M., de la Fuente J., Farber M. Genetic diversity of Anaplasma marginale in Argentina. Vet. Parasitol. 2009, 162:176-180.
36. Sacchi A.B.V., Duarte J.M.B., André M.R., Machado R.Z. Prevalence and molecular characterization of Anaplasmataceae agents in free-ranging Brazilian marsh deer (Blastocerus dichotomus). Comp. Immun. Microbiol. Inf. Dis. 2012, 35:325-334.
37. Santos P.S., Nascimento R., Rodrigues L.P., Santos F.A., Faria P.C., Martins J.R., Brito-Madurro A.G., Madurro J.M., Goulart L.R. Functional epitope core motif of the Anaplasma marginale major surface protein 1a and its incorporation onto bioelectrodes for antibody detection. PLoS ONE 2012, 7:e33045.
38. Santos P.S., Sena A.A., Nascimento R., Araújo T.G., Mendes M.M., Martins J.R., Mineo T.W., Mineo J.R., Goulart L.R. Epitope-based vaccines with the Anaplasma marginale MSP1a functional motif induce a balanced humoral and cellular immune response in mice. PLOS ONE 2013, 8:e60311.
39. Silva J.B., Cabezas-Cruz A., Fonseca A.H., Barbosa J.D., de la Fuente J. Infection of water buffalo in Rio de Janeiro Brazil with Anaplasma marginale strains also reported in cattle. Vet. Parasitol. 2014, 205:730-734.
40. Silva J.B., Fonseca A.H., Barbosa J.D., Cabezas-Cruz A., de la Fuente J. Low genetic diversity associated with low prevalence of Anaplasma marginale in water buffaloes in Marajó Island, Brazil. Ticks Tick Borne Dis. 2014, 5:801-804.
41. Silvestre B.T., Rabelo É.M., Versiani A.F., da Fonseca F.G., Silveira J.A., Bueno L.L., Fujiwara R.T., Ribeiro M.F. Evaluation of humoral and cellular immune response of BALB/c mice immunized with a recombinant fragment of MSP1a from Anaplasma marginale using carbon nanotubes as a carrier molecule. Vaccine 2014, 32:2160-2166.
42. Smith D.J., Lapedes A.S., de Jong J.C., Bestebroer T.M., Rimmelzwaan G.F., Osterhaus A.D., Fouchier R.A. Mapping the antigenic and genetic evolution of influenza virus. Science 2004, 305:371-376.
43. Smith N.H., Kremer K., Inwald J., Dale J., Driscoll J.R., Gordon S.V., van Soolingen D., Hewinson R.G., Smith J.M. Ecotypes of the Mycobacterium tuberculosis complex. J. Theor. Biol. 2006, 239:220-225.
44. Stackebrandt E., Goebel B.M. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 1994, 44:846-849.
45. Stackebrandt E., Frederiksen W., Garrity G.M., Grimont P.A., Kämpfer P., Maiden M.C., Nesme X., Rosselló-Mora R., Swings J., Trüper H.G., Vauterin L., Ward A.C., Whitman W.B. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 2002, 52:1043-1047.
46. Stackebrandt E., Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol. Today 2006, 33:152-155.
47. Sumner J.W., Nicholson W.L., Massung R.F. PCR amplification and comparison of nucleotide sequences from the groESL heat shock operon of Ehrlichia species. J. Clin. Microbiol. 1997, 35:2087-2092.
48. Torina A., Moreno-Cid J.A., Blanda V., Fernández de Mera I.G., de la Lastra J.M., Scimeca S., Blanda M., Scariano M.E., Briganò S., Disclafani R., Piazza A., Vicente J., Gortázar C., Caracappa S., Lelli R.C., de la Fuente J. Control of tick infestations and pathogen prevalence in cattle and sheep farms vaccinated with the recombinant subolesin-major surface protein 1a chimeric antigen. Parasites Vectors 2014, 7:10.
49. Wen B., Jian R., Zhang Y., Chen R. Simultaneous detection of Anaplasma marginale and a new Ehrlichia species closely related to Ehrlichia chaffeensis by sequence analyses of 16S ribosomal DNA in Boophilus microplus ticks from Tibet. J. Clin. Microbiol. 2002, 40:3286-3290.
50. Woese C.R. Bacterial evolution. Microbiol. Rev. 1987, 51:221-271.
51. Woo P.C., Lau S.K., Teng J.L., Tse H., Yuen K.Y. Then and now: use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology laboratories. Clin. Microbiol. Infect. 2008, 14:908-934.
52. Yu X.J., Zhang X.F., McBride J.W., Zhang Y., Walker D.H. Phylogenetic relationships of Anaplasma marginale and 'Ehrlichia platys' to other Ehrlichia species determined by GroEL aa sequences. Int. J. Syst. Evol. Microbiol. 2001, 51:1143-1146.
53. Zweygarth E., Cabezas-Cruz A., Josemans A.I., Oosthuizen M.C., Matjila P.T., Lis K., Broniszewska M., Schöl H., Ferrolho J., Grubhoffer L., Passos L.M.F. In vitro culture and structural differences in the major immunoreactive protein gp36 of geographically distant Ehrlichia canis isolates. Ticks Tick Borne Dis. 2014, 5:423-431.