Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T01:41:40.738Z Has data issue: false hasContentIssue false

Genetic diversity of Anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development

Published online by Cambridge University Press:  28 February 2007

José de la Fuente*
Affiliation:
Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078-2007, USA Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, Spain
Ala Lew
Affiliation:
Department of Primary Industries and Fisheries, Locked Mail Bag No. 4, Moorooka, 4105 qld, Australia
Hans Lutz
Affiliation:
Clinical Laboratory, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland
Marina L. Meli
Affiliation:
Clinical Laboratory, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland
Regina Hofmann-Lehmann
Affiliation:
Clinical Laboratory, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland
Varda Shkap
Affiliation:
Division of Parasitology, Kimron Veterinary Institute, P.O. Box 12, Bet Dagan, 50250, Israel
Thea Molad
Affiliation:
Division of Parasitology, Kimron Veterinary Institute, P.O. Box 12, Bet Dagan, 50250, Israel
Atilio J. Mangold
Affiliation:
Instituto Nacional de Tecnología Agropecuaria, Estación Experimental Agropecuaria Rafaela, CC 22, CP2300 Rafaela, Santa Fe, Argentina
Consuelo Almazán
Affiliation:
Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078-2007, USA
Victoria Naranjo
Affiliation:
Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, Spain
Christian Gortázar
Affiliation:
Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, Spain
Alessandra Torina
Affiliation:
Istituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Italy
Santo Caracappa
Affiliation:
Istituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Italy
Ana L. García-Pérez
Affiliation:
Departamento de Sanidad Animal, Instituto Vasco de Investigación y Desarrollo Agrario (NEIKER), Berreaga 1, 48160 Derio (Bizkaia), Spain
Marta Barral
Affiliation:
Departamento de Sanidad Animal, Instituto Vasco de Investigación y Desarrollo Agrario (NEIKER), Berreaga 1, 48160 Derio (Bizkaia), Spain
Beatriz Oporto
Affiliation:
Departamento de Sanidad Animal, Instituto Vasco de Investigación y Desarrollo Agrario (NEIKER), Berreaga 1, 48160 Derio (Bizkaia), Spain
Luigi Ceci
Affiliation:
Dipartimento di Sanità e Benessere degli Animali, Sezione di Clinica Medica, Facoltà di Medicina Veterinaria, Università degli studi di Bari, Strada per Casamassima km 3, Valenzano (Ba), Italy
Grazia Carelli
Affiliation:
Dipartimento di Sanità e Benessere degli Animali, Sezione di Clinica Medica, Facoltà di Medicina Veterinaria, Università degli studi di Bari, Strada per Casamassima km 3, Valenzano (Ba), Italy
Edmour F. Blouin
Affiliation:
Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078-2007, USA
Katherine M. Kocan
Affiliation:
Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078-2007, USA

Abstract

The genus Anaplasma (Rickettsiales: Anaplasmataceae) includes several pathogens of veterinary and human medical importance. An understanding of the diversity of Anaplasma major surface proteins (MSPs), including those MSPs that modulate infection, development of persistent infections, and transmission of pathogens by ticks, is derived in part, by characterization and phylogenetic analyses of geographic strains. Information concerning the genetic diversity of Anaplasma spp. MSPs will likely influence the development of serodiagnostic assays and vaccine strategies for the control of anaplasmosis.

Type
Research Article
Copyright
Copyright © CAB International 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, JR, Palmer, GH, Howard, CJ, Hope, JC and Brown, WC (2004). Anaplasma marginale major surface protein 2 CD4+-T-cell epitopes are evenly distributed in conserved and hypervariable regions (HVR), whereas linear B-cell epitopes are predominantly located in the HVR. Infection and Immunity 72: 73607366.CrossRefGoogle ScholarPubMed
Allred, DR, McGuire, TC, Palmer, GH, Leib, SR, Harkins, TM, McElwain, TF and Barbet, AF (1990). Molecular basis for surface antigen size polymorphisms and conservation of a neutralization-sensitive epitope in Anaplasma marginale. Proceedings of the National Academy of Sciences of the United States of America 87: 32203224.CrossRefGoogle ScholarPubMed
Arulkanthan, A, Brown, WC, McGuire, C and Knowles, DP (1999). Biased immunoglobulin G1 isotype responses induced in cattle with DNA expressing msp 1a of Anaplasma marginale. Infection and Immunity 67: 34813487.CrossRefGoogle Scholar
Barbet, AF, Palmer, GH, Myler, PJ and McGuire, TC (1987). Characterization of an immunoprotective protein complex of Anaplasma marginale by cloning and expression of the gene coding for polypeptide Am105L. Infection and Immunity 55: 24282435.CrossRefGoogle ScholarPubMed
Barigye, R, Garcia-Ortiz, MA, Rojas Ramirez, EE and Rodriguez, SD (2004). Identification of IgG2-specific antigens in Mexican Anaplasma marginale strains. Annals of the New York Academy of Sciences 1026: 8494.CrossRefGoogle ScholarPubMed
Blouin, EF de la Fuente, J, Garcia-Garcia, JC, Sauer, JR, Saliki, JT and Kocan, KM (2002). Applications of a cell culture system for studying the interaction of Anaplasma marginale with tick cells. Animal Health Research Reviews 3: 5768.CrossRefGoogle ScholarPubMed
Blouin, EF, Saliki, JT de la Fuente, J, Garcia-Garcia, JC and Kocan, KM (2003). Antibodies to Anaplasma marginale major surface proteins 1a and 1b inhibit infectivity for cultured tick cells. Veterinary Parasitology 111: 247260.CrossRefGoogle ScholarPubMed
Bock, RE de Vos, AJ, Kingston, TG and Carter, PD (2003). Assessment of a low virulence Australian isolate of Anaplasma marginale for pathogenicity, immunogenicity and transmissability by Boophilus microplus. Veterinary Parasitology 118: 121131.CrossRefGoogle ScholarPubMed
Bowie, JV, de la Fuente, J, Kocan, KM, Blouin, EF and Barbet, AF (2002). Conservation of major surface protein 1 genes of the ehrlichial pathogen Anaplasma marginale during cyclic transmission between ticks and cattle. Gene 282: 95102.CrossRefGoogle Scholar
Brayton, KA, Palmer, GH, Lundgren, A, Yi, J and Barbet, AF (2002). Antigenic variation of Anaplasma marginale msp2 occurs by combinatorial gene conversion. Molecular Microbiology 43: 11511159.CrossRefGoogle ScholarPubMed
Brayton, KA, Kappmeyer, LS, Herndon, DR, Dark, MJ, Tibbals, DL, Palmer, GH, McGuire, TC, Knowles, DP Jr (2005). Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proceedings of the National Academy of Sciences of the United States of America PNAS 102: 844849.CrossRefGoogle ScholarPubMed
Brown, WC, Shkap, V, Zhu, D, McGuire, TC, Tuo, W, McElwain, TF and Palmer, GH (1998a). CD4 + T-lymphocyte and immunoglobulin G2 responses in calves immunized with Anaplasma marginale outer membranes and protected against homologous challenge. Infection and Immunity 66: 54065413.CrossRefGoogle ScholarPubMed
Brown, WC, Zhu, D, Shkap, V, McGuire, TC, Blouin, ED, Kocan, KM and Palmer, GH (1998b). The repertoire of Anaplasma marginale antigens recognized by CD4 + T-lymphocyte clones from protectively immunized cattle is diverse and includes major surface protein 2 (MSP-2) and MSP-3. Infection and Immunity 66: 54145422.CrossRefGoogle ScholarPubMed
Brown, WC, McGuire, TC, Zhu, D, Lewin, HA, Sosnow, J and Palmer, GH (2001a). Highly conserved regions of the immunodominant major surface protein 2 of the genogroup II Ehrlichial pathogen Anaplasma marginale are rich in naturally derived CD4 + T lymphocyte epitopes that elicit strong recall responses. Journal of Immunology 166: 11141124.CrossRefGoogle Scholar
Brown, WC, Palmer, GH, Lewin, HA and McGuire, TC (2001b). CD4 + T lymphocytes from calves immunzied with Anaplasma marginale major surface protein 1 (MSP1), a heteromeric complex of MSP1a and MSP1b, preferentially recognize the MSP1a carboxyl terminus that is conserved among strains. Infection and Immunity 69: 68536862.CrossRefGoogle Scholar
Brown, WC, McGuire, TC, Mwangi, W, Kegerreis, KA, Macmillan, H, Lewin, HA and Palmer, GH (2002). Major histocompatibility complex class II DR-restricted memory CD4(+) T lymphocytes recognize conserved immunodominant epitopes of Anaplasma marginale major surface protein 1a. Infection and Immunity 70: 55215532.CrossRefGoogle ScholarPubMed
Brown, WC, Brayton, KA, Styer, CM and Palmer, GH (2003). The hypervariable region of Anaplasma marginale major surface protein 2 (MSP2) contains multiple immunodominant CD4+ T lymphocyte epitopes that elicit variant-specific proliferative and IFN-gamma responses in MSP2 vaccinates. Journal of Immunology 170: 37903798.CrossRefGoogle ScholarPubMed
Brown, WC, Palmer, GH, Brayton, KA, Meeus, PF, Barbet, AF, Kegerreis, KA and McGuire, TC (2004). CD4+ T lymphocytes from Anaplasma marginale major surface protein 2 (MSP2) vaccinees recognize naturally processed epitopes conserved in MSP3. Infection and Immunity 72: 36883692.CrossRefGoogle ScholarPubMed
Camacho-Nuez, J, De Lourdes, M, Suarez, CE, McGuire, TC, Brown, WC and Palmer, GH (2000). Expression of polymorphic msp1β genes during acute Anaplasma marginale rickettsemia. Infection and Immunity 68: 19461952.CrossRefGoogle ScholarPubMed
Carlyon, JA and Fikrig, E (2003). Invasion and survival strategies of Anaplasma phagocytophilum. Cellular Microbiology 5: 743754.CrossRefGoogle ScholarPubMed
Daniels, TJ, Battaly, GR, Liveris, D, Falco, RC and Schwartz, I (2002). Avian reservoirs of the agent of human granulocytic ehrlichiosis. Emerging Infectious Diseases 8: 15241525.CrossRefGoogle ScholarPubMed
de la Fuente, J and Kocan, KM (2001). Expression of Anaplasma marginale major surface protein 2 variants in persistently infected ticks. Infection and Immunity 69: 51515156.CrossRefGoogle ScholarPubMed
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF, Rodríguez, SD, García, MA and Kocan, KM (2001a). Evolution and function of tandem repeats in the major surface protein 1a of the ehrlichial pathogen Anaplasma marginale. Animal Health Research Reviews 2: 163173.CrossRefGoogle ScholarPubMed
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF and Kocan, KM (2001b). Differential adhesion of major surface proteins 1a and 1b of the ehrlichial cattle pathogen Anaplasma marginale to bovine erythrocytes and tick cells. International Journal of Parasitology 31: 145153.CrossRefGoogle ScholarPubMed
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF and Kocan, KM (2001c). Major surface protein 1a effects tick infection and transmission of the ehrlichial pathogen Anaplasma marginale. International Journal of Parasitology 31: 17051714.CrossRefGoogle Scholar
de la Fuente, J, Van Den Bussche, RA and Kocan, KM (2001d). Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Veterinary Parasitology 97: 6576.CrossRefGoogle ScholarPubMed
de la Fuente, J, Van Den Bussche, RA, Garcia-Garcia, JC, Rodríguez, SD, García, MA, Guglielmone, AA, Mangold, AJ, Passos, LM, Blouin, EF and Kocan, KM (2002). Phylogeography of New World isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae) based on major surface protein sequences. Veterinary Microbiology 88: 275285.CrossRefGoogle Scholar
de la Fuente, J, Van Den Bussche, RA, Prado, T and Kocan, KM (2003a). Anaplasma marginale major surface protein 1a genotypes evolved under positive selection pressure but are not a marker for geographic isolates. Journal of Clinical Microbiology 41: 16091616.CrossRefGoogle Scholar
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF and Kocan, KM (2003b). Characterization of the functional domain of major surface protein 1a involved in adhesion of the rickettsia Anaplasma marginale to host cells. Veterinary Microbiology 91: 265283.CrossRefGoogle ScholarPubMed
de la Fuente, J, Kocan, KM, Garcia-Garcia, JC, Blouin, EF, Halbur, T and Onet, V (2003c). Immunization against Anaplasma marginale major surface protein 1a reduces infectivity for ticks. The International Journal of Applied Research in Veterinary Medicine 1: 285292.Google Scholar
de la Fuente, J, Golsteyn Thomas, EJ, Van Den Bussche, RA, Hamilton, RG, Tanaka, EE, Druhan, SE and Kocan, KM (2003d). Characterization of Anaplasma marginale isolated from North American bison. Applied and Environmental Microbiology 69: 50015005.CrossRefGoogle ScholarPubMed
de la Fuente, J, Naranjo, V, Ruiz-Fons, F, Vicente, J, Estrada-Peña, A, Almazán, C, Kocan, KM, Martín, MP, Gortázar, C (2004a). Prevalence of tick-borne pathogens in ixodid ticks (Acari: Ixodidae) collected from European wild boar (Sus scrofa) and Iberian red deer (Cervus elaphus hispanicus) in central Spain. European Journal of Wildlife Research 50: 187196.CrossRefGoogle Scholar
de la Fuente, J, Vicente, J, Höfle, U, Ruiz-Fons, F, Fernández de Mera, IG, Van Den Bussche, RA, Kocan, KM and Gortazar, C (2004b). Anaplasma infection in free-ranging Iberian red deer in the region of Castilla-La Mancha, Spain. Veterinary Microbiology 100: 163173.CrossRefGoogle Scholar
de la Fuente, J, Passos, LMF, Van Den Bussche, RA, Ribeiro, MFB, Facury-Filho, EJ and Kocan, KM (2004c). Genetic diversity and molecular phylogeny of Anaplasma marginale isolates from Minas Gerais, Brazil. Veterinary Parasitology 121: 307316.CrossRefGoogle ScholarPubMed
de la Fuente, J, Massung, RF, Wong, SJ, Chu, FK, Lutz, H, Meli, M von Loewenich, FD, Grzeszczuk, A, Torina, A, Caracappa, S, Mangold, AJ, Naranjo, V, Stuen, S and Kocan, KM (2005a). Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. Journal of Clinical Microbiology 43: 13091317.CrossRefGoogle ScholarPubMed
de la Fuente, J, Torina, A, Caracappa, S, Tumino, G, Furlá, R, Almazán, C and Kocan, KM (2005b). Serologic and molecular characterization of Anaplasma species infection in farm animals and ticks from Sicily Veterinary Parasitology: in press.CrossRefGoogle ScholarPubMed
Dreher, UM, de la Fuente, J, Hofmann-Lehmann, R, Meli, ML, Pusterla, N, Kocan, KM, Woldehiwet, Z, Regula, G, Staerk, KDC and Lutz, H (2005). Serologic cross reactivity between Anaplasma marginale and Anaplasma phagocytophilum Journal of Clinical Microbiology: submitted for publication.Google ScholarPubMed
Dumler, JS, Barbet, AF, Bekker, CPJ, Dasch, GA, Palmer, GH, Ray, SC, Rikihisa, Y and Rurangirwa, FR (2001). Reorganization of the 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. International Journal of Systematic Evolutionary Microbiology 51: 21452165.CrossRefGoogle ScholarPubMed
French, DM, McElwain, TF, McGuire, TC and Palmer, GH (1998). Expression of Anaplasma marginale major surface protein 2 variants during persistent cyclic rickettsemia [published erratum appears in Infection and Immunity (1998) 66: 2400]. Infection and Immunity 66: 12001207.CrossRefGoogle Scholar
French, DM, Brown, WC and Palmer, GH (1999). Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infection and Immunity 67: 58345840.CrossRefGoogle ScholarPubMed
Garcia-Garcia, JC, de la Fuente, J, Bell, G, Blouin, EF and Kocan, KM (2004a). Glycosylation of Anaplasma marginale major surface protein 1a its putative role in adhesion to tick cells. Infection and Immunity 72: 30223030.CrossRefGoogle ScholarPubMed
Garcia-Garcia, JC, de la Fuente, J, Kocan, KM, Blouin, EF, Halbur, T, Onet, VC and Saliki, JT (2004b). 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. Veterinary Immunology and Immunopathology 98: 137151.CrossRefGoogle ScholarPubMed
Garcia-Garcia, JC, de la Fuente, J, Blouin, EF, Halbur, T, Onet, VC, Saliki, JT and Kocan, KM (2004c). Differential expression of the msp1 α gene of Anaplasma marginale occurs in bovine erythrocytes and tick cells. Veterinary Microbiology 98: 261272.CrossRefGoogle Scholar
Goethert, HK, Telford, SR III (2003). Enzootic transmission of Babesia divergens among cottontail rabbits on Nantucket Island, Massachusetts. American Journal of Tropical Medicine and Hygiene 69: 455460.CrossRefGoogle ScholarPubMed
Hofmann-Lehmann, R, Meli, ML, Dreher, UM Gönczi E Deplazes, P, Braun, U, Engels, M Schüpbach J Jörger K Thoma, R, Griot, C Stärk K Willi, B, Schmidt, J, Kocan, KM and Lutz, H (2004). Concurrent infections with vector-borne pathogens as etiology of fatal hemolytic anemia in a cattle herd from Switzerland. Journal of Clinical Microbiology 42: 37753780.CrossRefGoogle Scholar
Hope, M, Riding, G, Menzies, M and Willadsen, P (2004). A novel antigen from Anaplasma marginale: characterization, expression and preliminary evaluation of the recombinant protein. Vaccine 22: 407415.CrossRefGoogle ScholarPubMed
Kieser, ST, Eriks, IE and Palmer, GH (1990). Cyclic rickettsemia during persistent Anaplasma marginale infection in cattle. Infection and Immunity 58: 11171119.CrossRefGoogle Scholar
Knowles, D, Torioni, S, Palmer, G, McGuire, T, Stiller, D and McElwain, T (1996). Antibody against an Anaplasma marginale MSP5 epitope common to tick and erythrocyte stages identifies persistently infected cattle. Journal of Clinical Microbiology 34: 22252230.CrossRefGoogle ScholarPubMed
Kocan, KM, Stiller, D, Goff, WL, Claypool, PL, Edwards, W, Ewing, SA, McGuire, TC, Hair, JA and Barron, SJ (1992a). Development of Anaplasma marginale in male Dermacentor andersoni transferred from infected to susceptible cattle. American Journal of Veterinary Research 53: 499507.CrossRefGoogle ScholarPubMed
Kocan, KM, Goff, WL, Stiller, D, Claypool, PL, Edwards, W, Ewing, SA, Hair, JA and Barron, SJ (1992b). Persistence of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) transferred successively from infected to susceptible cattle. Journal of Medical Entomology 29: 657668.CrossRefGoogle Scholar
Kocan, KM, de la Fuente, J, Guglielmone, AA, Meléndez, RD (2003). Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clinical Microbiology Reviews 16: 698712.CrossRefGoogle ScholarPubMed
Kocan, K, de la Fuente, J, Blouin, EF and Garcia-Garcia, JC (2004). Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host–pathogen adaptations of a tick-borne rickettsia Parasitolology 129 S285S300.CrossRefGoogle ScholarPubMed
Lahmers, KK, Norimine, J, Abrahamsen, MS, Palmer, GH and Brown, WC (2005). The CD4+ T cell immunodominant Anaplasma marginale major surface protein 2 stimulates {gamma}{delta} T cell clones that express unique T cell receptors. Journal of Leukocyte Biology 77: 110.Google ScholarPubMed
Lappin, MR, Breitschwerdt, EB, Jensen, WA, Dunnigan, B, Rha, JY, Williams, CR, Brewer, M and Fall, M (2004). Molecular and serologic evidence of Anaplasma phagocytophilum infection in cats in North America. Journal of the American Veterinary Medical Association 225: 893896.CrossRefGoogle ScholarPubMed
Levin, ML, Nicholson, WL, Massung, RF, Sumner, JW and Fish, D (2002). Comparison of the reservoir competence of medium-sized mammals and Peromyscus leucopus for Anaplasma phagocytophilum in Connecticut. Vector Borne Zoonotic Diseases 2: 125136.CrossRefGoogle ScholarPubMed
Lew, AE, Bock, RE, Minchin, CM and Masaka, S (2002). A msp1 α polymerase chain reaction assay for specific detection and differentiation of Anaplasma marginale isolates. Veterinary Microbiology 86: 325335.CrossRefGoogle Scholar
Lin, Q, Rikihisa, Y, Felek, S, Wang, X, Massung, RF and Woldehiwet, Z (2004). Anaplasma phagocytophilum has a functional msp2 gene that is distinct from p44. Infection and Immunity 72: 38833889.CrossRefGoogle Scholar
Magnarelli, LA IJdo, JW, Ramakrishnan, U, Henderson, DW, Stafford, KC III Fikrig, E (2004). Use of recombinant antigens of Borrelia burgdorferi and Anaplasma phagocytophilum in enzyme-linked immunosorbent assays to detect antibodies in white-tailed deer. Journal of Wildlife Diseases 40: 249258.CrossRefGoogle ScholarPubMed
Massung, RF and Slater, KG (2003). Comparison of PCR assays for detection of the agent of human granulocytic ehrlichiosis, Anaplasma phagocytophilum. Journal of Clinical Microbiology 41: 717722.CrossRefGoogle ScholarPubMed
McGarey, DJ and Allred, DR (1994). Characterization of hemagglutinating components on the Anaplasma marginale initial body surface and identification of possible adhesins. Infection and Immunity 62: 45874593.CrossRefGoogle ScholarPubMed
McGarey, DJ, Barbet, AF, Palmer, GH, McGuire, TC and Allred, DR (1994). Putative adhesins of Anaplasma marginale: major surface polypeptides 1a and 1b. Infection and Immunity 62: 45944601.CrossRefGoogle ScholarPubMed
McGuire, TC, Stephens, EB, Palmer, GH, McElwain, TF, Leichtensteiger, CA, Leib, SR and Barbet, AF (1994). Recombinant vaccinia virus expression of Anaplasma marginale surface protein MSP-1a: effect of promoters, leader sequences and GPI anchor sequence on antibody response. Vaccine 12: 465471.CrossRefGoogle ScholarPubMed
Molad, T, Brayton, KA, Palmer, GH, Michaeli, S and Shkap, V (2004). Molecular conservation of MSP4 and MSP5 in Anaplasma marginale and A. centrale vaccine strain. Veterinary Microbiology 100: 5564.CrossRefGoogle ScholarPubMed
Molloy, JB, Bock, RE, Templeton, JM, Bruyeres, AG, Bowles, PM, Blight, GW and Jorgensen, WK (2001). Identification of antigenic differences that discriminate between cattle vaccinated with Anaplasma centrale and cattle naturally infected with Anaplasma marginale. International Journal of Parasitology 31: 179186.CrossRefGoogle ScholarPubMed
Morzaria, SP, Katende, J, Musoke, A, Nene, V, Skilton, R and Bishop, R (1999). Development of sero-diagnostic and molecular tools for the control of important tick-borne pathogens of cattle in Africa. Parasitologia 41(Supplement 1): 7380.Google ScholarPubMed
Munodzana, D, McElwain, TF, Knowles, DP and Palmer, GH (1998). Conformational dependence of Anaplasma marginale major surface protein 5 surface-exposed B-cell epitopes. Infection and Immunity 66: 26192624.CrossRefGoogle ScholarPubMed
Ndung'u, LWAguirre, C, Rurangirwa, FR, McElwain, TF, McGuire, TC, Knowles, DP and Palmer, GH (1995). Detection of Anaplasma ovis infection in goats by major surface protein 5 competitive inhibition enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 33: 675679.CrossRefGoogle ScholarPubMed
Palmer, GH (1989). Anaplasma vaccines. In: Wright, IG (ed.) Veterinary Protozoan and Hemoparasite Vaccines. Boca Raton, FL: CRC Press, pp. 229.Google Scholar
Palmer, GH, Kocan, KM, Barron, SJ, Hair, JA, Barbet, AF, Davis, WC and McGuire, TC (1985). Presence of common antigens, including major surface protein epitopes, between the cattle (intraerythrocytic) and tick stages of Anaplasma marginale. Infection and Immunity 50: 881886.CrossRefGoogle ScholarPubMed
Palmer, GH, Waghela, SD, Barbet, AF, Davis, WC and McGuire, TC (1987). Characterization of a neutralization sensitive epitope on the AM 105 surface protein of Anaplasma marginale. Journal of Parasitology 17: 12791285.Google Scholar
Palmer, GH, Abbott, JR, French, DM and McElwain, TF (1998). Persistence of Anaplasma ovis infection and conservation of the msp-2 and msp-3 multigene families within the genus Anaplasma. Infection and Immunity 66: 60356039.CrossRefGoogle ScholarPubMed
Palmer, GH, Rurangirwa, FR, Kocan, KM and Brown, WC (1999). Molecular basis for vaccine development against the ehrlichial pathogen Anaplasma marginale. Parasitology Today 15: 253300.CrossRefGoogle ScholarPubMed
Palmer, GH, Rurangirwa, FR and McElwain, TF (2001). Strain composition of the ehrlichia Anaplasma marginale within persistently infected cattle, a mammalian reservoir for tick transmission. Journal of Clinical Microbiology 39: 631635.CrossRefGoogle ScholarPubMed
Palmer, GH, Knowles, DP, Jr Rodriguez, JL, Gnad, DP, Hollis, LC, Marston, T and Brayton, KA (2004). Stochastic transmission of multiple genotypically distinct Anaplasma marginale strains in a herd with high prevalence of Anaplasma infection. Journal of Clinical Microbiology 42: 53815384.CrossRefGoogle Scholar
Parola, P (2004). Tick-borne rickettsial diseases: emerging risks in Europe. Comparative Immunology, Microbiology and Infectious Diseases 27: 297304.CrossRefGoogle ScholarPubMed
Petrovec, M, Bidovec, A, Sumner, JW, Nicholson, WL, Childs, JE and Avsic Zupanc, T (2002). Infection with Anaplasma phagocytophila in cervids from Slovenia: evidence of two genotypic lineages. Wiener Klinische Wochenschrift 114: 641647.Google ScholarPubMed
Polin, H, Hufnagl, P, Haunschmid, R, Gruber, F and Ladurner, G (2004). Molecular evidence of Anaplasma phagocytophilum in Ixodes ricinus ticks and wild animals in Austria. Journal of Clinical Microbiology 42: 22852286.CrossRefGoogle ScholarPubMed
Riding, G, Hope, M, Waltisbuhl, D and Willadsen, P (2003). Identification of novel protective antigens from Anaplasma marginale. Vaccine 21: 18741883.CrossRefGoogle ScholarPubMed
Rikihisa, Y, Zhang, C and Christensen, BM (2003). Molecular characterization of Aegyptianella pullorum (Rickettsiales, Anaplasmataceae). Journal of Clinical Microbiology 41: 52945297.CrossRefGoogle ScholarPubMed
Shkap, V, Pipano, E, McGuire, TC and Palmer, GH (1991). Identification of immunodominant polypeptides common between Anaplasma centrale and Anaplasma marginale. Veterinary Immunology and Immunopathology 29: 3140.CrossRefGoogle ScholarPubMed
Shkap, V, Molad, T, Brayton, KA, Brown, WC and Palmer, GH (2002a). Expression of major surface protein 2 variants with conserved T-cell epitopes in Anaplasma centrale vaccinates. Infection and Immunity 70: 642648.CrossRefGoogle ScholarPubMed
Shkap, V, Molad, T, Fish, L and Palmer, GH (2002b). Detection of the Anaplasma centrale vaccine strain and specific differentiation from Anaplasma marginale in vaccinated and infected cattle. Parasitology Research 88: 546552.CrossRefGoogle ScholarPubMed
Tebele, N, McGuire, TC and Palmer, GH (1991). Induction of protective immunity by using Anaplasma marginale initial body membranes. Infection and Immunity 59: 31993204.CrossRefGoogle ScholarPubMed
Telford, III SR Dawson, JE, Katavolos, P, Warner, CK, Kolbert, CP and Persing, DH (1996). Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick–rodent cycle. Proceedings of the National Academy of Sciences of the United States of America 93: 62096214.CrossRefGoogle Scholar
Theiler, A (1911). Further investigations into anaplasmosis of South African cattle. 1st Report of the Director of Veterinary Research, Department of Agriculture of the Union of South Africa pp. 746.Google Scholar
Valdez, RA, McGuire, TC, Brown, WC, Davis, WC, Jordan, JM and Knowles, DP (2002). Selective in vivo depletion of CD4 + T lymphocytes with anti-CD4 monoclonal antibody during acute infection of calves with Anaplasma marginale. Clinical and Diagnostic Laboratory Immunology 9: 417424.Google ScholarPubMed
Viseshakul, N, Kamper, S, Bowie, MV and Barbet, AF (2000). Sequence and expression analysis of a surface antigen gene family of the rickettsia Anaplasma marginale. Gene 253: 4553.CrossRefGoogle ScholarPubMed
Visser, ES, McGuire, TC, Palmer, GH, Davis, WC, Shkap, V, Pipano, E, Knowles, DP Jr (1992). The Anaplasma marginale msp5 gene encodes a 19-kilodalton protein conserved in all recognized Anaplasma species. Infection and Immunity 60: 51395144.CrossRefGoogle ScholarPubMed