Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T12:33:28.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host–pathogen adaptations of a tick-borne rickettsia

Published online by Cambridge University Press:  19 April 2005

K. M. KOCAN ,
J. DE LA FUENTE ,
E. F. BLOUIN  and
J. C. GARCIA-GARCIA
K. M. KOCAN
Affiliation:
Department of Veterinary Pathobiology, 250 McElroy Hall, Oklahoma State University, Stillwater, OK 74078-2007, USA
J. DE LA FUENTE
Affiliation:
Department of Veterinary Pathobiology, 250 McElroy Hall, Oklahoma State University, Stillwater, OK 74078-2007, USA
E. F. BLOUIN
Affiliation:
Department of Veterinary Pathobiology, 250 McElroy Hall, Oklahoma State University, Stillwater, OK 74078-2007, USA
J. C. GARCIA-GARCIA
Affiliation:
Department of Veterinary Pathobiology, 250 McElroy Hall, Oklahoma State University, Stillwater, OK 74078-2007, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

The tick-borne intracellular pathogen Anaplasma marginale (Rickettsiales: Anaplasmataceae) develops persistent infections in cattle and tick hosts. While erythrocytes appear to be the only site of infection in cattle, A. marginale undergoes a complex developmental cycle in ticks and transmission occurs via salivary glands during feeding. Many geographic isolates occur that vary in genotype, antigenic composition, morphology and infectivity for ticks. In this chapter we review recent research on the host–vector–pathogen interactions of A. marginale. Major surface proteins (MSPs) play a crucial role in the interaction of A. marginale with host cells. The MSP1a protein, which is an adhesin for bovine erythrocytes and tick cells, is differentially regulated and affects infection and transmission of A. marginale by Dermacentor spp. ticks. MSP2 undergoes antigenic variation and selection in cattle and ticks, and contributes to the maintenance of persistent infections. Phylogenetic studies of A. marginale geographic isolates using msp4 and msp1α provide information about the biogeography and evolution of A. marginale: msp1α genotypes evolve under positive selection pressure. Isolates of A. marginale are maintained by independent transmission events and a mechanism of infection exclusion in cattle and ticks allows for only the infection of one isolate per animal. Prospects for development of control strategies by use of pathogen and tick-derived antigens are discussed. The A. marginale/vector/host studies described herein could serve as a model for research on other tick-borne rickettsiae.

Keywords

Anaplasma marginaleticksrickettsiaanaplasmosis
Type
Research Article
Information
Parasitology , Volume 129 , Issue S1 , October 2004 , pp. S285 - S300
Copyright
© 2004 Cambridge University Press

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

REFERENCES

ALLRED, D. R., McGUIRE, T. C., PALMER, G. H., LEIB, S. R., HARKINS, T. M., McELWAIN, T. F. & BARBET, A. F. ( 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, USA 87, 3220–3224.CrossRefGoogle Scholar
ANTHONY, D. W. & ROBY, T. O. ( 1962). Anaplasmosis transmission studies with Dermacentor variabilis (Say) and Dermacentor andersoni (Stiles) (=D. venustus Marx) as experimental vectors. In Proceedings of the 4th National Anaplasmosis Research Conference, pp. 78–81. Reno, Nevada.
ANTHONY, D. W. & ROBY, T. O. ( 1966). The experimental transmission of bovine anaplasmosis by three species of North American ticks. American Journal of Veterinary Research 27, 191–198.Google Scholar
BARBET, A. F., BLENTLINGER, R., JOOYOUNG YI, LUNDGREN, A. M., BLOUIN, E. F. & KOCAN, K. M. ( 1999). Comparison of surface proteins of Anaplasma marginale grown in tick cell culture, tick salivary glands, and cattle. Infection and Immunity 67, 102–107.Google Scholar
BARBET, A. F., JOOYOUNG YI, LUNDGREN, A., McEWEN, B. R., BLOUIN, E. F. & KOCAN, K. M. ( 2001). Antigenic variation of Anaplasma marginale: Major surface protein 2 diversity during cyclic transmission between ticks and cattle. Infection and Immunity 69, 3057–3066.CrossRefGoogle Scholar
BARBET, A. F., LUNDGREN, A., JOOYOUNG YI, RURANGIRWA, F. R. & PALMER, G. H. ( 2000). Antigenic variation of Anaplasma marginale by expression of MSP2 mosaics. Infection and Immunity 68, 6133–6138.CrossRefGoogle Scholar
BARBET, A. F., PALMER, G. H., MYLER, P. J. & McGUIRE, T. C. ( 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, 2428–2435.Google Scholar
BELL-SAKYI, L. M., PAXTON, E. A., MUNDERLOH, U. G. & SUMPTION, K. J. ( 2000). Growth of Cowdria ruminantium, the causative agent of heartwater, in a tick cell line. Journal of Clinical Microbiology 38, 1238–1240.Google Scholar
BLOUIN, E. F., BARBET, A. F., JOOYOUNG YI, KOCAN, K. M. & SALIKI, J. T. ( 1999). Establishment and characterization of an Oklahoma isolate of Anaplasma marginale in cultured Ixodes scapularis cells. Veterinary Parasitology 87, 301–313.Google Scholar
BLOUIN, E. F., DE LA FUENTE, J., GARCIA-GARCIA, J. C., SAUER, J. R., SALIKI, J. T. & KOCAN, K. M. ( 2002 a). Applications of a cell culture system for studying the interaction of Anaplasma marginale with tick cells. Animal Health Research Reviews 3, 57–68.Google Scholar
BLOUIN, E. F. & KOCAN, K. M. ( 1998). Morphology and development of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in cultured Ixodes scapularis (Acari: Ixodidae) cells. Journal of Medical Entomology 35, 788–797.CrossRefGoogle Scholar
BLOUIN, E. F., KOCAN, K. M., DE LA FUENTE, J. & SALIKI, J. T. ( 2002 b). Effect of tetracycline on development of Anaplasma marginale in cultured Ixodes scapularis cells. Veterinary Parasitology 107, 115–126.Google Scholar
BLOUIN, E. F., SALIKI, J. T., DE LA FUENTE, J., GARCIA-GARCIA, J. C. & KOCAN, K. M. ( 2003). Antibodies to Anaplasma marginale Major Surface Protein 1a and 1b inhibit infectivity for cultured tick cells. Veterinary Parasitology 111, 247–260.CrossRefGoogle Scholar
BOCK, R. E. & DE VOS, A. J. ( 1999). Effect of cattle on innate resistance to infection with Anaplasma marginale transmitted by Boophilus microplus. Australian Veterinary Journal 77, 748–751.CrossRefGoogle Scholar
BOCK, R. E. & DE VOS, A. J. ( 2001). Immunity following use of Australian tick fever vaccine: a review of the evidence. Australian Veterinary Journal 79, 832–839.CrossRefGoogle Scholar
BOWIE, J. V., DE LA FUENTE, J., KOCAN, K. M., BLOUIN, E. F. & BARBET, A. F. ( 2002). Conservation of major surface protein 1 genes of the ehrlichial pathogen Anaplasma marginale during cyclic transmission between ticks and cattle. Gene 282, 95–102.Google Scholar
BOYNTON, W. H., HERMES, W. B., HOWELL, D. E. & WOODS, G. M. ( 1936). Anaplasmosis transmission by three species of ticks in California. Journal of the American Veterinary Medical Association 88, 500–502.Google Scholar
BRAM, R. A. ( 1975). Tick-borne livestock diseases and their vectors. 1. The global problem. World Animal Review 6, 1–5.Google Scholar
BRAYTON, K. A., KNOWLES, D. P., McGUIRE, T. C. & PALMER, G. H. ( 2001). Efficient use of a small genome to generate antigenic diversity in tick-borne ehrlichial pathogens. Proceedings of the National Academy of Sciences, USA 98, 4130–4135.CrossRefGoogle Scholar
BRAYTON, K. A., PALMER, G. H., LUNDGREN, A., JOOYOUNG YI & BARBET, A. F. ( 2002). Antigenic variation of Anaplasma marginale msp2 occurs by combinatorial gene conversion. Molecular Microbiology 43, 1151–1159.CrossRefGoogle Scholar
BROWN, W. C., PALMER, G. H., LEWIN, H. A. & McGUIRE, T. C. ( 2001). CD4(+) T lymphocytes from calves immunized 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, 6853–6862.CrossRefGoogle Scholar
BRUMPT, E. ( 1931). Transmission d'Anaplasma marginale par Rhipicephalus bursa et par margraopus. Annuals de Parasitologie 9, 4–9.Google Scholar
CAMACHO-NUEZ, J., DE LOURDES MUÑOZ, M., SUAREZ, C. E., McGUIRE, T. C., BROWN, W. C. & PALMER, G. H. ( 2000). Expression of polymorphic msp1β genes during acute Anaplasma marginale rickettsemia. Infection and Immunity 68, 1946–1952.CrossRefGoogle Scholar
CHRISTENSEN, J. F. & HOWARD, J. A. ( 1966). Anaplasmosis transmission by Dermacentor occidentalis taken from cattle in Santa Barbara County, CA. American Journal of Veterinary Research 27, 1473–1475.Google Scholar
DE LA FUENTE, J., BLOUIN, E. F. & KOCAN, K. M. ( 2003). Infection of ticks with the intracellular rickettsia Anaplasma marginale excludes infection with other genotypes. Clinical and Diagnostic Laboratory Immunology 10, 182–184.Google Scholar
DE LA FUENTE, J., GARCIA-GARCIA, J. C., BLOUIN, E. F. & KOCAN, K. M. ( 2001 a). Major surface protein 1a effects tick infection and transmission of the ehrlichial pathogen Anaplasma marginale. International Journal for Parasitology 31, 1705–1714.Google Scholar
DE LA FUENTE, J., GARCIA-GARCIA, J. C., BLOUIN, E. F. & KOCAN, K. M. ( 2001 b). Differential adhesion of major surface proteins 1a and 1b of the ehrlichial cattle pathogen Anaplasma marginale to bovine erythrocytes and tick cells. International Journal for Parasitology 31, 145–153.Google Scholar
DE LA FUENTE, J., GARCIA-GARCIA, J. C., BLOUIN, E. F. & KOCAN, K. M. ( 2003 a). Characterization of the functional domain of major surface protein 1a involved in adhesion of the rickettsia Anaplasma marginale to host cells. Veterinary Microbiology 91, 265–283.Google Scholar
DE LA FUENTE, J., GARCIA-GARCIA, J. C., BLOUIN, E. F., RODRIGUEZ, S. D., GARCIA, M. A. & KOCAN, K. M. ( 2001 c). Evolution and function of tandem repeats in the major surface protein 1a of the ehrlichial pathogen Anaplasma marginale. Animal Health Research Reviews 2, 163–173.Google Scholar
DE LA FUENTE, J., GARCIA-GARCIA, J. C., BLOUIN, E. F., SALIKI, J. T. & KOCAN, K. M. ( 2002 a). Infection of tick cells and bovine erythrocytes with one genotype of the intracellular ehrlichia Anaplasma marginale excludes infection with other genotypes. Diagnostic Laboratory Immunology 9, 658–668.Google Scholar
DE LA FUENTE, J., GOLSTEYN THOMAS, E. J., VAN DEN BUSSCHE, R. A., HAMILTON, R. G., TANAKA, E. E., DRUHAN, S. E. & KOCAN, K. M. ( 2003 b). Characterization of Anaplasma marginale isolated form North American bison. Applied and Environmental Microbiology 69, 5001–5005.Google Scholar
DE LA FUENTE, J. & KOCAN, K. M. ( 2001). Expression of Anaplasma marginale major surface protein 2 variants in persistently infected ticks. Infection and Immunity 69, 5151–5156.CrossRefGoogle Scholar
DE LA FUENTE, J. & KOCAN, K. M. ( 2003). Advances in the identification and characterization of protective antigens for development of recombinant vaccines against tick infestations. Expert Review of Vaccines 2, 583–593.CrossRefGoogle Scholar
DE LA FUENTE, J., KOCAN, K. M., GARCIA-GARCIA, J. C., BLOUIN, E. F., CLAYPOOL, P. L. & SALIKI, J. T. ( 2002 b). Vaccination of cattle with Anaplasma marginale derived from tick cell culture and bovine erythrocytes followed by challenge-exposure by infected ticks. Veterinary Microbiology 89, 239–251.Google Scholar
DE LA FUENTE, J., RODRIGUEZ, M., REDONDO, M., MONTERO, C., GARCIA-GARCIA, J. C., MENDEZ, L., SERRANO, E., VALDES, M., ENRIQUEZ, A., CANALES, M., RAMOS, E., BOUE, O., MACHADO, H., LLEONART, R., DE ARMAS, C. A., REY, S., RODRIGUEZ, J. L., ARTILES, M. & GARCIA, L. ( 1998). Field studies and cost-effectiveness analysis of vaccination with Gavac against the cattle tick Boophilus microplus. Vaccine 16, 366–373.Google Scholar
DE LA FUENTE, J., VAN DEN BUSSCHE, R. A., GARCIA-GARCIA, J. C., RODRÍGUEZ, S. D., GARCÍA, M. A., GUGLIELMONE, A. A., MANGOLD, A. J., PASSOS, L. M., BLOUIN, E. F. & KOCAN, K. M. ( 2002 c). Phylogeography of New World isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae) based on major surface protein sequences. Veterinary Microbiology 88, 275–285.Google Scholar
DE LA FUENTE, J., VAN DEN BUSSCHE, R. A. & KOCAN, K. M. ( 2001). Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Veterinary Parasitology 97, 65–76.CrossRefGoogle Scholar
DE LA FUENTE, J., VAN DEN BUSSCHE, R. A., PRADO, T. & KOCAN, K. M. ( 2003 c). Anaplasma marginale major surface protein 1α genotypes evolved under positive selection pressure but are not a marker for geographic isolates. Journal of Clinical Microbiology 41, 1609–1616.Google Scholar
DIKMANS, G. ( 1950). The transmission of anaplasmosis. American Journal of Veterinary Research 11, 5–16.Google Scholar
DUMLER, J. S., BARBET, A. F., BEKKER, C. P. J., DASCH, G. A., PALMER, G. H., RAY, S. C., RIKIHISA, Y. & RURANGIRWA, F. R. ( 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, 2145–2165.CrossRefGoogle Scholar
ERIKS, I. S., STILLER, D. & PALMER, G. H. ( 1993). Impact of persistent Anaplasma marginale rickettsemia on tick infection and transmission. Journal of Clinical Microbiology 31, 2091–2096.Google Scholar
EWING, S. A. ( 1981). Transmission of Anaplasma marginale by arthropods. In Proceedings of the 7th National Anaplasmosis Conference, pp. 395–423. Mississippi State University, MS, USA.
EWING, S. A., PANCIERA, R. J., KOCAN, K. M., GE, N. L., WELSH, R. D., OLSON, R. W., BARKER, R. & RICE, L. E. ( 1997). A winter outbreak of anaplasmosis in a non-endemic area of Oklahoma: a possible role for Dermacentor albipictus. Journal of Veterinary Diagnostic Investigation 9, 206–208.CrossRefGoogle Scholar
FRENCH, D. M., BROWN, W. C. & PALMER, G. H. ( 1999). Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infection and Immunity 67, 5834–5840.Google Scholar
FRENCH, D. M., McELWAIN, T. F., McGUIRE, T. C. & PALMER, G. H. ( 1998). Expression of Anaplasma marginale major surface protein 2 variants during persistent cyclic rickettsemia [published erratum appears in Infection and Immunity 1998, May, 66, 2400]. Infection and Immunity 66, 1200–1207.Google Scholar
GARCIA-GARCIA, J. C., DE LA FUENTE, J., BELL, G., BLOUIN, E. F. & KOCAN, K. M. ( 2002 a). Characterization of the glycosylation of Anaplasma marginale major surface proteins 1a and 1b. 83rd Conference of Research Workers in Animal Diseases, St. Louis, MO. Abstract 200.
GARCIA-GARCIA, J. C., DE LA FUENTE, J., BLOUIN, E. F., SALIKI, J. T. & KOCAN, K. M. ( 2002 b). Differential expression of major surface protein 1a by the cattle pathogen Anaplasma marginale in bovine erythrocytes and tick cells. In Proceedings of the 83rd Conference of Research Workers in Animal Diseases, St. Louis, MO. Abstract 199.
GE, N. L., KOCAN, K. M., BLOUIN, E. F. & MURPHY, G. L. ( 1996). Developmental studies of Anaplasma marginale (Rickettsiales[ratio ]Anaplasmataceae) in male Dermacentor andersoni (Acari[ratio ]Ixodidae) infected as adults by using non-radioactive in situ hybridization and microscopy. Journal of Medical Entomology 33, 911–920.CrossRefGoogle Scholar
HELM, R. ( 1924). Beitrag zum Anaplasmen-Problem. Zeitschrift für Infektionskr 25, 199–226.Google Scholar
HILDAGO, R. J. ( 1975). Propagation of Anaplasma marginale in bovine lymph node cell culture. American Journal of Veterinary Research 36, 635–640.Google Scholar
HOWARTH, J. A. & HOKAMA, Y. ( 1973). Tick transmission of anaplasmosis under laboratory conditions. In Proceedings of the 6th National Anaplasmosis Research Conference, pp. 117–120. Las Vegas, Nevada.
HOWARTH, J. A. & ROBY, T. O. ( 1972). Transmission of anaplasmosis by field collections of Dermacentor occidentalis Marx (Acarina: Ixodidae). 76th Meeting of the United States Animal Health Association, pp. 98–102.
HOWELL, D. E., STILES, G. W. & MOE, L. H. ( 1941). The fowl tick (Argas persicus), a new vector of anaplasmosis. American Journal of Veterinary Research 4, 73–75.Google Scholar
KESSLER, R. H. & RISTIC, M. ( 1979). In vitro cultivation of Anaplasma marginale: invasion of and development of noninfected erythrocytes. American Journal of Veterinary Research 40, 1744–1776.Google Scholar
KESSLER, R. J., RISTIC, M., SELLS, D. M. & CARSON, C. A. ( 1979). In vitro cultivation of Anaplasma marginale: growth pattern and morphological appearance. American Journal of Veterinary Research 40, 1767–1773.Google Scholar
KNOWLES, D. P., TORIONI DE ECHAIDE, S., PALMER, G. H., McGUIRE, T. C., STILLER, D. & McELWAIN, T. F. ( 1996). Antibody against an Anaplasma marginale MSP5 epitope common to tick and erythrocyte stages identified persistently infected cattle. Journal of Clinical Microbiology 34, 2225–2230.Google Scholar
KOCAN, K. M. ( 1986). Development of Anaplasma marginale in ixodid ticks: coordinated development of a rickettsial organism and its tick host. In Morphology, Physiology, and Behavioral Ecology of Ticks ( ed. Sauer, J. R. & Hair, J. A.), pp. 472–505. Chichester, Horwood, UK.
KOCAN, K. M., BLOUIN, E. F. & BARBET, A. F. ( 2000). Anaplasmosis control: past, present and future. Annals of the New York Academy of Science 916, 501–509.CrossRefGoogle Scholar
KOCAN, K. M., DE LA FUENTE, J., BLOUIN, E. F. & GARCIA-GARCIA, J. C. ( 2003 a). Adaptation of the tick-borne pathogen, Anaplasma marginale, for survival in cattle and tick hosts. In Proceedings of the 4th International Conference on Ticks and Tick-borne Pathogens, Experimental and Applied Acarology ( ed. Jongejan, F. & Kaufman, W. R.), Dordrecht, Boston, London, Kluwer Academic Publishers.
KOCAN, K. M., DE LA FUENTE, J., GUGLIELMONE, A. A. & MELENDÉZ, R. D. ( 2003 b). Anaplasma marginale: Antigens and control alternatives for a rickettsial hemoparasite of cattle. Clinical Microbiology Reviews, In press.Google Scholar
KOCAN, K. M., GOFF, W. L., STILLER, D., CLAYPOOL, P. L., EDWARDS, W., EWING, S. A., HAIR, J. A. & BARRON, S. J. ( 1992 a). Persistence of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) transferred successively from infected to susceptible calves. Journal of Medical Entomology 29, 657–668.Google Scholar
KOCAN, K. M., HAIR, J. A., EWING, S. A. & STRATTON, J. G. ( 1981). Transmission of Anaplasma marginale Theiler by Dermacentor andersoni Stiles and Dermacentor variabilis (Say). American Journal of Veterinary Research 42, 15–18.Google Scholar
KOCAN, K. M., HALBUR, T., BLOUIN, E. F., ONET, V., DE LA FUENTE, J., GARCIA-GARCIA, J. C. & SALIKI, J. T. ( 2001). Immunization of cattle with Anaplasma marginale derived from tick cell culture. Veterinary Parasitology 102, 151–161.CrossRefGoogle Scholar
KOCAN, K. M., MUNDERLOH, U. G. & EWING, S. A. ( 1998). Development of the Ebony isolate of Ehrlichia canis in cultured Ixodes scapularis cells. 79th Conference of Research Workers in Animal Diseases, Chicago. Abstract 95.
KOCAN, K. M., STILLER, D., GOFF, W. L., CLAYPOOL, P. L., EDWARDS, W., EWING, S. A., McGUIRE, T. C., HAIR, J. A. & BARRON, S. J. ( 1992 b). Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. American Journal of Veterinary Research 53, 499–507.Google Scholar
MARBLE, D. W. & HANKS, M. A. ( 1972). A tissue culture method for Anaplasma marginale. Cornell Veterinarian 62, 196–205.Google Scholar
MAZZOLA, V., AMERAULT, T. E. & ROBY, T. O. ( 1976). Survival of Anaplasma marginale in Aedes albopictus cells. American Journal of Veterinary Research 37, 987–989.Google Scholar
MAZZOLA, V., AMERAULT, T. E. & ROBY, T. O. ( 1979). Electron microscope studies of Anaplasma marginale in an Aedes albopictus culture system. American Journal of Veterinary Research 40, 1812–1815.Google Scholar
MAZZOLA, V. & KUTTLER, K. L. ( 1980). Anaplasma marginale in bovine erythrocyte cultures. American Journal of Veterinary Research 41, 2087–2088.Google Scholar
McBRIDE, J. W., XUE-JIE YU & WALKER, D. H. ( 2000). Glycosylation of homologous immunodominant proteins of Ehrlichia chaffeensis and Ehrlichia canis. Infection and Immunity 68, 13–18.CrossRefGoogle Scholar
McGAREY, D. J. & ALLRED, D. R. ( 1994). Characterization of hemagglutinating components on the Anaplasma marginale initial body surface and identification of possible adhesins. Infection and Immunity 62, 4587–4593.Google Scholar
McGAREY, D. J., BARBET, A. F., PALMER, G. H., McGUIRE, T. C. & ALLRED, D. R. ( 1994). Putative adhesins of Anaplasma marginale: major surface polypeptides 1a and 1b. Infection and Immunity 62, 4594–4601.Google Scholar
MEEUS, P. F. & BARBET, A. F. ( 2001). Ingenious gene generation. Trends in Microbiology 9, 353–355.CrossRefGoogle Scholar
MUNDERLOH, U. G., BLOUIN, E. F., KOCAN, K. M., GE, N. L., EDWARDS, W. & KURTTI, T. J. ( 1996 a). Establishment of the tick (Acari: Ixodidae)-borne cattle pathogen Anaplasma marginale (Rickettsiales: Anaplasmataceae) in tick cell culture. Journal of Medical Entomology 33, 656–664.Google Scholar
MUNDERLOH, U. G., JAURON, S. D., FINGERLE, V., LEITRITZ, L., HAYES, S. F., HAUTMAN, J. M., NELSON, C. M., HUBERTY, B. W., KURTTI, T. J., AHLSTRAND, G. G., GREIG, B., MELLENCAMP, M. A. & GOODMAN, J. L. ( 1999). Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. Journal of Clinical Microbiology 37, 2518–2524.Google Scholar
MUNDERLOH, U. G. & KURTTI, T. J. ( 1989). Formulation of medium for tick cell culture. Experimental and Applied Acarology 7, 219–229.CrossRefGoogle Scholar
MUNDERLOH, U. G., MADIGAN, J. E., DUMLER, J. S., GOODMAN, J. L., HAYES, S. F., BARLOUGH, J. E., NELSON, C. M. & KURTTI, T. J. ( 1996 b). Isolation of the equine granulocytic ehrlichiosis agent, Ehrlichia equi, in tick cell culture. Journal of Clinical Microbiology 34, 664–670.Google Scholar
MUNDERLOH, U. G., WANG, Y. L. M., CHEN, C. & KURTTI, T. J. ( 1994). Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. Journal of Parasitology 80, 533–543.CrossRefGoogle Scholar
NUTTALL, P. A. ( 1999). Pathogen–tick–host interactions: Borrelia burgdorferi and TBE virus. Zentralblatt für Bakteriologie 289, 492–505.CrossRefGoogle Scholar
OBERLE, S. M., PALMER, G. H., BARBET, A. F. & McGUIRE, T. C. ( 1988). Molecular size variations in an immunoprotective protein complex among isolates of Anaplasma marginale. Infection and Immunity 56, 1567–1573.Google Scholar
PALMER, G. H. ( 1989). Anaplasmosis vaccines. In Veterinary Protozoan and Hemoparasite Vaccines ( ed. Wright, I. G.), pp. 1–29. CRC Press, Boca Raton, FL.
PALMER, G. H., RURANGIRWA, F. R. & McELWAIN, T. F. ( 2001). Strain composition of the ehrlichia Anaplasma marginale within persistently infected cattle, a mammalian reservoir for tick transmission. Journal of Clinical Microbiology 39, 631–635.CrossRefGoogle Scholar
PALMER, G. H., WAGHELA, S. D., BARBET, A. F., DAVIS, W. C. & McGUIRE, T. C. ( 1987). Characterization of a neutralization sensitive epitope on the AM 105 surface protein of Anaplasma marginale. Journal of Parasitology 17, 1279–1285.CrossRefGoogle Scholar
PARKER, R. J. ( 1982). The Australian brown dog tick Rhipicephalus sanguineus as an experimental parasite of cattle and vector of Anaplasma marginale. Australian Veterinary Journal 58, 47–51.CrossRefGoogle Scholar
PETERSON, K. J., RALEIGH, R. J., STROUND, R. K. & GOULDING, R. L. ( 1977). Bovine anaplasmosis transmission studies conducted under controlled natural exposure in a Dermacentor andersoni=(venustus) indigenous areas of eastern Oregon. American Journal of Veterinary Research 38, 351–354.Google Scholar
PIERCY, P. L. ( 1938). Fifty-first Annual Report, Texas Agricultural Experiment Station, pp. 12.
PIERCY, P. L. & SCHMIDT, H. ( 1941). Fifty-fourth Annual Report, Texas Agricultural Experiment Station, pp. 110–111.
POTGIETER, F. T. ( 1979). Epizootiology and control of anaplasmosis in South Africa. Journal of the South African Veterinary Association 504, 367–372.Google Scholar
POTGIETER, F. T., KOCAN, K. M., McNEW, R. W. & EWING, S. A. ( 1983). Demonstration of colonies of Anaplasma marginale in the midgut of Rhipicephalus simus. American Journal of Veterinary Research 44, 2256–2261.Google Scholar
REES, C. W. ( 1930). Experimental transmission of anaplasmosis by Rhipicephalus sanguineus. North American Veterinarian 11, 17–20.Google Scholar
REES, C. W. ( 1932). The experimental transmission of anaplasmosis by Dermacentor variabilis. Science 75, 318–320.CrossRefGoogle Scholar
REES, C. W. ( 1933). The experimental transmission of anaplasmosis by Dermacentor andersoni. Parasitology 21, 569–573.CrossRefGoogle Scholar
REES, C. W. ( 1934). Transmission of anaplasmosis by various species of ticks. United States Department of Agriculture, Technical Bulletin 418, Washington, D.C.
REES, C. W. & AVERY, J. L. ( 1939). Experiments on the hereditary transmission of anaplasmosis by ticks. North American Veterinarian 20, 35–36.Google Scholar
RICHEY, E. J. ( 1981). Bovine Anaplasmosis. In Current Veterinary Therapy Food Animal Practice ( ed. Howard, R. J.), pp. 767–772. Philadelphia W.B. Saunders Co., Philadelphia.
RISTIC, M. ( 1968). Anaplasmosis. In Infectious Blood Diseases of Man and Animals ( ed. Weinman, D. & Ristic, M.), pp. 478–542. Academic Press, New York.CrossRef
RODRIGUEZ, S. D., GARCIA ORTIZ, M. A., HERNANDEZ SALGADO, G., SANTOS CERDA, N. A., ABOYTES TORRE, R. & CANTO ALARCON, G. J. ( 2000). Anaplasma marginale inactivated vaccine: dose titration against a homologous challenge. Comparative Immunology Microbiology of Infectious Diseases 23, 239–252.CrossRefGoogle Scholar
ROSENBUSCH, F. & GONZALEZ, R. ( 1927). Die Tristeza Uebertragung durch Zecken und dessen Immunitatsprobleme. Archiv für Protistenkunde 58, 300–320.Google Scholar
ROZEBOOM, L. E., STILES, G. W. & MOE, L. H. ( 1940). Anaplasmosis transmission by Dermacentor andersoni Stiles. Journal of Parasitology 26, 95–100.CrossRefGoogle Scholar
RURANGIRWA, F. R., STILLER, D., FRENCH, D. M. & PALMER, G. H. ( 1999). Restriction of major surface protein 2 (MSP2) variants during tick transmission of the ehrlichia Anaplasma marginale. Proceedings of the National Academy of Sciences, USA 96, 3171–3176.CrossRefGoogle Scholar
RURANGIRWA, R. F., STILLER, D. & PALMER, G. H. ( 2000). Strain diversity in major surface protein 2 expression during tick transmission of Anaplasma marginale. Infection and Immunity 68, 3023–3027.CrossRefGoogle Scholar
SALIKI, J. T., BLOUIN, E. F., RODGERS, S. J. & KOCAN, K. M. ( 1998). Use of tick cell culture-derived Anaplasma marginale antigen in a competitive ELISA for serodiagnosis of anaplasmosis. Annals of the New York Academy of Science 849, 273–281.CrossRefGoogle Scholar
SAMISH, M., PIPANO, E. & HADANI, A. ( 1993). Intrastadial and interstadial transmission of Anaplasma marginale by Boophilus annulatus ticks in cattle. American Journal of Veterinary Research 54, 411–414.Google Scholar
SAMISH, M., PIPANO, E. & HANA, G. ( 1988). Cultivation of Anaplasma marginale from cattle in a Dermacentor cell line. American Journal of Veterinary Research 49, 254–256.Google Scholar
SANBORN, C. E. & MOE, L. H. ( 1934). Anaplasmosis investigations. In Report of the Oklahoma Agricultural and Mining College and Agricultural Experiment Station, 1932–1934, pp. 275–279.
SANBORN, C. E., STILES, G. W. & MOE, L. H. ( 1938). Anaplasmosis transmission by naturally infected Dermacentor andersoni male and female ticks. North American Veterinarian 19, 31–32.Google Scholar
SANDERS, D. A. ( 1933). Notes on the experimental transmission of bovine anaplasmosis in Florida. Journal of the American Veterinary Medical Association 88, 799–805.Google Scholar
SCHMIDT, H. & PIERCY, P. L. ( 1937). In Fiftieth Annual Report of the Texas Agricultural Experiment Station, pp. 12–14.
SERGENT, E., DONTIEN, A., PARROT, L., ET LESTOQUARD, F. (IN MEMORIAM) ( 1945). Etudes sur les Piroplasmoses Bovines. Institut Pasteur d'Algerie’, p. 816.Google Scholar
SMITH, R., LEVY, M. G., KUHLENSCHMIDT, M. S., ADAMS, J. H., RZECHULA, D. G., HARDT, T. A. & KOCAN, K. M. ( 1986). Isolate of Anaplasma marginale not transmitted by ticks. American Journal of Veterinary Research 47, 127–129.Google Scholar
STICH, R. W., KOCAN, K. M., PALMER, G. H., EWING, S. A., HAIR, J. A. & BARRON, S. J. ( 1989). Transstadial and attempted transovarial transmission of Anaplasma marginale Theiler by Dermacentor variabilis (Say). American Journal of Veterinary Research 50, 1386–1391.Google Scholar
STILLER, D., CROSBIE, P. R., BOYCE, W. M. & GOFF, W. L. ( 1999). Dermacentor hunteri (Acari: Ixodidae): an Experimental vector of Anaplasma marginale and A. ovis (Rickettsiales: Anaplasmataceae) to calves and sheep. Journal of Medical Entomology 36, 321–324.Google Scholar
STILLER, D. & JOHNSON, L. W. ( 1983). Experimental transmission of Anaplasma marginale Theiler by adults of Dermacentor albipictus (Packard) and Dermacentor occidentalis Marx (Acari: Ixodidae). In Proceedings of the 87th Annual Meeting of the US Animal Health Association, pp. 59–65.
STILLER, D., LEATCH, G. & KUTTLER, K. ( 1981). Experimental transmission of bovine anaplasmosis by the winter tick, Dermacentor albipictus (Packard). In Proceeding of the National Anaplasmosis Conference, pp. 463–475. Mississippi State University, Mississippi.
THEILER, A. ( 1911). Further investigations into anaplasmosis of South African cattle, pp. 7–46. In 1st Report of the Director of Veterinary Research, Department of Agriculture of the Union of South Africa.
THEILER, A. ( 1912). Uebertragung der anaplasmosis mittels Zecken. Zeitschrift für Infektionskrankheiten 12, 105–116.Google Scholar
VISESHAKUL, N., KAMPER, S., BOWIE, M. V. & BARBET, A. F. ( 2000). Sequence and expression analysis of a surface antigen gene family of the rickettsia Anaplasma marginale. Gene 253, 45–53.CrossRefGoogle Scholar
VISSER, E. S., McGUIRE, T. C., PALMER, G. H., DAVIS, W. C., SHKAP, V., PIPANO, E. & KNOWLES, D. P. ( 1992). The Anaplasma marginale msp5 gene encodes a 19-kilodalton protein conserved in all recognized Anaplasma species. Infection and Immunity 60, 5139–5144.Google Scholar
WICKWIRE, K. B., KOCAN, K. M., BARRON, S. J., EWING, S. A., SMITH, R. D. & HAIR, J. A. ( 1987). Infectivity of three Anaplasma marginale isolates for Dermacentor andersoni. American Journal of Veterinary Research 48, 96–99.Google Scholar
WIKEL, S. K., RAMACHANDRA, R. N., BERGMAN, D. K., BURKOT, T. R. & PIESMAN, J. ( 1997). Infestation with pathogen-free nymphs of the tick Ixodes scapularis induces host resistance to transmission of Borrelia burgdorferi by ticks. Infection and Immunity 65, 335–388.Google Scholar
ZELLER, H. & HELM, R. ( 1923). Versuche zur Frage der Uebertragbarkeit des Texasfiebers auf Deutrsche Rinder durch die bei uns vorkommenden Zecken Ixodes ricinus und Haemaphysalis punctata Cinabarina. Berliner tierärztliche Wochenschrift 39, 1–4.Google Scholar