Skip to main content
SpringerLink
Log in

Adaptations of the tick-borne pathogen, Anaplasma marginale, for survival in cattle and ticks

  • Chapter
Ticks and Tick-Borne Pathogens

Abstract

The tick-borne cattle pathogen Anaplasma marginale (Rickettsiales: Anaplasmataceae) multiplies within membrane-bound inclusions in host cell cytoplasm. Many geographic isolates of A. marginale occur that vary in genotype, antigenic composition, morphology and infectivity for ticks. A tick cell culture system for propagation of A. marginale proved to be a good model for study of tick-pathogen interactions. Six major surface proteins (MSPs) identified on A. marginale from bovine erythrocytes were conserved on A. marginale derived from tick cells. MSP1a and MSP1b were adhesins for bovine erythrocytes, while only MSP1a was found to be an adhesin for tick cells. The tandemly repeated portion of MSP1a was found to be necessary and sufficient for adhesion to both tick cells and bovine erythrocytes. Infectivity of A. marginale isolates for ticks was dependent on the adhesive capacity of the isolate MSP1a, which was found to involve both the adhesive properties and sequence of the repeated peptides. Cattle immunized with A. marginale derived from bovine erythrocytes or tick cells demonstrated a differential antibody response to MSP1a and MSP1b that resulted from the differential expression of these proteins in cattle and ticks cells. MSP2, derived from a multi-gene family, was found to undergo antigenic variation in cattle and ticks and may contribute to establishment of persistent A. marginale infections. MSP1a has been used as a stable genetic marker for geographic isolates because the molecular weight varies due to differing numbers of the tandem repeats. However, phylogenetic studies of A. marginale isolates from North America using MSP1a and MSP4 demonstrated that MSP4 was a good biogeographic marker, while MSP1a varied greatly among and within geographic areas. Infection and development of A. marginale in cattle and tick cells appears to differ and to be mediated by several surface proteins encoded from the small genome.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Allred, D.R., McGuire, T.C., Palmer, G.H., Leib, S.R., Harkins, T.M., McElwain, T.F. and Barbet, A.F. 1990. Molecular basis for surface antigen size polymorphisms and conservation of a neutralization-sensitive epitope in Anaplasma marginale. Proc. Nat. Acad. Sci. USA 87: 3220–3224.

    Article  CAS  Google Scholar 

  • Barbet, A.F., Palmer, G.H., Myler, P.J. and McGuire, T.C. 1987. Characterization of an immunoprotective protein complex of Anaplasma marginale by cloning and expression of the gene coding for polypeptide AmI05L. Infect. Immun. 55: 2428–2435.

    PubMed  CAS  Google Scholar 

  • Barbet, A.F., Blentlinger, R.. Yi. J., Lundgren. A.M.. Blouin, E.F. and Kocan. K.M. 1999. Comparison of surface proteins of Anaplasma marginale grown in tick cell culture, tick salivary glands, and cattle. Infect. Immun. 67: 102–107.

    CAS  Google Scholar 

  • Bell-Sakyi, L.M., Paxton, E.A., Munderloh, U.G. and Sumption, K.J. 2000. Growth of Cowdria ruminantium, the causative agent of heartwater, in a tick cell line. J. Clin. Microbiol. 38: 1238–1240.

    PubMed  CAS  Google Scholar 

  • Blouin, E.F. and Kocan, K.M. 1998. Morphology and development of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in cultured trades scapularis (Acari: Ixodidae) cells. J. Med. Ent. 35: 788–797.

    CAS  Google Scholar 

  • Blouin, E.F., Barbet. A.F., Jooyoung Yi, Kocan, K.M. and Saliki, J.T. 1999. Establishment and characterization of an Oklahoma isolate of Anaplasma marginale in cultured Ixodes scapularis cells. Vet. Parasitol. 87: 301–313.

    Google Scholar 

  • Blouin, E.F., de la Fuente, J.. Garcia-Garcia. J.C.. Sauer, J.R.. Saliki, J.T. and Kocan, K.M. 2002. Applications of a cell culture system for studying the interaction of Anaplasma marginale with tick cells. Anim. Health Res. Rev. 3: 57–68.

    Article  PubMed  Google Scholar 

  • Blouin, E.F., Saliki J.T., de la Fuente, J., Garcia-Garcia, J.C. and Kocan, K.M. 2003. Antibodies to Anaplasma marginale Major Surface Protein la and lb inhibit infectivity for cultured tick cells. Vet. Parasitol. 111: 247–260.

    Article  PubMed  CAS  Google Scholar 

  • Bowie, J.V., de la Fuente, J., Kocan, K.M., Blouin. E.F. and 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.

    CAS  Google Scholar 

  • Bram, R.A. 1975. Tick-borne livestock diseases and their vectors. 1. The global problem. World Anim. Rev. 6: 1–5.

    Google Scholar 

  • Camacho-Nuez, J., De Lourdes Munoz. M., Suarez. C.E.. McGuire. T.C., Brown, W.C. and Palmer, G.H. 2000. Expression of polymorphic mspllJ genes during acute Anaplasma marginale rickettsemia. Infect. Immun. 68: 1946–1952.

    CAS  Google Scholar 

  • de la Fuente, J. and Kocan, K.M. 2001. Expression of Anaplasma marginale major surface protein 2 variants in persistently infected ticks. Infect. Immun. 69: 5151–5156.

    Article  PubMed  Google Scholar 

  • de la Fuente, J., Van Den Bussche, R.A. and Kocan, K.M. 200la. Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Vet. Parasitol. 97: 65–76.

    Google Scholar 

  • de la Fuente, J., Garcia-Garcia, J.C., Blouin, E.F. and Kocan, K.M. 2001b. Differential adhesion of major surface proteins la and lb of the ehrlichial cattle pathogen Anaplasma marginale to bovine erythrocytes and tick cells. Int. J. Parasitol. 31: 145–153.

    Article  PubMed  Google Scholar 

  • de la Fuente, J., Garcia-Garcia. J.C., Blouin, E.F. and Kocan, K.M. 2001c. Major surface protein 1a effects tick infection and transmission of the ehrlichial pathogen Anaplasma marginale. Int. J. Parasitol. 31: 1705–1714.

    Google Scholar 

  • de la Fuente, J., Garcia-Garcia, J.C., Blouin, E.F., Rodriguez, S.D., Garcia, M.A. and Kocan, K.M. 2001d. Evolution and function of tandem repeats in the major surface protein la of the ehrlichial pathogen Anaplasma marginale. Anim. Health Res. Rev. 2: 163–173.

    Google Scholar 

  • de la Fuente, J., Garcia-Garcia, J.C., Blouin. E.F. and Kocan, K.M. 2002a. Characterization of the functional domain of major surface protein la involved in adhesion of the rickettsia Anaplasma marginale to host cells. Vet. Microbiol. 91: 265–283.

    Google Scholar 

  • de la Fuente, J., Kocan, K.M., Garcia-Garcia, J.C., Blouin, E.F., Claypool, P.L. and Saliki, J.T. 2002b. Vaccination of cattle with Anaplasma marginale derived from tick cell culture and bovine erythrocytes followed by challenge-exposure by infected ticks. Vet. Microbiol. 89: 239–251.

    Article  PubMed  Google Scholar 

  • de la Fuente, J., Van Den Bussche, R.A., Garcia-Garcia, J.C.. Rodriguez, S.D., Garcia, M.A., Guglielmone, A.A., Mangold, A.J., Passos, L.M.. Blouin, E.F. and Kocan, K.M. 2002e. Phylogeography of New World isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae) based on major surface protein sequences. Vet. Microbiol. 88: 275–285.

    Google Scholar 

  • de la Fuente, J., Garcia-Garcia, J.C., Blouin, E.F., Saliki, J.T. and Kocan. K.M. 2002d. Infection of tick cells and bovine erythrocytes with one genotype of the intracellular ehrlichia Anaplasma marginale excludes infection with other genotypes. Diagn. Lab. Immunol. 9: 658–668.

    Google Scholar 

  • de la Fuente, J., Van Den Bussche, R.A., Prado, T. and Kocan, K.M. 2003. Anaplasma marginale major surface protein la genotypes evolved under positive selection pressure but are not a marker for geographic isolates. J. Clin. Microbiol. (in press).

    Google Scholar 

  • de la Fuente, J. Blouin, E.F. and Kocan, K.M. 2003. Infection of ticks with the intracellular rickettsia Anaplasma marginale excludes infection with other genotypes. Clin. Diagn. Lab. Immunol. 10: 182–184.

    PubMed  Google Scholar 

  • Dikman, G. 1950. The transmission of anaplasmosis. Am. J. Vet. Res. 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. and 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 phagocvtophila. Int. J. Sys. Evol. Microbiol. 51: 2145–2165.

    CAS  Google Scholar 

  • Ewing, S.A. 1981. Transmission of Anaplasma marginale by arthropods. In: Proceedings of the 7th National Anaplasmosis Conference, Mississippi State University, MS, USA, pp. 395–423.

    Google Scholar 

  • French, D.M., McElwain, T.F., McGuire. T.C. and Palmer. G.H. 1998. Expression of Ana-plasma marginale major surface protein 2 variants during persistent cyclic rickettsemia [published erratum appears in Infect. Immun., May 1998, 66: 2400]. Infect. Immun. 66: 1200–1207.

    CAS  Google Scholar 

  • French, D.M., Brown, W.C. and Palmer. G.H. 1999. Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infect. Immun. 67: 5834–5840.

    PubMed  CAS  Google Scholar 

  • Garcia-Garcia, J.C., de la Fuente, J.. Blouin. E.F., Saliki, J.T. and Kocan, K.M. 2002. Differential antibody response of cattle immunized with Anaplasma marginale derived from bovine erythrocytes or cultured tick cells. In: Proceedings of the 4th International Conference on Ticks and Tick-borne Pathogens. Banff, Alberta, Canada.

    Google Scholar 

  • Ge, N.L., Kocan, K.M., Blouin. E.F. and Murphy, G.L. 1996. Developmental studies of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) infected as adults by using non-radioactive in situ hybridization and microscopy. J. Med. Entomol. 33: 911–920.

    CAS  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, J.R. Sauer and J.A. Hair (eds), pp. 472–505. Chichester. Horwood.

    Google Scholar 

  • Kocan, K.M., Stiller, D., Goff, W.L.. Claypool. P.L.. Edwards, W., Ewing, S.A., McGuire, T.C., Hair, J.A. and Barron. S.J. 1992a. Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. Am. J. Vet. Res. 53: 499–507.

    CAS  Google Scholar 

  • Kocan, K.M., Goff, W.L., Stiller, D., Claypool. P.L., Edwards, W., Ewing. S.A., Hair, J.A. and Barron, S.J. 1992b. Persistence of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) transferred successively from infected to susceptible calves. J. Med. Entomol. 29: 657–668.

    PubMed  CAS  Google Scholar 

  • Kocan, K.M., Munderloh, U.G. and Ewing. S.A. 1998. Development of the Ebony isolate of Ehrlichia canis in cultured I.v - odes scapalari.c cells. In: Proceedings of the 79th Conference of Research Workers in Animal Diseases. Chicago (abstract 95).

    Google Scholar 

  • Kocan, K.M., Blouin, E.F. and Barbet. A.F. 2000. Anaplasmosis control: past. present and future. Ann. NY Acad. Sci. 916: 501–509.

    Article  PubMed  CAS  Google Scholar 

  • Kocan, K.M., Halbur. T., Blouin, E.F., Onet. V.. de la Fuente. J.. Garcia-Garcia, J.C. and Saliki, J.T. 2001. Immunization of cattle with Anaplasma marginale derived from tick cell culture. Vet. Parasitol. 102: 151–161.

    Article  PubMed  CAS  Google Scholar 

  • Kocan, K.M., de la Fuente, J., Guglielmone. A.A. and Melendéz, R.D. 2003. Anaplasma marginale: Antigens and control alternatives for a rickettsial hemoparasite of cattle. Clin. Microbiol. Rev. (submitted).

    Google Scholar 

  • Lew, A.E., Bock, R.E., Minchin. C.M. and Masaka, S. 2002. A mspla polymerase chain reaction assay for specific detection and differentiation of Anaplasma marginate isolates. Vet. Microbiol. 86: 325–335.

    CAS  Google Scholar 

  • McGarey, D.J. and Allred, D.R. 1994. Characterization of hemagglutinating components on the Anaplasma marginale initial body surface and identification of possible adhesins. Infect. Immun. 62: 4587–4593.

    PubMed  CAS  Google Scholar 

  • McGarey, D.J., Barbet, A.F., Palmer. G.H., McGuire, T.C. and Allred, D.R. 1994. Putative adhesins of Anaplasma marginale: major surface polypeptides la and lb. Infect. Immun. 62: 4594–4601.

    CAS  Google Scholar 

  • Munderloh, U.G., Blouin, E.F.. Kocan. K.M.. Ge. N.L., Edwards. W. and Kurtti, T.J. 1996a. Establishment of the tick (Acari: Ixodidae)-borne cattle pathogen Anaplasma marginale (Rickettsiales: Anaplasmataceae) in tick cell culture. J. Med. Entomol. 33: 656–664.

    CAS  Google Scholar 

  • Munderloh, U.G., Madigan. J.E.. Dumler, J.S.. Goodman. J.L., Hayes, S.F., Barlough, J.E., Nelson, C.M. and Kurtti. T.J. 1996b. Isolation of the equine granulocytic ehrlichiosis agent, Ehrlichia equi, in tick cell culture. J. Clin. Microbiol. 34: 664–670.

    CAS  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. and Goodman, J.L. 1999. Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. J. Clin. Microbiol. 37: 2518–2524.

    CAS  Google Scholar 

  • Palmer, G.H., Waghela, S.D., Barbet, A.F.. Davis,W.C. and McGuire, T.C. 1987. Characterization of a neutralization sensitive epitope on the AM 105 surface protein of Anaplasma marginale. J. Parasitol. 17: 1279–1285.

    CAS  Google Scholar 

  • Palmer, G.H. 1989. Anaplasmosis vaccines, In: Veterinary Protozoan and Hemoparasite Vaccines, I.G. Wright (ed.), pp. 1–29. CRC Press, Boca Raton. FL.

    Google Scholar 

  • Palmer, G.H., Rurangirwa, F.R. and McElwain, T.F. 2001. Strain composition of the ehrlichia Anaplasma marginale within persistently infected cattle, a mammalian reservoir for tick transmission. J. Clin. Microbiol. 39: 631–635.

    Article  PubMed  CAS  Google Scholar 

  • Richey, E.J. 1981. Bovine anaplasmosis. In: Current Veterinary Therapy Food Animal Practice, R.J. Howard (ed.), pp. 767–772. Saunders. Philadelphia.

    Google Scholar 

  • Ristic, M. 1968. Anaplasmosis. In: Infectious Blood Diseases of Man and Animals, D. Weinman and M. Ristic (eds). pp. 478–542. Academic Press, New York.

    Google Scholar 

  • Saliki, J.T., Blouin, E.F., Rodgers, S.J. and Kocan, K.M. 1998. Use of tick cell culture-derived Anaplasma marginale antigen in a competitive ELISA for serodiagnosis of anaplasmosis. Ann. NY Acad. Sci. 849: 273–281.

    Article  PubMed  CAS  Google Scholar 

  • Smith, R., Levy, M.G., Kuhlenschmidt, M.S., Adams, J.H.. Rzechula, D.G., Hardt, T.A. and Kocan, K.M. 1986. Isolate of Anaplasma marginale not transmitted by ticks. Am. J. Vet. Res. 47: 127–129.

    PubMed  CAS  Google Scholar 

  • Viseshakul, N., Kamper, S., Bowie, M.V. and Barbet, A.F. 2000. Sequence and expression analysis of a surface antigen gene family of the rickettsia Anaplasma marginale. Gene 253: 45–53.

    Article  CAS  Google Scholar 

  • Wickwire, K.B., Kocan, K.M., Barron, Si_ Ewing, S.A., Smith, R.D. and Hair, J.A. 1987. Infectivity of three Anaplasrna marginale isolates for Dermacentor andersoni. Am. J. Vet. Res. 48: 96–99.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Veterinary Pathobiology, College of Veterinary Medicine, Oklahoma State University, 250 McElroy Hall, Stillwater, OK, 74078-2007, USA

    Katherine M. Kocan, Jose De La Fuente, Edmour F. Blouin & Jose Carlos Garcia-Garcia

Authors
  1. Katherine M. Kocan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jose De La Fuente
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edmour F. Blouin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jose Carlos Garcia-Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katherine M. Kocan .

Editor information

Editors and Affiliations

  1. Utrecht University, Utrecht, The Netherlands

    Frans Jongejan (Scientific Program Chair TTP 4) (Scientific Program Chair TTP 4)

  2. University of Pretoria, South Africa

    Frans Jongejan (Scientific Program Chair TTP 4) (Scientific Program Chair TTP 4)

  3. University of Alberta, Edmonton, Canada

    W. Reuben Kaufman (Conference Chair) (Conference Chair)

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Kocan, K.M., De La Fuente, J., Blouin, E.F., Garcia-Garcia, J.C. (2003). Adaptations of the tick-borne pathogen, Anaplasma marginale, for survival in cattle and ticks. In: Jongejan, F., Kaufman, W.R. (eds) Ticks and Tick-Borne Pathogens. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-3526-1_1

Download citation

  • DOI: https://doi.org/10.1007/978-94-017-3526-1_1

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-6355-7

  • Online ISBN: 978-94-017-3526-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation