Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-05-17T00:44:00.234Z Has data issue: false hasContentIssue false
  • English
  • Français

Applications of a cell culture system for studying the interaction of Anaplasma marginale with tick cells

Published online by Cambridge University Press:  09 March 2007

Edmour F. Blouin ,
José de la Fuente ,
Jose C. Garcia-Garcia ,
John R. Sauer ,
Jeremiah T. Saliki  and
Katherine M. Kocan
Edmour F. Blouin*
Affiliation:
Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA
José de la Fuente
Affiliation:
Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA
Jose C. Garcia-Garcia
Affiliation:
Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA
John R. Sauer
Affiliation:
Department of Entomology, Oklahoma State University, Stillwater, OK 74078, USA
Jeremiah T. Saliki
Affiliation:
Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA Oklahoma Animal Disease Diagnostic Laboratory, College of Veterinary Medicine, Oklahoma State University, Stillwater, OK 74078, USA
Katherine M. Kocan
Affiliation:
Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA
*
*Corresponding author Department of Veterinary Pathobiology, College of Veterinary Medicine, Oklahoma State University, Stillwater, OK 74078–2007, USA E-mail: blouin@okstate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

A cell culture system for the tick-borne rickettsia Anaplasma marginale offers new opportunities for research on this economically important pathogen of cattle. A. marginale multiplies in membrane-bound inclusions in host cells. Whereas erythrocytes appear to be the only site of infection in cattle, A. marginale undergoes a complex developmental cycle in ticks and transmission occurs via the salivary glands during feeding. We recently developed a cell culture system for A. marginale using a cell line derived from embryos of Ixodes scapularis. Here we review the use of this cell culture system for studying the interaction of A. marginale with tick cells. Several assays were developed using the A. marginale/tick cell system. An adhesion assay was developed for the identification of proteins required by A. marginale for adhesion to tick cells. The effect of antibodies against selected major surface proteins in inhibiting A. marginale infection was tested in an assay that allowed further confirmation of the role of surface proteins in the infection of tick cells. A drug screening assay for A. marginale was developed and provides a method of initial drug selection without the use of cattle. The culture system was used to test for enhancing effects of tick saliva and saliva components on A. marginale infection. The tick cell culture system has proved to be a good model for studying A. marginale–tick interactions. Information gained from these studies may be applicable to other closely related tick-borne pathogens that have been propagated in the same tick cell line.

Type
Research Article
Information
Animal Health Research Reviews , Volume 3 , Issue 2 , December 2002 , pp. 57 - 68
Copyright
Copyright © CAB International 2002

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

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: 3220–3224.CrossRefGoogle ScholarPubMed
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: 2428–2435.CrossRefGoogle ScholarPubMed
Barbet, AF, Blentlinger, R, Yi, J, Lundgren, AM, Blouin, EF and Kocan, KM (1999). Comparison of surface proteins of Anaplasma marginale grown in tick cell culture, tick salivary glands, and cattle. Infection and Immunity 67: 102–107.CrossRefGoogle ScholarPubMed
Bell-Sakyi, LM, Paxton, EA, Munderloh, UG and Sumption, KJ (2000). Growth of Cowdria ruminantium, the causative agent of heartwater, in a tick cell line. Journal of Clinical Microbiology 38: 1238–1240.CrossRefGoogle Scholar
Blouin, EF and Kocan, KM (1998). Morphology and development of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in cultured Ixodes scapularis (Acari: Ixodidae) cells. Journal of Medical Entomology 35: 788–797.CrossRefGoogle ScholarPubMed
Blouin, EF, Barbet, AF, Jooyoung, YI, Kocan, KM and Saliki, JT (1999). Establishment and characterization of an Oklahoma isolate of Anaplasma marginale in cultured Ixodes scapularis cells. Veterinary Parasitology 87: 301–313.CrossRefGoogle Scholar
Blouin, EF, Kocan, KM, Sauer, JR and Saliki, JT (1999b) Putative role of phospholipase A2 in the invasion of Anaplasma marginale into tick cells. 80th Conference of Research Workers in Animal Diseases,Chicago Abstract 156.Google Scholar
Blouin, EF, Kocan, KM, de la Fuente, J and Saliki, JT (2002). Effect of tetracycline on development of Anaplasma marginale in cultured Ixodes scapularis cells. Veterinary Parasitology 2360: 1–12.Google Scholar
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: 95–102.CrossRefGoogle Scholar
Bowman, AS, Gengler, CL, Surdick, MR, Zhu, K, Essenberg, RC, Sauer, JR and Dillwith, JW (1997). A novel phospholipase A2 activity in saliva of the lone star tick, Amblyomma americanum (L). Experimental Parasitology 87: 121–132.CrossRefGoogle ScholarPubMed
Bram, RA (1975). Tick-borne livestock diseases and their vectors. 1. The global problem. World Animal Review 6: 1–5.Google Scholar
Brown, WC, Palmer, GH, Lewin, HA and McGuire, TC (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 ScholarPubMed
Camacho-Nuez, J, De Lourdes Muñoz, M, Suarez, CE, McGuire, TC, Brown, WC and Palmer, GH (2000). Expression of polymorphic msp1b genes during acute Anaplasma marginale rickettsemia. Infection and Immunity 68: 1946–1952.CrossRefGoogle ScholarPubMed
Connelly, MC and Kierszenbaum, F (1984). Modulation of macrophage interaction with Trypanosoma cruzi by phospholipase A2-sensitive components of the parasite membrane. Biochemical and Biophysical Research Communications 121: 931–938.CrossRefGoogle ScholarPubMed
de la Fuente, J, Van Den Bussche, RA and Kocan, KM (2001a). Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Veterinary Parasitology 97: 65–76.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: 145–153.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: 1705–1714.CrossRefGoogle Scholar
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF, Rodriguez, SD, Garcia, MA and Kocan, KM (2001d). 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.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 (2002a). Phylogeography of New World isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae) based on major surface protein sequences. Veterinary Microbiology 88: 275–285.CrossRefGoogle Scholar
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF and Kocan, KM (2002b). Characterization of the functional domain of major surface protein 1a involved in adhesion of the rickettsia Anaplasma marginale to host cells. Veterinary Microbiology. In: press.CrossRefGoogle Scholar
de la Fuente, J, Kocan, KM, Garcia-Garcia, JC, Blouin, EFClaypool, PL and Saliki, JT (2002) 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.CrossRefGoogle ScholarPubMed
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF, Saliki, JT and Kocan, KM (2002). Infection of tick cells and bovine erythrocytes with one genotype of the intracellular ehrlichia Anaplasma marginale excludes infection with other genotypes. Clinical Diagnostic Laboratory Immunology 9: 658–668.Google ScholarPubMed
Dikman, G (1950). The transmission of anaplasmosis. American Journal of Veterinary Research 11: 5–16.Google Scholar
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: 2145–2165.CrossRefGoogle ScholarPubMed
Ewing, SA (1981). Transmission of Anaplasma marginale by arthropods. In: Proceedings of the 7th National Anaplasmosis Conference,Mississippi State University,MS, USA,395–423.Google Scholar
Gale, KR, Leatch, M and Dimmock, CM (1992). Anaplasma marginale: failure of passive serum from immune cattle to confer protection in passive transfer experiments. Parasitology Research 78: 410–415.CrossRefGoogle ScholarPubMed
Garcia-Garcia, JC, Blouin, EF, Saliki, JT, de la Fuente, J, Sauer, JR and Kocan, KM (2001) Role of tick saliva phospholipase A2 in invasion of tick cells by Anaplasma marginale. In: 82nd Conference of Research Workers in Animal Diseases,St. Louis. Abstract 150.Google Scholar
Ge, NL, Kocan, KM, Blouin, EF and Murphy, GL (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. Journal of Medical Entomology 33: 911–920.CrossRefGoogle Scholar
Gomez Marin, JE, Bonhomme, A, Guenounou, M and Pinon, JM (1996). Role of interferon-g against invasion by Toxoplasma gondii in a human monocytic cell line (THP1): involvement of the parasite's secretory phospholipase A2. Cellular Immunology 169: 24–31.Google Scholar
Hildago, RJ (1975). Propagation of Anaplasma marginale in bovine lymph node cell culture. American Journal of Veterinary Research 36: 635–640.Google Scholar
Kessler, RH and 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 ScholarPubMed
Kessler, RJ, Ristic, M, Sells, DM and Carson, CA (1979) In vitro cultivation of Anaplasma marginale: growth pattern and morphological appearance. American Journal of Veterinary Research 40: 1767–1773.Google Scholar
Kocan, KM (1986). Development of Anaplasma marginale in ixodid ticks: coordinated development of a rickettsial organism and its tick host. In: Sauer, JR, Hair, JA (editors). Morphology, Physiology, and Behavioral Ecology of Ticks. Chichester: Horwood, pp. 472–505.Google Scholar
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 parasitemic to susceptible cattle. American Journal of Veterinary Research pp. 53: 499–507.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 calves. Journal of Medical Entomology 2: 657–668.CrossRefGoogle Scholar
Kocan, KM, Munderloh, UG & Ewing, SA (1998). Development of the Ebony isolate of Ehrlichia canis in cultured Ixodes scapularis cells. In: 79th Conference of Research Workers in Animal Diseases,Chicago. Abstract 95.Google Scholar
Kocan, KM, Blouin, EF and Barbet, AF (2000). Anaplasmosis control: past, present and future. Annals of the New York Academy of Science 916: 501–509.CrossRefGoogle ScholarPubMed
Kocan, KM, Halbur, T, Blouin, EF, Onet, V, de la Fuente, J, Garcia-Garcia, JC and Saliki, JT (2001). Immunization of cattle with Anaplasma marginale derived from tick cell culture. Veterinary Parasitology 102: 151–161.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: 4587–4593.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: 4594–4601.CrossRefGoogle ScholarPubMed
Marble, DW and Hanks, MA (1972). A tissue culture method for. Anaplasma marginale. Cornell Veterinarian 62: 196–205.Google Scholar
Mazzola, V and Kuttler, KL (1980). Anaplasma marginale in bovine erythrocyte cultures. American Journal of Veterinary Research 41: 2087–2088.Google ScholarPubMed
Mazzola, V, Amerault, TE and Roby, TO (1976). Survival of Anaplasma marginale in Aedes albopictus cells. American Journal of Veterinary Resear 37: 987–989.Google ScholarPubMed
Mazzola, V, Amerault, TE and Roby, TO (1979). Electron microscope studies of Anaplasma marginale in an Aedes albopictus culture system. American Journal of Veterinary Research 40: 1812–1815.Google Scholar
Munderloh, UG and Kurtti, TJ (1989). Formulation of medium for tick cell culture. Experimental and Applied Acarology 7: 219–229.CrossRefGoogle ScholarPubMed
Munderloh, UG, Wang, YLM, Chen, C and Kurtti, TJ (1994). Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. Journal of Parasitology 80: 533–543.Google ScholarPubMed
Munderloh, UG, Blouin, EF, Kocan, KM, Ge, NL, Edwards, W and Kurtti, TJ (1996a). Establishment of the tick (Acari: Ixodidae)-borne cattle pathogen Anaplasma marginale (Rickettsiales: Anaplasmataceae) in tick cell culture. Journal of Medical Entomology 33: 656–664.CrossRefGoogle Scholar
Munderloh, UG, Madigan, JE, Dumler, JS, Goodman, JL, Hayes, SF, Barlough, JE, Nelson, CM and Kurtti, TJ (1996b). Isolation of the equine granulocytic ehrlichiosis agent, Ehrlichia equi, in tick cell culture. Journal of Clinical Microbiology 34: 664–670.CrossRefGoogle ScholarPubMed
Munderloh, UG, Jauron, SD, Fingerle, V, Leitritz, L, Hayes, SF, Hautman, JM, Nelson, CM, Huberty, BW, Kurtti, TJ, Ahlstrand, GG, Greig, B, Mellencamp, MA and Goodman, JL (1999). Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. Journal of Clinical Microbiology 37: 2518–2524.CrossRefGoogle ScholarPubMed
Palmer, GH (1989). Anaplasmosis vaccines. In: Wright, IG (editor). In Veterinary Protozoan and Hemoparasite Vaccines. Boca Raton (FL): CRC Press: pp. 1–29.Google Scholar
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: 1279–1285.Google Scholar
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: 631–635.CrossRefGoogle ScholarPubMed
Reynard, AM (1992). Tetracycline and chloramphenicol. In: Smith, CM and Reynard, AM (editors). In Textbook of Physiology. Philadelphia: W. B. Saunders: pp. 856–860.Google Scholar
Richey, EJ (1981). Bovine anaplasmosis. In: Howard, RJ (editor). Current Veterinary Therapy Food Animal Practice Philadelphia: W. B. Saunders: pp. 767–772.Google Scholar
Ristic, M (1968). Anaplasmosis. In: Weinman, D and Ristic, M (editors). Infectious Blood Diseases of Man and Animals. New York: Academic Press: pp. 478–542.Google Scholar
Saffer, LD and Schwartzman, JD (1991). A soluble phospholipase of Toxoplasma gondii associated with host cell penetration. Journal of Protozoology 38: 454–460.Google ScholarPubMed
Saliki, JT, Blouin, EF, Rodgers, SJ and Kocan, KM (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 Sciences 849: 273–281.CrossRefGoogle Scholar
Samish, M, Pipano, E and Hana, G (1988). Cultivation of Anaplasma marginale from cattle in a Dermacentor cell line. American Journal of Veterinary Research 49: 254–256.Google Scholar
Sauer, JR, McSwain, JL, Bowman, AS and Essenberg, RC (1995). Tick salivary gland physiology. Annual Review of Entomology 40: 245–267.CrossRefGoogle ScholarPubMed
Smith, R, Levy, MG, Kuhlenschmidt, MS, Adams, JH, Rzechula, DG, Hardt, TA and Kocan, KM (1986). Isolate of Anaplasma marginale not transmitted by ticks. American Journal of Veterinary Research 47: 127–129.Google Scholar
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: 45–53.CrossRefGoogle ScholarPubMed
Wickwire, KB, Kocan, KM, Barron, SJ, Ewing, SA, Smith, RD and Hair, JA (1987). Infectivity of three Anaplasma marginale isolates for Dermacentor andersoni. American Journal of Veterinary Research 48: 96–99.Google ScholarPubMed
Walker, DH, Firth, WT, Ballard, JG and Hegarty, BC (1983). Role of phospholipase-associated penetration mechanism in cell injury by Rickettsia rickettsii. Infection and Immunity 40: 840–842.CrossRefGoogle ScholarPubMed