Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-18T16:33:34.082Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolution and function of tandem repeats in the major surface protein 1a of the ehrlichial pathogen Anaplasma marginale

Published online by Cambridge University Press:  28 February 2007

José de la Fuente ,
Jose C. Garcia-Garcia ,
Edmour F. Blouin ,
Sergio D. Rodríguez ,
Migel A. García  and
Katherine M. Kocan
José de la Fuente*
Affiliation:
Department of Veterinary Pathobiology, College of Veterinary Medicine Oklahoma State University, Stillwater, OK, 74078, USA
Jose C. Garcia-Garcia
Affiliation:
Department of Veterinary Pathobiology, College of Veterinary Medicine Oklahoma State University, Stillwater, OK, 74078, USA
Edmour F. Blouin
Affiliation:
Department of Veterinary Pathobiology, College of Veterinary Medicine Oklahoma State University, Stillwater, OK, 74078, USA
Sergio D. Rodríguez
Affiliation:
CENID-Parasitología Veterinaria, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, SAGARPA, Ado., CIVAC 62550, Jiutepec, Morelos, Postal 206, Mexico
Migel A. García
Affiliation:
CENID-Parasitología Veterinaria, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, SAGARPA, Ado., CIVAC 62550, Jiutepec, Morelos, Postal 206, Mexico
Katherine M. Kocan
Affiliation:
Department of Veterinary Pathobiology, College of Veterinary Medicine Oklahoma State University, Stillwater, OK, 74078, USA
*
*E-mail: jose_delafuente@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The major surface protein (MSP) 1a of the ehrlichial cattle pathogen Anaplasma marginale, encoded by the single-copy gene msp1α, has been shown to have a neutralization-sensitive epitope and to be an adhesin for bovine erythrocytes and tick cells. msp1α has been found to be a stable genetic marker for the identification of geographic isolates of A. marginale throughout development in acutely and persistently infected cattle and in ticks. The molecular weight of MSP1a varies among geographic isolates of A. marginale because of a varying number of tandemly repeated peptides of 28–29 amino acids. Variation in the sequence of the tandem repeats occurs within and among isolates, and may have resulted from evolutionary pressures exerted by ligand–receptor and host–parasite interactions. These repeated sequences include markers for tick transmissibility that may be important in the identification of ehrlichial pathogens because they may influence control strategies and the design of subunit vaccines.

Type
Research Article
Information
Animal Health Research Reviews , Volume 2 , Issue 2 , December 2001 , pp. 163 - 174
Copyright
Copyright © CAB International 2001

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 AM 105L. Infection and Immunity 55: 2428–2435.Google Scholar
Barbet, AF, Lundgren, A, Yi, J, Rurangirwa, FR and Palmer, GH (2000). Antigenic variation of Anaplasma marginale by expression of MSP2 mosaics. Infection and Immunity 68: 6133–6138.Google Scholar
Barbet, AF, Jooyoung, Yi, Lundgren, A, McEwen, BR, Blouin, EF and Kocan, KM (2001). Antigenic variation of Anaplasma marginale: MSP2 diversity during cyclic transmission between ticks and cattle. Infection and Immunity 69: 3057–3066.CrossRefGoogle ScholarPubMed
Bell-Sakyi, L, 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
Bowie, MV, de la Fuente, J, Kocan, KM, Blouin, EF and Barbet, AF (2001). Conservation of major surface protein 1 genes of the ehrlichial pathogen Anaplasma marginale during cyclic transmission between ticks and cattle. Gene. In press.Google Scholar
Brayton, KA, Knowles, DP, McGuire, TC and Palmer GH. (2001). Efficient use of a small genome to generate antigenic diversity in tick-borne ehrlichial pathogens. Proceedings of the National Academy of Sciences of the United States of America 98: 4130–4135.Google Scholar
Camacho-Nuez, M, de Lourdes Munoz, M, Suarez, CE, McGuire, TC, Brown, WC and Palmer, GH (2000). Expression of polymorphic msp1beta genes during acute Anaplasma marginale rickettsemia. Infection and Immunity 68: 1946–1952.CrossRefGoogle ScholarPubMed
Dayhoff, MO, Schwartz, RM and Orcutt, BC (1978). A model of evolutionary change in proteins. In: Dayhoff, MO, ed., Atlas of Protein Sequence and Structure, Vol. 5, Supplement 3. Washington, DC: National Biomedical Research Foundation, pp. 363–373.Google Scholar
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: 5151–5156.CrossRefGoogle ScholarPubMed
de la Fuente, J, Rodríguez, M, Redondo, M, García-García, JC, Méndez, L, Serrano, E, Valdés, M, Enriquez, A, Calnales, M, Ramos, E, de Armas, CA, Rey, S, Rodríguez, JL, Artiles, M and García L (1998). Field studies and cost-effectiveness analysis of vaccination with GavacTM against the cattle tick Boophilus microplus . Vaccine 16: 366–373.CrossRefGoogle Scholar
de la Fuente, J, Hidalgo, Y, Ochagavia, ME, Muzio, V and Rodríguez MP (1999). Analysis of enterovirus sequences recovered from the cerebrospinal fluid of patients with epidemic neuropathy. Annals of Tropical Medicine and Parasitology 93: 153–161.Google Scholar
de la Fuente, J, Garcia-Garcia, JC, Blouin, EF and Kocan, KM (2001 a). 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, Van Den Bussche, RA and Kocan, KM (2001 b). Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Veterinary Parasitology 97: 65–76.CrossRefGoogle ScholarPubMed
Dikmans, G (1950). The transmission of anaplasmosis. American Journal of Veterinary Research 11: 5–16.Google Scholar
Ewing, SA (1981). Transmission of Anaplasma marginale by arthropods. In: Proceedings of the 7th National Anaplasmosis ConferenceMississippi State UniversityMS, USA, 395–423.Google Scholar
French, DM, Brown, WC and Palmer, GH (1998). Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infection and Immunity 67: 5834–5840.CrossRefGoogle Scholar
García Ortiz, MA, Angeles Ojeda, LE, Hernández Salgado, G, García Tapia, D, Aboytes Torres, R and Rodríguez Camarillo, SD (1998). Caracterización de la virulencia de un aislado mexicano de Anaplasma marginale . Tecnica Pecuaria en Mexico 36: 197–202.Google Scholar
García Ortiz, MA, Aboytes Torres, R, Hernández Salgado, G, Cantó Alarcón, JG and Rodríguez, SD (2000). Anaplasma marginale: diferentes grados de virulencia en dos aislados mexicanos. Veterinaria México 31: 157–160.Google Scholar
Ge, NK, Kocan, KM, Blouin, EF and Murphy, GL (1996). Developmental studies of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) infected as adults using nonradioactive in situ hybridization. Journal of Medical Entomology 33: 911–920.CrossRefGoogle ScholarPubMed
Goh, C-S, Bogan, AA, Joachimiak, M, Walther, D and Cohen, FE (2000). Co-evolution of proteins with their interaction partners. Journal of Molecular Biology 299: 283–293.Google Scholar
Guglielmone, AA (1995). Epidemiology of babesiosis and anaplasmosis in South and Central America. Veterinary Parasitology 57: 109–119.CrossRefGoogle ScholarPubMed
Hawley, DK and McClure, WR (1983). Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Research 11: 2237–2255.CrossRefGoogle ScholarPubMed
Hofmann, K and Stoffel, W (1993). TMbase–a database of membrane spanning protein segments. Biological Chemistry 347: 166.Google Scholar
Jackson, JA, Tinsley, RC and Hinkel, HH (1998). Mutual exclusion of congeneric monogenean species in a space-limited habitat. Parasitology 117: 563–569.Google Scholar
Kneller, DG, Cohen, FE and Langridge, R (1990). Improvements in protein secondary structure prediction by an enhanced neural network. Journal of Molecular Biology 214: 171–182.CrossRefGoogle ScholarPubMed
Kocan, KM (1986). Development of Anaplasma marginale: 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, Hair, JA, Ewing, SA and Stratton, LG (1981). Transmission of Anaplasma marginale Theiler by Dermacentor andersoni Stiles and Dermacentor variabilis (Say). American Journal of Veterinary Research 42: 15–18.Google ScholarPubMed
Kocan, KM, Stiller, D, Goff, WL, Claypool, PL, Edwards, W, Ewing, SA, McGuire, TC, Hair, JA and Barron, SJ (1992 a). Development of Anaplasma marginale in male Dermacentor andersoni transferred from infected to susceptible cattle. American Journal of Veterinary Research 53: 499–507.CrossRefGoogle ScholarPubMed
Kocan, KM, Goff, WL, Stiller, D, Claypool, PL, Edwards, W, Ewing, SA, Hair, JA and Barron, SJ (1992 b). Persistence of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) transferred successively from infected to susceptible cattle. Journal of Medical Entomology 29: 657–668.CrossRefGoogle Scholar
Kocan, KM, Munderloh, UG and Ewing, SA (1998). Development of the Ebony isolate of Ehrlichia canis in cultured Ixodes scapularis cells. In: Ellis, RP (ed.), Proceedings, 79th Conference of Research Workers in Animal Diseases, Chicago. Ames (IA): Iowa State University Press, 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
Kuttler, KL (1984). Anaplasma infections in wild and domestic ruminants: a review. Journal of Wildlife Diseases 20: 12–20.CrossRefGoogle ScholarPubMed
Kyte, J and Doolittle, RF (1982). A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157: 105–132.CrossRefGoogle ScholarPubMed
McBride, JW, Yu, X and Walker DH. (2000). A conserved, transcriptionally active p28 multigene locus of ehrlichia canis. Gene 254: 245–252.CrossRefGoogle ScholarPubMed
McClelland, JL and Rumelhart, DE (1988). Explorations in Parallel Distributed Processing, Volume 3. Cambridge (MA): MIT Press, pp. 318–362.Google Scholar
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
Munderloh, UG, Blouin, EF, Kocan, KM, Ge, NL, Edwards, WL and Kurtti, TJ (1996). 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, 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.Google Scholar
Palmer, GH (1989). Anaplasmosis vaccines. In: Wright, IG, ed. 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, Barbet, AF, Cantor, GH and McGuire, TC (1989). Immunization of cattle with the MSP-1 surface protein complex induces protection against a structurally variant Anaplasma marginale isolate. Infection and Immunity 57: 3666–3669.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: 631–635.Google Scholar
Richey, EJ (1981). Bovine anaplasmosis. In: Howard, RJ, ed. Current Veterinary Therapy: Food Animal Practice. Philadelphia: W. B. Saunders, p.767.Google Scholar
Ristic, M and Watrach, AM (1963). Anaplasmosis. VI. Studies and a hypothesis concerning the cycle of development of the causative agent. American Journal of Veterinary Research 24: 267–276.Google Scholar
Rodriguez, SD, Garcia Ortiz, MA, Hernandez Salgado, G, Santos Cerda, NA, Aboytes Torres, R and Canto Alarcon, GJ (2000). Anaplasma marginale inactivated vaccine: dose titration against a homologous challenge. Comparative Immunology and Microbiology of Infectious Diseases 23: 239–252.Google Scholar
Roux, V and Raoult, D (1995). Phylogenetic analysis of the genus Rickettsia by 16S rDNA sequencing. Research in Microbiology 146: 385–396.CrossRefGoogle ScholarPubMed
Saitou, N and Nei, M (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.Google Scholar
Shine, J and Dalgarno, L (1974). The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proceedings of the National Academy of Sciences of the United States of America 71: 1342–1346.CrossRefGoogle Scholar
Smith, RD, Levy, MG, Kuhlenschmidt, MS, Adams, JH, Rzechula, DL, Hardt, TA and Kocan, KM (1986). Isolate of Anaplasma marginale not transmitted by ticks. American Journal of Veterinary Research 47: 127–129.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.CrossRefGoogle ScholarPubMed
van Geest, M and Lolkema, JS (2000). Membrane topology and insertion of membrane proteins: search for topogenic signals. Microbiology and Molecular Biology Review 64: 13–33.CrossRefGoogle 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: 45–53.Google Scholar
Walker, DH and Dumler, JS (1996). Emergence of the ehrlichioses as human health problems. Emerging Infectious Diseases 2: 18–29.Google Scholar
Welling, GW, Weijer, WJ, van der Zee, R and Welling-Wester, S (1985). Prediction of sequential antigenic regions in proteins. FEBS Letters 188: 215–218.CrossRefGoogle ScholarPubMed
Wickner, WT and Lodish, HF (1985). Multiple mechanisms of protein insertion into and across membranes. Science 230: 400–407.CrossRefGoogle ScholarPubMed
Wickwire, KB, Kocan, KM, Barron, SJ, Ewing, SA and Smith, RD (1987). Infectivity of three Anaplasma marginale isolates for Dermacentor andersoni . American Journal of Veterinary Research 48: 96–99.Google Scholar
Wren, BW (2000). Microbial genome analysis: insights into virulence, host adaptation and evolution. Nature Reviews Genetics 1: 30–39.Google Scholar
Yu, X, McBride, JW, Zhang, X and Walker, DH (2000). Characterization of the complete transcriptionally active Ehrlichia chaffeensis 28 kDa outer membrane protein multigene family. Gene 248: 59–68.CrossRefGoogle ScholarPubMed