Expression of Anaplasma marginale Major Surface Protein 2 Variants during Persistent Cyclic Rickettsemia

This Article

	Full Text
	Full Text (PDF)
	An erratum has been published
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by French, D. M.
	Articles by Palmer, G. H.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by French, D. M.
	Articles by Palmer, G. H.

Previous Article | Next Article

Infect Immun, March 1998, p. 1200-1207, Vol. 66, No. 3
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Expression of Anaplasma marginale Major Surface Protein 2 Variants during Persistent Cyclic Rickettsemia

Dorothy M. French,^* Terry F. McElwain, Travis C. McGuire, and Guy H. Palmer

Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington 99164

Received 3 September 1997/Returned for modification 20 October 1997/Accepted 10 December 1997

Anaplasma marginale is an intraerythrocytic rickettsial pathogen of cattle in which infection persists for the life of theanimal. Persistent A. marginale infection is characterized byrepetitive rickettsemic cycles which we hypothesize reflect emergenceof A. marginale antigenic variants. In this study, we determinedwhether variants of major surface protein 2 (MSP-2), a targetof protective immunity encoded by a polymorphic multigene family,arise during persistent rickettsemia. By using a quantitativecompetitive PCR to identify rickettsemic cycles, msp-2 transcriptsexpressed in vivo were isolated from peak rickettsemia of sequentialcycles. Cloning and sequencing of msp-2 cDNA revealed that geneticvariants of MSP-2 emerge representing a minimum of four geneticvariant types in each cycle during persistent infection. Two-colorimmunofluorescence using variant-specific antibody showed thatemergence of MSP-2 variants resulted in expression of a minimumof three antigenic types of MSP-2 within one rickettsemic cycle.Therefore immune control of each cycle would require responsesto an antigenically diverse A. marginale population. These findingsdemonstrate that polymorphic MSP-2 variants emerge during cyclicrickettsemia in persistent A. marginale infection and suggestthat emergent variants play an important role in persistence.

^* Corresponding author. Mailing address: Department of Veterinary Microbiology and Pathology, Washington State University, Pullman,WA 99164-7040. Phone: (509) 335-6030. Fax: (509) 335-8529. E-mail:dmf{at}vetmed.wsu.edu.

This article has been cited by other articles:

Futse, J. E., Brayton, K. A., Dark, M. J., Knowles, D. P. Jr., Palmer, G. H. (2008). Superinfection as a driver of genomic diversification in antigenically variant pathogens. Proc. Natl. Acad. Sci. USA 105: 2123-2127 [Abstract] [Full Text]
Granquist, E. G., Stuen, S., Lundgren, A. M., Braten, M., Barbet, A. F. (2008). Outer Membrane Protein Sequence Variation in Lambs Experimentally Infected with Anaplasma phagocytophilum. Infect. Immun. 76: 120-126 [Abstract] [Full Text]
delos Santos, J. R. C., Boughan, K., Bremer, W. G., Rizzo, B., Schaefer, J. J., Rikihisa, Y., Needham, G. R., Capitini, L. A., Anderson, D. E., Oglesbee, M., Ewing, S. A., Stich, R. W. (2007). Experimental infection of dairy calves with Ehrlichia chaffeensis. J Med Microbiol 56: 1660-1668 [Abstract] [Full Text]
Zhuang, Y., Futse, J. E., Brown, W. C., Brayton, K. A., Palmer, G. H. (2007). Maintenance of Antibody to Pathogen Epitopes Generated by Segmental Gene Conversion Is Highly Dynamic during Long-Term Persistent Infection. Infect. Immun. 75: 5185-5190 [Abstract] [Full Text]
Palmer, G. H., Futse, J. E., Leverich, C. K., Knowles, D. P. Jr., Rurangirwa, F. R., Brayton, K. A. (2007). Selection for Simple Major Surface Protein 2 Variants during Anaplasma marginale Transmission to Immunologically Naive Animals. Infect. Immun. 75: 1502-1506 [Abstract] [Full Text]
Ganta, R. R., Cheng, C., Miller, E. C., McGuire, B. L., Peddireddi, L., Sirigireddy, K. R., Chapes, S. K. (2007). Differential Clearance and Immune Responses to Tick Cell-Derived versus Macrophage Culture-Derived Ehrlichia chaffeensis in Mice. Infect. Immun. 75: 135-145 [Abstract] [Full Text]
Barbet, A. F., Lundgren, A. M., Alleman, A. R., Stuen, S., Bjoersdorff, A., Brown, R. N., Drazenovich, N. L., Foley, J. E. (2006). Structure of the Expression Site Reveals Global Diversity in MSP2 (P44) Variants in Anaplasma phagocytophilum. Infect. Immun. 74: 6429-6437 [Abstract] [Full Text]
PALMER, G. H, FUTSE, J. E, KNOWLES, D. P JR, BRAYTON, K. A (2006). Insights into Mechanisms of Bacterial Antigenic Variation Derived from the Complete Genome Sequence of Anaplasma marginale. Ann. N. Y. Acad. Sci. 1078: 15-25 [Abstract] [Full Text]
Macmillan, H., Brayton, K. A., Palmer, G. H., McGuire, T. C., Munske, G., Siems, W. F., Brown, W. C. (2006). Analysis of the Anaplasma marginale Major Surface Protein 1 Complex Protein Composition by Tandem Mass Spectrometry. J. Bacteriol. 188: 4983-4991 [Abstract] [Full Text]
Noh, S. M., Brayton, K. A., Knowles, D. P., Agnes, J. T., Dark, M. J., Brown, W. C., Baszler, T. V., Palmer, G. H. (2006). Differential Expression and Sequence Conservation of the Anaplasma marginale msp2 Gene Superfamily Outer Membrane Proteins.. Infect. Immun. 74: 3471-3479 [Abstract] [Full Text]
Wang, X., Kikuchi, T., Rikihisa, Y. (2006). Two Monoclonal Antibodies with Defined Epitopes of P44 Major Surface Proteins Neutralize Anaplasma phagocytophilum by Distinct Mechanisms. Infect. Immun. 74: 1873-1882 [Abstract] [Full Text]
Abbott, J. R., Palmer, G. H., Kegerreis, K. A., Hetrick, P. F., Howard, C. J., Hope, J. C., Brown, W. C. (2005). Rapid and Long-Term Disappearance of CD4+ T Lymphocyte Responses Specific for Anaplasma Marginale Major Surface Protein-2 (MSP2) in MSP2 Vaccinates following Challenge with Live A. marginale. J. Immunol. 174: 6702-6715 [Abstract] [Full Text]
Lahmers, K. K., Norimine, J., Abrahamsen, M. S., Palmer, G. H., Brown, W. C. (2005). The CD4+ T cell immunodominant Anaplasma marginale major surface protein 2 stimulates {gamma}{delta} T cell clones that express unique T cell receptors. J. Leukoc. Biol. 77: 199-208 [Abstract] [Full Text]
Brayton, K. A., Kappmeyer, L. S., Herndon, D. R., Dark, M. J., Tibbals, D. L., Palmer, G. H., McGuire, T. C., Knowles, D. P. Jr. (2005). Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proc. Natl. Acad. Sci. USA 102: 844-849 [Abstract] [Full Text]
Wang, X., Rikihisa, Y., Lai, T.-H., Kumagai, Y., Zhi, N., Reed, S. M. (2004). Rapid Sequential Changeover of Expressed p44 Genes during the Acute Phase of Anaplasma phagocytophilum Infection in Horses. Infect. Immun. 72: 6852-6859 [Abstract] [Full Text]
Stich, R. W., Olah, G. A., Brayton, K. A., Brown, W. C., Fechheimer, M., Green-Church, K., Jittapalapong, S., Kocan, K. M., McGuire, T. C., Rurangirwa, F. R., Palmer, G. H. (2004). Identification of a Novel Anaplasma marginale Appendage-Associated Protein That Localizes with Actin Filaments during Intraerythrocytic Infection. Infect. Immun. 72: 7257-7264 [Abstract] [Full Text]
Abbott, J. R., Palmer, G. H., Howard, C. J., Hope, J. C., Brown, W. C. (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. Infect. Immun. 72: 7360-7366 [Abstract] [Full Text]
Brown, W. C., Palmer, G. H., Brayton, K. A., Meeus, P. F. M., Barbet, A. F., Kegerreis, K. A., McGuire, T. C. (2004). CD4+ T Lymphocytes from Anaplasma marginale Major Surface Protein 2 (MSP2) Vaccinees Recognize Naturally Processed Epitopes Conserved in MSP3. Infect. Immun. 72: 3688-3692 [Abstract] [Full Text]
Brayton, K. A., Meeus, P. F. M., Barbet, A. F., Palmer, G. H. (2003). Simultaneous Variation of the Immunodominant Outer Membrane Proteins, MSP2 and MSP3, during Anaplasma marginale Persistence In Vivo. Infect. Immun. 71: 6627-6632 [Abstract] [Full Text]
Kocan, K. M., de la Fuente, J., Guglielmone, A. A., Melendez, R. D. (2003). Antigens and Alternatives for Control of Anaplasma marginale Infection in Cattle. Clin. Microbiol. Rev. 16: 698-712 [Abstract] [Full Text]
Lin, Q., Rikihisa, Y., Ohashi, N., Zhi, N. (2003). Mechanisms of Variable p44 Expression by Anaplasma phagocytophilum. Infect. Immun. 71: 5650-5661 [Abstract] [Full Text]
Li, J. S.-y., Winslow, G. M. (2003). Survival, Replication, and Antibody Susceptibility of Ehrlichia chaffeensis outside of Host Cells. Infect. Immun. 71: 4229-4237 [Abstract] [Full Text]
Brown, W. C., Brayton, K. A., Styer, C. M., Palmer, G. H. (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. J. Immunol. 170: 3790-3798 [Abstract] [Full Text]
Lohr, C. V., Brayton, K. A., Shkap, V., Molad, T., Barbet, A. F., Brown, W. C., Palmer, G. H. (2002). Expression of Anaplasma marginale Major Surface Protein 2 Operon-Associated Proteins during Mammalian and Arthropod Infection. Infect. Immun. 70: 6005-6012 [Abstract] [Full Text]
Brown, W. C., McGuire, T. C., Mwangi, W., Kegerreis, K. A., Macmillan, H., Lewin, H. A., Palmer, G. H. (2002). Major Histocompatibility Complex Class II DR-Restricted Memory CD4+ T Lymphocytes Recognize Conserved Immunodominant Epitopes of Anaplasma marginale Major Surface Protein 1a. Infect. Immun. 70: 5521-5532 [Abstract] [Full Text]
IJdo, J. W., Wu, C., Telford III, S. R., Fikrig, E. (2002). Differential Expression of the p44 Gene Family in the Agent of Human Granulocytic Ehrlichiosis. Infect. Immun. 70: 5295-5298 [Abstract] [Full Text]
Lin, Q., Zhi, N., Ohashi, N., Horowitz, H. W., Aguero-Rosenfeld, M. E., Raffalli, J., Wormser, G. P., Rikihisa, Y. (2002). Analysis of Sequences and Loci of p44 Homologs Expressed by Anaplasma phagocytophila in Acutely Infected Patients. J. Clin. Microbiol. 40: 2981-2988 [Abstract] [Full Text]
Shkap, V., Molad, T., Brayton, K. A., Brown, W. C., Palmer, G. H. (2002). Expression of Major Surface Protein 2 Variants with Conserved T-Cell Epitopes in Anaplasma centrale Vaccinates. Infect. Immun. 70: 642-648 [Abstract] [Full Text]
Stich, R. W., Rikihisa, Y., Ewing, S. A., Needham, G. R., Grover, D. L., Jittapalapong, S. (2002). Detection of Ehrlichia canis in Canine Carrier Blood and in Individual Experimentally Infected Ticks with a p30-Based PCR Assay. J. Clin. Microbiol. 40: 540-546 [Abstract] [Full Text]
Unver, A., Ohashi, N., Tajima, T., Stich, R. W., Grover, D., Rikihisa, Y. (2001). Transcriptional Analysis of p30 Major Outer Membrane Multigene Family of Ehrlichia canis in Dogs, Ticks, and Cell Culture at Different Temperatures. Infect. Immun. 69: 6172-6178 [Abstract] [Full Text]
de la Fuente, J., Kocan, K. M. (2001). Expression of Anaplasma marginale Major Surface Protein 2 Variants in Persistently Infected Ticks. Infect. Immun. 69: 5151-5156 [Abstract] [Full Text]
Barbet, A. F., Yi, J., 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. Infect. Immun. 69: 3057-3066 [Abstract] [Full Text]
Liang, F. T., Bowers, L. C., Philipp, M. T. (2001). C-Terminal Invariable Domain of VlsE Is Immunodominant but Its Antigenicity Is Scarcely Conserved among Strains of Lyme Disease Spirochetes. Infect. Immun. 69: 3224-3231 [Abstract] [Full Text]
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. J. Clin. Microbiol. 39: 631-635 [Abstract] [Full Text]
Shu-yi Li, J., Yager, E., Reilly, M., Freeman, C., Reddy, G. R., Reilly, A. A., Chu, F. K., Winslow, G. M. (2001). Outer Membrane Protein-Specific Monoclonal Antibodies Protect SCID Mice from Fatal Infection by the Obligate Intracellular Bacterial Pathogen Ehrlichia chaffeensis. J. Immunol. 166: 1855-1862 [Abstract] [Full Text]
Brown, W. C., McGuire, T. C., Zhu, D., Lewin, H. A., Sosnow, J., Palmer, G. H. (2001). 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. J. Immunol. 166: 1114-1124 [Abstract] [Full Text]
Barbet, A. F., Lundgren, A., Yi, J., Rurangirwa, F. R., Palmer, G. H. (2000). Antigenic Variation of Anaplasma marginale by Expression of MSP2 Mosaics. Infect. Immun. 68: 6133-6138 [Abstract] [Full Text]
Rurangirwa, F. R., Stiller, D., Palmer, G. H. (2000). Strain Diversity in Major Surface Protein 2 Expression during Tick Transmission of Anaplasma marginale. Infect. Immun. 68: 3023-3027 [Abstract] [Full Text]
Camacho-Nuez, M., de Lourdes Munoz, M., Suarez, C. E., McGuire, T. C., Brown, W. C., Palmer, G. H. (2000). Expression of Polymorphic msp1beta Genes during Acute Anaplasma marginale Rickettsemia. Infect. Immun. 68: 1946-1952 [Abstract] [Full Text]
Tuo, W., Palmer, G. H., McGuire, T. C., Zhu, D., Brown, W. C. (2000). Interleukin-12 as an Adjuvant Promotes Immunoglobulin G and Type 1 Cytokine Recall Responses to Major Surface Protein 2 of the Ehrlichial Pathogen Anaplasma marginale. Infect. Immun. 68: 270-280 [Abstract] [Full Text]
French, D. M., Brown, W. C., Palmer, G. H. (1999). Emergence of Anaplasma marginale Antigenic Variants during Persistent Rickettsemia. Infect. Immun. 67: 5834-5840 [Abstract] [Full Text]
Ijdo, J. W., Wu, C., Magnarelli, L. A., Fikrig, E. (1999). Serodiagnosis of Human Granulocytic Ehrlichiosis by a Recombinant HGE-44-Based Enzyme-Linked Immunosorbent Assay. J. Clin. Microbiol. 37: 3540-3544 [Abstract] [Full Text]
Walls, J. J., Aguero-Rosenfeld, M., Bakken, J. S., Goodman, J. L., Hossain, D., Johnson, R. C., Dumler, J. S. (1999). Inter- and Intralaboratory Comparison of Ehrlichia equi and Human Granulocytic Ehrlichiosis (HGE) Agent Strains for Serodiagnosis of HGE by the Immunofluorescent-Antibody Test. J. Clin. Microbiol. 37: 2968-2973 [Abstract] [Full Text]
Zhi, N., Ohashi, N., Rikihisa, Y. (1999). Multiple p44 Genes Encoding Major Outer Membrane Proteins Are Expressed in the Human Granulocytic Ehrlichiosis Agent. J. Biol. Chem. 274: 17828-17836 [Abstract] [Full Text]
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. Proc. Natl. Acad. Sci. USA 96: 3171-3176 [Abstract] [Full Text]
Barbet, A. F., Blentlinger, R., Yi, J., 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. Infect. Immun. 67: 102-107 [Abstract] [Full Text]
Palmer, G. H., Abbott, J. R., French, D. M., McElwain, T. F. (1998). Persistence of Anaplasma ovis Infection and Conservation of the msp-2 and msp-3 Multigene Families within the Genus Anaplasma. Infect. Immun. 66: 6035-6039 [Abstract] [Full Text]
Brown, W. C., Shkap, V., Zhu, D., McGuire, T. C., Tuo, W., McElwain, T. F., Palmer, G. H. (1998). CD4+ T-Lymphocyte and Immunoglobulin G2 Responses in Calves Immunized with Anaplasma marginale Outer Membranes and Protected against Homologous Challenge. Infect. Immun. 66: 5406-5413 [Abstract] [Full Text]
Brown, W. C., Zhu, D., Shkap, V., McGuire, T. C., Blouin, E. F., Kocan, K. M., Palmer, G. H. (1998). 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. Infect. Immun. 66: 5414-5422 [Abstract] [Full Text]

J. Bacteriol.	J. Virol.	Eukaryot. Cell

Microbiol. Mol. Biol. Rev.	Clin. Vaccine Immunol.	All ASM Journals