Differential expression and glycosylation of Anaplasma phagocytophilum major surface protein 2 paralogs during cultivation in sialyl Lewis x-deficient host cells

Infection and Immunity

Volumn 77, Issue 5, 2009, Pages 1746-1756

  Troese, Matthew J ^a   Sarkar, Madhubanti ^b,d   Galloway, Nathan L ^a   Thomas, Rachael J ^a   Kearns, Sarah A ^b   Reneer, Dexter V ^b   Yang, Tian ^c   Carlyon, Jason A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c Paul Laurence Dunbar High School   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; MAJOR SURFACE PROTEIN 2; MEMBRANE PROTEIN; PADGEM PROTEIN; SIALYL LEWIS X ANTIGEN; UNCLASSIFIED DRUG; 5 ACETYLNEURAMINYL (2 3) GALACTOSYL (1 4) (FUCOPYRANOSYL (1 3)) N ACETYLGLUCOSAMINE; 5-ACETYLNEURAMINYL-(2-3)-GALACTOSYL-(1-4)-(FUCOPYRANOSYL-(1-3))-N-ACETYLGLUCOSAMINE; MSP2 PROTEIN, ANAPLASMA PHAGOCYTOPHILUM; OLIGOSACCHARIDE; OUTER MEMBRANE PROTEIN; PROTEOME;

ANAPLASMA PHAGOCYTOPHILUM; ARTICLE; CARBOHYDRATE ANALYSIS; CELL STRAIN HL 60; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; HOST CELL; HUMAN; HUMAN CELL; HUMAN GRANULOCYTIC ANAPLASMOSIS; ISOELECTRIC POINT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BIOSYNTHESIS; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; GENE EXPRESSION PROFILING; GLYCOSYLATION; ISOLATION AND PURIFICATION; MICROBIOLOGY; NEUTROPHIL; PHYSIOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANAPLASMA PHAGOCYTOPHILUM; BACTERIAL OUTER MEMBRANE PROTEINS; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; GLYCOSYLATION; HUMANS; NEUTROPHILS; OLIGOSACCHARIDES; PROTEOME;

EID: 65449156907     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01530-08     Document Type: Article

References (47)

1. Barbet, A. F., J. T. Agnes, A. L. Moreland, A. M. Lundgren, A. R. Alleman, S. M. Noh, K. A. Brayton, U. G. Munderloh, and G. H. Palmer. 2005. Identification of functional promoters in the msp2 expression loci of Anaplasma marginale and Anaplasma phagocytophilum. Gene 353:89-97.
2. Barbet, A. F., A. M. Lundgren, A. R. Alleman, S. Stuen, A. Bjoersdorff, R. N. Brown, N. L. Drazenovich, and J. E. Foley. 2006. Structure of the expression site reveals global diversity in MSP2 (P44) variants in Anaplasma phagocytophilum. Infect. Immun. 74:6429-6437.
3. Barbet, A. F., P. F. Meeus, M. Belanger, M. V. Bowie, J. Yi, A. M. Lundgren, A. R. Alleman, S. J. Wong, F. K. Chu, U. G. Munderloh, and S. D. Jauron. 2003. Expression of multiple outer membrane protein sequence variants from a single genomic locus of Anaplasma phagocytophilum. Infect. Immun. 71:1706-1718.
4. Benz, I., and M. A. Schmidt. 2002. Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol. 45:267-276.
5. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
6. Carlyon, J. A., M. Akkoyunlu, L. Xia, T. Yago, T. Wang, R. D. Cummings, R. P. McEver, and E. Fikrig. 2003. Murine neutrophils require alpha-1,3- fucosylation but not PSGL-1 for productive infection with Anaplasma phagocytophilum. Blood 102:3387-3395.
7. Carlyon, J. A., W. T. Chan, J. Galan, D. Roos, and E. Fikrig. 2002. Repression of rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. J. Immunol. 169:7009-7018. (Pubitemid 36903245)
8. Dautin, N., and H. D. Bernstein. 2007. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61:89-112. (Pubitemid 350058201)
9. Dumler, J. S., K. S. Choi, J. C. Garcia-Garcia, N. S. Barat, D. G. Scorpio, J. W. Garyu, D. J. Grab, and J. S. Bakken. 2005. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg. Infect. Dis. 11:1828-1834. (Pubitemid 43361465)
10. Garcia-Garcia, J. C., J. de la Fuente, G. Bell-Eunice, E. F. Blouin, and K. M. Kocan. 2004. Glycosylation of Anaplasma marginale major surface protein 1a and its putative role in adhesion to tick cells. Infect. Immun. 72:3022-3030.
11. Girard, V., and M. Mourez. 2006. Adhesion mediated by autotransporters of Gram-negative bacteria: structural and functional features. Res. Microbiol. 157:407-416.
12. Goodman, J. L. 2005. Human granulocytic anaplasmosis, p. 218-238. In J. L. Goodman, D. T. Dennis, and D. E. Sonenshine (ed.), Tick-borne diseases of humans. ASM Press, Washington, DC.
13. Goodman, J. L., C. M. Nelson, M. B. Klein, S. F. Hayes, and B. W. Weston. 1999. Leukocyte infection by the granulocytic ehrlichiosis agent is linked to expression of a selectin ligand. J. Clin. Investig. 103:407-412. (Pubitemid 29069991)
14. Henderson, I. R., and A. C. Lam. 2001. Polymorphic proteins of Chlamydia spp. - autotransporters beyond the Proteobacteria. Trends Microbiol. 9:573-578.
15. Herron, M. J., M. E. Ericson, T. J. Kurtti, and U. G. Munderloh. 2005. The interactions of Anaplasma phagocytophilum, endothelial cells, and human neutrophils. Ann. N. Y. Acad. Sci. 1063:374-382.
16. Herron, M. J., C. M. Nelson, J. Larson, K. R. Snapp, G. S. Kansas, and J. L. Goodman. 2000. Intracellular parasitism by the human granulocytic ehrlichiosis bacterium through the P-selectin ligand, PSGL-1. Science 288:1653-1656. (Pubitemid 30387433)
17. Hotopp, J. C., M. Lin, R. Madupu, J. Crabtree, S. V. Angiuoli, J. Eisen, R. Seshadri, Q. Ren, M. Wu, T. R. Utterback, S. Smith, M. Lewis, H. Khouri, C. Zhang, H. Niu, Q. Lin, N. Ohashi, N. Zhi, W. Nelson, L. M. Brinkac, R. J. Dodson, M. J. Rosovitz, J. Sundaram, S. C. Daugherty, T. Davidsen, A. S. Durkin, M. Gwinn, D. H. Haft, J. D. Selengut, S. A. Sullivan, N. Zafar, L. Zhou, F. Benahmed, H. Forberger, R. Halpin, S. Mulligan, J. Robinson, O. White, Y. Rikihisa, and H. Tettelin. 2006. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet. 2:e21.
18. Huang, H., X. Wang, T. Kikuchi, Y. Kumagai, and Y. Rikihisa. 2007. Porin activity of Anaplasma phagocytophilum outer membrane fraction and purified P44. J. Bacteriol. 189:1998-2006.
19. Ijdo, J. W., W. Sun, Y. Zhang, L. A. Magnarelli, and E. Fikrig. 1998. Cloning of the gene encoding the 44-kilodalton antigen of the agent of human granulocytic ehrlichiosis and characterization of the humoral response. Infect. Immun. 66:3264-3269. (Pubitemid 28303125)
20. Ijdo, J. W., C. Wu, S. R. Telford III, and E. Fikrig. 2002. Differential expression of the p44 gene family in the agent of human granulocytic ehrlichiosis. Infect. Immun. 70:5295-5298.
21. Jauron, S. D., C. M. Nelson, V. Fingerle, M. D. Ravyn, J. L. Goodman, R. C. Johnson, R. Lobentanzer, B. Wilske, and U. G. Munderloh. 2001. Host cell-specific expression of a p44 epitope by the human granulocytic ehrlichiosis agent. J. Infect. Dis. 184:1445-1450. (Pubitemid 33108859)
22. Julenius, K., A. Molgaard, R. Gupta, and S. Brunak. 2005. Prediction, conservation analysis, and structural characterization of mammalian mucintype O-glycosylation sites. Glycobiology 15:153-164.
23. Li, S., B. Liu, R. Zeng, Y. Cai, and Y. Li. 2006. Predicting O-glycosylation sites in mammalian proteins by using SVMs. Comput. Biol. Chem. 30:203-208.
24. Lin, Q., and Y. Rikihisa. 2005. Establishment of cloned Anaplasma phagocytophilum and analysis of p44 gene conversion within an infected horse and infected SCID mice. Infect. Immun. 73:5106-5114.
25. Lin, Q., Y. Rikihisa, N. Ohashi, and N. Zhi. 2003. Mechanisms of variable p44 expression by Anaplasma phagocytophilum. Infect. Immun. 71:5650-5661.
26. Lin, Q., C. Zhang, and Y. Rikihisa. 2006. Analysis of involvement of the RecF pathway in p44 recombination in Anaplasma phagocytophilum and in Escherichia coli by using a plasmid carrying the p44 expression and p44 donor loci. Infect. Immun. 74:2052-2062.
27. Lin, Q., N. Zhi, N. Ohashi, H. W. Horowitz, M. E. Aguero-Rosenfeld, J. Raffalli, G. P. Wormser, and Y. Rikihisa. 2002. Analysis of sequences and loci of p44 homologs expressed by Anaplasma phagocytophila in acutely infected patients. J. Clin. Microbiol. 40:2981-2988.
28. McBride, J. W., C. K. Doyle, X. Zhang, A. M. Cardenas, V. L. Popov, K. A. Nethery, and M. E. Woods. 2007. Identification of a glycosylated Ehrlichia canis 19-kilodalton major immunoreactive protein with a species-specific serine-rich glycopeptide epitope. Infect. Immun. 75:74-82.
29. McBride, J. W., X. J. Yu, and D. H. Walker. 2000. Glycosylation of homologous immunodominant proteins of Ehrlichia chaffeensis and Ehrlichia canis. Infect. Immun. 68:13-18. (Pubitemid 30016671)
30. McEver, R. P. 2004. Interactions of selectins with PSGL-1 and other ligands. Ernst Schering Res. Found. Workshop 44:137-147.
31. Murphy, C. I., J. R. Storey, J. Recchia, L. A. Doros-Richert, C. Gingrich- Baker, K. Munroe, J. S. Bakken, R. T. Coughlin, and G. A. Beltz. 1998. Major antigenic proteins of the agent of human granulocytic ehrlichiosis are encoded by members of a multigene family. Infect. Immun. 66:3711-3718. (Pubitemid 28347828)
32. Park, J., K. S. Choi, and J. S. Dumler. 2003. Major surface protein 2 of Anaplasma phagocytophilum facilitates adherence to granulocytes. Infect. Immun. 71:4018-4025.
33. Park, J., K. J. Kim, D. J. Grab, and J. S. Dumler. 2003. Anaplasma phagocytophilum major surface protein-2 (Msp2) forms multimeric complexes in the bacterial membrane. FEMS Microbiol. Lett. 227:243-247. (Pubitemid 37329883)
34. Reneer, D. V., S. A. Kearns, T. Yago, J. Sims, R. D. Cummings, R. P. McEver, and J. A. Carlyon. 2006. Characterization of a sialic acid- and P-selectin glycoprotein ligand-1-independent adhesin activity in the granulocytotropic bacterium Anaplasma phagocytophilum. Cell. Microbiol. 8:1972-1984. (Pubitemid 44687334)
35. Reneer, D. V., M. J. Troese, B. Huang, S. A. Kearns, and J. A. Carlyon. 2008. Anaplasma phagocytophilum PSGL-1-independent infection does not require Syk and leads to less efficient AnkA delivery. Cell. Microbiol. 10:1827-1838.
36. Santoni, V., S. Kieffer, D. Desclaux, F. Masson, and T. Rabilloud. 2000. Membrane proteomics: use of additive main effects with multiplicative interaction model to classify plasma membrane proteins according to their solubility and electrophoretic properties. Electrophoresis 21:3329-3344.
37. Sarkar, M., D. V. Reneer, and J. A. Carlyon. 2007. Sialyl-Lewis x-independent infection of human myeloid cells by Anaplasma phagocytophilum strains HZ and HGE1. Infect. Immun. 75:5720-5725.
38. Sarkar, M., M. J. Troese, S. A. Kearns, T. Yang, D. V. Reneer, and J. A. Carlyon. 2008. Anaplasma phagocytophilum MSP2(P44)-18 predominates and is modified into multiple isoforms in human myeloid cells. Infect. Immun. 76:2090-2098.
39. Schmidt, M. A., L. W. Riley, and I. Benz. 2003. Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol. 11:554-561.
40. Scorpio, D. G., K. Caspersen, H. Ogata, J. Park, and J. S. Dumler. 2004. Restricted changes in major surface protein-2 (msp2) transcription after prolonged in vitro passage of Anaplasma phagocytophilum. BMC Microbiol. 4:1.
41. Singu, V., H. Liu, C. Cheng, and R. R. Ganta. 2005. Ehrlichia chaffeensis expresses macrophage- and tick cell-specific 28-kilodalton outer membrane proteins. Infect. Immun. 73:79-87.
42. Singu, V., L. Peddireddi, K. R. Sirigireddy, C. Cheng, U. Munderloh, and R. R. Ganta. 2006. Unique macrophage and tick cell-specific protein expression from the p28/p30-outer membrane protein multigene locus in Ehrlichia chaffeensis and Ehrlichia canis. Cell. Microbiol. 8:1475-1487. (Pubitemid 44201583)
43. Wang, X., T. Kikuchi, and Y. Rikihisa. 2006. Two monoclonal antibodies with defined epitopes of P44 major surface proteins neutralize Anaplasma phagocytophilum by distinct mechanisms. Infect. Immun. 74:1873-1882.
44. Yago, T., A. Leppanen, J. A. Carlyon, M. Akkoyunlu, S. Karmakar, E. Fikrig, R. D. Cummings, and R. P. McEver. 2003. Structurally distinct requirements for binding of P-selectin glycoprotein ligand-1 and sialyl Lewis x to Anaplasma phagocytophilum and P-selectin. J. Biol. Chem. 278:37987-37997. (Pubitemid 37175329)
45. Zhi, N., N. Ohashi, and Y. Rikihisa. 1999. Multiple p44 genes encoding major outer membrane proteins are expressed in the human granulocytic ehrlichiosis agent. J. Biol. Chem. 274:17828-17836. (Pubitemid 129519141)
46. Zhi, N., N. Ohashi, T. Tajima, J. Mott, R. W. Stich, D. Grover, S. R. Telford III, Q. Lin, and Y. Rikihisa. 2002. Transcript heterogeneity of the p44 multigene family in a human granulocytic ehrlichiosis agent transmitted by ticks. Infect. Immun. 70:1175-1184. (Pubitemid 34163389)
47. Zhi, N., Y. Rikihisa, H. Y. Kim, G. P. Wormser, and H. W. Horowitz. 1997. Comparison of major antigenic proteins of six strains of the human granulocytic ehrlichiosis agent by Western immunoblot analysis. J. Clin. Microbiol. 35:2606-2611. (Pubitemid 27402669)