A Plasmodium gene family encoding maurer's cleft membrane proteins: Structural properties and expression profiling

Genome Research

Volumn 14, Issue 6, 2004, Pages 1052-1059

  Sam Yellowe, Tobili Y ^a   Florence, Laurence ^f   Johnson, Jeffrey R ^b   Wang, Tongmin ^a   Drazba, Judith A ^e   Le Roch, Karine G ^b   Zhou, Yingyao ^c   Batalov, Serge ^c   Carucci, Daniel J ^d   Winzeler, Elizabeth A ^b,c   Yates III, John R ^b  

^a CLEVELAND STATE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Genomic Institute of the Novetis Foundation   (United States)

^d NAVAL MEDICAL RESEARCH CENTER   (United States)

^e LERNER RESEARCH INSTITUTE   (United States)

^f STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CELL INVASION; CELL MEMBRANE; CONTROLLED STUDY; ERYTHROCYTE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HOST CELL; IMMUNOPRECIPITATION; LIFE CYCLE; MULTIGENE FAMILY; NONHUMAN; ORTHOLOGY; PLASMODIUM; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTEOMICS; SEQUENCE HOMOLOGY; TROPHOZOITE;

PLASMODIUM; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII; PLASMODIUM YOELII YOELII;

EID: 3042516019     PISSN: 10889051     EISSN: None     Source Type: Journal    
DOI: 10.1101/gr.2126104     Document Type: Article

References (41)

1. Adisa, A., Albano, F.R., Reeder, J., Foley, M., and Tilley, L. 2001. Evidence for a role for a Plasmodium falciparum homologue of Sec31p in the export of proteins to the surface of malaria parasite-infected erythrocytes. J. Cell. Sci. 114: 3377-3386.
2. Albano, F.R., Berman, A., La Greca, N., Hibbs, A.R., Wickham, M., Foley, M., and Tilley, L. 1999. A homologue of Sar1p localises to a novel trafficking pathway in malaria-infected erythrocytes. Eur. J. Cell. Biol. 78: 453-462.
3. Bahl, A., Brunk, B., Coppel, R.L., Crabtree, J., Diskin, S.J., Fraunholz, M.J., Grant, G.R., Gupta, D., Huestis, R.L., Kissinger, J.C., et al. 2002. PlasmoDB: The Plasmodium genome resource. An integrated database providing tools for accessing, analyzing and mapping expression and sequence data (both finished and unfinished). Nucleic Acids Res. 30: 87-90.
4. Barnwell, J.W. 1990. Vesicle-mediated transport of membrane and proteins in malaria-infected erythrocytes. Blood Cells 16: 379-395.
5. Beeson, J.G. and Brown, G.V. 2002. Pathogenesis of Plasmodium falciparum malaria: The roles of parasite adhesion and antigenic variation. Cell. Mol. Life Sci. 59: 258-271.
6. Birago, C., Albanesi, V., Silvestrini, F., Picci, L., Pizzi, E., Alano, P., Pace, T., and Ponzi, M. 2003. A gene-family encoding small exported proteins is conserved across Plasmodium genus. Mol. Biochem. Parasitol. 126: 209-218.
7. Bright, J.N., Shrivastava, I.H., Cordes, F.S., and Sansom, M.S. 2002. Conformational dynamics of helix S6 from Shaker potassium channel: Simulation studies. Biopolymers 64: 303-313.
8. Carlton, J.M., Angiuoli, S.V., Suh, B.B., Kooij, T.W., Pertea, M., Silva, J.C., Ermolaeva, M.D., Allen, J.E., Selengut, J.D., Koo, H.L., et al. 2002. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419: 512-519.
9. Cheng, Q., Cloonan, N., Fischer, K., Thompson, J., Waine, G., Lanzer, M., and Saul, A. 1998. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol. 97: 161-176.
10. Craig, A. and Scherf, A. 2001. Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol. Biochem. Parasitol. 115: 129-143.
11. Eng, J.K., McCormack, A.L., and Yates III, J.R. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5: 976-989.
12. Fernandez, L.M. and Puett, D. 1996. Identification of amino acid residues in transmembrane helices VI and VII of the lutropin/choriogonadotropin receptor involved in signaling. Biochemistry 35: 3986-3993.
13. Florens, L., Washburn, M.P., Raine, J.D., Anthony, R.M., Grainger, M., Haynes, J.D., Moch, J.K., Muster, N., Sacci, J.B., Tabb, D.L., et al. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520-526.
14. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J.M., Pain, A., Nelson, K.E., Bowman, S., et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
15. Haldar, K. 1998. Intracellular trafficking in Plasmodium-infected erythrocytes. Curr. Opin. Microbiol. 1: 466-471.
16. Heddini, A., Pettersson, F., Kai, O., Shafi, J., Obiero, J., Chen, Q., Barragan, A., Wahlgren, M., and Marsh, K. 2001. Fresh isolates from children with severe Plasmodium falciparum malaria bind to multiple receptors. Infect. Immun. 69: 5849-5856.
17. Hinterberg, K., Scherf, A., Gysin, J., Toyoshima, T., Aikawa, M., Mazie, J.C., da Silva, L.P., and Mattei, D. 1994. Plasmodium falciparum: The Pf332 antigen is secreted from the parasite by a brefeldin A-dependent pathway and is translocated to the erythrocyte membrane via the Maurer's clefts. Exp. Parasitol. 79: 279-291.
18. Janssen, C.S., Barrett, M.P., Turner, C.M., and Phillips, R.S. 2002. A large gene family for putative variant antigens shared by human and rodent malaria parasites. Proc. R. Soc. London B Biol. Sci. 269: 431-436.
19. Kaviratne, M., Khan, S.M., Jarra, W., and Preiser, P.R. 2002. Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryot. Cell 1: 926-935.
20. Kilejian, A. 1980. Stage-specific proteins and glycoproteins of Plasmodium falciparum: Identification of antigens unique to schizonts and merozoites. Proc. Natl. Acad. Sci. 77: 3695-3699.
21. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. 2001. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305: 567-580.
22. Kyes, S.A., Rowe, J.A., Kriek, N., and Newbold, C.I. 1999. Rifins: A second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc. Natl. Acad. Sci. 96: 9333-9338.
23. Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., De la Vega, P., Holder, A.A., Batalov, S., Carucci, D.J., et al. 2003a. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 108: 7025.
24. Lopez-Estrano, C., Bhattacharjee, S., Harrison, T., and Haldar, K. 2003. Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum-infected erythrocytes. Proc. Natl. Acad. Sci. 100: 12402-12407.
25. Miller, L.H., Baruch, D.I., Marsh, K., and Doumbo, O.K. 2002. The pathogenic basis of malaria. Nature 415: 673-679.
26. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10: 1-6.
27. Pouvelle, B., Gormley, J.A., and Taraschi, T.F. 1994. Characterization of trafficking pathways and membrane genesis in malaria-infected erythrocytes. Mol. Biochem. Parasitol. 66: 83-96.
28. Przyborski, J.M., Wickert, H., Krohne, G., and Lanzer, M. 2003. Maurer's clefts - A novel secretory organelle? Mol. Biochem. Parasitol. 132: 17-26.
29. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A., and Barrell, B. 2000. Artemis: Sequence visualization and annotation. Bioinformatics 16: 944-945.
30. Sadygov, R.G. and Yates III, J.R. 2003. A hypergeometric probability model for protein identification and validation using tandem mass spectral data and protein sequence. Analyt. Chem. 75: 3792-3798.
31. Sam-Yellowe, T.Y., Fujioka, H., Aikawa, M., Hall, T., and Drazba, J.A. 2001. A Plasmodium falciparum protein located in Maurer's clefts underneath knobs and protein localization in association with Rhop-3 and SERA in the intracellular network of infected erythrocytes. Parasitol. Res. 87: 173-185.
32. Sansom, M.S. 1992. Proline residues in transmembrane helices of channel and transport proteins: A molecular modelling study. Protein Eng. 5: 53-60.
33. Sansom, M.S. and Weinstein, H. 2000. Hinges, swivels and switches: The role of prolines in signalling via transmembrane α-helices. Trends Pharmacol. Sci. 21: 445-451.
34. Spielmann, T., Fergusen, D.J., and Beck, H.P. 2003. etramps, a new Plasmodium falciparum gene family coding for developmentally regulated and highly charged membrane proteins located at the parasite-host cell interface. Mol. Biol. Cell 14: 1529-1544.
35. Tabb, D.L., McDonald, W.H., and Yates III, J.R. 2002. DTASelect and contrast: Tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1: 21-26.
36. Tamori, Y., Hashiramoto, M., Clark, A.E., Mori, H., Muranka, A., Kadowaki, T., Holman, G.D., and Kasuga, M. 1994. Substitution at Pro385 of GLUT1 perturbs the glucose transport function by reducing conformational flexibility. J. Biol. Chem. 269: 2982-2986.
37. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
38. Udeinya, I.J., Schmidt, J.A., Aikawa, M., Miller, L.H., and Green, I. 1981. Falciparum malaria-infected erythrocytes specifically bind to cultured human endothelial cells. Science 213: 555-557.
39. Washburn, M.P., Wolters, D., and Yates III, J.R. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19: 242-247.
40. Wickert, H., Rohrbach, P., Scherer, S.J., Krohne, G., and Lanzer, M. 2003a. A putative Sec23 homologue of Plasmodium falciparum is located in Maurer's clefts. Mol. Biochem. Parasitol. 129: 209-213.
41. Wickert, H., Wissing, F., Andrews, K.T., Stich, A., Krohne, G., and Lanzer, M. 2003b. Evidence for trafficking of PfEMP1 to the surface of P. falciparum-infected erythrocytes via a complex membrane network. Eur. J. Cell. Biol. 82: 271-284.