Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells

EMBO Journal

Volumn 17, Issue 14, 1998, Pages 3816-3826

  Frevert, Ute ^a   Galinski, Mary R ^a   Hügel, Frank Ulrich ^a   Allon, Nahum ^b   Schreier, Hans ^b   Smulevitch, Sergey ^a   Shakibaei, Mehdi ^a   Clavijo, Pedro ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Advanced Therapies Inc   (United States)

Author keywords

Circumsporozoite protein; Immune evasion; Membrane translocation; Plasmodium; Protein synthesis

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN; RIBONUCLEASE; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; CYTOSOL; GENETIC TRANSFECTION; HOST CELL; LIVER CELL; LIVER MICROSOME; MACROPHAGE; MEMBRANE TRANSPORT; MICROSOME; NONHUMAN; PLASMODIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TRANSPORT; RIBOSOME; SPOROZOITE;

AMINO ACID SEQUENCE; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELLS, CULTURED; CHO CELLS; CONSERVED SEQUENCE; CRICETINAE; CYTOPLASM; HUMANS; LIPOSOMES; MACROPHAGES, PERITONEAL; MEMBRANE FUSION; MICROSOMES, LIVER; MOLECULAR SEQUENCE DATA; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PROTEIN BIOSYNTHESIS; PROTOZOAN PROTEINS; RATS; RATS, INBRED BN; RIBOSOMES; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0032527804     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.14.3816     Document Type: Article

References (53)

1. Barbieri, L., Battelli, M.G. and Stirpe, F. (1993) Ribosome-inactivating proteins from plants. Biochim. Biophys. Acta, 1154, 237-282.
2. Burd, C.G. and Dreyfuss, G. (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science, 265, 615-621.
3. Cerami, C., Frevert, U., Sinnis, P., Takacs, B., Clavijo, P., Santos, M.J. and Nussenzweig, V. (1992) The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell, 70, 1021-1033.
4. Cerami, C., Frevert, U., Sinnis, P., Takacs, B. and Nussenzweig, V. (1994) Rapid clearance of malaria circumsporozoite protein (CS) by hepatocytes. J. Exp. Med., 179, 695-701.
5. Chander, R. and Schreier, H. (1992) Artificial viral envelopes containing recombinant human immunodeficiency virus (HIV) gp160. Life Sci., 50, 481-488.
6. Dame, J.B. et al. (1984) Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science, 225, 593-599.
7. Danforth, H.D., Aikawa, M., Cochrane, A.H. and Nussenzweig, R.S. (1980) Sporozoites of mammalian malaria: attachment to, interiorization and fate within macrophages. J. Protozool., 27, 193-202.
8. Eichinger, D.J., Arnot, D.E., Tam, J.P., Nussenzweig, V. and Enea, V. (1986) Circumsporozoite protein of Plasmodium berghei: gene cloning and identification of the immunodominant epitopes. Mol. Cell. Biol., 6, 3965-3972.
9. Ellington, A.D., Symensma, T.L., Giver, L. and Baskerville, S. (1995) A simple code for protein:RNA interactions. Nucleic Acids Res. Symp. Ser., 33, 156-159.
10. Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B. and Nussenzweig, V. (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J. Exp. Med., 177, 1287-1298.
11. Frevert, U., Sinnis, P., Esko, J.D. and Nussenzweig, V. (1996) Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei invasion in vitro. Mol. Biochem. Parasitol., 76, 257-266.
12. Gaetani, S., Smith, J.A., Feldman, R.A. and Morimoto, T. (1983) Preparation of rough microsomes and membrane-bound polysomes that are active in protein synthesis in vitro. Methods Enzymol., 96, 3-24.
13. Garré, C., Bianchi-Scarrà, G., Sirito, M., Musso, M. and Ravazzolo, R. (1992) Lactoferrin binding sites and nuclear localization in K562 (S) cells. J. Cell. Physiol., 153, 477-482.
14. Han, S.-H., Einstein, G., Weisgraber, K.H., Strittmatter, W.J., Saunders, A.M., Pericak-Vance, M., Roses, A.D. and Schmechel, D.E. (1994) Apolipoprotein E is localized in the cytoplasm of human cortical neurons: a light and electron microscopical study. J. Neuropathol. Exp. Neurol., 53, 535-544.
15. Hartland, E.L., Green, S.P., Phillips, W.A. and Robins-Browne, R.M. (1994) Essential role of YopD in inhibition of the respiratory burst of macrophages by Yersinia enterocolitica. Infect. Immun., 62, 4445-4453.
16. He, J. and Furmanski, P. (1995) Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA. Nature, 373, 721-724.
17. Hemmerich, P., Bosbach, S., von Mikecz, A. and Krawinkel, U. (1997) Human ribosomal protein L7 binds RNA with an α-helical argininerich and lysine-rich domain. Eur. J. Biochem., 245, 549-556.
18. Hügel, F.-U., Pradel, G. and Frevert, U. (1996) The malaria circumsporozoite protein interacts with host cell ribosomes. Mol. Biochem. Parasitol., 81, 151-170.
19. Jackson, R.J. and Hunt, T. (1983) Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol., 96, 50-74.
20. Kenan, D.J., Query, C.C. and Keene, J.D. (1991) RNA recognition: towards identifying determinants of specificity. Trends Biochem. Sci., 16, 214-220.
21. Lee, C.-Z., Lin, J.-H., Chao, M., McKnight, K. and Lai, M.M.C. (1993) RNA-binding activity of hepatitis delta antigen involves two arginine-rich motifs and is required for hepatitis delta virus replication. J. Virol., 67, 2221-2227.
22. Lee, H. and Iglewski, W.J. (1984) Cellular ADP-ribosyltransferase with the same mechanism of action as diphtheria toxin and Pseudomonas toxin A. Proc. Natl Acad. Sci. USA, 81, 2703-2707.
23. Ménard, R., Sultan, A.A., Cortes, C., Altszuler, R., van Dijk, M.R., Janse, C.J., Waters, A.P., Nussenzweig, R.S. and Nussenzweig, V. (1997) Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature, 385, 336-340.
24. Munson, P.J. and Rodbard, D. (1980) LIGAND: a versatile computerized approach for characterization of ligand-binding systems. Biochemistry, 107, 220-239.
25. Nagai, K. (1996) RNA-protein complexes. Curr. Opin. Struct. Biol., 6, 53-61.
26. Nardin, E.H., Nussenzweig, V., Nussenzweig, R.S., Collins, W.E., Harinasuta, K.T., Tapchaisri, P. and Chomcharn, Y. (1982) Circumsporozoite proteins of human malaria parasites Plasmodium falciparum and Plasmodium vivax. J. Exp. Med., 156, 20-30.
27. Nussenzweig, V. and Nussenzweig, R.S. (1985) Circumsporozoite proteins of malaria parasites. Cell, 42, 401-403.
28. O'Brien, A.D., Tesh, V.L., Donhue-Rolfe, A., Jackson, M.P., Olsnes, S., Sandvig, K., Lindberg, A.A. and Keusch, G.T. (1992) Shiga toxin: biochemistry, genetics, mode of action and role in pathogenesis. Curr. Top. Microbiol. Immunol., 180, 65-94.
29. Pancake, S.J., Holt, G.D., Mellouk, S. and Hoffman, S.L. (1992) Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J. Cell Biol., 117, 1351-1357.
30. Pelham, H.R.B., Roberts, L.M. and Lord, J.M. (1992) Toxin entry: how reversible is the secretory pathway? Trends Cell Biol., 2, 183-185.
31. Persson, C., Nordfelth, R., Holmström, A., Håkansson, S., Rosqvist, R. and Wolf-Watz, H. (1995) Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol. Microbiol., 18, 135-150.
32. Rosqvist, R., Bölin, I. and Wolf-Watz, H. (1988) Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2B protein. Infect. Immun., 56, 2139-2143.
33. Rosqvist, R., Magnusson, K.-E. and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J., 13, 964-972.
34. Salmond, G.P.C. and Reeves, P.J. (1993) Membrane traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem. Sci., 18, 7-12.
35. Sandvig, K., Garred, O., Prydz, K., Kozlov, J.V., Hansen, S.H. and van Deurs, B. (1992) Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature, 358, 510-512.
36. Sanger, F., Nicklen, S. and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 84, 5463-5467.
37. Shakibaei, M. and Frevert, U. (1996) Dual interaction of the malaria circumsporozoite protein with the low density lipoprotein receptor- related protein (LRP) and cell surface heparan sulfate. J. Exp. Med., 184, 1699-1711.
38. Shin, S.C.J., Vanderberg, J.P. and Terzakis, J.A. (1982) Direct infection of hepatocytes by sporozoites of Plasmodium berghei. J. Protozool., 29, 448-454.
39. Sidjanski, S.P., Vanderberg, J.P. and Sinnis, P. (1997) Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protien of Plasmodium falciparum. Mol. Biochem. Parasitol., 90, 33-41.
40. Sinden, R.E., Suhrbier, A., Davies, C.S., Fleck, S.L., Hodivala, K. and Nicholas, J.C. (1990) The development and routine application of highdensity exoerythrocytic-stage culture of Plasmodium berghei. WHO Bull., 68 Suppl., 115-125.
41. Sinnis, P., Clavijo, P., Fenyö, D., Chait, B.T., Cerami, C. and Nussenzweig, V. (1994) Structural and functional properties of region-II plus of the malaria circumsporozoite protein. J. Exp. Med., 180, 297-306.
42. Sinnis, P., Willnow, T.E., Briones, M.R.S., Herz, J. and Nussenzweig, V. (1996) Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J. Exp. Med., 184, 945-954.
43. Smith, J.E. and Alexander, J. (1986) Evasion of macrophage microbicidal mechanisms by mature sporozoites of Plasmodium yoelii yoelii. Parasitology, 93, 33-38.
44. Stewart, M.J. and Vanderberg, J.P. (1991) Malaria sporozoites release circumsporozoite protein from their apical end and translocate it along their surface. J. Protozool., 38, 411-421.
45. Stirpe, F., Barbieri, L., Battelli, M.G., Soria, M. and Lappi, D.A. (1992) Ribosome-inactivating proteins from plants: present status and future prospects. Bio/Technology, 10, 405-412.
46. Stüber, D., Matile, H. and Garotta, G. (1990) System for high-level production in Escherichia coli and rapid purification of recombinant proteins: application to epitope mapping, preparation of antibodies and structure-function analysis. Immunol. Methods, 4, 121-152.
47. Tan, R. and Frankel, A.D. (1995) Structural variety of arginine-rich RNA-binding peptides. Proc. Natl Acad. Sci. USA, 92, 5282-5286.
48. Vanderberg, J.P. and Stewart, M.J. (1990) Plasmodium-sporozoite-host cell interactions during sporozoite invasion. WHO Bull., 68 (Suppl.), 74-79.
49. Walter, P. and Blobel, G. (1981) Translocation of protein across the endoplasmic reticulum. III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol., 91, 557-561.
50. Weisgraber, K.H. and Mahley, R.W. (1996) Human apolipoprotein E: the Alzheimer's disease connection. FASEB J., 10, 1485-1494.
51. Wool, I.G., Glück, A. and Endo, Y. (1992) Ribotoxin recognition of ribosomal RNA and a proposal for the mechanism of translocation. Trends Biochem. Sci., 17, 266-269.
52. Ying, P., Shakibaei, M., Patankar, M.S., Clavijo, P., Beavis, R.C., Clark, G.F. and Frevert, U. (1997) The malaria circumsporozoite protein: interaction of the conserved regions I and II-plus with heparin-like oligosaccharides in heparan sulfate. Exp. Parasitol., 85, 168-182.
53. Yoshida, N., Nussenzweig, R.S., Potocnjak, P., Nussenzweig, V. and Aikawa, M. (1980) Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science, 207, 71-73.