The host targeting motif in exported Plasmodium proteins is cleaved in the parasite endoplasmic reticulum

Molecular and Biochemical Parasitology

Volumn 171, Issue 1, 2010, Pages 25-31

  Osborne, Andrew R ^a   Speicher, Kaye D ^b   Tamez, Pamela A ^a   Bhattacharjee, Souvik ^a   Speicher, David W ^b   Haldar, Kasturi ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b WISTAR INSTITUTE   (United States)

Author keywords

Acetylation; Plasmodium; Protease; Protein export

Indexed keywords

CELL MEMBRANE PROTEIN;

ACETYLATION; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HOST CELL; NONHUMAN; PLASMODIUM; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TARGETING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ACETYLATION; ENDOPLASMIC RETICULUM; PLASMODIUM; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

EID: 77649340470     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2010.01.003     Document Type: Article

References (38)

1. WHO world malaria report (2008)
2. Haldar K., and Mohandas N. Erythrocyte remodeling by malaria parasites. Curr Opin Hematol 14 (2007) 203
3. Maier A.G., Cooke B.M., Cowman A.F., and Tilley L. Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 7 (2009) 341
4. Kraemer S.M., and Smith J.D. A family affair: var genes PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9 (2006) 374
5. Osborne A.R., Rapoport T.A., and van den Berg B. Protein translocation by the Sec61/SecY channel. Annu Rev Cell Dev Biol 21 (2005) 529
6. Knuepfer E., Rug M., and Cowman A.F. Function of the plasmodium export element can be blocked by green fluorescent protein. Mol Biochem Parasitol 142 (2005) 258
7. Przyborski J.M., Miller S.K., Pfahler J.M., et al. Trafficking of STEVOR to the Maurer's clefts in Plasmodium falciparum-infected erythrocytes. EMBO J 24 (2005) 2306
8. Hiller N.L., Bhattacharjee S., van Ooij C., et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306 (2004) 1934
9. Marti M., Good R.T., Rug M., Knuepfer E., and Cowman A.F. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306 (2004) 1930
10. van Ooij C., and Haldar K. Protein export from Plasmodium parasites. Cell Microbiol 9 (2007) 573
11. Sargeant T.J., Marti M., Caler E., et al. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7 (2006) R12
12. van Ooij C., Tamez P., Bhattacharjee S., et al. The malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathog 4 (2008) e1000084
13. Boddey J.A., Moritz R.L., Simpson R.J., and Cowman A.F. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10 (2009) 285
14. Chang H.H., Falick A.M., Carlton P.M., Sedat J.W., DeRisi J.L., and Marletta M.A. N-terminal processing of proteins exported by malaria parasites. Mol Biochem Parasitol 160 (2008) 107
15. Lippincott-Schwartz J., Yuan L.C., Bonifacino J.S., and Klausner R.D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56 (1989) 801
16. Ivessa N.E., De Lemos-Chiarandini C., Tsao Y.S., et al. O-glycosylation of intact and truncated ribophorins in brefeldin A-treated cells: newly synthesized intact ribophorins are only transiently accessible to the relocated glycosyltransferases. J Cell Biol 117 (1992) 949
17. Tang H.Y., Ali-Khan N., Echan L.A., Levenkova N., Rux J.J., and Speicher D.W. A novel four-dimensional strategy combining protein and peptide separation methods enables detection of low-abundance proteins in human plasma and serum proteomes. Proteomics 5 (2005) 3329
18. Klemba M., and Goldberg D.E. Characterization of plasmepsin V, a membrane-bound aspartic protease homolog in the endoplasmic reticulum of Plasmodium falciparum. Mol Biochem Parasitol 143 (2005) 183
19. Banerjee R., Liu J., Beatty W., Pelosof L., Klemba M., and Goldberg D.E. Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Proc Natl Acad Sci USA 99 (2002) 990
20. Spielmann T., Hawthorne P.L., Dixon M.W., et al. A cluster of ring stage-specific genes linked to a locus implicated in cytoadherence in Plasmodium falciparum codes for PEXEL-negative and PEXEL-positive proteins exported into the host cell. Mol Biol Cell 17 (2006) 3613
21. van Dooren G.G., Marti M., Tonkin C.J., Stimmler L.M., Cowman A.F., and McFadden G.I. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol 57 (2005) 405
22. Kulzer S., Gehde N., and Przyborski J.M. Return to sender: use of Plasmodium ER retrieval sequences to study protein transport in the infected erythrocyte and predict putative ER protein families. Parasitol Res 104 (2009) 1535
23. Lee M.C., Moura P.A., Miller E.A., and Fidock D.A. Plasmodium falciparum Sec24 marks transitional ER that exports a model cargo via a diacidic motif. Mol Microbiol 68 (2008) 1535
24. Wong J.W., and Cagney G. An overview of label-free quantitation methods in proteomics by mass spectrometry. Methods Mol Biol 604 (2010) 273
25. Wang W., Zhou H., Lin H., et al. Quantification of proteins and metabolites by mass spectrometry without isotopic labeling or spiked standards. Anal Chem 75 (2003) 4818
26. Bondarenko P.V., Chelius D., and Shaler T.A. Identification and relative quantitation of protein mixtures by enzymatic digestion followed by capillary reversed-phase liquid chromatography-tandem mass spectrometry. Anal Chem 74 (2002) 4741
27. Dean N., and Pelham H.R. Recycling of proteins from the Golgi compartment to the ER in yeast. J Cell Biol 111 (1990) 369
28. Semenza J.C., Hardwick K.G., Dean N., and Pelham H.R. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61 (1990) 1349
29. Lotti L.V., Mottola G., Torrisi M.R., and Bonatti S. A different intracellular distribution of a single reporter protein is determined at steady state by KKXX or KDEL retrieval signals. J Biol Chem 274 (1999) 10413
30. Dalbey R.E., Lively M.O., Bron S., and van Dijl J.M. The chemistry and enzymology of the type I signal peptidases. Protein Sci 6 (1997) 1129
31. Saric T., Chang S.C., Hattori A., et al. An IFN-gamma-induced aminopeptidase in the ER ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 3 (2002) 1169
32. Serwold T., Gonzalez F., Kim J., Jacob R., and Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419 (2002) 480
33. Weihofen A., Binns K., Lemberg M.K., Ashman K., and Martoglio B. Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296 (2002) 2215
34. Gehde N., Hinrichs C., Montilla I., Charpian S., Lingelbach K., and Przyborski J.M. Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum. Mol Microbiol 71 (2009) 613
35. de Koning-Ward T.F., Gilson P.R., Boddey J.A., et al. A newly discovered protein export machine in malaria parasites. Nature 459 (2009) 945
36. Tasaki T., and Kwon Y.T. The mammalian N-end rule pathway: new insights into its components and physiological roles. Trends Biochem Sci 32 (2007) 520
37. Mogk A., Schmidt R., and Bukau B. The N-end rule pathway for regulated proteolysis: prokaryotic and eukaryotic strategies. Trends Cell Biol 17 (2007) 165
38. Maier A.G., Rug M., O'Neill M.T., et al. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134 (2008) 48