Acylation-dependent and-independent membrane targeting and distinct functions of small myristoylated proteins (SMPs) in Leishmania major

International Journal for Parasitology

Volumn 42, Issue 3, 2012, Pages 239-247

  Tull, Dedreia ^a   Heng, Joanne ^a,b   Gooley, Paul R ^a   Naderer, Thomas ^a   McConville, Malcolm J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Acylation; Flagellum; Lipids; Membranes; Trafficking

Indexed keywords

MEMBRANE PROTEIN; SMALL MYRISTOYLATED PROTEIN 1; SMALL MYRISTOYLATED PROTEIN 4; UNCLASSIFIED DRUG;

LIPID; MEMBRANE; PARASITE; PROTEIN; PROTOZOAN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CHIMERA; CONTROLLED STUDY; CYTOSKELETON; DENSITY GRADIENT CENTRIFUGATION; FLAGELLUM; LEISHMANIA MAJOR; MYRISTYLATION; NONHUMAN; PELLICULAR MEMBRANE; PROMASTIGOTE; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; SUBPELLICULAR CYTOSKELETON;

ACYLATION; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; HUMANS; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RABBITS; SEQUENCE ALIGNMENT;

LEISHMANIA MAJOR; TRYPANOSOMATIDAE;

EID: 84858299155     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2011.12.004     Document Type: Article

References (39)

1. Corvi M.M., Berthiaume L.G., De Napoli M.G. Protein palmitoylation in protozoan parasites. Front Biosci. 2011, 3:1067-1079.
2. de Paulo Martins V., Okura M., Maric D., Engman D.M., Vieira M., Docampo R., Moreno S.N. Acylation-dependent export of Trypanosoma cruzi phosphoinositide-specific phospholipase C to the outer surface of amastigotes. J. Biol. Chem. 2010, 285:30906-30917.
3. Denny P.W., Smith D.F. Rafts and sphingolipid biosynthesis in the kinetoplastid parasitic protozoa. Mol. Microbiol. 2004, 53:725-733.
4. Denny P.W., Gokool S., Russell D.G., Field M.C., Smith D.F. Acylation-dependent protein export in Leishmania. J. Biol. Chem. 2000, 275:11017-11025.
5. Denny P.W., Field M.C., Smith D.F. GPI-anchored proteins and glycoconjugates segregate into lipid rafts in Kinetoplastida. FEBS Lett. 2001, 491:148-153.
6. Emmer B.T., Souther C., Toriello K.M., Olson C.L., Epting C.L., Engman D.M. Identification of a palmitoyl acyltransferase required for protein sorting to the flagellar membrane. J. Cell Sci. 2009, 122:867-874.
7. Ersfeld K., Barraclough H., Gull K. Evolutionary relationships and protein domain architecture in an expanded calpain superfamily in kinetoplastid parasites. J. Mol. Evol. 2005, 61:742-757.
8. Farazi T.A., Waksman G., Gordon J.I. The biology and enzymology of protein N-myristoylation. J. Biol. Chem. 2001, 276:39501-39504.
9. Frearson J.A., Brand S., McElroy S.P., Cleghorn L.A., Smid O., Stojanovski L., Price H.P., Guther M.L., Torrie L.S., Robinson D.A., Hallyburton I., Mpamhanga C.P., Brannigan J.A., Wilkinson A.J., Hodgkinson M., Hui R., Qiu W., Raimi O.G., van Aalten D.M., Brenk R., Gilbert I.H., Read K.D., Fairlamb A.H., Ferguson M.A., Smith D.F., Wyatt P.G. N-myristoyltransferase inhibitors as new leads to treat sleeping sickness. Nature 2010, 464:728-732.
10. Furuya T., Kashuba C., Docampo R., Moreno S.N. A novel phosphatidylinositol-phospholipase C of Trypanosoma cruzi that is lipid modified and activated during trypomastigote to amastigote differentiation. J. Biol. Chem. 2000, 275:6428-6438.
11. Garami A., Mehlert A., Ilg T. Glycosylation defects and virulence phenotypes of Leishmania mexicana phosphomannomutase and dolicholphosphate-mannose synthase gene deletion mutants. Mol. Cell. Biol. 2001, 21:8168-8183.
12. Ghai R., Waters P., Roumenina L.T., Gadjeva M., Kojouharova M.S., Reid K.B., Sim R.B., Kishore U. C1q and its growing family. Immunobiology 2007, 212:253-266.
13. Godsel L.M., Engman D.M. Flagellar protein localization mediated by a calcium-myristoyl/palmitoyl switch mechanism. EMBO J. 1999, 18:2057-2065.
14. Hertz-Fowler C., Ersfeld K., Gull K. CAP5.5, a life-cycle-regulated, cytoskeleton-associated protein is a member of a novel family of calpain-related proteins in Trypanosoma brucei. Mol. Biochem. Parasitol. 2001, 116:25-34.
15. Ilgoutz S.C., Mullin K.A., Southwell B.R., McConville M.J. Glycosylphosphatidylinositol biosynthetic enzymes are localized to a stable tubular subcompartment of the endoplasmic reticulum in Leishmania mexicana. EMBO J. 1999, 18:3643-3654.
16. Levental I., Grzybek M., Simons K. Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 2010, 49:6305-6316.
17. Liu W., Apagyi K., McLeavy L., Ersfeld K. Expression and cellular localisation of calpain-like proteins in Trypanosoma brucei. Mol. Biochem. Parasitol. 2010, 169:20-26.
18. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science 1991, 252:1162-1164.
19. Maric D., Epting C.L., Engman D.M. Composition and sensory function of the trypanosome flagellar membrane. Curr. Opin. Microbiol. 2010, 13:466-472.
20. Maric D., McGwire B.S., Buchanan K.T., Olson C.L., Emmer B.T., Epting C.L., Engman D.M. Molecular determinants of ciliary membrane localization of Trypanosoma cruzi flagellar calcium-binding protein. J. Biol. Chem. 2011, 286:33109-33117.
21. Martin D.D., Beauchamp E., Berthiaume L.G. Post-translational myristoylation: fat matters in cellular life and death. Biochimie 2011, 93:18-31.
22. Mills E., Price H.P., Johner A., Emerson J.E., Smith D.F. Kinetoplastid PPEF phosphatases: dual acylated proteins expressed in the endomembrane system of Leishmania. Mol. Biochem. Parasitol. 2007, 152:22-34.
23. Mullin K.A., Foth B., Ilgoutz S.M., Callaghan J., McFadden G.M., McConville M.J. Regulated degradation of ER membrane proteins in a novel tubular lysosome in Leishmania mexicana. Mol. Biol. Cell 2001, 12:2364-2377.
24. Naderer T., Ellis M.A., Sernee M.F., De Souza D.P., Curtis J., Handman E., McConville M.J. Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc. Natl. Acad. Sci. USA 2006, 103:5502-5507.
25. Peitzsch R.M., McLaughlin S. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry 1993, 32:10436-10443.
26. Price H.P., Menon M.R., Panethymitaki C., Goulding D., McKean P.G., Smith D.F. Myristoyl-CoA:protein N-myristoyltransferase, an essential enzyme and potential drug target in kinetoplastid parasites. J. Biol. Chem. 2003, 278:7206-7214.
27. Price H.P., Guther M.L., Ferguson M.A., Smith D.F. Myristoyl-CoA:protein N-myristoyltransferase depletion in trypanosomes causes avirulence and endocytic defects. Mol. Biochem. Parasitol. 2010, 169:55-58.
28. Ralton J.E., Mullin K.A., McConville M.J. Intracellular trafficking of GPI-proteins and free GPIs in Leishmania mexicana. Biochem. J. 2002, 363:365-375.
29. Resh M.D. Myristylation and palmitylation of Src family members: the fats of the matter. Cell 1994, 76:411-413.
30. Resh M.D. Trafficking and signaling by fatty-acylated and prenylated proteins. Nat. Chem. Biol. 2006, 2:584-590.
31. Rosenbaum J.L., Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 2002, 3:813-825.
32. Sigal C.T., Zhou W., Buser C.A., McLaughlin S., Resh M.D. Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc. Natl. Acad. Sci. USA 1994, 91:12253-12257.
33. Tull D., Vince J.E., Callaghan J.M., Naderer T., Spurck T., McFadden G.I., Currie G., Ferguson K., Bacic A., McConville M.J. SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol. Biol. Cell 2004, 11:4775-4786.
34. Tull D., Naderer T., Spurck T., Mertens H.D., Heng J., McFadden G.I., Gooley P.R., McConville M.J. Membrane protein SMP-1 is required for normal flagellum function in Leishmania. J. Cell Sci. 2010, 123:544-554.
35. Tyler K.M., Fridberg A., Toriello K.M., Olson C.L., Cieslak J.A., Hazlett T.L., Engman D.M. Flagellar membrane localization via association with lipid rafts. J. Cell Sci. 2009, 122:859-866.
36. Vince J.E., Tull D.L., Spurck T., Derby M.C., McFadden G.I., Gleeson P.A., Gokool S., McConville M.J. Leishmania adaptor protein-1 subunits are required for normal lysosome traffic, flagellum biogenesis, lipid homeostasis, and adaptation to temperatures encountered in the mammalian host. Eukaryot. Cell 2008, 7:1256-1267.
37. Weston S.A., Camble R., Colls J., Rosenbrock G., Taylor I., Egerton M., Tucker A.D., Tunnicliffe A., Mistry A., Mancia F., de la Fortelle E., Irwin J., Bricogne G., Pauptit R.A. Crystal structure of the anti-fungal target N-myristoyl transferase. Nat. Struct. Biol. 1998, 5:213-221.
38. Williams A., Westhead D.R. Sequence relationships in the legume lectin fold and other jelly rolls. Protein Eng. 2002, 15:771-774.
39. Wu Y., Deford J., Benjamin R., Lee M.G., Ruben L. The gene family of EF-hand calcium-binding proteins from the flagellum of Trypanosoma brucei. Biochem. J. 1994, 304:833-841.