The Leishmania ARL-1 and Golgi traffic

PLoS ONE

Volumn 3, Issue 2, 2008, Pages

  Sahin, Annelise ^a,b   Espiau, Benoît ^a,c   Tetaud, Emmanuel ^a,b   Cuvillier, Armelle ^a,d   Lartigue, Lydia ^a,e   Ambit, Audrey ^a,f   Robinson, Derrick R ^a   Merlin, Gilles ^a  

^a University Victor Segalen   (France)

^b CNRS   (France)

^c Centre de Biologie et d Ecologie Tropicale et Méditerranéenne   (French Polynesia)

^d UNIVERSITÉ DE LIMOGES   (France)

^e LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^f INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADP RIBOSYLATION FACTOR LIKE PROTEIN 1; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MUTANT PROTEIN; NUCLEOTIDE; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP RIBOSYLATION FACTOR RELATED PROTEINS; ADP-RIBOSYLATION FACTOR RELATED PROTEINS; MEMBRANE PROTEIN; PROTOZOAL PROTEIN;

AMASTIGOTE; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; GENETIC CODE; GENOME; GOLGI COMPLEX; HAPLOIDY; IN VIVO STUDY; LEISHMANIA; LYSOSOME; MAMMAL; MYRISTYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMASTIGOTE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRYPANOSOMA; YEAST; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT;

HEXAPODA; MAMMALIA; TRYPANOSOMATIDAE;

ADP-RIBOSYLATION FACTORS; ANIMALS; GOLGI APPARATUS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; LEISHMANIA; MEMBRANE PROTEINS; MUTATION; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

EID: 45749105946     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001620     Document Type: Article

References (75)

1. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, et al. (2005) The genome of the kinetoplastid, parasite, Leishmania major. Science 309: 436-442.
2. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, et al. (2007) Comparative genomic analysis of three Leiskmania species that cause diverse human disease. Nat Genet 39: 839-847.
3. Howell GJ, Holloway ZG, Cobbold C, Monaco AP, Ponnambalam S (2006) Cell biology of membrane trafficking in human disease. Int Rev Cytol 252: 1-69.
4. Overath P, Engstler M (2004) Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol Microbiol 53: 735-744.
5. Pasqualato S, Renault L, Cherfils J (2002) Art, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication. EMBO Rep 3: 1035-1041.
6. Nie Z, Hirsch DS, Randazzo PA (2003) Arf and its many interactors. Curr Opin Cell Biol. 15: 396-404.
7. Li Y, Kelly WG, Logsdon JM JR, Schurko AM, Harfe BD, et al. (2004) Functional genomic analysis of the ADP-ribosylation factor family of GTPases: phylogeny among diverse eukaryotes and function in C. elegans. FASEB J 18: 1834-1850.
8. Kahn RA, Cherfils J, Elias M, Lovering RC, Munro S, et al. (2006) Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J Cell Biol 172: 645-650.
9. D'Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358.
10. Porter-Kelley JM, Gerald NJ, Engel JC, Ghedin E, Dwyer DM (2004) LdARF1 in Trafficking and Structural Maintenance of the trans-Golgi Cisternal Network in the Protozoan Pathogen Leishmania donovani. Traffic 5: 868-883.
11. Price HP, Stark M, Smith B, Smith DF (2007) TbARF1 influences lysosomal function but not endocytosis in procyclic stage Trypanosoma brucei. Mol Biochem Parasitol 155: 123-127.
12. Price HP, Stark M, Smith DF (2007) Trypanosoma brucei ARF1 Plays a Central Role in Endocytosis and Golgi-Lysosome Trafficking. Mol Biol Cell 18: 864-873.
13. Schürmann A, Breiner M, Becker W, Huppertz C, Kainulainene H, et al. (1994) Cloning of two novel ADP-ribosylation factor-like proteins and characterization of their differential expression in 3T3-L1 cells. J Biol Chem 269: 15683-15688.
14. Hong JX, Lee FJS, Patton WA, Lin CY, Moss, J, et al. (1998) Phospholipid- and GTP-dependent activation of cholera toxin and phospholipase D by human ADP-ribosylation factor-like protein 1 (HARLI). J Biol Chem 273: 15872-15876.
15. Price HP, Panethymitaki C, Goulding D, Smith DF (2005) Functional analysis of TbARL1, an N-myristoylated Golgi protein essential for viability in bloodstream trypanosomes.J Cell Sci 118: 831-841.
16. Tamkun JW, Kahn RA, Kissinger M, Brizuela BJ, Rulka C, et al. (1991) The ARF-like gene encodes an essential GTP-binding protein in Drosophila. Proc Natl Acad Sci USA 88: 3120-3124.
17. Lowe SL, Wong SH, Hong WJ (1996) The mammalian ARF-like protein 1 (ArI1) is associated with the Golgi complex. J Cell Sci 109: 209-220.
18. Lu L, Horstmann H, Ng C, Hong W (2001) Regulation of Golgi structure and function by ARF-like protein I (Arl1). J Cell Sci 114: 4543-4555.
19. Lee FJS, Huang CF, Yu WL, Buu LM, Lin CY, et al. (1997) Characterization of an ADP-ribosylation factor-like 1 protein in Sacchammyces cerevisiae. J Biol Chem 272: 30998-31005.
20. Abudugupur A, Mitsui K, Yokota S, Tsurugi K (2002) An ARL1 mutation affected autophagic cell death in yeast, causing a defect in central vacuole formation. Cell Death Differ 9: 158-168.
21. Rosenwald AG, Rhodes MA, Van Valkenburgh H, Palanivel V, Chapman G, et al. (2002) ARL1 and membrane traffic in Saccharomyces cerevisiae. Yeast 19: 1039-1056.
22. Moss J, Vaughan M (1995) Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J Biol Chem 270: 12327-12330.
23. Vaughan M, Moss J (1997) Activation of toxin ADP-ribosyltransferases by the family of ADP-ribosylation factors. Adv Exp Med Biol 419: 315-320.
24. Jochum A, Jackson D, Schwarz H, Pipkorn R, Singer-Kruger B (2002) Yeast Ys12p, homologous to Sec7 domain guanine nucleotide exchange factors, functions in endocytosis and maintenance of vacuole integrity and interacts with the Arf-Like small GTPase ArIIp. Mol Cell Biol 22: 4914-4928.
25. Liu YW, Huang CF, Huang KB, Lee FJ (2005) Role for Gcslp in regulation of Arllp at trans-Golgi compartments. Mol Biol Cell 16: 4024-4033.
26. Ding M, Vitale N, Tsai SC, Adamik R, Moss J, et al. (1996) Characterization of a GTPase-activating protein that stimulates GTP hydrolysis by both ADP-ribosylation factor (ARF) and ARF-like proteins - Comparison to the ARD1 GAP-domain. J Biol Chem 271: 24005-24009.
27. Van Valkenburgb H, Shem JF, Sharer JD, Zhu X, Kahn RA (2001) ADP-ribosylation factors (ARFs) and ARF-like 1 (ARL1) have both specific and shared effectors: characterizing ARL1-binding proteins. J Biol Chem 276: 22826-22837.
28. Setty SRG, Shin ME, Yoshino A, Marks MS, Burd CG (2003) Golgi Recruitment of GRIP Domain Proteins by Arf-like GTPase 1 Is Regulated by Arf-like GTPase 3. Curr Biol 13: 401-404.
29. Panic B, Whyte JR, Munro S (2003) The ARF-like GTPases Ar11p and Ar13p Act. in a Pathway that Interacts with Vesicle-Tethering Factors at the Golgi Apparatus. Curr Biol 13: 405-410.
30. Jackson CL (2003) Membrane Traffic: Arl GTPases Get a GRIP on the Golgi. Curr Biol 13: R174-176.
31. Lu L, Hong W (2003) Interaction of Ar11-GTP with GRIP domains recruits autoantigens Golgin-97 and Golgin-245/p230 onto the Golgi. Mol Biol Cell 14: 3767-3781.
32. Munro S (2005) The Arf-like GTPase Arl1 and its role in membrane traffic. Biochem Soc Trans 33: 601-605.
33. Lake JA, Cruz VFDL, Ferreira PCG, Morel G, Simpson L (1988) Evolution of Parasitism: Kinetoplastid Protozoan History Reconstructed from Mitochondrial rRNA Gene Sequences. Proc Natl Acad Sci USA 85: 4779-4783.
34. Bringaud F, Iler M, Cerqueira GC, Smith M, et al. (2007) Members of a Large Retroposon Family Are Determinants of Post-Transcriptional Gene Expression in Leishmania. PLoS Pathogens 3: e136.
35. Curotto de Lafaille MA, Laban A, Wirth DF (1992) Gene expression in Leishmania: analysis of essential 5′ DNA sequences. Proc Natl Acad Sci USA 89: 2703-2707.
36. Kjeldgaard M, Nyborg J, Clark BFC (1996) Protein motifs. 10. The GTP binding motif: Variations on a theme. FASEB J 10: 1347-1368.
37. Sahin A, Tetaud E, Merlin G, Santarelli X (2005) LdARL-1 His-tagged recombinant protein: purification by immobilized metal affinity expanded bed adsorption. J Chromatogr B 818: 19-22.
38. Kelly JM, Ward HM, Miles MA, Kendall G (1992) A shuttle vector which facilitates the expression of transfected genes in Trypanosoma cruzi and Leishmania. Nucleic Acids Res 20: 3963-3969.
39. Tetaud E, Lecuix I, Sheldrake T, Baltz T, Fairlamb AH (2002) A new expression vector for Crithidia fasciculata and Leishmania. Mol Biochem Parasitol 120: 195-204.
40. Ma DQ, Russell DG, Beverley SM, Turco SJ (1997) Golgi GDP-mannose uptake requires Leishmania LPG2 - A member of a eukaryotic family of putative nucleotide-sugar transporters. J Biol Chem 272: 3799-3805.
41. Honda A, Al-Awar OS, Hay JC, Donaldson JG (2005) Targeting of Arf-1 to the early Golgi by membrin, an ER-Golgi SNARE. J Cell Biol 168: 1039-1051.
42. Boutin JA (1997) Myristoylation. Cell Signal 9: 15-35.
43. Price HP, Menon MR, Panethymitaki C, Goulding D, McKean PG, et al. (2003) Myristoyl-CoA:protein N-myristoyltransferase, an essential enzyme and potential drug target in kinetoplastid parasites. J Biol Chem 278: 7206-7214.
44. Macia E, Luton F, Partisani M, Cherfils J, Chardin P, et al. (2004) The GDP-bound form of Arf6 is located at the plasma membrane. J Cell Sci 117: 2389-2398.
45. Allen CL, Goulding D, Field MC (2003) Clathrin-mediated endocytosis is essential in Trpanosoma brucei. EMBO J 22: 4991-5002.
46. Waller RF, McConville MJ (2002) Developmental changes in lysosome morphology and function Leishmania parasites. Int J Parasitol 32: 1435-1445.
47. Ilgoutz SC, Mullin KA, Southwell BR, McConville MJ (1999) Glycosylphosphatidylinositol biosynthetic enzymes are localized to a stable tubular subcompartment of the endoplasmic reticulum in Leishmania mexicana. EMBO J 18: 3643-3654.
48. Mullin KA, Foth BJ, Ilgoutz SC, Callaghan JM, Zawadzki JL, et al. (2001) Regulated Degradation of an Endoplasmic Reticulum Membrane Protein in a Tubular Lysosome in Leishmania mexicana. Mol Biol Cell 12: 2364-2377.
49. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN (2005) Acidocalcisomes - conserved from bacteria to man. Nat Rev Microbiol 3: 251-261.
50. Lemercier G, Dutoya S, Luo S, Ruiz FA, Rodrigues CO, et al. (2002) A vacuolar-type H+-pyrophosphatase governs maintenance of functional acidocalcisomes and growth ofthe insect and mammalian forms of Trypanosoma brucei. J Biol Chem 277: 37369-37376.
51. Kjer-Nidsen L, van Vliect C, Erlich R, Toh BH, Gleeson PA (1999) The Golgi-targeting sequence of the peripheral membrane protein p230. J Cell Sci 112: 1645-1654.
52. Gleeson PA, Lock JG, Luke MR, Stow JL (2004) Domains of the TGN: coats, tethers and G proteins. Traffic 5: 315-326.
53. McConville MJ, Ilgoutz SC, Teasdale RD, Foth BJ, Matthews A, et al. (2002) Targeting of the GRIP domain to the trans-Golgi network is conserved from protists to animals. Eur J Cell Biol 81: 485-495.
54. Vichi A, Payne DM, Pacheco-Rodriguez G, Moss J, Vaughan M (2005) E3 ubiquitin ligase activity of the trifunctional ARD1 (ADP-ribosylation factor domain protein 1). Proc Natl Acad Sci USA 102: 1945-1950.
55. Briones MR, Souto RP, Stolf BS, Zingales B (1999) The evolution of two Trypanosoma cruzi subgroups inferred from rRNA genes can be correlated with the interchange of American mammalian faunas in the Cenozoic and has implications to pathogenicity and host specificity. Mol Biochem Parasitol 104: 219-232.
56. Klein S, Franco M, Chardin P, Luton F (2006) Role of the Arf6 GDP/GTP cycle and Arf6 GTPase-activating proteins in actin remodeling and intracellular transport. J Biol Chem 281: 12352-12361.
57. Haynes LP, Thomas GM, Burgoyne RD (2005) Interaction of neuronal calcium sensor-1 and ADP-ribosylation factor 1 allows bidirectional control of phosphatidylinositol 4-kinase beta and trans-Golgi network-plasma membrane traffic. J Biol Chem 280: 6047-6054.
58. Cuvillier A, Redon F, Antoine J-C, Chardin P, DeVos T, et al. (2000) LdARL-3A, a Leishmania promastigote-specific ADP-ribosylation factor-like protein, is essential for flagellum integrity. J Cell Sci 113: 2065-2074.
59. Sabin A, Espiau B, Marchand C, Merlin G (2008) Flagellar length depends on LdARL-3A GTP/GDP Unaltered Cycling in Leishmania amazomensis. Mol Biochem Parasitol 157: 83-87.
60. Barr FA, Short B (2003) Golgins in the structure and dynamics of the Golgi apparatus. Curr Opin Cell Biol 15: 405-413.
61. Graham, TR. (2004) Membrane targeting: getting Arl to the Golgi. Curr Biol 14: R483-485.
62. Setty SR, Strochlic TI, Tong AH, Boone G, Burd CG (2004) Golgi targeting of ARF-like GTPase Arl3p requires its Nalpha-acetylation and the integral membrane protein Sys1p. Nat Cell Biol 6: 414-419.
63. Lodes MJ, Merlin G, DeVos T, Gosh A, Madhubala R, et al. (1995) Increased expression of LD1 genes transcribed by RNA polymerase I in Leismania donovani as a result of duplication in to the rRNA gene locus. Mol Cell Biol 15: 6845-6853.
64. Espiau B, Lemercier G, Ambit A, Bringaud F, Merlin G, et al (2006) A Soluble Pyrophosphatase, a Key Enzyme for Polyphosphate Metabolism in Leishmania. J Biol Chem 281: 1516-1523
65. Prina E, Lang T, Glaichenhaus N, Antoine JC (1996) Presentation of the protective parasite antigen LACK by Leishmania-infected macrophages. J Immunol 156: 4318-4327.
66. Morgan GW, Allen CL, Jeffries TR, Hollinshead M, Field MC (2001) Developmental and morphological-regulation of clathrin-mediated endocytosis in Trypanosoma brucei. J Cell Sci 114: 2605-2615.
67. Bakalara N, Seyfang A, Baltz T, Davis C (1995) Trypanosoma brucei and Trypanosoma cruzi: cycle-regulated protein tyrosine phosphatase activity. Exp Parasitol 81: 302-312.
68. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, et al. (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99: 7877-7882.
69. Ilgoutz SC, Zawadzki JL, Ralton JE, McConville MJ (1999) Evidence that free GPI glycolipids are essential for growth of Leishmania mexicana. EMBO J 18: 2746-2755.
70. Robinson DR, Gull K (1994) The configuration of DNA replication sites within the Trypanosoma brucei kinetoplast. J Cell Biol 126: 641-648.
71. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
72. El Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
73. Amor JC, Horton JR, Zhu X, Wang Y, Sullards C, et al. (2001) Structures of Yeast ARF2 and ARL1. Distinct roles for the N Terminus in the structure and function of ARF family GTPases. J Biol Chem 276: 42477-42484.
74. Panic B, Perisic O, Veprintsev DB, Williams RL, Munro S (2003) Structural basis for Ar11-dependent targeting of homodimeric GRIP domains to the Golgi apparatus. Mol Cell 12: 863-874.
75. Wu M, Lu L, Hong W, Song H (2004) Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Ar11. Nat Struct Mol Biol 11: 86-94.