Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote

Journal of Cell Science

Volumn 122, Issue 16, 2009, Pages 2846-2856

  Štefanić, Saša ^a,b   Morf, Laura ^a   Kulangara, Caroline ^a,c   Regös, Attila ^a,d   Sonda, Sabrina ^a   Schraner, Elisabeth ^a   Spycher, Cornelia ^a   Wild, Peter ^a   Hehl, Adrian B ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^d ETH ZURICH   (Switzerland)

Author keywords

Arf1; Cyst wall; Giardia; Golgi; GTPase; Membrane transport; Membrane tubule; Regulated secretion; Sar1

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAB PROTEIN; WATER; PROTOZOAL PROTEIN;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL CYCLE PROGRESSION; CELL MATURATION; CELL ORGANELLE; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; EUKARYOTE; EXTRACELLULAR MATRIX; GIARDIA LAMBLIA; GOLGI COMPLEX; HYPOTHESIS; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN TRANSPORT; PROTOZOAL GENETICS; TROPHOZOITE; ANIMAL; CELL FRACTIONATION; CYTOLOGY; CYTOPLASM VESICLE; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; PROTOZOA;

ADP-RIBOSYLATION FACTOR 1; ANIMALS; BIOLOGICAL TRANSPORT; CYTOPLASMIC VESICLES; ENDOPLASMIC RETICULUM; EUKARYOTIC CELLS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GIARDIA LAMBLIA; GOLGI APPARATUS; PROTOZOAN PROTEINS; RAB1 GTP-BINDING PROTEINS; SUBCELLULAR FRACTIONS;

EID: 70350007287     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.049411     Document Type: Article

References (62)

1. Adam, R. D. (2001). Biology of Giardia lamblia. Clin. Microbiol. Rev. 14, 447-475.
2. Altan-Bonnet, N., Sougrat, R. and Lippincott-Schwartz, J. (2004). Molecular basis for Golgi maintenance and biogenesis. Curr. Opin. Cell Biol. 16, 364-372.
3. Antonny, B., Madden, D., Hamamoto, S., Orci, L. and Schekman, R. (2001). Dynamics of the COPII coat with GTP and stable analogues. Nat. Cell Biol. 3, 531-537.
4. Aridor, M., Bannykh, S. I., Rowe, T. and Balch, W. E. (1995). Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131, 875-893.
5. Benchimol, M., Ribeiro, K. C., Mariante, R. M. and Alderete, J. F. (2001). Structure and division of the Golgi complex in Trichomonas vaginalis and Tritrichomonas foetus. Eur. J. Cell Biol. 80, 593-607.
6. Bevis, B. J., Hammond, A. T., Reinke, C. A. and Glick, B. S. (2002). De novo formation of transitional ER sites and Golgi structures in Pichia pastoris [comment]. Nat. Cell Biol. 4, 750-756.
7. Beznoussenko, G. V., Dolgikh, V. V., Seliverstova, E. V., Semenov, P. B., Tokarev, Y. S., Trucco, A., Micaroni, M., Di Giandomenico, D., Auinger, P., Senderskiy, I. V. et al. (2007). Analogs of the Golgi complex in microsporidia: structure and avesicular mechanisms of function. J. Cell Sci. 120, 1288-1298.
8. Bonifacino, J. S. and Glick, B. S. (2004). The mechanisms of vesicle budding and fusion. Cell 116, 153-166.
9. Calero, M., Chen, C. Z., Zhu, W., Winand, N., Havas, K. A., Gilbert, P. M., Burd, C. G. and Collins, R. N. (2003). Dual prenylation is required for Rab protein localization and function. Mol. Biol. Cell 14, 1852-1867.
10. D'Souza-Schorey, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
11. Dacks, J. B. and Field, M. C. (2007). Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J. Cell Sci. 120, 2977-2985.
12. Dacks, J. B., Davis, L. A., Sjogren, A. M., Andersson, J. O., Roger, A. J. and Doolittle, W. F. (2003). Evidence for Golgi bodies in proposed 'Golgi-lacking' lineages. Proc. Biol. Sci. 270 Suppl. 2, S168-S171.
13. Dascher, C. and Balch, W. E. (1994). Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J. Biol. Chem. 269, 1437-1448.
14. Davids, B. J., Reiner, D. S., Birkeland, S. R., Preheim, S. P., Cipriano, M. J., McArthur, A. G. and Gillin, F. D. (2006). A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS ONE 1, e44.
15. Davis-Hayman, S. R. and Nash, T. E. (2002). Genetic manipulation of Giardia lamblia. Mol. Biochem. Parasitol. 122, 1-7.
16. Davis-Hayman, S. R., Hayman, J. R. and Nash, T. E. (2003). Encystation-specific regulation of the cyst wall protein 2 gene in Giardia lamblia by multiple cis-acting elements. Int. J. Parasitol. 33, 1005-1012.
17. Donaldson, J. G., Honda, A. and Weigert, R. (2005). Multiple activities for Arf1 at the Golgi complex. Biochim. Biophys. Acta 1744, 364-373.
18. DuBois, K. N., Abodeely, M., Sakanari, J., Craik, C. S., Lee, M., McKerrow, J. H. and Sajid, M. (2008). Identification of the major cysteine protease of Giardia and its role in encystation. J. Biol. Chem. 283, 18024-18031.
19. Elias, E. V., Quiroga, R., Gottig, N., Nakanishi, H., Nash, T. E., Neiman, A. and Lujan, H. D. (2008). Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J. Biol. Chem 283, 35996-36010.
20. Feinstein, T. N. and Linstedt, A. D. (2007). Mitogen-activated protein kinase kinase 1-dependent Golgi unlinking occurs in G2 phase and promotes the G2/M cell cycle transition. Mol. Biol. Cell 18, 594-604.
21. Feinstein, T. N. and Linstedt, A. D. (2008). GRASP55 regulates Golgi ribbon formation. Mol. Biol. Cell 19, 2696-2707.
22. Gaechter, V., Schraner, E., Wild, P. and Hehl, A. B. (2008). The single dynamin family protein in the primitive protozoan Giardia lamblia is essential for stage conversion and endocytic transport. Traffic 9, 57-71.
23. Gillin, F. D., Reiner, D. S. and McCaffery, J. M. (1996). Cell biology of the primitive eukaryote Giardia lamblia. Annu. Rev. Microbiol. 50, 679-705.
24. Griffiths, G. (2000). Gut thoughts on the Golgi complex. Traffic 1, 738-745.
25. Hager, K. M., Striepen, B., Tilney, L. G. and Roos, D. S. (1999). The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112, 2631-2638.
26. He, C. Y., Ho, H. H., Malsam, J., Chalouni, C., West, C. M., Ullu, E., Toomre, D. and Warren, G. (2004). Golgi duplication in Trypanosoma brucei. J. Cell Biol. 165, 313-321.
27. Hehl, A. B., Marti, M. and Kohler, P. (2000). Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol. Biol. Cell 11, 1789-1800.
28. Heidtman, M., Chen, C. Z., Collins, R. N. and Barlowe, C. (2003). A role for Yip1p in COPII vesicle biogenesis. J. Cell Biol. 163, 57-69.
29. Jarroll, E. L., Macechko, P. T., Steimle, P. A., Bulik, D., Karr, C. D., van Keulen, H., Paget, T. A., Gerwig, G., Kamerling, J., Vliegenthart, J. et al. (2001). Regulation of carbohydrate metabolism during Giardia encystment. J. Eukaryot. Microbiol. 48, 22-26.
30. Jimenez-Garcia, L. F., Zavala, G., Chavez-Munguia, B., Ramos-Godinez Mdel, P., Lopez-Velazquez, G., Segura-Valdez Mde, L., Montanez, C., Hehl, A. B., Arguello-Garcia, R. and Ortega-Pierres, G. (2008). Identification of nucleoli in the early branching protist Giardia duodenalis. Int. J. Parasitol. 38, 1297-1304.
31. Kuge, O., Dascher, C., Orci, L., Rowe, T., Amherdt, M., Plutner, H., Ravazzola, M., Tanigawa, G., Rothman, J. E. and Balch, W. E. (1994). Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125, 51-65.
32. Lanfredi-Rangel, A., Attias, M., Reiner, D. S., Gillin, F. D. and De Souza, W. (2003). Fine structure of the biogenesis of Giardia lamblia encystation secretory vesicles. J. Struct. Biol. 143, 153-163.
33. Lanoix, J., Ouwendijk, J., Lin, C. C., Stark, A., Love, H. D., Ostermann, J. and Nilsson, T. (1999). GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COP I vesicles. EMBO J. 18, 4935-4948.
34. Lloyd, D. and Harris, J. C. (2002). Giardia: highly evolved parasite or early branching eukaryote? Trends Microbiol. 10, 122-127.
35. Losev, E., Reinke, C. A., Jellen, J., Strongin, D. E., Bevis, B. J. and Glick, B. S. (2006). Golgi maturation visualized in living yeast. Nature 441, 1002-1006.
36. Lujan, H. D., Marotta, A., Mowatt, M. R., Sciaky, N., Lippincott-Schwartz, J. and Nash, T. E. (1995a). Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 270, 4612-4618.
37. Lujan, H. D., Mowatt, M. R., Conrad, J. T., Bowers, B. and Nash, T. E. (1995b). Identification of a novel Giardia lamblia cyst wall protein with leucine-rich repeats. Implications for secretory granule formation and protein assembly into the cyst wall. J. Biol. Chem. 270, 29307-29313.
38. Lujan, H. D., Mowatt, M. R., Byrd, L. G. and Nash, T. E. (1996). Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proc. Natl. Acad. Sci. USA 93, 7628-7633.
39. Marti, M. and Hehl, A. B. (2003). Encystation-specific vesicles in Giardia: a primordial Golgi or just another secretory compartment? Trends Parasitol. 19, 440-446.
40. Marti, M., Li, Y., Schraner, E. M., Wild, P., Kohler, P. and Hehl, A. B. (2003a). The secretory apparatus of an ancient eukaryote: protein sorting to separate export pathways occurs before formation of transient Golgi-like compartments. Mol. Biol. Cell 14, 1433-1447.
41. Marti, M., Regos, A., Li, Y., Schraner, E. M., Wild, P., Muller, N., Knopf, L. G. and Hehl, A. B. (2003b). An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J. Biol. Chem. 278, 24837-24848.
42. Memon, A. R. (2004). The role of ADP-ribosylation factor and SAR1 in vesicular trafficking in plants. Biochim. Biophys. Acta 1664, 9-30.
43. Morrison, H. G., McArthur, A. G., Gillin, F. D., Aley, S. B., Adam, R. D., Olsen, G. J., Best, A. A., Cande, W. Z., Chen, F., Cipriano, M. J. et al. (2007). Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317, 1921-1926.
44. Pelletier, L., Stern, C. A., Pypaert, M., Sheff, D., Ngo, H. M., Roper, N., He, C. Y., Hu, K., Toomre, D., Coppens, I. et al. (2002). Golgi biogenesis in Toxoplasma gondii. Nature 418, 548-552.
45. Peyroche, A., Antonny, B., Robineau, S., Acker, J., Cherfils, J. and Jackson, C. L. (1999). Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol. Cell 3, 275-285.
46. Reiner, D. S., McCaffery, J. M. and Gillin, F. D. (2001). Reversible interruption of Giardia lamblia cyst wall protein transport in a novel regulated secretory pathway. Cell Microbiol. 3, 459-472.
47. Robbins, P. W. and Samuelson, J. (2005). Asparagine linked glycosylation in Giardia. Glycobiology 15, 15G-16G.
48. Rossanese, O. W., Soderholm, J., Bevis, B. J., Sears, I. B., O'Connor, J., Williamson, E. K. and Glick, B. S. (1999). Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145, 69-81.
49. Samuelson, J., Banerjee, S., Magnelli, P., Cui, J., Kelleher, D. J., Gilmore, R. and Robbins, P. W. (2005). The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc. Natl. Acad. Sci. USA 102, 1548-1553.
50. Saraiya, A. A. and Wang, C. C. (2008). snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog. 4, e1000224.
51. Stefanic, S., Palm, D., Svard, S. G. and Hehl, A. B. (2006). Organelle proteomics reveals cargo maturation mechanisms associated with Golgi-like encystation vesicles in the early-diverged protozoan Giardia lamblia. J. Biol. Chem. 281, 7595-7604.
52. Stephens, D. J. and Pepperkok, R. (2001). Illuminating the secretory pathway: when do we need vesicles? J. Cell Sci. 114, 1053-1059.
53. Stephens, D. J., Lin-Marq, N., Pagano, A., Pepperkok, R. and Paccaud, J. P. (2000). COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites. J. Cell Sci. 113, 2177-2185.
54. Struck, N. S., Herrmann, S., Schmuck-Barkmann, I., de Souza Dias, S., Haase, S., Cabrera, A. L., Treeck, M., Bruns, C., Langer, C., Cowman, A. F. et al. (2008). Spatial dissection of the cis- and trans-Golgi compartments in the malaria parasite Plasmodium falciparum. Mol. Microbiol. 67, 1320-1330.
55. Sun, C. H. and Tai, J. H. (2000). Development of a tetracycline controlled gene expression system in the parasitic protozoan Giardia lamblia. Mol. Biochem. Parasitol. 105, 51-60.
56. Sun, C. H., McCaffery, J. M., Reiner, D. S. and Gillin, F. D. (2003). Mining the Giardia lamblia genome for new cyst wall proteins. J. Biol. Chem. 278, 21701-21708.
57. Tisdale, E. J., Bourne, J. R., Khosravi-Far, R., Der, C. J. and Balch, W. E. (1992). GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J. Cell Biol. 119, 749-761.
58. Touz, M. C., Nores, M. J., Slavin, I., Carmona, C., Conrad, J. T., Mowatt, M. R., Nash, T. E., Coronel, C. E. and Lujan, H. D. (2002). The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 277, 8474-8481.
59. Tovar, J., Leon-Avila, G., Sanchez, L. B., Sutak, R., Tachezy, J., van der Giezen, M., Hernandez, M., Muller, M. and Lucocq, J. M. (2003). Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172-176.
60. Trucco, A., Polishchuk, R. S., Martella, O., Di Pentima, A., Fusella, A., Di Giandomenico, D., San Pietro, E., Beznoussenko, G. V., Polishchuk, E. V., Baldassarre, M. et al. (2004). Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat. Cell Biol. 6, 1071-1081.
61. Warren, G. and Malhotra, V. (1998). The organisation of the Golgi apparatus. Curr. Opin. Cell Biol. 10, 493-498.
62. Yang, X., Matern, H. T. and Gallwitz, D. (1998). Specific binding to a novel and essential Golgi membrane protein (Yip1p) functionally links the transport GTPases Ypt1p and Ypt31p. EMBO J. 17, 4954-4963.