Analogs of the Golgi complex in microsporidia: Structure and avesicular mechanisms of function

Journal of Cell Science

Volumn 120, Issue 7, 2007, Pages 1288-1298

  Beznoussenko, Galina V ^a   Dolgikh, Viacheslav V ^b   Seliverstova, Elena V ^c   Semenov, Petr B ^b   Tokarev, Yuri S ^b   Trucco, Alvar ^a   Micaroni, Massimo ^a   Di Giandomenico, Daniele ^a   Auinger, Peter ^d   Senderskly, Igor V ^b   Skarlato, Sergei O ^e   Snigirevskaya, Ekaterina S ^e   Komissarchik, Yan Yu ^e   Pavelka, Margit ^e   De Matteis, Maria A ^a   Luini, Alberto ^a   Sokolova, Yuliya Ya ^e   Mironov, Alexander A ^a  

^a Consorzio Mario Negri Sud ^*  (Italy)

^b ALL RUSSIAN INSTITUTE OF PLANT PROTECTION   (Russian Federation)

^c SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^d UNIVERSITY OF VIENNA   (Austria)

^e INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

COP I vesicles; Golgi; Intracellular transport; Microsporidia

Indexed keywords

COAT PROTEIN COMPLEX I; COAT PROTEIN COMPLEX II;

ARTICLE; CELL MEMBRANE; CELL ULTRASTRUCTURE; CELL VACUOLE; CELL WALL; CONTROLLED STUDY; CYTOCHEMISTRY; DEVELOPMENTAL STAGE; ENDOPLASMIC RETICULUM; FREEZING; GLYCOSYLATION; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MEMBRANE FUSION; MICROSPORIDA; NONHUMAN; PARANOSEMA GRYLLI; PARANOSEMA LOCUSTAE; PRIORITY JOURNAL; PROTEIN SECRETION;

ANIMALS; CELL MEMBRANE; COP-COATED VESICLES; ENDOPLASMIC RETICULUM; FAT BODY; GOLGI APPARATUS; GRYLLIDAE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LIFE CYCLE STAGES; MICROSPORIDIA; MICROSPORIDIOSIS; SPECIES SPECIFICITY;

MICROSPORIDIA; PARANOSEMA GRYLLI; PARANOSEMA LOCUSTAE;

EID: 34248203076     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03402     Document Type: Article

References (45)

1. Bannykh, S. L, Rowe, T. and Balch, W. E. (1996). The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135, 19-35.
2. Beznoussenko, G. V. and Mironov, A. A. (2002). Models of intracellular transport and evolution of the Golgi complex. Anat. Rec. 268, 226-238.
3. Bohne, W., Ferguson, D. J., Kohler, K. and Gross, U. (2000). Developmental expression of a tandemly repeated, glycine- and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi. Infect. Immunol. 68, 2268-2275.
4. Bonfanti, L., Mironov, A., Jr, Martinez-Menarguez, J., Martella, O., Fusella, A., Baldassare, M., Buccione, R., Geuze, H., Mironov, A. and Luini, A. (1998). Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95, 993-1003.
5. Cali, A. and Takvorian, P. M. (1999). Developmental morphology and life cycles of the microsporidia. In The Microsporidia and Microsporidiosis (ed. M. Witmer and L. M. Weiss), pp. 85-128. Washington, DC: American Society for Microbiology.
6. Cole, N. B., Sciaky, N., Marotta, A., Song, J. and Lippincott-Schwartz, J. (1996). Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell 7, 631-650.
7. Cosson, P., Ravazzola, M., Varlamov, O., Sollner, T. H., Di Liberto, M., Volchuk, A., Rothman, J. E. and Orci, L. (2005). Dynamic transport of SNARE proteins in the Golgi apparatus. Proc. Natl. Acad. Sci. USA 102, 14647-14652.
8. Delbac, F., Peyret, P., Metenier, G., David, D., Danchin, A. and Vivares, C. P. (1998). On proteins of the microsporidian invasive apparatus: complete sequence of a polar tube protein of Encephalitozoon cuniculi. Mol. Microbial. 29, 825-834.
9. Dolgikh, V. V., Semenov, P. B., Mironov, A. A. and Beznoussenko, G. V. (2005). Immunocytochemical identification of the major exospore protein and three polar-tube proteins of the microsporidia Paranosema grylli. Protist 156, 77-87.
10. Eugster, A., Frigerio, G., Dale, M. and Duden, R. (2004). The alpha- and beta'-COP WD40 domains mediate cargo-selective interactions with distinct di-lysine motifs. Mol. Biol. Cell 15, 1011-1123.
11. Faulstich, D., Auerback S., Orci, L., Ravazzola, M., Wegchingel, S., Lottspeich, F., Stenbeck, G., Harter, C., Wieland, F. T. and Tschochner, H. (1996). Architecture of coatomer: molecular characterization of delta-COP and protein interactions within the complex. J. Cell Biol. 135, 53-61.
12. Gallagher, S. R. (1998). One-dimensional SDS gel electrophoresis of proteins. In Current Protocols in Cell Biology, pp. 6.1.1.-6.1.34. New York: John Wiley.
13. Griffiths, G., Fuller, S. D., Back, R., Hollinshead, M., Pfeiffer, S. and Simons, K. (1989). The dynamic nature of the Golgi complex. J. Cell Biol. 108, 277-297.
14. Guo, Q., Vasile, E. and Krieger, M. (1994). Disruptions in Golgi structure and membrane traffic in a conditional lethal mammalian cell mutant are corrected by epsilon-COP. J. Cell Biol. 125, 1213-1224.
15. Hayman, J. R., Hayes, S. F., Amon, J. and Nash, T. E. (2001). Developmental expression of two spore wall proteins during maturation of the microsporidian Encephalitozoon intestinalis. Infect. Immun. 69, 7057-7066.
16. Hirschberg, K., Miller, C. M., Ellenberg, J., Presley, J. F., Siggia, E. D., Phair, R. D. and Lippincott-Schwartz, J. (1998). Kinetic analysis of secretory protein traffic and characterization of golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143, 1485-1503.
17. Jay, G. D., Culp, D. J. and Jahnke, M. R. (1990). Silver staining of extensively glycosylated proteins on sodium dodecyl sulfate-polyacrylamide gels:enhancement by carbohydrate-binding dyes. Anal. Biochem. 185, 324-330.
18. Katinka, M. D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., Barbe, V., Peyretaillade, E., Brottier, P., Wincker, P. et al. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450-453.
19. Keohane, E. M. and Weiss, L. M. (1999). The structure, function, and composition of the microsporidian polar tube. In The Microsporidia and Microsporidiosis (ed. M. Wittner and L. M. Weiss), pp. 196-224. Washington, DC: American Society for Microbiology.
20. Kepes, F., Rombourg, A. and Satiat-Jeunemaitre, B. (2005). Morphodynamics of the secretory pathway. Int. Rev. Cytol. 242, 55-120.
21. Kreppel, L. K., Blomberg, M. A. and Hart, G. W. (1997). Dynamic glycosylation of nuclear and cytosolic proteins. J. Biol. Chem. 272, 9308-9315.
22. Kweon, H.-S., Beznoussenko, G. V., Micaroni, M., Polishchuk, R. S., Trucco, A., Martella, O., Di Giandomenico, D., Marra, P., Fusella, A., Di Pentima, A. et al. (2004). Golgi enzymes are enriched in perforated zones of Golgi cistemae but are depleted in COP-1 vesicles. Mol. Biol. Cell 15, 4710-4724.
23. Ladinsky, M. S, Mastronarde, D. N., McIntosh, J. R., Howell, K. E. and Staehelin, L. A. (1999). Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149.
24. Ladinsky, M. S., Wu, C. C., McIntosh, S., McIntosh, J. R. and Howell, K. E. (2002). Structure of the Golgi and distribution of reporter molecules at 20 degrees C reveals the complexity of the exit compartments. Mol. Biol. Cell 13, 2810-2825.
25. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacterophage T4. Nature 277, 680-685.
26. Lussier, M., Sdicu, A. M., Bussereau, R, Jacquet, M. and Bussey, H. (1997). The Ktrlp, Ktr3p, and Kre2p/Mntlp mannosyltransferases participate in the elaboration of yeast O- and N-linked carbohydrate chains. J. Biol. Chem. 272, 15527-15531.
27. Marra, P., Maffucci, T., Daniele, T., Tullio, G. D., Ikehara. Y., Chan, E. K., Luini, A., Beznoussenko, G., Mironov, A. and De Matteis, M. A. (2001). The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment. Nat. Cell Biol. 3, 1101-1113.
28. McIntosh, J. R. (2001). Electron microscopy of cells: a new beginning for a new century. J. Cell Biol. 153, F25-F32.
29. Mironov, A. A., Beznoussenko, G. V., Nicoziani, P., Martella, O., Trucco, A., Kweon, H.-S., Di Giandomenico, D., Polishchuk, R. S., Fusella, A., Lupetti, P. et al. (2001). Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155, 1225-1238.
30. Mironov, A. A., Mironov, A. A., Jr, Beznoussenko, G. V., Trucco, A., Lupetti, P., Smith, J. D., Geerts, W. J., Koster A. J., Burger K. N., Martone M. E. et al. (2003). ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell 5, 583-594.
31. Mironov, A. A., Beznoussenko, G. V., Polishchuk, R. S. and Trucco, A. (2005). Intra-Golgi transport: a way to a new paradigm? Biochim. Biophys. Acta 1744, 340-350.
32. Miroux, B. and Walker, J. E. (1996). Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298.
33. Novikoff, A. B. and Goldfischer, S. (1961). Nucleoside-diphosphatase activity in the Golgi apparatus and its usefulness for cytological studies. Proc. Natl. Acad. Sci. USA 47, 802-810.
34. Opat, A. S., van Vliet, C. and Gleeson, P. A. (2001). Trafficking and localisation of resident Golgi glycosylation enzymes. Biochimie 83, 763-773.
35. Orci, L., Glick, B. S. and Rothman, J. E. (1986). A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in Protein transport within the Golgi stack. Cell 46, 171-184.
36. Pimpl, P., Movafeghi, A., Coughlan, S., Denecke, J., Hillmer, S. and Robinson, D. G. (2000). In situ localization and in vitro induction of plant COP-I-coated vesicles. Plant Cell 12, 2219-2236.
37. Rabouille, C., Hui, N., Hunte, F., Kieckbusch, R., Berger, E. G., Warren, G. and Nilsson, T. (1995). Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108, 1617-1627.
38. Scales, S. J., Pepperkok, R. and Kreis, T. E. (1997). Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COP-II and COP-I. Cell 90, 1137-1148.
39. Seleznev, K., Issi, I., Dolgikh, V., Belostotskaya, G., Antonova, O. and Sokolova, J. (1995). Fractionation of different life cycle stages of microsporidia Paranosema grylli from crickets Gryllus bimaculatus by centrifugation in percoll density gradient for biochemical research. J. Eukaryot. Microbial. 42, 288-292.
40. Sokolova, Y., Snigirevskaya, E. S., Skarlato, S. O., Komissarchik, Y. Y. and Mironov, A. A. (2001). Unusual Golgi apparatus at the proliferative stage of microsporidian life cycle. Dokl. Biol. Sci. 378, 290-293.
41. Sokolova, Y. Y., Dolgikh, V. V., Morzhina, E. V., Nassonova, E. S., Issi, I. V., Terry, R. S., Ironside, J. E., Smith, J. E. and Vossbrinck, C. R. (2003). Establishment of the new genus Paranosema based on the ultrastructure and molecular phylogeny of the type species Paranosema grylli Gen. Nov., Comb. Nov. (Sokolova, Selezniov, Dolgikh, Issi 1994), from the cricket Gryllus bimaculatus Deg. J. Invertebr. Pathol. 84, 159-172.
42. Sokolova, Y. Y., Issi, I. V., Morzhina, E. V., Tokarev, Y. S. and Vossbrinck, C. R. (2005). Ultrastructural analysis supports transferring Noserna whitei Weiser 1953 to the genus Paranosema and creation a new combination, Paranosema whitei. J. Invertebr. Pathol. 90, 122-126.
43. 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.
44. Vavra, J. and Larsson, J. I. R. (1999). Structure of the microsporidia. In Microsporidia and Microsporidiosis (ed. M. Witmer and L. M. Weiss), pp. 7-84. Washington, DC: American Society for Microbiology.
45. Volchuk, A., Ravazzola, M., Perrelet, A., Eng, W. S., Di Liberto, M., Varlamov, O., Fukasawa, M., Engel, T., Sollner, T. H., Rothman, J. E. et al. (2004). Countercurrent distribution of two distinct SNARE complexes mediating transport within the Golgi stack. Mol. Biol. Cell 15, 1506-1518.