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Golgi biogenesis in Toxoplasma gondii

Abstract

Two models have been put forward to explain the growth of new Golgi during the cell cycle. The first suggests that a new Golgi grows out of the endoplasmic reticulum by de novo synthesis1. The second suggests that a pre-existing Golgi is needed for the growth of a new one, that is, the Golgi is an autonomously replicating organelle2. To resolve this issue, we have exploited the simplicity of the apicomplexan parasite Toxoplasma gondii3, which has only a single Golgi stack4. Here we show, by using video fluorescence microscopy and three-dimensional reconstructions of serial thin sections, that the Golgi grows by a process of lateral extension followed by medial fission. Further fission leads to the inheritance by each daughter of a pair of Golgi structures, which then coalesce to re-form a single Golgi. Our results indicate that new Golgi grow by autonomous duplication and raise the possibility that the Golgi is a paired structure that is analogous to centrioles5.

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Figure 1: Stages of Golgi growth and division.
Figure 2: Stable expression of mammalian Golgi proteins.
Figure 3: Immunoelectron microscopy of transgenic parasites.
Figure 4: Biogenesis of the Golgi apparatus in living parasites.

References

  1. Lippincott-Schwartz, J. & Zaal, K. J. Cell cycle maintenance and biogenesis of the Golgi complex. Histochem. Cell. Biol. 114, 93–103 (2000)

    CAS  PubMed  Google Scholar 

  2. Bracker, C. E., Morre, D. J. & Grove, S. N. Structure, differentiation, and multiplication of Golgi-apparatus in fungal hyphae. Protoplasma 194, 250–274 (1996)

    Article  Google Scholar 

  3. Joiner, K. A. & Roos, D. S. Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J. Cell Biol. 157, 557–563 (2002)

    CAS  Article  Google Scholar 

  4. Roos, D. S. et al. Transport and trafficking: Toxoplasma as a model for Plasmodium. Novartis Found. Symp. 226, 176–195 (1999)

    CAS  PubMed  Google Scholar 

  5. Marshall, W. Centrioles take center stage. Curr. Biol. 11, R487–R496 (2001)

    CAS  Article  Google Scholar 

  6. Kelly, T. J. & Brown, G. W. Regulation of chromosome replication. Annu. Rev. Biochem. 69, 829–880 (2000)

    CAS  Article  Google Scholar 

  7. Warren, G. Membrane partitioning during cell division. Annu. Rev. Biochem. 62, 323–348 (1993)

    CAS  Article  Google Scholar 

  8. Whaley, W. G. The Golgi Apparatus (Springer, New York, 1975)

    Book  Google Scholar 

  9. Preuss, D., Mulholland, J., Franzusoff, A., Segev, N. & Botstein, D. Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell 3, 789–803 (1992)

    CAS  Article  Google Scholar 

  10. Zaal, K. J. et al. Golgi membranes are absorbed into and reemerge from the ER during mitosis. Cell 99, 589–601 (1999)

    CAS  Article  Google Scholar 

  11. Presley, J. F. et al. Golgi membrane dynamics. Mol. Biol. Cell 9, 1617–1626 (1998)

    CAS  Article  Google Scholar 

  12. Pelletier, L., Jokitalo, E. & Warren, G. The effect of Golgi depletion on exocytic transport. Nature Cell Biol. 2, 840–846 (2000)

    CAS  Article  Google Scholar 

  13. Shima, D. T., Haldar, K., Pepperkok, R., Watson, R. & Warren, G. Partitioning of the Golgi apparatus during mitosis in living HeLa cells. J. Cell Biol. 137, 1211–1228 (1997)

    CAS  Article  Google Scholar 

  14. Cole, N. B., Sciaky, N., Marotta, A., Song, J. & Lippincott-Schwartz, J. Golgi dispersal during microtubule disruption—regeneration of Golgi stacks at peripheral endoplasmic-reticulum exit sites. Mol. Biol. Cell 7, 631–650 (1996)

    CAS  Article  Google Scholar 

  15. Wooding, S. & Pelham, H. R. The dynamics of Golgi protein traffic visualized in living yeast cells. Mol. Biol. Cell 9, 2667–2680 (1998)

    CAS  Article  Google Scholar 

  16. Rossanese, O. W. et al. Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145, 69–81 (1999)

    CAS  Article  Google Scholar 

  17. Dubremetz, J. F., Garcia-Reguet, N., Conseil, V. & Fourmaux, M. N. Apical organelles and host-cell invasion by Apicomplexa. Int. J. Parasitol. 28, 1007–1013 (1998)

    CAS  Article  Google Scholar 

  18. Hager, K. M., Striepen, B., Tilney, L. G. & Roos, D. S. 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 (1999)

    CAS  PubMed  Google Scholar 

  19. Sheffield, H. G. & Melton, M. L. The fine structure and reproduction of Toxoplasma gondii. J. Parasitol. 54, 209–226 (1968)

    CAS  Article  Google Scholar 

  20. Radke, J. R. et al. Defining the cell cycle for the tachyzoite stage of Toxoplasma gondii. Mol. Biochem. Parasitol. 115, 165–175 (2001)

    CAS  Article  Google Scholar 

  21. Hu, K. et al. Daughter cell assembly in the protozoan parasite Toxoplasma gondii. Mol. Biol. Cell 13, 593–606 (2002)

    CAS  Article  Google Scholar 

  22. Seemann, J., Jokitalo, E., Pypaert, M. & Warren, G. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407, 1022–1026 (2000)

    ADS  CAS  Article  Google Scholar 

  23. Ward, T. H., Polishchuk, R. S., Caplan, S., Hirschberg, K. & Lippincott-Schwartz, J. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557–570 (2001)

    CAS  Article  Google Scholar 

  24. Wiggins, C. A. R. & Munro, S. Activity of the yeast mnn1 α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl Acad. Sci. USA 95, 7945–7950 (1998)

    ADS  CAS  Article  Google Scholar 

  25. Odenthal-Schnittler, M., Tomavo, S., Becker, D., Dubremetz, J. F. & Schwarz, R. T. Evidence for N-linked glycosylation in Toxoplasma gondii. Biochem. J. 291, 713–721 (1993)

    CAS  Article  Google Scholar 

  26. Lujan, H. D. et al. Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 270, 4612–4618 (1995)

    CAS  Article  Google Scholar 

  27. Field, H., Sherwin, T., Smith, A. C., Gull, K. & Field, M. C. Cell-cycle and developmental regulation of TbRAB31 localisation, a GTP- locked Rab protein from Trypanosoma brucei. Mol. Biochem. Parasitol. 106, 21–35 (2000); erratum 107, 329–330 (2000)

    CAS  Article  Google Scholar 

  28. Piel, M., Nordberg, J., Euteneuer, U. & Bornens, M. Centrosome-dependent exit of cytokinesis in animal cells. Science 291, 1550–1553 (2001)

    ADS  CAS  Article  Google Scholar 

  29. Roos, D. S., Donald, R. G. K., Morrissette, N. S. & Moulton, A. L. C. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45, 27–63 (1994)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank F. Barr and T. Nilsson for the GRASP55 and NAGTI plasmids; S. Trombetta for recombinant GFP; the Joiner and Roos labs—mainly F. Quittnat, T. Stedman and O. Harb—for advice and discussion; N. Andrews for the use of her cell-culture room; C. Roy and J. Kagan for help with confocal microscopy; K. Zichichi, C. Horensavitz and C. Deloyer-Pypaert for help with electron microscopy; Olympus for providing some of the microscopes; J. Shorter and E. Procyk for critically reading the manuscript; and the Warren and Mellman labs for discussions. This work was supported by National Institutes of Health grants (to G.W., I.M., K.A.J. and D.S.R.) and the Ludwig Institute for Cancer Research.

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Correspondence to Graham Warren.

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Pelletier, L., Stern, C., Pypaert, M. et al. Golgi biogenesis in Toxoplasma gondii. Nature 418, 548–552 (2002). https://doi.org/10.1038/nature00946

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