Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Sheets, ribbons and tubules — how organelles get their shape

Abstract

Most membrane-bound organelles have elaborate, dynamic shapes and often include regions with distinct morphologies. These complex structures are relatively conserved throughout evolution, which indicates that they are important for optimal organelle function. Various mechanisms of determining organelle shape have been proposed — proteins that stabilize highly curved membranes, the tethering of organelles to other cellular components and the regulation of membrane fission and fusion might all contribute.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Organelles have complex, conserved shapes.
Figure 2: Making high-curvature membranes.
Figure 3: Membrane tethering generates organelle shape by three mechanisms.
Figure 4: Balancing fission and fusion affects organelle shape.
Figure 5: Three mechanisms of maintaining differently shaped domains in a membrane.

References

  1. Frey, T. G. & Mannella, C. A. The internal structure of mitochondria. Trends Biochem. Sci. 25, 319–324 (2000).

    Article  CAS  Google Scholar 

  2. Nicastro, D., Frangakis, A. S., Typke, D. & Baumeister, W. Cryo-electron tomography of Neurospora mitochondria. J. Struct. Biol. 129, 48–56 (2000).

    Article  CAS  Google Scholar 

  3. Voeltz, G. K., Rolls, M. M. & Rapoport, T. A. Structural organization of the endoplasmic reticulum. EMBO Rep. 3, 944–950 (2002).

    Article  CAS  Google Scholar 

  4. Farsad, K. & De Camilli, P. Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372–381 (2003).

    Article  CAS  Google Scholar 

  5. Zimmerberg, J. & Kozlov, M. M. How proteins produce cellular membrane curvature. Nature Rev. Mol. Cell Biol. 7, 9–19 (2006).

    Article  CAS  Google Scholar 

  6. Bauer, M. & Pelkmans, L. A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett. 580, 5559–5564 (2006).

    Article  CAS  Google Scholar 

  7. Dudkina, N. V., Sunderhaus, S., Braun, H. P. & Boekema, E. J. Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria. FEBS Lett. 580, 3427–3432 (2006).

    Article  CAS  Google Scholar 

  8. Everard-Gigot, V. et al. Functional analysis of subunit e of the F1F0-ATP synthase of the yeast Saccharomyces cerevisiae: importance of the N-terminal membrane anchor region. Eukaryot. Cell 4, 346–355 (2005).

    Article  CAS  Google Scholar 

  9. Arselin, G. et al. The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J. Biol. Chem. 279, 40392–40399 (2004).

    Article  CAS  Google Scholar 

  10. Gavin, P. D., Prescott, M., Luff, S. E. & Devenish, R. J. Cross-linking ATP synthase complexes in vivo eliminates mitochondrial cristae. J. Cell Sci. 117, 2333–2343 (2004).

    Article  CAS  Google Scholar 

  11. Giraud, M. F. et al. Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae? Biochim. Biophys. Acta 1555, 174–180 (2002).

    Article  CAS  Google Scholar 

  12. Paumard, P. et al. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221–230 (2002).

    Article  CAS  Google Scholar 

  13. Allen, R. D., Schroeder, C. C. & Fok, A. K. An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell Biol. 108, 2233–2240 (1989).

    Article  CAS  Google Scholar 

  14. Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M. & Rapoport, T. A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573–586 (2006).

    Article  CAS  Google Scholar 

  15. McMahon, H. T. & Gallop, J. L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590–596 (2005).

    Article  CAS  Google Scholar 

  16. Choi, S.-Y., Jenkins, G. M., Chan, D. C., Schiller, J. & Frohman, M. A. A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nature Cell Biol. 8, 1255–1262 (2006).

    Article  CAS  Google Scholar 

  17. Nakanishi, H. et al. Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast. J. Cell Sci. 119, 1406–1415 (2006).

    Article  CAS  Google Scholar 

  18. Huang, P., Altschuller, Y. M., Hou, J. C., Pessin, J. E. & Frohman, M. A. Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1. Mol. Biol. Cell 16, 2614–2623 (2005).

    Article  CAS  Google Scholar 

  19. Bishop, W. R. & Bell, R. M. Assembly of the endoplasmic reticulum phospholipid bilayer: the phosphatidylcholine transporter. Cell 42, 51–60 (1985).

    Article  CAS  Google Scholar 

  20. Herrmann, A., Zachowski, A. & Devaux, P. F. Protein-mediated phospholipid translocation in the endoplasmic reticulum with a low lipid specificity. Biochemistry 29, 2023–2027 (1990).

    Article  CAS  Google Scholar 

  21. Buton, X., Morrot, G., Fellmann, P. & Seigneuret, M. Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J. Biol. Chem. 271, 6651–6657 (1996).

    Article  CAS  Google Scholar 

  22. Burkhardt, J. K., Echeverri, C. J., Nilsson, T. & Vallee, R. B. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139, 469–484 (1997).

    Article  CAS  Google Scholar 

  23. 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).

    Article  CAS  Google Scholar 

  24. Yang, W. & Storrie, B. Scattered Golgi elements during microtubule disruption are initially enriched in trans-Golgi proteins. Mol. Biol. Cell 9, 191–207 (1998).

    Article  CAS  Google Scholar 

  25. De Vos, K. J., Allan, V. J., Grierson, A. J. & Sheetz, M. P. Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr. Biol. 15, 678–683 (2005).

    Article  CAS  Google Scholar 

  26. Varadi, A. et al. Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J. Cell Sci. 117, 4389–4400 (2004).

    Article  CAS  Google Scholar 

  27. Eglea, G., Lazaro-Dieguez, F. & Vilella, M. Actin dynamics at the Golgi complex in mammalian cells. Curr. Opin. Cell Biol. 18, 168–178 (2006).

    Article  Google Scholar 

  28. Vedrenne, C., Klopfenstein, D. R. & Hauri, H. P. Phosphorylation controls CLIMP-63-mediated anchoring of the endoplasmic reticulum to microtubules. Mol. Biol. Cell 16, 1928–1937 (2005).

    Article  CAS  Google Scholar 

  29. Dreier, L. & Rapoport, T. In vitro formation of the endoplasmic reticulum occurs independently of microtubules by a controlled fusion reaction. J. Cell Biol. 148, 883–898 (2000).

    Article  CAS  Google Scholar 

  30. Terasaki, M., Chen, L. B. & Fujiwara, K. Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 103, 1557–1568 (1986).

    Article  CAS  Google Scholar 

  31. Turner, J. R. & Tartakoff, A. M. The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization. J. Cell Biol. 109, 2081–2088 (1989).

    Article  CAS  Google Scholar 

  32. Snapp, E. L. et al. Formation of stacked ER cisternae by low affinity protein interactions. J. Cell Biol. 163, 257–269 (2003).

    Article  CAS  Google Scholar 

  33. Endo, T., Yamamoto, H. & Esaki, M. Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. J. Cell Sci. 116, 3259–3267 (2003).

    Article  CAS  Google Scholar 

  34. Cipolat, S., Martins de Brito, O., Dal Zilio, B. & Scorrano, L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl Acad. Sci. USA 101, 15927–15932 (2004).

    Article  CAS  Google Scholar 

  35. Frezza, D. et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126, 177–189 (2006).

    Article  CAS  Google Scholar 

  36. Staehelin, L. A., Giddings, T. H. J., Kiss, J. Z. & Sack, F. D. Macromolecular differentiation of Golgi stacks in root tips of Arabidopsis and Nicotiana seedlings as visualized in high pressure frozen and freeze-substituted samples. Protoplasma 157, 75–91 (1990).

    Article  CAS  Google Scholar 

  37. Ladinsky, M. S., Mastronarde, D. N., McIntosh, J. R., Howell, K. E. & Staehelin, L. A. Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135–1149 (1999).

    Article  CAS  Google Scholar 

  38. Cluett, E. B. & Brown, M. J. Adhesion of Golgi cisternae by proteinaceous interactions: intercisternal bridges as putative adhesive structures. J. Cell Sci. 103, 773–784 (1992).

    CAS  PubMed  Google Scholar 

  39. Crisp, M. et al. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41–53 (2006).

    Article  CAS  Google Scholar 

  40. Padmakumar, V. C. et al. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J. Cell Sci. 118, 3419–3430 (2005).

    Article  CAS  Google Scholar 

  41. Tzur, Y., Wilson, K. & Gruenbaum, Y. SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton. Nature Rev. Mol. Cell Biol. 7, 782–788 (2006).

    Article  CAS  Google Scholar 

  42. Sesaki, H. & Jensen, R. E. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147, 699–706 (1999).

    Article  CAS  Google Scholar 

  43. Sesaki, H., Southard, S. M., Yaffe, M. P. & Jensen, R. E. Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane. Mol. Biol. Cell 14, 27781–27788 (2003).

    Article  Google Scholar 

  44. Bleazard, W. et al. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nature Cell Biol. 1, 298–304 (1999).

    Article  CAS  Google Scholar 

  45. Shaw, J. M. & Nunnari, J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12, 178–184 (2002).

    Article  CAS  Google Scholar 

  46. Hetzer, M. et al. Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nature Cell Biol. 3, 1086–1091 (2001).

    Article  CAS  Google Scholar 

  47. Kano, F. et al. NSF/SNAPs and p97/p47/VCIP135 are sequentially required for cell cycle-dependent reformation of the ER network. Genes Cells 10, 989–999 (2005).

    Article  CAS  Google Scholar 

  48. Roy, L. et al. Role of p97 and syntaxin in the assembly of transitional endoplasmic reticulum. Mol. Biol. Cell 11, 2529–2542 (2000).

    Article  CAS  Google Scholar 

  49. Uchiyama, K. et al. VCIP135, a novel essential factor for p97/047-mediated membrane fusion, is required for Golgi and ER assembly in vivo. J. Cell Biol. 159, 855–866 (2002).

    Article  CAS  Google Scholar 

  50. Puthenveedu, M. A., Bachert, C., Puri, S., Lanni, F. & Linstedt, A. D. GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nature Cell Biol. 8, 238–248 (2006).

    Article  CAS  Google Scholar 

  51. Mattaj, I. W. Sorting out the nuclear envelope from the endoplasmic reticulum. Nature Rev. Mol. Cell Biol. 5, 65–69 (2004).

    Article  CAS  Google Scholar 

  52. Shibata, Y., Voeltz, G. K. & Rapoport, T. A. Rough sheets and smooth tubules. Cell 126, 435–439 (2006).

    Article  CAS  Google Scholar 

  53. Luedeke, C. et al. Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth. J. Cell Biol. 169, 897–908 (2005).

    Article  CAS  Google Scholar 

  54. 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).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Ladinsky and J. Rist for providing images, and Y. Shibata and J. Hinshaw for reading the manuscript. W.P. was supported by the Intramural Research Program of the National Institute of Diabetes and Digestive and Kidney Diseases.

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voeltz, G., Prinz, W. Sheets, ribbons and tubules — how organelles get their shape. Nat Rev Mol Cell Biol 8, 258–264 (2007). https://doi.org/10.1038/nrm2119

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrm2119

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing