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Microtubules (red) and nuclei (blue) revealed in cultured cells by fluorescence microscopy
We study the organization and regulation of the microtubule cytoskeleton, and the relationship between the cell cycle and the cytoskeleton. Microtubules are polymers assembled from tubulin subunits, and are an essential element of the cytoskeleton. Microtubules are polar polymers, acting as directional tracks for the many motor proteins that move along them. Microtubules and motors move vesicles and organelles, and make up the spindle, which segregates chromosomes in mitosis and meiosis. How do cells organize microtubules into complex structures such as the mitotic spindle? One of the keys is the centrosome, which nucleates microtubule polymerization from free tubulin subunits, and organizes the array of microtubules. We're interested in understanding the centrosome, and its role in cell division and differentiation.

We use the yeast Saccharomyces cerevisiae to study the genetics of microtubule function. The entire genome of this yeast has been sequenced, and the ease of genetic manipulation is unparalleled in any other eukaryote. Yeast cell biology isn't too bad either, despite the small size of yeast cells (check out some GFP-tubulin movies). We use eggs from the frog Xenopus laevis to study biochemistry of microtubule function. Frog eggs are very large cells from which it is easy to make concentrated cytoplasmic extracts that carry out many of the reactions of the intact egg. These reactions include centrosome formation on sperm, as occurs during fertilization, and centrosome duplication, as occurs each cell cycle in intact cells. Lastly, we use cultured cells from human, mouse and frog to study the cell biology of microtubule and centrosome function.



There are four main projects in the lab:

1) Cell cycle control of centrosome duplication. We have shown that duplication of the centrosome, the microtubule organizing center of animal cells, is dependent on the cell cycle kinase cdk2, and on cell cycle-specific proteolysis. We are now trying to determine the molecular mechanisms of centrosome duplication and to understand how centrosome duplication is controlled so that it happens once and only once per cell cycle. Cancer cells often have aberrant centrosome numbers, and we are investigating the relationship between aberrant centrosome number and the generation of cells with abnormal numbers of chromosomes.

  • Wong, C. and Stearns, T. (2003) Centrosome number is controlled by a centrosome-intrinsic block to reduplication. Nature Cell Biol. 5:539-544.
  • Chang, P., Giddings, T. H., Winey, M., and Stearns, T. (2003) Epsilon-tubulin is required for centriole duplication and microtubule organization. Nature Cell Biol. 5:71-76.
  • Stearns, T. (2001) Centrosome duplication: a centriolar pas de deux. Cell 105:417-420.
  • Lacey, K. R., Jackson, P. K., and Stearns, T. (1999) Cyclin-dependent kinase control of centrosome duplication. Proc. Natl. Acad. Sci. 96:2817-2822.
  • Freed, E., Lacey, K. R., Lyapina, S. A., Huie, P., Deshaies, R. J., Stearns, T., and Jackson, P. (1999) The SKP1 and CUL1 ubiquitin ligase components localize to the centrosome and regulate the centrosome duplication cycle. Genes Dev. 13:2242-2257

2) Microtubule nucleation. Microtubules are polymers of tubulin, which is a heterodimer of alpha-tubulin and beta-tubulin. We have identified a remarkable complex of proteins associated with a third type of tubulin, gamma-tubulin. Gamma-tubulin and its associated proteins are localized to the centrosome and are critical for initiation, or nucleation, of microtubule assembly. The gamma-tubulin complex is a very large, ring-shaped complex and contains 5 proteins in addition to gamma-tubulin. We have now cloned all of these proteins, and are determining their role in microtubule nucleation.

  • Patel U., Stearns T. (2002) Quick Guide: Gamma-Tubulin. Curr Biol. 2002 12:R408.
  • Murphy, S.M., Preble, A.M., Patel, U.K., O'Connell, K.L., Dias, D.P., Moritz, M., Agard, D., Stults, J.T., and Stearns, T. (2001) GCP5 and GCP6: Two new members of the human gamma-tubulin complex. Mol. Biol. Cell 12:3340-3352.
  • Jeng, R. and Stearns, T. (1999) Gamma-Tubulin complexes: size does matter. Trends Cell Biol. 9:339-342.
  • Murphy, S. M., Urbani, L., and Stearns, T. (1998) The mammalian gamma-tubulin complex contains homologs of the yeast spindle pole body components Spc97p and Spc98p. J. Cell Biol. 141:663-674.
  • Leask, A., Obrietan, K., and Stearns, T. (1997) Synaptically-coupled central nervous system neurons lack centrosomal gamma-tubulin. Neuroscience Letters 229:17-20.
  • Marschall, L. G., Jeng, R. L., Mulholland, J. and Stearns, T. (1996) Analysis of Tub4p, a yeast gamma-tubulin-like protein: implications for microtubule-organizing center function. J. Cell Biol. 134:443-454.
  • Stearns, T. and Kirschner, M. (1994) In vitro reconstitution of centrosome assembly and function: the central role of gamma-tubulin. Cell 76:623-638.

3) Function of tubulin superfamily members. In addition to alpha, beta, and gamma-tubulin described above, we have identified two new tubulins in human cells, delta-tubulin and epsilon-tubulin. Both are localized to the centrosome, and we are working to determine their role in microtubule function. Epsilon-tubulin is asymmetrically distributed between the centrosomes after duplication; the old centrosome has epsilon-tubulin, whereas the new centrosome lacks it. Both delta-tubulin and epsilon-tubulin are conserved in vertebrates and some unicellular eukaryotes, but are absent from the sequenced genomes of fungi, plants, and lower animals.

  • Chang, P., Giddings, T. H., Winey, M., and Stearns, T. (2003) Epsilon-tubulin is required for centriole duplication and microtubule organization. Nature Cell Biol. 5:71-76.
  • Chang, P. and Stearns, T. (2000) Delta-tubulin and epsilon-tubulin: two new human centrosomal tubulins reveal novel aspects of centrosome structure and function. Nature Cell Biol. 2:30-35.

4) Tubulin folding/biogenesis. Alpha-tubulin and beta-tubulin undergo a complex series of interactions with proteins termed tubulin cofactors. These interactions are thought to be involved in bringing together the two tubulins to make the tubulin heterodimer. The components of this pathway are conserved in all eukaryotes, and mutations in the yeast components cause defects in the microtubule cytoskeleton. We are interested in how these interactions help to make functional tubulin heterodimer, and whether they are involved in controlling the level of active tubulin in the cell.

  • Feierbach, B., Nogales, E., Downing, K. H., Stearns, T. (1999) Alf1p, a CLIP-170 domain-containing protein, is functionally and physically associated with alpha-tubulin. J. Cell Biol. 144:113-124.
  • Tian, G., Lewis, S.A., Feierbach, B., Stearns, T., Rommelaere, H., Ampe, C., Cowan, N.J. (1997) Tubulin subunits exist in an activated conformational state generated and maintained by protein cofactors. J. Cell Biol. 138:821-832.