Limits...
A mechanism for nuclear positioning in fission yeast based on microtubule pushing.

Tran PT, Marsh L, Doye V, Inoué S, Chang F - J. Cell Biol. (2001)

Bottom Line: The MT bundles are organized from medial MT-organizing centers that may function as nuclear attachment sites.After an average of 1.5 min of growth at the cell tip, MT plus ends exhibit catastrophe and shrink back to the nuclear region before growing back to the cell tip.Computer modeling suggests that a balance of these pushing MT forces can provide a mechanism to position the nucleus at the middle of the cell.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, Columbia University, New York, New York 10032, USA. pt143@columbia.edu

ABSTRACT
The correct positioning of the nucleus is often important in defining the spatial organization of the cell, for example, in determining the cell division plane. In interphase Schizosaccharomyces pombe cells, the nucleus is positioned in the middle of the cylindrical cell in an active microtubule (MT)-dependent process. Here, we used green fluorescent protein markers to examine the dynamics of MTs, spindle pole body, and the nuclear envelope in living cells. We find that interphase MTs are organized in three to four antiparallel MT bundles arranged along the long axis of the cell, with MT plus ends facing both the cell tips and minus ends near the middle of the cell. The MT bundles are organized from medial MT-organizing centers that may function as nuclear attachment sites. When MTs grow to the cell tips, they exert transient forces produced by plus end MT polymerization that push the nucleus. After an average of 1.5 min of growth at the cell tip, MT plus ends exhibit catastrophe and shrink back to the nuclear region before growing back to the cell tip. Computer modeling suggests that a balance of these pushing MT forces can provide a mechanism to position the nucleus at the middle of the cell.

Show MeSH
A model for nuclear positioning and interphase MT architecture in S. pombe. MTs are organized from medial organizing centers (iMTOCs) in multiple bundles with an antiparallel configuration and dynamic plus ends facing the cell tips and minus ends in medial-bundled regions. One MT bundle is attached to the nuclear envelope at the SPB, and other MT bundles may be attached at additional sites. When an MT end contacts the cell tip, MT polymerization produces a transient pushing force that pushes the MT lattice and attached nucleus away from that cell tip. A balance of these pushing forces from these MTs may position the nucleus in the middle of the cell.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2169469&req=5

Figure 10: A model for nuclear positioning and interphase MT architecture in S. pombe. MTs are organized from medial organizing centers (iMTOCs) in multiple bundles with an antiparallel configuration and dynamic plus ends facing the cell tips and minus ends in medial-bundled regions. One MT bundle is attached to the nuclear envelope at the SPB, and other MT bundles may be attached at additional sites. When an MT end contacts the cell tip, MT polymerization produces a transient pushing force that pushes the MT lattice and attached nucleus away from that cell tip. A balance of these pushing forces from these MTs may position the nucleus in the middle of the cell.

Mentions: Here, our studies have defined a novel mechanism for how the nucleus is positioned by MTs at the middle of the fission yeast cell (Fig. 10). Key parameters include: (a) organization of MTs in three to four bundles in an antiparallel configuration, with the plus ends facing the cell tips and the minus ends near the middle of the cell; (b) regulated MT dynamics so that MT plus ends exhibit catastrophe 1.5 min after contacting the cell tip; and (c) transient MT pushing forces on the nuclear envelope when MT plus ends contact the cell tip so that MT ends are constantly sensing the position of the cell tips. A computer model shows that a mechanism based on these parameters can indeed center the nucleus. These studies illustrate how dynamic MTs can provide a way for a cell to measure distances, sense cell size, and define its middle.


A mechanism for nuclear positioning in fission yeast based on microtubule pushing.

Tran PT, Marsh L, Doye V, Inoué S, Chang F - J. Cell Biol. (2001)

A model for nuclear positioning and interphase MT architecture in S. pombe. MTs are organized from medial organizing centers (iMTOCs) in multiple bundles with an antiparallel configuration and dynamic plus ends facing the cell tips and minus ends in medial-bundled regions. One MT bundle is attached to the nuclear envelope at the SPB, and other MT bundles may be attached at additional sites. When an MT end contacts the cell tip, MT polymerization produces a transient pushing force that pushes the MT lattice and attached nucleus away from that cell tip. A balance of these pushing forces from these MTs may position the nucleus in the middle of the cell.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2169469&req=5

Figure 10: A model for nuclear positioning and interphase MT architecture in S. pombe. MTs are organized from medial organizing centers (iMTOCs) in multiple bundles with an antiparallel configuration and dynamic plus ends facing the cell tips and minus ends in medial-bundled regions. One MT bundle is attached to the nuclear envelope at the SPB, and other MT bundles may be attached at additional sites. When an MT end contacts the cell tip, MT polymerization produces a transient pushing force that pushes the MT lattice and attached nucleus away from that cell tip. A balance of these pushing forces from these MTs may position the nucleus in the middle of the cell.
Mentions: Here, our studies have defined a novel mechanism for how the nucleus is positioned by MTs at the middle of the fission yeast cell (Fig. 10). Key parameters include: (a) organization of MTs in three to four bundles in an antiparallel configuration, with the plus ends facing the cell tips and the minus ends near the middle of the cell; (b) regulated MT dynamics so that MT plus ends exhibit catastrophe 1.5 min after contacting the cell tip; and (c) transient MT pushing forces on the nuclear envelope when MT plus ends contact the cell tip so that MT ends are constantly sensing the position of the cell tips. A computer model shows that a mechanism based on these parameters can indeed center the nucleus. These studies illustrate how dynamic MTs can provide a way for a cell to measure distances, sense cell size, and define its middle.

Bottom Line: The MT bundles are organized from medial MT-organizing centers that may function as nuclear attachment sites.After an average of 1.5 min of growth at the cell tip, MT plus ends exhibit catastrophe and shrink back to the nuclear region before growing back to the cell tip.Computer modeling suggests that a balance of these pushing MT forces can provide a mechanism to position the nucleus at the middle of the cell.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, Columbia University, New York, New York 10032, USA. pt143@columbia.edu

ABSTRACT
The correct positioning of the nucleus is often important in defining the spatial organization of the cell, for example, in determining the cell division plane. In interphase Schizosaccharomyces pombe cells, the nucleus is positioned in the middle of the cylindrical cell in an active microtubule (MT)-dependent process. Here, we used green fluorescent protein markers to examine the dynamics of MTs, spindle pole body, and the nuclear envelope in living cells. We find that interphase MTs are organized in three to four antiparallel MT bundles arranged along the long axis of the cell, with MT plus ends facing both the cell tips and minus ends near the middle of the cell. The MT bundles are organized from medial MT-organizing centers that may function as nuclear attachment sites. When MTs grow to the cell tips, they exert transient forces produced by plus end MT polymerization that push the nucleus. After an average of 1.5 min of growth at the cell tip, MT plus ends exhibit catastrophe and shrink back to the nuclear region before growing back to the cell tip. Computer modeling suggests that a balance of these pushing MT forces can provide a mechanism to position the nucleus at the middle of the cell.

Show MeSH