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Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase.

Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ - J. Cell Biol. (1997)

Bottom Line: We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres.The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions.Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cell Biology, University of California at Berkeley 94720, USA.

ABSTRACT
We have analyzed the progressive changes in the spatial distribution of telomeres during meiosis using three-dimensional, high resolution fluorescence microscopy. Fixed meiotic cells of maize (Zea mays L.) were subjected to in situ hybridization under conditions that preserved chromosome structure, allowing identification of stage-dependent changes in telomere arrangements. We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres. Quantitative measurements on the spatial arrangements of telomeres revealed that, as cells passed through premeiotic interphase and into leptotene, there was an increase in the frequency of large telomere-to-telomere distances and a decrease in the bias toward peripheral localization of telomeres. By leptotene, there was no obvious evidence of telomere grouping, and the large, singular nucleolus was internally located, nearly concentric with the nucleus. At the end of leptotene, telomeres clustered de novo at the nuclear periphery, coincident with a displacement of the nucleolus to one side. The telomere cluster persisted throughout zygotene and into early pachytene. The nucleolus was adjacent to the cluster at zygotene. At the pachytene stage, telomeres rearranged again by dispersing throughout the nuclear periphery. The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions. Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

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Model of possible mechanisms of telomere cluster formation. The de novo clustering of randomly distributed telomeres is proposed to occur by one of two different mechanisms (1  and 2). Mechanism 1 proposes a two-step model; 1A, telomeres  move from their positions in the nucleus to the nuclear envelope  where they become attached, and 1B nuclear envelope-attached  telomeres move over the nuclear surface to the final cluster site.  Mechanism 2 proposes a one-step model in which telomeres  move from their positions in the nucleus directly to the region of  the nuclear envelope that will be the final cluster site.
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Figure 10: Model of possible mechanisms of telomere cluster formation. The de novo clustering of randomly distributed telomeres is proposed to occur by one of two different mechanisms (1 and 2). Mechanism 1 proposes a two-step model; 1A, telomeres move from their positions in the nucleus to the nuclear envelope where they become attached, and 1B nuclear envelope-attached telomeres move over the nuclear surface to the final cluster site. Mechanism 2 proposes a one-step model in which telomeres move from their positions in the nucleus directly to the region of the nuclear envelope that will be the final cluster site.

Mentions: The present study describes the sudden formation and the gradual dissolution of the meiotic telomere cluster. In light of these findings, we now consider the possible mechanisms underlying these dynamic changes in telomere localization. The abruptness of the initial cluster formation allows us to rule out one class of mechanisms relying on passive diffusion. Specifically, our data do not support a scenario in which a region of the nuclear envelope suddenly acquires an affinity for telomeres, and collects the telomeres on the basis of chance interaction. What then is the mechanistic basis for the formation of the telomere cluster? To begin to address this question, two possible mechanisms of bouquet formation are proposed in Fig. 10. The first mechanism involves a two-step process (movements indicated by arrows of nuclei 1A and 1B of Fig. 10) in which the telomeres first attach to any region of the nuclear envelope (arrows of 1A), followed by the movement of telomeres in the plane of the nuclear envelope (arrows of 1B) to end up at the final cluster site. The second mechanism would involve a one-step process (movements indicated by arrows of nucleus 2, Fig. 10) in which telomeres move directly to the region of the nuclear envelope that will be the final cluster site, the bouqet base (referred to as bb in Figs. 5 and 6). The two-step clustering mechanism is consistent with the observations on mouse spermatocytes (54). Our data on meiosis in maize does not allow us to distinguish between the two paths shown in Fig. 10. Although this model only addresses the mechanisms responsible for telomere movements, we recognize that telomeres are but one of many cellular components that show altered distributions at the bouquet stage (13).


Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase.

Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ - J. Cell Biol. (1997)

Model of possible mechanisms of telomere cluster formation. The de novo clustering of randomly distributed telomeres is proposed to occur by one of two different mechanisms (1  and 2). Mechanism 1 proposes a two-step model; 1A, telomeres  move from their positions in the nucleus to the nuclear envelope  where they become attached, and 1B nuclear envelope-attached  telomeres move over the nuclear surface to the final cluster site.  Mechanism 2 proposes a one-step model in which telomeres  move from their positions in the nucleus directly to the region of  the nuclear envelope that will be the final cluster site.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2139864&req=5

Figure 10: Model of possible mechanisms of telomere cluster formation. The de novo clustering of randomly distributed telomeres is proposed to occur by one of two different mechanisms (1 and 2). Mechanism 1 proposes a two-step model; 1A, telomeres move from their positions in the nucleus to the nuclear envelope where they become attached, and 1B nuclear envelope-attached telomeres move over the nuclear surface to the final cluster site. Mechanism 2 proposes a one-step model in which telomeres move from their positions in the nucleus directly to the region of the nuclear envelope that will be the final cluster site.
Mentions: The present study describes the sudden formation and the gradual dissolution of the meiotic telomere cluster. In light of these findings, we now consider the possible mechanisms underlying these dynamic changes in telomere localization. The abruptness of the initial cluster formation allows us to rule out one class of mechanisms relying on passive diffusion. Specifically, our data do not support a scenario in which a region of the nuclear envelope suddenly acquires an affinity for telomeres, and collects the telomeres on the basis of chance interaction. What then is the mechanistic basis for the formation of the telomere cluster? To begin to address this question, two possible mechanisms of bouquet formation are proposed in Fig. 10. The first mechanism involves a two-step process (movements indicated by arrows of nuclei 1A and 1B of Fig. 10) in which the telomeres first attach to any region of the nuclear envelope (arrows of 1A), followed by the movement of telomeres in the plane of the nuclear envelope (arrows of 1B) to end up at the final cluster site. The second mechanism would involve a one-step process (movements indicated by arrows of nucleus 2, Fig. 10) in which telomeres move directly to the region of the nuclear envelope that will be the final cluster site, the bouqet base (referred to as bb in Figs. 5 and 6). The two-step clustering mechanism is consistent with the observations on mouse spermatocytes (54). Our data on meiosis in maize does not allow us to distinguish between the two paths shown in Fig. 10. Although this model only addresses the mechanisms responsible for telomere movements, we recognize that telomeres are but one of many cellular components that show altered distributions at the bouquet stage (13).

Bottom Line: We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres.The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions.Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cell Biology, University of California at Berkeley 94720, USA.

ABSTRACT
We have analyzed the progressive changes in the spatial distribution of telomeres during meiosis using three-dimensional, high resolution fluorescence microscopy. Fixed meiotic cells of maize (Zea mays L.) were subjected to in situ hybridization under conditions that preserved chromosome structure, allowing identification of stage-dependent changes in telomere arrangements. We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres. Quantitative measurements on the spatial arrangements of telomeres revealed that, as cells passed through premeiotic interphase and into leptotene, there was an increase in the frequency of large telomere-to-telomere distances and a decrease in the bias toward peripheral localization of telomeres. By leptotene, there was no obvious evidence of telomere grouping, and the large, singular nucleolus was internally located, nearly concentric with the nucleus. At the end of leptotene, telomeres clustered de novo at the nuclear periphery, coincident with a displacement of the nucleolus to one side. The telomere cluster persisted throughout zygotene and into early pachytene. The nucleolus was adjacent to the cluster at zygotene. At the pachytene stage, telomeres rearranged again by dispersing throughout the nuclear periphery. The stage-dependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions. Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

Show MeSH