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Power law relationship between cell cycle duration and cell volume in the early embryonic development of Caenorhabditis elegans.

Arata Y, Takagi H, Sako Y, Sawa H - Front Physiol (2015)

Bottom Line: Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution.Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes.Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Cell Fate Decision, Center for Developmental Biology, RIKEN Hyogo, Japan ; Cellular Informatics Laboratory, RIKEN Saitama, Japan.

ABSTRACT
Cell size is a critical factor for cell cycle regulation. In Xenopus embryos after midblastula transition (MBT), the cell cycle duration elongates in a power law relationship with the cell radius squared. This correlation has been explained by the model that cell surface area is a candidate to determine cell cycle duration. However, it remains unknown whether this second power law is conserved in other animal embryos. Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution. Interestingly, the powers of the time-size relationship could be grouped into at least three classes: highly size-correlated, moderately size-correlated, and potentially a size-non-correlated class according to C. elegans founder cell lineages (1.2, 0.81, and <0.39 in radius, respectively). Thus, the power law relationship is conserved in Xenopus and C. elegans, while the absolute powers in C. elegans were different from that in Xenopus. Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes. The power of the volume relationship was closest to that of the time-size relationship in the highly size-correlated class. This correlation raised the possibility that the time-size relationship, at least in the highly size-correlated class, is explained by the volume ratio of nuclear size and cell size. Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

No MeSH data available.


Related in: MedlinePlus

Cell division timing of C. elegans embryos. (A) The cell division timings in an embryo cultured at 25°C. Cell identity is indicated on the horizontal axis. Cell division timing was determined by nuclear envelope breakdown (NEBD). The numbers in parentheses indicate the cell generation in each founder cell lineage. For example, AB(1) indicates the AB cell, and AB(2) indicates the AB daughter cells. (B) The average and standard deviation (SD) of cell division timings in the same generation in AB and MS lineages in an embryo were obtained; data obtained from six embryos were aligned on the horizontal axis in order (the leftmost of AB and in the leftmost of MS were obtained from an embryo). The CV of cell division timings in the same generation in AB and MS lineages in an embryo were averaged among the six embryos and were shown with SD [the average CV ± SD (%)] in the right side of data in the graphs after the third generation. The NEBD of the AB cells was set as time 0. AB, MS, C, P, E, and D are indicated with a green dot, blue square, light green triangle, magenta triangle, orange x-mark, and gray cross, respectively. The EMS cell was indicated by a light blue square.
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Figure 1: Cell division timing of C. elegans embryos. (A) The cell division timings in an embryo cultured at 25°C. Cell identity is indicated on the horizontal axis. Cell division timing was determined by nuclear envelope breakdown (NEBD). The numbers in parentheses indicate the cell generation in each founder cell lineage. For example, AB(1) indicates the AB cell, and AB(2) indicates the AB daughter cells. (B) The average and standard deviation (SD) of cell division timings in the same generation in AB and MS lineages in an embryo were obtained; data obtained from six embryos were aligned on the horizontal axis in order (the leftmost of AB and in the leftmost of MS were obtained from an embryo). The CV of cell division timings in the same generation in AB and MS lineages in an embryo were averaged among the six embryos and were shown with SD [the average CV ± SD (%)] in the right side of data in the graphs after the third generation. The NEBD of the AB cells was set as time 0. AB, MS, C, P, E, and D are indicated with a green dot, blue square, light green triangle, magenta triangle, orange x-mark, and gray cross, respectively. The EMS cell was indicated by a light blue square.

Mentions: We observed the timing of cell division in wild-type C. elegans embryos cultured at 25°C. The intervals of cell divisions between the generations in the same lineage appeared to increase gradually in all the founder cell lineages in an embryo (Figure 1A). The average and standard deviation of coefficient of variation (CV) of cell division timings in AB and MS lineages among different embryos were around several percent (1 to 4 ± 0.5 to 2.1) (Figure 1B), indicating that the cell divisions occurred synchronously in a highly reproducible manner among embryos. Thus, the C. elegans embryo is a good model system to study a deterministic mechanism to regulate cell division timings in animal embryos.


Power law relationship between cell cycle duration and cell volume in the early embryonic development of Caenorhabditis elegans.

Arata Y, Takagi H, Sako Y, Sawa H - Front Physiol (2015)

Cell division timing of C. elegans embryos. (A) The cell division timings in an embryo cultured at 25°C. Cell identity is indicated on the horizontal axis. Cell division timing was determined by nuclear envelope breakdown (NEBD). The numbers in parentheses indicate the cell generation in each founder cell lineage. For example, AB(1) indicates the AB cell, and AB(2) indicates the AB daughter cells. (B) The average and standard deviation (SD) of cell division timings in the same generation in AB and MS lineages in an embryo were obtained; data obtained from six embryos were aligned on the horizontal axis in order (the leftmost of AB and in the leftmost of MS were obtained from an embryo). The CV of cell division timings in the same generation in AB and MS lineages in an embryo were averaged among the six embryos and were shown with SD [the average CV ± SD (%)] in the right side of data in the graphs after the third generation. The NEBD of the AB cells was set as time 0. AB, MS, C, P, E, and D are indicated with a green dot, blue square, light green triangle, magenta triangle, orange x-mark, and gray cross, respectively. The EMS cell was indicated by a light blue square.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4309120&req=5

Figure 1: Cell division timing of C. elegans embryos. (A) The cell division timings in an embryo cultured at 25°C. Cell identity is indicated on the horizontal axis. Cell division timing was determined by nuclear envelope breakdown (NEBD). The numbers in parentheses indicate the cell generation in each founder cell lineage. For example, AB(1) indicates the AB cell, and AB(2) indicates the AB daughter cells. (B) The average and standard deviation (SD) of cell division timings in the same generation in AB and MS lineages in an embryo were obtained; data obtained from six embryos were aligned on the horizontal axis in order (the leftmost of AB and in the leftmost of MS were obtained from an embryo). The CV of cell division timings in the same generation in AB and MS lineages in an embryo were averaged among the six embryos and were shown with SD [the average CV ± SD (%)] in the right side of data in the graphs after the third generation. The NEBD of the AB cells was set as time 0. AB, MS, C, P, E, and D are indicated with a green dot, blue square, light green triangle, magenta triangle, orange x-mark, and gray cross, respectively. The EMS cell was indicated by a light blue square.
Mentions: We observed the timing of cell division in wild-type C. elegans embryos cultured at 25°C. The intervals of cell divisions between the generations in the same lineage appeared to increase gradually in all the founder cell lineages in an embryo (Figure 1A). The average and standard deviation of coefficient of variation (CV) of cell division timings in AB and MS lineages among different embryos were around several percent (1 to 4 ± 0.5 to 2.1) (Figure 1B), indicating that the cell divisions occurred synchronously in a highly reproducible manner among embryos. Thus, the C. elegans embryo is a good model system to study a deterministic mechanism to regulate cell division timings in animal embryos.

Bottom Line: Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution.Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes.Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Cell Fate Decision, Center for Developmental Biology, RIKEN Hyogo, Japan ; Cellular Informatics Laboratory, RIKEN Saitama, Japan.

ABSTRACT
Cell size is a critical factor for cell cycle regulation. In Xenopus embryos after midblastula transition (MBT), the cell cycle duration elongates in a power law relationship with the cell radius squared. This correlation has been explained by the model that cell surface area is a candidate to determine cell cycle duration. However, it remains unknown whether this second power law is conserved in other animal embryos. Here, we found that the relationship between cell cycle duration and cell size in Caenorhabditis elegans embryos exhibited a power law distribution. Interestingly, the powers of the time-size relationship could be grouped into at least three classes: highly size-correlated, moderately size-correlated, and potentially a size-non-correlated class according to C. elegans founder cell lineages (1.2, 0.81, and <0.39 in radius, respectively). Thus, the power law relationship is conserved in Xenopus and C. elegans, while the absolute powers in C. elegans were different from that in Xenopus. Furthermore, we found that the volume ratio between the nucleus and cell exhibited a power law relationship in the size-correlated classes. The power of the volume relationship was closest to that of the time-size relationship in the highly size-correlated class. This correlation raised the possibility that the time-size relationship, at least in the highly size-correlated class, is explained by the volume ratio of nuclear size and cell size. Thus, our quantitative measurements shed a light on the possibility that early embryonic C. elegans cell cycle duration is coordinated with cell size as a result of geometric constraints between intracellular structures.

No MeSH data available.


Related in: MedlinePlus