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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

Relationship between cell cycle duration and cell volume in loss-of-function embryos. (A) Images of embryos at the two-cell stage for wild-type, ptp-2(op194), and ima-3 RNAi embryos were obtained by differential interference contrast (DIC) microscopy. Scale bar = 20 μm. Relationship between cell cycle duration and cell volume in AB lineage in ptp-2(op194) [filled circles in (B)] and ima-3(RNAi) [filled circles in (C)] embryos are shown with that in wild-type embryos [open circles in (B,C)] in double logarithmic plots. Cell volume and cell cycle duration data in loss-of-function embryos were obtained from each of three embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. Degrees of freedom in fitting (B,C) were 19 and 19, respectively.
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Figure 6: Relationship between cell cycle duration and cell volume in loss-of-function embryos. (A) Images of embryos at the two-cell stage for wild-type, ptp-2(op194), and ima-3 RNAi embryos were obtained by differential interference contrast (DIC) microscopy. Scale bar = 20 μm. Relationship between cell cycle duration and cell volume in AB lineage in ptp-2(op194) [filled circles in (B)] and ima-3(RNAi) [filled circles in (C)] embryos are shown with that in wild-type embryos [open circles in (B,C)] in double logarithmic plots. Cell volume and cell cycle duration data in loss-of-function embryos were obtained from each of three embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. Degrees of freedom in fitting (B,C) were 19 and 19, respectively.

Mentions: We employed a genetic approach to assess the impact of altered cell volume and to examine the molecular mechanism of the T–V relationship. In C. elegans, genome-wide screening and classic genetics have identified genes related to egg size determination. Homozygous mutant embryos of ptp-2/SH2 domain-containing protein tyrosine phosphatase are larger than wild-type embryos, whereas ima-3/importin α RNAi embryos are smaller than wild-type embryos (Figure 6A) (Gutch et al., 1998; Sonnichsen et al., 2005). We measured cell cycle duration and cell volume in the AB lineage of these two loss-of-function embryos. Volumes of AB cells in the ptp-2 mutant embryos and ima-3 RNAi embryos were approximately twice and half the sizes, respectively, of AB cells from wild-type embryos (compare gray and black brackets in Figures 6B,C). The T–V relationship of the ptp-2 AB lineage was well-fitted with a power law model with the absolute power, 0.25 (R2 = 0.87; Figure 6B), which was close to that of the wild-type AB lineage (0.27; Figure 2). Larger AB cells in ptp-2 mutant embryos (black brackets) did not further shorten cell cycle durations compared to AB cells in wild-type embryos (gray brackets; Figure 6B). Thus, the cell cycle duration may have a minimum limit, and eventually appeared to have the minimum limit in the T–V relationship.


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)

Relationship between cell cycle duration and cell volume in loss-of-function embryos. (A) Images of embryos at the two-cell stage for wild-type, ptp-2(op194), and ima-3 RNAi embryos were obtained by differential interference contrast (DIC) microscopy. Scale bar = 20 μm. Relationship between cell cycle duration and cell volume in AB lineage in ptp-2(op194) [filled circles in (B)] and ima-3(RNAi) [filled circles in (C)] embryos are shown with that in wild-type embryos [open circles in (B,C)] in double logarithmic plots. Cell volume and cell cycle duration data in loss-of-function embryos were obtained from each of three embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. Degrees of freedom in fitting (B,C) were 19 and 19, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Relationship between cell cycle duration and cell volume in loss-of-function embryos. (A) Images of embryos at the two-cell stage for wild-type, ptp-2(op194), and ima-3 RNAi embryos were obtained by differential interference contrast (DIC) microscopy. Scale bar = 20 μm. Relationship between cell cycle duration and cell volume in AB lineage in ptp-2(op194) [filled circles in (B)] and ima-3(RNAi) [filled circles in (C)] embryos are shown with that in wild-type embryos [open circles in (B,C)] in double logarithmic plots. Cell volume and cell cycle duration data in loss-of-function embryos were obtained from each of three embryos. Data in the logarithmic scale were fitted to the formula, y = a + bx, by the linear least-squares method. Degrees of freedom in fitting (B,C) were 19 and 19, respectively.
Mentions: We employed a genetic approach to assess the impact of altered cell volume and to examine the molecular mechanism of the T–V relationship. In C. elegans, genome-wide screening and classic genetics have identified genes related to egg size determination. Homozygous mutant embryos of ptp-2/SH2 domain-containing protein tyrosine phosphatase are larger than wild-type embryos, whereas ima-3/importin α RNAi embryos are smaller than wild-type embryos (Figure 6A) (Gutch et al., 1998; Sonnichsen et al., 2005). We measured cell cycle duration and cell volume in the AB lineage of these two loss-of-function embryos. Volumes of AB cells in the ptp-2 mutant embryos and ima-3 RNAi embryos were approximately twice and half the sizes, respectively, of AB cells from wild-type embryos (compare gray and black brackets in Figures 6B,C). The T–V relationship of the ptp-2 AB lineage was well-fitted with a power law model with the absolute power, 0.25 (R2 = 0.87; Figure 6B), which was close to that of the wild-type AB lineage (0.27; Figure 2). Larger AB cells in ptp-2 mutant embryos (black brackets) did not further shorten cell cycle durations compared to AB cells in wild-type embryos (gray brackets; Figure 6B). Thus, the cell cycle duration may have a minimum limit, and eventually appeared to have the minimum limit in the T–V relationship.

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