OOC-3, a novel putative transmembrane protein required for establishment of cortical domains and spindle orientation in the P(1) blastomere of C. elegans embryos

Asymmetric cell divisions require the establishment of an axis of polarity, which is subsequently communicated to downstream events. During the asymmetric cell division of the P(1) blastomere in C. elegans, establishment of polarity depends on the establishment of anterior and posterior cortical domains, defined by the localization of the PAR proteins, followed by the orientation of the mitotic spindle along the previously established axis of polarity. To identify genes required for these events, we have screened a collection of maternal-effect lethal mutations on chromosome II of C. elegans. We have identified a mutation in one gene, ooc-3, with mis-oriented division axes at the two-cell stage. Here we describe the phenotypic and molecular characterization of ooc-3. ooc-3 is required for the correct localization of PAR-2 and PAR-3 cortical domains after the first cell division. OOC-3 is a novel putative transmembrane protein, which localizes to a reticular membrane compartment, probably the endoplasmic reticulum, that spans the whole cytoplasm and is enriched on the nuclear envelope and cell-cell boundaries. Our results show that ooc-3 is required to form the cortical domains essential for polarity after cell division.

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Roles of Actin in the Morphogenesis of the Early Caenorhabditis elegans Embryo

International Journal of Molecular Sciences ◽

10.3390/ijms21103652 ◽

2020 ◽

Vol 21 (10) ◽

pp. 3652

Author(s):

Dureen Samandar Eweis ◽

Julie Plastino

Keyword(s):

Cell Division ◽

Caenorhabditis Elegans ◽

Asymmetric Cell Division ◽

Cell Types ◽

Actin Dynamics ◽

Actin Binding ◽

Asymmetric Cell Divisions ◽

C Elegans ◽

Asymmetric Divisions ◽

Different Cell Types

The cell shape changes that ensure asymmetric cell divisions are crucial for correct development, as asymmetric divisions allow for the formation of different cell types and therefore different tissues. The first division of the Caenorhabditis elegans embryo has emerged as a powerful model for understanding asymmetric cell division. The dynamics of microtubules, polarity proteins, and the actin cytoskeleton are all key for this process. In this review, we highlight studies from the last five years revealing new insights about the role of actin dynamics in the first asymmetric cell division of the early C. elegans embryo. Recent results concerning the roles of actin and actin binding proteins in symmetry breaking, cortical flows, cortical integrity, and cleavage furrow formation are described.

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Cell polarity and asymmetric cell division: the C. elegans early embryo

Essays in Biochemistry ◽

10.1042/bse0530001 ◽

2012 ◽

Vol 53 ◽

pp. 1-14 ◽

Cited By ~ 10

Author(s):

Anna Noatynska ◽

Monica Gotta

Keyword(s):

Cell Migration ◽

Cell Division ◽

Cell Polarity ◽

Asymmetric Cell Division ◽

Early Embryo ◽

Animal Cells ◽

Par Proteins ◽

C Elegans ◽

Lethal Mutations ◽

Tissue Organization

Cell polarity is crucial for many functions including cell migration, tissue organization and asymmetric cell division. In animal cells, cell polarity is controlled by the highly conserved PAR (PARtitioning defective) proteins. par genes have been identified in Caenorhabditis elegans in screens for maternal lethal mutations that disrupt cytoplasmic partitioning and asymmetric division. Although PAR proteins were identified more than 20 years ago, our understanding on how they regulate polarity and how they are regulated is still incomplete. In this chapter we review our knowledge of the processes of cell polarity establishment and maintenance, and asymmetric cell division in the early C. elegans embryo. We discuss recent findings that highlight new players in cell polarity and/or reveal the molecular details on how PAR proteins regulate polarity processes.

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Binary decision between asymmetric and symmetric cell division is defined by the balance of PAR proteins in C. elegans embryos

10.1101/2020.08.24.264135 ◽

2020 ◽

Author(s):

Yen Wei Lim ◽

Fu-Lai Wen ◽

Prabhat Shankar ◽

Tatsuo Shibata ◽

Fumio Motegi

Keyword(s):

Cell Division ◽

Binary Choice ◽

Cell Stage ◽

Par Proteins ◽

Binary Decision ◽

C Elegans ◽

Show Evidence ◽

Differentiation And Proliferation ◽

Fate Determinants ◽

Sister Cells

ABSTRACTCoordination between cell differentiation and proliferation during development requires the balance between asymmetric and symmetric modes of cell division. However, the cellular intrinsic cue underlying the binary choice between these two division modes remains elusive. Here we show evidence in Caenorhabditis elegans that the invariable lineage of the division modes is programmed by the balance between antagonizing complexes of partitioning-defective (PAR) proteins. By uncoupling unequal inheritance of PAR proteins from that of fate determinants during zygote division, we demonstrated that changes in the balance between PAR-2 and PAR-6 are sufficient to re-program the division modes from symmetric to asymmetric and vice versa in two-cell stage embryos. The division mode adopted occurs independently of asymmetry in cytoplasmic fate determinants, cell-size asymmetry, and cell-cycle asynchrony between the sister cells. We propose that the balance between antagonizing PAR proteins represents an intrinsic self-organizing cue for binary specification of the division modes during development.

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Multiple levels of regulation specify the polarity of an asymmetric cell division in C. elegans

Development ◽

10.1242/dev.127.21.4587 ◽

2000 ◽

Vol 127 (21) ◽

pp. 4587-4598 ◽

Cited By ~ 3

Author(s):

J. Whangbo ◽

J. Harris ◽

C. Kenyon

Keyword(s):

Cell Division ◽

Wnt Signaling ◽

Epidermal Cell ◽

Asymmetric Cell Division ◽

Asymmetric Cell Divisions ◽

Signaling Systems ◽

Tissue Polarity ◽

C Elegans ◽

Cell Divisions ◽

A Cell

Wnt signaling systems play important roles in the generation of cell and tissue polarity during development. We describe a Wnt signaling system that acts in a new way to orient the polarity of an epidermal cell division in C. elegans. In this system, the EGL-20/Wnt signal acts in a permissive fashion to polarize the asymmetric division of a cell called V5. EGL-20 regulates this polarization by counteracting lateral signals from neighboring cells that would otherwise reverse the polarity of the V5 cell division. Our findings indicate that this lateral signaling pathway also involves Wnt pathway components. Overexpression of EGL-20 disrupts both the asymmetry and polarity of lateral epidermal cell divisions all along the anteroposterior (A/P) body axis. Together our findings suggest that multiple, inter-related Wnt signaling systems may act together to polarize asymmetric cell divisions in this tissue.

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Brief cytochalasin-induced disruption of microfilaments during a critical interval in 1-cell C. elegans embryos alters the partitioning of developmental instructions to the 2-cell embryo

Development ◽

10.1242/dev.108.1.159 ◽

1990 ◽

Vol 108 (1) ◽

pp. 159-172 ◽

Cited By ~ 15

Author(s):

D.P. Hill ◽

S. Strome

Keyword(s):

Cell Cycle ◽

Asymmetric Cell Division ◽

Critical Time ◽

Time Interval ◽

Critical Interval ◽

Cell Stage ◽

C Elegans ◽

Daughter Cells ◽

Correct Pattern ◽

Cell Embryo

We are investigating the involvement of the microfilament cytoskeleton in the development of early Caenorhabditis elegans embryos. We previously reported that several cytoplasmic movements in the zygote require that the microfilament cytoskeleton remain intact during a narrow time interval approximately three-quarters of the way through the first cell cycle. In this study, we analyze the developmental consequences of brief, cytochalasin D-induced microfilament disruption during the 1-cell stage. Our results indicate that during the first cell cycle microfilaments are important only during the critical time interval for the 2-cell embryo to undergo the correct pattern of subsequent divisions and to initiate the differentiation of at least 4 tissue types. Disruption of microfilaments during the critical interval results in aberrant division and P-granule segregation patterns, generating some embryos that we classify as ‘reverse polarity’, ‘anterior duplication’, and ‘posterior duplication’ embryos. These altered patterns suggest that microfilament disruption during the critical interval leads to the incorrect distribution of developmental instructions responsible for early pattern formation. The strict correlation between unequal division, unequal germ-granule partitioning, and the generation of daughter cells with different cell cycle periods observed in these embryos suggests that the three processes are coupled. We hypothesize that (1) an ‘asymmetry determinant’, normally located at the posterior end of the zygote, governs asymmetric cell division, germ-granule segregation, and the segregation of cell cycle timing elements during the first cell cycle, and (2) the integrity or placement of this asymmetry determinant is sensitive to microfilament disruption during the critical time interval.

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Emerging mechanisms of asymmetric stem cell division

The Journal of Cell Biology ◽

10.1083/jcb.201807037 ◽

2018 ◽

Vol 217 (11) ◽

pp. 3785-3795 ◽

Cited By ~ 42

Author(s):

Zsolt G. Venkei ◽

Yukiko M. Yamashita

Keyword(s):

Stem Cells ◽

Stem Cell ◽

Cell Division ◽

Asymmetric Cell Division ◽

Binary Outcomes ◽

Cellular Mechanisms ◽

Asymmetric Cell Divisions ◽

Cell Divisions ◽

Dividing Cells ◽

Stem Cell Division

The asymmetric cell division of stem cells, which produces one stem cell and one differentiating cell, has emerged as a mechanism to balance stem cell self-renewal and differentiation. Elaborate cellular mechanisms that orchestrate the processes required for asymmetric cell divisions are often shared between stem cells and other asymmetrically dividing cells. During asymmetric cell division, cells must establish asymmetry/polarity, which is guided by varying degrees of intrinsic versus extrinsic cues, and use intracellular machineries to divide in a desired orientation in the context of the asymmetry/polarity. Recent studies have expanded our knowledge on the mechanisms of asymmetric cell divisions, revealing the previously unappreciated complexity in setting up the cellular and/or environmental asymmetry, ensuring binary outcomes of the fate determination. In this review, we summarize recent progress in understanding the mechanisms and regulations of asymmetric stem cell division.

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