Coupled cycling programs multicellular self-organization of neural progenitors

Rezaei-Lotfi, Saba; Hunter, Neil; Farahani, Ramin Hamidi

doi:10.1080/15384101.2019.1638692

Cited by 8 publications

(27 citation statements)

References 40 publications

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“…It therefore is not surprising that amplified activity of β-catenin accelerates progression through cell cycle by installing a truncated G1 phase [29]. Contrarily, recruitment of β-catenin to adherens junctions [14,15] delays the entry to S phase of G1 dwelling cells in a cell density-dependent manner [7]. The described activity of β-catenin in coupling the individual cell cycles across a proliferating population is the basis for synchronised cycling of metazoan cells.…”

Section: β-Catenin and Coupling Of Cell Cyclementioning

confidence: 99%

“…A key signature of human neural progenitor cells [30] cultured in 2D monolayers is partial synchronicity of the entry into mitosis at population level [7]. The synchronicity manifests as periods of enhanced mitotic events (Fig.…”

Section: Molecular Basis Of Coupled Cyclingmentioning

confidence: 99%

“…In the face of genomic variability, robust emergence of a developmental blueprint suggests that interpretation of morphogenic programs is accomplished in a decentralized manner and at a platform higher than the level of individual cells. We recently investigated the biological platform that governs decentralized spatial, temporal and functional organisation of metazoan cells [7]. Findings revealed that multicellular organisation during neurogenesis is driven by an unexpected evolutionary adaptation of metazoan cell cycle.…”

Section: Introductionmentioning

confidence: 99%

“…Findings revealed that multicellular organisation during neurogenesis is driven by an unexpected evolutionary adaptation of metazoan cell cycle. Unlike autonomous cycling of unicellular organisms, metazoan cell cycle is coupled to those of neighboring cells [7]. In a coupled cycling mode, intercellular contacts relay extrinsic cues to override the intrinsic cycling rhythm of an individual cell.…”

Section: Introductionmentioning

confidence: 99%

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Coupled cycling and regulation of metazoan morphogenesis

Rezaei-Lotfi

Farahani

2020

Cell Div

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Metazoan animals are characterized by restricted phenotypic heterogeneity (i.e. morphological disparity) of organisms within various species, a feature that contrasts sharply with intra-species morphological diversity observed in the plant kingdom. Robust emergence of morphogenic blueprint in metazoan animals reflects restricted autonomy of individual cells in adoption of fate outcomes such as differentiation. Fates of individual cells are linked to and influenced by fates of neighboring cells at the population level. Such coupling is a common property of all self-organising systems and propels emergence of order from simple interactions between individual cells without supervision by external directing forces. As a consequence of coupling, expected functional relationship between the constituent cells of an organ system is robustly established concurrent with multiple rounds of cell division during morphogenesis. Notably, the molecular regulation of multicellular coupling during morphogenic self-organisation remains largely unexplored. Here, we review the existing literature on multicellular self-organisation with particular emphasis on recent discovery that β-catenin is the key coupling factor that programs emergence of multi-cellular self-organisation by regulating synchronised cycling of individual cells.

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Section: β-Catenin and Coupling Of Cell Cyclementioning

confidence: 99%

Section: Molecular Basis Of Coupled Cyclingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Coupled cycling and regulation of metazoan morphogenesis

Rezaei-Lotfi

Farahani

2020

Cell Div

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“…One such protein is β-Catenin (Dokumcu et al, 2018), the downstream mediator of Wnt signalling cascade (MacDonald et al, 2009). Wnt/β-Catenin pathway codes a developmental switch (Hayward et al, 2008) that integrates system-level signalling inputs into a binary outcome (Rezaei-Lotfi et al, 2019). Resolution of the proliferation/differentiation dichotomy under instruction from Wnt/βcatenin pathway (Hayward et al, 2008) is an example of the binarization activity of the cascade.…”

Section: Introductionmentioning

confidence: 99%

Genomic Competition for Noise Reduction Shaped Evolutionary Landscape of Mir-4673

Farahani

Rezaei-Lotfi

Hunter

2019

Preprint

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AbstractThe genomic platform that informs evolution of microRNA cascades remains unknown. Here we capitalized on the recent evolutionary trajectory of hominin-specific miRNA-4673 (Dokumcu et al., 2018) encoded in intron 4 of notch-1 to uncover the identity of one such precursor genomic element and the selective forces acting upon it. The miRNA targets genes that regulate Wnt/β-catenin signalling cascade. Primary sequence of the microRNA and its target region in Wnt modulating genes evolved from homologous signatures mapped to homotypic cis-clusters recognised by TCF3/4 and TFAP2A/B/C families. Integration of homologous TFAP2A/B/C cis-clusters (short range inhibitor of β-catenin (Li and Dashwood, 2004)) into the transcriptional landscape of Wnt cascade genes can reduce noise in gene expression (Blake et al., 2003). Probabilistic adoption of miRNA secondary structure by one such cis-signature in notch-1 reflected selection for superhelical curvature symmetry of precursor DNA to localize a nucleosome that overlapped the latter cis-cluster. By replicating the cis-cluster signature, non-random interactions of the miRNA with key Wnt modulator genes expanded the transcriptional noise buffering capacity via a coherent feed-forward loop mechanism (Hornstein and Shomron, 2006). In consequence, an autonomous transcriptional noise dampener (the cis-cluster/nucleosome) evolved into a post-transcriptional one (the miRNA). The findings suggest a latent potential for remodelling of transcriptional landscape by miRNAs that capitalize on non-random distribution of genomic cis-signatures.

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Cellular self‐organization: An overdrive in Cambrian diversity?

2022

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During the early Cambrian period metazoan life forms diverged at an accelerated rate to occupy multiple ecological niches on earth. A variety of explanations have been proposed to address this major evolutionary phenomenon termed the "Cambrian explosion." While most hypotheses address environmental, developmental, and ecological factors that facilitated evolutionary innovations, the biological basis for accelerated emergence of species diversity in the Cambrian period remains largely conjectural. Herein, we posit that morphogenesis by self-organization enables the uncoupling of genomic mutational landscape from phenotypic diversification. Evidence is provided for a two-tiered interpretation of genomic changes in metazoan animals wherein mutations not only impact upon function of individual cells, but also alter the self-organization outcome during developmental morphogenesis. We provide evidence that the morphological impacts of mutations on self-organization could remain repressed if associated with an unmet negative energetic cost. We posit that accelerated morphological diversification in transition to the Cambrian period has occurred by emergence of dormant (i.e., reserved) morphological novelties whose molecular underpinnings were seeded in the Precambrian period.

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Coupled cycling programs multicellular self-organization of neural progenitors

Cited by 8 publications

References 40 publications

Coupled cycling and regulation of metazoan morphogenesis

Coupled cycling and regulation of metazoan morphogenesis

Genomic Competition for Noise Reduction Shaped Evolutionary Landscape of Mir-4673

Cellular self‐organization: An overdrive in Cambrian diversity?

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