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Principles and Mechanisms of Asymmetric Cell Division Bharath Sunchu and Clemens Cabernard*

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Principles and Mechanisms of Asymmetric Cell Division Bharath Sunchu and Clemens Cabernard* © 2020. Published by The Company of Biologists Ltd | Development (2020) 147, dev167650. doi:10.1242/dev.167650 REVIEW Principles and mechanisms of asymmetric cell division Bharath Sunchu and Clemens Cabernard* ABSTRACT highlight studies that have revealed asymmetric segregation of Asymmetric cell division (ACD) is an evolutionarily conserved macromolecules or organelles and review the documented or mechanism used by prokaryotes and eukaryotes alike to control potential influence of these events on cell fate decisions in yeast and cell fate and generate cell diversity. A detailed mechanistic metazoans. We also discuss how asymmetries in the cytoskeleton, understanding of ACD is therefore necessary to understand cell spindle, centromeres and histones can contribute to ACD. fate decisions in health and disease. ACD can be manifested in the biased segregation of macromolecules, the differential partitioning of Polarized localization and biased inheritance of RNAs and cell organelles, or differences in sibling cell size or shape. These proteins events are usually preceded by and influenced by symmetry breaking Cell fate decisions can be induced through asymmetric partitioning events and cell polarization. In this Review, we focus predominantly of molecular determinants such as RNA species or proteins. For on cell intrinsic mechanisms and their contribution to cell polarization, example, mRNAs that are segregated into one sibling cell can ACD and binary cell fate decisions. We discuss examples of polarized quickly produce proteins to elicit a specific cell behavior. systems and detail how polarization is established and, whenever Alternatively, regulatory RNA species or proteins can affect gene possible, how it contributes to ACD. Established and emerging expression, protein localization and function. The polarized model organisms will be considered alike, illuminating both well- distribution of molecules often precedes biased segregation. In documented and underexplored forms of polarization and ACD. this section, we discuss examples and mechanisms of how the localization and segregation of RNA species and proteins is KEY WORDS: Asymmetric cell division, Cell fate decisions, Cell fate controlled and regulated. We also discuss potential contributions determinants, Non-random segregation, Organelle partitioning of this biased segregation to binary cell fate decisions. Introduction RNAs Asymmetric cell division (ACD) is a conserved mechanism evolved Differential RNA localization has been documented in a number of to generate cellular diversity. A key principle of ACD is the different species and cell types. One of the first examples of establishment of distinct sibling cell fates by mechanisms linked to asymmetric RNA localization was reported for Actin isoforms in the mitosis. Asymmetric fate can be established through exposure to early ascidian embryo Styela plicata using in situ hybridization cell extrinsic signaling cues. Alternatively, asymmetric inheritance (Jeffery et al., 1983). A recent global analysis of mRNA localization of cell intrinsic cell fate determinants such as proteins or RNA can dynamics using high-resolution fluorescent in situ hybridization induce asymmetric cell fate decisions. The latter was demonstrated (FISH) during early Drosophila melanogaster development more than 100 years ago by Edwin Conklin who showed that, revealed that 71% of genes expressed during this time window during early divisions in ascidian embryos, yellow cytoplasm display specific subcellular localization patterns. Notably, a number segregates asymmetrically to specify muscle cell fate (Conklin, of these genes display a polarized distribution, being preferentially 1905). In addition to macromolecules, cell organelles such as localized to either the apical or basal cell cortex (Lécuyer et al., centrosomes, midbodies, mitochondria, endoplasmic reticulum 2007). Subcellular localization of different RNA species, including (ER) or lysosomes have been described to segregate mRNAs, long non-coding RNAs and circular RNAs, was also asymmetrically. Interestingly, the asymmetric inheritance of found in a recent study using a combination of cell fractionation cellular organelles appears to be the norm rather than the combined with RNA sequencing of human and Drosophila cells exception, but its connection to differential cell fate establishment (Bouvrette et al., 2017). Although this study did not assay polarized remains unclear in many instances (Fig. 1). distribution of RNA species per se, it clearly demonstrated that the ACD is relevant during the development of both invertebrates and majority of RNAs are localized in specific cellular compartments. vertebrates, and our current knowledge about this process stems to a A clear example of how biased localization of mRNAs results in large extent from genetically tractable invertebrate systems such as their asymmetric segregation has been shown during spiralian Caenorhabditis elegans or Drosophila melanogaster. However, development. For instance, in I. obsoleta, mRNAs of the classic embryological studies on animals that are currently not developmental patterning genes Eve, DPP and Tld are localized to amenable to precise genetic manipulation, such as the mollusc the centrosome during the early cleavage cycles and subsequently Ilyanassa obsoleta, have also contributed a wealth of information to segregate into one daughter cell during cell division (Lambert and our current understanding of ACD. Here, we review recent literature Nagy, 2002). Centrosomal localization of mRNAs appears to be a that has provided new insights into symmetry breaking events. We dominant mechanism for embryonic patterning in this system, as it has also been observed for several other mRNAs (Kingsley et al., Department of Biology, University of Washington, Life Science Building, Seattle, WA 2007; Lambert and Nagy, 2002). Interestingly, all of the 98195, USA. centrosome-localized mRNAs show two discrete types of intracellular movement: an initial recruitment to particular *Author for correspondence ([email protected]) interphase centrosomes, presumably mediated by minus-end C.C., 0000-0003-3706-6401 directed transport, followed by movement to a cortical region that DEVELOPMENT 1 REVIEW Development (2020) 147, dev167650. doi:10.1242/dev.167650 A Cell extrinsic Fig. 1. Basic concepts of asymmetry and biased segregation. (A) Asymmetric cell division can be induced by cell extrinsic cues that are provided by the local niche. (B) Asymmetric cell division can also be induced by cell intrinsic mechanisms. Four examples that have been shown to, or potentially can, result in binary cell fate decisions, entail: (i) polarized cortical distribution of proteins, such as cell fate determinants; (ii) biased localization and segregation of RNA species; (iii) biased non- B Cell intrinsic random distribution of organelles; (iv) biased distribution of protein aggregates. i ii iii iv Key Contractile Niche Cortical cell fate Centrosomal Mitotic ring environment determinants cell fate determinant spindle New Old Protein Sibling cells with Chromosomes mitochondria mitochondria aggregates different fates is inherited exclusively by one daughter cell during cell division. An et al., 1997; Schuldt et al., 1998). Apical pros mRNA localization is intact microtubule cytoskeleton is necessary for centrosomal dependent on Inscuteable (Insc) protein and the RNA-binding accumulation of mRNA but not for the subsequent relocalization protein Staufen (STAU1/2 in vertebrates), which binds the Prospero to the cell cortex, which instead depends on Actin filaments 3′ untranslated region (Li et al., 1997; Schuldt et al., 1998). Miranda (Lambert and Nagy, 2002). The cytoskeleton is also important for protein, another neuroblast cell fate determinant, colocalizes with asymmetric localization and segregation of ASH1 mRNA in yeast; Staufen protein and pros mRNA during neuroblast division, and in this context, ASH1 is asymmetrically localized on the cortex via a both molecules depend on Miranda for their correct localization process that involves Actin and Type V myosin Myo4 (Long et al., (Schuldt et al., 1998). Interestingly, inscuteable mRNA has also 1997). Centrosomal localization of mRNAs also occurs in oocytes been observed to localize to the apical prophase neuroblast cortex of the surf clam (Spisula solidissima) (Alliegro et al., 2006) and in independently of Staufen; Inscuteable and Staufen proteins are both D. melanogaster embryos (Lécuyer et al., 2007). components of an apical complex (Li et al., 1997). Recently, the Additional mechanistic and functional insight into polarized MS2 system (Bertrand et al., 1998; Fusco et al., 2003) has made it RNA distribution and segregation has been learned from studying possible to assay the dynamics of mRNA localization in neuroblasts asymmetrically dividing Drosophila neural stem cells, called via live cell imaging (Ramat et al., 2017). Using this system, it neuroblasts. Neuroblasts divide asymmetrically to give rise to a was found that Miranda is localized in two distinct pools: around self-renewing neuroblast and a differentiating cell termed a ganglion the apical centrosome and on the basal neuroblast cortex. mother (GMC) (Gallaud et al., 2017; Homem and Knoblich, 2012). This study revealed that the apical localization of Miranda mRNA of the transcription factor Prospero (Pros; Prox1 in depends on centrosomes and Staufen, and that basal miranda vertebrates) is localized on the apical cortex of neuroblasts in mRNA is necessary
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