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Intracellular Scaling Mechanisms Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press Intracellular Scaling Mechanisms Simone Reber1,2 and Nathan W. Goehring3,4 1Max Planck Institute of Molecular Genetics and Cell Biology, 01307 Dresden, Germany 2Integrative Research Institute (IRI) for the Life Sciences, Humboldt-Universita¨t zu Berlin, 10115 Berlin, Germany 3The Francis Crick Institute, WC2A 3LY London, United Kingdom 4MRC Laboratory of Molecular Cell Biology, University College London, WC1E 6BT London, United Kingdom Correspondence: [email protected]; [email protected] Organelle function is often directly related to organelle size. However, it is not necessarily absolute size but the organelle-to-cell-size ratio that is critical. Larger cells generally have increased metabolic demands, must segregate DNA over larger distances, and require larger cytokinetic rings to divide. Thus, organelles often must scale to the size of the cell. The need for scaling is particularly acute during early development during which cell size can change rapidly. Here, we highlight scaling mechanisms for cellular structures as diverse as centro- somes, nuclei, and the mitotic spindle, and distinguish them from more general mechanisms of size control. In some cases, scaling is a consequence of the underlying mechanism of organelle size control. In others, size-control mechanisms are not obviously related to cell size, implying that scaling results indirectly from cell-size-dependent regulation of size- control mechanisms. cell is a highly organized unit in which We also know that cell size can vary dra- Afunctions are compartmentalized into spe- matically even within one organism. Xenopus cific organelles. Each cellular organelle carries laevis is an extreme example. The smallest so- out a distinct function, which is not only related matic cells are only a few micrometers in diam- to its molecular composition but, in many cas- eter, whereas the oocyte and one-cell embryo es, also to its size. The energetic capacity of span over a millimeter. In addition, in many the mitochondria and the biosynthetic capacity animals, including X. laevis, early cell divisions of endoplasmic reticulum (ER) and Golgi net- are rapid with little cell growth, leading to rap- works depend on their surface area. The mitotic idly changing cell size that is often characteris- spindle must be large enough to span sufficient tic for early embryogenesis. Thus, this transi- distance to physically separate chromosomes tion from very large to very small cells occurs into two opposite halves of the cell. The con- on the order of hours. Cellular organelles must, tractile ring must be able to span the cell diam- therefore, possess dynamic and robust mecha- eter and generate sufficient force to drive ingres- nisms to regulate their size, or scale, with the sion. Clearly, size matters. However, in each of size of the cell. these cases, it is not absolute size, but the ratio of Strictly speaking, the term scaling describes organelle to cell size that is critical. a mathematical relationship between measured Editors: Rebecca Heald, Iswar K. Hariharan, and David B. Wake Additional Perspectives on Size Control in Biology: From Organelles to Organisms available at www.cshperspectives.org Copyright # 2015 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a019067 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a019067 1 Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press S. Reber and N.W. Goehring quantities of a system, for example, length, vol- with a fixed length and shape, thereby templat- ume, or area. Scaling relations typically take ing the size of the target organelle (Fig. 1A). An the form of a power law y ¼ xa, with a being example is the product of gene H in the bacter- the scaling exponent of the law. For example, the iophage l, which sets phage tail length (Fig. circumference of a sphere scales with its radius, 1B). Here, tail length is proportional to gene its surface with radius squared, and its volume H protein length, with smaller gene H protein with radius cubed. products resulting in correspondingly shorter- In cell biology, the term “scaling” is often tailed phage particles (Katsura 1987). YscP plays used more loosely to describe the change in a similar role in regulating the length of the organelle size or functional capacity in response injectisome needle used by pathogenic bacteria to changes in cell size. Simply speaking, larger to introduce factors into host cells (Journet et al. cells typically have proportionally larger or 2003; Wagner et al. 2010). The giant protein, more organelles (see also Marshall 2015). The nebulin, may have a similar molecular ruler key parameter of organelle functional capacity function in actin filament length control in may vary depending on the organelle. Typical- myofibrils, although this remains somewhat ly, this parameter is volume, surface area, or controversial (Castillo et al. 2009; Pappas et al. length, which, for example, are important for 2010). centrosome, ER, and mitotic spindle function, Although perfectly good size-control mech- respectively. In other cases, the key parameter anisms, these simple molecular rulers have ob- could be force generation or a biochemical rate. vious limitations, most significant of which is Importantly, in many biological systems, scaling that protein size must equal organelle size. often is imperfect, obscuring the precise scaling There are few, if any, proteins that are large relation. enough to account for the majority of cellular For the purposes of this review, for a system structures, and, at least in the context of this to show scaling, there should be a clear, albeit review, it is very difficult to see how such a pro- potentially imperfect, relation between some tein ruler could allow the size of an organelle to parameter of cell size and the relevant parameter scale with cell size, or even to be adjusted by the describing organelle size or functional capacity. cell without inducing changes in protein se- Thus, we define scaling mechanisms as those quence. that directly regulate organelle size (or capacity) Other types of “molecular rulers” that are in response to changes in cell size and distin- more dynamically specified are potentially bet- guish these from size-control mechanisms, ter suited to achieve scaling. Such molecular which are the subject of reviews elsewhere in rulers could include structures, such as the pu- this collection (see also Amodeo and Skotheim tative spindle matrix (Schweizer et al. 2014) and 2015; Levy and Heald 2015; Marshall 2015; Golgi matrix (Xiang and Wang 2011), which Mitchison et al. 2015). Although scaling and have been proposed to be composed of complex size-control mechanisms are distinct, they are molecular networks. Although these structures often linked. We will highlight several cases are presumably subject to size control and, at where organelle size-control pathways either in- least in the case of the spindle matrix, also sub- herently show organelle scaling or can be mod- ject to cell-size-dependent scaling, we know lit- ified to achieve it. tle about how their size is controlled and even less about how their size is scaled appropriately to the size of the cell. INTRACELLULAR SCALING MECHANISMS Molecular gradients can also act as rulers, the clearest examples of which can be found Molecular Rulers during animal development where gradients Molecular rulers provide an intuitively simple of morphogens are established across tissues. method for size control. In its simplest form, a Cells then read out their position in the gradient molecular ruler provides a structural scaffold from local morphogen concentration. The sim- 2 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a019067 Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press Intracellular Scaling Mechanisms A B Head Tail Tail length (No. of discs) Gene H (No. of aa) Bacteriophage λ C ) λ L length ( Wing Dpp decay Source Width (L) Drosophila imaginal wing disc D ABp P0 AB P1 ABa P2 EMS Half spindle length λ) TPX2 gradient length ( TPX2 decay C. elegans half spindle Half spindle length (L) Figure 1. Molecular rulers. (A) In its simplest form, a molecular ruler provides a structural scaffold templating the size of the target organelle. (B) Bacteriophage l tail length is set by the product of gene H. Tail length correlates with protein length (i.e., number of amino acids). (C) Decapentaplegic (Dpp) gradients scale with tissue size of imaginal discs during Drosophila development. (Adapted from data in Wartlick et al. 2011.) (D) Centrosome size sets mitotic spindle length by controlling the length scale of a TPX2 gradient along spindle microtubules (Greenan et al. 2010). Cite this article as Cold Spring Harb Perspect Biol 2015;7:a019067 3 Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press S. Reber and N.W. Goehring plest examples of these gradients are formed size (Greenan et al. 2010). The centrosome itself by diffusion of morphogen away from a point scales with cell size via a limiting pool mecha- source. Diffusion of locally produced morpho- nism (discussed below), meaning that cell, cen- gen coupled to degradation or internalization trosome, and spindle size are all coupled in of the morphogen within the tissue gives rise to this system. The Ran gradient and its effectors an exponentially decaying gradient away from centered on chromatin appear to play a similar the source. In this case, the lengthpffiffiffiffiffiffi scale of the role in regulating spindle length in other sys- gradient, l, is specified by l ¼ Dt, where D tems (Kalab et al. 2002, 2006; Bird and Hyman is the diffusion coefficient and t is the mole- 2008).
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