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Determinator-Inhibitor Pairs As a Mechanism for Threshold

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Determinator-Inhibitor Pairs As a Mechanism for Threshold Proc. Nati. Acad. Sci. USA Vol. 83, pp. 679-683, February 1986 Developmental Biology Determinator-inhibitor pairs as a mechanism for threshold setting in development: A possible function for pseudogenes (cellular determination/segmentation/pattern formation/sense-antisense RNA/evolution) JOHN R. MCCARREY AND ARTHUR D. RiGGs Division of Biology, Beckman Research Institute of the City of Hope, Duarte, CA 91010 Communicated by Susumu Ohno, September 30, 1985 ABSTRACT Thresholds are frequently thought to be in- mass action equation does not give step functions. For example, volved in the development of discrete structures in response to transcription ofthe lac operon is proportional to the fraction of a shallow, monotonic gradient of morphogenetic information. lac operator free of lac repressor (18). In this example, and We propose a mechanism for threshold setting that incorpo- others, allostery sharpens the response to the inducer, but the rates two essential components: (i) determinator genes that transition is still not sufficiently acute (17, 18). Thus an addi- produce intracellular "determinators" that control cellular tional mechanism seems necessary to satisfactorily account for differentiation during development and (i) intracellular "in- the signal amplification and threshold setting required to control hibitors" that bind tightly and specifically to the determinators the quantized decisions during development of multicellular to form "determinator-inhibitor pairs" that are inactive with organisms. We have found that by imposing the presence of an respect to determinator function. The interaction of these intracellular macromolecular inhibitor capable of tightly components amplifies the intracellular response to an extra- complexing with the determinator gene product, the necessary cellular morphogen, thus producing a sharp transition in sharp intracellular transition can be realized. The system then determinator gene activity. This system could operate at either becomes more akin to a buffered acid-base titration. Further- the RNA level with the determinator-inhibitor pairs taking the more, by postulating different determinator-inhibitor pairs (D-I form of sense-antisense RNAs or at the protein level via a pairs) controlling the development of different discrete struc- competitive inhibition mechanism. In either case this model tures, the occurrence of multiple thresholds in response to a suggests a possible role for pseudogenes in development as a single gradient is facilitated. source of the intracellular inhibitors. There are two paramount requirements of the inhibitor molecules in this mechanism: each must be highly specific for The process of development in complex multicellular orga- its paired determinator molecule, and the binding coefficient nisms is characterized by a series of quantized decisions as for each pair must be relatively high. These requirements cells become progressively more restricted in their potential could be met either at the RNA level via an interaction of (1). Typically these decisions represent choices made at sense-antisense RNA or at the protein level, perhaps on the bidirectional branch points in pathways leading to develop- basis of competition between functional and nonfunctional ment of different cell lineages and/or discrete structures (2, subunits. In either case this suggests a potential function for 3). In many cases, these decisions seem to be based on the pseudogenes not previously considered. Thus we propose interaction of an extracellular source of morphogenetic that pseudogenes could play a significant role in morphogen- information and an intracellular mechanism that facilitates an esis as a source of intracellular inhibitor molecules. appropriate response to the extracellular morphogen (4-8). D-I The concept of morphogenetic information in the form of The Model a shallow, monotonic gradient extending over a large distance A fundamental version of our model is shown in Fig. 1. This has frequently been imposed as the extracellular phenome- version assumes an extracellular morphogen present in a non governing ordered differentiation in embryogenesis monotonic concentration gradient and responsible for be- (4-15). The intracellular response is assumed to involve stowing an overall order upon cellular differentiation within specific macromolecules that have been called "determina- a particular morphogenetic field, and an intracellular (or tors" (16). These determinators establish cellular commit- intranuclear) mechanism that mediates the appropriate re- ment or determination, by interacting with, and thus predis- sponse to the extracellular morphogen. Central to the intra- posing the eventual expression of, an appropriate set of cellular response mechanism are a determinator that is "differentiation" genes that are ultimately responsible for the transcriptionally regulated, its paired inhibitor that is pro- development of an observable cellular phenotype. In cases duced constitutively, and a cytoplasmic receptor that inter- where such differentiation involves the development of acts with the morphogen as it enters the cell. The determina- segments or other discrete structures, it has been proposed tor is the intracellular macromolecule ultimately responsible that the intracellular response involves thresholds that trans- for setting commitment to a certain cell lineage or differen- late the monotonic gradient into a step function (17). How- tiation pathway. The inhibitor is an intracellular macromol- ever, a specific mechanism defining this threshold effect at ecule that binds tightly to the determinator forming a complex the molecular level, so as to account for specific gene (D-I) that is inactive with respect to determinator function. expression, has yet to emerge. The receptor complexes with the morphogen to form a A key requirement ofan intracellular threshold mechanism is receptor-morphogen complex that, in this version of the the production ofsharp transitions in response to the monotonic model, acts to repress transcription from the determinator morphogenetic signal. The direct transcriptional response of a gene. Clearly, activation rather than repression could be determinator gene to a regulatory molecule as described by the readily accommodated. The key point is that the rate of transcription of the determinator gene directly reflects the The publication costs of this article were defrayed in part by page charge level of morphogen in the extracellular environment. Actual payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. Abbreviation: D-I, determinator-inhibitor. 679 Downloaded by guest on September 25, 2021 680 Developmental Biology: McCarrey and Riggs Proc. Natl. Acad Sci. USA 83 (1986) A determinator-inhibitor complex, and K is the equilibrium constant. Eq. 1 can easily be solved for DI as a function of (M)2 (R) No Determination and K. In conservation of mass (Df)=O02 Dt, It, addition, requires: (RM) =2 Df = Dt - DI, [2] 4(DI) I PD Dgene /gene where Dfis the concentration ofdeterminator free ofinhibitor B and thus active. Eqs. 1 and 2, together, then give Df as a function ofDt. We assume that the rate oftranscription ofthe (M)=1 (R) Determination K < (Dt) = ~1000 determinator gene is inversely proportional to the concen- tration of morphogen. Thus Eqs. 1 and 2 are sufficient to (RM)-= (DI) 1000 calculate active Df as a function of the concentration of morphogen. PD Dgene gene Fig. 2 illustrates the response of active determinator to the FIG. 1. Schematic representation of threshold setting by D-I extracellular signal as a function of the binding constant (K). pairing. The repressed (A) versus the expressed (B) states of a When It is several orders of magnitude greater than K, there particular determinator gene in response to varying levels ofexternal is a sharp threshold for the transition to the presence of morphogen concentration are schematically represented. (A) When significant intracellularDf. By the time Kis four orfive orders the extracellular (or extranuclear in the case of a syncytial system) of magnitude less than It, the transition is virtually a step concentration of morphogen is high, it is reflected in an equally high function, thus: intracellular concentration ofRM that results in a relative repression of determinator gene transcription. As a result the production of determinator gene RNA or protein is at a level equal to or below that Df = 0 when Dt < It; [3] ofthe corresponding constitutively produced inhibitor gene product. Df > 0 when Dt > It. [4] Thus the determinator gene product is completely consumed by the formation of D-I complexes and no free determinator is present, so There will be essentially no change in Df in response to the that the determinator function is fully inhibited. (B) As the extracel- decreasing concentration ofmorphogen or receptor-morpho- lular concentration of morphogen decreases, the intracellular con- gen complex until Dt = It, from which point Df will increase centration of RM decreases, which in turn results in a relative rapidly. Thus it is It that sets the threshold at which Df will derepression of determinator gene transcription. At a critical point appear and subsequently induce cellular determination. the determinator gene product rises to a level greater than that ofthe Consider the following application of this model. Suppose inhibitor gene product, and there is then a sharp increase in the intracellular concentration
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