Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies - PubMed (original) (raw)
Review
Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies
Edwin Li et al. Biochemistry. 2006.
Abstract
Receptor tyrosine kinases (RTKs) conduct biochemical signals via lateral dimerization in the plasma membrane, and their transmembrane (TM) domains play an important role in the dimerization process. Here we present two models of RTK-mediated signaling, and we discuss the role of the TM domains within the framework of these two models. We summarize findings of single-amino acid mutations in RTK TM domains that induce unregulated signaling and, as a consequence, pathological phenotypes. We review the current knowledge of pathology induction mechanisms due to these mutations, focusing on the structural and thermodynamic basis of pathogenic dimer stabilization.
Figures
Figure 1
Two models of RTK-mediated signaling. The difference between the two models is in the conformation and activity of the unliganded dimer. In model A, the unliganded dimer (3A) is active. The ligand (blue) stabilizes the dimer, but does not change the dimer structure (4A). In model B, the unliganded dimer (3B) is inactive. Ligand binding induces a structural change to an active dimer (4B). EC: extracellular domain. TM: transmembrane domain. IC: intracellular catalytic domain.
Figure 2
Pathogenic interactions, believed to contribute to the stability of mutant RTK TM domain dimers. (A) A putative hydrogen bond between Glu391 (orange) and Ile387 (magenta) in the pathogenic Ala391Glu FGFR3 mutant, linked to Crouzon syndrome with acanthosis nigricans and bladder cancer (86). (B) Putative cation-π interactions between Arg380 (red) and aromatic residues (green) in the achondroplasia-causing Gly380Arg FGFR3 mutant. These cation-π interactions likely compensate for the electrostatic repulsion between the two arginines in the mutant dimer. The comparison of these two mutant structures with the wild-type FGFR3 TM dimer structure (86) shows that the mutations induce modest changes in the relative orientation of the two helices close to the C-terminus (not discussed here in detail). Thus, the orientation of the catalytic domains is likely not perturbed due to the mutations, inaccordance with the structural hypothesis discussed here.
Figure 3
The increase in receptor dimer fraction due to a pathogenic mutation depends of three parameters: (1) the difference in dimerization propensities between wild-type and mutant receptors, (2) the dimerization propensity of the wild-type receptor, which in turn depends on the ligand concentration, and (3) the receptor concentration in the plasma membrane. The functional dependence of the receptor dimer fraction on receptor concentration in the membrane is shown for an arbirary dimerization propensity of the wild-type receptor (solid line). The dashed line depicts a higher dimer fraction due to a pathogenic mutation (86). The figure illustrates that the relative increase in dimer fraction [ΔD]/[D], where [D] is the wild-type dimer fraction and [ΔD] is the increase due to the mutation, depends on the receptor concentration in the membrane. For example, the relative increase in dimer fraction [ΔD1]/[D1] for concentration “1” is [ΔD1]/[D1] ~ 2, such that the dimer fraction increases 3- fold due to the mutation. However, a 100-fold increase in expression level will result in only about 10% increase in dimer fraction ([ΔD2]/[D2] ~ 0.1 for concentration “2”) due to the same mutation. Note that the dimerization propensity of the wild-type receptors in the plasma membrane, determining the exact position of the solid line, is yet to be characterized (the difference between the solid and the dashed line correspond to −1.3 kcal/mole (86)). This is a challenging task since the dynamic monomer-dimer distribution in the plasma membrane is expected to depend on the concentration of the available ligand (86), but may be accomplished in the future using FRET. Until this is accomplished, the dependence of the receptor dimer fraction on the expression level, as well as the increase in receptor dimer fraction due to pathogenic mutations, cannot be predicted quantitatively.
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References
- Fantl WJ, Johnson DE, Williams LT. Signaling by Receptor Tyrosine Kinases. Annu Rev Biochem. 1993;62:453–481. - PubMed
- van der Geer P, Hunter T, Lindberg RA. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol. 1994;10:251–337. - PubMed
- Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 2000;103:211–225. - PubMed
- Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature. 2001;411:355–365. - PubMed
- Robertson SC, Tynan JA, Donoghue DJ. RTK mutations and human syndromes - when good receptors turn bad. Trends Genet. 2000;16:265–271. - PubMed
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