Regulating Transmembrane Signaling Through Plexin- Neuropilin Oligomerization
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1 Regulating Transmembrane Signaling Through Plexin- Neuropilin Oligomerization Bryan W. Berger Department of Chemical Engineering Program in Bioengineering
2 Components of Cell Membranes Approximately 30-40% by volume of membrane is occupied by membrane proteins IMPs account for nearly 30% of the human genome, yet less than 1% of available protein structures in the Protein Data Bank (PDB)
3 Integral Membrane Proteins: The Next Frontier of Structural Biology Integral membrane proteins (IMPs) are central to a wide range of membrane-mediated processes such as signal transduction, fusion and transport MC Wiener (2004) Methods (Review) 34, 364
4 A Bottom-Up Chemical Engineering Process Ethanol separation from a binary mixture: H-O-H UNIQUAC: C chemical (VdW SA, V) R residual (empirical, experimental) Use molecular properties to estimate thermodynamic parameters Apply relevant models to predict phase behavior of system (binary or otherwise) Design equipment to separate components
5 A Bottom-Up Biological Process Platelet activation:
6 Proposed Cx43-Sema3d Pathway Fin length Segment length Cell proliferation Cx43 levels Sof Decreased Decreased Decreased Decreased Alf Increased Increased Increased Increased
7 Membrane Co-Receptor Oligomerization and Signaling: Neuropilins, Plexins and Vascular Endothelial Growth Factor Receptors Neurogenesis (Axon Guidance) Angiogenesis (Cell Proliferation)
8 Signal Transduction as an On-Off Switch OFF: - gate, - light ON: + gate, + light
9 Ligand Binding and Dimerization: 2 On-Off Switches During Signal Trasduction Sema 3D Plexin A3 OFF: - ligand - dimer - signal OFF: - ligand + dimer - signal ON: + ligand + dimer + signal
10 Ligand Binding and Dimerization: 2 On-Off Switches During Signal Trasduction Plexin A3 dimerizatio n Sema 3D binding + = Reduced Joint formation OFF: - ligand - dimer - signal OFF: - ligand + dimer - signal ON: + ligand + dimer + signal
11 What is a Dimer? A complex formed by 2 individual protein molecules, which are typically bound through non-covalent association Homodimer: A + A = A 2 Heterodimer: A + B = AB
12 How Do Proteins Dimerize? A protein dimer depends on its quarternary structure, and is stabilized through molecular interactions between each protein monomer A protein domain is a region within a protein that has a defined secondary or tertiary structure
13 Identifying individual domains within plexins and neuropilins Nrp2a PlexinA3 Sema3d MAM = conserved juxtamembrane domain CYTO CYTO MBP-Nrp2a-MAM MBP-Nrp2a-CYTO MBP-PlexinA3 CYTO GST-Sema3d His-Sema3d MBP-Sema3d
14 Linking Primary Sequence Patterns to Protein Structure: Domains and Motifs Proteins are comprised of amino acids, and the chemical identity of each amino acid in a protein sequence determines its secondary and tertiary structure There are 20 standard amino acids
15 Protein Sequence Probability: A Coin Toss Probability (P) = Number of possible outcomes Total number of outcomes P = 0.5 P = 0.5 x 0.5 x 0.5 = (0.5) 3
16 Linking Sequence Patterns to Protein Structure Plexin A3 Transmembrane Sequence AIIGIGGGGGVLLIAIIAVLIA Glycine (G): P(G) = 1/20 P(GGGGG) = (1/20) 5 = 3 x 10-7 But this is true for any 5-mer sequence, not just GGGGG! So how do we know this is actually a unique sequence motif??? We instead use a positional sampling approach (Gibbs Sampling Algorithim) that compares the motif across a family of sequences
17 gi MGSAAILSRQSPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi SP--LGRQQPPHPKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHSKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHPKR--PFITFTGEQAEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSSTLLPRQPPQMSQK-PSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPPSQKQRSFVTFQGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----NSRP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----N-RP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL
18 gi MGSAAILSRQSPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi SP--LGRQQPPHPKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHSKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHPKR--PFITFTGEQAEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSSTLLPRQPPQMSQK-PSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPPSQKQRSFVTFQGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----NSRP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----N-RP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL
19 gi MGSAAILSRQSPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi SP--LGRQQPPHPKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHSKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHPKR--PFITFTGEQAEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSSTLLPRQPPQMSQK-PSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL Positional probability: gi MGSSTLLTRQPAPPSQKQRSFVTFQGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi Frequency of MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL amino acid X occurring at position N gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi Probability of finding MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL amino acid by chance at position N gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----NSRP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----N-RP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL
20 gi MGSAAILSRQSPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi SP--LGRQQPPHPKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHSKR--PFITFTGDQTEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi TVSP--LGRQQPPHPKR--PFITFTGEQAEGNFNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLPRQSASLSQK-LSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLPRQPPQLSQK-PSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi MGSSTLLPRQPPQMSQK-PSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPPSQKQRSFVTFQGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSAALLSRQPPSSAQK-RSFLTFTAEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPTEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi LGSSMLLPRQPSPLSQK-RSFITFRGEPTEG-FNHLVVDERTGHIYLGAINRIYKLSSDL gi MGSSTLLTRQPAPLSQKQRSFVTFRGESAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi MGSSTLLSRQPPPLSQK-RSFVTFRGEPAEG-FNHLVVDERTGHIYLGAVNRIYKLSSDL gi gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi gi VGAVG-----SSRP--FPAFLV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----NSRP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----S-RP--FRAFVV--TDTKLTHLAVHRVTGEVFVGAVNRVFKLAPNL gi GGALG-----N-RP--FRAFMV--TDTTLTHLAVHRVTGEVFVGAVNRVFKLAPNL Higher Lower
21 Plexin A3 TMCY Hypothesis: PlexinA3 interacts with itself and Nrp2a through its CYTO and/or TM domains due to unique sequence motifs found in TM and CYTO. Previous work (our group and (2009) PNAS 106: ) has suggested this region (primarily CYTO) is important for signal transduction. Transmembrane: Coiled-coil: Wild-type: AIIGIGAGGGVLLIAIIAVLIAYKRKTRDADRTLKRLQLQMDNLESRV Glycine-rich region Heptad-repeat Oligomerization Hydrophobic residues pack together
22 Primary (1 0 ) and Secondary (2 0 ) Interactions That Stabilize Coiled-Coil Dimers Rho-associated kinase (PDB 1UIX) a..de.g a..de. KLEHLIENKDRMEDEVKNLNTLQL Hydrophobic (a, d) residues introduce a 1 o interaction to drive dimerization. Strength of association is modulated through 2 o (ionic) interactions
23 PDB 3IG3 Human: ZF: Error prone TMCY mutants Transmembrane: Coiled-coil: GLAAGGGLLLLAITAVLVAYK_RKTQDADRTLKRLQLQMDNLESRVALECKEAFAELQTDINELTNHMDEVQ AIIGIGAGGGVLLIAIIAVLIAYKRKTRDADRTLKRLQLQMDNLESRVALECKEAFAELQTDIQELTNDMDGVK AIIGIGAGGGALLIAIIAELIAYKRKTRDTDRSLKRLQLQMDNLESRVALECKEAFAELQTDIQELTNDMDGVK AIIGIGAGGGVLLIAIIAVLIAYKRKTRDADRTLKRLQLQMDNLESRFALECKEAFAELQTDIQELTNDMDGVK AIIGIGAGGGVLLIAIIAVLIAYKRKTRDADRTLKRLQLQMDNLESRVALECKEAFAELQTYIQELTNDMDGVK AIIGIGAGGGVLLIAIIAVLIAYKRKTRDADRTLKRLQLQMDNLESRVALECKEAFAELQTDIQELSNDMAGVK
24 Receptor Oligomerization in Live Cells Measured by BRET Plexin A3 GFP Rluc GFP Rluc 450 nm 520 nm BRET (heterooligomer) Fusions to C-terminal domains of full-length NRP2 and plexin A3 with complementary donor (Rluc) and acceptor (GFP) Addition of exogenous substrate (coelenterazine) to catalyze resonance energy transfer from Rluc to GFP Efficiency ratio (R) gives a proportionality constant to measure extent of energy transfer, which is proportional to separation distance
25 Signal Transduction as an Dimmer Switch Increasing light
26 Ligand Binding and Dimerization: 2 On-Off Switches During Signal Transduction Sema 3D Plexin A3 OFF: - ligand - dimer - signal OFF: - ligand + dimer - signal ON: + ligand + dimer + signal
27 Receptor Surface Density: A Dimmer Switch to Regulate Signal Intensity During Signal Transduction versus versus Increasing signal
28 Endocytosis Regulate Receptor Surface Density During Signal Transduction
29 Defining the Mechanism of PlexinA3 Activation by Sema3d Iovine/Berger Team BDSI 2012 Presentation Iovine/Berger Team (title) 7/26/2012
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