MOLECULAR CELL BIOLOGY
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1 1 Lodish Berk Kaiser Krieger scott Bretscher Ploegh Matsudaira MOLECULAR CELL BIOLOGY SEVENTH EDITION CHAPTER 13 Moving Proteins into Membranes and Organelles Copyright 2013 by W. H. Freeman and Company
2 Nuclear transport
3 Figure 13.1 Overview of major protein-sorting pathways in eukaryotes.
4 Nuclear transport Transport of macromolecules including mrnps, trnas, and ribosomal subunits out of the nucleus and transport of all nuclear proteins translated in the cytoplasm into the nucleus occur through nuclear pores in a process that differs fundamentally from the transport of small molecules and ions across other cellular membranes (Figure 13-1).
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6 Figure Nuclear pore complex at different levels of resolution.
7 Nuclear pore complex Numerous pores perforate the nuclear envelope in all eukaryotic cells. Each nuclear pore is formed from an elaborate structure termed the nuclear pore complex (NPC). An NPC is made up of multiple copies of some 50 (in yeast) to 100 (in vertebrates) different proteins called nucleoporins. The distal ends of these filaments are joined by the terminal ring, forming a structure called the nuclear basket. The membraneembedded portion also is attached directly to the nuclear lamina, a network of lamin intermediate filaments that extends over the inner surface of the nuclear envelope. Cytoplasmic filaments extend from the cytoplasmic side of the NPC into the cytosol (Figure 13-33).
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9 Table 12-3 Molecular Biology of the Cell ( Garland Science 2008)
10 Figure Molecular Biology of the Cell ( Garland Science 2008)
11 Experimental Figure Nuclear-localization signal (NLS) directs proteins to the cell nucleus.
12 Signal sequence We now know, for instance, that the information to target a protein to a particular organelle destination is encoded within the amino acid sequence of the protein itself, usually within sequences of amino acids, known generically as signal sequences, or uptake-targeting sequences. Each organelle carries a set of receptor proteins that bind only to specific kinds of signal sequences, thus assuring that the information encoded in a signal sequence governs the specificity of targeting (Table 12-3 Molecular Biology of the Cell). Nuclear-localization signal (NLS) 1. All proteins found in the nucleus are synthesized in the cytoplasm and imported into the nucleus through nuclear pore complexes. Such proteins contain a nuclear-localization signal(nls) that directs their selective transport into the nucleus. NLSs were first discovered through the analysis of mutants of simian virus 40 (SV40) that produced an abnormal form of the viral protein called large T-antigen. The wild-type form of this protein is localized to the nucleus in virus-infected cells, whereas some mutated forms of large T-antigen accumulate in the cytoplasm. The mutations responsible for this altered cellular localization all occur within a specific seven-residue sequence rich in basic amino acids near the C-terminus of the protein: Pro-Lys-Lys-Lys-Arg-Lys-Val (Figure Molecular Biology of the Cell). 2. Experiments with engineered hybrid proteins in which this sequence was fused to a cytosolic protein demonstrated that it directs transport into the nucleus, and consequently functions as an NLS. NLS sequences subsequently were identified in numerous other proteins imported into the nucleus (Experimental Figure 13-34).
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14 Figure Nuclear import. 2
15 Nuclear import 1. Ran is a monomeric G protein that exists in two conformations, one when complexed with GTP and an alternative one when the GTP is hydrolyzed to GDP. The two importins form a heterodimeric nuclear-import receptor: the α subunit binds to a basic NLS in a cargo protein to be transported into the nucleus, and the β subunit interacts with a class of nucleoporins called FG-nucleoporins. These nucleoporins, which line the channel of the nuclear pore complex and also are found in the nuclear basket and the cytoplasmic filaments, contain multiple repeats of short hydrophobic sequences rich in phenylalanine (F) and glycine (G) residues (FG-repeats). 2. A current model for the import of cytoplasmic cargo proteins mediated by a monomeric importin is shown in Figure In the cytoplasm, a free importin binds to the NLS of a cargo protein, forming a bimolecular cargo complex. In the case of a basic NLS, the adapter protein importin α bridges the NLS and importin β, forming a trimolecular cargo complex (not shown). The cargo complex diffuses through the NPC by interacting with successive FG-nucleoporins. 2 In the nucleoplasm, interaction of Ran GTP with the importin causes a conformational change that decreases its affinity for the NLS, releasing the cargo. To support another cycle of import, the importin-ran GTP complex is transported back to the cytoplasm. 3 A GTPase accelerating protein (GAP) associated with the cytoplasmic filaments of the NPC stimulates Ran to hydrolyze the bound GTP. This generates a conformational change causing dissociation from the importin, which can then initiate another round of import. Ran GDP is bound by NTF2 (not shown) and returned to the nucleoplasm, where a guanine nucleotide exchange factor (GEF) causes release of GDP and rebinding of GTP.
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17 Figure Ran-dependent and Ran-independent nuclear export.
18 Nuclear export Such shuttling proteins contain a nuclear-export signal (NES) that stimulates their export from the nucleus to the cytoplasm through nuclear pores, in addition to an NLS that results in their reuptake into the nucleus (Figure 13-37). 1. According to the current model shown in Figure 13-37a, a specific nuclear-export receptor, in the nucleus, exportin 1, first forms a complex with Ran GTP and then binds the NES in a cargo protein. Binding of exportin 1 to Ran GTP causes a conformational change in exportin 1 that increases its affinity for the NES so that a trimolecular cargo complex is formed. Like other nuclear transport receptors, exportin 1 interacts transiently with FG repeats in FG-nucleoporins and diffuses through the NPC. The cargo complex dissociates when it encounters the Ran-GAP in the NPC cytoplasmic filaments, which stimulates Ran to hydrolyze the bound GTP, shifting it into a conformation that has low affinity for exportin 1. The released exportin 1 changes conformation to a structure that has low affinity for the NES, releasing the cargo into the cytosol. The direction of the export process is driven by this dissociation of the cargo from exportin 1 in the cytoplasm that causes a concentration gradient of the cargo complex across the NPC so that it is high in the nucleoplasm and low in the cytoplasm. Exportin 1 and the Ran GDP are then transported back into the nucleus through an NPC. 2. Ran-independent nuclear export of mrnas. The heterodimeric NXF1/NXT1 act as a nuclear export factor and directs the associated mrnp to the central channel of the NPC by transiently interacting with FG-nucleoporins. An RNA helicase(dbp5) located on the cytoplasmic side of the NPC removes NXF1 and NXT1 from the mrna in a reaction that is powered by ATP hydrolysis Free NXF1 and NXt1 proteins are recycled back into the nucleus by the Ran-dependent import process depicted in Figure 13-37b.
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20 Figure Molecular Biology of the Cell ( Garland Science 2008)
21 Nuclear import receptors 1. To initiate nuclear import, most nuclear localization signals must be recognized by nuclear import receptors, which are encoded by a family of related genes. Each family member encodes a receptor protein that is specialized for the transport of a group of nuclear proteins sharing structurally similar nuclear localization signals. 2. The import receptors are soluble cytosolic proteins that bind both to the nuclear localization signal on the protein to be transported and to nucleoporins, some of which form the tentaclelike fibrils that extend into the cytosol from the rim of the nuclear pore complexes. The fibrils and many other nucleoporins contain a large number of short amino-acid repeats that contain phenylalanine and glycine and are therefore called FG-repeats. FG-repeats serve as binding sites for the import receptors. They are thought to line the path through the nuclear pore complexes taken by the import receptors and their bound cargo proteins. These protein complexes move along the path by repeatedly binding, dissociating, and then re-binding to adjacent repeat sequences. Once in the nucleus, the import receptors dissociate from their cargo and are returned to the cytosol (Figure Molecular Biology of the Cell).
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23 Figure Molecular Biology of the Cell ( Garland Science 2008)
24 Regulation of nuclear import and export 1. Some proteins, such as those that bind newly made mrnas in the nucleus, contain both nuclear localization and nuclear export signals. These proteins continually shuttle between the nucleus and the cytosol. The steady-state localization of such shuttling proteins is determined by the relative rates of their import and export. If the rate of import exceeds the rate of export, a protein will be located primarily in the nucleus. Conversely, if the rate of export exceeds the rate of import, a protein will be located primarily in the cytosol. Thus, changing the rate of import, export, or both, can change the location of a protein. 2. In many cases, this control depends on the regulation of nuclear localization and export signals; these can be turned on or off, often by phosphorylation of adjacent amino acids. The nuclear factor of activated T cells (NF-AT) is a gene regulatory protein that, in the resting T cell, is found in the cytosol in a phosphorylated state (Figure Molecular Biology of the Cell). 1 2 When T cells are activated, the intracellular Ca2+ concentration increases. In high Ca2+, the protein phosphatase, calcineurin, binds to NF-AT. Binding of calcineurin dephosphorylates NF-AT, exposing one or more nuclear import signals, and it may also block a nuclear export signal. The complex of NF-AT bound to calcineurin is then imported into the nucleus, where NF-AT activates the transcription of numerous cytokine and cell-surface protein genes that are required for a proper immune response. During the shut-off of the response, decreased Ca2+ levels lead to the release of calcineurin. Rephosphorylation of NF-AT inactivates the nuclear import signal, and it re-exposes the nuclear export signal of NF-AT causing NF-AT to relocate to the cytosol.
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26 Peroxisomal protein transport 3
27 Peroxisomal protein import Figure PTS1-directed import of peroxisomal matrix proteins. Figure Model of peroxisomal biogenesis and division
28 Figure PTS1-directed import of peroxisomal matrix proteins.
29 Figure Model of peroxisomal biogenesis and division.
30 Experimental Figure Studies reveal different pathways for incorporation of peroxisomal membrane and matrix proteins.
31 Peroxisomal protein import 1. All peroxisomal proteins are synthesized on cytosolic ribosomes and incorporated into the organelle posttranslationally. Catalase, a peroxisome-localized enzyme, efficiently decomposes H2O2 into H2O. 2. Most peroxisomal matrix proteins contain a C-terminal PTS1 targeting sequence; a few have an N-terminal PTS2 targeting sequence. Neither targeting sequence is cleaved after import. By testing various mutant catalase proteins in this system, researchers discovered that the sequence Ser-Lys-Leu (SKL in one-letter code) or a related sequence at the C- terminus was necessary for peroxisomal targeting. All proteins destined for the peroxisomal matrix bind to a cytosolic receptor, which differs for PTS1- and PTS2- bearing proteins, and then are directed to common import receptor and translocation machinery on the peroxisomal membrane. Translocation of matrix proteins across the peroxisomal membrane depends on ATP hydrolysis. Many peroxisomal matrix proteins fold in the cytosol and traverse the membrane in a folded conformation (Figure 13-30, 13-32). 1 Step 1: Catalase and most other peroxisomal matrix proteins contain a C-terminal PTS1 uptake-targeting sequence (red) that binds to the cytosolic receptor Pex5. 2 Step 2: Pex5 with the bound matrix protein interacts with the Pex14 receptor located on the peroxisome membrane. 3 Step 3: The matrix protein Pex5 complex is then transferred to a set of membrane proteins (Pex10, Pex12, and Pex2) that are necessary for translocation into the peroxisomal matrix by an unknown mechanism. 4 Step 4: At some point, either during translocation or in the lumen, Pex5 dissociates from the matrix protein and returns to the cytosol, a process that involves the Pex2/10/12 complex and additional membrane and cytosolic proteins not shown. Note that folded proteins can be imported into peroxisomes and that the targeting sequence is not removed in the matrix. 3. Fluorescent-antibody staining of peroxisomal biogenesis mutants reveals different pathways for incorporation of membrane and matrix proteins. Cells were stained with antibodies to PMP70, a peroxisomal membrane protein, or with antibodies to catalase, a peroxisomal matrix protein, then viewed in a fluorescent microscope. (a) In wild-type cells, both peroxisomal membrane and matrix proteins are visible as bright foci in numerous peroxisomal bodies. (b) In cells from a Pex12-deficient patient, catalase is distributed uniformly throughout the cytosol, whereas PMP70 is localized normally to peroxisomal bodies. (c) In cells from a Pex3-deficient patient, peroxisomal membranes cannot assemble, and as a consequence peroxisomal bodies do not form. Thus both catalase and PMP70 are mis-localized to the cytosol (Experimental Figure 13-31). 4. Unlike mitochondria and chloroplasts, peroxisomes can arise de novo from precursor membranes, as well as by division of preexisting organelles.
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